Volume 69
Number 1

Fishery Bulletin

U.S. DEPARTMENT OF COMMERCE

69 '^'^

National Oceanic and Atmospheric AdministJ^gpj^g gj^i^gj^g, ^^^^^^^^^^

NatJona! Marine Fisheries Service

LIBRA-

MAY 171971

WOODS HOLE, .vJASS.

Vol. 69, No. 1 January 1971

ROEDEL, PHILIP M. In Memoriam — Wilbert McLeod Chapman and Milner Baily Schaefer . 1

AHLSTROM, ELBERT H. Kinds and abundance of fish larvae in the eastern tropical

Pacific, based on collections made on EASTROPAC I 3

SMILES, MICHAEL C, JR., and WILLIAM G. PEARCY. Size structure and growth

rate of Euphausia pacifica off the Oregon coast '^9

THOMAS, WILLIAM H., and ROBERT W. OWEN, JR. Estimating phytoplankton
production from ammonium and chlorophyll concentrations in nutrient-poor water of
the eastern tropical Pacific Ocean 87

CLUTTER, ROBERT I., and GAIL H. THEILACKER. Ecological efficiency of a pelagic

mysid shrimp; estimates from growth, energy budget, and mortality studies 93

ROTHSCHILD, BRIAN J., and JAMES W. BALSIGER. A linear-programming solu-
tion to salmon management ^^'^

DUBROW, DAVID L., and BRUCE R. STILLINGS. Chemical and nutritional char-
acteristics of fish protein concentrate processed from heated whole red hake, Urophycis
chitss '■^'■

DUBROW, DAVID L., NORMAN L. BROWN, E. R. PARISER, HARRY MILLER, JR.,
V. D. SIDWELL, and MARY E. AMBROSE. Eflfect of ice storage on the chemical and
nutritive properties of solvent-extracted whole fish — red hake, Urophycis cJuiss 145

CREAR, DAVID, and IRWIN HAYDOCK. Laboratory rearing of the desert pupfish,

Cyprinodon inacularius ^^^

HAYDOCK, IRWIN. Gonad maturation and hormone-induced spawning of the gulf

croaker, Bairdiella icistia l" '

SECKEL, GUNTER R., and MARION Y. Y. YONG. Harmonic functions for sea-surface
temperatures and salinities, Koko Head, Oahu, 1956-69, and sea-surface temperatures,
Christmas Island, 1954-69 181

JELLINEK, GISELA, and MAURICE E. STANSBY. Masking undesirable flavors in

fish oils 215

COOK, HARRY L., and M. ALICE MURPHY. Early developmental stages of the brown

shrimp, Penaeus aztecxts Ives, reared in the laboratory 223

KOURY, BARBARA, JOHN SPINELLI, and DAVE WIEG. Protein autolysis rates at
various pH's and temperatures in hake, Merluccius productus, and Pacific herring,
Clupea harengus pallasi, and their effect on yield in the preparation of fish protein
concentrate 241

Notes

EMILIANI, DENNIS A. Equipment for holding and releasing penaeid shrimp during
marking experiments 247

TOPP, ROBERT W., and FRANK H. HOFF. An adult bluefin tuna, Thimnus thynnua,
from a Florida west coast urban waterway 251

U.S. DEPARTMENT OF COMMERCE

Maurice H. Stans, Secretary
NATIONAL OCEANIC AND ATMOSPHERIC ADMINISTRATION

NATIONAL MARINE FISHERIES SERVICE
Philip M. Roedel, Director

FISHERY BULLETIN

The Fishery Bulletin carries technical reports on investigations in fishery science. The Bulletin of the
United States Fish Commission was begun in 1881; it became the Bulletin of the Bureau of Fisheries in 1904
and the Fishery Bulletin of the Fish and Wildlife Service in 1941. Separates were issued as documents through
volume 46; the last document was No. 1103. Beginning with volume 47 in 1931 and continuing through volume
62 in 1963, each separate appeared as a numbered bulletin. A new system began in 1963 with volume 63 in which
papers are bound together in a single issue of the bulletin instead of being issued individually.

Bulletins are distributed free to libraries, research institutions, State agencies, and scientists. Some Bulle-
tins are for sale by the Superintendent of Documents, U.S. Government Printing Office, Washington, D.C. 20402.

EDITOR

Dr. Reuben Lasker

Scientific Editor, Fishery Bulletin

National Marine Fisheries Service

Fishery-Oceanography Center
La Jolla, California 92037

Editorial Committee

Dr. Elbert H. Ahlstrom

National Marine Fisheries Service

Dr. William H. Bayliff

Inter-American Tropical Tuna Commission

Dr. Daniel M. Cohen

National Marine Fisheries Service

Dr. Howard M. P'eder
University of Alaska

Mr. .John E. Fitch

California Department of Fish and Game

Dr. Marvin D. Grosslein
National Marine Fisheries Service

Dr. J. Frank Hebard

National Marine Fisheries Service

Dr. John R. Hunter

National Marine Fisheries Service

Mr. John C. Marr

Food and Agriculture Organization of
the United Nations

Dr. Arthur S. Merrill

National Marine Fisheries Service

Dr. Virgil J. Norton
University of Rhode Island

Mr. Alonzo T. Pruter

National Marine Fisheries Service

Dr. Theodore R. Rice

National Marine Fisheries Service

Dr. Brian J. Rothschild
University of Washington

Dr. Oscar E. Sette

National Marine Fisheries Service

Mr. Maurice E. Stansby
National Marine Fisheries Service

Dr. Majmard A. Steinberg
National Marine Fisheries Service

Dr. Roland L. Wigley

National Marine Fisheries Service

rfi"^

CONTENTS

Vol, 69, No. 1 January 1971

ROEDEL, PHILIP M. In Memoriam — Wilbert McLeod Chapman and Milner Baily Schaefer 1

AHLSTROM, ELBERT H. Kinds and abundance of fish larvae in the eastern tropical Pacific, based on collections

made on EASTROPAC I ^

SMILES, MICHAEL C, JR., and WILLIAM G. PEARCY. Size structure and growth rate of Euphausia pacifica

off the Oregon coast ^^

•THOMAS, WILLIAM H., and ROBERT W. OWEN, JR. Estimating phytoplankton production from ammonium

and chlorophyll concentrations in nutrient-poor water of the eastern tropical Pacific Ocean 87

CLUTTER, ROBERT I., and GAIL H. THEILACKER. Ecological eiBciency of a pelagic mysid shrimp; esti-
mates from growth, energy budget, and mortality studies 93

ROTHSCHILD, BRIAN J., and JAMES W. BALSIGER. A linear-programming solution to salmon management . 117

DUBROW, DAVID L., and BRUCE R. STILLINGS. Chemical and nutritional characteristics offish protein concentrate

processed from heated whole red hake, Urophycis chuss 141

DUBROW, DAVID L., NORMAN L. BROWN, E. R. PARISER, HARRY MILLER, JR., V. D. SIDWELL, and
MARY E. AMBROSE. Effect of ice storage on the chemical and nutritive properties of solvent-extracted whole
fish — red hake, Urophycis chuss 145

CREAR, DAVID, and IRWIN HAYDOCK. Laboratory rearing of the desert pupfish, Cyprinodon macularius . . 151

HAYDOCK, IRWIN. Gonad maturation and hormone-induced spawning of the gulf croaker, Bairdiella icistia 157

SECKEL, GUNTER R., and MARION Y. Y. YONG. Harmonic functions for sea-surface temperatures and sa-
linities, Koko Head, Oahu, 1956-69, and sea-surface temperatures, Christmas Island, 1954-69 181

JELLINEK, GISELA, and MAURICE E. STANSBY. Masking undesirable flavors in fish oils 215

COOK, HARRY L., and M. ALICE MURPHY. Early developmental stages of the brown shrimp, Penaeus aztecus

Ives, reared in the laboratory 223

KOURY, BARBARA, JOHN SPINELLI, and DAVE WIEG. Protein autolysis rates at various pH's and temper-
atures in hake, Merluccius producUis, and Pacific herring, Clupea harengus pallasi, and their effect on yield in
the preparation of fish protein concentrate 241

Notes

EMILIANI, DENNIS A. Equipment for holding and releasing penaeid shrimp during marking experiments .... 247

TOPP, ROBERT W., and FRANK H. HOFF. An adult bluefin tuna, Thunnus thynnus, from a Florida west coast

urban waterway "^l

Wilbert McLeod Chapman

Milner Baily Schaefer

IN MEMORIAM

Wilbert McLeod Chapman and Milner Baily Schaefer

'0^:

lea / -

<

Ilu I LIBRARY \':^\

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A

^

Fisheries science in particular and society in
general suffered two tragic losses within the
period of only a month with the deaths of W.
M. Chapman on June 25, 1970, and M. B.
Schaefer on July 26, 1970. It is indeed a strange
and sad commentary that these two men whose
careers were intimately entwined since college
days should pass within such a short time of
each other.

Death is never easy to accept; it is particu-
larly hard to do so when it occurs at an untimely
age. Both of these brilliant men, we would
have hoped, would have been with us for years
to come. Both were unique, each in his own
way, and while the world adjusts to such events,
each is in a very real sense irreplaceable.

I had the opportunity to work rather closely
with both of them in California over most of
the past two decades. Wib Chapman was a
member of the California Marine Research Com-
mittee for many years, during most of which I
served as that body's secretary. It was a chal-
lenge to try to capture the essence of his re-
marks. The breadth of his knowledge and the
incisiveness of his thinking stimulated all of
us to higher goals, and we who were close to
him are better today for the good fortune of his
friendship.

"Benny" Schaefer was equally brilliant. His
expositions on the scientific method and pop-
ulation dynamics before the Inter-American
Tropical Tuna Commission were models of trans-
lation into lay terms of highly complex mathe-
matical theories applied to living resources.
Again a personal note. A few years ago Benny
was a consultant to the California Department
of Fish and Game during the formation of that
body's Fish and Wildlife Plan and we worked
closely in developing the philosophy behind the
sections concerned with living marine resources.
His imprint is deeply ingrained in that docu-
ment and in subsequent legislation, as well as
in my thinking.

And, as Wib Chapman had a large input in
that task, so did Benny into the deliberations
of the Marine Research Committee. Meantime
both worked diligently as members of the Cal-
ifornia Marine Advisory Committee on Marine
and Coastal Affairs. While these men will right-
fully be remembered for their major contribu-
tions to national and international affairs, their
energy and interests were such that they en-
compassed an amazingly broad spectrum. Each
of their contributions to the State of California
is more than most men could accomplish in a
lifetime devoted to that pursuit alone. One
hears parallel stories throughout the scientific
and fisheries communities.

Wilbert McLeod Chapman was born in Ka-
lama, Washington, on March 31, 1910. He died
in San Diego, California, on June 25, 1970, and
is survived by his wife of 35 years, Mary Eliza-
beth, and five of their six children.

He did both his undergraduate and graduate
work at the University of Washington, obtaining
his Ph.D. (fisheries) in 1937. His publications,
ranging from morphology and systematic ich-
thyology through fisheries economics and inter-
national law, number some 250. One of these.
Fishing in Troubled Waters, is a book recounting
his experiences as a fisheries development oflicer
in the South Pacific during World War II. It
is fascinating reading and makes one regret all
the more that the other books he had in mind
will never be forthcoming. He was particularly
proud of his papers on systematics and morphol-
ogy and always spoke fondly of that part of
his career.

His honors were many: among them he was
a Fellow of the Guggenheim Foundation and of
the California Academy of Sciences, .Man of the
Year of the National Fisheries Institute in 1966,

and the recipient of the First Sea Grant College
Award in 1968.

He began his professional career in 1933 with
the International Fisheries (now Halibut) Com-
mission. He was later employed by the Wash-
ington State Department of Fisheries, the U.S.
Fish and Wildlife Service, and, in 1943, by the
California Academy of Sciences where he was
Curator of Fishes until 1947. It was during this
period that he served in a civilian capacity in
the South Pacific, his job being to develop sub-
sistence fisheries at advanced island bases.

In 1947, Dr. Chapman became director of the
School of Fisheries at the University of Wash-
ington. He left there in 1948 to become the
first Special Assistant to the Under Secretary
of State for Fish and Wildlife. In 1951 he be-
came Director of Research for the American
Tunaboat Association; a decade later he joined
the Van Camp Sea Food Company as Director
of the Division of Resources. When Van Camp
was acquired by the Ralston Purina Company
in 1968, he became Director, Marine Resources,
of that firm, a position he held until his death.

Milner Baily Schaefer was born in Cheyenne,
Wyoming, on December 14, 1912. He died in
San Diego, California, on July 26, 1970. He is
survived by his wife, Isabella, and three children.

Dr. Schaefer obtained his B.S. degree cum
laude from the University of Washington in
1936 and his doctorate from the same institution
in 1950. He worked for the Washington State
Department of Fisheries from 1935 to 1938 and
for the International Pacific Salmon Fisheries
Commission from 1938 until 1942.

Following wartime duty with the Navy, he
joined the U.S. Fish and Wildlife Service in
1946, serving first as a fishery research biologist

in the South Pacific Fisheries Investigations
at Stanford, and from 1948 to 1950 as Chief,
Research & Development, Pacific Oceanic Fish-
ery Investigations in Honolulu.

He became Director of Investigations of the
Inter-American Tropical Tuna Commission in
1951, holding that post until he became Director
of the Institute of Marine Resources and Pro-
fessor of Oceanography, Scripps Institution of
Oceanography, University of California, in 1962.
He remained there until his death save for an
18-month period in 1967-69 during which he
was Science Adviser to Secretary of the Interior
Stewart Udall.

Among other honors, he was a fellow of the
California Academy of Sciences and a member
of the National Academy of Sciences. He wrote
more than 100 scientific papers, particularly in
the area of population djTiamics and fisheries
development and utilization. He served on a
multitude of panels at the international, national
and state levels. Despite his huge workload, he
always found time to discuss individual problems
with people both large and small, and to ad-
minister and develop first the Inter-American
Tropical Tuna Commission and later the Insti-
tute of Marine Resources in an exemplarj' man-
ner, setting standards for each that others will
be hard-pressed to equal.

This recitation cannot give a measure of these
men: their unflagging energy, their knowledge
in fields far apart from fisheries, their ability
as raconteurs, their good fellowship. Nor does
it give a measure of their contributions to the
nation and to the world, contributions that will
help make it a better place in which to live for
a long time to come.

Philip M. Roedel

KINDS AND ABUNDANCE OF FISH LARVAE IN THE EASTERN
TROPICAL PACIFIC, BASED ON COLLECTIONS MADE ON EASTROPAC I

Elbert H. Ahlstrom'
ABSTRACT

This paper deals with kinds and counts of fish larvae obtained in 482 oblique plankton hauls taken
over an extensive area of the eastern tropical Pacific on EASTROPAC I, a four-vessel cooperative
survey made during February-March 1967. On the basis of abundance of larvae, the dominant fish
group in oceanic waters are the myctophid lanternfishes (47 %), gonostomatid lightfishes (23 %),
hatchetfishes, Stemoptychidae (6 %), bathylagid smelts (5 %). Scombrid larvae ranked fifth, and ex-
ceeded 2 % of the count.
Two kinds of larvae were outstandingly abundant : larvae of the lantemfish Diogenichthys latematus
made up over 25 % of the total, while larvae of the gonostomatid genus Vinciguerria made up almost
20 %. More fish larvae were obtained per haul, on the average, in the eastern tropical Pacific than
were obtained per haul in the intensively surveyed waters of the California Current region off Cal-
ifornia and Baja California.

EASTROPAC I was the first and most wide-
ranging of a series of cooperative cruises made
in tlie eastern tropical Pacific between February
1967 and April 1968. A vast expanse of the
eastern tropical Pacific was surveyed on EAS-
TROPAC I, extending from lat 20° N to 20° S,
and from the American coasts ofi'shore to long
126° W (Fig. 1). Four research vessels par-
ticipated in EASTROPAC I: Alaminos oper-
ated by Texas A & M, occupied the inner pat-
tern, while Rockaway operated by the U.S.
Coast Guard, David Star?- Jordan operated by
the Bureau of Commercial Fisheries (now the
National Marine Fisheries Service), and Argo
operated by the Scripps Institution of Ocean-
ography, occupied patterns successively seaward.
The oceanographic, biological, and meteorolog-
ical data collected on EASTROPAC cruises will
be graphically presented in a series of EAS-
TROPAC atlases, including generalized charts
dealing with fish eggs and larvae.

The present paper is the result of a chain of
events that began 2 decades ago, at the initiation
of CalCOFI (California Cooperative Oceanic
Fisheries Investigations) in which a large-scale
sea program was set up to investigate the distri-

' National Marine Fisheries Service Fishery-Ocean-
ography Center, La JoUa, Calif. 92037.

bution and abundance of sardine spawning, and
the factors underlying fluctuations in survival
of the early life-history stages of sardines. The
plankton collections not only contained eggs and
larvae of sardine but those of most other pelagic
fishes in the California Current region. A de-
cision was made to attempt to identify and enu-
merate all fish larvae in the collections in order
to obtain more precise information about the eco-
logical associates of the sardine. At that time
few fish larvae, other than those of the sardine
and anchovy, could be identified.

Within a few years most kinds of fish larvae
were identified to genus or species. Once the
larvae were identified and enumerated, it be-
came obvious that this was an exceptionally use-
ful tool for evaluating fish resources. Most
oceanic fishes have pelagic eggs and/or larvae
that are distributed in or just below the photic
zone, i.e. within the upper 150 to 200 m of depth.
At no other time in their life histories are so
many kinds of fishes associated together — deep-
sea fishes (mesopelagic and bathypelagic) as
well as epipelagic species — where they can be
collected quantitatively with a single type of
gear, a plankton net.

Once the larvae of the pelagic fish fauna of
a region, such as those in the California Cur-
rent region, are known, there is a large trans-

Manuscript received September 1970.

FISHERY BULLETIN: VOL. 69, NO. I, 1971.

FISHERY BULLETIN: VOL. 69. NO. I
90° 80°

Figure 1. — Location of plankton stations occupied by four research vessels participating in EASTROPAC I.
Symbols for vessels indicated in legend above. Samples collected from Argo are numbered as 11.000 series
(as 11.022, 11.173), samples from David Starr Jordan as 12.000 series, Rockaway samples as 13.000 series and
Alaminos samples as 14.000 series.

f erence of the accumulated knowledge and skills
for work in other areas, such as, in this in-
stance, the eastern tropical Pacific. My study
was undertaken to demonstrate the value of
identifying all elements of the fish fauna of
tropical regions, rather than restricting interest
to scombrid larvae. Much information can be
gained for little extra expense (a few percent
of the cost of collecting the material at sea) .
Of equal consequence, identification of all kinds
of fish larvae can be made more critically in-
cluding scombrid larvae.

METHODS OF MAKING
ZOOPLANKTON COLLECTIONS

Three nets, differing in size and in coarseness
of mesh, were employed to collect zooplankton
and micronekton on EASTROPAC cruises. In
this paper I am concerned primarily with
oblique hauls made with the net of intermediate
size and mesh — a net, 1-m mouth diameter, con-
structed of 505 /J. nylon (Nitex) cloth, with ap-
proximately a 5 to 1 ratio of effective straining
surface (pore area) to mouth area. This net
was paired in an assembly frame with a finer-

4

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

meshed net when hauled obliquely, but was used
alone for taking surface hauls. The finer-
meshed net was 0.5 m in diameter at the mouth,
constructed of 333 /^ Nitex cloth, with approx-
imately an 8 to 1 ratio of effective straining
surface to mouth area. The third net, used for
collecting micronekton, had a 5-ft square mouth
opening and was constructed of mesh measuring
approximately 5.5 X 2.5 mm; this net could
not be operated from the research vessel Rock-
away on EASTROPAC I but was employed from
the other three vessels.

Usually four zooplankton collections were
made at each "biological" station: an oblique
collection and a surface collection with the 1-m
net, an oblique collection with the 0.5-m net, and
an oblique collection with the micronekton net.

In taking oblique plankton hauls, the 1-m net
was paired in an assembly frame with the 0.5
m net. The assembly of nets was fastened to
the towing cable by a bridle about 5 m above
a 100-lb weight. The assembly was lowered to
depth by paying out 300 m of towing cable at
the controlled rate of 50 m of wire per minute.
The assembly remained at depth for 0.5 min and
then was retrieved at a uniform rate of 20 m
per min. Total towing time was about 21.5 min.
Towing speed was ca. 2 knots. The depth
reached by the net was estimated from the angle
of stray (departure from the vertical) of the
towing cable. We sought to maintain an angle
of stray of 45°, which lowered the assembly
to a depth of approximately 210 m. Our con-
cern was to sample the upper 200-m stratum.
The average depths of hauls taken by the four
research vessels are summarized in Table 1.
Over 80 % of the hauls made on EASTROPAC I
were lowered to depths of 200 m or more, and
nearly 95 ''r reached depths of 180 m or greater.
However, two hauls were exceptionally shallow
(71-90 m) , and nine additional hauls were taken
to depths of less than 150 m.

Usually four paired net-assembly hauls were
taken per day, spaced at about 6-hr intervals.
Although the four hauls were planned to be taken
at about midnight, dawn, noon, and sunset, the
timing of hauls was not coordinated between
research vessels. The middle-of-the-night hauls

Table 1. — Depth of paired oblique plankton hauls taken
by the four research vessels on EASTROPAC I. (Net
lowered by paying out 300 m of towing cable)

Number

of

houls

token

to eoch depth interval from

Average depth

of houl

Argo

D

avid St
Jordan

arr

Rockaway

Alaminot

All
vessels

M

70.1. 80.0

__

1

80.1- 90.0

_,

_.

_.

1

90.1-100.0

__

__

..

__

__

100.1-110.0

_^

1

110.1-120.0

..

__

__

_.

._

120.1-130.0

2

__

3

130.1-140.0

1

__

__

1

140.1-150.0

1

__

_.

150.1-160.0

__

__

1

2

3

160.1-170.0

2

__

2

2

6

170.1-130.0

2

2

2

1

7

180.1-190.0

15

5

4

5

29

190.1-200.0

21

10

11

10

52

200.1-210.0

41

59

58

30

188

210.1-220.0

26

44

57

41

168

220.1-230.0

9

_.

3

5

17

230.1-240.0

-'

—

1

—

1

Toral

119

121

139

103

482

were all taken before midnight (2201-2400)
on Rockaway, for example, while on Argo
most hauls, were made after midnight (be-
tween 0001 and 0400 hr). The time of day
of occupancy of stations (based on the midtime
of each haul) is summarized by hourly intervals
in Table 2. At least some hauls were taken
during every hour of the day, although fewer
than 10 (2-8) were obtained during six of the
hourly intervals. Fewest hauls were obtained
between 0901 and 1000 hr (2 hauls) and be-
tween 2101 and 2200 hr (4 hauls), whereas
the largest number of hauls were taken between
2201 and 2300 hr (59 hauls) and between 1001
and 1100 hr (53 hauls). Hauls were made
with equal frequency during the four periods
of the day on Argo, Jordan, and Rockaway;
most plankton hauls were taken near midnight
or noon from Alaminos.

The numbering system for observations em-
ployed on EASTROPAC cruises made use of five
digits divided into two groups, as 11.022, 12.002,
etc. The outer digit preceding the period is the
cruise number common to all vessels participat-
ing in a given EASTROPAC cruise; for EAS-
TROPAC I, this number is 1. The other digit
preceding the period is the identifying number
given to each research vessel, with the lowest

FISHERY BULLETIN: VOL. 69. NO. I

Table 2. — Hour of day that paired oblique plankton
hauls were taken from the four research vessels par-
ticipating in EASTROPAC I. (Midtime of haul used.)

Hours of
day

Number of hauls token during each hour of the day frorr

Argo

David Starr
Jordan

Rockaway

Alaminos

All

vessels

0001-0100

7

10

0

3

20

01 01 -0200

8

7

0

2

17

0201-0300

5

2

0

0

7

0301-0400

9

0

7

0

16

0401-0500

1

1

17

1

20

0501-0600

2

9

10

3

24

0601-0700

7

10

1

1

19

0701-0800

13

10

0

0

23

0801-0900

7

0

0

0

7

0901-1000

0

0

0

2

2

1001-1100

1

0

26

26

53

1101-1200

1

5

5

10

21

1201-1300

7

22

3

1

33

1301-1400

12

3

1

4

20

1401-1500

8

0

0

0

a

1501-1600

1

1

12

1

15

1601-1700

0

0

10

3

13

1701-1800

8

6

12

6

32

1801-1900

7

19

1

0

27

1901-2000

10

1

0

0

11

2001-2100

3

3

0

0

6

2101-2200

0

1

0

3

4

2201-2300

2

2

23

32

59

2301-2400

0

9

11

5

25

Total

119

121

139

103

482

number given to the offshore vessel. The three
digits following the period are numbers given
to observations made from each vessel during a
cruise, numbered sequentially. Not all "stations"
included obliqne plankton hauls; hence there are
gaps in numbers applied to plankton collections.
The locations of plankton stations occupied by
the four research vessels participating in
EASTROPAC I are showTi in Figure 1. Sam-
ples collected from the Argo are designated as
the 11.000 series, samples from the David Stan-
Jordan as 12.000 series, Rockaway samples as
13.000 series and Alaminos samples as 14.000
series. In tables to follow, the series of samples
taken by each vessel is designated by the above
identifying series numbers. The aggregate of
stations occupied by each vessel is referred to in
text discussions as its pattern.

PROCESSING SAMPLES ASHORE

As noted above, only samples from 1-m
oblique net hauls were sorted routinely for fish
eggs and larvae. As a rule the entire sample was
sorted; in fact only six collections out of 482

were aliquoted — four collections were split into
50 ^r aliquots, two collections into 2.5 '^r aliquots.

The author made all identifications and counts
of lan'ae from EASTROPAC I collections. Ac-
tual counts of larvae rather than standardized
values (see below) are used in tabulation
throughout this paper, except one (Table 7).
There are several reasons why I chose to do this.
As indicated previously, all hauls were made in
a roughly comparable fashion. In many studies
the investigator is interested in the presence or
absence of the larvae of a given species or as-
semblage of species as such relate to water
masses, community composition, time of day, etc.
Such information is most readily obtained from
records of actual counts. Some statistical tests
require the use of original counts rather than
standardized data. For persons interested in
deriving standardized counts comparable with
those employed for CalCOFI data (Ahlstrom,
1953), standard haul factors for the 482 oblique
hauls taken with the 1-m net on EASTROPAC I
are given in Appendix Table 7.

Two major considerations in the quantitative
sampling of fish larvae for resources evaluation
are (1) how well has their depth range been
covered and (2) how effectively have the larvae
been sampled within this layer?

We do not have direct answers to either of
these questions from EASTROPAC cruises.
No studies were made on depth distributions of
fish eggs and larvae in the EASTROPAC area.
As will appear, fewer fish larvae wei'e obtained
during daylight hours than in night hauls; how-
ever, we lack information on how completely
larvae were sampled in night hauls.

DEPTH DISTRIBUTION OF FISH
LARVAE

Although collecting methods used on EAS-
TROPAC did not permit a study of depth distri-
bution of fish larvae, such information for the
California Current region off California and
Baja California and in a less detailed way for
the NORPAC Expedition of 1955 are available
(Ahlstrom, 1959).

In the California Current region, most fish
eggs and larvae were distributed within the up-

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

per mixed layer or in the upper portion of the
thermocline, between the surface and approxi-
mately 125 m. Of the 15 most common kinds
of fish larvae taken in vertical distribution ser-
ies, 12 were so distributed (ibid., p. 134). Two
of the kinds that occurred most commonly below
the thermocline were bathylagid smelts, closely
related to the two common bathylagid smelts
taken on EASTROPAC I.

On the NORPAC Expedition of August 1955,
two depth strata were sampled at most stations ;
a closing net, fastened to the towing cable 200 m
below a standard open plankton net, sampled
the level between 262 and 131 m on the average,
while the upper net sampled from the surface
to approximately 131 m deep. Only about one-
ninth as many larvae were taken in the closing
net hauls as in the upper net hauls; fully half
of these were larvae of hatchetfish, family Ster-
noptychidae, largely absent from upper net
hauls. The two most abundant kinds of fish
larvae taken on EASTROPAC I were those of
the myctophid lanternfish, Diogenichthys kitem-
atics, and of the gonostomatid lightfish, Vinci-
guerria spp. In NORPAC collections, only 3 %
of the larvae of D. laternatus were taken in the
closing net hauls and only 2 % of the Vinciguer-
ria larvae. Among the kinds of larvae common
to both the NORPAC and EASTROPAC sur-
veys that occurred in significant numbers in the
deeper NORPAC collections were those of Chaul-
iodus (72 % taken in closing net hauls), Proto-
myctophum (48 %) and I diacanthus (32 %).

Inasmuch as the vertical distribution studies in
the California Current region had pointed up the

importance of the thermocline in the depth distri-
bution of larvae, the pattern of thermocline depth
was analyzed for EASTROPAC I (Table 3).

Thermocline depth was invariably shallow in
the inner pattern occupied by Alaminos (data
not included in Table 3) ; the greatest depth
recorded was only 40 m, and the majority of
observations were at depths shallower than 20
m. Along the six station lines covered in Table
3, thermocline depths were shallowest near the
equator, and usually were deepest at the north-
ern (20-15° N) and southern (15-20° S) ends
of the lines. The thermocline also deepened off-
shore; approximately three-fourths of the rec-
ords of thermocline depths of 50 m or greater
were from the tw^o outer lines, occupied by Argo.

Most oblique plankton hauls taken on EAS-
TROPAC I sampled to depths of 200 m or more
(Table 2), hence sampled considerably deeper
than the thermocline in all parts of the EAS-
TROPAC area.

EFFECTIVENESS OF SAMPLING FISH

LARVAE IN DAYLIGHT HAULS
AS COMPARED WITH NIGHT HAULS

Fewer fish larvae were obtained in hauls made
during daylight hours than at night (Table 4).
Original (unstandardized) counts of larvae av-
eraged 2.76 times as many in night hauls as in
day hauls, 285 larvae per occupancy as compared
with 103 larvae. Hauls made within 1 hr of
sunrise or sunset contained intermediate num-
bers of larvae, averaging 217 larvae per oc-
cupancy.

Table 3. — Summary of records of thermocline depths along six station lines occupied by the research vessels
Rockaway, David Starr Jordan, and Argo on EASTROPAC I.

Station line
along longitude

Range in depth of thermocline (m) at latitudes

15-10° N

5° N-0°

0-5" S

5-10° S

10-15° S

15-20° S

All
latitudes

92° W

0-1 S

7-14

5-29

0-16

15-40

24-45

30-54

0-54

98°

16-30

13-68

23-t4

5-13

2-27

13-32

20-48

40-60

2-68

105*

„

37-50

27-14

0-20

0-28

23-45

24-55

54-66

0^56

112°

8-42

41-79

32-58

0-37

2-22

33-52

..

0-79

119°

3«hS7

44-90

42-55

0-85

0-65

34-76

50-73

30-71

0-90

126°

52-116

45-79

35-49

0^2

0-60

40-71

43-71

43-70

0-116

% obs. with
T. D. shallower
than 10. 1 m

17 %

8 %

7 %

46 %

43 %

0

0

0

20 %

% obs. w
T. D. deep
thon 49.9

th

m

56 %

46 %

9 %

11 %

9 %

25 %

35 %

63 %

26 %

FISHERY BULLETIN: VOL. 69, NO. I

3
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AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

Larvae of some families of fishes were sampled
almost as well in day hauls as in night hauls
— including Sternoptychidae, Bathylagidae, and
Melamphaidae. In contrast, less than one-
fourth as many gonostomatid larvae and one-
third as many myctophid larvae were taken in
day hauls, on the average, as in night hauls.
Catches of scombrid larvae were more variable
with regard to time of sampling — the night-day
ratio in the outer half of the EASTROPAC area
was only about 1.5 to 1, whereas the ratio
jumped to about 7.5 to 1 in the inner pattern
occupied by Alaminos. Larvae collected about
in equal amounts in day and night hauls were
those known to occur principally below the
thermocline.

Despite the lower abundance of larvae in day
hauls as compared with night hauls, the per-
centage of hauls containing larvae of most fam-
ilies was only slightly lower (Table 5). The
most marked day/night difference in frequency
of occurrence was for scombrid larvae, these

Table 5. — Percentage of hauls containing larvae of
the more abundant fish families on EASTROPAC I,
grouped by day, night and dawn or sunset.

Family

Day
hauls

Night
hauls

Dawn or

sunset hauls

(± 1 hr)

All
hauls

%

%

%

%

Myctophidae

97.4

97.8

99.0

97.9

Gonostomctidae

92.7

97.3

95.2

95 0

Sternoptychidae

.70.5

76.1

67.6

69.9

Bathylagidae

61.1

65.2

61.9

62.9

Melamphaidae

60.6

65.2

58-1

61.8

Scombridae

31.1

45.1

40.0

38.4

All others

94.8

99.5

97.1

97.1

Total

97.9

100.0

100.0

99.2

were taken in 45 % of night hauls, but in only
31 '/'c of day hauls. In the discussions that fol-
low I make use of all collection data, irrespective
of time of collection.

NUMBERS OF FISH LARVAE
OBTAINED ON EASTROPAC I

Fish larvae were obtained in 478 of 482
oblique plankton tows made with the 1-m plank-
ton net on EASTROPAC I. The number of
larvae per collection ranged from 0 to 2,197,
averaging 197 larvae (actual counts).

Differences in abundance of larvae with lat-
itude are summarized for the four series in Table
6. Fish larvae were obtained in largest num-
bers, on the average, in an equatorial band ex-
tending from about lat 10° N to 5° S. The least
productive waters for fish larvae were in the
central water mass of the South Pacific, espe-
cially between lat 15° and 20° S.

Abundance of fish larvae also decreased off-
shore,' averaging only 130 larvae per haul in
the outer pattern, occupied by Argo, as com-
pared with 246 larvae per haul in the inner
pattern, occupied by Alaminos.

Tropical waters and oceanic waters are usu-
ally considered to be relatively unproductive,
compared with temperate coastal regions such
as the California Current region (Ryther, 1969).
Hence, it is surprising to find that the average
number of fish larvae obtained per haul on
EASTROPAC I was larger than either on the
CalCOFI cruises from the California Current
region (Ahlstrom, 1969) or on NORPAC (un-

Table 6. — Total catches of fish larvae (actual counts) taken by the four research vessels on EASTROPAC I,

summarized by latitude.

Argo
n.OOO Series

David S(flrr Jordan
12.000 Series

Ro(kaway

13.000 Series

Alaminos
14.000 Series

Total
EASTROPAC 1

Latitude

No.
hauls

No.
larvae

No.

hauls

No.
larvae

No.
hauls

No.

larvae

No. No.
hauls larvae

No.

houls

No.
larvae

Average no.

larvae per
haul

20° N-15° N

16

1,070

20

4,128

5

462

__

__

41

5,660

138.0

15° N-10° N

14

1,372

23

3,130

26

5,508

--

--

63

10,010

158.0

10° N- 5° N

14

2,516

14

3,344

29

10,104

15

5,167

72

21,131

293.5

5° N- 0°

14

4,797

15

4,403

14

4,331

27

11,329

70

24,860

355.1

0° ■ 5° S

14

2,089

18

5,454

14

4,350

17

5,042

63

16,935

268.8

5° S-10° S

13

1,370

15

1,051

14

2,360

16

2,113

58

6,894

118.9

10° 3-15° S

14

1,512

8

863

15

2,337

28

1,673

65

6,385

98.2

15° 3-20° S

20

793

8

513

22

1,928

—

-

50

3,234

64.7

Total

119

15,519

121

22,886

139

31,380

103

25,324

482

95,109

197,3

FISHERY BULLETIN: VOL. 69, NO. 1

published data) . Standard haul totals of larvae
are used in this comparison (Table 7) not ori-
ginal counts. CalCOFI cruises repeatedly sur-
veyed a coastal area extending 200 to 300 miles
offshore between San Francisco, California, and
Magdalena Bay, Baja California. NORPAC
was the first comprehensive survey of the North
Pacific, made in August-September 1955; the
area surveyed by four CalCOFI vessels partici-
pating in NORPAC was between lat 20° and 45°
N and offshore to long 150° W.

Table 7. — Comparison of the average number of fish
larvae obtained per haul (standard haul values) EAS-
TROPAC I, NORPAC, and CalCOFI cruises.

Number
hauls

Averoge Total

depth number of

of hauls fish larvae'

Average

number
larvae/haul

EASTROPAC 1

1967

482

CO.

200 m

274,131

569

NORPAC

1955

196

CO.

260 m

27,000

"138

CalCOFI cruises

1956

1,407

CO.

140 m

408,140

290

1957

1,493

CO.

140 m

493,550

331

1958

1,852

ca.

140 m

456,020

246

1959

2,182

CO.

140 m

470,450

216

1960

1,826

CO.

140 m

504,980

277

^ Standard houl totals.

2 Data from two net hauls combined: on overage of 124 larvae per
haul were token in upper net hauls (0 to 130 m) and an average of 14
larvae per haul in closing net hauls,, sampling between co. 260 and 130 m.

EASTROPAC hauls sampled a somewhat
deeper stratum than hauls made on CalCOFI
cruises, ca. 200 m as compared to ca. 140 m. As
indicated previously, information is available for
the majority of NORPAC stations on the rel-
ative abundance of fish larvae in the level be-
tween ca. 130 and 260 m (closing net hauls) as
compai'ed with the level above, 0 to 130 m. Only
about one-ninth as many larvae were taken in the
deeper hauls.

The difference between catches of larvae on
EASTROPAC I and NORPAC are particularly
marked — four times as many larvae were taken
per haul, on the average, on EASTROPAC I as
on NORPAC (both nets combined). For com-
parison with shallower CalCOFI hauls, I am as-
suming that 10 % of the EASTROPAC larvae
were obtained in the level between ca. 140 and
200 m. The adjusted value for EASTROPAC
larvae, 512 larvae per haul, on the average, is
1.55 times as large as the highest CalCOFI val-
ue listed (331 larvae per haul in 1957) and 2.35
times as large as the lowest value (216 larvae
per haul in 1959) .

The majority of EASTROPAC larvae were
those of fishes which never attain a large size as
adults — myctophids, gonostomatids, sternopty-
chids, etc. — hence numbers of larvae, per se,
cannot be considered reliable indices of biomass.
The familial composition of larvae was not dis-
similar on NORPAC and EASTROPAC, how-
ever; hence this comparison of relative abun-
dance of larvae is more relevant, as regards
biomass, than the comparison with CalCOFI
fauna.

KINDS OF FISH LARVAE OBTAINED
ON EASTROPAC I

The kinds of larvae obtained on EASTRO-
PAC I are summarized by family and vessel
pattern in Table 8, the principal summary table
in this paper. Larvae of more than 50 families
are listed, but larvae of 10 families contributed
90 9f of the total. The myctophids were the
dominant group with 47.2 % of the larvae oc-
curring in nearly 98 % of the collections. Gono-
stomatid lai-vae were about half as numerous,
contributing 23.2 % of the larvae while oc-
curring in 95 % of the collections. Hatchetfish
larvae (Sternoptychidae) ranked third in
abundance with 6 % of the larvae taken in 70 %
of the hauls. Bathylagid larvae also exceeded
5 % of the total and occurred in 63 % of the
collections. Scombrid larvae ranked fifth and
exceeded 2 % of the count, followed by Breg-
macerotidae, 1.9 %, Paralepididae, 1.7 %, Idia-
canthidae, 1.0 Yc, Nomeidae, 1.0 %, and Mel-
amphaidae, 0.9 %. About one-third of the re-
maining larvae were too poorly preserved (dis-
integrated) to identity.

On the basis of larval abundance, the domi-
nant orders of fishes in oceanic waters are the
Myctophiformes and Salmoniformes, making up
between 85 and 88 'li ; the latter value assumes
a proportionate representation of larvae of these
groups in the "disintegrated" category, i.e.,
larvae too damaged or disintegrated to identify
with certainty. Despite the dominance of fishes
of the above two orders, a number of other
groups of fishes are represented in the oceanic
pelagic fish fauna. The berycoid fishes are rep-

10

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

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11

FISHERY BULLETIN: VOL. 69, NO. I

resented by Melamphaidae, a family of fishes that
is almost as ubiquitous as the myctophids or
gonostomatids. Fishes of the gadoid family,
Bregmacerotidae, also are widely distributed in
the warmer waters of all oceans. Among the
ubiquitous epipelagics are the flyingfishes, Ex-
ocoetidae.

Only a moderate number of perciform fishes
are widely distributed in offshore, oceanic wa-
ters. Among the more important are fishes of
the families Scombridae, Gempylidae, Trichiur-
idae, Istiophoridae, Coryphaenidae, Bramidae,
Nomeidae, Apogonidae, Chiasmodontidae, and
Tetragonuridae.

Larvae of some demersal fishes have a much
wider offshore distribution than one would asso-
ciate with the known distribution of adults. In-
cluded in this group are larvae of bothid and
cynoglossid flatfishes, and larvae of Scorpaeni-
dae, Gobiidae, and Labridae.

Another widely distributed gi-oup in oceanic
waters are the bizarre ceratioid fishes. The
rotund larvae of these fishes were taken in about
30 % of the EASTROPAC collections, always in
small numbers.

The basic data on the kinds and numbers of
fish larvae obtained in the 482 EASTROPAC I
collections are contained in six appendix tables,
whose contents are summarized below, and keyed
to Table 8 and to other tables in this report.

Appendix Table 1. — Counts of fish larvae,
tabulated by family, for all stations occupied
on EASTROPAC I. This table contains 22
categories, mostly families, but for complete-
ness, a category is included for "other identi-
fied larvae," one for "unidentified larvae" and
one for "disintegrated larvae" (i.e., larvae too
damaged or disintegrated to identify with any
certainty) .

Appendix Table 2. — Myctophid larvae, tab-
ulated by genus or species, for all stations oc-
cupied on EASTROPAC I. Myctophid larvae
are tabulated by species for 12 kinds, and by
genus for 8 kinds. Also included are cate-
gories for unidentified myctophids, and total
myctophids. A summary of this appendix
table is contained in Table 15.

Appendix Table 3. — Counts of selected ca-
tegories of fish larvae by station. Table con-
tains 23 categories including 10 species, 10
genera, 2 families, and 1 suborder; 9 of these
were included in the category "other identi-
fied larvae" in Appendix Table 1.

Appendix Table 4. — Summary of occur-
rences and numbers of larvae of eight families
limited in distribution to a broad coastal band
or around offshore islands. Only positive
stations are included. These eight families
also were included in the category " other
identified larvae" in Appendix Table 1.

Appendix Table 5. — Numbers and kinds of
larvae of Gempylidae-Trichiuridae obtained
in EASTROPAC I collections. Only positive
stations are included. A summary of this ap-
pendix table is given in Table 19.

Appendix Table 6. — Numbers and kinds of
flatfish (Pleuronectiformes) larvae obtained
in EASTROPAC I collections. Only positive
hauls are included. A summary of this ap-
pendix table is given in Table 22.

Appendix Table 7.— Standardized haul
factors for the 482 oblique 1-m net hauls taken
on EASTROPAC I. These factors adjust ori-
ginal counts of larvae to the comparable stan-
dard of numbers of larvae in 10 m3 of water
strained per meter of depth fished.

I will not attempt to comment on all 58 cate-
gories (family or larger grouping) summarized
in Table 8, but will limit my discussion to 31
of these. In order to tie the text discussion
closely to this table, I i-etain the numbers for
categories as given in Table 8; those discussed
in the text ai-e preceded by an asterisk in this
table.

COMMENTS ON LARVAE OF THE

MAJOR FISH FAMILIES COLLECTED

ON EASTROPAC I

1. CLUPEIDAE
( 10 occurrences, 81 larvae)

Three species of clupeid larvae were taken
in EASTROPAC I collections — Opisthonema sp.

12

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

(5 occurrences, 12 larvae), Etrumeus acumina-
tus Gilbert (2 occurrences, 6 larvae), and Sar-
dinops sagax (Jenyns) (3 occurrences, 63
larvae). The latter two species were collected
in the vicinity of the Galapagos Islands.

2. ENGRAULIDAE
(10 occurrences, 205 larvae)

The majority of the engraulids (5 occurrences,
174 specimens) were those of the Peruvian an-
chovy, Engraulis ringens Jenyns, collected at
coastal stations between lat 6° and 13.5° S. Al-
though larvae from only a few surface hauls
have been sorted as yet, one haul was outstand-
ing: the surface tow taken at station 14.069
contained 10,466 larvae and transforming speci-
mens of Peruvian anchovy, E. ringens. Speci-
mens ranged in size from 3.5 to 37.5 mm ; most
were between 4.0 and 7.5 mm in length but even
transforming specimens, 20.0 to 37.5 mm long,
were rather common (83 individuals). In the
oblique 1-m haul at this station, 97 anchovy
larvae were obtained.

3. ARGENTINIDAE
(43 occurrences, 87 larvae)

Three kinds of argentinid larvae were ob-
tained: Argentina sp. (1 specimen), Nansenia
sp. A (84 lai-vae), and Nansetiia sp. B. (2
larvae) . The specific identities of the two kinds
of Nansenia larvae are still uncertain. On
EASTROPAC I, Nansenia sp. A was taken most
commonly in an equatorial band between lat 5°
N and 5° S (Fig. 2). Larvae of Nansenia sp.
A also occur in the southern portion of the area
surveyed on cruises of CalCOFI, particularly to
the south of Point San Eugenio, Baja California.
A Nansenia larva with markedly different pig-
mentation pattern was obtained at station 11.154
in the central water mass of the South Pacific.
A similarly pigmented Nanseyiia larva was ob-
tained on NORPAC from the central water mass
of the North Pacific.

4. BATHYLAGIDAE

( 304 occurrences, 4,880 larvae)

Although two kinds of Bathylagus larvae were
obtained, one species was taken in only two con-

tiguous southern stations, 12.142 and 12.144.
The eyes of the latter were carried on short
stalks. The distribution of larvae of the com-
monly occurring species, B. nigrigenys Parr
(296 occurrences, 2,987 larvae), was almost
identical with that of the myctophid, Diogenich-
thys laternatus (Garman) (Fig. 3). The larvae
of neither species occurred in the central South
Pacific water mass; on the four outer lines, sur-
veyed by Argo and Jordan, the occurrences of
B. nigrigenys larvae ended at about lat 5° S.
In the portion of the EASTROPAC area in
which larvae of this species were distributed,
they occurred in three-fourths of the stations
occupied.

In the innermost pattern occupied by Alami-
nos, larvae of Leuroglossus stilbius urotranus
(Bussing, 1965) were common (37 occurrences,
1,890 larvae). All but four specimens were
obtained between lat 10° N and 10° S, and most
within 300 miles of the coast (Fig. 2).

5. GONOSTOMATIDAE
(459 occurrences, 22,046 larvae)

Areal occurrence and relative abundance of
gonostomatid larvae on EASTROPAC I are
summarized in Table 9. They were obtained in
95 % of the hauls and made up approximately
23.2 % of the larvae.

As noted earlier, gonostomatid larvae were
markedly more abundant in night hauls than
in day hauls: 4.35 times as many, on the aver-
age. In contrast, larvae of the closely related
hatchetfishes, Sternoptychidae, were taken in
only slightly larger numbers at night (1.24
times as many as in day hauls). In the section
dealing with depth distribution of fish larvae it
was pointed out that the gonostomatid, Vinci-
guerria spp. occurred no deeper than ca. 130 m
in NORPAC collections, whereas sternoptychid
larvae were inhabitants of the aphotic zone be-
low 130 m. An interesting exception should be
noted: gonostomatid larvae of the subfamily
Maurolicinae had depth distributions similar to
sternoptychid larvae on NORPAC. Larvae of
two Maurolicinae, Mauroliciis and Araiophos,
genera were taken on EASTROPAC. Although
the depth distribution of these genera has not

13

FISHERY BULLETIN: VOL. 69, NO. I
90° 80"

Figure 2. — Distribution of larvae of the argentinid, Nansenia spp., and of the bathylagid, Letiroglossiis stilbius
urotranus (Bussing) on KASTROPAC I. Records of occurrence of A'awscnto larvae are shown as open circles
with dot in center, while those of Leuroglossus larvae are open squares with dot (1 to 100 larvae) or closed squares
(101 to 490 larvae). Small solid circles represent other stations occupied on EASTROPAC I.

Table 9. — Areal occurrence and relative abundance of lari'ae of Gonostomatidae on EASTROPAC I.

Argo

David Starr Jordan

Rod

away

jilaminoj

Total

11.000 series

12.000

series

13.00C

series

14.000

series

EASTROPAC 1

Lalilude

No.

No.

No.

No.

No.

No.

No.

No.

No.

No.

Average no.

pOSitiVQ

positivo

positive

positive

positive

larvae per
positive haul

hauls

larvae

hauls

larvae

hauls

larvae

hauls

larvae

hauls

larvae

20° H\S°

N

14 418

20

1,534

5

115

..

41

2,067 50.4

15° N-10°

N

14 380

22

745

24

607

__

60

1,732 28.9

10° N- 5°

N

13 185

13

242

27

2.085

14

417

67

2,929 43.7

5° N- 0°

14 2,112

IS

637

14

1,825

27

1,882

70

6,456 92.2

0° - 5°

S

14 409

18

912

14

1,577

16

1,036

62

3,934 635

5° S-I0°

S

13 202

14

161

14

799

10

647

51

1,809 35.5

)0° S -IS-

S

14 635

8

368

IS

524

21

490

58

2,017 34.8

IS" S-20°

S

20 322

8

183

22

597

—

—

SO

1.102 22.0

Totol

lis 4,663

118

4,782

135

8,129

88

4,472

459

22,046 48.0

14

AHLSTROM : FISH LARVAE IN EASTERN TROPICAL PACIFIC
130* 120° 110°

100°

90°

80°

Figure 3. — Distribution of larvae of Bathylagus nigrigenys Parr on EASTROPAC I. Two orders of abundance
are shown: open circles with dot in center represent counts of 1 to 25 larvae, large solid circles represent
counts of 26 or more larvae. Small solid circles represent negative hauls.

been determined, they were sampled more fully
during daylight hours than other gonostomatids;
the night/day ratio for Maurolmis and Arai-
ophos larvae was ca. 1.6 and 2.0 respectively.

Larvae belonging to six gonostomatid genera
were common to abundant (Table 10) and
larvae of several additional genera were taken
occasionally. Larvae of two genera were of
outstanding importance in the EASTROPAC
area — Vinciguerria and Cyclothone. Vinciguer-
ria occurred in 87.5 % of the collections, Cyclo-
thone in 62.4 %.

Charts showing the distribution and relative

abundance of larvae of Gonostomatidae and
Sternoptychidae (combined) on EASTROPAC
I will be included in the EASTROPAC Atlas.

Araiophos eastropas Ahlstrom and Moser ( 18
occurrences, 529 larvae)

Larvae of A raiophos eastropas were obtained
only on the outermost pattern to the south of
lat 10° S (Fig. 4). Within this limited area it
was the most common gonostomatid. The spe-
cies taken on EASTROPAC represented an un-
described species in a genus that previously

15

FISHERY BULLETIN: VOL. 69. NO. 1

Table 10. — Frequency of occurrence and relative abundance of the kinds of gonostomatid larvae on EASTROPAC I.

Argo

DavU St

arr Jordan

Rork

away

AlaminoJ

Total

11.000 series

12.000 series

13.00C

series

I4.00C

series

EASTROPAC 1

Gonostomatid
larvae

No.

No.

No.

No.

No.

No.

No.

No.

No.

No.

positive

positive

positive

positive

positive

hauls

larvae

hauls

larvae

houls

larvae

hauls

larvae

hauls

larvae

liraiaphos eastropaj

18 529

0

0

0

0

0

0

18 529

Cydothone spp.

94 697

71

582

89

735

47

167

301 2,181

Diplopkos taenia

IS 51

40

107

14

24

1

I

73 183

Ichthyococcu! spp.

7 9

11

16

18

31

5

5

41 61

Maurolicui muelleri

0 0

11

43

19

143

13

78

43 264

VincigutTria spp.

96 3,339

109

4,011

131

7,179

86

4,211

422 18,740

Other gonostomotids

13 38

9

23

12

17

8

10

42 88

Total

IIS 4,663

118

4,782

135

8,129

88

4,472

459 22,046

FiGUKE 4. — Distribution of larvae of three species of Gonostomatidae on EASTROPAC I. Records of occurrence
of larvae of Araiophos eastropas Ahlstrom and Moser are shown as triangles, Diplophos taenia (Giinther) as
large open circles, and Maurolicus muelleri (Gmelin) as squares. Solid triangles and squares are for counts
of 26 or more larvae. Small solid circles represent negative hauls.

16

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

was known from a single collection made off
Hawaii (Grey, 1961). Adults and larvae were
described by Ahlstrom and Moser (1969).

Cyclothone spp. (301 occurrences, 2,181 larvae)

Larvae of Cyclothone spp. were taken least
frequently in the northern quarter of the EAS-
TROPAC pattern (betweeen lat 10° and 20° N,
and in the inner pattern occupied by Alaminos
(Table 11 and Fig. 5). In the former area,
less than 20 Sf of the hauls (20 of 103) con-
tained Cyclothone larvae; in the inshore pat-
tern only about 45 % of the hauls (47 of 103)
contained Cyclothone larvae. Over the remain-
der of the EASTROPAC I pattern Cyclothone
larvae occurred at most stations (234 of 276).
The lowest number of larvae per positive haul,
2.15 larvae, was obtained in the northern sec-
tion; the next lowest, 3.55 larvae per positive
haul, in the Alaminos pattern. Over the re-
mainder of the pattern, 8.42 larvae were ob-
tained per positive haul.

No attempt was made to identify the larvae
of Cyclothone to species, and our hauls did not
extend deep enough to collect adults.

Diplophos taenia Giinther (73 occurrences, 183
larvae )

A study was made of larval and adult speci-
mens of Diplophos in an attempt to determine
whether the Pacific specimens should be as-
signed to D. taenia or retained as a distinct
species, D. pacificus Giinther. Grey (1960) had
placed Pacific specimens in D. taenia but later
she (Grey, 1964, p. 89) developed reservations

because of the consistently lower photophore
count of the ventral series in Pacific specimens.
Without detailing my observations on Diplophos,
which I plan to publish separately, I have con-
cluded that our eastern Pacific Diplophos is not
separable from the Atlantic D. taenia.

Larvae of Diplophos were taken most com-
monly to the north of lat 10° N — 36 occurrences,
105 larvae (Fig. 4). The remaining 37 occur-
rences, 78 larvae were distributed throughout
the EASTROPAC I pattern.

Ichthyococcus spp. (41 occurrences, 61 larvae)

Two kinds of Ichthyococcus larvae were taken
on EASTROPAC L The specific identity of
the more common form has been determined as
/. irregularis Rechnitzer and Bohlke; the other
form has yet to be identified to species.

Maurolicus muelleri (Gmelin) (43 occurrences,
264 larvae )

Larvae of this species were taken only on an
equatorial band between lat 5° N and 5° S and
were not taken in the outer pattern occupied
by Argo (Fig. 4). This distribution, without
additional information, could be misleading.
Maurolicus is known to have a wide latitudinal
distribution in the South Pacific. For example,
Maurolicus larvae were obtained at lat 33° S
on MARCHILE VL the portion of EASTRO-
PAC II occupied by the Chilean vessel Yelcho.
We also have collections from south of New
Zealand, obtained on an Eltanin cruise. The
species may be carried northward oflF South
America in the Humboldt Current and then off-
shore in the equatorial current system.

Table 11.— Area

occurrence and relative abundance of larvae of Cyclothone

spp. on EASTROPAC I.

Argo
1 1 .000 series

David Starr Jordan
12.000 series

Rockaway
13.000 series

Alaminos
14.000 series

Total
EASTROPAC 1

Latitude

No.

positive

hauls

No.
larvae

No.

positive

hauls

No.
larvae

No.

positive

hauls

No.
larvae

No.

positive
hauls

No.
larvae

No.

positive

hauls

No.
larvae

Average no.
larvae per
positive haul

20° N-10° N

12

31

4

8

4

4

20

43

2.2

10° N- 0°

24

136

25

137

33

235

23

69

105

577

5.5

0° -10° S

24

179

29

246

20

117

13

43

86

585

6.8

10° S-20° S

34

351

13

191

32

379

11

55

90

976

10.8

Total

94

697

71

582

89

735

47

167

301

2,181

7.2

17

130°

T — \ — I — I — r

-| — I — I — I — I — I — I — I — r

100"

-I — I — \ — TTT — I — I — I — I — I — r— T — I— T — I — I — I — 1—1 — I — I — I — I — I — I I I — r

FISHERY BULLETIN: VOL. 69, NO. 1
90° 80°

20'

10'

10"

®
0

e
@
0

0
0

©
©

0
0

0

0

VM4NZANILL0

20"

s

Q®®® ® 1^

A

3® ©0001

I L_

I I I J 1—1—1 I I I I I I

130°

120"

no*

100*

90*

80"

Figure 5. — Distribution of larvae of the gonostomatid Cyclothone spp. on EASTROPAC I. Collections of 1 to
25 larvae are shown as circles with dot in center, collections of 26 or more larvae as large solid circles; neg-
ative hauls are shown as small solid circles.

Vinciguerria spp. (422 occurrences, 18,740
larvae )

Larvae of Vinciguerria occurred in more hauls
than those of any other genus and ranked sec-
ond in abundance to the myctophid genus Dio-
genichthys. The distribution of Vinciguerria
larvae is shown in Figure 6. Although most
of the material unquestionably is V. bicetia
(Garman) , some of the collections from offshore
and particularly from the central South Pacific
water mass between lat 5° and 20° S represent
V. nimbaria (Jordan and Williams) . The larvae
of V. nimbaria are indistinguishable from those

of V. lucetia (Ahlstrom and Counts, 1958),
hence identification must be made on meta-
morphosing specimens, juveniles, and adults.
The two species are closely allied, but readily
separable from V. poweriae (Cocco) and V.
attenuata (Cocco), the other two species of
Vinciguerria, at all stages of development. A
trenchant difference between the two "pairs"
of species is the development of a pair of sym-
physeal photophores under the lower jaw in V.
lucetia and V. nimbaria and the absence of this
pair in V. poweriae and V. attenuata. The two
characters most readily used for distinguishing

18

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC
130' 120° MO"

Figure 6. — Distribution of larvae of the gonostomatid, Vindguerria spp. on EASTROPAC I. Collections of
1 to 100 larvae are shown as circles with dot in center, collections of 101 or more larvae as large solid circles;
negative hauls are shown as small solid circles.

between V. lucetia and V. nimbaria are (1)
number of gill rakers and (2) number of IV
(and OV) photophores. Material of V. nim-
baria studied from the eastern North Pacific
(ibid.) had 5 to 6 +15 gill rakers and 23 to
24 IV photophores (13 to 14 OV photophores)
whereas V. lucetia had 8 to 10 + 18 to 23 gill
rakers and 20 to 23 IV photophores (10 to 13
OV photophores) . In the EASTROPAC area,
V. lucetia maintained the high gill raker counts,
but usually had 21 IV (11 OV) photophores.
The offshore form referred to V. nimbaria usu-
ally had 22 IV (12 OV) photophores (1 less

per group than in V. nimbaria from the temper-
ate North Pacific) and 6 to 7 + 15 to 16 gill
rakers (a slightly higher count).

In most areas the adults of the two species
of Vindguerria did not co-occur, hence the
larvae can be assigned with some assurance to
one or the other. For example, all collections
made between lat 5° and 20° S from Argo and
Jordan patterns were exclusively V. nimbaria.
On these patterns the plankton hauls were sup-
plemented by micronekton net hauls, and the
latter contained material of Vindguerria ju-
veniles and adults from most stations occupied

19

FISHERY BULLETIN: VOL. 69. NO. I

at night. Unfortunately, the micronekton net
was not used on Rockaway (12.000 series), and
insufficient numbers of older stages (metamor-
phosing specimens and juveniles) were taken in
plankton hauls to permit a meaningful separa-
tion of the two species in waters to the south
of lat 5° S in this series.

Vinciguerria poweriae (Cocco) co-occurred
with V. nimbaria in the central water mass of
the North Pacific (Ahlstrom and Counts, 1958),
but no material of V. poweriae was obtained in
EASTROPAC collections. However, material
of V. attenuata (Cocco) was obtained from
farther south in the eastern Pacific on the
"Downwind Expedition" — hence all four spe-
cies of Vinciguerria do occur in the eastern
Pacific.

Other gonostomatids (42 occurrences, 88 larvae)

Included in this category are larvae of two
identified genera, Gonostoma and Woodsia, and
several kinds of larvae that are unmistakably
gonostomatid, but not identified as to kind.

6. STERNOPTYCHIDAE
(337 occurrences, 5,687 larvae)

Hatchetfish larvae ranked third in abundance
(5.98 /f of total), exceeded by larvae of Mycto-
phidae and Gonostomatidae. The majority of
hatchetfish larvae were those of Sternoptyx di-
aphana Hermann, and most of the remainder of
Argyropelecus lychmis Carman. Because larvae
of Sternoptychidae are more fragile than most
other kinds and are usually in poor condition, no
attempt was made to identify them to genus or

species. Areal occurrence and relative abun-
dance of sternoptychid larvae on EASTROPAC
I are summarized in Table 12. Larvae were not
only taken in markedly more collections between
lat 10° N and 10° S— 94 9^ of the collections
were positive as compared with only 41 % in
the remainder of the pattern — but more larvae
were taken per positive haul — 21.1 larvae as
compared with 5.2.

7. ASTRONESTHIDAE
(12 occurrences, 13 larvae)

Several kinds of astronesthid larvae were
collected in the EASTROPAC area: only one
kind had heavy pigmentation on the body; the
others were lightly, but characteristically pig-
mented. Larvae of Astronesthidae are similar
in appearance to other stomiatoid larvae; they
have a slender, elongated body, and a long in-
testine that underlies the body for about Yiq or
more of the standard length, and usually has
a free terminal, trailing portion that can be quite
long, often trailing beyond the caudal fin. As-
tronesthid larvae can be distinguished readily
from other stomiatoid larvae by the forward po-
sition of the dorsal fin in relation to the anal
fin. Developmental series of astronesthid larvae
have not been described in literature. Eleven
of the 12 occurrences of astronesthid larvae were
taken within 10° ± of the equator.

8. CHAULIODONTIDAE
(80 occurrences, 165 larvae j

Larvae of Chaidiodus are readily identifiable
to genus, but are difficult to separate at the spe-

Table 12. — Areal occurrence and relative abundance of larvae of Sternoptychidae on EASTROPAC I.

Areo
1 1 .000 series

David St
12.000

arr Jordan
series

Ro<l
13.000

away
series

iltaminol
14.000 series

Total
EASTROPAC 1

Lotitude

No.

No.

No.

No.

No.

No.

No.

No.

No.

No.

Averoge no.

positrve
houls

larvae

positive
hauls

larvae

positive
houls

larvae

positive
hauls

larvae

positive
hauls

larvae

larvae per
positive haul

20° HAS'

N

8 44

0

0

0

0

..

..

8

44

5.5

15° N-10°

N

6 41

3

31

9

66

_.

_.

18

138

7.7

10° N- S°

N

14 312

14

479

29

1,006

14

237

71

2,034

28.6

S° N- 0°

14 133

15

430

13

456

22

414

64

1,433

22.4

0° - 5°

S

14 140

18

353

14

303

16

129

62

925

14 9

5° S-10°

S

12 198

14

317

14

210

10

104

50

829

16.6

10° S-I5°

S

13 40

8

98

n

83

5

7

37

228

6.2

15° S-20°

S

9 15

2

4

14

37

-

—

27

56

2.1

Totol

90 923

74

1.712

106

2,161

67

89 1

337

5,687

16.9

20

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

cies level, because of lack of pigmentation. It
has not been determined yet whether one or
more species of Chauliodus occur in the EAS-
TROPAC area. Chauliodus larvae were widely
distributed, usually occurring singly (50 such
occurrences). In only five hauls were six or
more larvae obtained per haul; all of these were
in the outer patterns occupied by Jordan and
Argo.

9. IDIACANTHIDAE

( 167 occurrences, 960 larvae)

It is not known definitely whether one or two
species of Idiaca?ithns occur in the eastern Pa-
cific; the problem hinges on whether /. pan-
amensis is distinct from /. antrostomus Gilbert.
Gibbs (1964) considered the two species to be
"probably synonymous." In the EASTROPAC
area, Idiacanthus occurred more frequently in
the northern portion of the pattern, between
lat 10° and 20° N, as is shown in Table 13.

10. OTHER STOMIATOIDEI
( 203 occurrences, 502 larvae )

Larvae belonging to thi'ee families are in-
cluded as other Stomiatoidei — i.e., of Stomiati-
dae, Melanostomiatidae, and Malacosteidae. The
most common larva in this category, that of
Bathophilus filifer (Garman) (86 occurrences,
227 larvae) is separately tabulated in Appendi.x
Table 3. Larvae of Eustomius, representing
several species, occurred in 17 collections. Lar-
vae of Sto7nias were separately tabulated from
only eight collections; however, a number of
larvae tabulated as unidentified stomiatoid lar-
vae undoubtedly are those of Stomias. Accord-

ing to Gibbs (1969), no fewer than three spe-
cies of Stomias occur in the eastern Pacific.
Many stomiatoid larvae were poorly preserved,
and were not identifiable with any certainty.

11. SYNODONTIDAE
( 10 occurrences, 41 larvae)

All but three specimens were taken in the in-
ner pattern, occupied by Alaminos. Six of the
seven occurrences in this pattern were at con-
tiguous stations occupied off" Ecuador and the
Gulf of Panama (Fig. 7). Synodontidae are
coastal forms. No attempt was made to identify
the larvae to the species level.

12. CHLOROPHTHALMIDAE

( 1 occurrence, 4 larvae )

The only record of Chlorophthalmus larvae
was from station 13.052. Larvae in this sample
ranged from 5.0 to 6.5 mm long. Pigmentation
was limited to a large, single peritoneal pigment
patch — and to a few small melanophores on the
dorsal and ventral margin of the tail soon be-
fore the tip of the notochord. Two larger speci-
mens of Chlorophthalmus were taken in the
micronekton net hauls, a 23.0-mm specimen at
station 14.018 and a 39.5-mm specimen at sta-
tion 14.051. Pigment on both was limited to
the peritoneal patch, and a midline melanophore
over the hypural complex; otherwise both spe-
cimens were milky white, without scales. The
larger specimen had the following fin counts:
D. 11, A. 11, V. 9, P. 17. These are identical
to counts given by Garman (1899) for his spe-
cies, C. mento from the Gulf of Panama, to
which our material probably is referable.

Table 13. — Areal occurrence and relative abundance of larvae of Idiacanthidae on EA

lSTROPAC I.

.1'go
1 1 .000 series

Ddvid S(<irr Jordan
12.000 series

Rockatiay
13.000 series

Alamino!
14.000 series

Total
EASTROPAC 1

Lotitude

No.
positive
hauls

No.
larvae

No.

positive
hauls

No.
lorvoe

No.

positive

hauls

No.
larvae

No.

positive

hauls

No.
larvae

No.

positive

hauls

No. Average no.
larvae per
larvae positive haul

20' N-10° N

18

107

34

379

17

149

69

635

9.2

10° N- 0»

11

19

7

10

14

65

20

56

52

150

2.9

0° -10° S

4

6

2

4

7

44

4

9

17

61

3,6

10° S-20° S

9

15

3

4

8

53

9

42

29

114

3.9

Total

42

147

46

395

44

311

33

107

167

960

5.7

21

FISHERY BULLETIN; VOL. 69, NO. I
90° 80""

Figure 7. — Distribution of larvae of the paralepidids, Macroparalepis macrurus Ege and Sudis atrox Rofen, of
Synodus spp., and of the gempylid Nealotus tripes Johnson on EASTROPAC I. Records of occurrence of larvae
of Macroparalepis macrurus are shown as an open circle, larvae of Sudis atrox as a diamond, larvae of S^m-
odus spp. as a triangle, and larvae of Nealotus tripes as a square; negative hauls are shown as small solid
circles.

13. MYCTOPHIDAE
(472 occurrences, 44,913 larvae)

Myctophids made up 47.2% of the fish larvae
taken on EASTROPAC I. Of the 482 oblique
hauls taken on EASTROPAC I, 472 contained
myctophid larvae. This dominant group oc-
curred almost everywhere. However, as is
shown in Table 14, larger numbers of myctophid
larvae were taken per haul between lat 10° N
and 5° S.

The myctophid fauna is a large one in numbers

of genera and species represented in the eastern
tropical Pacific. This diversity is shown in
Table 15, in which occurrence and abundance
of myctophid larvae are summarized by genus
or species; the number of genera listed is 19.
Even so, larvae of Diogenichthys latematus
made up over half of the total.

The study of larval myctophids is aided by
the diversity of larval morphology found in this
family, and by the fact that the larvae of most
genera have a characteristic form that permits

22

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

identification to genus, even for genera in which
the species composition has not been fully
worked out. This point was stressed in two
recent papers dealing with identification of
myctophid larvae (Pertseva-Ostroumova, 1964;
Moser and Ahlstrom, 1970).

Because of the importance of this group in
the tropical ichthyoplankton, I will discuss its
composition in more detail than for any other
family except the Gonostomatidae.

Moser and Ahlstrom (1970) described devel-
opmental series for 14 species of lanternfishes
with narrow-eyed larvae in the California Cur-
rent. The following species also occur in the
EASTROPAC area: Electrona rissoi, Diogeiv-
ichthys atlantictis, D. latematus, Benthosema
panameiise, Hygopkum atratum, H. reinhardti,
Myctophiim nitidulum, Loweina rara, Gonich-
thys tenuiculus, and Centrobranchus choero-
cephalus.

Table 14. — Areal occurrence and relative abundance of larvae of Myctophidae on EASTROPAC I.

David Starr Jordan

Roekaivay

.^aminos

Total

1 1 .000 series

12.000

series

13.000 series

14.000

series

EASTROPAC 1

Latitude

No.

No.

No.

No.

No.

No.

No.

No.

No.

No.

Average no.

positive

posrtive

positive

positive

positive

larvae per

hauls

larvae

hauls

larvae

hauls

larvae

hauls

larvae

hauls

larvae

positive haul

20° N-15°

N

16 430

20

1,000

5 116

..

..

41

1,546 37.7

15° N-10°

N

14 568

23

1,444

24 2,826

61

4,838 79.3

10° N- 5°

N

14 1,323

14

2,136

29 5,856

15

2,730

72

12,045 167.3

5° N- 0°

14 1,988

15

2,327

14 1,325

27

6,075

70

11,715 167.4

0° - 5°

S

14 1,233

18

3,413

14 1,635

16

1,209

62

7,490 120.8

5° S-10°

S

13 567

15

408

14 994

13

635

55

2,604 473

10° 3-15°

,S

14 563

8

296

15 1,362

25

768

62

2,989 48.2

15° S-20°

S

19 321

8

250

22 1,115

—

—

49

1,686 34.4

Total

118 6,993

121

11,274

137 15,229

96

11,417

472

44,913 95,2

Table 15. — Summary, by genus or species, of occurrences and relative abundance of myctophid larvae in the four

vessel patterns occupied on EASTROPAC I.'

^reo

David Starr Jordan

Rockatcay

.ilar,

inos

Total

11.000

series

12.000

series

13.00C

series

14.000

series

EASTROPAC 1

larvae

No.
positive

No.

No.
positive

No.

No.
positive

No.

No.
positive

No.

No.
positive

No.

hauls

larvae

houls

larvae

hauls

larvae

hauls

larvae

hauls

larvae

Benthoitma panamense

0

0

1

63

5

918

1

46

7

1,027

Centrobranchus spp.

0

0

3

4

0

0

0

0

3

H

Ceratoscopelul towntendi-

complex

46

235

24

140

42

633

5

12

117

1,020

Diaphul spp.

62

490

96

1,363

72

949

21

71

251

2,873

Diogtnichthyi laternatui

69

2,202

89

5,259

92

9,089

89

8,775

339

25,325

DiogenichttiM atlanticus

3

4

6

11

18

75

2

2

29

92

Electrona sp.

5

6

9

34

19

34

0

0

33

74

Gonicktkyi tenuicului

5

8

20

56

39

101

28

67

92

232

Gonichthyi sp.

0

0

0

0

0

3

0

0

3

3

Hygopkum atratum & H

reinhardti

30

177

52

352

37

268

8

90

127

887

Hygophum proximum

67

611

30

215

19

72

0

0

116

898

Lompadena spp.

13

27

10

21

15

71

0

0

38

119

Lampanyctus spp.

99

1,240

96

2,063

107

1,347

74

1,232

376

5,882

Lepidophanes pyriobolul-

complex

7

26

14

109

10

22

3

6

34

163

Lobianchia sp.

2

14

2

3

12

22

0

0

16

39

Loweina rara

18

25

7

11

13

14

4

5

43

56

Myctophum spp.

52

624

48

323

47

160

40

286

187

1,393

Notolynckut valdiviae

40

210

47

290

60

344

11

24

158

868

Notoscopelus resplendent

13

37

21

104

21

73

15

69

70

283

Protomyctophum sp.

3

4

19

37

14

37

0

0

36

78

Symbolophorus evermann

71

535

47

248

58

381

36

318

212

1,482

Tripkoturus spp.

17

33

25

82

54

256

44

135

140

506

Unidentified myctophid

arvoe

39

98

36

65

62

190

26

56

163

409

Disintegrated myctophid

larvae
e

75

387

60

423

64

170

42

223

241

1,203

Total myctophid larva

118

6,993

121

11,274

137

15,229

96

11,417

472

44,913

1 The table summarizes the data presented by individual station in Appendix Table 2.

» Centrobranchus larvae ore included under unidentified myctophid larvae in Appendix Table 2.

23

FISHERY BULLETIN: VOL. 69, NO. I

Benthosema panatnense (Taning) ( 7 occurrences,
1,027 larvae)

The relatively large number of larvae taken
in a fewf hauls probably results from the adults
of this species occurring in more compact ag-
gregations than other myctophids (Alverson,
1961) . All occurrences were within a few hun-
dred miles of the coast, mostly off Mexico and
Costa Rica. Distribution of larvae of B. pana-
tnense in the eastern tropical Pacific was illus-
trated in Moser and Ahlstrom (1970).

Centrobranchus spp. (3 occurrences, 4 larvae)

The larvae assigned to Centrobranchus rep-
resent two kinds; one of these is identical to
the larvae described as C. choerocephalus (Mo-
ser and Ahlstrom, 1970). The other is pos-
sibly C. andrae.

Ceratoscopelus townsendi-complex (117
occurrences, 1,020 larvae)

Until recently, only two species of Ceratosco-
pelus were recognized: C. townseyidi (Eigen-
mann and Eigenmann) and C. maderensis
(Lowe). The larvae of these two species are
distinctively different, especially in pigmenta-
tion. Nafpaktitis and Nafpaktitis (1969) con-
cluded that C. warmingi (Lutken) was distinct
from C. townsendi and was the more wddely
distributed species. They indicated that C.
to^vyisendi probably was restricted in its distri-
bution to the eastern North Pacific. The major
difference between the two species is the pres-
ence on C. townseyidi of a large patch of luminous
tissue along the dorsal rim of the orbit on speci-
mens larger than ca. 21 mm SL; otherwise,
the two species are almost identical in meristic
characters, arrangement of photophores, and
the placement of most luminous patches.

Subsequent to the publication of the paper
by Nafpaktitis and Nafpaktitis (1969), my col-
league, H. G. Moser, and I studied developmen-
tal series of Ceratoscopelus larvae previously
assigned to C. townseyidi. Moser (unpublished)
studied eastern North Pacific material (Cal-
COFI and NORPAC) and material from the
eastern South Pacific obtained on EASTROPAC

I; I had the opportunity to examine a number
of collections of Ceratoscopelus larvae collected
by the Meteor in the Indian Ocean (through
the generosity of W. Nellen of the Institut fiir
Meereskunde, University of Kiel, Germany).
Based on criteria of Nafpaktitis and Nafpaktitis,
adults from both the Indian Ocean and southern
portion of the EASTROPAC area were refer-
able to C. ivarmingl, those from CalCOFI and
NORPAC to C. totunsendi. Larvae from the
three regions were strikingly similar in appear-
ance. Observed differences were mostly in rate
of development, particularly in the sizes at which
fin formation took place and at which photo-
phores developed. Even so, somewhat greater
differences were observed between Ceratosco-
pelus larvae from the Indian Ocean and those
from the EASTROPAC area, than between
larvae from the two eastern Pacific regions. For
the present, I choose to call attention to the
complexity of this problem by referring EAS-
TROPAC material to the C. townsendi-complex.
Distribution of C. townsendi-complex larvae
on EASTROPAC I is illustrated in Figure 8.
Most occurrences were in offshore waters be-
tween lat 5° and 20° S, i.e., in the South Pacific
central water mass. Ceratoscopelus larvae are
known to have a complementary distribution in
the eastern North Pacific. On the NORPAC
Expedition Ceratoscopelus larvae were the dom-
inant myctophid in the North Pacific central
water mass between ca. lat 20° and 40° N. The
occurrences of Ceratoscopelus larvae in the Argo
pattern between lat 17° and 20° N are a frag-
ment of this northern population. The few
occurrences of Ceratoscopelus larvae in waters
of the equatorial current system were small
individuals. A few adults also were collected
in this region, hence tropical waters may not
be a barrier to the interchange of fish between
the populations in the North and South Pacific.

Diaphus spp. (251 occurrences, 2,873 larvae)

Diaphus, the genus of myctophids with the
largest number of species, is represented in
the tropical eastern Pacific by a number of
larval forms whose specific identities have been
worked out only partially.

24

AHLSTROM; FISH LARVAE IN EASTERN TROPICAL PACIFIC

130* 120° MO^

20

Figure 8. — Distribution of larvae of the myctophid, Ceratoscopelus townsendi-complex on EASTROPAC I.
Collections of 1 to 25 larvae are shown as circles with dot in center, collections of 26 or more larvae as large
solid circles; negative hauls are shown as small solid circles.

The genus Diaphics is not a natural assem-
blage, inasmuch as there are two distinctive
larval morphs for the species in the EASTRO-
PAC area. One group has slender-bodied larvae
with persistent ventral midline pigment on the
tail; the adults of this group possess both Vn
and So occular photophores (subgenus Diaphus
of Fraser-Brunner, 1949) . The other and larger
group has stubby-bodied larvae which usually
are but lightly pigmented; in the EASTROPAC
area the larvae of Diaphus pacificus Parr is a
representative example.

Although Diaphus larvae were distributed

over most of the area covered on EASTROPAC
I, they were least common in the inner pattern
occupied by Alaminos (21 occurrences, 71 lar-
vae) and most consistently taken in the inter-
mediate pattern occupied by Jordan (96 oc-
currences, 1,363 larvae) .

Diogenichthys laternatus (Garman) (339
occurrences, 25,325 larvae)

Although this is by far the most abundant
kind of larva taken on EASTROPAC I, it did
not occur in the central water mass of the South

25

FISHERY BULLETIN: VOL. 69, NO. I

Pacific (Fig. 9). This species similarly is ab-
sent from the central water mass of the North
Pacific (Moser and Ahlstrom, 1970). There is
a striking similarity in the distributions of
larvae of D. laternatus and those of Bathylagus
nigrigenys Parr (Fig. 3) in the EASTROPAC
area. D. laternatus is one of the smaller species
of myctophids, measuring only 20.6 to 30.0 mm
as adults; hence its biomass probably is not as
great as its larval abundance would suggest.

Diogenichthys atlanticus ( Taning )
( 29 occurrences, 92 larvae)

In contrast to its cogener, larvae of Diogen-
ichthys atlantictis were taken mostly in the
central water mass of the South Pacific on
EASTROPAC I (Fig. 9). Most of the occur-
rences were to the south of lat 10° S on three ad-
jacent lines (along long 92°, 98°, and 115° W).
Two occurrences at the southern end of the
Alaminos pattern, however, indicate that this

20*

Figure 9. — Distribution of larvae of two species of myctophids of the genus Diogenichthys on EASTROPAC I.
Records of occurrence of larvae of D. atlanticus (Taning) are shown as triangles, records of occurrences of
larvae of D. latematits (Garman) as large circles with dot in center for hauls containing 0 to 100 larvae, and
as large solid circles for hauls containing 101 or more specimens of this species; negative hauls are shown
as small solid circles.

26

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

species is not restricted to the central water
mass but also can occur in the transitional
waters of the Humboldt Current. Larvae of
this species were taken close to the Chilean
coast between lat 20° and 30° S on MARCHILE
VI, the Chilean contribution to EASTROPAC II.
D. atlanticus appears to be a temperate-sub-
tropical species, whereas D. laternatus is a
tropical-subtropical species. The distribution of
larvae of this species in the eastern North Pa-
cific is given in Moser and Ahlstrom (1970, figs.
41 and 42). A larval specimen taken at lat 6°
N along long 119° W shows that this species can
bridge the tropical gap between its areas of
usual occurrence in more temperate waters of
the North and South Pacific.

Electrona sp. ( 33 occurrences, 74 larvae )

Distribution of Electrona larvae on EAS-
TROPAC I was limited to two bands — one cen-
tering on lat 5° N (6 occurrences, 16 larvae)
the other in the central water mass of the South
Pacific, between lat 8° and 20° S (27 occur-
rences, 58 larvae). The Electrona larvae all
resemble E. rissoi, although two kinds may be
present.

Gonichthys tenuiculus ( Garman )
(92 occurrences, 232 larvae)

Larvae of Gonichthys tenuiculus have a sim-
ilar distribution in the eastern tropical Pacific
to those of Diogenichthys laternatus. Larvae of
a different species of Gonichthys (3 occurrences,
3 larvae) were obtained at the southern end of
the Rockaway pattern. Beebe and Vander Pyl
(1944) reported collecting more adults of G.
tenuiculus (re\)orted &s Myctophum coccoi (Coc-
co) ) , than of any other myctophid on the Arc-
turus Expedition to the eastern Pacific in 1925.
Their collections were made on adults aggregat-
ing at the surface. Based on larval evidence, Go-
nichthys tenuiculus is only moderately common.

Hygophum atratum-reinhardti ( 1 27 occurrences,
887 larvae)

Larvae of these two species are similar in ap-
pearance and difficult to distinguish at some

stages of larval development. Larvae of Hygo-
phum atratum (Garman) were distributed over
much of the EASTROPAC pattern; however
some occurrences at the southern end of the
patterns of Rockaway, Jordan, and Argo were
referable to H. reinhardti (Lutken).

Hygophum proximum Becker (116 occurrences,
898 larvae)

Hygophum proximum is a truly oceanic spe-
cies, not occurring at all in the inner pattern
worked by Alaminos, and it was most abundant
in the outer pattern occupied by A7-go (Fig.
10). It occurs in the central water masses of
the North and South Pacific, but also in the
equatorial current system; the largest collection
of larvae (103 specimens) was obtained at the
equator.

Lampadena spp. (38 occurrences, 119 specimens)

Two and possibly three kinds of Lampadena
larvae were obtained on EASTROPAC. A de-
velopmental series definitely has been established
for only one species, Lampadena urophaos Pax-
ton. The relatively few occurrences of Lampa-
dena larvae on EASTROPAC I were mostly in
the southern portion of the three outer vessels
(24 of 38 occurrences) and most of the remain-
der in an offshore band lying between lat 4° and
8° N (9 occurrences).

Lampanyctus spp. (376 occurrences, 5,882 larvae)

Larvae of Lampanyctus were taken in more
collections than those of any other myctophid
genus but were not identified to species. A num-
ber of species of Lampanyctus occur in the
EASTROPAC area, of which L. idostigma Parr,
L. omostigma Gilbert, L. parvicatida (Parr),
and L. steinbecki Bolin are among the more
common. Larval series are being worked out
for these.

Lepidophanes sp. (34 occurrences, 163 larvae)

The species of Lepidophanes that occur in the
EASTROPAC area belong to the Lepidophanes

27

FISHERY BULLETIN: VOL. 69, NO. I
90° 80°

Figure 10. — Distribution of larvae of the myctophid Hygophum proximum (Becker) and of the bothid flatfish
Bothus leopardinus (Giinther) on EASTROPAC I. Records of occurrence of larvae of H. proximum are
shown as open circles with dot in center for hauls containing 1 to 25 larvae, and as large solid circles for hauls
containing 26 or more larvae; records of occurrence of larvae of B. leopardinus are shown as squares; neg-
ative hauls are shown as small solid circles.

pyrsobolus (Alcock) complex. Larvae of Lepi-
dophanes are almost unpigmented, big eyed, and
moderately deep bodied. They have few dis-
tinctive characters and can be confused with
larvae of Diaphus and Ceratoscopelus. The ma-
jority of the records for Lepidophayies were of
large larvae.

Lobianchia sp. (16 occurrences, 39 larvae)

Larvae of Lobianchia were not recognized
until the identification of EASTROPAC larvae

was well underway, hence our records of occur-
rences may be incomplete (some but not all
samples were rechecked subsequently). The
head of Lobianchia larvae is more massive than
in most myctophid larvae. The most diagnostic
feature, however, is the unusual manner in
which the pectoral fins develop: the upper fin
rays in each iiectoral develop sooner than the
remainder of the fin rays and become conspic-
uously elongated (Taning, 1918). Twelve of
the 16 occurrences were in the pattern worked
by Alami^ios and half of these were at adjacent

28

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

stations located between lat 6° and 2° N along
long 92° W.

Louieina rara (Lutken) (43 occurrences, 56
larvae )

The larger larvae of Loweina rara are among
the most elegant of myctophid larvae. Larvae
of this species were rather uncommon in the
EASTROPAC area, although widely distributed.
Larvae were taken most frequently, however, in
the vicinity of the equator, between ca. lat 8° N
and 7° S; 36 of the 43 occurrences were in the
equatorial zone. The largest collection of Lo-
weina larvae was only four specimens, and only
a single specimen was obtained in most collec-
tions (i.e., in 35 of 43). The distribution of
larvae of L. rara on EASTROPAC I is illus-
trated in Moser and Ahlstrom (1970).

Myctophutn spp. ( 187 occurrences, 1,393 larvae)

Myctophiim is one of the more abundant gen-
era represented in the eastern tropical Pacific.
Juvenile and adults of five species were ob-
tained in 1-m plankton hauls and micronekton
net hauls: Myctophum atirolaternatum Gar-
man, M. asperum Richardson, M. hrachygnathos
(Bleeker), M. lychnobium Bolin, and M. nitid-
ulum Garman. Body form and pigmentation of
the five of six kinds of Myctophum larvae taken
in EASTROPAC I are as diverse as has been
observed within a myctophid genus. Larvae of
M. nitiduliini, described by Moser and Ahlstrom
(1970), are broad headed and deep bodied with
eyes on short stalks; larger larvae of this spe-
cies are among the most heavily pigmented
myctophid larvae.

A quite different developmental pattern is dis-
played by larvae of M. asperum and M. hrachyg-
nathos. The larvae of these species are also
deep bodied and big headed, but the eyes are
not borne on stalks. The most characteristic
feature of the development of these larvae is
the early appearance of Dn photophores which
form on larvae between 4.0 to 5.0 mm in length,
soon after the appearance of the Bra photo-
phores. Larvae of M. asperum develop large
characteristic melanophores (Pertseva-Ostrou-

mova, 1964), but larvae of M. hrachygnathos
are only slightly pigmented.

Larvae of M. lychnobium also are but lightly
pigmented; they are much more slender and
elongated than larvae of M. hrachygnathos and
do not develop the Dn photophores early. A
notable feature is the marked length of the tear-
drop (choroid) tissue that develops under the
eyes (as long as in Gonichthys or Centrobranchus
larvae).

The extraordinary larvae of M. aurolatema-
tum were only recently recognized and are not
included in the above counts of Myctophum.

Notolychnus valdiviae (Brauer) (158
occurrences, 868 larvae )

This is probably the smallest species of myc-
tophid, and cei'tainly one of the most widespread
in offshore, oceanic waters. The larvae seldom
occur in large numbers (average number per
positive haul was 5.5 larvae). They were
present in about one-third of the collections
made on EASTROPAC I, although most occur-
rences were farther offshore than 300 miles of
the coast (Fig. 11). Juvenile and adult A'', val-
diviae were frequently taken in the oblique
plankton hauls. Perhaps as many juvenile and
adult specimens of N. valdiviae were obtained
by this means as of all other myctophids com-
bined. Since this species has only a middling
rank with regard to abundance of larvae, the
frequency of capture of adults is probably less
a measure of abundance than of their shallow
depth distribution and poor swimming ability.

Notoscopelus resplendens (Richardson)
(70 occurrences, 283 larvae)

This is the species of Notoscopelus known to
occur in the eastern Pacific. On EASTROPAC,
Notoscopebis larvae were taken more frequently
and in larger numbers in the equatorial zone
between lat 5° N and 5° S (40 occurrences, 209
larvae).

Protomyctophum sp. ( 36 occurrences, 78 larvae )

All occurrences of Protomyctophum larvae,
except one, were between lat 10° N and 5° S.

29

FISHERY BULLETIN: VOL. 69, NO. 1
90° 80°

Figure 11. — Distribution of larvae of the myctophid, Notolychnus valdiviae (Brauer) on EASTROPAC I. Col-
lections of 1 to 25 larvae are shown as circles with dot in center, collections of 26 or more larvae as large solid
circles; negative hauls are shown as small solid circles.

Only one kind of Protomyctophum larva, belong-
ing to the subgenus Hierops, was taken on
EASTROPAC. The specific identity is un-
known, as no juveniles or adults were obtained.
The larva has a single lateral pigment spot per
side over the gut, resembling in this respect the
larva of P. crockeri (Bolin) (Moser and Ahl-
strom, 1970). However, internal pigment de-
velops over the hypural bones of the caudal com-
plex in older larvae — resembling in this respect
the pigmentation of older larvae of P. thompsoni
(Chapman). The tropical form lacks ventral
pigment on the tail posterior to the anus, such

as is developed on larvae of P. thompsoni, and
probably represents an undescribed species.

Symbolophorus evermanni (Gilbert) (212
occurrences, 1,482 larvae)

Only one kind of Symbolophonis larvae ap-
pears to be present in the EASTROPAC survey
area, despite its distribution in different water
masses including the central water mass of the
South Pacific. Fewest occurrences were in the
northern portion of the EASTROPAC pattern,
between lat 10° and 20° N. The number of lar-

30

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

vae per positive haul ranged from 1 to 72 (aver-
age 7.0) ; 15 collections contained 25 or more
larvae, most distributed between lat 7° and 20° S.
Distribution of the larvae of S. eveiinanni on
EASTROPAC I is illustrated in Figure 12.

but larvae of the two species are differently pig-
mented. T. oculeiis occurs in a broad coastal
band between Panama and Chile, having in this
respect a complementary distribution of that of
T. mexicamis off California and Baja California.

Triphoturus spp. ( 140 occurrences, 506 larvae)

Larvae of at least tvvo species of Triphoturus
were taken in the EASTROPAC area. Of par-
ticular interest are larvae of Triphoturus oculeus
(Carman); this species previously was consid-
ered a synonym of T. mexicanus (Gilbert),

14. PARALEPIDIDAE
(290 occurrences, 1,648 larvae)

Larvae of Paralepididae were taken in ap-
proximately 60 % of the stations occupied on
EASTROPAC I. The area of heaviest concen-
trations was in an equatorial band between lat
5° N and 5° S (Table 16). Two species are

Figure 12. — Distribution of larvae of the myctophid, Symbolophorus evermanni (Eigenmann and Eigenmann)
on EASTROPAC I. Collections of 1 to 25 larvae are shown as large circles with dot in center, collections of
26 or more larvae as large solid circles; negative hauls are shown as small solid circles.

31

FISHERY BULLETIN: VOL. 69, NO. 1

Table 16. — Areal occurrence and relative abundance of larvae of Paralepididae on EASTROPAC I.

Argo
11.000 series

David Starr Jordan
12.000 series

Rockaway
13.000 series

Alam
14.000

inoJ
series

Total
EASTROPAC 1

LoJitude

No.
positive
hauls

No.
larvae

No.

positive
hauls

No.
larvae

No.

positive

hauls

No.
larvae

No.

positive

hauls

No.

larvae

No.

positive

hauls

No. Average no.
larvae per
larvae positive haul

20° N-15° N

7

9

15 63

4 19

__

26

91 35

15° N-I0° N

3

6

22 105

14 77

__

39

188 4.8

10° N- 5° N

10

38

10 25

8 39

8

21

36

123 3.4

5° N- 0°

12

83

15 100

11 145

21

219

59

547 9.3

0° - 5° S

8

22

18 217

14 136

11

72

51

447 8.8

5° S-IO° S

8

36

7 17

8 62

2

11

25

126 5.0

10° S-15° S

13

32

6 24

9 20

2

2

30

73 2.6

15° S-20° S

6

16

4 7

14 25

—

—

24

48 2,0

Total

67

242

97 558

82 523

44

325

290

1,648 5.7

separately tabulated in Appendix Table 3:
Mac)-oparalepis macruriis Ege (35 occurrences,
44 larvae), and Siidis atrox Rofen (13 occur-
rences, 15 larvae) . These two species have such
characteristic larvae that they are readily identi-
fiable. The larvae of Macroparale.pis macruriis
were widely distributed in the EASTROPAC
area, except in the inner pattern occupied by
Alaminos (Fig. 7). In contrast, the larvae of
Sudis atrox were confined to the central water
mass of the South Pacific (Fig. 7) . This species
was originally described from the central water
mass of the North Pacific (Rofen, 1963 ; see also
Berry and Perkins, 1966). Preliminary study
of the other paralepidid material indicated that
a number of species were represented, but that
the most common larva was the form illustrated
by Ege (1953, Fig. 27), simply as "Lestidium
spec."

15. EVERMANNELLIDAE
( 27 occurrences, 38 larvae )

The larvae of Evermannellidae in the EAS-
TROPAC area have not yet been worked out in

detail. Three species of Evermannellidae are
known to occur: Coccorella atrata (Alcock),
Evermannella indica Brauer, and a form with
a higher anal fin count than is found in these
two species. The identity of the latter, known
only as yet from larval specimens, remains un-
certain. Although larvae of Evermannellidae
were not common, the occurrences were distrib-
uted over much of the EASTROPAC pattern,
except nearshore.

16. SCOPELARCHIDAE
( 142 occurrences, 329 larvae)

Scopelarchids are widely distributed in the
eastern tropical Pacific, usually occurring in
small numbers, i.e., one to three larvae per haul.
Only 15 ',r of the positive hauls contained larger
numbei's of larvae, i.e. 4 to 20 larvae per haul.
Scopelarchid larvae were most common between
lat 10° and 20" N, as is shown in Table 17.

There are at least five species of scopelarchids
represented by the larvae, and perhaps si.x. I
have not attempted to attach specific names to
most of the kinds because the adult scopelarchids

Table 17. — Areal occurrence and relative abundance of larvae of Scopelarchidae on EASTROPAC I.

Argo
11.000 series

David Sla
12.000

rr Jordan
series

Rockaway
13.000 series

Alaminol
14.000 series

Totol
EASTROPAC 1

Latitude

No.

positive

hauls

No.
larvae

No.

positive

hauls

No.
larvae

No.

positive

houls

No.
lorvae

No. No.
positive
houls lorvae

No.

positive

houls

No.
larvae

Average no.

larvae per

positive haul

20° N-10° N
10° N- 0°
0° -10° S
10° S-20° S

16 38
4 4

11 15
4 7

25
7
9
5

67
12
IS
7

15 84
10 14
5 8
9 14

13 27

4 6

5 8

56
34
29
23

189 3.4
57 1.7
47 1.6
36 1.6

Total

35 64

46

104

39 120

22 41

142

329 2.3

82

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

of the eastern tropical Pacific are as yet inad-
equately known. Most larvae taken between lat
10° and 20° N were those of Scopelarchoides
nicholsi Parr.

17. SCOPELOSAURIDAE
(9 occurrences, 16 larvae)

stations between the coast and the outer line
occupied by Argo. Leptocephali of Hildebrand-
ia were restricted to a broad coastal band,
but leptocephali of Bathyconger and Para-
conger were almost as widespread as those
of Ariosoma. Only one record was obtained of
Gnathopis.

Two kinds of Scopelosaurus larvae were col-
lected in the EASTROPAC area, but neither has
been linked to its adult stages as yet; one of
these occurred in only a single collection. Most
of the specimens of the other form were taken
in an equatorial band, between lat 5° N and 5° S.

20. EEL LEPTOCEPHALI

(87 occurrences, 179 larvae in 1.0-m oblique net

hauls; 58 occurrences, 553 larvae in 5.0-ft

micronekton net hauls )

A total of 10 families of true eels of the order
Anguilliformes, suborder Anguilloidei, is rep-
resented in the EASTROPAC I collections. Eel
leptocephali were decidedly more common in
collections made with the 5-ft micronekton net
than in the 1-m net collections: 9.5 larvae per
positive haul as compared with 2.1 larvae. This
difference probably was due in large part to the
larger volume of water strained in taking micro-
nekton net hauls, but the faster towing speed
of these hauls, ca. 5 knots as compared with 1..5
to 2 knots for 1-m net hauls, also may have con-
tributed. In the discussion of eel families that
follows, I have utilized information on occur-
rence of eel leptocephali from the collections of
both nets.

Congridae

Leptocephali of congrid eels were taken at
more stations, 57, than those of any other fam-
ily, yet no congrid larvae were obtained to
the south of lat 6° S. Most congrid leptoceph-
ali could be identified to genus, of which five
were represented; some larvae, however, could
not be identified below the family level. Lep-
tocephali of Ariosovia were widely distributed
between lat 20° N and 3° S, occurring at 28

Derichthyidae

The only definite record is a metamorphosing
specimen obtained at station 11.167.

Moringuidae

Leptocephali of Neoconger were taken at five
coastal stations between lat 8° N and 1° S.

Muraenesocidae

Leptocephali were taken at four stations in
the inner pattern occupied by the Alaminos, all
within 3° of the equator.

Muraenidae

Muraenid leptocephali were taken at 17 sta-
tions; two were on the line of stations occupied
off Acapulco, Mexico, and the remainder in the
broad con-idor between Puntarenas, the Galap-
agos Islands, and the coast of Ecuador.

Nemichthyidae

Two genera of nemichthyid larvae were rep-
resented in the EASTROPAC area, Nemichthys
and Borodiniila. A specimen of Nemichthys,
310 mm long, was obtained at station 14.188.
Leptocephali of this family were taken at 24
stations scattered throughout the EASTROPAC
area, including the South Pacific central water
mass.

Nettastomidae

Taken at 17 stations in the inner half of the
EASTROPAC pattern between lat 9° N and 2° S;
two kinds of nettastomid larvae were obtained,

33

FISHERY BULLETIN: \0L. 69. NO. I

one of which was represented by a single speci-
men.

Ophichthidae

The 31 occurrences of ophichthid eels were
distributed in a broad coastal band between
Manzanillo, Mexico, and northern Peru (lat
7° S).

Serrivomeridae

Leptocephali of this family were taken at 33
stations, of which 21 were in the outer pattern
occupied by Argo. Occurrences were grouped
into two broad bands — one centered on lat 5° N,
the other located between lat 7° and 20° S in the
South Pacific central water mass.

Xenocongridae

The leptocephalus of Chlopsis was obtained
at 22 stations, most located between Panama Bay
and the Galapagos Islands.

21. MELAMPHAIDAE
(298 occurrences, 857 larvae)

Melamphaid fishes are the most important
family of berycoid fishes in the mesopelagic
zone. Four of the five recognized genera occur
in the EASTROPAC area: Melamphaes, Sco-
pelogadn-s, Scopelobryx, and Poromitra. Accord-
ing to Ebeling ( 1962) five species of Melamphaes
are common in the eastern tropical Pacific, two

additional species were collected within the
EASTROPAC area, and four other species were
collected on the fringes of the area. Only one
kind of Scopelogadus, S. mizolepis bispinosus
(Gilbert), is known from the eastern Pacific
(Ebeling and Weed, 1963) . The remaining two
genera, Scopeloberyx and Poromitra, await re-
vision; the species composition of these genera
in the EASTROPAC area is inadequately known.
Although melamphaid larvae can be identified
to the generic level with some assurance, few
developmental series have been worked out at
the species level.

Larvae of Melamphaidae were widely distrib-
uted in the EASTROPAC area, occurring in
62 ''r of the collections. Although negative
hauls were fewest between the equator and lat
15° N, the average number of larvae per pos-
itive haul was rather similar in all areas (Table
18).

23. BREGMACEROTIDAE
(194 occurrences, 1,805 larvae)

Larvae of the gadoid family, Bregmacerotidae,
ranked sixth in abundance, contributing 1.9 %
of the fish larvae of EASTROPAC L The only
genus, Bregmaceros, is widely distributed in
pelagic waters of the tropical and subtropical
regions of all oceans. D'Ancona and Cavinato
(1965) recognized seven species in a worldwide
treatment of the genus. These authors stressed
the difficulties in species identification.

A preliminary study of EASTROPAC col-
lections of Bregmaceros laiA'ae, supplemented
by collections of juveniles and adults obtained

Table 18,

—A real

occurrence and relative abundance of larvae of Melamphaidae on EASTROPAC I.

n.OOO series

Daiid Starr Jordan
12.000 series

Rockaway
13.000 series

Alaminoi
14.000 series

Totol
EASTROPAC 1

Latitude

No.

positive

hauls

No.
larvae

No.

positive

hauls

No.
larvae

No.

positive

hauls

No.

larvae

No.

positive
houls

No.

lorvoe

No.

positive
hauls

No.
lorvoe

Averoge no.

lorvoe per

positive haul

20°N-15"N

7

17

IS

41

3

5

25

63

2.5

15° N-tO° N

13

36

19

41

IS

48

50

125

25

10° N- 5° N

14

59

11

26

24

104

9

24

58

213

37

5° N- 0°

7

12

11

19

11

36

24

100

53

167

3.2

0° - S° S

8

12

9

17

11

56

10

41

38

126

3.3

5° S-10' S

9

18

8

17

9

27

10

21

36

83

2.3

10° S.IS° S

6

8

2

6

11

29

6

14

25

57

2 3

\S° S-20° S

2

3

2

4

9

16

—

—

13

23

1.7

Total

66

165

77

171

96

321

59

200

298

857

2.9

34

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

in micronekton hauls, has shown the presence
of five kinds. Larvae of B. bathymaMer Jordan
and Bollman had the most limited distribution,
being a coastal species, but were taken in the
largest numbers. Two species occurred in the
central water mass of the South Pacific (B.
japonicus Tanaka, and perhaps B. macclellandi
Thomp.son). Another species occurred in the
equatorial current system, and a fifth species
was widely distributed between lat 7° and 20°
N. One or both of the latter may be unde-
scribed.

26. EXOCOETIDAE
(78 occurrences, 189 larvae)

The species composition of flyingfish larvae
has not been worked out in detail as yet. Only
larvae of the most common species, Oxijpor-
hamphus micropterus (Cuvier and Valencien-
nes) (.51 occurrences, 121 larvae) have been sep-
arately tabulated (Appendix Table 3). Larvae
of Oxyporhamphus were taken at a number of
stations in a coastal band off Mexico and central
America. Offshore occurrences were limited
to an equatorial band between lat 5° S and 7° N.
Only one occurrence of larvae of this species
was obtained to the south of lat 5° S. Exo-
coetid larvae undoubtedly are undersampled in
oblique plankton hauls, both because of their
shallow depth distribution and their marked
swimming ability. Much more material of exo-
coetids — eggs, larvae, and juveniles — are pres-
ent in surface plankton hauls; only a few of
these have been sorted as yet from EASTRO-
PAC L

28. GEMPYLIDAE-TRICHIURIDAE
(103 occurrences, 231 larvae)

The larvae of these two families are grouped
together for reasons discussed below. Larvae of
four species of gempylids-trichiurids appear to
be widely distributed in the eastern Pacific:
these are Nealotus tripes Johnson (42 occur-
rences, 82 larvae. Fig. 7), Gempylus serpens
Cuvier and Valenciennes (40 occurrences, 57
larvae, Fig. 13), Diplospiniis rmdtistriatus Maul
(26 occurrences, 62 larvae, Fig. 14), and Lepid-
opus sp. (7 occurrences, 25 larvae, Fig. 14).
Records of the occurrence of these in EASTRO-
PAC hauls also are given in Appendix Table 5,
and summarized in Table 19. One or two speci-
mens each were taken of larvae of two or three
additional species of gempylids-trichiurids.

Late larval stages already have been described
for three of the above species (Voss, 1954;
Strasburg, 1964), but early developmental
stages have not been described, except for a
species of Lepidopus. We plan to describe the
early stage larvae of all the above species.

The larval series of these four species raise
questions about the distribution of genera be-
tween these two families, and perhaps, about
the need for two families. Larvae of Diplospi-
niis nmltistriatus are quite similar to those of
Gempylus serpens. This similarity is marked
enough to have led Voss (1954) to describe the
larvae of Diplospimis as those of Gempylus (i.e.
her Gempylus A). Her Gempulus B larvae are
those of Gempylus serpens.

Table 19. — Summary of occurrences and relative abundance of species of Gempylidae-Trichiuridae in the four

vessel patterns occupied on EASTROPAC I.

.*r£0
1 1 .000 series

David Starr Jordan
12.000 series

Rockaway
13.000 series

A lam
14,000

inos
series

Total
EASTROPAC 1

Species

No.

positivs

hauls

No.
larvae

No.

positiva
hauls

No.

larvae

No.

positiva

hauls

No.
larvae

No.

positiva

hauls

No.
larvae

No.

positiva

hauls

No.
larvae

Nfalotuj tripes
Gempylus serpens
Diplospinus multistriatus
Lepidopus sp. (xantusi)
Other

6
8
5

0
0

6
10
10
0
0

2

15
0
0
2

7
19
0
0
2

12
11
9
1
2

34
18
31
17
3

22
6

12
6
0

35

10

21

8

0

42 82
40 57
26 62
7 25
4 5

Total

19

26

13

28

31

103

35

74

103 231

35

FISHERY BULLETIN: VOL. 69, NO. 1

100°

Figure 13. — Distribution of larvae of the gempylid, Genipylus serpens Cuvier and Valenciennes, and of the
cynoglossid flatfish, Symphunis spp., on EASTROPAC I. Records of occurrence of larvae of G. serpens are
shown as large circles with dot in center, Symphnriis spp. as open squares for hauls containing 1 to 25 larvae
and solid squares for hauls with 26 or more larvae; negative hauls are shown as small solid circles.

29- SCOMBRIDAE
( 185 occurrences, 1,919 larvae)

Larvae of scombrid fishes ranked fifth in
abundance, and made up over 2 % of the larvae.
Larvae of the bullet mackerel, Aiixis spp., (161
occurrences, 1,563 larvae) were by far the most
abundant and widely distributed. Larvae of
skipjack tuna, Katmivotuis pelamis (Linnaeus)
(17 occurrences, 214 larvae) were taken mostly
in the offshore southern portion of the EAS-
TROPAC area. Other scombrid larvae included
yellowfin tuna, Thnnnus albacares (Bonnaterre)

(19 occurrences, 40 larvae) ; bigeye tuna, Thun-
nus obes7is Lowe (1 occurrence, 1 larva); black
skipjack, Euthynnus lineatus Kishinouye (2 oc-
currences, 77 larvae); regular Scomber sp. (2
occurrences, 7 larvae) ; Spanish mackerel,
ScomberomonLS sp. (2 occurrences, 3 larvae);
and the wahoo, Acanthocybium solandri (Cu-
vier) (1 occurrence, 1 larva). The tuna larvae
have been turned over to W. Klawe of the Inter-
American Tropical Tuna Commission for de-
tailed study. He kindly has given me permission
to include data on occurrence and abundance of
larvae of skipjack and bullet mackerel in Ap-

36

AIILSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

130* 120° I'O'

20°

120'

Figure 14. — Distribution of larvae of the apogonid, Howella pammelas (Heller and Snodgrass), and of the
trichiurids, Diplospinus multistriatus Maul and Lepidopus sp. Records of occurrence of larvae of H. pammelas
are shown as large circles with dot in center for hauls containing 1 to 10 larvae and large solid circles for hauls
containing U or more larvae; records of occurrence of larvae of D. midtistriatus are shown as squares, Le-
pidopus sp. are triangles; negative hauls are shown as small solid circles.

pendix Table 3. Charts showing distribution
and relative abundance of larvae of Auxis sp.
and of Katsuwonus pelamis on EASTROPAC
cruises will be included in the EASTROPAC
Atlas.

larvae of marlin and sailfish in EASTROPAC I
collections was unanticipated, inasmuch as adult
billfish are an important part of the Japanese
longline catches from the tropical eastern Pa-
cific (Kume and Schaefer, 1966).

30. ISTIOPHORIDAE
( 2 occurrences, 2 larvae )

The striking larvae of istiophorids are readily
identified to family. The marked paucity of

32. APOGONIDAE
(61 occurrences, 204 larvae)

Most species of apogonids are coastal, shal-
low-water forms. A few larvae of these were

37

FISHERY BULLETIN: VOL. 69, NO. !

taken on EASTROPAC I. However, the ma-
jority of apogonid larvae were those of Howella
pammelas (Heller and Snodgrass), a pelagic
species that occurred most commonly in the off-
shore pattern occupied by Argo (Fig. 14). An
excellent developmental series has been ob-
tained of this species.

36. CARANGIDAE
(31 occurrences, 183 larvae)

Although a number of kinds of carangid
larvae were obtained on EASTROPAC I only
larvae of the pilotfish, Naucrates ductor (L.),
are separately tabulated (Appendix Table 3).
Most carangid larvae were taken at stations
adjacent to the coast or in the vicinity of off-
shore islands or banks, and over 50 % of the
carangid larvae were obtained at two stations
(13.019-70 larvae, 14.016-34 larvae). In these
larger collections, the most common carangid
larvae were Chloroscomhrus orqueta Jordan and
Gilbert and Selene brevoorti (Gill). Several
times as many young carangids were taken in
one haul of the 5-ft micronekton net as in all
plankton samples: 384 specimens at station
14.014. Species composition was as follows:
Naucrates ductor, 288 specimens, 13.0 to 27.5
mm ; Elagatls bipinniilattis Quoy and Gaimard,
71 specimens, 18.5 to 42.0 mm; and Caranx
cabaUu3 Giinther, 25 specimens, 12.0 to
25.0 mm.

40. CORYPHAENIDAE
(86 occurrences, 118 larvae)

Larvae of the dolphin, Coryphaena spp., were
widely distributed throughout the EASTROPAC

area, but occurred in small numbers, usually
one or two specimens per positive haul (average
1.4). The occurrence and abundance of Cory-
phaena larvae in various parts of the EASTRO-
PAC area are summarized in Table 20. The
majority of specimens obtained were early-
stage larvae; no attempt was made to distin-
guish between the two species of Coryphaena.
Charts showing distribution of Coryphaena
larvae on EASTROPAC cruises will be included
in the EASTROPAC Atlas.

44. NOMEIDAE
(178 occurrences, 961 specimens)

The nomeids are an important constituent
of the epipelagic fauna of the open ocean. Two
genera were represented in the EASTROPAC
collections, Psenes and Cubiceps. Larvae of
Cubiceps were the more common, but more kinds
of Psenes larvae were obtained. Altogether,
eight different kinds of nomeid larvae have been
observed, which differ in meristics, pigmenta-
tion, and body shape. In several developmental
series of larvae of the genus Psenes the pelvic
fins developed early, and became conspicuously
long and pigmented on older larvae. The larger
collections of nomeid larvae were obtained be-
tween lat 10° N and 5° S (Fig. 15). Only a
few collections were obtained to the south of
lat 7° S in the patterns occupied by the Argo,
Jordan, and Rockaway, i.e. in the central water
mass of the South Pacific. Areal occurrences
and relative abundance of nomeid larvae on
EASTROPAC I are summarized in Table
21.

Table 20

— Areal occurrence and re

lative abundance

of larvae of Coryphaena spp. on EASTROPAC I.

Argo
11.000 series

David Starr Jordan
12.000 series

Rockaway
13.000 series

.llaminos
14.000 series

Total
EASTROPAC 1

Lotitudo

No. No.
positive
hauls larvoe

No.

posiTivo
hauls

No.
lorvoe

No.

positive

hauls

No.
lorvo©

No.

positive

houts

No.
lorvoe

No.
positive
hauls

No.
lorvoe

Average no.

larvae per

positive haul

20° N-10° N

3

4

7

9

6

6

__

16

19

1.2

10° N- 0°

14

17

9

17

6

6

9

13

38

53

1.4

0° -10' S

5

6

6

9

4

10

5

7

20

32

1.6

10° S-20° S

2

2

1

1

3

3

6

8

12

14

1.2

Totol

24

29

23

36

19

2J

20

28

86

118

1.4

38

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC
130° 120° lie

100°

80°

Figure 15. — Distribution of larvae of the family Nomeidae on EASTROPAC I. Collections of 1 to 25 larvae
are showTi as large circles with dot in center, of 26 or more larvae as large solid circles; negative hauls are
shown as small solid circles.

Table 21. — Areal occurrence and relative abundance of larvae of Nomeidae on EASTROPAC I.

^rgo

David Starr Jordan

Rock away

jilarttinoi

Total

1 1 .000 series

12.000

series

13.000 series

14.000

series

EASTROPAC 1

Latitude

No.

No.

No.

No.

No.

No.

No.

No.

No.

No.

Average no.

positive

positive

positive

positive

positive

larvae per

hauls

larvae

hauls

larvae

hauls

larvae

hauls

larvae

hauls

larvae

positive haul

20° N-I5°

N

0 0

11

39

3 7

14

46 3.3

15° N-10°

N

5 12

11

24

10 26

26

62 2.4

10° N- 5°

N

12 81

9

87

17 87

7

21

45

276 6.1

5° N- 0°

11 46

9

130

9 76

9

39

38

291 7.7

0° - 5°

S

8 26

8

60

6 78

8

30

30

194 6.5

5° S-10°

S

2 3

4

6

5 16

7

44

18

69 3.8

10* S-15°

S

0 0

0

0

1 1

5

12

6

13 2.2

15° S-20°

S

I 10

0

0

0 0

—

—

1

10 10.0

Total

39 178

52

346

51 291

36

146

178

961 5.4

39

FISHERY BULLETIN: VOL. 69, NO. 1

51. TETRAGONURIDAE
( 6 occurrences, 7 specimens)

Only a few specimens of Tetragonurus larvae
were obtained in EASTROPAC I collections.
Larvae of Tetragonurus have been taken rather
commonly in the California Current region and
were an important constituent in NORPAC col-
lections. These interesting oceanic fishes were
revised by Grey (1955), who recognized three
species. Two of these were present in the
EASTROPAC area: T. atlayiticiis Lowe and
T. cuvierl Risso. Late-stage larvae of the two
species can be separated by differences in their
meristics, and also by differences in pigmen-
tation and body form; larvae of T. atlayiticus
are more heavily and uniformly pigmented and
are deeper bodied than larvae of T. cuvieri
(Grey, 1955).

PLEURONECTIFORMES

(79 occurrences, 503 larvae)

Larvae of flatfishes (Pleuronectiformes) in
EASTROPAC collections belonged only to the
families Bothidae and Cynoglossidae. Informa-
tion concerning the kinds and numbers of flat-
fish larvae taken at each of 79 EASTROPAC I
stations is contained in Appendix Table 6; this
information is summarized in Table 22.

Flatfish larvae were taken in a broad coastal
band, several hundred miles wide, between Man-
zanillo, Mexico, and northern Peru. The occur-

rences of some kinds of flatfish larvae and ju-
veniles at considerable distances from shore have
been commented upon by a number of workers.
Kyle (1913) obtained larvae of Bothus from
across the North Atlantic and larvae of Syacium
at considerable distances from shore. Bruun
(1937a, 1937b) described bathyj^elagic occur-
rences of the bothid flatfish, Chascanopsetta and
Monolene, the latter from off Panama, and of
the pleuronectid flatfish, Poecilopsetta. Ahl-
strom (1965) illustrated the widespread offshore
distribution of larvae of Citharichthys spp. in
the California Current region.

54. BOTHIDAE
( 56 occurrences, 199 larvae )

Several kinds of bothid flatfish larvae were
taken in 20 or more collections, including larvae
of Bothus leopardinus (Giinther) ,Syacium ovale,
and Citharichthys-Etropus. Some interesting
forms taken less frequently included larvae of
Cyclopsetta sp., Engyophrys sa7icti-laurentii
Jordan and Bollman, and of Monolene. A short
section will be devoted to each of the above.

Bothus leopardinus ( Gunther ) ( 28 occurrences,
50 larvae)

Although Norman (1934) lists three species
of Bothus as occurring in the eastern tropical
Pacific — Bothus mancus (Broussonet), B. leop-

Table 22. — Frequency of occurrence and relative abundance of the principal kinds of flatfish larvae, Pleuronecti-
formes, on EASTROPAC I, summarized by vessel pattern.

AriO
1 1 .000 series

David Starr Jordan
12.000 series

Rock
13.000

away
series

Alam'r.ut
14 000 series

Totol
EASTROPAC 1

Flatfish larvae

No.

positive

hauls

No.
larvae

No.

positive

hauls

No.
larvae

No.

positive

houls

No.
larvae

No.

positive

hauls

No.
lorvoe

No.

positive

hauls

No.
arvoe

BOTHIDAE
Bothus leopardinus
Citkarickthyt-Etropul
Cyclopjetta sp.
Engyophrys sancti-laurentii
Syacium ovale
Other Bothidae

0
0
0
0
0
0

0
0
0
0
0
0

1

2
0
0
2
0

4
2
0
0
8
0

15
6
2
2

13

1

32
8
2
3

60

12

18

1

6
9
1

14

40

2

6

16

1

28
26
3
8
24
2

50

50

4

9

84

2

Total Bothidae

0

0

3

14

24

106

29

79

56

199

CYNOGLOSSIDAE
Symphurus spp.

0

0

S

17

21

102

37

185

63

304

Totol Pieuronectiformes

0

0

6

31

30

208

43

264

79

503

40

AHLSTROM: FISH LAR\AE IN EASTERN TROPICAL PACIFIC

pardlnus (Giinther), and B. constellatus (Jor-
dan) — he notes that the latter is very doubtfully
distinct from B. leopardinns. Based on larval
material, there appears to be only one common,
widely distributed species in the eastern Pacific
(Fig. 10), which is referred to B. leopardimis.
It lacks pigmentation, except for a dorsal and
ventral finfold spot near the end of the noto-
chord. This finfold pigment has been observed
on a number of species of Bothus, hence may
be a generic character. Bothus larvae are read-
ily separable from other bothid flatfish larvae
in the EASTROPAC area by a number of char-
acteristics. Young-stage larvae possess a single
elongated anterior dorsal ray, which becomes in-
conspicuous in older larvae. Older larvae are
very deep bodied, usually lack pigmentation and
lack head spination. The pelvic fin base on the
left side originates mostly anterior to the cleith-
rum, not posterior as in Syacium, Engyophrys,
Cyclopsetta, or Citharichthys, and the fin on
the ventral midline is much broader based than
in these genera. Almost 100 specimens of
Bothtis larvae from the tropical eastern Pacific
have been cleared and stained (based in part
on EASTROPAC material, in part on previous
expeditions). The modal number of vertebrae
was 10 -I- 28 = 38.

Several specimens of flatfish larvae were taken
on EASTROPAC I, and on previous expeditions,
that had an exceptionally heavy, elongated,
single anterior dorsal ray, such as have been
described for several genera of bothid flatfish
of the subfamily Bothinae. However, the pelvic
fins formed behind the cleithrum and the fin
on the ventral margin was not much wider
based than its recessed partner. These intrigu-
ing larvae appear to be those of Monolene.
Two difl'erent kinds have been obtained from the
eastern tropical Pacific, one form has 10 + 35
vertebrae, the other has 10 +28 vertebrae. The
latter may be the larva of Monolene asaedai
(Perkins, 1963).

genera. Larvae of both genera develop marked
opercular spination as well as a sphenotic spine
on either side of the head. Cyclopsetta larvae
develop 8 to 11 elongated anterior dorsal rays,
rather than 5 to 8 as in Syacium. Cyclopsetta
larvae also attain a larger size before transfor-
mation; larval specimens as large as 32 mm
have been observed in the EASTROPAC area.
In late-stage larvae of Cyclopsetta the anterior
group of dorsal rays is quite elongated, but a
more striking feature is the marked develop-
ment of three rays of the left pelvic fin which
may extend almost to the base of the caudal fin.
The Cyclopsetta larvae have a larger number
of vertebrae — usually 10 + 29, as compared
to 10 + 25 for larvae of Syacium ovale (Giin-
ther) . Three species of Cyclopsetta have been
described from the tropical eastern Pacific —
C. quema (Jordan and Bollman), C. panamensis
(Steindachner), and C. maculifera (Carman),
but only C. querna has been collected with any
frequency as juveniles and adults. The usual
count of vertebrae in C. quema and C. pana-
mensis is 10 + 29; the vertebral count of C.
maculifera is not known.

Engyrophrys sancti-laurentii Jordan and Bollman
( 8 occurrences, 9 larvae )

Larvae of Engyophrys are about as deep
bodied as those of Bothus. They possess heavy
serrations on the ventral edge of the body both
fore and aft of the cleithrum; three small spines
also develop on the otic region of the head. The
pelvic fins develop immediately posterior to the
cleithrum and anterior to the posterior group
of ventral serrations. A cleared and stained
specimen, 18 mm long, from station 13.040 had
10 + 31 vertebrae, 86 dorsal rays, 71 anal rays,
and 17 caudal rays.

Syacium ovale (Giinther) ( 24 occurrences,
84 larvae)

Cyclopsetta sp. (3 occurrences, 4 specimens)

Larvae of Cyclopsetta are more closely re-
lated to those of Syacium than to other bothid

A larval stage of Syacium was first illustrated
by Kyle (1913) ss"Ancylopsettasx>." Syacium
has a distinctive larva with heavy opercular
spination, a sphenotic spine on either side of

41

FISHERY BULLETIN: VOL. 69, NO. I

the head, and 5 to 8 elongated anterior dorsal
rays. Larvae of the closely related genus, Cy-
clopsetta, also develop opercular and head spina-
tion. The opercular spination Is more pro-
nounced in Syachim — particularly an antlerlike
spine that develops on the posterior border of
the preoperculum. The three anterior rays of
the left pelvic fin become only moderately elon-
gated in Syacium larvae; the rays are of about
equal length, firmly joined together by a mem-
brane, and pigmented distally. The full com-
plement of dorsal and anal fin rays usually are
laid down before the larvae attain a standard
length of 10 mm; the largest specimens studied,
ca. 20 mm long, were undergoing metamor-
phosis.

Citharichthys-Etropus (26 occurrences, 50 larvae)

Before discussing problems in identification
of Citharichthys-Etropus larvae from the EAS-
TROPAC area, some background information
will be given on Citharichthys larvae in the Cal-
COFI region. Illustrations of larvae of three spe-
cies of Citharichthys were given in Ahlstrom
(1965). Two species, Citharichthys sordidus
(Girard) and C. xanthostigma Gilbert, develop
2 elongated dorsal rays and also 2 elongated vent-
ral rays on larvae larger than about 5 mm ; the
other species never develops such rays. Another
species that occurs off central and southern Baja
California, C. fragilis Gilbert, also develops 2
elongated rays on the dorsal and ventral fins.

Two species of Citharichthys, C. gilberti
Jenkins and Evermann, and C. platophrys Gil-
bert, and the widely distributed Etropus cros-
sotus Jordan and Gilbert are known to occur in
the EASTROPAC area. Three kinds of larvae
were taken in EASTROPAC collections refer-
able to Citharichthys or Etropus. The most
common kind developed 3 elongated dorsal rays,
a less common form developed 2 elongated dorsal
rays, and some specimens lacked elongated rays.
The form with 3 elongated dorsal rays is almost
certainly referable to Citharichthys. Larvae of
a common Atlantic species, C. arctifrons Goode,
develop 3 elongated dorsal rays, confirming the
presence of this combination in Citharichthys

larvae. A cleared and stained specimen from
station 13.040 with 3 elongated dorsal rays pos-
sessed 10 + 25 vertebrae, 78 dorsal rays, and
59 anal rays. The meristics of the dorsal and
anal fins could fit either C. platophrys or C. gil-
berti. Yet so little is known of C. platophrys
that I would hesitate to refer the common
Citharichthys larvae in EASTROPAC material
to this species. A similar problem attends
larvae of the form that lacks elongated dorsal
rays. Two specimens, 11.5 and 12.0 mm, from
station 14.014 each had 88 dorsal and 67 anal
rays; vertebrae counts were 10 + 23 and 10
+ 24. These counts best fit E. crossotus, except
that the vertebral counts are low. No material
of the form with 2 dorsal rays (undoubtedly a
Citharichthys) has been cleared and stained for
precise meristics. A definite identification has
yet to be made on all three kinds of larvae.

55. CYNOGLOSSIDAE
(63 occurrences, 304 larvae)

Only one cynoglossid genus, Symphurus, oc-
curs in the eastern Pacific. Five or more kinds
of Symphurus larvae were obtained in EAS-
TROPAC collections; these were obtained in
more collections than larvae of bothid flatfishes
(63 as compared with 56) , and made up a larger
percentage of the total flatfish larvae (ca. 60 '^,'r ) .
A moderate number of recently transformed
specimens of Symphurus were obtained in
EASTROPAC collections; in contrast, all spe-
cimens of bothid flatfish were pretransformation
larvae. The distribution of Symphurus larvae
in EASTROPAC I is shown in Figure 13.

ACKNOWLEDGMENTS

I am indebted to a number of persons for as-
sistance during the preparation of this manu-
script. Kenneth Raymond prepared the distri-
bution charts. Amelia Gomes helped in many
facets of the work including the preparation of
cleared and stained specimens of flatfishes and
other groups. H. Geoff"rey Moser has worked
closely in studies of larvae of Myctophidae and
Gonostomatidae. W. L. Klawe has been help-

42

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

ful in many ways; he graciously has permitted
me to include station information on occurrence
and numbers of larvae of Auxis sp. and skip-
jack tuna. I wish particularly to thank David
Kramer and H. Geoffrey Moser for reviewing
the manuscript.

LITERATURE CITED

AHLSTROM, Elbert H.

1953. Pilchard eggs and larvae and other fish
larvae, Pacific Coast - 1951. U.S. Fish Wildl.
Serv., Spec. Sci. Rep. Fish. 102. 55 p.
1959. Vertical distribution of pelagic fish eggs and
larvae off California and Baja California. U.S.
Fish Wildl. Serv., Fish. Bull. 60: 107-146.

1965. Kinds and abundance of fishes in the Cal-
ifornia Current region based on egg and larval
surveys. Calif. Coop. Oceanic Fish. Invest. Rep.
10: 31-52.

1969. Mesopelagic and bathypelagic fishes in the
California Current region. Calif. Coop. Oceanic
Fish. Invest. Rep. 13: 39^4.
AHLSTROM, Elbert H., and Robert C. Counts.

1958. Development and distribution of Vinciguerria
lucetia and related species in the eastern Pacific.
U.S. Fish Wildl. Serv., Fish. Bull. 58: 363-416.
AHLSTROM, Elbert H., and H. Geoffrey Moser.

1969. A new gonostomatid fish from the tropical
eastern Pacific. Copeia 1969(3): 493-500.
Alverson, Franklin G.

1961. Daylight surface occurrence of myctophid
fishes off the coast of Central America. Pac.
Sci. 15(3): 483.
Beebe, William, and Mary Vander Pyl.

1944. Eastern Pacific expeditions of the New York
Zoological Society. XXXIII. Pacific Myctophi-
dae. (Fishes.) "Zoologica (New York) 29(2):
59-95.
Berry, Frederick H., and Herbert C. Perkins.

1966. Survey of pelagic fishes of the California
Current area. U.S. Fish Wildl. Serv., Fish. Bull.
65(3) : 625-682.

Bruun, Anton Fr.

1937a. Monolene danae, a new flatfish from Pan-
ama, caught bathypelagically. Ann. Mag. Natur.
Hist, 10th Ser. 19(110): 311-312.

1937b. Chascanopsetta in the Atlantic; a bathy-
pelagic occurrence of a flatfish, with remarks on
distribution and development of certain other
forms. Vidensk. Medd. Dansk Naturhist. Foren.
101: 125-136.
Bussing, William A.

1965. Studies of the midwater fishes of the Peru-
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arctic Res. Ser. 6. Nat. Acad. Sci. Nat. Res. Counc.
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d'Ancona, Umberto, and Geminiano Cavinato

1965. The fishes of the family Bregmacerotidae.
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Ebeling, Alfred W.

1962. Melamphaidae I. Systematics and zoogeogra-
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Melamphaes Glinther. Dana Rep. Carlsberg
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Ebeling, Alfred W., and Walter H. Weed III.

1963. Melamphaidae III. Systematics and distri-
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Ege, Vilh.

1953. Paralepididae I {Paralepis and Lestidium) .
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Fraser-Brunner, a.

1949. A classification of the fishes of the family
Myctophidae. Proc. Zool. Soc. London 118(4) :
1019-1106.

Garman, S.

1899. Reports on an exploration off the west coasts
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the Galapagos Islands, in charge of Alexander
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"Albatross," during 1891, Lieut. Commander Z.
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fishes. Mem. Mus. Comp. Zool Harvard Coll. 24,
431 p.

Gibbs, Robert H., Jr.

1964. Family Idiacanthidae. In Fishes of the
western North Atlantic, p. 512-522. Mem. Sears
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1969. Taxonomy, sexual dimorphism, vertical dis-
tribution, and evolutionary zoogeography of the
bathypelagic fish genus Stomias (Stomiatidae).
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Grey, Marion.

1955. The fishes of the genus Tetragonurus Risso.
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1960. A preliminary review of the family Gonos-
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1961. Fishes killed by the 1950 eruption of Mauna
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KuME, SusuMU, and Milner B. Schaefer.

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43

FISHERY BULLETIN: VOL. 69. NO. 1

Kyle, H. M.

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MosEH, H. Geoffrey, and Elbert H. Ahlstrom.

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Nafpaktitis, Basil G., and Mary Nafpaktitis.

1969. Lanternfishes (family Myctophidae) col-
lected during cruises 3 and 6 of the R/V Anton
Bruun in the Indian Ocean. Bull. Los Angeles
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Norman, J. R.

1934. A systematic monograph of the flatfishes
(Heterosomata). Vol. 1, Psettodidae, Bothidae,
Pleuronectidae. British Museum (Natural His-
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Perkins, Herbert C.

1963. Redescription and second known record of
the bothid fish, Monolene asaedai Clark. Copeia
1963(2) : 292-295.

Pertseva-Ostroumova, T. A.

1964. Come morphological characteristics of mycto-
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(Transl., 1966, In T. S. Rass (editor). Fishes of

the Pacific and Indian Oceans, biology and distri-
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Federal Scientific and Technical Information,
Springfield, Va., as 65-50120.)
Rofen, Robert R.

1963. Diagnoses of new genera and species of
alepisauroid fishes of the family Paralepididae.
Aquatica 2, 7 p.

Ryther, John H.

1969. Photosynthesis and fish production in the
sea. Science 166(3901): 72-76.
Strasburg, Donald W.

1964. Postlarval scombroid fishes of the genera
Acanthocybium, Nealotus, and Diplospinus from
the central Pacific Ocean. Pac. Sci. 18(2) : 174-
185.

Taning, a. Vedel.

1918. Mediterranean Scopelidae (Saurus, Aulopus,

Chlorophthalmus and Myctophiim) . Rep. Dan.

Oceanogr. Exped. 1908-10. Mediter. Adjacent

Seas 2(A.7), 154 p.
Voss, Nancy A.

1954. The postlarval development of the fishes of

the family Gempylidae from the Florida Current.

I. Nesiarchiis Johnson and Gempylus Cuv. and

Val. Bull. Mar. Sci. Gulf Carib. 4(2) : 120-159.

44

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

Appendix Table 1. — Counts of fish larvae, tabulated by family, for all stations occupied on EASTROPAC I.

s

§

V3

%

E

o

CD

s

o

o

u

1

s

CO

i

n

a>
c
o
u

<

H

c
o

1
1

o

s

c
o

2

'o

i

3
w

u

O

a;

'2

%
o

s

0}

■5
a

2

u

<A

§•

o

CO

I

a

%

•a
3
X

a

S

<A

;a

o
u
<u
u

u

8

f

o

X

cfl

E
o
o
CO

1

E
o

i

z

I..

c
o

•g

1

A
O

2

U

s

c

B

•D

2
n
u
bo

•a
m

3

01

t

■a

11.022

0

10

1

0

0

0

0

4

0

0

0

0

0

0

0

0

0

0

0

0

0

0

15

.025

0

52

0

0

0

0

0

11

1

3

0

0

0

0

0

0

0

0

0

0

2

0

69

.027

0

36

0

0

0

4

0

14

1

0

0

0

0

0

0

0

0

0

0

1

0

1

57

.030

0

1

0

0

0

0

0

1

0

0

0

0

0

0

0

0

0

0

0

0

0

1

3

.032

1

15

0

0

0

0

0

19

0

0

0

0

2

0

0

0

0

0

0

0

2

1

40

.034

1

88

0

0

0

1

0

35

0

0

0

0

0

0

0

0

0

0

0

0

1

2

128

.036

0

26

0

0

0

0

1

3

1

0

0

0

3

0

0

0

0

0

0

0

0

0

34

.038

4

22

0

0

0

4

0

21

2

0

0

0

6

0

0

0

0

0

0

0

1

0

60

.040

0

20

0

0

0

11

0

55

0

3

0

3

3

0

0

0

0

0

0

4

1

0

100

.044

2

9

0

0

0

20

0

5

1

0

0

2

4

0

0

0

0

0

0

0

3

0

46

.046

3

58

0

0

0

22

0

50

0

4

0

1

2

0

0

0

0

0

1

1

1

3

146

.048

12

41

0

0

0

12

0

20

3

1

0

3

1

0

0

0

0

0

0

0

0

1

94

.050

24

23

0

0

0

3

1

36

0

1

0

2

0

0

0

0

0

0

0

0

1

10

101

.052

15

3

15

0

0

2

0

58

0

0

0

4

2

0

0

0

1

1

0

0

0

1

102

.054

11

8

17

0

0

0

0

159

0

1

0

2

0

0

0

0

3

0

0

0

0

4

205

.056

10

8

0

0

0

0

0

67

0

5

0

0

0

0

0

1

5

0

0

0

5

12

113

.058

10

3

14

0

0

0

0

28

0

0

0

6

2

0

0

0

1

0

0

1

1

10

76

.060

13

9

30

2

1

0

0

72

2

0

0

2

0

0

3

0

5

0

0

2

5

1

147

.062

0

0

6

0

0

0

0

21

2

0

0

5

1

0

0

0

1

0

0

0

1

3

40

.064

0

1

22

0

0

0

2

51

0

0

0

3

3

0

0

1

7

2

0

2

3

2

99

.066

0

2

16

1

0

0

0

63

4

0

0

1

7

3

3

0

4

2

0

15

0

5

126

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5

77

49

0

2

0

3

229

4

0

3

6

45

1

2

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26

1

1

10

9

0

473

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1

24

21

0

5

1

0

96

6

0

3

1

25

1

0

0

9

1

0

12

8

9

223

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2

73

20

0

6

1

4

178

4

0

1

2

11

0

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16

1

0

12

8

0

340

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6

689

21

0

5

4

3

90

0

1

0

2

0

0

4

0

2

0

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4

7

20

858

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7

142

11

0

0

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6

36

3

0

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1

0

0

0

4

0

0

0

7

0

219

.084

11

361

3

0

1

1

0

131

6

1

0

0

1

0

4

0

3

0

1

2

0

26

552

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1

324

3

0

0

0

1

104

3

1

0

0

0

0

0

0

7

0

0

3

0

8

455

.094

0

50

2

0

1

0

0

66

14

0

0

0

0

0

0

0

1

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5

4

4

147

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2

107

2

0

0

0

0

907

20

0

0

2

1

0

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0

4

0

23

12

4

12

1097

11.102

6

33

4

0

0

0

0

99

7

0

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12

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5

168

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1

10

2

0

1

0

2

22

0

0

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48

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8

9

7

0

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0

57

0

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1

87

.114

1

57

43

0

0

0

1

243

1

0

0

1

0

0

0

1

3

0

0

5

1

1

358

.118

4

7

6

0

0

0

0

84

0

0

0

3

0

0

0

0

0

1

0

2

2

3

112

.120

1

3

2

0

0

0

0

9

0

0

0

1

0

0

0

0

0

0

1

2

3

0

22

.124

0

25

11

0

0

0

0

66

0

0

0

0

0

0

1

0

5

0

0

0

0

3

HI

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0

98

6

0

0

0

2

98

4

1

0

1

0

0

0

0

10

1

0

3

4

2

230

.130

0

7

6

0

2

0

1

29

2

0

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0

0

0

0

0

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1

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51

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8

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5

16

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0

0

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0

1

4

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42

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0

28

0

0

0

0

2

109

4

0

0

1

0

4

171

0

0

0

0

3

8

4

334

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0

46

33

0

0

2

2

168

9

2

6

4

0

0

2

0

0

0

0

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7

1

282

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0

8

34

0

0

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5

21

4

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0

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6

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87

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0

5

9

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12

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1

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33

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0

13

7

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69

8

1

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110

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22

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17

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49

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103

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38

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141

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138

4

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115

3

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4

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268

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8

4

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2

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15

1

0

0

2

1

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0

0

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5

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45

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0

88

3

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0

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2

29

4

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2

0

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21

157

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0

40

2

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1

6

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103

6

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0

1

3

0

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1

0

1

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4

2

29

199

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0

102

2

0

0

1

1

117

9

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27

286

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10

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0

0

2

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2

31

45

FISHERY BULLETIN: VOL. 69. NO. 1

Appendix Table 1. — Counts of fish larvae, tabulated by family, for all stations occupied on EASTROPAC I. —

Continued.

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14

.167

0

30

0

0

0

0

1

20

1

0

0

0

0

0

1

0

0

0

0

0

3

0

56

.169

0

4

1

0

0

0

0

3

1

0

0

0

0

0

0

0

0

0

0

0

0

0

9

.171

0

11

0

0

0

0

0

1

1

0

0

0

0

0

0

0

0

0

0

0

0

0

13

.173

0

9

0

0

0

0

0

5

0

1

0

0

0

0

0

0

0

0

0

1

0

0

16

.175

0

2

0

0

0

0

0

4

0

0

0

0

0

0

0

0

0

0

1

1

0

0

8

.177

0

5

0

0

0

0

0

3

0

0

0

0

0

0

0

0

0

0

0

2

0

1

11

.179

0

5

0

0

0

0

0

13

0

0

0

0

0

0

0

0

0

0

0

1

0

0

19

.181

0

13

3

0

0

0

0

13

1

0

0

0

0

0

0

0

0

0

0

1

0

0

31

.183

0

5

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

3

0

8

.185

0

5

0

0

0

0

0

4

0

0

0

0

0

0

0

0

0

0

0

0

0

0

9

.187

0

22

1

0

0

0

1

24

0

1

0

0

0

1

0

0

0

0

0

1

0

1

52

.189

0

21

1

0

0

0

0

19

0

0

0

0

0

0

0

0

0

1

0

0

0

1

43

.191

0

1

0

0

0

0

0

2

0

0

0

0

0

0

0

0

0

0

0

0

1

0

4

.195

0

14

0

0

0

0

0

4

0

0

0

0

0

0

0

0

0

0

0

0

0

0

18

.197

0

45

1

0

0

0

1

60

3

0

0

0

1

0

2

0

0

0

0

6

0

5

124

.199

0

6

0

0

0

1

0

9

0

0

0

1

0

0

1

0

0

0

0

3

0

5

26

11.201

0

2

2

0

0

0

0

8

0

0

1

0

1

0

0

0

0

0

0

1

0

0

15

.203

0

24

1

0

0

0

0

17

1

0

0

0

1

0

0

0

0

0

0

2

0

4

50

.205

0

53

1

0

0

1

3

40

2

0

0

0

7

0

0

0

0

0

0

0

0

5

112

.207

0

15

0

0

0

1

0

21

2

0

0

0

0

0

0

0

0

0

0

1

0

7

47

.209

0

7

1

0

0

1

0

12

2

3

0

1

4

0

0

0

0

0

0

2

1

2

36

.211

0

39

5

0

0

0

1

28

1

0

0

1

1

0

0

0

0

0

0

2

6

5

89

.213

0

37

5

0

0

0

3

71

3

2

0

0

3

0

4

1

0

0

0

2

4

1

136

.215

0

5

7

0

0

0

0

44

4

0

0

0

6

0

3

0

0

0

0

2

4

5

80

.217

0

8

7

0

0

0

1

16

0

0

0

1

4

0

0

0

0

1

0

3

0

1

42

.219

0

2

15

0

0

0

0

10

1

0

0

0

6

0

1

1

1

0

0

0

2

1

40

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0

56

35

0

0

0

0

74

6

2

3

2

6

0

1

0

2

2

0

1

3

1

194

.223

0

13

32

1

0

0

0

20

0

0

1

3

5

0

0

0

0

0

0

0

0

1

76

.226

0

5

4

0

0

1

0

7

0

1

3

1

3

0

0

0

0

0

0

0

0

0

25

.228

0

3

12

1

0

2

0

16

2

0

2

3

4

0

0

1

0

0

0

1

4

3

54

.234

2

17

19

0

0

0

0

46

1

2

0

1

0

0

0

1

0

0

0

6

5

17

117

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0

8

7

0

1

0

1

10

0

0

0

1

0

0

0

0

0

2

0

1

0

13

44

.242

4

50

20

1

1

0

0

95

1

1

0

2

0

1

0

0

2

2

1

5

3

6

195

.246

2

52

6

0

4

0

0

198

1

1

0

0

0

0

0

0

0

1

0

4

3

2

274

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1

20

6

0

0

0

0

57

1

0

0

2

0

0

0

0

2

0

0

6

0

5

100

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0

20

1

0

0

0

2

149

6

1

0

0

0

2

0

0

2

0

7

2

8

23

223

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3

54

6

0

0

0

0

108

9

0

0

2

0

0

0

0

0

0

0

2

3

2

189

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2

68

1

0

0

0

3

85

9

0

0

0

0

0

0

0

2

0

0

0

2

3

175

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3

33

5

0

0

0

0

38

1

0

0

0

0

0

0

0

5

0

0

0

4

0

89

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4

19

8

0

0

0

0

17

0

0

0

0

0

0

7

0

0

0

0

1

6

4

66

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13

155

13

0

0

0

116

3

0

1

1

4

0

0

0

1

0

0

2

4

3

317

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1

27

4

0

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1

82

6

0

5

0

7

0

0

0

0

3

I

3

5

4

151

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9

10

34

0

0

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30

5

0

3

1

13

1

0

0

1

0

0

5

3

25

142

.287

1

18

13

0

0

2

87

8

1

4

5

13

0

0

0

0

0

0

5

5

7

172

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0

17

18

0

0

1

131

2

0

3

10

6

0

0

0

0

0

0

25

2

10

229

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0

2

19

0

0

0

39

0

0

2

6

10

0

0

0

1

0

0

5

0

6

91

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7

3

46

0

0

1

50

2

0

1

5

5

0

6

0

9

3

1

16

2

8

166

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10

15

40

0

0

0

0

130

4

0

0

4

0

0

1

2

12

1

0

7

3

3

232

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5

12

3

0

0

0

0

297

4

0

0

1

4

0

3

2

2

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5

1

9

349

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27

2

15

0

0

0

0

29

0

0

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4

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5

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4

1

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4

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2

93

11.301

1

13

0

0

0

6

0

8

0

1

0

2

1

0

2

0

2

1

0

4

0

3

44

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12

47

0

0

1

8

0

44

0

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0

4

1

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0

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0

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7

127

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4

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0

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0

3

0

40

0

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0

4

1

0

1

0

0

0

1

1

0

4

123

46

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

Appendix Table 1. — Counts of fish larvae, tabulated by family, for all stations occupied on EASTROPAC I.-

Continued.

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44

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4

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15

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53

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0

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100

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5

32

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1

27

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74

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0

3

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8

0

0

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2

0

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3

0

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26

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0

3

13

0

0

0

0

34

0

1

0

1

2

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0

5

0

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0

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61

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1

10

5

0

0

2

0

11

1

0

0

0

2

0

0

1

0

0

0

1

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6

40

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0

35

11

0

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2

1

115

0

10

0

3

1

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0

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0

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186

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0

21

1

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1

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48

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0

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31

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81

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0

40

7

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4

1

55

2

3

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2

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122

12.002

3

13

0

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21

1

37

1

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83

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3

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32

3

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152

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123

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269

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90

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106

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69

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301

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199

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370

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3

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127

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56

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400

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268

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78

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398

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117

47

FISHERY BULLETIN': VOL. 69, NO. 1

Appendix Table 1. — Counts of fish larvae, tabulated by family, for all stations occupied on EASTROPAC I. —

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192

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26

41

33

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319

5

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452

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141

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32

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67

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17

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235

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330

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6

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15

3

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2

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1

1

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92

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5

36

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2

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30

2

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4

3

82

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8

24

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0

0

27

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0

0

1

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66

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0

22

17

0

14

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108

0

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172

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0

8

8

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66

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20

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62

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0

16

17

0

0

0

0

19

1

0

0

0

0

0

0

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0

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0

0

1

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56

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0

12

6

0

0

0

0

10

3

0

1

0

2

0

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36

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21

9

0

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69

0

0

0

2

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11

2

0

0

0

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3

2

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120

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110

11

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11

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3

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241

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1

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37

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292

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86

1

0

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0

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3

0

0

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4

0

151

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0

16

3

0

0

2

0

37

0

0

0

0

1

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0

1

0

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69

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0

11

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12

0

1

0

0

4

0

0

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0

0

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31

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8

0

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0

1

14

1

0

0

0

0

0

0

0

0

0

0

3

0

0

27

.158

0

50

1

0

0

0

0

41

4

1

0

1

0

0

0

1

0

0

0

1

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100

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0

19

0

0

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42

.162

0

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0

49

25

0

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1

0

45

4

5

0

1

0

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133

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20

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56

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12.200

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140

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83

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390

48

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

Appendix Table 1. — Counts of fish larvae, tabulated by family, for all stations occupied on EASTROPAC I. —

Continued.

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14

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348

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6

8

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51

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78

.250

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54

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6

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89

.252

3

5

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44

2

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64

.254

5

13

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84

5

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0

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0

0

0

1

0

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113

.256

3

1

15

0

0

0

2

23

5

0

0

0

5

0

0

0

0

0

0

1

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56

.258

0

0

26

0

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0

0

43

0

0

0

0

0

0

0

0

0

0

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0

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69

.260

2

20

4

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0

74

4

2

0

4

0

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0

1

1

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4

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3

120

.262

2

102

0

0

0

7

3

161

10

4

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0

3

0

0

1

0

0

0

2

0

0

295

.264

2

20

0

0

0

29

1

26

10

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8

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6

110

.265

3

18

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32

1

54

5

7

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2

17

0

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2

0

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1

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1

145

.268

0

105

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1

156

6

6

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4

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5

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316

.270

1

29

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1

60

6

4

0

2

7

0

0

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0

0

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3

135

.272

4

43

0

0

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6

2

81

4

1

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5

11

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0

I

0

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0

3

5

2

168

.274

0

40

0

0

0

36

1

85

5

1

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8

4

0

0

0

1

0

0

1

1

4

187

.276

0

138

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0

20

0

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167

.278

1

165

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45

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219

.280

0

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29

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1

23

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35

.284

0

120

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139

13.001

8

93

108

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0

41

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274

.003

14

II65

39

0

2

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1

385

14

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1657

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54

310

18

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.007

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133

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48

12

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177

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470

49

FISHERY BULLETIN: VOL. 69, NO, 1

Appendix Table 1. — Counts of fish larvae, tabulated by family, for all stations occupied on EASTROPAC I. —

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2

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257

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37

572

8

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6

318

9

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42

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53

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27

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172

27

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113

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257

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43

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268

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2

164

13

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1

16

2

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215

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5

43

4

0

0

0

0

17

1

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6

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0

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1

0

0

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0

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1

78

.085

0

2

1

0

0

0

0

17

0

0

0

0

0

0

0

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0

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0

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20

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0

66

6

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1

0

37

0

1

0

0

1

0

0

0

0

0

0

3

0

0

115

.089

0

26

29

0

0

0

0

105

2

0

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0

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0

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2

3

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15

183

.091

0

11

2

0

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1

49

6

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2

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1

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2

17

101

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0

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13

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6

146

4

1

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3

195

1

0

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4

7

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7

0

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12

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4

439

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3

103

11

0

0

7

2

205

2

2

0

6

4

0

1

5

0

1

4

9

2

1

368

.099

0

16

7

0

1

0

1

48

0

0

0

1

1

0

0

0

0

0

6

1

1

0

83

13.101

3

11

0

0

1

0

0

45

2

3

0

1

7

0

0

7

0

0

0

4

1

0

85

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1

162

6

0

1

3

4

255

5

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5

3

0

0

7

0

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3

14

3

7

479

.105

0

50

4

0

0

1

1

166

2

0

0

3

1

0

0

2

0

1

4

5

2

0

242

.107

0

1

0

0

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0

0

13

0

0

0

0

0

0

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1

0

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1

0

0

0

16

.109

0

12

0

0

0

0

0

27

0

0

0

0

0

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0

0

0

0

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2

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41

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0

18

1

0

0

0

0

49

1

0

0

1

0

0

0

0

0

0

0

1

0

0

71

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0

30

2

0

0

0

1

72

2

0

0

0

2

1

0

0

0

0

0

2

0

0

112

.115

0

8

0

0

0

0

0

25

1

0

0

0

1

0

0

0

0

0

0

1

0

1

37

.117

0

9

4

0

0

0

4

52

1

2

0

1

3

1

0

0

0

0

0

1

1

2

81

.119

0

36

0

0

0

0

4

86

4

0

0

0

0

0

0

4

0

0

0

0

0

0

134

.121

0

17

3

0

0

0

0

22

1

0

0

0

0

0

0

0

0

0

0

0

0

2

45

.123

0

3

2

0

0

0

0

3

1

1

0

2

0

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0

0

0

2

0

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14

.125

0

1

1

0

0

0

0

2

0

0

0

1

0

0

0

0

0

0

0

0

0

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5

.127

0

20

2

0

0

0

3

39

1

1

0

1

1

0

0

0

0

0

0

0

0

1

69

.129

0

11

1

0

0

0

2

14

0

0

0

0

0

0

0

0

0

0

0

0

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0

28

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0

6

0

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7

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16

.133

0

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21

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0

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140

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0

40

1

0

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0

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50

1

0

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0

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96

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0

0

0

8

0

0

0

0

0

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0

1

0

0

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24

.141

0

4

0

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8

0

0

0

0

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12

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0

76

2

0

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0

0

86

1

0

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1

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0

0

0

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0

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173

.145

0

20

2

0

0

0

2

44

2

0

0

0

2

0

0

0

0

0

0

0

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72

.147

0

17

0

0

0

0

0

33

0

0

0

3

4

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2

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3

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65

.149

0

14

6

0

0

0

0

29

0

0

0

2

0

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0

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1

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59

.151

0

22

0

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1

72

0

1

0

0

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103

.153

0

103

1

0

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3

1

394

2

1

1

5

3

0

0

1

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539

.155

0

8

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16

0

2

0

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38

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0

8

8

0

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1

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67

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53

1

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92

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0

24

6

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65

3

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102

.163

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0

0

0

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48

50

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

Appendix Table 1. — Counts of fish larvae, tabulated by family, for all stations occupied on EASTROPAC I.-

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51

FISHERY BULLETIN: VOL. 69. NO, 1

Appendix Table 1. — Counts of fish larvae, tabulated by family, for all stations occupied on EASTROPAC I. —

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52

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

Appendix Table 1. — Counts of fish larvae, tabulated by family, for all stations occupied on EASTROPAC I.-

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189

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176

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209

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137

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326

14.203

3

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179

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4

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208

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5

2

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0

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56

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34

96

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206

1

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1

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0

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11

0

2

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378

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27

39

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86

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73

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76

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2

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90

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9

49

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0

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0

31

1

2

0

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12

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139

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9

869

1

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185

9

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350

1748

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3

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34

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83

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18

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116

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85

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330

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24

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86

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169

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210

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11

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227

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59

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631

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149

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354

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154

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50

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123

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14.300

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38

53

FISHERY BULLETIN: VOL. 69, NO. 1

Appendix Table 2. — Myctophid larvae, tabulated by genus or species, for all stations occupied on EASTROPAC I.

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54

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

Appendix Table 2. — Myctophid larvae, tabulated by genus or species, for all stations occupied on EASTROPAC I.

— Continued.

t

K

11.156
.158
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11.201
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55

FISHERY BULLETIN; VOL. 69, NO. I

Appendix Table 2. — Myctophid larvae, tabulated by genus or species, for all stations occupied on EASTROPAC I.

— Continued.

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56

AHLSTROMt FISH LARVAE IN EASTERN TROPICAL PACIFIC

Appendix Table 2. — Myctophid larvae, tabulated by genus or species, for all stations occupied on EASTROPAC I.

— Continued.

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57

FISHERY BULLETIN: VOL. 69. NO. I

Appendix Table 2. — Myctophid larvae, tabulated by genus or species, for all stations occupied on EASTROPAC I.

— Continued.

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0 98
0 61
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1
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1

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6
2
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11
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6
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1
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0
0
0
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91

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70

300

202

127

209

1089

162

49

250

280

225

54

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248

51

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44

84

23

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74

161

26

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156

60

81

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20

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5

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0 315
0 1020
0 115
0 470
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58

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

Appendix Table 2. — Myctophid larvae, tabulated by genus or species, for all stations occupied on EASTROPAC I.

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19
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109

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318

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205

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59

FISHERY BULLETIN: VOL. 69. NO. I

Appendix Table 2. — Myctophid larvae, tabulated by genus or species, for all stations occupied on EASTROPAC I.

— Continued.

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60

AHLSTROM: FISH LARVAE IN ELASTERN TROPICAL PACIFIC

Appendix Table 2. — Myctophid larvae, tabulated by genus or species, for all stations occupied on EASTROPAC I.

— Continued.

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61

FISHERY BULLETIN: VOL. 69. NO. I

Appendix Table 2. — Myctophid larvae, tabulated by genus or species, for all stations occupied on EASTROPAC I.

— Continued.

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62

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

Appendix Table 2. — Myctophid larvae, tabulated by genus or species, for all stations occupied on EASTROPAC I.

— Continued.

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63

FISHERY BULLETIN: VOL. 69, NO. 1

Appendix Table 3. — Counts of selected categories of fish larvae, tabulated by station, EASTROPAC I.

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64

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

Appendix Table 3. — Counts of selected categories of fish larvae, tabulated by station, EASTROPAC I. — Continued.

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65

FISHERY BULLETIN: VOL. 69, NO. I

Appendix Table 3. — Counts of selected categories of fish larvae, tabulated by station, EASTROPAC I. — Continued.

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66

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

Appendix Table 3. — Counts of selected categories of fish larvae, tabulated by station, EASTROPAC I. — Continued.

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FISHKRY BULLETIN: VOL. 69, NO. I

Appendix Table 3. — Counts of selected categories of fish larvae, tabulated by station, EASTROPAC I. — Continued.

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68

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

Appendix Table 3. — Counts of selected categories of fish larvae, tabulated by station, EASTROPAC I. — Continued.

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69

FISHERY BLLLETIN: VOL. 69, NO. I

Appendix Table 3. — Counts of selected categories of fish larvae, tabulated by station, EASTROPAC I. — Continued.

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70

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

Appendix Table 3. — Counts of selected categories of fish larvae, tabulated by station, EASTROPAC I. — Continued.

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71

FISHERY BULLETIN: VOL. 69, NO. 1

Appendix Table 3. — Counts of selected categories of fish larvae, tabulated by station, EASTROPAC I. — Continued.

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72

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

Appendix Table 4. — Summary of occurrences and numbers of larvae of eight families, limited in distribution to a

broad coastal band or around offshore islands.

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0

0

0

3

0

.249

0

0

0

0

0

0

1

0

.220

0

0

0

0

0

I

1

0

.253

0

0

0

0

0

0

72

0

.222

0

0

0

0

0

1

0

0

.255

2

0

1

2

0

0

2

3

.224

0

0

0

3

0

0

0

1

.257

0

0

0

0

0

0

0

1

.228

0

0

0

0

1

0

0

4

.261

0

0

0

0

0

0

41

0

.230

0

0

0

2

0

0

0

2

.263

0

3

0

0

0

0

0

2

.232

0

0

0

0

0

0

2

0

.265

0

0

0

0

0

0

0

1

.234

0

0

0

9

3

0

8

3

.266

0

0

0

0

0

1

0

0

.236

0

0

0

0

0

0

1

0

.268

0

0

a

0

0

1

0

0

.240

0

0

0

0

0

0

1

1

.274

0

0

0

0

0

0

3

0

.243

0

0

0

0

0

0

1

0

.276

0

0

0

0

0

0

2

0

.247

0

0

0

0

0

0

2

0

13. 320

1

0

0

0

0

1

7

3

14.303

0

0

0

0

1

1

0

0

.328

0

0

0

0

0

0

2

1

.314

0

0

9

0

0

0

0

1

.330

0

0

0

0

0

0

4

0

.318

0

0

10

0

4

2

43

5

.334

0

0

0

0

0

0

1

0

.323

0

0

0

0

1

0

3

1

.338

0

0

0

0

0

0

17

0

.326

0

0

13

0

2

0

23

0

73

FISHERY BULLETIN: VOL. 69, NO. I

Appendix Table 5.— Numbers and kinds of larvae of Gempylidae-Trichiuridae obtained in EASTROPAC I collections.

03

3

«

IS

i

K

"E

m

s

§

.1
u

m

B
o

c

&

03

3

a

"a
E

01

3
C

S
03

u

a
m
s

1
u

2
o

D3

ta

3

1

03

3

£

03

a

o

ta

u

<

13

£
O

5

<

Z

1

a

S

3

i

11.056

0

1

0

0

0

13.107

0

0

1

0

0

.064

0

0

1

0

0

.119

1

3

0

0

0

.072

0

1

0

0

0

.137

0

2

0

0

0

11.114

1

0

0

0

0

.139

0

0

1

0

0

.138

1

0

0

0

0

.147

0

0

1

0

e

.140

1

0

0

0

0

.153

0

0

1

0

0

.146

0

1

0

0

0

.159

0

2

0

8

0

.158

1

0

0

0

0

.167

1

0

0

fl

0

.159

1

0

0

0

0

.171

0

1

0

(

0

11.213

0

1

0

0

0

.173

1

0

0

0

0

.219

0

1

0

0

0

.175

I

0

0

0

0

.228

1

0

0

0

0

.179

0

3

0

0

0

.234

0

1

0

0

0

.187

0

0

0

0

2

.295

0

2

0

0

0

.191

0

1

0

0

0

.297

0

2

0

0

0

13.235

1

0

0

0

0

11.318

0

0

5

0

0

.245

0

1

0

0

0

.320

0

0

1

0

0

.280

0

0

0

0

1

.324

0

0

1

0

0

.326

0

0

2

0

0

14.001

0

1

0

0

0

.010

1

0

0

0

0

12.004

0

1

0

0

0

.012

0

0

0

1

0

.014

0

1

0

0

0

.029

1

0

1

1

0

.020

0

1

0

0

0

.031

1

0

0

0

0

.047

0

2

0

0

0

.095

0

0

0

0

.081

0

1

0

0

0

14.122

0

0

0

0

12.115

0

0

0

0

1

.123

0

0

0

0

.118

6

0

0

0

1

.124

1

1

0

0

.120

1

0

0

0

0

.126

1

0

0

0

.144

0

1

0

0

0

.127

0

0

3

0

0

.150

0

3

0

0

0

.128

0

0

6

0

0

.152

0

1

0

0

0

.130

0

0

3

0

0

.158

0

1

0

0

0

.131

0

0

1

0

0

.188

0

1

0

0

0

.134

1

1

0

0

0

12.246

0

2

0

0

0

.138

3

0

0

0

0

.260

0

1

0

0

0

.142

2

0

0

0

0

.262

0

1

0

0

0

.146

2

0

0

0

0

.272

0

1

0

0

0

.150

1

0

0

0

0

.276

0

1

0

0

0

.164

1

0

0

0

0

.188

1

0

0

0

0

13. 048

1

2

0

0

0

.194

0

0

0

2

0

.054

0

0

0

17

0

.195

1

0

0

0

0

.056

2

0

0

0

0

14.222

1

0

0

0

0

.071

6

0

e

0

0

.224

1

0

0

0

0

.073

7

0

0

0

0

.234

8

0

0

1

0

.075

2

0

0

0

0

.240

1

0

0

0

0

.077

3

0

0

0

0

.259

3

0

0

0

0

.081

8

0

0

0

0

.280

1

4

1

0

0

.083

0

1

0

0

0

.283

0

0

1

0

0

.095

0

0

7

0

0

.287

1

2

0

0

0

.097

0

1

4

0

0

.295

0

1

0

0

0

.101

0

1

6

0

0

14.318

1

0

0

2

0

.103

0

0

7

0

0

.326

0

0

0

1

0

.105

0

0

2

0

0

.330

1

0

0

0

0

74

AHLSTROM; FISH LARVAE IN EASTERN TROPICAL PACIFIC

Appendix Table 6.— Numbers and kinds of flatfish (Pleuronectiformes) larvae obtained in EASTROPAC I collections.

5

t-
w

1

t3

w

a,
en

<D

a

3

8

&

§

3

(A

_o

CO

6^

g

£

^

o

o

w

U

a

W

w

CO

t-<

1

s

1

CO

^

c

ci

CO

o

&

CO

CO

1

E

3

5

o

>1

C3

a
£

U

O

U

W

Cfi

s

12.028

0

0

0

0

0

1

0

14.001

1

5

0

1

0

35

0

.030

0

1

0

0

0

0

0

.006

0

1

0

0

0

2

0

.031

0

0

0

0

2

e

0

.008

0

1

0

0

0

3

0

.033

4

1

0

0

6

6

0

.010

0

1

0

1

0

1

0

.035

0

0

0

0

0

3

0

.014

0

2

0

0

0

4

0

.045

0

0

0

0

0

1

0

.016

0

0

0

0

0

5

1

.017

0

0

0

0

0

2

0

.013

0

1

0

0

0

1

0

13.007

0

0

0

0

1

0

0

.020

0

0

0

0

0

5

0

.009

0

1

0

0

0

0

0

.022

1

3

0

0

0

1

0

.011

0

1

0

0

0

0

0

.024

0

1

0

0

0

9

0

.013

0

0

0

0

0

5

0

.027

1

6

0

1

3

9

0

.015

1

0

0

0

0

1

0

.029

1

5

0

0

2

24

0

.019

6

1

1

0

25

31

1

.031

0

0

0

1

0

30

0

.021

2

2

0

0

13

8

0

.033

0

0

0

1

0

2

0

.030

0

0

0

0

0

4

0

.040

0

1

0

0

2

4

0

.032

0

0

0

0

0

8

0

.047

0

0

0

0

0

1

0

.034

0

0

0

2

4

9

0

.055

0

1

0

0

0

2

0

.036

0

0

0

0

1

0

0

14.164

1

0

0

0

0

1

0

.040

1

2

0

1

0

3

0

.174

0

0

0

0

0

1

0

.042

1

0

1

0

6

1

0

.183

0

0

0

0

0

1

0

.054

1

0

0

0

0

0

0

.194

0

0

0

0

0

1

0

13.245

1

0

0

0

0

0

0

.195

0

0

0

0

0

1

0

.251

0

0

0

0

0

1

0

.199

0

0

0

0

0

1

0

.253

4

0

0

0

0

4

0

14.209

0

0

0

0

0

1

0

.255

3

1

0

0

0

9

0

.213

0

0

0

0

1

0

0

.257

0

0

0

0

0

1

0

.220

0

0

0

0

0

3

0

.259

0

0

0

0

1

1

0

.228

0

1

0

0

0

3

0

.261

1

0

0

0

1

1

0

.230

0

0

0

0

0

1

0

.263

1

0

0

0

3

8

0

.232

0

0

0

0

1

0

0

.265

0

0

0

0

2

1

0

.234

2

0

2

0

3

1

0

13.318

2

0

0

0

1

1

0

.236

1

0

0

0

0

2

0

.320

2

0

0

0

0

2

0

.240

0

0

0

0

1

0

0

.322

5

0

0

0

0

0

0

.259

2

0

0

0

0

0

0

.324

0

0

0

0

1

0

0

.295

0

1

0

0

0

0

0

.326

0

0

0

0

1

2

0

14.300

0

0

0

0

1

0

0

.328

0

0

0

0

0

1

0

.303

1

1

0

0

0

1

0

.334

1

0

0

0

0

0

0

.306

0

0

0

0

0

1

0

.314

0

0

0

0

0

1

0

.318

1

2

0

1

0

19

0

.323

1

3

0

0

2

2

0

.326

1

4

0

0

0

3

0

.330

0

0

0

0

0

1

0

75

FISHERY BULLETIN: VOL. 69, NO. 1

Appendix Table 7. — Standardized haul factors (SHF) : These factors are used to adjust original counts of
larvae to the comparable standard of numbers of larvae in 10 m" of water strained per meter of depth fished.

Station

SHF

Station

SHF

Station

SHF

Station

SHF

Station

SHF

11.022

3.06

LI. 156

2.74

11.291

3.46

12.061

3.33

12.192

3.27

11.025

2.87

11.158

3.12

11.293

2.93

12.063

3.27

12.194

3.45

11. 027

2.38

11.159

2.64

11.295

3.16

12.065

3.23

12.196

3.32

11.030

2.47

11.161

3.35

11.297

2.86

12.067

3.36

12.198

3.40

11.032

3.01

11.163

2.64

11.299

3.57

12.068

3.39

12.200

3.18

11.034

3.64

11.167

2.97

11.301

3.31

12.071

3.34

12.203

3.29

11.036

3.04 ]

11.169

3.27

11.303

3.19

12.075

3.33

12.206

3.53

11.038

2.80

11.171

2.92

11.306

3.22

12.077

3.42

12.209

3.51

11.040

3.32 ]

11.173

2.94

11.308

3.15

12.079

3.56

12.212

3.32

11.044

2.81 ]

11.175

3.47

11.310

3.19

12.091

3.53

12.215

3.27

11. 046

3.24 ]

11.177

1.36

11.312

3.42

12.084

3.73

12.218

3.02

11.048

3.08 ]

1.179

3.37

11.314

3.18

12.087

3.86

12.221

3.07

11.050

2.36 ]

LI. 181

2.74

11.316

2.84

12.090

3.10

12.224

2.58

11.052

2.86 ]

1.183

2.92

11.318

3.27

12.092

2.55

12.227

2.96

11.054

2.54 ]

1.185

3.19

11.320

3.34

12.094

2.29

12.230

3.72

11.056

2.90 ]

1.187

2.75

11.322

3.01

12.097

3.01

12.233

2.66

11.058

3.28 :

1.189

3.00

11.324

3.02

12.100

2.48

12.235

3.56

11.060

3.15 ]

1.191

3.79

11.326

2.84

12.103

3.28

12.238

3.21

11.062

3.72 ]

1.195

3.11

11.328

2.62

12.106

3.55

12.240

3.22

11.064

3.01 ]

1.197

3.14

12.109

3.39

12.242

3.41

11.066

2.12 ]

1.199

2.46

12.002

3.12

12.112

3.43

12.244

3.36

11.068

2.62 ]

1.201

3.27

12.004

3.02

12.115

3.48

12. 246

3.14

11.070

2.25 ]

1.203

3.09

12.006

3.31

12.118

2.45

12. 248

3.07

11.072

3.43 ]

1.205

3.20

12.008

3.08

12.120

3.46

12.250

2.49

11.076

2.92 ]

1.207

3.65

12.010

3.13

12.122

3.43

12.252

2.33

11.080

2.45 ]

1.209

3.06

12.012

3.17

12.124

3.17

12. 254

3.30

11.084

2.70 ]

1.211

3.39

12.014

3.28

12.126

3.47

12.256

3.26

11.088

3.19 ]

1.213

2.87

12.016

3.17

12.128

3.30

12.258

3.26

11. 094

3.61 ]

1.215

3.13

12.018

3.13

12.130

3.35

12.260

3.51

11.098

1.78 ]

1.217

2.90

12.020

3.12

12.132

3.38

12.262

2.98

11.102

2.72 ]

1.219

3.36

12. 022

3.43

12.134

3.29

12.264

3.38

11.106

1.36 ]

1.221

2.92

12.024

3.11

12.136

3.22

12.265

3.27

11.110

2.95 ]

1.223

3.71

12.026

3.30

12.138

3.38

12.268

3.35

11.114

3.35 ]

1.226

3.05

12.028

3.44

12.140

3.00

12.270

3.36

11.118

4.65 ]

1.228

3.29

12.030

3.44

12.142

3.42

12.272

3.12

11.120

3.68 ]

1.234

3.65

12.032

3.32

12.144

3.20

12.274

3.28

11.124

3.67 ]

1.238

3.41

12.033

3.21

12.146

4.36

12.276

3.34

11.128

2.85 ]

1.242

3.77

12.035

3.35

12.148

3.21

12.278

3.00

11.130

3.80 ]

1.246

3.01

12.037

3.20

12.150

3.14

12.280

3.39

11.132

3.37 ]

1.250

2.77

12.039

3.47

12.152

3.17

12.282

3.58

11.134

3.22 ]

1.254

2.51

12.041

3.42

12.154

3.27

12.284

3.41

11.136

3.24 ]

1.258

2.86

12.043

3.33

12.156

3.28

11.138

3.38 ]

1.262

3.23

12.045

3.35

12.158

3.22

13.001

2.26

11.140

2.77 ]

1.266

2.91

12.047

3.42

12.160

3.49

13.003

2.45

11.142

3.35 ]

1.270

3.69

12.049

3.39

12.162

3.21

13.005

1.42

11.146

3.25 1

1.278

3.09

12.051

3.31

12.164

2.98

13.007

2.42

11.148

2.54 ]

1.282

3.99

12.053

3.27

12.184

3.22

13.009

2.56

11.150

3.45 ]

1.285

3.20

12.055

2.84

12.186

3.22

13.011

3.68

11.152

2.59 ]

1.287

3.45

12.057

3.22

12.188

3.35

13.013

2.29

11.154

3.40 ]

1.289

3.12

12.059

3.41

12.190

3.39

13.015

2.76

76

AHLSTROM: FISH LARVAE IN EASTERN TROPICAL PACIFIC

Appendix Table 7. — Standardized haul factors (SHF) : These factors are used to adjust original counts of larvae
to the comparable standard of numbers of larve in 10 m' of water strained per meter of depth fished. — Continued.

Station

SHF

Station

SHF

Station

SHF

Station

SHF

Station

SHF

13.017

2.16

13.119

2.67

13.249

3.46

14.047

4.10

14. 203

3.15

13.019

1.88

13.121

3.14

13.251

3.46

14. 051

2.93

14. 209

3.23

13.021

2. 12

13.123

3.06

13.253

3.13

14. 055

3.77

14.213

3.26

13.022

2.72

13.125

3.50

13.255

3.58

14. 060

3.58

14. 218

2.87

13.028

1.53

13.127

3.30

13.257

3.68

14. 066

3.81

14.220

3.42

13.030

2.50

13.129

4.01

13.259

3.42

14. 069

3.65

14. 222

3.64

13.032

3.05

13.131

3.64

13.261

1.85

14.076

3.61

14. 224

3.77

13.034

3.21

13.133

3.84

13.263

3.49

14. 078

3.64

14. 228

3.87

13.036

2.34

13.135

2.51

13.265

3.29

14. 081

3.39

14. 230

2.96

13.038

2.25

13.137

2.58

13.266

3.31

14.084

3.86

14. 232

2.70

13.040

2.85

13.139

3.57

13.268

3.47

14.086

3.95

14.234

0.72

13. 042

2.74

13.141

3.36

13.270

3.30

14. 088

3.54

14. 236

2.96

13. 044

2.58

13.143

3.23

13.272

3.06

14. 091

3.08

14. 240

3.43

13. 046

3.08

13.145

3.49

13.274

3.73

14.095

3.87

14. 243

3.55

13. 048

2.71

13.147

3.58

13.276

3.54

14.099

3.70

14. 247

3.52

13.050

3.02

13.149

3.56

13.278

3.16

14.103

3.57

14.251

3.49

13.052

2.91

13.151

3.11

13.280

3.48

14.106

3.68

14.255

3.64

13.054

3.07

13.153

3.25

13.282

3.37

14.110

3.55

14.259

3.54

13.056

2.87

13.155

3.34

13.284

3.36

14.112

3.66

14.263

3.68

13.058

2.75

13.157

3.40

13.318

3.17

14.114

4.84

14.267

3.04

13.060

3.62

13.159

3.00

13.320

2.93

14.115

3.24

14.276

3.47

13. 062

3.15

13.161

3.30

13.322

3.22

14.117

4.29

14. 280

3.56

13.064

2.76

13.163

2.70

13.324

3.12

14.118

4.03

14. 283

3.60

13.065

2.81

13.165

3.22

13.326

3.05

14.120

3.76

14.287

3.53

13.067

2.67

13.167

3.64

13.328

3.15

14.122

3.78

14. 291

3.11

13.069

2.12

13.169

3.25

13.330

3.03

14.123

3.51

14.295

2.28

13. 071

2.61

13.171

3.12

13.332

3.13

14.124

3.38

14.300

3.58

13.073

3.11

13.173

2.80

13.334

2.85

14.126

3.69

14.303

3.48

13.075

3.42

13.175

2.71

13.338

3.02

14.127

3.89

14.306

3.29

13.077

2.72

13.179

2.46

13.340

3.00

14.128

3.66

14.310

2.85

13.079

2.53

13.183

3.39

13.342

3.03

14.130

3.62

14.314

3.60

13. 081

2.75

13.187

3.31

14.131

3.56

14.318

3.51

13.083

3.06

13.191

3.53

14.001

0.99

14.132

3.56

14.323

3.15

13.085

4.11

13.195

3.02

14. 006

2.94

14.134

3.67

14.326

1.51

13.087

2.87

13.199

2.77

14. 008

3.56

14.136

3.47

14.330

3.49

13. 089

2.65

13.203

2.60

14.010

5.83

14.138

3.83

13.091

2.97

13.207

3.31

14.012

3.50

14.142

3.69

13.093

2.87

13.211

3.01

14.014

3.51

14.146

3.75

13.095

2.81

13.215

2.97

14.016

3.28

14.150

3.60

13.097

3.02

13.219

2.44

14.017

4.19

14.154

4.24

13.099

2.64

13.223

3.01

14.018

3.13

14.158

2.45

13.101

2.75

13.227

3.32

14.020

2.89

14.164

1.01

13.103

2.77

13.231

2.42

14.022

3.45

14.172

3.55

13.105

2.77

13.235

3.05

14.024

3.55

14.174

3.57

13.107

2.76

13.237

3.56

14.027

3.55

14.177

3.88

13.109

2.90

13.239

3.51

14.029

2.63

14.183

3.94

13.111

2.88

13.241

3.55

14. 031

2.03

14.188

2.15

13.113

2.85

13.243

3.42

14.033

5.05

14.194

1.57

13.115

3.46

13.245

2.98

14. 040

3.65

14.195

1.39

13.117

2.99

13.247

3.27

14.043

3.53

14.199

1.54

77

SIZE STRUCTURE AND GROWTH RATE OF Euphausia pacifica
OFF THE OREGON COAST'

Michael C. Smiles, Jr.^ and William G. Pearcy'

ABSTRACT

Euphaiisia pacifica (Hansen) oflf Oregon has a maximum life expectancy of about 1 year. During this
time it grows rapidly to a length of 22-24 mm. Furcilia larvae were found throughout the year but
were most abundant during the autumn months. The population density and the proportion of juve-
niles was higher within 25 miles of the coast than in offshore oceanic waters.

Growth rates off Oregon are about twice those previously reported for this species from other re-
gions. Spawning also appears to be later in the year. All these features may be explained by the
high primary production which is extended throughout the summer by coastal upwelling and by the
lack of wide seasonal fluctuations of water temperatures along the Oregon coast.

Euphausia pacifica is one of the most abundant
euphausiids in the North Pacific Ocean. Dense
populations are found in Subarctic and Transi-
tional waters (Brinton, 1962a; Ponomareva,
1963) and off the Oregon coast (Hebard, 1966;
Osterberg, Pearcy, and Kujala, 1964 ; Pearcy
and Osterberg, 1967).

Euphausiids are important food for many
marine carnivores (see Mauchline and Fisher,
1969, and Ponomareva, 1963, for reviews) , and
Euphausia pacifica is no exception. It is preyed
upon by salmon (Ito, 1964), baleen whales (Ne-
moto, 1957, 1959; Osterberg et al, 1964), her-
ring (Ponomareva, 1963), sardine and mack-
erel (Nakai et al, 1957, as cited by Ponomareva,
1963; Komaki,1967),rockfish ( Pereyra, Pearcy,
and Carvey, 1969), pasiphaeid and sergestid
shrimp (Renfro and Pearcy, 1966), pandalid
shrimp (Pearcy, 1970), and myctophid fishes
(Tyler, 1970).

Studies on the growth of several species of
euphausiids are reviewed in the monograph by
Mauchline and Fisher (1969). Data on the

' This research was supported by the National Science
Foundation (GB-5494) and the Atomic Energy Com-
mission (AT (45-1) -1750; RLO 1750-50).

° Formerly, Department of Oceanography, Oregon
State University; present address: Biology Depart-
ment, State University of New York, Farmingdale, N.Y.
11735.

' Department of Oceanography, Oregon State Uni-
versity, Corvallis, Oreg. 97331.

growth and life history of E. pacifica are lim-
ited. Nemoto (1957) presented some growth
data for E. pacifica from the Japanese-Aleutian
area. Ponomareva (1963), in her study on the
distribution and ecology of euphausiids of the
North Pacific, estimated the growth of E. po/-
cifica from plankton samples collected during
the winter and spring. Lasker (1966) deter-
mined the growth of E. pacifica reared in the
laboratory. Preliminary growth rates of E. pa-
cifica based on some of our data were also pre-
sented by Small (1967).

Because growth rates are needed to under-
stand the ecology and energetics of a species,
we undertook this study on the abundance, size
structure, and growth rate of E. pacifica off
Oregon.

COLLECTION METHODS

We made a total of 174 collections using 1-m
mouth diameter plankton nets between June
1963 and July 1967 at stations located 15, 25, 45,
and 65 miles off Newport, Oreg. In addition, 25
collections were obtained from stations 85-285
miles off Newport. These provided samples of
E. pacifica for all seasons of the year over a
4-year period. Nets had 0.57 1-mm mesh open-
ings and were used with a flowmeter placed in

Manuscript received September 1970.

FISHERY BULLETIN: VOL. 69, NO. I, 1971.

79

FISHERY BULLETIN: VOL. 69. NO. 1

the mouth to measure the amount of water filt-
ered.

The first 20 samples were from oblique tows,
and the other 154 were from vertical tows. This
change to vertical tows was made to ensure equal
sampling at all depths throughout a tow. Com-
parison of the catches of several oblique and
vertical tows taken during the same night indi-
cated little difference in the number and size
of E. pacifica per unit volume filtei'ed.

Because euphausiids may avoid nets in the
daytime, all tows were taken during nighttime
when visual avoidance would be minimal (Brint-
on, 1967) . This is also a period when E. pacifica
presumably has migrated into the upper 100 m
of the water column. E. pacifica captured in
several 6-ft Isaacs-Kidd midwater trawls were
measured to see if large eui:)hausiids that were
possibly avoiding the small vertical meter net
could be captured. There was no indication that
the maximum size of trawl-caught was larger
than meter net-caught euphausiids.

The maximum depth of our tows was usually
200 m. Because Ponomareva (1963) suggested
that E. pacifica adults inhabit the 200-500-m
layer in their second winter and no longer mi-
grate daily to the surface, tows were taken to
1000 m with both the midwater trawls and
vertical meter nets. These deeper tows, how-
ever, did not contain any larger animals. Twelve
vertical meter net samples from de])ths of 200
m or 1000 m to the surface did not show appre-
ciable differences in size structure. Therefore,
we assumed that a representative sample of the
E. pacifica population was caught in the upiier
200 m at night.

The entire plankton sample was preserved at
sea in neutralized 10 'r Formalin. In the lab-
oratory ashore, all euphausiids were removed
from each sample unless the number of euphau-
siids was large (more than 200 individuals).
In such cases the samj^le was usually divided
in half with a Folsom plankton splitter (Mc-
Ewen, Johnson, and Folsom, 1954), and euphau-
siids were sorted from only one-half the sample.
Males and females were not differentiated.

The length of each individual E. pacifica was
measured to the nearest 0.1 mm from behind

the eye to the posterior margin of the carapace,
and each animal was then assigned to a 0.3-mm
size-group. Total lengths (from the posterior
of the eye to the tip of the telson) were also
measured from randomly selected individuals
of various lengths to enable comparisons of our
data with those of others. A least squares fit
of 146 comparisons gave the equation:

Y = 2.54 X + 0.66

where Y = total length and X = carapace
length. The variance was 248.19. Our measure-
ments are all given as total lengths.

RESULTS
RECRUITMENT AND ABUNDANCE

Although larval E. pacifica occurred during
almost all months of the year, definite trends
in abundance were evident over the 4-year per-
iod ( Fig. 1 ) . Larvae were usually most abun-
dant between October and December. During
some years recruitment began as early as June
and was also prominent in the summer months.
No major concentrations of larvae were found
during winter or spring.

These larval forms of E. pacifica were f urcilia
of about 7 mm or less, agreeing with Boden's
(1950) size measurements and description of E.
pacifica furcilia. Furcilia are found 16-18 days
after spawning, usually within the upper 100 m
of the water column (Ponomareva, 1963; Brint-
on, 1967).

Catch curves (Fig. 2) show the average num-
ber of different size-groups of E. pacifica col-
lected during the entire study. All sizes of E.
imcifica were much more abundant i)er m^ in-
shore over the continental shelf than in oceanic
offshore waters. Individuals larger than 15 mm
were rare at station 65 miles or farther offshore.
Our finding that larvae were less abundant at
offshore than inshore stations agrees with
Brinton (1962b), who also noted that E. pa-
cifica was more abundant inshore than oflFshore
of California. Thus, despite the wide oceanic
distribution of E. pacifica, the density of near-

80

SMILES and PEARCV : GROWTH RATE OF Eufhauna farifia

4000
3000
2000
1000

O 3000-
5 2000-
(t 1000

g 3000

2000

1000

0

1000

I I I I I I I I I I I I I I I I I

NH-15

I I I I I I I I I I I I I I I I I I I I I I I H I I I I I I I

10 o

o oi— I oHo OOP

OOP

SlSL

Us)
13.900

NH-25

o|— 10 0_0

NH-45

X\

r— lO I — I Q I — IQ Q

□

Q 0

.J3.

TO Q^

27000

_Q ^-~0 L.

n

Ql IQ 0.

■ Or- lO O-

n^

1963

1964

oelUl |io| |i2| loil |04| ioeTloal fio] |i2 |o2| M W H MoMi^ lo^lW W M lio| jiF |oi| H M

1965

pa] [iol [IF |o2| |o4|
1966 1967

Figure 1. — Number of furcilia of E. pacifica collected at four stations off Newport, Oregon (NH-15, 25, 45, 65)
during 1963-67. "0" indicates no sample taken for that month.

• INSHORE {NH-15, NH-25)

■ ALL STATIONS

▲ OFFSHORE (NH-65. NH-> 65)

TOTAL LENGTH (mm)

Figure 2. — Catch curves : the logarithm of the average
number of various sizes of E. pacifica caught per lO'^ m'^
for all samples during the study.

shore populations may be considerably higher

than offshore populations in the same region.

Although inshore tows were generally made

only to 50 m and 130 m at the 15- and 25-mile
stations respectively because of depth of water,
euphausiid abundance at these stations was ap-
proximately 10 times greater than at offshore
stations. This difference is too great to be ex-
plained by the differences in sampling depths
even assuming that all euphausiids were con-
centrated in the upper 50 m at night.

GROWTH RATE

The extended spawning season and variability
of catches of E. pacifica made interpretation of
growth difficult. Three related methods, all
based on progressions of size-frequency histo-
grams, generally gave similar growth rates
(Table 1) and led to the same conclusion: E.
pacifica lives for a period of about 1 year and
attains a maximum size of about 22-24 mm total
length. We tenuously assumed for all these
analyses that we sampled the same population,
or populations with similar age structures and
growth rates.

Two illustrations of growth based on monthly

81

FISHERY BULLETIN; VOL. 69. NO. 1

Table 1. — Summary of average growth rate estimated
from the progression of modes or means (see Figs. 3
and 4).

Year
class

Recruitmenf
month

Number
monHis
followed

Growth rotes

Modes

(Fig- 3 for

1965 and 1966

year classes)

Modes
(Fig. 4)

Mm/month

1963

09

10

1.6

1.9

1.6

1964

10

9

2.0

2.0

1.9

1965

10

8

2.1

2.2

2.0

1966

11

5

2.9

2.S

2.4

1967

03

3

2.6

2.5

2.5

size-fre(iuency histograms of all stations com-
bined (Fig. 3) illustrate the increasing modal
lengths between December and June for the 1965
and 1966 year classes. Recruitment of small
E. pacifica is also obvious during the spring of
1966 and 1967 and also shows a shift in modes
with time. The 1963 and 1964 year classes (not
shown here) showed similar trends.

A modified histogram plot (Fig. 4) was used
to show the data for all 4 years and all 4 stations
together. The advantage of this method is that
one can follow the main modes of different sizes
throughout the 4-year period. A disadvantage
is that these plots are distorted by the arbitrary
constraints that (1) at least 50 individuals per
103 m3 of water within one size-group had to
be present for plotting and (2) concentrations
above 5000/103 m3 were plotted only as 5000/
103 m3. All of the years represented in Figure
4 show some similarity. The main recruitment
pulses are in the fall and summer, and the max-
imum size attained is approximately 22-24 mm
length. After about 1 year, late in the second
summer or fall, these large individuals dis-
appeared from our collections. Interestingly,
many of the modes that were composed of small
euphausiids during the spring and early summer
disappeared or were undiscernible by the fall.
Either these individuals were subjected to high-
er mortality than the fall recruits or were trans-
ported out of the area. Apparently they made
no major contribution to the local adult popu-
lation.

Average lengths of size modes were also
calculated for each collection using the com-
puter techniques described by Hasselblad
(1966). The means were generally close to

the values for the modal lengths of various col-
lections shown in Figures 3 and 4 and, therefore,
are not illustrated here but are given in Table 1.

Our estimates of the growth of E. pacifica
by all these methods are summarized in Table 1.
As expected, estimates are similar for the same
year classes. Growth varied from 1.6 to 2.9 mm
per month among year classes, averaging about
2.0 mm per month. Growth rates were fastest
for young stages. Year-classes 1963 and 1964
had slower average rates (1.6 and 2.0 mm/
month) and were calculated over a longer period.
Year-classes 1966 and 1967, on the other hand,
were represented for the shortest periods of time
and had the fastest average rates (2.9 and 2.6
mm month) . This deceleration of growth at the
larger sizes is also apparent in Figure 3 where
the growth rate from January to March 1966
was about 3.2 mm/month, while from March
to June it was about 2.0 mm/month.

Our estimates are biased in several ways.
They favored the recruitment pulses of the fall
because the smaller modes of young that ap-
peared earlier (June through September) did
not comprise a good series of modal sequences.
Moreover, the modes and means of the smaller
sizes of E. pacifica are probably slightly over-
estimated since catch curves (Fig. 2) indicate
escapement from our nets of individuals below 6
mm. This may cause an underestimation of
growth rates.

DISCUSSION

Generalized growth curves of E. pacifica for
three regions of the North Pacific are con-
trasted in Figure 5. On the basis of bimodal
size-frequency distributions of winter and
spring samples, Ponomai-eva (1963) concluded
that E. pacifica lives for a period of 2 years.
She found predominantly 8 and 14-15 mm indi-
viduals in the winter and 12-13 mm (her 1-
yearolds) and 19 mm (2-year olds) in the spring.
Off Oregon not only were 12-13 mm individuals
rare or absent in sirring samples, but also 13-14
mm individuals, the size that Ponomareva would
expect to find in the summer and fall, were ab-
sent. Moreover, our data, unlike Ponomareva's,
show no large seasonal fluctuations of growth
with retarded growth of the 13-14 mm sizes

82

SMILES and PEARCY: GROWTH RATE OF Euphamia padfica

3S00-

20CX)-

1000-

400-

100-

10-

0-^

I I I I I I I I I I I I I I I I I

OCTOBER 1965 _

\m\^

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

NOVEMBER 1966

mn

3500-

NOVEMBER 1965

n rfT}n->-. r^ rn 1^

- J~

'-. DECEMBER 1966 _

3500-

Id

DECEMBER 1965 _ _

\im.

3500-

I

§
I

JANUARY 1966 _ _

rniiiirrrh

E im^

FEBRUARY 1967 _

~h-h-r-i

3500-

0-
3500-

FEBRUARY 1966

rfTTrmrrm

MARCH 1967

"hrhm rrTil il>n

0
3500-

MARCH 1966

APRIL 1967

TffHi m I ITTti n F

0-
3500-

APRIL 1966

On

MAY 1967

THth F =HTlTTTT^>rTTTnn

JUNE 1966

rmiinmTn

— — _ — — Cg(\J(sj

I I I I I i I I I T IT

tf>O)Or>Jrnio^<0ooO0)OO

(\J (NJ OJ

TOTAL LENGTH (mm)

Figure 3. — Size frequency distributions of E. pacifica from all stations for the 1965 year class (left) and the

1966 year class (right).

83

FISHERY BULLETIN: VOL. 69, NO. 1

361 |0e| 1 10 1 |I2| b2| M |06| |08| 1 10 1 ||2| |02| |04| |06|

1963 ' 1964 ' 1965

1966

Toil lo4l bel
1967

Figure 4. — Size frequency histograms for all stations, 1963-67. Dashed lines are an estimate of average
growth of individual year classes. "0" indicates no samples for that month.

22
20

^'^
§ 12

-J 8
6

2
0

S

OUR
RESULTS

OUR
RESULTS

>'l I I I I I.I I I I I I M I I I I I I I I I I

6 8 10 12 2 4 6 8 10 12 2 4 6 8 10

I MONTHS I

Figure 5. — Comparison of generalized growth curves
of E. pacifica.

in the summer and fall. Nemoto (1957 and per-
sonal communication) believes that E. pacifica
grows rapidly, reaching a length of 17-18 mm
after 1 year. Many individuals spawn after 1
year and then may continue to live for another
year, reaching a maximum of 22 mm after 2
years. We find no convincing evidence, how-

ever, for continuation of large adults through a
second year. Large euphausiids disappeared
from our samples by the winter (Fig. 4).

Thus our results indicate a faster growth rate
and shorter life cycle than those of Ponomareva
and Nemoto for the northwestern Pacific but a
similar maximum size. Our growth rates off
Oregon averaged 0.065 mm/day for the entire
life span, about twice those for the other field
studies of E. pacifica. Maximum rates for rap-
idly growing juveniles were 0.095 mm /day.
These rates are higher than Lasker's (1966)
maximum rates for juvenile E. pacifica reared
in the laboratory, suggesting that growth in
nature may exceed "optimal" conditions in the
laboratory.

Although our estimates of the growth of E.
pacifica are higher than previousl.v reported,
they approximate the estimates for .sevei'a! other
species of euphausiids. A length of about 22 mm
after 1 year was also found by Mauchline ( 1966)
for Thysanoessa raschii; by Ruud (1936),
Mauchline (1960), and Einarsson (1945) for
Meganyctiphanes norvegica; by Einarsson
(1945) for Thysanopoda aciitifrons; by Ruud

84

SMILES and PEARC\- : GROWTH RATE OF Eupham,a pa„fica

(1932), Bargmann (1945), and Marr (1962)
for Euphausia superba; and by Baker (1959)
for Enphau^ia triacantha. Most of these species
have a maximum life expectancy of 2 years,
reproduce each year, and grow slowly during
the winter. Other species are known to have
a life expectancy of 1 year (Mauchline and
Fisher, 1969).

Development, growth, and sexual maturity of
the same species of euphausiid are known to
vary among geographic iropulations (Einarsson,
1945; Nemoto, 1957; Ponomareva, 1963;
Mauchline and Fisher, 1969). Mauchline and
Fisher (1969) stress that this variability is
probably directly related to differences in food
and temperature. Hence, the rapid growth of
E. pacifica off Oregon may be related to the high
productivity of the region and the lack of large
seasonal temperature fluctuations in nearshore
waters.

Small, Curl, and Glooschenko' report high
values for primary productivity in the coastal
waters off Oregon. Curl and Small' found that
standing stocks of chlorophyll-n averaged high-
est inshore and steadily decreased offshore.
High production and stocks persist through the
summer, the upwelling season, in inshore waters,
whereas offshore waters have a tyijical summer
productivity minimum (Anderson, 1964). Note
that those seasonal and inshore-offshore gradi-
ents in phytoplankton are correlated in time and
place with the spawning of E. pacifica off Ore-
gon, mostly inshore and protracted over the
summer and fall months. Ponomareva (196?.)
believes that phytoplankton is not only im-
portant as food for euphausiid larvae, but also
may be necessary in the diet for development
of reproductive products of E. pacifica.

Water temperatures along the Oregon coast
are fairly uniform throughout the year and lack
the extremes found along the eastern coasts of
continents at similar latitudes. Advection of
cool water to the surface (upwelling) during
the summer and warm water toward shore dur-

* L. F. Small, H. Curl, Jr., and W. A. Glooschenko.
Seasonal primary production in a region of upwelling.
III. Effects of solar radiation and upwelling on daily
production. Unpublished MS.

^ H. Curl, Jr., and L. F. Small. MS.

ing the winter moderates the usual seasonal
variations. Pattullo, Burt, and Kulm (1969)
observed that the seasonal range of heat con-
tent was twice as large offshore as inshore (with-
in 65 miles) of the Oregon coast. The absence
of severe winter temperatures may help to ex-
plain the rapid growth of E. pacifica through-
out the year off Oregon. Conversely the slow
and seasonally variable growth of E. pacifica
found by Ponomareva (1963) was in the Far
Eastern Seas of Asia where temperatures are
often lower and where thermal variations are
greater. The fact that E. pacifica is the only
widespread euphausiid that spawns in the sum-
mer, when the phytoplankton bloom was almost
over, indicates that this boreal species may be
poorly adapted to the cold marginal Far Eastern
Seas (Ponomareva, 1963).

The main pulses of larvae, hence spawning,
of E. pacifica were in the fall, and not in the
spring and summer as found by Ponomareva
(1963), Nemoto (1957) off Japan, and Barham
(1957) in Monterey Bay, Calif. Brinton (per-
sonal communication) notes larval recruitment
throughout the year off Southern California.
The later spawning off Oregon, like the rapid
growth, may again be related to the prolonged
production cycle caused by upwelling off Oregon
and the moderate fall and winter water temper-
atures.

ACKNOWLEDGMENTS

We are grateful to J. Mauchline for his sug-
gestions and to T. Nemoto for providing his
growth curve for E. pacifica.

LITERATURE CITED

Anderson, George C.

1964. The seasonal and geographic distribution of
primary productivity off the Washington and
Oregon coasts. Limnol. Oceanogr. 9(3) : 284-302.
Baker, A. de C.

1959. The distribution and life history of Euphaus-
ia triacantha Holt and Tatersall. Discovery Rep
29: 309-340.
Bargmann, Helens E.

194.5. The development and life-history of ado-
lescent and adult krill, Euphausia superba. Dis-
covery Rep. 23: 10,3-176.

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Barham, Eric George.

1957. The ecology of sonic scattering layers in
the Monterey Bay area, California. Ph.D. Thesis,
Stanford Univ. 192 p. Univ. Microfilms, Ann
Arbor, Mich. Publ. 21, 564.
BoDEN, Brian P.

1950. The post-naupliar stages of the crustacean
Euphausia pacifica. Trans. Amer. Microsc. Sec.
69(4) : 373-386.
Brinton, Edward.

1962a. The distribution of Pacific euphausiids.
Bull. Scripps Inst. Oceanogr. Univ. Calif. 8(12) :
51-270.
1962b. Variable factors affecting the apparent
range and estimated concentrations of euphausiids
in the North Pacific. Pac. Sci. 16(4) : 374-408.
1967. Vertical migration and avoidance capability
of euphausiids in the California Current. Limnol.
Oceanogr. 12(3): 451-483.
EiNARSsoN, Hermann.

1945. Euphausiacea. 1. North Atlantic species.
Dana Rep. Carlsberg Found. 27, 1-185.
Hasselblad, Victor.

1966. Estimation of parameters for a mixture of
normal distributions. Technometrics 8(8) : 431-
444.
Hebard, J. F.

1966. Distribution of Euphausiacea and Copepoda
off Oregon in relation to oceanic conditions. Ph.D.
Thesis, Oregon State Univ., Corvallis. 85 p.

Ito, Jun.

1964. Food and feeding habit of Pacific salmon
(genus Oncorhynchits) in their oceanic life. Bull.
Hokkaido Reg. Fish. Lab. 29: 85-97.
Komaki, Yuzo.

1967. On the surface swarming of euphausiid
crustaceans. Pac. Sci. 21(4): 433-448.

Lasker, Reuben.

1966. Feeding, growth, respiration, and carbon
utilization of a euphausiid crustacean. J. Fish.
Res. Bd. Can. 23(9) : 1291-1317.
Marr, James.

1962. The natural history and geography of the
Antarctic krill {Euphausia superba Dana). Dis-
covery Rep. 32: 33-464.
Mauchline, J.

1960. The biology of the euphausiid crustacean,
Meganyctiphaves norvegica (M. Sars). Proc.
Roy. Soc. Edinburgh, Sect. B. (Biol.) 67: 141-179.
1966. The biology of Thysanoesaa raschii (M.
Sars), with a comparison of its diet with that of
Meganyctiphanes norvegica (M. Sars). 7n Harold
Barnes (editor), Some contemporary studies in
marine science, p. 493-510. George Allen and
Unwin Ltd., London.
Mauchline, John, and Leonard R. Fisher.

1969. The biology of euphausiids. In Frederick S.
Russell and Maurice Yonge (editors), Advances
in marine biology. Vol. 7, 454 p.

McEwEN, G. F., M. W. Johnson, and Th. R. Folsom.

1954. A statistical analysis of performance of the

Folsom plankton sample splitter, based on test

observations. Arch. Meteorol. Geophys. Bioklima-

tol., Ser. A. 7: 502-527.

Nemoto, Takahisa.

1957. Foods of baleen whales in the northern Pa-
cific. Sci. Rep. Whales Res. Inst. 12: 33-90.
1959. Food of baleen whales with reference to
whale movements. Sci. Rep. Whales Res. Inst.
14: 149-290.
Osterberg, Charles, William Pearcy, and Norman
Kujala.

1964. Gamma emitters in a fin whale. Nature
(London) 204(4962): 1006-1007.
Pattullo, June G., Wayne V. Burt, and Sally A.

KULM.

1969. Oceanic heat content off Oregon: Its vari-
ations and their causes. Limnol. Oceanogr. 14 (2) :
279-287.

Pearcy, William G.

1970. Vertical migration of the ocean shrimp,
Pa7idalus jordani: A feeding and dispersal mech-
anism. Calif. Fish Game 56(2): 125-129.

Pearcy, William G., and Charles L. Osterberg.

1967. Depth, diel, seasonal, and geographic vari-
ations in zinc-65 of niidwater animals of Oregon.
Int. J. Oceanol. Limnol. 1(2): 103-116.
Pereyra, Walter T., William G. Pearcy, and Forrest
E. Carxtiy', Jr.

1969. Sebastodes flai'idus, a shelf rockfish feeding
on mesopelagic fauna, with consideration of the
ecological implications. J. Fish. Res. Bd. Can.
26(8) : 2211-2215.

Ponomareva, Larisa Natal'evna.

1963. Euphausiids of the North Pacific, their dis-
tribution and ecology. Akad. Nauk SSSR Inst.
Okeanol. (Translated by Israel Program for Sci-
entific Translations, Jerusalem 1966, IPST cat-
alog no. 1368, 154 p.)

Renfro, William C, and William G. Pearcy.

1966. Food and feeding apparatus of two pelagic
shrimps. J. Fish. Res. Bd. Can. 23(12): 1971-
1975.

Ruur, John T.

1932. On the biology of southern Euphausiidae.

Hvalradets Skr. 2. 105 p.
1936. Euphausiacea. Rep. Dan. Oceanogr. Exped.
1908-1910 Mediter. Adjacent Seas 2D6(Biol.),
86 p.
Small, Lawrence F.

1967. Energy flow in Euphausia pacifica. Nature
(London) 215(5400): 515-516.

Tyi-er, H. R., Jr.

1970. The feeding habits of three species of lant-
emfishes (Myctophidae) off Central Oregon.
Master's Thesis, Oregon State Univ., Corvallis.
64 p.

86

ESTIMATING PHYTOPLANKTON PRODUCTION FROM AMMONIUM
AND CHLOROPHYLL CONCENTRATIONS IN NUTRIENT-POOR
WATER OF THE EASTERN TROPICAL PACIFIC OCEAN"°

William H. Thomas" and Robert W. Owen, Jr.*

ABSTRACT

Previous work has shown that nitrogen is the limiting nutrient in poor (nitrate-free) water in the
eastern tropical Pacific Ocean and has suggested that ammonium is the principal nitrogen source for
phytoplankton in this water. Enrichment and uptake experiments with various concentrations of
ammonium have provided values for the half-saturation constant, Kg, and the maximum growth rate,
/i^ax' which can be used to calculate actual growth rates with the hyperbolic model relating growth
rate to limiting nutrient concentration. At two stations, growth rates calculated from ammonium con-
centration agreed well with those calculated from chlorophyll and 14c production, and the hyperbolic
equation could be combined with that using production and chlorophyll to calculate production alone.
In this paper calculated production rates are compared with those observed from 14c uptake mea-
surements for a number of EASTROPAC cruises. The regression between calculated production and
observed production is highly significant and the slope is close to 1.0, indicating reasonable agreement,
particularly when all of the errors in the calculation, especially in Ks, are considered. The results
suggest rather close control of phytoplankton production by the limiting nutrient, ammonium, in these
near-surface, nutrient-poor waters.

This paper describes how concentrations of a
limiting nutrient in sea water and some mea-
sure of the standing crop of phytoplankton can
be used to estimate phytoplankton production.
Estimated production is compared with observed
i'*C production, and the two sets of values are
shown to agree reasonably well when all the
errors in the estimation are considered.

The EASTROPAC Expedition series has de-
lineated particularly well areas that are rich in
nutrients and that are nutrient-poor in the
eastern tropical Pacific Ocean. Rich areas in-

' Contribution from the Scripps Institution of Ocean-
ography.

" This work was part of the research of the STOR
(Scripps Tuna Oceanography Research) Program. It
is also a result of the EASTROPAC Expedition, a co-
operative study of the biological, chemical, and physical
oceanography of the eastern tropical Pacific Ocean. The
work was supported by National Science Foundation
Grant No. GB-8618 to the senior author and by contracts
#14-17-0007-963 and #14-17-0007-989 between the Bu-
reau of Commercial Fisheries (now the National Marine
Fisheries Service) and the Institute of Marine Resources.

' Institute of Marine Resources^ Scripps Institution of
Oceanography, University of California, San Diego, La
Jolla, Calif. 92037.

* National Marine Fisheries Service Fishery-Ocean-
ography Center, La Jolla, Calif. 92087.

Manuscript received September 1970.

FISHERY BULLETIN: VOL 69, NO. I, 1971.

elude the Peru Current, the Costa Rica Dome,
and an area of equatorial upwelling extending
across the EASTROPAC area (from the Amer-
ican coast to long 119° W). Poor areas lie to
the north and south of the equatorial upwelling
zone and to the west of the Peru Current and
Costa Rica Dome. Rich and poor near-surface
waters were mapped in previous papers (Thom-
as, 1969, 1970b) and will be shown in detail
in the EASTROPAC Atlas (Thomas, unpub-
lished data) . Nutrient values for rich and poor
water are also given in Table 1 of Thomas
(1970a).

Corresponding areal and seasonal changes in
the phytoplankton production in this region have
been observed and attributed in part to mecha-
nisms of nutrient supply (Owen and Zeitzschel,
1970). No accounting has been possible, how-
ever, for the variations observed within the
nutrient-poor surface layer of the region.

Near-surface water in poor areas is especially
low in nitrate-nitrogen; this nutrient is gener-
ally not detectable (<0.1 /ng-at./liter). Ammo-
nium-N is present in concentrations ranging up
to 1 /ng-at./liter and organic nitrogen can reach

87

FISHERY BULLETIN: VOL. 69, NO. 1

concentrations of 17 /.ig-at. /liter, but this latter
nitrogen source is probably not utilized by phy-
toplankton (Thomas, Renger, and Dodson,
in press).

Prior to EASTROPAC (pre-1967) low ni-
trate/phosphate ratios in tropical Pacific poor
water suggested that nitrogen was a limiting
nutrient although ratios were increased when
ammonium was included along with nitrate, and
it was suggested that this latter nutrient alle-
viated N deficiency (Thomas, 1966).

Recent EASTROPAC enrichment experi-
ments provided direct evidence for N limitation.
Phytoplankton growth occurred in experiments
where nutrients were added singly to sea water
samples only with N addition, and if N was de-
leted from an otherwise complete enrichment,
little or no growth resulted (Thomas, 1969,
1970b). The fact that photosynthetic assimi-
lation ratios were only slightly (but signifi-
cantly) decreased in poor water as compared
with rich water testified further to the allevi-
ation and control of deficiency by ammonium
(Thomas, 1970a).

Having established which nutrient is com-
monly limiting, one can use a quantitative nu-
trient requirement in an appropriate math-
ematical model to estimate growth rates (pro-
duction) from concentration of the limiting nu-
trient. Recent work (Caperon, 1967; Dugdale,
1967) indicates that the best model is hyperbolic:

(1)

K, + S
where /j. is the phytoplankton specific growth

rate, Mj

is the maximum rate which is un-

limited by low nutrient concentration, S is a
measured limiting nutrient concentration in sea

water, and Kg is the "half-saturation constant"
— a nutrient concentration that supports a rate
equal to /:tma.x/2. This equation is equivalent
to the Michaelis-Menton formulation for enzyme
kinetics and was first applied to bacterial growth
rates by Monod (1942). Many biological pro-
cesses follow the hyperbolic model and since
growth is the result of a series of coupled en-
zymatic reactions, the hyperbolic model is the
model of choice.

A previous paper (Thomas, 1970b) provides
information on /umax and Kg (for ammonium)
from which /i can be calculated. To obtain these
values we enriched samples of nutrient-poor Pa-
cific sea water from a depth of 10 m with a com-
plete mixture of non-nitrogenous nutrients to
which various concentrations of ammonium
were added. The samples were then incubated
in natural light approximating the intensity that
would be found at 10 m depth. Growth was es-
timated by successive daily measurements of
in vivo chlorophyll (Lorenzen, 1966) in each
treatment, and rates integrated over a daily peri-
od were calculated from the maximum increases
in chlorophyll. These rates were plotted against
ammonium concentrations to fit a hyperbolic
model and values of A',, and /xmax were obtained
from the plot. These values and their 95% con-
fidence limits are given in Table 1 for two such
experiments. Kg values can also be determined
from uptake experiments since recent work has
shown that A'., values for growth and uptake
are equivalent (Eppley and Thomas, 1969).
Also included in Table 1 are uptake Kg values
obtained by Maclsaac and Dugdale (1969) for
nutrient-poor tropical Pacific water. Their val-
ues for Vniax. the maximum uptake rate, are
not equivalent to /imax ^'id thus are not included

Table 1. — Rate parameters for growth and uptake on ammonium in nutrient-poor tropical Pacific sea water.

Cruise

Station

ilM)

95 percent
limits

''max

95 percent
limits

(Doublings/day)

EASTROPAC 76

007

1.68

± 3.28

1.12

± 0.83

Thomos (1970b)

EASTROPAC 76

173

1.47

i: 0.91

1.22

± 0.27

Thomas (1970b)

Thompson 26

IS

0.10

--

-

-

Maclsoac and
Dugdale (1969)

Thompson 26

3«

0.5S

-

~

~

Maclsoac and
Dugdale (1969)

Te Vega 13

651.a

0.62

~

—

~

Maclsaac and
Dugdola (1969)

Meon volues

0.88

1.17

95 % limits of mean

1.33

O.U

88

THOMAS and OWEN; ESTIMATING PHVTOPLANKTON PRODUCTION

in Table 1. It will be noted that confidence lim-
its for Ks values in given experiments are large
as is the confidence limit for the mean of all five
values which is used in subsequent calculations
(see Results and Discussion). This can be at-
tributed to lack of precision in measuring either
growth or uptake; even in controlled experi-
ments with laboratory cultures, A'., values are
imprecise (Eppley, Rogers, and McCarthy,
1969; Eppley and Thomas, 1969).

The integrated daily growth rate, fi, can also
be calculated from ^^C production estimates and
chlorophyll concentrations using the following
equation:

3'.32 [log,o(/? • chl + Prod ) - logio(/? • chl)]

^ =

1 day

(2)

as has been done for laboratory cultures by
Thomas (1964) and McAllister, Shah, and
Strickland (1964). In this equation R is the
carbon/chlorophyll ratio; R ■ chl thus is the
standing stock of phytoplankton carbon. The
constant 3.32 converts logarithms to the base 10
to logarithms to the base 2 and allows /x. to be
expressed as doublings of phytoplankton carbon
per day.

In the previous paper (Thomas, 1970b), ^
calculated from ammonium (equation 1) was
compared with /j, calculated from l^c production
and chlorophyll (equation 2) for the two EAS-
TROPAC stations where Ksand /^max were de-
termined from enrichment experiments. At
station 76.007, /x calculated from ammonium was
0.385 doublings/day while that calculated from
•^■^C uptake and chlorophyll was 0.365 doublings/
day. At station 76.173 both values were iden-
tical— 0.276 doublings/day. For the calcula-
tion we used an R value of 98, that found by
Eppley (1968) for nitrate-free water off La
Jolla.

This excellent agreement suggested that we
could set equation (1) equal to equation (2) and
solve for production as a function of ammonium
and chlorophyll using A's and fimax ^s constants.
The new equation thus derived is /q\

Prod = chl •

R antilog[^max
L \3.32

3.32 Ks+ S

1

This expression allows a direct comparison cal-
culated and measured ^'*C production (see Re-
sults and Discussion).

METHODS

Methods for determining A's and ^ma.x were
given previously (Thomas, 1970b; Maclsaac
and Dugdale, 1969) — see also the previous sec-
tion. Chlorophyll and production samples were
taken from the depth of the 50 % light level,
which was always in the upper mixed layer
and varied from 9 to 16 m. This depth was
determined by multiplying the depth at which
the Secchi disc disappeared by 0.38. This
factor employs the assumption that the Secchi
disc disappears at 16 % of surface light in-
tensity (Strickland, 1958).

Chlorophyll was determined in these samples
by filtration on glass fiber filters, followed by
90 % acetone extraction of the filters, and mea-
surement of fluorescence of the extract ( Yentsch
and Menzel, 1963; Holm-Hansen, Lorenzen,
Holmes, and Strickland, 1965) using equations
developed by Lorenzen (1966).

Simulated in s'itw production was measured
by adding 20 ^c Na^^'^COs solution to the
samples (Steemann Nielsen, 1952) and incu-
bating them in a tubular shipboard incubator
space in which natural light intensity was at-
tenuated to 50 % of that incident. Incubation
was started at noon and continued until sunset
at sea surface temperature. Following incuba-
tion the samples were filtered through HA Mil-
lipore®' filters and their radioactivity assayed
ashore by G-M counting of the filters. The l^c
solution was standardized by liquid scintillation
counting and the efficiency of the G-M counter
for these filters was determined by combusting
some of these and measuring the evolved ^^C02
with an ionization chamber. Daily uptake was
determined by multiplying the activity by 2;
we also corrected for the isotope effect by mul-
tiplying by 1.05. Darkened samples were incu-
bated with illuminated samples and dark uptake
was subtracted from light uptake. No cor-

° The use of trade names is merely to facilitate de-
scriptions: no endorsement is implied.

89

FISHERY BULLETIN: VOL. 69, NO. I

rections for respiration by phytoplankton were
made.

Ammonium was measured ashore in frozen
samples from a depth of 10 m by the method of
Richards and Kletsch (1964). Some labile
amino-N which is probably available to phyto-
plankton is measured along with ammonium by
this method.

RESULTS AND DISCUSSION

For the comparison of calculated and mea-
sured ^''C production, we have used samples

from 10 m incubated at light intensities approx-
imating those at 10 m to determine Ks and fimax.
and actual ^^C values from the 50% light level.
We did this so that light intensities would not
be a factor in the comparison — that is, light
was presumed to be at saturating intensities
but not inhibitory, which would be the case if
surface samples had been incubated in the
growth experiments and compared with surface
production.

Ammonium was not determined at all pro-
duction stations, and we selected those pro-
duction values where data were available for

/ /

/ /

/ /

-

Calcu

loted Prod. = 1.057 (Observed Prod.)^ / /

^~7 /

10

/ /

/ y
/ '''
/ /

■

/ ^
y /

/ / m

/ /

•

X /
/ /

"

/ y

•

/^

5

—

•
•

•
• •

/ /

•

//

• • .

//

•

'/

• * /

• //•

•

.

• • • • /^

•
• •

•
• •

//

•

•

• /y

*• A

-

•

•

•

•
— 1 — i — 1 —

1 , , , , 1 .

OBSERVED '*C PRODUCTION {Mg C/m'/Day)

10

Figure 1. — Phytoplankton production calculated from ammonia and chlorophyll con-
centrations at 10 m compared with simulated in situ ^^C production at the 50 7o light
level in northerly nutrient-poor water in the eastern tropical Pacific Ocean. The dashed
line is the regression that would be expected if agreement between the two sets of pro-
duction values were perfect.

90

THOMAS and OWEN : ESTIMATING PHYTOPLANKTON PRODUCTION

ammonium and where nitrate was undetectable.
One hundred and five such production stations
were available from 10 EASTROPAC cruises
in this nutrient-poor water.

Production calculated from equation 3 is com-
pared with measured ^*C production in Figure
1. There is a highly significant (P<.01) rela-
tionship between the two sets of values. The
slope of the regression line is 1.057, which is
very near to the value 1.0 which would be ex-
pected if agreement were perfect. Nevertheless,
there is a large amount of scatter in the values
of Figure 1; that is, the calculation overesti-
mates in some cases and underestimates in
others.

Table 2. — Errors in the calculation of production.

Parameter

Standard errors

Reference

Chlorophyll

± 12%

Holmes, Schaefer, and
Shimada (1958)

R

± 17%

Eppley (1968)

± 6%

Table 1 (this paper)

S

± 5%

Richards and Kletsch (1964)

K,

± 76%

Table 1 (this paper)

Total

± 79%

95% confidence limits

± 152%

Errors in the values used in the calculation
are given in Table 2. To figure total error these
have been converted to variances and summed.
The 95% confidence limit shows that any cal-
culated production value can vary by ± 1.5 fold.
Thus, one would expect quite a large scatter in
Figure 1.

Most of the error is in Ks. When only the
Ks values of Thomas (1970b) are used the cal-
culation generally underestimates the observed
•''*C production. Use of the mean of the Ks
values of Maclsaac and Dugdale (1969) results
in an overestimation. Since there is no reason
to doubt either set of Kg values, we have used
the overall mean Kg from Table 1. In applying
this method to any other nutrient-limited waters,
it would be well to obtain several values of Kg
so that the error due to lack of precision in
measuring Kg can be recognized.

Part of the scatter in Figure 1 may also be
due to the fact that the parameter Kg is species
— and temperature — dependent (Eppley, Ro-
gers, and McCarthy, 1969) and that variations
in species composition of the crop or slight var-

iations in temperature may have affected the
calculation. The parameters ^max and R are
also probably dependent upon the species com-
position of the crop and on temperature. Be-
cause of these factors, which are unknown, it
is perhaps surprising that the relationship be-
tween calculated and observed production is so
good when constant values of Kg, ^ma.x.and R are
used.

This evidence supports the hypothesis that
phytoplankton production in the upper mixed
layer is controlled by the limiting nutrient,
ammonium, and shows that the hyperbolic model
describes this control very well. In this latter
connection it should be noted that if a linear
model having a term "S/Smax" in equation 3
(where Smax is that concentration supporting
a maximum growth rate and which has a value
near 10.0 ^M from the data of Thomas, 1970b)
is used rather than the term "S/ (Kg + S),"
the calculation very much underestimates the
^^C production. The linear model was used
previously by Riley (1963) and Steele (1958)
but should now be considered obsolete in view
of more recent work using the hyperbolic model.

ACKNOWLEDGMENTS

We appreciate the assistance of many persons
in gathering these data. Ammonium analyses
were performed by Mr. Edward Renger, and
Mrs. Anne Dodson aided in the determination
of /-max and Kg. Sampling and incubation for
production measurements and determination of
chlorophyll concentrations were carried out by
the following: Messrs. Tapuni Mulitauaopele,
Michael Kruse, David Justice, James McCarthy,
Lawrence Klapow, David Judkins, Gerald John-
son, Eric Forsbergh, and Jack Metoyer. Dr.
Bernt Zeitzschel and Mr. Michael Kruse helped
to process and edit the ^'*C and chlorophyll data.
Most of these data were collected aboard the
NMFS vessel David Starr Jordan and we appre-
ciate the assistance of Capt. C. W. Forster and
his crew.

91

FISHERY BULLETIN: VOL. 69. NO. 1

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1967. Nutrient limitation in the sea: Dynamics,
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Eppley, Richard W.

1968. An incubation method for estimating the
carbon content of phytoplankton in natural sam-
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Eppley, Richard W., and William H. Thomas.

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Eppley, Richard W., Jane N. Rogers, and James J.
McCarthy.

1969. Half-saturation constants for uptake of ni-
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Lorenzen, Carl J.

1966. A method for the continuous measurement
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MACISAAC, J. J., AND R. C. DUGDALE.

1969. The kinetics of nitrate and ammonia uptake
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1964. Marine phytoplankton photosynthesis as a

function of light intensity: A comparison of

methods. J. Fish. Res. Bd. Can. 21(1) : 159-181.

Monod, J.

1942. Recherches sur la croissance des cultures
bacterienne. Hermann et Cie, Paris.
Owen, R. W., and B. Zeitzschel.

1970. Phytoplankton production: seasonal change
in the oceanic eastern tropical Pacific. Mar. Biol.
7(1) : 32-36.

Richards, Francis A., and Richard A. Kletsch.

1964. The spectrophotometric determination of
ammonia and labile amino compounds in fresh
and sea water by oxidation to nitrite. In Yasuo
Miyake and Tadashiro Koyama (editors). Ken
Sugawara festival volume; recent researches in
the fields of hydrosphere, atmosphere and nuclear
geochemistry, p. 65-81. Maruzen Company, Ltd.,
Tokyo.

Riley, G. A.

1963. Theory of food-chain relations in the ocean.
In M. N. Hill (editor) , The sea. Vol. 2, p. 438-463.
Interscience Publishers, New York.

Steele, J. H.

1958. Plant production in the northern North Sea.
Scot. Home Dep., Mar. Res. 7, 36 p.
Steemann Nielsen, E.

1952. The use of radio-active carbon (C^*) for
measuring organic production in the sea. J. Cons.
Cons. Perma. Int. Explor. Mer 18(2): 117-140.
Strickland, J. D. H.

1958. Solar radiation penetrating the ocean. A
review of requirements, data and methods of
measurement, with particular reference to photo-
synthetic productivity. J. Fish. Res. Bd. Can.
15(3) : 453-493.
Thomas, William H.

1964. An experimental evaluation of the C-'^'* meth-
od for measuring phytoplankton production, using
cultures of Dunaliella primolecta Butcher. U.S.
Fish Wild. Serv., Fish. Bull. 63(2): 273-292.

1966. Surface nitrogenous nutrients and phyto-
plankton in the northeastern tropical Pacific
Ocean. Limnol. Oceanogr. 11(3): 393-400.

1969. Phytoplankton nutrient enrichment experi-
ments off Baja California and in the eastern
equatorial Pacific Ocean. J. Fish. Res. Bd. Can.
26(5): 1133-1145.

1970a. On nitrogen deficiency in tropical Pacific
oceanic phytoplankton: Photosynthetic param-
eters in poor and rich water. Limnol. Oceanogr.
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1970b. Effect of ammonium and nitrate concen-
tration on chlorophyll increases in natural trop-
ical Pacific phytoplankton populations. Limnol.
Oceanogr. 15(3): 386-394.
Thomas, W. H., E. H. Renger, and Anne N. Dodson.

In press. Near-surface organic nitrogen in the
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Oceanogr. Abstr.
Yentsch, Charles S., and D. W. Menzel.

1963. A method for the determination of phyto-
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221-231.

92

ECOLOGICAL EFFICIENCY OF A PELAGIC MYSID SHRIMP; ESTIMATES
FROM GROWTH, ENERGY BUDGET, AND MORTALITY STUDIES '

Robert I. Clutter^ and Gail H. Theilacker^

ABSTRACT

The net ecological efficiency (yield/assimilated) of a population of Metamysidopsis elongata (Crus-
tacea, Mysidacea) is estimated to be 32 %. The gross ecological efficiency (yield/ingested) is probably
between 19 % and 29 %.

Energy use by the field population was calculated from estimates of age specific natural mortality
rates and data on growth, molting, reproduction, and respiration. Average growth and molting rates
were determined by rearing the mysids in the laboratory. Size specific fecundity was determined from
field and laboratory observations. The calorie contents of the mysids, their molts, eggs and larvae
were estimated by bomb calorimetry and in part from biochemical composition. The energy used in
metabolism was calculated from size specific respiration and data on body composition.

Biological systems are organized by the flow of
energ-y. Trophic structui-e, numbers of steps in
food chains, and numbers of conjunctions in
food webs depend on the amount of energy
passed through populations to other populations.
Energy units provide a means of expressing
productivity in terms common to all organisms.
The energy produced in the breakdown of
biomass by organisms is stored as chemical en-
ergy in the pyrophosphate bonds of adenosine
triphosphate (Horowitz, 1968). The overall
thermodynamic efficiency of this process is sim-
ilar in all animals, about 60 to 70 '}t according
to Krebs and Romberg (1957). It has been
suggested (e.g. Slobodkin, 1961, 1962) that the
efficiency of energy transfer between popula-
tions of animals is also fairly constant. This
efficiency is necessarily of lower order because,
for example, there are losses involved in syn-
thesizing macromolecules, in continually resyn-
thesizing proteins that undergo thermal dena-
turation, in transforming foodstuff energy into
work energy (about 65 ^r efficiency), and in
the degradation of energy during the perform-

' This research was supported in part by NSF Grant
GB 7132.

' Formerly of National Marine Fisheries Service Fish-
ery-Oceanography Center, La Jolla, Calif. 92037.

^ National Marine Fisheries Service Fishery-Oceanog-
raphy Center, La Jolla, Calif. 92037.

Manuscript received September 1970.

FISHERY BULLETIN: VOL. 69. NO. 1, 1971.

ance of work. All energy that passes through
a population is either lost as heat or passes on
to another trophic level. If one assumes that
all mortality is caused by predation, the gross
ecological efficiency (Phillipson, 1966) of energy
transfer through that population is the ratio
of the energy yield in mortality to the energy
ingested.

Through laboratory studies of growth, molt-
ing, reproduction, respiration, body composition,
and energy content, we have constructed an
energy budget for the pelagic mysid shrimp
Metamysidopsis elongata (Holmes). Various
aspects of the distribution, behavior, and pop-
ulation biology of this species have been de-
scribed by Clutter (1967, 1969) and Fager and
Clutter (1968). The energy budget data, to-
gether with estimates of natural population
mortality rates, are used to estimate net and
gross ecological efficiencies for the field popu-
lation.

GROWTH AND DEVELOPMENT

Metamysidopsis elongata is a member of the
Mysidae, a family that is ubiquitous and often
very abundant in most of the neritic zones of
the world ocean. This species is free-swimming
and occurs in shoals and swarms just above the
sand bottom in areas where surf is common

93

FISHERY BULLETIN: VOL. 69, NO. 1

(Clutter 1967, 1969).

As is characteristic of mysids, the eggs and
larvae are held by the oostegites (brood pouch)
of the adult females until they develop into juve-
niles that are similar in form to the adults.
The juveniles grow by shedding their exoskel-
etons (ecdysis) at intervals that become pro-
gressively longer until they reach maturity.
Males and females develop distinguishable
morphological features during the period of
rapid growth prior to maturity. Growth be-
comes progressively slower after maturity. Al-
though there is no evidence that death occurs
because of physiological aging, the maximum
age observed was about 9 months. Most animals
survive less than 3 months in the natural en-
vironment . We assume that most of the na-
tural mortality is caused by predation, especially
by fishes.

Some growth experiments have been reported
for other species of Mysidae. Blegvad (1922)
determined the growth rates of a few individu-
als of My sis inernils from first stage juveniles
through early maturity. Nouvel and Nouvel
(1939) made disjunct determinations of time
between molt stages for some size groups of
Praunus flexuosis. Nair (1939) observed the
time sequence in the egg and larva development
of Mesopodopsis orientalis, determined the size
and age at liberation, and noted the size at sex-
ual maturity of males and females. In his
review of growth in some marine Crustacea,
Kurata (1960) presented the results of growth
studies made by Ishikawa and Oshima on Neo-
mysis japonica and by Matsudaira et al. on
Gastrosaccus vulgaris. Mauchline (1967) main-
tained adult Schistomysis spiritus in the labora-
tory, estimated the time they take to attain sex-
ual maturity, and estimated the minimum incu-
bation time. Considering differences between
species, sizes, and environmental temperatures,
these reported patterns of development and size
increase per molt are compatible with the results
of our study.

CULTURE METHODS

Experimental animals were collected during
the day from the middle of their habitat with

nets (Clutter, 1965; Fager, Flechsig, Ford,
Clutter, and Ghelardi, 1966). They were placed
in large (20-50 liter), opaque plastic containei's
with covers and transported to the laboratory
within 1 to 2 hr after the time of capture.

The culture methods were about the same as
those described by Lasker and Theilacker (1965)
for euphausid shrimps. Individual animals were
placed in rectangular clear plastic containers in
about 500 ml of sea water. The small con-
tainers were partly immei-sed in trays of run-
ning sea water. Since the running sea water
was pumped continuously into the aquarium
from midwater ofl'shore, within the Metamysi-
dopsis habitation zone, the laboratory temper-
atures ( 14°-20° C) were about the same as those
that the animals would have experienced in their
natural environment.

Animals of both sexes and of several sizes
were selected for the e.xperiments. Young ju-
veniles were procured by j^lacing pregnant fe-
males in containers and recovering the young on
the day following their release from the brood
pouch, which occurred at night. These young
were then placed in separate containers. To
determine the incubation time, i.e. the time from
fertilization of the eggs to release from the brood
pouch as juveniles, pregnant females with
known times of fertilization were placed in in-
dividual containers so that larval development
could be observed.

Mysids of all ages were fed freshly hatched
nauplius larvae of brine shrimp, (Artemia sa-
lina). Twice each week the mysids were re-
moved while their containers were emptied of
excess food and cleaned with hot fresh water
followed by a sea water rinse. They were then
provided with excess quantities of fresh nauplii
in clean sea water.

The containers were examined every day for
the presence of molts or, occasionally, carcasses.
The molts and carcasses were removed and
placed individually in small vials of 5 % Forma-
lin for subsequent microscopical examination
and measurement.

OOGENESIS AND INCUBATION

Since Metamysidopsis has a transparent cara-

94

CLUTTER and THEILACKER: PELAGIC MYSID SHRIMP

pace and body wall, it is possible to observe the
late stages of oogenesis in live animals without
dissecting them. The ovary (cf. Nair, 1939, for
description) is situated in the interspace be-
tween the alimentary canal and the pericardial
floor. Its most obvious feature is the pair of
larger tubes that lay side by side. It is in these
tubes that the eggs to be extruded into the brood
pouch are invested with yolk. The process of
yolk formation takes about a week in Metamysi-
dopsis and is completed just before the female
molts and copulates. By observing the ova in
these tubes it is possible to estimate the size or
age at first reproduction in maturing females,
and to count the number of eggs that will be
spawned by reproducing females of all ages.

Copulation occurs at night within 2 to 3 min
after the mature female molts, during which
time sperm are passed into the empty brood
pouch by the attending adult male. The eggs
are subsequently extruded into the brood pouch
where they are fertilized. The eggs hatch from
the vitelline membrane after 2 to 3 days. Ac-
cording to Manton (1928) and Nair (1939) a
larval ecdysis occurs in the brood pouch shortly
before the larvae are liberated. These late stage
larvae have movable appendages and pigmented
eyes that show through the transparent ooste-
gites of the brooding female. The small quantity
of yolk that is present after the larval ecdysis
is absorbed, or nearly so, prior to liberation
from the brood pouch.

After liberation the larvae tend to sink, then,
according to Nair (1939), they undergo a sec-
ond larval ecdysis after which the statocysts
appear and they are capable of swimming. The
mysids assume this highly mobile juvenile form
within a few minutes after liberation. Although
we did not attempt to distinguish sexes of larvae
and juveniles, the observations of Nair (1939)
indicate that dimorphism is exhibited by the ant-
ennules and abdominal appendages even though
neither the brood pouch nor the penis is de-
veloped.

Incubation time was determined in the lab-
oratory. Adult females and adult males were
observed in an aquarium during molting and
copulation. Ten females were caught after be-
ing observed in copulo and were placed in sep-

arate containers of sea water at the temperature
of their natural environment at that time (17°-
19° C). Five of them were removed, at var-
ious times, to determine the stages of develop-
ment of the young. The remaining five all re-
leased their young as juveniles on the tenth day
after fertilization.

In addition, a large number of nonpregnant
adult females were kept in separate containers
for various periods up to 157 days. The range
of intermolt periods in 218 observations was
5 to 13 days; the median and modal values were
both 10 days. There was no obvious temper-
ature effect. The adult females molt just before
fertilization and just after liberation of the
young; therefore, the average incubation time
was taken to be 10 days. This is intermediate
between incubation times given for Mysidae that
live and reproduce at higher and lower temper-
atures. Nair (1939) determined the incubation
time of Mesopodopsis orientaUs to be 4 days at
25° to 29° C. Mauchline (1967) reports a min-
imum incubation time of 3 weeks for Schisto-
mysis spiritus at 12.5° C.

MOLTING

To avoid handling and possible injury of the
experimental animals, the growth rates were
determined by measuring molts. The molts suf-
fered no appreciable decomposition because they
were collected on the day following ecdysis. The
morphological development of the animals was
usually discernable from their molts. But the
molts are fragile, split just back of the cara-
pace where the animals emerge, and easily
stretched out of shape. Therefore, to measure
growth it was necessary to measure a part of
the molt that always retained its form and bore
a consistent relationship to the body length.

Uropod-Body Length Relationship

The exopod of the uropod (tail fan) was used
to estimate the body length of each animal for
its previous intermolt period. The uropods were
measured from the base (end of last abdominal
segment) to the tip, not including spines, which
were sometimes broken, with an ocular micro-

95

FISHERY BULLETIN: VOL. 59, NO. I

meter, at 27.5 x magnification.

The relationship between uropod length and
body length was established from a selected ser-
ies of 94 animals that had been collected in the
field and pi-eserved. The series included ani-
mals that ranged in body length from 0.8 mm to
7.2 mm, and included late stage larvae, juveniles,
immatures, and adults. Both sexes were in-
cluded; there was no difi'erence between sexes
in this relationship.

The body length was measured from the end
of the last abdominal segment (base of uropod)
to the anterior edge of the carapace, behind the
insertion of the eyestalk. Mysids tend to curl
when preserved, and they can be distorted to
appear longer if they are stretched when meas-
ured. To avoid this we chose specimens that
were at most only slightly curved, and measured
the length of the arc through the midline of
those that had significant curvature, rather than
the straight line distance between head and tail.

As shown in Figure 1, the relationship be-
tween uropod length and body length is linear.
The body length is 4.5 times the uropod length.

Table 1. — Frequency of molting periods observed for
Metamysidopsis in the laboratory.

FiGUKB 1. — Relationship between uropod length and
body length of Metamysidopsis.

Molting Frequency

Average intermolt periods were estimated
from 414 observations, 146 on males and 268 on
females. In many cases several observations
were made on the same animal. The maximum
period of laboratory survival for a single ani-
mal was 157 days, and the maximum number of
molts observed for a single animal (not the same

Infermo

t Period

(dc

ys)

Sex
and
length

3

4

5

6

7

8

9

10

11

12

13

o

c
D

1

c
o

Females

2

3

4

4

4.0

1 3

6

2

4

4

4.3

jr 4

5

3

1

4

4-5

4.6

ai

£ 5

3

7

7

1

5

2

5-6

6

6.2

i 6

10

7

9

13

13

28

17

5

8

10

9-10

9.2

" 7

11

8

6

9

16

12

28

9

9

11

10

9.4

Males

E 2

11

3

3

3.0

^ 3

2

II

1

4

4

3.9

JZ

? '^

2

15

8

1

1

4

4

4.4

~ 5

6

29

20

4

5

5-6

5.4

m 6

6

II

8

7

3

5

5-6

5.7

animal) was 21. The molting frequency data
for animals reared in the laboratory are sum-
marized in Table 1. The sex of the juveniles
was established after they had grown large
enough to develop obvious morphological dif-
ferences.

Supplementary data on molting frequency in
the field population were obtained indirectly.
Over a period of 3 days, 1,211 juveniles + im-
matures and 2,979 adults were brought into the
laboratory late in the day and placed in large
aquaria. The following morning all the animals
and their molts were collected and counted. Of
the juveniles + immatures 218 or 18 % had
molted, and of the adults 356 or 12 % had molted.
The recii)rocal of the relative number molting
is an estimate of molting period. The observed
reciprocals were 5.6 for juveniles + immatures
and 8.3 for adults. Since these values are mid-
way in the ranges shown by laboratory animals
(3-8 days for juveniles + immatures and 4-13
days for adults) we assume that the laboratory
observations are valid estimates of molting fre-
quency in the population as a whole.

Although our observations were made from
February to October, and the water tempera-
tures in the rearing troughs varied from 14°
to 20° C, we were unable to detect any obvious
effects of temperature or time of year on molting

96

CLUTTER and THEILACKER: PELAGIC MYSID SHRIMP

frequency or growth rates. Nouvel and Nouvel
(1939) stated that the intermolt period for
Praunus flexiiosis is least during the warmest
months, and the incubatory period is 15 days
in August and 3 to 4 weeks in September. Las-
ker (1966) showed that Euphausia pacifica in-
termolt ijeriods varied as the water temperature
fluctuated, and that the intermolt period was
shortened by an artificially produced warm per-
iod, but that temperatures above 12° C did not
accelerate molting further.

Since we do not have evidence to the contrary,
we must assume that our laboratory observa-
tions on molting frequency provide adequate
average values. From the median values given
in Table 1 and estimated average growth rates
(see below) we have estimated the molting
schedules of females and males from juveniles
to mature adults as follows:

Females: first six molts — 4 days
seventh molt — 5 days
eighth molt — 6 days
ninth molt — 8 days
tenth molt and thereafter — 10 days

IVIales: first four molts — 3 days

fifth to eighth molts — 4 days
ninth and tenth molts — 5 days
eleventh molt and thereafter —
6 days

GROWTH AND MATURATION

Evidence of the temporal sequence of growth
and maturation can be obtained from following
peaks of abundance of size groups in natural
populations. We sequentially sampled the my-
sids in the field and observed some shifting peaks.
But we consider that the results are not very
reliable because of temporal changes in age-
specific mortality rates (Fager and Clutter,
1968). Therefore, all the age-specific growth
estimates presented here were obtained from
laboratory studies.

Observed Gro'wth

A few mysids were reared in the laboratory
from fertilized egg to adult. Several were reared
from egg through the juvenile stage. In addi-

tion, larger numbers of various sizes were col-
lected in the field and kept in the laboratory
for several molts.

The growth data from these animals were
combined as shown in Figure 2 (females) and
Figure 3 (males). The sexes were separated
because the growth and molting rates of males
and females are different. As they are shown
in Figures 2 and 3, these individual growth
curves are simplified and slightly incorrect rep-
resentations of true growth, for two reasons.
First, the growth of the body integument is
represented to be continuous, whereas it actually
occurs in discrete increments. Second, the age

Figure 2. — Observed growth in length (from molts)
of Metamysidopsis females in the laboratory.

Figure 3. — Observed growth in length (from molts)
of Metamysidopsis males in the laboratory.

97

FISHERY BULLETIN: VOL. 69, NO. I

shown is the age of the animal at the time it
molted, rathei- than the age at the time that the
molted integument was first formed. The pro-
cedure for combining the various growth curves
of individual animals was to first plot the growth
of the animals of known age, and then plot the
other gro\vth curves (actual ages unknown) in
a manner that showed the least variation from
the apparent trend.

Some of the apparent variability in growth
rates may be attributable to differences in the
temperature at which the growth occurred, but
we did not detect any obvious temperature efl^ect.
Considerable individual variability occurred
among animals of the same size or age that were
reared simultaneously.

Maturation

Changes in morphology in relation to size, and
known or estimated age, wei'e observed in the
molts of animals reared in the laboratory. Ob-
servations were made on live females collected
from the field population to determine the size
at which yolk invested ova first appear in the
ovaries. Supplementary observations on the re-
lationship between size and body form were
made on preserved animals that had been col-
lected in the field. There is some evidence from
previous samples taken for other purposes
(Clutter, 1967, 1969) that the relationship be-
tween size and stage of development may vary
seasonally. But during the period of observa-
tions reported here, this did not appear to be
significant.

In particular, we wished to determine (1)
the size (and subsequently the age) at which
males and females were easily distinguishable
by their secondary sexual characteristics, (2)
the size at the onset of maturity, and (3) the
size at which spawning and brooding of eggs
and larvae occurs. The external characteristics
that most obviously separate males from females
of this species are the enlarged oostegites (brood
pouches) of the females and the enlarged pleo-
pods (abdominal legs) and antennae of the
males.

There is some variability in the size at which
the stages of development occur. Therefore,

our estimates are average values. The larvae
are released and juvenile form is attained at
age 10 days; at this time both sexes are about
1.2 mm long (body length; excluding antennae,
eyes, and tail fan). Males exhibit sub-adult
morphology when about 3.7 mm long, and be-
come mature at 4.3 mm. Females exhibit sub-
adult form at 4.0 mm, the ova become infused
with yolk at 4.5 mm, and the eggs are extruded
into the brood pouch, fertilized, and incubated
at slightly less than 5.2 mm.

Average Growth in Length

Average continuous growth curves were fitted
by eye to the combined growth data plotted in
Figures 2 and 3. These curves are represented
by the lower curves (fine, continuous unbroken
lines) in Figure 4 (females) and Figure 5
(males) . These continuous curves represent the
size of the molt at the time — days from fertili-
zation— that the molt was shed. Actually the
integument of the animal had attained that size
by the beginning of the intermolt period in
question. The true growth of the integument
of the average animal is represented by the stair-
step pattern, which is based on the molting fre-
quency analysis. The broken curved line of con-
tinuous growth (Fig. 4 and 5) represents the
probable pattern of temporal change in average
organic weight of the animal. This curve con-
nects the points halfway betw^een the beginnings
and endings of the intermolt periods.

Since the average sizes at various stages of
development were determined, it was possible
to estimate the average time schedules of ma-
turation and reproduction for females and males
on the basis of the growth curves. The average
female begins to develop a brood pouch at the
seventh molt, 39 days after becoming a fertilized
egg. Yolk invested ova begin to be formed at
45 days, during the ninth intermolt period; the
ova are extruded into the developed brood pouch
and fertilized at the beginning of the tenth in-
termolt period, at 53 days; and reproduction
can occur at 10 day intervals thereafter.

Males and females gi-ow at rates that are in-
distinguishable up to the age of about 30 days,
even though the juvenile males molt more fre-
quently than juvenile females. After that the

98

CLUTTER and THEILACKER: PELAGIC MYSID SHRIMP

Figure 4. — Average growth in length of female Meta-
mysidopsis in the laboratory. The lower curve (fine
continuous line) was fitted to molt size data (Fig. 2).
The steps represent changes in integument size. The
upper curve (heavy broken line) represents the average
size of the animals, assuming that the addition of body
tissue is continuous.

- alongalion of pleopodi ond or'enna* 1 3B dart I

Figure 5. — Average gro%vth in length of male Meta-
mysidopsis in the laboratory. The lower curve (fine
continuous line) was fitted to molt size data (Fig. 3).
The steps represent changes in integument size. The
upper curve (heavy broken line) represents the average
size of the animals, assuming that the addition of body
tissue is continuous.

males grow more slowly. The males develop
easily recogriized secondary sexual character-
istics at an average age of 38 days and become
sexually mature after about 48 days. Average
age at maturity was estimated from observa-
tions of testes and copulatory behavior in the
laboratory as well as from external morphology.

Average Growth in Weight

To estimate gro\vth in terms of energy it is
necessary to translate growth in length into
growth in dry weight. This growth in dry
weight is then translated into growth in organic
(ash-free) weight and thereafter into calories.

The dry weights of Metamysidopsis of body
lengths ranging from 1.9 mm to 6.5 mm were
determined. The animals were captured alive,
measured, washed very briefly with distilled
water, and dried at 60° C in an oven for 24 hr.
They were then weighed individually on a Cahn
electrobalance immediately after they were re-
moved from the oven.

The observed relationship between body
length and dry weight is shown in Figure 6.

Figure 6. — Relationship between body length and dry
weight of Metamysidopsis.

The equation for the relationship was deter-
mined empirically by fitting a straight line to
the logarithms of body length and dry weight
by the method of Bartlett (1949). The rela-
tionship is:

log,, (weight) = -5.436 + 2.77 log,, (length)

or

weight = 0.00436 (length)^ "
where weight is expressed in mg and length in
mm.

It is common to assume that body weight and
body volume have a linear relationship, and that
body volume is proportional to the third power
of length. Therefore dry weight is expected to

99

FISHERY BULLETIN: VOL. 69, NO. 1

be proportional to the third power of body length
(Bertalanffy, 1951). The observed relationship
does not quite conform to the expected. The re-
lationship between body length and body di-
ameter appears to be linear (Fig. 7); therefore
the body volume must be proportional to the
third power of the body length. The observed
relationship between weight and length could
be the result of orthogonal growth of the ap-
pendages, which become progressively larger
as the animals mature.

From the average length-weight relationship
and the average continuous growth in length
curves (Fig. 4 and 5) we have calculated the
average growth in weight curves shown in Fig-
ure 8. The average continuous growth in length
curves represented by the heavy broken lines
in Figures 4 and 5 were used to calculate growth
in weight, because we assume that growth in
organic weight is continuous during intermolt
periods even though growth of the integument
occurs in discrete steps. The estimated growth
in weight of males was extrapolated by eye from
age 175 days to age 204 days. We do not have
laboratory growth estimates for these larger
males, but they occurred in the field population.
The average dry weight per egg (140 eggs in
sample) was 5.5 fig. Larvae weigh slightly
less than this because they lose weight through
metabolism while in the brood pouch, even
though their ash content is slightly higher than
that of the eggs.

Figure 7. — Relationship between body length and body
diameter of Metamysidopsis.

Figure 8.— Average growth in dry weight of Meta-
mydisopsis females and males in the laboratory.

REPRODUCTION

Data on reproduction and associated energy
use are easier to obtain for Mysidae than for
most pelagic invertebrates. The eggs and larvae
are carried in the brood pouch of the female,
and the incipient eggs can be counted prior to
their full development and extrusion because the
body walls of the mysids are transparent. In
addition, copulation and fertilization can be ob-
served in the laboratory, and frequency of preg-
nancy among mature females can be observed
in the natural population through sequential
sampling because all stages live in the same area
while gestating as they do when not reproducing.
Nevertheless, average reproduction rate in these
animals is not easy to assess with absolute
certainty.

FECUNDITY

Minimum Estimate

The most straightforward way to estimate
fecundity is to collect animals in the field, pre-
serve them, and count the number of eggs or
larvae carried by females of diff"erent sizes.
Figure 9 shows the relationship between body
lengths and number of young for 310 females
collected in the field at various times during
the year. The data include 125 females bearing
eggs and 185 bearing larvae; we excluded ani-
mals that had obviously lost young during cap-
ture and preservation. For both eggs and lar-

100

CLUTTER and THEILACKER: PELAGIC MYSID SHRIM'

number roung : 4 9(body langth] - 14 5
numb*r vgo* : S.4[body Unglh) -16.0 .

the time of extrusion of the eggs and the esti-
mated average age at which they were counted
(7 days) was estimated to be about 0.91. The
number of brood pouch young per female was
adjusted to the equivalent number of eggs ex-
truded per female by multiplying the number
of young by 1/0.91 = 1.10. The relationship
(Fig. 9) then becomes: number of eggs = 5.4
(body length, mm) - 16.0, which is shown in
Figure 9 as the upper, dashed line.

We consider this to be a minimum estimate
of fecundity, because some females that had lost
eggs and larvae from the brood pouches during
collection and preservation were probably in-
cluded, despite our attempt to exclude them.

Figure 9. — Relationship between body length and num-
ber of brood pouch young (eggs and larvae) of preserved
animals that were collected in the field. The lower line
(continuous) was fitted to the points by the method of
Bartlett (1949). The upper line (dashed) represents
the equivalent relationship for newly laid eggs, assuming
a brood pouch mortality of 0.013/day (see text).

vae, the number of young per female is highly
variable. The average relationship between the
size of the female and the number of young,
calculated by the method of Bartlett (1949), is
represented by the straight line: number of
young = 4.9 (body length, mm) - 14.5.

This estimate of fecundity is not quite cor-
rect because it was made from counts of eggs
and larvae that were a few days old. Some eggs
and larvae apparently are lost from the brood
pouch during the incubation period. Therefore,
we adjusted the relationship to account for the
mortality which occurs during the incubation
period. To estimate the mortality during incu-
bation, counts were made of the maturing ova
in the ovaries of 40 adult females and counts
were made of late stage larvae in the brood
pouches of 27 females of the same size, collected
at the same time. The ratio of mean number
of larvae/mean number of ova was 0.90. The
larvae were estimated to be 8 days old, giving
an instantaneous mortality rate of 0.013/day.

The average age of the eggs and larvae from
the 310 preserved females (Fig. 9) was esti-
mated to be 7 days. Therefore, the relative sur-
vival of the young in the brood pouch between

Maximum Estimate

We observed that the females that had re-
leased young during the laboratory experiments
had a higher apparent fecundity than those that
were collected and preserved in the field. It is
possible that there was some bias in selecting
animals for the laboratory experiments, but we
were not aware of any. The number of young
released per female is plotted against the body
length of the female for those 17 specimens in
Figure 10. The average relationship between

K)

numbe. oggt -- 5 5 ( bod, lengihl-ll? , ^ "^

2i

\,^

o

I 30

^■^ ^^^-"''''^

£>

E IS

3 '^

z

-^^^ \

Int^mb*' lo'.a* '- d.Slbody l*nglh ) - 10.4

10

s

1 1 l^

Figure 10. — Relationship between body length and num-
ber of young released by experimental animals in the
laboratory. The lower line (continuous) was fitted to
the points by the method of Bartlett (1949). The upper
line (dashed) represents the equivalent relationship
for newly laid eggs, assuming a brood pouch mortality
of 0.013/day (see text).

101

FISHERY BULLETIN: VOL. 69, NO. 1

body length and number of young, calculated
by the method of Bartlett ( 1949) , was: number
of young = 4.8 (body length, mm) -10.4. This
is represented by the lower, unbroken straight
line in Figure 10.

This relationship gives estimates of fecundity
that are about 1.5 to 2 young per female higher
than the relationship calculated from preserved
animals. But this is not quite a maximum esti-
mate of fecundity because it does not include
the reduction from mortality that occurs during
incubation.

As already demonstrated, we can assume a
brood pouch mortality rate of 0.013 per day.
The relative survival of young in the brood
pouch during the 10 days between the extrusion
of eggs and the release of larvae was therefore
estimated to be 0.87. The number of young
released per female was adjusted to the equiv-
alent number of eggs extruded per female by
multiplying the number of young by 1/0.87 =
1.15. The relationship (Fig. 10) then becomes:
number of eggs = 5.5 (body length, mm) -11.9,
which is shown in Figure 10, as the upper,
dashed line.

This relationship gives estimates of fecundity
that are about four eggs per female higher than
the minimum estimates calculated from pre-
served animals. We consider this to be the max-
imum estimate of fecundity. It is the same as
that used by Fager and Clutter (1968).

COPULATION AND FERTILITY

The fecundity estimates given above apply
only to the females that engage in copulation
and are fertilized. Mature females that are not
fertilized apparently extrude some eggs, but only
about one-half the usual number.

Many observations of copulation were made
in the laboratory (Clutter, 1969). It occurs in
artificial light as well as in the dark, but only at
night, between about 2000 and 2400 hr. It oc-
cui-s within only 2 to 3 min after the mature
females molt, and apparently only when the fe-
male exudes a pheromone to attract adult males
of the same species.

Ten females were captured immediately after

they were observed in copulo and kept in sep-
arate chambers for 10 days. Impregnation had
been successful and the usual number of eggs
were extruded in every instance. Some adult
females that molt do not stimulate males to at-
tend them. Ten adult females were captured
after they had been observed to be unattended
by males during molting and recovery. They
later extruded only about one-half of the normal
number of eggs, which eventually disappeared
from the brood pouch, presumably because they
were infertile. Therefore, the unfertilized fe-
males expended only about half the amount of
energy in eggs that the fertilized females ex-
pended.

Since the mature females are subject to fertil-
ization for only a few minutes following molting,
and they apparently do not always attract males
during the time, copulation does not always oc-
cur. Therefore, not all produce young every
10 days. In a large number of field collections
during all seasons, the observed fraction of ma-
ture females carrying eggs or larvae in their
brood pouches varied from 18 ^r to 78 Sr I the
mean was 51 '}r . We are not certain of the
source of this variability; there is some evi-
dence that it could be related to population den-
sity (Clutter, 1969) . We have assumed an aver-
age value of 50 fr for the purpose of calculating
the amount of energy used in reproduction.

On the average, mature females extrude the
usual number of eggs about one-half of the time,
and they otherwise extrude only one-half of the
usual number of eggs. Therefore, the effective
average fecundity, in terms of energy used in
reproduction (but not in terms of the number
of viable young produced), is 0.5 + (0.5) (0.5)
= 75 % of the fecundity estimated from counts
of young produced/female. For the purpose of
calculating the amount of energy used in repro-
duction the fecundity equations are:

minimum — number of eggs = 4.1 (body length,

mm) - 12.0

maximum — number of eggs = 4.1 (body length,

mm) -8.9

The second of these relationships is used in the
ensuing energy budget calculations.

102

CLUTTER and THEILACKER; PELAGIC MYSID SHRIMP

RESPIRATION

A polarographic oxygen electrode (Kanwish-
er, 1959) was used in a closed system to measure
the respiration rates of Metamysidopsis. Both
temperature and oxygen were recorded contin-
uously on a strip chart.

The experimental animals were taken from
large constant-flow holding tanks (temperature
14°. 17° C) and acclimated overnight at the tem-
perature used in the experiments (13.8°-18.1°
C) , to avoid the overshoot in oxygen consumption
described by Grainger (1956). They were then
washed in millipore-filtered seawater, counted,
and transferred to previously filtered seawater
in the oxygen electrode system. In each experi-
ment an attempt was made to use animals of a
limited size range. During the run they were
held within a 10- ml chamber, baffled at each
end with silk screen cloth of 282 /i mesh aperture
size. The water in the closed system circulated
through this chamber and then past the electrode
at a constant rate. The whole system was im-
mersed in a temperature-controlled water bath.

Oxygen use by bacteria was measured by mak-
ing blank runs with the same water both befoi-e
and after each test run. Bacterial use amounted
to less than 2 ^c . Oxygen consumption by the
mysids was corrected for bacterial uptake. The
decrease in relative oxygen tension with time
was nearly linear in both the blank runs and the
test runs.

The results of the respiration experiments are
shown in Table 2. Observed weight-specific

Table 2. — Summary of respiration experiments on
Metamysidopsis.

Specimens

Number

Mean dry
weight

Water
temper-
ature

Weight-specific

resp

ration rote

Uncorrected

Corrected^

Juveniles

99

Ml.
003

° C.
13.8

(ill Oi/mg
7.71

dry

wt hr)
7.54

Juvenile ond
immature
moles and
females

176

0,07

18.0

5-40

4.76

"

297
297
132

0-08
0.08
0.14

18.1
18.1
138

5.03
6.78
3.92

4.48
5.93
3.82

Immature
females

85

0.28

15.2

1.95

2.46

Males
Brooding
females

51
27

0.31
0.47

138
13.8

3.60
3.22

3.53
3.16

27

0.66

13.3

2.65

2.59

lOO

BO

_-«■ ^ : 0 ^

. ""i^j... „,.

cadu'*)

-'

^^

\

T

B = 27wO"

-X

V

E

{Boxlan p'ocaduia 1

V.

6-

NJ

i 30

X

S.

\^

10

Figure 11. — Relation between respiration rate of Met-
amysidopsis and size at 16° C. The symbol if' rep-
resents respiration rate per dry unit weight (R/W).
The lines were fitted to the circle points by two sta-
tistical pocedures. The x points are values calculated
from published data on other species of Mysidae: 1-
Neo7nysis americana (RajTnont and Conover 1961) ;
2-Neomysis integer (Raymont, Austin and Linford
1966); 3-Hemimysis labornae (Grainger 1956).

respiration rates (/tl Oj/mg dry weight hr) were
corrected for the initial percent oxygen satura-
tion and for temperature. In correcting for
temperature, a Q,o of 1.9 was used (Grainger,
1956). All values were corrected to 16° C,
which is about the median of the year-round
temperatures that occur in the natural environ-
ment of the mysids.

The corrected weight-specific respiration data
are plotted in Figure 11 on log-log scales. The
symbol R' (Conover, 1960) represents the res-
piration rate per unit dry weight (R/W). The
average relationship between mean dry weight
and R' was estimated by two statistical pro-
cedures. First, a straight line was fitted to the
logarithmically transformed data by the median
procedure (Tate and Clelland, 1957). This gave
the relationship:

or

R' = 2.0 H'-o-3«
R = 2.0 (^"-ss

^ Corrected for oxygen saturation level and corrected to temperature
of 16.0° C by using Qio = 1.9 (Grainger, 1956).

where R = respiration rate in fi\ Oj/hr

and W = mean dry weight in mg.
Second, a straight line was fitted to the logarith-
mically transformed data by the method of

103

Bartlett (1949). This gave the relationship:

R' = 2.2 W-"-'^-
or

R = 2.2 f^»-«»

Theoretically, the respiration rate is expected
to be proportional to the % power of weight.
Since our estimates are slightly above (0.68) and
slightly below (0.62) the expected value of 0.67,
we consider that the % power relationship is
the best estimate for Metanujsidopsis and that
the best estimate of respiration rate (/nl Oj/hr)
is given by the equation:

/? = 2.1 1^""

Estimates of weight -specific respiration for
three other, somewhat larger, species of Mysidae
are compared with Metamysidopsis in Figure
11. The upper four points ("1" on Fig. 11)
represents results for Neomysis americana from
Ravmont and Conover (1961) that were ad-
justed from 4° C or 10° C to 16° C by using
a Q,o value of 1.6 that was estimated from their
data. The intermediate point is an estimate of
the median value oxygen consumption rate cal-
culated from 12 determinations on Neomysis
integer (Raymont, Austin, and Linford, 1966)
that had been adjusted to 16° C by using a Q,o
of 1.9 (Grainger, 1956). The lower point was
estimated from the results of Grainger (1956)
for Hemimysis lamomae. The ranges of values
for these three larger species are about the same
as the range (1-3 ^il/hr) calculated from the
seasonal change data of Raymont et al. (1966)
that had been adjusted to 16° C. The estimates
for Metamysidopsis and the other three Mysidae

FISHERY BULLETIN: VOL. 69. NO. I

all lie well above the relationships calculated for
marine planktonic Crustacea by Conover (1960) .

BODY COMPOSITION AND
ENERGY CONTENT

To estimate the amounts of energy used in
respiration, molting, and reproduction it was
necessary to determine the body composition of
the mysids, their molts, and their young. For
these analyses the animals were captured alive
and, within 2 hr, placed in a constant-flow hold-
ing tank at 15° to 17° C where they were kept
for a short time prior to analysis.

BODY COMPOSITION

The estimates of body composition of dried
animals and molts are summarized in Table 3.
The estimates for ash, protein, lipid, carbohy-
drate, and chitin are not considered to be accu-
rate past the first decimal point. The fractional
percentage values are entered so that the sums
will equal 100 ^/c. The methods by which these
values were determined will be explained item
by item.

To determine dry weights, the animals were
washed very briefly with distilled water while
still alive, then were oven-dried to constant
weight at 60° C. Materials that were available
only in small quantities were weighed on a Cahn
electrobalance.

Ash

Ash content was estimated by incinerating

Table 3. — Average composition and energy content of dry Metamysi-
dopsis bodies, molts, eggs, and larvae. Tabulated values for composition
are %, and for energy content are cal/mg. The sums of % ash, "pro-
tein", lipid, carbohydrate and chitin = 100 %.

Nitrogen

Carbon

Ash

"Protein"*

Lipid

Carbo-
hydrate

Chitin

Energy

%

%

%

%

%

%

%

Cal/mg

Body, whole

II.5

36.8

12.5

69.0

10.0

1.5

7.0

4.60

Body, organic

13.2

42.0

0

79.0

11,4

1,6

8.0

5.24

Molt, v^hole

23.5

44 8

30.9

0

0

24.3

2.48

Molt, organic

42.S

0

56 0

0

0

44.0

4.49

Egg, whole

58.0

6.0

35.2

588

0

0

7.16

Egg, organic

61.8

0

37.5

62.5

0

0

7.62

Lorva, whole

45.7

66

60.8

28.9

0

3.7

5.78

Larva, organic

—

48.8

0

65.0

31.0

0

4.0

6.20

* "protein" may include free omino acids.

104

CLUTTER and THEILACKER, PELAGIC MYSID SHRIMP

whole animals or molts in a muffle furnace at
500° C and weighing the residue. Ash determi-
nations were made on six samples composed of
mixed animals, juveniles, immatures, adult
males, and adult females. The samples con-
tained from 2.7 to 7.3 mg of dried animals ;
the mean ash content was 12.5 % of the dry
weight, and the range was 9.4 to 13.3 % . There
was no obvious difference between age groups
or sexes. This ash content is within the range,
but slightly higher than the mean, of values re-
ported for other Mysidae: Mysis flexuosa —
16 ^f (Hensen, 1887) and 11.9 '^h (Delff, 1912,
quoted by Vinogradov, 1953); Neomysis integer
— 7.9 % (Raymont, Austin, and Linford. 1964) ;
Siriella aequiremis ■ — 10.2 ^r (Omori, 1969).

Molts used for ash determinations were col-
lected in the laboratory immediately after they
were shed. Two samples, weighing 1.1 and 0.6
mg, composed of molts from a wide size range
of mysids of both sexes had ash contents of
44.4 % and 45.7 Sf; the mean was 44.8 %.
Lasker (1966) reported a similar value (46 %)
for Euphausia pacifica. This high ash content
in the molts suggests that a large fraction of
the total body ash resides in the integuments of
the whole animals. From 10 observations, we
have found that the dry weight of the molt is
on the average 13 "^r of the dry weight of the
animal that sheds the molt. Assuming that the
ash content of the molt is the same as the ash
content of the integument of the whole animal,
we estimate that 47 % of the body ash resides
in the integument.

Ash content of brood pouch young was esti-
mated fi-om a large number of specimens taken
from live females. A dry sample of 0.6 mg of
newly hatched larvae had an ash content of
6.1 %. A sample of 1.2 mg of late stage larvae
had an ash content of 6.6 ',? ■ Ash content of
eggs was not determined; we assume that the
ash content is slightly less than that of the
newly hatched larvae, and we have used a value
of 6.0 %.

Nitrogen and Carbon

Nitrogen content was determined by the
micro-Kjeldahl method from three samples of
mixed juvenile-adult animals. The dry weights

of the samples were 12, 24, and 63 mg, and
contained 13.1 %, 11.7%, and 11.2 % nitrogen
respectively; the mean was 11.5 % of total dry
weight. From a large number of determina-
tions, Raymont et al. (1964) found a value of
11.4 % for Neo?nysis integer. Omori (1969)
reported 11.0 % for Siriella aequiremis, and
Jawed (1969) found 11.9 % for Neomysis rayii.

Carbon content was determined with an F
and M carbon analyser model 180, described
by Lasker (1966). We assume that all organic
carbon, including that in chitin, is liberated by
this method.

Three samples of females, without young, that
weighed 0.2 to 0.4 mg, had carbon fractions be-
tween 35.6 9f and 38.1 % of dry weight; the
mean was 36.8 %. This estimate is intermedi-
ate among other values reported for mysids:
Lophogaster sp. (family Lophogastridae) —
46.8 % (Curl, 1962a); Neomysis integer —
30.2 % and 29.5 % (Raymont et al., 1964, 1966) ;
mixed mysids and euphausids — 40.7 % (Beers,
1966); Siriella aequiremis — 42.4 (Omori,
1969). From his analysis of several kinds of
arthropods, Curl (1962a) found an average of
about 38 ':? of the dry weight as carbon. He
points out that this is about % of the commonly
assumed value of 50 % (Krogh, 1934).

In our carbon analysis of molts and young,
we found that a 0.2-mg sample of fresh dried
molts had 23.5 ^'r carbon, a 0.4-mg sample of
eggs had 58.0 % carbon, a 0.4-gm sample of
midstage larvae had 47.1 % carbon. The carbon
contents of the ash-free organic fractions of the
material were calculated from these values.
Lasker (1966) found 17 % carbon in the molts
of Euphausia pacifica and 50 % carbon in the
eggs.

Macromolecular Components

We assume that the body nitrogen of our spe-
cies, Metamysidopsis , is present as protein, free
amino acids, and chitin (Raymont, Austin, and
Linford, 1968). We made no evaluation of
chitin content, but used the value of 7 % de-
termined for Neomysis integer by Raymont et al.
(1964). The percent "protein" (may include
free amino acids) was estimated by the follow-
ing relationship, given that 16 % of "protein"

105

FISHERY BLLLETIN: VOL, 69, NO- I

is nitrogen, 6.5 "^r of ciiitin is nitrogen, and 7 '/c
of the dry body is chitin: 0.16 ("protein") +
(0.065) (0.07) = 0.115. From this relation-
ship, the "protein" content of the whole dry
body was estimated to be 69 %, which is sim-
ilar to the value to 71 % protein estimated di-
rectly by Raymont et al. (1964) for Neomysis
integer. According to the estimates of Raymont
et al. (1968) , the percent nitrogen in proteins of
Mysidae may be lower than the value of 16 %
commonly assumed for animal tissues. They
found 13.3 9r N in the body protein of Neomysis
integer, and estimated that about 17 ^/c of what
we would have designated as "protein" nitrogen
was actually free amino acid nitrogen. They
suggest that the amino acids may function in
osmoregulation for Neomysis integer, which is
a euryhaline-brackish water species. We know
nothing directly about this for Metamysidopsis.
Our species lives in a constant oceanic salinity,
and we estimated the ash content to be higher
than that of N. integer. Therefore, a high con-
centration of free amino acids may not be ne-
cessary for osmoregulation in our species. What-
ever the ratio of protein/free amino acids may
be in Metamysidopsis , our energy calculations
should not be affected materially.

The lipid content of the mysid bodies was esti-
mated by placing samples of dried, crushed
bodies successively for 1 hr in each of two 10-ml
portions of ethyl alcohol and two 10-ml washes
of petroleum ether. The lipid content was esti-
mated as the difference in dry weight before
and after extraction. Two dry samples of mixed
animals, weighing 62.9 mg and 13.4 mg, gave
values of 9 % and 11 % lipid respectively. A
third sample, containing 24.1 mg of brooding
females that had full complements of young in
their brood pouches, gave a value of 19 Cr lipid.
Linford (1965) found that large females of
Neomysis integer carrying young had higher
lipid contents than males. From our knowledge
of the number of young per female and the esti-
mated percent lipid in the young, we calculate
that i/i. to 1/2 of the 19 ^r lipid value could be
contributed by the brood pouch young. There-
fore, we have excluded the 19 ^r value from our
estimate, and we have used 10 '/c as the estimate
of average lipid content of the dry bodies. This

is slightly less than the value of 13 7r estimated
for Neomysis integer by Raymont et al. (1964),
but within the range of means for three species
estimated from a large number of determina-
tions by Linford (1965): Mesopodopsis slavveri
— 9.0 % ; Neomysis integer- — 10.1 S^ ; Praimus
neglectus — • 9.3 %.

The carbohydrate content of the mysids was
estimated as the amount of macromolecular
material remaining after the average estimates
for ash, protein, chitin, and fat are subtracted
from the dry weight. This remainder is 1.5 %.
Apparently the carbohydrate fraction is low in
all pelagic Crustacea. Raymont and Conover
(1961) found that 1 '? of the dry weight of
Neomysis aniericana was glucose; Raymont and
Krishnaswamy (1960) found 1.3 ^r carbohy-
drate in dry Neomysis integer; and Raymont
et al. (1964) found 2.4 9( carbohydrate in dry
Neomysis integer.

We did no detailed analyses of the composition
of molts, but we assume that the molt is com-
posed of structural materials rather than energy
storage materials. Since we consider that carbo-
hydrates and lipids are virtually absent, we
entered zero values for them in Table 3. The
"protein"/chitin relationship was determined in-
directly. First, we estimated the smiount of
carbon in the average protein of the mysids from
the relationship:

(■■f C as protein) = C/c C in body)

— (% C as chitin)

— (% C as lipid)

— (% C as carbo-

hydrate) .

The percent carbon in the organic fraction of
the body is 42 ""f , the chitin fraction is taken
as 8 '( , the chitin is assumed to be 50 % carbon
(Curl, 1962a), the lipid content of the organic
fraction is 11 ""r , the lipid is assumed to be 77 ^c
carbon (Lasker and Theilacker, 1962), the car-
bohydrate fraction is about 2 % . and the carbo-
hydrate is assumed to be 40 % carbon (Curl,
1062a). Therefore, the percent carbon in the

106

CLUTTER and THEILACKER: PELAGIC MYSID SHRIMP

mysid protein is calculated as:

% C

(0.08) (0.50) -(0.11) (0.77)

L[0.42

-0.79

— (0.02) (0.40)]

= 0.364

= 36.4 %

This is considerably less than the average value
of 52 '( carbon in protein given by Hawk, Oser,
and Summerson (1954), but similar to an esti-
mate of 37 % made from the data of Lasker
(1966), and higher than an estimate of 23 Sr
made from the data of RajTiiont et al. (1964).
The second step in finding the relationship
between chitin and protein in the molts was to
estimate the chitin fraction from the following
relationship:

(chitin fraction) (9f C in chitin)

+ (protein fraction) (9f C in pi-otein)
= (% C in molt)

where

chitin fraction + protein fraction

1.0.

The chitin fraction calculated from this rela-
tionship is 44 % for the organic molt. The
protein fraction is therefore estimated to be
56 ^,x . This result suggests that a large fraction
of the chitin may be reabsorbed by the animals
before molting. This seems reasonable because
in Crustacea the new endocuticle is formed dur-
ing the intermolt period (between 2 % and 46 %
of the time between molts, according to Passano,
1960).

To estimate the protein content of eggs and
larvae, we have made some arbitrary assump-
tions that seem reasonable, and that do not
measurably affect our energy calculations in any
event. We have assumed that the eggs do not
contain a measurable amount of carbohydrate,
and that they contain little or no chitin because
the integument is not yet formed. Therefore,
we have assumed that the organic fraction of
the eggs is either protein or lipid. For late
stage larvae we have also assumed that carbo-
hydrate is absent, but that some chitin is pre-
sent because they form integument and molt

once before they are released. We have as-
sumed that the organic fraction of the larvae
contains half the amount of chitin as the adults,
or 4 %.

The protein-lipid composition of the eggs was
calculated from the carbon content of the ash-
free fraction. We have estimated (above) that
36.4 % of the mysid protein is composed of
carbon, that 77 % of the lipid is carbon, and
that 61.8 '~r of the ash-free egg is carbon. By
using these values we calculate that the organic
fraction of the eggs is 62.5 % lipid and 37.5 %
protein. The carbon content of intermediate
age brood pouch young (about 5 days old) was
less than that of eggs and more than that of
late stage larvae. For these intermediate age
young we calculate a lipid content of 43 %.

ENERGY CONTENT

Juveniles - Adults

The ash-free calorie content of Metamysidop-
sis was determined in a Parr non-adiabatic cal-
orimeter. The data, converted to ash-free
values, are given in Table 4. Three of the
samples contained so little material that Nujol
supplement had to be added to raise the heat of
combustion to a measurable level. All three of
these measurements fell outside the 95 % con-
fidence limits of the six determinations made
without the Nujol supplement. The variability
among the three supplemented determinations
can be attributed to the ± 2 % variation of the
caloric content of the Nujol supplement (10,791
± 200 cal/g) , because the weight of the supple-
ment greatly exceeded the weight of the sample
material in each case.

Table 4. — Ash-free' caloric content of Metamysidopsis.

Specimens

Dry
weight

Calorie
content

Ms

Cal/i

Young juveniles

1.0S

23028.9

Juveniles

2.45

=6462.6

Young females

4.80

=4242.3

Advanced juveniles

12.55

5021.7

Immature males

1 7 JO

5049.0

Immature moles

17.30

5358.0

Mature males

15.75

51238

Mature females

12.40

5185.7

Mature females

17.25

5699.1

^ Ash content 12.5 % used in all calculations.
2 Nujol supplement used in determinotions.

107

FISHERY BULLETIN: VOL. 69, NO. 1

The mean for the six nonsupplemented sam-
ples is 5,240 cal/g (shown as 5.24 cal/mg in
Table 3). No significant differences in energy
content among developmental stages nor be-
tween sexes were found.

This mean calorie content estimate is some-
what lower than those reported for other Crus-
tacea. Slobodkin and Richman (1961) gave
values of 5.4 to 5.6 cal/ash-free mg; Lasker
(1965) reported a range of 4.9 to 5.4 cal/mg (in-
cluding ash) for two species of copepods. Our
mean value is also lower than the value that can
be calculated from the information on body
composition, together with reported average
values of the calorie content of animal pi-otein,
fat, and carbohydi'ate. Conversion factors given
by Horowitz (1968) are: protein, 5.5 cal/mg;
fat, 9.3 cal/mg; and carbohydrate, 4.1 cal/mg.
Since chitin is glucosamine, we have assumed
that it, like carbohydrate, has a calorie content
of 4.1 cal/mg. From these conversion factors
and the composition data given in Table 3, we
calculated an expected value of about 5.77
cal/ash-free mg.

We use the empirical value, 5.24 cal/ash-free
mg, in our subsequent energy budget calcula-
tions. We consider this to be a conservative
estimate, because it assumes that the mysid pro-
tein has an energy content of only 4.8 cal/mg.
This lower than expected estimate may be re-
lated to the empirical observation that the mysid
protein contains only 36 9^ carbon, rather than
about 50 % as is commonly assumed for animal
protein.

The juvenile and adult Metamysidopsis con-
tained 12.5 % ash; therefore, the energy in the
whole dry body of an adult or juvenile is esti-
mated to be: (4.6 cal/mg) x (dry weight,
mg).

Molts

We estimated the energy content of molts in-
directly, because it was difficult to obtain enough
material for calorie measurements. The ash-
free fraction (55 '.i ) of the molts was estimated
to be composed of 44 % chitin and 56 9ir protein.
By assuming that chitin has an energy content
of 4.1 cal/mg, and that the mysid protein has
an energy content of 4.8 cal/mg, we calculate

that the ash-free fraction of the molts has an
energy content of 4.5 cal/mg.

From a sample of 10 animals and their molts
we found that the dry weight of molts is on
the average 13 % (range 9-19 /r) of the dry
weight of the animals that shed them. Lasker
(1964, 1966) and Jerde and Lasker (1966)
found that the dry molts of a euphausiid were
about 10 % of the dry weight of the animals
that produced them (range 4-14 %).

The energy lost by molting Metamysidopsis
is thei'efore proportional to the size of the
animal:

(0.13) (0.55) (4.5 cal/mg)

X (dry weight of animal, mg)
or

(0.32 cal/mg) x (dry weight of animal, mg).

Eggs and Larvae

We estimated that eggs were 6 ^r ash, 35 %
protein, and 59 % lipid. The energy content of
an egg is estimated to be: (0.35) (4.8 cal/mg)

+ (0.59) (9.3 cal/mg) = 7.16 cal/mg. A
sample of 140 eggs was dried and weighed; the
mean dry weight per egg was 0.0055 mg. The
energy content per egg is tlierefore 0.039 cal-
orie.

We estimated that, just before being released
from the brood pouch, the larvae are about 6 %
ash, 61 '"r protein, 29 Sr lipid, and 4 ''/c chitin.
The energy content of a late stage larva is esti-
mated to be: (0.61) (4.8 cal/mg) + (0.29)

(9.3 cal/mg) + (0.04) (4.1 cal/mg) = 5.78
cal/mg. The mean dry weight per larva, esti-
mated from 110 individuals, was 0.0051 mg.
The energy content per larva is therefore 0.029
calorie.

ENERGY BUDGET AND
EFFICIENCY OF ENERGY TRANSFER

From the data on average growth, age-spe-
cific fecundity, respiration rate, and energy con-
tent we have calculated cumulative curves of
energy use by individual mysids in attaining
various stages of development. Data on age-
specific natural mortality rates (Fager and Clut-
ter 1968) were used to estimate Ix (probability

108

CLUTTER and THEILACKER: PELAGIC MYSID SHRIMP

of animal being alive at age x) schedules and
average generation time of the field population.
The field and laboratory data were combined in
an analysis of the efliciency of energy transfer
through the Metamysidopsis population to the
organisms that feed on them.

CUMULATIVE ENERGY CURVES

At age zero the egg contains about 0.04 cal.
Ten days later, at the time it is released from
the brood pouch, the larva contains about 0.03
cal. Thereafter the average calorie content in-
creases in proportion to the dry weight (4.6 cal/
mg). The average schedules of energy incor-

16

-

U

-

1

12

-

/

10

-

/

5

a

/

>.

1

c

1 respiration

6

-

/ /

4

2

0

" ,^

/ y//^^.^^'^ growth

1 1 1

0 10 30 50 70 90

Aga Idon)

Figure 12.— Cumulative energy used by individual Meta-
mysidopsis females. The curves are additive, i.e. the
space between the lower two curves represents the
cumulative energy lost in molts, the next higher space
represents energy used to produce eggs (both fertilized
and unfertilized), etc. — so that the upper curve repre-
sents cumulative energy used for all processes.

poration differ between males and females after
about 30 days; the rate of incorporation becomes
lower and levels off sooner in males. The ac-
cumulation of body energy is shown as the low-
est curves in Figure 12 (females) and Figure
13 (males).

The amount of energy lost in molts varies
with age because the size of the molt increases
and the molting frequency decreases. Females
and males have different cumulative losses of
energy from molting because their growth rates
are different after age 30 days, and their molting
frequencies are different (Table 1.) Although
the actual loss of energy in molting occurs at
discrete intervals, we have plotted the cumula-
tive energy loss as smooth curves, because the
accumulation of energy for integument forma-
tion probably is continuous. Cumulative energy
loss in molting is shown as the second curve in
Figure 12 (females) and Figure 13 (males).
The cumulative energy curves are additive, i.e.
the area between the first curve (body energy)
and second curve (molting energy) represents
the cumulative energy loss in molts.

Figure 13. — Cumulative energy used by individual Meta-
mysidopsis males. The curves are additive (see Fig. 12) .

109

FISHERY BULLETIN: VOL. 69. NO. 1

Males use a small amount of energy in pro-
ducing sperm, but we assume that this is negli-
gible. In females, the ova begin to be infused
with yolk about age 45 days. The actual dis-
charge of eggs occurs at discrete intervals of
about 10 days, beginning at age 53 days. We
assume that the accumulation of energy for re-
production is more continuous than this, there-
fore we have shown reproductive energy use as
a smooth curve. The reproduction energy curve
shown in Figure 12 is based on the maximum
fecundity estimate given previously [number of
eggs = 4.1 (body length, mm) — 8.9]. A repro-
duction energy curve based on our minimum es-
timate of fecundity [number of eggs = 4.1 (body
length, mm) — 12.0] would be 0.12 cal (3.1
eggs) lower per spawning. This would make
the minimum estimate 72 Sr of the maximum
estimate at the age of first spawning (53 days)
and progressively higher in percentage there-
after, e.g. 85 9f at the age of fifth spawning
(93 days). All our reproduction energy cal-
culations take into account the observation that,
on the average, mature females extrude the usual
number of eggs only one-half of the time and
otherwise extrude only one-half the usual num-
ber of eggs.

The amount of energy used in respiration was
calculated from the weight-specific respiration
equation: R' — 2.1 (dry weight, mg)-"'^^ and
from energy conversion factors based on our
estimates of body composition.

We do not know what substrate Metamysidop-
sis catabolizes. The organic fraction of the body
is largely protein; the storage ])roduct (carbo-
hydrate and lipid) content is low. Raymont
and Krishnaswamy (1960) observed that the
carbohydrate content of Neomysis integer de-
creased slightly, from about 1.30 % (of dry
weight) to 1.06 ^(, when a marked reduction
in feeding occurred. For the same species, Lin-
ford (1965) found no significant change in lipid
level whether the animals were starved, fed a
lipid-free diet, or fed a high lipid diet. Raymont
et al. (1968) asserted that N. integer uses pro-
tein as an energy source.

We agree with Linford (1965) that it seems
likely that the mysids must live largely on their
daily ingestion. We think that the food they

ingest has composition similar to their bodies.
Therefore, our energy calculations assume that
they use catabolic substrates in proportion to
their presence in the body. This is supported
by the results of Jawed (1969). To convert
the amount of oxygen used in respiration into
the equivalent energy lost as heat we have used
the following values for calories lost//il Oq con-
sumed (Hawk et al., 1954; Prosser, 1950):
protein, 4.5 X 10"^; lipid, 4.7 X lO"'; car-
bohydrate, 5.0 X 10 ~^ Therefore, our esti-
mate of the average amount of energy used in
respiration is about 4.5 X 10""'cal /A O2.

The cumulative energy used in respiration is
shown as the uppermost curve in Figure 12
(females) and Figure 13 (males). The area
between that curve and the next lower curve
represents the catabolic heat loss. These res-
piration data were calculated for a temperature
of 16° C, which was the median temperature
of the natural environment of Metamysidopsis.
Our respiration measurements were made in
flowing water during the daylight hours. There-
fore, they represent basal metabolism + energy
expended in active swimming. There is some
evidence (Clutter, 1969) that the mysids may
be less active at night, even though they con-
tinue to swim at all times. For this reason we
think that the field population may use some-
what less than this amount of energy in respir-
ation.

Our estimated rate of energy loss in catabo-
lism is higher than that estimated by Jawed
(1969) in his study of nitrogen excretion in
Neoviysis rayii. He suggested that protein is
catabolized in relatively large quantities, there-
fore nitrogenous excretion may provide a good
estimate of catabolism. He found an average
catabolism of about 2.5 % of body nitrogen
per day in adult animals that were probably 8
to 10 mg dry weight, that were held at 10° C.
The rate for adult Metamysidopsis of average
size (0.6-0.8 mg) was 5 to 6 % of the body
energy i)er day. This disparity in catabolism
may result from diff'erences between the size
and between the environmental temperatures
of the two species.

Jawed (1969) showed that about 15 % of the
nitrogen was excreted as amino acids. We did

110

CLUTTER and THEILACKER: PELAGIC MYSID SHRIMP

not investigate this in Metamysidopsis, there-
fore, our estimate of total catabolism could be
slightly low because it includes only losses of
heat energy.

NET ECOLOGICAL EFFICIENCY
Mortality and Generation Time

Estimates of natural mortality in the field
population were made during the same period
that the laboratory growth experiments were
done (Fager and Clutter, 1968).

Brood pouch mortality rate was estimated to
be 0.013/ day (maximum of 0.017/day). Mor-
tality rates for juveniles, immatures, and adults
were estimated from consecutive series of field
collections. The field mortality rates varied
during the year. Survival curves (Ix = proba-
bility of being alive at age x) for periods of
at least mortality, median mortality, and great-
est mortality are shown in Figure 14. The mor-
tality rates that we used to calculate these Ix
curves are shown in Table 5. The greatest
mortality rate results in a declining population;
at the median mortality rate the population size
remains about constant; and at the least mor-
tality rate the population increases.

An average female first reproduces at about
age 53 days. The generation length for the
population is somewhat longer because the fe-
males reproduce more than once. The gener-
ation length for the field population varied be-
tween 67 days and 71 days; the median was 68
days (Fager and Clutter, 1968).

Figure 14. — Age specific survival (l^ = probability of
being alive at age x) of Metamysidopsis calculated from
estimates of greatest, median, and least mortality in the
field population (Table 5).

Table 5. — Mortality rates (per day) used to calculate
Ir schedules for the Metamysidopsis field population.

Least

Median

Greatest

Specimens

mortality

mortality

mortality

Brood pouch young

0.013

0.013

0.017

Juveniles

0.02

0.06

0.15

Immatures

0.02

0.05

0.14

Adults

0.02

0.04

0.13

Relative Energy Use by Individuals

We determined the calories of energy used
by average individual female and male mysids,
and the fractions used for growth, molting, re-
production, and respiration from the estimates
of cumulative energy use (shown in part in
Figures 12 and 13). The amounts and the per-
centage distributions required to reach selected
stages of development are shown in Table 6.

Table 6. — Energy used by individual Metamysidopsis to reach selected
stages of development.

Age

Energy

Relative use

Respira-
tion

Repro-
duction

Molt,
ing

Growth

Days

Cat

%

%

%

%

Females:

Egg yolk production
First reproduction
Generation
i^ = 0.0 1

45

53

68

1103

2.7
4.6
8.7
18.4

52
49
50
55

0
9
15
19

8

7
7
7

40
35
28
19

Males:

Maturity
/^ = 0.01

48
1103

3.0
12.8

54
67

0
0

10

12

36
21

* Approximate age at which l^ = 0.01 in a nearly stable population (r-».0).

Ill

FISHERY BULLETIN: VOL. 69. NO. 1

The indicated age at which the probability of
being alive reaches 0.01 applies to the stable
population (median death rates).

The males require less energy to reach ma-
turity than females, but relatively more of this
energy goes into molting and respiration and
less is incorporated. Two-thirds of the energy
used in reproduction remains in the population;
one-third is lost as unfertilized eggs.

The estimates of relative use of assimilated
food by Metamysidopsis females during a life
span are compared with estimates for a copepod
and a euphausid (Corner, Cowey, and Marshall,
1967) in Table 7. The mysids apparently use
a fraction of assimiliated energy for growth that
is intermediate between the other two species,
a lower fraction for metabolism, and a higher
fraction for producing eggs.

Table 7. — Use of assimilated food by Metamysidopsis
females (life span 103 days) compared with the copepod
Calanus finmarchicus^ (life span 10 weeks) and the
euphausid Euphausia pacifica' (life span 20 months).

Assimiloted
energy used by
Metamysidopsis

Assimilated

N used by

Calanui

Assimiloted
C used by
Euphausia

Growth

%

19

%
25.3

%
10.1

Metabolism

55

61.4

72.3

Molts

7

0.9

\6.6

Eggs

19

12.4

1.0

* From Corner, Cowey, and Morshcll (1967).
- From Losker (1966), revised in Corner et al.

Relative Energy Use by the Population

The values of relative energy use given in
Tables 6 and 7 apply to individuals, or to pop-
ulations wherein all members live a full life
span. They do not apply to the natural popu-
lation, because some die during all stages of
growth.

We have estimated the relative amounts of
energy that would be lost by populations in res-
piration, production of infertile eggs, molting,
and mortality at the observed minimum, median
and maximum mortality rates shown in Table 5.
This was done by calculating the fraction of
the population that died during each intermolt
period (A/^), and multiplying this times: (1)
the mean body energy content for the midpoint
of that period, (2) the quantity of cumulative
energj' lost in infertile eggs \x\) to the midpoint

of that period, and (4) the quantity of cumula-
tive energj' used in respiration up to the mid-
point of that period. The product values for
each of these loss categories (mortality, molting,
etc.) were then summed over all ages (to Zx ^
0.001). The relative energy use values were
calculated as fractions of the overall sum for
all categories combined. We excluded fertilized
eggs because this reproduction energy is retained
in the population.

The age specific distribution of energy use
(representing energy loss, because fertilized
eggs are excluded) by a population (females
and males) of Metamysidopsis at the median
mortality rate is illustrated in Figure 15. All
the curves are plotted with reference to the base
line, zero. The rate of energy loss is low among
eggs and larvae, and much higher among the
juveniles that have just emerged from the
brood pouch and begun to swim. In the larger
animals, the respiration per unit weight is low-
er, but the respiration per animal is higher, so
that the respiration rate per day is highest
among the animals that are about 25 days old.
The loss of energy per day from all causes is
highest among the animals that are about 30
days old. After this the curve declines because
the effect of larger size becomes less than the
effect of smaller numbers.

The estimated relative amounts of energy
lost by the population of females, males, and
both sexes combined, for each loss category and

Ao* Id

Figure 15. — Age specific distribution of energy loss by
a Metamysidopsis population at the median mortality
rate. Production of fertilized eggs is excluded.

112

CLUTTER and THEILACKER: PELAGIC MYSID SHRIMP

for each of three mortality rates, are shown in
Table 8. The percentages for females and males
combined are not quite the same as the means
of the separate pei-centages for females and for
males. At the minimum death rate 55 S^ of the
energy loss would pass through the female half
of the population (58 ^'r if fertile eggs are in-
cluded). At the median death rate 52 Sr would
pass through the females, and at the maximum
death rate, 50 %.

Table 8. — Relative amount (%) of energy lost by
Metamysidopsis populations in respiration, production
of infertile eggs, molting, and mortality; at minimum,
median and maximum mortality rates.

Sex

Death
rate

Respira-
tion

Infertile
eggs

Molting

Mortality

%

%

%

%

Females

minimum

63.7

6.7

8.6

20,9

median

55.6

3.7

7.7

33.0

maximum

45.4

0.1

6.1

48.4

Moles

minimum

67.4

0.0

12.6

20,0

median

58.3

0.0

9.9

31.8

maximum

47.9

0.0

6.5

45,6

Females and

minimum

64.5

3.7

10.4

20,5

Males

median

56.9

1.9

8.8

32,4

maximum

46.7

0.1

6.3

47.0

If we assume that all the mortality is yield
to predators (Odum and Smalley, 1959; Engel-
mann, 1961), our mortality fractions are an
estimate of net ecological efficiency (energy
yield/energy assimilated). Apparently some
Crustacea regularly die from natural causes
other than mortality (e.g. Daphnia, Slobodkin,
1959). Many mysids of all ages died in our
laboratory cultures, but we do not attribute this
to senescence. In the field and in the laboratory
we observed Metamysidopsis much older than
the oldest animals that are involved significantly
in our energy calculations. Our best estimate
of the net ecological efficiency of the mysid pop-
ulation, for transfer of energy to a higher troph-
ic level, such as fishes, is about 32 'Jr. The net
efficiency of transfer to all trophic levels is
1 — respiration fraction = 43 S^-

ASSIMILATION AND
GROSS ECOLOGICAL EFFICIENCY

Assimilation Efficiency

Gross ecological efficiency (energy yield/en-

ergy ingested) is the product of net ecological
efficiency (energy yield/energy assimilated) X
assimilation efficiency (energy assimilated/en-
ergy ingested). Therefore, an estimate of as-
similation efficiency is required to estimate gross
ecological efficiency for the mysid population.

We attempted to estimate the assimilation ef-
ficiency of Metamysidopsis directly by a carbon-
14 method described by Lasker (1960). This
failed because .the mysids did not filter sufficient
amounts of radioactive phytoplankton. An ex-
periment with another member of the family
Mysidae, taken from the same area, was suc-
cessful. This gave an estimate of 90 Tr assim-
ilation efficiency.

Lasker (1966) obtained a similar high value
(84 Cf ) for the morphologically similar Eiiphau-
siapacifica; and Marshall and Orr (1955) found
values greater than 90 % for the copepod Cal-
ami^ finmarchicm. In his detailed reviews of
assimilation in zooplankton, Conover (1964,
1966) suggests that these values probably are
too high. The very large number of observa-
tions, many of them his own, that are cited by
Conover seem to be evidence that, although var-
iable, the mean assimilation efficiency for crus-
tacean zooplankton is at least 60 % and perhaps
greater.

Gross Ecological Efficiency

From the information presently available we
consider that the assimilation efficiency of the
mysids is between 60 9f and 90 ^r. Our best
estimate of net ecological efficiency (yield/as-
similated) is 32 Sf. Therefore, the minimum
estimate of gross ecological efficiency (yield/in-
gested) is 19 9r and the maximum estimate is
29 ^c.

These estimates are well within the broad
range of available estimates of gross ecological
efficiency (see reviews by Patten, 1959; Slobod-
kin, 1961; Phillipson, 1966; Reeve, 1966), and
within the range of 8 '^'r to 30 'c that Engel-
mann (1961) considers to be acceptable. They
are about 2 to 3 times as high as the median
value of 10 % that is suggested by Slobodkin
(1961, 1962) , but lower than the values of 30 %
to 50 % suggested for marine zooplankton by

113

FISHERY BLXLETIN: VOL. 69, NO. I

Ketchum (1962), Steemann Nielsen (1962), and
Curl (1962b).

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115

A LINEAR-PROGRAMMING SOLUTION TO SALMON MANAGEMENT'

Brian J. Rothschild^ and James W. Balsiger"

ABSTRACT

A linear-programming model was constructed to allocate the catch of salmon among the days of the
salmon run. The objective of the model was to derive a management schedule for catching the salmon
which would result in maximizing the value of the landings given certain constraints. These con-
straints ensured that cannery capacity was not exceeded, and that escapement of both male and fe-
male fish was "adequate." In addition to considering the allocation of the catch in the primal problem,
the dual problem considered the shadow prices or marginal value of the various sizes of fish, eggs,
and cannery capacity, thus enabling the manager to view his decisions in light of the marginal values
of these entities. As an example, the model was applied to a run of sockeye salmon in the Bristol Bay
system. In the particular example, which was chosen to replicate the 1960 run, the additional value
of the catch owing to optimality amounted to an ex-vessel value of a few hundred thousand dollars.
In addition it appeared that the required processing time could be reduced by several days. The op-
timum allocation was obtained through conformance to the linear-programming model. The cost of
this conformance was not, however, determined.

The Pacific salmon fisheries have been cited as
an example of irrational conservation (Crutch-
field and Pontecorvo, 1969). Much of this ir-
rationality is reflected in the dissipation of
a sizable fraction of the available economic
rent, a situation which results from the open-
access nature of the fishery and legislated in-
efficiency. The remedy for this situation is
to alleviate the open-access and inefficiency
problem. Such alleviation would require the
dissolution of rather formidable institutional
problems. In the present paper, we examine
the salmon problem from a slightly different
vantage point than Crutchfield and Pontecorvo.
We examine the salmon problem under the
status quo; we do not consider the optimal
amount of gear or its efficiency (this should
not, however, be construed as reflecting any
diminution in the importance of these prob-
lems); rather we consider, as an interim ap-
proach, whether it is possible, under the strin-
gent condition of knowing in advance the
structure of the run, to increase the value of
the fish on the dock by optimally allocating the

' Contribution No. 333, College of Fisheries, Uni-
versity of Washington.

" Center for Quantitative Science and Fisheries Re-
search Institute, University of Washington, Seattle,
Wash. 98105.

' Fisheries Research Institute, University of Wash-
ington, Seattle, Wash. 98105.

catch among the days of the run.

The traditional approach to salmon manage-
ment might be considered, at the risk of several
simplifications, as consisting of (1) forecasting
the magnitude of the run ; (2) setting an escape-
ment goal and a catch implied by the forecast
and the escapement; and (3) daily fishing
closures and other devices which allocate the
catch in varying quantities to the days of the
run. The traditional approach, then, also in-
volves an allocation of the catch to the days
of the run. In the traditional approach, the
allocations are usually based on the experience
of management biologists. Although the ob-
jectives of their allocations are not always
clearly and explicitly stated, there is a tendency
for the primary objective of management to be
simply the attainment of the escapement goal.
Our approach is to use the theory of linear pro-
gramming to advise on a non-intuitive optimum
allocation of the salmon catch among the days
of the run where the objective of management
does not explicitly involve escapement. Rather,
we develop our allocation strategy to maximize
the value of the catch on the dock given a va-
riety of constraints which include the necessity
for a given number of fish to escape the fishery.
The objective of maximizing the value of the
fish on the dock and the constraints explicitly
define the objectives of the management scheme.

Manuscript received October 1970.

FISHERY BULLETIN: VOL. 69. NO. I, 1971.

117

FISHERY BULLETIN; VOL, 69. NO. I

We consider these problems in three additional
sections. In the first, we describe the linear-
programming allocation model, which we be-
lieve to be applicable, with simple modifications,
to a variety of salmon management situations.
In the second, we consider how the model might
be applied to a run of salmon in the Naknek-
Kvichak system of Bristol Bay, Alaska. As an
example, we choose data from the 1960 run
to that system and obtain an optimum allocation
of large and small, male and female fish, on each
day of the run to the daily catch. This optimum
allocation served to maximize the value of the
fish on the dock subject to constraints which
ensured that the catch did not exceed the daily
run, that the catch would be less than the can-
nery capacity, and that an "adequate" escape-
ment, both in terms of the number of eggs and
sex ratio, passed the fishery. Thus, in addition
to managing the run by a non-intuitive optimum
allocation and satisfying an escapement goal,
we also considered the quality of the run in terms
of its sex and age composition. In order, how-
ever, to achieve this optimum allocation we
needed certain data on the structure of the run
in advance and we also needed a mechanism
by which we could select large and small male
and female fish. It would most likely be im-
practical to have either a precise prediction of
the daily run or an ability to select, with high
precision, large or small, male or female fish.
We show that even if we had the necessary data,
a technique for precise selection of the various
entities of fish, and maintained the 1960 escape-
ment and sex-ratio conditions, optimum alloca-
tion would yield us a catch having a value of
several hundred thousand dollars more than the
actual catch. Thus given the cost of obtaining
the necessary information to perform the op-
timum allocation and the constraints extant in
1980, it is questionable whether biological man-
agement could yield a better allocation than that
which was obtained. This serves to re-empha-
size the approach of Crutchfield and Pontecorvo,
indicating that the system is most sensitive to
variables which lie outside the objective and
constraint equations specified in the present
paper. On the other hand, our results show
that it is possible, at least in terms of the model.

to reduce the number of days during which the
cannery operates and yet process the same num-
ber of fish. Furthermore as previously indicated,
we constrained our example to fit the statistics
of the 1960 run and thus we had, in our ex-
ample, a nearly 1:1 sex ratio; but as we indi-
cate later, we could have caught a considerably
larger number of male fish and still would have
had sufficient male fish in the escapement to en-
sure the efficient production of fertilized eggs.
And finally the model was quite sensitive to de-
creasing the escapement but unfortunately there
is little guidance in the literature which would
indicate the optimum escapement for the Nak-
nek-Kvichak system and furthermore there ap-
pears to be little hope of learning the magnitude,
in the reasonably near future, of the optimum
escapement for the Naknek-Kvichak system.
Thus evaluation of the cannery processing time,
catch problem, and relaxation of sex ratio and
escapement constraints might result in an ad-
ded value to the catch which would make some
attempts at allocation practical. We also, in
the second section, place some stress on in-
terpretation of the shadow prices of the var-
ious variables in the problem. This is of in-
terest to operations researchers because it
provides an example, in addition to those con-
ventionally used, of an application of the inter-
pretation of the linear-programming primal-
dual relation. The shadow prices are of interest
to the fishery manager because from them it is
possible to impute values to the various resources
under the manager's control, and, in making a
decision, the manager can thus consider these
values which, as we show, are not always intui-
tively obvious. In the third and final section
we conclude the paper with a general discussion
of salmon management in a linear-programming
setting.

MODEL

Most linear-programming models generally
involve finding values A'j which maximize (or
minimize) an objective function i;r,A',-, subject
to a set of constraints each of which has the
form :^PiXi « Lj, where the inequality can be
in either direction or can, in fact, be an equality.

118

ROTHSCHILD and BALSIGER: LINEAR-PRCXSRAMMING SOLUTION

The Pi's and the L/s are constants appropriate
to a particular problem. The details of the LP
(linear-programming) procedure can be found
in the many treatises on the subject (e.g., Gass,
1964) or in most texts on operations research
(e.g., Hillier and Lieberman, 1967).

In our application of the LP model, we max-
imize the following objective function

A/ N

Z = I Z CijXij, (1)

where M refers to the total number of age-sex
categories and N refers to the days of the run.
The variable A',,- is the number of fish caught
in the ith entity on the jth day of the run and
cij corresponds to the value of the fish caught
in the ith entity on the yth day (Table 1). The
age-sex category classification results from the
fact that salmon runs are comprised of a va-
riety of age-groups. Because each age-group
is usually of a different average size, the indi-

Table 1. — Linear program model notation.

Af — The total number of age-sex categories.

N — The total number of days in the run.

Xij — The number of fish in the t'th oge-sex category which are
caught on day ; of the run.

C-- — The value of a fish caught in the tth oge-sex category on

day y of the run.

R — The number of fish in the ith age-sex category which run past

the fishery on day ; of the run.

Kj — The copocity, in numbers of fish, of the canneries on day ;'

of the run,

K — The total seosonol copocity of the canneries in numbers of fish,

J¥^j — The number of fish of the ith oge-sex category in the escape-
ment on day ;' of the run.

a — The overage number of eggs in each fish of the ith oge-sex

category.

T — The total number of eggs contained in the escopement and

catch.

£ — The minimum number of eggs required in the escapement,

^ — The totol number of moles in the escapement and catch.

F — The average fecundity of the female oge-sex cotegories, ex-

pressed in number of eggs,

f{ — The sex ratio desired in the escapement, expressed as the

number of females per mole.

/.,- — The number of fish of the ith oge-sex category desired in

the season's escapement.

S — The number of fish in the totol season run of the ifh oge-sex

category,

P(j) — The proportion of the run thot arrives by doy ; of the run.

P' (j) — The proportion of the run that orrives on day > of the run.

viduals in each age-group also have a different
average value which we denote by cij. It should
be mentioned that size is not the only criterion
which can be used for classification. For ex-
ample, in the Naknek-Kvichak run of Bristol
Bay, the sex of the fish can also be used be-
cause within an age-group the male fish tend to
be larger than the female fish and thus more
valuable in terms of weight of fish-flesh; but,
on the other hand, the eggs of the females are
a valuable commodity and thus the per-pound
value of females may be greater than the per-
pound price of males. If the value of the fish
were constant during the course of the run, we
could replace the C;j with Cj and the allocation
problem would become rather uninteresting.
But the value, however, does tend to vary dur-
ing the course of the run. One reason for this
is a deterioration of the quality of fish, as in-
dicated by declining oil content and reduction
in color intensity with the progression of the
run. Another way in which Cy could vary is
that the average value of the fish on a par-
ticular day would tend to vary during the course
of the run because of a within-entity trend in
the average size of the fish during the course
of the run; this, however, is not considered in
the present paper. It is obvious that, if we
had sufficient information, we could establish
a large number of different c,/s.

As indicated previously, equation (1) is max-
imized subject to a variety of constraints. For
the salmon problem, the first set of constraints is
rather obvious and constrains the catch, of any
entity, on any day, to be less than, or equal to,
the number of fish in that entity in the run.
These constraints are of the form

<Y„

(2)

Xij is always ^ 0 and Rij is the number of fish
of the ith entity which run past the fishery
on the yth day. There can be as many asM x N
constraints of this form, but in some applica-
tions, either the number of entities or the num-
ber of days will be collapsed owing to either the
nature of the problem or a lack of information.
Note also we can easily "close" the fishery for

119

FISHERY BLLLETIN: VOL. 69, NO. 1

any entity or all entities on any day simply by
setting the appropriate Rij = 0.

The second set of constraints constrains the
catch on any day to be less than the daily ca-
pacity of the canneries. Thus, we have the set
of constraints,

M
i = \

K:

(3)

where Kj is the capacity of the cannery or can-
neries on the yth day. Another form of this
constraint might be incorporated in situations
such as in the Bristol Bay fishery, which has a
short season, is remote from supply points, and
thus has a finite seasonal capacity; these con-
straints can be expressed by

I L A',

(4)

/ = i

= 1

The constraint is redundant if K ^ L Kj.

J = I
and hence is only used when the season's ca-
pacity is less than the sum of the daily capa-
cities, i.e.,

K'

Ki.

y=i

The next set of constraints results from the
need to ensure that an adequate number of fish
escape the fishery and are thus permitted to
spawn. We formulate this constraint in terms
of the egg complement of the number of females
escaping the fishery rather than the number of
females escaping per se or the total number
of fish (males and females) escaping.

In order to formulate this constraint set, we
define T as

XL ajWij + LXa//Yy = T

(5)

where a; is the average number of eggs in each
fish in the ith entity, Wij is the escapement of
fish in the /th entity on the jth day and thus

T is the egg complement of the escapement and
the catch. Now if we need a minimum number
of eggs to represent the escapement, a quantity
which we denote by E, we must have

ZZa,H',/ & E.

(6)

So substitution of (6) into (5) yields the con-
straint set conformable to the Xi/s of our other
constraints, viz.

ZI a,Xii ^ T-E.

(7)

We can see that by using the same reasoning we
could construct a consti'aint set which would
constrain the egg complement to be less than
some maximum egg complement.

Our next constraint involves the sex ratio of
the spawning fish. The utility of allowing a
particular egg complement to escape the fishery
could be negated by not allowing a sufficient
number of males to escape for the purpose of
fertilizing the eggs. In order to ensure that
an adequate number of males escape the fishery,
we formulate the necessary constraint by noting
that

Z M'/ + Z Xj = .^i

(8)

where in this particular equation the TF's refer
to the number of males in the escapement and
the A'''s to the number of males in the catch and
M to the total number of males in the run. Now
to satisfy our constraint, we must have

ZlV,

£ X /y

(9)

where the sum extends over all male entities
and days of the run; F is the average fecundity
of the female entities in the run, and H is the
desired male to female sex ratio. Substitution
of (9) into (8) then yields the desired con-
straint

Z,V,y

J(

£,■ X W

(10)

120

ROTHSCHILD and BALSIGER: LINKAR-PROGRAMMING SOLUTION

This constraint can also be formulated in a va-
riety of ways.

In addition to escapement goals established
in terms of eggs and a sufficient number of males
to fertilize the eggs, we desired to establish, for
some sample problems, escapement goals in
terms of total numbers of fish of each entity
in the escapement; this would greatly simplify
the simulation of the actual escapements for any
historic salmon season. Hence, we developed
the constraint

m

^W„

maximize 2- r,vV/

(11)

( = /

m

subject to Z, fl//'V, ^ /),
/ = l

j=\ n (14)

where we have used slightly different notation
than in the salmon problem, but the analogue
between (14) and the salmon problem should,
nevertheless, be quite clear. If (14) is the
primal, then the dual of this primal is

where L; is an escapement goal set for entity
i which would ensure escapements identical with
any historic year. To make (11) conform to
our constraint set, we note that

inimize L ^jYj

Zn-'y +Y.Xij = Si

(12)

where Wij and Xij are the escapement and catch
(respectively) of entity / on day j and Si is the
total season's run of entity (', we can substitute
(11) into (12) and get the constraint in the
proper form:

Li.

(13)

Thus a seasonal limit can be placed upon the
catch of any entity /.

As indicated earlier, once the objective func-
tion and the constraints have been formulated,
then optimization of the objective function, given
the constraints, is a standard procedure out-
lined in some detail in the literature, and, with
a computer facility, is a relatively simple task.
There are. however, interpretations which are
of further interest than the solution of the ob-
jective function. These interpretations rest in
the primal-dual relationship of the LP problem.

In order to demonstrate this relation, we will
denote a general form of the primal problem as

./ = l

subject to L aijYj ^ c,

/ = l m (15)

In the primal we are allocating scarce resources,
the hj's (number of fish in the run. cannery
capacity, egg complement, and male fish) , among
the / activities (which consist in our problem
of catching a particular entity of fish on a par-
ticular day). The intensity of the activity is
Xi, the catch of the ith entity on the yth day
and the "profit" per unit of the activity is, of
course, cj. It might be mentioned at this point
that most LP computer codes provide as out-
put the value of slack variables which in (14)
is the difference between the right-hand side
and the left-hand side of the constraint equa-
tions. The slack variables have a rather im-
portant interpretation for the salmon problem
in that the slack variable in the run constraint
(2) is the escapement; in the cannery con-
straint (3), it is the unused capacity of the
cannery which we might want, in viewing the
problem from a different context, to minimize;
in the egg constraint (7), it is the number of
eggs which are not caught that could be caught
— another quantity which we might wish to
minimize — and finally we have the slack var-
iable associated with constraint (10) denoting
the number of males which are not caught, but

121

FISHERY BULLETIN; VOL. 69, NO. 1

could be caught, and which we might, similarly,
wish to minimize. Thus, for example, we simul-
taneously derive, by virtue of the LP model, as
we have formulated it, both the escapement and
the catch.

Now, in the dual, we can place unit values
on the scarce resources rather than on the levels
of the activities, as in the primal. It is thus
helpful, in making management decisions, to
know the imputed unit value of a unit of cannery
capacity, a large male fish, an egg, etc. These
imputed values are commonly known as shadow
prices and correspond to the optimal values of
the Yj's in (15) ; they will be discussed briefly
in our interpretation of the salmon model. It
should also be mentioned that we have slack
variables in the dual formulation just as we had
slack variables in the primal.

The dual slack variables can be viewed as
opportunity costs in the sense that if we fail
to meet a constraint, this is an opportunity
foregone ; and the dual slack variable then gives
the value foregone by the "bad" management
either of nature (that is, the vagaries induced
in the system which are uncontrollable by the
management agency) or of the management
agency.

Finally, it is worth noting a feature of the
shadow prices vis-a'-vis the relation of the right-
and left-hand side of the constraint equations.
If in some solution of a particular problem, the
right-hand side becomes equal to the left-hand
side, then we say the constraint is binding. If
the constraint is binding, then the shadow price
has some positive value, namely the imputed
value of an additional unit of scarce resource;
but if, on the other hand, the constraint is not
binding, then an additional unit of the resource
is "free" within the bounds of the problem for-
mulation— consequently the shadow price of the
free resource is zero.

EXAMPLES BASED ON THE
NAKNEK-KVICHAK RUN

As an example, we have decided to consider
the implications of a LP ajipi'oach to implement-
ing the management framewoik of one of the
most important salmon runs in North America,

the sockeye salmon run to the Naknek-Kvichak
system of Bristol Bay, Alaska. Our approach
was to use the LP model described in the pre-
vious section employing actual data where avail-
able for the constraints and the objective func-
tion. Although we examined behavior of the
model for several of the years for which we
had data, we are presenting in this paper our
partial analysis for the 1960 run only. Initially,
we indicate how we assigned values to the var-
ious coefficients in the problem and then we give
the actual examples.

First, we assigned values to the objective
function (1) which is to be maximized. With
respect to the number of entities in the objective
function, there is a relatively large number of
ocean-age groups represented in the Naknek-
Kvichak run, but the very great majority are
either the relatively large .3 ocean-age fish or
the relatively small .2 ocean-age fish. Because,
as we will see in subsequent paragraphs, the
male fish are valuated diff'erently than the fe-
male fish, we used four entities: male or fe-
male, .2 or .3 ocean-age fish.

Next, in order to assign values c,-; to each
entity in the objective function according to the
conventional per-fish management unit, we used
the aforementioned observation that the male
fish in each age group tend to be larger and
hence more valuable than the female fish. On
the other hand, the eggs which are contained
in the females are processed into a caviar-type
product, "sujiko." by Japanese firms in the
Bristol Bay canneries. Thus, the females, be-
cause of the eggs which they contain, are more
valuable than males of the same weight. Taking
these factors into consideration and using an
average ex-vessel value of $0.25, pound, we have
computed the average value for each entity.
These calculations are set forth in Table 2 which
shows, among other things, that the added value
of eggs tends to offset the reduced value of fe-
males relative to males of the same age class.

As indicated previously, the $0.25 pound is
an average value and it should be emphasized
at this point that it is not a computed average
since generally speaking a fixed price is paid
for fish throughout the season. But as we in-
dicated earlier, some fish are certainly more

122

ROTHSCHILD and BALSIGER: LINEAR-PROGRAMMING SOLUTION

Table 2.— Computations used to determine the value
of each entity classification for the model.

Entity

Sex

Ago

Average
weight'

Average
no. of eggs'*

Average
value

Male
Male
Female
Female

2-ccean
3-ocean
2-ocean
3-ocean

Lb.
5.1
7A
4.5
6.2

Number

3,700
4,384

S

),23
1.85
1.38
1.84

1 Willi the price of salmon at $0.25/pound, the value of each entity
can bo calculated as follows:

entity 1 - 5,1 X $0.25 = $1.28;

entity 2 - 7.4 X $0,25 = $1.85;

entity 3 - 4.5 X $0.25 = $1.13;

entity 4 - 6.2 X $0.25 = $1.55.

2 With the price of salmon eggs at $0.50/pound, the additional value
of each female entity con be calculated as follows (it should be noted
that eggs were not processed in I960):

entity 3 — 3,700 eggs X ,061 g/egg -^
453,6 g/lb X $0,50 = $0.25

entity 4 — 4,384 eggs X .061 g/egg -1-
453.6 g/Ib X $0.50 = $0.29.

valuable than others. Thus, we deduced that
this fixed price must reflect an average value
and we note, parenthetically, the important
point that the bias and precision (we take the
liberty of using these terms in the statistical
sense even though the estimation procedure may
not be statistical in nature) with which this
average is estimated is a subject of significance
to the management of the salmon stocks.

In addition to the value of salmon differing
among entities, the value of salmon usually de-
teriorates within an entity during a season.
Thus, even though a fixed price is paid for
salmon during a season, the value decreases
owing to a reduction in quality. For example,
the value of pink salmon may be 25 7c less near
the end of the run than near the beginning of
the run. The decline in value of red salmon
is not so severe, amounting to a range of about
$0.03/pound from the beginning to the end of
the season. (While a few cents decline in value
during the course of the season may seem to
be a negligible quantity, we must remember that
this factor must be multiplied by the several
pounds in weight of each fish and the several
million fish that are involved in the value re-
duction.) So just as we deduced $0.25/pound
to be an average price among entities, we must
likewise deduce that the values tabulated in
Table 2 are average values for each entity for
the season. In the Naknek-Kvichak run, which

usually begins around June 27 and ends around
July 15, the decline in value appears to be
centered on July 4.

In order to arrive at a unique allocation, we
must deduce how the c,y's for each of the ;/ days
of the run differ from the average of the cj/s
listed in Table 2. The ideal way of doing this
would be to develop a model which is descriptive
of the value change during the run. Unfortu-
nately, we have no information upon which to
base such a model, so we used three arbitrarily
chosen functions to de.scribe the day-to-day value
change of the salmon. An example of these
is shown in Figure 1.

2.0i

1.9-

=^0=

1.8

1.7-

Average value
of all functions-i

Function I ( step)'

Function II ( logistic )'"

Function III (quadratic)-

1.64

0

5
Day

10
of season

15

18

Figure 1. — Value functions as objective function co-
efficients in the linear-programming model for entity 2
(large male fishes).

Next we needed to determine the quantity, in
the objective function, of N, the number of
days of the run. We utilized an empirical equa-
tion presented by Royce (1965) to obtain both
N and the daily run for each entity Rij. The
function Royce used for each of several years
to describe the temporal change in the Naknek-
Kvichak catch is

PkU)

1

1 +e

-(ak + biJ)

(16)

123

FISHERY BULLETIN: VOL. 69, NO. 1

where k specifies the year of the run, a/^. and
b); are constants, ./' is time in days, and Pkij)
is the cumulative proportion of the total catch.
In order to choose N, we defined the fishing
season to be those days for which .05 ^s P(j)
^ .95 and the difference between the initial and
closing day was, to the nearest integral value,
set equal to N.

We also used expression (16) to obtain Rij
from P'uU) = Pkii) — PkU-l) and then

Ri

Pk (J) Si, where Si is the number of fish

of the /th entity in the run during the year
under consideration. The assumptions involved
in obtaining the Rij's are (1) the catch is pro-
portional to the "average" run as defined by the
fitted curve (16); and (2) Rij is proportional
to R.j. It should also be mentioned that our
Rij's are certainly different from the ti'adition-
ally used Rij's because the latter are based on
counts made several days after the fish enter
the fishery area. This, however, is not important
in the allocation whereas the relative daily size
of the run is important. We feel that these as-
sumptions are reasonable for the present model
until more accurate information can be obtained
on the behavior of the fish in the run.

On some occasions, the catch in Bristol Bay
is limited by the cannery capacity. This ca-
pacity can be, of course, adjusted by the in-
dustry, but it appears that, according to Math-
ews (1966) , 1 million fish per day is a maximum
capacity and we used this value in constraint
equation (2). It would appear that the most
important assumption implicit in the nature of
this constraint is independence among the days;
that is to say, we assume that processing a cer-
tain number of fish on one day does not affect
the processing capacity on the next day. A sec-
ond assumption is that the maximum capacity
is not dependent upon the average size of the
fish processed. There is some question, when the
cannery operates near peak capacity, as to the
effect of overtime payments to cannery employ-
ees and to the effect of processing large numbers
of fish on the quality of the pack.

For our example, of the 1960 run, the total
season constraint was not reached and so this
constraint had no effect on any of the examples
which we present. It is relevant to note, how-

ever, that if this constraint is needed, then the
maximum number of fish ever processed (up
until 1969) in the Naknek-Kvichak system was
19.1 million.

The next constraint is the escapement con-
straint. Desjjite the fact that the level of escape-
ment has, for salmon stocks, been the primary
management criterion, there is very little doc-
umentation on the proper escapement level for
many systems. The latest synthesis of the ex-
tensive work on the Naknek-Kvichak system is
addressed to the problem of optimum escapement
in that particular system as well as others
(Burgner, DiCostanzo, Ellis, Harry, Hartman,
Kerns, Mathisen, and Royce, 1969), but un-
fortunately no advice on optimum escapement
is given for the Naknek-Kvichak. Another
study implies, on the basis of limited data, that
escapements beyond about 10 million fish will
not result in any increased productivity of
smolts (Mathisen, 1969: Fig. 6), and thus if we
make a simplifying assumption and assume that
marine survival rates are independent of den-
sity, we can further assume that an increased
return will not accrue from an escapement larger
than 10 million fish (very roughly 20 billion
eggs).

Despite the fact that we do not "know" the
optimal minimal escapement for the Naknek-
Kvichak system, it is clear that there must be
some level which is, in some sense, optimal.
This statement must, of course, be tempered
with our knowledge of the cyclical nature of the
run.

Because of our uncertainty, we examined the
model under a variety of escapement conditions
but keeping under each set, what would appear
to be, according to studies by Mathisen (1962),
a conservatively high male-to-female sex ratio
of at least one male for every three females.
We found in general, as one might expect, that
as we increased escapement we decreased the
value of the catch. The objective function was
quite sensitive to this manipulation, focusing
again upon the need for a well-defined e.sca))e-
ment policy. What is not so obvious, however,
as we will see subsequently, is that as we change
the escapement level, we can obtain consider-
able changes in the imputed values of the var-

124

ROTHSCHILD and BALSIGER: LINEAR-PROGRAMMING SOLUTION

ious entities. The 1960 run had an escapement
of 31 billion eggs. We estimate that this escape-
ment was partitioned among the entities as
follows:

Entity 1, 57.5 % or 8,136,000 fish escaping
Entity 2, 43.4 % or 210,000 fish escaping
Entity 3, 74.8 '~'r or 7,964,000 fish escaping
Entity 4, 30.8^; or 389,000 fish escaping

It is interesting to note that in addition to
8,350,000 females which were estimated to have
escaped in 1960, there were, in addition,
8,300,000 males that escaped, signifying a nearly
1 : 1 sex ratio.

Our general approach in presenting our par-

ticular 1960 run example was to concentrate up-
on simulating the actual events in 1960 by using
the above run data in equations (13) and (7),
the fecundities listed in Table 2, and the lo-
gistic value function. We also present some
results where we effectively drop equation (13)
and replace it with equation (10) using a low
escapement of 5 billion eggs in order to dem-
onstrate the sensitivity of the model to various
escapement goals.

In Figures 2, 3, 4, and 5, we depict the op-
timum allocation of the catch which we obtained
using the actual 1960 escapement data. The
figures also include the smoothed catches de-
rived from Royce's work. From these figures.

Catch ollocotion of linear program model
Total run of entity 1 males

I200n

—A Actual

CQtch

/

allocation of I960

iOOO-

/\

^3

L\

§ 800-

1

f

\

si

/

\

o 600-

/

^
§

/

5 400-

//

200-

i/

1 X

0-

1
1

r

\

r^ , ,

120-1

100-

^ ^ Cotcfi ollocotion of
lineor program model

o— — o Total run of entity 4 femoles

A — ^ Actual catch allocation of 1960

5 10

Day of season

15 18

10
Day of season

r
15

18

Figure 2. — Year 1960 small male catch allocations
(entity 1). The actual catch allocations are the
smoothed average values obtained from Royce (1965).

Figure 3. — Year 1960 large female catch allocations
(entity 4). The actual allocations are the smoothed
average values obtained from Royce (1965).

125

FISHERY BULLETIN: VOL. 69. NO. 1

60

40-

20-

-O Totol run of
enfify 2mQles

-• Cotch ollocation

of linear program nriodel

-A Actual catch

allocation of I960

<:

8

10
Day of season

Figure 4. — Year 1960 large male catch allocations
(entity 3). The actual catch allocations are the
smoothed average values obtained from Royce (1965).

— ^ Catcti allocation of linear program model
— o Totol run of entity 3 females
I000-] —A Actual cotch allocotion of I960

5 10

Doy of season

8

Figure 5.— Year 1960 small female catch allocations
(entity 3). The actual catch allocations are the
smoothed average values obtained from Royce (1965).

we can observe various properties of the op-
timally allocated catches. For example, in Fig-
ures 3 and 4, the catch allocation of the early-
season is identical to the number of fish in the
run. These large male and large female fish
are more valuable than the smaller fish and
most valuable in the early part of the season
because of the value function. Hence, all the
large fish available are caught until the season's
limit for each of the large-fish entities has been
reached. We must be cautious here, however,
because as we point out in our discussion, there
is a possibility of modifying the characteristic
of the run by selective fishing.

In order to interpret Figures 5 and 6, we must
realize that the next most valuable fish are the
small females. The difference in price between
small females and small males increases through
the season. This owes to the fact that small
females weigh less than small males and thus
decrease in value less towards the end of the
season. (Recall that the small females are more
valuable than small males only because of the
eggs which they contain.) We have assumed
that the value of the eggs is constant through-
out the season.

The optimal solution shows that the cannery
is at capacity from days 4 to 10 with as many
small males being caught through day 6 as are
available, and as many additional small females
being caught as the cannery can process. On
days 7 to 9 there are enough fish exclusive of
the small females to bring the cannery to ca-
pacity. However, by day 10, the season's limit
of small males has been caught and small fe-
males must be caught to keep the cannery at
capacity. It must be remembered that the price
difference between females and males is greater
later in the season. For example, if a small
female is caught instead of a small male on the
6th day of the season, the increased profit is
$1,430 — $1,337 = $0,093, where the figures
are the value of small females and small males,
respectively, on day 6 for the logistic value
function which we used. But if a female is
caught instead of a male on day 10, the increased
profit is $1,371 — $1,270 ~_ $0,101, for the same
value function. Hence, while the cannery is be-
ing operated to capacity and since the total num-

126

ROTHSCHILD and BALSIGER: LINEAR-PROGRAMMING SOLUTION

ber of fish of any entity is fixed by the seasonal
limit, it is more profitable to catch the small,
less valuable, males earlier in the season, which
may seem contrary to the intuition. The impli-
cations of the optimal allocation are considered
in the discussion and conclusions section.

=vk

125-

.100-

,075-

§

■S .050-

I 025-

Cannery conslroints
binding these days

o-^

Entity 1 daily run
constroints not binding
day 7 or after

10
Day of season

15

18

Figure G. — Shadow prices for daily cannery constraints
— an e.xample in which seasonal entity limits are imposed.

As indicated previously, the shadow prices
are useful in considering various management
implications. We consider, as examples, the egg
shadow prices, the cannery shadow prices, and
the run shadow prices. It might be mentioned
somewhat parenthetically that although the
shadow prices can be explained and interpreted
as in the following paragraphs, in the LP calcu-
lation, they are not found in this manner. The
shadow prices are calculated as simultaneous
results of an iterative solution procedure and
include the results of pi-evious iterations. In
fact, the shadow prices associated with each
constraint at the end of each iteration are used
to determine how to manipulate the matrix to
improve the objective function in the subsequent

iteration. With very involved problems, it might
not be possible to examine the shadow prices
as below, and in any case, only a good deal of
insight into the problem permits their delinea-
tion in this manner. One other caution is that
while applying the following equations to deter-
mine a total increase in profit, care must be taken
to see that the same constraints remain binding
or nonbinding. Once a constraint changes from
binding to nonbinding, the solution basis
changes, also changing the relationships between
variables and constraints.

The increase in value of the objective func-
tion corresponding to a relaxed egg constraint
(allowing one more egg in the catch) is the shad-
ow price associated with the egg constraint. The
shadow price is dependent upon which, if any,
of the constraints in the LP model are binding.
If the egg catch constraint' is not binding, indi-
cating that the value of this catch scheme is not
being limited by this constraint, then the shadow
price associated with the egg constraint is zero.
If the egg catch constraint is binding, shadow
prices associated with the egg constraint, de-
pending upon which of the other constraints
are effective, can be calculated.

The imputed value of an egg, its shadow price,
thus depends on whether the cannery constraint
is binding. Now, if the cannery constraint is
binding on day j (indicating that the max-
imum number of fish are being processed and
the addition of a single or marginal fish to the
processed catch requires that a fish already ex-
isting in the catch must, to maintain the con-
straint, be replaced by the marginal fish), and
the entity 4 run constraints are binding through-
out the season (indicating that all large females
are caught), then the shadow price associated
with the egg catch (ESP) constraint is

ESP = (C7.J -f|,,)/3,700
where day / is a day on which the entity 3 run

' Although the egg constraint arose from a minimum
egg escapement requirement, it was necessary to con-
vert it to a maximum egg catch requirement constraint
for use with the LP model, as was described earlier.
It is convenient to think of the constraints in terms of
"egg catch" for purposes of discussing the shadow
prices.

127

FISHERY BULLETIN: VOL. 69, NO. 1

constraint is not binding, i.e., there are entity
3 females available to be caught. The formula
indicates that allowing the catch of one more
egg essentially allows the catch of 1/3,700 of
an entity 3 female which requires the escape-
ment of 1/3,700 of some other fish since the
cannery constraint is binding. The fish to be
included in the escapement is, of course, the low-
valued entity 1 male.

If the cannery constraint on day j is binding,
but there is a day when the entity 4 run con-
sti'aint is not binding, and since the value of a
large female per egg is greater than the value
of a small female per egg, the value of allowing
the catch of an additional egg is

ESP= (C4J -C|j)/4,384

where day .;" is a day on which the entity 4 run
constraint is not binding.

If the cannery constraint is not binding on
day j then catching additional females does not
require the escapement of an equal number of
males, or, in other words, the addition of the
marginal fish does not require the release of
a fish extant in the catch. If, however, all the
entity 4 run constraints are binding through
the season, then

ESP = C3,,/ 3,700

where day ; is a day on which the entity 3 run
constraint is not binding. Or, if an entity 4 run
constraint is not binding on day j and again
since the value of a large female is greater than
that of a small female,

ESP=C4j4M4-

The next shadow price that we will evaluate is
the increase in value of the ability to process
an additional or marginal fish. The imputed
value of processing a marginal fish is called
the shadow price of the cannery constraint
(CSP), and we must remember that this mar-
ginal fish only has an imputed positive value
if the cannery constraint is binding. In other
words, we can impute a value to an additional
unit of cannery capacity. Following the format

above, the shadow prices for the cannery con-
straint can be outlined. For emphasis, we re-
peat again that if the cannery constraint is not
binding, indicating that the value of this catch
scheme is not being limited by this constraint,
then the shadow price associated with the can-
nery constraint is zero. If the cannery con-
straint is binding, shadow pi'ices associated with
the cannery constraint, given which other con-
straints are effective, can be determined.

The objective function will be increased by
an amount equal to the value of the additional
fish which is included in the new catch scheme
(the scheme arising from relaxing the cannery
constraint), and hence the most valuable fish
will be caught. If run constraints are not bind-
ing, the shadow price is

CSPj = C2j

since the large males are the most valuable.
As the run constraints become binding for the
more valuable entities, the shadow price of the
cannery constraints is equal to the value of the
most valuable entity available.

If, for example, the egg catch constraint is
binding as well as the entity 2 run constraint,
the shadow price of the cannery constraint is

CSPj =c4j

/ 4,384
y 3,700

C3,

The modification of the equation assures that
enough eggs will escape (via entity 3 female) to
enable the catch of the more valuable entity 4
female.

To emphasize the effect of reduced escape-
ments and concomitant binding egg catch con-
straints, we employed the 1960 run model but
dropped equation (13) and used an effective
escapement of 5 billion eggs in equation (10).
If the egg catch constraint is binding as well
as entity 4 run constraints, the only fish avail-
able for catching are the entity 1 (small males),
since no more females can be caught without
violating the egg catch constraint. Hence

CSPj = c|j.

128

ROTHSCHILD and BALSIGER: LINEAR-PROGRAMMING SOLUTION

"UV

—

.45-1

1.40-

1.35-

1.30-

.25-

1.20-

Cannery constraints
binding ttiese days

1 1 1 1

0 5 10 15 18

Day of season

Figure 7. — Shadow prices for daily cannery constraints
— an example in which seasonal entity limits are not
imposed.

As an example of this situation where we have
an escapement of 5 billion eggs, consider Figure
7, where the curve representing the cannery
shadow prices is exactly the value function
curve for entity 1 males. If, however, we con-
trast the 5 billion egg constraint situation with
the actual 1960 run where the seasonal limit
constraints are binding for all entities, then the
improvement in the objective function attributed
to the one unit of increased cannery capacity will
only be equal to

CSPj

<^ii

since to catch a fish of entity / on day j another
fish of entity i must be released on day j* (i Vj)
to avoid breaking the seasonal limit constraint.
Figure 6 gives an example of this situation.
The particular example is taken from the LP
model using the logistic value function and
actual escapements of 1960 by entity (thus the
seasonal limit constraints). In this case, the

total number of fish processed remains the same
(since season limits are binding for all entities
already) , but processing a fish earlier in the
season can result in an increased profit because
of the shape of the value-function curve.

The implications of Figure 6 are quite subtle.
In Figure 6, until day 4, the cannery is not at
capacity, and hence there is obviously no value
associated with an increased unit of capacity.
All fish are included in the catch allocation in
the early-season, high-value situation. On day 4
the cannery is at capacity and some fish must
be included in the escapement (excluded from
the catch). Intuitively, we would expect the
highest value fish to be caught. This is partly
reflected by the continued catch of all entities

2 and 4 fish (the large males and females), but,
keeping in mind the fact that catches in all
entities are being limited by the seasonal limit
constraints and the idea of the decreasing pi'ice
diff'erential between entity 3 and entity 1 fish,
entity 3 fish become part of the escapement.
This says that on days 4 to 6, an increase in the
capacity of the cannery will result in an entity

3 fish being caught on that day and a less valu-
able entity 3 fish released later in the season
(to avoid breaking the season's limit constraint) .
We can see in Figure 5 that the last day on
which an entity 3 fish can be released is day 11.
The value of an entity 3 fish on day 4 is $1,445,
the value of an entity 3 fish on day 11 is $1,356.
Hence we would expect to gain exactly $0,089
by increasing the cannery capacity by one unit
on day 4. Checking Figure 6, we see this is
exactly what the graph shows for day 4. Days
5 and 6 can be calculated similarly.

On days 7 to 10, entity 1 daily run constraints
are no longer binding, and hence an additional
unit of cannery capacity could result in an entity
1 fish being caught on day 7. From Figure 5
the least valuable entity 1 fish in the catch scheme
is on day 10, and one of these would go into
the escapement. The increased value is

or

C|.7 - f'l.io
$1,324 - $1,270

or a profit increase of $0,054. In Figure 6, the

129

FISHERY BULLETIN: VOL. 69, NO. I

shadow price of the cannery constraint on day
7 is shown as $0,069. Note, however, that when
an entity 1 fish is released on day 10 that the
cannery is no longer at capacity on day 10,
hence an entity 3 fish could be caught on day 10
if an entity 3 fish was released on day 11. This
is an additional contribution to the shadow price
for day 7 of

or

«'3.10 ~ <^3,11
$1,371 - $1,356

or a profit increase of $0,015. Adding this to
the value of catching an earlier entity 1 fish
gives $0,054 + $0,015 = $0,069, and this is
exactly what is shown for day 7 in Figure 6.
Values for days 8 to 10 can be calculated sim-
ilarly.

Next let us consider the run shadow prices
(RSP). The increase in value of the objective
function corresponding to relaxed run con-
straints allowing one more fish of any entity
in the catch is the shadow price of that run
constraint. If the cannery constraint is not
binding, if seasonal run constraints are not used
or are not binding, and if egg catch or male
escapement consti'aints are not binding, there
is no restriction other than the run constraint
limiting the catch. Since there is a run con-
straint for each entity and day

RSPij = dj.

However, if the cannery constraint is effective
on day j

RSPij = Cij - Ci*j

where entity i* {i*ri) is the fish that must
escape to allow the catch of entity i since the
cannery is already processing as many fish as
possible. And if the egg catch constraint and/
or the male escapement constraint is binding,
appropriate numbers of fish must be released
when additional fish are caught. As an example
of the behavior of the system when the 5 billion
egg constraint is used, consider Figure 8. As
shown in Figure 8, daily cannery constraints
are binding from days 4 to 15, and, in addition.

I.Male 2-'
2. Mole 3-

3. Femole 2 -

4, Female 3-

•Oceon

Cannery constraints
binding these days

2.00n

0 5 10

Day of season

Figure 8. — Shadow prices for daily entity run con-
straints— an e.xample in which seasonal entity limits are
not imposed.

the egg catch constraint is binding. Although
it is not illustrated in the figure, it is essential,
in understanding the problem, to realize that the
entire escapement satisfying the egg escapement
constraint is made up of small (entity 3) females,
and that the entire escapement satisfying the
male escapement constraint is made up of small
(entity 1) males. Also, all fish of all entities
are in the catch scheme on days 1 to 3 and 16
to 18 (all days on which the cannery constraints
are not binding).

In Figure 8, on days 1 to 3, the cannery con-
straints are not binding; and since entity 2
escapement is not being used to satisfy any con-
straints of any form, the run shadow prices on
days 1 to 3 will be equal to the value function
(this can be checked with the values listed in
Appendix Table 2). In addition, since the male
catch constraint is not binding, the run shadow
price for entity 1 is also equal to its value func-

130

ROTHSCHILD and BALSIGER: LINEAR-PROGRAMMING SOLUTION

tion for the first 3 days of the season. This
is not true for entity 3 or 4 since the egg-catch
constraint is binding, indicating that no more
eggs can be "caught" without breaking the con-
straint. Hence, when an entity 4 female is
caught on a day 1 to 3 (catching 4,384 eggs),
4,384 eggs must be released on some other day
of the season. This can be done with the smallest
loss by releasing 4,384/3,700 entity 3 females
(entity 3 females have 3,700 eggs). To further
decrease the loss, the above fractional parts of
an entity 3 should be released on a day on which
there are entity 1 or 2 available to be caught,
since this will keep the cannery constraint in-
tact and not violate the male catch constraint
since it is not binding. Remembering that the
price differential between entity 1 and entity 3
increases over the season, it is desirable to catch
the additional entity 1 fish as early as possible,
which is on day 7. Then (note that all of the
larger males are already in the catch scheme) :

RSP4J = c-4.,- ^Q,7+ ^ ci,7
4,384

= $1,941

3,700

$1,419)

+ AMI ($1,324)
= $1,828,

which can be seen on the graph as the shadow
price for entity 4 day 1. To calculate the value
of the run shadow price for entity 3 in days 1
to 3, we must realize that catching an entity 3
female requires the release of a female some
other time during the season in order to avoid
breaking the egg catch constraint. Since the
entity 3 females are of lesser value than the
fractional part of an entity 4 female which must
be released to account for the 3,700 extra eggs
caught, the release of this fish on a day on which
there are entity 1 fish available will lessen the
loss. As before, the price differential between
entities 1 and 3 is smaller early in the season,
and the earliest date on which an entity 1 male
is available is day 7. For example,

RSPy,i = C3.1 - r3.7 + ci.7

= $1,453 - $1,419 + $1,324
= $1,358,

which is the value shown in Figure 8.

The run shadow price for entity 1 day 4 re-
sults from the catch of entity 1 on day 4 requir-
ing the release of entity 3 (to avoid breaking
the cannery constraint) which, in turn, allows
the catch of an entity 3 and the release of an
entity 1 on day 11 (the last day on which there
are entity 3's not in the catch scheme). Essen-
tially, what we have done is to exchange the
catch of entity 1 and entity 3 for a time when
the price differential is more favorable.

RSP\4 =C],4 - C3,4 + C3,7 - <^1.7

= $1,353 - $1,445 + $1,419 - $1,324
= $0,003,

which is the value shown in Figure 8. Run
shadow prices for entity 1 days 5 and 6 can be
figured similarly. For entity 1 days 7 to 15,
the daily run constraints are not binding, and
hence, the run shadow prices are zero.

Run shadow prices for entity 2 days 4 to 15
(still referring to Figure 8) can be calculated
as the difference between the value of an entity
2 and entity 1 on those days. The entity 1 must
be released in order to satisfy the cannery con-
straints for those days. In addition, for days
4 to 6, calculating the value of this new avail-
ability of an entity 1 released in order to catch
an entity 2 is essentially the same situation as
calculating the shadow price of entity 1 on those
days, and hence, the value of the scheme and
the run shadow price is increased by that addi-
tional amount.

Run shadow prices for entity 3 days 4 to 7
in Figure 8 are zero since the run constraints
of entity 3 for those days are not binding. For
entity 3 days 8 to 15, they can be calculated as
follows: If another entity 3 is caught on day 8,
an entity 1 must be released on day 8 to main-
tain the cannery constraints. The catch requires
the escape of an entity 3 fish on another day to
maintain the egg catch constraint. In turn, if

131

FISHERY BULLETIN: VOL. 69, NO. 1

the release of the entity 3 is on a day which a
male entity is available, that entity can be caught
without breaking the cannery constraint, e.g.,

(Note that day 7 is the first day on which there
is a male entity not already in the catch scheme,
and hence, the price differential is smallest.)

/?SP3,8, = $ 1 .404
= $o'.002,

$1,307 - $1,419 + $1,324

which is that value shown in Figure 8.

Run shadow price for entity 4 days 4 to 15
can be calculated by releasing and catching the
fractional parts 4,384/3,700 of entities 3 and 1
as requii-ed to maintain cannery and egg catch
constraints, in a manner similar to that for days
1 to 3. The run shadow prices for the male
entities for days 16 to 18 (those days after the
cannery constraints are no longer binding) are
simply equal to the value of those entity-days,
since they are not involved in satisfying any
constraints of any form. The run shadow prices
for the female entities on these days are a little
more difficult to arrive at, since as they are
caught, an equal number of eggs must be re-
leased, resulting in a slack cannery constraint
which can be filled by catching additional male
entities when available.

Consider, in contrast. Figure 9, where the run
shadow prices are shown for a case in which we
used the actual escapement for the 1960 run in
constraint equation (13). The seasonal limit
constraints are binding for all entities in this
example. It follows that in every case when cal-
culating a run shadow price for an entity day,
the inclusion of an additional unit of any entity
on that day implies that a unit of that entity
must escape on some other day of the season to
maintain the equality of the seasonal limit con-
straint for that entity.

In Figure 9, shadow prices are plotted for the
daily run constraints for the particular example
in which seasonal limits were imposed to achieve
the actual escapements of 1960. Neither the
egg catch constraint nor the male catch con-

l.Male 2-

2. Mole 3-

3. Female 2 -

4. Femole 3-

• Ocean

Cannery constraints
binding these days

0.20

0

5 10

Day of season

Figure 9. — Shadow prices for daily entity run con-
straints— an example in which seasonal entity limits are
imposed.

straint was binding; the seasonal limit con-
straint was binding for each entity. Cannery
constraints were binding from days 4 to 10, as
indicated on the figure. In calculating the run
shadow price for any entity on any day, note that
whenever an additional fish is included in the
catch scheme, a fish of that same entity must
be eliminated from the catch scheme on some
other day in order to maintain a valid seasonal
limit constraint for that entity. Thus, for entity
1 days 1 to 3, the run shadow price can be cal-
culated as the value of a fish included on the
day being considered minus the value of the low-
est valued fish of entity 1 in the catch scheme
which must be released to keep the constraints

132

ROTHSCHILD and BALSIGER: LINEAR-PROGRAMMING SOLUTION

effective. If this low-valued fish is released on
a day on which the cannery constraint was bind-
ing, then the cannery constraint is no longer
binding and a fish of another entity can be
caught on that day if a fish of that other entity
is available. For example,

f(SPii = tij - Clio + C.I. 10 - C'3 11

= $1,362 - $1,270 + $1,371 - $1,356
= $0,107,

which is the value shown in Figure 9. The run
shadow prices for entities 2 to 4 on days 1 to 3
are simply calculated as the value of the entity
on that day minus the value of that entity on
the lowest priced, and hence, last day on which
it is included in the catch scheme. For example,

RSP}j = C3 I - Oil

= $1,453 - $1,356

= $0,097.

Checking Figure 5, we see that day 11 was the
last day or which entity 3 fish were caught, and
Figure 9 shows that the value ($0,097) is
correct.

Run constraints for entity 3 are not binding
after day 3, so run shadow prices associative are
zero.

To obtain the run shadow price for entity 1
for days 4 to 6, one may, for example, subti-act
from the value of entity 1 day 4, the value of
entity 3 day 4 (which must be released to main-
tain the daily cannery constraints) , subtract the
value of entity 1 day 10 (which must be released
to maintain the season entity 1 limit), and add
the value of entity 3 day 10 (which can be
caught since an entity 1 has been released on
day 10); or

RSP\,4.(, = C\4 - Ct,4 - f I 10 + C3,io

= $1,353 - $1,445 - $1,270 + $1,371
= $0,009,

which can be seen in Figure 9.

Run shadow prices for entities 2 and 4 for
days 4 to 6 are similar. For illustration, entity

4 day 4 will be calculated:

RSP44 = ('4 4 - £-3,4 - c-4 13 + f3,ll-

That is, the run shadow price of entity 4 day
4 equals the value of entity 4 day 4 less the value
of entity 3 day 4 (to preserve the daily cannery
constraint) less the value of entity 4 day 13 (to
preserve the seasonal entity 4 limit) plus the
value of entity 3 day 11 (since an entity 3 day
4 was excluded, this will be within the entity 3
seasonal limit constraint) . Thus

RSP4_4 = $1,930 - $1,445 - $1,780 + $1,356
= $0,061.

This is the- value shown in Figure 9.

The run shadow prices for entity 1 after day
7 are zero since the daily run constraints are no
longer binding. For entities 2 and 4 days 7 to
10, the run shadow prices can be calculated sim-
ilarly. For example,

RSP

2,10

C2.\0 - C3.10 - Q.I I + O.ll.

That is, the run shadow price of entity 2 day
10 equals the value of entity 2 day 10 less the val-
ue of entity 3 day 10 (to preserve daily cannery
constraints) less the value of entity 2 day 11 (the
last day on which entity 2's are caught and,
hence, the cheapest entity 2 which can be re-
leased to preserve the seasonal limit) plus the
value of entity 3 day 11 (since an entity 3 was
released on day 10, this will not fracture the
seasonal entity 3 limit constraint). Thus

RSP2.\o = $1,836 - $1,371 - $1,812 + $1,356
= $0,009,

which is shown as the correct value in Figure 9.
The run shadow prices for entity 4 on days 11
and 12 are easily calculated since the cannery
constraints are no longer binding and this is
the only entity being caught after day 12. Hence,

RSP4,l\ = C4J1 - C4,|3

= $1,808 - $1,780
= $0,028.

133

FISHERY BULLETIN: VOL. 69. NO. 1

It is interesting to note that the run shadow
prices of entity 4 throughout the season are high-
er than those of entity 2 (see Figure 9), even
though the value for an entity 4 is less, for any
given day, than the value of entity 2. This is
due to the optimal catch scheme which has
catches of entity 4 until day 13, while entity 2
catches are only made until day 11. The effect
is that when an additional fish of an entity is
caught early in the season (requiring the re-
lease of a fish of the same entity later in the
season), the entity 2 fish released is from day
11 of value $1,812, the entity 4 fish released
is from day 13 of value $1,780. The value of
the entity scheme then, decreases least (propor-
tionately) for releasing the entity 4 fish.

DISCUSSION AND CONCLUSIONS

It can be seen that the linear-programming
(LP) approach to salmon management, as with
all other modelling approaches, involves a va-
riety of assumptions which are either intrinsic
to the procedure or to the way the procedure
is applied to real-world problems. We have gone
into some detail to show the richness of inter-
pretations that the salmon model affords, and
we believe that the application of this procedure
to salmon management will provide increased
guidance to and widen the spectrum of possible
management decisions. The procedure we have
used for the Naknek-Kvichak run is widely ap-
plicable to a variety of situations both within
the Naknek-Kvichak sockeye salmon setting and
to other salmon runs as well. The setting, the
necessary data, and the formulation of the
problem really depend on the problem situation.
Our purpose was to demonstrate a conceptual
method and we have chosen our data and ex-
amples accordingly.

There will naturally be difl'erences of opinion
in the formulation of the model (that is, dif-
ferent ways of expressing the constraint equa-
tions, some of which are indicated) or the ap-
propriate data which should be used for actual
management situations. These differences can
at times be easily resolved by examining the
sensitivity of the model to various data or
formulation modifications.

Nevertheless, we should not ignore the as-
sumptions which are implicit in the LP pro-
cedure. These are outlined by, for example, Hil-
lier and Lieberman (1967), and constitute three
concepts that should be recognized. These in-
volve the linearity property of the model, the
problem of divisibility, and the deterministic
nature of the LP approach. In addition, it is
important to consider that the LP approach
models only static situations. First, the linear-
ity property asserts, for example, that the value
of any term in the constraint or objective func-
tion must be directly proportional to the level
of activity involved. Expressed in another way,
the relation between the level of an entity and
its contribution toward filling the constraint or
modifying the objective function must be a
straight line passing through the origin, a con-
dition not often met in practice but frequently
approximated. Furthermore, there should be
no synergism among the terms of the objective
or constraint functions. For example, the unit
catch value on day j for the tth entity, ca, can-
not be affected, a posteriori, by the unit catch
value on day /-l for the (th entity c;, j.i- The
problem of divisibility refers to the fact that
the LP approach that we have used gives solu-
tion values which are not necessarily integers.
A usual practice is to round solutions to the near-
est integer value, thus avoiding the embarrass-
ment of having, e.g., 7,012,342.631 salmon. In
other applications, such as allocating 10 fishing
boats, say, to perhaps three fishing grounds, the
possibility of having non-integer answers may
lead to erroneous conclusions and one of the
integer programming techniques would then be
most appropriate. Next, the deterministic na-
ture of the LP approach is, of course, a deficiency
in the probabilistic real world. The manager
must realize that a full stochastic treatment of
the salmon allocation as an optimization problem
would most likely be a very difficult task. As
alternates, an error structure could be applied
to various elements in the problem, thus enabling
one to explore a variety of probabilistic phe-
nomena, or chance-constrained programming
might be employed. Monte Carlo and simula-
tion approaches might also be utilized but these
are not per se optimization procedures. Finally,

134

ROTHSCHILD and BALSIGER: LINEAR-PROGRAMMING SOLUTION

the static nature of the LP approach provides
a challenge to application in the sense that the
unit values in the objective function, the con-
straints, and the right-hand sides of the con-
straint equations must not only be known in
advance, but also must not change as a result
of any of the allocations in the model.

The above assumptions can be handled in a
variety of ways such as those indicated to handle
problems of the deterministic nature. For ex-
ample, we might, in some instances, use qua-
dratic programming to handle the problem of
non-linearity or d>-namic programming or apply
the outlined procedure in real time to handle the
static nature of the programming problem, but
unfortunately these approaches will present
what can be quite complicated computational
difficulties which may, in some instances, be in-
surmountable. It is thus clear that we have
made certain approximations, trading off real-
ism for an easily computable solution which
certainly provides management guidance.

As we implied previously, we do not consider
our departures from realism to seriously affect
the utility of the model to provide guidance for
decision making. Thus we believe that, for ex-
ample, fixing the cannery capacity independent
of the entities involved (or we could consider
the cannery capacity to be fixed at a level which
would accept a reasonable mixture of the en-
tities) or using a simple average fecundity of
the female entities to represent the average
fecundity of the spawning females materially
affects our conclusions. These, however, can
be evaluated in direct applications by a sensi-
tivity analysis.

Having outlined some cautions with respect
to assumptions, we can now examine some of
the indications provided by the various trials
of the procedure. These involve the value of the
fish on the dock, a reduction in processing-season
length, changing value of entities during the run,
and finally future data needs.

First with respect to the value of the total
catch on the dock, we experimented with three
value functions which set the daily value of each
entity. Using the value functions to determine
the value for each entity and day, and the actual
distribution of the catch over the 1960 season,

a total value of the catch was calculated which
corresponds to the use of each of the three value
functions. These values of the actual allocation
of the catch were compared with the value of the
optimal allocation as determined by the linear
program as an indication of the value of op-
timally allocating the catch over the season. The
increased value of the optimally allocated catch
ranged from approximately $350,000 to $420,000
dependent on which value-function curve was
considered. Table 3 shows these results. In
the table, a fourth value function is indicated,
which is simply a straight-line function such
that the value of each entity remained constant
through the season. Each of the other value
functions was determined such that the average
value of each curve was equal to the constant
value for that entity for the season.

Table 3. — Comparison of the value of the optional al-
location with the value of the actual allocation of the
catch for the 1960 season.

Value
function P

Value
function 2^

Value
function 3^

Value
function 4*

Optimal
allocation

Actual
allocation

$13,787,050
13,378,650

$13,927,860
13,506,250

$13,792,555
13,439,825

$13,517,870
13,517,890

Increased
value

$ 408,400

$ 421,610

$ 352,730

$ 'i-20

^ After doy 6, the price dropped 3(f per pound.

2 The price was reduced by subtracting a logistic curve that reduced

the price of eoch entity by 3tf per pound over the season.

^ The price was reduced by subtracting a quodratic curve that reduced

the price of each entity by 3^ per pound over the season.

* The price for each entity remained constant through the season (actual
situation.)

^ Difference due to rounding in the linear programming algorithm.

All three value functions had the effect of
placing emphasis, in the optimal solution, on
catching fish on the early days of the season.
For tw'o of the functions the value for any entity
of fish on a given day is less than the value for
that entity on the previous day. This is not true
in the step function and thus we do not have
a unique allocation, but rather a set of alloca-
tions under the high values and a set of allo-
cations under the low values. But results are
exactly the same; optimal allocations of fish are
identical under the three value functions, al-
though the total value of the catch changes some-
what, according to the exact shape of the value-
function curve. Again, we emphasize that these
gains from allocation can only be obtained by

135

FISHERY BULLETIN: VOL. 69. NO. 1

knowing in advance of the run the information
that we actually used in the allocation and having
the ability to select the entities in the run as
they are selected in the allocation.

Next, an examination of the 1960 optimal
allocation reflects that this optimal allocation
not only increases the value of the fish on the
dock, it also shortens the length of time which
a cannery needs to operate. Thus, the same
amount of fish could be processed in a shorter
period of time, by the same labor force, etc.
In the optimal allocation for the 1960 run, all
of the fish could have been processed in the first
13 days of the season, 5 days less than the actual
operation. Naturally, we need to assume that
a policy of catching salmon only from the early
part of the run would not aff"ect the genetic
constituency of the stock. Furthermore, we
must be careful here because, as we have em-
phasized in several places, by our LP assump-
tions, we cannot, a priori, let the cannery oper-
ations on day ;/-l, for example, affect the can-
nery operations on day / and we cannot at least
in our formulation allow operating at peak ca-
pacity to affect quality of the fish or overtime
payments since the variables are external to
our model.

Another indication is that the values of fish
change during the course of the season and that
these values change in rather subtle ways de-
pending upon the "rules" that we set forth (e.g.,
contrast Figures 8 and 9) and that in the fishery
the marginal value of less valuable entities in
Table 2 can be greater than the more valuable
entities in Table 2. These changes in values
need to be acknowledged in any management
scheme.

Thus, it appears that we have the opportunity
to increase the economic efliciency of some salm-
on runs. This is, of course, not a new concept,
having been treated in some detail by, for ex-
ample, Crutchfield and Pontecorvo (1969). Our
approach is slightly different, however, in that
we have concentrated on oiitimality only from
the point of view of increasing the value, as we
have defined it, of the fish on the dock. Any full
treatment of the management problem must, of
course, consider the distribution of fishing eff'ort
and its ancillary fishing and economic implica-

tions.

Now if we accept the premise that conserva-
tion is "optimum" allocation of resources in the
times-space stream (c.f. Crutchfield and Ponte-
corvo, 1969), and if we observe that mathema-
tical programming provides guidance for optimal
allocation, and note that LP is a special case of
mathematical programming, and suggest that
the kinds of information required to allocate
salmon among the days of the run in an LP
model are not going to be much different from
the kinds of information required for more so-
phisticated programming procedure, then we are
led to the conclusion that perhaps we have not
addressed ourselves to asking, in our research,
the "right questions" concerning salmon man-
agement. Following our argument, it would
then be implicit that the right questions are con-
tained in our formulation of the LP model.
These answers must be feasible to obtain and
they would contain either needed data or doc-
umented policies which would be reflected in
the right-hand side of the constraint ecjuations
and, more importantly, provide an opportunity
for enlightened dialogue. There is unfortu-
nately a cost associated with asking right ques-
tions. This cost involves the cost of doing new
work, or that which inevitably results when ex-
isting research activities are reallocated. Are
these costs worth the expenditure? These, how-
ever, are the kind of questions, the answers to
which can be guided by the LP problem. For
the salmon management model, we impute values
to units of cannery capacity, etc., but, and per-
haps of equivalent importance, we impute a val-
ue, in meaningful terms, to information. Thus,
for our salmon jn'oblem, we have cleverly avoid-
ed indicating how we could catch Xij fish for
some /,,/. But it is well known that catching can
be approximated because it is i)ossible to catch
salmon in traps (although this has never been
done to any large extent in Bristol Bay) and,
upon visual inspection, to distinguish between
large and small, male and female fish, and doing
this by virtue of ceteris paribus, the allocative
process, we could add about 0.5 million dollars
to the value of the salmon on the dock. This is,
of course, not the full picture, because we would
have to trade off the added value of salmon (it

136

ROTHSCHILD and BALSIGER: LINEAR-PROGRAMMING SOLUTION

is a common opinion that salmon caught in traps
are of better condition and higher vahie than
the salmon which are taken by gill netting, for
example), the reduction in cannery days used
to process the fish, the cost of building traps,
and the political problems which are described
in some detail in Crutchfield and Pontecorvo
(1969). It would not, however, be dithcult to
determine the discounted present value of the
various alternate ijrocedures and thus evaluate
the wisdom of engaging in any. In this eval-
uation, we need not be bound by what are per-
haps extreme solutions such as traps, but we
could examine the value of other selectivity pro-
cedures such as modifying gill net selectivity,
etc. In general, then, we can evaluate the value
of information by approximating that informa-
tion, employing it in the model, and contrasting
the change in the objective function with the
objective function when the information is not
in the model.

Additional information is needed on the pat-
tern of the run. For the earlier years, this is
available in Royce (1965), a publication which
needs to be updated and implemented to obtain
even rough estimates of the temporal movement
of the fish of various entities through the fishery.
This might be quite difficult to accomplish with
present concepts, and the feasibility of a system
which would acoustically monitor the passage
of salmon through the entire river system and
developing a central computer-oriented unit
which would process the signals from all acoustic
units and provide, in real time, through appro-
priate algorithms, rules for catching fish and
making observations on escapement is presently
being explored.

In our model, because of a lack of information,
we used the total run and allocated this propor-
tionately among the days of the fishery to de-
termine the daily run. This emphasizes the need
to have, for the purpose of management, a fairly
accurate preseason guess of the total magnitude
of the run and the Xij's. These guesses are
already being made and the predictions need
to be judged on the basis of whether the pre-
dictions do better than simply averaging the
run for cycle years and simply averaging the
run for noncycle years and applying these aver-

ages as predictions. The trick then may not be
to estimate the average catch but rather to de-
termine which years are cycle years.

We have included cannery capacity in a rather
simple way in our model and this is a subject
that also needs additional data since the can-
nery capacity constraint can be formulated in
a variety of ways. It would be interesting to
explore in a simulation setting the behavior of
the slack variables in the cannery constraint.
This is because it seems quite likely that there
is a positive correlation between the cost of op-
erating a cannery and the magnitude of the
slack variable in the cannery constraint. If the
run was constant from year to year, then it
would be relatively easy to determine an optimal
value for the magTiitude of the slack variable in
the canneiy constraint. But the run varies con-
siderably from year to year, and so in those
years when the cannery constraint might be too
low, we have an opportunity cost which appears
as a slack variable in the dual formulation of
the cannery constraint. It would seem then that
the best value of the cannery constraint would
be somewhere in between the capacity for a
maximum run and a minimum run and that this
might be investigated by employing the LP
model in a simulation setting.

We have also emjjloyed egg and sex ratio con-
straints in our model. The egg constraints re-
quire information on fecundity and escapement.
There is not much information on fecundity but
this should be either easily obtainable or easily
approximated. Again, the static nature of the
LP problem makes it difiicult to attribute a val-
ue to an egg for years in the future. This is,
of course, important, emphasizing the need of
thinking not, as is conventionally done, in terms
of the forthcoming year, but rather in terms of,
for example, a series of years maximizing (c/.
Riff'enburgh, 1969) economic benefits. In other
words, the utilizers of resources may not be
interested (even though they may think they
are) in management on a year-to-year basis;
rather, they are interested in some long-run sat-
isfactory behavior of the time stream of economic
benefits. Alternatively, though, we must be
cautious of on-the-average management schemes
which are typically presented in fishery appli-

137

FISHERY BULLETIN: VOL. 69, NO. 1

cations. This is because a particular manage-
ment scheme might be on-the-average quite prof-
itable in the long run but might frequently
completely bankrupt the system for the first 20
years of operation.

The problem of sex ratio is quite important
because it appears that the objective function
would be quite sensitive to selectively decreasing
the number of males in the escapement and thus
increasing the catch perhaps substantially. As
indicated previously, Mathisen's study (1962)
gives us some guidance on this subject and it
would appear that, in some instances, the 3:1
ratio might be conservative. Furthermore,
it should be mentioned that a year-to-year modi-
fication of sex ratio might be a useful cushion
for approaching stability for some economic as-
pect of the fishery. Finally, the problem of
escapement eludes us because in the wealth of
literature on the subject there appears to be
very little that is useful in setting the egg-min-
imum constraint. It is generally agreed that the
stock-recruitment relation for salmon is the fa-
miliar Ricker-type curve. It is well known that
the variability in these relations is quite large
(in the case of the Naknek-Kvichak run, at-
tempting to draw similarities between stock and
recruitment places tremendous stresses on the
imagination anyhow) and as a consequence, if
the dome-shaped model holds, a minimum escape-
ment set sufficiently, but not unreasonably high,
could, on the average be reducing the return
rather than increasing the return.

It might be difficult even after several years
of setting the minimum escapement value at too
high a level, to detect, owing to the variability
in the system, the effect of this policy. If this
is true, then again we are asking the wrong
questions by studying the stock and recruitment
model per se. We are faced with a system that
is so variable, either intrinsically or in terms of
measurement techniques, or both, that a large
number of data points is required before we can
evaluate the relation between the empirical data
and the theoiy and then use the theory to jjredict.
There is but one point a year and so we are
asking nature to "stand still" for a large number
of years. Given these observations and our past
experience, we wonder whether it might not be

more appropriate for management purposes to
avoid looking at stock and recruitment per se, to
intensify study of the physiology and behavior
of very young stages of fish, and thus examine
fundamental problems of cause and eff'ect, vis-
a-vis the variables that influence the magnitude
of egg production and survival of these eggs
and larvae or other young stages through the
first several months of their life. And finally,
in the meantime, would it be more appropriate
to consider measuring stock and recruitment in
terms of transition probabilities which might
be estimated by computing the median stock
and the median recruitment? Stock sizes which
are below the median would be poor, those which
are above, good, and similarly with recruitment.
The empirical data could then be used to esti-
mate probabilities of good-good, good-poor, poor-
good, and pooi'-poor transitions. We need not in
this procedure be restricted to medians, but
could in fact use any fractile, and in fact we
need not be restrained by fractiles because we
might want to place the dividing line at some
"optimal value" and explore the consequences.
In conclusion, then, we have formulated a LP
model for salmon runs and have shown how it
might be related to the Naknek-Kvichak run.
We see in this relationship that, given informa-
tion on the structure of the run, we can both in-
crease the value of the fish on the dock and at
the same time reduce processing time. Whether
it is worth obtaining the information in terms
of the indicated data and the ability to select
fish from the run to approach this allocation
and whether decreased processing time is, in
fact, a saving, are questions that must be an-
swered by the processing industry in light of
the increased value of salmon on the dock. If
our estimate of increased value is approximately
correct, we can see that allocation can add an
interesting value to the catch, but far greater
additions could come from reducing the escape-
ment, if this is possible, and alleviating the open-
access related problems. Perhaps the most in-
teresting feature of the model is the richness
of interpretations that LP aflfords in the salmon
situation and the nature of questions and data
needs raised by the model. Finally, we emi)ha-
size that, as Hillier and Lieberman (1967) note.

138

ROTHSCHILD and BALSIGER: LINEAR-PROGRAMMING SOLUTION

"A practical problem which completely satisfies
all of the assumptions of LP is very rare indeed.
However, the LP model is often the most accu-
rate representation of the problem, which will
yield a reasonable recommendation for action be-
fore implementation is required."

ACKNOWLEDGMENTS

Much of the data used in this paper was un-
available in the literature. We obtained un-
published information on cannery operations
from several members of the salmon industry.
Bruce B. Bare was kind enough to advise us on
several aspects of the linear-programming tech-
nique. We also thank Donald E. Rogers for sup-
plying us with unpublished biological data and
considerable advice. We appreciate the critical
reviews which were given by Robert L. Burgner,
Gardner M. Brown, Douglas G. Chapman, and
Allan C. Hartt, all of the University of Wash-
ington, and we appreciate as well the various
suggestions made by anonymous referees.

LITERATURE CITED

Burgner, Robert L., Charles J. DiCostanzo, Robert
J. Ellis, George Y. Harry, Jr., Wilbur L. Hartman,
Orra E. Kerns, Jr., Ole A. Mathisen, and William

F. ROYCE.

1969. Biological studies and estimates of optimum

escapements of sockeye salmon in the major river
systems in southwestern Alaska. U.S. Fish WildL
Serv. Bull. 67(2): 405-459.

Crutchfield, James A., and Giulio Pontecorvo.

1969. Pacific sahnon fisheries: A study of irra-
tional conservation. Johns Hopkins Press, Balt-
imore, Md., 220 p.

Gass, Saul I.

1964. Linear programming. McGraw Hill, Inc.,
New York, N.Y., 280 p.

Hillier, F. S., and G. J. Lieberman.

1967. Introduction to operations research. Hold-
en-Day, Inc., San Francisco, Calif., 639 p.
Mathisen, Ole A.

1962. The effect of altered sex ratios on the spawn-
ing of red salmon. In Ted Swei-yen Koo (ed.),
Studies of Alaska red salmon, p. 137-245. Uni-
versity of Washington Press, Seattle, Wash.

1969. Growth of sockeye salmon in relation to
abundance in the Kvichak district, Bristol Bay,
Alaska. Fiskeridir. Skr. Ser. Havunders. 15(3):
172-185.
Mathews, Stephen Barstow.

1966. The economic consequence of forecasting
sockeye salmon (Oncorhynchus nerka Walbaum)
runs to Bristol Bay, Alaska: A computer simu-
lation study of the potential benefits to a salmon
canning industry from accurate forecasts of the
runs. Ph.D. Thesis, University of Washington,
Seattle, Wash., 238 p.
Ripfenburgh, Robert H.

1969. Stochastic model of interpopulation dynam-
ics in marine ecology. J. Fish. Res. Bd. Can.
26(11): 2843-2880.
RoYCE, William 6.

1965. Almanac of Bristol Bay sockeye salmon.
Univ. Wash., Fish. Res. Inst., Giro. 234, 48 p.

139

FISHERY BULLETIN: VOL. «9. NO- 1

Appendix Table 1. — Constants used in value-function
equations for each entity and day of the 1960 run.

Function P

Function 2-

Function 3^

Entity I

1.382
.153

1.365
.153

1.331
.000417

Entity 2

IP2
i2

1.998
.222

1.974
.222

1.925
.000583

Entity 3

1.470
.135

1.455
.135

1.425
.000472

Entity 4

1.964
.186

1.944
.186

1.903
.000694

For entity i on day ;,

Value i,j = !Pi. for ; < 6. Value ,-,/ = !Pi - .03X (weight of

entity i in pounds), for / > 6.

■ For entity t on day /,
Value a = IP: - •

(4.5 + .5J)

^ For entity i on day ;,
Value i^j = IPi - A,.V'2

Appendix Table 2. — Total run, total catch, and value functions for each entity and day of the 1960 season.

Entity

Day

Total

Totol

Value

Value

Value

Entity

Day

Total

Total

Value

Value

Value

run

catch

function n

function 2-

function 3^

run

catch

function P

function 2-

function 3^

1 I

280,351

119,149

1.382

1.362

1.331

3 1

211,080

53,192

1.470

1.453

1.425

2

368,062

156,426

1.382

1,361

1.329

2

277,120

69,834

1.470

1.451

1.423

3

475,118

201,925

1.382

1.358

1.327

3

357,724

90,146

1 470

1.449

1.421

4

600,110

255,046

1.382

1.353

1.323

4

451,832

113,861

1.470

1.445

1.418

5

737,489

313,432

1.382

1.347

1.319

5

555,267

139,927

1.470

1.439

1.415

6

876,389

372,465

1.382

1.337

1.314

6

659,846

166,281

1.470

1.430

1.410

7

1 ,000,833

425,354

1.229

1.324

1.308

7

753,542

189,892

1.335

1.419

1.405

8

1,092.325

464,238

1.229

1.307

1.301

3

822,427

207,252

1.335

1.404

1.398

9

1,134,780

482,281

1.229

1.238

1.293

9

854,393

215,307

1-335

1-387

1.391

10

1,120,032

476,014

1.229

1.270

1.284

10

843,289

212,488

1-335

1-371

1.383

11

1 ,050,967

446,661

1,229

1.253

1.274

11

791,289

199,404

1-335

1-356

1.375

12

940,395

399,668

1.229

1.240

1.264

12

708,038

178,426

1-335

1-345

1.365

13

806,344

342,696

1.229

1.230

1.251

13

607,110

152,992

1-335

1-336

1.355

14

666,514

283,268

1.229

1.224

1.238

14

501,829

126,460

1-335

1.330

1.343

15

534,438

227,136

1.229

1.219

1.225

15

402,387

101,401

1-335

1.326

1.331

16

418,185

177,729

1.229

1.216

1.210

16

314,858

79,344

1-335

1.324

1.318

17

321,003

136,426

1.229

1.215

1.195

17

241,688

60,905

1.335

1.322

1.304

18

242,797

103,188

1.229

1.214

1.178

18

182,805

46,066

1.335

1.321

1.290

2 1

9,590

5,427

1.998

1.970

1.924

4 1

24,985

17,289

1.964

1-941

1.902

2

12,590

7,126

1.998

1.967

1.922

2

32,803

22,700

1.964

1-939

1.901

3

16,252

9,199

1.998

1.963

1.919

3

42,344

29,302

1.964

1-935

1.898

4

20,528

11,618

1.998

1.957

1.914

4

53,484

37,010

1.964

1-930

1.894

5

25,227

14,278

1.998

1.948

1.908

5

65,727

45,483

1.964

1-922

1.888

6

29,978

16,967

1.998

1.934

1.900

6

78,106

54,050

1.964

1-910

1.882

7

34,235

19,377

1.776

1.914

1.891

7

89,197

61,724

1.778

1-894

1.874

8

37,365

21,149

1.776

1.890

1.881

8

97,351

67,367

1.778

1,874

1.866

9

38,817

21,970

1.776

1.863

1.669

9

101,135

69,985

1.778

1.851

1.856

10

38,313

21,968

1.776

1.836

1.856

10

99,820

69,075

1.778

1.828

1.845

11

35,950

20,347

1.776

1.812

1.841

11

93,665

64,816

1.778

1.808

1.832

12

32,168

18,207

1.776

1.792

1.825

12

83,811

57,997

1.778

1.792

1.819

13

27,582

14,479

1.776

1.778

1.808

13

71,864

49,730

1.778

1.780

1.804

14.

22,800

12,905

1.776

1.769

1.789

14

59,402

41,106

1.778

1.772

1-789

IS

18,281

10,347

1.776

1.763

1.769

15

47,631

32,960

1.778

1.767

1.772

14

14,305

8,096

1.776

1.759

1.747

16

37,270

25,790

1.778

1.763

1.754

17

10,980

6,215

1.776

1.756

1.724

17

28,609

19,797

1.778

1.761

1.735

18

8,305

4,700

1.776

1.754

1.700

18

21,639

14,974

1.778

1.760

1.714

' After day 6, the price dropped 3tf per pound.

2 The price was reduced by subtracting a logistic curve that reduced the price of each entity by 3(f per pound over the season.

^ The price wos reduced by subtracting a quadratic curve that reduced the price of each entity by 3^ per pound over the season.

140

CHEMICAL AND NUTRITIONAL CHARACTERISTICS OF
FISH PROTEIN CONCENTRATE PROCESSED FROM
HEATED WHOLE RED HAKE, Urophycis chuss

David L. Dubrow and Bruce R. Stillings'

ABSTRACT

This study was to determine whether cooking lean, whole fish before they are extracted by solvent af-
fects the chemical and nutritional characteristics of the resulting fish protein concentrate. When red
hake were heated at 100° and 109° C for as long as 80 min, the chemical and nutritional properties
of the fish protein concentrate were not adversely affected significantly. The nutritional quality was
slightly lower, however, in fish protein concentrate produced from red hake that were heated at 121° C
for 10 to 80 rain.

Fish protein concentrate (FPC) contains pro-
tein tliat is high in quality. It tlierefore can be
used to supplement diets that contain inadequate
amounts of high-quality protein.

Fish protein concentrate is prepared by re-
moving most of the lipids and water from whole
fish. Several methods for preparing FPC have
been investigated. They can be classified as
chemical, biological, and physical. Most inves-
tigators have used chemical methods in which
solvents extract the lipids and water from whole
fish.

In the United States, two processes for making
FPC have been approved by the Food and Drug
Administration. Both of these are chemical
processes in which solvents are used. In the
overall program of the National Marine Fisher-
ies Service National Center for Fish Protein Con-
centrate, various approaches to processing are
being investigated. One such approach is cook-
ing and pressing fish prior to solvent extraction.
This procedure would tend to reduce the volume
of solvent required for extraction, inasmuch as
water and lipids would be expressed during the
pressing stage.

Raw fish are diflicult to press because of their
physical consistency. The processor can over-
come this problem by cooking the fish before

' National Marine Fisheries Service National Center
for Fish Protein Concentrate, College Park, Md. 20740.

pressing them. If he subjects the fish to a high
temperature for a long time, however, undesir-
able chemical reactions may occur that decrease
the quality of the protein.

The purpose of this study therefore was to
find whether or not the chemical composition
and nutritional quality of fish protein coilcen-
trate are altered when the FPC is produced by
solvent extraction of fish that have been cooked
at different temperatures for varying periods
of time.

CHEMICAL COMPOSITION

Reported here are both the proximate compo-
sition and amino acid composition of the FPC
produced from cooked fish.

PROXIMATE COMPOSITION

We used red hake, Urophycis chuss, which are
lean fish. They were caught off the coast of
New England in the area of Block Island, situ-
ated south southwest of Point Judith, R.I. The
hake were iced on board the vessel and were
then frozen in 25-lb. wax laminated cartons at
the dock. The hake were kept frozen while
being shipped to the National Marine Fisheries
Service National Center for Fish Protein Con-
centrate in College Park, Md. The shipment
contained about 96 cartons. From these 96
boxes, 15 cartons (375 lb.) were picked at
random for the investigation and were stored

Manuscript received August 1970

FISHERY BULLETIN: VOL. 69, NO. I, 1971.

141

FISHERY BULLETIN: VOL. 69, NO. 1

at — 20° C (The other cartons were used in
another experiment.) The hake were used with-
in 1 month after storage.

About 17 to 18 hr before studying each pro-
cessing variable, we placed one carton of fish
in a refrigerated room at a temperature of 5°
to 6° C. This treatment allowed the fish to thaw
sufliciently so that they could be handled indi-
vidually. The fish were ground through a Ho-
bart meat grinder," which was equipped with an
end plate containing holes that were one-quarter
inch in diameter. After the hake were ground,
they were thoroughly mixed, and a sample that
weighed 20 lb was removed. The sample was
divided into three equal portions, and each por-
tion was placed in a 2-inch-deep tray lined with
aluminum foil. (This procedure was used in
order to permit existing equipment to be used.)

The trays were placed in an autoclave and
were heated at 100°, 109°, or 121° C for 10,
20, 40, or 80 min. Thermocouples were used to
measure the temperature of the samples. After
being heated, the trays were removed from the
autoclave, were covered with aluminum foil, and
were cooled in a refrigerated room at 5° to 6° C.
A control sample was also prepared, which con-
sisted of raw, unheated ground hake.

The entire contents of the trays were mixed
with solvent at a 2:1 (w/w) ratio of solvent
to solid. The samples were extracted by the
"cross-current" batch-extraction procedure de-
scribed by Brown and Miller (1969). The
solvent used for extraction was 91 % , by volume,
isopropyl alcohol.

The extracted and dried samples of FPC were
ground in a Rietz Disintegrator.

The samples were analyzed for crude protein,
volatiles, and ash by the methods described by
Horwitz (196.5). Lipids were determined by
the method of Smith, Ambrose, and Knobl
(1964).

Table 1 shows the concentrations of crude
protein, ash, and lipids found.

The concentration of crude protein in the
samples that were heated was slightly lower
than in the sample that was not heated. The

Table 1. — Proximate composition, expressed on a mois-
ture-free basis, of samples of FPC prepared from hake
that were heated for var>'ing times and temperatures
before being extracted with solvent.

Sompla

Crudo protein

Ash

Lipid

Nonheated control

%
88.7

%
13.8

%
0.16

Heated sompies:

100° C for:

10 min

86.0

15.3

0.16

20 min

8S.3

15.4

0.16

40 min

063

15.0

0.20

80 min

85.9

15.5

0.15

Mean

85.9

15.3

0.17

109° C for,

10 min

87.5

14.4

0.12

20 min

85.6

15.8

0.12

40 min

86.8

15,7

0 21

80 min

87.4

13.8

0.15

Mean

86.8

14.9

0.15

121° C for:

10 min

87.3

13.6

0.12

20 min

85.9

15.2

0.14

40 min

86.5

13.7

0.16

80 min

86.8

14.3

0.16

Mean

86.6

14.2

0.14

' The use of trade names is merely to facilitate de-
scriptions; no endorsement is implied.

concentration of crude protein, however, was
not significantly affected by the temperature at
which the samples were heated. Also, the time
of heating did not significantly aflFect the con-
centration of crude protein in the samples,
except for the 20-min treatment. The samples
that were heated for 20 min had a slightly low-
er concentration of crude protein than did those
that were heated for the other intervals of time.

The concentration of ash was slightly higher
in the samples that were heated than in the
sample that was not heated. The concentration
of ash in the heated samples was not afl!'ected
by either the temperature of heating or the
length of time of heating.

The concentration of lipid in the samples was
somewhat variable, but it was not significantly
affected by the treatments.

AMINO ACID COMPOSITION

Es.sential amino acids, excejjt for tryptophan,
were determined with an automatic amino acid
analyzer by the method described by Moore,
Spackman, and Stein (1958). Tryptophan was
determined chemically by the method of Spies
and Chambers ( 1949) . Cystine was determined

142

DUBROW and STILLINGS : FPC PROCESSED FROM HEATED RED HAKE

microbiologically by the method of Henderson
and Snell (1948). Available lysine was deter-
mined by the method described by Carpenter
(1960).

We found only slight changes in the concen-
trations of amino acids in the samples (table 2).
The treatments that we used did not consistently
affect the concentrations of amino acids, except
for cystine and available lysine. The concen-
tration of cystine was reduced in the sample
heated at 121° C for 80 min. The concentrations
of available lysine were slightly lower in the
samples heated at 100° and 109° C for 20 min.
The reason for these decreases is not apparent
to us.

Evans and McGinnis (1948) previously re-
ported that cystine was reduced when soybeans
were autoclaved at 130° C for 60 min.

NUTRITIONAL QUALITY

The nutritional quality of the samples was
determined in a feeding study using rats. Diets
were prepared that contained 10 ''r protein from
the heated samples, the nonheated sample, or
casein. The diet that contained the nonheated
sample served as a control, and the one that
contained casein served as a reference standard.
The composition of the basal diet was described
earlier by Stillings, Hammerle, and Snyder
(1969).
Male weanling rats of the Carworth Farms

CFE strain were received when they were 22
days old. The rats were housed individually
in cages with screen bottoms and were kept in
an air-conditioned room maintained at about
23° C. During the first 2 days, the rats were
fed a basal diet containing 15% casein. They
were then allotted to groups on the basis of
weight, and the groups were randomly assigned
to different diets. Each group contained 10
rats, and the rats were offered feed and water
ad libitum for 4 weeks.

The amount of feed consumed was recorded
three times each week, and the gains in weight
were determined once each week. At the end
of the experiment, the protein efficiency ratio
was determined by dividing the gain in weight
by the weight of protein consumed.

The data were analyzed statistically. Dif-
ferences between means were determined by
Tukey's procedure as described by Steel and
Torrie (1960: 109).

Table 3 shows the data on the nutritive qual-
ity of the FPC samples. Based on the gain in
weight, intakes of feed, and protein efficiency
ratios, the quality of the samples that were
heated at 100° and 109° C was not significantly
different from the quality of the control, which
was not heated. Samples that were heated at
121° C, however, had a lower quality than the
control sample. In general, the quality of the
samples heated at 100° and 109° C was equal
to that of casein or was slightly higher than

Table 2. — Amino acid composition of FPC samples prepared from hake that were heated for varying times and

temperatures before being extracted with solvent.

acid

Concentration

of amino

acid in:

Unheated
control
sample

Samples h

eated at:

Amino

100°

C for:

109°

: for:

121°

: for:

10

20

40

80

10

20

40

80

10

20

40

80

mm.

mm.

mm.

mm.

mm.

mm.

mm.

mm.

mm.

mm.

mm.

mm.

—

- Grams

per 16 s

rami 0/ n

itrogfil -

6.2

6.7

6.4

6.8

6.4

5.7

7.0

6.1

6.4

6.9

6.1

6.6

6.3

Histidine

1.8

2.0

1.9

1.9

1.8

1.7

1.9

1.7

1.8

2.1

19

1.8

2.0

Isoleucine

4.5

4,3

4.4

4.5

4.3

4.3

4.6

4.5

4.5

4.9

4.6

4.4

4.8

Leucine

7.4

7.2

6.9

7.1

6.9

7.0

7.5

7.0

7.2

8.0

7.2

7.3

7.6

7.7

8-3

7.8

8.0

74

7.1

77

7.1

7.5

8.4

7.5

7.9

7.6

Methionine

3.2

3.1

3.1

3.1

3.0

3.0

3.0

3.1

3.0

36

3.1

3.1

3.4

Phenylaion

ne

4.1

4.1

4,0

4.1

4.0

4.0

4.2

4.1

4.1

4.5

4.1

4.2

4.3

Threonine

4.3

4.2

4.1

4.2

4.0

4.0

4.4

4.2

4.0

4.6

4.1

4.2

4.4

Tryptophan

1.0

1.2

1.2

1.0

1.3

1.2

1.1

l.I

1.2

1.1

1.2

1.3

1.2

Valine

5.1

4.9

50

5.0

5.1

4.8

5,2

4.6

5,0

5.5

5.0

5.0

5.3

Cystine

09

1.2

1.2

1.2

0.9

1.1

1.1

1.1

1.1

1.1

1.1

—

0.7

Avoilable

ysine

7.9

7.8

6.9

7.2

7.9

7.7

6.9

7.2

7.6

7.8

7.1

7.2

7.6

143

FISHERY BULLETIN: VOL. 69, NO, 1

Table 3. — Weight gain, feed intake, and protein effi-
ciency ratio of groups of 10 rats fed diets of FPC samples
prepared from red hake that were heated for varying
times and temperatures before being extracted with
solvent.

Sample

Average daily
weight gain

Averog© daily
feed intake

Protein
efficiency

ratio

Grami

Grams

Nonheated control

4.85

13.8

3.37

Heated samples:

100° C for:

10 min

4.96

14.0

3.41

20 min

4.37

13,0

3.25

40 min

4.50

13.1

3.37

80 min

4.29

13.3

3.16

Mean

4.53

13.4

3.30

109° C lor;

10 min

4.37

12.7

3.35

20 min

4.31

13.1

3.11

40 min

4.45

13.4

3.20

80 min

4.20

12.6

3,28

Mean

4.34

13.0

3,24

121° C for:

10 min

3.21

10,6

3.01

20 min

4.01

12,2

3.13

40 min

3.52

11,1

3.10

80 min

3.20

10,3

3.02

Mean

3.49

11.0

3,07

Casein

3.85

12.0

3.18

Tukey's W (P<0.051

0.81

2.0

0.26

that of casein. When the temperature was in-
creased to 121° C, the quality of the samples was
slightly lower than that of casein but not sig-
nificantly so. At each temperature, the temper-
ature at which the samples were heated had a
more significant effect on the quality of the
samples than did the length of time of heating.

SUMMARY AND CONCLUSIONS

We conducted a study to determine the chem-
ical composition and nutritional quality of FPC
produced from fish that are heated before they
are extracted with solvent. Red hake, which
are lean fish, were heated at 100° C for 10, 20,
40, or 80 min. Other samples were heated for
these same lengths of time at 109° or 121° C.
The samples were then e.xtracted with isopropyl
alcohol. The FPC produced from the samples
of hake that were heated contained slightly less
crude protein and more ash than did the FPC
produced from the samples that were not heated.
The amino acid composition of samples that had
been heated did not differ markedly from the

composition of those that were not heated. The
nutritive quality of the samples that were heated
at 100° and 109° C was not significantly affected.
Samples heated at 121° C, however, were lower
in quality than was the control sample.

We conclude that red hake can be heated at
temperatures of 100° and 109° C for as long
as 80 min before being extracted by solvent with-
out the quality of the protein being affected sig-
nificantly.

LITERATURE CITED

Brown, Norman L., and Harry Miller, Jr.

1969. Experimental production of fish protein con-
centrate (FPC) from Mediterranean sardines.
Commer. Fish. Rev. 31(10): 30-33.
Carpenter, K. J.

1960. The estimation of available lysine in animal-
protein foods. Biochem. J. 77(3): 604-610.
Evans, Robert John, and James McGinnis.

1948. Cystine and methionine metabolism by chicks
receiving raw or autoclaved soybean oil meal.
J. Nutr. 35(4) : 477-488.
Henderson, L. M., and Esmond E. Snell.

1948. A uniform medium for determination of
amino acids with various microorganisms. J.
Biol. Chem. 172(1) : 15-29.

HoRwiTZ, William (chairman and editor).

1965. Official methods of analysis of the Asso-
ciation of Official Agricultural Chemists. 10th
ed. Association of Official Agricultural Chemists,
Washington, D.C., xx -f 957 pp. Sections 22.003,
22.010, and 22.011.
Moore, Stanford, Darrel H. Spackman, and
William H. Stein.

1958. Chromatography of amino acids on sulfo-
nated polystyrene resins. Anal. Chem. 30(7):
1185-1190.
Smith, Preston, Jr., Mary E. Ambrose, and
George N. Knobl, Jr.
1964. Improved rapid method for determining
total lipids in fish meal. Commer. Fish. Rev.
26(7) : 1-5.
Spies, Joseph R., and Dorris C. Chambers.

1949. Chemical determination of tryptophan in
proteins. Anal. Chem. 21(10): 1249-1266.

Steel, Robert G. D., and James H. Torrie.

1960. Principles and procedures of statistics with
special reference to the biological sciences. Mc-
Graw-Hill Book Company, Inc., New York, xvi -|-
481 pp.

Stillings, B. R., O. a. Hammerle, and D. G. Sntoer.
1969. Sequence of limiting amino acids in fish pro-
tein concentrate produced by isopropyl alcohol
extraction of red hake {Urophycis chtiss). J.
Nutr. 97(1) : 70-78.

144

EFFECT OF ICE STORAGE ON
THE CHEMICAL AND NUTRITIVE PROPERTIES OF
SOLVENT-EXTRACTED WHOLE FISH-RED HAKE, Urophycis chuss

David L. Dubrow, Norman L. Brown, E. R. Pariser,
Harry Miller, Jr., V. D. Sidwell, and Mary E. Ambrose'

ABSTRACT

Because red hake that are to be used in the future production of fish protein concentrate will be caught
in quantity, the preservation of the hake during periods of glut will present a problem that possibly can
be solved by storage of the hake in ice.

In our study of this problem, whole red hake were held in ice for 2, 6, 8, and 11 days. Organoleptic
tests on the fresh fish showed that they were edible on the 8th day but were not edible on the 11th day.

Samples of fish were removed during each period of storage and were processed ( 1 ) by f reeze-drying to
produce a reference sample (2) by solvent extraction with isopropyl alcohol to produce a fish protein
concentrate. Proximate composition, amino acid composition, and nutritive quality were determined
comparatively on both of these two kinds of processed samples.

From the data obtained, we concluded that red hake stored in ice for 8 days are suitable for use in
the production of fish protein concentrate and that they would be suitable for this use up to the point
of spoilage of the fish, which occurs sometime between 8 and 11 days.

In the period between the capture and processing:
of fish that are to be used in products for human
consumption, they must be preserved in a man-
ner that maintains their food-grade quality.
This requirement applies to the production of
fish protein concentrate (FPC) as well as to
that of more common fish products.

The preservation of fish is a problem not only
aboard the harvesting vessel but at the shore
processing plant as well. The problem ashore
becomes especially important during periods of
glut when the fresh fish must be held several
days before being processed.

In the manufacture of FPC by the method
we use, oil and moisture are removed from the
fish with isopropyl alcohol. We therefore in-
vestigated the possibility of holding fish in this
solvent (Dubrow and Hammerle, 1969). We
found the method to be entirely suitable for pe-
riods of holding up to 11 days.

Although storage in isopropyl alcohol was
satisfactory, more conventional means of holding

' National Marine Fisheries Service National Center
for Fish Protein Concentrate, College Park, Md. 20740.

the fish, such as storing them in ice, are likely
to be used in commercial operations. During
the time fish are held in ice, however, consider-
able change may occur in the components of
the fish tissue. Endogenous and bacterial en-
zymes may break down protein into water-sol-
uble and volatile components, causing off-flavors
and odors in the fish. In addition, the highly
unsaturated lipids of the fish may oxidize rapidly,
causing the fish to become rancid.

While these changes are taking place in iced
fish, the water from the melting ice is leaching
out some of the compounds that are forming.
Furthermore, the subsequent extraction with
alcohol during the production of FPC, if ade-
quate, removes most of the undesirable com-
Ijounds that were not leached out by the melt
water.

Just what effect the enzymatic and oxidative
changes have on the various components of the
tissues as well as on the nutritive quality of
the protein in the finally processed FPC is not
known. Accordingly, solubilization of the com-
ponents of the fish tissues could alter the com-
position of the finally processed FPC. We should

Manuscript received August 1970.

FISHERY BULLETIN; VOL. 69, NO. 1. 1971.

145

FISHERY BULLETIN: VOL. 69, NO. I

know, of course, what occurs, because FPC is of
value solely as a protein supplement of high
quality.

The aim of this study therefore was to de-
termine the effect that storage of food-grade
fish in ice has on the chemical composition of
the components of the tissue and on the nutritive
quality of the protein. We accomplished this
aim by comparing FPC made from samples of
the ice-stored fish with reference samples made
by freeze-drying samples of the fish. We used
freeze-drying because we believe that this meth-
od of production results in minimum alteration
in the samples during drying.

CHEMICAL COMPOSITION

Both the proximate composition and the
amino acid composition of the samples were
determined.

PROXIMATE COMPOSITION

As indicated earlier, we used standard refer-
ence samples produced under ideal conditions, as
a basis on which to evaluate our samples of FPC.

Standard Reference Sample

About 600 lb of red hake were caught on Jan-
uary 6, 1965, in 25 to 26 fathoms of water oflf
the coast of Rhode Island. The fish were di-
vided randomly into lots of 100 lb each, were iced
immediately, and then were taken to the Bureau
of Commercial Fisheries (BCF) (now National
Marine Fisheries Service) Technological Lab-
oratoiy at Gloucester, Mass., where they were
held in ice.

During the next 11 days, each lot of fish was
inspected periodically for freshness by exper-
ienced BCF fish inspectors at Gloucester. The
factors they considered were (1) damage to the
fish, (2) conditions of the skin, eyes, and gills,
and (3) texture, odor, and flavor of cooked
samples. A numerical score ranging from one
to four was used to rate fish of varying quality
for each of the factors. Fish of perfect or
nearly perfect quality were assigned a value of
1, whereas those at the limit of acceptability
or beyond the limit were assigned a value of 4.

Table 1 shows the data on the subjective eval-
uation of the raw fish. The samples of fish
tested after storage for 11 days in ice were
judged to be at the limit of acceptability. The
fish that had been stored in ice for 8 days were
of acceptable quality and were considered to be
of food grade.

Table 1. — Freshness evaluations of raw red hake stored

in ice for periods up to 11 days.

[Each sample had 50 fish.]

Storoge

Averc

ge sub

ecfive evaluations of:

Time

Damage

Sk.n

Eyes

Gills

Texture

Odor

Flavor

Day!

2

1.00

1.00

1.02

1.40 1.50

1-08

1.0

d

2.26

2.22

2.04

2.32 260

2.38

2.0

8

2.44

2.50

3.00

2.92 3.18

3.10

2,5

11

3.10

4.00

3.86

3.92 3.98

4.00

—

Fish of perfect or nearly perfect qualify were assigned a value of I;
ose of unacceptable quality were assigned a value of 4.

those

After the iced fish had been inspected for
quality, they were shipped in ice to College Park,
Md. Each box of fish, upon receipt at College
Park, was divided into two gi-oups and were
processed immediately— one into a standard
reference sample and the other into FPC.

One portion of 20 lb was selected at random
from the group of fish to be used as a standard
reference sample. The standard reference
sample was prepared by freezing the fish in
liquid nitrogen and grinding the whole fish
through a Rietz Disintegrator' under a stream
of liquid nitrogen, and then freeze-drying the
liquid-nitrogen slurry of ground fish. The
freeze-drying step was carried out under a pres-
sure of 500;* of mercury and at a platen tem-
perature of 40° C. The dried samples were
then removed from the freeze dryer in an at-
mosphere of nitrogen and were sealed in con-
tainers. The containers were maintained at
— 40° C until the samples were needed.

The freeze-dried samples were analyzed for
crude protein, ash, and volatiles in accordance
with standard procedures (Horwitz, 1965). To-
tal lipids were determined by the method of
Smith, Ambrose, and Knobl (1964).

Table 2 shows the ])roximate composition of

' The use of trade names is merely to facilitate de-
scription; no endorsement of products is implied.

146

DUBROW ET AL, : EFFECT OF ICE STORAGE

Table 2. — Proximate composition of freeze-dried, ground
whole hake (standard reference samples) stored in ice
for periods up to 11 days.

Storage
time

Volatiles

Lipids!

Ash'

Crude
protein^

Days
2
6
8
11

3.80
2.49
2.46
4.70

»■(. %
15.30
14.06
14.34
15.07

in. %

13.44
12.84
12.43
12.49

(ff. %
74.47
77.34
77.38
77.01

' The data on lipids, osh, and protein were based on the dry weight
of sample.

2 Crude protein was calculated as N X 0.25.

the various samples of freeze-dried whole fish.
Data are presented on a dry-weight basis to re-
veal possible losses during storage.

The concentration of lipid varied between 14
andl5';r; that of ash, between 12 and 13^c. The
data indicate that the nitrogen fraction did not
change greatly. The crude protein remained rel-
atively constant at about 77 Sr (on a dry- weight
basis) except on the second day of sampling.
This deviation on the second day was probably
the result of a sampling error. Analyses for
nonprotein nitrogen would have been helpful
for interpretive purposes. Unfortunately, they
were not made. Dassow" has reported that the
nonprotein nitrogen fraction of whole Pacific
hake stored in ice did not change significantly
over a period of 11 days.

Fish Protein Concentrate

From the remaining portion of each lot of
fish, 20 lb were selected at random and were ex-
tracted with isopropyl alcohol according to
established procedures (Brown and Miller,
1969). In brief, the fish were ground through
a Hobart meat grinder, were slurried with 15
liters of 91% (v/v) isopropyl alcohol for 30
min, and were centrifuged. The centrifuged
solids were then extracted continuously with hot
isopropyl alcohol at 60° to 70° C and at a rate
of flow of 0.2 gal per minute. After 2 hr the
solids were removed by centrifugation and were
desolventized under vacuum at 60° C.

= Dassow, John A. 1966. Statement of project ac-
complishment, Utilization of fishery resources program.
In Quarterly progress report of the BCF Technological
Laboratory, Seattle, Wash., July 1 - September 30, 1966.
Unpublished report, 6 p.

This method of processing was not intended
to be representative of commercial methods. It
was used in our laboratory at that time solely
as an experimental technique to evaluate selected
variables in the preparation of FPC by solvent
extraction. It has since been replaced by a sev-
eral-stage countercurrent extraction system,
which is both much more economical in the vol-
ume of solvent needed and is more representa-
tive of commercial processing methods. A com-
parison of FPC made by each system has shown
no significant differences, however, either in
chemical composition or in nutritive value.

The proximate composition was determined
by the same method used with the freeze-dried
fish.

Table 3 lists the proximate compositions of the
FPC's prepared from the fish stored in ice for
various periods. The concentrations of lipids

Table 3. — Proximate composition of FPC prepared from
raw fish stored in ice for periods up to 11 days.

Storage
time

Volatiles

Lipids!

Ash'

Crude
protein^

Days

Wl. %

Ifl. %

Ifl. %

»■(. %

2

4.25

0.18

12.30

89.70

6

5.10

0.13

12,44

89.65

3

5.12

0.10

13.19

89.30

11

4.10

0.21

16 04

86.94

! The dato on lipids, ash, and protein were based on the dry weight
of sample.

- Crude protein was calculated as N X 6.25.

and volatiles remained essentially unafi'ected by
storage. The concentration of ash increased,
however, and that of protein (that is, of nitro-
gen) decreased. The major change occurred
after the 8th day of storage. Because the con-
centration of protein in the standard reference
samples did not drop in the same manner as
the concentration of protein did in the FPC's,
the loss of protein could not have occurred dur-
ing storage but must have occurred during pro-
cessing. This conclusion could be accounted for
by the formation, during storage, of soluble ni-
trogenous products resulting from enzymatic
breakdown or bacterial breakdown, or from
both, that were not leached out of the fish during
storage but that were subsequently leached out
during the extraction process used in making
the FPC. This conclusion was further support-

147

FISHERY BULLETIN: VOL. 69. NO. 1

ed by the observed decrease in yield after pro-
cessing— namely, 12.0 percent of 2-day-old fish
to 10.0 percent of 8-day-old fish.

Storage of whole red hake in ice up to 11 days
did not influence the extractability of the lipids.
A slight loss of nitrogen occurred, however, dur-
ing the processing of whole fish stored for 11
days as compared with fish stored for shorter
periods.

AMINO ACID COMPOSITION
Standard Reference Sample

Amino acids were determined by the method
of Spackman, Stein, and Moore (1958).

Table 4 shows that the recovery of amino
acids was relatively constant at about 92'^^'c of
the protein. The essential amino acids for
which analyses were made ranged between 45.5
and 46.3 "^r of the total. No major change in
the pattern of any one particular amino acid
resulted from storage.

In general, this finding agrees with those by
Cohen and Peters (1963) on whiting, Mer/«cc»«
bilinearis, that were stored in ice. These auth-
ors reported, however, that methionine de-
creased after the 13th day with a subsequent

Table 4. — Amino acid composition of raw freeze-dried
whole ground fish. The samples were prepared after fish
were held in ice for periods up to 11 days.

increase in methionine sulfoxide. We do not
know whether this compound was present in the
hake that we studied.

Fish Protein Concentrate

The same methods were used as with the
standard reference sample. That is, the amino
acids were determined by the method of Spack-
man, Stein, and Moore (1958).

Table 5 shows the concentration of amino
acids in the FPC's processed from the fish held
in ice. The data indicate that about 1009c of
the amino acids were recovered.

The essential amino acids constituted 47%
of the total amino acids in the FPC made from
fish stored 2 days, but the concentration of these
amino acids dropped to 43 Sr after the fish had
been stored 11 days. Individual amino acids
decreased in concentration. Of these amino
acids, leucine and isoleucine decreased slightly,
whereas lysine and histidine decreased markedly
after the 8th day of storage. The total concen-
tration of lysine was about 11 '^r less in the FPC
made after the fish had been stored for 11 days
than in the FPC produced after they had been
stored for 2 days. The concentration of histidine

Table 5. — Amino acid composition of FPC prepared
from raw fish held in ice for periods up to 11 days.

Concentration of the
Standard Reference So

given omino acid in the
Tiples after they were held:

Amino acid

Concentration of the
samples extracted o

given amino acid in the
fter they were held for:

2 doys

1 6 days

8 doys

11 doys

2 days |

6 doys

8 days

11 days

Perirnl 0/ Iht

protein (N X

6.25

j

Percent oi the

prot

ein (N X

6.25)

Lysine

7.63

7.44

7.72

7.56

Lysine

867

8.14

8.38

7.72

Histidine

1.92

1.77

1.92

1.76

Histidine

2.06

1.88

2.00

1.74

Ammonia

1.68

1.57

1.58

1.59

Ammonia

1.47

1-57

1 39

1.44

Arginins

5.96

5.82

6.05

5.76

Arginine

7.12

698

7.24

6.92

Aspartic acid

9.50

9.41

9.45

953

Aspartic acid

10.36

10.36

10.17

10.00

Threonine

4.07

4.16

4.08

4.14

Threonine

4.45

4.48

4.51

4.44

Serine

4.08

4.22

4.11

4.11

Serine

4.60

4.59

4.70

4.75

Glutamic acid

14.05

14.32

14.27

14.23

Glutamic acid

15.47

15.57

15.34

15.27

Proline

4.57

4.79

4.69

4.76

Proline

5.01

5.64

559

6.47

Glycine

7.70

8 23

768

7.52

Glycine

8.04

9.20

912

10.23

Alanine

6.50

6.56

6.36

6.41

Alanine

6.78

7.10

6.96

7.23

Valine

4.88

4.78

4.63

4.98

Valine

5.14

5.24

4.95

4.90

Methionine

3,02

3.00

2.91

3.05

Methionine

3.32

3.32

3.46

3.29

Isoleucine

4.21

4.17

4.13

4.32

Isoleucine

4.52

4.46

4.37

4.24

Leucine

7.07

7.03

7 06

7.21

Leucine

7.70

7.54

7.44

7.17

Tyrosine

3.01

2.90

2.88

2.99

Tyrosine

3.39

3.31

3.28

3.14

Phenylalanine

3.82

3.98

3.98

3.94

Phenylolanine

4.12

4.05

4.07

3.91

Total amino acid
recovery

91.99

92.58

91.92

92.27

Total amino acid
recovery

100.75

101.86

101.58

101.44

Percent essential
omino acids

46.29

45.51

44.21

46.30

Percent essential
amino acids

47.00

45.25

45.70

43.71

148

DUBROW ET AL. : EFFECT OF ICE STORAGE

decreased about 15.5'^f within the same period of
time. Both glycine and proline increased in
percentage of the total amino acid concentra-
tion. This increase could possibly be due to
the lack of enzymatic breakdown of the fish
collagens, thereby increasing the percentage of
these amino acids as compared with that of the
amino acids of the myofibrillar proteins.

In retrospect, an analysis of the raw, unpro-
cessed fish for free amino acids or total non-
protein nitrogen would have made the interpre-
tation of these results more certain.

No marked differences in the amino acid
pattern of the standard reference sample could
be detected after storing the whole fish in ice
for periods up to 11 days. The amino acid pat-
tern of the FPC's produced from the same
batch of fish as was the standard reference
sample, did, however, show changes, which were
more pronounced in the FPC processed from
11-day-old fish. These changes appeared to be
the result of alcohol extraction of solubles that
were apparently formed during ice storage and
not leached out by the melt water from the ice.

PROTEIN QUALITY

Table 6. — Mean weight gained, food consumed, and ad-
justed protein efficiency ratio of groups of eight rats fed
freeze-dried whole hake prepared from fish stored in
ice, compared with casein.

Storage
time

Meon
werghr gained

Mean weight of
food consumed

Adjusted

protein

efficiency

ratio^

Day:

Grami

Grams

2

158.6 ± 3,16

390 ± 5.7

3.46 ±

.05

6

150,8 ± 3,08

385 ± 5,9

3.35 ±

.08

B

155.6 ± 5,28

381 ± 7.7

3.49 ±

.07

11

148.6 ± 3.35

400 ± 3.9

3.18 ±

.07

Casein

113.5 ± 5.65

323 ± 3.9

3,00 ±

.00

^ The protein efficiency ratios were odjusted ta a protein efficiency
ratio of 3,00 for casein.

protein quality of the standard reference sample
taken on the 11th day was similar to that of
casein and therefore was lower than that of
the three samples taken earlier.

Proximate composition and concentrations of
amino acid do not account for the difference ob-
tained in the quality of the protein in the
sample of fish held in ice for 11 days. Because
the fish were from the same lot and were chosen
randomly, we can only speculate either that the
utilization (digestibility) of the protein (amino
acids) was decreased or that compounds de-
pressing growth were formed during storage.

STANDARD REFERENCE SAMPLE

Protein efficiency ratios were determined by
the method of Campbell (1960). Diets of the
standard reference samples and of FPC pre-
pared from raw fish stored in ice were fed ad
libitum to male albino rats (Charles River
strain), which were randomly allotted to groups
of 10 animals. The samples were added to a
basal diet at a 10 ""r level of crude protein. Gain
in weight and consumption of food were re-
corded each week for 4 weeks, and the protein
efficiency ratio was calculated as (weight gain)/'
(weight of protein consumed) . A diet in which
casein was the source of protein was used as a
reference.

Table 6 shows the data obtained from the
animal-feeding studies comparing the quality
of the protein of the various samples. Except
for the sample jjrepared from fish held 11 days,
the protein quality of the standard refei'ence
samples was better than that of casein. The

FISH PROTEIN CONCENTRATE

The same methods were used to determine
protein quality as were used with the freeze-
dried fish.

Table 7 shows the data obtained from the
feeding tests made on FPC's produced from
the fish held in iced storage. All the FPC's
gave a greater gain in weight and a higher pro-

Table 7. — Mean weight gained, food consumed, and pro-
tein efficiency ratio of groups of eight rats fed diets of
FPC prepared from raw fish stored in ice for periods
up to 11 days compared with casein.

Storage
time

Mean
weight gained

Mean weight of
food consumed

Adjusted

protein

efficiency

ratio!

Days
2
6
8
11

Grams

154.0 ± 8,63

155.1 ± 8.12
154.4 ± 4.95
145.4 ± 4.80

Grams
363 ± 12.0
362 ± 12.3
368 ± 7.6
358 ± 10.3

3.62 ± .05
3.65 ± .09
3.59 ± .10
3.47 ± .10

Casein

113.5 ± 5.65

323 ± 3.9

3.00 ± .00

1 The protein efficiency ratios were adjusted to a protein efficiency
ratio of 3.00 for casein.

149

FISHERY BLXLETIN: VOL. 69, NO. I

tein efficiency ratio than did the casein. Diets
containing FPC made from fish stored for 2, 6,
and 8 days in ice resulted in protein efficiency
ratios ranging between 3.59 and 3.65. The diet
containing FPC from the U-day-old fish yielded
a slightly lower gain in weight and a protein
efficiency ratio of 3.47. These results agree
with those obtained with the standard reference
samples made from the same fish. The nutritive
quality of the 1 1-day standard reference samples,
however, was poorer than that of the FPC
sample. This anomalous result suggests either an
improved utilization of protein as a result of ex-
traction with isopropyl alcohol or the removal
of some factor that may have depressed growth.
Freeze-dried fish produced from whole red
hake stored in ice 2 to 8 days did not differ in
protein quality. Freeze-dried fish produced
from whole red hake stored for 11 days, how-
ever, was lower in protein quality but still had
a protein efficiency ratio equal to that of casein.
FPC produced from whole fish stored for 2 to
11 days showed no diff'erences in protein quality.
All the FPC's had protein efficiency ratios high-
er than that of casein.

SUMMARY AND CONCLUSIONS

Whole red hake were stored, in ice for 2, 6, 8,
and 11 days. The fish were organoleptically
evaluated for freshness at each storage period
and were then processed by freeze-drying to
form a reference sample or by solvent extraction
with isopropyl alcohol to form a fish protein
concentrate. These products were then analyzed
for proximate composition and amino acid con-
centration and for protein quality.

The results of the subjective evaluation for
freshness indicated that the fish stored up to 8
days were still acceptable for food but that those
stored for 11 days were not acceptable.

The proximate composition and the amino
acid concentration of the freeze-dried whole
samples of fish showed very little change as a
result of the storage of the raw fish in ice. Rat-
feeding tests indicated a loss in protein quality
of the freeze-dried sample prepared from 11-
day-old raw fish. Protein efficiency ratio values
ranged from 3.35 to 3.49 for fish stored up to 8

days, whereas the llth-day sample resulted in
a protein efficiency ratio of 3.18. All protein
efficiency ratio values, however, were equal to
the value for casein or were higher.

The proximate composition of FPC's pro-
duced from fish stored up to 8 days in ice re-
mained relatively constant. The crude protein
in the concentrate produced from fish stored for
1 1 days decreased about 2.5 9f ■ The concentra-
tion of amino acids also followed this pattern
with a resultant lowering in the concentration
of lysine and a slight increase in that of proline
and glycine. The protein quality of the FPC
processed from the 11-day-old fish was also
slightly lower than that of FPC processed from
fresher fish. All FPC's, however, had protein
efficiency ratios higher than that of casein.

We conclude that storage of whole hake in
ice up to 8 days is a satisfactory means of hold-
ing them prior to extracting the ground hake
with isopropyl alcohol to produce FPC.

LITERATURE CITED

Brown, Norman L., and Harry Miller, Jr.

1969. Experimental production of fish protein con-
centrate (FPC) from Mediterranean sardines.
Commer. Fish. Rev. 31(10): 30-33.
Campbell, J. A.

1960. Evaluation of protein in foods for regulatory
purposes. J. Agr. Food Chem. 8(4): 323-327.
Cohen, Edward H., and John A. Peters.

1963. Effect of storage in refrigerated sea water
on amino acids and other components of whiting
(Merluccius bilinearis) . Fish. Ind. Res. 2(2):
5-11.

DuBROw, David, and Olivia Hammerle.

1969. Holding raw fish (red hake) in isopropyl
alcohol for FPC production. Food Technol. 23(2) :
254-256.
HoRWiTZ, William (chairman and editor).

1965. Official methods of analysis of the Associa-
tion of Official Agricultural Chemists. 10th ed.
Association of Official Agricultural Chemists,
Washington, D.C., xx + 957 pp.
Smith, Preston, Jr., Mary E. Ambrose, and George N.
Knobl, Jr.

1964. Improved rapid method for determining total
lipids in fi.sh meal. Commer. Fish. Rev. 26(7) : 1-5.

Spackman, Barrel H., William H. Stein, and
Stanford Moore.

1958. Automatic recording apparatus for use in
the chromatography of amino acids. Anal. Chem.
30(7): 1190-1206.

150

LABORATORY REARING OF THE DESERT PUPFISH, Cyprinodon macularius

David Crear' and Irwin Haydock^

ABSTRACT

The desert pupfish, Cyprinodon macularius, may ba reared in the laboratory for use in the study of
embryology, genetics, physiology, and behavior. It is euryhaline (0-70 %c) and eurythermal (8°-44.6° C)
and may be useful as a bioassay for either freshwater or marine pollutants. In the Salton Sea area
of California, the recent introduction of exotic species and the encroachment of civilization have
drastically reduced the formerly abundant pupfish populations. Laboratory rearing eliminates the need
for continuous exploitation of a rapidly contracting natural population and could supply adequate stocks
for sanctuaries, thereby preserving the species from extinction. Laboratory apparatus and conditions
are described for maintaining larval and adult pupfish. Parasites and diseases encountered are dis-
cussed and successful treatments described. Methods for spawning and rearing the desert pupfish in
the laboratory are detailed. These methods may also be applicable to many other species of pupfish
that are in danger of extinction.

The desert pupfish, Cyprinodon macularius
Baird and Girard, is a killifish (Cyprinodonti-
dae) native to the Lower Colorado River Basin
from southern Arizona to southern California
and the Sonoyta River of northern Sonora, Mex-
ico (Miller, 1948). It thrives under the harsh
conditions of the desert environment. It lives
in fresh water as well as highly saline pools
that few other vertebrates can tolerate. Its
ability to survive in such environments, plus
other important biological characteristics listed
in Table 1, renders it an exceptionally hardy
laboratory animal potentially valuable for re-
search in many fields.

POTENTIAL FOR RESEARCH

Desert pupfish has many characteristics fa-
vorable for embryological research. It can be
spawned with relative ease and can be main-
tained in the laboratory throughout the year
to supply large eggs (approximately 2 mm in di-
ameter) , suitable for vital marking and grafting

' Formerly, California Department of Fish and Game,
Inland Fisheries Branch, Sacramento, Calif.; present
address: School of Public Health, 1890 East-West Road,
University of Hawaii, Honolulu, Hawaii 96822.

' Formerly, California Department of Fish and Game,
Inland Fisheries Branch, Sacramento, Calif.; present
address: Southern California Coastal Water Research
Project, 10845 Lindbrook Drive, Los Angeles, Calif.
90024.

Manus<!ript received September 1970.

FISHERV BULLETIN: VOL. 69. NO. 1. 1971.

experiments. Other favorable characteristics
are the transparent chorion and the long devel-
opmental period which can be temperature-con-
trolled (New. 1966). The sticky filaments that
are attached to the chorion of its demersal egg
can be partially removed by rolling the eggs
gently on filter paper 4 to 8 hr after fertiliza-
tion. Any remaining filaments are matted to-
gether and can be easily removed with small
forceps.

Desert pupfish, since they mature quickly,
could be used for research in fish genetics and
on the aging process. Barlow (1961) reported
that pupfish reach maturity in the field in 3
months. F, pupfish, reared from eggs and
maintained at 27° C, were observed spawning
in the laboratory approximately 4 months after
hatching.

The desert pupfish, a euryplastic species, also
possesses physiological and behavioral traits that
make it valuable for scientific research. The
juveniles can tolerate salinities ranging from
fresh water to 90 <,;, (Barlow, 1958). The
adults, although less euryhaline, are known to
spawn in salinities as high as 70 %r (Kinne and
Kinne, 1962). The salinity tolerance of newly
hatched pupfish render them potentially useful
for comparative bioassay of freshwater and
marine pollution. The extreme temperature tol-
erance is an additional asset. Desert pupfish

151

FISHERY BULLETIN; VOL. 69. NO. 1

Table 1. — Biological characteristics of

the desert pupfish, Cyprinodon macularius, and other important fish in
research."

items

Desert pupfish,
Cyprinodon
macularius

Trout:

Salmo trutta
S. gairdneri

Killifish,
Fundulus
heteroclitus

Medaka,
Oryzias
latipes

Salinity tolerance:

Adults

0-70 %o

Euryholine

Marine-estuarine

Fresh water

Eggs

0-90 X,

Fresh water

Wide tolerance

- ? -

Natural

spawning season

April to
Octobers

Spring or
foil

June to
August

April to
October

Artificial spawning

Spawns naturolly
oil year, cannot
be stripped

Seasonol spowning,
eggs ore stripped

Seasonal spawning,
eggs ore stripped

Spawns naturally
all year, eggs
can be stripped

Egg type

Demersal;
transparent

Demersal;
opoque

Demersal;

transparent

Demersol;
transparent

Egg diameter

Co. 2 mm

Ca. 5 mm

Ca. 2 mm

Ca. 1 mm

Incubotion temperature
Range

13°-36^ C;
at 20° C,
10 days

3»-I3° C;

at I0» C,
34-37 days

15°-27« C;
ot 20' C,
9.5 days

13''-25° C;
at 25' C.
8 days

Length of adult

4-5 cm

15-30 cm at
first spawnir

g

8-12 cm

2-4 cm

Age at maturity

3-4 months

2-4 years

1-2 years (?)

1-2 months

1 Data compiled from: Borlow, 1958, 1961, Frost
Rugh, 1962; Trinkaus, 1967; Yomamoto, 1967.

* Desert pupfish has not been recorded spowning
under the proper conditions [Bunnell, 1970).

and Brown, 1967; Kinne and Kinne, 1962; Miller, 1970 (personol communication); New, 1966;
throughout the year in noture as have other species of pupfish but presumably would do so

have been found in the field at temperatures
ranging from 8° to 44° C (Lowe and Heath,
1969; Kinne, 1960).

Since it can be relatively easily spawned in
the laboratory, the desert pupfish is a good model
for the study of reproductive behavior. Nu-
merous and rapid behavioral sequences precede
the actual spawning act. On occasion, however,
fish in high spawning readiness eliminate many
behavioral sequences and commence spawning
immediately. When properly stimulated the fish
swim parallel to one another, the male slightly
behind the female, twist into an S-curve, and
spawn. Release of the gametes is accompanied
by a quivering movement of both fish. The
male wraps his anal fin under the female's vent
and fertilizes each e^g as it is extruded. The
female then dips, leaving the fertilized egg at-
tached to the substrate. This process is re-
peated until the female is spent, having spawned
50 to 200 eggs in about 2 hr under laboratory
conditions. In nature the female only rarely
spawns more than one or two eggs in succession
(Barlow, 1961). The mature male is easily rec-
ognized by his aggressiveness and his brilliant,
blue coloration. The pugnacious male ])upfish
must be separated in the laboratory from fe-

males and other males. The determination of
the male to spawn, regardless of circumstances,
makes the pupfish a potentially valuable species
for classroom demonstrations. Barlow (1961)
has presented a complete and detailed descrip-
tion of the social and reproductive behavior of
the desert pupfish.

LABORATORY REARING THE
DESERT PUPFISH FOR CONSERVATION

Another value in rearing desert pupfish lies
in the preservation of the species. Today the
pupfish faces elimination from many areas of
its natural range due to predation and compe-
tition from exotic species and the modification
or destruction of its habitat. Lai-ge populations
of desert pupfish, once prevalent around the
Salton Sea, have been alarmingly reduced. At
the present rate of population reduction, the spe-
cies may well become extinct in this area in the
near future unless steps are taken to insure its
survival. Artificial rearing is one of the pos-
sible means.

Coleman (1929) conducted an ecological sur-
vey of the Salton Sea for the California Depart-

152

CREAR and HAVDOCK: REARING DESERT PUPFISH

ment of Fish and Game and judged that the
numbers of mosquitofish, Gambnsia affhiis, and
desert pupfish were sufficient to support a large
population of carnivorous game fish. Cowles
(1934) reported the pupfish populations to be
exceedingly large in and around the Salton Sea.
In 1956 Barlow (1961) observed schools of ju-
venile pupfish of nearly 10,000 individuals. He
estimated that one large, isolated, shore pool
at the Salton Sea contained 150 adults per square
meter. Today, in the Salton Sea area desert
pupfish are almost totally confined to a few trib-
utaries. In response to the severe reduction of
pupfish populations in the Salton Sea area, Jack
Hesemeyer, Supervisor of the Anza-Borrego
State Park, has built a pupfish sanctuary near
the Park headquarters at Borrego Springs. This
small sanctuary was stocked on June 24, 1970,
with 48 laboratory-reared fish produced by the
techniques outlined below. Several hundred
additional fish were placed in the Palm Canyon
pools nearby.

The authors hope that this article, in addition
to demonstrating the value of the desert pup-
fish as a teaching and research animal, will help
in its preservation by describing laboratory-
spawning methods that can provide adequate
stocks for sanctuaries in natural and artificial
habitats. In addition, the rearing techniques
described here for desert pupfish may be useful
for the preservation of many other species of
pupfish that are in danger of extinction.

MATERIALS AND METHODS

The desert pupfish used to develop spawning
techniques were seined from an irrigation ditch
emptying on the northwestern shore of the
Salton Sea in Riverside County, Calif. Speci-
mens were transported in plastic garbage pails
filled with aerated ditch water to the Fishery-
Oceanography Center at La JoUa, Calif. We
found that the water temperature during trans-
port should not be allowed to fluctuate radically
from that at which the fish are found.

Many of the specimens collected were infected
by a freshwater parasitic copepod of the family
Lernaeidae (possibly introduced with home-
aquarium fish). The large egg cases of this

copepod were clearly visible on the fish, usually
at the base of the fins. Individuals carrying
this parasite were weak and commonly died dur-
ing or soon after transport. Reichenbach-Klinke
and Elkan (1965) recommend a salt bath (NaCl,
0.76-1.1'^r) to eliminate such copepods. To
treat this infection, all fish on arrival at the
laboratory were converted to seawater over a
5-day period. Kinne (1960) reported that a 1-
month-old pupfish can survive sudden salinity
changes up to 35 '/ic, whereas 1-year-old adults
cannot survive sudden salinity changes of more
than 10 to 15 7^. Robert R. Miller (1970, per-
sonal communication), however, reports that in
1937 he found that this species could be shifted
with ease directly from fresh water to seawater
and back. After conversion to seawater all
traces of the parasitic copepod vanished. To-
ward the end of the experiment, several fish
died from a devastating protozoan infection in
the epithelial tissue surrounding the mouth.
The tissue appeared bloody and often had com-
pletely disintegrated. Many apparently healthy
fish died with little or no warning in less than
12 hr. The marine parasitic protozoan, Cryp-
tocaryon irritans, prevalent in the Scripps water
system was suspected ( Wilkie and Gordin, 1969) .
The surviving fish were transferred back to fresh
water and, fortunately, the parasite failed to
make the transition.

LABORATORY CONDITIONS

The fish were maintained in 20-gal tanks with
subsurface filters covered with crushed oyster
shell. The water was changed completely and
the shell washed approximately every 6 weeks.
Four individuals were isolated in each aquarium
by plastic, perforated dividers. The tanks were
maintained at room temperature, 20° to 22° C.
Standard aquarium heaters were used whenever
higher temperatures were needed. No attempt
was made to control pH other than the use of
the crushed oyster shell substrate.

The fish were fed frozen adult brine shrimp,
Artemia salina, three times daily during the
week and once a day on weekends. Kinne (1960)
and Kinne and Kinne (1962) used two species of

153

FISHERY BULLETIN. VOL. 69, NO. I

worms {Enchytraeus albidzis' and Tubifex sp.),
two species of crustaceans (Daphnia and Cy-
clops), beef liver, fresh lettuce, spinach, and
several brands of commercial fish food.

The fish were subjected to a daily 16-hr light
and 8-hr dark cycle. The lighting used was a
combination of daylight fluorescent bulbs and
mercury vapor arc lamps. Most fish were ready
to spawn under these conditions within 3 weeks
of capture, although there was marked seasonal
and individual variation. Observations made
suggest the length of the light period is more
important than light intensity for the induction
of spawning. Kinne and Kinne (1962) reported
using a 14L-10D cycle with a combination of
fluorescent tubes and natural daylight.

SPAWNING METHODS

The fish were spawned on a varied schedule,
depending on the readiness of the female. The
average female spawned 50 to 200 eggs, de-
pending upon her size, approximately once a
week. One large, exceptionally prolific female
spawned 200 eggs twice a week for 2 months.
Subsequently, this female was not spawned on
schedule, became eggbound, and was unable to
extrude her eggs. After her death the large,
single ovary contained over 800 eggs and ac-
counted for 44 ""r of the total body weight. Fe-
males that would not spawn at room temperature
were spawned at 27° C. Females that could
not spawn at either room temperature or 27° C
were removed from isolation to a community
tank (4 females, 2 males) on a 12L-12D photo-
period, wherein they quickly spawned out their
eggs at 27° C. Kinne (1960) reported that the
fish do not spawn in the laboratory at temper-
atures below 20° C and seem to spawn optimally
between 28° and 32° C. He also noted that
the temperature in the field varies betw-een 25°
and 35° C for most of the spawning season.

Kinne and Kinne (1962) reported that i)up-
fish embryos have one period of low thermal
stability between fertilization and gastrulation
and a second period just before hatching. Ob-

' See Kinne (1960) for details on mass culturinK
Enchytraeus albidus.

sei-vations made during our study indicate an-
other period of low thermal stability just before
fertilization. When a female maintained at
room temperature is transferred to a higher tem-
perature to induce spawTiing, most of the eggs
either are not fertilized or do not develop. We
found that females should be maintained and
spawned at one temperature. If maintained at
a temperature above 25° C, they will need to
be spawned regularly; otherwise, the eggs are
dropped to the bottom of the aquarium un-
fertilized. A more flexible spawning schedule
is possible if the female is kept at a lower tem-
perature.

The fish were spawned in white, plastic, food
containers measuring 27 x 20 x 10 cm, con-
taining 2.5 liters of water at 22° C. Immedi-
ately after the spawning these containers were
suspended in a water bath at 27° C. This tech-
nique produced good hatches in spite of the re-
ported low thermal stability bet^veen fertiliza-
tion and gastrulation (Kinne and Kinne, 1962).
The water bath was a 20-gal tank with a stand-
ard aquarium heater.

Either a green plastic mat or white cheese-
cloth was used as a substrate on which the fe-
males could attach the adhesive eggs. On several
occasions, when the plastic mat was used, the
pupfish were observed eating the previously
spawned eggs, which were readily visible against
the green background. The substitution of
cheesecloth with L-shaped glass-rod weights at
its periphery successfully reduced parental egg
consumption. The cheesecloth was a superior
substrate because many of the eggs were buried
in the material and thus were inaccessible to
the parents. Furthermore, the combination of
a white spawning bin, white cheesecloth, and
nearly transparent eggs made the latter virtually
invisible to the experimenters and, presumably,
to the fish.

The parent fish were well fed prior to spawn-
ing to help reduce the number of eggs consumed.
The spawning bin, containing the female, was
placed in a quiet location. Five to fifteen min
later the male was introduced to the spawning
bin which was then left undisturbed for 1 to
2 hr. Barlow (1961) reported that spawning

154

CREAR and HAVEWCK: REARING DESERT PUPFISH

lasts from 30 min to 2 hr, depending on the
size of the female and the number of eggs laid.
In order to prevent the serious injury or death
of the female, the male was not left in the spawn-
ing bin for longer than 2 hr. After termination
of spawning the fish were returned to their
aquaria and the feces were removed from the
container. The spawning bin was then sus-
pended in a 27° C water bath with aeration.
Kinne and Kinne's (1962) data on hatching
shows that any incubation temperature between
24° and 30° C should produce hatches of at least
80 Sf in 100 '~r air-saturated seawater. Pup-
fish eggs left at room temperature in the lab-
oratory at La Jolla suffered extremely high mor-
talities owing to daily temperature fluctuations
between 18° and 24° C. Kinne and Kinne (1962)
supplied data on egg mortalities and incubation
periods at different temperatures from 10° to
37° C.

Hatching success of different breeding pairs
varied unexplainably under constant conditions.
A large sample of eggs from one breeding pair
showed, however, that salinity and temperature
markedly effected the hatching success of pup-
fish eggs (Table 2). Eggs in small clusters,
apparently laid at nearly the same instant, sel-
dom hatched. Kinne and Kinne (1962) also
reported reduced development and increased
mortalities for conglomerated eggs.

Pupfish larvae are large enough (5.5 mm total
length at 27° C in 50 9 seawater) to feed from
the day of hatching on brine shrimp nauplii
(Salt Lake variety), Artemia salina. The
larvae when handled were drawn with a bulb
into a long glass tube. Kinne and Kinne (1962)
gave extensive data on the growth, food intake,

Table 2. — Hatching success of desert pupfish eggs.

Salinity

Temperature

Eggs

Developing

1

t5ead

Total

Fresh water

" C
22

No.
74

%
54.0

No.
66

No.
140

27
27

4
3

5.4
5.0

70

57

74
60

Half seawate

r 27

92

85.1

16

loa

Seawoter

27
27
27

17
13
7

29.6
29.5
166

40
31
35

57
44
42

and food conversion for pupfish larvae at dif-
ferent temperatures and salinities.

CONCLUSIONS

The desert pupfish may be reared in the lab-
oratory over a wide range of temperatures and
salinities. Half-strength seawater at 27° C pro-
vided the best hatch observed during this study.
The pupfish is a hardy laboratory animal that
does well in captivity if proper attention is paid
to food, space, and hygiene. However, a note
of caution should be added, since we reared only
two generations of pupfish. Bunnell (1970)
states that when a pupfish stock is bred in cap-
tivity from a single pair, the fish do well at first,
but gradually die out over several generations.
This possibility should be further substantiated
before committing experimental studies to a
single line of descent.

The authors believe that the desert pupfish is
an excellent experimental animal for many types
of biological research. Studies of the syste-
matics (Miller, 1948) , behavior (Barlow, 1961),
and physiology (e.g., Kinne and Kinne, 1962)
provide a wealth of background information on
the basic biology of pupfish which will prove
valuable to investigators interested in using this
species in teaching and research. Other reports
(e.g., Bunnell, 1970) indicate the critical status
of some species of Cyprinodon, including C.
macularius, and point out the need to provide
sanctuaries to avoid extinction of this unique
species. Laboratory rearing of pupfish will not
only provide material for scientific observation
and experimentation, but will also remove some
of the pressure on an already rapidly contracting
natural population by providing adequate stocks
for present and future sanctuaries. Both
measures should enhance the value of the desert
pupfish and emphasize the importance of saving
the species from extinction.

ACKNOWLEDGMENTS

The authors wish to extend their deep appre-
ciation to Robert Rush Miller and Carl Hubbs
for their valuable suggestions and extensive
editing of this manuscript.

155

FISHERY BULLETIN, VOL. 69. NO. 1

LITERATURE CITED

Barlow, George W.

1958. High salinity mortality of desert pupfish,
Cyprinodon macularius. Copeia 1958(3) : 231-232.

1961. Social behavior of the desert pupfish, Cyprin-
odon macularius, in the field and in the aquar-
ium. Amer. Midi. Natur. 65(2): 339-359.

Bunnell, Sterling.

1970. The desert pupfish. In Pupfish of the Death
Valley region. Cry Calif. 5(2): 2-13.
Coleman, George A.

1929. A biological survey of Salton Sea. Calif.
Fish Game 15(3) : 218-227.
Cowles, Raymond B.

1934. Notes on the ecology and breeding habits
of the desert minnow, Cyprinodon 7nacidariits
Baird and Girard. Copeia 1934(1): 40-42.
Frost, W. E., and M. E. Brown.

1967. The trout. Collins, London. 286 p.
Kinne, Otto.

1960. Growth, food intake, and food conversion
in a euryplastic fish exposed to different temper-
atures and salinities. Physiol. Zool. 33(4) : 288-
317.
Kinne, Otto, and Eva Maria Kinne.

1962. Rates of development in embryos of a cyprin-
odont fish e.xposed to different temperature-sa-
linity-oxygen combinations. Can. J. Zool. 40(2) :
231-253.

Lowe, Charle. H., and Wallace G. Heath.

1969. Behavioral and physiological responses to
temperature in the desert pupfish Cyprinodon
macularitis. Physiol. Zool. 42(1): 53-59.

Miller, Robert R.

1948. The cyprinodont fishes of the Death Valley
system of eastern California and southwestern
Nevada. Misc. Publ. Mus. Zool. Univ. Mich. 68.
155 p.

New, D. a. T.

1966. The culture of vertebrate embryos. Logos
Press, Academic Press, London, x -f- 245 p.

Reichenbach-Klinke, H., and E. Elkan.

1965. The principal diseases of lower vertebrates.
Academic Press, London. 600 p.
RuGH, Robert.

1962. E.xperimental embryology. Burgess Publish-
ing Company, Minneapolis. 501 p.
Trinkaus, J. P.

1967. Fimdidus. In Fred H. Wilt and Norman K.
Wessells (editors), Methods in developmental bi-
ology, p. 113-122. Thomas Y. Crowell Company,
New York.

WiLKiE, Donald W., and Hillel Gordin.

1969. Outbreak of Cryptocaryoniasis in marine
aquaria at Scripps Institution of Oceanography.
Calif. Fish Game 55(3): 227-236.
Yamamoto, Toki-o.

1967. Medaka. In Fred H. Wilt and Norman K.
Wessells (editors). Methods in developmental bi-
ology, p. 101-111. Thomas Y. Crowell Company,
New York.

156

GONAD MATURATION AND HORMONE-INDUCED SPAWNING
OF THE GULF CROAKER, Bairdiella icistia'

Irwin Haydock"

ABSTRACT

Successful methods of capture, transport, disease treatment, and laboratory maintenance of the gulf
croaker, Bairdiella icistia, are described. Gonad maturation was achieved out of season by the use of
appropriate controlled photoperiods, temperatures, and abundant feeding. Mature fish or fish brought
to maturity in the laboratory were spawned with suitable hormone injections and the time of spawning
could be accurately predicted. Eggs obtained from hormone-induced spawning were normal in all re-
spects and the larvae were reared through metamorphosis using rotifers and brine shrimp nauplii as
food; thus, the life history of this marine fish can, for the first time, be completed under controlled lab-
oratory conditions. The techniques developed for croakers may have application to mariculture, biossay
of marine pollution, and in more general research on marine fish reproduction.

Reproduction in fishes which spawn annually
is controlled by the interaction of exogenous and
endogenous stimuli, particularly the endocrine
activity of the pituitary-gonadal axis which is
indirectl.v influenced by environmental factors
such as day length and temperature. Against
this basic background, which determines the
gonadal maturation cycle, the actual spawning
act is controlled by neurohumeral and neuro-
muscular connections activated by rapidly
changing environmental parameters and behav-
ioral cues (Liley, 1969; Malven, 1970). This
basic reproductive pattern and the lacunae in
our understanding of it have recently teen re-
viewed in detail (Breder and Rosen, 1966; Hoar,
1969).

Much of the work on reproductive physiology
of fishes has been done with freshwater species
of interest to aquarists (Wickler, 1966) or ex-
perimentalists (New, 1966; Hoar, 1969; Liley,
1969). There is, however, no reason to suspect
that the basic features of reproduction, eluci-
dated with freshwater species convenient to

' This research was supported, in part, by Federal
Aid to Fish Restoration Funds, Dingell-Johnson Project
California F-24-R, "Salton Sea Investigations."

" Formerly, California Department of Fish and Game,
Inland Fisheries Branch, Sacramento, Calif. ; present ad-
dress: Southern California Coastal Water Research
Project, 18045 Lindbrook Drive, Los Angeles, Calif.
90024.

Manuscript received September 1970.

FISHERY BULLETIN: VOL. 69. NO. 1, 1971.

maintain, will differ significantly from those of
marine forms, which require more elaborate
facilities for study.

Because of increasing demand for fish as a
source of protein, as well as for sport and for
scientific studies on reproductive success of
fishes in generally deteriorating natural environ-
ments, there are now intensive and extensive
efforts to artificially culture commercially val-
uable freshwater species (Hickling, 1962; Hora
and Pillay, 1962; Bardach, 1968). Recent in-
terest has also focused on mariculture, the culti-
vation of marine species. Some success has been
achieved in Great Britain (plaice and sole —
Shelbourne, 1964 and 1970), Japan (bream and
yellowtail — Harada, 1970), and in the United
States (pompano — Finucane, 1970). However,
all such cultures are started either with young
fish caught at sea or with eggs spawned in the
sea or stripped from mature fish captured during
their normal spawning season. The field work
necessitated by this method can be costly and
unpredictable, drawbacks which are compounded
by the difficulty usually experienced in simul-
taneously finding running-ripe fish of both sexes,
especially females. These pi-oblems are avoided
in the culture of salmonids because of the unique
determination of the fish to return to the same
place to spawn at a fairly predictable time
(Leitritz, 1959). The grunion is a striking

157

FISHERY BULLETIN: VOL. 69, NO. 1

example of a marine fish showing similar deter-
mination (Walker, 1952).

The necessity of working with the reproduc-
tive products of one species only during its
normal spawning season is one of the major
obstacles faced by experimentalists and fish
culturists. Most species of temperate and high
latitudes show rather well-defined, short spawn-
ing seasons, probably related to the annual cycle
of day length, temperature, and associated pro-
ductivity. This seasonality generally means
that experimental work proceeds at a hectic pace
for a short time and then must be dropped or
switched to another species available in breed-
ing condition. This causes numerous difficulties,
delays, and expenses for both research and re-
searcher. The answer to this problem is to
artificially induce maturation and spawning
under controlled laboratory conditions.

To my knowledge, artificial gonad maturation
under controlled conditions of light and temper-
ature, hormone-induced spawning, and labora-
tory rearing of the fragile larvae through meta-
morphosis have not been accomplished for any
single marine fish prior to this time. Pompano
have been spawned with hormones, but the fer-
tilized eggs did not hatch (Finucane, 1970). A
euryhaline form, Fundulus heteroclitiis, has been
spawned with pituitary extract (Joseph and
Saksena, 1966) ; however, only mature fish re-
cently obtained from their natural environment
were used.

Protocols for hormone-induced spawning of
numerous species of freshwater fishes is well
established (Dodd, 1955; Fontenele, 1955; Clem-
ens and Sneed, 1962). A useful review of liter-
ature on the eflfects of hormones in fishes (Pick-
ford and Atz, 1957) has been updated with a
comprehensive, annotated bibliography (Atz and
Pickford, 1964), and a timely review of various
aspects of reproductive physiology of fishes is
also available (Hoar and Randall, 1969, 1970).

Hormone-induced spawning is an accepted
part of several commercial fish culture ventures
and will be used in many more when techniques
become reliably standardized for various spe-
cies. Brazilians pioneered the use of hormones
in spawning carp, while in Russia, where hydro-

electric dams block the spawning migrations of
sturgeons and salmonids, hormone-induced
spawning has been practiced for many years
(Atz and Pickford, 1959) . In India, carps spawn
naturally in flowing streams but must be in-
jected with conspecific pituitaries before they
will spawn in ponds (Chaudhuri, 1960; Das and
Khan, 1962). Catfish respond to similar treat-
ment (Sundararaj and Goswami, 1968). In the
United States, several freshwater and anadro-
mous species are spawned with hormones (Ball
and Bacon, 1954; Clemens and Sneed, 1962;
Stevens, 1966).

My investigation focused on the use of hor-
mones in inducing maturation and spawning of
the gulf croaker, Bairdiella icistia (Jordan and
Gilbert) , both for the specific purpose of obtain-
ing eggs for physiological studies of salinity tol-
erance and for the more general purpose of
studying factors which influence spawning in
marine fishes. Once success had been achieved
in spawning fish under controlled laboratory
conditions, the influences of biological and phys-
ical factors on the spawning process were ex-
amined in detail.

THE SALTON SEA FISHERY

The Salton Sea is a large, saline, inland lake
in the lower desert of southern California. The
present body of water was formed when the
flood waters of the Colorado and Gila Rivers
broke through irrigation dikes in 1905 and
poured into the then dry Salton Sink. The ir-
rigation canals were repaired and the water
again brought under control in 1907. Subse-
quently, the Salton Sea was declared an agri-
cultural sump for the deposition of large quanti-
ties of irrigation waste water. This water
leached large quantities of salt out of the sur-
rounding agricultural land and carried it into
the sea. Consequently, over the years the sa-
linity gradually increased. Short-term fluctu-
ations occurred — reflecting changes in inflow,
annual rainfall, surface area, temperature, and
evaporation. The salinity of the Salton Sea in
1970 is about 37 %o.

During the period 1950-56, when the salinity
of the Salton Sea approximated that of the ocean,

158

HAYDOCK: GONAD MATURATION OF GULF CROAKER

the California Department of Fish and Game
transplanted a variety of fishes from the Gulf
of California with the intent of establishing
a productive sport fishery. The present fishery
stems from the descendants of a total original
introduction of 57 gulf croaker, 67 sargo, Anis-
otremus davidsoni, and 100 to 200 orangemouth
corvina, Cynoscion xanthulus, transplanted to
Salton Sea in 1951-52 (Walker, 1961; Whitney,
1967). The fishes thrived and developed large
populations in the simple, man-made ecosystem,
but increasing salinity now threatens the con-
tinuing existence of the famous fishery.

The Salton Sea Investigations was a joint Fed-
eral-State pi-oject whose overall goal was to pre-
dict a target salinity at which a water quality
control project could be aimed that would not
be detrimental to the present highly esteemed
fishery. Engineering studies had suggested a
method by which the salinity of the Salton Sea
could be controlled, but the maximum permis-
sible salinity levels still had to be established
on the basis of biological information. Other
sciaenid species live in the Gulf of Mexico in a
wide range of salinities up to 75 ^r, but it is
considered unlikely that spawning occurs in ex-
tremely high salinities or that the larvae could
tolerate such osmotic stress (Gunter, 1967;
Hedgpeth, 1959).

To attain our goal in the short time available,
we have developed all of the necessary tech-
niques for spawning Salton Sea fishes under
controlled laboratory conditions. These tech-
niques have proved successful for obtaining
viable spawn for the necessary salinity tolerance
studies of both croaker and sargo.' I had ori-
ginally assumed that the close relationship of
gulf croaker to corvina, both of the family
Sciaenidae, would make it possible to apply
croaker spawning techniques directly to the cor-
vina. However, the carnivorous nature of cor-
vina and the general difliculty of handling this
powerful fish in the laboratory demanded special
feeding and holding techniques and precluded

successful laboratory spawning. Hormone-in-
duced spawning has been achieved in our lab-
oratory with other mature marine fishes, includ-
ing Eucinostomus sp. (family Gerridae), Geny-
ovemus lineatus (Sciaenidae), and sargo (Hae-
mulidae). The techniques developed for in-
ducing spawning with hormones in gulf croakers
may thus have general applicability.

METHODS

CAPTURE, TRANSPORT, CARE, AND
HANDLING OF FISH

Two year classes of gulf croakers were cap-
tured with a 60-m beach seine in May and Oc-
tober 1969. The first sample consisted of ma-
ture fish, 1 year old, and the second of young-of-
the-year fish which were subsequently matured
under controlled photoperiod and temperature
conditions in the laboratory. The fish were
captured on sandy beaches north of the U.S.
Navy Base and north of the Salton Bay Marina,
both on the west side of the Salton Sea. A beach
seine is the most dependable method for captur-
ing large numbers of these fish in good condition,
e.Kcept in midsummer and late winter, when
fish are unavailable near shore.

The fish were transported to La Jolla, Calif.,
in a 500-liter tank equipped with aeration and
filtration devices. In transport, and for several
subsequent days in the laboratory, the fish were
treated with Furacin antibiotic' at an initial con-
centration of 250 mg/3.8 liter. Several early
failures showed that careful handling, high
standards of water quality, and, especially, anti-
biotic treatment are all essential to high sur-
vival rates of Salton Sea fishes after capture.

In the laboratory, the fish were held in 2,000-
liter rectangular tanks (2 m x 1 m X 1 m deep)
supplied continuously from the seawater supply
of the Fishery-Oceanography Center in La Jolla.
A general description of this extraordinary fa-
cility is available (Lasker and Vlymen, 1969).
A water temperature of 22 ± 1° C was main-

' Reuben Lasker and Richard R. Tenaza. 1968.
Salton Sea fish larvae investigation progress report:
techniques and preliminary experiments on osmotic stress
(spring-summer 1968) . Inland Fisheries .Administrative
Report No. 68-7, Oct. 1968, (Unpublished).

' Sharpe and Vejar, Los Angeles, Calif. Use of trade
names is merely to facilitate descriptions; no endorse-
ment is implied.

159

FISHERY BULLETIN; VOL. 69, NO. I

tained except for special studies ox- for short
maintenance periods. An artificial photoperiod
of 16 hr light: 8 hr dark (16L:8D) was main-
tained by time clocks (Tork, Model 7100') in a
light-tight room with 400 w, white mercury
lamps (Sylvania, H33-1-GL/C'), suspended 1.5
m above the water surface at the center of each
tank. Deviations from this water temperature
and light schedule are reported where appro-
priate.

Young fish, less than 13 cm in length, were
fed 0.238 cm Oregon Moist Pellets' from Allen
automatic trout feeders' activated with time
clocks (Paragon Model 4001-0"). As fish grew
larger their consumption of pellets diminished
until they were fed exclusively on squid which
was ground semifrozen into pieces ranging
from 0..5 to 2.5 cm^. All fish were fed squid
ad libitum twice daily during the week and once
a day on weekends. I consider adequate feeding
to be an important factor in gonad maturation,
but it was not a variable in this study. In the
laboratory, young fish doubled their weight in
2 months and, later, added about 10 g each
month, reaching 80 to 100 g by the end of the
first year. Salton Sea fish weigh 40 to 50 g
at the end of 1 year; the largest gulf croaker
caught during this study weighed 420 g.

Initially, and for later studies of the effects
of a series of hormone injections, fish were
never disturbed without first draining the tanks
to within 10 to 15 cm of the bottom and then
adding anaesthetic until the fish could be touched
without causing a sudden reaction. Fish to be
injected were then removed and completely an-
aesthetized for 1 to 3 min in MS-222 (Tricaine
Methanesulfonate)" at 0.6 g/3.8 liters. Treated
fish were replaced in fresh seawater; if neces-
sary, fish were held with gloved hands and
moved rapidly back and forth at the surface to
aerate the gills and assist their recovery. There
is little danger of fish mortality when the an-
aesthetic is properly used, and no adverse effects

on fish reproduction were found. Later, exper-
ience enabled us to net unanaesthetized fish rap-
idly and place them directly into buckets with
MS-222 until they were unconscious. This was
done routinely when spawning techniques were
thoroughly known.

Fish were individually marked with subcuta-
neous injections of a 65 mg/ml stock solution of
Bismark Brown or Fast Turquoise PT.'° Hor-
mone, antibiotic and other injections wei'e car-
ried out with 0.5- to 1.0-cc disposable syringes
fitted with 25- to 26-gauge, 1.27- to 1.90-cm
('/2-%inch) needles. Needles 0.95 cm (% inch)
long proved useful for intraperitoneal (ip) in-
jection where internal damage was possible, but
these allowed too much fluid to escape when in-
tramuscular (im) injections were used. Inmost
cases the needle was carefully slipped into the
skin between scales, and carrier fluid (oil and sa-
line) was slowly injected into the deep muscles of
the back adjacent to the dorsal fin. Slow with-
drawal and pressure over the wound site helped
to retain most of the fluid. Sesame oil was used
in most cases as a carrier, but no essential dif-
ferences were noted between oil and Holtfreter's
saline injections.

LIST OF HORMONES AND
THEIR PREPARATION

1. Oxytocin (Pitocin, Pituitary grade I)." In-
jectable solution, 20 lU/ml, used as obtained
and stored at 4° C.

2. Deoxycorticosterone Acetate (DOCA, grade
II)." Injected as a slurry in sesame oil.'-

3. Human Chorionic Gonadotropin (HCG,
stock No. CG-2)." Anhydrous powder was
made to volume with Holtfreter's saline just
prior to injection.

4. Gonadotropin from Pregnant Mare's Serum
(PMS)." Powder dissolved in distilled
water and stored at —10° C.

5. Carp Pituitary (freeze-dried powder)."

' Pacific Wholesale Electric Company, San Diego,
Calif.

* R. V. Moore Company, La Conner, Wash.
' G-Z Company, Sacramento, Calif.
' J. F. Zwiener Company, San Diego, Calif.
' Crescent Research Chemicals, Scottsdale, Ariz.

'° Allied Chemical Company, San Francisco, Calif.

" Sigma Chemical Co., St. Louis, Mo.

" A. Sahadi Co., Moonachie, N.J.

" Stoller Fisheries, Spirit Lake, Iowa.

160

HAYDOCK: GONAD MATURATION OF GULF CROAKER

Powder was homogenized wt/vol in sesame
oil or Holtfreter's saline.

6. King Salmon, Oncorhynchus tshaivytscha,
Pituitary." Glands removed and placed in
acetone for extraction within 15 min of
spawning. Whole glands were homogenized
wt/vol in sesame oil or Holtfreter's saline.

Multiple intramuscular (im) or intraperi-
toneal (ip) injections were accompanied with
200 lU Potassium Penicillin G and 0.025 mg ac-
tive Streptomycin Sulfate. Fish that were
handled several times, with disposable plastic
gloves, were routinely treated with Furacin
water-mix antibiotic (Vet. grade), at an initial
concentration of 250 mg/3.8 liters.

PREPARATION OF SALMON PITUITARIES

Early in the project my attention was directed
to the possible usefulness of fish pituitaries for
inducing spawning (Pickford and Atz, 1957;
Clemens and Sneed, 1962; Atz and Pickford,
1964) . Carp pituitaries are commercially avail-
able, but there is no assurance that these are
removed from spawning fish, a time at which the
glands are assumed to have high titers of spawn-
ing hormones. Glands from Bairdiella, taken
during the spawning season, would be ideal, but
the bony nature of the brain case makes their
removal difficult and their small size makes the
effort relatively unrewarding. Spawning grun-
ion, Leuresthes tenuis, are seasonally abundant
locally but, again, collecting a large number of
glands would require great effort. Salmon pro-
vide a convenient source of fish pituitaries, since
they are available in large numbers at fixed lo-
cations (fish hatcheries) . Each gland is of con-
siderable size (about 13 mg dry weight), and
the bony brain case is reduced to a soft cartilage
by decalcification near the time of spawning.
Each fish is graded at the hatchery so that
spawning females are only sacrificed when at
the peak of running ripeness. Fish return to
spawn at different times at various hatcheries
which allows some flexibility in the timing of
collecting operations. All these advantages, plus

'* Nimbus Fish Hatchery, Rancho Cordova, Calif.

the fact that the glands proved useful in spawn-
ing croakers, justify a detailed discussion of the
method developed by Nimbus Hatchery person-
nel for removing the pituitary from king salmon.
I thank W. H. Jochimsen and D. R. Von Allmen
for originally demonstrating this technique to me.
A technique for removing pituitary glands
from salmon with a special tool exists (Tsuyuki,
Schmidt, and Smith, 1964), and similar equip-
ment was available at the Nimbus Hatchery.
However, hatchery personnel have developed a
simple and rapid technique which allows one
person, with a little practice, to directly remove
100 to 200 pituitary glands during the course
of a morning's spawning activities at the hatch-
ery. The number of fish spawned limits the
number of glands obtained; several hundred fish
are spawned each week during November, the
peak season at Nimbus Hatchery. The largest
numbers of fish enter the hatchery ponds from
the river on overcast days or during winter rains.
Female and male pituitary glands were re-
moved from spawned fish within 15 min of death
(unfortunately, following death, a severing of
the head artery which bleeds the fish often
destroys the pituitary in the process) . The fish
to be used for pituitary extraction are held up-
right with the gill cover slipped over a sharp
stake clamped to a table. A large, sharp butcher
knife is used to slice through the cartilaginous
tissue of the brain case, parallel to the jaw and
just above the level of the eye (a metal glove,
as worn by fish-market personnel, would be use-
ful for this step, which is carried out while the
neuromuscular system of the large fish is still
active). A rubber coat and rubber boots are
also necessary accouterments at this gross stage
of dissection. The cut exposes the brain, or, if
at the appropriate depth, the pituitary stalk
(sometimes the gland itself) is severed and the
gland can be removed from its cavity with a
pair of forceps or a narrow scoop. Some cuts,
at odd angles, sever nerve cords as well as the
pituitary stalk and expose three cavities. Once
learned, the location, consistency, and color of
the pituitary differentiate it from nervous or
other fatty tissues with which it might be con-
fused. At first, shallow cuts can be made to

161

FISHERY BULLETIN: VOL. 69, NO. 1

expose the brain; the gland's cavity and stalk
are readily seen when the brain is lifted from
its cavity and the entire gland can be removed
with forceps. A direct approach is more appro-
priate to the speed with which spawning ac-
tivities proceed and 1 day of practice is suffi-
cient to enable one person to remove glands as
fast as fish are available without undue loss of
damaged or partial pituitaries.

The glands are placed directly in chilled ace-
tone until spawning and gland-taking activities
are finished. The acetone is decanted and re-
placed 2 or 3 times over a period of 3 days until
all loose material is washed away. The final
wash of acetone is decanted, and the glands are
blotted gently on filter paper, placed in tightly
stoppered vials, and kept at — 10° C in a jar
of desiccant. Glands stored 1 or 2 years by
this method showed no detectable loss of activity.

It was found that pituitaries were easier to
homogenize if they were not completely dried.
Just prior to preparing a stock solution, the
glands were removed from vials, air-dried for a
few minutes, and weighed. They were then
immediately placed in glass tissue grinders and
homogenized in sesame oil or saline. The re-
sulting brei was finely divided and was used
unfiltered without clogging 25- and 26-gauge
needles. Stock solutions (1-10 mg/ml) were
stored in rubber-capped serum bottles (5 ml) at
— 10° C. All injections were 1.0 to 0.5 ml im
and up to 1 ml ip. I used oil rather than saline
in most cases on the assumption that oil may
slow the rate of absorption and more evenly dis-
tribute the hormone.

EVALUATING THE EFFECTS OF
HORMONE TREATMENT

Three basic criteria — gonad index, spawning,
and fertilization of eggs — were chosen to test
the effects of gonadotropin injections. Devel-
opment of fertilized eggs to hatching is also a
useful test of the absolute success of the hormone
treatment used to obtain spawn, but hatching
success is also very sensitive to other factors,
e.g., salinity, temperature, dissolved oxygen, and
bacterial contamination.

A commonly used measure of the effects of

hormone treatment is the gonosomatic index
(GSI) which expresses wet gonad weight as a
percent of total wet body weight. The GSI is a
reasonable measure of the state of reproductive
maturity of a fish. Its measurement, of course,
requires that the fish be sacrificed. Histological
examination of gonads or measuring egg di-
ameters to assess the stage of maturation are
more elaborate approaches which were not used
after it was found that GSI accurately predicted
spawning readiness of the fish. Mclnerney and
Evans (1970) have shown a direct relationship
between GSI and the histological index in fe-
male threespine stickleback. Among more re-
cent approaches to this problem is Stevens'
(1966) development of a technique for removing
eggs from striped bass by means of a catheter.
He was able to determine the stage of the eggs
and predict the time of optimal ripeness with
a fair degree of accuracy.

Samples of 4 or 5 fish were used to assess the
effects of hormone treatment. Controls of un-
injected or sham-injected groups of fish were
maintained where these were appropriate to
understanding the eflfects of hormone treatments
on GSI. The GSI of laboratory-held fish var-
ied, understandably, through time, and the ef-
fects which this had on the results obtained are
discussed where appropriate. The dates of most
experiments are given to help explain this var-
iation.

Two fundamental processes in spawning, hy-
dration and ovulation, were evaluated separately
with respect to various hormone treatments.
Hydration was measured as an increase in total
body weight over a period of 1 to 2 days after
injection, a process distinct from gonad growth
which occurs over longer time periods. This
rapid weight gain is due mostly to water uptake
by the fi.=h and is reflected in much higher GSI
values, as most of the water appears to go into
the gonad. Externally, a hydrated fish is grossly
bloated, and, in some cases, the fish are listless
and remain motionless on the bottom of the
tank. Ovulation was assessed by attempting to
strip eggs from fish at various times after in-
jection. Eggs may be forced from nearly ripe
fish, but these eggs invariably are surrounded

162

HAVDOCK: GONAD MATURATION OF GULF CROAKER

by a single layer of vascularized ovarian tissue.
Overripe eggs have no covering but are spotted
with areas of coagulated yolk. Usually, eggs
taken within 1 to 2 hr of ovulation are perfectly
round, 0.7 to 0.8 mm in diameter, and have the
single oil drop characteristic of this species.
These eggs float in normal Salton Sea water
(37 %, ) and are perfectly transparent and viable.
Fertilization of viable eggs and development
to hatching was followed for random samples
of eggs obtained from hormone treatments.
Eggs which did not cleave were considered un-
fertilized. In most cases, test fertilizations were
conducted in charcoal-filtered Salton Sea water,
which has an ionic composition different from
that of normal seawater (Carpelan, 1961).
Fertilization and hatching served as final criteria
of the usefulness of various preparations for
spawning.

EXPERIMENTAL RESULTS

The reproductive process in fishes can be ex-
perimentally divided into four phases: (1) go-
nad maturation — measured as a slow increase in
GSI over several weeks; (2) gonad hydration
— the final preparation of reproductive products
for spawning; (3) the actual spawning act — re-
leasing eggs and sperm; and (4) fertilization
and development of the eggs. These phases
are interdependent and proceed in a timed se-
quence as part of a cycle keyed to external and
internal cues which are integrated by the fish.
Thus, spawning is the culmination of a whole
series of events, each of which has particular
physical and biological requirements for success-
ful completion.

Although each process in the spawning cycle
can be separately evaluated with appropriate ex-
periments, it is important to keep in mind that
the results must be judged against the general
reproductive status of the organism. For ex-
ample, the effects of hormone injections differ
among croakers with different GSI's. For rea-
sons explained in the following section, most of
the experiments were focused on the repro-
ductive processes of female croakers.

GONAD MATURATION (MALES)

Effects of Photoperiod and Temperature

Male croakers became running ripe in the
laboratory under all combinations of experi-
mental conditions. Fish of 20 to 30 g, captured
in October, well beyond the normal breeding
season of the species in Salton Sea, became run-
ning ripe within 3 weeks after being placed in
tanks with various combinations of 14° C and
22° C water and 16L:8D or 8L: 16D photoperiod
schedules. Adult fish, captured at the height
of the breeding season in May and June, were
still ripe under all laboratory conditions in No-
vember and remained in this state until the end
of the experiments in July of the following year.
In the field, males become running ripe at least
1 month prior to the natural spawning season
and can thus serve as indicators of the ap-
proaching breeding season in Salton Sea. They
are not ripe prior to this time or after about 1
month following the spawning season, although
water temperatures and day lengths are similar
to those maintained in some laboratory situa-
tions in which the males did remain running
ripe. It may be that either the absence of the
normal Salton Sea cycle of light and temperature
conditions (in which the fish experience very
warm water — 25°-30° C — followed by a period
of winter dormancy), or the omission of the
normal spawning act in the laboratory, helped
to maintain the fish in running ripe condition.
The threshold at which environmental factors
induce spermiation may also be quite low, and in
the laboratory, food, light intensity, photoperiod,
and temperature acting in concert may have ex-
ceeded this level.

Effects of Hormones

Hormone injection of 1 mg salmon pituitary
caused a seminal thinning response similar to
that discussed by Clemens and Grant (1964).
In comparison, the milt taken from uninjected
fish was quite viscous and formed clots which
had to be mechanically broken up to disperse
the sperm. However, quantitative injections of
smaller doses of salmon pituitary caused no ap-
parent increase in the percent water of the testes
(Table 1). In males, the reaction to hormones

163

FISHERY BULLETIN: VOL. 69, NO. 1

Table 1. — Total weight, GSI (gonad weight/body weight
X 100) and percent water in testis of male Bairdiella
icistia injected with various dosages of salmon pituitary.

Treatment ,^|,^„ ^ jp, ^^^^^ ^ jp, j^^^,^ _^ sp,

Control;

0.01 ml/9 67.96 ± 13.38 7.03 ± 1.13 85,2 ± 1.08 5

sesame oil

Salmon

pitu.tory 59.97 ± 11.67 5.25 :t 1.61 86.0 ±1.20 5

0.005 mg/g

Salmon

pituitary 59.34 ± 6:99 5.53 ± 1.74 85.8 ± 1.14 5

0.01 mg/g

was not comparable to hydration in females and
was not further pursued. Possibly stronger
doses of pituitary would give a positive response.
The time scale and extent of the seminal hydra-
tion and thinning response might be useful in
assessing the effect of various hormones and
dosage relationships where female fish are at
a premium and males would otherwise be in ex-
cess. This bioassay technique has been used for
salmon pituitary gonadotropin (Yamazaki and
Donaldson, 1968a, 1968b).

were captured in October 1969, placed in 14° C
or 22° C water on a 16L or 8L photoperiod, and
given an abundance of food (Oregon moist chow
and chopped squid). These fish grew to ma-
turity in a little less than 4 months at 16L:8D
and 22° C (Table 2, group 1) . Similar fish kept
on 8L:16D at 14° C did not grow as rapidly as
warm-water fish and did not mature under these
conditions (compare groups 1 and 2, Table 2, 16-
11-70). The lack of maturity was not due to
the slower growth rate of the fish kept in cold
water, as Salton Sea fish of lower average weight
showed higher GSI values at their capture dur-
ing the spawning season (Table 2, group 3).
Short days, therefore, inhibited the maturation
process. These same fish (Table 2, group 2) did
mature rapidly, in 2 months, when the water
temperature was increased to 22° C along with
increased photoperiod. Young fish in their first
year do not have as high a percentage of gonad as
fish older than 1 year (Table 2, groups 3 and 4) .
Mature fish. — A sample of fish more than 1
year old, captured in November 1968, 6 months

GONAD MATURATION (FEMALES)

Seasonal Maturation Cycle in the Salton Sea

A series of croaker samples was taken from
the Salton Sea at monthly or more frequent
intervals during the year. GSI values were less
than 2 % from January to mid-March 1969,
prior to spawning, and less than 1 "Jr from mid-
June to December 1969, following spawning.
From mid-March to mid-April, the mean GSI
increased rapidly from 2 '}i to 10 ';> and reached
a high of 12 % in mid-May (Fig. 1); at this
time, individual females were caught with GSI's
of more than 17 %. Peak spawning in the
Salton Sea was observed in May and early June
in 1969. Le.ss frequent sampling and obser-
vations confirmed a similar pattern of events
in 1970. In the years 19.5.5, 1956, and 19.57,
Whitney (1961) found that the peak abundance
of croaker eggs and larvae in the Salton Sea fell
in middle and late May.

Laboratory Cycle and Effects of Photoperiod,
Water Temperature, and Food

Immature fish. — Young-of-the-year croakers

Salton Sea Bairdiella 1968-

A M J
MONTH

Figure 1. — Seasonal change in GSI of female Bairdiella
icistia captured in the Salton Sea. Hori7.ontal line in-
dicates the mean GSI value; vertical line indicates
range; on either side of the mean, open bar indicates
the standard deviation, and closed bar two standard er-
rors of the mean of each sample. The number of fish
sampled is given in parentheses. Horizontal dashed
line indicates 5 % GSI for comparison w-ith laboratory
fish (Fig. 2).

164

HAYDOCK: GONAD MATURATION OF GULF CROAKER

Table 2. — GSI values of female Bairdiella icistia cap-
tured in Salton Sea compared with captured fish matured
in the laboratory.

Group

Dots of
sample

Weight
(mean ± SD)

GSI
(mean ± SD)

1

23- X -<59i

10.47

±

3.56

096

It 0.28

9

S-Xll-69

34.30

^

5.15

0.93

±L 0.15

11

19-X:i-69

35.40

:+;

4.78

1.07

± 0.46

10

16-11 -70

60.14

^

11.84

5.46

± 3.32

5

2

23- X -691

10.47

±

3,56

0,96

± 0.28

9

5-X1I-69

31.90

^

8.04

0,92

± 0.14

10

19.x 11-69

33.10

zt

4.94

0-80

± 0.09

9

16-11 -70

39.40

±

7.16

1.28

± 0.22

5

4- IV -70

49.30

±

5,01

9.69

± 3,46

5

3

14- V.70»

32.38

±

8.32

5.90

± 3.84

25

4

I4-V-701

170.4

±

84.1

7.93

± 1.35

24

5

19-111-69

161.6

=t

22.8

10.2

± 1.94

23

Treatments

Group 1- Laboratory stock fish sampled irregularly. All fish kept on
16L:8D photoperiod at 22° C.

Group 2. Laboratory stock seporated from group 1 and maintained on
8L:160 photoperiod at 14° C until 16.11-70, when they were
switchea step-wise (15 min/day) to 16L:8D and 22° C.

Group 3: Young fish captured during their first breeding season in
Salton Sea.

Group A: Fish more than 1 year old, captured during the breeding
season in Salton Sea.

Group 5: Fish more than I year old, captured following the breeding
season in Salton Sea ond matured early under laboratory
conditions of 15L:9D and 14° to 16° C.

1 At capture.

before their normal breeding season, reached
maturity in the laboratory sometime prior to
being sampled in mid-March 1969 (Table 2,
group 5). These fish experienced 15L:9D and
ambient La Jolla seawater temperature (14°-
16° C) during 4 months in the laboratory. Cold
water may slow down the maturation process,
but it is evidently not as important as the stim-
ulation of long days.

A second sample of adult fish was captured in
mid-May (at the peak of the breeding season),
subjected to various experimental laboratory
conditions and sampled every 2 weeks to deter-
mine the status of their GSI (Fig. 2). Fish
maintained on long days (16L:8D) at 14° C and
22° C showed a slow decline in GSI from a high
of 12 9^ at capture to below 5 % by late-August
and September. The GSI values at 22° C were
more variable and, in general, showed a more
rapid decline than those at 14° C. Similar fish
given 10L:14D at high and low temperatures
showed a similar but much more rapid decline in
GSI, and their GSI also declined to a lower

overall level (1-2 '/c by mid-August) than that
of fish which never experienced short-day con-
ditions.

Both groups of short-day fish subsequently
showed a slow but steady increase in their GSI
in response to having the photoperiod increased
15 min/day from lOL to 16L. Although this
increase was not followed through a complete
cycle, it was evident that exposure to long days
for 2 to 3 months would have been required to
bring the fish up to the GSI level necessary for
spawning (about 5 % — see below).

It is likely that adult fish brought into the
laboratory just prior to the normal increase in
GSI observed in the Salton Sea would respond
rather quickly, I estimate within 1 month, if
they were given adequate light, temperature, and
food. It may also be possible to mature fish
rapidly after they have gone through their na-
tural GSI decrease (Fig. 1), but this was not
tested.

Effects of Hormones on Maturation of Fish
Maintained in the Laboratory

Groups of fish maintained on various light and
temperature regimes were subjected to hormonal
treatments to enhance gonad maturation. Adult
fish captured prior to the breeding season were
not available for these experiments, which were
conducted after the spawning season on fish
undergoing a decline in GSI, as in Fig. 2. None-
theless, the results obtained probably indicate
the extent to which maturation can be influenced
by hormone treatment. In croakers, the tech-
nique of hormone-induced maturation is of rel-
atively little practical importance, since fish can
be matured by appropriate manipulation of
photoperiod, temperature, and feeding sched-
ules. The results are, therefore, reported for
their possible application to other species in
which maturation proves more intractable.

Since the treatments were carried out on fish
being used for photoperiod and temperature ex-
periments, the results can only be evaluated in
relation to the GSI value of the population under
each set of conditions. In some cases, sham-in-
jected controls were used while in others unin-
jected fish sampled for the light- temperature

165

FISHERY BULLETIN: VOL. 69. NO. I

15n

LaboratoTLj Bairdiella 1969

5-

15r
10

-

r

a

c

_

IGL-.SD 22C

— -1

lOL*-^ 16L
r I i

22c

-

\

"

\

- J- X~~-i;— 2; — +
J 1 1 1 1

-

\

1 1 1

1 1

1

leUSD 14C

i^F

I I I I I I I I L_ I I

J J A

MONTH

0 N

lOL*^ 16L

14C

l\l-.-I'

-rn

I I I I

J L.

J J A

MONTH

0 N

Figure 2. — GSI of female Bairdiella icistia captured during the spawning season and maintained under the
following laboratory conditions: (a) 16L:8D, 22° C; (b) 16L:8D, 14° C; (c) 10L:14D, 22° C for 2 months;
then, photoperiod was increased 15 min/day to 16L:8D; (d) 10L.14D, 14° C for 2 months; then, photope-
riod was increased 15 min/day to 16L:8D. Mean GSI of all fish at capture (May 13, 1969) was 12.2 %. Dashed
value in (d) indicates GSI of five fish injected with 1 mg of salmon pituitary 1 day prior to last sampling per-
iod. Horizontal line at 5 % GSI indicates approximate minimum level necessary for successful hormone-induced
spawning.

studies served as controls when they were sched-
uled to be sampled at the same time as the in-
jected fish. In all cases the gonad index
responded positively to hormone treatment.
Differences seen in the tabular data (Tables 3,
4, and 5) were due to the number of injections,
strength and type of hormone injected, the water
temperature and the GSI value of the fish at
the beginning of the experiment.

In Tables 3, 4, and 5 the symbols (S, E, + , — )
record the initial (2 days after the first in-
jection) and the maximal (at some point during
the series of injections) response noted for each
group of fish. Two factors, water temperature
and GSI, were found to have an im])ortant bear-
ing on the results observed following hormone
injection. Fish kept in 14° C water showed the
most consistent and largest positive response
to long-term hormone injections which were giv-

Table 3. — GSI of Bairdiella icistia given five injections,
every other day for 9 days (17-26-IX-1969). Photope-
riod was 16L:8D and temperature 14° C during this e.\-
periment. The response of the fish to injection was as-
sessed every day and the maximal response is indicated
by S (= spawned viable eggs), E (= obtained non-
viable eggs), -f (= swollen papillae observed, no eggs
obtained), or — (^ no observed response). The sec-
ond column under each heading indicates the reproductive
status of the fish 2 days after the first injection. The
third column (in parentheses) indicates the maximum
reaction noted during the experiment.

Treatment

1 mg salmon
pituitary
extract

100 lU

HCG

5 mg

OOCA

Uninjected
control

GSI

12.4 -1- (E)

12.1 -

(E)

11.4

- (E)

4.1 (-)

11.6

+ (E)

1 0.0 —

(E)

6.1

- (E)

3.6 (-)

11.1

+ (E)

8.8 -

(-H

5.2

- (E)

3.2 (-)

10.9

- !-)

6.6 -

(+)

4.6

- (-H

2.7 (-)

6.0

- (-1-)

S.9 -

(-)

malo

2.7 (-)

X * SD

10.4

± 2.6

8.7 ±:

2.5

6.8

± 2.7

3.2 i: 0.6

166

HAYDOCK; GONAD MATLRATION OF GULF CROAKER

Table 4. — GSI of Bairdiella leistia given six injections over a 15-day period (18-VIII-69 — 2-IX-69). Each in-
jection consisted of 1 mg salmon pituitary extract. Fish in groups 1 and 2 experienced a 16L:8D photoperiod;
groups 3 and 4 experienced 10L:14D for 2 months (to 28-VII-69) followed by day length increases to 16L:8D (by
22-VIII-69). Groups 1 and 3 were maintained at 22° C, groups 2 and 4 at 14° C throughout the experiments.
Symbols (S, E, +, — ) are the same as in Table 3.

Group 1
(16U 22° C)

Gro
(16L,

up 2
14° C)

Group 3
(10L-16L, 22° C)

Group 4
(10L-16L, 14° C)

Injected

Control

Injected

Control

Injected

Control

Injected Control

6.5 E (E) 10.2 (-)
5.0 E (E) 3.2 (-)
4.2+ (E) 1.9 (-)
4.2 + (+) 1.3 (-)

3.6 - (-) 0.9 (-)

11.3 + (E)
9.4 + (E)
9.1 + (E)
9.1 + (E)
7.6 + (E)

10.2 (-)
6.0 (-)
5.5 (-)

5.2 (-)

2.3 (-)

5.6 - (E) 3.6 (-)
4.9- (E) 1.6 (-)
1.8 - (+) 1.4 (-)
1.6 - (-) 1.4 (-)
1.2 - (-) 1.3 (-)

7.3 - (E) 2.4 (-)
3.3 - (+) 2.0 (-)
1.9 - (-) 1.9 (-)
1.7 - (-) 1.6 (-)
1.2 - (-) 1.4 (-)

X ± SD

4.7 ±1.1 3.5 + 3.8

9.4 ± 1.3

5.8 ± 2.8

3.2 ± 2.0 1.9 ± 1.0

3.1 ± 2.5 1.9 ± 0.4

Table 5.— GSI of Bairdiella icistia given three injections,
one every other day for 7 days (16-IX— 23-IX-1969).
Photoperiod was 16L:8D and temperature 22° C during
this experiment. Symbols (S, E, +, — ) are the same
as in Table 3.

1 mg salmon

1 mg salmon

1 mg carp

0.1 mg salmon

Control

sesame oil

Holtfreter's

sesame oil

sesame oil

sesame oil

5.5 S (S)

5.0 S (S)

8.1 +(E)

6.0 -(E)

4.9 (-)

4.9 S (S)

5.0 S (S)

6.3 + (E)

3.3 - (+)

1.4 (-)

4.7 -(E)

4.6 -(E)

2.7 -(E)

3.0 - (+)

1.4 (-)

4.1 -(E)

3-6 -(E)

2.7-(+)

2.5 - (+)

1.1 (-)

1.8-(-)

I.4-(-)

2.5 - (+)

1 .5 - (-)

1.0 (-)

X± SD 4.2 ± 1 .4

3.9 ± 1 .5

4.5 ± 2.6

3.2 ±1.7

2.0 ± 1.6

en every other (3ay for 1 to 2 weeks (Table 3;
Table 4, groups 2 and 4). Fish in 22° C water
also showed a positive response (Table 4, groups
1 and 3; Table 5) ; however, this response is
less clear because warm-water fish occasionally
shed their eggs prior to sampling and this re-
duced the observed GSI.

In general, fish with GSI values below 5 %
did not respond to the first injection ( — ), re-
sponded with a weak swelling in the genital area
( + ) , or gave nonviable eggs ( E ) only after
several injections. This indicated that threshold
values of GSI and temperature exist below
which "growth" and above which hydration and
ovulation occur in response to hormone in-
jections. These values will be further discussed
in the section on ovulation. Here it will suffice
to point out that hormone treatment does give
rise to increases in gonad size which can perhaps
be considered the equivalent of gonad growth.

The tabular data indicate that salmon pitui-
tary caused the greatest increase in GSI of fish
kept in cold water. Salmon was followed by
HCG and then DOC A (Table 3) . Salmon pitui-

tary produced smaller increases in warm water
than in cold (Tables 3, 4, and 5), and the re-
sponse tended to vary in proportion to the dosage
used (Table 5). The relatively small response
at 22° C in Table 5 was probably due in part to
the lesser number of injections (3) in this batch
and in part to the fact that three of the fish
spawned relatively large quantities of eggs (see
qualitative responses in Table 5) , thus reducing
their GSI values, which were measured after
testing for the presence of viable eggs. How-
ever, the results of the longest series of injections
(Table 4) suggest that there is a general pat-
tern of greater increase in GSI in cold water,
except in the case of fish with a very low initial
GSI.

In warm water (Table 4, group 1; Table 5),
fish produced viable eggs (S) or nonviable eggs
(E) which could be forced out the day after the
first injection. Cold-water fish (Table 3; Table
4, groups 2 and 4) required several injections
to produce a response and never spawned viable
eggs on stripping.

In a further experiment, young-of-the-year
fish collected in October were injected shortly
thereafter with various concentrations of salmon
pituitary to assess usefulness of immatures as
a bioassay in testing dose-response relationships.
Each fish received five injections over a 10-day
period. At each dose level a large number of fish
(20) was injected, but, because of the difficulty
in identifying the sex of these immature fish, the
number of females actually injected was some-
what smaller. Also, the gonads were quite small,
and the overall GSI response was slight. This
made any meaningful analysis difficult. How-

167

FISHERY BULLETIN: VOL. 69, NO. 1

Table 6. — GSI of young female Bairdiella icistia after
five injections of various concentrations of salmon pitui-
tary extract over a 10-day experimental period (4-XI-
14-XI-69).

Dosa

Weight (s)
mean ± SD

GSI
mean ± SD

N

Control
sesome oil

26.07 ± 5.78

0 79 ± 0.08

13

0.1 mg salmon

23.90 ± 6.23

0.82 ± 0.22

10

0.5 mg salmon

28.40 ± 4.46

0 88 ± 0.18

13

1.0 mg salmon

26.97 ± 6.88

0.99 ±0.19

17

ever, the results (Table 6) do indicate a general
increase in GSI corresponding to dose. That
these fish were not too small to respond to treat-
ment is indicated by the high GSI observed in
similar sized fish captured in Salton Sea during
the breeding season (Table 2, group 3). It is
possible that the rather small response observed
was due in part to the fact that the fish were
handled frequently and did not feed readily dur-

ing the course of the experiment. This test
would probably be more successful if carried
out with 30- to 50-g fish kept under short-day
conditions at 14° C.

GONAD HYDRATION

Water Uptake Following Hormone Injections

Weight gain on various hormones. — Short
term changes in body weight occurred 1 to 2 days
following the injection of various hormones.
This weight change was recorded as a percent
of the initial total body weight (Table 7) and
was found to vary from slightly negative values
to positive values of over 13 Sr of the body
weight. Single injections were given, and fish
were weighed prior to, and 30 hr after, injection.
With few exceptions, the fish showed little or

Table 7. — Effects of hormones of GSI of Bairdiella icistia at 30 hr post-injection.

or ovulate.)

(1 = did, 0 = did not hydrate

Initial

Weight

GSI
(% final
weight)

Initial

Weight

GSI

Preparation, dose,
and dote

body

weight

(l)

change

(% initial

weight)

Hydrote

Ovulate

Preparation, dose,
ond date

body

weight

(s)

change
(% initial
weight)

(% final
weight)

Hydrate

Ovulate

Carp pituitary lOmg

Salmon pituitary 5 mg-Con.

lO-VI-70

51.07

-1-10.99

9.34

1

0

91.7

-1-10.09

25.94

1

1 (poor

70.46

-H5.42

19.80

1

0

62.3

-1-8.06

26.64

I

0 %%'

72.79

-f 11.72

25.50

1

0

PMS 100 lU

eggs)

57.22

-f 12.82

28.60

1

0

27-IV-70

86,8

—

21.00

0(?)

1

Carp pituitary 5 mg

1 2-V-70

88.7

-HIS

—

0(?)
I

1
1

16-VI-70

71 40
54.22

-

5.42
8.14

0
0

0
0

7-V-70
PMS 50 lU

173.6

-1-11.98

24.02

1

0

Salmon pituitary

9-VI-70

80 38

—3.06

2.90

0

0

0.1 mg, 5-VI-70

48.33

-0.93

2.38

0

0

54.89

-M.IO

14.60

I

I

55.90

-2.45

3.60

0

0

69.90

-f-7.77

18.50

1

I

49.40

-f2.39

10.97

(1)

0

62.18

-1-12.06

24.10

I

1

66.14

-1-0.06

12.41

0

0

HCG 100 lU

Salmon pituitary

28-IV-70

68.5

28.76

1

0

0.5 mg, 2-VI-70

65.18

-2.59

3.83

0

0

14-IV-70

87,5

29.37

1

0

62.77

-1.96

5.02

0

0

15-IV.70

84.5

30.29

1

0

74.83

-0.64

5.18

0

0

56.22

-1-8.75

21.76

1

1

HCG 50 lU

16-VI-70

78.51

-2.09

2.69

0

0

Salmon pituitary 1

mg

57.03

-1.95

3.65

0

0

28-IV-70

96.12

-1-9.40

15,90

1

1

67.91

— 1.29

3.68

0

0

15-V-70

65 50

-fl3.40

-_

1

1

80.41

-f7.15

19.80

1

1

18-V-70

79.90

-1-13.10

__

1

1

15-V-70

131.20

-(-600

1

1

Oxytocin 20 lU

ie-vi-70

59.12

-0.70

1.60

0

0

Salmon pituitary 2

mg

65.66

-1.02

3.37

0

0

lO-lV-70

93 30

__

24.47

I

t

72.11

-0.11

3.95

0

0

23-111-70

68.92

__

25.67

1

I

60.08

4-2.39

11.97

1

0

IO-lV-70

100.03

-

28.08

1

1

DOCA 5 mg

Salmon pituitary 5

mg

15- VI -70

54.78

-0.51

4.07

0

0

28-V-70

66.1

-f7.35

20.79

1

0 (few

53.70

-3.07

4.28

0

0

65.4

+6.)\

21.23

I

0 !Pew

55.33

-0.55

7.98

0

0

eggs)

73.10

-1.20

9.78

0

0

168

HAYDOCK : GONAD MATURATION OF GULF CROAKER

no response to 0.1 and 0.5 mg salmon pituitary,
5 mg carp pituitary, 50 lU HCG, 20 lU oxy-
tocin, and 5 mg DOCA. On the other hand, 1
to 5 mg salmon, 10 mg carp, and 100 lU HCG,
gave uniformly positive results, all fish showing
weight gains of 5 to 13 %. Variable results
were observed with 50 and 100 lU PMS. Al-
though most PMS fish which were weighed
showed some gain in weight, this was in general
less than that observed with carp, salmon, and
HCG. In fact, it was noted that two fish in-
jected with 100 lU PMS spawned freely without
ever appearing grossly bloated, a characteristic
of all fish which were spawned with other prep-
arations.

The time scale of weight gain. — A comparison
was made of the weight gained by fish given
one injection of 5 mg salmon, 10 mg carp, and
50 III PMS (Table 8). The time span of hy-
dration was arbitrarily divided into the weight
gained between 7 and 23 hr post-injection and
the total weight gained, including that added
between 23 and 30 hr. At 30 hr ovulated eggs,
if present, were stripped from the fish. Gen-
erally, all fish lost weight in the first 7 hr, pro-
bably because of handling and lack of feeding
during the experiment. The weight gains are
due mostly to water uptake and movement of
water into the gonad.

Table 8. — Effects of hormones on time-course of weight
gain.

fleets some fundamental difference in the way
these preparations afl!"ect the physiological mech-
anism causing hydration. The time-course of
hydration (Table 8) may be important in de-
termining the condition of eggs at ovulation
(Table 7). It should be noted that among the
three groups tested for the time-course of hy-
dration, viable eggs were obtained only from
the PMS-injected fish (Table 7) ; unfortunately,
there is no comparable data on the time-course
of weight gain in fish given 1 mg salmon, which
also produces viable eggs.

Factors Affecting Hydration

GSI. — It is apparent from Table 7 that the
gonad must be close to 5 % of the body weight
to respond to an otherwise adequate dose of
hormone. Although GSI could not be measured
prior to injection, almost all fish which failed to
respond had final GSI's below 5 %. Table 9
presents further confirmation of this. These
fish, injected with 1 mg salmon, came from a
stock which had shown a general decline in GSI,
because of being kept on a long photoperiod for
an extended time. Of four injected fish, three
hydrated and one of these subsequently spawned.
The fish that neither hydrated nor spawned had
a final GSI of just under 3 %. Only 1 of 11 un-
infected fish from this same stock showed a GSI
above 5 %, while 3 more were above 4 %.

Table 9. — GSI of Bairdiella icistia measured on 26-VI-70.

Initial

fish

weight

Percent weight gain

Preparation

A. Fish
(1

injected
= did, 0

with 1 mg salmon
= did not hydrate

pituitary, after
or ovulate).

GSI hod declined

ond
dose

7-23 hr
post-injection

7-30 hr
post-injection

Initial

Weight change

GSI

G

%

%

body
weight

(% initial

(% final

Hydrate Ovulate

Salmon pituitary 5 mg

66 1

4.58

7.35

weight)

weight)

91.7

7.72

10.09

53.10

-1-14.73

24.42

1 I

65,4

4.59

6.11

65.38

-1-7.40

10.55

1 0

62.3

4.41

8.46

60.14

-H4.21

6.94

) 0

Carp pituitary 10 mg

57.22

7.38

13.13

79.89

-2.21

2.77

0 0

51.07

4.17

10.44

B. Unin

iected fish

from same tank.

72.79

6.76

13.11

Total weight

GSI

PMS 50 lU

54.89

0.13

5.25

62.18

4.86

13.11

67.65

1.63

69.9

2.88

9.69

53.20
93.28

1.79
0.05

58.86

4.38

The results sho

w that t

he weight

increase

63.48

1.27

in the final 7 hr p

rior to sp

awning is

less than

61.90
78.60

4.57
1.70

50 % of the total

increase

with sail

non pitui-

74.70

2.08

tary, more than 50

^f with P

MS, and a

bout equal

53.24
69.29

2.59
7.86

when carp pituitai

-y is used

This ev

idently re-

59.46

4.80

169

FISHERY BULLETIN: VOL. 69, NO. I

Hormone dosage. — In general, there appears
to be a threshold response to dosage. Fish with
high GSI values and between 50- and 100-g body
weight hydrated after one injection of 10 mg
carp but not 5 mg (Table 7) . With salmon, 1 to
5 mg were adequate doses for 50- to 350-g fish
while 0.1 and 0.5 mg were inadequate except in
one case. In the case of HCG, 100 lU caused
hydration while 50 lU did not except in a single
case. Note, however, the low GSI value meas-
ured for three of the fish given 50 lU HCG.

It must be noted that the highest dosages used
were adequate for hydration but inhibited
spawning (see section following on ovulation).
This was true for 10 mg carp, 5 mg salmon and,
especially, 100 lU HCG where the fish continued
to gain weight and eventually died in the tank
without ovulating a single egg. These results
would suggest that it is important to determine
the lowest possible dosage which will consistently
bring about hydration.

Temperahire. — A temperature threshold un-
derlies the entire spawning process. Between
14° and 17° C the fish did not hydrate in re-
sponse to an otherwise adequate dosage of 1 mg
salmon pituitary. Two days later these same
fish spawned within 30 hr when given a second
1-mg-salmon injection 24 hr after being trans-
ferred to 22° C water.

OVULATION

Ovulation and Hydration as Separate Events

Some early results with 100-IU-PMS and 100-
lU-HCG injections led to speculation that the two
hormones were acting on different physiological
processes. PMS brought about ovulation with-
out gross hydration while HCG hydrated fish
to the point of death without ovulation (Table
7). This result was not confirmed with 50-IU
doses, but, in general, the impression gained was
that PMS produced high quality eggs with less
hydration than either HCG or salmon pituitary.

In sharp contrast to the PMS results, HCG
caused uniform hydration but, with one excep-
tion, failed to bring about ovulation. In a pre-
liminary test, it was found that oxytocin (20 lU)

or salmon (1 mg) caused some eggs to be ovu-
lated when the injection was given 24 hr after
the fish were injected with HCG. Oxytocin and
salmon pituitary had the same effect on carp-
injected fish which otherwise did not ovulate.

Ovulation without apparent hydration was
also achieved by using multiple, subthreshold
doses of 0.1 and 0.5 mg salmon pituitary, but the
time of ovulation could not be accurately pre-
dicted, and therefore the eggs obtained usually
were not viable. (The importance of obtaining
eggs just at ovulation is discussed in the section
on fertilization.)

In summary, carp pituitary, HCG, DOCA, and
oxytocin were uniformly inadequate for bring-
ing on ovulation except in the case of one fish
treated with HCG. Both carp- and HCG-in-
jected fish hydrated, some becoming grossly
distorted. On the other hand, salmon pituitary
and PMS regularly brought about ovulation.
Dosage appeared to be critical in the case of
salmon pituitary, as nonviable eggs resulted
from injections of 5 mg and no spawn could
be obtained with a single dose of 0.1 and 0.5 mg.
A 1-mg-salmon dosage seems to be optimal for
fish of 50- to 100-g total weight. Both 50- and
100-IU dosages of PMS gave good results with
remarkably clear eggs obtained from all fish.
In one case, a 50-IU dose of HCG was adequate
for spawning, but 100 lU appeared to be inhib-
itory to ovulation.

The Time Scale of Ovulation

The combined results from 28 fish which pro-
duced viable eggs following injection with a
single dose of salmon (1-3 mg) showed that the
average time elapsed from injection to spawning
was 30.4 hr, with a standard deviation of 3.3 hr
and a range of 24.5 to 35.5 hr (Fig. 3). This
30-hr latent period following injection gener-
ally held regardless of the type of hormone used,
its dosage, or the time of day the injection was
made. In the case of a few large fish (100 to
300 g) given 1 mg salmon, a second 1-mg in-
jection was given 24 hr later, but this did not
affect the time of spawning. Five fish given 5
mg salmon spawTied 28 hr after injection, but
their eggs were not viable. In one experiment.

170

HAYDCXTK: GONAD MATURATION OF GULF CROAKER

I

I I I I I

I I I I I I I I I I I

060O 1200

TIME OF INJECTION tPST)

Figure 3. — Time of injection (Pacific Standard Time)
and time of spawning (hours post-injection) in relation
to photoperiod. All injections were 1-3 mg salmon pitui-
tary extract and all fish produced viable eggs. Solid
black bar indicates dark period; dashed line indicates
mean time of spawning.

five fish were injected with 1 mg salmon at a
time corresponding with the beginning of the
laboratory dark cycle. All these fish spawned
24 hr later, indicating a possible enhancement
by the normal diurnal cycle of glandular activity.
Natural spawning in the Salton Sea is I'elated
to the normal diurnal light cycle, with most
spawning occurring in the early evening.

Factors Affecting Ovulation

It has already been shown that GSI level,
hormone dosage and type of hormone are criti-
cal interacting factors which must be considered
in any spawning eff'ort. Injection of high levels
of salmon (5 mg) may possibly assure a more
uniform hydration response (see GSI of Table
7), but the nonviable eggs which result speak
against using more than the minimal dose found
to give consistent results.

The eflfect of temperature on ovulation per se
was not studied. Hydration is effectively
blocked at temperatures lower than 17° C, but
this effect was reversed after 24 hr acclimation
at 22° C. In the cases in which this transfer
was carried out, a second injection was given
24 hr after transfer, and spawning took place
approximately 30 hr later.

As a matter of practical interest, it was found
that fish could be injected and spawned twice
(tried, successfully, with two fish) or three times

(one fish) with a period between spawnings of
3 to 4 weeks. This is in contrast to the much
longer time required for maturation after fish
had slowly resorbed their gonads in photoperiod
experiments (Fig. 2). Apparently the rapid
emptying of the gonad consequent upon hor-
monal injection quickly leads to a renewed cycle
of egg maturation.

The direct and indirect effects of various in-
jections on the gonad were assessed by biopsy
following spawning or the lack of spawning.
These qualitative observations are listed in Table
10; no attempt is made to interpret these results,
except to point out that fish injected with salmon
pituitary extract had gonads most closely re-
sembling those of naturally spawning fish.

Table 10. — Appearance of mature Bairdiella icistia
ovaries during natural spawning and 30 hr after various
hormone injections, and color reaction of fish to
injections.

1. Sollon Sea fish at spawning

Gonad color white, light yellow or red-orange. Consistency of
■nature gonad is granular with patches of tronsporent eggs which
are close to being ovulated or are lying free in the ovarian lumen.

2. Salmon pituitary extroct

Gonad color and consistency very close to naturally spawning fish.
Mast eggs ovulated and free in lumen. Fish blanch on injection.

3. Corp pituitary extract

Gonad color red-orange; few eggs ovulated. In fish given 5 mg
dose, blood clots oppeared to be blocking oviducts near vent.
Fish blanch on injection.

4. PMS

Gonad whitish, translucent; strikingly different from other prepa-
rations. Most eggs ovulated and free in lumen. Possibly, greater
degree of ovulotion with less hydration makes gonad appear lighter
in color. Fish do not blanch on injection.

5- HCG

Eggs either not ovulated or partially ovulated; those not ovulated
appear as white patches in the ovary. Many vacuoles and dis-
persed oil drops appear in eggs. Fish do not blanch on injection.

6. Oxytocin

Ovary was very bloody. Eggs white (not hydroted); different
sized eggs (mostly large) apparent in ovarian folds. Fish do not
blanch on injection.

7. DOCA

Fish showed no observable reaction.

FERTILIZATION

Relationship ot Egg Viability to the Time
of Ovulation

Shortly before ovulation, eggs could be
squeezed from females by applying strong pres-
sure to the abdomen, but eggs obtained in this
way still had an investiture of blood vessels and
ovarian tissue and could not be fertilized. An
analysis of viability in relation to the time after

171

FISHERY BULLETIN: VOL. 69, NO. 1

Table 11. — Fertilization and viability of Bairdiella icistia
eggs tested over a 4-hr period following first ovulation.
Fish was injected with 1 mg salmon pituitary extract
at 0930 l-V-70; first eggs expressed with some difficulty
at 1530 2-V-70.

Time of
fertilization

Development
to early
tailbud

Hatching

1530 hr (not quite
running ripe)

%
100

%
91

%
84

1630 hr (running
ripe)

100

91

83

1730 hr

100

78

72

1830 hr

90

62

44

1930 hr (eggs
spotty, opaque)

5

52

34

ovulation was made in the case of one fish which
remained ripe for 4 hr (Table 11). To check
for viability, eggs were test-fertilized at hourly
intervals following the first sign of ovulation,
taken as the earliest time when normal eggs
could easily be expressed from the fish by gentle
pressure applied to the abdomen. Fertilization
and early cleavage remained above 90 '^f up to
3 hr post-ovulation. By 4 hr the eggs looked
crinkled, opaque, and spotty, and less than 5 %
could be fertilized. A further measure of via-
bility was made by culturing 100 early cleaving
eggs from each batch until hatching. A decrease
in hatching success was noted in the eggs ob-
tained 2 hr after the initial ovulation, and hatch-
ing decreased still further in the 3- and 4-hr
post-ovulatory samples. It appears that the
maximum grace period for egg-taking is about
2 hr. In another experiment I studied eggs from
a larger sample of 10 fish determining fertil-
ization success as a function of time after ovu-
lation; the optimum time for taking eggs was
1 hr after the fish first showed signs of running
ripeness and gave viable eggs.

Although eggs rapidly deteriorated when kept
in the ovary following hormone-induced ovula-
tion, it was found that they retained their ability
to be fertilized up to several hours after they
were placed in a moist storage chamber. Eggs
placed in seawater remained fertile for several
minutes; in one case, a few cleaving eggs re-
sulted from fertilization carried out after the
eggs had been in seawater for 30 min.

Viability of Sperm

Although eggs kept in seawater remained
viable for several minutes, sperm were no longer
able to fertilize eggs 30 sec after the sperm mass
had been introduced into seawater. It is thus
readily apparent that croaker sperm and eggs
should be mixed immediately after the sperm
is obtained, in order to achieve maximum fertil-
ization. Microscopic examination showed that
sperm were immediately activated by addition
of water and retained motility for a period of
1-5 min. In some tests it was apparent that
water from the Salton Sea caused greater ac-
tivity for a longer time than water taken from
the ocean at La Jolla, Calif., but there was great
variability between males, and a proper tech-
nique of quantifying this relationship awaits
further studies.

Number of Eggs Obtained by Hormone
Treatment

The number of eggs obtained by hormone in-
jection varied between 700 and 1,000 per gram
of fish wet weight (Table 12). This provided
50,000 to 100,000 eggs for experiments from
each fish of 50 to 100 g used in this study.

Table 12. — Number of eggs obtained from hormone-induced spawning of Bairdiella icistia.

Wet weight

GSI

Ripe eggs

Actuol

count

(1 g eggs)

Eggs/g

fpsh
weight

Approximate

Total
fish

gonad

Body
weight

Gonad
weight

total eggs/
fish

G

C

%

%

82.0

17.7

21.6

16.0

74.0

4,700

841

69,000

86.6

17.6

20.3

15.5

78.1

■793

'69,000

91.7

26.0

25.9

197

76.1

5,590

1.101

101,000

342.7

62.1

__

_-

750

■699

■240,000

441.5

129.7

--

17.1

-

-

■878

■388,000

Indicates volues colculoted from meosured parameter and mean number of eggs per gram counted.

172

HAYDOCK: GONAD MATURATION OF GULF CROAKER

DISCUSSION

MATURATION

Many experiments have shown that gonad
maturation can result from hormone therapy
(for reviews see Pickford and Atz, 1957; Ahsan
and Hoar, 1963; Atz and Pickford, 1964; and
Hoar, 1969), but in most cases this is a long
and tedious approach and has proved of prac-
tical use only on a short-term basis for eluci-
dating mechanisms of hormone action. A re-
cently described catheter implant technique
(Frogner and Hendrickson, 1970) , allowing fre-
quent or continuous administration of hormones,
has been used with partial success to mature
mullet, Mugil cephalus, with a minimum of dam-
age from excessive handling (Shehadeh, person-
al communication ) . A mass of tangled catheters
is envisioned if this technique were applied to
commercial fish production, but the ease of this
method may have considerable merit for exper-
imental situations. Implanted pituitary glands
might also be used to enhance maturation, and
this could easily be tested in croakers.

In the present study, a slight increase in GSI,
possibly reflecting enhanced gonad "growth,"
followed 1 to 2 weeks of hormone injections giv-
en every other day to fish held in 22° C water.
Even greater "growth" enhancement was ob-
served in 14° C water, and these fish could have
been spawned using techniques which were fully
developed later in the study. However, for prac-
tical purposes, it proved simpler to mature
croakers in large groups using appropriate
schedules of long days, warm water, and abun-
dant feeding.

The fact that fish kept in cold water respond
to hormones by gonad enlargement without sub-
sequent hydration or ovulation indicates that
different temperature thresholds exist for these
various processes. It is possible that the rate
of absorption of hormone is considerably slowed
in cold water, as some fish do develop a slight
reaction following several days of injection at
14° C.

The general relationship of light and temper-
ature to gonad maturation is well known (see
Harrington, 1959; Henderson, 1963; Wiebe,
1968; and Hoar, 1969, for reviews) and requires

no lengthy discussion here. It is sufficient to
note that long-day photoperiod (16L:8D) and
high temperature water (22° C) induce gonad
maturation in croakers several months prior to
the normal breeding season observed in the
Salton Sea. Also, a combination of long days
and low temperature (14° C) will retard the
normal GSI decline when the fish have been cap-
tured at the peak of breeding. This technique
may prove useful for maintaining fish in a ma-
ture state for prolonged periods; such fish may
be subsequently spawned following transfer to
warm water (22° C) for a period of 1 day.

Studies on the relationship between maturity
and spawning indicate the existence of a GSI
threshold value of about 5 %, below which hor-
mone injections are ineffective. Also, fish
brought to maturity with photoperiod and tem-
perature control eventually resorb gonadal tis-
sues if they are not subsequently spawned. This
resorption process requires several weeks, and
the gonad will not grow in response to photo-
period and temperature during this time. Fish
which are spawned with hormones do not show
a refractory state and can be respawned within
a few weeks. The practical implication of these
findings is that the GSI of maturing fish should
be frequently checked so that spawning can be-
gin soon after the 5 'r GSI threshold is reached
and the fish should be spawned before they reach
the maximum GSI value and begin gonad re-
sorption. A useful approach would be to hold
stock supplies of fish on short days at low tem-
perature and mature separate groups as needed
for experiments.

Samples of croakers taken throughout the
year from Salton Sea showed that maturation
is quite rapid, the GSI increasing from 2 to 10 %
in a little over 1 month. It is probable that the
increased light, temperature, and food stimu-
lation available in the laboratory could bring
about even more rapid maturation, but the pro-
per fish (early spring) to test this were not ob-
tained during this study.

HYDRATION

Hormone-induced gonadal hydration is a rel-
atively rapid phenomenon which is completed

173

FISHERY BULLETIN: VOL. 69, NO, 1

in a little over 1 day following injection under
laboratory conditions. In croakers, the total
water uptake is reflected primarily in increased
gonad weight and may amount to more than a
10 % increase in total body weight. A detailed
study of the gonadal hydration of carp, Cyprinus
carpio, and goldfish, Carasshis aurahis, following
injections of carp pituitary extracts showed a
similar pattern of water movement into the go-
nad with respect to time (Clemens and Grant,
1964). These authors measured the increased
water content of the gonad following injection
and found that, in the case of males, the peak
of seminal fluidity was 24 hr after a single ip
injection. A similar response was observed
with im injection. Goldfish females injected
with 10 mg/g carp pituitary extract showed sim-
ilar responses, increasing gonad water by up
to 7.2 % over carrier-injected controls. Un-
fortunately, the changes they describe are in the
relative water content of gonads and various
other tissues including blood, and no mention
is made of any increase in total body weight re-
sulting from water taken up from the external
medium.

Hydration under laboratory conditions results
in a grossly distorted appearance in females,
the abdominal cavity becoming bloated several
hours prior to spawning. In the Salton Sea, fe-
males appear plump but never grossly enlarged
at spawning. It is possible that naturally
spawning females hydrate and ovulate fre-
quently but in small amounts over the course
of the breeding season and that the laboratory
fish show the maximum hydration and ovulatory
response because of unnatural overstimulation
with the injection of salmon pituitary. Use of
10 mg carp pituitary and 100 lU HCG caused
an equally strong hydration response, but gen-
erally this did not culminate in ovulation when
these preparations were used alone. A dose
threshold for response was indicated by the in-
ability of 1 to 5 mg of carp pituitary to cause
hydration. With 100 lU HCG, continued hy-
dration without ovulation evidently overstressed
the fish and led to their eventual death. On
the contrary, PMS gave somewhat variable re-
sults, but appeared to have less effect on gonad

hydration while, at the same time, proving to be
a potent ovulating agent. Subthreshold doses
of salmon pituitary do not appear to cause hy-
dration, but a sequence of injections given at
daily intervals will eventually lead to ovulation
of small quantities of eggs. This may reflect
the response of exceptionally ripe eggs which are
able to hydrate and ovulate.

Thresholds of GSI (above 5 %), water tem-
perature (between 17° and 22° C), and hormone
dose (e.g., 1 mg or more of salmon pituitary
for 50- to 100-g fish) exist, and if any one of
these factors is below its threshold, hydration
does not occur.

OVULATION

Ovulation in croakers is a rapid process,
taking 1 to 2 hr for completion when induced
with hormones in the laboratory. The period
between injection and spawning includes the
hydration phase and culminates in ovulation at
about 30 hr post-injection. Stevens (1966)
found a similar 30-hr latent period for fully
mature striped bass, Roccus saxatilis. Clemens
and Sneed (1962) found a shorter latent period
of 15 hr for goldfish. Fontenele (1955) gave
injections to several Brazilian fish species at 6-
hr intervals. He stated that spawning usually
occurred just prior to the 5th injection (i.e.,
close to 30 hr after the first injection), although
in most cases the fish were allowed to spawn
naturally in ponds and were not tested by strip-
ping. Indian carp are also allowed to spawn
naturally in ponds after injection. Chaudhuri
(1960) states that spawning may come 6 to 8
hr after the first injection of very mature fish;
if a second injection is necessary, the total
elapsed time may be 14 to 18 hr. It would ap-
pear that in most recorded cases (see above
and Pickford and Atz, 1957, Table 46) hormone
injection will bring about final maturation and
spawning within 1 to 2 days if the gonads are
fully mature. In only a few cases (e.g., Joseph
and Saksena, 1966) have longer series of in-
jections been successfully used to produce viable
eggs.

A constant time period for spawning latency
was found to hold for croakers used in this
study. When GSI, water temperature, and hor-

174

HAYDOCK: GONAD MATURATION OF GULF CROAKER

mone dosage all exceed certain threshold levels,
the fish spawned viable eggs an average of 30
hr after the first injection. Hormone dosages
above threshold and the type of preparation had
no apparent effect on this result, which exhibited
only small variability. Subthreshold doses of
salmon pituitary did delay ovulation, but this de-
lay could not be accurately predicted, and there-
fore the spawn obtained was never viable. Sub-
threshold doses might theoretically be useful if
females were to spawn naturally in captivity,
but croakers never exhibited complete spawning
behavior in tanks following hormonal injections.
Injection of oxytocin in hydrated females and
in males appeared to cause heightened pre-
spawning behavior, with males following and
touching the vent of females, but actual spawn-
ing was not observed. Hydrated females event-
ually expelled their eggs into the tanks if they
were not hand-stripped shortly after ovulation.
Actually, the relatively constant latency and the
fact that fish must be hand-stripped are highly
advantageous to scheduling laboratory oper-
ations.

At Salton Sea, eggs of gulf croakers sampled
from the plankton and staged at various times
during the day and night showed that there is
a diurnal pattern of spawning, most early cleav-
age stages appearing in the early evening (Whit-
ney, 1961). The same diurnal pattern was
found in a closely related species from the East
Coast, B. chrysura (Kuntz, 1914). When the
effect of this diurnal pattern on laboratory
spawning was tested by injecting fish at a time
corresponding to the beginning of the labora-
tory dark cycle, all five injected fish spawned just
at "dusk," 24 hr after injection rather than the
usual 30 hr. However, such enhancement was
not found in any subsequent spawning attempts
carried out at many diff"erent times of day and
night. Clemens and Sneed (1962) found no
change in latency in goldfish, groups of which
were injected at 2-hr intervals over a period of
12 hr. Evidently, the injection of hormones
usually overrides any effect of diurnal spawning
patterns.

Clemens and Sneed (1962) found that the
latent period decreased with increasing temper-

ature, doubling from 12 hr at 30° C to 25 hr
at 10° C. Croakers spawn above 20° C in the
Salton Sea, and eggs develop to hatching between
20° and 30° C in the laboratory (Robert C. May,
Scripps Institution of Oceanography, personal
communication). However, all laboratory
spawning was accomplished at 20° to 22° C, and
no tests were run to determine if higher tem-
peratures would decrease the latent period. At
temperatures below 17° C, the croaker does not
hydrate or ovulate in response to hormone in-
jection.

For 50- to 100-g croakers, with GSI levels
above 4 to 5 %, a single injection of 50 lU PMS,
50 lU HCG, or 1 mg salmon pituitary proved
adequate to induce spawning. A dosage of 100
lU PMS and 2-3 mg salmon also produced viable
eggs, but 5 mg salmon produced nonviable eggs
in the four fish tested. A single injection of 10
mg (not 5 mg) carp pituitary or 100 III HCG
was adequate for hydration but not for ovulation.

An injection of 20 lU oxytocin or 5 mg DOCA
apparently had little or no effect on hydration,
although DOCA may have caused some slight
change in the GSI.

Oxytocin may affect spawning directly. Liley
(1969) reviews evidence that the spawning re-
flex is controlled by behavioral stimulation of
the CNS which releases oxytocin. Oxytocin is
used up during the reproductive season of fishes,
e.g., Fjindulics and Oncorhynchus (Perks, 1969).

The possibility that a second hormone, acting
(in concert or independently) directly on ovula-
tion, was absent from HCG or in too low a con-
centration in carp pituitary was evaluated in a
preliminary way by injecting 10 mg carp or 100
lU HCG fish with 20 lU oxytocin at 30 hr or an
otherwise inadequate dose (0.1 mg) of salmon
24 hr after the initial injection. Evidence was
obtained for ovulation shortly after injection
(oxytocin) or at 30 hr (salmon), although the
eggs usually were not viable. These experiences
indicated that hydration alone was not sufficient
to initiate ovulation and that the latter may be
a separately controlled process.

The apparent contrast observed with respect
to the different abilities of HCG and PMS to
hydrate and ovulate fish may possibly be

175

FISHERY BULLETIN: VOL. 69, NO. I

interpreted as additional evidence tiiat a two-
hormone system exists for reproductive control
in fishes similar to the FSH-LH system of birds
and mammals (see Ahsan and Hoar, 1963; Hy-
der, 1970, for details). HCG is LH-like while
PMS is FSH-like; fish pituitary extracts show
strong LH and slight FSH activity in mammals,,
but there is a great deal of conflicting evidence
and interpretation (Sundararaj and Goswami,
1966; Hoar, 1969). Other evidence indicates
that PMS acts like a combination of FSH and
LH when tested in mammals (Ball, 1960), but
this effect can be modified by the dosage used.
Hoar (1969) pi-esently considers it likely that
teleost pituitaries contain only a single gona-
dotropin.

Sundararaj and Goswami (1966) demonstrate
how wide the range of conflicting results can be,
when they report that hypophysectomized cat-
fish, HeteropnenMes fossilis, spawned ripe eggs
after injection with appropriate concentrations
of LH, HCG, PMS, and DOCA, while FSH
brought about ripening but no spawning (LH
contamination was possible) . PMS did cause
ovulation in striped bass (Stevens, 1966) . HCG
has been used successfully in other fish spawn-
ing studies (e.g., Sneed and Clemens, 19.59;
Stevens, 1966). The fact that both PMS and
HCG can lead to successful spawning and, yet,
reflect basically antagonistic systems in mam-
mals should make these hormones prime targets
in future experiments.

It is quite evident that considerable work re-
mains to be done to untangle the connections be-
tween hydration and ovulation, which are cer-
tainly i-elated events, but may be controlled by
different hormones acting at different threshold
levels.

The puzzling fact that one out of four .50 lU
HCG fish hydrated and spawned while three out
of three 100 I U fish hydrated Ijut never spawned,
might be explained by postulating that a "criti-
cal dose" exists, with doses above or below this
level being unable to induce the complete se-
quence of spawning events. The three 50 lU
fish which did not hydrate would perhaps have
spawned if their GSI had been above 5 Sf . A
"critical dose" phenomenon might also be in-

volved in the observed difference in hydration
and the comjilete lack of spawning obtained with
5 mg and 10 mg carp pituitary, as both groups
showed GSI values above 5 % ; in this case the
"critical dose" might lie between 5 mg and 10
mg.

Carp is considered a universal donor by Cle-
mens and Sneed (1962) and was successfully
used to spawn several species of freshwater
fishes. Bioassay with goldfish showed 100 lU
HCG to be equivalent to 0.5 mg acetone-di'ied
carp pituitary (Sneed and Clemens, 1959), and
ovulation was obtained with 100-1600 lU HCG
and 0.5-3.0 mg carp. Most other workers also
report no inhibition of spawning from very
large doses, but they all point out the critical
nature of exceeding some lower threshold dose
to initiate ovulation. The strength of pituitary
extracts for spawning is assumed to be related
to the reproductive status of the donors, a datum
not given by the company selling the carp pitui-
taries used in the present experiments. Salmon
pituitaries, however, were removed only from
fish graded at the hatchery for optimal ripeness
and the glands were taken within 15 min of
death. Nonetheless, from the results of this
study 1 mg of salmon pituitary appears to be
5 to 10 times more potent than 1 mg carp and
about equal to 50 lU HCG or PMS, although
definite qualitative differences in response exist.
A truly valid comparison of the strength of var-
ious fish pituitary preparations can of course be
made only by standardized bioassay (for reviews
of methods see Clemens and Sneed, 1962; Das
and Kahn, 1962; and Yamazaki and Donaldson,
1968a and 1968b).

It is clear that the effects of hormones vary
with the GSI level of the experimental fish. Most
of these spawning experiments were carried out
over a 2-month period beginning in mid-Ajn-il
and ending in mid-.June, while the GSI was
gradually decreasing in the stock of fish used for
the experiments. Thus, it is difficult to directly
compare the effects of 50 lU and 100 lU HCG,
as they were tested almost 2 months apart and
the average GSI values of the experimental fish
may have been somewhat different. The effect
of the population's declining GSI is clear in the

176

HAYDOCK: GONAD MATURATION OK OLLF CROAKER

case of a standard 1 mg dose of salmon pitui-
tary, which caused hydration, but produced eggs
from only one fish in the last test (late June
1970) carried out with the same stock of fish
which had been spawned regularly with the same
dose over the prior 2 months.

FERTILIZATION

Several early attempts to fertilize gulf croaker
eggs all ended in failure. These eggs were ob-
tained from hormone-induced spawning, and
they appeared normal in all respects; however,
the sperm mass was dispersed in the water some
time prior to adding the eggs. Later studies
showed that no fertilization resulted when the
sperm and eggs were mixed more than 30 sec
after sperm had been placed in water, while eggs
retained their ability to be fei-tilized for several
minutes when kept in water and for several
hours when stored in moist chambers. The early
failures to fertilize eggs thus resulted from not
utilizing diluted sperm quickly enough. It is
well known that sperm may be stored for long
periods of time if it is maintained in concen-
trated form or is not activated by the diluent.
The rapid decrease in the viability of sperm in
water is probably important for maintaining the
genetic integrity of the spawners; its signifi-
cance for practical laboratory work is that
sperm should be added to the eggs and not vice
versa.

Sperm tended to be more active and to re-
main motile longer in water from the Salton Sea
than in ordinary seawater from La Jolla, Calif.
Moreover, developing eggs always floated in
Salton Sea water (salinity in 1970, about ;57 /i.
on the basis of total dissolved solids) , while they
sank in La Jolla seawater (33.5 ',,,). These ob-
servations may have important implications for
the salinity tolerance and adaptability of Salton
Sea fishes (transplanted originally from the Gulf
of California), matters of crucial interest in the
initiation of this study of fish reproductive physi-
ology.

Several batches of eggs obtained from hor-
mone-induced spawning were allowed to develop
to hatching, and a few of the resulting larvae
were reared to metamorphosis in the laboratory

on a diet of rotifiers, Bianchionus plicatilis,io\-
lowed by brine shrimp, Artemia sali)ia, nauplii.
Thus the entire life history of the gulf croaker
can probably be completed under controlled lab-
oratory conditions. This opens up the jjossibility
of using this species for many other biological
studies where large numbers (50,000-100,000)
of pelagic eggs are desired from a marine spe-
cies of known genetic history. Some of these
studies are now in progress (Robert C. May,
Scripps Institution of Oceanography, personal
communication) . It is hoped that future studies
will include comparative work on this species,
especially with respect to the possible adapta-
tions of Salton Sea croakers since their sepa-
ration from the Gulf of California population.

SUMMARY

1. Adult and immature gulf croakers captured
by beach seining in the Salton Sea were trans-
ported to the Fishery-Oceanography Center lab-
oratory in La Jolla, Calif., and used in labora-
tory studies on gonad maturation and hormone-
induced spawning.

2. A bacterial disease which invariably devel-
oped on recently captured or frequently handled
fish was successfully treated with Fui'acin anti-
liiotic.

3. Long photoperiods (16 hr of light ijer 24
hr) and warm water (22° C) , along with optimal
feeding, accelerated the gonadal maturation of
females captured prior to their natural cycle of
gonadal maturation. These fish were ready to
spawn in the laboratory 1 to 3 months prior to
the spawning season observed in the Salton Sea.
Male fish became ripe under all combinations of
laboratory conditions and remained ripe
throughout the study.

4. Concomitant field studies confirmed earlier
work showing that female croakers ripened in
April, while day length was increasing, and
spawned when the water temperature reached
about 20° C; peak spawning occurred in May
of 1969 and 1970.

5. Mature fish, captured during the spawning
season at the Salton Sea, quickly resorbed their
gonads when held under short photoperiods (10
hr of light) in the laboratory, but similar fish

177

FISHERY BULLETIN: VOL. 69. NO. 1

maintained on long photoperiods (16 hr of light)
remained in spawning condition for 2 months
(at 22° C) or 3 months (at 14° C) beyond the
normal season.

6. At 14° C, injection of mature fish with
salmon pituitary, carp pituitary, chorionic go-
nadotropin from human pregnancy urine
(HCG), and deoxycorticosterone acetate (DO-
CA) caused increases in gonad size over sham-
injected or uninjected fish.

7. A single injection of 1 mg (acetone dried)
salmon pituitary, 50 lU of gonadotropin from
pregnant mare serum (PMS) or 50 lU of HCG
induced spawning in mature croakers (50-100 g)
with gonad index values about 5 "^.'f . Fish with
gonad index values below about 5 ^r did not re-
spond to otherwise adequate hormone doses.
Hormone-spawned fish could be spawned a sec-
ond or third time at 1- to 2-month intervals.

8. Eggs could be stripped from the fish an
average of 30.4 hr following injection. This
latent period consisted of a slow hydration phase
of water uptake followed by a rapid ovulation
phase which released eggs from the follicles in-
to the ovarian lumen.

9. The eggs remained viable only for 1 to 2 hr
following ovulation, unless they were stripped
from the fish and stored in moist chambers.
Each female produced 700 to 1000 eggs per gram
of wet body weight.

10. Sperm are viable for less than 30 sec after
dispersion in water.

11. Low dosages (0.1 mg) of salmon pituitary
were insufficient to cause hydration, while very
high dosages (5 mg) caused hydration but, evi-
dently, inhibited ovulation. High dosages (100
lU) of HCG caused fish to overhydrate and
eventually die without having ovulated.

12. Carp pituitary caused hydration but was
inadequate for ovulation. Deoxycorticosterone
acetate and oxytocin, given alone, had little or
no effect on the fish.

13. Fish did not respond to single hormone in-
jections if the water temperature was at or be-
low 17° C. One day of acclimation to a higher
temperature was sufficient to prepare fish from
cold water for spawning.

14. A few larvae hatched from eggs obtained

by hormone-induced spawning were reared
through metamorphosis; thus, the entire life
cycle of the gulf croaker can be completed under
laboratory conditions.

ACKNOWLEDGMENTS

Many people contributed to the total success
of this project, a cooperative effort made pos-
sible by Alex Calhoun, Chief of Inland Fisher-
ies, California Department of Fish and Game,
and Reuben Lasker, Program Director for Be-
havior and Physiologj', National Marine Fish-
eries Service Fishery-Oceanography Center, La
Jolla. Their interest made possible the funds
and facilities for this study, supported by Fed-
eral Aid to Fish Restoration Funds, Dingell-
Johnson Project California F-24-R, "Salton Sea
Investigations."

Robert F. Elwell, Senior Research Supervisor,
IFB, Sacramento, saved me from many admin-
istrative details and provided aid and encour-
agement at critical points in time. Fred Murin,
Salton City, was my able field assistant and com-
panion; and David Crear, now at the University
of Hawaii, was of inestimable value in our lab-
oratory ventures. Robert C. May. Scripps In-
stitution of Oceanography, La Jolla, contributed
much of his time to the successful completion
of the study.

Technical assistance was provided by Charles
F. Wright and Bert D. Kitchens, National Ma-
rine Fisheries Service Fishery-Oceanography
Center, La Jolla, who built the fish-holding facil-
ities and maintained the critical seawater sup-
ply. W. H. Jochimsen and D. R. Von Allmen,
Nimbus Fish Hatchery, Rancho Cordova, ar-
ranged for me to collect salmon pituitaries. Da-
vid Powell, Curator of Fishes, Sea World-San
Diego, taught me how to transport and care
for fish, and Vince Catania, California Deiiart-
ment of Fish and Game at Antioch, showed me
how to capture Salton Sea fishes. To each of
these persons I extend my gratitude for their
help, interest, and ideas.

I also thank the many other members of the
California Fish and Game Department and in-
terested Salton Sea sportsmen and merchants

178

HAYDOCK: GONAD MATURATION OF GULF CROAKER

that provided aid, comfort, and fellowship which
made the sometimes arduous field work a
pleasant and rewarding experience.

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1959. The use of pituitary hormones in fish culture.
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1964. The pituitary gland and its relation to the
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Ball, J. N.

1960. Reproduction in female bony fishes. Symp.
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1966. Modes of reproduction in fishes. Natural
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1961. Physical and chemical characteristics. In
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Chaudhuri, Hiralal.

1960. Experiments on induced spawning of Indian

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1964. Gonadal hydration of carp (Cyprimts cnrpio)

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1962. Bioassay and use of pituitary materials to
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Das, S. M., and H. A. Khan.

1962. The pituitary and pisciculture in India, with
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Dodd, J. M.

1955. The hormones of sex and reproduction and
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1970. Pompano mariculture in Florida. Amer.
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1955. Injecting pituitary (hypophyseal) hormones
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1970. A technique for coelomic administration of
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1967. Vertebrates in hypersaline waters. Contrib.
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Harrington, Robert Whiting, Jr.

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1963. Influence of light and temperature on the
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1970. Histological studies on the testes of pond
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FISHERY BULLETIN: VOL. 69. NO. 1

Joseph, Edwin B., and Vishnu P. Saksena.

1966. Determination of salinity tolerances in mum-
michog {Fii7idtdiis heterocUtua) larvae obtained
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1914. The embryology and larval development of
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1959. Trout and salmon culture (hatchery meth-
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1966. The culture of vertebrate embryos. Logos
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1969. The neurohypophysis. In W. S. Hoar and
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Pickford, Grace E., and James W. Atz.

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1964. The artificial propagation of marine fish.
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1959. The u.se of human chorionic gonadotrophin
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Stevens, Robert E.

1966. Hormone-induced spawning of striped bass
for re.servoir stocking. Progr. Fish-Cult. 28(1):
19-28.

Sundararaj, Bangalore I., and Shashi V. Goswaml

1966. Effects of mammalian hypophysial hormones,
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adrenal corticosteroids on ovulation and spawning
in hypophysectomized catfish, Hetcropneiistes fos-
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1968. Some aspects of induced spawning in the
hypophysectomized catfish, Heteropneustes fos-
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Tsu-iTiKi, H., p. J. Schmidt, and M. Smith.

1964. A convenient technique for obtaining pitui-
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21(3) : 635-637.
Walker, Bo^t) W.

1952. A guide to the grunion. Calif. Fish Game
38(3) : 409-420.
Walker, Boyd W. (editor).

1961. The ecology of the Salton Sea, California,
in relation to the sportfishery. Calif. Dep. Fish
Game, Fish Bull. 113, 204 p.
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1961. The bairdiella, BairdieUa icistius (Jordan
and Gilbert). In Boyd W. Walker (editor). The
ecology of the Salton Sea, California, in relation
to the sportfishery, p. 105-151. Calif. Dep. Fish
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1967. Introduction of commercially important spe-
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Wickler, W.

1966. Breeding aquarium fish; an introduction to
the biology of their reproduction [in German].
Transl. by D. W. Tucker. Van Nostrand, Prince-
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Wiebe, John P.

1968. The effects of temperature and daylength on
the reproductive physiology of the viviparous
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J. Zool. 46(6): 1207-1219.

Yamazaki, Fumio, and Edward M. Donaldson.

1968a. The .spermiation of goldfish (Cnrasshis
aaratus) as a bioassay for salmon {Oncorlnpichus
tahawytscha) gonadotropin. Gen. Comp. Endo-
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19fi8b. The effects of partially purified salmon
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180

HARMONIC FUNCTIONS FOR SEA-SURFACE TEMPERATURES AND

SALINITIES, KOKO HEAD, OAHU, 1956-69, AND SEA-SURFACE

TEMPERATURES, CHRISTMAS ISLAND, 1954-69

GUNTHER K. SECKEL' AND MARIAN Y. Y. YONG''

ABSTRACT

Harmonic functions have been fitted to time-series, sea-surface temperatures and salinities in order to
facilitate studies of the oceanographic climate near Hawaii and Christmas Island. The manner in
which Fourier analysis has been adapted to this application has been described. The standard errors
of estimate for Koko Head temperatures and salinities are less than 0.26° C and less than 0.05/^»,
respectively. The standard errors of estimate for Christmas Island temperatures are approximately
60 % above those for the Koko Head temperature. The expected values of the Koko Head tem-
perature and salinity functions have an uncertainty of ±0.1° C and ±0.015^fr, respectively, when
samples are obtained twice weekly. Error terms of the Christmas Island temperatures, with daily
sampling, are on average 0.07° C. Harmonic analysis spanning the entire sampling duration shows that
long-term variations in the Christmas Island temperature and Koko Head salinity are larger than the
seasonal variations. Seasonal variations in the Koko Head temperatures are dominant and longer
term variations small. The results of the harmonic analyses are presented in the appendixes: (1)
a listing of coefficients that define the Koko Head temperature and salinity functions for each year
and the Christmas Island temperature functions for each quarter of each year, (2) graphs of the fitted
curves together with the observed values for each year.

In this paper harmonic functions are presented
of sea-surface temperatures and salinities that
have been regularly measured near Koko Head,
Oahu (lat. 21°16' N., long. 157°41' W.) since
1956 and at Christmas Island (lat. 1°51' N.,
long. 157°23' W.) since 1954 (Fig. 1).

Sea-surface temperatures and salinities
change in response to, and therefore reflect,
sea-air interaction processes (heat exchange,
evaporation minus precipitation) and ocean-
ographic processes (advection, diff'usion). For
example, the mean sea-surface temperature for
a month at Koko Head provides a measure of
the mean heat content of the water near the
surface. Thus, if the mean temperature for
March is above that for February, then meteor-
ological and oceanographic processes must have
taken place to raise the mean heat content of

Figure 1. — Location of Koko Head, Oahu
and Christmas Island.

' National Marine Fisheries Service Environmental
and Fishery Forecasting Center, Monterey, Calif. 93940;
formerly National Marine Fisheries Service Hawaii Area
Fishery Research Center, Honolulu, Hawaii.

' National Marine Fisheries Service Hawaii Area
Fishery Research Center, Honolulu, Hawaii 96812.

165°

160' 155'

150" W {{

/

_ KOKO HEAD
OAHU t^

N.

c^.HAWAI 1

¥\

.

10*

10*

^CHRIST*

AS 1

165-

160' I55'

ISC

Manuscript received September 1970.

FISHERY BULLETIN. VOL. 69, NO. I, 1970.

181

FISHERY BULLETIN: VOL. 69. NO. I

the surface water in March above that in Feb-
ruary. This concept was used in studies of the
Hawaiian oceanographic climate (Seckel, 1962,
1969) and has been ajipHed to Hawaiian fishery
problems (Seckel and Waldron, I960; Seckel,
1963).

Rigorously, the theory of distribution of pro-
perties in the sea states that the change of sea-
surface temperature during a time interval, say
from the first day of one month to the first day
of the next month, is equal to the integral of
all meteorological and oceanographic processes
affecting the temperature during the time in-
terval: 1^

8 h — S II = f (all processes) J/.

e I, is the temperature at the beginning and di,
is the temperature at the end of the interval.
In application, the choice of e „ and 0/, presents
the following problems: The difference in the
observed temperatures at times a and b also
reflects the effect of short-term variability
("noise") that is not of interest in monitoring
the large-scale events. If one uses monthly
mean temperatures in the heat budget equation
that include observations made 15 days before
and after times a and b, then the change of
temperature incorporates the effect of processes
that lie outside the interval of interest. Al-
though mean values usually provide an adequate
measure of the temperature change during given
time intervals, the true change of temperature
can be obscured. One can overcome the problems
caused by the two unsatisfactory methods of
obtaining measures of the temjierature change
by finding suitable functions that filter out un-
desirable short-term variability without obscur-
ing the basic temperature and salinity trends.

Techniques that can be used in the smoothing
of time series data have been reviewed by Hol-
loway (1958) and usually involve moving aver-
ages of the data to which weighting factors have
been assigned.

Curve fitting provides another method of aji-
proach. A useful technique that has been used
in this report, is to obtain an analytic expression
for the temperature and salinity as a function
of time by Fourier analysis. The Fourier series
is efficiently, and therefore inexpensively, de-

rived by computer. Efficiency is furthered in
that graphs can be produced by automatic plot-
ter. The Fourier series provides a least-squares
fit of the observed values. It permits filtering
of undesired variability, facilitates statistical
evaluation of the data, and — within limits — pro-
vides insight into the properties of the distri-
bution.

These advantages will become apparent in the
following sections of this report. The results
of the analyses for each year of observation
are presented in the appendi.x in both tabular
and graphical form.

THE FOURIER METHOD

Fourier series are well known, widely applied,
and adequately described in texts of advanced
calculus. A good description can be found in
Sokolnikoff (1939) where the derivation of the
Fourier coefficients by least-squares method is
also presented.

The temperature or salinity is expressed as
a function of time, t, in the Fourier series:

.S„ (/) = h L (/l„cos/;a)' + B,is\nnu>i),

where w

2tt

1,2,3,

, and T is the fundamental

period. For example, if harmonic analysis is
to be performed on data collected for a dura-
tion of 1 year, T would be 365 days.

The Fourier series contains the coefficients
.4(1, A„, and B„ that are given by the Fourier
integrals
2

An =

and

«,, =

i=T

T ^0

F{!)cos{nui)ili. n

0.1,2,

F(thin{nui)dr. n = 1,2.3,

The coefficient Aq is the special case of A^i with
n — 0. In our application F(i) is the temper-
ature or salinity at the time t. Of course, the
functional relationship between temperature and
time or salinity and time is not known so that

182

SECKEL and YONG : HARMONIC FUNCTIONS

F{t) is the observed temperature or salinity
at the time t. Furthermore, F{t) is known only
at finite intervals of time so that the above
Fourier integrals must be obtained by numer-
ical integration. This integration, approxi-
mating the area under the curves F{t) cos (nU)
and F{t) sin (?i<.>f), is performed by summing
areas of rectangles with height G(t) cos (wuO
or G{t) sin (no>t), and with width Af, the
sampling interval.

The finite difference form of the Fourier in-
tegrals is

A„ =

and

X G{l)iCos{nut)Ati. n = 0,1,2, ...k.

B„ = — X G(l)iSm(nut)M,. n = 1,2,3, ...k.

• i = \

The number of samples in the interval (
io t = T \s m + 1,

0

and G(t)i = ViiFU,) 4- F(/,. i)], / = 1,2,3, ...m.

The time used to evaluate the geometric factor
is 1/2 (^' + i'-\)- Other schemes of obtaining
the best estimate of G(t) cos {riud) during the
interval Ai can be used but would not signifi-
cantly affect the results in our application (see
Kaplan, 1953: p. 168-172).

Library programs for the evaluation of Four-
ier coefficients by computer usually require that
the sampling interval, A?, be constant. Since
this condition is not necessarily met in our ap-
plication, a more flexible computer program was
written to evaluate the coefficients. In this
program the sampling interval may vary, and
the number of samples for the basic period of
analysis need not be the same in each application.

The Fourier coefficients evaluated in the
above manner enable us to describe anal.vtically
the temperature or salinity as a function of time.
If we wish to go further and gain insight into
the properties of the temperature or salinity
distribution, it is more useful to express the

Fourier series as a sum of cosines:

S„ (!) = — + X Cicos u(ni — a„),

2 " n = 1,2,3 k.

The transformation is accomplished by the use
of the trigonometric indentities

A„ = C„ cos wa„,
B,, = C, sin uia.i.

and

C„=±{Al+ B^y\
B„

ua„ — arctan -

A,

In the application described in this report
the fundamental period in the Fourier series is
the sampling duration or any portion of this
duration that may be arbitrarily chosen; the
amplitudes and phase angles do not necessarily
coincide with natural variations in temperature
or salinity; and the harmonic functions have no
predictive value.

In some cases, such as the Koko Head tem-
peratures with a well-defined annual cycle, the
fundamental period of the Fourier series de-
rived for each year approximates the annual
cycle. At Christmas Island, however, an annual
temperature cycle is not always clearly apparent.
Despite the fact that choice of the fundamental
period may be arbitrary and may not coincide
with a naturally occurring period, the spectrum
is resolved beyond the first few harmonics. For
example, if the fundamental period, n — 1, is 12
months then the period of the first harmonic,
n = 2, is 6 months. A naturally occurring 9
months cycle in the observations would in this
case not be resolved. As n increases, however,
resolution improves to 4, 3, 2.4, 2, etc., months.

The highest harmonic, or ?i-value, to which
harmonic analysis can be carried, is limited by
the number of observations. In the ideal case
and when samples are equally spaced in time,
there must be at least 2n observations, i.e., at
least two samples per cycle. In nature, where
we are dealing with noncyclical variations and
unequal spacing of samples a sinusoidal curve
cannot be resolved with only two samples, and

183

FISHKRY BLXLETIN: VOL. 69. NO. 1

a minimum of four or, better, six samples is
required to achieve good resolution. For ex-
ample, sea-surface temperatures are to be mon-
itored and the fundamental period of observa-
tions is to be 12 months. Resolution of a 1-
month cycle (?i = 12) , requires four samples per
month, or sampling once per week.

APPLICATION OF THE
FOURIER METHOD

In practice, the Fourier method described
above must be adapted to each specific applica-
tion. In addition to the minimum number of
samples necessary in order to attain a desired
resolution another restriction applies to vari-
ations in the sampling interval. Although the
computer program used to obtain the results of
this paper allows a varying sampling interval,
thus accepting a sequence with missing obser-
vations, the sampling interval can be allowed
to vary only within limits. For example, at
least four samples per month are necessary to
resolve a monthly cycle. This cycle will, how-
ever, not be resolved if the samples are taken
on four consecutive days, rather than being
evenly distributed throughout the month. It is
also possible to aid the hai-monic analysis in
rapid convergence to its best fit with the ob-
served values by adjusting the fundamental
period of analysis and by performing some pre-
liminary operations which are described below.

APPLICATION TO KOKO HEAD SEA-
SURFACE TEMPERATURES AND SALINITIES

The sampling station is located near Koko
Head at the exposed, eastern shore of Oahu so
that the sea-surface temperatures and salinities
measured there reflect open-ocean conditions.
The salinities appear to be affected by runofl'
only on rare occasions of heavy rainfall. Both
the tempei'atures and salinities are based on
bucket samples. The salinity is determined in
the Hawaii Area Fishery Research Center,
Honolulu.

Before 1961 samples were collected at weekly
intervals and subsequently twice weekly, usually
on Tuesday and Friday mornings. Occasionally

sampling has been missed. The computer pro-
gram must therefore accept data with an ir-
regular sampling interval.

The basic period for analysis has been chosen
to be 1 year. Harmonic analysis began with the
first sample and ended with the last sample of
the year. The sampling time, in days and
months, was converted to days of the year be-
ginning with the first of the year.

Owing to a longer term trend, the value of a
property at the beginning is not necessarily the
same as at the end of an annual cycle. In the
case of Koko Head salinities and Christmas
Island temperatures, it will be seen later that
an annual cycle is, in fact, not always apparent.
The noncyclic trend during the analysis period
can be obtained by linear approximation. Rapid
convergence to the best fitting function can then
be achieved by performing the harmonic anal-
ysis on the residuals of the observed values from
a linear fit.

In our application the first observed value,
F(to), and the last observed value, F(ti), for
the period were used to obtain the linear equation

S' = F(?o) + bi

FUi) - FUo)
where b = •

'/ - '0

The residuals, /?„, = F(t,n) — [F(to) + bt^},

m — 0.1,2, ... /, were used to obtain the Fourier

coefficients. The Koko Head temperatures and

salinities for each year are then expressed by

the function

k
S = K + bt + ^ C„ co<iu(ni — a„)

« = 1

where K = FUq) + — and w = — ■
2 T

The phase angles and coeflicients for each of
the years 19.56-69 of the sea-surface tempera-
tures are listed in appendix A Table 1, and of
the sea-surface salinity are listed in appendix
A Table 2.

The functions for each year together with the
observed values of the sea-surface temperature
and salinity have been drawn by automatic plot-
ter and are presented in appendix B.

184

SECKEL and YONG: HARMONIC FUNCTIONS

Quality control of the data was achieved by
two passes of the data through the computer.
First, the fitted graphs and plots of the observed
values as well as listed deviations of observed
values from the functions that resulted from the
first computer analysis were used to reject ob-
viously erroneous observations. The analysis
was then repeated without the rejected obser-
vations. The tabulations in appendix A and
figures in appendix B are the result of the second
pass through the computer. The rejected val-
ues are plotted and identified in the figures of
appendix B.

APPLICATION TO CHRISTMAS ISLAND
SEA-SURFACE TEMPERATURES

The Christmas Island sea-surface tempera-
tures are measured with a bucket thermometer
each morning (about 0900 local time) in the
channel leading from the open sea to the lagoon.
The diff'erences between open sea and lagoon
water temperatures have not been determined.
It is reasonable to assume that these tempera-
tures diff'er, and so introduce variability in the
observed temperature as tidal currents in the
channel change from day to day. The tide-
induced variability will, however, not be reflected
by a harmonic function where the resolution of
the highest harmonic is longer than 1 month.
Although the sampling site is not ideal, the ob-
served temperatures are believed to reflect, with
some bias induced by lagoon temperatures, the
changes of sea-water temperature from month
to month.

The procedure to obtain functions of the
Christmas Island temperatures was the same
as that used for the Koko Head temperatures
and salinities with the exception that a difl'erent
fundamental period was chosen. In contrast to
Koko Head where an annual cycle dominates the
sea-surface temperature, longer term changes
dominate the temperature at Christmas Island.
The basic temperature pattern at Christmas
Island also changes from year to year. For these
reasons a duration of 120 days was chosen as
fundamental period and Fourier analysis was
performed, as before, on the residuals of the
observed values from a linear fit.

For each year, the 120-day periods followed
in sequence with an overlap of 30 days. The
periods ran from the first day of the year to
day 120, from day 91 to day 210, from day 181
to day 300, and from day 271 to day 390, ex-
tending 25 days into the following year. In
this manner rapid convergence of the harmonic
function to the best fit was obtained.

With daily sampling and a fundamental per-
iod of 120 days, harmonic analysis could be car-
ried to the harmonic n — 30, but to do so would
introduce variability that we wish to smooth out.
Although a resolution of 1 month requires har-
monic analysis to w = 4 only, the analysis was
arbitrarily carried out to n ~ 7, resolving a
period of 16 days.

The resulting phase angles and coefficients for
1954-69 of the sea-surface temperature are listed
in appendix C. The functions for each year
together with the observed values have been
drawn by automatic plotter and are presented
in appendix D.

Quality control procedures were identical to
those for the Koko Head analyses. Relatively
large data gaps occurred at Christmas Island
in 1964, 1967, and 1968. Because some obser-
vations were available during each of the 120-
day periods in question, harmonic analysis pro-
duced coefficients that enabled drawing of curves
in appendix D although there were no data.
These curves were not erased since it is in-
structive to see what harmonic analysis will do
when faced with insufficient data.

DISCUSSION OF RESULTS

In this paper we are concerned with the deri-
vation and presentation of harmonic functions
of regularly observed sea-surface temperatures
and salinities at fixed stations rather than with
oceanographic interpretations. In the discussion
of the results we will, therefore, concern our-
selves primarily with the quality of fit of the
functions. We will also briefly discuss some
properties of the temperature and salinity dis-
tributions that are reflected by the functions and,
finally, show functions spanning the entire time
of observations.

185

FISHERY BULLETIN: VOL. 69, NO. 1

QUALITY OF FIT

A superficial inspection of the figures in ap-
pendixes B and D shows that the harmonic
functions follow the trend of the observed val-
ues very well. Closer inspection, however, re-
veals that there are cases where the fitted curves
depart from the observed trend. An example
occun-ed when the Koko Head salinity function
(appendix B) for 19.56 fluctuated about the ob-
served values from day 145 to day 180. The
fluctuations were caused by a data gap between
these days. A 15-day data gap is too large when
harmonic analysis resolves a period of 1 month.
Another example of deviations occurred in the
Christmas Island temperature function (appen-
dix D) for 1968 between day 240 and day 275.
Again, a 30-day data gap is too large when har-
monic analysis resolves a period of 19 days.

These examples illustrate that the sampling
interval in harmonic analysis may vary only
within limits and that the interval of permissible
sampling gaps depends upon the period resolved
by the analysis. In cases such as were cited,
where the fundamental period of analysis is
much longer than the sampling gap, it is pos-
sible to constrain the harmonic function by in-
serting "dummy" values based on linear inter-
polation of the last sample before, and the first
sample after, the data gap.

There are cases where the fitted curve fails
to follow the observed trend. When the devi-
ations from the fitted curves are relatively large,
there is a tendency to reject the observed values
during quality control procedures, blaming the
deviations on erroneous sampling. Temperature
deviations of this type occurred at Koko Head
during days 65 to 90 of 1967. First the ob-
served temperatures fell to 0.6° C belov/ the
fitted curve and then rose abruptly 1.3° to 0.6° C
above the fitted curve. Erroneous sampling is
ruled out since more than one sample was in-
volved in establishing the trend that was abrupt-
ly broken and, in addition, the salinity showed
similar variability during the same time interval.
First the observed salinity rose to 0.15',,, above
the expected value and then dropped abruptly
0.37';, to 0.16;,, below the expected value.
In the Hawaiian region the temperature in-

creases and the salinity decreases southward.
Thus, northward-southward displacements of
the water that would result in the observed
temperature and salinity changes were the pro-
bable cause for the large deviations rather than
sampling error.

In order to assess the quality of fit quantita-
tively, we will consider several aspects of the
standard error of estimate (root mean square
deviations of the observed from the expected
values). This statistical parameter is listed in
three tables for each function, with harmonic
analysis carried out for the fundamental peri-
od, the first harmonic, the second harmonic, etc.
in = 1,2,3, . . .). Table 1 applies to Koko Head
temperatures. Table 2 to Koko Head salinities,
and Table 3 to Christmas Island temperatures.

In each case the listed standard error of esti-
mate decreases or reaches a constant value with
increasing n. The fit of the function therefore
improves or levels off as the analysis is carried
out to higher harmonics. Exceptions to this
trend occurred in 1956, 1959, and 1961 when
the standard errors of estimate for the Koko
Head salinity functions (Table 2) increase as
the highest n values are reached. Prior to May
1961, only four or five samples per month were
obtained at Koko Head and therefore the high-
est n value permitted by the sampling frequency
had been reached. In addition, sampling gaps
occurred in 1956, as mentioned before, and in
1961 between days 220 and 241.

The fit of the Koko Head temperature func-
tions (Table 1) improves most rapidly during
the first few harmonics and with analysis car-
ried out to M = 6, the standard error of estimate
is near or below 0.3° C. With analysis carried
out to 7? = 13, the standard error of estimate
is below 0.2° C for all years excepting 1963 and
1965-68.

Greatest improvement of fit for the Koko
Head salinity functions (Table 2) does not al-
ways occur during the first few harmonics but
continues as analysis is carried beyond n = 6.
In 1960, for example, the standard error of esti-
mate with analysis to n = 1, w = 6, and n =
13, is 0.090',,, 0.075'^, and 0.038'rV, respectively.
The standard error of estimate at the « value
of best fit in Table 2 is below 0.04^. except

186

SECKEL and YONG: HARMONIC FUNCTIONS

Table 1. — Standard error of estimate {° C) for each annual temperature function at Koko Head, 1956-68, with
harmonic analysis carried out in sequence to n ^ 1, 2, 3, . . . and 13.

N-V4LUE5

VE/>K

1

2

3

'.

5

6

7

8

9

10

11

12

13

llib

0.21

0.19

0.17

0.16

3.16

0.1'.

0.1'.

0. I',

n.i3

0.13

0.12

0.12

0. U

1957

t). 36

0,29

0.2'.

0.2*

0.23

0.23

0.23

0.21

0.20

0.20

0.19

0.19

0.18

1S53

0.31

0. 29

0.2'.

0.24

0.22

0.22

0.22

0.22

0.22

0.20

0.20

0.18

0.17

1<)59

0.<il

0.38

0.29

0.29

0.26

0.2'.

0.2'.

0.2'.

0.22

0.21

0.2C

0.20

0. 19

1 ybO

0.3a

J. 27

0.2'.

0.2'.

0.23

0.23

a. 22

0.22

0.1 9

0.19

0.17

0.16

0.15

1<J6 1

0. <.?

0.37

0.35

0.33

0.32

0.31

C.31

0. 28

0. 2'.

0.23

0.2C

0.18

0. 17

116?

0.3?

0.25

0.25

0.25

0.23

0.21

0.21

0.21

0.20

0. 19

0 .19

0.19

0.17

l<)63

0.10

0.29

0.23

0.28

C.27

0.26

0.23

0.23

0.21

0.21

0.21

0.21

0.21

196-.

0.29

0.29

n.28

0.25

0.25

0 .2'i

0.23

0.21

0.20

0.18

0.17

0.17

0. 16

1965

C.'>9

O.-^S

0.38

0.36

0.3'i

0.30

0.28

0.27

0.27

0.27

0.27

0.26

0.26

1966

0.<.3

U.32

0.32

0. 30

0.30

0.27

0.27

0.27

0.26

0.26

0.26

0.26

0.26

196 7

0.4<i

0. M

0.3<.

0.31

0.32

0.27

0.26

0.25

0.25

0.2<.

0.2'.

0.2".

0.23

1968

0.37

0.32

0.24

0.28

0.28

0.27

0. 26

0.25

0.24

0.2'.

0.23

0.23

0,23

Table 2. — Standard error of estimate (f.^,,) for each annual salinity function at Koko Head, 1956-68, with har-
monic analysis carried out in sequence to )^ = 1, 2, 3, . . . and 13.

N-VALUES

YEAR

1

2

3

'.

5

&

7

8

9

10

11

12

13

1956

0.0". 5

0.034

0.032

0.031

0.031

1957

0 .068

0.057

0.054

0.054

0,045

i->5a

0.06 9

0.066

0.059

0,059

0.056

19 59

0.174

0.099

0.076

0,075

0.074

1960

0.090

0.083

0.081

0,078

0.077

1961

0.06 4

0.061

0.051

0,047

0.04 3

196 2

0.049

0.046

0. 046

0.044

0.043

1963

0.054

J. 0 53

0.052

0.046

0.045

196 4

0.086

0.078

0.069

0.063

0.061

1965

0.094

0.085

0.078

0.072

0.072

1966

0.044

0.043

0.042

0.037

0.037

1967

0.079

0.07S

0.07'.

0.072

0.068

196 3

0.060

0.057

0.051

0.046

0.042

0.030 0.030 0.029 0.028 0.025

0.041 0.039 0.037 0,034 0,034

0.053 0.053 0.052 0.049 0.048

0.073 0.069 0.064 0.060 0.058

0.075 0.069 0.063 0.356 0.053

0.038 0.037 0.036 0,033 0,030

0,041 0.037 0.037 0.036 0.035

0.045 0.043 0.041 0.037 0.037

0.059 0.052 0,052 0.051 0.044

0.071 0.066 0.064 0.058 0.056

0.034 0.U34 0.033 0.033 0.030

0,061 0.055 0.054 0.052 0,051

0.040 0.038 0.038 0.035 0.C35

0,025

0.028

0.030

0,032

0,030

0.030

0,041

0,036

0.036

0.054

0.053

0.054

0.050

0.042

0.038

0.027

0.028

0.02 8

0.034

0.034

0.034

0.034

0.033

0.033

0.044

0.04 3

0.0 38

0.054

0.048

0.045

0.030

0.029

0.028

0.050

0.046

0.044

0.033

0.033

0,033

187

FISHERY BULLETIN: VOL. 69, NO. 1

Table 3.— Standard error of estimate (° C) for each quarterly temperature function at Christmas Island, 1954-68,
with harmonic analysis carried out in sequence to n =r 1, 2, 3, . . . and 7.

N

-VALlJf S

YEAR

QUARTER

1

2

3

4

5

6

7

1954

0.-.4

0.41

0.41

0.41

0. 32

0.30

0,29

0.36

0.35

0.33

0.33

0.37

0.30

0.30

0.51

0.50

0.50

0.50

0. 47

0.45

0.44

J. 39

U.33

0.37

0.33

0. 30

0. 30

0.29

19 65

0.3 0

0.2R

0.27

0. 26

0.26

0.26

0.25

0.29

0.29

0.28

0.28

0.28

0.27

0.26

0.3<.

0.33

0. 33

0. 33

0.32

0.32

0.32

0.46

0.45

0.43

0.42

0. 40

0.39

0.39

1956

0.40

0. 38

0. 38

0.37

0.36

0.35

0.35

0.52

0.50

0.4 8

0.48

0.46

0.45

0.45

0.43

0. 47

0.45

0.44

0.43

0.41

0.41

0.38

0.39

0. 36

0.3s

0.36

0.32

0.32

1957

0.48

0. 46

0.45

0.44

0.43

0.43

0.43

0.61

0.54

0.54

0.54

0.53

0.51

0.51

0.44

0.44

0.43

0.43

0.40

0.39

0.38

0.40

0.39

0.35

0.34

0.33

0.30

0.28

1958

0.26

0.25

0.24

0.24

0.24

0.23

0.23

0.33

0.33

0.33

0.32

0.3 1

0.30

0.29

0.37

0.35

0.30

0. 29

0.28

0.28

0.28

0.32

0.31

0.28

0.27

0.26

0.25

0.25

19 59

0.41

0.34

0.30

0. 28

0.28

0.27

0.27

J. 40

0.38

0.36

0.35

0. 34

0.34

0.33

0.48

0.39

0. 36

0.34

0.37

0.32

0.32

0.43

0.39

0.36

0.32

0. 31

0 .29

0.29

1960

C.30

0.29

0.27

0.2b

0.26

0.25

0.25

0.35

0. 33

0.32

0.31

0.31

0.31

0.31

0.32

0. 31

0.30

0.27

0.26

0.26

0. 25

T.39

0.32

0.29

0.26

0 .2 6

0.24

0.23

1961

0. 36

0.34

0.34

0.32

0.31

0. 30

0.27

0.34

0.34

0.31

0.27

0.26

0.26

0.25

0. 36

0.29

0.29

0.28

0.27

0.25

0.25

0.2 6

0.24

0.22

0.22

0.20

C. 19

0. 18

1962

0 .39

0.34

0.30

0. 30

0.30

0.2 7

0.27

0.38

(1.33

0.31

0.30

0.29

0.27

3.25

0.26

0.74

0.71

0. 20

0.70

0.1 9

0.19

0. 30

0.26

0.25

0.24

0.24

3.24

0.24

196 3

0.36

0.36

0.34

T.34

0.32

0.32

0.28

0. 46

0.38

0.31

0.3 0

0 .78

0.27

0.71

0.36

0.29

0.29

0.77

0.26

0.25

0. 24

0.30

0.29

0.28

0.26

0. 26

O.Z'

n.25

1964

0. 32

0.32

0.31

0.30

0.79

0.29

0.28

0.37

0.31

0.30

0.29

0.28

0.28

0.27

0.34

0.31

0.79

0.29

0.28

0.27

0.26

0.28

0.27

0.26

0. 73

0.22

0.21

0.21

1965

0. 30

0.29

0.28

0.27

0. 26

0.75

0.25

0.36

0.32

n. 79

J. 29

0.29

0.29

0.29

0.53

0.52

0.45

0.42

0. 39

0.38

0.37

0.37

0.32

0.31

0.30

0.30

0.30

0.29

1966

0.42

0.39

0.35

0. 34

0.33

0.30

0.29

0.42

0.35

0.35

0.34

0.34

0.31

0.30

0.60

0.51

0.48

0. 46

0.43

0.42

0.40

0.68

0.68

0.53

0.52

0.51

0.51

0.47

1967

0.42

0.40

0.34

0.34

0.34

0.32

0.32

0.40

0.39

0.36

0.36

0.36

0 .36

0.35

0.39

0.38

0.37

0.36

0.34

0.33

0. 33

0.32

0.30

0.28

0.27

0. 27

0.27

0.26

1968

0.42

0.37

0.36

0.33

0.33

0.33

0.32

0.37

0.35

0.31

0. 11

0.31

0.30

0.30

0.29

0.29

0.29

0.30

O.'l

0, 78

0.28

0.28

0.27

0.26

0.24

0.23

0.21

0.21

188

SECKEL and VONG; HARMONIC FUNCTIONS

in 1959 and 1965 when it is 0.054/rr, and
0.045%f, respectively.

At Christmas Island (Table 3), the average
standard error of estimate at n = 4 (resolution
of 1 month) is near 0.33° C and therefore about
60 % higher than that for the Koko Head
temperatures. As previously mentioned, high
temperature variability is to be expected at the
Christmas Island sampling site.

A standard error of estimate based on all
samples used to obtain a function obscures the
month-to-month changes in variability that may
have occurred. At Koko Head the month-to-
month changes in temperature variability as re-
flected by the standard error of estimate for
each month ranges from 0.05° to 0.45° C, the
same values for the Koko Head salinities range
from 0.006%<. to 0.136%f , and those for Christmas
Island temperatures range from 0.17° to 0.66°
C. Assuming that sampling error remains
constant, the range of variability reflects changes
in oceanographic conditions.

The standard error of estimate computed from
the temperature and salinity observations of
each month also reflects sampling quality in
that low values indicate the residual variability
in the ocean plus sampling error. For the Koko
Head temperature, low values of the monthly
standard error of estimate are near 0.1° C
and for the Koko Head salinity they are near
0.02%c. The sampling error is therefore with-
in ±0.1° C for the temperature and ±0.02^0
for the salinity. These are the limits to be ex-
pected when bucket sampling of the temperature
and salinity is carefully done.

Finally, how is the quality of fit affected by
sampling frequency and how reliable are the
expected values that may be obtained from the
harmonic functions? The constraint imposed
by the sampling frequency on the resolution that
may be attained by harmonic analysis has al-
ready been discussed. The present question con-
cerns improvement of fit when the sampling
frequency is increased above the minimum re-
quirements.

At Koko Head the sampling frequency was
increased from once to twice weekly in 1961.
No significant change can be seen in the stand-

ard errors of estimate listed in Tables 1 and
2 as a result of doubling the sampling frequen-
cy. This observation is consistent with results
obtained from oceanographic data collected
at Ocean Weather Station "P" in the Gulf
of Alaska. Tabata (1964: Table 8) lists the
monthly mean value and the standard deviation
of the temperature at 10-m depth based on data
obtained twice daily, data obtained every second,
third, fourth, fifth, sixth, and seventh day of
July 1959 and May 1961. For July 1959 the
mean temperatures range from 10.70° to 10.81°
C and the standard deviations range from 0.60°
to 0.76° C. For May 1961 the mean temper-
atures range from 5.84° to 5.90° C and the
standard deviations range from 0.39° to 0.46° C.

In May 1961 Koko Head temperatures and
salinities were sampled on 25 days. The mean
of all temperature observations was 24.67° C
with standard deviation 0.27° C. The mean of
temperatures taken every fifth day was 24.58°
C with standard deviation 0.39° C. The mean
of all salinity observations was 34.759%o with
standard deviation 0.051%r. The mean of
salinities taken every fifth day was 34.772%o
with standard deviation 0.058%^. The temper-
ature results from Koko Head are comparable
to those from Ocean Weather Station "P" in
that mean values and standard deviations based
on diff'erent sampling frequencies fall within ap-
proximately the same range. The standard er-
rors of estimate for the May 1961 Koko Head
temperatures and salinities, based on the har-
monic functions with resolution of 1 month, are
lower than the standard deviations, namely,
0.25° C and 0.02T/,c, respectively. The stand-
ard errors of estimate as well as the standard
deviations do not change significantly when the
sampling frequency is increased above the re-
quired minimum to attain a desired resolution
by harmonic analysis.

Increasing the sampling frequency does, how-
ever, improve the confidence limits of a mean
value or the expected value of a harmonic func-
tion. A good measure of the confidence limits
of a mean value is the standard error of the
mean (the standard deviation divided by the
square root of the number of samples) . Return-

189

FISHERY BULLETIN: VOL. 69. NO, 1

ing to Tabata's table the standard error of the
mean for July 1959 is for twice daily sampling
every day 0.086° C, and for twice daily sampling
every seventh day 0.253° C. For the same
sampling frequencies in May 1961 the standard
errors of the mean are 0.053° and 0.15° C, re-
spectively. For the May 1961 Koko Head tem-
peratures the standard error of the mean is
0.055° C with 25 samples and 0.16° C with
sampling every fifth day. The standard error
of the mean for the May 1961 Koko Head sa-
linities is 0.010'/,, with 25 samples and 0.024',,
with sampling every fifth day. On the basis
of these considerations, the expected values ob-
tained from the temperature functions have an
uncertainty of ±0.10° C, and those from the sa-
linity functions have an uncertainty of ±0.015'/(c
when samples are obtained twice weekly.

At Christmas Island temperatures are sampled
daily rather than twice weekly as at Koko Head.
In consequence, despite the larger variability,
expected values obtained from the harmonic
functions have approximately the same uncer-
tainty as those obtained from the Koko Head

harmonic functions. This statement is con-
firmed by considering the error terms that can
be obtained by taking the difference of the ex-
pected values at the midpoint of the 30-day over-
lap portion of the Christmas Island temperature
functions (see appendix D). On average this er-
ror term is 0.07° C and ranges from 0 to 0.26° C.

SOME PROPERTIES OF THE TEMPERATURE
AND SALINITY DISTRIBUTIONS

Although the harmonic functions are merely
analytic expressions of the temperature and sa-
linity as a function of time, they do provide, to
some extent, insight into the nature of the dis-
tributions. For instance, the monthly standard
error of estimate, mentioned in the previous
section, provides a measure of the month-to-
month changes in variability. At Koko Head
there is no seasonal pattern in this variability
of the temperature; however, there is a seasonal
pattern in the variability of the salinity. The
monthly standard errors of estimate of the sa-
linity function with harmonic analysis carried
out to n = l;i, are listed in Table 4.

Table 4. — Standard error of estimate (/(c) for each month, 1956-68, of the Koko Head salinity. Harmonic

analysis is carried out to n = 13.

MONTH

YEAR

1

2

3

4

5

6

7

8

9

in

11

12

iq^o

O.OIO

0,017

0,02 7

0.04H

0,064

0.052

0.02 4

0,008

0.012

0.014

0.014

0.015

195 7

o.c^

0.013

0,021

0.015

0,030

0.034

0.02 9

0.017

0.036

0.031

O.OIH

0.034

1958

O.OCo

0.041

0,052

0.049

0,059

0.02 6

0.02 8

0.028

0.013

0.02 3

0.044

0.022

1959

0.0 'i9

0.035

0,044

0.136

0,040

0,036

0.054

0.02 3

0.047

0.032

0.023

0.035

1960

CO'.?

0.032

0.0 18

0.019

0,056

0.043

0.075

0.035

0.033

0.014

0.014

0.024

1961

0,036

0.019

0.017

0.0 19

0.027

0.054

0.01 1

n.020

0.025

0.021

0.023

0.023

1962

0,054

0.0 40

0,064

0.021

0.013

0.J23

0,02 5

0,033

0.031

0.031

O.niB

0.02 7

1963

0.CZ9

0.026

O.Oltl

0.073

0.045

0.036

0.02 1

0.025

0.0 20

0.022

0.032

0.036

1964

0,031

0.033

0.031

0.030

0.0 29

0.019

0.035

0.050

0.053

0.052

0.024

0.036

1965

CO**

0.053

0.059

0.092

0.03?

0,043

0.034

0.016

0.018

0,033

0.019

0.019

1966

0 ,026

0.016

0.011

0.014

0.072

0,021

0.011

0.012

0.016

0.03?

0.065

0.036

1967

0,026

0.0 29

0.097

0.055

0.050

0.015

0.019

0.021

0.017

0.031

0.0 29

0.056

1968

0.034

0.024

0.057

0.041

0.040

0.019

0.035

0.026

0.018

0.021

0.016

0.038

190

SECKEL and YONG; HARMONIC FUNCTIONS

In each year excepting 1957, 1964, and 1966,
highest variability occurred during the first 7
months of the year. In 1957 a seasonal pattern
was not clearly apparent and in 1964 and 1966
highest variability occurred during the last 5
months of the year. Although the seasonal pat-
tern of variability has not been examined in de-
tail, it is consistent with the results of previous
studies (Seckel, 1962, 1969). First, Hawaii is
located in the vicinity of a relatively high sa-
linity gradient that delineates the boundary of
the North Pacific Central Water. Thus, the
salinity measured at the Koko Head sampling
station is sensitive to variations in the location
of this water type boundary. Secondly, north-
ward displacement of water (warm advection)
tends to occur during the first 7 months of the
year. In consequence the water tyi^e boundary
that generally lies south of the Koko Head
sampling station during autumn and winter is
brought to within the vicinity of the sampling
station. The months with higher variability
tend to be associated with declines in the Koko
Head salinity.

Insight into the nature of the distributions is
also obtained by examining the spectra of the
harmonic functions. It is evident from the fig-
ures in appendix B, that considei-able temper-
ature and salinity variability at Koko Head
occurs with timespans of 35 to 60 days. Rather
than showing the amplitudes for each harmonic
of every function, the 13-year mean of the ab-
solute magnitude of amplitudes for each har-
monic of the Koko Head temperature and sa-
linity functions is presented in Figure 2.

For both the temperature and the salinity, the
amplitude of the annual cycle (n = 1) is largest.
The am]ilitudes then decline rapidly with in-
creasing harmonics ton =5. In the case of the
temperature, a slight increase in amplitude oc-
curs at M = 6 and )i = 9. Similar small in-
creases in amplitudes occur in the case of the
salinity at w = 7 and n = 9. The increased
amplitudes at « = 6 and w = 7, resolving 60-
and 52-day periods, reflect the climatic signals
described by Seckel (1962, 1969). The in-
creased amplitude at w = 9, resolving a 41-day
period, reflects shorter term variability that may
be due to large geostrophic eddies with dimen-

I 1 I 1 1 I I T -r 1 1 1

1

11

I

1 r

Mill

llllllii

I 2 3 4 5 6 7 8 9 10 II 12 13
365 182 122 91 73 61 52 46 40 36 33 30 28

PERIOD IN DAYS

Figure 2. — Mean magnitude of amplitudes for each
harmonic of the Koko Head temperature and salinity
functions, 1956-69.

sions near 200 km (Wyrtki, 1967) or eddying
flow near the Hawaiian Islands.

LONG-TERM HARMONIC FUNCTIONS

Long-term harmonic functions with the fun-
damental period spanning the entire duration of
observations, can be obtained by the method
described before in this paper. Temperatures
and salinities were used as computed for the

191

FISHERY BULLETIN: VOL. 69. NO. I

1st and 16th of each month from the harmonic
functions whose phase angles and coefficients
are tabulated in appendixes A and C. Harmonic
analysis was carried to w = 42 for the Koko
Head temperature and salinity, and n = 48 for
the Christmas Island temperature, giving in
each case a 4 months' resolution. The fitted
curves resulting from this analysis are shown
in Figure 3, together with the values that were
used as input data. Clearly the annual cycle
forms the dominant signal in the Koko Head
temperature curve. In the Koko Head salinity
and Christmas Island temperature curves longer
term changes are more pronounced than the an-
nual cycle.

The relatively large deviations of the input
data from the long-term function are to be ex-
pected. The figures of appendixes B and D show
that variations with a duration of less than 4
months can be relatively large and are not re-
solved by the long-term analyses made.

The spectra of the long-term harmonic func-
tions for the Koko Head temperatures and sa-
linities and the Christmas Island temperatures
are shown in Figure 4.

As is also apparent from Figure 3, the spec-
trum of the Koko Head temperature function is
distinct fi'om those of the Koko Head salinity
and Christmas Island temperature functions.
In the former the 12-month period has the most
pronounced amplitude, but in the latter two, al-
though the annual period has a large amplitude,
the amplitudes of longer period changes are
large and for some periods exceed those of the
annual period.

CONCLUSION

The results of this paper show that sea-surface
temperatures and salinities regularly monitored
at island sampling stations can be expressed by
harmonic functions of time. Advantages of an-
alytic expressions for the temperature and salin-
ity were cited in the introduction. Important
applications will be in climatic oceanography
where one may wish to filter out undesired "back-
ground noise." At Christmas Island, for ex-
ample, the short-term variability with a dura-
tion of 1 month or less can be filtered out by

using only the harmonic terms to n = 3 in the
quarterly functions. At Koko Head, the vari-
ability with duration of less than 50 days, that
may be due to large geostrophic or island-in-
duced eddies, can be filtered out by using only
the harmonic terms to w = 7 in the annual
functions.

We mentioned in the introduction that the
rates of change of temperature reflect the cli-
matic processes of change and that distortions
or aliasing may occur when monthly mean
temperatures are used to compute the change
of a property. Consider, for example, the Christ-
mas Island temperatures from March to May
1968 (appendix D, days 61 to 152). In Table 5
are listed the monthly mean observed temper-
atures, the month-to-month changes of mean
temperature, the expected temperatures from the
harmonic functions for the 16th of each month
(computed with harmonic terms up to w = 4),
and the month-to-month changes of expected
temperatures. It is clear from this illustration
that the use of mean values would result in an
underestimate of the rise in temperature from
March to April, and would obscure the decline
in temperature from April to May. The ex-
ample is not isolated and other instances can
be found in both the Koko Head and the Christ-
mas Island data.

Table 5. — Month-to-month temperature differences using
mean observed temperatures and expected tempera-
tures from the harmonic function, Christmas Island,
March to May 1968.

Mean
temperature

Change of

mean
temperature

Expected
temperature

Change of

expected

temperature

March 1968
April 1968
May 1968

° C

25.1

26.0
26.2

' C
09
0.2

° C

25.1

26.3
26.0

' c

1.2

-0.3

The results also aid in the choice of an opti-
mum sampling frequency. Both the desired
confidence limit and the desired resolution must
be considered. If the harmonic functions are
to be used in monitoring the oceanographic
climate as is the case of those presented in this
paper, then the limits of about ±0.1° C for the
expected temperature value and ±0.02%<! for
the expected salinity value are adequate. As-

192

SECKEL and YONG : HARMONIC FUNCTIONS

1954 1955 1956 1957 1958 1959 I960 1961 1962 1963 1964 1965 1966 1967 1968 1969

Figure 3. — Fitted curves with 4 months' resolution of the Koko Head temperature, 1956-69, Koko Head salin-
ity, 1956-69, and the Christmas Island temperatures, 1954-69. Input data are indicated by small triangles.

193

FISHERY BULLETIN: VOL. 69. NO. 1

"1 1 [ 1 T"

~] — [ — \ — r

n — I — I — I — n

-KOKO HEAD.OAHU

iLLtilljil

li.iiii.i.iil,

ml.mllll

iffWfCk MrAn nAHii

1

,

-

1 tI i.tilt..1irilllllllTLrii

_ I 2 3 4 5 6 7 8 9 lO I I 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42

OOOOU>ppp'^CD'^O<nOM«na>'O00^O(i)rOO'^int\JO00U)^tvJ — CJ>0DN.inVfOrj— o

S^towioo)^— odiDtn^cNjcvi — oo>(T>(Ij<Ilto^-^-^•^O^O^D^Dlnu^lf)^^l^ovv^J■rI■v vi ^^
_cDjnv(Ocj(ycM— ——— — — — —

PERIOD IN MONTHS

P 0.30 —

I

IM

-CHRISTMAS ISLAND

■■■■■iJii-iillLi.

li-iii.ii.i

__l 2 3 4 5 6 7 8 9 10 I I 12 13 M 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 J4 35 36 37 38 39 40 41 42 43 *4 45 "16 47 48

OOOOVOVO''>cy^oa>K<oo'')r^— tfl — p^roof^^— 0>i0vc\JO'D>fi"O''iw— oiCDKiomvKiw

PERIOD IN MONTHS

Figure 4. — Spectra of the long-term harmonic functions for Koko Head temperatures, 1956-69, Koko Head
salinities, 1956-69, and Christmas Island temperatures, 1954-69.

194

SECKEL and YONG : HARMONIC FUNCTIONS

suming that temperature and salinity samples
are of Koko Head quality, then for a resolution
of 1 month, weekly sampling is sufficient. Oc-
casionally, however, a scheduled sample is not
taken or an erroneous value must be eliminated.
In such cases sampling gaps would become too
large for the desired resolution. Undesirable
sampling gaps can be avoided by doubling the
minimum sampling frequency.

The simplicity and economy of deriving har-
monic functions by computer are of practical
value, particularly in the analysis of data
sampled automatically. By this method large
quantities of data can be brought into useful
form rapidly.

The results of this paper, based on manual
sampling, are useful in the investigations of
changes with a duration of more than 1 month.
Automated sampling would broaden the spec-
trum and permit analyses of shorter term var-
iations such as diurnal changes, changes of tidal
period, and other changes with durations of less
than 1 month.

Automated sampling would also improve the
quality of data since instruments can be placed
in locations where undesirable variability is min-
imized and where manual sampling is difficult.
At Koko Head, for example, samples are ob-
tained from an exposed rock ledge where the
island effects on the temperature and salinity
are small. At Christmas Island, however, the
sampling site is convenient and the best obtain-
able for manual sampling, but it is not the best
in terms of monitoring open-ocean temperatures.
This shortcoming is often also the case when
temperatures and salinities are measured at
tide stations located in protected bays or harbors.

The value of regularly monitoring the sea-
surface temperatures and salinities has been
demonstrated in many instances. For example,
empirical relations between Koko Head temper-
atures and salinities and the availability of skip-
jack tuna to the Hawaiian fishery have been
demonstrated (Seckel, 1963). Bjerknes (1969)
has shown the relationship between anomalously
high equatorial sea-surface temperatures using
primarily Canton Island observations, and the
intensification of the North Pacific westerlies

and trades. This relationship must, in turn,
affect temperatures and salinities in the North
Pacific.

In view of these factors, serious consideration
should be given to the establishment of auto-
mated sampling stations at selected islands in
the Pacific. The derivation of harmonic func-
tions, as demonstrated in this paper, would make
reduction of data into usable form simple and
economical and so facilitate the study of pro-
cesses which govern the climate in both ocean
and atmosphere.

LITERATURE CITED

Bjerknes, J.

1969. Atmospheric teleconnections from the equa-
torial Pacific. Mon. Weather Rev. 97(3) : 163-172.

HOLLOWAY, J. LeITH, JR.

1958. Smoothing and filtering of time series and
space fields. Advances in Geophysics 4: 351-389.
Academic Press, New York.
Kaplan, Wilfrbh).

1953. Advanced calculus. Addison-Wesley Pub-
ishing, Cambridge, Mass., 679 pp.
Seckel, Gunter R.

1962. Atlas of the oceanographic climate of the
Hawaiian Islands region. U.S. Fish Wildl. Serv.,
Fish. Bull. 61: 371-427.

1963. Climatic parameters and the Hawaiian skip-
jack fishery. In H. Rosa, Jr. (editor), Proc.
World Sci. Meet. Biol. Tunas Related Species.
FAO Fish. Rep. 6, 3: 1201-1208.

1969. The Hawaiian oceanographic climate, July
1963-June 1965. Bull. Jap. Soc. Fish. Oceanogr.,
Spec. No. (Prof. Uda's Commem. Pap.), pp. 105-
114.
Seckel, Gunter R., and Kenneth D. Waldron.

1960. Oceanography and the Hawaiian skipjack
fishery. Pac. Fisherman 58(3): 11-13.
Sokolnikoff, Ivan S.

1939. Advanced calculus. McGraw-Hill Book Co.,
New York and London, 446 pp.
Tabata, S.

1964. A study of the main physical factors gov-
erning the oceanographic conditions of station P
in the northeast Pacific Ocean. D. So. thesis,
Univ. Tokyo, 264 pp., 55 figs., 17 tables, 41 pp.
appendixes.

Wyktki, Klaus.

1967. The spectrum of ocean turbulence over dist-
ances between 40 and 1000 kilometers. Deut.
Hydrog. Z. 20(4) : 176-186.

195

FISHERY BULLETIN: VOL. 69, NO. !

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197

FISHERY BULLETIN: VOL. 69, NO. I

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198

SECKEL and YONG: HARMONIC FUNCTIONS

in ^ r^

^ ^ o

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en

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m —

199

FISHERY BULLETIN: VOL. 69. NO. 1

APPENDIX B

Sea-surface temperatures and salinities, Koko Head, Oahu, 1956-69: Fitted curves
with observed values for each year.

Note: Circled observations have not been used in the harmonic analysis.

1959

1963

40 80 120 160 200 240 280 320 J60 0 40 80 120 160 200 240 280 320 360
DAYS DAYS

Appendix B Figure 1. — Sea-surface temperatures, Koko Head, 1956-69.

200

SECKEL and YONG: HARMONIC FUNCTIONS
28

Appendix B Figure 1. — Sea-surface temperatures, Koko Head, 1956-69. — Continued.

201

55 5

1956

r- I I [

A

•^^^^VA,

.-.^^v^"

1 35,0

-

Wv-^

-

34 5

1 1

1 1 1 1

1 ) 1

t 35 0

1957

J I I \ I I L.

1 r

1958

-I 1 r

_J I [ 1 L_

-I r

I960

"1 1 1 1 1 1 r

1962

FISHERY BULLETIN: VOL. 69, NO. I

■T r

-r

-I I I I I I I I L

_; I I L.

-I 1 r

1 1 1 \ 1 1 I 1 r

1961

T 1 1 1 1 \ 1 1 r

1963

0 40 80 120 160 200 240 280 320 3€0 0 40 80 120 160 200 240 280 320 360

DAYS DAYS

Appendix B Figure 2.— Sea-surface salinities, Koko Head, 1956-69.

202

SECKEL and YONG: HARMONIC FUNCTIONS

35 5

— !■ ■

1964

1 ■ I ■

1

— 1 —

-

^'

•-,

.

)

t 350

i

_

v\.

^^H*_ "Jt \

y?^"

X

/

3«5

-

1965

_l 1 I L.

"T \ \ r

1966

T i 1 r

1968

I I 1 r-

1969

MEAN

355

1967

III'

350

r^ A *

' S^ '

\j ' """^

s. -^^y^^^*^

■^x^/^-rv;/^

0

•

v

34.5

o

40 80 120 160 200 240 280 320 360

40 80 120 160 200 240 280 320 360

DAYS

Appendix B Figure 2. — Sea-surface salinities Koko Head, 1956-69 — Continued.

203

FISHERY BL'LLETIN: VOL. 69. NO. I

Appendix C Table 1. — Phase angles and coefficients for
sea-surface temperatures, Christmas Island, 1954-69.

APPENDIX C

Sea-surface temperatures, Christ-
mas Island, 1954-69. Phase angles
and coefficients for harmonic functions
for each quarter of each year:

Days 1 to 120 = First quarter,
91 to 210 = Second quarter,
181 to 300 = Third quarter,
271 to 390 = Fourth quarter, ex-
tending 25 days
into new year,

S = K + hi + Y C„ cosuint — a„) ,
n = l

2n
120

days"

t is the time in days beginning with
the first day of each quarter.

Note: Mean values do not include
phase angles and coefficients for the
third and fourth quarters of 1967.

PHSSE

SNCies

IN DAYS

N-VSLUES 1

VEAR

ou.

1

2

3

4

S

6

7

1954

1

29.96

-14.98-

0

58

22

60

-16

29

0

45

-28.43

2

21.92

24.40

-25

77

15

21

23

02

24

75

8.06

-19.<,6

21.45

-25

73

-10

27

-14

81

-6

52

-20.70

-15.22

27.64

6

23

-9

84

25

21

27

55

-26.39

1955

-25.04

-14.36

-19

56

-25

05

10

26

1

57

-17.43

-1.3*

-22.95

16

15

-12

52

-27

83

-6

10

24.53

-28.76

23.27

29

69

-21

77

-13

26

28

12

10. 11

-5.04

-11.73

-11

08

5

52

9

94

-2

89

-1.09

1956

-15.33

29.40

18

77

24

08

27

16

17

61

-20.53

25.55

29.94

-23

88

27

18

-22

20

-10

40

-15.15

-25.54

21.39

-22

54

13

46

20

29

29

39

-17.29

-28.99

16.56

-15

87

-0

61

6

14

-27

58

1.48

1957

-20.33

9.55

-3

33

-13

.39

-22

18

24

07

4. 11

12.45

3.80

-2 1

56

22

.60

5

.19

18

04

15.55

12.50

-8.47

27

08

22

.42

5

53

4

72

-74.37

1.99

-11.91

-1

14

15

.68

5

.08

-17

77

-21.22

195B

-15.55

-9.55

16

21

-19

.82

-16

02

-9

08

8.91

-25.92

-8.31

-7

41

25

.09

-26

.16

-28

53

17.52

17.11

-4.98

25

83

9

.96

6

39

-15

05

-24.35

-25.45

15.23

-11

73

19

.38

7

.25

16

83

2 0.96

1959

-11.25

18.21

25

.30

27

.40

2

.42

-3

.45

-27.76

-4.58

-18.05

-2

17

-6

.57

15

.76

-29

98

29.65

-13.92

-7.90

26

00

-0

.14

15

.14

3

09

21.42

-25.63

-23.22

-13

08

18

.13

-10

.51

-22

25

23.72

1960

-21.36

3.15

-22

57

15

.60

-I

.99

22

75

21.91

14.95

-26.09

18

68

5

.43

23

12

-22

73

28.33

21.14

17.18

10

04

7

.87

5

.23

20

84

-2.55

-0.89

0.25

-28

.94

9

.45

17

99

23

48

-26.06

1961

-4.50

2.29

14

03

9

.01

9

.50

-26

75

14.55

-9.38

-18.74

15

60

10

81

5

59

-IB

31

-27.53

-27.87

-27.55

27

26

25

.89

21

47

-10

55

-13.26

-19.95

-17.14

-3

05

0

39

-13

80

-7

92

24.95

1952

10. 13

-24.95

-15

24

29

64

4

40

15

34

-1.98

-10.33

-1.79

27

51

28

58

-0

31

3

38

-15.25

18.78

20.95

-6

12

-29

1'

-7

99

-1

52

2.56

29.70

7.75

14

37

-13

15

-25

15

-4

47

13.65

1963

18.62

14.96

21

65

21

78

-21

72

-8

72

-19.15

-25.86

-23.08

-21

84

-25

95

-12

90

-7

23

-3.15

27.97

-11.92

17

92

-10

01

20

37

-9

25

15.05

5.53

-27.74

-4

23

12

23

13

77

5

GO

-14.49

196'.

10.51

23.82

-4

95

-11

50

-?2

13

13

52

9.47

29.78

-24.66

11

54

-19

75

22

21

-13

85

-22.39

3.66

-21.54

13

24

5

89

-17

78

15

09

6.34

9.57

-19.61

-22

27

-11

15

-17

19

-18

45

-4.51

196 5

-12.81

22.40

-29

54

24

56

25

12

16

28

-23.00

-15.03

-23.97

-7

39

-19

45

2

93

-11

03

1.10

28.09

-13.92

12

10

-9

87

6

09

14

42

-23.32

-10.42

20.99

27

57

29

49

-18

90

17

82

-18.33

1966

-2.72

-22.51

-8

68

9

75

-10

67

-6

62

29.58

29.77

26.12

4

26

21

28

15

23

27

61

-22.03

7.34

25.04

9

12

25

58

1

93

10

76

4.92

8.34

0.12

-20

67

1

80

-28

17

3

39

26.99

196 7

-22.45

14.34

-25

09

18

95

0

56

10

45

-20.57

-8.35

-8.8B

-I

85

-22

37

-74

08

15

50

21.27

-29.90

-2.2*

18

31

26

99

-16

01

9

55

-12.24

-19.32

23.12

7

45

-6

85

-19

51

7

19

8.69

1968

-9.18

-10.55

23

64

-20

93

11

65

-2 0

43

-24. *0

-14.96

-23.53

13

31

-14

18

7

83

27.

96

70.00

-0.07

-22.76

5.

17

5

55

-23

92

-n

81

-2.39

27.65

-15.84

3

23

-21

90

-10

38

-2*.

36

6.48

1969

13.34

14.46

6

54

-17

39

7

54

6.

53

-7.79

8.02

-23.81

-20

76

26

56

-28

81

29.

11

27.75

22.54

11. ?8

U.

96

25

05

-B.

17

12.

69

29.92

-24.65

-0.88

-15

33

-12

66

-11

06

-13.

65

4.95

MEAN

-14.97

-10.80

-22.

92

-20.

97

16.

82

20.

22

20.72

9.25

11.74

20.

56

15.

71

28.

30

-19.

45

-9.57

5.57

22.63

15.

62

1*.

65

25.

53

22.

30

-25.12

-4.77

-2.6*

-27.

75

-25.

*3

20.

79

-26.

95

10.88

204

SECKEL and YONG : HARMONIC FUNCTIONS

Appendix C Table 1. — Phase angles and coefficients for sea-surface temperatures, Christmas

Island, 1954-69— Continued.

AMPLITUDES

N-V4LUES

YEAR

OLF.

K

b

1

2

3

4

5

6

7

1954

26.0740
27.5957
26.4268
25.6919

0.0070
-0.0169
-0.0139
-0.0090

-0.2543

-0.3583

0.6131

0.2918

-0. 1310

-0.1443

0.0815

-0.1571

0.1609

0. 1307

-0.0171

-0.0880

-0.0772

-0.1171

0.1332

0.251 7

-0.2329

-0.1275

0.2404

0.1746

0.0637
-0.1517

0.1808
-0.1001

0.0743
-0.0342
-O.llll
-0.0948

1955

25.1633
26.2916
26.1027
24.8187

0.0067
-0.0017
-0.0107
-0.0041

0.2697
-0.1687
-0.0046

0.2259

0.1614

0.0292

0.1350

-0.1449

-0.0373

-0.0565

-0.0375

0.1578

0.1008
-0.0347
-0.0213
-0. 1789

-0.0 360
0.0635
0.0353
0. 1836

-0.0632
0. 1000

-0.0234
0.0316

-0.0693

0. 1044

-0.0917

-0.0946

1956

24.3949
27.7890
27.0093
26.1278

0.0183
-0.0174
-0.0139
-0.0049

0.4678

-0.4323

0.5433

0.1022

-0.1493

-0.2228

-0.1689

0.0890

-0,0999
0. 1648
0.1537

-0. 1479

0. 131 1
-0.1209
-0.1784

-0,0249

-0.1 107

0. 1879

-0.1535

-0.0544

-0.0674
0.0361
0.1329
0.2481

0.0277

0.0232

0.0787

-0.0168

1957

25.4577
27.7558
27.6226
28.0288

0.0176
0.0025
0.0008
0.0066

0.3612
-0.2169

0.4254
-0.5153

0.1892

-0.4098

0.0970

0.0870

0. 1458

0.1621

0,0939

-0,2655

0,1574
-0.0302
-0,1184
-0.1550

0.104 5
-0,1359
-0,2340

0.0453

0.0540

0.2283

-0.1508

0.2115

0.0693
-0.1088
-0.1202

0. 1495

1958

28.6567
28.2124
26.6129
26,2684

-0.0050
-0.0091

0.0

0.0066

0. 1989
-0.2768

0. 3456
-0.2862

0.1052
-0.0700
-0.1571

0.0679

0.0983

-0,0795

0.2536

0,1955

0.0407

-0.0335

0.0694

0.1226

0.0531
-0.1346
-0.1207

0.0867

-0.0732

-0.0783

0.0260

-0.0355

-0.0469
0.1074
0.0474
0.0184

1959

26.8512
27.8849
26.3895
26.7237

0.0025
-0.0132
-0.0025
-0.0091

0.3797
-0.2731

0.5706
-0.1536

-0.3106

-0.1508

0.4088

-0.2531

-0.2379
-0. 1839
-0.2084
-0.2372

-0.1429
-0.1429
-0,1502
-0,2151

0.0562
-0.0674
-0.1315

0.1113

-0.0545

-0.0819

-0.0472

0.1418

0.0333

0.0641

-0.0216

-0.0299

1960

25.6504
26.9858
26.5916
26.0923

0.0042
-0.0025
-0.0033
-0.0049

0.4722

-0.3299

0.3107

0.1670

0.0679

0.1787

0.1345

-0.3030

0. 1461

-0.1260

0. 1430

0.190'=

0,1082
-0.0797
-0.1676
-0.1630

0.0721

0.0321

-0.0941

-0,0272

-0.0691

-0.04 04

0.0284

-0.1538

0.0460
-0.0377
-0.0720
-0.1171

1961

25.3508
26.7608
26.5390
25.3383

0.0109

0.0025

-0.0066

0.0016

0.3816
-0.1900
-0.4129
-0.2387

0.1665
-0.0611
-0.2944

0.1069

0.0125

-0. 1699

0,0796

0. 1592

-0.1322

-0.2093

0.0568

-0.0197

-0.1105
0.1176

-0.1021
0 . U 2 2

0.1068

0.0254

-0.1658

0.0396

0.1995

0.0986

-0.0319

0.0913

1962

24.9107
26.5159
26.9093
25.6078

0.0168

0.0033

-0.0139

-0.0090

0.1042
-0.2921
-0.2714
-0.2539

-0.2920

-0.2701

0.1472

0.2136

0,2226
-0.1616
-0.1661

0.0377

0.0317

0.107 7

-0.0770

0.0963

0.O329
-0,0996

0.0532
-0.0275

0.1702
-0.1532

0.0723
-0.0509

-0,0358

0,1131

-0.0359

-0.0641

1963

24.5106
27.3700
27.2705
27.6762

0.0202
-0.0033

0.0041
-0.0066

-0.1137
0.5749
0.3865

-0.0697

-0.0707
0.3627

-0.2983
0.1280

0.1670
0.3065
0.0802
0.0933

0.0583

0,1391

-0,1328

0,1403

0.1332
0. 1594
0. 1014
0.0886

-0.0370
0.0779
0.1157

0.0333

-0,2257
0.2440

-0.0641
0.0603

1964

26.7596
26.2958
26.0159
24.8755

-0.0025

-0.0017

-0.0092

0.0033

0.4138
0.2579
0.4285
0.1803

-0.0692
-0.2425
-0.1814
-0.1368

0.0988

-0. 1394

0. 1304

0.0999

0,1046

0,0522

-0.0741

0.1655

-0.0832
0.1147
0.1106

-0.0848

-0.0360
0.0422
0.0733
0.0989

-0.0658
-0.0869
-0.1184
-0.0299

1965

25.0849
26.4776
27.2809
27.3759

0.0151
0.0149
0.0033
0.0098

0.2248
-0.2682

0.6393
-0.7293

-0.1215

-0.2288

0. 1140

-0.2572

0.0998
-O.ldOl

0.3702
-0.0559

-0.0676

-0.0793

0.2312

-0,1109

-0.1001

-0.0111

-0.2151

0.0830

0.0939

0.0295

0.1376

-0.0606

-0.0430
-0.0471
-0.0732
-0,0654

1966

28.3584
28.5148
26.6145
27.2510

-0.0076
-0.0198
-0.0041
-0.0164

-0.5145

-0.8788

0.4308

-0.8011

0.1954
-0.3261

0.4345
-0.0462

-0.25B5
0.0899
0.2067
0.6174

0.0741

-0.0254

0.2310

0.1390

-0.1413

-0.0921

0.2313

-0.1069

0.1728
-0. 1870

0.0932
-0.0289

0,1227

0,0975

0.1893

-0.2482

1967

25.3932
26.4576
26.8336
27.8062

0.0076

0.0066

-0.0044

-0.0233

0.3944
-0.5433

0.1341
-0.0832

0.1627

-0. 1613

0.1093

0.0851

0.2864

-0,1932

0,0717

0,0734

-0.0779

-0.0712

0.0649

0.0593

0.0240
-0.0620
-O.0396

0.0301

-0.1438
0.0473

-0.0322
0.0046

0.0926
0.0553
0.0505
0.0312

1968

25.1250
25.9567
26.2971
26.9967

0.0033
0.0066
0.0057
0.0

0.5597

-0.1308

0.3013

0.1068

0.2691
-0.1705

0.0743
-0.0967

-0. 1413
-0.2038
-0.1219
-0. 1344

0.2029
0.0706
0.2030
0. 1499

0.0708

0.0276

0.1886

-0.1181

0.0239
-0.1003
-0.2381
-n.1165

0.0730
0.0172
0.2042
0.0213

1969

26.4649
28.5357
27.0045
26.4789

0.0168
-0.0165
-0.0025

0.0074

0.1895
-0.2815
-0.0625
-0.2169

0.1321

0.3460

0.1304

-0.0886

-0,0369

0, 13J4

-0.0353

-0. U90

-0.1854
-0.1603
-0.1166
-0.1053

0.066 3

0.1393

-0.0388

-0,1537

-0.0638

-0,1347

0.1949

-0.0353

0,0926
-0.1080

0.0671
-0.0390

MEAN

25.8678
27.2124
26.7124
26.3568

0.0082
-0.0041
-0.0044
-0.0019

0.2151
-0.1744

0.1770
-0.C997

0.0484
-0.0779

0.0789
-0.0317

0.0522

-0,0930

0.0498

0.0509

0.0285
-0.0509
-0.0071

0.0459

-0,0074

-0,0233

-0.0629

0.0341

-0.0107
0,0283
0,0384
0.0573

0.0132

0.0229

-0.0094

-0.0145

205

FISHERY BULLETIN: VOL. 69, NO. 1

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214

MASKING UNDESIRABLE FLAVORS IN FISH OILS"

GiSELA JELLINEK" AND MAURICE E. STANSBY'

ABSTRACT

The odor of fish oil used medicinally may require masking by flavoring materials. During a search
for suitable masking materials, fresh, specially refined menhaden oil having a minimum of flavor was
stored with and without added flavoring materials for 5 days at 75° F and for longer periods at sev-
eral lower temperatures. In initial preliminary screening tests with 66 diff'erent flavoring materials,
the masking of rancid or other unpalatable flavors developing in the stored oil was evaluated by a
small panel. In later tests, a large consumer-type panel consisting of untrained laboratory personnel
was used to determine the preference for the flavors of those materials that worked best in the screen-
ing test and that were of a type approved by the U.S. Food and Drug Administration for use in foods.
Several flavoring materials showed promise, particularly those having the flavor of root beer, lemon,
wintergreen (methyl salicylate), and wild cherry.

When fish oil is used medicinally — for example,
as a cholesterol depressant or as a source of
vitamins — the presence of "fishy," rancid, or
other flavor components may make it unpalat-
able. One way of overcoming this problem is
to add some flavoring material that will mask
the undesirable flavor. It is important that the
added flavor be one that is pleasing to most con-
sumers so that we do not merely substitute one
undesirable flavor for a slightly more undesir-
able one. The aim of this work therefore was
to find flavoring materials, approved for food
use, that would adequately mask the unpleasant
flavor components developing in stored men-
haden oil (the fish oil produced in largest
quantity in the United States) and that would
also have a flavor pleasing to most customers.

We carried out this study in two experiments.
In Experiment 1, reasonably palatable men-
haden oil refined by a special technique was
stored for 5 days at room temperature with and
without added flavoring materials. A small
trained panel was used to determine the effi-
ciency of over 66 different flavoring materials

' This research was carried out as a cooperative pro-
gram between the University of California Food Science
and Technology Department, Davis, Calif. 95616, and
the Bureau of Commercial Fisheries (now National
Marine Fisheries Service) Technological Laboratory,
Seattle, Wash. 98102.

" Mozartstrasse 15, 69 Heidelberg, Germany.

' National Marine Fisheries Service Pioneer Research
Laboratory, Seattle, Wash. 98102.

in masking the developing undesirable flavor
components in the stored oil. Then, in Exper-
iment 2, those materials giving the best masking
action, excluding any not approved for use with
food, were further tested by a larger consumer-
type panel for hedonic rating of the different
flavors resulting from adding the selected flavor-
ing materials to the oil before it was stored.

EXPERIMENT 1 -MASKING TESTS

The first series of tests were set up as a rapid
screening of many flavoring materials to see
which ones best masked the undesirable off fla-
vors that develop in stored menhaden oil. At
this stage, no consideration was given to indi-
vidual preference for the flavor additive, which
was investigated in Experiment 2.

MATERIALS

Menhaden oil was specially refined by a com-
bination of clay bleaching, molecular distillation,
and treatment with massive quantities of silica
gel (Stansby and Jellinek, 1965). This treat-
ment yielded an oil that was free of fishy and
rancid flavor components but that still retained
some small burnt flavor.

Sixty-six flavor additives that were screened
initially included synthetics and isolates.

Manuscript received August 1970.

FISHERY BULLETIN, VOL. 69, NO, 1, 1971.

215

FISHERY BULLETIN: VOL. 69, NO. I

undiluted and in alcoholic solution, essential oils,
and imitation flavoring compositions. The ad-
ditives were obtained from many sources.

METHODS

In the initial work, 5-ml samples of menhaden
oil, with or without flavor additive, were held
in covered plastic petri dishes (100 by 15 mm)
for 5 days at 75° F (22° C). Preliminary tests
indicated that 1 part by volume of flavoring ma-
terial per 400 parts by volume of oil gave about
the proper concentration with most flavor prep-
arations, so this concentration was used through-
out the work. With the large surface of oil
exposed to air in this test, a fairly advanced
stage of rancidity was reached in 5 days.

In some of the later work in which larger
samples were required, oil in both 200-ml (8-oz)
and 25-ml (1-oz) stoppered bottles was stored:
(1) at 40° F (4° C) for 8 to 12 weeks, (2) at
_20° F (—29° C) for 8 to 12 weeks, and (3)
at room temperature— that is, at 75° F (22° C)
for 4 weeks.

For various aspects of this work, especially
in preliminary observations, paired comparison
tests, duo-trio tests, ranking tests and descriptive
tests — all described by Jellinek (1964) were
used. For most of this work, however, descrip-
tive tests and ranking tests were used; only the
descriptive and ranking tests will be tabulated
in this report.

Samples of oil were tasted by immersing the
tip end of a plastic spoon into the oil and placing
the spoon into the mouth. This procedure
avoided coating the lips with oil, and it elim-
inated much of the objection of some panel mem-
bers to an undesirable oily feel during protracted
examination of many samples.

The panel used in this part of the work con-
sisted of 5 to 7 laboratory workers all of whom
had had some previous experience with odors
and flavors of fish oils. Several preliminary
training sessions were held in order for them
to become familiar with and be able to use con-
sistent terminology for the odors and flavors
to be encountered in the experimental work.

RESULTS

Initial Screening Test

In an initial screening test of all 66 flavoring
compounds, a degree-of -masking scale was used
as follows: + + , very good masking; + , good
masking; ±, good masking when first tasted
but did not mask aftertaste; ?, questionable
masking; — , negative masking — that is, the
taste was not masked (Table 1). The flavoring
materials are listed in alphabetical order with-
in each category.

Main-Examination Test

We then made a more detailed examination,
paying greater attention to the type of flavor
which sometimes varied at diff'erent stages dur-
ing the storage of the oil. The following com-
ments show certain limitations of many of the
flavor additives.

Fkivoring materials with "green" or "floral"
flavor properties. — Because fresh fish oil has a
"green-grassy" or "green-cucumber" odor and
flavor, two green standards had been worked
out in earlier experiments (Stansby and Jellinek,
1965). These standards were cis-hexen-3-ol-l
and Green Aroma Hr (coded sample of Haar-
mann and Reimer, Holzminden, West Germany,'
probably: nona-2-enal or nona-2-dienal or a
mixture of both (Forss, Dunstone, Ramshaw,
and Stark, 1962). These two green standards
were tried as masking agents.

Cis-he.xen-3-ol-l contributed a definite green-
grassy note to the menhaden oil and also showed
very good masking abilities in the exposed men-
haden oil.

Gi'een Aroma HR contributed a green-cucum-
ber note to the fish oil but seemed to have pro-
oxidant qualities. In comparison with the con-
trol sample, the menhaden oil got rancid faster
and reached a higher intensity. These observa-
tions seem to be similar to those made about 20
years ago on butter with a high content of di-

' The use of trade names is merely to facilitate de-
scriptions; no endorsement is implied.

216

JELLINEK and STANSBV : MASKING FLAVORS IN FISH OILS

Table 1. — Effectiveness of 66 flavoring materials in masking the fishy flavor and odor of menhaden oil.

Category and substance

Flavor type
and descriptions

Masking

effect

Category and substance

Flavor type
ond descriptions

Masking
effect

Synthetics and isolates

Essential orls-Con.

Acetoin

butterlike

±1

Lemon oil, U.S.P.

fruity-lemon

+

Agrumen aldehyde

fruity-citrus

—

Lime oil

fruity-lime

+

Anethol, U.S. Pharmacopoeia

(U.S. P.) spicy-anise

+ +

Orange oil, U.S.P.

fruity-oronge

+

Benzaldehyde

sweet-bitter almond

—

Peppermint oil

cooling-peppermint

i-Butyl quinoline

green-spinachlike or

Root beer oil

wintergreen group

+ +

eorthy (asparagus

)

—

Spearmint oil, rectified

cooling -spearmint

Carvol

spicy-caraway

—

Cinnamic aldehyde

spicy-cinnamon

?

Imitation flavoring compositions

Citral

fruity-lemon

—

Blood Orange Flavor

fruity-orange

+

Ethyl phenyl acetate

sweet-honayliko

+

Imitation Boysenberry Flavor

fruity-boysenberry

Ethyl salicylate

wintergreen

+ +

Butter Aroma

butterlike

-t-

Eucalyptol

cooling

—

Cherry Bouquet

fruity-cherry or sweet cherry -(--}-

Eugenol

spicy-cloves

—

Imitation Cranberry Flavor

fruity-cranberry

_

Foretine

green-mushroomy/earthy

—

Fruity Bouquet

fruity

++

Geraniol

green-leafy & floral

rosy

—

Green Aroma HR

green-cucumber

+

Geranyl acetote

green-leafy & floral

rosy

—

Imitation Honey Flavor

sweet-honeylike

+

Geranyl butyrate

green-leafy & floral

rosy

—

Imitation Lemon Juice Flovor

fruity-lemon

+

Geranyl propionate

green-leofy & floral

rosy

—

#5I.I24A

cis-hexen-3-ol-]

green-grassy

+ 4-

Lemon Mint Flavor

fruity-lemon

+

i-Jasmone

green-leafy

—

Lime Mint Flavor

fruity-lime

-1-

Linalool

florol

—

Imitation Melon Base

fruity-melon

^

Melonal (2,6-dimethyl-5-hepten-I-al)

fruity-melony

+

Orange Mint Flavor

fruity-oronge

+

Menthol

cooling

—

Tetrorome Orange

fruity-citrus

+

Methyl nonyl ketone

green-?

—

Violet Flavor

floral-violet

Methyl salicylate

wintergreen

-H-

Imitation Essence Arrack

fruity-brondy

_

Slyrolyl ocetate

green

fruity-peach

_

Imitation Butterscotch

sweet-caramel

?

-Undecalacton

—

Oil Brandy Flavor

brandy-like

Vanillin

sweet-vanilla

?

Imitation Essence Caramel

sweet-caromel-vanilla

?

Essenlrol oils

Imitation Oil Soluble Flavor

fruity-cherry

++

Wild Cherry #12009

Anise oil, U.S. P.

spicy-anise

+ +

Imitation Oil Chocolate

sweet-caramel-chocolate

?

Bay oil

spicy-bay

—

Imitation Essence Cocoa

sweet-molt-chocolcte

?

Coraway oil

spicy-caraway

—

Malt True Concentrate

sweet-molt

_

Cassio oil

spicy-cassia

+ +

Imitation Aroma Maple

sweet-maple

_

Cinnamon oil, U.S. P.

spicy-cinnamon

+ +

Imitation Oil Rum, Jamaica

fruity-rumlike

-I-+

Clove oil

spicy-clove

—

#017

Ginger oil

spicy-ginger

-

Tutti Frutti Oil

fruity-candy

++

acetyl. Butter with a high diacetyl content has
more butter flavor and turns rancid faster than
does butter with a low diacetyl content. For this
reason, export butter has to be washed carefully
to lower the content of diacetyl (MoncriefF,
1951).

In addition to these two green standards, some
other chemicals with green character or floral
character, or both, were tried but without suc-
cess. They are listed among the synthetics and
isolates above. Some of them — namely, i-butyl
quinoline, foretine, i-jasmone, methyl nonyl ke-
tone, and styralyl acetate — contributed sharp-
ness and a biting note to the menhaden oil.

Geraniol, geranyl acetate, geranyl butyrate,
and geranyl propionate contributed a green,
somewhat leafy note combined with sharpness.
In addition, a flowery "rosy" note was observed.
These materials have been recommended re-

)3eatedly by aroma companies. However, the
materials do not seem to be suitable for use with
menhaden oil. The same observation was made
with "violet" flavor.

Flavoring materials with "fruity" flavor pi'O-
perties. — Citral added a refreshing lemon odor
and flavor to fish oil; but in addition, it is sharp
in taste with the sharpness lingering in the after-
taste. Repeat tests with other concentrations
confirmed that citral alone is too sharp. In com-
bination with fruity flavoring compositions, it
might help to introduce a refreshing note.

Melonal (2,6-dimethyl-.5-hepten-l-al) contrib-
uted a fruity refreshing note, lingering in the
aftertaste. In addition, it gave a greenness sim-
ilar to that described by some panel members
as "green-melony." Unfortunately, the sample
turned rancid rapidly toward the end of the

217

FISHERY BULLETIN: VOL. 69, NO. 1

5-day period of storage when melonal was
added.

y-Undecalactone (peach lactone), when used
alone, is too artificial in odor and too sharp in
flavor.

Lemon oil made the odor of the menhaden
oil aromatic-fruity. It was retested with good
results.

Lime oil gave a refi'eshing citrus taste to the
menhaden oil, contributed some astringency, but
it did not linger in the aftertaste. The aftertaste
was more lemon-"candy"-like. (It was probably
not pure lime oil; artificial flavoring material
probably had been added, giving this "candy"-
like flavor.)

Orange oil has good masking properties.

Blood Orange Flavor, Lemon Juice Flavor,
Lemon Mint Flavor, Lime Mint Flavor, Orange
Mint Flavor, Tetrarome Orange had good mask-
ing properties.

Imitation Boysenberry Flavor and Imitation
Cranberry Flavor had masking properties for
the odor rather than for the flavor. In addition,
the flavor was quite artificial and unpleasant.
The fruits that were imitated were not recog-
nizable as such either in odor or in flavor. We
tried to obtain a natural cranberry oil, but it is
not available on the market.

Cherry Bouquet was outstanding in the mask-
ing properties of rancidity and oily feeling.

Wild Cherry Flavor also had very good mask-
ing properties.

Fruity Bouquet had very good masking pro-
perties; the flavor was fruity-candylike.

Imitation Melon Base, in alcoholic dilutions,
gave a fruity-melon type of odor. In undiluted
form, it smelled fruity and honey sweet. The
oily feeling was well masked in the flavor with
fruitiness and sweetness lingering in the after-
taste. After the oil was exposed for 1 day, there
was in addition some lingering sharpness.

Imitation Oil Rum had good masking proper-
ties.

Flavoring materials with "butterlike" flavor
properties. — Acetoin contributed a butterlike
flavor and feeling, lingered in the aftertaste.
The butter feeling is perceivable longer in the

aftertaste than is the oily feeling. Unfortu-
nately, the sample became rancid after only 3
days, indicating some prooxidant eflfect.

Butter Aroma showed good masking proper-
ties but only at the start of the test.

Flavoring materials with "sweet" flavor pro-
perties.— Benzaldehyde (bitter almond flavor)
alone is not satisfactory. It has to be used in
a flavoring complex such as Cherry Bouquet.

Ethyl phenyl acetate and Imitation Honey
Flavor mask the oily feeling. In addition they
contribute a honey flavor.

Vanillin was tried in diff'erent concentrations,
but the results obtained were not satisfactory.

Flavoring materials ivith "spicy" flavor pro-
perties.— Anethol contributeed an anise flavor.
It masked the oily feeling very well and changed
it into a pleasant anise flavor (similar to that
of cough drops flavored with anise oil or an-
ethol).

Carvol and eugenol were not suitable. They
added a sharp, somewhat burnt note to the men-
haden oil.

Anise oil showed very good masking proper-
ties.

Bay oil, caraway oil, clove oil, and ginger oil
were not suitable. They added a sharp, some-
what burnt note to the fish oil.

Cassia oil and cinammon oil were equally suit-
able.

Flavoring materials of the "wintergreen"
grojip. — Ethyl salicylate, methyl salicylate, and
root beer oil all masked the oily feeling very
well.

Flavoring materials with "cooling" flavor pro-
perties.— Menthol, peppermint oil, and spear-
mint oil contributed initially only a bland taste
and pleasant oily feeling to the menhaden oil.
Samples with eucalyptol had a sharp note in
flavor. All samples had a rancid flavor at the
end of the 5-day storage test at room temper-
ature.

218

JELLINEK and STANSBY: MASKING FLAVORS IN FISH OILS

Reduction in the List of Potential Masking Materials

The number of potential flavoring materials
for masking the objectionable flavor components
in the menhaden oil, based upon the preliminary
screening tests, was too large to subject them
all to a large-scale consumer-type test and there-
fore had to be decreased. The most promising
flavoring materials for masking were:

Synthetics and isolates:
Anethol

Ethyl phenyl acetate
Ethyl salicylate
cis-hexen-3-ol-l
Methyl salicylate

Essential oils:
Anise oil, U.S.P.
Cassia oil

Cinnamon oil, U.S.P.
Lemon oil
Orange oil, U.S.P.
Root beer oil

Imitation flavoring compositions:
Blood Orange Flavor
Butter Aroma
Cherry Bouquet
Fruity Bouquet
Imitation Honey Flavor
Imitation Lemon Juice Flavor *51.124A
Lemon Mint Flavor
Lime Mint Flavor
Orange Mint Flavor
Tetrarome Orange
Imitation Oil Rum #017
Imitation Oil Wild Cherry #12009
Tutti Frutti Oil

Because using more than a dozen flavoring
materials in the large-scale consumer tests was
not desirable, we considered limiting further
the number of flavoring materials for additional
study. The results of this phase of the exam-
ination permitted us to eliminate additional ma-
terials, based upon the following observations.

Ethyl phenyl acetate was described as per-
fumelike by some consumers and was therefore
disliked by them.

Ethyl salicylate was partly liked, partly dis-

liked by diff"erent panel members. The scores for
methyl salicylate were higher.

Cis-hexen-ol-1 tested in samples stored at 40° F
and — 20° F for 8 weeks did not result in observ-
able rancidity. The samples still had a green-
grassy character. The control sample stored at
40° F was rancid; the control sample stored
at — 20° F was almost odorless and was faint
cucumber green in flavor.

Even though cis-hexen-3-ol-l masked the oily
feeling and rancidity, it was not liked by the
panel.

Cassia oil and cinnamon oil have much the
same flavor; cinnamon oil was therefore arbi-
trarily selected for further experiments.

To reduce the number of fruity flavors, we
made a preliminary consumer test. From six
flavors — Blood Orange, Lemon Juice, Lemon
Mint, Lime Mint, Orange Mint, and Tetrarome
Orange — Lemon Juice Flavor was chosen for
further experiments.

Fruity Bouquet with its candy, fruitlike flavor
was disliked by some panel members who de-
scribed it as being perfumelike.

Cherry Bouquet not only was outstanding in
the masking properties of rancidity and oily
feeling but received the highest rating in the
consumer test.

Only flavoring materials allowed by the U.S.
Food and Drug Administration could be con-
sidered. The Cherry Bouquet and Fruity Bou-
quet are perfume compositions and are not per-
mitted as food additives.

Butter Aroma was not satisfactory. As was
already experienced with acetoin, samples flav-
ored with a butter-aroma composition turned
rancid faster in the storage test at 40° F than
did the control. The 40° F sample was definitely
rancid after 8 weeks of storage, although the
samples held below freezing were not.

Imitation Honey Flavor was too artificial in fla-
vor and therefore disliked by most of the panel.

Masking of Fish Oil with Pronounced Burnt
Flavor

As was described in Materials, menhaden oil
was refined both by the regular three-stage (clay
bleaching, molecular distillation, silica gel)

219

FISHERY BULLETIN: VOL. 69, NO. 1

process and by a modified two-step process in
which the silica-gel procedure was eliminated
but in which the collection of distillate during
molecular distillation was restricted. Such a
procedure greatly simplified refining but resulted
in a menhaden-oil product containing consider-
able burnt-flavor component. Flavoring ma-
terials giving best results with the latter oil
did not necessarily give optimum results with
the silica gel refined oil.

Of the flavoring materials found to be most
successful for the ordinarily refined procedure,
those with a fruity-type flavor — especially
Cherry Bouquet and Fruity Bouquet — masked
the burnt flavor better than did such flavors as
root beer oil, methyl salicylate, or anethol.
None of these compounds was able to mask
the burnt flavor completely when added to the
freshly distilled oil. After 6 weeks of storage
at 40° F (4° C) samples masked with Cherry
Bouquet or Fruity Bouquet had no burnt flavor,
but considerable remained when root beer oil
or methyl salicylate was used, and an interme-
diate amount remained when anethol was used.

Flavoring materials liaving good masking
properties and giving promise for good consumer
acceptability were as follows: anethol, anise
oil, cinnamon oil, lemon oil, Lemon Juice Flavor,
methyl salicylate, orange oil, root beer oil. Imi-
tation Oil Rum, Imitation Oil Wild Cherry, and
Tutti Frutti Oil.

When considerable burnt flavor is present in
menhaden oil, such as occurs when the two-stage
modified refining process is used, none of the
masking agents completely obscures this burnt
flavor. Certain fruity flavors such as Cherry
Bouquet or Fruity Bouquet are the most efl'ective
in masking this flavor, with methyl salicylate or
root beer oil being less effective.

EXPERIMENT 2-CONSUMER-TYPE
TESTS

The next stage of the investigation was to
determine consumer hedonic rating for the sev-
eral masking suljstances that had been found
to be almost equally suitable for disguising the
objectionable flavors developing in menhaden
oil during storage.

MATERIALS

The same materials— both menhaden oil and
flavor additives — were used in this phase.

The flavors used were those that in Experi-
ment 1 had given the best masking results. Any
flavors that were used in Experiment 1 and that
were not approved for food additive use by the
U.S. Food and Drug Administration were elim-
inated in this part of the work. Table 2 shows
the identity and source of these substances.

Table 2. — Flavor components rated in the consumer test.

Flavor moterial

Suppliers^

Anethol, U.S. P.

Anise oil, U.S. P.

Cinnamon oil, U.S. P.

Lemon oil, U.S.P.

Imitation Lemon Juice Flovor #5I.I24A

Methyl salicylote

Orange oil, U.S.P_.

Root beer oil

Imitation Oil Rum #017

Imitotion Oil Wild Cherry #12009

Tutti Frutti Oil

1,4
3
3
4
2

1,4
4
3
4
4
4

1 — Fellon Chemicals Co., Inc., Brooklyn, N.Y.

2 - Firmenich, New York, N.Y.

3 — Florosynth Laboratories, Inc., New York, N.Y.

4 - Frilzche Brothers, Inc., New York, N.Y.

METHODS

A modified molecular distillation procedure
was used. This procedure eliminated the ne-
cessity for carrying out the time-consuming
treatment with silica gel. The oil was distilled
only until the pot residue amounted to 10 %
(as contrasted to 3 ^r in the usual methods).
This decreased amount of distillation resulted
in much less burnt flavor (although in consider-
ably more burnt flavor than when a silica-gel
treatment was used). The oil could be used,
however, directly without silica-gel treatment
when sufficiently effective masking agents were
used.

Oils were stored at (1) 40° F (4° C) (2) at
—20° F (—29° C) for 4 to 12 weeks.

The panel for the consumer-type test consisted
of Bureau of Commercial Fisheries personnel
who had no previous experience in taste testing.
The 15 to 20 participants were asked to rate

220

JELLINIiK. a..d STANSBY: MASKING FLAVORS IN FISH OILS

Name

Please indicate by check
and rank it in order of

mark ( -^ ' )
preference

Date

how much you like or dislike each sample
(1-best, 2-second best, etc.).

Hedonic Scale

Scale

Code Code Code

Like very much
Like moderately
Neither like nor dislike
Dislike moderately
Dislike very much

1

2
3
4
5

Comments:

Too weak
Satisfactory
Too strong

Flavor recognized as:
Ranking order:

Figure 1. — Score sheet for the consumer test.

two to three flavored samples on a hedonic scale,
using the score sheet shown in Figure 1.

Five ml of oil was rated by the panel 5 days
a week for about 3 months. It was necessary
to determine whether a flavor, liked initially,
was still liked after continuous intake. Likes
and dislikes were expressed on an hedonic scale
of 5 points (Fig. 1).

RESULTS

Table 3 summarizes the consumer ratings over
the period of test.

Some consumers were consistent in their ra-
ting throughout the entire period of the test.
Other consumers were consistent only with some
flavors but were inconsistent with others.

DISCUSSION

Table 3 shows that all of the tested flavors
received high ratings (1 or 2) as main ratings
by the consumer-type panel. It should be noted
that these high ratings were not given by the
consumer panel as a whole but rather by groups

within the panel. It also should be noted that
there is a split of like and dislike for the same
flavor.

This split is understandable, and it may be
due to different causes. Individuals with var-
ious background show widely different flavor
preferences. For example, Europeans who are
used to methyl salicylate being used primarily
for flavoring medicinal products or in disinfect-
ants would doubtlessly have rated this substance
lower for fish-oil masking than did our Amer-
ican panel. In parts of Asia where anise seed

Table 3. — Consumer ratings for different flavored fish oil.

Flavoring moteriol
added to fish oil

Hedonic ratings'

Anelhol I, 2, (4)

Anise oil (I) 2, (4)

Cinnamon oil 1, 2, (3) 4

Lemon oil (I) 2, (3) (4)

Imitation Lemon Juice Flavor #5I.124A 1, 2, (4)

Methyl salicylate 1, 2, 3,

Orange oil (I) 2, 3, (4)

Root beer oil 1, 2, (3) (4)

Imitation Oil Rum #017 (I) 2, (3) (4)

Imitation Oil Wild Cherry #12009 1, (2) 3, (4)

Tutti Fruiti Oil I, 2, (4)

' Rating numbers not in parentheses were the ones given by most
consumers; those in parentheses were the ones given by fewer members—
for example, lemon oil was liked moderately (Rating 2) by most con-
sumers, but some gave a higher rating (1) and some gave a lower rating
(3) or (4).

(5)

(5)

221

FISHERY BULLETIN: VOL 69. NO 1

is grown, frequently anise is disliked as a flavor-
ing material. In addition to differences due to
nationality, childhood experience has a definite
influence on likes and dislikes. Orange oil is a
good example. Panel members who had been
forced during childhood to take orange-flavored
cod-liver oil as a medicine objected to orange
flavor. As can be observed in daily food intake
where some persons prefer sweet foods and
others prefer acid foods, there is likewise the
same split of like and dislike with sweet flavor-
ing materials (cinnamon oil and Tutti Frutti
Oil) and with acid flavors (Lemon Juice Flavor).
Even though the consumer-type panel as a
whole did not rank the flavors in a definite order
of preference, a pronounced like for any of the
oflFered flavors by smaller consumer groups is
obvious. This finding should encoui-age trial of
these fish-oil masking flavors with larger con-
sumer groups.

ACKNOWLEDGMENTS

The following concerns supplied information
on, and furnished samples of, flavoring mater-
ials: Felton Chemicals Co., Inc., Brooklyn, N.Y.;
Firmenich, New York, N.Y.; Florasynth Lab-

oratories, Inc., New York, N.Y.; Fritzche Broth-
ers, Inc., New York, N.Y. ; Haarmann and
Reimer, Holzminden, West Germany; Interna-
tional Flavors and Fragrances, New York, N.Y.;
Norda Essential Oil and Chemical Co., New
York, N.Y.; Polak's Frutal Works, Middletown,
N.Y.; and Ritter and Company, Los Angeles,
Calif.

LITERATURE CITED

H. Ramshaw, and
J. Food Sci. 27(1):

FORSS, D. A., E. A. DUNSTONE, E.

W. Stark.

1962. The flavor of cucumbers.
90-93.
Jellinek, Gisela.

1964. Introduction to and critical review of mod-
ern methods of sensory analysis (odour, taste, and
flavour evaluations) with special emphasis on de-
scriptive sensory analysis (flavour profile meth-
od). J. Nutr. Diet. 1(3): 219-260.

MONCRIEF, R. W.

1951. The chemical senses. 2d ed. Leonard Hill
Limited, London, vii -|- 538 p.
Stansby, Maurice E., and Gisela Jellinek.

1965. Flavor and odor characteristics of fishery
products with particular reference to early ox-
idative changes in menhaden oil. hi Rudolf
Kreuzer (editor). The technology of fish utiliza-
tion, contributions from research, p. 171-176.
Fishing News (Books) Ltd. London.

222

EARLY DEVELOPMENTAL STAGES OF THE BROWN SHRIMP,
Penaeus aztecus IVES, REARED IN THE LABORATORY'

Harry L. Cook- and M. Alice Murphy'

ABSTRACT

The larval and first postlarval stages of the brown shrimp, Penaeus aztecus Ives, reared from eggs
spawned in the laboratory, as well as the eggs themselves, are described and illustrated. The larvae
and first postlarva are compared with those of the pink shrimp, P. duoranim Burkenroad, and white
shrimp, P. setifenis (Linn.).

Commercial shrimp landings from Gulf of Mex-
ico and South Atlantic waters of the United
States are comprised mainly of three species:
the brown shrimp, Penaeus aztecus Ives; the
pink shrimp, P. duoranim Burkenroad; and the
white shrimp, P. setiferus (Linn.). The Gulf
coast shrimp fishery is the most valuable of do-
mestic commercial fisheries, and in 1968 the
value to fishermen for shrimp caught in the
Gulf amounted to nearly $95 million. Because
of their relative importance, these shrimps are
being intensively studied by the National Ma-
rine Fisheries Service in an effort to understand
more fully their biology and ecology.

Thirteen species of penaeid shrimp repre-
senting five genera inhabit the shallow near-
shore waters of the northwestern Gulf. At the
present time their larvae can only be identified
to genus (Cook, 1966). Within genera the
larvae are so similar morphologically that at
any given stage the various species cannot yet
be distinguished. Since adults of the three com-
mercially important species often occur together
and overlap in their spawning activity, there is
also some intermingling of their planktonic
larvae. To answer basic questions about larval
distribution, growth, and survival of each spe-

• Contribution No. 309, National Marine Fisheries
Service Biological Laboratory, Galveston, Texas 77550.

^ Formerly National Marine Fisheries Service Bio-
logical Laboratory, Galveston, Texas; present address:
Division of Contract Research, Texas Division, Dow
Chemical Company, Freeport, Texas 77541.

' National Marine Fisheries Service Biological Lab-
oratory, Galveston, Texas 77550.

Manuscript received September 1970.

FISHERY BULLETIN: VOL. 69. NO. 1, 1971.

cies, accurate identification of larvae is essential.
The larval and early postlarval stages of the
pink shrimp were described by Dobkin (1961),
and those of the white shrimp by Pearson ( 1939)
and Heegaard (1953). These shrimp have five
nauplial, three protozoeal, three mysis, and sev-
eral postlarval stages. Their morphological
characteristics during these stages are so alike,
however, that biologists still encounter diflSculty
in differentiating the two species. Since the
early developmental stages of the brown shrimp
have not been described, the purpose of this
])aper is to do so and at the same time compare
them with corresponding stages of the pink and
white shrimps.

METHODS AND MATERIALS

Larvae of the brown shrimp were first suc-
cessfully cultured in the laboratory during the
fall of 1963. Since that time, culture techniques
have improved greatly. The methods used in
our culture of larval penaeid shrimp were de-
scribed by Cook and Murphy (1966), Cook
(1969), and Cook and Murphy (1969).

Specimens of each stage were preserved for
descriptive purposes. Drawings were made
with the aid of a camera lucida. The figures
of each substage are composite and represent
an "average" larvae rather than any one indi-
vidual. Also, with the exception of the nauplii,
appendages on these figures ai-e intended to in-
dicate only relative size and position, not to show
details of setation. The enlarged figures of

223

FISHERY BULLETIN: VOL. 69. NO. 1

mouth parts and other appendages were taken
from two individuals representing each sub-
stage. Setules on the setae of the larvae were
deliberately omitted, and nauplial appendages
were rotated on their axes to avoid cluttering
the figures and obscuring important diagnostic
characters.

Abbreviations used in the text are: TL =
total length, including rostrum when present but
excluding caudal spines; W = body width at
the point of greatest width; CL = carapace
length, including the rostrum; and N = the
number of specimens examined.

DESCRIPTION OF
DEVELOPMENTAL STAGES

EGG AND HATCHING

(Fig- 1)
Diameter 0.26 mm

Viable eggs are round, golden brown, and
translucent. As the nauplius develops, it fills
the egg case and can be seen moving sporadically.
At hatching, the egg case splits and the posterior
portion of the nauplius protrudes. Then the
nauplius, unmoving, appears to swell until it is

forced from the shell, the entire process taking
about 30 sec.

When first hatched, the nauplius rests almost
motionless for 3 to 5 min. Although the ap-
pendages do not move during this time, spastic
movement can be seen within the body near the
base of each appendage. Suddenly the nauplius
folds its appendages posteriorly along the ven-
tral margins of the body, and, in one quick move-
ment, sheds from its posterior end a loose-fitting
exoskeleton and starts swimming actively. At
fii-st, the nauplius alternates 2- to 3-sec periods
of swimming with resting periods of equal
duration.

NAUPLIUS I

(Fig- 2)
Mean TL = 0.35 mm (0.32-0.38 mm)
Mean W =0.19 mm (0.18-0.21 mm)

N = 55

The pyriform body is unsegmented and pos-
sesses a ventrally projecting labrum. An ocel-
lus, which persists in subsequent nauplial sub-
stages, is present near the anterior end. The
dorsal surface of the body is smooth except for
a small median spine posteriorly (Fig. 2b). The
posterior portion of the body is rounded and
bears a single pair of caudal spines.

The body color in all nauplial substages is a

Figure 1. — Nauplius emerging from egg.

Figure 2. — Nauplius I : a, ventral view ; b, lateral view.

224

COOK and MURPHY: DEVELOPMENTAL STAGES OF BROWN SHRIMP

golden brown, with the appendages tinged red
apically. The translucent body appears filled
with small granules that flow freely when the
cuticle is ruptured.

Three pairs of appendages are present. The
first antennae are uniramous and slightly less
than three-quarters the length of the body. Each
second antenna is biramous, its endopod slightly
shorter than the exopod, and approximately
three-quai'ters the body length. The mandibles
are biramous and slightly less than one-half the
body length.

In this substage all setae are smooth, but in
subsequent substages, the longer ones are plu-
mose.

Setation of appendages:

First antenna: Two short ventrolateral;
two long terminal plus a
small spike; one long
dorsolateral.
Second antenna:

Endopod: Two short ventrolateral;
two long terminal plus a
small spike.
Exopod: Three long ventrolateral;

two long terminal.
Mandible: Both branches bear three

long setae.

NAUPLIUS II

(Fig- 3)

Mean TL = 0.39 mm (0.36-0.41 mm)

Mean W = 0.20 mm (0.20-0.21 mm)

N = 27

Body shape is similar to that of the first
nauplius except that the posterior end is no
longer rounded; the portion between the single
pair of furcal spines has become straightened.
The small dorsomedian spine near the posterior
end (present in the first substage) is absent
in this substage.

Setation of appendages:

First antenna: One short and one medium
ventrolateral; one short,
one medium, and one
long terminal ; one me-
dium dorsolateral.

Figure 3. — Nauplius II, ventral view.

Second antenna:

Endopod: Two short ventrolateral;
one small spike and two
long terminal.
Exopod: Three long ventrolateral;

two long and one short
terminal.
Mandible: Same as Nauplius I.

NAUPLIUS III

(Fig. 4)
Mean TL = 0.40 mm (0.36-0.43 mm)
Mean W = 0.21 mm (0.20-0.23 mm)

N = 51

The posterior portion of the body is more
elongate than in previous substages, but the
shape remains essentially the same. The body
is slightly depressed between the two developing
furcal processes, each of which bears four
spines. The small dorsomedian spine, absent
in the second nauplius, reappears. The begin-
nings of ventral appendages can be seen as small
indentations posterior to the labrum. The bases
of the mandibles have become slightly swollen,
and small frontal organs are present at the an-
terior end of the body.

Setation of appendages:

First antenna: One short and two medium
ventrolateral; one short,
one medium, and one

225

FISHERY BULLETIN: VOL, 69. NO. 1

Exopod:

Four long ventrolateral;
two long, one medium,
and one short terminal.

Same as Nauplius I.

Figure 4. — Nauplius III, ventral view.

long terminal; one short
dorsolateral.
Second antenna:

Endopod: Two short ventrolateral;

three long terminal.
Exopod: Three long ventrolateral;

three long and one short
terminal.
Mandible: Same as Nauplius I.

NAUPLIUS IV

(Fig. 5)
Mean TL = 0.44 mm (0.41-0.47 mm)
Mean W =0.21 mm (0.20-0.22 mm)

N = 35

The posterior portion of the body has become
more slender and two definite rounded furcal
processes are formed, each one with six spines.
The small dorsomedian spine on the body is
absent and does not reappear in later substages.
Ventral appendages (first and second maxillae
and first and second maxillipeds), still covered
by the cuticle, are visible posterior to the man-
dibles. Frontal organs are present.

Setation of appendages:

First antenna: Same as Nauplius III.
Second antenna:

Endopod: Two short ventrolateral;

one short and three long
terminal.

Figure 5. — Nauplius IV, ventral view.

NAUPLIUS V

(Fig. 6)

Mean TL = 0.50 mm (0.43-0.58 mm)

Mean W = 0.20 mm (0.18-0.22 mm)

N = 41

The body is further elongated and the furcal
processes are more pronounced, each giving rise
to seven spines. The maxillae and maxillipeds
are now external and show more advanced de-
velopment. The swelling at the base of the
mandible is large and prominent and has a
masticatory surface composed of several rows
of small teeth. The endopod and the exopod of
the mandible are frequently hollow and trans-
parent. The outline of a developing carapace
can be seen on the dorsal surface of the body,
and frontal organs are present.

In living specimens, eyes and an anal canal
are visible internally. In preserved specimens,
the anal canal appears to open externally.

It was not possible to determine if the ap-
pendages were truly segmented. The append-
ages of some specimens appeared segmented,
i.e., their surfaces possessed annular indenta-
tions; those of others did not.

226

COOK and MURPHY : DEVELOPMENTAL STAGES OF BROWN SHRIMP

Figure 6. — Nauplius V, ventral view.

Setation of appendages:

First antenna: Two short and one medium
ventrolateral; two long
and one medium termi-
nal; two medium and
one short dorsolateral.

Second antenna:
Endopod:

Exopod:

Mandible:

Two short and one medium
ventrolateral; one me-
dium and three long
terminal.

Five long ventrolateral;
three long and one short
terminal.

Same as Nauplius I.

PROTOZOEA I

(Fig. 7)
Mean TL = 0.96 mm (0.89-1.21 mm)
Mean CL = 0.45 mm (0.40-0.49 mm)

N = 40

With the molt from Nauplius V to Protozoea
I, the larvae change radically. A large, loose-
fitting carapace covers the anterior portion of
the body. The narrow posterior portion is di-
vided into a six-segmented thorax and an un-
segmented abdomen. The masticatory surface
of the mandible has become greatly enlarged,
and the endopod and exopod have been lost. The
maxillae and maxillipeds are large and func-
tional.

The carapace is rounded with a median notch
at the anterior end; two rounded frontal organs

are the only protuberances on it. An ocellus,
which persists in subsequent protozoeal sub-
stages, is present between a pair of compound
eyes covered by the carapace. The labrum is
smaller than in the preceding stage and has a
short spine on its anterior mai'gin. Two lobes
of the labium, with short bristles on their in-
ner margins, are posterior to the labrum. The
mandibles curve inward and several of their
teeth can be seen between the labrum and
labium.

The first antenna, which is about equal in
length to the endopod plus the protopod of the
second antenna, is composed of three major seg-
ments. The basal segment is divided into five
subsegments and bears one short seta. The
second segment possesses three setae, two ven-
trolateral, and one posterolateral. The distal
segment has three terminal and three subter-
minal setae.

The second antenna consists of a protopod of
three segments, an endopod of two segments,
and an exopod of 10 segments. The endopod
bears one seta at the juncture with the protopod,
another on the first segment, two at the juncture
of the first and second segments, and five ter-
minal setae on the distal segment. The exopod
has eight setae on its ventrolateral and two on
its dorsolateral margins, as well as three ter-
minal setae.

The mandible has lost its exopod and endopod.
The masticatory surface now faces medially and
has several rings of teeth.

The first maxilla is composed of an unseg-
mented protopod, an endopod of three segments,
and a small knoblike exopod. The protopod con-
sists of two large lobes, each bearing several
stout, toothed spines. The first segment of the
endopod possesses two or three setae; the sec-
ond, two; and the distal, five. The exopod bears
four setae.

The second maxilla is about the same size
as the first. It has an unsegmented protopod,
an endopod of four segments, and a knoblike
exopod. The protopod has five lobes on its
ventral margin; the basal lobe bears approxi-
mately eight setae, the remainder three to six.
The first three segments of the endopod each

227

FISHERY BULLETIN: VOL 69, NO. 1

Figure 7. — Protozoea I: a, ventral view; b, antenna I; c, antenna IT; d, mandible; e, maxilla I; f, maxilla 11;

K, maxilliped I; h, maxilliped II.

228

COOK anJ MLRPHY: DEVELOPMENTAL STAGES OF BROWN SHRIMP

have two setae, and the fourth, three. The ex-
opod has five setae.

The first maxilliped is biramous and longer
than the maxillae. It has a protopod of two
segTnents, an endopod of four segments, and an
unsegmented exopod. The protopod bears about
17 setae. The basal segment of the endopod
possesses three setae; the second, one or two;
the third, two; and the terminal, five. The
exopod has four lateral and three terminal setae.

The second maxilliped, though smaller, is al-
most identical to the first. The protopod bears
six setae. The endopod is composed of four seg-
ments, the first and third giving rise to two
setae; the second, one or two; the fourth, five.
The exopod has three lateral and three terminal
setae.

The third maxilliped is present only as a small
bud.

The caudal furcae each retain seven spines
and are separated by a well-defined anal opening.
The digestive tract is visible posterior to the
labrum.

The body is colorless and almost transparent
with the exception of two red spots, one on each
side of the anal opening.

PROTOZOEA II

(Fig. 8)
Mean TL = 1.71 mm (1.28-2.01 mm)
Mean CL = 0.80 mm (0.72-0.87 mm)

N = 25

The most apparent modification from the pre-
ceding substage is the presence of stalked com-
pound eyes. Additional features that charac-
terize this substage are a ventrally projecting
rostrum, a pair of bifurcate supraorbital spines,
and a segmented abdomen.

Frontal organs are absent in this and later
stages.

Segmentation of the appendages remains the
same as described for the first protozoea. The
only changes in setation are on the first antenna.
Several setules are added near the posterolateral
seta on the second segment, and an additional
terminal seta is found on the last segment. Ru-
diments of the third maxilliped and five pairs
of pereiopods are present.

The abdomen is divided into six segments, the
telson not being separated from the sixth. The
number of furcal spines remains constant at
seven pairs.

PROTOZOEA III

(Fig. 9)
Mean TL = 2.59 mm (2.40-2.59 mm)
Mean CL = 1.06 mm (0.93-1.40 mm)

N = 15

The principal diflferences between this sub-
stage and the preceding one are the presence
of biramous uropods and spines on the abdom-
inal segments.

The carapace is close fitting and covers all
but the last three thoracic somites. The supra-
orbital spines are no longer bifurcate.

The five subsegments comprising the basal
section of the first antenna in the preceding
protozoeal substages have fused into a single
unit. The ventrolateral seta that originated
from the middle of the second segment has been
lost, and a similar one is present on the distal
margin. The second antenna, mandible, and
maxillae remain essentially the same as in the
preceding substage. Two setae have been added
to the exopod of the first maxilliped. The first
segment of the endopod and the exopod of the
second maxilliped have gained a seta. Although
the third maxilliped and five pereiopods have
developed further and are now biramous, they
remain functionless.

The abdomen is divided into six segments, the
telson being distinct from the sixth segment.
The sixth segment is about three-fourths the
length of the preceding five combined. Each
of the first five segments has a dorsomedian
spine on its posterior margin. The fifth seg-
ment also possesses a pair of midlateral spines,
and the sixth somite has paired midlateral and
ventrolateral spines.

A pair of biramous uropods are present, orig-
inating from the ventroanterior mai'gin of the
telson. The exopod, slightly longer than the
endopod, bears five or six setae at its apex.

An additional pair of caudal spines have been
added medially on the telson, making a total of
eight pairs.

229

FISHERY BULLETIN: VOL. 6<3, NO. I

Figures. — Protozoea II: a, dorsal view; b, antenna I; c, antenna II; d, maxilla I ; e, maxilla II; f, maxilliped I;

g, maxilliped II.

230

COOK and MLIRPHY: DEVELOPMENTAL STAGES OF BROWN SIIRLMP

Figure 9. — Protozoea III: a, dorsal view; b, antenna I; c, antenna II; d, teeth of mandible; e, maxilla I;
f, maxilla II; g, maxilliped I; h, maxilliped 11; i, abdominal segments V and VI.

231

FISHERY BULLETIN: VOL. 69. NO. I

MYSIS I

(Fig. 10)
Mean TL = 3.3 mm (3.2-3.5 mm)
Mean CL = 1.2 mm (1.1-1.3 mm)

N = 18

With the molt from the third protozoeal to the
first mysis substage, the larvae undergo another
radical change and assume a more shrimplike
appearance. The most apparent change is the
development of functional pereiopods with long
brushlike exopods. The antennae also undergo
considerable change, with the exopods of the
second antennae becoming modified to form
flattened antennal blades.

The carapace fits the body more closely than
in preceding stages and covers all but the last
two thoracic somites. The rostrum is not de-
pressed as in the protozoeal substages, but pro-
trudes forward on a horizontal plane. Supra-
orbital spines are still present although reduced
in size. A small spine now occurs on the antero-
ventral corners of the carapace. In addition,
a pair of hepatic spines have been added to the
carapace, one spine on each side originating
from a point located approximately one-sixth the
carapace length from the anterior margin.

An ocellus is present in this and subsequent
mysis substages.

The first antenna is composed of three seg-
ments, the first being I'/j times the length of
the second and third combined. Numerous
setae now occur along the apjiendage, and sev-
eral arise at the apex of each segment. In ad-
dition, a prominent ventromedian spine is pre-
sent on the first segment. The distal segment
gives rise to two unsegmented branches, the ex-
ternal one bearing six or seven setae and being
twice as long as the internal one, which bears
two terminal setae.

The second antenna consists of a protopod of
two segments, an unsegmented endopod with
three lateral and three terminal setae, and a
flattened, unsegmented, bladelike exopod with
a single lateral seta and 11 setae along the
medial and terminal margins.

The mandible and maxillae remain essentially
the same as in the preceding substage except

that the exopod of the second maxillae has be-
come enlarged and bears 10 setae. The first
and second segments of the endopod of the first
and second maxillipeds have acquired an addi-
tional seta. The exopod of the first maxilliped
has gained a seta and that of the second has lost
three. The third maxilliped has evolved further
and is now longer than the first two. It has
a two-segmented protopod that bears two setae.
The first segment of the five making up the
endopod possesses two setae; the second, one;
the third, none; the fourth, three; and the fifth,
five. The unsegmented e.xopod has five or six
terminal and subterminal setae.

The five pairs of pereiopods have undergone
considerable enlargement and their exopods
serve as the principal swimming organs during
the mysis stage. The endopods of the first three
pairs are modified into rudimentary chelae that
have four or five terminal setae. The first
pereiopod consists of a protopod of two seg-
ments, an unsegmented endopod, and an exopod
which bears five or six terminal and subterminal
setae. The last four pereiopods were not ex-
amined in detail.

The dorsomedian spines of the first two ab-
dominal segments have been lost while those on
the third, fourth, and fifth segments are still
prominent. The fifth segment retains a pair
of midlateral spines. A dorsomedian and a
ventromedian sjiine are present on the sixth
segment in addition to the paired midlateral and
ventrolateral spines found in the preceding sub-
stage. Anlages of the pleopods can he seen on
the ventral surface of the first five abdominal
segments.

The uropod has developed an unsegmented
protopod that possesses a large posteroventral
spine and a smaller postei'olateral spine. The
endopod carries 11 setae on its medial and termi-
nal borders, while the exopod, which has about
13 setae on its medial and terminal margins,
has, in addition, a prominent spine on its postero-
lateral edge.

The telson is cleft terminally and bears seven
pairs of terminal and one pair of lateral spines.

232

COOK and MURPHY: DEVELOPMENTAL STAGES OF BROWN SHRIMP

Figure 10. — Mysis I: a, dorsal view; b, lateral view; c, antenna I; d, antenna II; e, mandible; f, maxilla I;
g, maxilla II; h, maxilliped I; i, maxilliped II; j, maxilliped III; k, pereiopod I.

233

FISHERY BULLETIN: VOL, 69, NO. 1

MYSIS II

(Fig. 11)
Mean TL ^ 3-8 mm (3.3-4.2 mm)
Mean CL = 1.3 mm (1.2-1.4 mm)

N = 11

This substage can be distinguished from the
first mysis by the presence of unsegmented
pleopods and a spine on the antennal blade.

The addition of a dorsal spine on the rostrum
is the only change in armature of the carapace
which now covers the entire thorax.

The terminal branches of the first antenna are
almost equal in length. A developing statocyst
appears as a slight bulge near the base of the
appendage.

Setation on the endopod of the second an-
tenna has been reduced to a single terminal seta.
The number of setae on the exopod has increased
to 18, and they occur along the medial border
and around the tip to the point of insertion of
a subterminal spine on the lateral margin. A
spine has been added to the terminus of the
protopod.

The mandible has developed a small unseg-
mented palp.

The exopod of the first maxilla is no longer
present; that of the second maxilla has increased
in size and now bears 13 setae. A seta now
arises from the protopod of the first maxilliped
at a point between the insertion of the endopod
and exopod. In addition to a seta on the distal
segment, the endopod of the second maxilliped
gains a fifth segment that does not possess setae.
The protopods of the third maxilliped and first
pereiopod have gained a seta. A single seta on
the basal segment is the only one present on the
three segments that have been added to the
endopod of the first pereiopod. Rudiments of
gills are present as small protuberances on the
bases of the protopods of the maxillipeds and
first pereiopods.

The armature of the abdomen and uropods
is unchanged from the preceding substage. Ru-
dimentary, unjointed pleopods are present on
the ventral surface of the first five abdominal
segments.

The telson has six pairs of terminal and two
pairs of lateral spines.

MYSIS III

(Fig. 12)

Mean TL = 4.3 mm (3.9-4.7 mm)

Mean CL = 1.4 mm (1.3-1.5 mm)

N = 21

In this substage, the pleopods and endopod
of the second antenna are composed of two seg-
ments. These characters serve to differentiate
third mysis from preceding substages.

Spination of the carapace remains essentially
the same as in Mysis II, although a second
dorsal spine on the rostrum was found in approx-
imately one-half of the preserved specimens.

The outer branch arising from the distal seg-
ment of the first antenna is longer than the in-
ner branch and is composed of two segments.
A lateral seta has been added to the endopod
of the second antenna which is now also com-
posed of two segments; the exopod likewise
possesses one more seta.

The mandibular palp is slightly longer and
has a weak apical seta.

The first maxilla and first maxilliped remain
unchanged. The exopod of the second maxilla
has become elongate and has 18 setae, while
those of the second and third maxillipeds and
first pereiopod have two segments. The fourth
segment of the endopod of the second maxil-
liped has gained one seta, as has the exopod.
One seta has been added to the second segment
of the endopod of the third maxilliped and two
to the third; the fourth has lost one. The en-
dopod of the first pereiopod is composed of five
segments, with the fourth forming the propodus
of the chela and the fifth the dactylus ; the sec-
ond segment has gained one seta, and the third,
two. The gills on the maxillipeds and first pe-
reiopod have enlarged.

The only change of consequence in the pos-
terior portion of the body involves the pleopods,
which are now composed of two segments and
bear two or three terminal setae.

234

COOK and MURPHY ; DEVELOPMENTAL STAGES OF BROWN SHRIMP

01 MM.

Figure 11. — Mysis II: a, lateral view; b, antenna I; c, antenna II; d, maxilla I; e, maxilla II; f, maxilliped I;
g, maxilliped 11; h, maxilliped III; i, pereiopod I; j. tip of telson.

235

FISHERY BULLETIN: \0L. 69, NO. 1

0 1 MM

Figure 12. — Mysis III: a, lateral view; b, antenna I; c, antenna II; d, mandibular palp; e, maxilla I; f, max-
illa II; g, maxilliped I; h, maxilliped II; i, maxilliped III; j, pereiopod I; k, tip of telson.

236

COOK and MURPHV: DEVELOPMENTAL STAGES OF BROWN SHRLVIP

POSTLARVA I

(Fig. 13)
Mean TL = 4.6 mm (4.2-5.0 mm)
Mean CL = 1.5 mm (1.4-1.6 mm)

N = 15

No drastic changes in morphology are as-
sociated with the molt from the third mysis
to the first postlarval stage. The pleopods, now
well developed and setose, are the principal
swimming organs. There is usually a reduction
in the size of the exopods of the pereiopods,
which, if present, are only vestigial.

The carapace is much the same as in the third
mysis. The rostrum bears one or two spines and
extends slightly beyond the distal border of the
eye. The small spine present on the antero-
ventral corners of the carapace in the preceding
substage is absent. The supraoi'bital spines are
now minute or absent. A pair of hepatic spines
and ocelli are present.

The inner branch of the first antenna is com-
posed of two segments, and the outer, three.
The statocyst at the base of the first antenna
is fully developed. The endopod of the second
antenna is composed of five or six frequently in-
distinct segments. The exopod bears 23 setae.

The mandibular palp is two-segmented and
possesses five setae.

The endopods of the first and second maxillae
have been reduced greatly and are now unseg-
mented and usually without setae. Setation of
the protopod of the second maxilla has been re-
duced while its exopod has become enlarged and
now bears 21 setae.

The first maxilliped retains only rudiments
of its endopod and exopod. The second and third
maxillipeds and the first pereiopod have lost all
but a vestige of their exopods. The endopod
of the second maxilliped has become recurved,
and its setation has changed greatly: the first
segment has three setae; the second, four; the
third, one; the fourth, five; and the fifth, six.
The second and third segments of the endopod
of the third maxilliped have each gained one
seta, the fourth, three; the number of setae on
the terminal segment varies from three to six.
The dactyl of the first pereiopod now possesses
several small teeth and short bristles terminally.

Each pleopod is composed of two segments,
the distal one bearing about 10 setae.

The presence of dorsomedian spines on the
third, fourth, and fifth abdominal segments is
variable. Such spines may be absent or present
on one or more of the segments. The midlateral
spines have been lost from the fifth and sixth
segments. The sixth segTnent retains a dorso-
median and paired ventrolateral spines.

The telson, which is now only faintly cleft,
bears five pairs of terminal and three pairs of
lateral spines.

COMPARISON WITH
PINK AND WHITE SHRIMP

During the fall of 1964, pink shrimp hatched
from eggs spawned in the laboratory were
reared to postlarvae. White shrimp were reared
during the summer of 1966. Examination of
these larvae showed them to be identical to
brown shrimp larvae in setation and other ma-
jor morphological characteristics. Various parts
of the body were measured to determine if body
proportions differed between the species; the
results proved inconclusive.

Dobkin (1961) described the larval develop-
ment of the pink shrimp but was absolutely
certain only of the identity of the nauplial and
first protozoeal substages which he obtained
from eggs hatched in the laboratory. Descrip-
tions of the more advanced stages were based
on specimens sorted from plankton samples.
When the pink shrimp we had reared were com-
pared with the specimens described by Dobkin,
several diflferences were noted. These are listed
in Table 1.

Pearson (1939) and Heegaard (1953) de-
scribed the larval development of the white
shrimp from material taken in plankton tows.
Com]3arison of these descriptions and our spec-
imens was not attempted because we feel both
Pearson's and Heegaard's descriptions of the
later stages are not detailed enough for itemized
comimrison. In addition, Heegaard's editors felt
that his figures of the first and second protozoeae
were not referable to P. setiferus, but should be
attributed to Trachypenaeus, Sicyonia, or Xlph-
openaeus. From material at our disposal it

237

FISHERY BULLETIN: VOL. 69, NO. I

k.

0 1 MM

Figure 13. — Postlarva I: a, lateral view; b, antenna I; c, antenna II; d, mandibular palp; e, maxilla I;
f, maxilla II; g, maxilliped I; h, maxilliped II; i, maxilliped III; j, pereiopod I; k, tip of telson.

238

COOK, and MURPHY: DF.VELOPMENTAL STAGES OF BROWN SHRIMP

Table 1. — Comparison between published description of
P, duorarutn and specimens examined by authors

Substage and
body port

Nauplius 111
Antenna I

Caudal spines
Nauplius IV

Caudal spines
Nauplius V
Antenna I

Protozoea I
Antenna I

Protozoea II and 111

Antenna 1

Mysis

Sixth abdominal
segment

Protopod of uropod

Dobkin (1961)

Cook and Murphy

No mention of postero- A minute posteroloteral
loteral seta. spine may be present.

Three pairs.

Three or four pairs.

Two anterolateral and
no posterolateral
spines.

Five pairs.

Two posterolateral
setae.

Two or three anterolat-
eral spines. Minute pos-
teroloteral spine may be
present.

Six pairs.

Two or three postero-
lateral spines.

Five terminal and sub- Six terminal and sub-
terminal setae. No terminal setae. Middle
posterolateral seta on segment with short pos-
middle segment. terololeral seta.

Five terminal and sub- Seven terminal and sub-
terminal setae. terminol setae.

Two pairs of postero-
lateral spines.

Three spines on distal
margin.

One pair of posterolat-
eral spines.

Two spines on distal
margin.

would seem that the editors were correct and
that the figures presented are species of Trachy-
penaeus.

LITERATURE CITED

Cook, Harry L.

1966. A generic key to the protozoean, mysis, and
postlarval stages of the littoral Penaeidae of the
northwestern Gulf of Mexico. U.S. Fish Wildl.
Ser\'., Fish. Bull. 65(2) : 4.37-447.

1969. A method of rearing penaeid larvae for ex-
perimental studies. In M. N. Mitakidis (ed.).
Proceedings of the world scientific conference on
the biology and culture of shrimps and prawns,
FAO (Food Agr. Organ. U.N.) Fish. Rep. 57,
3: 709-715.
Cook, Harry L., and M. Alice Murphy.

1966. Rearing penaeid shrimp from eggs to post-
larvae. Proc. 19th Annu. Conf. Southeast. Ass.
Game Fish Comm., p. 283-288.

1969. The culture of larval penaeid shrimp. Trans.
Amer. Fish. Soc. 98(4): 751-754.
Dobkin, Sheldon.

1961. Early developmental stages of pink shrimp,
Penaeus duorarum, from Florida waters. U.S.
Fish Wildl. Serv., Fish. Bull. 61 : 321-349.
Heegaard, Poul E.

1953. Observation on spawning and larval history
of the shrimp, Pendens fseti ferns (L.). Publ. Inst.
Mar. Sci., Univ. Tex. 3(1) : 73-105.
Pearson, John C.

1939. The early life histories of some American
Penaeidae, chiefly the commercial shrimp, Penneus
setiferus (Linn.). Bull. U.S. Bur. Fish. 49(30):
1-73.

239

PROTEIN AUTOLYSIS RATES AT VARIOUS pH'S AND TEMPERATURES IN

HAKE, Merluccius productus, AND PACIFIC HERRING, Clupea harengtis pallasi,

AND THEIR EFFECT ON YIELD IN THE PREPARATION

OF FISH PROTEIN CONCENTRATE

Barbara Koury, John Spinelli, and Dave Wieg'

ABSTRACT

The rate of protein autolysis at temperatures ranging from 30° to 80° C and at pH's ranging from 3.0
to 7.0 were determined on hake and Pacific herring. Autolysis rates were generally greatest at acidic
pH's and began to decrease after temperatures exceeded 50° C. Autolysis rates were much greater in
hake than in Pacific herring. The yield of fish protein concentrate prepared from hake showed a close
inverse correlation to the degree of autolysis.

The production of fish protein concentrate
(FPC) requires a process that efficiently re-
moves oil and water from the fish and provides
high yields of protein. Although FPC can be
prepared by several different methods (Knobl,
1967), the most effective procedures developed
to date are based on systems in which commin-
uted fish is successively extracted with a suitable
solvent system.

Dambergs (1969), in studying the extracting
efficiency of isopropyl alcohol (IPA) -water mix-
tures in producing FPC from herring, found
that low molecular weight compounds were
readily removed with these solvent systems.
Fish flesh and viscera contain highly active ca-
theptic enzjTTies which utilize fish tissue as a
substrate, forming low molecular weight pro-
tein degradation products (Siebert, 1962; Ting,
Montgomery, and Anglemeier, 1968). Normal
autolysis of fish tissue during storage has been
related to decreased yields in FPC production.
Dubrow, Brown, Pariser, Miller, Sidwell, and
Ambrose (1971) found that when ice-stored fish
was u.sed to make FPC, the yield was signifi-

' ^rational Marine Fisheries Service Technological
Laboratoij, ''725 Montlake Boulevard East, Seattle,
Wash. 98102.

Manuscript received September 1970.

FISHERY BULLETIN: VOL. 69. NO. I, 1971.

cantly lower than the yield obtained when FPC
was prepared from freshly caught fish. In an-
other study by Dubrow and Hammerle (1969),
in which FPC was prepared from samples of
comminuted fish held in 91 ''r IPA for various
lengths of time, similar results were obtained.

Preliminary studies in this laboratory, on the
development of an aqueous process for FPC pro-
duction, indicated that under certain conditions
significant protein losses may also occur during
actual processing pi'ocedures as a result of en-
zymatic hydrolysis.

In solvent extraction procedures for FPC pro-
duction, the yield of product (excluding physical
losses) is dependent upon the amount of pro-
teinaceous material soluble in the extracting
solution. While losses can be controlled to some
extent by the choice of solvent systems, the
possibility of losses due to enzymatic degradation
of protein must also be considered.

The purposes of this study were as follows:

1. To determine the eflfect of pH, time, and
temperature on the rate of protein autolysis
in two species of fish that are considered for
use in the ijroduction of FPC.

2. To determine the effect of autolytic ac-
tivity on FPC yields.

241

FISHERY BULLETIN: VOL, 69, NO. I

PROTEOLYTIC ENZYME ACTIVITY IN

WHOLE AND EVISCERATED FISH

Presented in this experiment are data on the
effect of time, temperature, and pH on the rate
of proteolytic enzyme activity in samples of
whole and eviscerated comminuted fish.

MATERIALS AND METHODS

Fish

Hake, Merluccius productus, and Pacific her-
ring, Ciupea harengus pallasi, were used in this
study. Hake samples were obtained from both
coastal waters (outside hake) and Puget Sound
(inside hake). Herring were obtained from
Bellingham Bay. All samples were obtained
fresh and were immediately frozen and held at
—20° C.

Preparation of Samples

To insure sample homogeneity, lots of fish
were partially thawed and then ground in a Ho-
bart grinder' through a Vs-inch plate. The
ground fish was mixed well and divided into
portions of approximately 50 g each. These
were frozen to — 40° C in a plate freezer and
stored at —20° C.

Sufficient comminuted fish was prepared to
permit running all pH and temperature vari-
ables on subsamples from the same lot. Samples
of herring and outside hake were prepared from
both whole and eviscerated fish. With inside
hake, autolj-lic rates were measured only on
whole fish.

METHODS

Fifty grams of comminuted fish were allowed
to thaw at room temjierature and then were
mixed well with 100 ml of H2O to form a slurry.
The pH of the slurry was adjusted to the de-
sired level with 0.1 M HCl and then sufficient
water was added to give a final volume of 250
ml. After dilution, the sample was placed in
a water bath.

' The use of trade names is merely to facilitate de-
scriptions; no endorsement is implied.

Aliquots of the slurry were taken (1) imme-
diately after the final dilution was made, (2)
when the sample reached the desired temper-
ature, and (3) at intervals of 10, 20, 30, and 60
minutes after the sample reached the desired
temperature. These aliquots were mixed im-
mediately with an equal volume of 10% TCA,
allowed to stand for 30 min, and then filtered.
The nonprotein nitrogen (NPN) content of the
filtrates was determined by the procedure of
Lowry, Rosebrough, Farr, and Randall (1951)
and is presented in terms of optical density
(OD) measurements at 500 m^.

Rates of proteolytic enzyme activity at pH
6.0, 5.0, 4.5, 4.0, and 3.0 were measui'ed at tem-
peratures of 30°, 40°, 50°, 60°, 70°, and 80° C.
Controls consisted of samples in which no pH
adjustment had been made.

RESULTS AND DISCUSSION

The results of the above experiments are
shown in Figures 1 through 5.

In whole herring (Fig. 1), no significant de-
gree of proteolytic enzyme activity was observed
at pH levels higher than pH 5.0 over the temper-
ature range studied. At pH 4.0-4.5, maximum
activity was found at 40° C, and at pH 3.0, max-
imum activity was found at 30° C.

Under these experimental conditions, only
negligible proteolytic enz.\'me activity was ob-
served in eviscerated herring .samples (Fig. 2)
indicating that in herring proteolytic enzymes
are essentially of visceral origin.

Figures 3 and 4 show the results of the ex-
periments using whole inside and outside hake.
At 30° C, the rate of proteolytic activity in both
control samples was negligible. As the pH was
lowered, the rate of activity increased. At 40° C,
the rate increased at all iiH levels, and these
rates remained elevated until the temperature
exceeded 60° C. In the.se two samples, differ-
ences were observed in the pH of optimum ac-
tivity at various tenijiei-atures. These variations
were attributed to difl'erences in the age, feeding
habits, etc., of the two populations.

The eflE'ects of pH and temperature on the rate
of enzyme activity in eviscerated outside hake

242

KOURY. SPINELLI, and WIEG: PROTEIN AUTOLYSIS RATES

TEMPERATURE
400r '0°'^

TEMPERATURE
40°C

TEMPERATURE
50°C

TEMPERATURE
300r 60° C

200

20 30 40
TIME ( MIN )

TEMPERATURE
70° C

20 30 40
TIME (MIN.)

4,0
50

163

MO

TEMPERATURE
80°C

20 30 40
TIME (MIN)

Figure 1. — Protein autolysis rates of whole herring homogenates held at various pH's and temperatures.

40

45

30

!50

re.e

50 60

TEMPERATURE
30-0

TEMPERATURE
40- C

TEMPERATURE
50° C

TEMPERATURE
60°C

20 30 40
TIME (MINI

TEMPERATURE
70°C

10 20 30 40
TIME (MIN 1

TEMPERATURE
80° C

10 20 30 40
TIME (MIN.)

30

50

45

■ 40

(67

50 60

Figure 2. — Protein autolysis rates of eviscerated herring homogenates held at various pH's and temperatures.

are shown in Figure 5. The pattern is similar
to that of whole hake, both in magnitude of ac-
tivity and the effects of pH and temperature.
Previous investigations in this laboratory (Das-
sow, Patashnik, and Koury, 1970) have shown
that hake is often infected with the parasite,
myxosporidian. The degree of this infestation
is much greater in the outside than in the inside

hake (Patashnik, personal communication,
1970) . These investigators reported that infest-
ed hake autolyze rapidly during storage, mak-
ing them unsuitable for processing into blocks
or poi'tions. No detailed study relating to par-
asites was made in this study, but the similar
autolytic rates between whole and eviscerated
outside hake shows that the main source of pro-

243

FISHERY BULLETIN: VOL. 69. NO. 1

TEMPERATURE
30° C

TEMPERATURE
40° C

TEMPERATURE
50°C

JOOr

TEMPERATURE
60°C

20 30 40
TIME IMIN.)

TEMPERATURE
70° C

TEMPERATURE

eo°c

20 30 40
TIME (MIN.)

Figure 3. — Protein autolysis rates of whole hake (outside) homogenates held at various pH's and temperatures.

TEMPERATURE
30°C

TEMPERATURE
40" C

TEMPERATURE
50° C

300

O 100

m

< 300

TEMPERATURE

r- 60°C

z

< 200

-

^

100

^^^^

___^

10 20 30 40
TIME (MINI

5.0
40
" 9

TEMPERATURE
70°C

20 30 40
TIME IMIN)

TEMPERATURE
80°C

20 30 40
TIME ( MIN 1

Figure 4. — Protein autolysis rates of whole hake (inside) honioRenates held at various pH's and temperatures.

teolytic enzyme in the outside hake taken for
this study resides in the tissue.

EFFECT OF AUTOLYTIC ACTIVITY
ON YIELD OF FPC

MATERIALS AND METHODS

Whole inside hake wei'e used throughout this
experiment. For the preparation of FPC, whole

hake was comminuted by passing through a Ho-
bart grinder (equipped with a i ..-inch plate).
Aliquots of the comminuted fish were acidified
with 0.1 M HCl to pH 5.5 and 4.5. The original
pH of the fish was 6.9. The treated fish was
allowed to autolyze at 50° C for 0, 20, 40, and
60 min. After each time interval, FPC was pre-
l)ared by isopropanol (IPA) extraction as fol-
lows: The fish was successively extracted (4

244

KOURV. SPINELLI, and WIEG: PROTEIN AUTOLYSIS RATES

TEMPERATURE
30°C

TEMPERATURE
40°C

TEMPERATURE

sec

200

TEMPERATURE
60°C

10 20 30 40
TIME (MIN)

TEMPERATURE
70°C

20 30 40
TIME (MIN)

TEMPERATURE
80°C

20 30 40
TIME (MIN)

Figure 5. — Protein autolysis rates of eviscerated hake (inside) homogenates held at various pH's and temperatures.

times) with azeotropic IP A at a ratio of 2 parts
IPA to 1 part fish. The first extraction was
carried out at ambient temperature, and the
final three extractions were carried aut at 70° C.
Yields were calculated after drying the fish
solids for 16 hr at 70° C at 25 inches of vacuum.

RESULTS AND DISCUSSION

The effect of autol.\i;ic activity on the sub-
sequent yield of FPC is shown in Figure 6. It
can be seen that while the acidified samples
showed the greatest loss of yield with time of
autolysis, the largest yield losses occurred dur-
ing the first 20 min. The pH values, time, and
temperature were arbitrarily chosen to simply
demonstrate the effect of autolysis with respect
to yield. They do, however, show a close cor-
relation with the autolysis data shown in the
previous experiment. For example, in refer-
ring to Figures 1 through 5, it can be seen
that the rate of NPN formation is greatest dur-
ing the first 20 min regardless of pH and tem-
perature. Several investigators (Whaley, 1966;
Sen, Sayanarayana Rao, Kadkol, Krishnaswamy,
Venkata Rao, and Lahiry, 1969) have proposed
acidifying comminuted fish prior to processing
without taking into account the effect of protein
losses due to autolysis. The combined exper-

iments presented here clearly demonstrate the
need to control temperature and pH, both before
and during processing.

SUMMARY AND CONCLUSIONS

The above study shows that the endogenous
proteolytic enzymes in fish hydrolyze the pro-
teins into subunits that are not coagulable by

Figure 6. — Effect of protein autolysis on the yield of
PFC made from inside hake. Autolysis was allowed
to proceed for 0, 20, 40, and 60 min at 50° C prior to
preparation of FPC.

245

FISHERY BULLETIN, VOL. 59, NO. I

the isopropanol concentration normally used in
the preparation of FPC. The preparation of FPC
made from autolyzing hake showed that the
yield bore a close inverse relation to the degree
of autolysis.

The autolysis rates in Pacific herring and
hake were related to pH and temperature, the
rates showing an increase with increasing tem-
perature and a decreasing pH. Maximum ac-
tivity was reached at about 50° C. Inactivation
of the enzymic systems occurred when temper-
atures exceeded 70° C.

Since the economic success of any method that
is used for the preparation of FPC is largely de-
pendent on the yield of finished product obtained
from a given amount of raw material, autolysis
rates are a process parameter that should be
closely controlled.

LITERATURE CITED

Dambergs, N.

1969. Isopropanol-water mixtures for the pro-
duction of fi.sh protein concentrate from Atlantic
herring (Clu.i>ea hnrengns). J. Fish. Res. Bd.
Can. 26(7) : 1919-1926.

Dassow, John A., Max Patashnik, and Barbara J.

KOURY.

1970. Characteristics of Pacific hake (Merluccius
productuts) that effect its suitability for food.
In Pacific hake, p. 127-136. U.S. Fish Wildl.
Serv., Circ. 332.

DuBRow, David L., Norman L. Brovi'N, E. R. Pariser,
Harry Miller, Jr., V. D. Sidwell, and Mary E.
Ambrose.

1971. Efl'ect of ice storage on the chemical and
nutritive properties of solvent-extracted whole
fish — red hake, Urophycis chuss. Fish. Bull. 69
(1) : 145-150.
DuBROw, David, and Olivia Hammerle.

1969. Holding raw fish (red hake) in isopropyl
alcohol for FPC production. Food Technol. 23 (2) :
254-256.
Knobl, George M., Jr.

1967. The fish protein concentrate story. Food
Technol. 21(8) : 1108-1111.

LowRY, Oliver H., Nira J. Rosebrough, A. Lewis Fakr,

AND Rose J. Randall.
1951. Protein measurement with the folin phenol

reagent. J. Biol. Chem. 193(1): 265-275.
Sen, D. p., T. S. Sayanarayana Rao, S. B. Kadkol,

M. A. Krishnaswamy, S. Venkata Rao, an-d

N. L. Lahiry.
1969. Fish protein concentrate from Bombay-duck

(Harpoden nehereus) fish: Effect of processing

variables on the nutritional and organoleptic

qualities. Food Technol. 23(5): 683-688.

SlEBERT, G.

1962. Enzymes of marine fish muscle and their role
in fish spoilage. In Eirek Heen and Rudolf
Kreuzer, Fish in nutrition, p. 80-82. Fishing News
(Books) Ltd., London.
Ting, Chao-titin, M. W. Montgomery, and A. F.
Anglemeier.

1968. Partial purification of salmon muscle cath-
epsins. J. Food Sci. 33(6): 617-620.

Whaley, Wilson M.

1966. Production of fish proteins. U.S. Patent
No. 3,252,962.

246

NOTES

EQUIPMENT FOR HOLDING AND

RELEASING PENAEID SHRIMP

DURING MARKING EXPERIMENTS'

Personnel of the National Marine Fisheries
Service Biological Laboratory at Galveston,
Texas, have conducted numerous mark-recap-
ture ex]3eriments to obtain information on the
movement, growth, and mortality of penaeid
shrimp. These experiments were carried out
under a variety of conditions at sea and in coastal
bays. Several types of specialized equipment
were developed to overcome problems of holding,
handling, and releasing shrimp during the mark-
ing phase of these experiments. Some of this
equipment has been described previously by
Costello (1964). Holding tanks, a cooling unit,
and two devices used to transport shrimp to the
sea floor are described here.

Holding Facilities

A number of factors were considered in the
design of tanks for holding shrimp. Construc-
tion materials had to be relatively light in weight,
require little maintenance, and be nontoxic to
shrimp. Provisions also were needed to permit
lapid water exchange, minimize water turbu-
lence within tanks, and control water temper-
ature. The tank design in Figure 1 meets these
needs and has proved successful for both sea-
and land-based operations. It is constructed of
light gray fiberglass with wood reinforcement
and weighs about 114 kg (250 lb.) . Advantages
of the light color are that it reflects heat and
makes shrim]) easily visible in the tank. To
permit rapid drainage or water exchange, a
polyvinyl chloride (PVC) pipe, 7.6 cm (3 inch-
es) in diameter, is molded into each end of the
tank near the bottom. Filter .screens, used to

' Contribution No. 304, National Marine Fisheries
Service Biological Laboratory, Galveston, Texas.

prevent loss of shrimp in outflowing water, have
a large surface area to minimize clogging. A
one-quarter section of PVC pipe, 7.6 cm (3
inches) in diameter, is molded to the top of the
tank at each end as a splash rail to reduce
spillage.

Five sets of guides in the tank support baffles
that reduce water turbulence at sea and are used
to separate groups of shrimp in a tank (Fig. 1).
The baffles have a frame of aluminum flashing
covered with sheets of patterned aluminum
0.063 cm (0.025 inch) thick.

During field use, a series of two to four tanks
are linked to provide either recirculating water
or continually flowing new water. The pump
used depends on the volume of water required.
Normally, we use a cast-iron pump powered by
a 0.5-hp electric motor (110-220 v) that dis-
charged 114 to 132 liters (30 to 35 gal) per min.
As the water is discharged into the tanks, it
passes through siphon filler-drain nozzles (Cos-
tello, 1964) which draw air into the circulation
system and aerate the water. The aeration unit
(Fig. 2), made of 1.9-cm (0.75-inch) pipe, may
be attached temporarily at any convenient place
on the tank. The amount of air that enters the
water is regulated by valves in each air line.

Because it is difficult to keep shrimp alive
when water temperatures exceed about 27° C
(80° F), cooling units are used to lower and
maintain temperatures in holding tanks. A
cooling unit of our own design is shown in Fig-
ures 3 and 4. The casing consists of a PVC
pipe, 25.4 cm (10 inches) inside diameter, 45.7
cm (18 inches) long, and 0.9 cm (0.37 inch),
thick, and top and bottom pieces of PVC flat
stock, 30.5 by 30.5 by 1.3 cm (12 by 12 inches
by 0.5 inch) with circular grooves 0.6 cm (0.25
inch) deep. 0-ring gaskets that fit the grooves
prevent leakage of water. The refrigerant coil
is made from 0.9-cm (0.37-inch) diameter stain-
less steel tubing, 9 m (30 ft) long. A thei-mo-
stat sensor receptacle, inserted through the top

247

Figure 1. — The holding tank, baffles, and filters used in shrimp marking experiments.

Figure 2. — Aeration unit and siphon filler-drain nozzle
through which water enters tank.

plate of the cooling tank, consists of a piece of
0.6-cm (0.3-inch) diameter stainless steel tubing,
20.3 cm (8 inches) long, and is sealed at one
end. The top of the chilling tank is reinforced
by a 30.5 by 30.5 cm (12 by 12 inches) frame
made from angle aluminum stock 3.8 by 3.8 by
0.6 cm (1.5 by 1.5 inches by 0.25 inch).

Two experiments were completed to deter-
mine the cooling capability of the unit. Water
was recirculated through the chilling unit at
rates of 114 to 132 liters (30 to 35 gal) per
min, and thermographs recorded water and air
temperatures (Fig. 5). The temperature at-
tained after 24 hr was about 15.6° C (60° F)
and was lower than that required for shrimp-
marking procedures. Field observations have
indicated that water temperatures can be main-
tained within 2° C (4° F) of desired levels, ir-
respective of fluctuations in air temperatures.

A table top with plastic pans 33.0 cm (13 inch-
es) long, 38.1 cm (15 inches) wide, and 13.97
cm (5.5 inches) deep equipped for continuous
water circulation (Fig. 6) slides over the lip
of the holding tank and extends about 5 cm (2
inches) beyond the ends of the tank. When in

248

^ «r

'L^.

NUT '
WASHER - 5

Figure 3. — One-hp single-pliase cunipressor and con-
densing unit (12,000 BTU factory rated) attached to
a PVC chilling tank and mounted on angle iron stand.
A. vibration joint; B. expansion valve; C. thermostat
control; D. compressor; E. sight glass; F. dryer; H.
condensing unit; J. chilling tank; K. angle iron stand.

place, the table tojj serves as a work area for
staining and tagging shrimp which are held in
the pans.

Equipment for Releasing Shrimp

Three types of release devices have been de-
veloped to protect shrimp from exposure to pre-
dation during their return to the sea floor. Cos-
tello (1964) described a release box that is low-
ered to the bottom with a winch and opened by

Figure 5. — Reduction of water temperatures in a 1,892-
liter (500-gal) tank compared to surrounding air tem-
peratures during trials with the chilling unit.

£ ALUMINUM SUPPORT

COIL INLET

STAINLESS STEEL
ROD-

2S4 CM PVC PIPE— -
(10 IN I

PVC TOP PLATE

STAINLESS STEEL ROO

PVC BOTTOM PLATE

/

FlGiniE 4. — Details of the chilling tank assembly.

— 1 — I — I — r-

249

PLASTIC PAN
330>3e II 13 9 CM
(13115x550 IN )

I 9 CM PLVWOOO
(0 75 IN )

0 3 CM PLASTIC CONNECTION (0 12 IN )

TUBING CLAMP

PLASTIC "T"

Figure 6. — Removable table top and holding pans
equipped for continuous water circulation.

a messenger dropped down the cable. Use of
this device is restricted to large vessels equipped
with a winch, and requires that the vessel be
stopped when shrimp are released. To circum-
vent these requirements, we designed an ex-
pendable release canister that can be put over-
board while a vessel is underway and a release
tube for use in shallow water.

The canister (Fig. 7) is constructed of high-
impact styrene plastic formed into a hollow cyl-
inder. Tabs on each of the styrene plastic end
pieces have holes to accommodate retaining rods

used in assembling the canister. Assembly and
loading are accomplished in a cradle attached
to the inner wall of a holding tank so that shrimp
will remain submerged until the canister is
ready to be put overboard. Slots in the canister
allow it to fill with water.

A salt block, a rubber band, and a paper clip
constitute the release mechanism. This mech-
anism is set by folding together the two ends of
the styrene plastic sheet (thus forming a cyl-
inder) and securing them with a rubber band.
When ends A and B (see canister. Fig. 7) are
folded, the paper clip is inside the canister with
the attached rubber band inserted through a
hole (end A) and a slot (end B). The salt
block is then inserted in the loop formed by
the rubber band, and the retaining rods are
removed.

A cement weight (1.1 kg or 2.5 lb.) is attached
and the canister is lowered to the water surface
and released. When the salt block dissolves,
tension in the canister wall pulls the rubber band
from the slot (end B) and the canister disas-
sembles, releasing the shrimp. Although never
obsen-ed during the actual release of shrimp in
offshore waters, this release devise was tested
in shallow estuarine waters and in the labora-
tory. In all tests it performed as expected. The
canister accommodates up to 100 shrimp that

CANISTER ENDS

r76CM (3IN )

r*4^

(0 03 IN)
-008 CM Thick

ASSEMBLY OF CANISTER
B

SALT BLOCK,

06 CM (0 25 IN) ^^
11.4 CM (4 SO IN j

81.3 CM

(32 IN)

CANISTER SIDE

ASSEMBLED
CANISTER
WEIGHT

Figure 7. — Disposable release canister showing release mechanism, loading cradle, and

method of assembly.

250

are released on the sea bottom within 5 to 15
min from the time the unit enters the water,
depending on the size of the salt block.

The release tube (Fig. 8), intended for use
in shallow water, consists of two telescoping
aluminum pipes, each about 3 m (10 ft) long.
To release shrimp, the outer pipe is lowered to
the bottom and shrimp are poured from a pail
into the funnel. After each pail of shrimp is
poured into the unit, the apparatus is flushed
with several pails of water to insure that shrimp
do not remain in the tube. The pouring and
flushing of one pail of shrimp usually take about
1 min.

The new equipment described herein and the
improved techniques for staining and tagging
described by Neal (1969) enabled us to hold.

(lOIN )

FUNNEL

TELESCOPING
ALUMINUM PIPES

LINE FOR
LOWERING '

12 7 CM
5 InT

3 1 M (10 FT)

mark, and release large numbers of shrimp.
We can now process between 1,500 and 3,000
shrimp per day, depending on the type of mark
used.

Literature Cited

COSTELLO, T. J.

1964. Field techniques for staining-recapture ex-
periments with commercial shrimp. U.S. Fish
Wildl. Serv., Spec. Sci. Rep. Fish. 484, 13 p.
Neal, Richard A.

1969. Methods of marking shrimp. FAO (Food
Agr. Organ. U.N.) Fish. Rep. 57, 3: 1149-1165.

Dennis A. Emiliani

National Marine Fisheries Service
Biological Laboratory
Galveston, Texas 77550

AN ADULT BLUEFIN TUNA, Thunnus thynnus,

FROM A FLORIDA WEST COAST

URBAN WATERWAY'

The bluefin tuna, Thunnus thymius (Linnaeus),
is a wide-ranging pelagic species occurring in
most tropical and temperate seas (Gibbs and
Collette, 1966: 119). In the Gulf of Mexico
exploratory and commercial catches have been
limited to the northern, western, and central
parts, from waters beyond the continental shelf.
The collection of a large adult from the Florida
west coast represents a new record for the Flor-
ida shelf.

The specimen, a female, was captured by local
fishermen with harpoons in a waterway at
Hudson, Fla., (lat 28°21'24" N, long 82°42'42"
W) on 10 May 1970. It weighed 239 kg (525
lb.), was 244 cm (96 inches) in fork length and
168 cm (66 inches) in girth, and appeared to
be in healthy but lean condition, characteristic
of post-spawning fish in May on the Bahama
Banks (Rivas, 1955: 139).

Histological examination of gonadal tissue
sectioned at 6 ,u, and stained with Harris hema-
toxylin and Eosin Y showed early and late atretic

Figure 8. — Release tube used to place marked shrimp
on the bottom.

' Contribution No. 154.

251

body formations, indicating recent spawTiing.
The stomach contained a mussel, Brachidontis
recurv2is (Rafinesque), a piece of marl (no
doubt ingested accidentally), and a digenetic
trematode ; gills and other tissues were free of
parasites.

The fish had entei'ed the waterway through
a shallow navigation channel from the adjacent
grass flats. The waterway, a network of chan-
nels cut through marl, consists of several 161 m
by 15 m "fingers" branching from a 1370 m by
22 m central channel, with depths averaging less
than 5 m at low tide. Surface salinity in the
waterway, tested at a sub.^equent low tide, was
27.0 '/i,; surface temperature in the adjacent
Gulf was 26° C.

This occurrence, although admittedly irreg-
ular, may help to fill a gap in our emerging
picture of the origin and distribution of Gulf of
Mexico bluefin tuna stocks.

Bluefin tuna are taken from the Greater
Antilles in spring, with substantial numbers of
large adults being reported from the Windward
Passage in April (Bullis, 195.5: 6) . During May
they begin their dramatic migration through
the Straits of Florida toward the summer feed-
ing grounds (Rivas, 1954, 1955).

The occurrence of large bluefins at Grand
Cayman and east of Cozumel in April (Bullis
and Mather, 1956: 9) suggests that at least
a component of these Cariljbean stocks may
undertake a similar northward movement
through the Yucatan Straits and into the Gulf
of Mexico. The occurrence of ripe or nearly
ripe females in the Gulf in May and of small
juveniles (less than 8 cm) in the northern Gulf
in late May and early June (Mather, 1962: 5)
implies that these stocks sjiawn in the Yucatan
Straits or in the Gulf of Mexico proper. Our
spent female on the Florida shelf could be from
the Caribbean stock or from a stock wintering
in the Gulf (Bullis, 1955: 13; Wathne, 1959: 16).

We are indebted to Gordon D. Marston, St.
Petefsburrj Times, for informing us of the in-
cident, to Bud and Marvin Mattix and others
for allowing us to examine the fish and viscera,
to Richard B. Roe for providing information on
specimens collected during exploratory fishing

by U.S. Fish and Wildlife Service vessels in the
Gulf of Mexico and Caribbean, to Alice Gennette
for preparing histological sections, and to Frank
J. Mather, III for critically reviewing the man-
uscript.

Literature Cited

Bullis, Harvey R., Jr.

1955. Preliminary report on exploratory long-line
fishing for tuna in tlie Gulf of Mexico and the
Caribbean Sea. Part I - Exploratory fishing
by the Oregon. Commer. Fish. Rev. 17(10) : 1-15.

Bullis, Harvey R., Jr., and F. J. Mather, III.

1956. Tunas of the genus Thunnus of the northern
Caribbean. Amer. Mus. Nov. 1765, 12 p.

GiBBS, Robert H., Jr., and Bruce B. Collette.

1966. Comparative anatomy and systematics of the
tunas, genus Thunnus. U.S. Fish Wihil. Serv.,
Fish. Bull. 66(1) : 65-130.
Mather, Frank J., III.

1962. Distribution and migration of North Atlantic
bluefin tuna. Proc. 7th Int. Game Fish Conf.
Pap. 6, 7 p.
Rivas, Luis Rene.

1954. A preliminary report on the spawning of
the western north Atlantic bluefin tuna (Thunnus
thynmis) in the Straits of Florida. Bull. Mar.
Sci. Gulf Carib. 4(4): 302-322.

1955. .A comparison between giant bluefin tuna
(Thunnus thynnus) from the Straits of Florida
and the Gulf of Maine, with reference to migra-
tion and population identity. Proc. Gulf Carib.
Fish Inst., 7th Annu. Sess., p. 133-149.

Wathne, Fredrick.

1959. Summary report of exploratory long-line
fishing for tuna in the Gulf of Mexico and Car-
ibbean Sea, 1954-1957. Commer. Fish. Rev. 21 (4) :
1-26.

Robert W. Topp and
Frank H. Hoff

Florida Department of Natural Resources
Marine Re.iearch Laboratory
Sf. Petrrshurg, Fla. 337.31

252

SWIMMING SPEED, TAIL BEAT FREQUENCY, TAIL BEAT AMPLTrUDE,

AND SIZE IN JACK MACKEREL, Trachurns symmetric^

AND OTHER FISHES

John R. Hunter and James R. Zweifel'

ABSTRACT

The tail beat frequency and tail beat amplitude of jack mackerel, Trachnrus symmetricus, 4.5 to 27.7
cm were measured at speeds of 15 to 212 cm/sec. Tail beat amplitude was a constant proportion of
length at all speeds but tail beat frequency changed with speed; thus speed depended only on fre-
quency of the tail beat an<l length. A simple mathematical model for estimating swimming speed from
tail beat frequency and fish length was derived from the Trachurus data and applied to data for three
marine fish — Scomber jnponicus, Triakis henlei, and Sardinops sagax — and to data for freshwater
fish from the literature. The general form of the model was V — Vg = L(KF — Fg) where V is fish
speed, V'o is length-dependent minimum swimming speed at minimum tail beat frequency F„, and L is
fish total length. The model represented a major improvement over previous equations because it
provided an unbiased correction for length, was sensitive to specific diff'erences, and provided a more
accurate estimation of speed.

Of the variables that determine the swimming
speed of a fish, the size of the fish, the frequency
of the tail beat, and the amplitude of the tail
beat are among the most important. Knowl-
edge of the relationships between swimming
speed and these variables is important not only
for an understanding of the mechanism of lo-
comotion in fish but because it may be used to
forecast maximum swimming speeds (Bain-
bridge, 1958) , to estimate swimming speeds
indirectly by analysis of tail beat frequencies,
and possibly to estimate fish size and make spe-
cific identifications of fish targets with doppler
Continuous Transmission Frequency Modulated
sonar (Hester, 1967).

Bainbridge (1958) described the relationship
between tail beat frequency, tail beat amplitude,
and size for three species of freshwater fish:
dace, Leiiciscus leuciscus; trout, Salmo gairdneri
(S. irideus); and goldfish, Carassiiis auratus.
He concluded that the amplitude of the tail beat
increased with the tail beat frequency to about
5 tail beats/sec and thereafter became constant.

' National Marine Fisheries Service Fishery-Ocean-
ography Center, La Jolla, Calif. 92037.

Manuscript received January 1971,

FISHERY BULLETIN: \0L. 69. NO. 2. 1971.

Speeds above 5 beats/sec were dependent only
on the frequency of the tail beat and the length
of the fish. The relationship between speed,
frequenc.v, and length above 5 beats, sec was
nearly the same in the three species studied;
consequently, he used a single equation to ex-
press this relationship for all three species. No
similar study exists for marine fish although
some measurements of tail beat frequency and
amplitude have been made incidental to other
studies. Yuen (1966) measured the tail beat
frequency of ski])jack tuna, Katsuivomis pelamis,
and yellowfin tuna, Thmmus albacares, from
cine photographs taken from the viewing port
of a research vessel and Magnuson and Prescott
(1966) measured the tail beat frequency of
Pacific bonito, Sarda chiliensis, from cine pho-
tographs taken through a window in an ocean-
arium. The slopes of the lines relating tail
beat frequency to speed in body lengths per sec-
ond for skipjack and yellowfin tunas and bonito
were sufficiently different from those of Bain-
bridge (1958), for Hester (1967) to speculate
that species might be identifiable by this re-
lationship. The measurements were taken from
lateral photographs of free-swimming schools;
thus the tail beat amplitude and the absolute

253

FISHERY BULLETIN: VOL. i'). NO. 2

size of the fish were not measured and tail beat
frequency was measured over a limited speed
range. Fierstine and Walters (1968) measured
both tail beat frequency and amplitude of wavy-
back skipjack, Euthynnus affinis, from dorsal
cine photographs of free-swimming fish in cir-
cular swimming pools but only five, one-beat se-
quences of swimming were analyzed.

The objective of the present .study was to de-
termine the relationships between swimming

speed, fish length, tail beat amplitude, and tail
beat frequency in a pelagic marine fish, jack
mackerel, Trachurus symmetricus. To accom-
plish this objective, dorsal cine photographs were
taken of fish swimming in currents of different
speeds in a specially designed activity chamber.
For comparative purposes tests were also run
on three other marine fish: chub mackerel,
Scomber japovicns; Pacific sardine, Sardinops
sagax; and a shark, Triakis henlei.

Figure 1. — .'Vpparatu.s used to measure .swimming speeds of fishes. Inset upper left apparatus shown with
opaque walls; center, isometric, three dimensional scale drawing, walls, deflectors and other structures are shown
as transparent for purposes of illustration; arrows indicate direction of current flow; and lower right, scale
for vertical and horizontal planes of drawing.

254

HUNTER and ZWEIFEL: SWIMMING SPEED AND TAIL BEAT FREQUENCY

APPARATUS

Swimming speeds were measured in an ac-
tivity chamber (Figure 1) built after that of
Beamish ( 1966) . A fiber glass tube 230 cm long
and 41 cm in diameter was immersed in an open
bath. An 80-cm section of tube was the swim-
ming compartment. The compartment had
metal screens at the ends and a transparent
acrylic plastic hatch which conformed to the
contours of the tube. The walls of the tube
within the swimming compartment were white
and had black stripes spaced at 5.0-cm intervals
to provide a visual reference for the swimming
fish. Water velocity in the chamber was reg-
ulated by the speed of a 39-cm propeller driven
by a variable speed 50-hp motor and by changing
the screens at the two ends of the swimming
compartment. Water was drawn into the com-
partment from the bath over deflectors, and
through baffles and screens. The screens, bafiles,
and deflectors i-educed tui-bulence and provided
water of relatively uniform velocity throughout
the swimming compartment. Their arrange-
ment and design were determined empirically
by measurement of the horizontal and vertical
distribution of flow in the chamber.

The speed range of the apparatus was 12 to
212 cm/sec. The full range was obtained by
changing the screens at the ends of the swim-
ming compartment. A velocity range of 12 to
69 cm/sec was obtained when screens of 39%
open area were used, one of 15 to 139 cm/sec for
screens of 56 Sr open area, and one of 19 to 212
cm 'sec for screens of 15'','r open area.

A digital voltmeter measured to the nearest
millivolt the voltage produced by a voltage gen-
erator attached to the propeller shaft. The volt-
age produced by the generator was proportional
to propeller revolutions and was used to regulate
them. An impeller flowmeter (Marine Advisers
Inc., Model B-7C)" was used to relate propeller
revolutions in volts to water flow in the appa-
ratus. The meter sampled an area 7.6 cm in
diameter and had an accuracy of ± 2.5 cm/sec
when moved through static water at a known

^ Reference to commercial products does not imply
endorsement.

speed (for a description of the meter and a cal-
ibration curve see Olson, 1967).

Propeller revolution was related to water
speed in the chamber by three series of cali-
brations, one for each of three screen types used.
Nine to 19 difl'erent speed levels were measured
in each series of calibrations. More levels were
required for slow speed ranges than for fast
ones because the response of the flowmeter was
nonlinear at low speeds. At each level water
speed was measured at 12 different radial po-
sitions midway in the swimming compartment.
The speed of the water at a given level was the
average of the 12 measurements, adjusted for
the extent of the area sampled by the meter
(Tranter and Smith, 1968). Variation among
the 12 sampling points did not exceed ±10%
of the mean speed and was usually much lower.
The relationship between mean water speed in
the chamber and propeller revolutions was li-
near, and the error in estimating the mean water
speed from revolutions did not exceed ± 0.2
cm/sec. Thus, the principal sources of error
in estimating the speed of the water in which
a fish swam were the possible 10 '^r variability
in flow within the chamber and the ± 2.5 cm/sec
accuracy of the flowmeter.

Fish swimming in the compartment were as-
sumed to be swimming at the mean speed of
the water in the compartment. They were
photographed from above with a 16 mm high-
speed motion picture camera at speeds of 64 to
200 fps. Camera speed was adjusted to pro-
vide about 10 frames per complete tail beat. A
viewing box floated on the water surface above
the swimming compartment to eliminate distor-
tion in the photographs caused by ripples.

METHODS

Film was analyzed by use of a coordinate
reader and digitizer (Hunter, 1966) and a com-
puter program was used to calculate tail beat
frequency and tail beat amplitude from the
digitized information. One tail beat was one
complete oscillation of the tail, and the tail beat
frequency was the number of beats per second.
Tail beat amplitude was the distance in centi-
meters between the lateral most excursion of

255

FISHERY BULLETIN: VOL. 69, NO. 2

the tip of the tail measured perpendicular to the
axis of progression plus the mirror image of
that measurement on the other side of the axis
of progression.

The film sequences selected for analysis were
usually ones in which the fish held a constant
position in the current and swam steadily. Oc-
casionally at higher speeds it was not possible
to obtain such a sequence because the fish did
not maintain a constant position but rather ac-
celerated and decelerated. In this case a se-
quence was chosen in which no net movement
existed between the beginning and end of the
sequence although the fish moved slightly for-
ward and backward within the sequence. Usu-
ally 5 complete tail beats were analyzed per
speed level but occasionally as few as 2.5 and
as many as 11 were analyzed.

Sixteen speed levels were used in the exper-
iments; seven of the levels, 15 to 60 cm/sec,
were graduated at intervals of 25''r of the pre-
ceding level and nine of the levels, 69 to 212
cm/sec were graduated at intervals of 15%. A
speed level interval greater than 10% was used
because of the possible 10 "^f variability in flow
within the swimming compartment.

A grand total of 176 speed tests was analyzed
for 14 jack mackerel, varying in total length
from 4.5 to 27.7 cm. Owing to the diflTerences
in length, no fish was able to swim at all levels.
All 14 fish swam at five levels, 24, 30, 38, 48,
and 60 cm sec, and all but the two smallest fish
swam at the next five higher levels, 79, 91, 105,
121, and 139 cm^sec. Only fish of 16 cm or
larger were tested at speeds above 139 cm sec
and only those less than 16 cm were tested at
15 cm/sec.

Other species were tested for comparative
])urposes but fewer observations were made.
Seventy-four swimming sequences of five Scom-
ber, 26.3 to 32.2 cm total length, were analyzed,
nine sequences of five Sai-dinops, average length
13.6 cm, and seven sequences of one Triakia,
23.6 cm.

All fish were tested singly except for Sardi-
nops, which was tested in a group of five. Fish
were held in the swimming compartment at a
low speed for about 30 min before an experi-

ment began. Seawater temperature ranged
from 17.0° to 19.5° C among experiments but did
not vai-y over a degree within an experiment.

RESULTS

The tail beat amplitude of Trachurus did not
change with speed but was constant at all speed
levels and was directly related to length (Fig-
ures 2 and 3) . Tail beat frequency, on the other

VELOCITY (cm /sec)

Figure 2. — Tail beat amplitude at various speeds for six
Trachurus, 4.5 to 27.7 cm total length.

LENGTH (cm)

FiGl'RE 3. — Relationship between tail beat amplitude and
total length for 14 TracliKnis, 4.5 to 27.7 cm total length.
{A = 0.23177L, s„^ = 5.068, and N = 176.)

hand, changed with speed and, therefore, was
the only speed modulator measured in these ex-
periments. In all species studied the relation-
ship between tail beat frequency and velocity

256

HUNTER and ZWEIFEL: SWIMMING SPEED AND TAIL BEAT FREQUENCY

was linear throughout the rang-e of test speeds,
but the slope and intercept of the regression
lines varied with fish length (Figure 4, Table 1) .

10 15

FREQUENCY (tail beafs/sec)

Figure 4. — Relationship between speed and tail beat fre-
quency for six Trachurus, 4.5 to 27.0 cm total length.
Equations for regression lines shown in figure are given
in Table 1.

Table 1. — Standard deviation (s„r), intercept (a), and
slope (b) for regression of speed (cm/sec) on tail beat
frequency and slope and intercept for regression of
speed/length on frequency for Trachurus.

Length

Speed (cm/sec) on f

requencY

Speed/
on free

ength
uency

(cm)

N

a

b

s

a

b

45

8

-17786

3.996

3,889

-3.952

0.888

64

9

-29.761

6.838

4284

-4.650

1.068

79

11

-37.527

8.326

4.135

-4,624

1.054

83

11

-39.736

9.374

10.096

-4.787

1.129

9.4

13

-35.241

8.953

5,258

-3.749

0 952

10.7

13

-29.012

10.431

5.612

-2.781

0.975

13,2

13

-19.860

11,514

10.762

-1.504

0.873

16.4

14

-32541

14.780

9.060

-1.934

0.901

22.8-

15

-15.407

17.497

6.945

-0.676

0.767

23.7

13

-13.723

19.753

6.457

-0.579

0 833

25.0

15

-33.403

23.394

1 1 .832

-1.336

0.936

25.8

13

-23.220

21.730

3.734

-0.900

0.842

27,0

13

-20521

23.960

9.157

-0.760

0.887

27.7

15

-11.240

20509

9.182

-0.406

0.740

Totol

176

The length-dependent differences in intercept
were probably a function of differences in min-
imum speed and minimum tail beat frequency.
Fish have a minimum tail beat frequency and
a minimum swimming speed below which they
cannot swim by movement of the caudal fin and
these minima were a function of body length.

In the past, speed was scaled directly to length;
that is, speed was divided by length and re-
gressed on frequency (Bainbridge, 1958; Mag-
nuson and Prescott, 1966; Yuen, 1966). Our
data suggest, however, that division of speed
by length would introduce bias because of the
existence of a minimum speed and tail beat
frequency different from zero, the dependence
of minimum speed on length, and possible length-
dependent differences in the slope of the regres-
sion of speed on frequency. For example, when
we divided speed by length, size-dependent dif-
ferences in intercept and possibly the slojie still
existed (Table 1, last two columns) . In addition
a curvilinear trend is introduced at low speeds
in the combined data because of the lack of an
intercept (minimum speed) correction. Thus
an equation that relates speed to tail beat fre-
quency for fish of different length must include
an adjustment for size-dependent differences in
minimum swimming speed, minimum tail beat
frequency, and perhaps also for size-dependent
differences in the slope coefficient.

The existence of size-dependent variables in-
troduces certain problems in the interpretation
of these data because of the possibility that spe-
cific differences in size dependency may exist.
For example, differences exist among species
in the coeflicients used to relate size to vaiious
swimming characteristics such as burst and sus-
tained speeds (Bainbridge, 1960) but it is un-
certain whether or not these differences reflect
real specific differences or if they are simply
differing estimates of a common coefficient.
Owing to the great variability inherent in swim-
ming speed studies and because of the sensitivity
of the length coefficients to the size range of an-
imals in the sample, these two alternatives are
equally plausible. In addition, specific differ-
ences in the relationship between size and swim-
ming functions may also depend on the partic-
ular function considered (Bainbridge, 1960).
For example, the coefficient relating size to max-
imum sustained speed may be different from
the one that relates size to beat frequency or
burst speed. Thus, species may differ from one
another in the way each swimming function is
related to size. If such specific differences exist

257

FISHERY BULLETIN: VOL. 69. NO. 2

then direct comparisons between species are im-
possible, but if they do not exist then a general
model can be derived from our data which can
be used to make specific comparisons. In the in-
terpretation of our data on Trachurus we will
consider the alternatives, Case I where all swim-
ming functions are related to size on a species-
specific basis, and Case II where swimming
functions are proportional to the same power of
length in different species.

To evaluate Case I where length coefficients
are considered to be species-specific we regressed
speed on frequency by the general relationship.

V = a.L"

+

a^L* * F

where V is swimming speed in centimeters per
second. F is tail beat frequency in beats per sec-
ond, L is total length in centimeters and w.L"'
is the intercept function and ajL"^ is the slope
function for the tail beat frequency-swimming
speed relationship. Estimates were obtained by
use of Marquardt's Algorithm for fitting non-
linear models (Conway, Glass, and Wilcox,
1970). For Trachurus the 90% support-plane
confidence intervals (Conway et al., 1970) for
03 and 04 were 0.72 <«3 <1.82 and 0.72 <a^

<1.01 where S, = 1.28 and «,

0.86.

To evaluate Case II where length coefficients
are the same for all fish we assumed the slope
coefficient a^ equaled one. When a^ = 1, a^ =

0.86 with 90''f confidence limits of 0.79 < «,
< 0.91. On the basis of the Trachurus data
alone there seems to be little or no difference
between the use of unity for the slope coefficient
or use of the estimated value of 0.86. The simi-
larity in the two estimates is apparent when
the actual fish lengths are substituted into the
two equations and the two sets of slopes are
compared (Table 2, columns 1 and 2).

We fitted the Case I model to four additional
species to determine the extent they differed in
the length coefficient for the slope in the speed-
tail beat frequency relationship. Used in this
comparison were data we collected on Scomber,
and data presented in scatter plots of velocity
and frequency for individual Carassius, Salmo.
and Le?tc/so!« by Bainbridge (1958). We used
the XY digitizer to transcribe Bainbridge's data
onto cards. We may have failed to interpret
correctly some of the overlapped points in his
graphs but the effect of these errors on the sta-
tistical parameters we estimated would be ne-
gligible. We did not use the data presented by
Magnuson and Prescott (1966), Yuen (1966),
or Fierstine and Walters (1968) because in these
studies the absolute speeds and the lengths of
the fish were unknown.

Our estimates of the slope coefficient for the
speed-tail beat relationship, 5.,, varied from 0.76
in Salmo to 1.22 in Carassius, and the 90%

Table 2. — Slopes for the speed-frequency relationship for individual Trachurus
when the general relationship is slope = 1.28 L^^^ (Case I) and when slope =:
0.86L (Case II) ; estimated minimum speed (V„) for each fish when V^ = 0.80L2/3;
lowest observed test speed (Fobs); the minimum tail beat frequency (F„) estimated
by substitution of Fq the Case II equation for each fish; and the lowest observed
tail beat frequency (fobs)-

Length
(cm)

= 1.28/."
Case I

i = 0.86i
Case II

= 3.98i
Case II

4.5

4.67

3.87

2.19

14.9

2.41

7.77

6.4

6.32

5-50

2.77

18.9

2.14

6.60

7.9

7J7

6.79

3.19

24.0

2.00

6.75

8.3

7.90

7.14

3.30

240

1.97

6.68

9.4

8.79

8.08

3.59

15.1

1.88

5.22

10.7

9.83

9.20

3.92

15.0

1.81

4.18

13.2

10.98

11.35

4.51

15.0

1.68

2.91

16.4

14.19

14.10

5.21

19.0

1.56

3.56

22.6

18.84

19.61

6.50

18.9

1.40

2.18

23.7

19.48

20.38

6.67

24.1

1.38

1.86

25.0

20.39

21.50

6.91

19.8

1.36

2.46

25.8

20.95

22,19

7.06

24.7

1.35

2.11

27.0

21.78

23.22

7.28

31,4

1.33

2.16

27.7

22.27

23.82

7.40

19.0

1.32

1.78

258

HUNTER and ZWEIFEL: SWIMMING SPEED AND TAIL BEAT FREQUENCY

support-plane intervals for «^ in all species in-
cluded unity (Table 3). Clearly if a common
slope-length coefficient exists among these spe-
cies, it must be close to 1. We conclude the
assumption of unity for the slope-length co-
-efficient is an acceptable practice and that it
appears to introduce no significant bias in the
species studied.

We now turn to the problem of estimation
of the length-dependent coefficient for the in-
tercept of the speed-tail beat relationship, that
is, a.,. We noted previously that the biological
significance of the existence of an intercept dif-
ferent from zero in the speed-frequency rela-
tionship may be that fish have a minimum speed
below which they cannot swim by movements
of the caudal fin. If we assume that the inter-
cept is a function of the minimum swimming
speed of a fish we can make an independent esti-
mate of the intercept coefficient using an equa-
tion derived by Magnuson (1970) for estimation

of the minimum swimming speed (Vo) of E.
affinis. A somewhat simplified form of his equa-
tion is:

Vo =

1 —

g * Ma

(C«A/0 * —
2

where D,. is 1.025 (the density of sea water),
Df is the density of the fish, g is 980 cm/sec
(the acceleration of gravity), Ma is mass of
fish in air, Cu is the coefficient of lift for the
pectorals (assumed to equal 1), Aft is the total
lifting area of the extended pectoral fins in
square centimeters, and p is the density of sea
water, 1.025 g/cc. If we let Ma = 0.004407
7^321215 (i^jjg length-weight relationship for T.
symmetrictis, N = 264, unpublished data, Na-

Tarle 3. — Estimates of length coefficients for slope and intercept for five

species of fish.

Species

r = a, i«J + a, i «» * f

90% support-plane
infervali

Tracfiiihiii symmetricui

r

= -44.57/. "-^ + 1.28/."*'^ • f

-111.18 <ai< 22.65

-0.80 <a,< 0.31

0.73 <<«,< 1.82

0.72 < a, < 1.01

Scombtr japoniiuj

;■

= -0.56i°=^^ + 1.20L°»^ • F

-160.78 <ai<159,66

-84.14 <aj< 85,25

-8.15 <«,< 10,57

-1.46 <a,< 3.13

Leuciicui Uueistits^

y

= -3.36i" ^^ + 0.80Z.'"'8 . f

-14.95 <Oj< 8.24

-0.84 <a,< 1.65

0.47 <o,< 1.12

0.83 <«,< 1.12

'./ = 781

Salmo gairdnfri^

V

= -1.771° «^ + 1.40i°^'' • r

-14.79 <a,< 11.26

-0.70 <a2< 2.97

0.33 <a3< 2.46

0.52 <a,< 1.00

V = 14.16

Coraisiuj auratus^

V

= -0.12i'^- + 0.40i^'^- * F

-0.89 <«!< 0.64

-0,50 <a3< 3,53

0.17 <Oa< 0.63

1.01 <o,< 1.44

',1 = 5.54

1 Simultaneous confidence intervals for all poronneters (Conway, Glass, and Wilcox, 1970).
a Data from Boinbridge (1958).

259

FISHERY BULLETIN; VOL. 69, NO. 2

tional Marine Fisheries Service, La Jolla, Calif.) ,
Area = 0.0281 lL'°'--» (lifting area of pectorals
of T. symmetricus was equal to twice the pec-
toral fin area), and Df — 1.03 (the density of
T. trarhurus from Alexander (1959b), a closely
related species to T. symmetricus), we obtain
an estimate of Fo = 0.86L°<'5 for Trachurus.
This value is considerably below lOL"^" obtained
for Euthynnus by Magnuson (1970) . The min-
imum swimming speed of Trwhnrus would be
expected to be lower than that of Euthynnus be-
cause Euthynmis lacks a swim bladder and has
a high specific gravity. Indeed, the minimum
speed of Euthynnus is close to the endurance
speed of many fishes with swim bladders (Mag-
nuson, 1970).

In all other species except Carasshis estima-
tion of minimum speed was not possible because
we had few or no estimates of the variables
required in Magnuson's equation. In Carassius
we used the specific gi'avity for carp, 1.002 g/cc
(Alexander, 1959a), the pectoral fin area re-
lationship of Area = 0.02811Li"-^ from data we
collected on seven Carassius 4.6 to 22.5 cm total
length (the lifting area of the pectorals equaled
twice the pectoral fin area) and the length-
weight relationship of Ma = O.OOGSL^^" for the
seven Carassius. The estimate of minimum
swimming speed Vo for Carassius from these
data was 0.87L'"^^ This estimate was nearly
the same as the one estimated above for Tra-
churus and it had the same coefiicient of length.
Thus, in Trachurus and in Carassius the min-
imum speed coeflncient of length or, in our
equation, the intercept coefiicient 5,. was 0.65.

That the length coefiicient for the intercept
was the same in Carassius and Trachurus sup-
ports the basic assumption of the Case II model,
that is, the existence of common length coefiicient
among different species. To further test this
assumption we estimated the intercept coeffi-
cient by fitting the combined data from all five
species listed in Table 3 to the reduced Case II
model

<1.92. Although the limits were wide, the
estimate was very close to the other independent
estimate for Carassius and Trachurus and sug-
gests that the true value may be close to 2/3.
The evidence we presented supported the use
of the Case II equation and the use of 2/3 for
the length-dependent coefficient for the intercept
function and of unity for the length-dependent
coefiicient of the slope function. Thus, we fit
the reduced Case II model

V = cc.U'^ + a,L * F

to the data from each of the five species listed
in Table 3 and to that from two additional species
Triakis and Sardinops for which we had a small
number of ob.servations. The resultant equa-
tions were useful nonbiased predictive models
for the estimation of speed (V) from length
(L) and tail beat frequency (F) in each spe-
cies (Table 4). The regression lines for these
equations do not pass through the origin, how-
ever. They cut the abscissa before zero and
consequently the intercept terms are negative.
We pointed out previously that we believe the
existence of a negative intercept in the raw
data implied that the fish had a minimum swim-
ming speed below which they cannot swim by
beating only the caudal fin. Thus, to make the
model more biologically meaningful we adjusted
the elevation of the intercept function to cor-
respond to the theoretical minimum swimming
speed, Vo. (It should be remembered that the
length-dependent slope of Vo was about the same
as the length coefiicient, a.^, and it was this simi-
larity that led us to use 2 3 as the intercept
coefficient.)

To express the Case II model in terms of min-
imum sjjeed we used Fo estimated from Mag-
nuson's equation to solve for a minimum tail
beat frequency, Fn, and expressed the final re-
lationship in the form

Vo

KF — Fo.

a^L

+ a,L* F

The estimate a., for the combined data was
0.68 with 90% confidence limits of —0.56 Ka^

In species other than Trachurus and Carassius,
a theoretical estimate of Vo was not possible
and consequently we assumed Fo was propor-

260

HUNTER and ZVVEIFEL: SWIMMING SPEED AND TAIL BEAT FREQUENCY

Table 1. — Swimming speed-tail beat frequency equations for seven species

of fish.

Species

r = a, i2/3 + a^ ' F

90% support-plan©
interval^

Triakt! hftiUi

Trachurul symrmtricu!

Scomber japonicul-

Leucucuj Uuciicus

Carasiiul auratus

Salmo gairdneri

V = -1.39i-^' + 0.93Z. • F

l.SOL-^^ + 0.83i * F

V = -2.20L~^'^ + 0.82i * F

-2.71 <«!< -0.01
0.77 < Oj < 1 .09

V = 2.49

-3.28 <«!< -1.59
0.78 <a^< 0.88

! , = 12.39

-3.18 <a^< -1.13
0.76 <aa< 0.88

s , = 12.31

—2.21 <Qt.< -0.86
0.71 <a3< 0.78

J , = 7.78

-1.47 <aj< 0.17
0.61 <a^< 0,74

-2.63 <a^< 0.13
0.59 < Oj < 0.69

Sardtnopl sagax

0.49i-^^ + 0,50i • /

-1.61 <0!^< 2.58
0.39 <a3< 0.62

^Simultaneous confidence intervals for alt parameters (Conway, Glass, and Wilcox, 1970).

"On© deviant fish omitted; if fish included F

-0.53L

!/3

+ 0.66i • F, and s. = 21.31.

tional to L--'^ The elevation of the line relating
Vo to length for a species was estimated by as-
suming that the lowest observed speed fell on
that line. For Trachunis and Carassius we
recalculated the elevation for a slope of 2/3.
Our estimates of Vo and Fo were not definitive.
For Trachunis no fish were tested at speeds
close to the theoretical minimum. Our esti-
mates based on the theoretical minimum speed
were closest to the observed minimum speeds in
fish 9.4 cm total length and larger (Table 2)
because in these larger fish the test speeds were
sufiiciently low for fish to swim with pectoral
fins fully extended, an event that occurs near
the minimum swimming speed (Magnuson,
1970). For Carassius the agreement between
the theoretical estimate of minimum speed and
observed minimum speeds was better (Table 5).
The explanation for this is that the techniques
used by Bainbridge (1958) permitted estimates
at much lower speeds than the one we used.
These data clearly show that in neither Trach-

unis (Table 2) nor Carassius (Table 5) was
either Vo or Fo seriously overestimated. We feel
that our estimates for these two species were
reliable.

The fit to the general equation was good in
all species (Figure 5, Table 6). The intercept
for the regression line did not differ from zero
and the scatter at low velocities was less than
it was when no intercept correction was used
(see figures in Bainbridge (1958) for compar-
ison) . The regression coefficient, K, in our equa-
tion diff'ered among species. For the five species
for which significant data were available, it was
the highest in Trachunis and lowest in Salmo.
Since amplitude was a constant, these results
implied that the speed output per beat of the
caudal fin was greater in Trachunis and Scomber
than it was in Salmo and Carassius. In Scomber,
the coefficient, K, may be uncertain because the
values of one of the five fish tested deviated con-
siderably from the rest. In Figure 5, all of the
values to the right of the regression line above

261

Trochurus

-

15

■

••■■

10

-

• *i

* ' '

• '.'•..

5

n

1 I 1 1

10

15

20

15

10

>°

5-

15

10

Leuciscus

•

■

1

.-•O'-

• 1- • ■

.-. <■■

1 1

15

10

Scomber

FISHERY BULLETIN; VOL. 69, NO. 2

0 5

Corossius

10

. .■ •■*•■

15

20

10

15

20 0

10

15

20

15

10

Solmo

OL-^

10

15

20

F-Fn

Figure 5. — Relationship between swimming speed corrected for minimum s|)eed over lenprtli and tail beat fre-
quency corrected for minimum frequency for Trdrhiiriis and Scomber from the present data, and for Leuciscus,
Salmo, and Carassius from Bainbridge (1958). Graph at lower right shows individual regression lines for all
above species, equations for linos are given in Table 6.

262

HUNTER and ZWEIFEL: SWIMMING SPEED AND TAIL BEAT FREQUENCY

Table 5. — Slopes for the velocity-frequency relationship
for individual Carassius studied by Bainbridge (1958)
when the general relationship is slope ^= 0.68L; esti-
mated minimum speed when Vq = O.SIL-/^; observed
minimum swimming speed (I'obs) > the tail beat fre-
quency Fq estimated by substitution of Vg into the cor-
rected slope equation ; and the lowest observed tail beat
frequency (F„f,J.

Length
(cm)

* = 0.66L

^0 =

= 0.81i2/3

*'obs

^0

= 2.22i"

-1/3

'^obs

4.6

3.04

2.25

3.50

1.34

1.30

7.0

4.62

2.98

9.30

1.17

1.52

9.5

6.27

3.66

11.60

1.04

2.03

15.2

10.03

5.01

33.70

0.90

3.38

22.5

14.85

6.52

13.70

0.78

1.63

1 Data from Bainbridge (1958).

Table 6. — Minimum speed (Vq), minimum tail beat fre-
quency (Fq), the coefficient K in equation V — F„ =
L(KF — Fq) arranged in order of K.

Species

N

>'o

"o

K

Triakis kenlei

6

0.15L^/^

1.66L"

-1/3

0.93

TrackuTus svmmetricus

176

■o.aor'''

3.98i"

-1/3

0.83

Scomber japonicus

261

1.3U^^^

3.51i"

1/3

0.82

Leuciscui leuciscus^

149

0.67i2/3

3.04/."

-1/3

0.74

Carassius auratus^

111

lo.eii"''^

2.22i"

-1/3

0.66

Salmo gairdneri^

109

0.52Z,2/^

2.81i"

1/3

0.64

Sardinops sagax

9

2.23i^^^

3.48/."

-1/3

0.50

1 y theoretical estimote based on equation of Magnuson (1970).
3 One deviant fisli omitted; if fish included. A' = 74, K = 0.66.
» Original dota from Bainbridge (1958).

4 beats/sec on the abscissa were from this single
deviant fish. If the deviant fisli is included K =
0.66, but if not, K = 0.82. We are inclined to
use K = 0.82 because the values for the four
fish were very similar and the protocol indicated
that the deviant fish may have been overly fa-
tigued when tested. Triakis appears to have
a relatively high coefficient but not too much
significance can be attached to the exact value
for Triakis or for Sardi^iops because these were
based on so few measurements.

In sum, the speed-tail beat equation (Case II)
— Table 6 — was biologically as well as statisti-
cally relevant, was sensitive to specific differ-
ences in swimming behavior, provided an un-
biased correction for length, and made possible
a more accurate estimation of swimming speed
from tail beat frequency than heretofore has
been possible.

TAIL BEAT AMPLITUDE

We pointed out previously that tail beat ampli-
tude was a constant and was directly propoi--
tional to length and consequently the size coeffi-
cients for amplitude are probably the same as
those for length. Thus amplitude (A) in centi-
meters can be substituted for length in the ori-
ginal Case II equation V = a^vl^/s -j_ ^ L * F.
When this was done for Trachurus using all
individual amplitude values (iV = 176) , we ob-
tained the equation; V = —6.5767/12/3 +
3.5637/1 * F. The amplitude coefficient may
be also estimated by substitution of the ampli-
tude-length relationship for Trachurus (A =
0.23177L) , into the Case II equation.

The tail beat amplitude data collected by
Bainbridge (1958) were insufficient for specific
estimates of an amplitude coefficient. The mean
amplitudes for each of the fish we studied and
for each of those studied by Bainbridge were
nearly the same, when adjusted for body length.
Variation within a species was as great as that
between species (Figure 6). The relationship

UJ
Q

3

Q.

s
<

Z
<
UJ

S

3-

♦ CorosBius (FROM BfllNeRlOGE, 19581
■ Enqroulis

• Leuciscus (FROM BfilNBRIOGE, 19581
D Solmo (FROM BaiNBRlDGE, 1958)

0 Sofdinops

* Scomber

o Trachurus
^ Tnokis

DO

o i

10 15 20 25

TOTAL LENGTH (cm)

30

35

Figure 6. — Relationship between mean tail beat ampli-
tude and length for every fish we studied and all those
studied by Bainbridge (1958), A = 0.21L.

between mean tail beat amplitude and length
for all species combined was A = 0.21L.

263

FISHERY BULLETIN: VOL. 69. NO.

DISCUSSION

In all previous studies speed was divided by
length then related to tail beat frequency. In
our data when speed was converted to body
lengths per second the relationship between
speed and frequency was nearly identical to that
given by Bainbridge (1958) for Carasslus,
Leuciscus, and Salmo The confidence intervals
for the slopes in the speed-frequency relation-
ship in Eiifhynntis and Thmnivs (Yuen, 1966)
and in Sarda (Magnuson and Prescott, 1966)
overlap the slope in the Bainbridge equation and
the ones for Trachurus and Scomber when the
body length conversion is used. Thus, when
speed is in body lengths per second, the relation-
ship between it and frequency is about the same
in all fish studied to date from goldfish to mack-
erel and is adequately described by the Bain-
bridge equation V/L = bf. Thus the Bainbridge
equation provides a description of the average
relationship for fish in general but little sig-
nificance can be attached to specific differences
in slope. If more than a rough estimate of
speed is required or if specific difterences are
important, or if estimates are needed near the
minimum swimming speed it would be neces-
sary to use the equation developed in this study.

Bainbridge (1958) concluded from his data
that the frequency-speed relationship was curvi-
linear below a frequency of about 5 beats sec
because fish modulated their tail beat amplitude.
His evidence for this conclusion was that in
some fish amplitude appeared to decrease at low-
er frequencies, and that the distance per beat,
calculated by dividing speed by frequency, de-
clined at frequencies below 5 beats sec but was
constant above that frequency. His evidence
for amplitude modulation at low speeds was
weak. In the three Salmo studied no trend ex-
isted; in Cara,'isius he suggested there might be
a decrease in amplitude in one of the two fish
studied, and in one of the two Leuciscus studied
a trend existed slightly stronger than the one
in Camssius. In sum, the evidence for a de-
cline in amplitude measurements was based on
possible trends in two of the seven fish studied.
Two fish could easily give a misleading picture
of the general trend in the data, especially when

the variability in ami)litude measurements are
considered. In our .studies we measured the tail
beat amplitude in every fish at all possible speed
levels and no evidence existed for a consistent
change in amj^litude with speed.

In Bainbridge's data the departure of distance
traveled per beat from a constant at low fre-
quencies was caused by the division of speed
liy frequency. Had the line relating frequency
to speed passed through the origin, no bias
would have existed but because the line inter-
sected the abscissa at about 1 beat/sec division
by frequency produced an artificial curvilinear
trend at lower frequencies. We produced the
same trend in distance per beat in our data
by dividing speed by frequency but the trend
was eliminated when a correction for the in-
tercept was used. Thus the curvilinear trend
in distance per beat in Bainbridge's data was an
artifact caused by the method of calculation
and consequently distance per beat was a con-
stant at all frequencies. In addition, the appar-
ent nonlinearity below 5 beats/sec in his graphs
relating speed divided by length to frequency
was also the result of the same intercept problem.
Therefore, no evidence exists for consistent
amplitude modulation at any speed range and
speed appears to be related only/ to tail beat
frequency and length in the species studied by
Bainbridge (1958) as well as in the ones we
studied. We concluded that during steady swim-
ming at any speed, tail beat amplitude is a
constant proportion of body length of the order
of 0.21 L.

That the mean amplitude during steady swim-
ming was constant does not mean that amplitude
is not modulated under certain conditions. It
is widely known that fish modulate tail beat
amplitude when they accelerate (Gray. 1968).
Further, we had the impi'ession that some of
the variability in the speed-frequency relation-
shi]) was caused by diflJ'erences in amplitude.
These diff'erences were infrequent and irregular
in occurrence and consequently we were not able
to evaluate them statistically. We are inclined
to believe, however, that fish occasionally made
minor adjustments in amplitude and frequency
over the entire range of sjieeds, but these adjust-

264

HUNTER and ZWEIFEL: SWIMMING SPEED AND TAIL BEAT FREQUENCY

ments were merely individual deviations from
the general relationship we have described.

We do not wish to detract from the original
and important contribution of Bainbridge
(1958), by emphasis on the differences between
his and our conclusions. His basic conclusions
and equations were not greatly different from
our own. We were able to examine more closely
the form of the relationships he described be-
cause of a larger sample size made possible by
the availability of automatic film analysis equip-
ment and because of the existence of his data
in the literature.

The question of species-specific size effects re-
mains unresolved. In our general model a good
fit was obtained in seven species when the min-
imum stalling speed was proportional to L~^^, the
frequency at this minimum speed was propor-
tional to L-'^^ and the slope coefficient was pro-
portional to W. A com])arative study on speed-
related size effects in fishes would certainly be
of value.

It also remains to be resolved whether or not
it was appropriate to apply the minimum swim-
ming speed equation developed by Magnuson
(1970) for Euthijnnus affinis, a fish that lacks
a swim bladder, to such a broad assortment of
species. The equation implies a functional re-
lationship between minimum speed and hydro-
static equilibrium and implies existence of neg-
ative buoyancy at minimum speeds. We do not
know if these relationships exist in all species;
nevertheless his equation did provide a reason-
able estimate for minimum speed and it func-
tioned well in our equation.

The relationship between swimming speed
and tail beat frequency we have described could
be used in any application where it is necessary
to measure swimming speeds of fish. For ex-
ample, a sonic internal tag could be developed
that telemetered tail beat frequency and thus
the speed of free-swimming fish could be mon-
itored continuously over extended periods.

The tail beat frequency-speed relationship
could be used for size or species identification
using Continuous Transmission Frequency Mod-
ulated sonar as suggested by Hester (1967).
The increase of speed with frequency (our K

value) varied from species to species and thus
might be used for identification. If size were
known, the minimum observed velocity would
provide additional information for identification.
Alternatively, if the species were known, min-
imum (or maximum) speed would provide an
indication of size. The equation could also be
used to estimate size from tail beat amplitude,
but caution should be exercised because in our
study amplitude was not modulated and conse-
quently, we do not know whether or not speed
and tail beat amplitude are linearly related
within an individual.

ACKNOWLEDGMENTS

We wish to thank David Holts and George
W. Rommel of the NMFS Fishery-Oceanography
Center, La Jolla, Calif., who assisted in con-
ducting the experiments and in calibration of
the apparatus. Albert Good wrote the program
for digitizing the photographic data, and John
J. Magnuson, Department of Zoology, University
of Wisconsin, Madison, Wis., reviewed the man-
uscript.

LITERATURE CITED

Alexander, R. M.

1959a. The densities of Cyprinidae. J. Exp. Biol.

36: 333-340.
1959b. The physical properties of the swimblad-
ders of fish other than Cypriniformes. J. Exp.
Biol. 36: 347-355.
Bainbridge, R.

1958. The speed of swimming of fish as related to
size and to the frequency and amplitude of the
tail beat. J. Exp. Biol. 35: 109-133.
1960. Speed and stamina in three fish. J. Exp.
Biol. 37: 129-153.
Beamish, F. W. H.

1966. Swimming endurance of some northwest At-
lantic fishes. J. Fish. Res. Bd. Can. 23: 341-347.
Conway, G. R., N. R. Glass, and J C. Wilcox.

1970. Fitting nonlinear models to biological data by
Marquardt's algorithm. Ecology 51 : 503-507.

FlERSTINE, H. L., and V. WALTERS.

1968. studies in locomotion and anatomy of scom-
broid fishes. Mem. S. Calif. Acad. Sci. 6: 1-29.
Gray, J.

1968. Animal locomotion. Weidenfeld, London,
479 p.

265

FISHERY BULLETIN: VOL. 69. NO. 2

Hester, F. J.

1967. Identification of biological sonar targets from
body-motion Doppler shifts. Mar. Bio-Acoustics
2: 59-74.
Hunter, J. R.

1966. Procedure for analysis of schooling behavior.
J. Fish. Res. Bd. Can. 23: 547-562.
Magnuson, J. J.

1970. Hydrostatic equilibrium of Eutbynnus af-
finis, a pelagic teleost without a gas bladder.
Copeia 1970: 56-85.
Magnuson, J. J., and J. H. Prescott.

1966. Courtship, locomotion, feeding, and miscel-
laneous behaviour of Pacific bonito (Sarda chil-
iensis). Anim. Behav. 14: 54-67.

Olson, J. R.

1967. Flowmeters in shallow-water oceanography.
Nav. Undersea Warf. Center, San Diego, Calif.
TP 5, 44 p.

Tranter, D. J., and P. E. Smith.

1968. Filtration performance. In D. J. Tranter
(editor), Reviews on zooplankton sampling meth-
ods, p. 27-56. UNESCO (U.N. Educ. Sci. Cult.
Organ.) Monogr. Oceanogr. Method. 2, Part 1.

Yuen, H. S. H.

1966. Swimming speeds of yellowfin and skipjack
tuna. Trans. Amer. Fish. Soc. 95: 203-209.

266

SUSTAINED SPEED OF JACK MACKEREL, Trachurus symmetricus

John R. Hunter'

ABSTRACT

Jack mackerel, Trachurus symmetricus, were forced to swim for up to 6 hr at various speeds in an
activity chamber. The probit estimate for the swimming speed at which 50% of Trachurus would fa-
tigue during 6 hr was 93.4 cm/sec (8.4 L/sec) for fish 10.0 to 11.9 cm and was 22.4 L^'^/sec for fish
9.0 to 17.6 cm where L is the total length of the fish in centimeters. At higher speeds, Trachurus, 15
cm, swam for 3 min at 160 cm/sec or 10 L/sec. The swimming speed at which 50% fatigued declined
exponentially with time for about the first 22 min of swimming and thereafter declined linearly with
time. The possible significance of the time-speed relationship for Trachurus is discussed.

Although a substantial literature on the swim-
ming speed of fishes exists (see Bainbridge,
1958; Gray, 1968), few reliable estimates of
maximum sustained speed exist. Much of the
literature on swimming speed of fishes is con-
cerned with estimates of maximum speed or
burst speed, that is, speeds that can be main-
tained for only a few minutes or less. A sus-
tained speed implies, on the other hand, that
the animal is capable of swimming at that speed
for hours. For example, Brett (1967) recom-
mended a minimum of 200 min for a fixed sus-
tained speed test. Fairly wide agreement exists
that 2 to 3 L/sec can be maintained for an hour
or more and salmonids and herring seem capa-
ble of sustaining 3 to 4 L/sec for such periods
(Blaxter, 1969) . These conclusions were drawn
primarily from studies of freshwater fish and
salmon; no estimates of maximum sustained
speeds have been made for fast-swimming pe-
lagic marine forms. The object of this study
was to determine the sustained speed thresh-
hold of jack mackerel, Trachurus symmetricus,
a pelagic marine fish of commercial importance.
The body form and musculature of Trachurus
appear to be designed for greater hydrodynamic
efficiency at high speeds than other species here-
tofore studied. In Trachurus, lateral muscula-
ture is concentrated in the anterior portion of
the trunk, and inserts by tendons on a small
deeply forked caudal fin.

' National Marine Fisheries Service Fishery-Ocean-
ography Center, La JoUa, Calif. 92037.

Manuscript received January 1971.

FISHERY BULLETIN: VOL. 69, NO. 2, 1971.

In addition to the interest in comparing the
sustained speed capabilities of Trachurus with
that of fish with other body forms, sustained
speed data have significance in prediction of
migratory capabilities and physiological limits.

APPARATUS AND METHODS

The apparatus used in the experiments was
an activity chamber provided with a water cur-
rent of various calibrated speeds. The appa-
ratus was the same as the one described and
figured by Hunter and Zweifel (1971) in this
issue except that a port was provided in the
transparent hatch of the swimming chamber
so that fatigued fish could be removed by hand
from the downstream screen without reducing
the flow in the chamber. The error in estimating
the water speed in the swimming chamber did
not exceed 10% and it was assumed that the
fish were swimming at the estimated speed.

The experimental design was essentially the
same as that used by Brett (1967) for deter-
mining the sustained speed threshhold for sock-
eye salmon, Oncorhynchus nerka. Fifty-five
groups of five Trachurus (9.0 to 17.6 cm total
length, mean = 12.43 ± 0.11 cm) were subjected
to a fixed speed of 38 to 160 cm/sec for 360 min
or longer after an introductory period of about
30 min at a low speed. A time-lapse camera
photographed the fish at 1-min intervals and
the time to fatigue for each fish was determined
from the photographs. The temperature of the
water in the activity chamber and in the holding

267

FISHERY BLXLETIN: VOL. 69, NO. 2

tank (a plastic swimming pool 15 ft in diameter)
was maintained by a temperature regulation
system at about 18.5° C. The mean test temper-
ature was 18.48 ± 0.03° C. The fish were cap-
tured near Santa Catalina Island, Calif., on 12
September 1969. Tests began 2 weeks later and
ended on 21 November 1969. Fish were fed an
abundant ration of chopped squid, anchovies,
and frozen brine shrimp. Probit analysis, a sta-
tistical technique first applied to sustained speed
data by Brett (1967), was used to estimate sus-
tained speed threshholds.

Variability in length posed a problem in the
analysis. Although all fish were from the same
school, differences in length existed; also the
fish grew in the course of the study. These dif-
ferences were insufficient, however, to determine
the form of the relationship between length and
sustained speed. In general, the relationship
between length and sustained speed for other
species (Bainbridge, 1962; Brett, 1965), theo-
retical considerations (Gray, 1968; Fry and
Cox, 1970), and relationships between length
and other swimming capabilities (Magnuson,
1970), indicate that speed is proportional to a
fractional power of length equal to about U"^ - "'.
In addition, the minimum swimming speed
of Trachurus was proportional to L"^ when esti-
mated from Magnuson's equation (Hunter and
Zweifel, 1971). In light of the above evidence
it seemed preferable to use 0.6 as the coefficient
of length, although unity has been commonly
employed in cases where length coeflficients were
unknown. As an alternative to this procedure
I also estimated the percent fatigued at different
speeds in centimeters per second and in body
lengths per second for a narrow length range
(10.0 to 11.9 cm total length) where the effect
of diflFerences in length would be negligible.

RESULTS

Within a few minutes after Trachurus were
placed in the swimming compartment they be-
came quiescent, swam steadily, and remained in
about the same position in the compartment
throughout the test or until they became fa-
tigued and fell against the rear screen. This

was in contrast to some other species which did
not swim steadily, but swerved and oscillated
from side to side.

The relationship between water speed and
percent fatigue had the normal sigmoid form
of a dosage response curve (Finney, 1952).
Probit estimate of the applied water speed at
which 50^; fatigue occurred in 360 min of swim-
ming and the 95 5r confidence limits were 94.40
± 5.15 cm/sec for Trachurus 10.0 to 11.9 cm
total length, N = 127 (Figure 1, Table 1). Thus,

Table 1. — Swimming endurance of Trachurus sym-
metricus in cm/sec and in L^Vsec.

Length 10.0-11.9 cm

Length 9.0-17.6 cm

Speed

S

Percent
fatigued

ler

gth

Speed'
i0.6/sec

N

Percent

cm/sec

Mean

SO

fatigued

71

8

0

10.69

0.61

15.9

3

0

78

16

13

10.71

0.47

16.9

10

0

85

16

31

10.84

067

17.8

14

0

92

14

50

10 97

0.54

18.7

17

6

99

21

62

11.23

0.43

19.7

18

17

106

21

76

10.85

0.56

20.6

23

39

113

15

100

11.41

0.42

21.5

39

31

120

8

100

11.27

0.45

22.5

42

67

138

8

100

11.20

0.51

23.4

19

58

Tolol

127

24.3
25.3
26.2
27.2
28.1
29.0
30.0
30.9
31.8
32.8
33.7
Total

20
29
19
9
4
3
1

3
7
10
4
294

60
72
100
100
100
100
100
100
100
100
100

' Totol speed range divided into 20 equal intervals; speeds listed are
midpoints of those intervals.

50 ''r of Trachurus in this length range could
be expected to sustain a speed of about 8.4 L/sec
or 22.1 L" Vsec for 360 min. For all Trachurus
(N = 294) the water speed at which 50 ':r fa-
tigue occurred after 360 min of continuous
swimming and the 95 ''r confidence intervals
were 22.4 ± 1.2 L" Vsec. The first estimate,
based on a narrow length range, and the second
one, based on all data, were reasonably close.
On the other hand, when all data were in the
form V L'" the 50^r threshold was 9.34 L sec
which is higher than the preceding estimates.
Inspection of these data, however, showed that
the coefficient for length clearly was less than
one and that use of unity biased the estimate.

268

HUNTER: SPEED OF JACK MACKEREL
98 r

Figure 1. — Probit lines for sustained speed threshold
for 6 hr of forced swimming at 18.5° C in juvenile
Trachurus symmetrieus. Upper panel, range fish length
10.0 to 11.9 cm iV = 127, probit = 0.077A' - 2.238;
lower panel, range fish length 9.0 to 17.6 cm, N =; 294,
speed expressed in L" ^/sec where L is the total length
of the fish, probit = 0.355:? — 2.958.

To determine the form of the relationship
between the duration of the swimming period
and the ability to maintain a certain speed,
probit estimates of speed for five levels of fa-

tigue were made for swimming periods varying
from 10 to 360 min. The form of the relation-
ship was about the same for all fatigue levels;
speed estimates declined exponentially with time
for short swimming periods and linearly with
time for longer ones (Figure 2). The point

40r

u 30

UJ

99%

100

200 300

MINUTES

Figure 2. — Relation between speed in L'^'^/sec and the
time it can be sustained for 1, 25, 50, 75, and 99 per-
cent fatigue levels in Trachelitis symmetrieus. Estimates
of speed for each fatigue level made at 10-min intervals
of cumulated time.

of inflection from the exponential to the linear
relationship was examined in detail for the 50%
fatigue level. Probit estimates of the speed at
which 50% of the fish fatigued were made for
2-min intervals of swimming cumulated over
the first 100 min of observation. The data were
plotted on semilog paper and a line fit by eye
to the exponential function. The point of in-
flection appears to occur at about 22 min (Fig-
ure 3) . Thus, speed at which 50% fatigued and
the duration of the swimming period were ex-
ponentially related for durations up to about
22 min and were linearly related for longer pe-
riods of swimming.

The performance of juvenile Tmchimis at
high speed was of interest. Fifteen fish 14.6 cm
mean total length (range = 13.4 to 16.6 cm)
swam at the highest speed used in the study
(160 cm/sec) for 2 to 6 min, mean time 3.4 min.
Thus, Trachurus 15 cm total length were able
to swim for about 3 min at about 10 L/sec or
about 32 L" Vsec. A slightly higher level of

269

FISHERY BULLETIN: VOL. 69, NO. 2

■ \

1 1

1 1 1 1 1 1 T-

-

\

-

■

\

-

•n.

-

1.

i-jt-lA 1 1 I 1 lihl

20 30

MINUTES

100

Figure 3. — Relation between speed at which 50% Trach-
unis fatigued and the duration of the swimming period.
Duration of swimming period in minutes plotted on log
scale to show exponential trend ; line fit by eye. Speed
estimates made at 2-min intervals of cumulated time
over the first 100 min of swimming.

performance in length per second is obtained
if we consider smaller fish. For example, fish
of mean length 11.2 cm (length range 10.4 to
11.9 cm, A'^ = 8) swam for 3 to 5 min (mean =
4.5 min) at 139 cm/sec or about 12 L/sec. This
difference between large and small fish becomes
negligible if 0.6 is used as a coefl^cient of length
instead of unity because, as was pointed out
previously, the length coeflicient for Trachurus
appears to be less than 1.

DISCUSSION

The exponential decline in swimming speed
with time in fish is well documented; see for
example Bainbridge (1960), Brett (1967), and
Blaxter (1969). The general form of the re-
lation between time and swimming speed in
other fish resembles that for Trachurus al-
though the speeds and endurance times are dif-
ferent in Trachurus. The physiological mech-
anisms responsible for the exponential relation-
ship between swimming speed and endurance
are generally believed to be the limited enery
stores in the muscle, the rate these stores can
be replaced and the rate catabolites are removed
from the muscle (Bainbridge, 1960). A study

by Pritchard, Hunter, and Lasker (1971) in
this issue has provided an explanation for the
form of the speed-time relationship in Trach-
urus. Pritchard et al. found that at speeds
where an exponential relationship exists be-
tween time and speed the principal cause of
failure of Trachurus was most likely the de-
pletion of glycogen in the white muscle. On
the othei- hand, fish that failed at speeds near
the 6-hr 50% threshold, where a linear relation-
ship exists between speed and time, had de-
pleted not only the glycogen in the white muscle
but that in the red muscle and liver as well.
Thus, in Trachurus the form of the time-speed
relationship could be explained on the basis of
the extent of glycogen reserves available for
locomotion and the time required to mobilize
them from sites other than the white muscle.
An exponential relationship between speed and
time could be produced when the speeds are so
high that the glycogen supply would be limited
almost entirely to the white muscle because the
supply in the white muscle would be used up and
the fish would fail before significant amounts of
glycogen could be mobilized from other sources.
A linear relationship could exist where swim-
ming speeds are sufficiently low that reserves
in the white muscle could not be depleted before
other sources in the red muscle and the liver are
mobilized. We have, on one hand, a high rate
of consumption using a more limited supply of
fuel which could lead to an exponential relation-
ship between speed and time and, on the other
hand, a much lower rate of consumption using
a relatively much larger fuel supply which could
produce a linear relationship with time. An
exponential relationship between energy con-
sumption and swimming speed would enhance
these effects.

Let us now consider the significance of the
6-hr sustained speed threshold determined for
Trachurus. When compared with other deter-
minations, this threshold appears to be unique
because of different physiological mechanisms
and because it is higher than those estimated
for other fish. Trachurus at threshold speed
appeared to use glycogen as fuel, white muscle
for locomotion and maintained a high lactic acid

270

HUNTER: SPEED OF JACK MACKEREL

level in the muscle (Pritchard et al., 1971).
These results are inconsistent with the conclu-
sion that at sustained cruising speeds, fish use
lipid metabolism to drive red muscle (Bone,
1966; Gordon, 1968; Blaxter, 1969) and that
no oxygen debt is incurred (Brett, 1963). Re-
liance on glycogen as the principal fuel pro-
bably severely limits the time a speed can be
maintained as compared with one where lipid
metabolism is used exclusively. Thus the bio-
chemical evidence indicates that the 6-hr speed
threshold for Trachurus probably could be main-
tained only for a period of hours or perhaps
days but certainly not weeks as one would ex-
pect if fat were used as fuel. The 6-hr thresh-
old was also considerably above sustained speed
thresholds for other fish where presumably fat
may be employed as fuel. Brett (1967), in a
study directly comparable with the current one,
found the 50% fatigue time for sockeye salmon
was 4 L/sec (about 11.3 U"^) whereas for comp-
arable size jack mackerel it would be about 7.6
L/sec or 22.0 L"^. Other less comparable data
give sustained or cruising speeds in the range
of 3 to 4 L/sec (Blaxter, 1969). Thus, Trach-
urus has special physiological and structural
adaptations that permit swimming for periods
of hours at elevated speeds and it was the thresh-
old for this swimming behavior that was meas-
ured. Other fishes, especially the scombroid
fishes, may have similar abilities. For example,
skipjack tuna can swim at 8 knots, or about 43
L"^, for over an hour (Commercial Fisheries
Review, 1969) and yellowfin tuna and skipjack
tuna have higher levels of white muscle gly-
cogen than many other species of fish (Barrett
and Connor, 1964).

It seems possible another speed threshold may
exist for Trachurus below the present one where
fat is the principal fuel, only red muscle is used
for locomotion, and swimming can be main-
tained almost indefinitely. It would not be sur-
prising if this lower threshold were closer to
those determined for other fishes.

LITERATURE CITED

Bainbridge, R.

1958. The speed of swimming of fish as related
to size and to the frequency and amplitude of

the tail beat. J. E.xp. Biol. 35: 109-133.
1960. Speed and stamina in three fish. J. Exp.
Biol. 37: 129-153.

1962. Training, speed and stamina in trout. J.
Exp. Biol. 39: 537-555.

Barrett, I., and A. R. Connor.

1964. Muscle glycogen and blood lactate in yellow-
fin tuna, Thunnus albacares, and skipjack, Katsu-
wonus pelamis, following capture and tagging.
Inter-Amer. Trop. Tuna Comm., Bull. 9: 219-268.

Blaxter, J. H. S.

1969. Swimming speeds of fish. FAO (Food Agr.
Organ. U.N.) Fish. Rep. 62: 69-100.
Bone, Q.

1966. On the function of the two types of myotomal
muscle fibre in elasmobranch fish. J. Mar. Biol.
Ass. U.K. 46: 321-349.

Brett, J. R.

1963. The energy required for swimming by young
sockeye salmon with a comparison of the drag
force on a dead fish. Trans. Roy. Soc. Can.,
Ser. 4, Vol. 1, Sect. 3: 441-457.

1965. The relation of size to rate of oxygen con-
sumption and sustained swimming speed of sock-
eye salmon {Oncorhynchus nerka) . J. Fish. Res.
Bd. Can. 22: 1491-1501.

1967. Swimming performance of sockeye salmon
(Oncorhynchus nerka) in relation to fatigue time
and temperature. J. Fish. Res. Bd. Can. 24:
1731-1741.

Commercial Fisheries Review.

1969. Underwater tuna school tracked by sonar.
Commer. Fish. Rev. 31(11) : 9-10.

Finney, D. J.

1952. Probit analysis. 2d ed. Cambridge Univ.
Press, Cambridge, Engl., 318 p.
Fry, F. E. J., and E. T. Cox.

1970. A relation of size to swimming speed in
rainbow trout. J. Fish. Res. Bd. Can. 27: 976-978.

Gordon, M. S.

1968. Oxygen consumption of red and white mus-
cles from tuna fishes. Science 159: 87-90.

Gray, J.

1968. Animal locomotion. Weidenfeld, London,
479 p.
Hunter, J. R., and J. R. Zweifel.

1971. Swimming speed, tail beat frequency, tail
beat amplitude, and size in jack mackerel, Trach-
urus symmetriciis, and other fishes. Fish. Bull.
69: 253-266.

Magnuson, J. J.

1970. Hydrostatic equilibrium of Euthynnus af fin-
is, a pelagic teleost without a gas bladder. Copeia
1970: 56-85.

Pritchard, A. W., J. R. Hunter, and R. Lasker.

1971. The relation between exercise and biochem-
ical changes in red and white muscle and liver
in the jack mackerel, Trachurus symmetrictts.
Fish. Bull. 69: 379-386.

271

THE TRANSPLANTING AND SURVIVAL OF TURTLE GRASS,
Thalassia testudinum, IN BOCA CIEGA BAY, FLORIDA'

John A. Kelly, Jr., Charles M. Fuss, Jr., and John R. Hall=

ABSTRACT

Turtle grass was transplanted to an unvegetated, dredged canal and a hand-cleared portion of a flour-
ishing grass bed. Complete or partial success was attained in 7 of 14 methods used. The best method,
in which short-shoots (rhizomes removed) were dipped in a solution of plant hormone (Naphthalene
Acetic Acid) and attached to construction rods for transplanting, was 100% successful and may be
suitable for general application.

Turtle grass, Thalassia testudinum, and other
marine grasses are an invaluable asset to the
marine ecosystem. They are primary producers
and form an essential ecological niche in which
a great number and variety of species find food
and shelter. They are also important agents
in the control of substrate erosion and the de-
positions of sediments (Stephens, 1966).

Uncontrolled dredging and filling of sub-
merged lands have destroyed many turtle grass
beds and their dependent fauna, some of which
are economically important. An immediate need
exists not only for sharply restricting further
destruction of sea grass beds but also for re-
placing lost beds. One method of replacing them
may be by transplanting sea grasses to areas
that are suitable for their growth or to areas
that are made favorable by soundly planned en-
gineering (Phillips, 1960; Strawn, 1961).
Areas surrounding spoil banks and finger-fill
canals (dredged canals between filled land mass-
es) would be suitable if they were constructed
to supply zones of optimum depth for growth of
marine grasses.

Unsuccessful earlier attempts to transplant
turtle grass in Tampa Bay showed that the main
problem was erosion by tidal currents. Turtle
grass is buoyant, and new transplants tend to

' Contribution No. 64 from the National Marine Fish-
eries Service Biological Laboratory, St. Petersburg
Beach, Fla. 3.3706.

' National Marine Fisheries Service Biological Lab-
oratory, St. Petersburg Beach, Fla. 33706.

work free of the sediments and float to the sur-
face when disturbed by water movement (Phil-
lips, personal communication)." Another ma-
rine plant, eelgrass (Zostera marina), was
transplanted successfully on the coast of Wash-
ington by Phillips (1967) and in the Aleutian
Islands by Jones* and McRoy' (personal com-
munication), but details on methods are not yet
published. Successful growth of turtle grass
under artificial conditions (Fuss and Kelly,
1969) led us to attempt transplanting it from
one field location to another as described in the
present paper.

Turtle grass spreads vegetatively by creeping
rhizomes (long-shoots) buried in the substrate
(Figure 1). Work by Tomlinson and Vargo
(1966) showed that this growth is dependent
entirely upon the vigorous activity of meriste-
matic tissue in the apexes of rhizomes. The
apex is also the only source of short-shoots (erect
lateral branches) that develop from buds at this
site. In the Miami area (Phillips, 1960) and
tropical parts of its range, the plants also re-
produce by flowering. Tampa Bay, however, is
near the northern limit of the flowering capa-
bihty of Thalassia (Phillips, 1960); thus, we

Manuscript received January 1971.

FISHERY BULLETIN: VOL. 69. NO. 2, 1971.

' Phillips, Ronald C, Department of Botany, Seattle
Pacific College, Seattle, Wash. 98119.

' Jones, R. D., Jr., Range Manager, Bureau of Sport
Fisheries and Wildlife, Aleutian Islands National Wild-
life Refuge, Cold Bay, Alaska 99571.

° McRoy, C. P., Institute of Marine Science Univer-
sity of Alaska, College, Alaska 99701.

273

FISHERY BULLETIN: VOL. 69, NO. 2

m ^"O"'- M

RHIZOME ,

iW-SHOOlJf

APEX

(lONG-SHOOl) i

IT //

^^

Figure 1. — External features of Thalassia testudinum.

confined our restoration studies to the trans-
plantation of adult plants. This paper describes
the procedures for and results of transplantation
of turtle grass into modified environments.

trol site was 95.5% sand (>62.5/x) and 4.5%
silt and clay (<62.5/Lt) on a dry weight basis.
At the planted areas of the finger-fill canals,
sediments averaged 98.6% sand and 1.4% silt
and clay. No analysis of the carbonate fraction
was made for these samples; however, all sites
had shell fragments, which appeared to be more
abundant in the canals than at the control site.

MATERIAL AND METHODS

The work was divided into two phases: Phase
I extended from July 1966 through August 1967
and phase II from April through October 1967.
In phase I, methods of deflecting and reducing
the force of tidal currents and waves in the vi-
cinity of transplants and of anchoring new trans-
plants in the substrate were tested. Concrete
building blocks were laid in parallel rows at
both transplant sites to form enclosed areas for
sheltering new transplants against the forces
of moving water (Figure 3). Plugs of grass
approximately 8 inches square (20 X 20 cm)

DESCRIPTION OF TRANSPLANT SITES

All experiments took place in the southern
end of Boca Ciega Bay, Fla., an elongate coastal
lagoon joined to Tampa Bay and separated from
the Gulf of Mexico by a line of barrier islands
(Figure 2). The area it encompasses is a par-
amount example of grass bed destruction by
hydraulic engineering (Hutton et al., 1956;
Phillips, 1960; Taylor and Saloman, 1968).

A rectangular area 8.2 by 21 m (27 by 7 ft)
in a large turtle grass bed was cleared by hand
to serve as the control site. Two other trans-
plant areas of the same size were in two adjacent
finger-fill canals in a large land-fill development.

Construction of houses had not begun along
the canals selected, and none was built during
the experiments. Boating in the canals was
light, and during periodic inspections we saw
no disturbance of the plants directly attributable
to man.

Sediments from transplant sites were an-
alyzed by particle size. A sample from the con-

FlGURE 2. — Locations of experiments (phases I and II,
and control area).

274

KELLY, FUSS, md HALL: TRANSPLANTING TURTLE GRASS

and containing four to five short-shoots were
dug from natural beds adjacent to the control
site. Three methods of transporting and anch-
oring the plugs were tried: (1) placing them
in tin cans, (2) balling them in burlap, and (3)
temporarily bagging the roots and rhizomes in
polyethylene, which was removed just before
planting.

A total of 120 plugs was transplanted — 60
at the control site and 60 at the finger-fill canal.
At both locations, 30 were placed inside and 30
outside of enclosures. Each group of 30 plugs
was planted three ways: 10 in cans, 10 in bur-
lap, and 10 unanchored (Figure 3).

Phase II consisted of testing additional an-
choring devices to hold individual sprigs of turtle
grass in the substrate of the finger-fill canal.
The devices were cast iron, 2-inch (5.1-cm)
pipe, brick, and construction rod. Sprigs used
in this study were single short-shoots with
leaves, many roots, and with or without a por-
tion of the parent rhizome. Also tested in phase
II was the plant hormone, NAPH (Naphtha-
lene Acetic Acid),° which is used for rooting
grass stolons and plant cuttings.

Sixty sprigs, obtained from the same natural
bed as the plugs in phase I, were washed and
prepared for the experiment by breaking entire
rhizomes from some, breaking only the apexes
of rhizomes from others, and leaving the rhi-
zomes attached and entire on others. Half of the
sprigs were placed in a 10% solution of NAPH
in seawater for 1 hr. The other half were left
untreated. The sprigs were planted in groups
to test various combinations of treatment and
non treatment with NAPH, presence and ab-
sence of apexes of rhizomes, presence and ab-
sence of rhizomes, and types of anchors ( Figure
4).

Sprigs anchored with construction rod had
no rhizomes. Sprigs anchored with pipe had
rhizomes that were buried in hand-dug holes;
whereas, sprigs anchored with brick were simply
placed on the surface of the substrate and their

POLYETHYLENE

' Manufactured by Nutri-Sol Chemical Company,
Tampa, Fla. 33609. References to trade names in this
publication do not imply endorsement of commercial
products.

Figure 3. — Details of concrete-block wave and current
barriers, tin-can anchors for plugs, and placement of
transplants at planting sites.

rhizomes held in contact with the sediment by
the weight of the brick.

RESULTS

Transplants were considered successful if
they established themselves in the new envi-
ronment and exhibited new rhizome growth
(Figure 5) . Individual sprigs met these criteria
if short-shoots appeared healthy, had new roots,
and had either given rise to a new rhizome or
were still part of an old long-shoot with an active
apex. Plug transplants (phase I) were con-
sidered successful if only one of the short-shoots
met the above criteria.

275

FISHERY BULLETIN: VOL. 69, NO. 2

CONSmUCTJON
ROD

APEXES

o
oo

w

o
oo

w

o
oo

w o

o

oo

w o

o

o

NR

0

o

o

NR

o

(TTT]

W

Em
Em

W - WITH

[ O - WITMOUf

NR NO RHIZOME

OlD SHORI-SHOOT

NEW SHORI-SHOOI
APEX

NEW RHIZOME

(LONG-SHOOI)

NEW ROOTS

Figure 5. — New rhizome, root, and short-root growth
on a sprig of turtle grass transplanted without an intact
rhizome apex.

made in the finger-fill canal in phases I and II,
respectively, and 40 Sr of the transplants made
in the control bed (Tables 1 and 2). Transplant
attempts made with burlap in phase I were not
included in the above percentages because all
failed within 1 month.

FiGUKE 4. — Details and treatment of sprigs anchored
by pipe, brick, and construction rod; and placement of
transplants at planting sites.

Plugs in phase I planted July 1966 were re-
moved from the sites late in August 1967, ap-
proximately 13 months after planting. Six of
the 40 transplants at the canal area and 16 of
the 40 at the control area were successful
(Table 1).

Planting individual sprigs of turtle grass in
phase II yielded similar results. Of the 60
sprigs planted in the second canal in April 1967
and removed in mid-October 1967 (about 6
months after they were transplanted), 11 were
successful (Table 2).

Successful new growth of rhizomes repre-
sented 15 and 18'; of the number of transplants

EROSION CONTROL

Results of planting plugs within concrete-
block enclosures were completely different in
the finger-fill canal and grass bed locations
(Table 1). In the canal the only successful
transplants grew within the protection of the
block enclosures; none planted without this pro-
tection survived, and most of the latter failed
within the first 6 months of the experiment.
Most of the successful plugs placed in the con-
trol area were planted outside the concrete
blocks and, throughout the study, appeared to
be in better condition than those inside the en-
closures. The enclosures fulfilled their purpose
in the canal but ai)i)eared detrimental in the
control area. In the latter region, surrounding
grass beds apparently provided suflicient pro-
tection from water movement. Enclosures in

276

KEXLY. FUSS, and HALL: TRANSPLANTING TURTLE GRASS

Table 1. — Surviving transplants, successful transplants, and seasonal mortality of transplant-
ed plugs of Thalassia in the finger-fill canal and the control site, phase I, July 1966 through
August 1967.

Method of

protecting

and anchoring

plants

Surviving plants

Mortality

Winter Spring Summer

Inside concrete block enclosures;
Anchored in cons
Unanchored

Totol

Outside concrete block enclosures:
Anchored in cons
Unanchored

Total
Grand total

No. % No.

Finger-fill canal site

No.

No.

No.

10
10

0
0

3
3

30
30

3
2

4
4

0
0

0

I

20

0

6

30

5

8

0

1

10
10

0
0

0
0

0
0

9

10

1
0

0
0

0
0

20

0

0

0

19

I

0

0

Inside concrete block enclosures:
Anchored in cans
Unanchored

Total

Outside concrete block enclosures:
Anchored in cans
Unanchored

Total
Grand total

10
10

1
2

3
0

30
0

5
4

1
1

0
2

0

1

20

3

3

15

9

2

2

I

10
10

1
2

7
6

70
60

0

1

1

1

0
0

1

0

20

3

13

65

1

2

0

1

40

10

1 Transplants survived but did not exhibit new rhizome growth.
3 Transplants exhibited new rhizome growth.

the control area often filled with a heavy accumu-
lation of light-robbing algae, dead grass, and
other detritus, which quickly resulted in burial
and death of the entire transplant.

ANCHORING METHODS FOR PLUGS

Of the plugs anchored with tin cans, 50%
were successful at the control site, but only 15%
in the canal (Table 1) . None of the plugs plant-
ed in cans outside of the concrete-block enclo-
sures survived. Cans were thus ineffective
against currents unless used in conjunction with
the concrete-block current barrier.

Plugs transported in polyethylene bags and
then directly transplanted served to evaluate the
effect of tin cans. We noted no adverse effects
from the metal in the cans. The ratio of suc-
cesses of unanchored to anchored transplants
was 3:5.

The reasons for the rapid failure of plugs
with roots and rhizomes wrapped in burlap is

unknown. Possibly decomposition products of
the decaying burlap, such as H2S, or toxic chem-
icals in the material caused the plants to die.

ANCHORING METHODS FOR SPRIGS

In phase II sprigs were planted with added
anchoring devices but without the aid of the
wave and current barriers.

Construction rod was the most effective device
used to anchor sprigs. It was the easiest to
handle because all sprigs fixed to it were trans-
planted without rhizomes and were simply fas-
tened to the rod with plastic-coated wire and
inserted into hand-dug holes in the substrate.
Of the 12 sprigs anchored with rod, only the 6
that had been treated with the hormone NAPH
became established (Table 2). Sprigs that did
not survive failed early in the experiment and
simply disappeared, probably because they were
dislodged by water movement in the canal be-
fore roots were developed.

277

FISHERY BULLETIN: VOL. 69, NO. 2

Table 2. — Surviving transplants, successful transplants, and monthly mortality of transplanted sprigs of Thalassia
in a finger-fill canal, phase II, April through October 1967.

Method of anchoring
and treoting

Trons-
plants

Surviving plants

Mortality!

Unsuccessful*

Successful^

May

July

Aug.

Sept.

Pipe*

With apexes, with NAPH
With opexes, without NAPH
Without opexes, with NAPH
Without apexes, without NAPH

Total

Bricks

With opexes, with NAPH
With apexes, without NAPH
Without opexes, with NAPH
Without opexes, without NAPH

Total

Construction rod^
With NAPH
Without NAPH

Total
Grand total

60

n

0

0
33.3
16.7

25

24

7

3

12.5

6

6

0

2

0

6

4

2

33 3

0

0

0

0

0

6

0

0

0

0

6

0

0

0

6

0

0

0

0

6

0

0

0

6

0

0

0

3

3

0

0

0

24

4

2

8.3

3

15

0

0

0

6

0

6

100.0

0

0

0

0

0

6

0

0

0

0

4

2

0

0

12

0

6

50.0

0

4

2

2

0

* Mortality not observed in June.

' Transplants survived but did not exhibit new rhizome growth.

* Tronsplants exhibited new rhizome growth.

* Rhizomes were buried; two sprigs per anchor.

^ Rhizomes were not buried; three sprigs per anchor.

« Rhizomes were removed before planting; tv/o sprigs per anchor.

Pipe and brick were poor anchors. The sprigs
anchored with pipe were transplanted with their
rhizomes and special care was required in bury-
ing them to avoid breakage. Almost half of the
24 sprigs held with pipe lived to the end of the
experiment, but only 3 exhibited new rhizome
growth (Table 2) . Sprigs secured to the bottom
with brick were not buried but were simply laid
on the bottom and the substrate was scooped
over them by hand. They were also transplanted
with their rhizomes but were difficult to handle
because of their tendency to slip out from under-
neath the brick before they were finally set in
place. Six of the 24 sprigs lived for awhile,
but only 2 were successful. Sprigs that were
anchored with brick and failed did so shortly
after they were planted. Water movement prob-
ably eroded away enough sediment to allow
the buoyant sprigs to float from under the brick.

TREATMENT OF TRANSPLANTS IN PHASE II

The effect of NAPH on marine grasses is ap-
parently similar to its effect on terrestrial plants,
primarily inducing rapid and heavy rooting.

Ten of the 11 sprigs producing new rhizomic
growth were treated with it (Table 2) . Because
of the small number of transplants attempted
and successes achieved, we cannot definitely
establish the significance of NAPH in such ex-
periments. Our results indicate to us, however,
that NAPH was one of the main factors con-
tributing to transplant success.

Particular care was taken to avoid damaging
rhizomes and rhizome apexes of sprigs before
and during transplanting. No apparent advant-
age was gained from this care ; invariably old
rhizomes withered away and were replaced by
new ones developing from the bases of the short-
shoots.

MORTALITY OF TRANSPLANTS

Visual checks made throughout the year
showed that the most critical period for the
survival of turtle grass was during the first
3 months after transplanting. In phase I, mor-
tality of plugs planted in the canal was 60%
through the third month (October), 22.5%
through the sixth month (January), zero

278

KELLY. FUSS, and HALL; TRANSPLANTING TURTLE GRASS

through the 3-month period February-April, and
2.5Cf during the remainder of the study. Losses
in the control area for the same time intervals
were 25, 10, 5, and 5%, respectively.

Mortality experienced during phase II was
also high. Over half (BTSr ) of the sprigs trans-
planted in April failed before the end of the
third month (July) and T;} from August to Oc-
tober. Additional failures within this phase
might have occurred had the experiment con-
tinued through the winter.

CONCLUSIONS AND
RECOMMENDATIONS

Our experiments resulted in the first success-
ful field transplantation of turtle grass. All
new short-shoots produced by transplants were
from the new rhizome apexes (Figure 5). This
finding supports the observations of Phillips
(1960) and Tomlinson and Vargo (1966) that
buds on the rhizome apex are the only source
of short-shoots. It is also in agreement with
findings in the tank culture of Thalassia (Fuss
and Kelly, 1969). Continuous growth of turtle
grass depends on the activity of vigorous rhi-
zome apexes, but the apexes do not contain the
only meristematic tissue in the plant. New
rhizomes can be produced from residual meris-
tematic tissue present in the old short-shoot.
Phillips (1960) observed such branching in the
field and stated that it could account for the
continued growth of turtle grass if the apex
of the rhizome were damaged or lost, but be-
lieved that the frequency of this branching was
small. Tomlinson and Vargo (1966) also re-
ported that vegetative branching in short-shoots
occurs and indicated that it is rare.

Undamaged leaves may not be required for
sprig transplanting. Further studies are needed
to determine, for example, if the leaves could be
cut back to reduce the surface area and buoy-
ancy of the sprig. Results of investigations in
Boca Ciega Bay by Prest, Saloman, and Taylor'
show that turtle grass leaves clipped as much

as 50% of their original height (about 26 cm)
would regrow as much as 3 to 4 cm (1.2 to 1.6
inches) per week. It would thus appear that
physical damage to leaves is quickly overcome
by regrowth of the plant.

We have shown that turtle grass can be trans-
planted in the field and that it will grow in an
area denuded by coastal dredging. A simple
transplant method using only the short-shoots
of this grass, the hormone NAPH, and con-
struction rod was 100% successful (six trans-
plants) in a land-fill finger canal (Table 2). This
method has value for use in restoring Thalassia
to estuarine environments when conditions fa-
vorable for plant growth exist or can be arti-
ficially created. We must emphasize however,
that no large-scale transplant program has been
attempted. Moreover, recent observations (No-
vember 1970)' of vegetative growth into our
original control site indicate that turtle grass
spreads at an annual rate of only 20 cm (8
inches) or less.

LITERATURE CITED

Fuss, C. M., Jr., and J. A. Kelly, Jr.

1969. Survival and growth of sea grasses trans-
planted under artificial conditions. Bull. Mar.
Sci. 19: 351-365.
HuTTON, R. F., B. Eldred, K. D. Woodburn, and R. M.
Ingle.

1956. The ecology of Boca Ciega Bay with special
reference to dredging and filling operations. Part
I. Fla. State Bd. Conserv., Tech. Ser. 17, 87 p.
Phillips, R. C.

1960. Observations on the ecology and distribution
of the Florida seagrasses. Fla. State Bd. Con-
serv., Mar. Lab. Prof. Pap. Ser. 2, 72 p.

1967. On species of the seagrass, Halodule, in
Florida. Bull. Mar. Sci. 17: 672-676.
Stephens, W. M.

1966. Life in the turtle grass. Sea Frontiers 12:
264-275.
Strawn, K.

1961. Factors influencing the zonation of sub-
merged monocotyledons at Cedar Key, Florida.
J. Wildl. Manage. 25: 178-189.

' Unpublished data on file National Marine Fisheries
Service Biological Laboratory, St. Petersburg Beach,
Fla. 33706.

' Unpublished data on file National Marine Fisheries
Service Biological Laboratory, St. Petersburg Beach,
Fla. 33706.

279

FISHERY BULLETIN: VOL. 69. NO. 2

Taylor, J. L., and C. H. Saloman. Tomlinson, P. B., and G. A. Vargo.

1968. Some effects of hydraulic dredging and 1966. On the morphology and anatomy of turtle

coastal development in Boca Ciega Bay, Florida. grass, Thatassia testudinum (Hydrocharitaceae).

U.S. Fish Wildl. Serv., Fish. Bull. 67: 213-241. '^^ Vegetative morphology. Bull. Mar. Sci. 16.

748-761.

280

EFFECT OF DIETARY FISH OIL ON THE FATTY ACID COMPOSITION
AND PALATABILITY OF PIG TISSUES'

Robert R. Kifer,° Preston Smith, Jr..'' and Edgar P. Young"

ABSTRACT

Basically, this report deals with the problem of a "fishy" flavor in the meat of pigs, which sometimes
results when pigs are fed fishery products, such as fish meal, above a certain concentration in the diet.

In this study, pigs were fed diets containing fish oil to investigate specifically: (1) the effect, on
the taste of the meat, of feeding pigs fish oil, (2) the effect, on the taste of the meat, of withdrawing
the oil from the diet at given times, (3) the fatty acid composition of the various body tissues of the pigs,
and (4) the relation of composition to the taste of the meat.

The principal findings of the study were: (1) The amount of the fish oil co3 fatty acids fed and de-
posited was significantly positively correlated with the weighted organoleptic score' when the pigs were
fed the oil containing diets to a market weight of 90.9 kg. (2) Removal of the fish oil from the pigs'
diets when the pigs obtained body weight (of either 68.0 or 79.5 kg) resulted in a loss of the signifi-
cant positive correlation above. (.3) Differences in the degree of unsaturation and in fatty acid comp-
osition were found among the oils in the tissues examined. (4) A signifiant positive correlation was
obtained between the quantity of the characteristic fatty acids (&>3) of fish oil fed and the quantity de-
posited in three of the four tissues examined, the exception being the longissimtis dorsi tissue.

Both the processors of fishery industrial prod-
ucts and the feed manufacturers who use the
products are sometimes confronted with the
problem of a fishy flavor in the carcasses of
animals fed diets in which these products are
included. Fish oil fed directly to the animals
or fed as a residual component of fish meal or
of fish solubles has been shown to pi-oduce an
off-flavor under certain conditions (Banks and
Hilditch, 1932; Hilditch and Williams, 1964).
Through practical research, the problem has
been partly solved by reducing the quantity (that
is, the percentage) of fish oil in the diet or by
eliminating the oil during an interval of time
before the animals are marketed (Frazer, Stot-
hart, and Gutteridge, 1934). This latter tech-
nique is not always effective, especially when
fairly high (8.25'^r) levels of fish oil have been
fed (Anglemier and Oldfield, 1957).

' Contribution number 4304 Maryland Agriculture
Experiment Station, Department of Animal Science,
Project number C33-Scientific Article A-1586.

' National Marine Fisheries Service, Washington,
D.C. 20235.

" Department of Animal Science, University of Mary-
land, College Park, Md. 20740.

' Note the organoleptic score increased with greater
unacceptability.

Manuscript received January 1971.

FISHERY BULLETIN: VOL. 69. NO. 2, 1971.

Investigations to relate more specifically the
causal agents of the oflF flavor resulting from
the use of fish oil have led to the hypothesis
that the long-chain polyunsaturated fatty acids
of the C20-22 series commonly found in fish oil
are pi-ecursors of the flavor-producing compo-
nents (Banks and Hilditch, 1932; Marion and
Woodroof , 1963 ; Miller, Gruger, Leong, and
Knobl, 1967). Investigations by the Animal
Nutrition Unit of the Bureau of Commercial
Fisheries (now the National Marine Fisheries
Service) Technological Laboratory, College
Park, Md., using chickens, have indicated that
a further partitioning of the C2(i 22 fatty acid
series results in a positive correlation between
individual fatty acids of these series deposited
and the detection of the off-flavor (Miller et al.,
1967).

In a continuation of this line of investigation,
the work reported here was divided into four
experiments. Their purposes were to determine
the following information:

1. The relation between the menhaden-oil fat-
ty acid fed and the fatty acid pattern of tissue
samples (namely, those of the outer and the in-

281

FISHERY BULLETIN: \'0L 61. NO 2

ner backfat, the longissimus dorsi muscle, and
the liver) of pigs fed various diets with and
without menhaden oil and for various intervals
of time before they are marketed.

2. The organoleptic effect of the different di-
etary levels of menhaden oil on the meat of the
pigs and the retention or disap])earance of the
off-flavor by removal of menhaden oil from the
diet of the pigs when they reach a body weight
of 68.0 or 79.5 kg and are subsequently marketed
when they reach a weight of 90.9 kg.

3. The relation, if any, between the detection
of off-fiavor and the pattern of fatty acid de-
liosition in the tissue samples.

4. The metabolic interrelation of fatty acids
of the various fatty acids of the omega families
(coS, 0)6. 0)9).

RELATION BETWEEN MENHADEN OIL

FATTY ACIDS FED TO PIGS AND

DEPOSITIONAL PATTERNS OF THESE

FATTY ACIDS IN THE PIG TISSUES

Callow (1935, 1938) indicated that the rate
of deposition of fat in pigs is correlated with
the iodine number of the fat and that slower
growing pigs deposit a more unsaturated fat.
Accordingly, we felt that our exiierimental pigs
should be handled so that they would develop
uniformly, thus minimizing the variation in the
composition of depot fat resulting from differ-
ential rates of growth.

The first part of this experiment was a gen-
eral study to monitor the uniformity of growth
of the pigs and of the development of their car-
casses. That is. we wanted to determine wheth-
er the diets fed and our treatment of the pigs
would I'esult in any abnormalities that might
invalidate the specific findings in this first ex-
periment and in the other three experiments
to follow.

UNIFORMITY OF GROWTH OF PIGS AND
OF DEVELOPMENT OF CARCASSES

Uniformity of Growth

Described here are the diets, the allotment
and management of the pigs, and the statistical
analyses used.

The diets were balanced on an equal-protein
and equal-calorie basis and were fortified to sup-
ply all the known nutrients required by pigs.
Crude menhaden fish oil that had been stabilized
with butylated hydroxy toluene' was added at
levels of 0.4 Sr to 1.4 '^r. The oil replaced var-
ious proportions of cerelose and Solka Flox' to
give isocaloric and isonitrogenous diets (Table
1). The diets were mixed in a ribbon-type mix-
er and were pelleted weekly through a 12-mm
die. Steam was not used in the pelleting pro-
cess. Table 2 shows the gas-liijuid chromato-
graphic analyses of the oil and of the diets fed.

" Level of aildition is trade secret.
" Trade names are used merely to simplify descrip-
tions; no endorsement is implied.

Table 1. — Diet formulation used in experiment to determine the dietary level of menhaden oil that will impart off-
flavors to the meat of pigs.

Concentration

of the g

ven ingredients

in the diet

when th

e percer

tage

ingredients

of menhaden oil in

the diet

was:

0

0.4

0.6

0.8

I.O

1.2

1 '-^

%

%

%

%

Te

%

%

fixed basal ingredients:

Corn US #2

67.0

67,0

67.0

67.0

670

67.0

67.0

Soybean oil meal

203

20.3

20.3

20.3

20.3

20.3

20.3

Alfalfa leaf meal

3.0

3.0

3.0

3.0

3 0

3.0

3.0

Dicolcium phosphate

2.0

2.0

2.0

2.0

20

20

2.0

Salt {trace mineroD*

.6

.6

.6

.6

.6

.6

.6

Vitamin mix^

.2

.2

.2

.2

.2

.2

J2

Variable ingredients;

Cerelose

6.9

5.5

4.8

4 1

3.4

2.7

2.0

Cellulose

1.0

1. 5

20

2.5

3.0

3.5

Menhaden oil

—

,4

.6

.8

1.0

1.2

1.4

Sufficient (race minerals and vitamins were present to meet the reciuiremenrs of the Notional Reseorch Council.

282

KIFER, SMITH, and YOUNG: EFFECT OF DIETARY FlSil OIL

Table 2. — Gas chromatographic analysis of methyl esters of the fatty acid components of the menhaden oil and

of the diets fed to pigs.

Folly
QCid

Concenlrolion
of Ihe given
folly acid in

menhaden oil

Concenlrolion of Ihe given folly acid

in the diet when Ihe percentage of

menhoden oil in the diet wos:

0

0.4

1 0.6 1

0.8

1.0

1.2

1.4

%

%

%

%

%

%

%

%

M4:0

5.96

0.17

1.03

1.42

1.62

1.98

2.05

2.51

Mil

..

0.05

0.05

006

0.06

0.08

0.08

0,10

15:0

0.34

0.13

0.05

0 15

0.21

0.06

0.06

0.07

?

air

0.06

0.17

0.05

0.06

0.27

0.27

0.31

15:1

0,09

__

tr

Ir

tr

Ir

tr

tr

16:0

13,10

11.77

13.15

13 59

13.26

14.10

13.46

14.85

= 16:1 a'7

10.36

0.31

1.31

1.59

1.86

2,31

2.34

2.85

17:0

0.64

0.16

0.21

0.24

026

0,26

0,27

0.31

7

__

0.11

tr

tr

tr

Ir

tr

tr

1(5:2

__

_^

.^

__

__

17:1

1.06

0.10

0.23

0,29

0.32

0,36

0.39

0.4S

?

0.10

0.04

0.04

0,03

0.05

0.05

18:0

4.36

2.70

2.86

2.95

3.17

3-16

3.26

3.17

18:1 019

27.59

27.45

24.97

24.06

23.57

22,90

22.63

20.44

19:0

1,45

0.10

0.27

0.35

0.42

0,43

0.48

0,58

18:2 u6

1.57

51.22

44.60

41.86

40.96

39.14

38.22

35.22

?

0,32

tr

tr

tr

tr

tr

tr

tr

?

024

on

0.13

0.14

0.18

0.12

0.16

0.17

20:0

0,31

0.78

0.78

0.75

0.81

0,65

0.68

0.69

18

3 o'3

0.94

3.31

2.60

2.89

2.75

2,62

2.49

2.97

20

1

1.32

0.40

0.68

0.73

0.76

0-75

0.79

0.86

18

4o-3

289

0.50

0.65

0.76

0,84

0.94

1.11

7

0.37

0.07

0.17

0.19

0.24

0,21

0.27

0.30

20:2 u9

0.18

0.07

O.II

0.12

0.13

0,07

0.13

0.14

20:2 0)6

0.06

tr

tr

tr

ir

Ir

Ir

0.06

20:3 o9

0.13

tr

0.08

0.08

009

0,05

0.10

0.11

22:3 ^6

0.05

Ir

tr

0,04

ir

Ir

tr

tr

20:4 o;6

0.69

0.22

0.37

042

0.42

0,37

0.45

0.53

22:1 oj2

0.30

tr

0.12

0,09

0.12

0,07

0.13

0.16

20:4 o;3

1.25

0.08

0.29

0,34

0.41

0,42

0.52

0.59

20:5 0.3

12.95

0.11

2.19

2,95

3.35

3,96

4.28

5.01

7

__

0.23

0.40

0,26

0.34

0,15

0.28

0.40

24:0

0 09

__

tr

tr

tr

Ir

tr

tr

22:4 w6

059

0.29

0.53

0.47

0.48

0,46

0.54

0.57

22:5 oj6

0,43

..

tr

0.24

Ir

0,26

0.46

0.45

22:5 oj3

1.63

0.40

0.50

0.63

0,65

0.77

0.86

22:6 0)3

8.47

—

1.71

2.49

2.76

3,29

3.44

4.14

"14:0" meons that the fatly acid has 14 carbon atoms per molecule ond no unsoluroted bond.

"16:1 oj7" means thot in the folly acid Ihe unsaturated bond occurs at Ihe seventh bond from the terminal methyl group.

"Ir" means trace.

Seven Yorkshire gilts each weighing about
27.3 kg were allotted to each of the seven treat-
ment groups. Two of the seven pigs of each
menhaden-oil group were fed the appropriate
oil-containing diet until they attained a body
weight of 68.0 kg and then were fed the control
diet until they attained a body weight of 90.9
kg. Similarly, two additional pigs of each men-
haden-oil group were fed the appropriate oil-
containing diet to a body weight of 79.5 kg and
then also were fed the control diet to a body
weight of 90.9 kg. The remaining three pigs
were continuously fed the various test diets con-
taining menhaden oil until they each also at-
tained a body weight of 90.9 kg. Feed was

offered twice a day (for a maximum of 1 hr
per feeding) to the pigs in individual crate-
type pens. This interval of time was considered
to be adequate to permit the pigs to eat the same
total amount of food that they would have eaten
ad lib. Data on rates of gain and consumption
of feed were recorded weekly.

Data obtained on rates of gain and utiliza-
tion of feed were subjected to an analysis of
variance (Snedecor, 1956).

Table 3 presents the rates of gain, utilization
of feed, and quantity of oil consumed by the pigs
fed diets containing the various percentages of
menhaden oil.

Results of the analyses of variance for each

283

FISHERY BULLETIN' : \ OL. 09. NO- I

Table

-Rates of gain, utilization of feed, and quantity of oil consumed by pigs fed diets containing
various percentages of menhaden oil.

Relative

amount

of nienhaden

Average

doily
gain

Ratio
of feed
to gain

Mean quontity of oil consumed
by pigs fo o body weight of:

oil in diet

Mean

SD

Mean SD

68.0 kg 1 79.5 kg 90.9 kg

■/o

kv.

H

*?

H

i:%

0

0 63

0 065

3.45

0.136

0

0

0

0.4

.64

065

3.26

.105

0 52

0.62

0.85

0.6

.60

,047

3.34

.093

0.85

0.96

1.30

0.8

.64

.045

3.47

095

1.03

1 32

1.90

1.0

.64

.025

3.26

.080

1.20

1.48

2.16

1.2

.66

.068

3.28

.100

1.53

1.78

2,70

1.4

.64

.044

3.25

.084

1.61

2.12

3.22

criterion of evaluation indicate that tlie.se cri-
teria did not differ significantly.

Development of Carcasses

The .yield of lean cuts was obtained as an
accumulative value for the four commercial lean
cuts — namely, hams, loins, shoulders (picnics),
and Boston butts. Ci'os.s-sectional measure-
ments of the longlsi^hnus dorsi muscle of the
loin were obtained by cutting- the loin at the
10th rib, tracing- the muscle area onto pajjer,
and measuring the perimeter of the area by
means of a ])lanimeter to convert the encom-
passed area to square centimeters. The thick-
ness of the backfat was based on an average of
three measurements taken at positions opposite
the first rib, the last rib. and the last lumbar
vertebra.

Table 4 presents the data on the dressing per-
centage, lean-cut percentage, loiu/lssiiniis dorsi
area, and backfat thickness obtained from pigs
fed the various diets containing menhaden oil.
The analyses of variance for each criterion of
evaluation indicate that no significant differ-
ences occurred among these factors that reveal
the growth reaction of the pigs to their diet.

Thus the pigs develojied uniformly during the
feeding trials. Consequently any differences
that may be found in the fatty acid composition
of the tissues should be related to the oil in the
diet rather than to markedly different growth
of the pigs.

RELATION OF DEPOSITIONAL PATTERNS
TO FATTY ACIDS IN OIL FED TO PIGS

In this section, we are concei-ned with the fol-

lowing three sulyects: (1) the differences
found in the degree of saturation both within
and among tissues, (2) the fatty acids identified,
and (3) the relations of the quantity of fatty
acids fed to the quantity deposited in the var-
ious tissues.

Differences Found in Degree of Saturation Both
Within and Among Tissues

Described here are (1) the tissue samjiles
used, (2) the extraction of lipids, (.3) the prep-
aration of methyl esters, and (4) the quantita-
tive gas-liquid-chromatographic technique.

Samples were taken from the outer and the
inner backfat tissue, the lo)igissi>nus dorsi, and
the liver in the following manner. From each
animal, a sample of backfat was obtained dor-
sally to the 10th to 12th ribs. This sample was
then divided into the "outer" and "inner" fat
layers. Samples of the muscle were taken from
the eye of the Io)u/issimiis dorsi at the 10th rib.
Samples of the liver were taken from the right
central lobe. All samples were i)!aced in vials,
Ijrotected with nitrogen, and held at —20° C
until the lipids were extracted from them.

The lipids were extracted from the samples
by the homogenization of the tissue in a mechan-
ical blender with a 2: 1 mixture of chloroform
and methanol for 2 min. The solvent mixture
was added in the proportion of 5 ml of mixture
to 1 g of sami^le. The slurry was filtered through
a Buchner funnel, and the filter paper and the
nonfilteral)le portion were re-extracted for an-
other 2-min period. The filtrate was evaporated
in a rotary vacuum evaijorator over a 60° C wa-
ter bath. The dried sample was redissolved in

284

KIFER. SMITH, and YOUNG; EFFECT OF DIETARY FISH OIL

Table 4. — Dressing percentage, lean-cut percentage, longistiimns dorsi area, and backfat thickness obtained from

pigs fed various diets containing menliaden oil.

Relative

Relative

yield of;

Lonsiilimul
doni area

Backfar

amount
of menhaden

Dressing

Lean c

jtsi

thickness

oil in diet

Mean

SD

Mean

SD

Meon SD

Mean SD

%

%

%

%

%

cm^ rm"

cm cm

0

83 8

±2.36

38.9

±2.45

32.39 ±5.78

3.56 ±062

0.4

83.4

±1.23

40.2

±1.68

33.68 ±4.83

3.30 ± .45

0.6

82.0

±1.89

39.6

±1.07

31.87 ±3.68

3.61 ± .19

0.8

83.1

±1.06

39.4

±1.32

30.78 ±5.08

3.61 ± ,29

I.O

82.7

±1.62

40.1

±0.88

32.78 ±4.39

3.30 ± .27

1.2

82.0

±2.21

38.3

±2.14

31.74 ±4.00

3.53 ± ,62

1.4

82.1

±1.86

38.1

±1.61

30.91 ±5.19

3.65 ± .40

petroleum ether (30° to 60° C boiling point),
poured into a separatory funnel, and washed
twice with a 20^^ solution of NaCl. The layer
of petroleum ether was evaporated in the rotary
evaporator, and the e.xtracted fat was trans-
ferred to containers in which it was protected
by nitrogen and was stored at — 20° C until
methyl esters were prepared from it for analysis.

The methyl esters of the fatty acids were pre-
pared as follows:

Five ml of anhydrous methanol and about 50
mg of freshly cut and shiny sodium were placed
into a small test tube. After the sodium had
reacted, six to eight drops of the extracted oil
were added and heated to reflux on a steam bath
for 2 min with agitation. The end point of the
reaction was signaled when the solution became
clear.

The reaction solution was quenched with 5 ml
of distilled water and was transferred to a sep-
aratory funnel. The mixture was extracted with
two 10-ml portions of petroleum ether (30° to
60" C boiling point). The final water layer was
discarded, and the two petroleum ether extracts
were combined. The petroleum ether solution
was washed with 10 ml of 5 ""r aqueous HCl so-
lution. The acid wash was followed by succes-
sive washes with 15-ml and 10-ml aliquots of
20''r NaCl solution. The washing was com-
pleted when pH paper tested neutral.

The ethereal solution of methyl esters was
dried over 3 g of anhydrous Na2S04, filtered,
and evaporated over a 60° C water bath, using
a vacuum rotary evaporator.

To check for purity, we made a thin-layer

chromatogram of the ester solution using silicic
acid paper. Methyl myristate was used as the
control. A solution of 90 parts petroleum ether,
10 parts ethyl ether, and 1 part formic acid was
used to elute the esters. The chromatogram was
develo])ed in iodine vapor.

Methyl esters of pure fatty acids were used
as reference standards for the C14-24 saturated
acids, Cii; -:24 monoenoic acids, plus linoleic, lino-
lenic, ai'achidonic, eicosapentaenoic, and docosa-
hexaenoic acids. Also concentrates of 16: 2, 16:3,
16:4, and 18:4 methyl esters that were obtained
by fractional distillation and urea-inclusion com-
pound fractionalization were used as reference
standards." As a secondary reference mixture,
methyl esters from whole menhaden oil were also
analyzed. From a plot of the logarithms of the
retention times (relative to stearate) versus the
number of carbon atoms, nearly linear relations
were observed for homologous series (Farquhar,
Insull, Rosen, Stoff'el, and Ahrens, 1959). Iden-
tifications were further verified by applying the
graphical method of James (1960) for analyses
on columns jiacked with diethylene glycol succi-
nate polyester and Apiezon L. These plots pro-
vided the necessary reference data for identifi-
cation of the various tissue lipids analyzed."

' Tlie staff of the National Marine Fisheries Service
Technological Laboratory, Seattle, Wash., made the
fractional distillations and urea-inclusion compound frac-
tionations.

' The fatty acids of the oil fed and of the animal
tissues were identified initially in collaboration with the
staff of the National Marine Fisheries Service Techno-
logical Laboratory, Seattle, Wash.

285

FISHERY BULLETIN: VOL. 69, NO.

Methyl esters of fatty acids taken from the
various tissues were analyzed with an F&M Bio-
medical Model 400 gas chromatograph. The in-
strument was equipped with a hydrogen flame
detector. The column used was comi)osed of 4.0-
mm ID by 243.8-cm Pyrex glass containing 5.0'^ r
(by weight) of diethylene glycol succinate poly-
ester (DEGS from Wilkens Instrument and Re-
search Inc.) supported on 80- to 90-mesh acid-
base washed and siliconized flux-calcinated
diatomaceous eai-th (Anakron ABS). The op-
erating conditions were as follows: column
temperature, 165° C; flash-heater temperature,
285° C; detector temperature, 200° C; and in-
itial attenuation that corresponds to 10 to 14

amp full-scale deflection. The inlet pressure
of the column measured 40 psi of helium, the
flow measured 53 ml per min at the outlet of
the column. The size of the injected sample was
about 0.12 juliter.

The area-percent method was used to deter-
mine the corresponding peak areas of the curves
obtained from the gas-liquid chromatographic
recorder. The fatty acid composition (in aver-
age percentage) of each sample was calculated
by multiplying peak height by retention time
and then multiplying this product by 100 and
dividing by the total area.

Certain diff'erences were obtained in the total
degree of saturation and quantity of specific

Table 5. — Summary of gas-liquid cliromatographic analyses indicating comparative degree of unsaturation and
quantity of selected fatty acids within and among the tissues obtained from pigs fed either 0% or 1.47c dietary
menhaden oil.

Type of fatty octd

Concentration of the vorious fatty acids in the vorious tissues
when the relative amount of menhaden oil in the diets was:

0%

Backfat

Inner
tissue

Outer
tissue

Longijiimul
dorsi tissue

Liver
tissue

1 .4%

Backfat

Inner
tissue

Outer
tissue

Longiisimus
dorti tissue

Liver
tissue

%

%

%

%

%

%

%

%

Saturated fatty ac

ids

34.56

28.37

33.74

34,63

35.42

28.77

33,05

34.66

Unsaturated fatty

acids

65.44

71.63

62,82

65,37

64.58

71.23

64,62

65.34

Unsaturoted bond

in

the fatty acids:

I

47.68

49.03

39,38

17,53

47.17

46.16

45,96

15.44

2

16,35

20.49

14,40

16.85

17.39

20.75

11.46

17.43

3

0.93

1.40

1.37

2.35

1.40

1.73

1.15

1.85

4

0.40

0.72

4.95

19.08

0.84

0.88

3.27

12.80

5

0.19

0.27

2.03

2.96

0.80

1,53

2.17

8.52

6

of

0.03

0.05

0.69

2.26

0.40

0,50

0.62

8,11

Equivalent degree

unsoturotion in

the

fatty acids:

1

47,68

49.03

39.38

17.53

47.17

46,16

45.96

15.44

2

32.70

40.98

28.80

33.70

34.78

41,50

22.92

34.86

3

2.79

4.20

4.11

7.05

4.20

5,19

3.45

5,55

4

1.60

2.88

19,80

76.32

3.36

3,52

13.08

51.20

5

095

1.35

10,15

14.E0

4.00

7,65

10.85

42.60

6

ed

0.18

0.30

4,14

13.56

2.40

3,00

3.75

48.66

Total

85.90

98.74

106,38

162.96

95.91

107,02

99.98

198.31

Individually select

fatty acids:

16:0

19.90

18.49

21,78

13.04

20.39

18,64

19.62

12.80

18:0

12.18

7.78

9,24

19.37

12.49

8,08

10,74

18.76

18:1 u9

43.67

44.94

34,33

15 86

40.52

42,04

41,16

13.57

18:2 (..-d

15.07

18,99

13,24

15.27

16.18

19.40

10.47

15.87

18:3 li3

0.74

1.18

0,59

0.44

1.02

1,37

0.52

0.57

18:4 u6

0.34

0.49

2,44

18.29

0.32

0,41

I.6I

12.15

20:4 0.-3

0.06

0.08

2.42

0.49

0.20

0,31

1.61

0.54

20:5 k3

0.09

0.13

0.98

0.51

0.27

0,52

1.12

4.18

22:5 f3

0.10

0.14

1.05

2.45

0.53

l.OI

1.04

4.34

22:4 k3

0.03

0,05

0.69

2.26

0.40

0.50

0.62

8.11

Note: The equivalent degree of unsaturation In the fatty adds was obtained by multiplying the number of double bonds by the quantity of fatty acid.

286

KIKER. SMITH, and VOLXG: EFFECT OF DIETARY FISH OIL

fatty acids found within and among the tissues
examined. All the fatty acids that were identi-
fied will be discussed in the next section. For
illustrative purposes. Table 5 presents selected
results obtained with the various tissues. The
outer backfat had the lowest total concentration
of saturated fatty acids of all the tissues, regard-
less of whether the diet contained menhaden
oil or did not contain it. The remaining- tissues
(inner backfat. liver, and lonpissimus doisi)
were all higher than the outer backfat and did
not differ markedly from each other in the total
concentration of saturated fatty acids.

The difference in degree of saturation when
confined to comparisons between the inner and
outer backfat is in agreement with rei^orts l\v
Banks and Hilditch (1932) and Sink, Watkins,
Ziegler, and Miller (1964). The simple ratio
of the total quantity of saturated to unsaturated
fatty acids, however, does not describe the true
character of the unsaturated fatty acids found
within the tissues or among them.

An examination of the quantity of unsatura-
tion on the basis of the number of double bonds
and the relative quantities of the corresponding
fatty acid groups indicates marked differences
among the tissues.

Both the longissimns do)-si tissue and the liver
tissue contain markedly less fatty acids with one
unsaturated bond than do either of the back-
fat tissues, regardless of the dietary treatment.
This difference no doubt is reflected by the 18:1
co9 content.

The concentration of fatty acids with two un-
saturated bonds in the outer backfat tissue is
higher than that in the remaining tissues and
apparently indicates a differential concentration
of 18:2 w6.

The difference most evident among the tis-
sues with respect to the fatty acids with three
unsaturated bonds is the higher concentration
found in the liver tissue.

Both the longissimus dorsi and the liver tissue
contained considerably more of the four-unsatu-
rated-bond fatty acids than did the backfat tis-
sues. The liver, in turn, contained about four
times the concentration found in the Inngissimus
dorsi. Incorporating menhaden oil into the diet

lowered the magnitude of these differences
among the tissues.

The relative differences among the tissues in
the case of the longissimns dorsi tissue reflect
about equal quantities of the isomeric fatty acids
20:4 ojG and 20:4 coo. The concentration of the
fatty acids with four unsaturated bonds in the
liver tissue is due jirimarily to the 20:4 w6 iso-
mer; only small concentrations of the 20:4 w3
isomer were found.

Similarly, the concentration of fatty acids
with five and six unsaturated bonds in the lon-
gissimns dorsi and liver tissues was markedly
higher than in the l)ackfat tissues. The incor-
lioration of menhaden oil into the diet resulted
in increased concentrations of these fatty acids
in all tissues, although the differences among
tissues were of the same magnitude as the dif-
ferences occurring in the absence of the men-
haden oil. The variable concentrations of the
fatty acids with five and six unsaturated bonds,
owing to treatment differences, reflect differ-
ences in the quantities of 20:5 coo. 22:. 5 coo, and
22:6 w3 fatty acids.

On the basis of the equivalent degree of un-
saturation obtained by the multiplication of the
number of unsaturated bonds by the quantity of
fatty acids of that category, the relative degree
of unsaturation of the four tissues is: inner
backfat, 8-5.9; outer backfat, 98.7; longissimus
dorsi. 106.4; and liver, 164.0. The incorporation
of menhaden oil did not change the relative dif-
ferences among tissues, but it did result in a
treatment difference. The relative degree of
unsaturation among the treatments was of the
magnitude of 10 to 30 units greater for all tis-
sues exce])t the loiigissimus dorsi.

Thus, these results generally conform with
those previously reported that various tissues
differ in fatty acid comjiosition (Brown and
Deck, 1930: Banks and Hilditch, 1932; Sink
et al, 1964) and that dietary oils alter this fatty
acid jjattern and degree of unsaturation of the
animal tissues of monogastric animals (Ellis
and Isbell, 1926a, 1926b; Ellis and Zeller, 1930;
Ellis, Rothwell, and Pool, 1931; Bhattacharya
and Hilditch, 1931; Hilditch and Pedelty, 1940).

287

FISHERY BULLETIN: VOL. 69, NO. 2

Fatty Acids Identified

Table 6 reports the fatty acids identified by
the method of gas-liquid chromatographic anal-
ysis described in the preceding section.

Table 6. — Fatty acids identified in pig tissues.

Presence or absence

of the fotty acid in:

Fatty acid

Backfat

Longisjimui
dorii tissue

Liver

Inner tissue Ou

ter tissue

tissue

22:6 a-3

+

-1-

-1-

+

22:5 a-3

+

+

+

+

20:5 a..3

+

+

-f-

+

20:4 u3

+

+

-t-

+

18:4 <.-3

+

+

+

+

18:3 c;3

+

-t-

-t-

+

22:5 ic6

_

Irace

trace

+

22:4 ^6

—

+

+

+

20:4 u6

-1-

-1-

+

+

20:2 ..■6

—

—

+

+

18:2 ^•6

+

+

+

+

21:1 u9

_

—

+

+

20:2 u9

+

+

+

+

20:1 10-9

+

+

+

+

18:1 1^9

+

+

+

+

22:1 (?)

—

—

trace

+

20:3 (?)

+

+

+

+

16:2

+

+

+

+

16:1 u7

+

+

+

+

15:1

+

+

trace

+

14:1

+

+

+

+

20:0

+

-t-

-1-

+

19:0

+

—

+

+

18:0

+

-t-

-t-

+

17:0

+

+

+

+

16.0

+

+

+

+

15:0

+

+

-t-

+

14:0

+

+

+

4-

Twenty-eight fatty acids were identified in
the liver tissue, whereas a lesser number was
identified in the three other tissues (inner and
outer backfat and Io)n;issim us doisi) . The fatty
acids identified included those reported by Sink
et al. (1964) plus unsaturated 18, 20, 22 carbon
fatty acids of three of the fatty acid families
— co3, 0)6, and aj9 — according to current classi-
fication (Mohrhauer and Holman, 1963a).

With respect to the two backfat tissues, the
acids found in addition to those reported by
Sink et al. (1964) are as follows: 15:1, 16:2.
20:1 aj9, 18:4 co3, 20:2 aj9. 20:3, 20:4 0)3,
20:. 5 0)3, 22:4 o)6, and 22:5 oj3. The liver
and lonf/isshmis dorsi tissue also contained
20:2 oj6, 21:1 w9, 22: 1, 22:5 w6, and 22:6 w3.
Ilill (1966) reported, however, the presence of

most of these fatty acids in various tissues of
miniature pigs with the exception of 20:4 oj3,
which we found in our pigs. All of these fatty
acids, except 20:4 o)3, have also been noted in
rat tissue (Mohrhauer and Holman, 1963a,
1963b, 1963c) , and all of them including 20: 4 oj3,
have also been noted in chick tissue (Miller et
al., 1967), in fish tissues and in seal tissue
(Ackman, Burgher, and Jangaard, 1963; Ack-
man, Jangaard, Hoyle, and Brockerhoff', 1964).

The relation of the fatty acids fed (A') to
those deposited in the various tissues (Y) was
established by correlation and polynomial re-
gression analyses. A polynomial regression
computer program prepared by the Biomedical
Division of the University of California, Los
Angeles, was used. The extent of analysis of
the data was limited to the fourth polynomial
degree. Regression coefficients, standard errors
of regression, correlation coefficients, analyses
of variance, and data plots (predicted and ob-
served) were obtained.

Correlation and polynomial regression anal-
yses of the gas-liquid chromatographic data
presented in Tables 7 to 10 indicate that the
marine-type polyunsaturated fatty acids of the
linolenic acid (oj3) family were deposited in all
four tissues examined.

In general, a significant positive correlation
was obtained between the quantity of the o>3
fatty acids fed and the quantity deposited in
the various tissues. This relation was not ob-
tained, however, with the longissimus dorsi tis-
sue. The only explanation we have is that the
reaction caused by difficulties in the extraction
of the fatty acids and their subsequent sepa-
ration masked any pattern.

Definite relations between the amounts of
most of the o)3 fatty acids fed to pigs and the
amounts deposited were found in the liver tis-
sues and in the inner backfat tissues and the
outer ones.

Specifically, the quantity of two of the men-
haden oil fatty acids (22:5 w3, and 22:6 o)3)
found in the liver was positively correlated
(0.01 'r ) with the quantity of oil fed to the pigs
until they were of market weight (90.9 kg) . The
correlation for 20:5 coS approached significance.

288

KIFER, SMITH, and YOUNG:

Table 7. — Liver tissue:

EFFECT OF DIETARY HSU OIL

concentration of fatty acids found in liver tissue and correlation to quantity of various
fatty acids fed for various time intervals.

Fatly
acid

22:6 i^3

20:4- a.-3

18:4 u3

20:4 u6

18:2 i^6

weight
group

Concentrotion of fotty acid in liver tissue

when the percentage of menhaden oil in the

diet wos;

Correlotion
coefficient

«g

— — —

— — — —

— .Irea

ptTCent 0/

fatty acid —

— —

90.9

2 25

5.70

7.88

7.72

840

8.90

7.49

0.69**

Quadratic

79.5

2 25

4.65

4.98

5.11

6.25

5.82

7.43

0.70"

Linear

68.0

2.25

4.30

4.70

4.33

5.69

5.54

5.12

0.65*

Linear

90.9

2.55

3.66

4.42

4.48

5.12

5.17

4.85

0.78**

Quodratic

79.5

2.55

2.94

3.59

3.47

4.00

3.73

4.05

0.56*

Linear

68.0

2.55

2.70

4.64

3.75

3.70

3.93

4.11

0.59*

Linear

90.9

0.56

3.55

6.23

6.52

8.11

8.46

8.14

0.89**

Quadratic

79.5

056

1.57

2.07

1.96

3.33

2.30

2.20

0.50

680

0.56

1.00

1.25

1.65

2.12

3.49

2.20

0.67*

Linear

909

039

0.71

054

0.50

0.56

0.43

044

-0.21

79.5

0.39

1.45

0.75

0.50

0.60

069

0.29

-0.42

68.0

039

0.58

0.11

067

0.71

0.54

0.89

0.39

—

90.9

008

0.11

0.05

0 08

0.09

0.12

0.07

0.00

79.5

008

0.26

0.05

0 07

0.04

0.06

0.06

-0.29

68.0

0.08

0.07

0.05

0.08

0.06

0 10

0.09

0.33

—

90.9

0.47

0.67

0.59

0.66

0.73

0.94

0.66

0.26

79.5

0.47

0.77

0.89

0.54

0.56

051

0.48

-0.39

__

68 0

0.47

0.52

0.45

0.57

0.50

0.39

0.59

0.12

—

90.9

0.24

0.05

0.06

0.05

0 12

Oil

0.03

-0.27

79.5

0.24

0.23

0.10

0.05

0.17

0.16

0.00

-0.60*

Linear

68.0

0.24

0.17

0.10

0.10

009

014

0.03

-0.83**

Linear

90.9

1 21

0.43

0.28

033

0.29

0.33

0.21

-0.65**

Cubic

79.5

1.21

0.53

0.34

0.45

0.47

0.48

0.40

-0.63*

Cubic

68.0

1 21

0.74

0.74

0.64

058

0.53

0.63

-0.69*

Linear

90.9

18.58

12.37

11.53

10.50

882

8.84

9.69

-0.70"

Quadratic

79.5

18.58

15.23

14.48

14.65

15.12

14.99

12.84

-0.19

._

68.0

18.58

17.93

16.95

15.98

16.06

16.66

13.92

-0.74**

Lineor

90.9

0.52

0.19

0.18

020

0 14

0.17

0.17

-0.52*

Cubic

79.5

0.52

0.43

0.50

0.46

0.26

0.40

0 36

-0.34

68.0

052

0.20

0.40

0.23

0.40

0.48

0.38

0.13

_

90.9

15.87

17.03

16.17

16.32

15.95

15.93

15 79

-0.33

..

79.5

15 87

14.28

15.69

16.00

17.05

15.93

15.40

0.16

68.0

15.87

16.78

16.27

16.10

16.39

14.48

16.41

-0.12

—

90.9

0 27

0.31

0.13

0.15

0 15

0.15

0.14

-0.59**

Linear

795

0.27

0.52

0.45

0.30

0.13

0.25

020

-0.40

..

68.0

027

0-42

0.22

0.28

0.29

0.27

0.18

-0.47

—

90.9

0.82

054

0.60

0.54

0.59

0.58

0.54

-0.12

..

79.5

0.82

1.29

0.78

0.68

0.44

0.63

0.52

-0.48

68.0

0.82

0 42

0.59

0.56

1.25

0.59

1.05

0.52

—

90.9

0.28

0.24

0.19

0.30

0.20

0.23

0.17

-0.22

„

79.5

0.28

0.44

0.41

0.26

0.20

0.21

0.22

-0.38

._

68.0

0.28

0.22

0.27

0.25

0.22

0.23

0.25

-0.28

~

90.9

16.61

15.28

13.16

14.80

13.56

14.91

14.17

-0.09

..

79.5

16.61

16.49

18.55

16.18

12.67

13.33

13.56

-0.49

68.0

16.61

15.64

15.55

16.09

14.59

9.68

1299

-0.54

_.

P <.os

P < 01

Polynomial regression analyses of these data in-
dicate that the incorporation pattern of the fatty
acids (20:5 co3, 22:5 co3, 22:6 aj3) was quad-
ratic, with the rate of deposition being greater
at the lower levels in the diet. Removal of men-

haden oil from the diet of the pigs at the two
body weights, 68.0 or 79.5 kg, did not alter this
pattern markedly. The principal changes were
a reduction in the relative degree of significant
response (O.Ofr to 0.059r) and an alteration

289

FISHERY BULLETIN: VOL. 69, NO. 2

Table 8. — Inner backfat tissue: concentration of fatty acids found in backfat tissue and correlation to quantity

of various fatty acids fed for various time intervals.

Fatty
acid

Pig

weight
group

Concentration of fotty acid in inner
fat tissue wtien the percentage of me
oil in the diet was:

back-
nhoden

Correlation
coefficient

Kind of
regression

0

0.4

0.6

_L

0.8

1.0

1.2

1.4

90.9
79.5
68.0

.

percent ol jatty acid
0.29 0.54
0.51 0.37
0.20 1 .06

0.49
0.31
0.28

0.48
0.40
0.31

0.76"

0.56*

0.49

22:6 u;3

0
0
0

0.13
0.19
0.09

0.28
0.21
0 15

Linear
Linear

22:5 u;3

90,9
79.5
68.0

0 10
0.10
0.10

0.35
0.25
0.18

0.48
0.46
0.20

0.54
0.28
0.39

0.96
0.60
0.24

0.73
0.23
0.54

0.88
0.19
0.51

0.77"
-0.01
0.71"

Linear
Linear

20:5 ^3

90.9
79.5
680

0 07
0.07
007

0.12
0.08
0 04

0.18
0.17
Oil

0.29
0.20
0.12

0.44
0.27
0.12

041
0,16
0.33

0.39
0.22
0.19

0.71"

0.55*

0.71*>

Linear
Linear
Linear

20:4 US

90.9
79.5
68 0

0 06
0.06
0.06

015
Oil
0.06

0.17
0.14
0.10

0.24
0.23
0.19

0.34
0.34
0.11

0.26
0.19
0.14

0.29
0.17
0.14

0.72"

0.43

0.89'*

Linear
Linear

18:4 u3

90.9
79.5
68.0

0 06
0.06
0.06

0.10
0.10
0.06

0.13
0.11
0.04

0.13
0.11
0.08

0.18
0.17
0.10

0.16
0.06
0.15

0.18
0.12
0.30

0.70* •

0.15

0.54

Linear

18:3 u3

90,9
79.5
68 0

0.74
0.74
0-74

0.82
0.72
0 86

0.89
0,88
080

0.94
0.92
0.77

1.04
1.08
1.03

1.02
0.77
0.71

1.10
0.82
1.15

0.52'
0.17
0.52

Linear

22:5 u6

90,9
79.5
68.0

Not

identified

-

--

22:4 U!6

909
79.5
68.0

Not

identified

-

--

20:4 m6

90.9
79.5
68.0

0 34
034
0.34

0,33
028
0.36

0.33
0.35
0.30

0.29
0.38
0.34

0.39
0.34
0.34

0.44
0.32
0.32

0.33
0.33
0.28

0.03

0.09

-0.60-

Linear

20:2 w6

90.9
79.5
68.0

Not

identified

-

-

18:2 u6

90.9
79.5
68.0

15.07
15.07
15.07

1553
13.15
17.45

1545
15.43
16.70

15.25
16.46
14.69

17.51
17.97
17.48

16 30
15.16
13.12

17,38
14.06
17.09

0.41

0.10
-0.01

—

P <.05

P <.01

in the patterns of incorporation of these fatty
acids (quadratic to linear).

No statistical relation was found for the re-
maining three fatty acids (18:3 w3, 18:4 c<j3,
and 20:4 w3).

Results of statistical analyses of the data ob-
tained with the inner backfat tissue and the
outer backfat tissue, however, indicate that all
six of the fatty acids of the 0)3 family are de-
posited in the tissue in i^roportion to the quantity
consumed by the pigs. When menhaden oil was
fed to the pigs until they attained a body weight
of 90.9 kg, a highly significant positive correla-
tion was obtained for all six wS fatty acids.

Removing the oil from the diet of the pigs when
they weighed 79.5 kg changed the pattern slight-
ly with respect to the outer backfat tissue. The
quantity of 18:4 a)3 fed was no longer correlated
with the amount deposited. Removal of the oil
when the pigs weighed (58.0 kg resulted in
only three of the qj3 fatty acids (20:5 ojS,
22:5 w3, and 22:6 0)3) being correlated.

Similarly with respect to inner backfat tis-
sue, removal of the menhaden oil when the jiigs
weighed either 68.0 or 79.5 kg resulted in the
(juantity of certain of the oj3 fatty acids fed no
longer being correlated with the quantity de-
posited. Polynomial regression analyses of

290

KIFER. SMITH, and YOUNG: EFFECT OF DIETARV FISH OIL

Table 9. — Outer backfat tissue: concentration of fatty acids founil in outer backfat tissue and correlation to
quantity of various fatty acids fed for various time intervals.

Fatty
acid

Pig

weight
group

Concentration of fatty acid in outer back-
fat tissue when the percentage of menhaden
oil in the diet was:

1.2

Correlotion
coefficient

22:6 1^3

22:5 io3

20:4 l;3

18:4 u3

20:2 a'6

A'S

— ... —

— — — —

— Area

percenl oj fatty

arid —

— .

90.9

0.04

0.23

0.37

0,47

0.59

0.69

0.58

0.85"

Linear

79.5

0 04

0.25

0.24

035

0 63

0.30

0.49

0.58"

Linear

68.0

0.04

0.20

0.26

0,16

0.34

0,33

0,43

0.74"

Linear

90.9

0.14

0.54

0.52

085

1.01

1,06

1.14

0.89"

Linear

79.5

0.14

0.52

0.52

0,66

0,85

0.78

1.04

0,85"

Linear

68.0

0.14

0.36

0.19

0,63

0.72

0.59

0.85

0,84""

Linear

90.9

0.13

0.19

0.24

0,40

0.49

0.56

0.68

0,89"

Linear

79.5

0 13

0.13

0.21

0,30

040

0.28

0.57

0.79"

Linear

68.0

0.13

0.17

0.20

0,17

0,28

0.24

0.33

0.74"

Linear

90.9

0.08

0,14

0.15

0,28

0,33

0.27

0.38

0.76"

Lineor

79.5

008

010

0.13

020

0,23

0 23

0.37

084"

Lineor

68.0

008

0.10

0,12

026

0-20

0,22

0.19

0,41

.—

90.9

0,13

0 12

0,12

017

0,17

0,19

0.20

0.58"

Linear

79.5

0,13

0.18

0,11

0 14

0.13

0,34

0.19

0,36

..

68.0

0,13

0.07

0,11

009

015

013

0,10

0.18

—

90.9

1,12

1.24

1,23

1,26

1,32

1,29

1,51

0.49*

Linear

79.5

1.12

1.11

1,31

1,33

1,32

1,29

1,34

0,72"

Linear

68.0

1,12

1.24

1.25

1.20

1,12

1.18

1,24

0-08

—

90.9

0,02

trace quontities

79.5

68.0

—

—

90.9

0,11

0.08

0.05

0.11

0,11

0.04

0.08

79.5

0.11

0.09

0.07

0.10

0,06

0.07

__

68.0

0.11

0.05

0.13

0

0,11

an

0.11

—

—

90.9

0.49

0.44

0.36

0-44

0,43

0,35

0.43

-0-26

79.5

049

0.43

0.44

0.42

0,41

0.38

0.44

-0,28

..

68.0

0.49

0.42

0.53

0.19

0.45

0.51

0.34

-0.16

—

90.9

..

„

79.5

Not identified

__

_.

68.0

—

—

90.9

18,99

19,80

19,58

19 33

19.90

19,20

20,72

004

79.5

18,99

17,28

21.56

20,43

20,39

1932

19,26

0.13

._

680

18,99

20.31

21.27

19.35

18.60

19,89

18,22

-0.36

._

P <.05

P <.01

these data indicate that, where a correlation ex-
isted, the data relative to the incorporation of
the to3 fatty acids were linear.

EFFECT OF MENHADEN OIL

CONSUMPTION ON ORGANOLEPTIC

EVALUATION OF PIG TISSUE

This second part of the study was made to
determine (1) the organoleptic effect on the
meat of the pigs fed different levels of menhaden
oil in their diet and (2) the retention or dis-
appearance of off-flavors by removal of men-
haden oil from the diet of the pigs when they
attained a body weight of 68.0, 79.5, or 90.9 kg.

TRIAL I: LEVEL OF MENHADEN OIL THAT
RESULTS IN A FISHY FLAVOR

As was just indicated. Trial I was conducted
to determine if menhaden oil fed at various
levels in the diet would cause off- (fishy) flavor
in pork. The levels used in the experiment
bracketed a l.O'c level, which was reported by
Vestal, Shrewsbury, Jordon, and Milligan
(194.5) to cause a fishy flavor.

Experimental Procedure

Reported here are the diets, management,
samples, and tests.

291

FISHERY BULLETIN: VOL. 69, NO. 2

Table 10. — Longissimus dorsi tissue: concentration of fatty acids found in longissimus dorsi tissue and correla-
tion to quantity of various fatty acids fed for various time intervals.

3tty
icid

Pig

weight
group

Concentration of falty acid in longissimus

dorsi tissue when the percentage of menhaden

oil in the diet was:

Correlation
coefficient

Kind of
regression

22:5 a;3

20:4 w3

18:4 w3

18:3 u'Z

Kg

— — — _

_ — — —

— Jrea

percent of fatty

acta —

— _

— — — —

90.9

0.23

0 94

0,79

0.78

0.91

0,89

0,51

-0 09

79.5

0.23

0,37

0,59

0.58

0.64

1,26

0,90

046

__

68,0

0-23

0,47

0,47

0-25

0.42

0,48

0,85

0.46

—

90.9

0-32

1,15

1,34

0-85

1 02

0,85

0,85

79.5

0-32

0,76

0.85

094

0-79

1,70

1.25

0,75"

Linear

68.0

0,32

1,05

0,59

0-47

0-78

0,57

1.14

0,25

—

90.9

0.19

1,61

1,68

1.09

1-23

1,24

1,31

001

79,5

0,19

0,47

098

0-58

0-52

1,88

1,47

0 43

__

68.0

0,19

0-30

0.69

0.51

0.63

0,44

0.77

059"

Lineor

909

0,53

2-42

2.87

0.92

0-91

0,89

0.87

-034

79.5

0,53

0 23

1,24

2-30

021

1,51

0,28

0,05

__

68.0

0,53

0-12

1,04

0-94

0-94

2,15

3,03

0.10

—

90.9

0,04

0 08

0,09

0-03

.,

0,07

0,10

79.5

0,04

0 05

0.24

__

__

68,0

0,04

004

--

0.10

0.16

0,16

—

—

—

90,9

045

053

0,64

0.56

0.58

0,56

057

0,07

79,5

0,45

038

0-53

0.62

0.43

0,63

0.44

0,20

..

68,0

0,45

0-77

1-05

081

0-57

0,51

0,50

-0.23

—

90-9

0.02

006

0-09

0.12

__

__

..

-0.22

79.5

0.02

tr

tr

0.18

Ir

tr

tr

68.0

0,02

tr

tr

0.04

0-29

tr

tr

—

—

90-9

0,34

041

084

0.37

__

0,32

0,16

-0.26

79.5

034

048

0-40

022

0-15

0,19

0,16

0,09

_.

68-0

034

0-37

0 27

0.12

0-16

0,17

0,36

023

—

90.9

242

2-85

2-13

2-35

1-92

1,65

1,32

-058-

Linear

79.5

2,42

2,04

3-00

1 62

1,52

3,55

2,64

0,10

..

68.0

2,42

2 00

2-12

0-74

1 53

0,92

1.39

-044

—

90.9

0,13

0,19

025

0-09

tr

005

tr

-0.46"

Linear

79.5

0.13

0,11

0 10

tr

005

tr

tr

-0,68**

Linear

68.0

0.13

0,10

tr

0-05

0,11

tr

0.09

-0.21

—

90-9

946

12,54

10-18

10-96

11,08

10 34

9,65

-0.25

..

79-5

9.46

1056

13.39

9.45

11.44

17.33

13.84

0,53-

Linear

68.0

9.46

15,63

10.14

12.36

10.39

8.81

9.61

-0.39

„

P <.05

P <.01

Table 1 shows how the diets used were for-
mulated, and Table 2 shows the gas-liquid-chro-
matographic analyses of the menhaden oil and
the diets fed. Management and allotment are
described in Table 11.

The right loin of each animal was collected,
and three slices, each 1.37 cm thick, were cut
proceeding posteriorly from the 10th rib. The
slices and the remaining portion of the loin were
held in frozen storage until used in the taste
tests to be described shortly.

The slices of loin were placed in uncovei'ed
pans, one-half cup of water was added to each
pan, and the pans were held for 50 min in a
gas oven at 163.0° C. No seasoning was added

Table 11. — Design of Trial I to determine the level of
menhaden oil in the diet that will impart a fishy flavor
to the meat of pigs.

Level of

menhaden oil

in the diet

%

0

04

0,6

08

1,0

1.2

1.4

Pigs allotted
per treatment

Number
3
3
3
3
3
3
3

to the samples. The remaining portions of the
loins, which were used in a home-consumer test
described in the next section, were prepared

292

KIFER. SMITH, and YOUNG: EFFECT OF DIETARY FISH OIL

using variable cooking times and temperatures.
Salt and pepper were the only condiments used.
Two tests were made: a panel test and a
home-consumer test. Twelve panel members
tested (once daily) a portion of the loin from
various animals in a triangular test pattern.
In addition to matching like samples, the panel
members indicated a score according to the nu-
merical standard: 1 (good) to 10 (inedible)
and made any additional subjective comments
that they felt would be helpful concerning the
samples. The remaining portions of the loins
were distributed randomly to staff members and
were accompanied with a form requesting a de-
scription of the method of cooking used, a state-
ment of the number of persons tasting, and a
subjective evaluation of the flavor.

Results and Discussion

Tables 12, 13, and 14 present the results of
Trial I, which was conducted to establish the
level of fish oil in the diet that would induce
a fishy flavor in pork. The results, as presented

Table 12. — Panel test Trial I — organoleptic results ob-
tained with loins of pigs fed menhaden oil at various
levels in the diet.

Concentration of
menhaden
oil in diet

Samples
tested

Detection of
adverse flavor

Fishy

%

Number

Number

Number

0

18

14

3

0.4

3

7

1

0.6

3

4

1

0.8

3

10

2

1.0

3

S

1

1.2

3

10

5

1.4

3

13

3

Table 13. — Panel test Trial I — organoleptic results
(selected data) obtained with loins of pigs fed men-
haden oil at various levels in the diet.

Concentration of
menhaden
oil in diet

Sample
tested

Detection of
adverse flavor

Off

Fishy

%

Number

A'

umber

N

umber

0

\\

0

0

0.4

1

0

0

0.6

2

2

0

0.8

2

2

0

1.0

3

4

0

1.2

2

4

2

1.4

1

6

1

Table 14. — Home-consumer test Trial I — organoleptic
results obtained with loins of pigs fed menhaden oil at
various levels in the diet.

Concentrat

of
menhaden
in diet

on
oil

Samples
tested

Testers

Detect
adverse

on of
flavor

Off

Fishy

%

Number

Number

Number

Number

0

14

48

I

1

0.4

6

28

6

0

0.6

6

12

0

0

0.8

6

18

I

0

1.0

6

25

1

0

1.2

5

9

2

2

1.4

3

22

7

7

in Table 13, are somewhat misleading, because
two facts need to be considered in interpreting
them. First, part way through the taste test,
the freezer in which the test samples were stored
malfunctioned. The samples of meat thawed
for 2 days and then refroze. Subsequently, a
number of panelists detected off-flavors in the
control sample as well as in the samples from
the pigs receiving the lower levels of fish oil.
Second, one panelist continuously detected off-
flavor and fishiness regardless of the dietary
treatment. In view of these two facts. Table 14
is included ; here results are presented of tests
conducted before the freezer malfunctioned and
without the evaluations of the one panelist. The
organoleptic results (Table 14) indicate that an
off-flavor in pork could be detected when pigs
consumed menhaden oil at a level of 0.8% of
their diet and that a fishy flavor could be de-
tected when the pigs consumed menhaden oil
at a level of 1.2% of their diet and were fed
when they attained a weight of 40.5 kg until they
attained a market weight of 90.9 kg.

These results confirm a previous report by
Vestal et al. (1945), which established that a
level of 1.0 Sr menhaden oil in the diet would
cause a fishy flavor.

The results of the home-consumer test agree
in general with those of the panel test that a
fishy flavor was detected when menhaden oil
was fed at a level of 1.2% in the diet. The one
indication of off-flavor and fishy flavor in the
control sample was found by the judge who had
consistently done so in the panel test. All
samples in the home-consumer test had been sub-
jected to the thawing and refreezing process.

293

FISHERY BULLETIN: VOL. 69. NO. 2

The fact that persons unaware of the feeding
regimen were less able to detect the off-flavor
may indicate that the members of the test panel
were overly critical in their evaluation. In
view of the subjectivity of organoleptic tests,
we felt that the aim of the trial was attained
and that a suitable gradient in the concentration
of fish oil in the diet was established for the
further study of fishy flavor.

TRIAL II: RELATION OF FLAVOR OF MEAT

TO BODY WEIGHT AT TIME MENHADEN

OIL WAS REMOVED FROM DIET

As in Trial I, in Trial II loin samples were
used in two organoleptic tests (panel and home-
consumer) to determine if any fishy taste was
imparted to animals fed the experimental diets.
Twelve panel members tested six loin samples
{longissimus dorsi and inner backfat) per day
during the test. The panelists were asked to
pick the conti-ol and to score each sample (lean
and fat) on a numerical scale of 1 (good) to 5
(inedible). In addition, the members of the
panel were asked to describe, subjectively, the
flavor of the samples. All panelists were aware
of the experimental design.

A home-consumer test was conducted in the
same way as in Trial I.

The diets used were formulated and prepared
in a manner similar to that indicated in Table 1.
Table 2 shows the gas-liquid chromatographic
analyses of the oil and of the diets fed.

The samples were collected and prepared as
in Trial I.

The results of both organoleptic tests (panel
and home-consumer, Tables 15 and 16) agree
with those obtained in Trial I. In the panel
tests, the i-esults indicate that off-flavors were
detected at the 0.8 Sr level of menhaden oil in
the diet and that a fishy flavor was detected at
the 1.0-:; level.

In the home-consumer tests, a fishy flavor was
not detected until the pigs were fed menhaden
oil at the 1.2''r level in the diet.

Table 15. — Panel test Trial II — organoleptic results
obtained with longissimus dorsi and inner backfat tissue
of pigs fed various levels of menhaden oil in the diet
until the pigs attained a body weight of 90.9, 79.5, or
68.0 kg.

Concentration

Weight of

pigs

Delect

on of

ot

menhaden oil

in diet

when oil wos

omitted from

diet

Samples
tested

adverse

flavor

Off

Fishy

%

Kg

Number

Number

Number

0

7

0

M

0.4

90.9

3

1

1

79.5

2

0

2

«8.0

2

0

0

0.6

90.9

3

0

0

79.5

3

0

0

68.0

1

0

0

0.8

90.9

3

0

0

79.5

2

0

1

68.0

2

1

2

1.0

90.0

3

0

0

795

2

0

1

68.0

2

3

6

1.2

90.9

4

0

0

79.5

2

2

2

68.0

1

3

3

1.4

90.9

2

0

0

79.5

2

1

2

68.0

2

0

0

* As wos indicated in Trial I, one ponelist detected off-flavor and fishy
flavor in the control sample and in somples from pigs fed the low levels
of menhoden oil in the diet. Because this panelist wos unable to distin-
guish between the control and the test samples, he was replaced.

Table 16. — Home-consumer test Trial II — organoleptic
results obtained with longissimus dorsi and inner back-
fat tissue of pigs fed various dietary levels of menhaden
oil in the diet until the pigs attained a body weight of
90.9, 79.5, and 68.0 kg.

Concentration
of men-
haden oil
in diet

Weight of

] pigs when

1 oil was

omitted from

diet

Samples
tested

Number

of
testers

Detection of
adverse flavor

Off

Fishy

%

Kg

Number

Number

Number

Number

0

7

21

0

0

0-4

90.9

3

15

0

0

79.5

2

3

0

0

68,0

2

12

0

0

0.6

90.9

3

3

0

0

795

3

11

0

0

68.0

1

5

0

0

0.8

90 9

3

8

0

0

79.5

2

6

0

0

68.0

2

4

2

0

10

90.9

3

10

0

0

79.5

2

9

5

0

68.0

2

12

0

0

1.2

909

4

19

3

3

795

2

5

0

0

68.0

1

4

0

0

1.4

909

2

4

2

0

795

2

3

3

3

68.0

2

a

0

0

294

KIFER. SMITH, and YOUNG: EFFECT OF DIETARY FISH OIL

RELATION OF MENHADEN OIL

FATTY ACIDS DEPOSITED TO

ORGANOLEPTIC VALUES OBTAINED

WITH PIG TISSUES

This third part of the study was made to
determine if a relation exists between the degree
of off-flavor detection and the fatty acid depo-
sition pattern of the samples of pig tissue.

PROCEDURE

The details of management, patterns of fatty
acid deposition in the tissues, and organoleptic
tests wei'e the same as those described earlier.

To establish the relation (if any) of the char-
acteristic polyunsaturated ojS fatty acids of men-
haden oil to the off-flavor of pig tissue, we first
had to establish a positive correlation (if any)
between the concentrations of these fatty acids
fed to the pigs to the concentrations of the fatty
acids deposited in the various pig tissues. Once
such a correlation (if it existed) was established,
then the transformational relation of the con-
centration of fatty acids fed and deposited to
the organoleptic evaluation could be undertaken.

Results of gas-liquid chromatographic anal-
yses of the diets fed (Table 2) indicate that,
in general, as the percentage of menhaden oil
in the diet increased, the percentage of linolenic
0)3 family acids (18:3 &j3, 18:4 co3, 20:4 &j3,
22:5 0)3, and 22:6 &)3) characteristic of men-
haden oil increased proportionately in the diet.

To determine whether the concentrations of
these fatty acids in the diet are correlated with
the taste of the pig flesh, we had to develop
a weighted numerical score of organoleptic data.
We obtained the weighted score for each sample
tested by multiplying the number of testers times
the numerical values of their scores and sum-
ming to a total. For example, if five of the pan-
elists scored the sample 3 and if seven scored
the sample 4, the weighted score would be 5 X
3 = 15 plus 7x4 = 28, or a total of 15 + 28
= 43. The weighted scores were used as the
Y axis, and the quantity of oil in kilograms or
in percent consumed by each pig was used as

the A' axis in a subsequent correlation and ]3oly-
nomial regression analysis.

Although four tissues were examined with
respect to the deposition of wS fatty acid, only
two of these tissues (the inner backfat and the
longisstmus dorsi) were evaluated organoleptic-
ally. This comparison was further limited in
view of the lack of correlation between the a-
mount in the diet of w3 fatty acids fed and the
concentration of these fatty acids deposited in
the longissimus dorsi (Tables 17, 18, and 19).
Consequently, the relation of the concentration
of the 0)3 family fatty acids deposited in the
inner backfat and the organoleptic score ob-
tained with this tissue was used for the com-
parison of the relation of the concentration of
the w3 family fatty acids to the organoleptic
score.

Because all six of the marine polyunsaturated
(wS) family fatty acids deposited in the inner
backfat tissue were positively correlated with

Table 17. — Pigs fed to 90.9 kg [correlation and poly-
nomial regression analyses of menhaden oil consumed
(A') to individual fatty acids deposited (Y) in longis-
sinucs dorsi tissue of pigs when oil was fed until the
pigs attained a body weight of 90.9 kg].

fatly
acid red

and
deposited

Corre-
lation
coef-
ficient

Regres-
sion coef-
ficient

Standard
error of
regression

Last degree of
polynomial significant

Degree

F valu

22:4 0.3

-ow

-0,016

0,041

_.

0.15

22:5 ..•3

_,

__

..

22:5 n.'6

-0.22

-0 038

0,041

__

0.85

22:4 io6

-0.26

-0,052

0,048

1.19

20:5 ^'3

0.01

0,003

0,077

__

0.00

20:4 U'3

-0.34

-0,029

0 191

._

2.26

22:1 (?)

__

__

,.

__

20:4 u:6

-0,58"

-0,220

0.074

Linear

8.76*'

20:3

-0 22

-0,022

0.024

__

0.84

21:1 u9

-0.32

-0 029

0.021

__

1.96

20:2 1^6

-0.46'

-0,036

0,017

Linear

4.56-

20:2 U.-9

-0,34

-0,072

0,048

..

2.24

18:4 a;3

__

__

_.

._

__

20:1 U.-9

0.02

0.002

0 024

„

0.01

18:3 a:3

0.07

0.004

0014

__

0.09

20:0

-001

-0.001

0,016

._

0.00

18:2 o.'6

-0.25

-0.210

0,194

._

1.15

19:0

0 29

0047

0,039

1.50

18:1 0.-9

0 46-

1.130

0,527

Linear

4.59*

18:0

0.09

__

16:2

-0.04

-0 002

0,013

__

0.02

17:0

-0.05

-0.009

0,045

._

0.04

16:1 u7

-0.09

-0,035

0,099

0.13

16:0

-0.04

-0,054

0,300

0.03

15:1

__

..

15:0

-0.22

-0 026

0,027

._

0.89

14:1

-0.06

-0,009

0,033

0.06

14:0

— 0.20

-0,033

0,038

—

0.74

P <.05

•• P <.01

295

FISHERY BULLETIN: VOL. 69. NO. 2

the concentration of menhaden oil in the diet
fed, the quantity of oil consumed (A') could be
compared with the organoleptic scores (Y) ob-
tained for the pigs in each weight group (68.0,
79.5, 90.9 kg).

RESULTS

Tables 20, 21, and 22 give the weighted or-
ganoleptic scores obtained from the panel or-
ganoleptic tests. (Larger numerical values in-
dicate an unacceptable product or a trend toward
an unacceptable product.)

Statistical analyses of these data indicate a
positive correlation between increased consump-
tion of oil and higher organoleptic scores for tis-
sues from pigs fed the oil until they attained
a body weight of 90.9 kg (Table 23). Removal
of the oil from the diet of the pigs at a body
weight of either 68.0 or 79.5 kg resulted in a

Table 18. — Pigs fed to a body weight of 79.5 kg [cor-
relation and polynomial regression analyses of menhaden
oil consumed (.Y) to individual fatty acids deposited
(Y) in longissi7mis dorsi tissue of pigs when oil was
fed until the pigs attained a body weight of 79.5 kg].

Fatty
acid fed

Corre-

lation

and

coef-

deposited

ficient

Regres-
sion coef-
ficient

Standard
error of
regression

Last degree of
polynomial signrficont

Degree F value

22:6 ^3

0.46

0.189

0,104

3,29

22:5 ..■3

0.75"

0.235

0.059

Linear

15,82"

22:5 ^6

._

__

__

__

22:4:^6

0,09

0.012

0,039

0,10

20 5 i.'3

0.43

0.170

0,103

__

2.73

20:4 ^3

0.05

0.036

0224

0.03

22:1 (?)

__

_.

__

_-

20:4 u'6

0.10

0.069

0,209

0.11

20:3

0.27

0.028

0,029

0.91

21:1 u:9

-065"

-0,039

0013

Linear

8, 70'

20:2 0.6

-068"

-0 039

0012

Linear

10,47"

20:2 0.9

-0.39

-0.123

0084

2.17

18:4^3

20:1 0.9

-0 45

-0.092

0,053

3.05

18:3 :x3

0,20

0,020

0.027

0.51

20:0

-0,05

-0,006

0-029

0.04

18:2 u6

0.53*

1.216

0.557

Linear

4.77'

19:0

-0.02

-0.002

0.027

0.00

18:1 u9

-0.36

-1.085

0.815

1.77

18:0

-0.17

-0.172

0 290

0.35

16:2

0.11

0.014

0.037

0.14

17:0

-0.11

-0017

0.043

..

0.15

16:1 a7

-0,32

-0 101

0.088

1,33

16:0

-0.58'

-0.918

0.372

Linear

6,09'

15:1

__

15:0

-0.04

-0.006

0.046

0.02

14:1

0.32

0.038

0.032

1.35

14:0

-0.26

-0.039

0.043

—

0.84

Table 19.— Pigs fed to a body weight of 68.0 kg [cor-
relation and polynomial regression on analyses of men-
haden oil consumed (X) to individual fatty acids de-
posited (Y) in longissimns dorsi tissue of pigs when
oil was fed until the pigs attained a body weight of
68.0 kg].'

Fatty
acid ted

Corre-
lotion
coef-
ficient

Regres-
sion coef-
ficient

Standard
error of
regression

Last deg
polynomial

ree of
ignificant

deposited

Degree

F value

22:6 a'3

0.46

0.113

0.073

2.38

22:5 u3

0.24

0.087

0.120

0.53

22:5 u6

._

22,4 U.6

0.23

0.049

0.068

0.52

20:5 ^-3

0.59'

0.130

0.059

4.79

20:4 u-3

0.10

0.201

0.680

0.09

22:1 (?)

._

20:4 a-6

— 0.44

-0.363

0247

2.16

20:3

-0 20

-0.029

0.047

0,38

21:1 u-9

0.38

0.039

0.032

1.50

20:2 u6

-0,21

-0.012

0019

0.41

20:2 o9

-0,43

-0.301

0,212

2.02

18:4 a'3

._

20:1 u9

-0,42

-0.139

0,101

1.91

18:3 u'3

-0,23

-0.056

0078

0.51

20:0

-0.27

-0.042

0 050

0.68

18:2 a;6

-0.39

-1.081

0,345

1.64

19:0

-0.24

-0.057

0.077

0.55

18:1 0)9

0.44

1 392

0.944

2.17

18:0

0.40

0.556

0,422

1,73

16:2

-0.13

-0.036

0.094

0,14

17:0

-0.12

- 0.029

0.077

0,14

16:1 u7

0.08

0.080

0.313

0.06

16:0

-0.16

-0.531

1.065

0.25

15:1

__

15:0

-0,03

-0,013

0,129

0.01

14:1

-0.08

-0.019

0.080

0.06

14:0

-0.11

-0.029

0.083

-

0.12

P <.05

" P <.01

Table 20.— Panel test Trial II— weighted organoleptic
scores obtained with inner backfat of pigs fed various
levels of menhaden oil in the diet until the pigs attained
a body weight of 90.9 kg.

Quantity of oil
consumed (-V)

Weighted organoleptic
score (K)

P <.05

/> <.01

Kg
0

0.81
.83
.91

1 26
1,29
1,36
1.77
1.86
2.07

2,00
2.15
2,35

2,55
2.74
2.74

2.82
3.20
3.25

.l! % ol Jill
0

0.4

1.0

1.2

23
21
27

22
22
25

31
26
32

30
34
35

29
36
28

37
32

296

KIFER. SMITH, and YOUNG: EFFECT OF DIETARY FISH OIL

Table 21.— Panel test Trial II— weighted organoleptic
scores obtained with inner backfat of pigs fed various
levels of menhaden oil in the diet until the pigs attained
a body weight of 79.5 kg.

Quantity of oil
consumed (X)

Weighted organoleptic
score (}')

Kg
0

As

% of diet
0

21

0.55
.64

0.4

25
27

.94
.99
.99

0.6

20
21

la

1.30
1.34

0.8

20
20

1.36
1.48

1.0

35
23

1.77

1.2

34

2.11

1.4

32

Table 22. — Panel test Trial II — weighted organoleptic
scores obtained with inner backfat of pigs fed various
levels of menhaden oil in the diet until the pigs attained
a body weight of 68.0 kg.

Quantity of oil

consumed (A')

W

'ighted organoleptic
score ()')

Kg
0

.is

% of dut
0

21

0.45
.54

0.4

23
20

.72

0.6

21

.98

1.09

0.8

23
22

1.21
1.21

1.0

22
25

1.54

1.2

26

1.61
1.61

1.4

23
17

Table 23. — Correlation and polynomial regression anal-
yses of quantity of menhaden oil consumed (.Y) to
weighted organoleptic score {Y) when the oil was fed
until the pigs attained a body weight of 90.9, 79.5, or
68.0 kg.

Oil fed
to

Correlotion
coefficient

Regression

coefficient

Standard

error of
regression

Lost degree of

polynomial significant

Degree

Kg
90.9
79.S
68.0

0.82"
.49
.21

2.169
2.375
0.617

0,371
1.325
0.967

329.58"
3.21
0.41

P <.01

loss of the significant positive correlation be-
tween the variables, although the correlation

coefficient obtained for die group weighing
79.5 kg approached significance.

These results of organoleptic tests are in
agreement with reports of Miller et al. (1967),
which indicate that co3 family fatty acicds, when
fed and subsequently deposited, are positively
correlated with organoleptic scores obtained
with broiler flesh. The results are in partial
agreement with the hypothesis of Banks and
Hilditch (1932), who suggested that the fatty
acids of the C20-22 series are associated with an
off- (fishy) flavor. Both the results reported
here and those reported by Miller et al. (1967)
indicate that fatty acids of the coS family con-
taining 18 to 22 carbon atoms are positively cor-
related with the incidence and degree of off"-
flavor in pig or broiler flesh. These fatty acids
may be causal agents for the oflf-flavor, or they
may not be. In fact, they probably are the
precursors of the compound producing the off-
flavor.

In these experiments, the inclusion of the men-
haden oil in the diet of the pigs resulted in no
physiological abnormalities other than the pro-
duction of off-flavor and an alteration in the pat-
tern of fatty acids in the tissues. This result
was not unexpected, because previous work at
the National Marine Fisheries Service Techno-
logical Laboratory at College Park had indi-
cated that levels of menhaden oil in excess of
10% of the diet are necessary to produce the
physiological abnormalities of e.Kudative diath-
esis and muscular dystrophy exiierimentally.
Adding various antioxidants (vitamin E, sele-
nium, and ethoxyquin) to the diet at compen-
satory levels prevented the development of these
abnormalities (exudative diathesis and muscu-
lar dystrophy) in chicks fed menhaden oil at
high concentrations (Miller, Leong, Knobl, and
Gruger, 1965).

METABOLIC INTERACTIONS OF

FATTY ACIDS OF THE OMEGA

FAMILY ( (o3, u6, w9)

Mohrhauer and Holman (1963a), Rahm and
Holman (1964), Tinsley (1964), and Lowry and
Tinsley (1966) have demonstrated that feeding

297

FISHERY BULLETIN: VOL, 69, NO. 2

rats increasingly higher concentrations of lin-
olenicacid (18:3co3) increases the concentration
of the fatty acids of the &;3 family in the liver
and that the proportion of the fatty acids of
the oleic (18:1 w9) and linoleic (18:2 coG) fam-
ilies are concomitantly reduced. They hypothe-
size that this interaction is due to the compe-
tition for enzymes necessary for elongation and
desaturation within the individual families of
fatty acids.

Since our pig e.xperiment included an in-
creasing quantity of 18:3 coS in the diet, the
question arose as to whether this hypothesized
competitive interaction actually occurred.

Trial II results were analyzed by correlation
analysis and polynomial regression analysis as
previously described. The quantity of men-
haden oil consumed constituted the X axis, and
the quantity of the 17:1 o)9 or 18:2 co6 family
fatty acid in question the Y axis.

The 0)3 family fatty acids incorporated into
the diet of the pigs as menhaden oil and sub-
sequently ingested resulted in a significantly
depressed deposition of the quantity of certain
members of the w6 and c<j9 families of fatty
acids. The mechanism involved, according to
the accepted hypothesis, is that the parent fatty
acids of the various fatty acid families trigger
a highly competitive mechanism for the meta-
bolic enzymes of the systems of carbon-chain
elongation and dehydrogenation. Successful
comijetition for the enzymes depends upon an
affinity preference (aj3, co6, and co9) and upon
the relative concentration of the various fatty
acids, or upon both affinity and concentration.
These results agree in part with the experi-
mental evidence (Mohrhauer and Holman,
1963a) whereby the feeding of increasing levels
of one of the parent acids or other members
of a family results in an accumulation of acids

Table 24. — Liver tissue — comparison of correlation coefficients and significant degree of poljTiomial regression
obtained by relating the quantity of menhaden oil consumed (.Y) until the pigs attained body weights of 90.9,
79.5, or 68.0 kg to the amount of individual fatty acids deposited in liver tissue (F).

Fatty
acid fed

and
deposited

Correlation coefficients

when oil is fed until

the pigs weighed:

Lost degree of polynomial significant when oil was
fed until the pigs weighed:

90.9 kg

79.5 kg

68.0 kg

90.9 kg 79.5 kg 68.0 kg

Degree F value

Degree F value

Degree F value

22:6 ..-S

0.69"

0.70"

0.65*

Quadratic

7.78'

Lineor

11.52"

Linear

6.46*

22:5 f3

0.78"

0.56"

0.59*

Quadratic

5.94'

Linear

5.49*

4.68

22:5i.'6

-0.27

-0.60-

-0.83"

._

0.92

Linear

6.73*

Linear

19.30"

22:4 ic6

-065"

-0.63-

-0.69-

Cubic

58.73"

Cubic

5.38'

Linear

8.08**

20:5 u3

0.89"

0.50

0.67"

Quadratic

14.53"

._

3.98

Linear

7.45"

20:4 u3

-0.21

-0.42

0.39

0.77

__

2.57

__

1.63

22:1 (7)

-0.40

-0.23

023

3.30

0.68

0.49

20:4 u6

-0.70"

-0.19

-0.74"

Quadratic

6.62*

0.46

Linear

10.79"

20:3

-0.14

0.36

0.43

_.

0.32

_,

1.74

__

202

21:1 U-9

-0.59"

-0.40

-0.47

Linear

9.19"

2.26

2.56

20:2 U.6

-0.52*

-0.34

0.13

Cubic

759*

_.

1.60

0.15

20:2 u9

-0.12

-0.48

0.52

0.26

_

3.61

3.42

18:4 ..'S

-0.00

-0.29

0.33

..

0.00

l.ll

1.06

20:1 c9

-0.22

-0.38

-0.28

__

0.87

_.

2.04

077

18:3 u-3

0.26

-0.39

0.12

1.20

2.14

0.13

20:0

0.16

-0.22

0.07

_.

0.47

0.61

0.05

18:2 u6

-0.33

0.16

-0.12

__

2.10

._

0.31

0.13

19.0

0.10

0.03

0.43

0.16

0.01

2.02

18:1 u9

-0.09

-0.49

-0.54

__

0.15

3.80

3.76

18:0

-0.06

0.33

-0.07

_.

0.06

__

1.46

__

0.05

16:2

0.24

-0.30

0.47

__

1.08

1.20

2.53

17:0

0.13

0.02

0.47

_.

0.31

0.00

2.48

16:1 d.-/

0.02

-0.49

-0.12

..

0.01

__

3.72

0.13

16:0

-0.26

-0.42

-0.22

_.,

1.25

2.56

0.46

15:1

0.10

-0.13

0.45

0.17

0.22

2.25

1j:0

-0.28

-0.27

0.75"

..

1.44

_.

0.94

Linear

11.76"

14.1

-0.0 1

-0.27

0.iS

0.00

0.96

3.84

14:0

0.01

-0.47

0.06

—

0.00

-

3.32

-

0.03

;• <.03

p <.oi

298

KIFER. SMITH, and YOUNG: EFFECT OF DIETARY FISH OIL

Table 25. — Inner backfat tissue — comparison of correlation coefficients and significant degree of polynomial re-
gression obtained by relating the quantity of menhaden oil consumed (A') until the pigs attained a body weight
of 90.9, 79.5, or 68.0 kg to the amount of individual fatty acids deposited in inner backfat tissue (Y).

Fatty
ocid fed

and
deposited

Correlation coefficients
when oil is fed until

Lost degree of polynomial significont when oil was
fed until the pigs weighed:

the pigs weighed:

90.9 kg

79.5 kg

68.0 kg

90.9 kg 79.5 kg

68-0 kg

Degree

F volue

Degree

F volue

Degree

F value

22:6 a'3

0.76"

0.58'

0.49

L

near

23.54

22:5 u-3

0.77"

-0.01

0.71"

L

neor

24.94

22:5^'6

__

__

22,4 u-6

__

20:5 f3

071*'

0.55*

0.71"

L

near

17.64

20:4 U.3

0.72"

0.43

0.89"

L

near

18.15

22,1 (7)

-_

20,4 0.6

0.03

0,09

-0.60"

0.02

20,3

-0.02

0,11

0.13

—

0.01

21,1 w9

20,2 ^6

__

__

20,2 u.'9

-0,28

-0,25

-0.32

1.43

18,4 C.-3

0,70"

0,15

0.54

L

near

16.65

20,1 1.9

-0,48-

-0.31

-0.32

L

neor

5-19

18,3 1.-3

0-52'

0.17

0,52

L

near

6.46

20,0

-0.33

0.01

-0,07

_^

2.01

18,2 u;6

0,41

0.10

-0-01

3.49

19:0

18:1 UV

-0.09

-0.37

-0.46

0.14

)8:0

-0,21

-0.13

0.17

0.82

16:2

0.50'

-0.03

0.50

L

near

5.96-

17:0

0,49"

0.43

0.51

L

near

5.52"

16:1 u7

0.31

-0.17

0.08

1.87

16:0

-0.24

0.37

0.21

1.06

15:1

-0.31

0,12

0.33

_.

1.77

15:0

0.13

-0,25

0.19

0.28

14:1

-0.18

0.27

0.35

_.

0 60

14:0

-0.24

0.19

0.46

1.03

6.02"

2,87

000

Linear

9.28

..

5.31"

Linear

9.33

2.70

Linear

35 51

0.10

Linear

4 99-

0.15

—

0.16

—

—

—

—

0,77

1,06

0,26

__

3.77

1.25

0.99

0.36

__

3.30

0.00

0.05

0.11

-

0.00

1.96

""

2.37

0.20

0.25

O.OI

2.96

2.72

„

3.22

0.37

__

0.07

1.94

__

0.40

0.18

__

t-13

0.79

__

0,34

0.91

1-23

0,43

_

2.39

P <,05

P <,01

derived from these acids and in a concomitant
decrease in the quantity of acids of the other
families.

In Trial II, we demonstrated the interrela-
tion of fatty acid families.

Specific evidence that the deposition of the cj6
and &j9 families are inhibited appears in Tables
24 to 27. As the quantity of the uiZ fatty acids
fed and deposited increased, the quantity of the
20:2 w6, 21:1 aj9, 20:4 w6, and 22:4 co6 fatty
acids found in the various tissues decreased
significantly. The linolenic (co3) family fatty
acids of the menhaden oil therefore inhibited
the conversion of oleic (18:1 ttj9) and linoleic
(18:2 ojG) to the elongated and dehydrogenated
members of their respective families by prevent-
ing the addition of two carbons or the removal
of two hydrogens, or by preventing both the
addition of two carbons and the removal of two
hydrogens.

SUMMARY AND CONCLUSIONS

Pigs were fed diets containing fish oil in two
feeding trials to investigate (1) the organo-
leptic effect produced in pig tissue by feeding
pigs stabilized crude menhaden oil; (2) the pos-
sible retention or disappearance of off-flavor by
withdrawing the fish oil from the diet at given
times; (3) the nature of the fatty acid compo-
sition of the inner backfat tissues, the outer
backfat tissues, the liver tissues, and the longis-
simus dorsi tissues; (4) the relation of compo-
sition to off -flavor (if an off-flavor is produced) ;
and (.5) the hyi)othesized metabolic interactions
of fatty acid families.

An off-flavor and a fishy flavor were detected
in the meat of pigs fed diets containing about
fr of menhaden oil.

Gas-liquid chromatographic analyses of the
tissues indicated that up to 28 saturated and

299

FISHERY BULLETIN: VOL. 69. NO. 2

Table 26. — Outer backfat tissue — comparison of correlation coefficients and significant degree of poIjTiomial re-
gression obtained by relating the quantity of menhaden oil consumed (.Y) until the pigs attained body weights
of 90.9, 79.5, or 58.0 kg to the amount of individual fatty acids deposited in outer backfat tissue (K).

Fattv
acid ted

and
deposited

Correlotion coefficients

when oil is fed until

the pigs weighed:

Last degree of polynomial significont when oil was
fed until the pigs weighed:

90.9 kg

79.5 kg

68.0 kg

90.9 kg 1 79.5 kg 68.0 kg

Degree F value

Degree F value

Degree | F

value

22,6 0.-3

0.85"

0.58-

0.74"

L

near

43.30"

L

near

666*

Linear

11.15"

22:5 1^-3

0.89"

0.85"

0.84"

L

neor

66.64"

L

near

30.88"

Linear

21.23**

22:5 U.6

__

._

22:4 io6

..

..

__

_.

._

20:5 u;3

0.89"

0.79"

0.74"

L

near

6325"

L

near

19.53**

Linear

11.12**

20:4 o.'3

0.76" •

0.84"

0.41

L

near

23.48"

L

near

28.60**

1.82

22:1 (?)

_..

..

20:4 u6

— 0.26

-0.28

-016

1.25

__

0.98

0.24

20:3

-0.03

-0.12

-0.15

—

0.01

—

0.17

0.19

21:1 l:.-9

—

—

—

—

—

20:2 a6

__

__

_.

20:2 1^-9

-0.36

-0.44

-0.37

_.

2.57

__

2.84

1.43

18:4 ■.■3

0.58"

0.36

0.18

L

near

8.63"

1.75

__

0.32

20:1 u9

-0 54"

-0.32

-0.37

L

near

7.14*

..

1.37

1.40

18:3 0.'3

0.49"

0.72"

0.08

L

near

5.45'

L

near

13.09"

0.06

20:0

0.57"

0.73"

0.35

L

near

8.32"

L

near

13.62**

1.29

18:2^:6

19:0

18:1 uj9

0.04

013

-0.36

-

0.03

--

0.22

—

1.35

-0.24

-0.47

-0.22

::

1.04

"

3.42

—

0.46

18:0

-0.13

-0.03

0.47

_.

0.27

_.

0.01

256

16:2

0.44-

-0.01

0.07

4.18

0.00

._

0.05

17:0

0.50*

0.06

0.24

L

near

5.66*

0.04

0.57

16:1 uj7

0.14

0.48

-0.40

..

0.33

__

3.59

1.70

16:0

-0.39

0.14

010

3.00

0.23

__

0.09

15,1

0.26

-0.18

006

._

1.28

__

0.40

0.40

15:0

0.43

0.04

0.08

3.89

0.02

__

0.06

14:1

0.32

— 0.05

O.OI

1.96

0 03

0.00

14:0

0.18

-0.25

-0.78*"

--

0.56

-'

0.81

Linear

14.14*

P <.05

P <.0I

unsaturated fatty acids were present. Unsat-
urated fatty acids from four of the fatty acid
families (co3, co6, aj9, and co7) were found in
each of the tissues.

The quantity of the characteristic fatty acids
(aj3) of the fish oil fed correlated significantly
and positively with the quantity of these fatty
acids deposited in the inner backfat tissues and
the outer ones and the liver tissues, but not in
the lovgisfsimus dorsi tissues.

Similarly, the quantity of these cuS fatty acids
fed correlated sio^nificantly and positively with
a weighted organoleptic score of the inner back-
fat tissues. Removal of these fatty acids from
the diet of the pigs at two different body weights
— namely, 68.0 and 79.5 kg — prior to their be-
ing marketed at 90.9 kg resulted in a loss of
significance by the correlation coefficients, al-
though the correlation coefficients obtained were
positive.

On a practical feeding basis, fish oil with sim-
ilar fatty acid composition consumption should
be limited to 0.8 Sr of the diet if fed until ]3igs
are marketed. If the oil is withdrawn from the
diet prior to marketing, higher levels can be fed.

LITERATURE CITED

AcKMAN, R. G., R. D. Burgher, a.nd P. M. Jang.aard.
196.3. Systematic identification of fatty acids in
the gas-liquid chromatography of fatty acid meth-
yl esters: a preliminary survey of seal oil. Can.
J. Biochem. Physiol. 41: 1627-1641.
Ackman, R. G., p. M. Jangaard, R. J. Ho^xe, and H.
Brockerhoff.

1964. Origin of marine fatty aciiis. I. Analyses
of the fatty acids produced by the diatom Skel-
etonema costatum. J. Fish. Res. Bd. Can. 21:
747-756.
Anglemier, a. F., and J. E. Oij)field.

1957. Feeding of various levels of pilchard (Cal-
ifornia sardine) oils to swine. J. Anim. Sci. 16:
922-926.

300

KIFER. SMITH, and VOUNG: EFFECT OF DIETARY FISH OIL

Table 27. — Loyjgissiimis doj-si tissue — comparison of correlation coefficients and significant degree of polynomial
regression obtained by relating the quantity of menhaden oil consumed (A') until the pigs attained body weights
of 90.9, 79.5, or 68.0 kg to the amount of individual fatty acids deposited in lonr/issimvs dorsi tissue (Y).

Fatty

Correlation coefficients
when oil is fed until

Lost degree of polynomial significant when oil was
fed until the pigs weighed:

and
deposited

the pigs weighed:

90.9 kg

79.5 kg 68.0 kg

90.9 kg

79.5 kg 1 68.0 kg

Degree

F value

Degree

F value Degree F value

22;6.^'3

-0.09

0.46

0.46

22,5 1^3

-0.22

0.75- •

0.24

22;5i.'6

..

__

22:4 ui

-0,26

0.09

0.23

20:5 al3

0.01

0.43

0.59-

20:'! 0.3

-0.34

0.05

0.10

22:1 (7)

__

__

20:4 u6

-0.58"

0.10

— 0.44

20:3

-0.22

0.27

-0.20

21:1 aj9

-0.32

-0.65"

0.38

20:2 ^.■6

-0.46"

-0.68"

-0.21

20:2 io9

-0.34

-0.39

-0.43

18:4 a'3

__

20:1 U'9

0.02

-0.45

-0.42

18:3 1^3

0.07

0.20

-0.23

20:0

-0.01

-0.05

-0.27

18:2 u6

-0.25

0.53'

-039

19:0

0.29

-0.02

-0.24

18:1 0)9

0.46"

-0.36

0.44

18:0

0.09

-0.17

0.40

16:2

-0.04

0.11

-0.13

17:0

-0.05

-O.ll

-0.12

16:1 w7

-0.09

-0.32

0.08

16:0

-0.04

-0.58*

-0.16

15:1

I5;0

-0.22

-0.04

-0.03

14:1

-0.06

0.32

-0.08

14:0

-0.20

-0.26

-0.11

0.15

3.29

Linear

15.82

0.85

__

1.19

0.10

0.00

__

2.73

2.26

-

0.03

8.76"

~~

0.11

0.84

0.91

1 96

Linear

8.70

4.56*

Linear

10.47'

2.24

--

2.17

O.OI

::

3.05

0.09

_.

051

0.00

__

0.04

t.15

Linear

4.77-

1 50

0.00

4.59*

__

1.77

0.35

0.02

__

0 14

004

__

0.15

0.13

_.

1.33

003

Linear

6.09"

0.89

::

0.02

006

._

1.35

0.74

0.84

2.38

0.53

0.52

4.79

0.09

2.16

0.38

1.50

0.41

2.02

1.91

0.51

0.68

1.64

0.55

2.17

1.73

0 14

0.14

0.06

0.25

0.01

0.06

0.12

P <.05

p <m

Banks, A., and T. P. Hilditch.

1932. The body fats of the pig. II. Some aspects
of the formation of animal depot fats suggested
by the composition of their glycerides and fatty
acids. Biochem. J. 26: 298-308.
Bhattacharya, R., and T. P. Hilditch.

1931. The body fats of the pig. I. Influence of
ingested fat on the component fatty acids. Bio-
chem. J. 25: 1954-1964.
Brown, J. B., and E. M. Deck.

1930. The occurrence of arachidonic acid in lard.
J. Amer. Chem. Soc. 52: 1135-1138.
Callow, E. H.

1935. Carcass quality of the pig in relation to

growth and diet. Empire J. Exp. Agr. 3: 81.
1938. The quality of the bacon pig's carcase. [Gt.
Brit.] Dep. Sci. Ind. Res., Rep. Food Invest. Bd.
1937: 41-44.
Ellis, N. R., and H. S. Isbell.

1926a. Soft pork studies. II. The influence of the

character of the ration upon the composition of

the body fat of hogs. J. Biol. Chem. 69: 219-238.

1926b. Soft pork studies. III. The effect of food

fat upon body fat, as shown by the separation

of the individual fatty acids of the body fat. J.
Biol. Chem. 69: 239-248.
Ellis, N. R., C. S. Rothwell, and W. O. Pool.

1931. The efi'ect of ingested cottonseed oil on the
composition of body fat. J. Biol. Chem. 92: 385-
398.
Ellis, N. R., and J. H. Zeller.

1930. Soft pork studies. IV. The influence of a
ration low in fat upon the composition of the body
fat of hogs. J. Biol. Chem. 89: 185-197.
Farquhar, J. W., W. Insi'll, .Jr., P. Rosen, W. Stoffel,
and E. H. Ahrens, Jr.

1959. The analysis of fatty acid mi.xtures of gas-
liquid chromatography: construction and opera-
tion of an ionization chamber instrument. Nutr.
Rev. (Suppl.) 17(8), Part 2, 30 p.
Frazer, E. B., J. H. Stothart, and H. S. Gutteridge.
1934. Feeding value for livestock and poultry —
Fish meals and oils. Can. Dep. Agr., Pam. 163,
9 p.
Hilditch, T. P., C. H. Lea, and W. H. Pedelty.

1939. The influence of low and high planes of
nutrition on the composition and synthesis of fat
in the pig. Biochem. J. 33: 493-504.

301

FISHERY BULLETIN, VOL. 61. NO. 2

HiLDITCH, T. P., AND W. H. PeDELTY.

1940. The influence of prolonged starvation on
the composition of pig depot fats. Biochem. J.
34: 40-47.
HiLDITCH, T. p., AND P. N. WILLIAMS.

1964. The chemical constitution of natural fats.
4th ed. Wiley, New York, 745 p.

Hill, E. G.

1966. Fatty acid composition of miniature swine
tissue lipids. In L. K. Bustad, R. 0. McClellon,
with M. p. Burns (editors), Swine in biomed-
ical research, p. 705-712. Frayn Print. Co.,
Seattle, Wash.

James, A. T.

1960. Qualitative and quantitative determination
of the fatty acids by gas-liquid chromatography.
/)( D. Click (editor) , Methods of biochemical anal-
ysis 8: 1-59. Intersci. Publ. Inc., New York.

LnwRY, R. R., AND I. J. TiNSLEY.

1966. Oleic and linoleic acid interaction in poly-
unsaturated fatty acid metabolism in the rat. J.
Nutr. 88: 26-32.

Marion, J. E., and J. G. Woodroof.

1963. The fatty acid composition of breast, thigh,
and skin tissues of chicken broilers as influenced
by dietary fats. Poultry Sci. 42: 1202-1207.
Miller, D., E. H. Cruger, Jr., K. C. Leong, and G. M.
Knobl, Jr.

1967. Dietary effect of menhaden-oil ethyl esters
on the fatty acid pattern of broiler muscle lipids.
Poultry Sci. 46: 438-444.

Miller, D., K. C. Leong, G. M. Knobl, Jr., and E. H.
Gruger, Jr.

1965. Increased nutritive requirements for chicks
to prevent exudation and dystrophy due to dietary

long-chain polyunsaturates. Poultry Sci. 44:
1072-1079.
Miwa, T. K.

1963. Identification of peaks in gas-liquid chroma-
tography. J. Amer. Oil Chem. Soc. 309-313.

Mohrhaler, H., and R. T. Holman.

1963a. Eff'ect of linolenic acid upon the metabolism

of linoleic acid. J. Nutr. 81: 67-74.
1963b. The eifect of dose level of essential fatty

acids upon fatty acid composition of the rat liver.

J. Lipid Res. 4: 151-159.
1963c. The effect of dietary essential fatty acids

upon composition of polyunsaturated fatty acids

in depot fat and er.vthrocj'tes of the rat. J. Lipid

Res. 4: 346-350.
Rahm, J. J., and R. T. Holman.

1964. Effect of linoleic acid upon the metabolism
of linolenic acid. J. Nutr. 84: 15-19.

Sink, J. D., J. L. Watkins, J. H. Ziegler, and R. C.
Miller.

1964. Analysis of fat deposition in swine by gas-
liquid chromatography. J. Anim. Sci. 23: 121-125.
Snedecor, C. W.

1956. Statistical methods, applied to experiments
in agriculture and biology. 5th ed. lov.-a State
Coll. Press, Ames, Iowa, 534 p.
TiNSLEY, I. J.

1964. The fatty acid composition of liver lipids
from rats raised on pork rations. J. Food Sci.
29: 130-135.
Vestal, C. M., C. L. Shrewsbury, R. Jordon, and 0.

MiLLIGAN.

1945. The influence of fish meal and fish oil on
the flavor of pork. J. Anim. Sci. 4 : 63.

302

CETACEANS FROM THE LESSER ANTILLEAN ISLAND OF ST. VINCENT

David K. Caedwell,' Melba C. Caldwell,'^ Warren F. Rathjen," and John R. Sullivan'

ABSTRACT

A preliminary list of cetaceans collected and observed during the course of a fishery for blackfish or
pilot whales (Glohicepliala) in the waters of the Lesser Antillean island of St. Vincent is presented
and includes: Megaptera novaeangliae, Steno breclaiiensis, Tiirsiops triincatus. Grampus griseus, two
species of Steiiella to which specific names are not formally applied, Feresa attenuata, Pseudorca cras-
sidens, Globicejjhala macrorhyncha, Orcinus orca, Physeter catodo^i, and Ziphius cavirostris. Nearest
published records in the western Atlantic are given, as well as limited biological notes on some of the
species. The taxonomic relationships of the two forms of Stenella are suggested and both species are
illustrated. Landings of pilot whales in the fishery over a period of 9 years are included.

There is a small but active fishery for blackfish
or pilot whales (Globicephala) centered around
the village of Barrouallie on the western or lee
side of the Lesser Antillean island of St. Vincent.
While the major direction of this fishery is the
pursuit of blackfish, intensive studies made by
the writers independently and cooperatively
over the past several years have shown that a
number of other small cetaceans are captured
as well. The primary purpose of the fishery
is the production of meat and cooking oil, both
used locally, and the species taken is not espe-
cially important to the fishermen, except that
the larger animals are the more profitable.
Hence the concentration on blackfish. Anything
that is seen is pursued except the larger and
fast baleen whales. The techniques and history
of the blackfish fishery have been discussed by
Brown (1945, 1947). Hickling (19.50), Morice
(1958), Allen (1966),° Morris (1966)," .Jackson

' The Florida State Museum and the Communication
Sciences Laboratory, University of Florida, Gainesville,
Fla. 32601.

" The Communication Sciences Laboratory, University
of Florida, Gainesville, Fla. 32601.

' National Marine Fisheries Service Exploratory
Fishing and Gear Research Base, Woods Hole, Mass.
02543.

' Formerly, U.S. Peace Corps, St. Vincent, West In-
dies ; present address : 49 Monroe Street, Lynbrook, N.Y.
11563.

' Allen, W. O. 1966. The fishing industry in St. Vin-
cent. St. Vincent Teachers College, Kingstown, St.
Vincent, Unpublished report (file no. 50), 42 p.

° Morris, E. L. 1966. A brief history of Barrouallie
from 1719 to present day (1966). St. Vincent Teachers

(1967),' Rathjen and Sullivan (1970), Caldwell
and Caldwell (in press), and others. In brief
it is conducted from small open boats launched
daily from shore and powered primarily by sail
and oar (see Rathjen and Sullivan, 1970). One
motor launch recently has been employed and it
produces the majority of the catches of the faster
swimming small dolphins. Other motor launch-
es, both inboard and outboard, are planned
(Caldwell and Caldwell, in press). The ceta-
ceans are taken both by hand harpoon and by
small gun harpoons fired from a fixed stand on
the bow of the boat.

We present here a summary of our findings
to date regarding species taken in the fishery.
The records of odontocetes are supported by
skeletal remains and/or recognizable photo-
graphs of carcasses or parts of carcasses. Copies
of all of the photographs mentioned below are
in the Caldwells' files with duplicates of some
in those of Rathjen and Sullivan. The skeletal
material, unless otherwise stated, presently is
being studied by the Caldwells at the Florida
State Museum, Gainesville. The "SV" numbers
associated with records discussed in the text
are field numbers in the Caldwells' files. With
more collecting and analysis of the results.

Manuscript received January 1971.

FISHERY BULLETIN: VOL. 69. NO. 2, 1971.

College, Kingstown, St. Vincent, Unpublished report
(file no. 39), 51 p.

' Jackson, L. R. 1967. The blackfish industry of
Barrouallie, St. Vincent. St. Vincent Teachers College,
Kingstown, St. Vincent, Unpublished report (file no. 26),
38 p.

303

FISHERY BULLETIN; VOL. ()9. NO.

both of which are ongoing, it should be possible
to say more about some of the St. Vincent faunal
elements than is appropriate now. Our purpose
here is only to provide an annotated summary
of the existing records for this island in order
to give for the first time a relatively complete
list of such a fauna from one specific locality
in the Antilles and to iirovide a firmer basis for
zoogeographic statements required for ongoing
studies in this and other disciplines in the West
Indies and Caribbean.

Although there are a number of individual
records of cetaceans from the West Indies (in
part summarized by Hershkovitz, 1966) , or re-
ports which include as many as three or four
species, there are few reports which include
enough of the expected species to give sufficient
data for evaluating the local cetacean fauna.
The best of these are from the northern Antilles
(from Cuba by Cuni, 1918, and Aguayo, 1954 ;
and from Puerto Rico to Antigua by Erdman,
1970).

Studies similar to ours on small cetaceans, but
more detailed, have been conducted on the At-
lantic coast of Africa in the vicinity of Senegal
and to some lesser degree the Ivory Coast and
the Cape Verde Islands. The odontocete ceta-
cean fauna in those similar latitudes is remark-
ably similar to that of St. Vincent even though
the two areas lie some 5000 km apart across the
open sea. This similarity extends even to forms
such as Steno and Ferrsa that are generally
rare in collections. Cadenat and others have
published a series of reports on their studies
of the African fauna, but a list of the s])ecies
found can be had by consulting a combination
of two of these (Cadenat, 1919, 1959). The
latter also summarizes much of the other liter-
ature on the cetaceans of the area. Van Bree
and Cadenat (1968) in addition recorded Pepo-
nocephala electra from Senegal.

SPECIES ACCOUNTS

With the exception of a spotted dolphin, we
follow Rice and SchefYer (1968) in our arrange-
ment of species and in the scientific and/or com-
mon names ai)plicd to them.

Megaptera novaeangUae (BOROWSKI) —
HUMPBACK WHALE

In early May 1968, an individual of adult
size slowly passed close along the lee shore of
St. Vincent in a southward direction. Several
of the St. Vincent whalemen, familiar with this
species from seeing it in a nearby humpback
fishery at Bequia, observed this individual from
boats but made no effort to harpoon it. The
St. Vincent whalemen tell us that they see a
few individuals of this species each year but that
they never try to harpoon one because of the
large size of these whales.

A few humjjbacks are usually taken each year
(mostly from February to April) in the Bequia
fishery just to the south in the St. Vincent Gren-
adines which utilizes bomb guns in addition to
hand harpoons. Accounts of the latter fishery
were given by Brown (1945), Fenger (1958),
Mitchell (1965), and Quashie (1966).^ An early
account of New England whaling vessels hunt-
ing humpbacks in the region was included by
Lindeman (1880) , but Clark (1887: pi. 183) for
as early as 1880 included waters near St. Vincent
on a map showing abandoned humpback whaling
grounds. These and other reports mention
Megaptera in St. Vincent and or nearby waters.

Steno bredatieiisis (LESSON) —
ROUGH-TOOTHED DOLPHIN

A skull (SV-l-SB) of a specimen of unknown
size and sex was obtained from the fishery in
the spring of 1969. This is the first record for
this species from St. Vincent and from the Ca-
ribbean. We find no prior and contemporary
basis for Kellogg's (1940: 69) inclusion of this
species in the Caribbean fauna, nor for the in-
dication by Hall and Kelson (1959: 819) that
its range is continuous in the western Atlantic
from Virginia to South America.

The records closest to St. Vincent in the west-
ern Atlantic are from off Havana, Cuba (and
thus non-Caribbean) to the north, as S. mstratNS
(see Aguayo, 1954), and from an unstated lo-
cality off the Brazilian coast to the south (Ham-

" Quashie, I. N. 1966. The whale indu-stry in Bequia.
St. Vincent Teachers College, Kingstown, St. Vincent,
Unpublished report (file no. 80), 32 p.

304

CALDWELL ET AL.: CETACEANS OF ST. VINCENT

ilton, 1945). S. fuscus Gray, from an un-
stated area in Cuban waters, may be this species
(True, 1889: 27) and if so would represent
another Cuban record. However, the unique
type of this latter species, a preserved fetus,
apparently was lost even in True's time and the
record cannot be substantiated. Presumably the
previous Caribbean records of this species (see
above) have been based on this Cuban material.

Tiirsiops truiicatus (MONTAGU) —
BOTTLENOSED DOLPHIN

The Caldwells have color ijhotographs of the
head of an immature specimen of unknown size
and sex taken in the fishery on 17 May 1968.
The head was obtained from a market where
it had been split longitudinally in order to get
to the brains, which are eaten. The skull (SV-
1-TT) is also split but comjilete.

This species has not been reported from St.
Vincent before, but Turner (1912: 13.5) listed
the mandible (as Turslops tursio) of a speci-
men from nearby Barbados.

Grampus grhet/s (G. CUVIER) —
RISSOS DOLPHIN OR GRAY GRAMPUS

The Caldwells have the skull (SV-l-GG) and
color ijhotographs of the intact head of a speci-
men of unknown size and sex taken in the fish-
ery in the summer of 1968. They also have
the skulls of two more specimens (SV-2-GG,
SV-3-GG) , of unknown size and sex, taken dur-
ing the summer of 1970.

In addition, the Caldwells have black and
white photographs (SV-4-GG) of an individual
(also of unknown size and sex) taken in Sep-
tember or October 1967.

Until recently this species was considered a
northern foi'm in the western Atlantic, but
specimens are now available from Florida (Paul,
1968) and there is a recent sight record from
the Virgin Islands (Erdman, 1970). The rec-
ords from St. Vincent seem to be the mo-st south-
ern in the western Atlantic, and the only West
Indian ones supported by specimens. Mention
of this species in the St. Vincent fishery was
made by Caldwell and Caldwell (in press).

Stenella, SPECIES A— LONG-SNOUTED
OR SPINNER DOLPHIN

The Caldwells have color photographs of the
head of a specimen of unknown size and sex
taken in the fishery on 17 May 1968. The skull
(SV-l-SL) was saved but is split longitudinally
(see Tursiops account above).

The Caldwells measured three females (177.0
[SV-2-SL], 166.5 [SV-3-SL] and 1.50.0 [SV-4-
SL] cm from tip of upper jaw to fluke notch)
which were taken on 24 May 1968. They have
black and white photographs (Figure 1) of the
middle-sized animal taken from several angles,
and the skulls of the two largest.

There is confusion in the literature regarding
the systematics of the long-snouted spinning
dolphins of the genus Stenella, and the group
is badly in need of revision. The St. Vincent
dolphins clearly spin, as observed by all of us
at sea off the island, and our specimens (ex-
ternally) and their skulls compare favorably
with those reported from the northern Gulf of
Mexico as S. longhvstris (Gray) by Layne
(1965), but neither we nor Layne made similar
comparisons with S. roseiventris (Wagner)
which Rice and Scheflfer (1968) retained as a
species separate from 5. loiigirostris although
many writers consider them to be synonyms.
For the present we do not apply a specific name
to our material but note only that the specimens
from St. Vincent appear to belong to the "long-
iwstris-roseiventris" group of Stenella.

The closest western Atlantic records for dol-
phins of this type are from the Bahamas near
Miami. Fla., to the north (Moore, 1953) and
(as Delphinus micivps) from Brazil (no local-
ity) to the south (Gray, 18.50: 126).

Stenella, SPECIES B— SPOTTED OR
BRIDLED DOLPHIN

The Caldwells measured a 172.5-cm male
taken in the fishery on 24 May 1968, and have
black and white ])hotographs (Figure 2) taken
from several angles and the skull (SV-l-SF).
The photographs, taken under adverse lighting
conditions, do not show the spotted ])igmenta-
tion pattern of the specimen because in addition

30.-

FISHERY BULLETIN: VOL. 69. NO. 2

Figure 1. — Stenella, species A, 166.5-cm female spinner dolphin (SV-3-SL) landed at Barrouallie, St. Vincent,
on 24 May 1968. UPPER: lateral view of entire carcass; LOWER: view of head and pectoral region showing
prominent features of pigmentation. Photographs made under conditions of adverse lighting several hours after
the animal had been harpooned and kept in the sun in an open boat at sea. (Photographs by William A. Huck.)

it had been in the sun most of the day and had
turned essentially black as dolphins often do
under such circumstances. The underlying spot-
ted pigmentation was, however, like that in the
photographs noted below.

The Caldwells also have a color lateral photo-
graph of the anterior part of the body and one
of most of the ventral side of a male, apparently
an adult (SV-2-SF), taken in early June 1967.
Both of these photographs show details of the

spotted pigmentation, and a black and white
reproduction of the one of the head clearly
shows this (Figure 3).

The St. Vincent spotted dolphins we have seen
seem best to fit Eraser's (19r)0b) and Nishiwaki's
(1965) discussions and illustrations of S. fron-
talis (G. Cuvier). We tentatively would as-
sign the St. Vincent records to that si)ecies
were it not better to refrain from doing so at
this time becau.se of the already chaotic taxo-

306

CALDWELL ET AL. : CETACEANS OF ST. VINCENT

Figure 2. — Stenella, species B, 172.5-cm male spotted dolphin (SV-l-SF) landed at Barrouallie, St. Vincent,
on 24 May 1968. Photograph made under conditions of adver.se lighting several hours after the animal had been
harpooned and kept in the sun in an open boat at sea. (Photograph by William A. Huck.)

nomic situation in which one finds the spotted
dolphins of this genus.

The Caldwells have had considerable exper-
ience in Florida with carcasses and live speci-
mens of the spotted species S. phtqiodon (Cope)
(see D. K. Caldwell and M. C. Caldwell, 1966)
and do not believe that that species as they
understand it is the same as the St. Vincent
form. Perrin (1970) concurred that S. plagi-
odon is separable from S. frontalis at least on
the basis of color pattern. We concur with
Mitchell (1970: pi. .5) that the spotted dolphin
he pictured as having been taken from conti-
nental shelf waters near Trinidad is best as-
signed to the species S. plagiodon. Despite the
relatively close proximity of the Trinidad record
to St. Vincent (some 275 km), we believe that
two species of spotted dolphins are involved and
that Mitchell's record bears out an earlier con-
tention by the Caldwells (D. K. Caldwell and
M. C. Caidwell, 1966: 2) that S. plagiodon is a
species found primarily in offshore waters near
continents. Around the seemingly more isolated
noncontinental islands of the Antilles, at least,
it appears in our experience to be replaced by
S. cf. frontalis or some very similar spotted spe-
cies. We believe, therefoi-e, that Rice and

Scheffer (1968) wei-e too conservative in their
conclusions regarding spotted dolphins and that
more than one species exists.

A mandible, reported as Prodelphimis sp., but
probably of the same species as ours from St.
Vincent, was listed from nearby Barbados by
Turner (1912: 138). The next closest western
Atlantic record (as Prodelphinus froenatus) is
from southeastern Florida (Allen, 1925) to the
north. It ap])arently has not been recorded to
the south (see Hershkovitz, 1966: 36).

Feresa attenuata GRAY —
PYGMY KILLER WHALE

An adult skull (SV-l-FA) of undetermined
sex was obtained from the fishery in the sjjring
of 1969. A detailed report on this specimen was
prepared (Caldwell and Caldwell, 1971) as
it then was the first record for the western
Atlantic. After this report was accepted for
publication, a record from Texas was published
(James, Judd, and Moore, 1970) . To our knowl-
edge the St. Vincent specimen is still the only
record from the Caribbean and West Indian
region.

307

FISHERY BULLETIN, VOL. 69. NO. 2

FlcrBE 3. — Stenella, species B, apparently adult male
spotted dolphin (SV-2-SF) landed at Barrouallie, St. Vin-
cent, in early June 1967. Lateral view of head showing
prominent features of pigmentation not shown (but pre-
sent) in the animal depicted in Figure 2. Animal in fresh-
ly killed condition. (Photograph by John R. Sullivan.)

Pseudorca crassidens (OWEN) —
FALSE KILLER WHALE

The Caldwells have two adult skulls, a male
(SV-l-PC) and a female (SV-2-PC), from an-
imals of unstated size taken in the fishery on 10
September 1970.

Three individuals of this species were taken
in the fishery on 9 March 1969, and the Cald-
wells have several teeth (SV-3-PC) said to have
come from one or more of these animals. Five
others had been taken on 12 February and seven
more were obtained on 7 December 1969.

Except for a brief mention by Caldwell and
Caldwell (in press), false killer whales have
not been reported from St. Vincent previously.
The closest record based on a specimen is from
Aves Island off the Venezuelan coast some 675
km to the southwest (Miller, 1920). Bruyns
(1969) included a sight record made at sea 115
km east of Tobago (some 280 km southeast of
St. Vincent).

Glohicephala macrorhyncha GRAY— SHORT-
FINNED PILOT WHALE OR BLACKFISH

It is upon this species that the St. Vincent
whale fishery is based and it is therefore by
far the most abundant species in the overall
landings in the fishery. From the fishery we
have eight skulls: two from males measuring
about 5 (SV-l-GM) and 6 (SV-2-GM) m in total

length collected in the second week of June 1967;
two from females measuring about 4.5 (SV-3-
GM) and 5 (SV-4-GM) m collected with the
males; and four others (SV-5 to 8-GM) from
adults or near adults of unknown size and sex
collected in the summer of 1968.

We have seen many carcasses of fresh-caught
animals and have various color and black and
white photographs in our files. We also have
examined many skulls on the St. Vincent beaches
where the carcasses are butchered. The car-
casses all have short pectoral flippers and the
skulls have expanded premaxillary bones cov-
ering the maxillaries. These characters are
typical of this species (see Fraser, 1950a).

A female taken on 20 May 1968 contained a
male fetus measuring 69 cm in length in a
straight line from the anteriormost part of the
head to the fluke notch. The Caldwells did not
have facilities to preserve this specimen, but
have a color photograph (SV-9-GM) which
shows it to be a light reddish brown.

A male measuring 4 m in total length that
was taken on 21 May 1968 had several of the
obligate cetacean barnacle {Xenobalaynis globi-
cipitus) on the trailing edge of its left flipper.

We have not examined .stomach contents of
pilot whales landed at St. Vincent, but the whale-
men tell use that they include both squid (in-
cluding very large ones) and fish.

Cyamid parasites and remoras have been ob-
served on blackfish landed at St. Vincent but
no specimens so far have been collected.

Blackfish previously have been recorded from
or near St. Vincent by Brown (1945, 1947),
Hickling (1950), Fenger (1958), Morice (1958),
Caldwell and Erdman (1963), Allen (see foot-
note 5), Morris (see footnote 6), Jackson (see
footnote 7), Rathjen and Sullivan (1970), Cald-
well and Caldwell (in in'ess), and others. Al-
though specific identifications were not always
given, our experience has shown that only G.
macrorhyncha likely is involved.

Obtained from the Barrouallie Fishermen's
Cooperative Society, catch statistics for the ])eri-
od 1962-1970 are included in Table 1. These
are pilot whales landed at Barrouallie, the main
whaling port of St. Vincent. The monthly var-

308

CALDWELL ET AL.: CETACEANS OF ST. VINCENT

Table 1. — Landings of blackfish (Glohiceplinlii macrorhyiichn) at the port of Barrouallie, St. Vincent, for the peri-
od January 1962, through December 1970. Precise data concerning the following variables, in part affecting the
numbers of blackfish landed, are not available : weather conditions, seasonal holidays, numbers of whaling boats
operating that month, and more recently, the presence or absence of engines.

Month

1962

1963

1964

1 1965

1964

1967

1968

1969

1970

Tolol

Average

January

6

9

8

15

8

6

28

4

10

94

10.4

February

7

15

37

18

5

35

85

12

15

229

25.4

March

n

32

17

19

7

15

12

6

12

131

14.6

April

6

32

42

12

46

24

49

12

21

244

27.1

May

5

57

9

22

50

41

40

53

55

332

36.9

June

)5

80

48

12

41

53

21

50

28

348

38.7

July

7

70

11

18

7

21

25

12

27

198

22.0

August

2

31

20

27

12

14

48

(')

5

= 159

= 19.9

September

4

55

43

24

67

16

27

(')

22

=258

=32.3

October

4

33

26

9

30

24

44

(')

14

= 184

=23.0

November

25

10

7

4

40

17

2

24

23

152

16.9

December

5

I

7

3

10

3

6

3

0

=38

=4.8

Total

97

425

275

183

323

269

387

= 176

232

2367

^ No records kept, but blackfish taken.
2 Based on landings for 8 years only.
^ Year incomplete.

iations reflect local weather conditions which
affect the ability of the boats to go out and the
whalemen to see their quarry, more than tlie
true abundance of whales. In addition, whaling
usually almost or completely ceases for approx-
imately 2 weeks before and 2 weeks after Christ-
mas, in observance of the holidays. We are told
that the blackfish are there year round.

Orcintts orca (LINNAEUS)-KILLER WHALE

On 13 May 1968, two females (an adult [SV-
1-00] and subadult [SV-2-00] of unknown
sizes) and one juvenile male (SV-3-00 of un-
known size) were harpooned from a pod of six
animals. The young male was harpooned first,
and the other animals reportedly stood by (see
M. C. Caldwell and D. K. Caldwell, 1966, re-
garding this kind of behavior) just as the St.
Vincent whalemen report the blackfish in that
fishery often do when certain ones of their kind
ai-e harpooned. We have several color photo-
graphs of the carcasses which show the striking
black and white color pattern characteristic of
this species. The skulls of the three harpooned
specimens are now in the possession of the
Caldwells.

Sullivan noted that one of the larger animals
had several cyamid parasites on the skin, but
specimens were not collected. His photographs
show only that the parasites are cyamids but as

Leung (1967) did not include Orclnus among
the known hosts for cyamids the observation is
noted. Caldwell and Caldwell (1969) reported
that all three of these whales had eaten leather-
back sea turtle (Dermochebjs coriacea).

Three additional killer whales, including a
6-m male with very heavily worn teeth, were
taken from a school of eight on 11 July 1968,
but no specimens or photographs are available.
One of the animals reportedly had cyamid |)ar-
asites. The school was said to have been moving
north about 10 km off the lee shore of the island.
The fishermen's records show that four more
were taken on 4 June 1969.

Jackson (see footnote 7) noted that killer
whales are taken in the St. Vincent fishery and
included photographs of carcasses being butch-
ered on shore- Rathjen and Sullivan (1970) and
Caldwell and Caldwell (in press) also noted the
occasional capture of individuals of this species
by the St. Vincent whalemen.

These records are the southernmost in the
western Noilh Atlantic for killer whales.
Moore (1953) listed this species from off Miami,
and Backus (1961) from the Bahamas. Erdman
(1970) included several sight records from the
general vicinity of the Virgin Islands. In the
western South Atlantic, killer whales have not
been reported north of Buenos Aires (as the
type of Orca magellanica Burmeister — see
Hershkovitz, 1966: 84).

309

FISHERY BULLETIN; VOL. 69. NO.

Physeter catodon (LINNAEUS) —
SPERM WHALE

The Caldwells have the prepared lower jaw
(SV-l-PCA) and color photographs of the en-
tire carcass of a juvenile female (ca. 8 m in total
length) taken in the fishery on 23 May 1968.
The teeth were just beginning to erupt and their
pulp cavities were completely open. Mention
of the stump of the left pectoral flipper of this
animal, possibly missing as the result of a shark
bite, was made by Wood, Caldwell, and Caldwell
(1970), and a photograph of the carcass on the
beach was included by Caldwell and Caldwell
(in press).

The Caldwells have partial sets of mandibular
teeth from two other sperm whales taken in the
fishery prior to 1968. In one set (SV-2-PCA)
the pulp cavities are fully open, while in the
other set (SV-3-PCA), actually smaller teeth,
the cavities are fully closed.

The fishermen's records show the capture of
three sperm whales on 19 April 1967, two on 2
January 1969, and two on 25 April 1969 (a third
was harpooned on this latter occasion but was
lost with the boat). Mr. Griffith Arrindell, a
leader of the St. Vincent whale fishery, told us
that sperm whales are seen most commonly in
the region from October to late spring, although
some appear to be present year round.

Jackson (see footnote 7) and Rath j en and Sul-
livan (1970) mentioned that sperm whales are
sometimes taken in the St. Vincent fishery and
the latter writers included a photograph of the
head of an 8-m male. Townsend (1935: chart B)
showed sperm whales between St. Vincent and
Barbados in January and February, Brown
(1942) noted that a few sperm whales once were
taken off the lee (western) side of Barbados
(toward St. Vincent) and Brown (1945) and
Fenger (1958: 44) recorded the fact that this
species sometimes is taken in the nearby waters
of Bequia and other islands of the Grenadines.
Clark (1887: pi. 183) showed active sperm
whaling grounds, fished by New England whal-
ers, all around the southern Lesser Antilles
in 1880, and this whaling continued thereon
into the first part of the 20th century.

Ziphius cavirostrh G. CUVIER— GOOSE-BEAKED
WHALE OR CUVIER'S BEAKED WHALE

The Caldwells have color photographs of the
head of a female (SV-l-ZC) and somewhat
longer views of the carcass of her nearly term
fetus calf (SV-2-ZC) of undetermined sex taken
in the fishery in late summer 1967. Although
it was recently reported from nearby Barbados
(Caldwell, Rathjen, and Caldwell, in press),
this species has not been reported previously
from St. Vincent.

UNRECORDED
BUT EXPECTED SPECIES

Both the descriptions given us by the whale-
men and distributional records from other lo-
calities in the region lead us to expect that
several additional species eventually will be re-
corded from St. Vincent. It is beyond the scope
of the present preliminaiy report to discuss
these, but a summary of all known records of
marine mammals from the West Indies and
Caribbean that is in preparation by the Cald-
wells suggests that the list from St. Vincent
might be expected to include any of several spe-
cies of Balaenoptera, Stenella caeruleoalba, Del-
phimis, and Mesoplodon. Kogia and Pepono-
cephala might also be expected, but the present
suggestive evidence is not as strong.

ACKNOWLEDGMENTS

A number of people at Barrouallie, the prin-
cipal and most active whaling ]5ort on St. Vin-
cent, have been of tremendous help in our study
in providing observations from their own direct
experience, access to records of the Barrouallie
Fishermen's Cooperative Society, and in the col-
lection and shipping of specimens. In this
regard Griffith Arrindell has given us unselfish
and unswerving assistance desjnte our constant
pressure and questions. Conrad Francis and
William O'Garro of that town also have given
much of their energy. Partial financial sup-
liort for certain jihases of the study has come
to DKC from the American Philosophical So-

310

CALDWELL ET AL : CETACEANS OF ST. VINCENT

ciety (gi'ant number 962 — Johnson Fund) and
the U.S. National Science Foundation (g-rant
number GF-241). Marineland, Inc. has aided
in the preparation of photographs and in pro-
viding temporary storage for specimens.

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Ertrage in den Jahren, 1869-1878. Dr. A. Peter-
mann's Mittheilungen aus Justus Perthes' Geo-
graphischer Anstalt, Gotha, Erganzungsband 13,
1879-1880, Ergiinzungsheft No. 60, 95 p.
Miller, G. S., Jr.

1920. American records of whales of the genus
Pseudorca. Proc. U.S. Nat. Mus. 57(2311) : 205-
207, pis. 27-31.
Mitchell, C.

1965. Finisterre sails the Windward Islands. Nat.
Geogr. Mag. 128(6): 755-801.
Mitchell, E.

1970. Pigmentation pattern evolution in delphinid
cetaceans: an essay in adaptive coloration. Can.
J. Zool. 48: 717-740, pis. 1-15.
Moore, J. C.

1953. Distribution of marine mammals to Florida
waters. Amer. Midi. Natur. 49: 117-158.
MORICE, J.

1958. Animaux marins comestibles des Antilles
Francaises (Oursins, Crustace's, Mollusques, Pois-

sons, Tortues et Cetace's). Rev. Trav. Inst. Peches
Mar. (Inst. Sci. Tech. Peches Mar., Paris) 22(1) :
85-104.

NiSHIWAKI, M.

1965. Whales and pinnipeds. [In Japanese.]
Univ. of Tokyo Press, Tokyo, 439 p.
Paul, J. R.

1968. Risso's dolphin. Grampus griseiix, in the
Gulf of Mexico. J. Mammal 49: 746-748.
Perrin, W. F.

1970. Color pattern of the eastern Pacific spotted
porpoise Stenella graffmani Lbnnberg (Cetacea,
Delphinidae). Zoologica 54(4) : 1.35-142, pis. 1-7.
Rathjen, W. F., and J. R. Sullivan.

1970. West Indies whaling. Sea Frontiers
16: 130-i;j7.
Rice, D. W., and V. B. Scheffer.

1968. A list of the marine mammals of the world.
U.S. Fish Wildl. Serv., Spec. Sci. Rep. Fish. 579,
16 p.
Townsend, C. H.

1935. The distribution of certain whales as shown
by logbook records of American whaleships.
Zoologica 19(1): 1-50, 4 maps.
True, F. W.

1889. Contributions to the natural history of the
cetaceans, a review of the family Delphinidae.
Bull. U.S. Nat. Mus. 36, 191 p., 47 pi.
Turner, W.

1912. The marine mammals in the Anatomical
Museum of the University of Edinburgh. Mac-
millan, London, 207 p.
Wood, F. G., Jr., D. K. Caldwell, and M. C. Caldwell
1970. Behavioral interactions between porpoises
and sharks. In G. Pilleri (editor), Investigations
on Cetacea 2: 264-277, 2 pis.

312

CONTRIBUTIONS TO THE BIOLOGY OF THE ROYAL
RED SHRIMP, Hymenopenaeus rohnstus SMITH'

William W. Anderson^ and Milton J. Lindner"

ABSTRACT

The royal red shrimp, Hymenopenaeus robustus, has been located in commercial concentrations in three
areas off the coast of the United States in depths from about 250 to 550 m : one area, known as the St.
Augustine Grounds, is off the east coast of Florida; another is off the Dry Tortugas; and the third
is off the Mississippi River Delta.

Information on the biology of the species on the St. Augustine Grounds was collected intermittently
from 1957 to 1967.

The reproductive systems of males and females are described and illustrated. The ovaries of ripe
females are dark red or maroon, and the exceedingly large spermatophores are bright yellow. We
observed no indication of sex reversal.

Burrowing and swimming habits as observed from the research submarine Aluminaut are summarized.

The early life history of H. robushis is unknown. Neither larval nor postlarval stages were en-
countered in the plankton collections of the M/V Theodore N. GUI. Juveniles under 50 mm total
length were not caught.

Size of shrimp was not correlated with depth but appeared to be correlated with latitude. Usu-
ally shrimp were larger north of lat 29°39' N than between lat 29°00' and 29°39' N.

Males mature at about 125 mm and females at about 155 mm total length. In each sex, maturity
is reflected by a change in the regression of carapace length on total length.

Spawning probably occurs throughout the year, but the peak is between January and May.

Year classes are evident in the length distributions. Recruitment on the fishing grounds begins
when the shrimp are approaching 1 year of age and are less than 100 mm total length. They reach
maturity at about 3 years, and minimum life span appears to be no less than 5 years. Recruitment
is probably not complete until at least 2 years. Most of the shrimp on the fishing grounds are mature.

The royal red shrimp, Hymenopenaetis robustus
Smith, a large deepwater penaeid (Figure 1),
has a wide distribution from the east coast of
the United States to well down the east coast
of South America, principally in depths of 256
to 549 m (140-300 fm).

Surveys by the Bureau of Commercial Fish-
eries (now the National Marine Fisheries Ser-
vice) have indicated three major concentrations
of these shrimp off the coast of the United States
that have commercial possibilities: (1) off St.
Augustine on the east coast of Florida (Figure
2), (2) off the Dry Tortugas in the Florida

' Contribution No. 301, National Marine Fisheries
Service Biological Laboratory, Galveston, Tex. 77550.

- State Game & Fish Commission, Coastal Fisheries
Division, Brunswick, Ga. 31520.

' Formerly National Marine Fisheries Service Bio-
logical Laboratory, Galveston, Tex. 77550.

Manuscript received January 1971.

FISHERY BULLETIN: VOL. 69, NO. 2, 1971.

im-.

m >>

t,

v^'

Figure 1. — Adult female and male royal red shrimp,
showing great difference in size of sexes. Female (up-
per) 210 mm and male (lower) 160 mm total length.

313

FISHERY' BULLETIN: VOL. 69, NO. 2

Figure 2. — Royal red shrimp grounds off east coast of
Florida. Large dots, lat 28°30' to 30°00' N, represent
most productive portion.

Straits, and (3) off the Mississippi River Delta.
Accounts of these surveys were given by Spring-
er and Bullis (1952, 1954), Bullis (1956), Bullis
and Rathjen (1959), Bullis and Thompson
(1959), Cummins and Rivers (1962), and Bullis
and Cummins (1963). Anderson and Bullis
(1970) gave an account of direct observations
made on the St. Augustine grounds during a

dive with the research submarine Aluminaut on
September 21, 1967; Klima (1969) gave the
length-weight relation; and Roe (1969) sum-
marized the distribution on the three major
grounds off the southeastern United States.

Biologists at the former BCF Biological Lab-
oratory, Brunswick, Ga., studied the biology of
royal red shrimp at the grounds off St. Augus-
tine, Fla., by accompanying vessels of the BCF
Exploratory Fishing and Gear Research Base,
Pascagoula, Miss., and of the Exploratory Fish-
ing Station, Brunswick, Ga. The work contin-
ued from 1957 to 1967, as opportunities arose,
on the exploratory fishing vessels Combat, Silver
Bay, and Oregon.

This paper presents the results of these 11
years of intermittent data-gathering.

THE ST. AUGUSTINE GROUNDS

The part of these grounds generally fished
extends from about lat 28°30' N to 30°00' N
in 256 to 475 m (140-260 fm) but the most
productive part is between lat 29°00' N and lat
30°00' N, and it is from this area that most
of the data were obtained.

The BCF surveys of the St. Augustine
Grounds indicate that they average about 15.4
km (8.3 nautical miles) in width and have a
steep angle of descent. The bottom between
183 and 256 m (100 and 140 fm) is largely un-
trawlable owing to dense stands of deep-sea
alyconarians (sea fans) and limestone forma-
tions. Between 256 and 475 m ( 140 and 260 fm)
the bottom is largely sand or silty-sand sedi-
ments (referred to as "green mud" by fisher-
men), is relatively free of obstructions, and
provides excellent trawling conditions. Deeper
than 475 m (260 fm) , extensive patches of deep-
sea coral, Lophelia proUfera, make the bottom
hazardous to trawling with standard shrimp
gear.

Anderson and Bullis (1970) made the follow-
ing observations from the Aluminaut in 457 to
274 m (250-150 fm), and beUveen lat 29°10' and
29''20' N: "The bottom was remarkedly free
from obstructions and consisted of a grayish,
loosely constituted sediment that readily clouded
the water at the least disturbance. It was

314

ANDERSON and LINDNER; BIOLOGY OF ROVAL RED SHRIMP

formed into a myriad of shallow depressions and
mounds, pitted with holes. Claws protruding
from many of these holes indicated the richness
of the crustacean bottom fauna. Some fishes
were also observed in holes, but these were not
nearly so numerous. From the bottom port it
was possible to see directly into some of the
holes, and we observed animals that would have
been invisible at an angle."

These fishing grounds are directly under the
Gulf Stream.

DATA AND METHODS

The data were obtained from operations of
several vessels either owned or leased by the
BCF — M/ V Combat, a 30-m converted mine-
sweeper; M/V Silver Bay. a 29-m New England-
type trawler; and the R/V Oregon, a 30-m
trawler. Bullis (1956) and Bullis and Rathjen
(1959) have given details of vessels, gear, and
operating procedures.

The data consist of length measurements and
observations on ovarian development taken from
random samples (100 specimens, if this number
or more were caught; the total catch if fewer
wei'e caught) at irregular intervals from 1957
to 1967 (Table 1). They also consist of one set

Table 1. — Cruise dates, number of stations, and number
of H. robustiis in samples.

Vessel

Cruise dates

Stations
sampled

Shrimp

measured

Males

Females

Number

Number

Number

Combat

Apr 26-28, 1957

7

495

624

Combat

May 29-31, 1957

3

187

373

Combat

July 17-30, 1957

9

350

456

Combat

Aug, 13-20, 1957

18

798

874

Sili'tr Bay

Nov. 20-25, 1957

14

441

755

Silver Bay

June 11-22, 1958

23

1,136

1,811

Silver Bay

Jan. 18-28, 1960

13

403

356

Silver Bay

Apr. 30-May 3, 1960

10

379

463

Silver Bay

Apr. 28-May 1, 1961

12

489

601

Silver Bay

Jan. 16-Feb. 22, 1962

24

831

1,386

Stiver Bay

Aug. 22-28, 1962

10

393

525

Silver Bay

Sept, 25-28, 1962

8

373

376

Silver Bay

Feb. 5-7, 1964

6

290

309

Oregon

Nov. 11-18, 1964

21

863

1,233

Oregon

July 20-22, 1967

6

251

299

Total

189

7,734

10,441

of total length-carapace length measurements
from nonrandom samples taken during July

1957. Date, location, depth (with two excep-
tions) , and duration of haul are known for each
trawling station from which the samples were
taken. Data on bottom temperatures are not
available. The location of each trawling station
was obtained by sonar fixes and the depth, in
fathoms, from sonic depth recordings. The
depths have been converted to the nearest meter.

Throughout almost every cruise during which
length measurements were taken, the operation
simulated commercial fishing; consequently the
shrimp measured were caught by several types
of trawls in a wide range of sizes. Mesh sizes,
however, probably did not vary much. The
most commonly used trawl was constructed of
"commercial" nylon webbing with 2-inch (50.8-
mm) stretched mesh in the body and li/>-inch
(38.1-mm) stretched mesh in the cod end. These
sizes of mesh are generally used by commercial
shrimp fishermen. As shown by Berry and
Hervey (1965), the greatest inside dimensions
usually are somewhat less than 50.8 mm and 38.1
mm, respectively. Measurements we made on
the greatest inside mesh dimensions of the
shrimp trawls used by the exploratory vessels
for capturing H. robustus indicate a range be-
tween 43 and 48 mm (mean 45.7 mm or 1.8
inches) for the "commercial" 50.8-mm mesh and
between 30 and 34 mm (mean 31.7 mm of I14
inches) for the "commercial" 38.1-mm mesh.

Mesh selectivity studies have not been made
on H. robustus, but we doubt that the variabiHty
in types and sizes of trawls appreciably aflfected
the lengths of shrimp caught. We assume that
mesh selectivity would be about the same as that
shown by Berry and Hervey (1965) for Penaeus
aztecus for 2-hr tows. Most of our tows lasted
2 to 4 hr, with 3-hr tows predominating. The
50 C^ escapement length for 31.7-mm mesh would
thus be about 70 mm total length and specimens
of H. robustus less than 50 mm total length, if
present, would have been represented in the
catches. We can expect, however, that speci-
mens less than about 100 mm total length prob-
ably were not represented in their true per-
spective in the random samples.

Total length measurements (tip of rostrum
to end of telson — all length measurements are

315

FISHERY BULLETIN: VOL, 69. NO. 2

total length unless otherwise indicated) were
made in Va-cm units on a measuring board so
adjusted that when the y^^-cm units were con-
verted to millimeters the midpoints fell on 3 and
8 (e.g., a length of 25 Y^-cm units represents
lengths between 121 and 125 mm with midpoint
at 123 mm; similarly, the midpoint in milli-
meters for 26 Vi-cm units is 128 mm). Cara-
pace lengths (orbital angle to mid-dorsal end of
carapace) were measured with calipers to the
nearest millimeter. Both total length and car-
apace length measurements were made of fresh-
ly caught specimens.

The ovarian stages, determined by visual in-
spection at the time each female was measured,
were based on size and color of the ovaries.
We also noted whether spermatophores were
attached to females.

SYSTEMATICS

In the shrimp family Penaeidae the royal red
shrimp, Hymenopenaeus robustus Smith, be-
longs in the subfamily Solenocerinae, which is
distinguished from the three other subfamilies
by having a postorbital spine (Figure 3).

ORBITAL ANGLE
TOOTH OR SPI

POS

BRANCHIOSTEGAL SPINE

Figure 3. — Outline of carapace of H. rohustjts showing
position of spines.

Three genera (Haliponis Bate, Hymenopen-
aeus Smith, and Solenocera Lucas) make up the
subfamily Solenocerinae. Solenocera is distinct
from the other two genera in having the anten-
nular flagella flattened or hollowed out — chan-
nellike in structure — rather than cylindrical and
filiform. Hymenopenaeus has a single pair of
lateral telson spines and lacks podobranchs be-
hind segment VIII, whereas Hnliporus has sev-
eral pairs of lateral telson sjjines and podo-
branchs posterior to segment VIII.

Within the genus Hymenopenaeus, three spe-
cies (H. rohiistus, H. modestus Smith, and H.
lucasii Bate) are separated from all other species
by the following combination of characters:
branchiostegal spine present, pterygostomian
spine absent, and no postrostral teeth separated
from the rostral group (Figure 3).

H. robustus is distinct from H. modestus and
H. lucasii in having a tooth or spine in the or-
bital angle (Figure 3).

BIOLOGY OF THE SHRIMP
REPRODUCTIVE SYSTEMS
Internal

The internal reproductive organs of royal red
shrimp are so similar to those described by
Angelescu and Boschi (1959) for Hymenopen-
aeus muelleri and by King (1948) and Young
(1959) for the white shrimp, Penneus setiferus,
that only gross anatomy is given here.

The ovaries are paired. In the cephalothor-
acic region they are partly fused; each ovary
has an anterior pointed lobe and 6 to 8 finger-
like lateral projections which lie over the hepa-
topancreas. A lobe from each ovary extends
nearly the full length of the abdomen dorsolat-
eral to the intestine. The oviducts lead to gen-
ital pores at the bases of the third pereiopods
(Figure 4).

The testes are also paired and occupy a po-
sition in the cephalothoracic region similar to
that of the ovaries. Each testis has several
lateral lobes, and a looped vas deferens which
connects to the terminal am])oule on the coxa
of the fifth pereiopod. The testes do not extend
into the abdomen.

External

Details of the structure of the thelycum in
the female (considered to be modifications to
the sternal plates of somites XII, XIII, and XIV)
are shown in Figure 4. Note the bristly, cuplike
paired openings of the oviducts at the bases of
the third pereiopods; the rectangular plate with

316

ANDERSON and LINDNER: BIOLOGY OF ROYAL RED SHRIMP

5 mm

Figure 4. — Ventral view of thorax of adult female.

a forward projecting cone-shaped protuberance
which Hes between the fourth pereiopods; the
paired triangular protuberances about midway
between the fourth and fifth pereiopods; and
the dome-shaped area between the fifth perei-
opods.

Burkenroad (1936) described in detail the
petasma of H. robustus but did not illustrate it.
Figure 5 shows the petasma of H. robustus,
spread open to show its structure.

Spermatophore

Compared with the spermatophores of the
white shrimp (Penaeiis setiferus), the brown
shrimp (P. aztecus), and the pink shrimp (P.
duorarum) — all penaeid shrimp similar in size
to H. robustus — the spermatophore of the royal
red shrimp is exceptionally large. In fresh ma-
terial the spermatophore is bright yellow.

5 mm

Figure 5. — Petasma of male spread open to show
arrangement of rods and folds.

Figure 6 shows a spermatophore in attached
position; Figure 7 shows a detached spermato-
phore. The winglike protuberances extend be-
tween the pereiopods, and the knobby and bristly
sections of the coxae help hold the spermato-
phore in place. A gluelike substance that ac-
companies the spermatophore when attached by
the male also helps hold it secure. The spermat-
ophores of royal red shrimp are much more
securely attached than those of the white shrimp
and are not easily dislodged.

HABITS

Anderson and Bullis (1970) contributed most
of our limited knowledge of the habits of this
deep-sea shrimp. Their observations from the
submarine Aluminmd were as follows: "Bottom
photographs had previously indicated that royal-
red shrimp stayed on the sea-floor surface, but
we saw numerous shallow furrows (1 to 3 ft
long) in the bottom in which royal-red shrimp
were partly buried. They apparently do not
burrow as deeply or completely as do brown and
pink shrimp. We believe the shrimp plow into
the bottom in search of food rather than pro-
tection, and that this feeding activity produces
the grooves or furrows.

"When disturbed, the royal-red shrimp rise
gently from the furrows and swim in normal

317

FISHERY BULLETIN: VOL. 69, NO. 2

opening of

eiopod

Figure 6. — Ventral view of thorax of adult female with
spermatophore (shaded) attached.

upright position. If frightened, they flip back
in typical penaeid fashion by quick flexing of
the abdomen and then swim forward rapidly,
but usually they are turned on their sides so
that they bounce off the bottom every few feet.
At the end of the run they stand on the bottom
rather than burrow in. The shrimp walk either
forward or sideways. Color varied from grayish
pink to red — similar to colors observed on trawl-
caught specimens."

LARVAL, POSTLARVAL, AND JUVENILE
STAGES

The larvae of Hymenopenaetcs robustus are
unknown. Several attempts were made by An-
derson to hatch eggs from ripe females bear-
ing spermatophores. The eggs failed to devel-
op, however — perhaps because of the drastic
changes in temperature and pressure when the
animals were quickly brought from the cold

5 mm

FiGLiRE 7. — Ventral view of detached spermatophore.

waters of about 385 m (200 fm) to the warm
surface waters of the Gulf Stream.

In attempts to find larval and postlarval royal
red shrimp, we examined numerous plankton
samples from the M/V Theodore N. Gill cruises,
covering all seasons, in an area from about the
183-m (100 fm) contour to well beyond the axis
of the Gulf Stream and over the entire length
of the St. Augustine Grounds. Only a few larval
or postlarval penaeids were found and only one
of these, a Sole7wcera-\ike mysis stage, was con-
sidered as possibly being Hymenopenaeiis (Har-
ry L. Cook, then a fishery biologist at the BCF
Biological Laboratory. Galveston, Tex., kindly
made the identifications).

Burkenroad (1936) has provided the only rec-
ord of postlarval H. robtistus. He described nine
specimens (all dead when examined), which he
believed to be juveniles (postlarvae), that were
collected in the northern Gulf of Mexico off the
mouth of the Mississippi River. Eight (12.0-
21.5 mm total length) were taken at R/V At-
lantis station 2377 on March 24, 1935, and one
(no length given) was taken at Atlantis station
2381 on March 26. 1935.

318

ANDERSON and LINDNER: BIOLOGY OF ROYAL RED SHRIMP

LATITUDE AND DEPTH DISTRIBUTIONS

A preliminary examination of our data sug-
gested that royal red shrimp tended to be larger
in the northern part of the collection area than
in the central part, and that size was inversely
related to depth. Correlations were significant
between median lengths of females and latitude
(,• = +0.46; ( = +6.65; 7= 23.39 + 0.09X)
and between median lengths of females and depth
(,. = —0.46; t = —6.65; 7= 53.78 — O.llX).
The data used for these correlations were from
the 164 stations at which 20 or more females
were measured; the lengths are in Vo-cm units.
We did not repeat the calculations for the males
because when the smaller size groups of females
were caught in a tow, invariably the smaller
size groups of males also were caught.

For the latitude correlation we grouped the
median lengths by 10' intervals of latitude. A
gi-aph of the data showed that female shrimp
tended to be smaller between lat 29°00' and
29°39' N than between lat 29°40' and 30°13' N.
We had samples fi'om only five stations south of
lat 29°00' N, of which four were between lat
28°00' and 28°39' N. Although the data sug-
gested that large shrimp also tended to inhabit
the southern part of the grounds, we are un-
willing to draw conclusions for the area south
of lat 29°00' N from this small sample.

The size and latitude relation confirmed re-
ports of the fishermen that usually, but not al-
ways, they encountered larger shrimp on the
northern portion of the grounds than on the
central portion. The fishermen rarely fish the
southern part of the grounds, and we received
conflicting reports on the size of shrimp caught
in this area.

For the depth relation we grouped the data
by25-fm (46-m) depth intervals (151-175; 176-
200, etc.). The highly significant negative re-
lation between size and depth (large shrimp in
shallow water and smaller shrimp in deeper
water) did not agree with some of our data
(Table 2) nor with reports from the fishermen
and exploratory fishing personnel; hence we
suspected that this relation and perhaps that
with latitude were fortuitously caused by the
fishing pattern at the times our samples were

Table 2.— Median length of H. robustus and depth of
hauls for eight stations in the same latitude — Silver Bay
cruise September 25-28, 1962.

Depth of hauls

Median

length

Males

Females

ffl

/m

mm

mm

29° 54'

324-329

177-180

138

178

29° 54'

329-338

180-185

138

178

29° 54'

348

190

138

178

29°54'

357-362

195-198

138

178

29°53'

366

200

138

183

29°53'

375

205

138

178

29°53'

384

210

138

173

29-53'

411-421

225-230

138

178

taken. We therefore re-examined the data and
selected only those cruises during which more
than one depth class was fished in the same lat-
itude zone and those cruises during which the
same depth class was fished in the two latitude
zones. The depth classes used were 150 to 175
fm (274-320 m), 176 to 200 fm (322-366 m),
201 to 225 fm (368-411 m). and 226+ fm
(413+ m). The latitude zones chosen were lat
29°00' to 29°39' N and 29°40' to 30°13' N. We
had no stations south of lat 29°00'N that met
the requirements.

After the selection was made, we had 12
cruises with 93 stations and 2 depth classes
that could be compared by latitude zone for the
same depth class; and 18 cruises with 95 sta-
tions and 4 depth classes that could be compared
by depth class for the same latitude zone. Only
those stations were selected from which 20 or
more females were measured. The results are
shown in Figures 8 and 9 and in Appendix Tables
1 and 2.

In Figure 8 we have plotted the mean median
lengths (in ' o-cm units) as scatter diagrams
against depth class with latitude zone lat 29°00'
to 29°39' N as the abscissa and latitude zone lat
29°40' to 30=13' N as the ordinate. If no re-
lation existed between the length of the shrimp
and the latitude, the dots and crosses would be
scattered along and on either side of the 45°
lines. All 12 marks fall above the 45° lines,
however, showing that shrimp tended to be
larger north of lat 29°39' N than in the area
between lat 29°00' and 29°39' N.

In Figure 9 we have plotted the mean median
lengths as scatter diagrams separately for each

319

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^

.<f

-

:f\y

-'

.

<^.f

,

K

/:

■

■\X

" /

-

•

• •/

■ /

-

■

;

y

_

^

/

4'

:

. . 1 .

. . 1 .

/

. 1 .

. . . 1 . . . . 1 . ,

25

30

35 Jo

25

30 35

MEAN MEDIAN LENGTH (V2 cm)

LATITUDE 29°00' TO 29°39-N

Figure 8. — Mean median length of females by latitude
and depth (see text for explanation).

FISHERY BLXLETIN: VOL. 69, NO. 2

shrimp and the deptli from which they were
caught. Thi.s figure also indicates that the aver-
age size of shrimp is usually, but not always,
larger in that part of the St. Augustine Grounds
north of lat 29°39' N than between lat 29°00'
and 29°39' N.

We are not certain why shrimp tend to be
smaller in the central than in the northern por-
tion of the St. Augustine Grounds unless most
of the recruitment is in the central area. If
shrimp also are larger in the southern portion
of the grounds (as our meager data from that
area suggest), the obvious conclusion is that
most of the recruitment occurs in the central
portion of the grounds; otherwise, it may be that
recruitment is from the south.

SIZE AT MATURITY

FIRST DEPTH SECOND DEPTH

. 274 -320 METERS . 322 -366 METERS

050-175 FATHOMS) {I 76 - 200 FATHOMS)

. 368-411 METERS . 413 + METERS

(201 - 225 FATHOMS) (226+ FATHOMS)

o<

Z 25

MEAN MEDIAN LENGTH ( 1/2 c

FIRST DEPTH

Figure 9. — Mean median length of females by depth and
latitude (see text for explanation).

latitude zone, with the first or shallowest depth
class as the abscissa and the next succeeding
depth class as the ordinate. The marks for each
latitude zone appear to fall in a random fashion
about the 45° lines; con.sequently there was no
apparent relation between the length of the

The terminal ampoules were small and poorly
developed in most males less than about 125 mm
long but were large and prominent in specimens
greater than this length. This observation sug-
gests that sexual maturity in the males is reached
at about 125 mm total length.

Development of the ovaries, began in most
females at about 136 mm total length, but ma-
turity was not attained until they were about
155 mm long. In the random samples, all of
the 1,327 females that had attached spermato-
phores were ripe. Of this number only 55 or
about A'^'r were less than 151 mm long. The
smallest ripe shrimp with attached spermato-
phores (three individuals) were in the 136- to
140-nun size class.

Lindner and Anderson (1956) demonstrated
that female Penaens setifems underwent cer-
tain morphometric changes on attaining matur-
ity. It is evident from Figures 10 and 11 and
Appendix Table 3 that the regressions of cara-
pace length on total length for both male and
female royal red shrimp also show changes in
slope at about the lengths at which each sex
reaches maturity. Male royal red shrimp (Fig-
ure 10) demonstrate a change in slojje at the
midpoint of the 126- to 130-mm class interval,
which agrees with field observations on the size
at which the males reach maturity.

320

ANDERSON and LINDNER: BIOLOGY OF ROYAL RED SHRIMP

"1 — ; — I — I — I — I — r— I — i— 1 — I — I — I — I — I — I — I — I — I — r

-J I I i_

3 133 143 153 163 173 183

TOTAL LENGTH [fA.ff,)

Figure 10. — Regression of carapace length on total
length for males.

For female H. robustiis (Figure 11) the break
occurs at the midpoint of the 151- to 155-mm
class interval and the new slope is not reached
until the midpoint of the 161- to 165-mm class
interval. Here again this morphometric change
is associated with maturity.

These regressions were made from data gath-
ered in July 1957. Possibly the lengths at which
the slopes change would be different at other
times of the year.

SPAWNING

It was possible to separate several stages of
ovarian development in the field without micro-
scopic examination, because maturation is ac-
companied by changes in size of the ovaries
and by very distinct color changes. In the field,
however, we were unable to distinguish with
certainty the spent females. These were in-
cluded in the "undeveloped" and "developing"
categories. We usually recorded ovary develop-
ment in the following stages:

1. UN = undeveloped. In this stage the tiny
ovaries are almost threadlike and trans-
parent.

2. D = developing. The ovaries have in-
creased markedly in size and are opaque
but have not developed a distinctive color.

3. P = pink. The ovaries continue to in-
crease in size and first take on a light yel-
low color which rapidly becomes light pink.

4. R = ripe. Now swollen to full size, the
ovaries are a dark red or maroon color.
At this stage the male attaches the sper-
matophore to the female.

The length distribution of shrimp with pink
ovaries difl^ered little from the length distribu-
tion of those with ripe ovaries. Because we
have no conception of the time required for
the pink stage to develop to the ripe stage, and
because the sizes were similar, we grouped these
two ovarian stages and called them ripe. We
also grouped females with undeveloped and de-
veloping ovaries, mainly to avoid discarding the
data collected during the first two cruises in
1957, when these two stages were not difl'erenti-
ated.

We have presented this material in Figure 12
by seasonal periods. The periods chosen were
November; January and February ; April, May,
and June; and July, August, and September.

BB 99 108 118 UB I3> 148 ISB

Figure 11. — Regression of carapace length on total
length for females.

321

FISHERY BULLETIN; VOL. 69, NO. Z

Because many more shrimp were measured dur-
ing some cruises than during others in the same
season, we weighted the data in Figure 12 and
Appendix Table 4 to give each cruise equal
weight, irrespective of the number of shrimp
in the samples. Figure 12 demonstrates that
the peak of spawning is during the winter and
spring. Spawning probably is not extensive be-
fore December and is essentially completed
by June, although some spawning continues
throughout the year. Figure 12 also indicates
that few females less than 150 mm long have
ripe ovaries.

The occurrence of small specimens reported
by Burkenroad (1936) in March corresponds
with our estimate of the peak spawning season.

AGE CLASSES

In compiling total length distributions for
males and females, we have again given equal
weights to data from each cruise irrespective

10 20 30 <0 50 60 70 80 90 100 110 1J0 130 1*0 150 160 170 180 190 JOO 310

IQ ^0 30 40 50 60 70 BO 90 100 110 IJQ 130 MO 150 160 170 IBO 190 JOO JIO

■ ' ' 1 1 1 ' 1 T T .

NOV.

1 349 UN + 0

- —^ 612 P + B

1 1 1 1 1 1 1 1 1 I 1 ' 1 ' 1 ■ ! I ! i-T 1 1 ' M 1 1 M 1 '

I I ' 1 1' T ' 1 ' 1 '
'. JAN -FEB

;4S UN * D

- 1,266 P+B

_/ --• =^ ^^

' ' T 1 1 1 T-r-i 1

APBIl- JUNE

2,201 UN + 0

- 1 650 P + B

JUIT-SEPI

2 119 UN ♦ 0

_ .._ 401 P * fl

./" - A\ :

NOV
1 349 UN ♦ D

, — - 612 P + B

W\ :

5 15 25 33 45 55 65 75 85 M 105 115 125 135 145 155 145 175 185 l» 205 215
TOT*l LENGTH (MM)

Figure 12. — Seasonal length distributions of female
H. robtistns by ovarian stage.s. (UN = undeveloped;
D = developing; P ^= pink; R == ripe.)

o! 6

I ' I ' I ' I ' I ' I ' I ■ I ' M I ' I ■ I ' I ■ I I I ' I I I ' I ■ I ' I '

/A ...

./ "X. ' '

T I '"! 1' 'I ' ! ' I ' I ' 1 ' I

JAN - FEB

- 1,579 MALES

- 2,051 fEMAlES

/

A^.

TT^

2 6B6 MAlES
3.872 FEMALES

/

\ /•■'■""\

I I I I I I I I I'i'rT'rV' I ' I 1 I I I ' I 1 I I I I r

JUIT - SEPI A

I I I ' I ' I ' I ' I ' I ' I ' I ' I ' I I I ' I ' I ' I

■rn--

1,304 MALES
I.9SS FEMALES

.,.J-

y?.

f-r

TOTAL LENGTH (MM)

Figure 13. — Length distributions of H. robustus by sex
and season.

of the number of shrimp measured, and we pre-
sent the data for the same seasonal periods used
to show the spawning season (Figure 13 and
Appendix Table 5). The relative heights of the
modes can be misleading because the data are
scattered sparsely through 11 years and the
appearance of a dominant year class in one
sample (as occurred in November 1964) can
have a disproportionate effect when applied to
the material as a whole.

The graphs for the females are more readily
interpreted than those for the males. In No-

322

ANDERSON and LINDNER: BIOLOGY OF ROYAL RED SHRIMP

vember the females show a mode at about 80 mm
total length that can be followed readily through-
out the year to a second mode at about 120 mm.
The mode at 120 mm can also be traced through-
out the year to the bimodal group with modes
at 143 and 153 mm. The bimodality of this
latter group we believe to be fortuitous, but it
can be followed to a hump between 153 and 158
mm in the January-February distributions.
Thereafter the modes become lost in the large
group of mature females. We believe that the
two additional modes in our November distri-
butions (173 and 183 mm) also are fortuitous
and result from the sampling procedures.

A group of small male shrimp also appears
in November, forming a mode at about the same
length as that for the females, which can be
traced throughout the year to the second mode
at about 115 mm. This second mode can be
traced as a hump to the left of the main mode
from January through September to the third
mode at 128 mm, beyond which it is lost.

We made various attempts to fit Von Bert-
alanfy growth curves to the data without sat-
isfactory results other than it was apparent the
first two modes could be attributed to 1- and 2-
year-old shrimp. Evidently morphometric
changes associated with maturity preclude the
use of total length as a means of determining
age of H. robustus after they reach maturity.

We believe the first three groups of males and
females we have cited are 3 distinct age classes.
If the peak of spawning is in Maixh, both sexes
would be about 100 mm total length at 1 year of
age. From our data it is impossible to disting-
uish more than the first 3 age classes. The older
age classes, which probably represent 2 or more
additional years, would give a minimum life span
of 5 years. Probably, however, at least some
of the largest shrimp are older than this.

SIZE AND AGE AT RECRUITMENT

When we consider all of our length measure-
ments as a unit, either unweighted, weighted
to give each cruise equal weight, or weighted
to give each year equal weight, we obtain almost
identical distributions. In Figure 14 we show

'° ■ y ■ y ■ *° ■ ^° .^^ ^° ^ ^'^ '°° "° '^ '^° '*° '^° '^° '^° '»° '^° MO 210

I I 1 I I I I I I I

ANNUAl
— 7,734 MAltS
--10,441 FEMALES

/

A

/.-.'— -V

■V

rr^

TOTAL LENGTH if/,f/t)

Figure 14. — Length distributions of H. robustus by sex
for all samples combined.

these length distributions weighted to give equal
weight to collections during each cruise. It is
readily evident from these curves that only the
groups presumed to represent the second, third,
and fourth and older age groups are present
in substantial numbers and that the population
is composed largely of mature shrimp.

Although the data are not adequate, they sug-
gest that recruitment starts at about 1 year of
age, but the shrimp are not fully recruited until
about 2 years of age, and recruitment may not
be complete until the shrimp are mature — about
3 years old. In the combined length distribu-
tions (Figure 14), 55% of the females were
longer than 160 mm and 61% of the males were
longer than 125 mm (the lengths at which we
believe each sex is fully mature). Only 6% of
the males and 4'/r of the females were less than
100 mm long. The smallest shrimp we sampled
was in the 56- to 60-mm length class. As we
mentioned earlier, we do not believe that gear
selectivity causes the scarcity of shrimp under
100 mm long and the lack of them under 56 mm
long. Royal red shrimp do not appear on the
fishing grounds at sizes smaller than about 55
mm. The observations of Anderson and Bullis
(1970) who had clear visibility of the bot-
tom from a distance of less than 1 m, substanti-
ated the lack of small shrimp on the St. Augus-
tine Grounds. Furthermore, 37 H. modestm,
43 to 93 mm long (mode, 63 mm) were taken
on April 20, 1957, in 225 fm with a 40-ft flat
shrimp trawl fitted with commercial 2-inch
stretched mesh in the body and 11/2-inch mesh
in the cod end. In addition, H. R. Bullis, BCF
Pascagoula, Miss, (personal communication),
concerning trawling on the H. robustus grounds

323

FISHERY BULLETIN: VOL. 69. NO. 2

off the Mississippi River Delta, stated, "Of spe-
cial interest was the discovery of high densities
of small red (Hymenopenaeus debilis) shrimp
in 208 fathoms. These shrimp averaged less
than 35 mm total length." These two species
of Hymenopenaeus are similar in shape to H.
robustus; consequently, we believe that small
H. robustus would have been taken in our gear
if they had been present on the fishing grounds.
We have no idea where they might be.

The sex ratios for all the data combined show
A2.&'''r males and hlA'^'c females. Some, but
probably not all, of this difference is undoubtedly
the result of mesh selectivity. We observed no
indication of sex reversal in the species.

Appendix Table 6 shows the length distribu-
tions in numbers of shrimp by sex for each
cruise.

LITERATURE CITED

Anderson, W. W., and H. R. Bullis, Jr.

1970. Searching the shrimp beds by sub. Sea
Frontiers 12: 112-119.
Angelescu, v., and E. E. Boschi.

1959. Estudio biologico pesquero del langostino de

Mar del Plata en conexion con la Operacion Nivel

Medio. [With English summary.] Argent. Seer.

Mar. Serv. Hidrogr. Nav., Publico H. 1017, 135 p.

Berry, R. J., and J. B. Hervey.

1965. Mesh selectivity studies. In Biological Lab-
oratory, Galveston, Tex. fishery research for the
year ending June 30, 1964, p. 41-44. U.S. Fish
Wildl. Serv., Circ. 230.
Bullis, H. R., Jr.

1956. Preliminary results of deep-water explora-
tion for shrimp in the Gulf of Mexico by the
M/V Oregon (1950-1956). Commer. Fish. Rev.
18(12) : 1-12.
Bullis, H. R., Jr., and R. Cummins, Jr.

1963. Another look at the royal red shrimp re-
source. Proc. Gulf Carib. Fish Inst., 15 Annu.
Sess., p. 9-13.

Bullis, H. R., Jr., and W. F.' Rathjen.

1959. Shrimp explorations off southeastern coast
of the United States (1956-1958). Commer. Fish.
Rev. 21(6) : 1-20.
Bullis, H. R., Jr., and J. R. Thompson.

1959. Shrimp exploration by the M/V Oregon
along the northeast coast of South America.
Commer. Fish. Rev. 21(11) : 1-9.
Burkenroad, M. D.

1936. The Aristaeinae, Solenocerinae, and pelagic
Penaeinae of the Bingham Oceanographic Col-
lection. Bull. Bingham Oceanogr. Collect. Yale
Univ. 5, Art. 2, 151 p.
Cummins, R., Jr., and J. B. Ri\'ers.

1962. New deep water shrimp fishery developed
off Florida's east coast. Fish Boat 7(12) : 19-23,
33-34.
King, J. E.

1948. A study of the reproductive organs of the
common marine shrimp, Penaeus setiferus (Lin-
naeus). Biol. Bull. (Woods Hole) 94: 244-262.
Klima, E. F.

1969. Length-weight relation and conversion of

"whole" and "headless" weights of royal-red

shrimp, Hymenopenaeus robustus (Smith). U.S.

Fish Wildl. Serv., Spec. Sci. Rep. Fish. 585, 5 p.

Lindner, M. J., and W. W. Anderson.

1956. Growth, migrations, spawning, and size dis-
tribution of shrimp, Penaeus setiferus. U.S.
Fish Wildl. Serv., Fish. Bull. 56: 555-645.
Roe, R. B.

1969. Distribution of royal-red shrimp, Hymeno-
penaeus robusttis, on three potential commercial
grounds off the southeastern United States. U.S.
Fish Wildl. Serv., Fish. Ind. Res. 5: 161-174.
Springer, S., and H. R. Bullis.

1952. Exploratory shrimp fishing in the Gulf of
Mexico, 1950-51. U.S. Fish Wildl. Serv., Fish
Leafl. 406, 34 p.
1954. Exploratory shrimp fishing in the Gulf of
Mexico, summary report for 1952-54. Commer.
Fish. Rev. 16(10) : 1-16.
Young, J. H.

1959. Morphology of the white shrimp, Penaeus
setiferus (Linnaeus 1758). U.S. Fish Wildl.
Serv., Fish. Bull. 59: 1-168.

324

ANDERSON and LINDNER: BIOLOGY OF ROYAL RED SHRIMP

APPENDIX TABLES

Appendix Table 1. — Mean median lengths of female H. robustus by depth, latitude, and cruise.

322 to 366 m (176-200 ftr)

Lot 29°00' to 29°39' N

Lot 29°40' to 30°I3' N

Cruise
dotes

Aug.
13-20
1957

Nov.
20-25
1957

Juna

n-22

1958

Jon.
18-28
1960

Apr. 28-

May 1

1961

Jon. 16-

Feb 22

1962

Aug.
13-20
1957

Nov.
20-25
1957

Juna
11-22
1958

Jon.
18-28
1960

Apr. 28-

May I

1961

Jan. 16-

Feb. 22

1962

Number of
stations

8

5

3

1

2

2

1

4

22

1

2

1

Mean

median

lengtti (V2 cm)

32.8

30.9

32.7

24.5

29.0

33.8

35.0

33.4

33.6

35.0

36.0

35.0

368 to 411 m (201-225 fm)

Lot 29°00' to 29°39' N

Lot 29°40' to 30° 13' N

Cruise
dotes

Number of
stations

Apr.
26-28
1957

July Aug. Aug. Feb.

17-30 13-20 22-28 5-7

1957 1957 1962 1964

Nov.

Apr.

July

Aug.

Aug.

Feb.

Nov.

11-13

26-28

17-30

13-20

22-28

5-7

11-18

1964

1957

1957

1957

1962

1964

1964

Meon
median
length V/2 cm) 25.8

38.0

35.3

325

FISHERY BULLETIN: VOL. 69. NO. 2

Appendix Table 2. — Mean median lengths of female H. robustus by latitude, depth, and cruise.

Lot 29°40' to 30°13' N

Item

First depth
274-320 m (150-175 fm)

Second depth
322-366 m (176-200 fm)

Cruise dates

May
29-31
1957

Jan. Apr. 28-
18-28 May I
1960 1961

Jan. 16-

Feb. 22

1962

Moy
29-31
1957

Jan.
18-28
1960

Apr. 28-

Moy 1

1961

Jon. 16-

Feb. 22

1962

Number of
stations

I

1 6-

6

1

1

2

1

Meon median
length (V2 cm)

37.0

34.0 34.9

35.6

37.0

35.0

36.0

35.0

First depth
322-366 m (176-200 fm)

Second depth
368-411 m (201-225 fm)

Cruise dates

July
17-30
1957

Aug.
13-20
1957

Aug. Sept.
22-28 25-28
1962 1962

Feb.
5-7
1964

Nov.
11-18
1964

July
17-30
1957

Aug.
13-20
1957

Aug.
22-28
1962

Sept.
25-28
1962

Feb.
5-7
1964

Nov.
11-18
1964

Number of
stations

5

1

3 5

I

1

I

2

2

2

1

5

Mean median
length (I/2 cm)

33.8

35.0

35.7 36.2

36.0

23.0

38.0

35.3

360

355

37.0

27.0

First depth
368-411 m (201-225 fm)

413

Second depth
plus m (226 plus

fm

Cruise dates

Sept.
25-28
1962

Sept.
25-28
1962

Number of
stations

2

I

Mean median
length Vh cm)

35.5

36.0

Item

Lot 29" OO' tc

29°39' N

First depth
322-366 m (176-200 fm)

Second depth
368-411 m (201-225 fm)

Cruise dates

April
26-28
1957

Aug Nov. Jon.
13-20 20-25 18-28
1957 1957 1960

Apr. 30-

Moy 3

1960

April
26-28
1957

Aug.
13-20
1957

Nov.
20-25
1957

Jan.
18-28
1960

Apr. 30-

May 3

1960

Number of
stations

2

8

5 1

6

2

4

2

1

4

Meon median
length (V2 cm)

30.0

32.8 30.9 24.5

31.3

25.8

31.9

29.0

33.0

30.6

First depth
368-411 m (201-225 fm)

413

Second depth
plus m (226 plus

fm)

Cruise dotes

July
17-30
1957

Jul/
20-22
1967

July
17-30
1957

July
20-22
1967

Number of
stotions

2

4

I

2

Mean median
length ('/2 cm)

30.0

25.3

29.0

27.8

326

ANDERSON and LINDNER: BIOLOGY OF ROYAL RKD SHRIMP

Appendix Table 3. — Regression of carapace length on
total length for H. robustus.

Total length

Males

Females

Mean

carapace length

Males

Females

mm

Number

Nvmbtr

mm

mm

83

._

1

._

20.0

88

6

1

20.2

20.0

93

8

4

21.3

21.5

98

12

5

22,8

22.3

103

22

10

24.0

24.2

103

23

12

24.9

25.1

113

45

18

25.9

262

118

63

23

275

27.6

123

94

20

28.8

23.9

128

86

17

30.1

30.3

133

104

34

31.7

31 4

138

115

46

33.1

32.8

143

94

53

34.5

34.1

148

34

60

35 6

35.4

153

14

36

368

37.0

158

3

36

37.7

39.3

163

__

56

41.7

168

1

86

41.0

43.1

173

__

102

_,

44.6

178

1

82

45.0

46.3

183

._

77

48.1

188

__

81

49.4

193

__

49

51 J

198

16

S2.9

203

-

6

~

55.5

Total

725

931

327

FISHERY BULLETIN: VOL. 69. NO. 2

Appendix Table 4. — Length distributions of ovarian stages by season and cruise.
[UN = undeveloped; D ^ developing; P = pink; R ^ ripe]

Fall

Winter

Total length

Nov

20-25, 1957

Nov. 11

18, 1964

Jan. 18-28

1960

Jon. 16-Feb.

22, 1962

Feb. 5-7,

1964

UN +

D P + R

UN + D

P + R

UN + D

P + R

UN + D 1

P + R

UN + D

P + R

mm
S3
58

%

%

%
0.2

%

%

%

%

%

%

%

63
68
73

—

—

0.2
0.7
0.9

—

0.1

—

0.3

—

78

0.1

__

I.l

0.3

__

0.1

__

0.3

..

83

0.S

1.2

24

0.1

0.7

88

0.5

__

1.1

3.4

__

0.3

0.7

__

93

__

1.0

6.7

0.3

16

98

0.7

__

1.2

5,3

__

02

3.3

__

103

2.3

_.

2.7

8.0

__

0.6

._

5.8

__

108

5.2

__

6.1

2.4

0.3

07

1.3

__

H3

5.6

__

9.0

1,5

__

0.3

__

20

__

lis

5.2

__

12.7

__

1.2

._

1,3

0.1

26

__

123

3.2

__

13.7

0.2

1.8

1.8

0.1

3.6

__

128

2.7

0.1

12.2

0.1

3.2

..

10

01

6.1

_.

133

2.4

0.6

7.3

0.1

2-4

__

1 0

0.1

4.3

_.

138

1.5

1.6

4.0

0.1

23

0.9

0.5

0.1

2.6

0.7

143

2.1

2.8

2.7

0.4

03

06

0.3

0.1

23

1.0

148

1.0

2.7

2.7

0.9

0.9

1 8

07

03

1.0

03

153

0.8

3.2

2.5

1.4

1.5

3.0

0.5

0,9

1.0

1.6

158

1.5

3.1

1.4

1.0

2.4

3.3

1.4

1.4

1 0

2.3

163

0.4

4.5

1.2

1.1

1.5

4.2

1.9

42

0.3

2.0

163

7.4

0.7

0.7

0.6

7.5

27

85

07

3.0

173

..

8.5

0.6

1.2

1.2

3.9

4,4

12,4

07

3.6

178

0.4

6.5

0.3

0.8

1.5

5.8

3.7

129

16

4.6

183

0.5

9.6

0.5

0.5

0,9

4.1

1.8

12,9

1.6

8.5

188

0.1

7.7

0.4

0.3

2.1

3.6

1.4

8.4

3.0

6.9

193

0.3

2.6

0.2

1.6

1.2

2.7

1.0

5.2

3,0

32

198

__

1.6

0.2

0.6

0.6

0.3

04

2 1

1,0

3.0

203

__

0.5

__

0.2

0.6

0.9

O.I

1.0

__

1.6

208

0.3

0.3

0.1

05

0.3

213

—

—

—

O.I

—

—

—

—

—

—

218

—

—

—

—

—

—

—

—

--

—

Total

37.0

63.0

88.7

11.3

56.8

43.2

23.7

71.3

52.4

47.6

Number of

females

278

476

1.071

136

193

146

392

975

160

145

328

ANDERSON and LINDNER: BIOLOGY OF ROYAL RED SHRIMP

Appendix Table 4.-
[UN

-Length distributions of ovarian stages by season and cruise — Contimied.
= undeveloped; D = developing; P =^ pink; R = ripe]

Spring

Total length

Apr. 26-28

1957

May 29-31, 1957

June

11-22, 1958

Apr. 30-May

3, 1960

Apr. 28-Moy

1, 1961

UN -(- D

P + R

UN + D

P+ R

UN +

D P + R

UN -f D 1

?+ R

UN + D

P + R

mm

%

%

%

%

%

%

%

%

%

%

53

—

—

—

58

__

0.3

__

__

__

..

63
68
73

0.2

--

--

--

--

--

-

-

-

—

0.2

II

II

II

~s_

0.2

II

78

0.3

0.5

__

0.2

__

83

1.6

0.3

—

0.2

0.3

_.

88

1.3

__

__

0.5

..

93

1.8

0.1

0.9

__

2.5

98

3.8

__

0.3

0.2

_.

0.4

__

2.4

103

4.2

0.3

0.4

2.0

__

32

108

2.6

0.5

0.2

4.2

__

2.5

__

113

3.0

1.1

0.9

5.3

__

2.5

0.2

118

2.4

_.

0.8

1.3

__

5.5

0.2

1.5

123

3.2

02

1.1

2.2

4.6

..

0.5

128

59

0,2

1.6

__

2.9

..

2.4

..

0.8

133

78

0,3

3.2

__

4.6

4.0

._

0.5

138

6.4

0.5

2.9

._

5.7

0.1

5,7

0.7

2-0

0-2

143

4,2

1.2

3,2

0.8

4.6

0-9

3.1

1.3

1.7

0.4

148

2,2

0-8

1,1

1,6

3 4

1-6

2.9

1.6

1.2

1.2

153

0,6

0,5

1.1

1.1

4.0

2-5

24

2.0

1.5

2.7

158

1.1

08

0,3

0-5

3.8

2-8

3.1

20

1-5

2.6

163

22

1.2

1.3

3,5

3,1

3-8

3,3

40

I.O

3.5

168

2.2

1,6

1.1

7.2

32

3-0

35

4,0

1.5

7.2

173

2.2

30

1.3

7.5

3 3

3-9

35

5,0

2.4

10.4

178

1.9

2.5

1,3

8.8

3-6

4-4

4,4

4.7

1.0

12.5

183

3.4

2.4

1.6

12.7

3-7

5-5

2.2

2.4

1.0

8.5

188

3,7

4,0

1.9

11-3

4.1

4-1

2.2

1.6

1.2

6.7

193

4,2

2,3

1.3

6.7

2.8

3,4

1,5

0,9

0.7

5.1

198

2.6

1,0

__

6.2

1-7

26

02

1.1

..

22

203

08

0,5

0.5

2.4

0-4

0.7

0,4

0.2

0.2

1.2

208

0,6

0,2

0.8

0.2

0.1

0.2

0.2

..

0.5

213

0,2

__

O.I

_.

__

0.2

218

--

--

-

-

--

0.1

--

--

—

—

Total

76.8

23.2

28.9

71.1

60.4

396

68,1

31.9

3^5

65-5

Number of

females

480

144

108

265

1,098

713

310

144

205

384

329

FISHERY BULLETIN: VOL. 69, NO. 2

Appendix Table 4. — Length distributions of ovarian stages by season and cruise-
[UN = undeveloped; D = developing; P = pink; R = ripe]

-Continued.

Summer

Total length

July 17-30

1957

Aug. 13-20

1957

Aug. 22-28, 1962

Sept. 25-28

1962

July 20-22,

1967

UN + D 1

P + R

UN + D

P + R

UN + D

P + R

UN -t- D 1

P + R

UN + D 1

P -f R

mm
53
SB

%

%

%

%

%

%

%

%

%

%

63
68
73

—

--

—

—

-

0.3

-

78

__

0.3

__

0.3

__

__

83

0,2

_.

0.2

0.2

0.3

88

0.2

0.5

__

__

--

-_

__

93

0.9

__

0.9

0.8

__

__

0.7

98

1.3

__

1.9

0.6

__

0.8

1.3

103

2.2

..

3.3

_.

0.6

__

0.8

7.4

__

108

26

__

3.9

0.1

3.3

__

1.6

10.1

113

4.0

..

3.8

__

4.8

0.8

13.4

..

118

4.9

..

3.3

3.5

__

0.8

13.7

123

2.9

._

2.8

__

3.3

1.3

8.1

__

128

1.5

..

1.3

3.5

1.1

3.7

133

4.4

..

3.2

__

2.9

0.5

3.7

138

54

0.2

4 4

02

1.7

1.6

5.4

0.3

143

4.8

0.4

40

0.2

1.3

0.8

1.0

0.3

148

3.9

0.4

43

0.8

1.7

__

0.8

2.4

__

153

2.9

08

2.3

04

1.0

0.2

2.1

3.4

0.7

158

1.1

02

3.2

0.5

1.7

0.2

1,3

2.4

1.3

163

3.1

0.4

6.2

0.8

65

0.4

3,6

1.1

1.3

0.3

168

3.1

2.0

6.0

1.8

9.1

1.0

6,4

1.3

2.7

2,0

173

4.2

4.6

72

2,1

10.7

1.5

9.9

1.9

2.7

1.3

178

3.5

38

6.5

1.2

14.7

1.9

183

1.9

1.0

3.4

183

3.3

5.1

5.5

23

10.7

1.0

14.8

2.4

1.0

1.7

188

3.3

7.5

43

2.4

6.3

9.9

0.8

0.7

1.3

193

26

5.0

2,8

1.1

2.5

0.4

6.4

1.3

0.7

198

0.9

1.3

1.1

0.9

0.8

2.9

0.8

__

0.3

203

0.2

0.9

1.1

05

1.0

__

1.1

__

208

__

0.3

0.1

02

__

213

—

—

--

--

—

—

0.3

—

--

—

218

—

—

--

--

—

—

--

—

—

—

Total

67.4

32.6

84.6

15.4

93.4

6.6

88.5

11.5

87.1

12.9

Number of

females

305

149

738

136

487

34

330

43

259

39

330

ANDERSON and LINDNER: BIOLOGV OF ROYAL RED SHRIMP

Appendix Table 5. — Length distributions by sex for season and cruise.

Fall

Winter

Total length

Nov.

20-25, 1957

Nov.

11-18, 1964

Jan.

18-28, I960

Jon. 16-Feb

22, 1962

Feb. 5-7, 1964

Moles

Females

Moles

Femoles

Moles

Femoles

Moles

Females

Moles

Females

mm

53

58

%

%

%

%

%

%

%

%

%

%

0.2

II

II

II

63

.0.2

—

—

—

__

68

0.2

0.1

0.7

73

__

__

0.9

0.1

__

0.3

78

o.s

__

0.2

1.1

0.7

0.3

._

0.1

__

0.3

83

0.9

0.5

0.4

1.1

1.7

2.3

0.1

0.7

0.7

88

0.2

0.5

0.4

1.1

3.7

3.4

0.1

0.1

2.1

0.7

93

0.9

__

0.2

1.0

3.7

6.7

O.I

0.3

5.2

1.6

98

3.9

0.7

1.7

1.1

3.4

5.1

0.6

0.3

6.2

3.2

103

7.7

2.3

4.9

2.6

2.0

7.6

0.8

0.2

5.9

5.8

108

10.0

5.2

9.3

6.0

2.0

2.5

1.6

0.6

4.5

1.3

113

10.3

5.6

14.6

8.8

. 1.7

1.4

1.8

0.7

4.5

1.9

118

8-2

5.2

16,5

12.8

3.4

1.1

3.2

0.3

6.6

2.6

123

9.1

32

12.1

13.4

7.6

2.0

3.6

1.8

3.1

3.6

128

14.Q

2.8

11.3

12,4

20.4

3,1

9.0

1.8

7.9

6.1

133

12.0

2.9

8,6

7,3

18,6

2.5

20.4

1.3

9.3

4.2

138

9.8

3.1

6.2

4.1

15.4

3.9

26.4

0.9

10.0

3.2

143

6.4

4.9

42

3.0

9.6

0.8

21.3

0.4

17.6

3.6

148

5.2

3.7

4.2

3.4

2.7

2.5

7.4

0.8

11.0

1.3

153

0.5

4.1

2.6

4.1

2,0

5.1

1.8

1.6

4.1

2.9

158

._

4.5

0.9

2.4

0,5

5,3

0,8

2.8

0.7

3.2

163

..

4.9

1.0

2.4

__

5,6

06

6.6

2.3

168

_.

7.4

0.4

1.4

0,5

8.7

0.1

10.0

__

3.6

173

0.2

8.6

__

2.0

0,2

56

O.I

17.0

4.2

178

_.

6.9

0.1

1.4

0.2

7.6

0.1

16.3

0.3

6.5

183

__

10.1

0.1

1.2

._

4.8

0.1

15.4

0.3

10.0

188

8.0

0.8

5.3

0.1

9.7

9.7

193

__

2.8

1.8

3.7

6.3

__

11.4

198

1.6

0.9

1.1

2.7

3.9

203

__

0.5

0.2

1.4

1.2

__

1.6

208

0.1

0.6

0.6

0.3

213

—

—

—

0.1

—

—

—

—

—

—

213

—

—

—

—

—

—

—

—

—

—

Total

100.0

100.0

100 0

100.0

100.0

100,0

100,0

100.0

100.0

100.0

Number of

shrimp

441

755

863

1,233

408

356

881

1,386

290

309

331

FISHERY BULLETIN: VOL. 69, NO. 2

Appendix Table 5. — Length distributions by sex for season and cruise. — Continued.

Spring

Total length

Apr. 26-28, 1957

May 29-31

1957

June

11-22, 1958

Apr. 30-May 3, 1960

Apr. 28-May

1, 1961

Males

Females

Moles

Females

Moles

Femoles

Moles

Females

Moles 1

Femoles

mm

%

%

%

%

%

%

%

%

%

%

53

__

—

—

—

—

—

—

—

--

—

S6

0.3

--

—

—

—

—

—

63

0.2

0.5

—

—

0.1

—

—

—

—

68

0.2

--

—

—

—

—

—

—

73

0.4

0.2

__

—

—

—

0.2

78

0.8

0.3

__

0.5

__

—

—

0.2

83

1.0

1.6

__

0.3

__

--

0.2

0.6

0.3

88

1.8

1.3

0.5

0.3

__

--

08

0.5

93

5.7

1.8

2.1

__

0.3

O.I

0.3

0.9

2.0

2.5

98

5.1

3.8

0.5

0.3

0.4

0.2

OS

0.4

3.9

2,3

103

5.5

4.2

2.7

0.3

0.7

0,4

2.4

1.9

5.1

3.2

108

5.1

2.6

7.0

0.5

2.5

0.2

4.2

4.1

3.1

2,5

)13

6.5

3.0

4.3

1.1

4.2

0.9

40

5.4

1.4

2.7

118

8.5

2.4

3,0

0.8

7.6

1.3

77

5.6

1.8

1.5

123

12.2

3.4

17.2

I.l

19.1

22

16.0

4,5

3.3

0.5

128

7.3

6.1

13.4

1.6

17.6

2,9

19.2

2,6

16.4

0.8

133

8.3

8.2

10.8

3.2

18.3

47

18.1

3.9

21,9

0.5

138

9.3

6.9

13.9

3.0

11.2

5,9

13.5

6.3

19,4

2.2

1«

10.2

5.5

6.4

4.0

9.1

5,4

7.9

4.3

11,9

20

148

8.5

3.0

7.5

2.7

5.5

5,0

1.6

4,3

4,3

2.5

153

2.4

1.1

2.7

2.1

1.7

6,5

1.6

45

2,5

4.3

158

0.8

1.9

__

0.8

0.2

6.6

0.8

5.0

0.8

4.0

163

0.2

3.4

4.8

0.4

6.9

1.1

7.6

—

5.0

168

3.8

__

8.3

__

6.1

0.3

7.7

—

9.0

173

0.2

5.3

0.5

8.8

0.3

7,2

0.5

8.9

0.2

12.7

178

4.5

0.5

10.2

0.4

8.1

8.9

0.2

13,0

183

5.8

0.5

14.2

0,1

9.1

0.3

4.5

0.2

9.7

188

7.6

13.1

0.1

8.2

__

3-7

.-

8,0

193

6.3

__

8.0

6.2

—

2.4

0.2

5-7

198

3.5

0.5

6.2

4,3

__

1.3

—

2,2

203

1.3

0.5

3.0

1.2

--

0.7

—

1.3

208

0.8

._

0.8

0.2

0.4

—

0.5

213

._

0.2

--

—

0.1

—

—

--

0.2

218

—

--

—

—

—

--

—

—

—

Total

100.0

100-0

100.0

100-0

100.0

100.0

100.0

100.0

100.0

100.0

Number of
shrimp

495

624

187

373

1,136

1.811

379

463

489

601

332

ANDERSON and LINDNER: BIOLOGY OF ROVAL RED SHRIMP

Appendix Table 5. — Length distributions by sex for season and cruise. — Continued.

Summer

Total length

July

17-30, 1957

Aug.

13-20, 1957

Aug

22-28, 1962

Sept.

25-28, 1962

July 20-22

1967

Males

Femoles

Males

Females

Males

1 Females

1

Males

Females

Males

Females

mm

%

%

%

%

%

%

%

%

%

%

53

—

—

—

—

—

—

—

—

—

—

58

—

—

—

—

—

—

—

63
68
73

--

-

--

--

-

0.2

-

-

-

—

;:

'_\

0.3

::

0.3

78

0.4

0.3

__

0.3

83

__

0.2

0.4

0.2

__

0.2

__

0.3

0.4

88

1.7

0.2

1.1

0.5

05

0.3

._

93

2.3

0.9

1.3

0.9

1.5

0.8

0.5

0,8

0.7

98

3.4

1.3

2.3

1.9

3.3

0.6

0-8

06

3.2

1.3

103

5.7

2-2

4.5

3.3

6.9

0-6

1.9

0.8

11.2

7.4

108

5.1

2.6

5.9

4.0

8.1

3.2

0.8

1.6

9.2

10.0

113

8,3

40

4.1

3.6

7.9

4.6

3.0

0.8

13.8

13.4

118

7.1

4.8

7.4

3.3

3.8

3.4

2.7

0.8

10.0

13.6

123

94

2.9

14.9

2,8

8.1

3.2

3.2

1.3

12.3

8.0

123

11.4

1.5

13.0

1.3

12.0

2.9

5.4

1.3

1 0.0

3.7

133

12.6

4.4

15.4

3.2

19.8

2.9

16.4

0.5

11.5

3.7

138

13.3

5-5

15.4

4.6

18.6

1.7

26.3

1.9

6.8

5.7

143

13.4

50

8.9

4.2

43

1.3

25.5

0.8

7.2

1.3

148

2.6

4.4

4.4

5.2

4.1

1.7

8.8

0.8

0.8

2.7

153

1.7

3.7

0.6

2.8

0.5

1.1

1.3

2.1

1.6

4.0

153

0.9

1-5

3.8

_„

1.9

0.5

1.3

0.8

3.7

163

3.5

7.0

0,3

6.8

__

4.5

0.4

1.7

163

0.3

50

._

7.8

__

10.1

0.3

7.7

4.7

173

__

8.8

9.1

12.0

0.3

11.7

4.0

178

0.3

7.2

7.6

17.6

19.9

._

4.4

183

8.4

7.8

11.8

__

17.1

2.7

188

10.8

6.7

6.3

10.9

_.

2.0

193

7.9

__

4.0

__

2.7

__

7.7

0.7

193

2.2

1.9

1.0

3.7

__

0.3

203

__

1.1

__

1.5

__

1.0

..

1.1

208

0.5

0.2

__

__

213

—

—

—

—

—

—

—

0.3

--

218

—

—

—

—

—

—

—

—

—

—

Total

100.0

100.0

100.0

100.0

100.0

100-0

100.0

100.0

100.0

100.0

Number of

shrimp

350

456

798

874

393

525

373

376

251

299

333

FISHERY BULLETIN: VOL. 69, NO. 2

Appendix Table 6. — Length distributions by cruise and sex.

Total length

Apr. 26-28

1957

May 29-31

1957

July 17-30, 1957

Aug. 13-20, 1957

Nov.

20-25, 1957

Males

Females

Males

Females

Males

Females

Males

Females

Males

Females

mm
53
58

Number

Number

Number

Number

Number

Number

Number

Number

Number

Number

_^

_^

1

—

—

—

—

—

—

<3

—

I

1

—

—

—

—

—

—

—

68

I

—

—

—

—

--

—

—

1

--♦

73

2

1

—

—

-_

—

—

78

4

2

2

--

--

3

3

2

__

83

5

10

_,

1

1

3

2

4

4

88

9

8

1

6

1

9

4

1

4

93

28

n

4

__

8

4

10

8

4

._

98

25

24

1

1

12

6

18

17

17

5

103

27

26

5

1

20

10

36

29

34

17

108

25

16

13

2

18

12

47

35

44

39

113

32

19

8

4

29

18

33

33

46

42

118

42

15

15

3

25

22

59

29

36

39

123

61

21

32

4

33

13

119

24

40

24

128

36

38

25

6

40

7

104

11

62

21

133

41

51

20

12

44

20

123

28

53

22

138

45

43

26

11

48

25

123

40

43

23

143

51

34

12

15

47

23

71

37

28

37

148

42

19

14

10

9

20

35

45

23

28

153

12

7

5

8

6

17

5

24

2

31

158

4

12

3

3

7

33

34

153

1

21

_.

18

__

16

61

__

37

168

24

__

31

I

23

68

56

173

1

33

1

33

40

__

80

1

65

178

__

28

1

38

1

33

67

52

183

„

36

1

53

_-

38

-_

68

77

188

._

48

__

49

49

_-

59

61

193

40

__

30

36

35

21

198

__

22

1

23

10

__

17

__

12

203

__

8

1

11

—

5

—

13

—

4

208

5

—

3

—

—

—

4

—

—

213

—

I

—

—

—

—

—

—

—

—

218

—

—

—

—

—

—

—

—

—

—

Total

495

624

187

373

350

456

798

874

441

755

Number of
stations

7

3

9

8

14

334

ANDERSON and LINDNER: BIOLOGY OF ROYAL RED SHRIMP

Appendix Table 6. — Length distributions by cruise and sex. — Continued.

Total length

Aug. 22-28

1962

Sept. 25-28, 1962

Feb. 5-7,

1964

Nov. 11-

18, 1964

July 20-22, 1967

Males

Females

Males

Females

Males 1

Females

Moles

Females

Moles

Females

mm

Number

Number

Number

Number

Number

Number

Number

Number

Number

Number

53

—

—

—

—

—

—

—

—

—

-^

58

—

—

—

—

—

—

2

—

—

63

—

1

—

-

—

—

—

2

—

—

68

_-

—

—

-

—

—

I

8

73

1

1

_..

11

__

1

78

._

-_

1

_.

1

2

13

._

__

83

1

1

2

2

3

14

1

..

88

2

1

__

6

2

3

13

93

6

4

2

15

5

2

12

2

2

98

13

3

3

3

18

10

15

14

8

4

103

27

3

7

3

17

18

42

32

28

22

108

32

17

3

6

13

4

80

74

23

30

113

31

25

11

3

13

6

127

no

35

40

118

15

18

10

3

19

8

143

159

25

41

123

32

17

12

5

9

11

105

167

31

24

128

47

15

20

5

23

19

97

154

25

11

133

78

15

61

2

27

13

74

90

29

11

138

73

9

too

7

29

10

53

50

17

17

143

17

7

95

3

51

11

36

37

18

4

148

16

9

33

3

32

4

36

42

2

8

153

2

6

5

8

12

9

22

50

4

12

158

10

2

5

2

10

8

29

2

11

163

1

36

17

7

9

29

1

5

168

53

1

29

n

3

17

__

14

173

_.

63

1

44

_.

13

__

25

_.

12

178

93

75

1

20

1

17

__

13

183

..

62

64

1

31

1

15

__

8

188

33

41

30

10

__

6

193

__

14

__

29

35

22

._

2

198

5

14

12

_,

II

_.

1

203
208

::

S

1

::

4

—

5

1

—

2

1

—

—

213

218

—

—

—

1

—

—

~~

\

—

::

Total

393

525

373

376

290

309

863

1,233

251

299

Number of
stations

10

S

6

21

t

335

FISHERY BULLETIN: VOL. 69. NO. 2

Appendix Table 6. — Length distributions by cruise and sex. — Continued.

Total length

June 11-22

1958

Jon. 18-28, 1960

Apr. 30-Moy

3, I960

Apr. 28-May

I, 1961

Jan. 16-Feb.

22, 1962

Males

Females

Males

Females

Males

Females

Males

Females

Moles

Females

mm

Number

Number

Number

Number

Number

Number

Number

Number

Number

Number

53

—

—

—

—

—

—

—

—

—

—

58

—

—

—

—

—

—

—

—

--

—

63

—

1

—

-

—

—

--

—

--

—

63

—

—

—

—

—

—

—

—

—

—

73

__

—

—

—

1

__

I

78

__

3

1

—

--

1

1

83

_.

..

7

8

_,

1

3

2

2

88

3

_.

15

12

4

3

I

2

93

3

2

15

24

1

4

10

15

1

4

98

4

3

14

18

2

2

19

14

5

4

103

8

7

8

27

9

9

25

19

7

3

108

28

3

8

9

16

19

15

15

14

8

113

48

17

7

5

15

25

7

16

16

10

118

86

23

14

4

29

26

9

9

28

4

123

218

40

31

7

61

21

16

3

32

25

128

201

53

83

11

73

12

80

5

79

25

133

209

85

76

9

69

13

107

3

180

18

138

128

107

63

14

51

29

95

13

232

13

143

104

98

39

3

30

20

58

12

188

5

148

62

91

11

9

6

20

21

15

65

11

153

19

117

8

18

6

21

12

26

16

22

158

2

119

2

19

3

23

4

24

7

39

163

4

125

20

4

35

30

5

91

168

in

2

31

1

36

—

54

138

173

3

130

1

20

2

41

1

77

236

178

4

146

I

27

..

41

1

79

225

183

1

166

..

17

1

21

1

58

213

188

1

149

19

17

__

48

135

193

113

_.

13

11

1

34

—

83

198

78

_.

4

6

__

13

38

203

22

_.

5

3

_-

8

—

17

208

._

4

2

2

—

3

—

8

213

1

—

—

—

—

—

1

—

—

218

—

—

—

—

—

—

—

—

—

—

Total

1,136

1,811

408

356

379

463

489

601

881

1,386

Number of

stations

28

3

10

12

24

336

SEX PHEROMONE ACTIVITY OF THE MOLTING HORMONE,
CRUSTECDYSONE, ON MALE CRABS

(Pachygrapsus crassipes. Cancer antennarius, AND C. anthonyi)

James S. Kittredge,' Michelle Terry,' and Francis T. Takahashi'

ABSTRACT

The pheromone released by premolt female Pachygrapsus crassipes is a heat stable non-ionic polar lipid.
The coincidence of the release of the pheromone and the nubial molt suggested that the molting hormone,
crustecdysone, may also function as a sex pheromone. Adult male crabs were observed to display
typical precopulatory behavior when exposed to dilute solutions of crustecdysone. The threshold con-
centration for behavioral response was found to be 10~i3 m fgj. p crassipes, 10^ i" M for Cancer
antetmariiis and 10-8 m for C. anthovyi. These findings provide the basis for a theory of the evolu-
tion of pheromone communication in the Arthropoda.

The dominant position of chemoreception in the
behavior of marine invertebrates and the impli-
cation of sex pheromones in the reproductive
activities of many species is supported by many
behavioral observations, but no pheromone has
yet been characterized from the marine environ-
ment. In many marine decapod Crustacea copu-
lation takes place immediately after the female
molts. The male of the species recognizes the
premolt condition of the female, is attracted to
her, and usually seizes and carries her until
she molts. This recognition at a distance has
been repoi-ted for many genera of Crustacea
(Hay, 1905 ; L. Agassiz in Verrill, 1908; Needier,
1931; Burkenroad, 1947; Williamson, 1953;
Hughes and Matthiessen, 1962; Knudsen, 1964;
Snow and Neilsen, 1966). Ryan (1966) de-
scribed the search and display behavior exhib-
ited by male Portunus anguinotentus when a
premolt female crab was placed in the holding
tank with them. Each male became active,
walked about on the tips of its dactyls, elevated
its body, and extended its chelae. When thus
stimulated they often attempted to pull any

' Division of^eurosciences. City of Hope National
Medical Center, Duarte, Calif. 91010.

' Zoology Department, Oregon State University, Cor-
vallis, Oreg. 97331. The data in this paper are taken
in part from a dissertation by F.T.T. to be submitted
to Oregon State University in partial fulfillment of the
requirements for the degree of Doctor of Philosophy.

Manuscript received January 1971.
FISHERY BULLETIN; VOL. 69, NO.

crab they met into a precopulatory carrying
position. Ryan demonstrated that this behavior
is released by a sex pheromone in the urine of
the premolt female crab.

METHODS

BIOASSAY

Observation vessels for determining the re-
sponse of male Pachygrapsus crassipes to dilute
solutions of molting hormone were constructed
from 4-liter beakers. With a glass blowing
torch and the edge of a carbon flat we formed
an indent in the side of each beaker approxi-
mately 4 cm deep, parallel to and 3 cm above
the bottom of the beaker. The outside of the
beakers was masked with black paint with the
exception of an 8 cm window opposite the in-
dent. When a crab was placed in seawater in
the observation chamber, they always scurried
into the niche between the bottom of the beaker
and the indent. If the seawater contained molt-
ing hormone, the crabs were stimulated to come
out of the niche and assume a premating stance.
The time elapsing after adding a solution of
crustecdysone in seawater to an empty vessel
containing a male crab until the crab elevated
its cephalothorax in a typical stance was noted.
Six crabs were timed at each concentration of

337

FISHERY BULLETIN: VOL. 69. NO. 2

crustecdysone, and fi-esh male crabs were used
for each different concentration. The male
crabs were held for several days in isolation
from female crabs before testing.

ISOLATION COLUMNS

Columns (5 x 50 cm) of Amberlite XAD-2, a
divinylbenzene polymer, were found to be ef-
fective in the recovery of polar steroids from
seawater. The columns were washed with three
void volumes of water to remove the salts, and
the polar steroids were eluted with three volumes
of 60 Sr ethanol. The more nonpolar lipids were
removed with 95 '^r ethanol. After repeated use
the columns were reconditioned by cycling
through 95 "^r ethanol, diethyl ether, hexane,
diethyl ether, ethanol, and water.

FRACTIONATION COLUMNS

Chromosorb 102, which is an 80/100 mesh
fraction of Amberlite XAD-2, in a 0.9 X 100 cm
column was used to fractionate the ]iolar lipids.
This column was eluted with a gradient of eth-
anol (20^; to 80 r; ) (Hori, 1969). The gradient
was formed by an Isco Dialagrad dual pump"
with the following settings: 40 ml/hr; reser-
voir for "A" pump, 80 "^r ethanol; reservoir for
"B" pump, 20*"^ ethanol; percentage settings
for "B" pump, 100, 100, 90, 80, 70, 60, 50, 30,
15, 0, 0 (this pump makes five intermediate li-
near steps between each setting) ; total time 16
hr. The fractionation was monitored at 254 /jl
with an Isco Model UA-2 UV monitor and frac-
tions were collected in an Isco Model 327 fraction
collector.

A silicic acid column (0.6 X 30 cm) eluted
with chloroform-ethanol (5; 1, v/v) and mon-
itored in the UV was employed for further
fractionation (Horn et al., 1968).

OBSERVATIONS ON THE PREMATING

BEHAVIOR AND THE SEX PHERO-

MONE OF Pachygrapsus crassipes

Although the premating behavior of the lined
shore crab, Pachygrapsus crassipes, as described

by others (Hiatt, 1948; Bovbjerg, 1960), did
not include the typical stance of other Brach-
yura, the abundance and ease of collection of this
specie.? prompted us to re-examine their be-
havior. We found that male P. crassipes, in
the presence of a premolt female, exhibit an
easily recognizable stance. The males elevate
their cephalothoraxes and tilt the anterior
margin up. They walk on the tips of the dactyls
of their first three pairs of walking legs and
extend their fourth pair horizontally backwards.
The chelipeds are partially extended but lowered,
as opposed to the elevated defensive position.
When thus stimulated they will often attempt
to seize any other P. crassipes they encounter,
male or female, and turn them over into the
holding position with which they maintain con-
trol of a premolt female. This behavior com-
pares with that described by Ryan (1966) for
male P. sanguinolentiis. There were two ad-
ditional characteristics of the male P. crassipes
behavior that paralleled the premating behavior
of Cancer magister as described by Snow and
Neilsen (1966). They observed that the male
C. magister, while carrying the female, fre-
quently extended his fourth pair of walking legs
straight back. We have observed that C. ynagis-
fer will thus extend his legs while holding his
body elevated when stimulated by the sex phe-
romone before he seizes the female, as does P.
crassipes. Snow and Neilsen (1966) also noted
that "on occasion the male would rise up on
the tips of his walking legs and raise the female
up into an elevated position nearly 6 inches
off the bottom of the tank. This movement
would be accompanied by a continuous flexing
of the male's abdominal flap." A frequent ob-
servation with pairs of P. crassipes was that
they would stand facing each other, both with
their legs extended and body elevated, but with
the male higher. In this position the female
would lower her abdominal flap slowly and then
flex it rapidly but not into a completely re-
tracted position. She would repeat this move-
ment several times. The male would then repeat
an identical movement of his abdominal flap.

' Reference to commercial products does not imply
endorsement.

338

KITTREDGE, TERRY, and TAKAllASHI; ACTIVITY OF CRUSTECDYSONE

This aspect of their behavior could be inter-
preted as a courting gesture, but in the context
of chemical communication we prefer to inter-
pret this as a fanning motion facilitating the
distribution of pheromones that may be aphro-
disiac in nature. Commercial fishermen for
both the American lobster, Homarus american-
its. and the California spiny lobster, PanuUrus
interrtiptus, have suspected that the males of
each species could be used to attract the females.

A single active premolt female Parhygrapsus
crassipes released sufficient pheromone to stim-
ulate all of the males in a 25-gal recirculating
aquarium. A single female P. crassipes in an
aerated 2-gal container released a phei-omone
which stimulated a male Cancer antennarins
to exhibit a premating stance.

With these observations providing the bio-
assay, we examined the nature of the sex pher-
omone. Water which had contained a premolt
female crab was boiled for 10 min, cooled, and
aerated. The active principle was still present.
The active principle was not retained by cation
nor anion exchange resins nor by charcoal. The
active substance could, however, be extracted
from "active seawater" with isopropanol/di-
ethyl ether. These observations, together with
the premolt condition of the active females, led
us to suspect that the females might be releasing
molting hormone into the water, and that this
steroid might be functioning as a sex pheromone.

BIOASSAY OF CRUSTECDYSONE

We soon confirmed that dilute solutions of
crustecdysone (/3-ecdysone, 20R-hydroxyecdy-
sone, ecdysterone, isoinokosterone) , which is
one of the molting hormones of Crustacea (Horn
et al., 1968), elicited a typical response from
male P. crassipes. In order to establish the
threshold concentration that would release re-
sponse we standardized the conditions for the
bioassay. As described under "Methods," the
test adopted allowed the male crab to be flooded
with a known concentration of the steroid in
seawater, in contrast to the diffusion techniques
often em]3loyed. P. crassipes proves to be ideal
for this mode of testing because they are an

intertidal species and in nature normally leave
the tide pools at low tide to feed on the rocks.
They were not disturbed on being placed in a
wet empty observation vessel and sought out
the artificial niche provided. On flooding with
seawater they would remain in the niche for
long periods or occasionally come out to explore
briefly and then return to the niche. When a
male P. crassipes was flooded with a solution
of crustecdysone in seawater, he was stimulated
to come out of the niche and explore the vessel
and then to assume the premating stance. The
time elapsing until the crab raised its body to
assume the stance was found to be a function
of the concentration of crustecd.vsone. Although
the male crabs would often exhibit a full stance
in a brightly illuminated laboratory at the high-
er concentrations of crustecdysone, the response
was often erratic. All of the bioassays were
conducted in an isolated room illuminated with
an Eastman darkroom lamp with a 1.5-w bulb
and an Eastman No. 00 yellow filter. The ob-
server was stationed quietly before the "win-
dow" of the test vessel. On removal from the
test vessel the male crabs were transferred to
a 2-liter beaker of seawater to rinse off the ex-
traneous crustecdysone and then were trans-
ferred to a small aquarium for further obser-
vation. In spite of the handling during the two
transfers, male crabs that had been stimulated
to display a premating stance in the observa-
tion vessel usually resumed this posture shortly
after being transferred to the aquarium. When
thus stimulated they often attemjited to seize
any other male crab in the aquarium.

All of the male P. crassijies utilized in estab-
lishing the response curve were collected at the
same time and in the same area where we had
just succeeded in collecting a number of in-e-
molt females. They were all held for three or
more days in isolation from any female crabs.
The curve was started with a concentration of
10^'' M crustecdysone in filtered seawater. At
this concentration the resjionse was rapid, aver-
aging 7 sec. Succeeding tests were performed
with ten-fold dilutions of the crustecdysone.
Fresh solutions of crustecdysone were prepared
after three steps of dilution or at the start of
each day's testing. Previous experience had

339

FISHERV BULLETIN, \0L. 69, NO. 2

demonstrated that dilute solutions in seawater
lost some or all of their activity on storage even
at 0° C, presumably through bacterial degra-
dation or adsorption. It was planned that six
male crabs would l)e tested at each concentration
and that the five most consistent times would
be averaged; however, the response was found
to be remarkably uniform and in all but three
cases all six crabs responded within a narrow
time range. There was no sharp threshold of
concentration. The average response times
jilotted as a smooth curve extending to lO"''^ M
crustecdysone concentration where the average
response time was 22 min (Figure 1). No re-

CRUSTECDYSONE

500 1000 1500

REACTION TIME (sec)

Figure 1. — Time elapsed following immersion of male
Paehygrapsus ci'assipes in seawater solutions of crus-
tecdysone before the body elevation phase of the pre-
copulatory behavior.

sponse was observed at 10"'" M. The scatter
of response times was greatest at 10"^ M, prob-
ably because of the short-term di.sturbance of
the male crab during flooding. The standard
deviation of the normalized response times for
'15 crabs, from 10 " m to 10 '■' M crustecdysone,
was 8.6.

Since the ijrecopulatory l)ehavior of males in
the presence of premolt females ajipears to 1)C
general among the Brachyui-a, we examined the

response of two species of Cancer to crustecdy-
sone. Both C. antennaruis and C anthonyi dis-
played typical premating behavior when exposed
to dilute solutions of crustecdysone. When the
respon.^e time vs. concentration study was car-
ried out with these two species each yielded a
response curve similar to that developed by P.
cmssipes. There was, however, a marked dif-
ference. There was an abrupt break in the re-
sponse yielding a distinct threshold at lO"'" M
for C. antenna I i us and 10~* M for C. anthonyi.
We then attempted to determine if C. anten-
na rius males could detect a gradient in the con-
centration of crustecdysone. For this i)urpose
we employed a simple "T" maze with a baflle
at the head of each arm separating the seawater
sources and forming mixing chambers. Five
male C. antennarhis were placed at the head of
the maze and the water flows from each arm
balanced. WHiile seawater alone was flowing
through the maze the C. ontennarhw remained
quiet in the two corners at the origin of the
maze. When a flow of crustecdysone solution
was added to the mixing chamber at the head
of one arm all five of the male C. antennarhis
soon became active. They ex])lored up and down
each arm of the maze but demonstrated no
tendency to select the arm containing the crus-
tecdysone. While these tests did not indicate
any ability to detect or follow up a gradient,
there was a positive re?i3onse to the crustecdy-
sone. All five of the male crabs were stimu-
lated simultaneously to undertake an active ex-
ploratory behavior when the crustecdysone was
introduced.

DEVELOPMENT OF THE TECHNIQUES
FOR THE ISOLATION AND FRAC-
TIONATION OF THE SEX
PHEROMONE{S)

Liquid-liquid extraction procedures are inef-
ficient for the recovery of trace quantities of
polar lipids. Columns of Amberlite XAD-2 have
been employed for the recovery of steroids from
urine (Bradlow, 1968; Shackleton, Sjovall, and
Wisen, 1970). Recently, Hori (1969) has em-
ployed a column of this resin eluted with a li-

340

KITTREDGE. TERRY, and TAKAIIASHE ACTIVITY OF CRUSTECDYSONE

near piadient of ethanol in water for the frac-
tionation of the phytoecdysones. We have found
that a column of XAD-2 could be used to re-
cover traces of crustecdysone from seawater and
from crab urine. Using the above two columns
we have examined the seawater in which female
P. crassipes, C. magistev. and C. productns had
been maintained for 3 to 6 hr. The product
of individual Cancer were assayed, while the
seawater from two or more P. crassipes was
combined before extraction. We have also ex-
amined the urine of female C. magister. The
Cancer were staged according to Drach (1939),
and the female P. crassipes were selected for
activity by observing the behavior of males in
their presence. During our observations we
found the female C. magister continued to re-
lease a pheromone for up to 2 weeks post molt.
The material recovered from the isolation
column in 60 ';r ethanol was reduced in volume
to a few microliters and transferred in 20';'r
ethanol to the Chromosorb 102 column. Elu-
tion of this column yielded an ultraviolet-ab-
sorbing peak near the front and two or more
succeeding peaks. Each of three stage "D" C.
magister and one stage "D" C. productns studied
were found to have released an ultraviolet-ab-
sorbing compound that eluted from the column
at the same ethanol concentration that a crus-
tecdysone standard did. Both extracts of P.
crassipes seawater yielded a peak in the position
of crustecdysone. One stage "A" C. magister
also yielded a peak in this position. A stage
"C-4" C. magister did not yield any peak in
the position of crustecdysone nor did urine from
a stage "C-4" C. magister yield a peak in this
position. Also one of the C. magister females
that had yielded material eluting as crustecdy-
sone while in stage "D" did not yield this sub-
stance during molting (stage "E"). The ultra-
violet-absorbing fractions corresponding to
crustecdysone from the above columns did not
have an ultraviolet-absoi'ption spectrum corres-
ponding to that of crustecdysone. The absorp-
tion peak included the spectrum of crustecdy-
sone, but had a double peak at a lower wave
length. These fractions were concentrated and
applied to a silicic acid column. The elution of

this column with chloroform-ethanol yielded an
ultraviolet-absorbing peak near the front and
a peak eluting in the same volume as a crus-
tecdysone standard. The material from this
column has an ultraviolet-absorption spectrum
that corresponds closely to that of crustecdysone.
We are now developing a derivitization tech-
nique that will permit us to subject our final
samples to gas chromatography-mass spectro-
photometry for structural confor'mation. Katz
and Lensky (1970) have published a technique
for the silylation of a-ecdysone for GLC analy-
sis. We have employed silylation techniques
with crustecdysone and observed decomposition
during GLC.

RESULTS AND CONCLUSIONS

The pheromone released by P. crassipes stim-
ulates premating behavior in C. antennarius.
Male C. magister are excited into seizing and
clasping female C. productns by their phero-
mone. Crustecdysone mimics the pheromone in
its effects on male P. crassipes, C. antennarius,
and C. anthonyi in the release of the premating
stance. After exposure to crustecdysone all
these species of male crabs attempt to seize
other crabs, male or female, and pull them into
a precopulatory position. In addition crustec-
dysone triggers a search behavior in male C.
antennarius. These observations demonstrate
a lack of specificity in the sex pheromones of
these species and either that crustecdysone is
the sex pheromone or sufficiently similar in mo-
lecular structure to the natural pheromones to
mimic them.

A possible explanation of the discrepency be-
tween our results and those of Ryan (1966)
that indicated a species specificity for the sex
pheromones in the three species of crabs that
he studied may be that some species may re-
spond to deoxycrustecdysone, callinecdysone A
(inokosterone) or callinecdysone B (makister-
one), other ecdysones that have been isolated
from Crustacea, (Gailbraith et al, 1968; Faux
et al., 1969), or they may respond to one of the
metabolic products of crustecdysone detected in
insects (Gailbraith et al, 1969; Moriyama et al.,

341

FISHERY BLLLETIN: VOL, 69, NO. 2

1970; Cherbas and Cherbas, 1970; Heinrich
and Hoffmeister, 1970).

The isolation and analysis of the material
released into seawater by active female P. cras-
sipes, C. mac/ister, and C. i)roductus demon-
strated that a compound could be detected that
is eluted from two different columns in the same
position as crustecdysone and has a UV absorp-
tion spectra that is similar to that of crustec-
dysone.

The semilogs plot of the response times for
male P. cmssiiies to varying concentrations of
crustecdysone is approximately ]3arabolic, and
the scatter of response times at each concen-
tration is remarkably narrow. This, the range
of response times, and the continued resjionse
of the male crabs after removal from the stim-
ulus, permit an interpretation of the chemore-
ception of pheromones from dilute solutions.
The observations suggest that the pheromone
has a high affinity for the receptor site resulting
in a long half life for the receptor-pheromone
complex. Indeed, one might have postulated that
even a polar steroid might be strongly bound to a
lipoid receiitor in an aqueous medium. It is aj)-
parent that the crabs are capable of summating
the chemical information for a considerable per-
iod of time before a threshold which releases re-
sponse liehavior is reached. Though summation
may take place at any level in the nervous sys-
tem, the simplest interpretation suggests that
this takes place at the receptors. This summa-
tion of "information quanta" can function either
in extremely dilute solutions or, in nature, it
would permit the accumulation of subthreshold
amounts presented in random turbulences of
the current from the source.

This finding has significance in a consider-
ation of the evolution of pheromone communi-
cation. It has been suggested that chemical
signals between cells were evolved before the
evolution of the metazoans and that these sig-
nals were later internalized as hormones and
synaptic transmitters (Haldane, 195r); Wilson,
1968). In the present instance we have a re-
versal of this internalization. The Crustacea,
having evolved polar steroid hormones to reg-
ulate molting, on externalization of the receptor

site onto chemoreceptor organs and on altera-
tion of the resorption process in the antennual
gland during the premolt stage of the females
were then capable of signaling the approach of
the nubial molt. This interpretation obviates
the concern over the improbability of the simul-
taneous de novo origin of both the genetic in-
formation directing the biosynthesis of the pher-
omone and that concerned with the architecture
of the i-eceptor site. We may assume that an
unmasking of that portion of the chromosome
that specifies the receptor site for the hormone
on the membranes of the target organs occurred
in the chemosensory neurons. A masking of the
active transport system for the hormone from
the fluid of the antennule gland of the female
is also assumed. These two innovations are
reasonably small evolutionary steps and con-
ceptually preferable to the two de nova origins
that must be assumed otherwise. This evolu-
tionary step, the pheromone function of a hor-
mone, may have been the origin of pheromone
communication in the Arthropoda, for once fixed
because of its reproductive value, it was then
susceptible to a gradual evolutionary drift to-
ward a variety of more specific pheromones.

ACKNOWLEDGMENTS

We thank the National Marine Fisheries Ser-
vice, Fishery-Oceanography Center, La Jolla,
Calif., for providing seawater facilities. This
research was supported by ONR Contract
N00014-70-C-0059 and NSF Institutional Sea
Grant GH-10 and was also made possible in
]iart by an Irving Genett Research Fellowship
(J. S. Kittredge) and a California Biochemical
Foundation Summer Student Fellowship (M.
Terry).

LITERATURE CITED

BOVBJERG, R. V.

19G0. Courtship behavior of the lined .shore crab,
Paclij/grapsus crassipes (Randall). Pac. Sci. 14:
421-422.
Bradlow, H. L.

1968. Extraction of steroid conjugates with a
neutral re.sin. Steroids 11: 265-272.

342

KITTREDGF., TERRY, and TAKAHASHE ACTI\ITV OF CRUSTF.CDVSONE

BlIRKENROAD, M. D.

1947. Reproductive activities of decapod Crustacea.
Amer. Natur. 81: 392-398.

Cherbas, L., and p. Cherbas.

1970. Di.stribution and metabolism of a-ecdysone
in pupae of the silkworm Antheraea poIyphemus.
Biol. Bull. (Woods Hole) 138: 115-128.

Drach, p.

1939. Mue et cycle d'intermue chez les crustace's
de'capodes. Ann. Inst. Oceanogr., New Ser. 19:
103-391.
Faux, A., D. H. S. Horn. E. J. Middleton, H. M. Fales,
and M. E. Lowe.

1969. Moulting hormones of a crab during ecdysis.
J. Chem. Soc. (London), Sect. P, Chem. Commun.,
p. 175-176.
Gailbraith, M. N., D. H. S. Horn, E. J. Middleton, and
R. J. Hackney.

1968. Structure of deoxycrustecdysone, a second
crustacean moulting hormone. J. Chem. Soc.
(London), Sect. D, Chem. Commun., p. 83-85.

Gailbraith, M. N., D. H. S. Horn, E. J. Middleton,
J. A. Thompson, J. B. Siddal, and W. Hafferl.

1969. Catabolism of crustecdysone in the blowfly
CnlUfnra stygifi. J. Chem. Soc. (London), Sect.
D, Chem. Commun., p. 1134-1135.

Haldane, J. B. S.

1955. Animal communication and the origin of
human language. Sci. Progr. 43: 385-401.

Hay, W. p.

1905. The life history of the blue crab {Calhnectes
sapidus). Rep. [U.S.] Bur. Fish. 1904: 395-413.
Heinrich, G., and H. Hoffmeister.

1970. Bildung von Hormonglykosiden als Inakti-
vierungsmechanismus bei Calliphora erythroceph-
ala. Z. Naturforsch. 25b: 358-361.

HiATT, R. W.

1948. The biology of the lined shore crab, Pachy-
grnpsiis crassipes Randall. Pac. Sci. 2: 135-213.

HoRi, M.

1969. Automatic column chromatographic method
for insect-molting steroids. Steroids 14: 33-46.
Horn, D. H. S., S. Fabbri, F. Hampshire, and M. E.
Lowt:.

1968. Isolation of crustecdysone (20 R-hydroxy-

ecdysone) from a crayfish (Jasiifi lalaiidei Milne-
Edwards). Biochem. J. 109: 399-406.
Hvgiies, J. T., and G. C. Matthiessen.

1962. Observations on the biology of the American
lobster, Hnmnrus americanus. Limnol. Oceanogr.
7: 414-421.
Katz, M., and Y. Lensky'.

1970. Gas chromatographic analysis of ecdysone.
Experientia 26: 1043.
Knudsen, J. W.

1964. Observations of the reproductive cycles and

ecology of the common Brachyura and crablike

Anomura of Puget Sound, Washington. Pac.

Sci. 18: 3-33.

MORIYAMA, H., K. Nakanishi, D. S. King, T. Okauchi,

J. B. Siddall, and W. Hafferl.

1970. On the origin and metabolic fate of a-ecdy-
sone in insects. Gen. Comp. Endocrinol. 15: 80-
87.
Needler, a. B.

1931. Mating and oviposition in Pandalus danae.
Can. Field Natur. 45: 107-108.
Ryan, E. P.

1966. Pheromone: evidence in a decapod crus-
tacean. Science (Washington) 151: 340-341.
Shackleton, C. H. L., J. Sjovall, and 0. Wise'n.
1970. A simple method for the extraction of ster-
oids from urine. Clin. Chim. Acta 27: 354-356.
Snow, C. D., and J. R. Neilsen.

1966. Premating and mating behavior of the Dun-
geness crab (Cancer magister Dana). J. Fish.
Res. Bd. Can. 23: 1319-1323.
Verrill, a. E.

1908. Decapod Crustacea of Bermuda, I. Brachyura
and Anomura. Their distribution, variations,
and habits. Trans. Conn. Acad. Arts Sci. 13:
299-474.
Williamson, D. T.

1953. Mating behaviour in the Talitridae (Amphi-
poda). Brit. J. Anim. Behav. 1: 83.
Wilson, E. 0.

1968. Chemical systems, /n T. A. Sebeok (editor),
Animal communication, p. 75-102. Indiana Univ.
Press, Bloomington.

343

CHARACTERISTICS OF SEA-SURFACE TEMPERATURE ANOMALIES

L. E. Eber'

ABSTRACT

Sea-surface temperature anomalies in the North Pacific Ocean, constructed from a 14-year series (1949-
62) of monthly mean charts, exhibit numerous instances of quasi-stationary behavior. Selected exam-
ples from this series reveal a recurring pattern in which the principal feature is a positive or negative
cell in the anomaly field, located approximately between lat 30° N and 50° N. The cell in this pat-
tern is partially encircled by anomalies of opposite sign to the north, east, and south in a zone contig-
uous with the North American coast. This anomaly configuration, viewed with consideration of the
associated sea-temperature field, suggests the existence of a standing wave in the current structure.
Such a wave could affect the partitioning of the West Wind Drift Current as it approaches the coast
and splits into northward and southward flowing branches. Physical data for verification of a stand-
ing wave are not available, but dimensional attributes inferred from the sea-temperature anomaly
structure conform loosely to theoretical constraints.

The temperatures in the upj^er mixed layer of
the ocean undergo annual cycles, induced by
seasonal heating and cooling, which vary from
year to year. This variation can be expressed
in terms of departures from the mean annual
temperature cycle obtained by averaging over
a number of years. The magnitudes, area) dis-
tributions, and time changes of such departures
define anomalous conditions in the surface layer
of the sea.

The 14-year series, 1949-62, of monthly sea-
surface temperature charts, published by Eber,
Saur, and Sette (1968), provides a base for
studying temperature variations in the North
Pacific Ocean. Monthly anomaly charts were
constructed from this series by taking the dif-
ference between the sea-surface temperature
fields for each month and year and the corres-
]3onding monthly normal fields. The latter were
obtained by computing the 14-year averages, by
month, at grid points. A number of selected
examples are presented here to show the char-
acter of some of the prominent and long-lasting
anomalies that occurred in the North Pacific
Ocean between 1949 and 1962.

Many of the features to be discussed are in
the vicinity of the transition zone between the
subarctic and subtropic oceanographic regions
as described by Tully (1964). Through this

' National Marine Fisheries Service Fishery-Ocean-
ography Center, La Jolla, Calif. 92037.

zone, which is located approximately at lat 35° N
to 45° N between long 160° E and 140° W,
the surface current flows eastward as the West
Wind Drift. The mean surface temperature
distribution in this region is essentially zonal
with isotherms oriented along the circles of lat-
itude. The chart of the 14-year average for
October (Figure 1) illustrates these charac-
teristics. As the West Wind Drift approaches

IZO" 130* 140* aO- 160* 170* WO* ITO* WO* OO* I40* 130* 120* IW* 100* 90* 90*

Figure 1. — Average sea-surface temperatures of the
North Pacific Ocean in October, based on data from the
14-year period 1949-62.

the North American coast, it splits. One part
turns north and moves in a counterclockwise
trajectory around the Alaska Gyre and the other
part turns south to become the California

Manuscript received January 1971.

FISHERY BULLETIN: VOL. 69. NO. 2. 1971.

345

FISHERY BULLETIN: VOL. 69, NO. 2

Current. The sea-surface isotherms, corre-
spondingly, bend north and south, effecting a
much-reduced temperature gradient parallel to
the coast.

BEHAVIOR OF SEA-SURFACE
TEMPERATURE ANOMALIES

To facilitate description, I shall designate as
"warm" or "cold" cells, areas where the mag-
nitude of departure from noi-mal was 1° C or
greater. The evolution of an anomaly can be
readily followed by noting the configuration of
its principal cell, or cells, in successive months.
This is evident in the figures used to illustrate
selected examples (Figures 2-30). These show

of the positive departures from normal within
this cell exceeded 3° C. Off the North American
coast, the temperature anomalies were negative,
with magnitudes greater than 1° C in a broad
zone from Alaska to the tip of Baja California.
Figui'es 3-5 show subsequent positions of the
warm cell in March, July, and October, respec-
tively. The maximum intensities waxed and
waned over this time period, dropping in March,
increasing again to more than 3° C in July and
diminishing once more in October. Except for
a slight northward shift, the warm cell remained
essentially stationary. During most of the peri-
od, negative anomalies prevailed in the coastal

Figure 2. — Sea-surface temperature anomaly for Jan-
uary 1949. Hatched areas colder than normal. Heavy
lines represent the 1° C anomaly contours which define
warm (-f) or cold ( — ) cells.

Figure 3. — Sea-surface temperature anomaly for March
1949. Hatched areas colder than noi-mal. Heavy lines
represent the 1° C anomaly contours which define warm
(-I-) or cold ( — ) cells.

the sizes and locations of the principal cells,
enclosed by heavy lines representing a magni-
tude of 1° C, in the regions relevant to the dis-
cussion. The cells are marked by plus or minus
symbols according to the sign of the anomalies.
The thin lines rei)resent the zero anomaly con-
tour separating areas of below normal temper-
ature (hatched areas) from those where the
temperature was above normal.

A good example of persistence was the warm
anomaly present in the eastern North Pacific
throughout mo.st of 1919. In January the warm
cell (defined by the 1° C anomaly contour) cov-
ered most of the area from lat 30° N to 45° N
and long 145° W to 180° W. Maximum intensity

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Figure 4. — Sea-surface temperature anomaly for July
1949. Hatched areas colder than normal. Heavy lines
represent the 1° C anomaly contours which define warm
(-I-) or cold ( — ) cells.

346

EBER: SEA-SURKACE TEiMPERATURE ANOMALIES

Figure 5. — Sea-surface temperature anomaly for Oc-
tober 1949. Hatched areas colder than normal. Heavy
lines represent the 1° C anomaly contours which define
warm ( + ) or cold ( — ) cells.

zone and in a southwestward tongue below 30° N
but with fluctuating magnitudes.

The warm cell shrank in November and lost
its specific identity in December. However, the
general configuration of the colder than normal
coastal zone and warmer than normal offshore
region persisted through the winter and spring
of 1950. In May 1950, the positive anomalies
intensified and spread westward to Japan. The
pattern stabilized in June and July marked by
prominent warm cells in the east and far west
portions of the positive area (Figure 6). At
the same time, a cold cell in the Gulf of Alaska
had begun to grow and jnish southward; this

movement continued through September (Fig-
ure 7) accompanied by an eastward expansion
of the warm belt. Ultimately, there was a de-
formation of the broad-scale pattei-n which had
for many months dominated the central and
eastern North Pacific, as negative anomalies
spread through the Gulf of Alaska.

Figure 6. — Sea-surface temperature anomaly for July
1950. Hatched areas colder than normal. Heavy lines
represent the 1° C anomaly contours which define warm
( -f ) or cold ( — ) cells.

Figure 7. — Sea-surface temperature anomaly for Sep-
tember 1950. Hatched areas colder than normal. Heavy
lines i-epresent the 1° C anomaly contours which define
warm ( -f ) or cold ( — ) cells.

The years 1951-54 presented no striking ex-
amples of persistent sea temperature anomalies.
Some relatively large-scale anomalies did devel-
op in this period but they were short-lived.
Much of the time the anomaly field was flat and
featureless. Midway through 1955, however,
a long-term progression of events began to
evolve with the development of an anomaly pat-
tern which was characterized by a positive belt
that stretched eastward from Japan and a neg-
ative zone along most of the North American
coast. The anomaly field intensified in August
(Figure 8) when maxima exceeded 2° C in the
warm cell and an extensive cold area was in'esent
in the coastal zone with negative departures
exceeding 1 ° C in magnitude. The negative area
stretched southwestward below lat 30° N. This
pattern prevailed through November 1955 (Fig-
ure 9) but became weaker in Decemljer. In
January 1956, the positive area contracted to
the west while the region of negative anomalies
to the east became flat and disorganized. Figure
10 shows the situation in February 1956. The

347

FISHERY BULLETIN: VOL. 69, NO. 2

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Figure 8. — Sea-surface temperature anomaly for August
1955. Hatched areas colder than normal. Heavy lines
represent the 1° C anomaly contours which define warm
( + ) or cold ( — ) cells.

•J

Figure 10. — Sea-surface temperature anomaly for Feb-
ruary 1956. Hatched areas colder than normal. Heavy
lines represent the 1° C anomaly contours which define
warm ( -|- ) or cold ( — ) cells.

Figure 9. — Sea-surface temperature anomaly for No-
vember 1955. Hatched areas colder than normal. Heavy
lines represent the 1° C anomaly contours which define
warm ( -|- ) or cold ( — ) cells.

Figure 11. — Sea-surface temperature anomaly for Au-
gust 1956. Hatched areas colder than normal. Heavy
lines represent the 1° C anomaly contours which define
warm (-f ) or cold ( — ) cells.

warm cell at lat 36° N to 50° N, long 175° W to
150° E was the only prominent feature in evi-
dence and remained so until August 1956, when
a large cold cell developed just east of it (Figure
11). This latter feature was short-lived, how-
ever, and during the next few months the posi-
tive area once again expanded eastward while
the tendency of anomalies along the North Amer-
ican coast changed from variable to predomi-
nantly negative. The chart for November 1956
(Figure 12) depicts the result of this process.
Transition to a second phase in the long-term
evolution of the anomaly (ield was foreshadowed
l)y a small cold cell at lat 25° N to 30° N, long

160° E to 170° E (Figure 12). This cold cell
grew in size but remained in about the same
location through March 1957 (Figure 13) while
the area of positive anomalies edged toward the
North American coast. The transition was
complete by June, when the cold cell shifted
north and stretched eastward in a belt of neg-
ative anomalies between lat 30° N and 40° N
(Figure 11). Positive values prevailed in the
Gulf of Alaska and along the North American
coast, effecting an almost complete reversal
from the late 1955 iiattern.

The negative anomalies in the west central
sector, long 175° W to 160° E, contracted to form

348

EBER: SEA-SURFACE TEMPERATURE ANOMALIES

Figure 12. — Sea-surface temperature anomaly for No-
vember 1956. Hatched areas colder than normal. Heavy
lines represent the 1° C anomaly contours which define
warm ( -|- ) or cold ( — ) cells.

Figure 14. — Sea-surface temperature anomaly for June
1957. Hatched areas colder than normal. Heavy lines
represent the 1° C anomaly contours which define warm
( + ) or cold ( — ) cells.

CO" ISO* MO* OO" 160* ITO" IBO* ITO* leC I50» 140' ISO" 120* "0* 100* SO- 80*

Figure 13. — Sea-surface tempei'ature anomaly for March
1957. Hatched areas colder than normal. Heavy lines
represent the 1° C anomaly contours which define warm
( -f ) or cold ( — ) cells.

Figure 15. — Sea-surface temperature anomaly for Au-
gust 1957. Hatched areas colder than normal. Heavy
lines represent the 1° C anomaly contours which define
warm ( + ) or cold ( — ) cells.

a single prominent cell which, in August 1957,
was centered at about lat 40° N, long 175° E
(Figure 15). This feature remained fairly
steady through November 1957 (Figure 16),
but all remnants of the cold anomalies in the
east sector vanished.

The cell structure in the negative anomaly
deteriorated at the beginning of 1958, but re-
formed in March with the cold cell east of its
earlier position, at lat 30° N to 40° N, long 145°
W to 170° W (Figure 17) . Further fluctuations
took place in the negative region until August
1958, when a dominant cold ceil appeared at
lat 35° N to 50° N, long 150° W to 175° W

(Figure 18). The zone of positive anomalies
along the North American coast was strongly
developed during most of 1958 and 1959. How-
ever, the emphasis in the distribution shifted
to the south after mid-1958, and the warm
tongue reaching southwestward, south of lat
30° N, was most intense in the early months of
1959 (Figures 19 and 20).

Elsewhere the pattern tended to be somewhat
weak and disorganized, and remained so until
November 1959, when prominent cells, in which
departures from normal exceeded 2° C, were
evident in the central oceanic region of neg-
ative anomalies and in the positive coastal zone

349

FISHERY BULLETIN: VOL. 69, NO. 2

^

1

i

Ik^

)l

II

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;

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y

^

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tm

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lilC~-iX^^ '^

' ■

fiX^Li^BCi^

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JJ

+H~N-im

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H

_

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ZW IZO* 150- 140* ISO*

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170

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ro-

le

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20-

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Figure 16. — Sea-surface temperature anomaly for No-
vember 1957. Hatched areas colder than normal. Heavy
lines represent the 1° C anomaly contours which define
warm (-|-) or cold ( — ) cells.

IZO* ISO* 140* 00* 160* ITO* «0* ITO* HCT ISO* 140* 130* 00* HO* ICO* 90* 80*

Figure 18. — Sea-surface temperature anomaly for Au-
gust 1958. Hatched areas colder than normal. Heavy
lines represent the 1° C anomaly contours which define
warm ( + ) or ( — ) cells.

Figure 17. — Sea-surface temperature anomaly for March
1958. Hatched areas colder than noi-mal. Heavy lines
represent the 1° C anomaly contours which define warm
(-I-) or cold ( — ) cells.

Figure 19. — Sea-surface temperature anomaly for Jan-
uary 1959. Hatched areas colder than normal. Heavy
lines represent the 1° C anomaly contours which define
warm ( -|- ) or cold ( — ) cells.

(Figure 21). The intensity and size of the wai-m
cells diminished by February 1960 (Figure 22)
and anomalies along the North American coast
were generally weak, although mostly positive,
through mid-1961.

The cold cell present in the west central Pa-
cific in November 19*59 had, by February 1960,
pushed eastward to a new location, at lat 32° N
to 48° N, long 155° E to 155° W (Figure 22).
Thereafter it remained essentially within this
region until the spring of 1961. However, the
size and shape of the cold cell fluctuated con-
siderably during this extended interval, as in-
dicated in the charts for June 1960, November

1960, and February 1961 (Figures 23-25). This
cold cell began to shift eastward in May 1961 and,
by June, had reached a position at lat 32° N
to 45° N, long 137° W to 160° W (Figure 26)
where it remained through August. A new
warm cell had appeared in the west sector at
lat 30° N to 40° N, long 170° W to 165° E in
June, but cannot easily be related to an impend-
ing transition in the anomaly field. It appeared
to shift we.stward in July and August then
vanished in September 1961, when the over-
all pattern collapsed.

The third and final phase in the progression
of events began rather abruptly in October 1961

350

EBER: SEA-SURFACE TEMPERATURE ANOMALIES

120* 130* 140* OO* 160* 170* WO* 170* 160* 150* 140* 130* BO* 110* lOO* 90* BO*

Figure 20. — Sea-surface temperature anomaly for March
1959. Hatched areas colder than normal. Heavy lines
represent the 1° C anomaly contours which define warm
( + ) or cold ( — ) cells.

IZO* 130* 140* ISO* ISO* (TO* IBO* 170* 160* 130* 140* 130* 120* 110* 100* 90* 80*

Figure 22. — Sea-surface temperature anomaly for Feb-
ruary 1960. Hatched areas colder than normal. Heavy
lines represent the 1° C anomaly contours which define
warm (-|-) or cold ( — ) cells.

Figure 21. — Sea-surface temperature anomaly for No-
vember 1959. Hatched areas colder than normal. Heavy
lines represent the 1° C anomaly contours which define
warm ( -|- ) or cold ( — ) cells.

I20- I30* 140* 130* 160* 170* WO* 170* ISO* OO* 140* 130* IZO* 110* lOff 90* 60*

Figure 23. — Sea-surface temperature anomaly for June
19ti0. Hatched areas colder than normal. Heavy lines
represent the 1 ° C anomaly contours which define warm
( + ) or cold ( — ) cells.

with a second reversal of the anomaly field in
the central and eastern North Pacific Ocean
(Figure 27). The principal feature of the new
pattern was a warm cell which developed at lat
35° N to 45° N, long 145° W to 175° W.
Departures from normal temperatures along
the coastal zone and in the region to the south-
east of the warm cell were weak but predomi-
nantly negative. In a broad sense, this distri-
bution remained essentially undisturbed for
nearly a year. The warm cell shifted eastward
in January 1962 (Figure 28), diminished in
size and intensity in March and April, but re-
vived in June 1962 (Figure 29) . A second warm

cell was present at that time, but did not re-
tain a separate identity for long. The original
warm cell began a westward movement which,
liy September (Figure 30), returned it to the
same location it occupied 11 months earlier in
October 1961 (Figure 27).

MAINTENANCE OF PERSISTENT
ANOMALIES

The examples de.scribed in the iireceding
section depict a recurring pattern in the distri-
bution of sea-surface temperature anomalies.
Schematically, the princijwil features consist of

351

FISHERY BULLETIN: VOL. 69, NO. 2

Figure 24. — Sea-surface temperature anomaly for No-
vember 1960. Hatched areas colder than normal. Heavy
lines represent the 1° C anomaly contours which define
vifarm { + ) or cold ( — ) cells.

Figure 26. — Sea-surface temperature anomaly for June
1961. Hatched areas colder than normal. Heavy lines
represent the 1° C anomaly contours which define warm
( -i- ) or cold ( — ) cells.

Figure 25. — Sea-surface temperature anomaly for Feb-
ruary 1961. Hatched areas colder than normal. Heavy
lines represent the 1° C anomaly contours which define
warm (-|-) or cold ( — ) cells.

Figure 27. — Sea-surface temperature anomaly for Oc-
tober 1961. Hatched areas colder than normal. Heavy
lines represent the 1° C anomaly contours which define
warm ( -|- ) or cold ( — ) cells.

a dominant, quasi-stationary cell in a latitudinal
belt of either tJositive or negative anomalies, lo-
cated appro.ximately between lat 30° N and
50° N, partially encircled by anomalies of op-
posite sign to the north, east, and south, in a
zone contiguous with the North American coast.
The dominant cell in this model is embedded in
the North Pacific West Wind Drift Current. It
reflects a wavelike displacement of the isotherms,
which normally are very nearly zonal from
about long 150° E to 140° W in the vicinity of
lat 40° N.

The fact that this cell, which defines an area
of maximum departure from normal in the tem-

perature field, is not i^ropagated eastward with'
the ocean current suggests the existence of a
standing wave, or perturbation, in the current
structure. Assuming this to be so, water enter-
ing the wave would turn north (or south) of
its normal course, cutting across the normal iso-
therms and thereby causing anomalous local ad-
vection of high (or low) temperature. Down-
stream from the point of maximum excursion
the water cuts back toward its original course
and temperature conditions revert toward nor-
mal. Because the temperature gradient across
the \\'est Wind Drift Current is moderately
strong, a small displacement of the isotherms

352

EBER: SEA-SURFACE TEMPERATURE ANOMALIES

■'n.^y^#_)ii/^~--Z77

■fy-UtS^^^'^ ^^

^^^

tSMSm

-^rrr^-

'•HS-JIlr

\ JyJi"

yfffJl

tH

■cl''«L

H

^1

~^H

'Ft^SiOI^X -

^

j j

\ ''-^mT^^^

•

/ / '~r

\'^Mki \vL

1

Figure 28. — Sea-surface temperature anomaly for Jan-
uary 1962. Hatched areas colder than normal. Heavy
lines represent the 1° C anomaly contours which define
warm ( + ) or cold ( — ) cells.

P'iGi'RE 29. — Sea-surface temperature anomaly for June
1962. Hatched areas colder than normal. Heavy lines
represent the 1° C anomaly contours which define warm
( + ) or cold ( — ) cells.

relative to the width of the current can create
an anomaly of 1° C to 2° C. The ampHtude of
the perturbation in the current must, of course,
be greater than that in the temperature field,
since the water must adjust toward new equili-
brium temperature appropriate to the local heat
exchange processes as it changes latitude. Thus,
a parcel of water following a northward de-
flection of the streamlines would arrive at the
northern bend, or crest, of a standing wave with
a temperature lower than it would have had if
no deviation from zonal flow had occurred. Ow-
ing to the advective eff'ect, it would nonetheless
be warmer than an equivalent parcel of water

120* ISO* WO* iXr 160* ITO* wo- ITO- WO* 00* 140* 130* 120* IW* 100* 90* BO*

Figure 30. — Sea-surface temperature anomaly for Sep-
tember 1962. Hatched areas colder than normal. Heavy
lines represent the 1° C anomaly contours which define
warm ( -|- ) or cold ( — ) cells.

reaching the same location by a normal, zonal
trajectory.

The existence of a perturbation upstream
from the location where the West Wind Drift
splits may have a significant effect on the pro-
portional flow into the Alaska Gyre and the Cal-
ifornia Current. For example, in a wave
formed by a northward deflection of the zonal
current, water moving downstream from the
crest would have a southward component which
might favor more transport into the California
Current. A strengthening of this current would
cause the isotherms to adjust to the effects of in-
creased cold advection and local heat exchange
processes southward of their normal positions,
creating a negative anomaly. Correspondingly,
the reduced northward transjiort would decrease
warm advection into the Gulf of Alaska and
the isotherms would adjust to equilibrium po-
sitions farther south than normal, also creating
a cold anomaly.

If the northward deflection in the foregoing
example is replaced by a southward deflection,
then, after passing the southern bend or trough
of the wave, the water would approach the
coast with a northward component, favoring
more transport into the Gulf of Alaska. The
balance between advection and local heat ex-
change would be established with the isotherms
north of their normal positions, creating a warm
anomalv.

353

FISHERY BULLETIN; VOL. 69, NO. 2

In a comprehensive treatment of oceanograph-
ic survey data taken in 1955-58, Tully, Dodimead,
and Tabata (1960) found the warm coastal
anomaly of 1957-58 to be associated with in-
creasing transport into the Alaska Gyre. They
describe this condition in terms of a south-
ward shift of the point of separation of flow
from the West Wind Drift. From their study
of the djTiamic topography, they inferred that
prior to the shift, in 1955 and 1956, most of the
water approaching the coast south of lat 45° N
entered the California Current. The fact that
negative anomalies prevailed along the coastal
zone in the latter half of 1955 and, to a lesser
extent, in 1956 suggests that the point of sep-
aration in this period was farther north than
usual.

Whether the partition of the West Wind Drift
is influenced by upstream perturbations in the
zonal flow structure cannot be established with
certainty from the available survey data. The
geopotential topography as presented by Dodi-
mead, Favorite, and Hirano (1963) for the years
1955-59 does not reveal conclusive evidence of
upstream wave structure. The physical evi-
dence is limited to the anomalous characteristics
of the surface temperature field which have al-
ready been discussed.

Some added perspective might be gained by
looking briefly at the dynamic constraints ap-
plicable to a standing wave in the West Wind
Drift. The average eastward current speed, U,
for a wave of length L and lateral (north-south)
extent D is given by Panofsky (1956) as fol-
lows:

U — C =

2ncos<^L=
477-- £•

ll + L'/D^

This expression reduces to the Rossby wave
equation for a uniform zonal stream on a ro-
tating planet when the value of D approaches
infinity.

In order to evaluate the right side of the above
equation, we will assume dimensional similarity
between the inferred wave and areas enclosed
by the plus or minus 1° C anomaly contours for
those cases where we presume a causal relation
with the current structure. Estimates of the
wave length L and of the ratio L/D were de-
termined from rough measurements of the lon-
gitudinal and lateral extent of the warm cell
pre.sent from October 1961 to September 1962.
Excluding two extreme cases (April and July
1962) the longitudinal dimensions of the warm
cell ranged between about 800 (March 1962)
and 1600 (January 1962) nautical miles. The
corresponding ratios of longitudinal to lateral
extent for these particular cases were 1.3 and
2.0 respectively. Substitution of these values
for L and L/D in the wave equation yields 35
and 85 cm/sec (approximately) for average cur-
rent speed through a stationary wave. Of
course, the areas enclosed by the 1° C anomaly
contours presumably define only a portion of
the hypothetical wave, and to substitute the di-
mensions of these areas for L and D would
understate the theoretical current speed.

Current speeds in the West Wind Drift, com-
puted from dynamic height anomalies, are gen-
erally less than 10 cm sec (Dodimead et al,
1963). Data from drift bottles (Dodimead and
Hollister, 1962) indicate current speeds up to
20 cm sec in the same region. Thus, the theo-
retically computed results are too high, but con-
sidering the approximations used they are not
altogether unreasonable.

where C is the wave speed (zero for a standing
wave)

<\> is the mean latitude

n is the angular velocity of the earth
(7.292 X 10-^ sec-')

E is the radius of the earth
(6.37 X 10« m).

LITERATURE CITED

Dodimead, A. J., and H. J. Hollister.

1962. Canadian drift bottle releases and recoveries
in the North Pacific Ocean. Fish. Res. Bd. Can.,
Manuscr. Rep. Ser. (Oceanogr. Limnol.) 141, 64 p.
(Processed.)

Dodimead, A. J., F. Favorite, and T. Hirano.

1963. .Salmon of the North Pacific Ocean. Part II.
Review of oceanography of the Subarctic Pacific
region. Int. N. Pac. Fish. Comm., Bull. 13, 195 p.

354

EBER: SEA-SURFACE TEMPERATURE ANOMALIES

Eber, L. E., J. F. T. Saur, and 0. E. Sette. Tully, J. P., A. J. Dodimead, and S. Tabata.

19C8. Monthly mean charts, sea surface temper- 1960. An anomalous increase of temperature in

ature. North Pacific Ocean, 1949-62. U.S. Fish the ocean off the Pacific coast of Canada through

Wildl. Serv., Circ. 258, vi p., [168 charts]. 1957 and 1958. J. Fish. Res. Bd. Can. 17: 61-80.

Panofsky, H. Tully, J. P.

1956. Introduction to dynamic meteorology. Penn- 1964. Oceanographic regions and processes in the

sylvania State Univ., University Park, 243 p. seasonal zone of the North Pacific Ocean. In

K. Yoshida (editor). Studies on oceanography,
p. 68-84. Univ. of Tokyo Press, Tokyo.

355

INDUCED SPAWNING OF THE NORTHERN ANCHOVY,

Engraulh mordax GIRARD

Roderick Leong^

ABSTRACT

Anchovies were induced to mature their gonads by an artificial photoperiod of 4 hr light and 20 hr dark-
ness at 15° C. Single injections of suspensions of salmon pituitary, carp pituitary, or a solution of human
chorionic gonadotropin (HCG) promoted increase in egg diameters but did not induce spawning. Two in-
jections, a first of HCG and the second 2 days later of either salmon pituitary or carp pituitary, in-
duced spawning. At each spawning 6,000 to 16,000 eggs were collected, and 257c to 80% of the eggs
hatched. Larvae grown from these eggs were morijhologically similar to those caught in the sea.

An investigation was started at the National
Marine Fisheries Service Fisher.v-Oceanography
Center, La Jolla, Cahf., in 1969, to examine
methods for spawning the northern anchovy,
Eng vaults mordax Girard, under controlled lab-
oratory conditions in order to supply eggs and
larvae for experimental studies. The strategy-
for spawning anchovies in captivity was to pro-
vide an environment in which the fish would
mature their gonads and subsequently to induce
spawning through hormone treatment. The role
of the environment and the use of hormone in-
jections for inducing spawning in other sijecies
of fish has been well documented by Pickford
and Atz (1957). This report describes a meth-
od for bringing the anchovy to ripeness and
the effectiveness of various hormone treatments
in inducing spawning. As far as is known this
was the first successful attempt to artificially
mature and spawn this pelagic fish in the lab-
oratory.

MATERIALS AND METHODS

Anchovies, averaging 90 mm in length, were
purchased from a San Diego bait dealer in
March of 1969, transported to the laboratory,
and held in circular plastic lined wading pools
4.6 m in diameter with 0.9 m of water. By
the beginning of the injection trials in August
of 1970, the fish had grown to an average length
of 125 mm, at which length half of the fish should

have been mature (Clark and Phillips, 1952).
The fish were subjected to a photoperiod of 4 hr
light (32 ft-c at the brightest spot on the surface
of the water) and 20 hr dark (1 ft-c) for 3
months prior to the trials. Observations in
the preceding year revealed that anchovies tend
to mature more readily under relatively pro-
longed dark conditions. The tanks were con-
stantly supplied with fresh seawater and the
temperature was maintained at 15° C (Lasker
and Vlymen, 1969). Much of the spawning of
anchovies in nature occurs at or near this tem-
perature (Ahlstrom, 1956). The fish were fed
twice a day. In the first feeding, given at the
beginning of the 4-hr light period, the fish were
fed 6% of their live body weight in rotating
daily rations of ground squid, ground anchovies,
and brine shrimp. In the second feeding, given
near the end of the light period, the fish were
fed l''r of their body weight in trout chow."
Under this light, temperature, and food regimen
approximately one-fourth of the fish developed
gonads which weighed more than 6Sf of their
body weight.

Three series of injection trials were conduct-
ed. In the first series the following dosages
and types of injections were tested: 2.5, 5.0, and
pituitary" pi'epared essentially by the method of
10.0 mg of salmon (Oncorhynchus tshaivyfscha)

' National Marine Fisheries Service Fishery-Ocean-
ography Center, La Jolla, Calif. 92037.

Manuscript received January 1971.

FISHERY BULLETIN: VOL. 69, NO. 2, 1971,

" Ralston Purina trout chow, size 2. Reference to
commercial products does not imply endorsement.

" Obtained through the courtesy of Dr. Irwin Haydock
and the California Department of Fish and Game, Nim-
bus Fish Hatchery, Rancho Cordova, Calif.

357

FISHERV BLXLETIN: VOL. 69, NO. 2

Haydock (1971), 2.5, 5.0, and 10.0 mg of com-
mercial carp pituitary,* 1.0, 2.5, and 5.0 mg of
deoxycorticosterone acetate (DOC A),' 1.0 mg of
luteinizing hormone (PLH) ," and 25, 50, and 100
international units (lU) of human chorionic
gonadotropin (HCG)." The ti-eatments were
given in single 0.1-ml injections using a carrier
of Holtfreter's solution (Emmel and Cowdry,
1964) in all cases except for DOCA where se-
same oil was used. The suspensions of pituitary
were prepared by triturating a weighed quantity
in a small tissue grinder with enough liquid to
form the proper concentration. The suspension
was then pipetted into a small serum bottle
where it could be withdrawn with an injection
syringe. The injections were administered in-
traperitoneally with a 24-gauge needle between
the pelvic fin and vent. Prior to injection the
fish were anesthetized in 50 liters of water
with 7 ppm quinaldine (Vrooman and Paloma,
1966).

Under each treatment 12 to 15 fish were in-
jected. The sex and level of ripeness of living
anchovies are difficult to distinguish and a por-
tion of the fish in these trials were immature.
Therefore it was necessary to inject this rel-
atively large number of fish to increase the
probability that some would be sufficiently de-
veloped to respond to hormone injections. In-
jected fish were placed in small holding tanks
1.2 X 1-2 m with 0.9 m of water. These tanks
had running seawater and the temperature was
also maintained at 15° C. Nets with 202-fj. mesh
were placed at the outflows of these tanks to
collect eggs in the event of spawning. If no
spawning occurred after 48 hr, the fish were
stripped and fertilization attempted by the dry
method (Davis, 1961). In this method the eggs
and sperm are expressed, mixed, and left to
stand in a dry container for 5 to 10 min before
being placed in water. It was noticed in all
trials that at least some males produced motile
sperm.

The fish were killed after stripping and

' Purchased from StoUer Fisheries, Spirit Lake, Iowa.

" DOCA and HCG purchased from Sigma Chemical
Co., St. Louis, Mo.

* PLH and PMS purchased from Calbiochem, Los
Angeles, Calif.

ovaries were removed from the females. Each
ovary was teased apart and the major dia-
meters of the most advanced eggs measured.
The maximum diameters of injected fish were
compared with the diameters of more than 500
captive uninjected females sampled during the
previous 16 months to determine which of the
treatments were efl^'ective in producing growth.

The eff'ect of two injections of different hor-
mones were examined in the second series of
trials. The first injection was 50 lU of HCG
and the second, given 48 hr later, was one of the
following: 2.5 mg of salmon pituitary, 10.0
mg of carp pituitary, 5.0 mg of DOCA, 1.0 mg
of PLH and 250 lU of gonadotropin from preg-
nant mare serum (PMS).° The methods of
anesthetizing, injecting, and holding of fish were
the same. If spawning did not occur within
48 hr after the second injection, the fish were
stripped and fertilization attempted. In this
and the final series of trials the fish were not
killed after stripping and measurements of egg
diameters were not made. Here the only cri-
terion for success was spawning or production
of viable eggs through stripping.

The eff'ect of three injections of the same
hormone was tested in the third and final series
of trials. One group of fish was given three
injections of 2.5 mg of salmon pituitary and
another group three injections of 50 lU of HCG.
The injections were spaced a day apart and the
procedures were the same as described earlier.
If no spawning occurred within 24 hr after the
third injection, the fish were stripped and fertil-
ization attempted.

RESULTS

None of the fish that were given a single
injection spawned or produced viable eggs
through stripping. Most of the stripped eggs
were clumped, opaque, and apparently had not
ovulated. Some of the treatment, however, pro-
duced noticeable increases in egg diameters.
Table 1 shows the number of females under
the various single-injection treatments and the
number with and without eggs larger than 1.0
mm. The number of females was small in some

358

LEONG: INDUCED SPAWNING OF ANCHOVY

Table 1. — Female anchovies after various hormone in-
jections having eggs larger than 1.0 mm in diameter.
The occurrence of females with eggs larger than 1.0 mm
is considered to be an indication of induced egg matur-
ation. Of more than 500 captive uninjected fish sampled
during the previous 16 months none had eggs larger than
1.0 mm. The average injected fish weighed about 25.0 g
and measured 125 mm in length.

Type of injection

Dose/fish

No. females
injected

No. females
with eggs
>I.O mm

Salmon pituitary

(Oncorhynckui

tshawytichaj

2.5 mg
5.0 mg
10.0 mg

8

7
8

2

4
1

Commercial carp
pituitary

2,5 mg
5.0 mg
10.0 mg

5
3

4

0
0

1

Humon chorionic
gonadotropin (HCG)

25 lU
50 lU
100 lU

4
8
6

1
1
0

Deoxycorticosterone
acetate (DOCA)

I.O mg
2.5 mg
5.0 mg

3
5
8

0
0
0

Luteinizing hormone

(PLH)

1.0 mg

4

0

cases because most of the injected fish were
males or had died through handling. Of the
more than 500 females examined during the
previous 16 months, none had eggs larger than
1.0 mm. The occurrence of females, Table 1,
with eggs larger than 1.0 mm indicates that
salmon pituitary, carp pituitary, and HCG are
capable of promoting overnight growth of eggs.
Salmon pituitary appeared to be the most po-
tent for producing growth. The largest eggs
observed were over 1.3 mm in diameter and
within the size range, 1.23 to 1.5 mm, of na-
turally spawned eggs (Bolin, 1936). DOCA
and PLH at the dosages tested were not effec-
tive in stimulating egg growth- The prepon-
derance of fish with smaller eggs may be due to
a low state of ovarian development at the time
of injection.

In the second series of trials, HCG followed by
DOCA, PLH, or PMS did not induce spawning
and subsequent stripping produced only unovu-
lated eggs which were not successfully fertilized.
The combinations of HCG followed by salmon
pituitary and HCG followed by carp pituitary
induced spawning within 18 hr after the second
injection. The fish spawned and fertilized the
eggs themselves and large numbers of eggs were

caught in the nets at the outflows of the tanks.
Spawning was repeated several times with each
of these two combinations of injections. The
spawnings produced from 6,000 to 16,000 eggs
with the percentage hatching varying from 25
to 80 '^r. The larvae from the.se induced spawn-
ings appeared morphologically normal and many
were reared past 25 days by the methods of
Lasker et al. (1970). The differences in the
hatching percentage mqy be attributed to var-
iation in the state of gonad development of
parent fish at the time of injections.

The number of eggs collected suggests that
only one or two females from any of the spawn-
ing groups contributed eggs. According to es-
timates by MacGregor (1968) female anchovies
spawn almost 600 eggs per gram of fish. The
average female in these trials weighed approx-
imately 25 g and should have produced nearly
15,000 eggs. Only one or two females from any
of the twice-injected groups extruded ovulated
eggs upon stripping. Although the eggs were
translucent and measured about 1.5 mm in di-
ameter less than 10 Cr hatched after being mixed
with motile sperm.

In the final series of trials, three injections
of salmon pituitary or three injections of HCG
over a 3-day period failed to induce spawning.
The stripped eggs were opaque and fertilization
was not successful. These limited results sug-
gest that the combination of HCG followed by
salmon pituitary is more eflfective for induction
of spawning than when these hormones are
administered alone.

The results of these injection trials demon-
strate that the northern anchovy can be induced
to spawn in captivity and two eff'ective treat-
ments are HCG followed by salmon pituitary or
HCG followed by carp pituitary after gonads
are matured by a specific light-dark treatment
of the fish. The induction of spawning of an-
chovies in the laboratory provides a practical
way for supplying viable eggs for studies on
larvae. In this study the time of spawning
was controlled and eggs can probably be pro-
duced the year around if a large stock of fish
is maintained. This was emphasized by the
fact that the fish in this study were induced to

359

FISHERY' BULLETIN: VOL. 69, NO- 2

spawn during the late summer and fall months
when anchovy eggs are virtually absent from
the sea off San Diego. As far as is known,
these are the first reported spawnings of En-
graulis mordax in captivity and the first hor-
mone-induced spawnings of engraulids.

LITERATURE CITED

Ahlstrom, E. H.

1956. Eggs and larvae of anchovy, jack mackerel,
and Pacific mackerel. Calif. Coop. Oceanic Fish.
Invest., Progr. Rep. 1 Apr. 195.5 - 30 June 1956,
p. 3:3-42.
BOLIN, R. L.

1936. Embryonic and early larval stages of the
California anchovy, Engranlis mordax Girard.
Calif. Fish Game 22: 314-321.
Clark, F. N., and J. B. Phillips.

1952. The northern anchovy {Engraulis mordax
mordax) in the California fishery. Calif. Fish
Game 38: 189-207.
Davis, H. S.

1961. Culture and diseases of game fishes. Univ.
of Calif. Pre.ss, Berkeley, 332 p.

Em.mel, V. M., AND E. V. COWDRV.

1964. Laboratory technique in biology and medi-
cine. 4th ed. Williams & Wilkins, Baltimore,
453 p.
Haydock, I.

1971. Gonad maturation and hormone-induced
spawning of the gulf croaker, Bairdlella icistia.
Fish. Bull. 69: 157-180.
Lasker, R., H. M. Feder, G. H. Theilacker, and R. C.
May.

1970. Feeding, growth, and survival of Eiigriiiilis
mordax larvae reared in the laboratory. Mar.
Biol. 5: 345-353.
Lasker, R., and L. L. Vly.me.v.

1969. Experimental sea-water aquarium. Bureau
of Commercial Fisheries Fishery-Oceanography
Center, La JoUa, California. U.S. Fish Wildl.
Serv., Circ. 334, 14 p.
MacGregor, J. S.

1968. Fecundity of the northern anchovy, Enrjrau-
lis mordax Girard. Calif. Fish Game 54: 281-288.
Pickford, G. E., and J. W. Atz.

1957. The physiology of the pituitary gland of
fishes. New York Zoological Society, New York,
613 p.
Vrooman, a. M., and p. a. Paloma.

1966. Experimental tagging of the northern an-
chovy, Engraulis mordax. Calif. Fish Game 52:
228-239.

360

GILL RAKER APPARATUS AND FOOD SELECTIVITY AMONG
MACKERELS, TUNAS, AND DOLPHINS

John J. Magnuson and Jean G. Heitz'

ABSTRACT

Gill raker morphology and fork length wei-e measured from 411 fish, representing eight species of scom-
brids and two species of coryphaenids (dolphin). For each species linear regressions passing through
the origin were determined relating mean gill raker gap in millimeters (first gill arch) with fork length
in centimeters (/), and log filtering area (first gill arch) with log fork length. Mean gill raker gaps
equaled: Avxis rochei — 0.0144/, Katsuwonus pelamis — 0.0211/, Aiixis thazard — 0.0213/, Thunnus alba-
cares — 0.0344/, Thunnus alahmga — 0.0365/, Eidhynnus affiuis — 0.0386/, Thunnus obesus — 0.0391/, Sarda
chiliensis — 0.0509/, Coryphaena hippurus — 0.0650/, Coryphaena equisetis — 0.0655/, and Acanthocybium
solanderi — no gill rakers. Among the species gill raker gap was directly proportional to the number
of gill rakers, but no relation occurred between mean gap and filtering areas. Gill raker gap differed
markedly among species and lengths of fish. A 50-cm A', pelamis, a 30-cm T. albacares, and a 10-cm Sarda
orientalis all had an estimated mean gap of 1 mm. Conversely the gaps of a 50-cm fish of each species
were estimated to be ca. 1.0, 1.7, and 4.5 mm respectively.

Mean gill raker gaps from this study were compared with the percentage of crustaceans in stomachs
of Central Pacific fishes based on literature records. Body sizes of fishes and squids in the stomachs were
larger than crustaceans. Percent volumes that crustaceans contributed to the stomach content were
inversely related to mean gaps (Kendall rank correlation coefl5cient, t = —0.59, n = 16, P<0.001).
Partial correlation indicated that gap was more important than fork length in predicting the quantity
of crustaceans. Thus, the gill raker gap was related functionally with the quantity of smaller orga-
nisms in the stomachs. Presence of euphausids in stomachs of K. pelamis and their absence in T. alba-
cares from the eastern tropical Pacific may result from the small size of euphausids and the smaller
gill raker gaps of K. pelamis relative to T. albacares. Gill raker gap and the maximum distensi-
bility of the esophagus would set physical limits on the size of food eaten. The diverse fauna assem-
blage of crustaceans, fishes, and squids within this size range has masked to a great extent the selective
feeding that does occur among scombrids and coryphaenids on the basis of food size.

Most scombrid fishes have a varied diet that
includes numerous crustaceans, cephalopod mol-
luscs, and fishes. The Indian mackerel, Rastrel-
Uger kanagurta (Cuvier), even eat phytoplank-
ton (Bhimachar and George, 1952). The high
diversity of organisms in their stomach contents
has generated the opinion that scombrids are
nonselective feeders, preying upon anything
they encounter. CoryiDhaenid fishes, dolphins,
eat fish predominantly.

Yet selectivity does exist in food habits of
scombrids. Within a species, larger fish contain
relatively fewer cru.staceans and more fishes.
Crustaceans constituted 44 5r of the stomach vol-
ume of skipjack tuna, Katsuwonus pelamis (Lin-

' Laboratory of Limnology, Department of Zoology,
University of Wisconsin, Madison, Wis. 53706.

Manuscript received January 1971.

FISHERY BULLETIN: VOL. 69, NO. 2, 1971.

naeus), shorter than 50-cm fork length but only
1.5% of the volume for fish longer than 60 cm
(Yuen, 1959). Similarly, crustaceans consti-
tuted 35% of the stomach volume of yellowfin
tuna, Thunnus albacares (Bonnaterre), shorter
than 130 cm but only 1% for those longer than
130 cm (Reintjes and King, 1953). Reintjes
and King suggested that these differences might
result, as the fish grew, from a change in food
preference or a change in the ability to search
out and capture larger, more mobile prey (fish-
es) . Another considei'ation, in our view, is that
larger predators have a reduced ability to catch
small prey (crustaceans).

Prevention of food loss through the opercular
gap is generally recognized as the primary func-
tion of gill rakers. Species with more closely

361

spaced gill rakers are more likely to feed on
plankton than those with more widely spaced
rakers (Suyehiro, 1942; Yasuda, 1960a; Brooks
and Dodson, 1965; Kliewer, 1970).

This paper (1) quantitatively describes the
gill raker apparatus of certain scombrids and
coryphaenids with respect to the gap between
gill rakers and the filtering area of the first gill
arch, (2) compares differences in gill raker gap
among species and lengths of fish, and (3) con-
siders the proposition that observed inter- and
intraspecific variations in the diet are associated
functionally with the morphometries of the gill
raker apparatus.

MORPHOMETRY OF GILL RAKER
APPARATUS

Gill raker morphometry and fork length were
measured from 411 fish, representing eight spe-
cies of scombrids and two species of coryphae-
nids. Albacore, Thunniis alalunc/a (Bonna-
terre), were fi'om the commercial longline
fishery operated from American Samoa, the
Pacific bonito, Sarda chiliensis (Cuvier), were
from waters off Palos Verdes, Calif., and chub
mackerel. Scomber japonk.iui Houttuyn, were
from the Honolulu fish market. All other spe-
cimens were from Hawaiian waters and were
caught with pole and line or longline by com-
mercial fishermen or on numerous cruises of
the research vessel Charles H. Gilbert of the
Bureau of Commercial Fisheries Biological Lab-
oratory, Honolulu (now National Marine Fish-
eries Service Hawaii Area Fishery Research
Center) .

Measurements were from the first right gill
arch of fresh or thawed specimens. The arch
was removed from the fish and extended by pull-
ing the upper and lower branches apart until
the rakers were stiffly erect. Gaps between ad-
jacent rakers (Figure 1) were measured at the
base of the rakers by expanding a vernier cal-
iper until the two gill rakers began to spread
apart. Arch length and gill raker length were
also measured with the caliper (Figure 1). De-
pending on the species, six to nine gaps and six
to eight gill raker lengths spaced along the arch

FISHERY BULLETIN: VOL. 69, NO. 2

-LENGTH OF GILL RAKER

GILL RAKER GAP

LENGTH j/^s
UPPER ' ■
ARCH

FiGlTRE 1. — Diagram of the first right gill arch of a
scombrid as viewed from oral chamber showing the
morphometric measurements. Numbers indicate par-
ticular rakers.

were obtained from scombrids and three gaps
and five gill raker lengths from coryphaenids.
Mean gap was the average of those measured
along the arch. A gap near the middle of the
lower arch was also used to represent gap width
in the primary filtering area. Filtering area
was calculated from average length of gill rakers
and length of the arch. Lower and upper arch
filtering areas were computed separately and
summed.

DESCRIPTION

Gill rakers of the first arch of most scombrids
were conspicuous and well developed. Inner
edges of the rakers of most species were covered
with numerous short, spiny protuberances. For
S. japoniciis, these spines were thin, about as
long as the gill raker gap, and evenly spaced to
form a finer sieve between adjacent gill rakers.
The other three arches of scombrids lacked gill
rakers, but smaller rakerlike processes on the
inner faces of the all arches projected posteri-
orly to the adjacent arch forming a sieve. Inner
edges of these processes had short, «piny pro-
tuberances similar to the gill rakers.

Rakers were articulated so that they became
stiffly erect forming a parallel row of blade-
shaped rakers when the acute angle between the
upper and lower arch was expanded toward 90
degrees. In the branchial chamber the tips of
the rakers extended to the inner surface of the
flared gill cover.

The wahoo, Acanthocybinm solanderi (Cuv-
ier) , has no gill rakers, but most scombrids have
more than 20 elongated rakers — K. pelamis in

362

MAGNUSON and HEITZ: GILL RAKER APPARATUS

our samples had 53 to 64. Longest rakers were
near the joint between the upper and lower
branches of the arch. They became progres-
sively shorter toward the ends of the arch. For
example, a K. pelamis 50 cm long had gill rakers
21 mm long at the joint but only 2 and 8 mm
at the ends of the upper and lower branches,
respectively. The largest gap (1.8 mm) was
near the center of the lower branch. Gaps were
smaller on the upper branch than lower branch
and were most narrow at the ends of the arch
(0.2 mm and 0.9 mm for the upper and lower
branches). Often the gap between the first
raker of the upper and the first raker of lower

arch was as great as the widest gap on the lower
arch.

Most of the filtering area of scombrids was
confined to the lower branch of the gill arch.
The lower branch comprised 73 to 80 '^f of the
total. The filtering area of coryphaenids was
essentially restricted to the lower arch. Dol-
phin, Coryphaena hippurus Linnaeus, had no
rakers on the upper arch, pompano dolphin,
Coryphaena eqnlsetis Linnaeus, had only one.

Gill rakers of the two coryphaenids were
shorter and more uniform in length than those
of scombrids. The longest gill raker from a
55-cm C. equisetis was only 9 mm contrasted

E
E

a.

<

a:
lij

<

z
<

UJ

Katsuwonus pelamis

y=0.034x

"T 1 1 1 1 1 1 1 1 1 1 1 1 1 1 r

Euthynnus offlnls

-y = 0.038x

Thunnus alalunga

1 1 1 1 r 1 1 r r-

0 50 100 0

FORK LENGTH (cm)

1 1 — I — I — I — I — I — I — I — I — 1 — I — I —

50 100 150

FORK LENGTH (cm)

Figure 2. — Relation between mean gill raker gap and fork length showing the advantage of using
regression through the origin for predicting mean gill raker gap especially when sample sizes are
small and restricted in length range.

363

FISHERY BULLETIN: VOL. 69. NO. 2

to 21 mm from a 50-cm K. pelamis. Even the
longest raker of a 125-cm C. hippuriis was only
16 mm — shorter than that of a 50-cm K. pelamis.

SIZE AND SPECIES COMPARISONS

METHODS

Linear regressions relating gill I'aker gap to
fork length and log filtering area to log fork
length were computed for each species. Re-
gressions were computed once about the mean,
and a second time, were forced to pass through
the origin. The latter procedure was used be-
cause the ranges of fork lengths of some species
were not sufficient to obtain reasonable equations
(Figure 2).

Both K. pelamis and T. albacares were rep-
resented by large samples that included small
and large specimens. Their regressions of gill
raker gap on foi-k length passed close to the
origin even when not forced to do so; the y-in-
tercept was 0.00 mm for K. pelamis and 0.19 mm
for T. albacares (Figure 2) . In contrast, kawa-
kawa, Eiithynnus af finis (Cantor), and T. ala-
lunga were represented by small samples that
did not include small specimens. Regressions

extrapolate outside the size ranges represented
in our samples, the regressions forced to pass
through the origin were used for all computa-
tions of gill raker gap.

The same reasoning was used for the relations
between log filtering area and log fork length.
In this case, the zero-zero intercept was equi-
valent to 1 cm fork length and 1 mm- filtering
area rather than zero fork length and zero filter-
ing area. Since most comparisons made later
were for fish at least 35 cm long with filtering
areas near 100 mm', errors owing to the posi-
tion of the intercept were believed negligible.

SIZE AND SPECIES COMPARISONS

Linear regressions passing through the origin
that relate gill raker gaj) to fork length and log
filtering area to log fork length are presented
in Table 1 along with the numbers and lengths
of fishes measured.

Mean gill raker gap increased with fork length
and was equal to 1.4 and 6.6 '"r of fork length
for frigate mackerel, Auxis rochei (Risso), and
C. hippuriis, respectively. Gill raker gap in the
middle of the lower branch was usually 1.0 to
1.2 times the mean gill raker gap except for

Table !.■ — Linear regressions passing through the origin that relate mean gill raker gap to forl< length and log
filtering area to log fork length and the number and length of fish measured.

Species

Number

of (ish

measured

Regressions
of gap (G)
and fork
length (/)

Fork length

Mean
(cm)

Range
(cm)

G

(mm)

Standard

error of

estimate

for G

(mm)

Regressions of log

filtering area (log A)

and log fork

length (log /)

Log /
(cm)

Log A
(mm-)

Standard

error of

estimate

for Log A

(mm-)

Sarda chiluniii

8

C

= 0.0509 /

50.13

38.7- 58.8

2.56

0.27

log A

=

1.73 (log I)

1.7001

2.924«

0.0584

Auxis thazard

16

G

= 0.0213 ;

31.40

25.1- 35.7

0.67

0.10

log A

=

1.79 (log /)

1.4969

2.6730

0.0393

Auxil rochei

11

G

= 0.0144 /

30.24

29.2- 32.9

0.44

0.06

log A

=

1.78 (log ;i

1 .4706

2.6291

0.0192

EuthvTtnuj affinij

25

G

= 0-0386 /

36.29

33.4- 54.6

1.41

0.29

log A

=

1.82 (log /)

1 .5598

2.8421

0.0234

Katjuwonul pelamis

63

G

= 0.0211 ;

47.60

21.0- 67.5

1.00

0.10

log A

=

1.83 (log /)

1.6776

3.0135

0.0697

Tkunnus alalunga

12

G

= 0.0365 /

98.56

84.0-118.8

3.59

0.25

log A

=

1.81 (log /)

1 .9937

3.6088

0.0343

Tkunnus albacares

74

C

= 0.0344 /

94.86

27.1-166.9

3.31

0.36

log A

=

1.78 (log /)

1.9771

3.3468

0.0405

Tkunnus obesus

82

C

= 0.0391 /

132.96

75.2-175.3

5.26

0.60

log A

=

1.85 (log /)

2.1236

3.9058

0.0449

Coryphaena equisetis

38

C

= 0.0655 ;

94.90

30.8- 58.7

6.16

0.54

log A

=

1.39 (log /)

1 .9773

2.7339

0.0704

Coryphaena hippurus

68

C

= 0.0650 /

40.52

63.2-126.4

2.69

0.34

log A

=

1.36 (log /)

1.6077

2.1716

0.0727

of gill raker gap on fork length for these two
species did not closely approach the origin (Fig-
ure 2) ; we believe these equations would also
have had ^/-intercepts near 0.0 mm if lengths
of our specimens had been more evenly distrib-
uted. Since some comparisons were made that

A. rochei (1.3) and K. pelamis (1.4). Mean
gap increased in direct proportion to fish length;
i.e., if length doubled, gap also doubled.

Filtering area increased as the 1.4 to 1.8 pow-
er of fork length. When these regressions were
not forced to pass through the origin, the filter-

364

MAGNUSON and HEITZ : GILL RAKER APPARATUS

ing area increased as the 2.2 i^ower of fork length
for A', pelamis and the 1.9 power for T. alba-
cares. Forcing the regressions to pass thi'ough
the origin may have decreased the slope.

To facihtate comparison of different species,
the mean gap and filtering area were cominited
from the regression in Table 1 for fish with a
fork length of 35 cm. These are listed in Table 2
in order of decreasing number of gill rakers,
increasing gap, and decreasing filtering area.

As expected, the number of rakers and gill
raker gap were closely related (Table 2). Lack
of comjilete correspondence may have resulted
from differences in the thickness of gill rakers,
differences in the length of the gill arch, or both.

Among scombrids no relation was evident be-
tween filtering area and number of rakers or
between filtering area and mean gill raker gap
(Table 2) . Apparently, the length of raker was
an important variable determining differences

Table 2. — Scombrid and coryphaenid species (35-cm fork length) listed in order of increasing numbers of gill rakers,

and decreasing mean gill raker gap and filtering area.
(Data on S. orientalis from one fish, S. japovicus from two fish.)

Rank

Mean

number of

rokers

(»)

Species

Mean gill
raker
gap
(mm)

Species

Filtering
area
(mm-)

Species

12

8

Corypharna ftippurus

3.3

Sarda orientalis

Scomber japoniius

n

10

Corypkaena equisetij

2-3+

Coryphaena egutsetts

685

Thunnus obesus

10

11

Sarda oruntaUl

2.3-

Coryphatna hippurus

650

Euthynnus affinis

9

25

Sarda chiliensii

1.8

Sarda chiUemif

620

Thunnus alalunga

8

26

Tftunnuj obeiui

1.4

Thunnus obesus

530

Katsuwonus pelamis

7

29

Tkunnus alalunga

1.4

Euthynnus affinis

570

Auxis thazard

6

30

Thunnu! albacares

Scomber japonicui

550

Auxis Tockei

S

31

Eiithynnus affinis

1.3

Thunnus alalunga

450

Sarda chiliensis

4

37

Scomber japonicui

1,8

Thunnuj albacares

41C

Thunnus albacares

3

40

Auxis (hazard

0.74

.4uxis (hazard

Sarda orientalis

2

45

Auxis rochet

0.74

Katsuwonus pelamis

135

Coryphaena hippurus

1

58

Katsuwonul pelamis

0.51

Auxis Tochex

120

Coryphaena equisetis

100
FORK LENGTH

Figure 3. — Comparison of the mean gill raker gap and
fork length relationship for various scombrid and cory-
phaenid fishes. Lengths shown approximate ranges
known for each species.

in filtering area among species. Coryphaenids
had a larger gill raker gap and smaller filtering
area than any scombrid except striped bonito,
Sarda orientalis (Temminck and Schlegel).

Among scombrids 35 cm long, Sarda had the
largest gaps (1.8-3.3 mm) and Auxis and Katsu-
■ivoniis the smallest (0.51-0.74 mm). Thunmis,
Euthynnus, and Scomber had intermediate gap
widths (1.2-1.4 mm). Among Sarda, Auxis, and
Thunnus represented in our samples, species
within genera had more similar gill raker gaps
than those in different genera. On this basis
alone food habits for fish of the same length
would be expected to be more similar within
genera than among genera.

Mean gill raker gap differed markedly with
species and length of fish (Figure 3). For ex-
ample, a 50-cm K. pelamis, a 30-cm T. albacares,
and a 10-cm S. orientalis all had a mean gill raker
gap of approximately 1 mm. Conversely, gill
raker gaps of these three species differed mark-
edly at the same fork length. Gaps of 50-cm K.
pelamis, T. albacares, and S. orientalis were ca.

365

FISHERY BITLETIN: VOL. 69, NO. 2

Table 3. — The average size of individual crustaceans, squids, and fishes in the stomachs of scombrids from the

central Pacific.

Species

Volume of individual organisms (ml)

Squids

Fishe

Volume

of food

analyzed

(mi)

Source

Thunnut albacareS
Thunnus obesus
Tkunnus albacares
Katsuwonus pelamxs
Mean (unweighted)

03

4.8

6.4

44,680

King & Ikehara (1956)

0.6

9.5

8.2

22.297

King & Ikehara (1956)

0.2

3.8

4.6

52,336

Reintjes & King (1953)

0.2

4.3

3.7

13,974

Waldron & King (1963)

0.3

5.6

5.7

1.0, 1.7, a.nd 4.5 mm, respectively. Selectivity
of the gill raker appai'atus would vary with gill
raker gap, a function of both species and length
of the fish. Thus, a small T. albacares and a
large K. pelamis should have more similar diets
than a small and a large T. albacares. Any
number of such predictions can be generated
from Figure 3. A fish with smaller mean gap,
regardless of its species or length, would be
expected to be more planktivorous.

RELATION BETWEEN GILL RAKER
GAP AND DIET

Stomach-content data from published liter-
ature from the central Pacific were compared
with the mean gill raker gaps reported here to
test the hypothesis that fish with a finer gill
raker gap have a greater proportion of smaller
organisms (crustaceans) in their diet.

Crustaceans in the diet of scombrids from
the central Pacific were smaller than were the
other major food organisms (squids and fishes)
(Table 3). The volume of individual, partially
digested crustaceans in the stomachs of five spe-
cies averaged 0.3 ml whereas individual, partially
digested squids and fishes averaged 5.6 and 5.7
ml, respectively. The much smaller body size
of the crustaceans was not likely the result of
diflferential digestion, especially since the exo-
skeleton of crustaceans, if anything, might be
expected to slow, rather than accelerate, diges-
tion (Pandian, 1967).

For comparison with gill raker data, the per-
cent volumes of the stomach content comprised
by crustaceans, squids, or fishes are presented
in Table 4 for five scombrids and one coryphae-
nid. Only stomach data from the central Pa-
cific were used because difl'erences in typical
body size of crustaceans in scombrid stomachs
from other regions would have invalidated these

Table 4. — Food of scombrid and coryphaenid fishes from the central Pacific divided into the percentages of the
stomach volume that were crustaceans, squids, or fishes. The median fork length of fishes in the sample is also
given along with the literature source for the data.

Species

Stomach content
{percent volume)

Crusta-
ceans

Squids

Fork length

Median
("n)

Range
(cm)

Number

of
stomachs

Literature source

Acanthoeybium solanderi
Aeanthocybium iolanderi
Euthynnus affinis
Katsuwonus pelamxs
Katsuwonus petamis
Katsuwonus pelamis
Katsuwonus pelamxs
Katsuwonus pelamis
Katsuwonus pelamis
Thunnut albacares
Thunnus albacares
Thunnus albacares
Thunnus albacares
Thunnus albacares
Thunnus obesus
Thunnus obesus
Coryphaena hippurus

0

0

100

111

104-123

3

Tester & Nakamura (1957)

0

__

__

54-198

235

Iversen & Yoshida (1957)

8

0

92

49

31-67

32

Tester & Nakamura (1957)

44

„

40

44

39-49

>25

Yuen (1959)

4.0

23

72

47

33^50

305

Waldron & King (1963)

67

7

26

50

40-61

67

Tester & Nakamura (1957)

25

70

55

50-60

>25

Yuen (1959)

3.7

19

74

73

60-89

254

Waldron & King (1963)

1.5

_..

91

73

62-84

>25

Yuen (1959)

45

14

33

80

53-100

544

Reintjes & King (1953)

39

9

49

115

100-130

205

Reintjes & King (1953)

1.7

29

6S

135

85-140

188

King & Ikehoro (1956)

3

4

93

140

130-168

26

Reintjes & King (1953)

0.8

30

60

148

140-175

251

King & Ikehara (1956)

2J

26

70

128

75-140

63

King & Ikehara (1956)

1.4

34

58

158

140-200

103

King & Ikehara (1956)

1.«

2

97

81

42-121

52

Tester & Nakamura (1957)

366

MAGNUSON and HEITZ: GILL RAKER APPARATUS

Table 5. — Percent crustaceans by volume in the stomachs, median fork length, mean gill raker gap, and species
of fish. (Ranks are from smallest to largest and ordered by the percentage of crustaceans in the stomachs.)

Species

Crustacea

Median
forl< length

Mean gill

raker gap

%

Rank

(cm)

1

Ronic

(mm)

Rank

Atanthocybium jolanderi

0

1

111

10

0

16

Thunnus alhacares

0.8

2

148

15

5.2

13

Thunnut obtiuj

1.4

3

158

16

6.3

15

Katsuti'onul pilamis

1.5

4

73

6

1,5

5

Coryphaentt hippurus

1.6

5

81

9

5.3

14

Thjinnuj albacarej

1.7

6

135

13

4.7

10

Thurtnu! obelus

2.3

7

128

12

5.1

12

Thunnu! albaiares

3

8

140

14

4.9

11

Katsuwonus pelamis

3.7

9

73

6

1.5

5

Katsuwonul pelamis

4.0

10

47

2

0.99

2

Eulhynnus aginis

8

11

49

3

1.9

7

Katsuwonus pelamis

25

12

55

5

1.2

4

Thunnus albacores

39

13

115

11

4.0

9

Thunnus albacares

44

14

80

8

2.8

8

Katsuwonus pelamis

45

15

44

1

0.92

1

Katsuwonus pelamis

67

16

50+

4

1.0

3

analyses. The galatheids and portunids domi-
nating the crustaceans found in T. albacares
stomachs in the eastern tropical Pacific (Alver-
son, 1963) are much larger (Longhurst, 1967;
Jerde, 1967b) than the tyijical crustaceans from
the stomachs of central Pacific scombrids given
in Table 3. Also, data were not used if fewer
than 25 stomachs had been examined. None of
the 238 A. solanderi contained crustaceans and
O'^f crustaceans in the stomach was considered
a reasonable estimate for any \&Yger A. solanderi.
The median or midrange fork length of fish
was determined for each set of stomach data.
Then mean gill raker gaps for fish of those spe-
cies and length were estimated with the regres-
sions from Table 1. Data on median fork length,
mean gill raker gap, and percent crustaceans
by volume in the stomach are presented in nu-
merical and ranked form in Table 5.

Percent volumes that crustaceans contributed
to the stomach content were inversely related
to mean gill raker gap (Figure 4a) (Kendall
rank correlation coefficient, r = — 0.59; n = 16;
P <0.001) and to fork length (Figure 4b)
(Kendall rank correlation coefficient, t = — 0.45;
n = 16; P <0.01). Several notable exceptions
occurred in the relation with fork length
(Table 5, Figure 4b). C. hippurus, 81 cm long,
contained 2% crustaceans while T. albacares,
80 cm long, contained 45 "^f crustaceans. T.
albacares, 135 cm long, also contained 2% crus-

taceans. Not unexpectedly, C. hippurus, 81 cm
long, and T. albacares, 135 cm long, both had
mean gill raker gaps near 5 mm whereas the
81-cm T. albacares had a smaller mean gill raker
gap near 3 mm. The somewhat closer corres-
pondence of percentage of crustaceans to gill
raker gap than to fork length can be observed
by comparing Figures 4a and 4b or by comparing
the associated probabilities of no correlation
(<.01 versus <.001).

Kendall partial rank correlation coefficients
were computed to determine the association be-
tween percent crustaceans in the stomach and
gill raker gap, with the effect of fork length
held constant. The partial correlation coefficient
between percent crustaceans and gap, indepen-
dent of variation in fork length, was — 0.43
while the partial correlation between percent
crustaceans and fork length independent of var-
iations in gap, was only — 0.05. Thus, although
fork length was correlated with the percent
crustaceans, this correlation resulted from the
association between gill raker gap and fork
length. Gill raker gap was the important var-
iable correlated to percent crustaceans in the
diet.

Data on percent crustaceans in the stomach
by volume were also presented for K. pelamis
and T. albacares of various size by Alverson
(1963) and for K. pelamis and blackfin tuna,
Thunnus atlanticus (Lesson), by Suarez Caabro

367

FISHERY BULLETIN: VOL. 69, NO. 2

z
<

z
<

UJ

u

<

3
K
u

UJ

o
a:

UJ
Q.

15-

•

•

•

A

10-

•

•

\

\

\

•

5-

•

0-

1

1 1

0 5 10 15

MEAN GILL RAKER GAP (RANKS)

15- •

10-

T 1 r

0 5 10 15

MEDIAN FORK LENGTH (RANKS)

Figure 4. — Relation between percentage crustaceans by
volume of diet (ranked) and the (a) mean gill raker
gap of a fish (ranked) and (b) fork length of fish
(ranked). The diagonal line depicts a perfect inverse
relationship.

and Duarte Bello (1961). These were not used
in the present analysis because sample sizes were
fewer than 25 fish or because the size of the
individual crustaceans was unavailable. Re-
gardless, larger A', pelamis in both studies con-
tained less crustaceans. However, larger T.
albacares in Alverson's study tended to eat more
crustaceans than did smaller specimens. This

may have been because the crustaceans in their
diet were relatively large.

Alverson's paper also presents a good example
of selectivity among crustaceans that may be
based on size of gill raker gaps. K. pelamis and
T. albacares from the same areas had markedly
different diets. Crustaceans contributing the
greatest volume to the stomachs were galatheids
and portunids for T. albacares but euphausids
for K. pelamis. Euphausids were rare in stom-
achs of T. albacares even when common in the
micronekton (Blackburn, 1968). Galatheids and
portunids (Longhurst, 1967; Jei'de, 1967b) are
typically larger in size than euphausids (Jerde,
1967a). The small euphausids were not impor-
tant in stomachs of T. albacares (i.e., 1% of
the volume) in any of the areas of the eastern
tropical Pacific studied by Alverson (1963),
but the larger galatheids and portunids were
important in the stomachs of K. pelamis from
certain areas. The above observations would
be the predictions from gill raker gaps — T. al-
bacares have broader gaps than K. pelamis and
would not be expected to capture the smaller
crustaceans.

The major hypothesis under investigation in
the present study was that the quantity of smal-
ler organisms (crustaceans) eaten should be re-
lated to the selectivity of the gill raker apparatus.
The above coi'relations on central Pacific data,
although only crude in nature, lend support to
this idea. A more definitive test would require
extensive data on the size of food organisms
and the diet of scombrids over more narrow
length ranges than are available from the pub-
lished literature.

Even though the structure of the gill raker
apparatus ultimately determines the smallest
size of prey, it is possible that actual selection
of fishes is made prior to ingestion (Ivlev, 1961;
Galbraith, 1967). Galbraith believed that the
gill rakers of yellow perch, Perca flavescens
(Mitchill), and rainbow trout, Salmo gairdrieri
Richardson, could have retained smaller zoo-
plankton than were typically found in their
stomachs. These species ate only larger Daph-
nia even though numerous smaller ones were
in the zooplankton.

368

MAGNUSON and HEITZ: GILL RAKER APPARATUS

Several authors have pointed out that fish
tend to select the largest food organisms avail-
able to them (Hayashi, 1956, as cited in Yasuda,
1960b; Ivlev, 1961; Brooks, 1968). The large
mouth of larval scombrids facilitates capture
of large copepods at first feeding and contributes
to their rapid early growth I'ates (Shirota, 1970) .
The responsiveness of at least one scombrid to
food is influenced by the size of the food or-
ganism— A', pelamis ate whole shrimp and squid
at the beginning of a feeding, but as they be-
came sated, they would only eat cut-up pieces
of smaller size (Nakamura, 1962). Feeding be-
havior of Atlantic mackerel, Scomber- scombnis
Linnaeus, (Sette, 19.50) and northern anchovy,
EngrauUs mordax Girard, (Leong and O'Connell,
1969) changes with the size of food. When small
food is present, they open the mouth wide and
flare the opercles in a filter feeding mode, but
with larger food they make individual biting
attacks. S. japonicus eats food smaller than
would be predicted by gill raker gap (Hiyama
and Yasuda, 1957). The spiny process we ob-
served on the rakers of S. japonicus probably
form an even finer sieve than is formed by the
rakers themselves. Regardless of the mode of
selection (anatomical, behavioral, or perceptu-
al), the selective capabilities of scombrids and
coryphaenids would appear to be correlated with
the anatomy of the gill raker apparatus.

An individual scombrid is able to prey on or-
ganisms differing greatly in size. It is capable
of engulfing and retaining crustaceans, small
fishes, and squid by means of a well-developed
gill raker apparatus. It is also capable of pur-
suing, capturing, and ingesting fast-moving
fishes and squids, provided they are not too large
to be swallowed whole. The gill raker gap and
maximum distensibility of the mouth and esoph-
agus then would be expected to set limits on the
range of food sizes eaten by scombrids. Within
this size i-ange a diverse faunal assemblage exists
in the sea that includes numerous species of
ci'ustaceans, fishes, and molluscs. The diversity
of species in the size range consumed by an in-
dividual scombrid has, to a great extent, masked
the selectivity that does occur. The present pa-
per provides some evidence for selection of or-

ganisms above a minimum size determined by
the magnitude of gill raker gaps.

ACKNOWLEDGMENTS

We thank Reginald Gooding for assistance
with collection of data, Marian Yong and Betty
Ann Keala for computer processing the data,
and William H. Neill and Dr. James F. Kitchell,
Laboratory of Limnology, Madison; Witold L.
Klawe, Inter-American Tropical Tuna Commis-
sion, and Dr. Maurice Blackburn, Scripps Insti-
tution of Oceanography, who critically reviewed
the manuscript. This project was supported
entirely by the Bureau of Commercial Fisheries
Biological Laboratory, Honolulu.

LITERATURE CITED

Alverson, F. G.

196.3. The food of yellowfin and skipjack tunas in
the Eastern Tropical Pacific Ocean. Inter-Amer.
Trop. Tuna Comm., Bull. 7: 293-.396.
Bhimachar, B. S., and p. C. George.

1953. Observations on the food and feeding of the
Indian mackerel, Rastrelliger canagurta (Cuvier).
Proc. Indian Acad. Sci., Sect. B 36: 105-118.
Blackburn, M.

1968. Micronekton of the eastern tropical Pacific
Ocean: family composition, distribution, abun-
dance, and relations to tuna. U.S. Fish Wildl.
Serv., Fish. Bull. 67: 71-115.
Brooks, J. L.

1968. The effects of prey size selection by lake
planktivores. Syst. Zool. 17: 272-291.
Brooks, J. L., and S. I. Dodson.

1965. Predation, body size, and composition of
plankton. Science (Washington) 150: 28-35.
Galbraith, M. G., Jr.

1967. Size-selective predation on Daphnia by rain-
bow trout and yellow perch. Trans. Amer. Fish.
Soc. 96: 1-10.
HrvAMA, Y., and F. Yasuda.

1957. The methods of utilization of plankton by
fishes. Rec. Oceanogr. Works Jap., Spec. No.
[1] March 1957: 67-70.

IVERSEN, E. S., AND H. O. YOSHIDA.

1957. Notes on the biology of the wahoo in the
Line Islands. Pac. Sci. 11: 370-379.
IVLEV, V. S.

1961. Experimental ecology of the feeding of fishes.
(Translated from the Russian by Douglas Scott.)
Yale Univ. Press, New Haven, 302 p.

369

FISHERY BULLETIN: VOL. 69, NO. 2

Jerde, C. W.

1967a. A comparison of euphausiid shrimp collec-
tions made with a micronekton net and a one-
meter plankton net. Pac. Sci. 21: 178-181.

1967b. On the distribution of Portunus (Achelous)
affiyiis and Eiiphijlax dovii (Decapoda Brachyura,
Portunidae) in the eastern tropical Pacific. Crus-
taceana 13: 11-22.
King, J. E., and I. I. Ikehara.

1956. Comparative study of food of bigeye and
yellowfin tuna in the central Pacific. U.S. Fish
Wildl. Serv., Fish Bull. 57: 61-85.
Kliewer, E. v.

1970. Gill raker variation and diet in lake white-
fish, Coregonus clupeafomiis, in northern Man-
itoba. In C. C. Lindsey and C. S. Woods (edi-
tors) , Biology of coregonid fishes, p. 147-165.
Univ. of Manitoba Press, Winnipeg.

LEONG, R. J. H., AND C. P. O'CONNELL.

1969. A laboratory study of particulate and filter
feeding of the northern anchovy (Engraulis mor-
dax). J. Fish. Res. Bd. Can. 26: 557-582.

LONGHLIRST, A. R.

1967. The pelagic phase of Pleuroncodes planipes
Stimpson (Crustacea, Galatheidae) in the Cal-
ifornia Current. Calif. Coop. Oceanic Fish. In-
vest., Rep. 11: 142-154.
Nakamura, E. L.

1962. Observations of the behavior of skipjack
tuna, Eidhynnus pelamis, in captivity. Copeia
1962: 499-505.
Pandian, T. J.

1967. Transformation of food in the fish Megalops
oyprinoides. I. Influence of quality of food. Mar.
Biol. 1: 60-64.
Reintjes, J. W., and J. E. King.

195.3. Food of yellowfin tuna in the central Pa-
cific. U.S. Fi.sh Wildl. Serv., Fish. Bull. 54: 91-
110.

Sette, O. E.

1950. Biology of the Atlantic mackerel (Scomber
scombrus) of North America, Part II — migra-
tions and habits. U.S. Fish Wildl. Serv., Fish
Bull. 51: 251-358.
Shirota, a.

1970. Studies on the mouth size of fish larvae.
[In Japanese, English abstract.] Bull. Jap. Soc.
Sci. Fish. 36: 353-368.

SUAREZ CAABRO, J. a., and P. P. DUARTE BELLO.

1961. Biologfa pesquera del bonito (Katsuwomis
petainis) y la albacora (Thunnus atlaytticns) en
Cuba. I. Inst. Cubano Invest. Tecnol. Ser. Estud.
Trab. Invest. 15, 150 p.
SUYEHIRO, Y.

1942. A study of the digestive system and feeding
habits of fish. Jap. J. Zool. 10: 1-303.
Tester, A. L., and E. L. Nakamura.

1957. Catch rate, size, sex, and food of tunas and
other pelagic fishes taken by trolling oflF Oahu,
Hawaii, 1951-55. U.S. Fish Wildl. Serv., Spec.
Sci. Rep. Fish. 250, 25 p.
Waldron, K. D., and J. E. King.

1963. Food of skipjack in the central Pacific. In
H. Rosa, Jr. (editor), Proceedings of the world
scientific meeting on the biology of tunas and
related species, p. 1431-1457. FAO (Food Agr.
Organ. U.N.) Fish. Rep. 6.
Yasuda, F.

1960a. The relationship of the gill structure and
food habits of some coastal fishes in Japan. Rec.
Oceanogr. Works Jap., New Ser. 5(2): 139-152.
1960b. The feeding mechanism in some carnivorous
fishes. Rec. Oceanogr. Works Jap., New Ser.
5(2): 153-160.
Yuen, H. S. H.

1959. Variability of skipjack response to live bait.
U.S. Fish Wildl. Serv., Fish. Bull. 60: 147-160.

370

NATURE OF FREE RADICALS IN FREEZE-DRIED FISHERY PRODUCTS
AND OTHER LIPID-PROTEIN SYSTEMS

William T. Roubal'

ABSTRACT

The electron paramagnetic resonance spectrometer makes it possible to detect and study radicals which
are produced during lipid peroxidation in freeze-dried lipid-protein systems. In such systems, two gen-
eral types of resonances are observed. By studying effects of added antioxidants, added autoxidizable
lipid, and type of substrate, it is possible to differentiate and characterize the two signals which are ob-
served. It is postulated that the immobilized radicals observed in dry systems are the same as those
that are responsible for damage at the molecular level in o.\ygenated lipid-protein-water emulsions,
stored meats of normal moisture content, and in antioxidant deficiency states in man and animals.

Fish from the sea are rich in polyunsaturated
fatty acids. Furthermore, when fish are pro-
cessed as a foodstuff, the unsaturated fatty acids
will, if unprotected, readily undergo lipid perox-
idation.

In the presence of proteins, enzymes, nucleo-
tides and other classes of biological materials,
lipid peroxidation is radiomimetic, that is, it
produces similar if not the same effects as ion-
izing radiation — a damage mechanism which is
known to be mostly free radical in nature. Ac-
cordingly, such materials as freeze-dried fish
tissue, dried fish meals, and protein concentrates
incompletely freed of residual unsaturation,
are all prone to undergo various deteriorative
changes as a consequence of lipid peroxidation.

Although much emphasis has been placed in
the past, and continues to be at present, on the
participation of radicals in events leading to
damage, radicals of the oxy or peroxy type have
not been directly characterized by electron para-
magnetic resonance (EPR) spectroscopy in liv-
ing systems or in emulsions for in these the
steady state concentration of radicals is univer-
sally low. Nevertheless, the EPR method re-
mains as the one method best suited for char-
acterizing radicals.

' National Marine Fisheries Service Pioneer Research
Laboratory, Seattle, Wash. 98102.

Manuscript received January 1971.

FISHERY BULLETIN: VOL, 69, NO 2, 1971.

This paper discusses recent research employ-
ing systems which, for the first time, are fa-
vorable for the detection and study of EPR
signals which arise with the onset of lipid oxi-
dation. Mechanisms for the formation of radi-
cals as well as reactions of radicals themselves
are discussed.

MATERIALS AND METHODS

Freeze-dried and isopropyl-extracted rockfish
myofiljrillar protein, and freeze-dried rockfish
sacroplasmic protein were provided by the
NMFS Technological Laboratory in Seattle. In
addition, a polyunsaturated fatty acid (PUFA)
concentrate (75':r C22:6 + 25^r C22:5) was
also provided by this laboratory. Freeze-dried
human serum albumin (Grade III) and bovine
serum albumin (BSA; crude powder) were
obtained from Sigma. Freeze-dried silver salm-
on light flesh was prepared from a slurry of
fresh fillet. All freeze-dried materials were
stored at — 60° C in the dark under nitrogen
prior to exposure to air. Lipid-protein mixtures
were prepared merely by thoroughly mixing
the C22:6 concentrate with protein, usually in
a ratio of 2: 1 (protein to lipid) by weight. All
oxidations were conducted in air at room tem-
perature. All EPR studies were conducted at
room temperature according to the procedures
of Roubal (1970).

371

FISHERY BULLETIN': VOL, 69, NO, 2

RESULTS AND DISCUSSION
ELECTRON MIGRATION IN PROTEINS

As a base for comparing EPR signals in pro-
cessed food materials, it will be instructive at
this point to consider briefly the mechanism (s)
which may be operative (disregarding for the
moment, lipid oxidation) in the production of
the observed signals in carefully freeze-dried
tissue. In recent years, considerable attention
has been given to the idea of the migration of
energy over comparatively long distances in
cells; such transfer of electrons is implicated
in the process of mutation by ionizing radiation,
in the process of nerve conduction, and in cer-
tain biochemical photo dissociations. There are
problems of a theoretical nature associated with
such hyi^otheses, and these are reviewed in the
discussions of Blyumenfel'd (1957).

Terenin (1947) and Terenin and Krasnovskii
(1949) have criticized Szent-Gyorgyi's hypo-
thesis that electrons move along the protein
polypeptide backbone in conductivity bands
analoguous to the movement of electrons in
conductivity bands of semiconducting metals.
Although polypeptide chains e.xhibit properties
reminiscent of conjugated unsaturation, Terenin
poses the interesting observation that some 70
kcal/mole, a large amount of energy, would
be required to mobilize electrons; evidently
at usual temperatures, conductivity bands are
empty.

Notwithstanding the fundamental objections
to energy migration in native proteins, Blyumen-
fel'd (1957) considered the participation of
triplet states in energy transfer, a possibility
that is partially confirmed by the fact that the
phosphorescence spectrum of proteins lies in
the region of 4000 A and corresponds closely
to the calculated excitation energy which would
be sufficient for energy transfer across molecu-
lar orbitals originating within the framework
of hydrogen bonds. However, in the absence of
prosthetic groups, it seems reasonable that few,
if any, electrons would be free for mobilization.
When prosthetic grouiis are present, however,
and when they lie close to those of the ])rotein
(energetically speaking), electrons could be

transferred into low lying orbitals of protein.
Once in these molecular orbitals, the forbidden
triplet transition to the singlet ground state
would tend to maintain electrons in the triplet
state energy levels. Under these circumstances,
the electron would move along a chain of pep-
tide hydrogen bonds until disposed of into some
other favorably bound group.

RADICAL CONTENT IN PROCESSED
FISHERY MATERIALS

For conventionally processed foodstuffs, tis-
sues, and meals (that is, solvent-extracted pro-
teins or proteins processed at room tempera-
ture) , the situation is quite difl'erent. No longer
do we have a protein substance identical in
character to the native material; bonds have
been broken, and the original geometrical ar-
rangement of the protein chains has been com-
pletely disrujjted. In many instances, certain
compounds or classes of compounds have been
selectively removed while at other times other
substances are purposely added back to the pro-
tein.

Interestingly, the present study has shown
that such materials as protein concentrates con-
taining some residual lipid, fish meal, and freeze-
dried tissue samples not processed with utmost
caution in the freezing and freeze-drying steps,
all exhibit characteristic EPR signals when e.\-
posed to air. Indeed, it is generally true that the
radical content of haphazardly handled ma-
terials is usually higher than for an equal weight
of similar material which has been processed
by careful handling, freezing in liquid nitrogen,
and careful removal of water. Unable to mi-
grate along conductive pathways, effective
charge ti-ansfer to radicals from donor mole-
cules or reactants is apparently reduced (thus
the radicals act as though caged or matrixed)
and no longer do radicals interact freely with
one another nor do they react at once with
other cellular constituents. However, the ef-
ficiency in the reduction of charge transfer un-
doubtedly depends on the nature of the sample
and its treatment. Just how immobilized such
radicals are is open to conjecture. They are im-

372

ROUBAL; NATURE OF FREE RADICALS

mobilized sufficiently, however, so as to be de-
tectable for fairly long periods of time.

CHARACTERISTIC FORM AND APPEARANCE

OF EPR SIGNALS OBSERVED IN

DRIED PRODUCTS

Although a high resolution EPR analysis can
usually be performed with dilute solutions of
soluble, low molecular weight organic radicals,
the same is seldom true for powdered samples,
and especially for powdered samples of complex
molecules. The requirements for resolution are:
magnetically dilute systems (in order to prevent
spin-spin interaction), long relaxation times,
and a low rf field. In the solid state, relaxation
times are shortened because of the more effective
coupling between spin states and the surround-
ing lattice — cooling the sample (perhaps to the
temperature of liquid nitrogen or below) will
often increase the relaxation time to acceptable
values. Related to relaxation is the line broad-
ening arising with molecular dipole interactions.
The notable example is the so-called "oxygen
effect" — some radicals will be far removed from
the magnetic influences of the molecular oxygen
di-radical while other free radicals in the sam-
ple will be near oxygen molecules. Consequently,
free radicals of the sample will experience a
variety of magnetic fields, producing a collective
band of resonances resulting from the distribu-
tion of collective magnetic fields superimposed
on the external instrument magnetic field. There-
fore, in solid state studies, radicals, because of
their random alignment, exhibit anisotropic
coupling which broadens the lines and makes
interpretation difficult. Spectral features which
can be used to characterize the radicals are the
measurement of the g-value, line shape, and
changes in these parameters upon chemical or
physical treatment of samples.

Figure 1. — EPR spectra for protein essentially free of
lipid and for a lipid-treated protein, all exposed to air.
A. Freeze-dried and solvent extracted rockfish myofibril-
lar protein. B. Freeze-dried human serum albumin. C.
Crude bovine serum albumin (BSA) (upper trace).
Crude BSA -|- C22:6 fatty acid (2:1 by \vt) oxidized
in air at room temperature for 2 hr (middle trace).
Same material in air at room temperature at the end
of 4 hr (lower trace). The arrows denote the g = 2 or
free-spin value.

Figure 2. — EPR lipid signals in marine protein con-
centrates expo.sed to air. A. Freeze-dried rockfish flesh
exposed to air for 20 hr at room temperature. B. Com-
mercially available FPC, now 2 years old, low lipid ini-
tially, which still exhibits a weak lipid signal. C. Freeze-
dried silver salmon light flesh exposed to air for 10 hr
at room temperature. Arrows denote g =r 2.

EPR SPECTRA OF FISHERY PRODUCTS

Shown in Figures 1, 2, and 3 are EPR signals
which are observed in lipid-]3rotein models and
in dry ice-frozen, freeze-dried fish tissue, all of

which are under investigation in this laboratory.
As with carefully freeze-dried samples of the
type discussed above (liquid nitrogen frozen and
freeze-dried), the resonances are devoid of
hyperfine structure of the type normally

373

FISHERY BULLETIN: VOL. 69, NO, 2

Figure 3. — EPR lipid signals in a hydroperoxide-treated
protein and in a sacroplasmic protein. A. Rockfish myo-
fibrillar protein upon removal from the freeze-drier
(lower trace). The same material 40 min after incor-
porating a small amount of a hydropero.xide mi.xture pre-
pared from a marine oil (upper trace). B. Freeze-dried
rockfish sacroplasmic protein after storage in air at
room temperature for 1 day. Arrows denote g ^ 2.

observed for dilute solutions of low molecular
weight radicals. Without exception, all powdered
materials of proteinaceous nature, which ex-
hibited any type of signal at all, gave a single
absorption line in the "free-spin" or g = 2 re-
gion. The g = 2 signal is exemplified in Figure
la (for solvent-extracted myofibrillar protein),
or in Figure lb for human serum albumin. I will
have more to say about the g — 2 signal; how-
ever, let us concern ourselves for the moment
with other resonances which are seen in those
samples containing oxidizable lipid in addition
to protein.

Freeze-dried Pacific cod, silver salmon, rock-
fish, and other marine fish, though devoid of the
g = 2 signal initially (before lipid oxidation has
taken jilace) soon give rise to two resonances
when samples are exposed to air — the central
g = 2 resonance and, downfield (to the left)
from the central resonance, an area of EPR ac-
tivity which I have designated as the "lipid
signal" region (Figures 2 and 3). Unlike tissue
samples, many single proteins considered to be
quite pure exhibit a g = 2 resonance only.

When, however, a thin film of oxidizable lipid
is deposited on such materials and the mixture
is exposed to air, in addition to the central res-
onance, a lipid signal is also observed (Figure
1 ) . A preliminary study of lipid signals in var-
ious models is to be found in the recent work
of the author (1970). Although it has not been
possible to measure the g-value with the neces-
sary precision needed to fingerprint the radical
completely, the available data suggest a radical
of the peroxy type. This is further illustrated
by the two traces of Figure 3a. No indications
of hyperfine splitting (hfs) are also consistent
with a radical of this nature.

CHARGE TRANSFER IN TISSUES

In the present study, it is of particular inter-
est to find that in carefully handled freeze-dried
tissue samples, there often occurs after the lipid
signal reaches a maximum, an abrupt increase
in the g = 2 region. In those "native" samples
containing a complement of cellular lipid, this
may indicate a charge migration (a strong
D-»A — donor-to-acceptor interaction; strong
charge-transfer process) between a cellular con-
stituent acting as a donor and a peroxy radical
acceptor. Such a process is also consistent with
the observation that it is at this point in time
that the lii)id signal begins to decay. This draws
our attention to the likelihood that once radical
content has increased to some critical concentra-
tion, overlap of wave functions between a rad-
ical acceptor and a donor is sufficient to allow
reactions to proceed. The abrupt change in the
g = 2 region is illustrated by the spectra of
Figure 3. Figure 3b for sacroplasmic i)rotein
under air for 1 day is to be compared with the
lower trace of Figure 3a for the same material
immediately on removal fi'om the freeze-dryer.

Another point in favor of a mechanism of
this type is the fact that only proteins are really
effective as matrices for the formation as well
as for the decay of radicals. Powdered glass,
quartz wool, and amino acids are essentially
without effect when used as substrates for thin
films of reactants. Although there ai-e many
unanswered questions concerning the mechanism

374

ROUBAL; NATURE OF FREE RADICALS

of trapping and charge migration, the data are
consistent with the scheme shown below:

POLYPEPTIDE CHAINS

A«

D •••• C — N — H

0 = C— N— H

D •••• C N-— H

0

D .... c — N— H
0

C— N— H
11 I

0

0=C— N — H •- A*

0 — C — N— H •- A"

0=C— N— H

and Fomin, 1965). In the present work, for in-
stance, when hydroquinone or various hydro-
quinone derivatives with free hydroxy! groups
are incorporated into proteins coated with thin
films of unsaturated lipid, an enhanced central
resonance is obtained which is identical to that
obtained for oxidizing tissue alone. For the
protein-lipid hydroquinone systems, the author
has shown that central resonance consists chiefly
of trapped semiquinone radical ions. The g = 2
resonance in "lipid-free" proteins may very
well indicate prior lipid oxidation but now at
a point in time at which lipid signal has decayed.
The g = 2 retention could then be explained
because of resonance stability or other stabiliz-
ing factors for this species. For instance, some
commercial preparations of bovine serum albu-
min exhibit an EPR signal somewhat displaced
from the usual g = 2 signal while others do not.
Likewise some of the samples that are E PR-
active exhibit fluorescence quite characteristic
of malonaldehyde-amino acid interaction (for-
mation of iminopropene derivatives) . The var-
ious data taken collectively suggest the follow-
ing mechanism:

C — N— H -•

II I

0

0=C — N— H ••

Scheme 1. — Charge-transfer between donor (D) and
a free radical acceptor (A) in biological systems. Al-
though the actual pathway is not known with certainty,
available data are in accord with the idea that hydrogen
bonding of the type shown may play a role in the transfer
of charge.

where D is a cellular electron donor material
acting in the role of an antioxidant and A is a
peroxy radical acceptor. To completely sub-
stantiate that such a mechanism does exist would
be very exciting indeed for this would be the
first instance in which the role of an antioxidant
at the molecular level could be designated as a
strong D-*A interaction.

The data are also in accord with the idea put
forth sometime ago by some Russian investi-
gators, that the g = 2 signal in tissue is semi-
quinone in nature (Chetverikov, Blyumenfel'd,

Hydroperoxide

r,l

Decay

Nonradicals

D- — * Slow Decay
where d is shown here as hydroquinone

Resonance
'structures

Scheme 2. — Interaction between radicals (R-, R-') and
cellular antioxidants (D).

375

FISHERY BULLETIN: VOL. 69, NO. 2

Other radicals, however, may make some small
contribution to the central resonance pattern.
A recent investigation by Wekell and RoubaP
has shown that free radicals arise during car-
bony] amine browning. What is more, although
hfs is seen in early stages of the browning, the
signal changes to a single line in the g = 2 re-
gion as polymerization progresses. The brown-
ing reaction, without the implication of free
radicals in lipid-protein systems, though not a
dominant pathway to pigments, was first dis-
cussed by Venolia and Tappel (1958) as a pos-
sible cause of color formation during the ox-
idation of such systems [but because the more
recent work, polymeric masses are, for the
most pai-t, attributed to lipid peroxy induced
protein-protein polymerization together with
malonaldehyde cross-linked proteins (conju-
gated Schiff base)].

Thus, although recent studies in this labora-
tory have uncovered new facts concerning rad-
icals in lipid-protein systems, the exact nature
of the resonances observed in freeze-dried tis-
sue and in dry model mixtures remains to be
fully characterized. Nonetheless, this pioneer-
ing piece of research has paved the way for use
of EPR studies in systems of oxidizing lipids
together with other cellular constituents. Con-
current studies have shown that transition metal
ion impurities, if present, play only a minor role
in radical production. Other studies of this lab-
oratory have shown that pi-otein-free fish bone
does not give EPR signals. Freshly prepared
freeze-dried tissue samples give no lipid signal
resonances, but signal amplitudes grow on ex-
posure to oxygen. Depending on the type of
l)rotein, type and amount of lipid, or added ma-
terial, lipid signals exhibit various lifetimes
ranging from hours to years. (For instance,
compare Figure Ic for BSA with Figure 2b
for 2-year-old FPC.) Polysaccharides are only
partially effective as radical matrices.

For living systems, or for any system con-
taining residual and unprotected oxidizable lipid,
the implications of the various interactions dis-
cussed are significant. It is known that products
of lipid oxidation in lipid-protein systems inter-

' Unpublished data; to be published.

act with proteins, enzymes, and nucleotides. Not
only are these native biopolymers further poly-
merized by such interactions, constituent build-
ing blocks are destroyed (Roubal and Tappel,
1966b, 1967) ; notable are the sulfur amino acids
which have been shown to be easily destroyed
by free radicals (Roubal and Tappel, 1966a).
In this presentation I have not discussed con-
sequences of unwanted lipid peroxidation in nu-
tritional deficiency states or in other pathol-
ogies in living systems. Nevertheless, such
lipid-protein interaction is quite significant. The
geronotological implications of these reactions
leading to the formation of age pigments, based
on studies of Roubal and Tappel (1966b) and
others, have been reviewed by Bjorksten (1965) ,
Packer, Deamer, and Heath (1967), and Tappel
(1968).

LITERATURE CITED

Bjorksten, J.

1965. Thirteen-year report on the studies on aging
(1952-1965). Bjorksten Res. Found. Rep. Mad-
ison, Wis., 23 p.

Blyumenfel'd, L. a.

1957. Paramagnetic resonance spectra of biolo-
gical objects and migration of energy. [In Rus-
sian.] Izv. Akad. Nauk SSSR, Ser. Biol. No. 3:
285-292. (Translation, Clearinghouse, Fed. Sci.
Tech. Inform., Springfield, Va., as OTS 61-19575.)

Chetverikov, a. G., L. A. Blvtjmenfel'd, and G. V.

FOMIN.

1965. Possible mechanisms of formation and de-
struction of free radical states in cells. Bio-
physics 10: 526-538. (Translated from Biofizika
10: 476-486.)
Packer, L., D. W. Deamer, and R. L. Heath.

1967. Regulation of deterioration of structure in
membranes. In B. L. Strehler (editor), Advan.
Gerontol. Res. 2: 77-120. Academic Press, New
York.
Roubal, W. T.

1970. Trapped radicals in dry lipid-protein sys-
tems undergoing oxidation. J. Amer. Oil Chem.
Soc. 47: 141-144.
Roubal, W. T., and A. L. Tappel.

1966a. Damage to proteins, enzj-mes, and amino
acids by peroxidizing lipids. Arch. Biochem. Bio-
phys. 113: 5-8.

376

ROUBAL: XATLRE OF FREE RADICALS

ROI'BAL AND TAPPEL — Coil.

1966b. Poljnrierization of proteins induced by free-
radical lipid peroxidation. Arch. Biochem. Bio-
phys. ll.S: 150-155.

1967. Damage to ATP by peroxidizing lipids,
chem. Biophys. Acta 136 : 402-403.

Tafpel, A. L.

1968. Will antio.xidant nutrients slow aging

Bio-

pro-

cesses? Geriatrics. 23(10) : 97-105.

Terenin, a. N.

1947. Fundamental problems of photobiochemistr.v.

[In Russian, English summary.] Izv. Akad.
Nauk SSSR, Ser. Biol., No. 3: 369-376.
Terenin, A. N., and A. A. Krasnovskii.

1949. On the question of energy migration in bio-
logical processes. [In Russian.] Usp. Fiz. Nauk
37: 65-69.
Venolia, a. W., and a. L. Tappel.

1958. Brown-colored oxypolymers of unsaturated
fats. J. Amer. Oil Chem. 35: 135-138.

377

THE RELATION BETWEEN EXERCISE AND
BIOCHEMICAL CHANGES IN RED AND WHITE MUSCLE AND
LIVER IN THE JACK MACKEREL, Trachnrus symmetricns

Austin W. Pritchard," John R. HuNTERr and Reuben Lasker''

ABSTRACT

Glycogen, lactic acid, and fat concentration in red and white muscle and glycogen in the liver of jack
mackerel, Trachurus symmetricns, were measured after periods of forced swimming by Trachurus at
speeds above, below, and at the sustained speed threshold. Failure to swim at any speed was associ-
ated with an almost complete depletion of glycogen in the white muscle only. The trend of glycogen
use in the red muscle closely followed that of the liver and was not correlated with failure to swim.
Reduction of glycogen levels in red muscle and liver were associated with extended periods of swim-
Lipid use was slow and not correlated with fatigured muscle and was insignificant in white muscle,
ming. High lipid content was characteristic of e. A decline in lipid concentration after exercise
occurred only in the red muscle and only after a swimming period of 6 hr at a subthreshold speed.
High lactate levels were characteristic of both muscle types and did not appear to be related to fatigue
at any swimming speed.

The high lactate levels in white muscle, the almost complete depletion of glycogen in the white mus-
cle of exhausted fish, and the parallel pattern of glycogen depletion in red muscle and liver suggested
that white muscle was the primary locomotor organ near and above the threshold for sustained speed.
At these speeds red muscle like the liver may provide nutrients to the white muscle, provided time
for mobilization is sufficient. At speeds below the sustained speed threshold our analysis indicated
that both the red and white muscle systems were used but the relative significance of the locomotory
role played by each system could not be evaluated.

The lateral musculature of many fishes may be
readily segregated by color into red and white
portions. Typically in active fishes the red
muscle makes up from 10 to 20^^ of the total
musculature and is arranged in a thin lateral
sheet just beneath the skin whereas the white
muscle makes up the underlying mass of the
myotome. The two muscle types also differ in
the diameter of their muscle fibers, speed of
contraction, blood supply, mitochondrial content,
patterns of innervation, and glycogen and fat
content (Bone, 1966).

The accepted view of the function of red
and white muscle tissues in fishes was outlined
by Bone (1966). He concluded from his own
work on dogfish and from an extensive liter-
ature review that the two muscle fibers repre-
sent two separate motor systems which operate

^ Zoology Department, Oregon State University, Cor-
vallis, Oreg. 97331.

' National Marine Fisheries Service Fishery-Ocean-
ography Center, La Jolla, Calif. 92037.

Manuscript received January 1971.

FISHERY BULLETIN: VOL. 69, NO. 2, 1971.

independently, utilize different metabolites, and
serve different locomotory functions, viz., the
red muscle is used for slow cruising speeds and
functions by aerobic metabolism of fat whereas
the white muscle is used for rapid bursts of
swimming and is driven by anaerobic glycolysis.
Bone's conclusions have subsequently been sup-
ported by measurements of oxygen uptake in
red and white muscle by Gordon (1968) and by
electrophysiological studies on oceanic skipjack,
Katsiuvonus pelamis, by Rayner and Keenan
(1967). On the other hand, Braekkan (1956)
and Wittenberger (1967) believe the red muscle
has no independent locomotor role and functions
as a metabolic organ for the white muscle. Elec-
trode recordings from the red muscle (Bone,
1966; Rayner and Keenan, 1967) have provided
irrefutable evidence for an independent loco-
motor function of red muscle at certain slow
speeds, but the metabolic independence of the
two muscle systems and their metabolic and
locomotor function at higher speeds is still open

379

FISHERY BULLETIN: VOL. 69. NO, 2

to question. Although the roles assigned to the
two muscle systems are dependent on swimming
speed, no studies have been made on the function
of the muscle systems using normally swimming
intact animals at known speeds. The objective
of this study was to re-examine the metabolic
and locomotor roles of red and white muscle by
measurement of glycogen, lactate, and fat levels
in the muscle and glycogen levels in the liver
in fish exposed to various velocity treatments
of known strength and duration. Juvenile jack
mackerel, Trachums synimetricics, were used in
this study because the maximum sustained speed
threshold for 6 hr of continuous swimming had
already been established for this species (Hun-
ter, 1971), and consequently we were able to re-
late all of our chemical measurements to known
levels of swimming performance.

METHODS AND PROCEDURES

SWIMMING TESTS

Jack mackerel were maintained at a regu-
lated seawater temperature of 18.5° C in a plastic
swimming pool 4.57 m diameter and fed an
abundant ration of brine shrimp, Artemia, and
chopped fish and squid each day. The fish were
not fed for 20 hr prior to testing. Jack mack-
erel were tested in an activity chamber patterned
after that of Beamish (1968) and described in
detail by Hunter and Zweifel (1971). The swim-
ming compartment of the apparatus consisted
of a tube 230 cm long and 41 cm in diameter
through which seawater could be moved at
speeds ranging from 12 to 212 cm/sec. Fish
were placed in the tube and forced to swim at
a water speed for certain periods varying from
8 min to 6 hr. At the end of the swimming
period they were removed and dropped imme-
diately into liquid nitrogen and the frozen fish
were stored at — 30° C until used for chemical
analysis. The time required for removal and
freezing did not exceed 1 min.

Speed treatments for the experiments were
chosen relative to the 50'^ endurance threshold
for jack mackerel at 22 L^^/sec for 6 hr of
swimming where L is total length (Hunter,

1971). Five jack mackerel, nrean length 14.6
cm, were tested at the subthreshold speed of
19.6 L"'' sec (98 cm sec); 14 jack mackerel,
mean length 16.3 cm, were tested at the near
threshold speed of 21.1 L''Vsec (113 cm/sec);
and 10 jack mackerel, mean length 14.7 cm, were
tested at the superthreshold speed of 27.7 L^V
sec (139 cm 'sec). Fish tested at the sub-
threshold speed swam continuously for 6 hr and
were sampled at the end of that period. Fish
tested at the threshold speed were divided into
two groups: seven fish that were sampled after
6 hr of continuous swimming; and seven fish
that fell from exhaustion at some time during
the 6-hr period. The latter group of seven fish
were quickly removed from the apparatus and
frozen as soon as they fell against the rear
screen. Fish tested at the superthreshold speed
were also divided into two groups: those that
swam successfully for 8 min; and those that
failed after 8 or less minutes of swimming.
Ten jack mackerel, mean length 14.5 cm, were
used as controls. Five of the control animals
were removed from the holding tank, placed in
the apparatus, allowed to swim for 30 min at
the slow speed of 6.2 L°''/sec (30 cm sec), re-
moved, and frozen. The other five control fish
were removed from the holding tank and imme-
diately frozen. The data from these two con-
trol groups were later combined because no dif-
ference between them was detected.

CHEMICAL ANALYSES

White and red muscle were dissected from
the frozen fish while still frozen. One lateral
striiJ of red muscle was used for fat analysis
and the other divided into two equal portions for
lactate and glycogen analysis respectively.
About 1 g of white muscle from the dorsal por-
tion of the myotome was used for glycogen de-
terminations, 0.5 g for lactate, and 0.5 g for fat
measurements. Fish were returned to the
freezer and liver samples (0.1-0.2 g) were an-
alyzed for glycogen about a month after the
muscle determinations.

380

PRITCHARD, HUNTER, and LASKER: EXERCISE AND BIOCHEMICAL CHANGES

For lactate measurements muscle was quickly
cut into small pieces, weighed, and homogenized
in 10% trichloroacetic acid in prechilled tubes.
Proteins and cellular debris were spun down in
a clinical centrifuge. Aliquots of the protein-
free supernatant fluid were analyzed for lactate
enzymatically using the test reagents supplied
by SIGMA Chemical Company.'' The test is
based on the conversion of nicotine adenine nu-
cleotide (NAD) to the reduced form (NADH)
as lactate is converted to pyruvate by lactate de-
hydrogenase. All readings were made at 340 m/jL
on a Beckman DU spectrophotometer. Results
are expressed as mg of lactic acid per 100 g wet
weight muscle tissue.

Muscle and liver samples for glycogen de-
terminations were drojiped into preweighed
graduated centrifuge tubes containing 3 ml of
30% potassium hydroxide. Glycogen was pre-
cipitated with alcohol and determined according

' P.O. Box 14508, St. Louis, Mo. 63178. Reference
to commercial products does not imply endorsement.

to the method of Montgomery (1957) . All read-
ings were made at 490 m/^ on a Beckman DU
spectrophotometer. Results are expressed as
mg glycogen (as glucose) per 100 g wet weight
in the case of muscle, and as percent glycogen
in the case of liver.

Muscle tissue was dried in an oven at 60° C
to constant weight for fat analysis. Fat was
removed by a soxhlet extraction with chloro-
form-methanol (2: 1, v: v) . After the extraction
the solvent in the tissue was evaporated and
the difference in weight of the tissue recorded
(Krvaric and Muzinic, 1950).

RESULTS

Fish that swam continuously for 6 hr at the
subthreshold speed of 98 cm/sec and at the
threshold speed showed no difl'erence in the gly-
cogen content of the white muscle from the
controls (Table 1). On the other hand, in fish

Table 1. — Glycogen in red and white muscle, and liver of jack mackerel following various forced swimming con-
ditions. Red and white muscle glycogen in mg per 100 g wet weight; liver glycogen is percent of wet weight. -- in-
dicates measurement was lost during analysis.

Controls

S

19 I"'
jbthreshoid speec

21 i""

Threshold speed

successes

Red

White 1

Liver

Red

White

Liver

Red

White

Liver

76.6

85.9

6.42

15.23

53.90

0.125

26.71

204.3

0.043

102.8

__

9.49

52.80

143.2

4.36

33.33

159.4

1.63

176.3

_..

22.74

192.5

76.69

.317

37.59

80.74

1.85

277.8

276.8

8.75

145.2

316.2

8.31

95.93

492.8

.125

562.0

142.6

18.59

147.6

102.6

3.16

152.4

223.2

3.42

706.0

157.9

18.17

191.7

638.0

3.19

1075

267.8

10.26

475.1

216.3

1.38

1394

72.9

17.00

1417

71.1

11.82

1706

216.5

24.24

Mean 749.4

161.4

14.75

1110.7

138.5

13.25

1144.7

287.8

11.66

21 i"»

Threshold speed

fotigued

28 L'-'
Superthreshold speed-
individually fatigued

28 L"'

Superthreshold speed,

8-min test

Red

White

1

Liver

Red

While

Liver

Red

White

Liver

11.5

26.50

.073

_.

0.546

39.93

10.00

14.00

4.51

.034

149.6

8.02

4.73

298.6

141.9

10.00

17.10

20.63

3.30

215.0

19.56

3.83

473.3

25.44

3.16

40.55

27.77

5.04

490.4

6.76

13.23

533.1

141.0

iO.94

104.8

11.96

654.5

18.49

5.81

553.9

57.22

11.31

151.8

11.15

.820

241.5

50.2

12.50

Mean 183 27

'23.46

M.82

377.4

113.21

1563

464.7

181.1

9.08

1 Differed from the controls, P ^ 0.05, Mann Whitney U test (Siegel, 1956).

381

FISHERY BULLETIN; VOL. 69, NO. 2

that failed to swim the full 6 hr at the same
speed the glycogen levels in the white muscle
were lower and were different from the controls
(P = 0.001 Mann Whitney Latest, Siegel, 1956).
Glycogen levels in white muscle of all fish tested
at the superthreshold velocity were also much
lower and statistically different from the controls
(P = 0.05). The lowest glycogen levels of all
were in fish that failed from exhaustion at su-
perthreshold speeds. The values in these ex-
hausted fish were statistically different from
those of fish that swam at the same speed but
which were removed after 8 min of swimming
before they could fall from exhaustion. In sum,
strenuous exercise and exhaustion regardless of
speed were associated with a marked depletion
of glycogen reserves in the white muscle, where-
as successful swimming for 6 hr at subthreshold
or threshold speed produced no. significant
change in white muscle glycogen.

The glycogen content of the liver and red
muscle were lower and different from the con-
trols in fish tested at threshold and subthreshold
speeds (P = 0.05). At superthreshold speed,
on the other hand, the glycogen content of the
red muscle was not different from the controls
and that of the liver was different only in fish
that failed from exhaustion (P = 0.02).

Thus, the trends in the levels of red muscle
and liver glycogen in relation to swimming speed
were nearly the reverse of that for white muscle
glycogen. Low levels of glycogen in red muscle
and liver were associated with slow speeds that
could be sustained for extended periods. These
results suggest that glycogen from red muscle
and liver provide energy to the white muscle at
nearly all swimming speeds. We believe that
no drop occurred in red muscle glycogen in fish
fatigued at high speeds because the time was
too short for the white muscle to mobilize sig-
nificant amounts of glycogen. This view is sup-
ported by the negative correlation between the
level of glycogen in the red muscle and swim-
ming time to fatigue at threshold speed. This
is illustrated in the following table:

Threshc

Id speed =

21

LO-6

Time to fatigue

Glycogen

in red muscle

(mm)

{mg per

100 g wet weight)

282

11.5

110

16.0

131

17.1

79

40.6

15

104.

38

241.

{r, = -0.857, P <0.05)

In fish exercised at the superthreshold speed
the lactic acid content of the red and white
muscle was considerably above that of the con-
trols and statistically different from them (P =
0.05) (Table 2). At threshold and subthreshold

Table 2. — Concentration of lactic acid in red and white
muscle of jack mackerel following various forced swim-
ming conditions. Values given are mg lactic acid per
100 g wet weight.

19 L°

a

21

/."

J

Co

ntrols

Subthres

hold

Threshold

speed

speed

successes

Red

Whit9

Red

Whits

Red

1

Whits

40,49

233.0

94.6

5209

20.60

310.4

59.29

425.3

97,6

596.6

22.83

344.5

71.53

387.5

99,2

521.9

26.79

385.3

77.46

521.0

117.1

630.3

45.66

464.8

79.53

570.3

156.3

762.3

56.94

403.1

82.19

341.5

82.19

345,2

86,76

390.6

83.87

410,2

86 76

319.0

86.76

553.4

95.44

589.6

Mean 76.63

433.1

'113.1

606.4

'48.41

380.S

21

Thresh

fa

i'

Did

28 i° "

28

1"

0

speed
ed

Superthreshold
speed ■ indivtduolly

Superthreshold
speed, 8-min

fatigu

ed

test

Red

White

Red I

White

Red

Whits

26.23

564.6

101.2

422.9

124.2

724.1

39.61

545,3

108.4

538.6

132,3

668.9

56.58

404.4

120.4

723.1

189,0

799.9

66.6

499.2

151.9

745.8

202.8

807.4

86.76

489.7

230.5

800.6

237.4

733.5

122.5

486.2

205.5

646.1

Mean 86.25

519.4

1142.5

'646.2

'177.1

'746.8

> Differed from the controls, P ^ 0.05, Mann Whitney i' test (Siegel,
1956).

speeds, the lactic acid concentration in red and
white muscle formed no distinct pattern. At
threshold speed the lactate levels of red and
white muscle were about the same as the con-
trols and did not diflfer from them except for
one case where the values were actually lower

382

PRITCHARD. HUNTER, and LASKER: EXERCISE AND BIOCHEMICAL CHANGES

than the controls; at this subthreshold speed
lactate levels of red and white muscle were
higher than the controls and differed statistically
(P = 0.02) . We have no explanation for these
differences except to suggest that the high
muscle lactate concentration in the control an-
imals may have obscured changes resulting from
moderate exercise. A larger sample size may
be required to obtain reliable measurements of
differences in lactic acid concentration caused
by moderate exercise.

Muscle lactate level did not appear to be re-
lated to fatigue at any swimming speed. Lac-
tate levels in fish that fatigued at the threshold
speed were not different from the controls. Fish
that failed at superthreshold s])eeds had a higher
muscle lactate level than did the controls but
the level did not differ from that of fish that
swam at the same speed but were removed be-
fore they became exhausted. These results sug-
gest that high lactic acid concentration in muscle
was not the principal cause of exhaustion.

Red muscle contained considerably more fat
per unit weight than white muscle. Indeed,
white muscle fat levels were almost undetectable
in many cases (Table 3). White muscle fat
levels did not differ from the control at any
speed level. Red muscle fat did not differ from
the controls at threshold and superthreshold
speeds but at the subthreshold speed the mean
level of fat in the red muscle was lower than
the controls and differed statistically from them
(P = 0.02). Thus only when the fish swam
for at least 6 hr at subthreshold speed was there
evidence of fat utilization in the red muscle.*
The reduction in fat in the red muscle suggests
that the red muscle system may have been used
at the subthreshold velocity. On the other hand,
presence of high muscle lactate in both red and
white muscle and the drop in red muscle and
liver glycogen at subthreshold speeds implies
that the white muscle was also active.

Table 3. — Fat analyses in red and white muscle of jack
mackerel following various forced swimming conditions.
Where 0.0% is given for white muscle, only traces of fat
were found with the chloroform-methanol extraction.
For convenience zeros were used for averaging. Values
given as percent dry weight of tissue.

Controls

19
Subthres

lold speed

21 i"'

Threshold speed

successes

Red

While

Red

White

Red

Whila

20.16

1.98

15.07

0.230

16.91

0.0

2I.0Q

0.0

15,69

2 12

22.45

0.0

21.78

.337

16.19

1.24

23.80

2.19

22.24

1.15

20.54

0.0

24.67

0.0

23.05

1.32

24.63

0.0

24,97

1.54

25.11

0.0

26,43

4.09

25.14

.390

29.37

4.10

25.89

.924

27.29

2.65

32.32

2.20

Mean 24.40

1.10

M8.42

.718

24.08

1.70

28

L"»

28 L"-

Threshold speed

Super
speed -

hreshold
ndividuolly

Superthreshold
speed, 8-min

fatig

fatigued

test

Red

White

Red

1 While

Red

While

21.30

0.0

16,54

0.0

21.96

2,01

21.97

0.0

1671

0.0

23,08

,04

22.47

0.0

26.47

1.22

24,20

.18

28.70

0.0

28.19

.732

25,57

.50

30.11

2.56

28.70

2.13

29,54

2.26

32.08

1.12

32.90

6,46

Mean 27.03

1.45

23.32

.816

24.87

.998

' In an earlier and preliminary experiment, five
smaller jack mackerel, mean length 9.2 cm, swam at
the subthreshold speed of 12.7 L" Vsec (48 cm/sec) for
48 hr without failure and we recorded a decrease in the
mean fat content of red muscle from 23.7% (range, 20.4-
28 4%; K = 5) to 18.0% (range, 16.2-20.8%; n — 5)
(P<0.05).

1 Differed from the controls, P = 0.02, Mann Whitney U lest (Siegel,
1956).

DISCUSSION

Control levels of jack mackerel white muscle
glycogen were similar to those recorded by Can-
adian workers for mixed red and white muscle
in salmonids (Black, Robertson, and Parker,
1961; Black et al, 1962; Connor et al, 1964)
and to those from a variety of marine teleosts
(Beamish, 1968; Eraser et al, 1966; Witten-
berger, 1968; Wittenberger et al., 1969). Red
muscle glycogen has not often been separately
determined. Our mean control value of 750 mg
percent was somewhat higher than the mean of
420 mg percent reported by Wittenberger
(1968) for Tnichuncs mediterrayieiis ponticus,
a related species from the Black Sea. Fraser
et al. (1966) gave a range of 215 to 279 mg per-
cent for red muscle glycogen of cod, based on
analysis of three fish in a relaxed (anesthesized)
state. Wittenberger et al. (1969) reported 320

383

FISHERY BULLETIN: VOL. 69, NO. 2

mg percent in a clupeid, Harengtda Mimeralis.
A much higher level of 1866 mg percent was
given by Bone (1966) for dogfish. In most
cases, the concentration of glycogen in red
muscle was considerably higher than in white
muscle.

Liver glycogen controls in jack mackerel were
much higher than those reported previously in
teleosts. Connor et al. (1964) for example, ob-
tained values of about 1 Sr in chinook and sockeye
salmon and steelhead trout, and found that
moderate exercise associated with ascending
fishways had no effect on liver glycogen levels.
Black etal. (1960) reported liver glycogen levels
of 0.5-4 '/f in rainbow trout, and Dean and Good-
night (1964) obtained 0.8-3 9r in four species of
warmwater centrachid fishes. Values similar
to ours were reported by Wittenberger and
Diaciuc (1965) in carp (13.8%) and by Bellamy
(1968) in recently fed red piranha (10.3'^f ).
Even if a high degree of gluconeogenesis were
operative in jack mackerel, it seems unlikely
that this could entirely explain the high levels
of liver glycogen.

Control levels of glycogen in jack mackerel
white muscle appeared to be similar to those
in other fishes. However, in the red muscle and
especially in the liver, glycogen levels were usu-
ally higher than in fishes studied earlier.

The most striking finding of this study was
the virtually complete depletion of glycogen in
the white muscle of fish that failed from ex-
haustion. The depletion of glycogen in white
muscle occurred in all fish that failed regardless
of the speed of swimming or how long they
swam. In fish that did not fail at a near thresh-
old speed of 21 L" Vsec (Hunter 1971) the gly-
cogen in the white muscle did not differ from
controls, whereas in the fish that failed, glycogen
in the white muscle was at nearly the same
low level as it was in fish that failed after a few
minutes of exertion at a much higher speed.
Red muscle glycogen was also depleted at some
swimming speeds but the pattern of glycogen
depletion in red muscle closely paralleled that
of the liver. Red muscle had one-fifth the lac-
tate found in white muscle on a percent basis
but only about one-fiftieth on an absolute basis

because the mass of white muscle exceeds the
red by 10 to 1.

The high lactate levels in the white muscle,
the almost complete depletion of glycogen in the
white muscle of exhausted fish, and the parallel
pattern of glycogen depletion in red muscle and
liver all point to the same hypothesis. In jack
mackerel at threshold and higher speeds the
energy used for swimming was derived primar-
ily from glycolysis in the white muscle which
was the principal locomotor organ. Red muscle
like the liver may serve as a storage organ whose
resources could be used to drive the white
muscle, given sufficient time for mobilization.
Thus at threshold speeds, red muscle function
appeared to be tied to that of the white and it
could not be considered as acting independently.
No change in red muscle glycogen was detected
at the highest test speed, possibly because time
was insufficient to mobilize the glycogen reserves
other than in the white muscle itself. This time
dependency for mobilizing red muscle glycogen
under conditions of strenuous exercise could ex-
plain why Bone (1966), Wittenberger and Di-
acuic (1965), Wittenberger (1968), and Fraser
et al. (1966) detected no change in red muscle
glycogen after strenuous exercise. It must be
remembered that in all of these previous studies
the strength and the duration of the exercise
was unknown, except that it was considered
to be extreme.

The decrease in fat content plus the high
lactate levels suggest that the red muscle was
used for swimming at subthreshold speeds.
Bilinski (1969) showed that the rate of oxidation
of fatty acids in red muscle of rainbow trout
and sockeye salmon exceeded that in the white
muscle by one or more orders of magnitude de-
pending on the fatty acid substrate. On the
other hand, neither the high oxidative capacity
nor the decline in lipid levels in red muscle with
moderate exercise are suflicient evidence for an
independent locomotor role. In addition, the
presence of high lactate levels in white muscle
and the drop in the glycogen content of the white
muscle indicated that the white muscle was also
used at the subthreshold speed of 19 L"" 'sec.
The electrophysiological evidence for indepen-

384

PRITCIIARD, HUNTER, and LASKER: EXERCISE AND BIOCHEMICAL CHANGES

dent locomotor activity of tlie red muscle cannot
be ignored. At some speed slower than any
used in the present experiment jack mackerel
may depend only on red muscle for propulsion
and on lipids for fuel. At what velocity red
muscle begins to play a major role or how sig-
nificant this speed may be in the life of the an-
imal are questions that remain to be answered.
The most tenable explanation for these data is
that both muscle systems were used at the sub-
threshold speed but we are unable to choose
which system played the more significant role.
Jack mackerel appear to be specialized in
body form and swimming capabilities for high-
speed continuous swimming (Hunter, 1971).
Thus the physiological characteristics we have
described, namely use of glycolysis in white mus-
cle for swimming, high liver glycogen levels,
and tolerance of high muscle lactate levels may
represent specializations for high-speed swim-
ming and may not be representative of the gen-
eral pattern in fishes. On the other hand,
Tmchiirits may share these characteristics with
other fishes of similar habits, for example other
carangids and the scombroid fishes. It seems
possible that evolution may have favored the
development of these physiological character-
istics because severe velocity limits may be set
by aerobic lipid metabolism.

ACKNOWLEDGMENTS

We thank Messrs. David Holts, William Rom-
mel, and Andrew Kuljis for their technical as-
sistance during this study.

LITERATURE CITED

Beamish, F. W. H.

1968. Glycogen and lactic acid concentrations in
Atlantic cod (Gadiis morliua) in relation to ex-
ercise. J. Fish. Res. Bd. Can. 25: 8.37-851.

Bellamy, D.

1968. Metabolism of the red piranha (Roosevelti-
ella nattereri) in relation to feeding behaviour.
Comp. Biochem. Physiol. 25: 343-347.

BiLINSKI, E.

1969. Lipid catabolism in fish muscle. In 0. W.
Neuhaus and J. E. Halver (editors). Fish in
research, p. 135-151. Academic Press, New York,

Black, E. C, A. R. Connor, K.-C. Lam, and W.-G. Chiu.

1962. Changes in glycogen, pyruvate and lactate

in rainbow trout (Snlmo gairdneri) during and

following muscular activity. J. Fish. Res. Bd.

Can. 19: 409-436.

Black, E. C, A. C. Robertson, A. R. Hanslip, and

W.-G. Chiu.

1960. Alterations in glycogen, glucose and lactate
in rainbow and kamloops trout, Salmo gairdneri,
following muscular activity. J. Fish. Res. Bd.
Can. 17: 487-500.

Black, E. C, A. C. Robertson, and R. R. Parker.

1961. Some aspects of carbohydrate metabolism
in fish. In A. W. Martin (editor), Comparative
physiology of carbohydrate metabolism in hetero-
thermic animals, p. 89-124. Univ. of Wash. Press,
Seattle.

Bone, Q.

1966. On the function of the two type of myotomal
muscle fibre in elasmobranch fish. , J. Mar. Biol.
Ass. U.K. 46: 321-349.
Braekkan, 0. R.

1956. Function of the red muscle in fish. Nature
(London) 178: 747-748.
Connor, A. R., C. H. Elling, E. C. Black, G. B.
Collins, J. R. Gauley. and E. Trevor-Smith.
1964. Changes in glycogen and lactate levels in
migrating salmonid fishes ascending experimental
"endless" fishways. J. Fish. Res. Bd. Can. 21:
255-290.
Dean, J. M., and C. J. Goodnight.

1964. A comparative study of carbohydrate metab-
olism in fish as affected by temperature and ex-
ercise. Physiol. Zool. 37: 280-299.
Eraser, D. L, W. J. Di-er, H. M. Weinstein, J. R.
Dingle, and J. A. Mines.

1966. Glycolytic metabolites and their distribution
at death in the white and red muscle of cod fol-
lowing various degrees of antemortem muscular
activity. Can. J. Biochem. 44: 1015-1033.
Gordon, M. S.

1968. Oxygen consumption of red and white mus-
cles from tuna fishes. Science (Washington) 159:
87-90.
Hunter, J. R.

1971. Sustained speed of jack mackerel, Trachurus
symmetricus. Fish. Bull. 69: 267-271.
Hunter, J. R., and J. R. Zweifel.

1971. Swimming speed, tail beat frequency, tail
beat amplitude, and size in jack mackerel, Tra-
churus symmetricus, and other fishes. Fish. Bull.
69: 253-266.
Krvaric' M., and R. Muzinic.

1950. Investigation into the fat content in the sar-
dine tissues (Clupea pilchardus Walb). Acta
Adriat. 4: 289-314.

385

FISHERY BLXLETIN: VOL. 69. NO. 2

Montgomery, R.

1957. Determination of glycogen. Arch. Biochem.
Biophys. 67: 378-386.
Rayner, M. D., and M. J. Keenan.

1967. Role of red and white muscles in the swim-
ming of the skipjack tuna. Nature (London)
214: 392-393.

SlEGEL, S.

1956. Nonparametric statistics: for the behav-
ioral sciences. McGraw, New York, 312 p.
WiTTENBERGER, C.

1967. On the function of the lateral red muscle
of teleost fishes. Rev. Roum. Biol., Ser. Zool.

12: 139-144.

1968. Biologie du chinchard de la Mer Noire (Tra-
churiis mediterraneus posticus) . XV. Recherches
sur le metabolisme d'effort chez Trachnrus et
Gobius: Mar. Biol. 2: 1-4.

WiTTENBERGER, C, A. CORO, G. SUAREZ, AND N. PORTILLA.

1969. Composition and bioelectrical activity of the
lateral muscles in Harengula humeralis. Mar.
Biol. 3: 24-27.

WiTTENBERGER, C, AND I. V. DiACIUC.

1965. Effort metabolism of lateral muscles in carp.
J. Fish. Res. Bd. Can. 22: 1.397-1406.

386

Sehastes variegatus, SP. N. FROM THE NORTHEASTERN PACIFIC OCEAN

(PISCES, SCORPAENIDAE)

Jay C. Quast'

ABSTRACT

A new scorpaenid fish, Sehastes variegatus, from the Gulf of Alaska is characterized by an elongate
body that tapers symmetrically anteriorly and posteriorly; presence of preocular, postocular, tympan-
nic, and parietal spines and lack of supraocular, coronal, and (usually) nuchal spines; 18 (rarely 17
or 19) rays in the pectoral fin; a second anal fin spine that is longer than the third; black membranes
in the spinous dorsal and caudal fins; a dark brown to jet black peritoneum; and a dark blotched
pattern on the sides that is interrupted over the posterior 2/3 of the body by an unpigmented band
along the lateral line. The known geographic range is from Unimak Pass (Aleutian Islands) to
Queen Charlotte Sound (British Columbia).

On February 28, 1967, the Bureau of Commer-
cial Fisheries RV Murre II obtained three
specimens of a new species of rockfish from the
vicinity of Point McCartney in Frederick Sound,
southeastern Alaska. The specimens were cap-
tured when a 6-ft-diameter Isaacs-Kidd trawl
inadvertently was allowed to touch bottom at
135 m.

The specimens were tentatively identified as
Sebastes zacentrus but were not adequately de-
scribed by Phillips' (1957) account of this
species. In some respects they seemed to be
intermediate between S. zacentrus and S. pro-
riger. The evidence for an undescribed species
became convincing when additional specimens
were taken, and the similarity to S. zac.eyitrus
and S. proriger was underscored when several
more specimens were found in old collections
that had been labeled as these species.

The species is placed in Sebastes Cuvier in
concurrence with opinions of numerous authors
that northeastern Pacific Sebastodes are con-
generic with North Atlantic Sebastes — including
Matsubara (1943b: 178); Tsuyuki, Roberts,
Lowes, Hadaway, and Westrheim (1968:2494);
Eschmeyer (19(59:104); Chen (1969:12); and
American Fisheries Society (personal commu-
nication with Reeve M. Bailey, University of
Michigan, December 1969).

' National Marine Fisheries Service Biological Lab-
oratory, Auke Bay, Alaska 99821.

The name variegatus refers to the contrasting
coloration of most specimens when fresh. Ac-
cording to Brown (1956:830), the word means
"of different sorts, particularly colors." I sug-
gest "harlequin rockfish" as the common name.

MATERIALS AND METHODS

The study utilized 39 specimens of S. varie-
gatus and included 35 from the ichthyological
collection of the National Marine Fisheries Ser-
vice Biological Laboratory at Auke Bay, Alaska,
and 3 from the collection at the Institute of An-
imal Resource Ecology, University of British
Columbia, Vancouver, Canada. This series in-
cluded 21 males, 13 females, and 4 of unknown
sex, and no important differences were found
between the sexes in measurements, counts, or
coloration. Measurements on the University of
British Columbia specimens were not as com-
plete as those from the Auke Bay Laboratory;
hence the numerical basis of the morphometric
analysis varies by 3, depending on the char-
acter. An additional male specimen was used
for electrophoretic analysis.

Methods for counts and measurements are
based on Hubbs and Lagler (1949:8-15), with
the following exceptions or modifications. In
counts: tubed lateral line scales on caudal fin
lie after hypurals; tubed scales over hypurals
are included in count of tubed lateral line scales

Manuscript received November 1970.

FISHERY BULLETIN: VOL. 69. NO. 2. 1971.

387

FISHERY BULLETIN': VOL, 61, NO. 2

on body; and scale rows are taken below lateral
line. In measurements: standard length (SL)
is measured from anterior upper lip or upper
teeth, whichever is more anterior, to caudal
base; head length is measured from midline
on upper jaw to limit of opercular flap; inter-
orbital width equals bony interorbital measure-
ment; lower jaw projection equals distance that
lower jaw extends anteriorly to upper jaw, pro-
jected on longitudinal axis of fish; length of
gill raker equals length of raker at bend of gill
arch, measured from fleshy tip to, but not in-
cluding, T-shaped base; length of prenarial pore
equals length of enlarged ])ore on anterior snout
near junction of premaxilla and premaxillary
process; length of subnarial pore equals length
of large pore on a shelf formed by upper margin
of lacrimal bone, immediately below nares; body
depth (pelvic) is measured from articulation of
pelvic fin spine; body depth (anal) is mea-
sured from base of anal fin anterior to first
anal spine; length of pectoral fin is measured
from base of uppermost ray to apex of fin when
fin is aligned with longitudinal axis of fish;
length of soft dorsal fin base is measured from
axil of last dorsal fin spine to axil of last soft
ray; length of base of anal fin is measured to

axil of last ray; and length of pelvic fin is mea-
sured from articulation of pelvic fin spine to
tip of fin.

Terminology for spines and ridges of head
follows Jordan and Evermann (1898, 11:1765,
1768).

Sebastes variegatus SP. N.

(FIG. 1-3)

HOLOTYPE

(Original number AB' 69-25) ; 201 mm SL;
male; Gulf of Alaska south of Kodiak Island
(approximately long 1.52°25' W and lat 56°
25' N); on bottom in 284 m; 12 June 1969;
Ted Shigyo, U.S. fishery observer on Japanese
stern trawler Kirishima Maru. California Acad-
emy of Sciences, San Francisco, Cafif. (Number
CAS 24857).

' Museum designations: AB — National Marine Fish-
eries Service Biological Laboratory, P.O. Box 155 .A.uke
Bay, .Alaska 99821; BC— University of British Columbia
Institute of Animal Resource Ecology, Vancouver 8,
British Columbia, Canada; CAS — California Academy
of Sciences, Golden Gate Park, San Francisco, Calif.
94118; SIO— University of California, San Diego,
Scripps Institution of Oceanography, P.O. Box 109,
La Jolla, Calif. 92037; USNM— U.S. National .Museum,
Washington, D.C. 20560.

iJSf^iosiS} variesaiiii Quaff

Figure 1. — Sebastes variegatus sp. n., holotype CAS 24857; 201 mm; male.

388

QUAST: Srbaitri varirsalui SP. N.

. ^ ,^,^1-^^^ vatSSsLi^ (Sua W
i4|.V-'< iyo»,. /3w4">i! >^(9

L

Figure 2.— Sefcos/cs variegatus sp. n., paratypes USNM 204937 (upper) and SIO 70-171 (lower) ; 185 and 193
mm; both males. (Depth and date of Paratype 2 should be the same as for Paratype 1.)

PARATYPES (NOS. 1 and 2)

OTHER MATERIAL

(Original number AB 69-26); U.S. National
Museum 204937, 185 mm, and SIO 70-171 Uni-
versity of California, San Diego, 193 mm; males;
Gulf of Alaska south of Kodiak Island (ap-
proximately long 152°25' W and lat 56°25' N);
on bottom in 240 m; 13 June 1969 ; Ted Shigyo,
U.S. fishery observer on Japanese stern trawler
Kirishima Maru.

Western Gulf of Alaska. Davidson Bank:
AB 68-598 (3, 175-182 mm SL), 26 October
1968, RV Miller Freeman. East of Simeonof
Is.: BC 65-70 (2, 145-196 mm SL), 5 August
1964, G. B. Reed. Kodiak Island vicinity: AB
67-171 (1, 235 mm SL), 19 April 1964, Taiyo
Maru No. 81; AB 67-22 (1, 277 mm SL), 21
April 1967, Yutaka Maru; AB 66-154 (1, 286

389

FISHERY BULLETIN: VOL. 69. NO. 2

7////(/|(il|fii|iiigiif|(|ipjW|i|l|i|l!jJlilJ|l|l|l!^^^

Fii;i KK .'i. — Melanistic specimen of Sthuxtts rnniijiUiis (AB (iV-fi^l; '111 mm SL; Kodiak Island vicinity.

mm SL), 8 May 1966, Tahjo Marti No. 2; AB
67-68 (1, 210 mm SL), 28 April 1967, Yutaka
Maru; AB 64-847 (1, 153 mm SL) , 10 Sep-
tember 1964, Taiyo Maru No. 77; AB 68-10
(1, 197 mm SL), 3 September 1964, Tahjo Maru
No. 77; AB 63-120 (2, 137-143 mm SL), 4 Au-
gust 1962, RV Yaquina. Middle Gulf of Alas-
ka. Portlock Bank (S of Seward): AB 63-123
(2, 157-230 mm SL), 13 August 1962, RV Ya-
quina; BC 64-292 (1, 223 mm SL), 26 August
1963, G. B. Reed. Vicinity of Port Bainbridge
(ESE of Seward): AB 64-651 (2, 120-132 mm
SL), 16 July 1963, RV Yaquina. West of Mon-
tague Is.: AB 64-645 (1, 109 mm SL), 16 July
1963, RV Yaquina. South of Montague Is.: AB
68-527 (5, 147-169 mm SL), 18 July 1968, RV
Oshoro Maru. Off Cape Yakataga: AB 68-526
(1, 193 mm SL) , 25 July 1968, Daishin Maru No.
12. OffYakutat: AB 70-23 (2, 245-278 mm SL).
15 July 1968, RV Oshoro Maru. EASTERN GULF
OF Alaska. Queen Charlotte Sound: BC 70-2
(1, 237 mm SL), 12 June 1970, RV G. B. Reed
(Electrophaerogram). Frederick Sound: AB
67-11 (3, 241-266 mm SL), 28 February 1967,
RV Murre II. Forrester Is. vicinity: AB 68-
524 (1, 211 mm SL), 24 July 1968, Ishikari

Maru; AB 68-525 (1, 242 mm SL), 24 July
1968, I shikari Marti. West of Dall Is.: AB
68-24 (3, 146-171 mm SL), 5 November 1956.
RV John N. Cobb.

DIAGNOSIS

A species of Sebastes with body outline
slender and symmetrically terete; preocular,
postoculai-, tympannic, and parietal spines pre-
sent and supraocular, coronal, and (usually)
nuchal spines absent; second anal spine longer
than third; symphyseal knob not prominent;
18 (rarely 17 or 19) rays in pectoral fin; black
spinous dorsal and caudal fin membranes; per-
itoneum dark brown to jet black; and dark
blotched pattern of pigmentation on back and
sides, the pattern partly interrupted by a broad
unpigmented band that extends over posterior
2 3 of body and includes lateral line.

MORPHOLOGY (PRINCIPALLY FROM
HOLOTYPE AND PARATYPES)

Body form, including head, slender, the out-
line smooth and tapers nearly symmetrically

390

QUAST: Srbaslri vatugatui SP. N.

to body axis anteriorly and posteriorly. Body
near head flattened laterally, body width slightly
greater than 1/2 body dejith at pelvic fins. In-
terorbital region flat to convex. Cranial ridges
over orbit usually lower than dorsal profile of
head when viewed from side, but sometimes
tangent or project slightly above the profile.
Dorsal outline of head usually smooth and
slightly concave between snout and nape. Low-
er jaw projects and enters dorsal profile of head.
Symphyseal knob weakly developed or absent.
Posterior profile of caudal fin indented; that of
anal fin slants upward-posteriorly. Pectoral fin
symmetrical; both it and pelvic fin extend to or
nearly to vent.

Head spines low but strong and well devel-
oped— nasal, preocular, postocular, tympannic,
and parietal present. Other cranial spines ab-
sent except occasionally one nuchal present.
Two opei'cular spines diverge slightly and are
contained within outline of opercular flap. Some
specimens with one (rarely two) small spines
on lower opercle. Two strong suprascapular
spines. Five preopercular spines: upjier three
longest and diverge slightly; second from top
longer than either first or third. Lower two
preopercular spines broadly triangular and
strong. Lacrimal bone has two blunt or rounded
prominences ventrally but no spines. Spines
absent on suborbital bones and stay.

Spinous rays in dorsal fin strong and sharp,
third to fifth usually longest. Interspinous mem-
branes markedly indented posteriorly in each
space; indention varies from about 1/2 of length
of following spine in first to about 1/4 of fol-
lowing spine in fourth space and posteriorly.
Spinous rays of anal and pelvic fins strong and
prominent; second anal spine longest, and 14-
23 Sf of its length exceeds third. Each soft ray
in dorsal fin branched at least once, usually with
posterior and sometimes anterior branchlet di-
vided again. Bordering principal rays on caudal
fin simple, but branched rays have three sets of
dichotomies each (end in eight branchlets).
Soft rays of anal fin branched at least once, and
usually each branchlet divided again; sometimes
posterior branchlet divided several times. Soft
rays of pelvic fin branched at least twice, usually

with further dichotomies. Uppermost ray of
pectoral fin simple; ventrally, degree of branch-
ing increases from one dichotomy to 1-1/2 or 2;
lowermost rays slightly thickened and simple,
rarely with one dichotomy.

Squamation on head ctenoid and nearly com-
plete— includes snout between premaxillaiy pro-
cesses (in holotype but not in paratypes), sides
of snout, dorsal surface of head, preopercle,
opercle, lacrimal area, maxilla, mandible, and
branchiostegals. Lips and branchiostegal mem-
branes not scaled. Body fully scaled; scales
finely ctenoid on body sides, but ctenation re-
duced on belly and breast and even more reduced
to absent on scales of isthmus, which are all
small. A few small, smooth scales extend in
line posteriorly from axilla of each pelvic fin.
Scales on bases of vertical fins and between pel-
vic fins markedly reduced in size. Scaled areas
on dorsal fin spines extend nearly to tips. In-
terspinous membranes usually scaled on prox-
imal 1/3; scaled areas usually extend farther
distally near fin spines. Dorsal fin squamation
mostly smooth on holotyise but mostly ctenoid
on paratypes. Scales usually absent in areas
of dorsal fin membranes with heavy black pig-
mentation. Rays of soft dorsal fin scaled nearly
to tips, but membranes not as completely scaled.
Scaled areas of soft dorsal fin usually limited
to proximal 2/3 of fin — all scales ctenoid. Squa-
mation of caudal fin ctenoid, its membranes
scaled nearly to end of fin. Posterior unpig-
mented border of fin naked. Caudal rays scaled
only near their bases (but scales possibly lost
from more distal portions of rays in specimens
of this series owing to collection methods).
Squamation of anal fin ctenoid; fin spines scaled
nearly to tips; interspinous membranes naked
except for narrow area bordering third spine.
Membranes between anal soft rays scaled over
proximal 1/2-3/4; scaled areas extend farther
distally on soft rays. Pelvic fin has spines and
soft rays scaled nearly to tips; scales mostly
smooth. Upper pectoral rays scaled nearly to
tips, but squamation absent at unpigmented tips
of rays. Proceeding downward on ventral 1/2
of pectoral fin, rays have progressively more
naked area distally ; extent of naked area pro-

391

FISHERY BULLETIN': VOL. 69, NO. 2

gresses fi'om about 1/4 length of uppermost
single ray to about 1/2 of lowermost ray.

Upper jaw teeth simple and in two modal
sizes. A larger outer row, sometimes mainly
uniserial, extends nearly length of each pre-
maxillary. Anteriorly, teeth larger yet and band
broadens. A medial gap where tooth patches at
lower jaw tip meet upper jaw (small papilla
in middle of gap) . A smaller inner row of teeth,
may also be uniserial, in narrow band over most
of premaxillary; it loses uniserial character near
large anterior teeth, skirts behind them and con-
tinues to medial gap. Teeth of lower jaw simple,
uniserial, and similar in size to large teeth in
row of upper jaw. Anteriorly, lower jaw teeth
are larger and in a tuft that is separated from
midline by narrow gap — with jaws shut, from
1/2 to all of each tuft is visible. Vomerine teeth
small, in broad V-shaped patch, and sometimes
slightly enlarged to suggest a tuft at ajjex of
patch. Palatine teeth small, uniserial except
anteriorly where row broadens. Gill rakers
slender and pointed, one at bend of arch steps
1.6-2.2 (mode 1.8) into orbit. A small slit be-
hind last gill arch.

A large prenarial pore on side of snout in
angle formed by premaxillary process and pre-
maxilla. A larger subnarial pore on flat shelf
immediately below nares — outer margin of shelf
formed by part of dorsal margin of lacrimal
bone. Smaller pores occur singly above nares
and below nasal spine. Two large pores on
ventral surface of lacrimal bone — one slightly
anterior to vertical through subnarial pore and
another slightly posterior to this vertical and
beneath anterior blunt projection on ventral
surface of lacrimal bone. Four prominent pores
on each mandible — first in or near fold formed
by symphyseal knob and remaining three in a
line along ventral surface.

Suborbital bones continuous around eye; sec-
ond (suborbital stay) conforms to Type 1 of
Matsubara (1943a: 10-13), i.e. stay tapers to
point posteriorly and does not reach i)reopercle.
Sensory canal terminates at midlength of stay.
Third and fourth suborbitals tubular. Seven
branchiostegais, .^'/i on ceratohyal and V/o on
epihyal.

COLOR

Background color of body (based on Koda-
chrome transparencies of seven freshly caught
young adult specimens from Davidson Bank,
near Unimak Pass, and the Yakutat vicinity)
varies from light pink or light purple-pink to
deep red, masked with irregular pattern of dark
pigmentation that varies between specimens
from barely detectable grey through brown to
melanistic black. Masking nearly absent on one
large individual with red coloration. Some in-
dividuals had faded, nearly colorless appear-
ance. Pattern of black pigmentation on sides
below dorsal fin basically three large irregular
areas extending from midline to or onto fin.
One pigmented area beneath middle and another
beneath last 1/4 of spinous dorsal fin — first
slightly interrupted by narrow light area where
it crosses lateral line; second broadly interrupt-
ed by light band reminiscent of band along lat-
eral line of S. proriger. Third large pigmented
area beneath soft dorsal fin forms irregular
circle with light spot at center, continues onto
lower 1/2 of soft dorsal fin, interrupted near
lower border by broad light-colored band along
lateral line. Band extends over posterior 2/3
of body. Small pigmented area on dorsal caudal
peduncle extends downward to but not across
lateral line and forms anterior boundary of
I)upil-sized lighter spot on dorsal shoulder of
caudal fin. Head with diffuse brown to black
shading from symphyseal knob and nearby por-
tions of lower jaw to nape; on snout, shaded
area extends ventrally to a line through 7 o'clock
position on eye. Behind eye, dark shading ex-
tends ventrally to about 5 o'clock position and
posteriorly over preopercle. Nape dusky to a
line between 1 o'clock position of eye and an-
terior lateral line. Opercle with two broad pig-
mented bands whose converging axes meet when
projected into lower hemisjihere of eye. Ujtper
band includes both opercular spines; lower ex-
tends toward pectoral base and includes upper
two preopercular spines. Lower band aligiis
generally with irregular pigmented areas on
upper 1 2 of jjcctoral base. On cheek of most
specimens a short pigmented streak extends
posteriorly and slightly downward from ujiper

392

QUAST: Srbanri ■..arirsatus SP. N.

corner of maxilla. Lower cheeks, jaws, and
opercular membranes suffused with pink, i-ose-
pink, or red. Spinous dorsal fin with distal 12
to 2 '3 of interspinous membranes black; re-
mainder above back has pink-related back-
ground color of body. Dark pigmentation ab-
sent in .skin over fin spines, contrasting with
dark interspinous membranes. Soft dorsal fin
usually distinguished by continuation of body
pigmentation onto its lower half where pigmen-
tation forms flattened ujiper 1 2 of irregular
doughnut- or tire-shaped mark. Distally on soft
dorsal fin, interspinous membranes darkly pig-
mented near rays; intervening areas some shade
of translucent pink or red. Dark pigmentation
terminates equally along fin to form translucent
pink border. Caudal fin membranes almost en-
tirely black. Caudal fin terminates with narrow
clear or translucent pink or red border. Anal
fin pink or red, usually with narrow area or
streak of black pigmentation between spines II
and III; soft-rayed portion has dusky pigmen-
tation on distal 12 of membranes. Background
color of pectoral fin same as body but masked
by dusky pigmentation in large circular or oval
area on upper 2/3 of fin. Small dark pupil-
sized spot usually near insertion of rays near
midline of fin. Pelvic fin colored as belly.

In preserved specimens dark areas of head,
body, and fins persist and include black mem-
branes in spinous dorsal and caudal fins, black
stripe between anal spines II and III, dusky
pigmentation of lower jaw tip, radiating bands
on opercle, black spot in center of pectoral fin,
doughnut- or tire-shaped mark below soft dorsal
fin, and broad light stripe that accompanies lat-
eral line over posterior 2/3 of body and inter-
rupts two of three large dark areas on body
sides. Peritoneum normally dark brown to jet
black (one specimen had brown peritoneum with
black spots) ; a melanistic specimen (Figure 3)
had light brown peritoneum with black spots).

MERISTIC CHARACTERS
See Table 1.

Table 1. — Counts for meristic characters for holotype
of Sebastes imi-iegatiis and ranges of frequent and in-
frequent counts for all specimens.

Specimens including holotype

Character

Holotype

N

Counts and their

frequencies {N)

Precaudal vertebrae

10

3

10

Caudal vertebrae (including

urostyle)

17

3

17

Dorsal fin spinous rays

13

38

13(36); 14(2)

Dorsal fin soft rays

14

38

13(1); 14-15(37)

Total rays in dorsal fin

27

38

27-28

Anal fin soft rays

7

38

17

Lower single pectoral rays

(2 sides)

8,

9

75

7(3); 8-9(72)

Total pectoral rays

(2 sides)

IB,

18

75

17(4); 18(70); 19(1)

Pored lateral line scales

on body (2 sides)

49,

51

73

42(1); 43-51(71); 52(1)

Pored lateral line scales

on caudal fin (2 sides)

1,

1

73

0(1); 1(70); 2(2)

Scale rows below lateral

line C2 sides)

58,

58

45

46(1); 47-57(42); 58(2)

Rakers on upper limb

11

38

9(1); 10-12(37)

Rakers on lower limb.

including raker at bend

28

38

26-28(37); 29(1)

Total rakers

39

38

36-40(37); 41(1)

1 One of two odditional
rays in the anal fin.

specimens, examined subsequently, hod 6 soft

Table 2. — Measurements (mm) of tjT)e material,
Sebastes variegahis.

Head length

70.0

63.0

64.6

Upper jaw length

32.3

28.8

29.3

Prenariol pore length

1.7

1.0

1.4

Subnoriol pore length

2.4

2.5

2.5

Orbit diameter

22.4

18.5

19.0

Interorbital width

14.2

13.4

13.7

Raker length

12.0

10.7

12.0

Lower jaw projection

3.8

3.3

3.6

Snout length

17.5

16.4

17.0

Suborbital width

2.5

2.7

2.2

Head width

30.2

29.3

29.8

Pectoral fin length

60.0

53.1

56.7

Pectoral base length

19.0

18.3

19.2

Coudal peduncle depth

18.0

15.9

16.0

Dorsol caudal peduncle

length

28.7

26.0

26.5

Ventral caudal peduncle

length

44.3

40.2

40.9

Body depth (pelvic)

58.4

56.5

56.5

Body depth (anal)

47.5

45.2

48.9

Anal spine 1 length

18.5

16.9

16.5

Anal spine II length

40.2

36.6

37.8

Ano! spine III length

33.4

30.9

30.8

Soft dorsal fin base length

52.3

43.7

45.3

Anal fin base length

32.1

27.6

31.0

Pelvic fin spine length

31.7

28.8

30.3

Pelvic fin length

48.0

42.7

44.5

Pelvic insertion to midvent

45.4

46.5

45.6

Midvent to anal fin

11.5

Il.O

11.3

Longest dorsal fin spine

length

29.8

29.3

28.2

Longest dorsal soft ray

ength

29.2

26.7

27.2

Longest anal soft ray length

37.9

35.7

35.4

SIZE OF BODY PARTS

Metrical data on 30 characters are summar-

ized in Tables 2-4. Two methods for fitting re-
gressions of measurements on standard length

393

FISHERY BULLETIN: \'0L. 69, NO. 2

Table 3. — Regression of measurements (Y) on SL (X) in the point-slope form of the log-transformed allometric
equation Y =: aX'' over the interval 109<SLmm<286, Sehastes variegatus.

Character (No. specimens)

4(±95%)i

Head length (38)

Upper jaw (38)

Prenarial pore (38)

Subnoriol pore (38)

Orbit (38)

Interorbital (38)

Raker (37)

lower jaw projection (35)

Snout (35)

Suborbital (35)

Head width (34)

Pectoral fin (35)

Pectoral base (38)

Cauda! peduncle depth (35)

Dorsal caudal peduncle (35)

Ventral coudol peduncle (35)

Body depth (pelvic) (38)

Body depth (anal) (35)

Anal spine I (38)

Anal spine II (37)

Anol spine III (35)

Soft dorsal base (35)

Anal base (35)

Pelvic fin spine (34)

Pelvic fin (38)

Pelvic insertion to midvent (38)

Midvent to anal fin (35)

Longest dorsal fin spine (36)

Longest dorsol soft ray (34)

Longest anal soft ray (35)

2,26567

1.80164

1.03704(±0.02555)*

0.0100

0 995

2.26567

1 .46445

I.00526(±0.03700)n,s.

0.0100

0,988

2.26567

0.12076

0,68961 (±0,22125)-

0,4499

0.526

2.26567

0.36358

0,64076(i0, 15785) •

0.0510

0.653

2.26567

1 .29809

0,89650(±0,07000)•

0,0224

0.949

2.26567

1.10458

1.17465(±0,05915)-

0.0200

0,978

2.26051

1 .02983

0.99778(±0.09776)n.s.

0.0300

0,926

2.26552

0.59671

1. 40000(±0. 18610) •

0.0583

0.876

2.26552

1 .20640

1.05453(i0.05560)n.s.

0.0173

0.978

2.26552

0.39634

0,76861 (±0,I7I85)-

0.0539

0.714

2.27223

1.47624

l,03266(±0 07375)n,s.

0,0224

0,962

2.26539

1.71905

0.96682(±0,04611)n.s.

0,0115

0.982

2.26539

t .24749

0,95907;±0,04845)n,s.

0,0144

0.979

2.25292

1.21462

0,93501 (±0,05720)'

0,0173

0.971

2.26552

1.42222

0,98447(±0.068S5)n,s.

0,0224

0.962

2.26552

1 .59340

0,92085(±0,04905)-

0,0141

0.978

2.26567

1 .74993

1.01305(±0.06455)ns,

0,0200

0.966

2.26552

1 .66765

0,89023(S:0,06100)-

0,0200

0.964

2.26567

1 .20583

0,81995(±0,10465)'

00332

0.876

2.26051

1 ,54643

0,735I9(±0,06340)*

0,0200

0.940

2.26552

1 ,46436

0 83416l±0,05255)'

0,0173

0.968

2,26552

1 .63887

0,90102(±0.10955)n,s.

0,0346

0.894

2.26552

1 .46978

0.81406(±0,07225)'

0,0224

0.941

2,26648

1.45182

0,852 1 8(±0,04725)'

0,0141

0.976

2,26567

1 .62047

0-93l85(±0 035951-

0,0100

0.987

2,26567

1,63431

1.15544(i0.ll405)'

0,0361

0.922

2.26552

1 ,00595

1 10201(±0-25370)n.s.

0.0794

0,703

2.26180

1 .40658

0.94004(±0.09285)n,s.

0.0283

0.926

2.26648

1 .42402

0,96599(±0,08310)n,s.

0.0265

0,945

2.26552

1.54610

0.97441 (±;0,04500)n.s.

0,0141

0,983

1 Asterisk indicates a difference in the slope exponent (i) significantly different from unity at the 95%
ence at this confidence level.

n,s. indicates no significant differ-

were explored, the power or allometric equation,
Y — aX'", in logio transformed form, and the
first degree or rectilinear equation, Y — a + bX,
untransformed. Both functions were fit by a
computer regression program (Sokal and Rohlf,
1969:696). Degree of fit was judged by the
"coefficient of percentage variation explained by
regression," the square of the correlation co-
efficient for regression, /- (Table 3). In 18 of
the 30 characters, nearly identical r^'s were ob-
tained by the alternative equations, including
9 characters for which the allometric exponent
differed in a minor (<0.20) but significant de-
gree from unity at the 95% confidence level,
i.e. the growth relationships seemed to depart
significantly from isometry. Plots of selected
examples from the nine characters showed only
minor differences between the two functions in
these instances. In four comparisons, three of
which showed significant departure from unity
in the allometric exi)onent (subnarial pore, low-
er jaw projection, and suborbital), the first-

degree equation appeared to give a superior fit.
For the remaining eight comparisons, the allo-
metric equation was superior.

In the light of these considerations, the logio
transformations of the allometric equation (log
Y = log a + b log X) was chosen for general
application because it is more versatile and gave
a satisfactory fit in all comparisons. Those
few characters which were fit somewhat better
by the first-degree equation appear to be of rel-
atively minor utility in rockfish systematics.
Parameters are presented in the point-slope
form of^ the transforrned allometric equation
{Y = Y + b (X — X), where Y = logic Y
and X = logio X) to emphasize the working in-
terval about the means of the variates and to
de-emphasize the I'-intercept which has no
theoretical value in these representations.

The measurements are also presented in the
form of Q^-i'r confidence limits for proportions
of future individual specimens, based on the
material examined (Table 4). The limits were

394

QUAST; Srbaitrs vmirsatus SP. N.

Table 4. — Upper and lower 95% confidence limits for
single future observations on proportions (percent of
SL), based on the material examined.'

Character

Standard length

(mm)

120

160

200

240

280

Head length

35-52
32.19

35-84
32-59

36.13
32.86

36.40
33.06

36.64
33.22

Upper jow

16-56
15.01

16 56
15-06

16.58
15.08

16.61
15 08

16.64
15.08

Prenariol pore

1-16
0-58

1.05
0.53

0.93
0.50

0.93
0.47

0-89
0-44

Subnorial pore

1-88
1.14

1.68
1.04

1.55
0.96

1.46
0.89

1-39
0-84

Orbit

12-57
10,09

12.16
9.33

11.88
961

11.67
9.42

11-52
9-25

Interorbrtal

7.06
5.80

7.40
6.12

7.70
6.37

7.96
6.57

8-19
6-73

Raker

6.82
5.08

6.78
5.10

6.78
5.10

6.79
5.08

6-81
5-07

lower ]av/ projection

2-41
1-35

268
1.53

292
1 68

3.16
1.80

3-38
1.90

Snout

9-29
7.83

9.41
7.97

9.52
8.07

9.63
8.14

9.73
8.20

Suborbital

1-95
1-14

1.81
1.08

1.71
1.03

1.65
0 98

1.60
0-94

Head width

17-63
14-10

17.71
14.30

17,83
14,41

17.97
14.48

18-11
1451

Pectoral fin length

30-52
27 23

30.17
27.03

29.95
26.83

29 79
26.65

29 67
26-48

Pectoral base

10-46
9-11

10.32
9.02

10.22
8.94

10.15
8.86

10.11
8.80

Caudal peduncle depth

10-24
8-63

10.02
8.49

9 87
837

9.77
8.26

9.70
8.16

Dorsal caudal peduncle

16-13
12-93

16.00
12.92

15.94
12 88

15-91
12-83

15.91
12.76

Ventral caudal peduncle

23-60
20-52

23.02
20.11

2261
19.76

22-31
19-46

22.07
19.20

Body depth (pelvic)

33-46
27 49

33.48
27.68

33.56
27.77

33-69
27-80

33.83
27-80

Body depth (anal)

29-21
23-97

28.20
23.30

27 51
22.75

27-01
22-27

26-61
21.84

Anal spine 1

11-08
8-00

10.46
7.64

10 05
7 34

9-74
7.09

9.51
6.87

Anal spine II

23 81
19-55

21.99
18.18

20 72
17.14

19.77
16.31

19,03
15,62

Anal spine III

18-49
15 58

17.58
14.90

16.93
14.36

16.45
13.92

16.06
13.54

Soft dorsal fin base

29 25
2077

28.26
20.31

27 63
19.87

27.20
19.47

26.89
19.11

Anal fin base

21-70
13-85

20.39
13.24

19.43
12.79

18.68
12.43

18.07
12.14

Pelvic fin spine

17-52
15-23

16.75
14.63

16.20
14.16

1578
13.77

1545
13.44

Pelvic fin length

24-68
2238

24,17
21.98

23.80
21.65

23.52
21.37

23.30
21.12

Pelvic insertion to
midvent

26-13
18-33

27.16
19.28

28.11
19.97

23.98
20.50

29.80
20.92

Midvent to anal fin

7.80
3.56

7.92
3.71

8.09
3 80

8.29
3.85

8.49
388

Longest dorsal fin spine

16-46

12-45

16.10
12.30

15.88
12.14

15.74
11.98

15.64
11.83

Longest dorsal soft ray

16-63
12-79

16.39
12.73

16.26
12.64

16.19
12.54

16-15
12-44

Longest onal soft ray

20-69
17-99

2049
17.90

20.37
17.80

20.29
17.70

20-24
17-61

' Based on confidence belts for individual predicted measurements
(Soliial and Rohlf, 1969:422) from the parameters for regression (Table 3).
Dota were bacl<-transformed to orjthmetic values for computation of pro-
portrons. If limits ore desired in the form of measurements, the percent-
ages moy be multiplied by the appropriate SL.

obtained from dn'r confidence limits for fits to
regression (Table 3) back-transformed to the
original variates and converted to percent of
standard length. Marr (1955) discussed the
disadvantages of using proportions in syste-
matics, particularly when size-specific changes
are not identified, but neglected several advant-
ages. Size-specific changes are here identified,
and the presentation of data in the form of pro-
portions facilitates rapid comparisons between
specimens and allows data on measurements to
be presented more economically than in graphs.
Proportions vary much less with length than
original measurements, sometimes surprisingly
little when the numerous factors that influence
their variation are considered (Table 4), and
therefore allow easier interpolation between
tabulated reference points than representations
of original variates. Also, the continued use of
pi-oportions in fish systematics, often without
indication of size-specific changes, attests to a
prevailing opinion that proportions are useful
despite their occasional misuse and other draw-
backs.

Plots of the limits for proijortions (Table 4)
disclose that they are slightly curvilinear and
asymmetrical from left to right. These char-
acteristics reflect the y-intercept effect dis-
cussed by Marr (1955) combined with the ef-
fects of normal divergence of confidence belts
in regression with distance from the combined
mean, allometry between the original variates,
and distortion caused by back-transformation
from the logarithm of a function. Size-specific
confidence limits for proportions whose allomet-
ric coefticients did not differ significantly from
unity (Table 3) are included in Table 4 because
the calculated value is a better estimate of the
exponent than is arbitrarily assumed isometry.

AXIAL SKELETON

X-rays of types show 27 vertebrae, including
urostyle (Table 1). Pterygiophores of spinous
dorsal fin single in spaces between neural spines
except between neural spines 2 and 3, which
contains pterygiophores of dorsal fin spines 2
and 3. Pterygiophores of soft dorsal fin usually
doubled in interneural spaces except single pre-

395

FISHERV BULLETIN. \0L. 69, NO. 2

ceding neural spines 5 and 8 or 9. Caudal skel-
eton apparently with hypurals 2 and 3 and 4 and
5 fused into upper and lower plates, respectively,
as determined for other scorpaenid representa-
tives by Quast (1965:580). Point of enlarged
pterygiophore that supports anal fin spines I
and II contacts haemal arch of 11th vertebra,
here considered the first caudal vertebra.

ELECTROPHORETIC PATTERN

A standardized starch gel electrophaerogram
of haemoglobin from a male adult S. variegatus
(BC 70-2, from Queen Charlotte Sound, British
Columbia), with comparative material on S.
zacentrus, was kindly furnished by Henry Tsu-
yuki of the Fisheries Research Board of Canada
(Figure 4).'

S. variegatus
S. zacentrus

I I S. variegatus
I I S. zacentrus

t

Figure 4. — Comparative starch gel electrophaero-
grams of the haemoglobins from S. variegatus and
S. zacentrus furnished by Henry Tsuyuki, Fisheries
Research Board of Canada (see text). The arrow
represents the origin in the schematized pattern.
The anode is to the right and the cathode to the left.
The minor cathodal zone, which Tsuyuki found to be
consistently diagnostic for the two species, could not
be reproduced photographically and is shown in
schematic form in approximately the concentrations
found.

' Vancouver Laboratory, 6640 NW. Marine Drive,
Vancouver 8, British Columbia, 28 July 1970. "f:ry-
throcytes were washed once with a 1% sodium chloride
solution before hemolysis to avoid contamination from
serum proteins. Haemoglobins from washed and un-
washed red cells possessed identical patterns." For
methods used in obtaining blood samples and for elec-
trophoresis, see Tsuyuki et al. (1968). Identity of the
S. variegatus specimen verified by the author; how-
ever, the specimen had a head size much larger than
normal (38.3% of SL) and was the only specimen out
of 40 seen that had 6 soft rays in the anal fin instead
of 7.

SIMILAR SPECIES

Sebastes variegatus resembles S. emphaeus, S.
proriger. S. saxicoki., S. ivilsoni, and S. zacentrus
in morphology, morphometry, meristics, and col-
oration. The six species appear to be closely
related members of a complex that generally
shares the characters of S. variegatus other than
the pectoral count of 18, the unpigmented band
that encloses the lateral line and extends about
2/3 along the body sides, and the black color-
ation of the spinous dorsal and caudal fin mem-
branes. The complex may also include S. dalli,
S. elongatus, S. jordani, and S. semicinctus
which also seem to resemble the six species, but
these appear to be easier to diflFerentiate from
S. variegatus and I do not further consider them
here. Although the analyses of rockfish haemo-
globin and muscle proteins by Tsuyuki et al.
(1968) shed little light on the group's validity,
subsequent work by Tsuyuki (see footnote 3)
suggests a close relationship between S. varie-
gatus and S. zacentrus (Figure 4). The possi-
bility that S. variegatus represents a hybrid may
be dismissed because of a normal degree of var-
iation in measurements, distinctiveness and con-
sistency of pectoral ray counts and body col-
oration, abundance of specimens, and normal
reproduction as indicated by normally developed
gonads and gravid females.

As a natural group, the six species do not ap-
pear to coincide with those at the subgeneric
level erected by Cramer, Eigenmann, and Beeson,
or Jordan and Evermann, as described by Jord-
an and Evermann (1898. II: 1765-1777). How-
ever, in some respects it does resemble the sub-
genus Hatumeus, erected by Matsubara (1943b:
192) under Sebastes. and the type species, Se-
bastodes owstoni, as figured by Jordan and
Thompson (1914: pi. 31, fig. 3).

Ranges of meristic characters for most spe-
cies in the hypothetical grouii (from Phillips
(1957) plus personal examination of representa-
tives— Table 5) either are nearly identical (soft
rays in the dorsal, anal, and pectoral fins) or
overlap broadly (pored scales in the lateral line,
gill rakers, and .scale rows below lateral line).
In characteristics for which most of the group
are nearly identical, S. variegatus deviates mark-

396

QUAST: Stballn varirgatus SP. N.

Table 5.— Data and material for species comparisons

with Sehastes variegattts.

Phillips (1957)

Material examined

Species

No.
Specimens

Meristics

No.
specimens

Meristics

No. SL

No.

SL

S. emphaeui

_.

7

7

101-131

S. proris^r

7

6

230-389

12

12

161-270

S. saxicola

35

9

103-308

__

—

S. uilioni

3

3

102-133

6

6

50-174

S. zaantruj

15

10

166-338

20

20

133-281

edly only in pectoral count. In those species
where means of characteristics differ noticeably
but ranges overlap broadly, S. variegatiis usu-
ally is of central value, which suggests that it
may be a more generalized member of the group.

Comparisons of morphometric characters be-
tween S. rariegatus and the other species lead
to a similar conclusion. Ranges for the species
overlap broadly, based on Phillips (1957) and
my own measurements (head length, longest
dorsal fin spine, least depth of caudal peduncle,
pelvic insertion to vent, raker at bend of gill
arch, width of pectoral fin base, body depth at
pelvic girdle, bony interorbital, orbit, length of
pectoral fin, length of pelvic fin, and length of
upper jaw — in percent of standard length).

To assist difl'erentiating S. raiiegatus from
similar species a table of discriminatory charac-
ters is presented (Table 6).

GEOGRAPHIC AND BATHYMETRIC RANGE

Present known range of S. variegatns is from
Unimak Pass, Aleutian Islands, to Goose Island
Bank, Queen Charlotte Sound' (Figure 5).
Depth of capture ranges from 70 to 305 m.

ACKNOWLEDGMENTS

William I. Follett (California Academy of
Sciences), Warren C. Freihofer (Stanford Uni-
versity), and Norman J. Wilimovsky (Univer-
sity of British Columbia) gave permission for
examination of collections or shipped material.

' The record for Queen Charlotte Sound was obtained
by Sigurd J. Westrheim, Fisheries Research Board of
Canada, Nanaimo Research Station, Nanaimo, British
Columbia, on the RV G. B. Reed during Cruise GBR
70-1 (personal communication, 5 August 1970).

Table 6. — Summary of salient comparative features of
Sebastes variegatus with five similar speces. (Propor-
tions of S. variegatus refer to 95% confidence limits of
Table 4. Source and quantity of data on other species
are summarized in Table 5. Code for sources: *, Phil-
lips (1957); **, original material (Tables 1-4); ***,
both sources. In some instances my data on northeastern
Pacific specimens differ from Phillips (1957) in degree
of discrimination.)

S emphaius.

Counts: Pectoral rays 17 (occos. 18)*', varie^atui 18 (occos. 17); scale
rows ^46*, variegatus ^46. Percent of SL (opply to interval of size
overlap, 109-131 mm): Upper jaw ^15.0*', variegatus ^15.0; vent-
ral caudal peduncle ^20,8**, variegatus ^20.5; anal spine I ^8.3**,
variegatus ^8.0; anal spine II ^19. 4**, vartegatus ^19,6; anal spine
III $15.8"*, variegatus ^15-6, Pigmentation: Blotches on sides not
interrupted by an unpigmented bond along laterol line; no black area
on fin membrane between anal spines II and 111 (both choracteristics
from pi. 31 of Storks, 1911).

S. proriger.

Counts: Pectoral rays 17*" (occos. 18)'*, variegatus 18 {occos. 17);
scale rows ^55* {47-56)*', variegatus $58. Percent of SL (apply to
interval of size overlap 161-270 mm, for Quost doto): Upper jow $14.7"
($15.7)**, variegatus ^15-1; orbit $9.3' ($10.5)"*, vartegatus >9.3;
anol spine II $15.4* ($16.4 but normally below 95% limits of var-
iegatus at size [Table 4])"*; anal spine 111 {below 95% limits of
variegatus at size [Table 4])**; pelvic fin (below 95% limits of var-
iegatus at size [Table 4])**, longest dorsal soft ray $12.5*, variegatus
^12.4; longest anal soft ray $16.1", variegatus '^\7.6. Pigmentation:
Unpigmented band along lateral line extends to head.

S. saxicola.

Counts: Dorsa! soft rays 12 (occas. 13)*, variegatus 14 or 15 (occas.
13); pectoral roys 16 (occos. 15 or 17)*, variegatus 18 (occas. 17);
lateral line pored scales $42*, variegatus ^42; raters $34*, variegatus
S36. Percent of SL: heod 535.7*, vartegatus $36.6; orbit ^11.8*,
variegatus $12.5; longest onol soft ray $18.2*, variegatus ^\7.6.
Pigmentation: Blotches on sides not interrupted by unpigmented bond
along loteral line.

S. wtlsoiti.

Counts: Anal soft rays 6*'* .variegatus 7 (rarely 6); pectoral rays 16-17*
(occos. 18)**, variegatus 18 (occos. 17); lateral line pored scales $41*
($43)**, variegatus ^42; scale rows 45-50* (41-45)'*, variegatus >46.
Percent of SL (apply to interval of size overlop, 109-174 mm, in Quost
doto): pelvic fin length $22.0**, variegatus ^22.0. Pigmentation:
Dork blotches on sides not interrupted by an unpigmented bond along
lateral line.

S. zaeentrus.

Counts: Pectoral rays 17 (occos. 18)*, (occas. 19)**, variegatus 18 (rarely
17 or 19)**; scale rows 43-50* ($47)**, variegatus ^46; rokers $37*
($38)**, variegatus 536. Percent of SL (apply to interval of size over-
lap, 133-281, for Quost data): Upper jow 15.6-16.9* (normally above
95% limits of variegatus at size [Table 4])**; longest anal soft ray
$17.9*, variegatus 517.6. Pigmentation: Blolchts on sides not inter-
rupted by unpigmented bond along lateral line.

/ '

1111

4,000-*

CONTOUR

^ oXA

^/Ov^^-»^

_

U-

%

--j^r^

.'m _

•>•..-■

GULF OFALASKA

•

.':.:;;..__

1111

170* 165° 160*

150- H5* I40' 135* 130*

Figure 5. — Localities at which Sebastes variegaUis
were captured.

397

FISHERY BULLETIN. VOL. 69, NO. 2

Sigurd J. Westrheim ( Fisheries Research Board
of Canada, Nanaimo Research Station) fur-
nished fresh material and reviewed the manu-
script, and Henry Tsuyuki (Fisheries Research
Board of Canada, Vancouver Laboratory) con-
tributed the haemoglobin electrophaerograms.
Daniel M. Cohen (United States National Mu-
seum) , William N. Eschmeyer (California Acad-
emy of Sciences), and Bruce L. Wing (National
Marine Fisheries Service Biological Laboratory,
Auke Bay, Alaska) provided editorial and sci-
entific comments.

LITERATURE CITED

Brown, W.

1956. Composition of scientific words. The author,
Washington, D.C., 882 p.
Chen, L. C.

1969. Systematics, variation, distribution, and bi-
ology of rockfishes of the subgenus Sebastomtis.
Ph.D. Thesis, Univ. Calif., San Diego, 266 p.
Eschmeyer, W. N.

1969. A systematic review of the scorpionfishes of
the Atlantic Ocean (Pisces: Scorpaenidae). Oc-
cas. Pap. Calif. Acad. Sci. 79, 143 p.
HUBBS, C. L., AND K. F. Lagler.

1949. Fishes of the Great Lakes region. Cran-
brook Inst. Sci., Bull. 26, 186 p.
Jordan, D. S., and B. W. Evermann.

1898. The fishes of North and Middle America.

Bull. U.S. Nat. Mus. 47, Part 2: 1241-2183.
Jordan, D. S., and W. F. Thompson.

1914. Record of the fishes obtained in Japan in
1911. Mem. Carnegie Mus. 6(4): 205-313.
Mark, J. C.

1955. The use of morphometric data in systematic,
racial, and relative growth studies in fishes.
Copeia 1955: 23-31.
Matsubara, K.

1943a. Studies on the scorpaenoid fishes of Japan:
anatomy, phylogeny and taxonomy (I). Trans.
Sigenkagaku Kenkyusyo 1943: 1-170.
1943b. Studies on the scorpaenoid fishes of Japan:
anatomy, phylogeny and taxonomy (II). Trans.
Sigenkagaku Kenkyusyo 1943: 171-486.
Phillips, J. B.

1957. A review of the rockfishes of California
(Family Scorpaenidae). Calif. Dep. Fish Game,
Fish Bull. 104, 158 p.
Quast, J. C.

1965. Osteological characteristics and affinities of
the hexagrammid fishes, with a synopsis. Proc.
Calif. Acad. Sci., 4th Ser. 31: 563-600.

SOKAL, R. R., and F. J. ROHLF.

1969. Biometry. Freeman, San Francisco, 776 p.
Starks, E. C.

1911. Results of an ichthyological survey about
the San Juan Islands, Washington. Ann. Car-
negie Mus. 7: 162-213.
TsiTYUKi, H., E. Roberts, R. H. Lowes, W. Hadaway,
and S. J. Westrheim.

1968. Contribution of protein electrophoresis to
rockfish (Scorpaenidae) systematics. J. Fish.
Res. Bd. Can. 25: 2477-2501.

398

CALICO SCALLOP DISTRIBUTION, ABUNDANCE, AND YIELD
OFF EASTERN FLORIDA, 1967-68'

Richard B. Roe," Robert Cummins, Jr.,' and Harvey R. Bullis, Jr.*

ABSTRACT

During 18 months, from August 1967 to December 1968, the National Marine Fisheries Service Explor-
atory Fishing and Gear Research Base in Pascagoula, Miss., conducted a comprehensive survey of the
calico scallop (Argopecten gibbiis) grounds off eastern Florida. The survey disclosed various aspects
of the life history, distribution, abundance, and yield and annual variation in geographical and depth
distribution. Predictions for a fall fishery are possible since distribution and abundance are established
at spat set and can be delineated by midsummer. A fall fishery is recommended as catch rates and
yield were highest between September and December and decreased rapidly during late winter and
spring.

There are two or more species of Argopecten
called "calico" scallops (Waller, 1969); how-
ever, the more common is A. gibbus (L.). This
is the species involved in our study, occurring
from Delaware Bay to the Caribbean Sea and
throughout the Gulf of Mexico (Johnson, 1934;
Bullis and Ingle, 1959; Carpenter, 1967; Waller,
1969). Calico scallops derive their name from
the blotched coloration of their shells which
vary from red to light brown on a white back-
ground, giving a "calico" effect to the shell.

Three commercial grounds have been delin-
eated by the Exploratory Fishing and Gear Re-
search Base at Pascagoula, Miss., and its Field
Station in Brunswick, Ga. These are located
off North Carolina (Cummins, Rivers, and
Struhsaker, 1962) , off eastern Florida near Cape
Kennedy (Bullis and Cummins, 1961; Cummins,
et al., 1969;' Drummond, 1969), and in the

' Exploratory Fishing and Gear Research Base, Pas-
cagoula, Miss., Contribution No. 232.

" National Marine Fisheries Service Exploratory
Fishing and Gear Research Base, Pascagoula, Miss.
39567.

' National Marine Fisheries Service Exploratory
Fishing and Gear Research Station, Brunswick, Ga.
31520.

' National Marine Fisheries Service, Washington,
D.C. 20240.

' Cummins, R., Jr., R. Maurer, L. May, and J. Rivers.
1969. Summary log of scallop locations with predicted
catch rates of Cape Kennedy grounds — fall 1969. Is-
sued by Bureau of Commercial Fisheries Exploratory
Fishing and Gear Research Field Station, Brunswick,
Ga., for limited distribution.

Manuscript received January 1971.

FISHERY BULLETIN; VOL. 69. NO. 2. 1971.

northeastern Gulf of Mexico (Bullis and Ingle,
1959; Carpenter, 1967). Explorations had
shown a large resource exists, particularly off
Florida, but monthly and yearly changes in dis-
tribution and abundance had seriously hampered
delineation of the resource.

In August 1967 an 18-month survey was ini-
tiated on the Cape Kennedy grounds to assess
the scallop stock and determine the causes of
variation in distribution, abundance, and yield.
These grounds were selected because of size,
location, and a developing industry.

The survey provided information on the dy-
namics of the scallop population present at that
time, but there is a need for additional studies
on life history, age, and growth.

METHODS

Cruises were conducted monthly between Au-
gust and December 1967, and bimonthly between
February and December 1968. Four standard
transects, each extending from 10 to 40 fm, were
made on each cruise. These were: transect A at
lat 28°03' N, transect B at lat 28°27' N, transect
C at lat 29°03' N, and transect D at lat 29°25' N
(Figure 1). Tows were also made between
transects. An 8-ft scallop dredge, fitted with
2-inch bag rings and 21/2-inch mesh nylon liners,
was used in the survey. All tows were 30 min.

399

FISHERY BULLETIN; VOL. 69, NO. 2

Figure 1. — General distribution of calico scallops and
four standard transects occupied during the 1967-68
survey off the Florida east coast.

ploratory Fishing and Gear Research Base at
Pascagoula, Miss.

The survey results are subdivided according
to spawning, age and growth, mortality, distri-
bution and abundance, and yield.

SPAWNING

Bourne and Bligh (1965) found sea scallop
(Placopecten niagellanicus) ovaries change
color during maturation, progressing from pink
at early stages to deep coral-red when ripe.
Color changes were also noted in calico scallop
ovaries, undeveloped ovaries being whitish, ripe
ovaries bright reddish-orange.

Yellowish-orange coloration was seen in very
few scallops during the August cruise, but by
September the rate and incidence of color change
was highly noticeable. Coloration and incidence
increased into fall and winter and by February
ovaries were predominantly reddish-orange or
ripe. The majority of ovaries taken in April
were bright reddish-orange. June ovaries were
largely uncolored.

Sexual maturation in sea scallops begins in
March, spawning occurring 7 months or so later
in September or October. Calico scallops ap-
parently have a similar maturation period based
on color change progression which begins in
August and ends in March or April. Protracted
spawning does take place in some areas since
small numbers of 5 to 30 mm scallops occur
throughout the year (Figure 2).

A total of 1,483 drags was made during the
survey — 285 in transect A, 403 in transect B,
493 in transect C, and 302 in transect D. The
following were determined for each drag: total
catch in bushels (using a standard steel shrimp
basket averaging 70 lb.), number of bushels of
live scallops, pounds of meat per bushel, number
of pints of meat per bushel, number of meats per
pint, and size frequency (measured as shell
diameter in millimeters). Randomly selected
individuals were examined for gonad coloration
and .sexual maturation. The data were analyzed
with the UNIVAC 9200 computer at the Ex-

Figure 2. — Monthly size/frequency distribution of scal-
lops for the combined transects off the Florida east coast
during the 1967-68 survey.

400

ROE, CUMMINS, and BULLIS : CALICO SCALLOP OFF FLORIDA

AGE AND GROWTH

Monthly size frequencies are shown in Fig-
ure 2. From June until September the distri-
bution is bimodal, but in October the lower mode
disappears and a single mode exists until April.
This is clearly illustrated in the 1968 data be-
ginning in June when modes occur at 11.9 and
62.1 mm. In August modes are present at 26.0
and 60.6 mm and in October at 34.0 and 61.5
mm. Only one mode at 51.0 mm occurs in De-
cember.

The lower mode value gradually increases
during this period while the upper mode de-
creases. These changes reflect a melding of year
classes caused by a more rapid growth rate in
the younger year class than in the older one. In
December the two year classes are indistinguish-
able. Since year classes cannot be separated
in the winter data, it is difficult to determine
when the older class disappears. Presumably
this occurs some time between December and
April.

Growth rates could not be accurately deter-
mined from the data because of gear selectivity
for the smaller sizes and because year classes
were often inseparable in the size-frequency dis-
tribution. A growth estimate was derived for
a selected bed located on transect C in 22 to 27
fm. The size-frequency data indicate two year
classes were present most of the survey period
( Table 1 ) . These are more distinct in the sep-
arated 1968 data (Table 2).

The mean size increases linearly by about
1.0 to 2.0 mm per month during August to Feb-
ruary (Table 1). From April to December the

Table 2. — Monthly size frequency data for transect C,
22 to 27 fm, divided by year class. Classes are 10 mm.

Size

Year c

ass A

Year class B

class

Juno

Aug.

Oct.

Dec.

Juno

Aug.

Oct.

Dec.

0-9

6

I

10-19

24

57

2

20-29

4

163

61

125

30-39

__

41

3

260

40-49

__

._

116

1

50-J9

_.

103

44

41

8

60-69

__

__

72

211

103

138

70-79

-

-

—

—

31

38

21

7

Mean

13.9

23.8

25,7

37.8

63-5

64.4

65.5

65.0

mean gradually decreases because of recruit-
ment from the spring spawn.

Since the age groups interact the means given
in Table 1 actually represent a combined year
class average. Therefore, the June to December
1968 data have been separated into two year
classes based on size (Table 2). Year class A
was spawned in the spring of 1968 and year
class B, representing the larger sizes, was
spawned in the spring of 1967. The monthly
mean for year class A increased curvilinearly
24 mm from June to December. Year class B
mean increased only 2.0 mm from June to Oc-
tober then decreased slightly in December. The
increase appeared linear.

Both year classes show evidence of a sigmoid
growth curve. Gibson (1956) gives a sigmoid
curve for Pecten maximus where time is mea-
sured in years rather than months as in calico
scallops.

MORTALITY

Calico scallops on the Ca]3e Kennedy grounds
e.xperienced light commercial exploitation prior

Table 1. — Monthly size frequencies for transect C, 22 to 27 fm, by 10-mm size classes,

1967-68.

Size

1967

1968

class

Aug.

Sept.

Oct,

Nov.

Dec.

Feb.

Apr.

June

Aug,

Oct

Dec.

0-9

__

__

6

1

10-19

1

4

_-

24

57

2

20-29

1

4

I

1

..

__

4

163

61

125

30-39

1

3

.,

3

3

__

_.

41

3

260

40-49

2

16

3

7

4

38

1

116

5059

11

58

72

23

38

295

185

44

41

8

103

60-69

9

42

43

39

25

567

343

72

211

103

138

70-79

2

18

2

7

1

28

46

31

38

21

7

80-89

-

-

-

-

-

-

1

—

--

--

--

Mean

55.2

56.4

57.9

59.1

58.7

61.3

61.0

54.2

45,1

51.9

430

401

FISHERY BULLETIN: VOL. 69. NO. 2

to 1967. Landings in 1967 totaled approximately
5,000 bu and although several vessels fished the
area in 1968, the overall catch was light. Mor-
tality during the survey period was therefore
assumed largely due to natural causes.

Catch curves using Ricker's (1958) method
of plotting loge (average number per drag per
month) were constructed (Figure 3). A linear

Transect A

H \ 1-

H — I — I — I-

A, B Old C CombinM

Figure 3. — Catch curves for transects A, B, C, and
combined.

regression was applied to the descending curve
according to Beverton and Holt (1957), using
b as an estimate of F -{- X. Since F was negli-
gible, b is an estimate of X or natural mortality.
The instantaneous mortality rate (0 is equal to
b and the monthly mortality rate (a) was de-
rived from Ricker's appendix.

Data used in the analysis represented the 1967
year class except in transect D where catch

data were too sparse for analysis. December
1968 data were not available except for transect
C. October 1968 was omitted from transect A
because of insufficient data.

The ascending left limb of the curve reflects
recruitment. Mortality during this period is
diflicult to determine because small scallops are
inaccessible to the dredge. The dome varied
among transects but occurred from October to
December or February. The descending limb
extended from December to October (August
in transect A). All limbs are curvilinear but
vary in shape. The curve for transect A is vari-
able. That for transect B is concave from Feb-
ruary to June then becomes convex. Transect
C curve is almost linear.

Monthly mortality rates, computed assuming
a linear relationship (as in Beverton and Holt,
1957) , are given in Table 3. Two time periods

Table 3. — Monthly mortality rates (a) and instanta-
neous mortality rates (i) for transects A, B, and C,
individually and combined, for various time periods.

Transect

Time period

i

a

A

10/67-12/67
12/67- 8/68

-0.012
-0.327

%

1

27

B

10/67-12/67
12/67-10/68

-0.365
-0.286

31
25

C

10/67-12/67
12/67-10/68

-0-150
-0.236

14
21

COMBINED

10/67-12/67
12/67-10/68

-0.020
-0.189

2

IS

C (22-27 fm)

2/68-10/68

-0.231

21

were treated: one from October to December
(the optimum fishing season) and the other from
December to October (the descending limb).
The latter period includes the spawning season.
Although accurate rates for the first period
(the dome) could not be accurately ascertained,
a crude mortality estimate was desired for the
fishing season.

Monthly mortality rates ranged from 1% to
31% for the dome and 18% to 27% for the
descending limb. Averages were 12% and 23%
respectively.

Age classes were difficult to distinguish and
all data may not have been from the 1967 year
class. This could have caused difl'erences in the

402

ROE, CU\L\11NS. and BL'LLIS: CALICO SCALLOP OFF FLORIDA

catch curves. To test this possibility, data from
a bed of known age composition were used to
construct a catch curve. This bed, located at
lat 29° 16' N in 22 to 27 fm on transect C, was
established in August 1967 and can be accurately
traced through October 1968 with length-fre-
quency data.

The catch curve for the bed (August 1967
to October 1968) is given in Figure 4. Recruit-

9

1 1 \ 1

1 1 1 I

Tnrsecl C

__^ 22-27 FATHOMS

^

B

e>—-® ®

^^^^^®^

-

7

;/

^^\

-

s

\v

1 5

-

\

"

. 4

s

3

_

\

N

2

-

! 1 1 1

1111

Figure 4. — Catch curve for transect C, 22 to 27 fm.
Data are for the 1967 year class.

ment in late summer and fall was strong. Re-
cruitment and mortality seem balanced from
October to February, but neither can be accu-
rately determined. The convex descending limb
(February to October) indicates a nonuniform
mortality rate, increasing rapidly after June
with the termination of spawning.

The February to October segment was treated
linearly to estimate monthly mortality. Results
were / = —0.231 and a = 21 Si (see Table 1).
Mortality rates for the dome (October to Feb-
ruary) were not calculated.

Although these rates are similar to those in
Table 3, enough discrepancy exists to indicate
more than one year class might have been in-
cluded in Table 3 data, causing some differences
in mortality rates. This does not jjreclude mor-
tality rate differences on the grounds.

The major calico scallop predator appears to
be the starfish {Asterias) which is often taken
in large numbers in dredge tows (Figure 5) and

has been seen by submarine observers feeding
on scallops (Figure 6). Rays and skates may
feed on calico scallops (Struhsaker, 1969) and
puffers (Sphoeroides) have been taken with
numerous small (2 to 5 mm) scallops in their
stomachs. Other predators are not known.

Little is known about those environmental fac-
tors affecting scallops though water temperature
is considered most important. Past explorations
have shown evidence of occasional mass mortal-
ities that may have been due to temperature
fluctuation. Dickie and Medcof (1963) reported
that mass mortalities often occur in sea scallops
when water temperatures fluctuate rapidly.
Further, temperature changes may indirectly
cause death through dehabilitation, thereby
rendering scallops highly susceptible to preda-
tion.

DISTRIBUTION AND ABUNDANCE

Calico scallops occurred in 13 to 37 fm with
greatest concentrations between 19 and 30 fm
(Figure 1).

Depth distributional differences north and
south of the Cape were noted (Figure 7). Scal-
lops south of the Cape were generally found
shallower than north of the Cape. The reasons
for this are unknown though the thermal struc-
ture may be different in these areas. Also the
shelf is narrower with a steeper gradient south
of the Cape, and available habitat is restricted.
Optimum bottom may occur 4 to 5 fm shallower
in that area.

A slight seasonal change in depth distribution
occurred in both areas. Scallops were in slightly
deeper water in winter than summer, this dif-
ference being less noticeable north of the Cape.

Yearly differences in bed distribution were
noted during the survey. In 1967 beds were
primarily located between 19 and 30 fm; how-
ever, in the fall of 1968 very few scallops oc-
curred in that depth range and a developing bed
was found at lat 29° 10' N in 15 to 17 fm. This
bed extended northward beyond lat 29°25' N.

Scallops were usually found in north-south
windrows several hundred yards to a quarter
mile long. Bed size varies but without a means

403

FISHERY BULLETIN; VOL. 69, NO.

V->^'

V

Figure 5. — Dredge catch of starfish aboard the RV Oregmi taken during an exploratory fishing survey on

the Cape Kennedy grounds.

of underwater observation there is no way of
mapping beds definitively. A remote-controlled
underwater assessment vehicle (RUFAS) has
since been used to survey the Cape Kennedy
grounds and preliminary data analysis verifies
our findings (Cummins et al., see footnote 5).
Major abundance occurred at slightly differ-
ent depth ranges north and south of the Cape
(Figure 8). Seasonal changes, while not no-
ticeable in these areas, did occur at some depth
ranges. Abundance was highest in 21 to 23 fm
south of the Cape and 24 to 27 fm north of the
Cape. By August 1968. scallops were gone south
of the Cape. North of the Cape the population

diminished through October 1968 and had prac-
tically disappeared by December.

YIELD

Yield is presented as pounds of meat per drag.
Preliminary calico scallop investigations had
used bushels per drag as a yield criterion, but
owing to differences in size, barnacle encrusta-
tion on the shell, and changes in meat condition,
the meat yield per bushel was highly variable.

Variation in bushel yield due to size differ-
ences is obvious, but the effect of barnacle en-
crustation is more subtle. The sedentary nature

404

ROE, CUMMINS, and BULLIS : CALICO SCALLOP OFF FLORIDA

^^jt^,

Figure 6. — Starfish (Asterias) observed attacking calico scallops during a submarine survey off Cape Kennedy

in September 1969.

405

FISHERY BULLETIN, VOL. 69. NO. 2

"T r

II

H \ h

Mil I III ■ I

I I I I

_1 I I I L-

OCT DEC FEB APB JUN AUG OCT DEC

FlGiTJE 9. — Average number of scallop meats per pint
by month during the 1967-68 Florida east coast survey.

FiGUBE 7. — Monthly depth distributions north and south
of Cape Kennedy.

30

1 1 1 1 1

1

1

1

1

1

1

25

|l-

1

■

1

■

-

1 ..

■

1.

1 1 1 1 1

1

1

1

1

1

1

X

t 50

1 1 1 1 1

1

1

1

1

1

1

o
25

ZO

•■'■

■

■

1

-

15

1 1 1 1 1

1

1

1

1

1

1

AUG OCT DEC FEB APR JUJ AUG OCT OEC

r967 1966

Figure 8. — Depths at which ma.ximum abundance
occurred north and south of Cape Kennedy.

of scallops enables a gradual buildup of bar-
nacles on the shell which decreases the number
of scallops per bushel. This leads to an over-
estimate of meat yield per bushel.

Meat condition was found to fluctuate season-
ally. From December to April meat counts in-
creased rapidly (Figure 9) owing to increased
flaccidity resulting from physiological changes

associated with spawning. Though most scal-
lops are generally large (50 to 60 mm) at spawn-
ing, the meat yield per bushel is much lower
than during the fall when scallops are smaller.

These conditions caused us to discard number
of bushels and use total pounds of meat p)er
drag as a more meaningful measurement of
yield.

Meat count per pint is an excellent inde.x of
fishing productivity when used in conjunction
with total pounds. A wide seasonal variation
in meat count was caused by differences in meat
condition and scalloj) size (Figure 9). From
August to December the meat count ])er pint
stabilized at 70 to 80. During December through
June the count increased due to deterioration
of meat firmness and or contribution by a non-
spawning population remnant.

The fall increase in meat count per pint is
due to increasingly large numbers of small scal-
lops entering the fishery from the shallow bed
on tran.sect C.

Commercially significant yields were taken be-
tween September and February with a maxi-
mum in October (Figure 10). Yield rapidly
decreased after February because of spawning.
Yield in the fall of 1968 was api)reciabiy lower
than in 1967 owing to the failure of the survey
to locate quantities of scallop. The population
in Uy to 17 fm at hit 29°10' X, spawned in 1968,
was not found in any abundance during the Oc-

406

ROE, CUMMINS, and BULLIS: CALICO SCALLOP OFF FLORIDA

OCT DEC

am juc

AUG OCT

Figure 10. — Average number of pounds of scallop meats
per 30-min drag by month during the 1967-68 Florida
east coast survey.

tober or December cruises, indicating spawning
occurred much later in 1968 than in 1967.

DISCUSSION

Reproduction in calico scallops is related to
age rather than size. It is probably triggered
by water temperature as Loosanoff and Davis
(1950) have shown that raising the ambient
water temperature induces spawning in some
bivalves. Since spawning generally occurs in
the spring, rising temperatures would be ex-
pected to be the initiating mechanism.

Maturation, taking 7 to 9 months beginning
in late summer, is easily detected in the field
by coloration changes in the ovaries. Resting
ovaries are whitish-yellow but as maturation
progresses their color changes through various
stages of deepening yellow-oranges to a reddish-
orange at the ripe condition. Ripe gonads have
been collected from a wide size range indicating
that the minimum age of sexual maturity is
quite low. Data indicate maturation does not
begin simultaneously in all scallops within even
the same bed. This presumably accounts for
the 2- to 3-month differential in maturation time.

Spawning begins in late February or early
March and continues to June. In some areas
the season is protracted since small scallops are

caught throughout most of the year. This is
probably due to variation in sexual maturation
rate, growth rates, and water temperature. The
lowest frequency of small scallops occurred in
February indicating decreasing temperatures
in the fall terminate any protracted spawning.

Protracted spawning during one season con-
ceivably leads to protraction during the next.
Since growth is related to temperature, scallops
spawned early in spring have a longer growing
season than do those spawned later in the year.
Therefore, the older individuals in a year class
would undoubtedly be larger at spawning than
the younger individuals. Further, maturation
is probably controlled by hormones which in
turn are influenced by some environmental fac-
tor such as water temperature. This interaction
between age, environment, and reproduction
needs clarification.

Growth curves through all sizes ranges can-
not be calculated from the survey data since
the earliest stages are omitted. The curve is
sigmoid from seed size to senility, rapidly in-
creasing from 5 to 50 mm. Then the rate de-
creases through senility with maximum size
about 80 mm.

Data from 1967 and 1968 indicate only one
year class is present in spring but two year
classes are present from early summer through
winter. Therefore, the maximum age reached
by calico scallops must not be greater than 24
months and averages 18 to 20 months.

Mortality rates computed from the survey
data support a 2-year maximum life span. Post-
spawning mortality averages 23 '^r per month.
At that rate only 20% of the year class would
remain by early fall. Assuming that some mor-
tality occurs during the pre-spawning period,
the remaining population in 18 to 20 months
would be exceedingly small.

Scallops are not randomly distributed but
form north-south windrow configurations.
These configurations, established at spat set, are
heavily influenced by currents. Olsen (1955)
indicates that windrow-like configurations result
from strong tides, their orientation running
lengthwise to the tide. He also shows strong
linear configurations result in eddy systems.

407

FISHERY BULLETIN; VOL. 69. NO. 2

This latter situation is ana]og:ous to that off
eastern Florida. Little is known about substrate
preference. Some beds offering optimum con-
ditions may be perpetuated for several years,
but competition for space between adults and
spat must minimize such occurrences. If spat
are unable to compete effectively for substrate,
the presence of live adult scallops on the bed
may prevent spat set. This question needs to
be answered in the near future.

Yearly distribution and abundance depend on
both spawning success and spat set. Commer-
cial size and abundance are generally reached
by early fall, usually in October. Fishing re-
mains optimal until February when catch rates
and yield decrease. This is due to spawning and
associated factors such as increased mortality
and meat deterioration.

In October 1967 scallops averaged about 45 mm
and yielded 75 to 80 meats per pint. During Oc-
tober the survey produced an average catch of
70 lb. of meats per 30-min drag as compared with
20 lb /drag in April.

A fall and early winter fishery is expected to
be most productive. Fishing is not recommend-
ed during spring because catch rates and yield
are generally low and a spring fishery could
have an adverse effect on the spawning popu-
lation.

The nonrandom distribution and variable size
of beds make it diflicult to estimate the standing
crop from dredge surveys. Scallops were found
over approximately 285 square miles of bottom
during the survey but less than 14% (37 miles)
was covered by the dredge. About 6,500,000
scallops were caught during the survey. Scal-
lops are not randomly distributed on the grounds
but occur in beds where very high densities are
often reached. Relatively few individuals occur
between beds. Beds are diflicult to measure but
some were estimated to be several hundred yards
in width and over a half mile in length.

Photographs taken during the Alummaut dive
show that densities of five scallops per square
foot occur on some beds (Taylor, 1967). A
minimum of 285 square miles of scallop bottom
was found during the survey and varied densi-
ties occurred over that area. If 10% (28 square

miles) supported densities approximating those
found by the Alumiuaut, then an estimated
standing crop of 3,892,000,000 scallops existed in
1967-68. This figure is derived from the fol-
lowing: 28 X 27.8 million (no. ft= /mile') X 5.
That population could easily support 10 boats
fishing at a rate of 1,500 lb day. At an average
of 70 scallops per pound, 10 boats would take a
total of 31,500,000 scallops per month at the
above rate. This is approximately I'^'r of the
estimated standing crop.

Recent explorations with RUFAS indicate
that densities estimated from the Ahiminaut
cruise may be ultraconservative (Cummins et
al., see footnote 5). Films from the RUFAS
survey indicate that scallops may reach densities
as high as 10 or more per square foot providing
a standing crop is considerably above that given
previously. Findings from the RUFAS survey
will be published in the near future by personnel
from the Exploratory Fishing Station in Bruns-
wick, Ga.

Yearly variations in distribution and abun-
dance may at first glance be discouraging to a
fisheiy. However, the remarkable opportunity
to predict each fall fishery exists because dis-
tributional and abundance jjatterns are estab-
lished in spring or early summer — perhaps as
early as May or June. Population assessment
at that time would provide estimates on the
standing crop and determine the success of a
fall fishery some 4 or 5 months prior to its onset.
The authors tested this hypothesis in the
spring and summer of 1970 using the RUFAS
vehicle.

SUMMARY AND CONCLUSIONS

The survey data show that calico scallops have
a short life span of 18 to 24 months. Sjiawning
occurs after a 7- to 9-month sexual maturation
period in early spring. Some protracted spawn-
ing was noted for localized areas. Although
growth rates were not determined for sizes
smaller than about 5 mm, the estimated growth
curve between 5 mm and senility (75 to 80 mm)
is sigmoid, rapidly increasing to about 50 mm
and then decreasing to death.

408

ROE, CLNLMIXS, and BLLLIS: CALICO SCALLOP OFF FLORIDA

Monthly mortalities for December to October
average approximately 20^/. Mortality curves
were generally curvilinear after spawning, in-
dicating a rapid post-spawning dieofF.

LITERATURE CITED

Beverton, R. J. H., AND S. J. Holt.

1957. On the dynamics of exploited fish popula-
tions. Fish. Invest. Min. Agr. Fish. Food (Gt.
Brit.) Ser. II, 19, 533 p.
Bourne, N., and E. G. Bligh.

1965. Orange-red meats in sea scallops. J. Fish.
Res. Bd. Can. 22: 861-864.
BuLLis, H. R., Jr., and R. Cummins, Jr.

1961. An interim report of the Cape Canaveral
calico scallop bed. Commer. Fish. Rev. 23(10):
1-8.

BuLLis, H. R., Jr.. and R. M. Ingle.

1959. A new fishery for scallops in western Flor-
ida. Proc. Gulf Carib. Fish. Inst., 11th Annu.
Sess., p. 75-78.
Carpenter, J. S.

1967. History of scallop and clam explorations in
the Gulf of Mexico. Commer. Fish. Rev. 29(1) :
47-53.
Cummins, R., Jr., J. B. Rivers, and P. J. Struhsaker.

1962. Exploratory fishing off the coast of North
Carolina, September 1959-JuIy 1960. Commer.
Fish. Rev. 24(1) : 1-9.

Dickie, L. M., and J. C. Medcof.

1963. Causes of mass mortalities of scallops
{Placopecten 7nagellanicus) in the southwestern
Gulf of St. Lawrence. J. Fish. Res. Bd. Can.
20: 451-482.

Drummond, S. B.

1969. Explorations for calico scallop, Pecten gib-

bus, in the area off Cape Kennedy, Florida, 1960-
66. U.S. Fish Wildl. Serv., Fish. Ind. Res. 5:
85-101.
Gibson, F. A.

1956. Escallops (Pecten maximum L.) in Irish
waters. Sci. Proc. Roy. Dublin Soc, New Ser.
27: 253-271.
Johnson, C. W.

1934. List of marine mollusca of the Atlantic coast
from Labrador to Texas. Proc. Boston Soc.
Natur. Hist. 40: 1-203.
Loosanoff, V. L., and H. C. Davis.

1950. Conditioning V. mercenaria for spawning in
winter and breeding its larvae in the laboratory.
Biol. Bull. (Woods Hole) 98: 60-65.
Olsen, a. M.

1955. Underwater studies on the Tasmanian com-
mercial scallop, Notovola meridionalis (Tate)
(Lamellibranchiata: Pectinidae). Aust. J. Mar.
Freshwater Res. 6: 392-409.
Ricker, W. E.

1958. Handbook of computations for biological sta-
tistics of fish populations. Fish. Res. Bd. Can.,
Bull. 119, 300 p.
Struhsaker, P.

1969. Observations on the biology and distribution
of the thorny stingray, Dasyatis centroiira
(Pisces: Dasyatidae). Bull. Mar. Sci. 19: 456-
481.
Taylor, D. M.

1967. Billion-dollar scallop find? Ocean Ind. 2
(12) : 20-24.
Waller, T. R.

1969. The evolution of the Argopecten gibbus
stock (Mollusca: Bivalva), with emphasis on the
tertiary and quarternary species of eastern North
America. Paleontol. Soc, Mem. 3, 125 p. (J.
Paleontol. 43 Suppl.)

409

EFFECTS OF DELAYED INITIAL FEEDING ON LARVAE OF THE
GRUNION, Leuresthes tenuis (AYRES)

Robert C. May'

ABSTRACT

The initial feeding of newly hatched larvae of the grunion, Leuresthes tenuis (Ayres), was delayed for
various periods of time under laboratory conditions at 18° C. Unfed larvae did not develop morpho-
logically beyond the stage reached at the time of yolk absorption, about 4 days after hatching, although
some survived as long as 3 weeks. Regardless of how long initial feeding was delayed, 80% or more of
previously unfed larvae began feeding when food was made available to them, and at least 40% of the
larvae alive when food was offered were able to survive to the end of a 20-day experiment. Some lar-
vae feeding for the first time after 1 to 2 weeks without food, died after gorging themselves with
Artemia nauplii. When food was offered to starved larvae, growth began and generally proceeded
at about the same rate as in larvae fed from day 1, although there was some indication that a few
days' delay in initial feeding increased the conversion efficiency of grunion larvae feeding on Artemia
nauplii. Catabolism of fat provided most of the energy for metabolic processes during starvation. The
condition factors and carbon/nitrogen ratios of unfed larvae were below those of fed larvae; condi-
tion factor seemed to be the better index of nutritional state. Grunion larvae probably do not exper-
ience high mortality at sea due to starvation, nor do they exhibit a classical "critical period" at the
time of yolk absorption.

Most marine fishes pass through a free-swim-
ming larvae stage, and it is well documented that
survival through this stage is very low, gener-
ally being much less than 0.1 "^r (e.g., Sette,
1943; Ahlstrom, 1954; Pearcy, 1962; lizuka,
1966). The rate of survival through the larval
stage is probably the most important factor
determining the strength of year classes (Be-
verton, 1962; Gulland, 1965). Hjort (1914,
1926) advanced the hypothesis that larval sur-
vival was drastically affected by the abundance
of food at the time the yolk was completely
absorbed, and that poor year classes resulted
when insufficient food was available to larvae
at this "critical period." As Marr (1956) point-
ed out, Hjort's "critical period" concept has had
a profound effect upon the thinking of fishery
biologists.

Increased larval mortality at the time of yolk
absorption has, however, proved difficult to dem-
onstrate in nature. Marr (1956) concluded that

' Scripps Institution of Oceanography, University of
California, San Diego, La Jolla, Calif. 92037, and Na-
tional Marine Fisheries Service Fishery-Oceanography
Center, La Jolla, Calif. 92037.

the published evidence did not establish the ex-
istence of such increased mortality at sea ; even
in the light of more recent field data (Farris,
1961; Pearcy, 1962; Stevenson, 1962; lizuka,
1966; Karlovac, 1967), it is difficult to decide
from survival curves whether increased mortal-
ity at yolk absorption does in fact occur in na-
ture. It has proved equally difficult to demon-
strate that starvation is a major cause of larval
mortality in the sea. Wild larvae found with
empty guts (Lebour, 1920; Bowers and Wil-
liamson, 1951; Arthur, 1956; Bhattacharyya,
1957; Berner, 1959) may indicate imminent
death by starvation or may reflect artifacts such
as defecation or selective capture by plankton
nets (Blaxter, 1965. 1969). Reports of appar-
ently emaciated larvae, sometimes caught in re-
gions where food is scarce (Soleim, 1942; Ar-
thur, 1956; Shelbourne, 1957; Nakai, 1962;
Hempel and Blaxter, 1963; Nakai et al, 1969),
are suggestive but inconclusive (Marr, 1956;
Blaxter, 1965, 1969). Field data thus indicate
the possibility of high larval mortality due to
starvation after the yolk has been absorbed but
have not demonstrated its existence conclusively

Manuscript received January 1971.

FISHERY BULLETIN: VOL. 69, NO. 2. 197L

411

FISHERY BULLETIN, VOL. 69, NO. 2

or determined its significance for year-class
strength.

The response of larvae to food deprivation in
the laboratory may provide badly needed evi-
dence of how susceptible they are to starvation
at sea. There have, however, been few attempts
to determine experimentally the effects of de-
layed initial feeding on the larvae of marine
fishes. Fabre-Domergue and Bietrix, the two
pioneers of marine fish culture who coined the
term "critical period," which Hjort later adopt-
ed, believed that feeding before the yolk supply
was exhausted was essential to assure larval sur-
vival in laboratory rearing attempts. They
stated that among larvae which received food
prior to yolk absorption, ". . .la phase que noiis
avians nornmee periode critique post-larvaire
n'existe jms" (Fabre-Domergue and Bietrix,
1898: 468) . These authors went on to say that
larvae which did not receive food early would
subsequently become weak and unable to capture
food and would exhibit considerable, if not total,
mortality (Fabre-Domergue and Bietrix, 1898).
The importance of early feeding for marine fish
larvae was not further investigated in the lab-
oratory until Blaxter and Hempel (1963) stud-
ied the effects of delayed initial feeding on the
behavior of larval herring, Chipea hareiu/us L.
By feeding larvae after successively longer times
without food, Blaxter and Hempel determined
the time beyond which the larvae failed to ex-
hibit feeding movements when supplied with
food, a time they called the "point of no return."
This point came 5 to 9 days after complete yolk
absorption, at temperatures of 12° to 8° C, much
later than the statements of Fabre-Domergue
and Bietrix would have led one to expect. Re-
cently, Lasker et al. (1970) observed the mor-
tality of larvae of the northern anchovy, En-
graulis mordax Girard. which had been fed at
progressively later times after hatching. At
temperatures of 1.5° to 22° C, larvae for which
initial feeding had been delayed until 2.5 days
after complete yolk absorption, showed the same
pattern of mortality as grouiis of starved con-
trols, while larvae receiving food 1.5 days after
yolk absorption exhibited good survival — a phe-
nomenon which these authors termed "irrever-
sible starvation."

The purpose of the present study was to in-
vestigate in detail the changes which take place
in starving larvae and in larvae whose initial
feeding is delayed for various lengths of time,
and thus to bring more evidence to bear upon
the perennial questions of how susceptible lar-
val fishes are to food deprivation and whether
they do pass through a "critical period" at the
time of yolk absorption. This study also sought
to broaden the range of our knowledge of larval
fish ecology by utilizing a species belonging to
a group other than the Clupeiformes or Pleuro-
nectiformes, or which nearly all of our infor-
mation has hitherto been based. The fish chosen
for study was the grunion, Leuresthes tenuis
(Ayres), a member of the family Atherinidae.
Atherinids produce rather large demersal eggs
(Breder and Rosen, 1966), and the well-devel-
oped larvae which hatch provide an interesting
contrast with flatfish and clupeoid larvae. Spe-
cifically, these experiments were designed to de-
termine the effects of delayed initial feeding on
mortality, on growth, and on the ability of
grunion larvae to begin feeding and to utilize
ingested food, and to ascertain what changes
in the morphology and chemical composition of
the larval body occur during starvation.

MATERIALS AND METHODS

SOURCE OF EGGS; HATCHING

The grunion is best known for its unusual
habit of spawning on the sandy beaches of south-
ern California and northern Baja California
(Thompson and Thompson, 1919; Walker, 1952;
Breder and Rosen, 1966). The eggs are depos-
ited in the sand at night at certain times in the
tidal cycle and are washed free some days later
by a succeeding high tide, at which time the lar-
vae hatch if the develojimental period has been
sufficiently long. The spawning season extends
from late February or early March to late Au-
gust or early September, with spawning inten-
sity reaching a peak in April and May (Walker,
1952). During this time it is relatively easy
to collect grunion eggs, which therefore provide

412

MAY: EFFECTS OF DELAYED INITIAL FEEDING

convenient material for the study of embryonic
and larval development.

Eggs for the present study were collected dur-
ing a spawning run on the night of March 24,
1970, at the beach in front of Scripps Institution
of Oceanography, La Jolla, Calif. The eggs from
a running ripe female were expressed into a
small plastic container and artificially fertilized
by adding milt from one male and a small amount
of seawater; after approximately 1 min the
water was decanted and sperm removed with
several washes of fresh seawater. At the Na-
tional Marine Fisheries Service Fishery-Ocean-
ography Center in La Jolla, developing eggs
were dispersed in a layer of washed, slightly
moist beach sand approximately 1 cm deep at
the bottom of rectangular plastic containers
(16 X 12 X 11 cm), and a paper towel moist-
ened with seawater was placed on the surface
of the sand. The tops of the containers were
covered with aluminum foil. This incubation
procedure, essentially the same as one described
by Morris (1956), kept the eggs moist and pro-
duced good hatching when excess water (which
quickly brought on anoxic conditions) was
avoided. The containers were placed in a water
bath held at 20° ± 1° C by manually mixing
water from the warm and cold seawater systems
of the Fishery-Oceanography Center (see Las-
ker and Vlymen. 1969). The day before hatch-
ing, the temperature of the water bath was
lowered to 18° C over a period of 3 hr.

On April 3, 1970, after 10 days of incubation
(a common incubation time in nature, according
to Walker, 19.52), hatching was induced by ad-
ding filtered seawater at 18° C to the incubation
containers and agitating the water and sand by
drawing water i-apidly in and out of a pipette.
Hatched larvae were immediately transferred
via pipette (4-mm bore) to 18° C water in rear-
ing containers. In this paper the day of hatch-
ing will be referred to as day 0, the day after
as day 1, and so forth.

DESIGN OF EXPERIMENT

A total of 20 rearing containers was set up,
each with approximately 50 newly hatched grun-

ion larvae. Seven containers (*l-7) were used
to determine the efl"ect of delayed initial feeding
on mortality and growth; in six containers in
this group, feeding was begun at progressively
later times at 3-day intervals beginning on day
1— i.e., on days 1, 4, 7, 10. 13, and 16— while the
larvae in one container (-»7) were not fed and
served as a control.. On the 20th day after
hatching, all surviving larvae which had received
food in this series were collected, and the length,
weight, and chemical composition of the larvae
were determined. Seven of the other containers
(#8-14) were fed daily beginning on day 1, and
six (*15-20) were given no food; these con-
tainers, referred to as "supply containers" in
what follows, supplied fed and unfed larvae for
measurements of length, weight, and chemical
composition and also for experiments on feeding
and growth. On the same days when feeding
was begun in a new container in the delayed
feeding series (containers *l-7), larvae from
both the "fed" and the "unfed" supply containers
were used to determine the incidence of feeding
and to begin quantitative feeding experiments.

PHYSICAL CONDITIONS

Water of approximately 33 '/,, salinity was
taken from the seawater system of the Fishery-
Oceanography Center. The larval fish contain-
ers were originally filled with HA Millipore-
filtered seawater, and at weekly intervals
filtei-ed water was added to the fed containers in
order to replace water removed with uneaten
food and fecal matter (see below), the volume
added usually being between 1 and 2 liters. The
temperature in the water bath was kept at 18°
± 1° C, and temperatures in the larval contain-
ers were within 0.5° C of the bath temperature.
Eighteen degrees is the midpoint of the 14°-22°
C range of water temperatures which occurs off
La Jolla during the spawning season of the
grunion (Reid et al., 1958). Banks of two 40-
watt "daylight" fluorescent lamps ]30sitioned 76
cm above the surface of the water illuminated
the containers for 12 hr each day. The lights
were timed to go on after sunrise, so that dif-
fuse light entering through windows increased

413

FISHERY BULLETIN: VOL. 69. NO. 2

slowly in intensity as the sun rose and no abrupt
dark-light transition was imposed upon the
larvae.

CONTAINERS

The containers used for rearing larvae in this
study were the same as those described by Las-
ker et al, 1970) , being circular (35 cm diameter,
14 cm deep) and made of the plastic alloy Ky-
dex.' These containers have nonglossy black
surfaces and hold 10 liters of seawater. For
feeding studies with individual larvae, smaller
Kydex containers were used (10.5 cm diameter,
4.2 cm deep) which held 300 ml of water. Both
large and small containers were covered with
clear plexiglass tops to reduce evaporation and
keep out dust particles.

FEEDING

Nauplii of the brine shrimp, Artemia salina,
were used exclusively as a food source. Artemia
nauplii have proven to be poor food for larval
clupeids but excellent for several other types
of larvae (May, in press), and they appear to
satisfy the nutritional requirements of larval
grunion. Nauplii were obtained by hatching
San Francisco brine shrimp eggs in trays mo-
deled after those described by Riley (1966).
Two trays were used, which allowed harvesting
of trays on alternate days with a time lapse of
48 hr between inoculation of eggs and harvesting
of nauplii. The water in the trays was kept
at about 20° C. Nauplii were rinsed in filtered
seawater and added to rearing containers shortly
after the lights went on each morning, and more
were added during the day if the concentration
dropped low enough to prevent ad libitum feed-
ing. If any uneaten nauplii remained from the
previous day, as many as possible were removed
by pipette before the morning addition of new
nauplii. Fecal matter was siphoned daily from
the bottoms of the "fed" containers.

' Kyde.x is manufactured by Rohm and Haas, Phil-
adelphia, Penn. Use of trade name does not imply
endorsement of the product.

QUANTITATIVE FEEDING STUDIES

At 3-day intervals beginning on day 1, 6-day
quantitative feeding experiments were begun to
measure the food consumption and growth of
previously fed and unfed larvae. Larvae were
transferred individually, from both the "fed"
and the "unfed" suppl.v containers, to small (300
ml) containers late in the afternoon on the day
before the beginning of the feeding experiment.
Three larvae from a "fed" container and three
from an "unfed" container were used in each
feeding experiment; individual larvae were kept
in separate containers during the feeding study.

On the morning following transfer to the feed-
ing containers, and for six mornings thereafter,
a known number of Artemia nauplii was counted
out with a pipette under a dissecting microscope
and added to each container. Shortly before
the lights went off at the end of the day, the
grunion larvae were transferred by pipette to
new containers, and the uneaten Artemia in the
old containers were concentrated on a nylon
mesh, preserved in Formalin and later counted.
The difference between the number of nauplii
added in the morning and the number left at
the end of the day gave the number eaten by a
larva. At the start of the series of feeding ex-
periments, on day 1, 100 nauplii were added to
each experimental container; when larvae con-
sumed 70% or more of the nauplii offered, the
number offered the following day was increased
bv 50 nauplii. On the morning following the
final (6th) day of feeding, the experimental
larvae were collected and analyzed as described
below. The weight of a larva at the start of
the feeding experiment, estimated from the
mean weight of 10 larvae sampled at that time,
was subtracted from the weight of the exper-
imental larva at the end of the feeding period
to yield its gain in dry weight.

In order to determine the weight of the in-
gested material, the weight of a single Artemia
nauplius was estimated by making several
weighings on an electrobalance' of groups of 5
to 20 nauplii, collected at the same interval after
inoculation of eggs as the nauplii used in the
feeding study. The nauplii were rinsed with
distilled water and dried to constant weight at

414

MAY: EFFECTS OF DELAYED INITIAL FEEDING

60° C before weighing. The mean weight per
nauplius was 1.64 jj-g, almost identical to Paf-
fenhofer's (1967) vakie of 1.65 fig per newly
hatched Artemia nauplius. Where the larvae
had yolk sacs at the beginning of the feeding
period, the mean weight of the yolk masses dis-
sected off the 10 larvae sampled at the start
of the experiment (the dissection technique is
described below) was added to the weight of
the nauplii consumed to yield the total dry weight
of the consumed material.

The growth and food consumption of indi-
vidual larvae during the feeding period were
thus known and allowed calculation of the ef-
ficiency of food conversion:

percent conversion efficiency = dry weight goined ^ ,og
dry werght consumed

INCIDENCE OF FEEDING

The percentage of larvae which fed after
progressively longer times without food, termed
here the incidence of feeding, was determined
in separate experiments in 10-liter containers.
Approximately 25 larvae were transferred from
one of the "unfed" supply containers to a 10-
liter container with filtered seawater late in the
afternoon preceding the experiment, and on the
following morning large numbers of Artemia
nauplii were introduced into the container. One
hour later, the anesthetic MS-222 (tricaine meth-
anesulfonate) was added to the container to a
concentration of 132 mg/liter, and the anesthe-
tized larvae were examined under a dissecting
microscope for the presence of an orange-col-
ored gut indicative of feeding on Artemia naup-
lii. Simultaneously, the incidence of feeding
among larvae from one of the "fed" supply con-
tainers was determined in the same way, to
serve as a control with which hitherto unfed
larvae could be compared. Experiments of this
sort were conducted on the same days on which
food intake and conversion experiments were
started, beginning with day 4. Owing to mor-
tality from starvation, the numbers of larvae
available in the "unfed" containers dwindled so
that only 13 larvae were available for the feeding

Cahn Instrument Company, Paramount, Calif.

incidence experiment on day 13 and 4 on day 16.
By day 16, body pigmentation had developed in
larvae from the "fed" containers to such an ex-
tent that feeding incidence could not be assessed
by examining the coloration of the gut, and no
value was obtained for previously fed larvae
on this day.

Anesthesis stimulated peristalsis in grunion
larvae, as Blaxter (1965) observed in larval her-
ring, but the procedure in the present experi-
ment was rapid enough that at most only the
contents of the rectum were being extruded dur-
ing examination and all larvae which had in fact
fed were recorded as such. It should be pointed
out that, unlike the straight, tubelike gut of
clupeid larvae, the gut of larval grunion is al-
ready differentiated at hatching into three more
or less distinct portions, the last of which, the
rectum, is separated from the rest of the gut
by an "ileo rectal valve" (Al-Hussaini, 1947)
which inhibits rapid defecation of material not
in the rectum.

MORTALITY

Dead larvae were removed from the contain-
ers each morning by pipette. A larva was con-
sidered dead when its brain had become opaque
and it did not respond to water current or to
tactile stimulation. Dead larvae were routinely
examined with a dissecting microscope.

SAMPLING PROCEDURE AND ANALYSIS
OF LARVAE

Larvae were collected by pipette, and their
lengths measured with an ocular micrometer
from snout to tip of notochord, or, after upward
flexion of the tip of the notochord had taken
place, to the posterior edge of the hypural ele-
ments (standard length). Only free-swimming
larvae were sampled, although in "unfed" con-
tainers these became increasingly rare toward
the end of the experiment. Sampled larvae were
rinsed quickly in distilled water and placed on
glass microscope slides. Since larvae which
were sampled on days 1 and 4 still possessed
yolk sacs, they were preserved in 3%

415

FISHERY BULLETIN: VOL. 69, NO.

Formalin (in 50% seawater). Within 1 week of
sampling they were rinsed in distilled water
and their yolk dissected off, separated larvae and
yolk masses being placed on microscope slides.
The samples on slides were dried to constant
weight at 60° C and weighed to the nearest
microgram on an electrobalance. In agreement
with the results of Blaxter and Hempel (1966),
no effect of Formalin on the dry weight of lar-
vae was found, nor was there a significant effect
of Formalin on the dry weight of yolk masses
(this was tested in a previous experiment by
comparing dry weights of yolk dissected from
preserved larvae with yolk dissected from fro-
zen larvae or collected in preweighed capillary
tubes) .

Larvae sampled from the supply containers
at 3-day intervals, and those collected from the
delayed-feeding series on day 20, were analyzed
for their ash, carbon, hydrogen, and nitrogen
content. Percent ash was determined by weigh-
ing separately three randomly chosen larvae
from each sample before and after combustion
at 500° to 520° C. In the case of larvae fed
from day 16 and sampled on day 20, only one
larva was available for the ash determination.
During combustion, larvae were held on tarred
pieces of precombusted aluminum foil, and
weighings were made on an electrobalance. The
remaining larvae in each sample were ground
into fine particles with an agate mortar and
pestle, and two aliquots of this material from
each sample were analyzed for carbon, hydrogen,
and nitrogen content with a Model 185 carbon-
hydrogen-nitrogen analyzer.' The number of
replicates was limited by the amount of material
available, but variation between replicate deter-
minations was small, and means calculated from
the replicates were accepted as the ash, C, H, and
N values for the sample. This appi'oach to the
chemical analysis of larvae was chosen because
it allowed determination of C,/'N ratios, estima-
tion of protein and fat content, and calculation
of caloric content (.see Results section).

Larvae which had been used in the feeding
incidence experiments described above were pre-
served in 3'f Formalin and later cleared in KOH
and stained with Alizarin Red-S, the standard

stain for bone, to allow comparison of ossifica-
tion in fed and unfed larvae.

RESULTS

BEHAVIOR

Newly hatched grunion larvae have functional
eyes and jaws and are extremely active (Thomp-
son and Thompson, 1919; David, 1939). Grun-
ion larvae which received food in the present
experiment remained very active as they grew,
and some schooling behavior was noted as early
as day 6. Of more immediate concern was the
behavior of starved larvae. On day 7 it was
noted that unfed larvae were much easier to
catch with a pipette than fed larvae. As the
period of starvation lengthened, larval activity
declined and the number of larvae remaining
quiescent on the bottom Increased. Near the end
of the experiment, no starved larvae were swim-
ming freely above the bottom, and their activity
consisted in occasional erratic movements, fol-
lowed by long quiescent periods.

SURVIVAL

Figure 1 shows the survival to day 20 of
larvae which were fed at various times after

DAY OF
FIRST FEEDING

AGE (doysl

Figure 1. — Survival curves for larvae with different
times of initial feeding, at 18° C. The number at the
end of each curve indicates the day of initial feeding.
The control group was given no food during the exper-
iment.

' Hewlett Packard Corporation, Palo Alto, Calif.

■416

MAV: EFFECTS OF DELAYED INITIAL FEEDING

hatching and a starved control Yolk was com-
pletely used up in unfed larvae by day 4, and
on this day only a minute amount was left in
fed larvae. The survival curve for unfed larvae
passed the 50<^f line between days 11 and 12.
roughly the same as the starvation time given
by Hubbs (1965) for larval grunion at 18° C.
The starved control larvae were all dead by day
21. There is a direct relationship between per-
cent survival of original larvae to day 20 and
the day of first feeding (Table 1). The number

Table 1. — Sur\-ival to day 2U of larvae with different
times of initial feeding.

Day of

first
feeding

Original
number
of larvae

Number of
larvae alive
when food
first offered

Number of

larvae

alive on

day 20

Percent survival
to day 20

Original

larvae

Larvae

aliva when

food first

offered

1

51

51

49

96.1

96.1

4

52

51

43

82.7

84.3

7

53

49

29

54.7

59.2

\0

55

44

18

32.7

40.9

13

48

23

11

22.9

47.8

16

51

4

4

7.8

1000

of larvae which survived to day 20, expressed
as a percentage of those which were alive when
food was first offered, is also listed in Table 1.
This figure never dropped below 40'^r, and all
of the previously unfed larvae alive in container
#6 on day 16 (i.e., four larvae) began feeding
when food was supplied and survived to day 20,
and their general appearance and behavior in-
dicated that they would easily have survived
longer, had the experiment been prolonged.

In the group of larvae which was fed for the
first time on day 7, 11 larvae were found dead
on the morning following the day of first feed-

ing; 9 dead larvae had food in their guts and
5 of these had guts which were bright orange
and so stuffed with Artemia nauplii that the
abdomen was noticeably distended. In the
group fed initially on day 10, all eight larvae
found dead the next morning had food in their
guts, and four of these had bright orange, packed
guts. On day 14, only one out of four dead lar-
vae, found in the container which had been fed
for the first time on the previous day, had food
in its gut and showed the orange and bulging
abdomen noted in dead larvae from the previous
two groups.

GROWTH

The increase in length and dry weight of
larvae sampled from the "fed" supply containers
is presented in Table 2. The rate of growth
was higher from day 16 on; variability like-
wise increased after this time, an example of
the "growth depensation" which is commonly
found in growing fish (Ricker, 19.58). On day
7, the hypural elements were beginning to form
along the posterior ventral margin of the noto-
chord, and on day 10 the tip of the notochord
was beginning its upward flexion. The greatest
increase in length occurred between days 1 and
4, and owing to the upturning notochord the
mean length actually decreased between days
13 and 16 (Table 2) . On day 4, only the cleith-
rum and a very few cranial and branchial ele-
ments were ossified, but by day 10 about half
of the vertebrae (the anterior ones) and some
of the caudal rays were beginning to take up
alizarin, and by day 16 all vertebrae and hy-
pural elements were ossified.

Table 2. — Length and weight of fed and unfed larvae, x = mean, SD
deviation, n = number of larvae measured.

standard

Length (mm)

!

Dry weight (mg)

Age
(days)

Fed

Unfed

Fed

Unfed

X

SD

1 "

X

SD

X

SD

n

X

SD

n

1

__

__

__

8.96

0.17

9

._

0.362

0.021

9

4

9.64

0.34

10

9.31

0.20

10

0.428

0.038

10

0.386

0.030

10

7

10.70

0.59

10

9.27

0.12

10

0,771

0.130

10

0.409

0.015

9

10

11.66

0.28

10

9.11

0.23

10

1.027

0.100

10

0.355

0.032

10

13

12.28

0.34

10

8.98

0.19

10

1.340

0.183

10

0.311

0.013

10

16

12.22

0.60

10

8.78

0.19

10

1,517

0.361

10

0.266

0.018

10

19

13.53

0.58

10

_,

__

__

2433

0.458

10

25

15.12

0.45

10

-

--

--

3.804

0.464

10

—

--

--

417

FISHERY BULLETIN: VOL. 69, NO. 2

Starved larvae exhibited a slow decline in
dry weight after yolk absorption, with little
variability between larvae (Table 2). Although
rudiments of the hypural elements were just
discernible in starved larvae on day 7, their
notochords never showed evidence of upward
flexion, even as late as day 16. On day 16, ossi-
fication in starved larvae was comparable to
that in fed larvae from day 4 or day 7, with
only the cleithrum and a few elements of the
cranium and visceral skeleton taking up alizarin.

The lengths and weights of 20-day-old larvae
from the delayed feeding series (containers
#1-6) are listed in Table 3, and in Figure 2 the

Table 3. — Length and weight of 20-day-old larvae with
different times of initial feeding, x = mean, SD =:
standard deviation, n = number of larvae measured.

Day of

Length (mm)

Dry weight (mg)

feeding

X

SD 1 n

X SD

n

I

14,24

0,61

20

2.702

0.420

20

4

14,03

0,36

20

2.513

0-193

20

7

12,38

0.31

20

1.638

0.148

20

to

11,10

0.38

13

0.995

0.086

18

13

9,87

0.51

11

0.561

0.137

11

16

9,82

0.35

4

0.436

0.036

4

"

3

-

-

(201

„

^^''

(201

E

H ?

/"'V

X

UJ

S
>

^'''' ,-''' - (20)

S 1

0

I '''' i ''''.'''''.'''' ■-

10
AGE (days)

Figure 2. — Dry weights of 20-day-old larvae with dif-
ferent times of initial feeding. Means and ranges are
plotted, and the number of 20-day-old larvae measured
in each group is given in parentheses. Dashed lines con-
nect mean weights at day 20 with the mean weights of
unfed larvae on the days when feeding was initiated.

weights are plotted and connected by dotted lines
to the weights of starved larvae on the days

when food was first off"ered. As expected, the
later the initial feeding, the lower the mean
weight on day 20, although the range of weights
of larvae fed from day 4 falls within that of lar-
vae fed from day 1, and larvae fed from days
13 and 16 likewise overlap (Figure 2) . The rate
of gain in weight decreases with delay of initial
feeding, as indicated by the decreasing slopes
of the dotted lines in Figure 2, but these rates
are similar to those of larvae feeding for com-
parable lengths of time from day 1 (e.g., the
weight gain of fed larvae between days 1 and 10
is about the same as that of larvae fed initially
on day 10 and sampled on day 20) . Larvae fed
from days 1, 4, and 7 had completed notochordal
flexion by day 20, and those fed from day 10
were at an intermediate stage of flexion at this
time; in those fed from days 13 and 16, the
process of flexion had not yet begun by day 20.
Larvae from both the fed series and the delayed-
feeding series indicated that notochordal flexion
did not begin until a length of about 11 mm and
a dry weight of about 1 mg had been reached.
Condition factors have been used in the past
to assess the nutritional state of fish larvae
(Hempel and Blaxter, 1963; Blaxter, 1965) and
were calculated for each sample in the present
experiment as

(mean dry weight, mg)
(mean standard length, mm)

X I0>

Figure 3 A shows that after day 4, the condition
factors for fed larvae increased until the end
of the experiment on day 25, while those for
starved larvae, after showing a slight rise on
day 7, decreased until the final sampling on day
16. As shown in Figure 4A, the condition
factors of 20-day-old larvae decreased in groups
for which initial feeding had been delayed 7 days
or more, with larvae fed from day 16 showing a
condition factor between those of starved larvae
10 and 13 days old.

FEEDING INCIDENCE

On day 4, larvae which had been oflfered food
since day 1 showed a higher feeding incidence
(88 ^fc) than those which were given food for

418

MAY: EFFECTS OF DELAYED INITIAL FEEDING

the first time on this day (SS-^f)— Table 4.
However, on days 7, 10, and 13 the feeding in-

Table 4. — Feeding incidence of previously fed and un-
fed larvae. Larvae were exposed to Artemia nauplii for
1 hr, after which they were examined for evidence of
feeding.

Age
(days)

Larvae previously fed

Number
of larvae
feeding

Number

of larvae

not

feeding

Percent
feeding

Lorvae previously unfed

Number
of larvae
feeding

Number

of larvae

not

feeding

Percent
feeding

4
7
10
13
16

22
21
22
20

88.0
91.3
91.7
83.3

9

23

24

8

4

17
I
1
2

34.6
95.8
96.0
80.0
100.0

cidence was similar (between 80 and 96%) in
larvae which had fed and those which had not
fed prior to the test. On day 16, the darkly
pigmented abdomen of previously fed larvae
made it impossible to determine their feeding
incidence, but all of those larvae tested which
had received no food prior to day 16 did con-
sume food on this day. The failure of pre-
viously fed larvae to show a feeding incidence
of 100% in these experiments probably reflects
the stress associated with transfer between con-
tainers.

FOOD INTAKE AND CONVERSION

On day 1, the mean dry weight of the larval
yolk supply was 0.027 mg (range, 0.015-0.039
mg), and on day 4, fed larvae retained 0.003

mg of yolk (range, 0-0.011 mg) while starved
larvae had no yolk left.

In the quantitative feeding experiments, con-
ducted in small, 300-ml containers, some larvae
did not survive the 6-day experimental period,
and some exhibited erratic swimming behavior.
Only data from the surviving larvae which dis-
played normal behavior have been retained. Lar-
vae did not begin feeding until day 2, although
food was available to them on day 1. The num-
ber of nauplii consumed daily per larva increased
as larvae grew, from less than 50 in first-feeding
larvae to almost 300 in larvae 2 weeks old and
older. Table 5 gives the total food consumption,
growth, and conversion efficiencies of all healthy
larvae which survived the feeding experiments
in small containers. Larvae which displayed
growth comparable to that of larvae in 10-liter
containers may be expected to give the most
reliable conversion efficiency values and are
identified by asterisks in Table 5. One larva, fed
from day 1, showed the extremely high efficiency
of 73 % . Table 5 suggests a trend toward de-
creasing conversion efficiency as larvae get older.
In the experiment begun on day 7, the previously
unfed larva for which data are available showed
a much higher eflSciency than the previously fed
larva.

BODY COMPOSITION

Results of the analyses of carbon, hydrogen,
nitrogen, and ash in sampled larvae are given

Table 5. — Food consumption, growth, and conversion efficiencies of individual larvae in small con-
tainers during 6-day feeding experiments. Asterisks identify larvae which exhibited growth comparable
to that of larvae in large containers and hence probably provide the most reliable conversion efficiency
figures.

Age at start

—

Previous
treatment

Dry wei

ght (mg)

Percent conversion

efficiency

[= (goin /total food

experim
(days

ng
;nt

Total food

Larva,

Larva,

Larva,

consumed

mitiol

finol

gam

consumed) X l(X)]

1

10.433

0.362

0.678

0.316

73.0-

1

10.771

0.362

0.700

0.338

43.8*

4

fed

■1.321

0.428

1.189

0.761

57.6*

4

unfed

1.074

0-386

0.880

0.494

46.0

7

fed

1.053

0.771

0.962

0.191

18.1

7

unfed

1.026

0.409

0.826

0.417

40.4

10

fed

2.250

1.027

1.940

0913

40.6*

10

fed

1.640

1.027

1.528

0.501

30.5*

10

unfed

0.978

0.355

0.668

0.313

32.0

13

fed

2.000

1.340

1.657

0.317

15.9

16

fed

2.365

1.517

2.002

0.485

20.5

2.155

1.517

2.418

0.901

41.8

1 Includes

0.027

mq

of yolk.

» Includes

0.003

m

g

of yolk.

419

FISHERY BULLETIN: VOL. 69, NO. 2

Table 6. — Carbon, hydrogen, nitrogen, and ash in larval
samples, as percentages of total dry weight.

(T 10-
o

Age
(days)

C

(%)

H
(%)

N

(%)

Ash

(%)

1

45.7

7.0

10.2

5.1

4

fed

45.5

7.0

10-5

5.4

7

fed

46.2

7.1

10.5

7.9

10

fed

47.1

7.1

10-8

8.6

13

fed

46.2

7.2

11.3

8.6

16

fed

45.2

7.0

10.9

8.7

19

fed

45.0

7.0

10.7

9.2

25

fed

43.1

6.6

10.9

10.0

4

unfed

46,5

6,9

10.4

6.6

7

unfed

44.5

6.9

10.6

7.8

10

unfed

44.0

6.8

11.1

9.4

13

unfed

44,0

6-8

11.2

9.2

16

unfed

432

6.4

11.3

7.3

20

fed from

doy

1

45.0

6.7

11.3

9.9

20

fed from

day

4

43,1

6.7

11.1

9.8

20

fed from

day

7

44.8

6.8

11.4

9.4

20

fed from

day

10

44.8

6.7

10.8

8.2

20

fed from

day

13

44,6

6.7

10.9

8.8

20

fed from

day

16

43.3

6.5

10.6

11.4

in Table 6. In this paper the term level will be
used in the sense of Giese (1969) to denote the
percentage of the total dry weight which a par-
ticular body component constitutes. In fed lar-
vae, the level of ash increased from 5.1% on day
1 to 10.0% on day 25. The ash level was higher
in unfed than in fed larvae, except on days 7
and 16. The nitrogen level increased with age
in both fed and starved larvae, but the increase
was more steady in the latter. Fed larvae fluc-
tuated between 10.7 and 11.3% nitrogen from
day 10 to day 25. Accompanying the increase
in nitrogen was a decrease in the level of carbon.
Among 20-day-old larvae, the level of ash was
higher, nitrogen lower, and carbon the same or
slightly lower in larvae whose initial feeding had
been delayed for 16 days than in larvae fed
earlier. Nitrogen in 20-day-old larvae decreased
with time of first feeding, from day 7 to day 16.
The ratio of carbon to nitrogen has been plotted
in Figures 3 and 4 along with condition factors.
The C/N ratio is lower in starved than in fed
larvae after day 4 but shows a decreasing trend
with time even in fed larvae whose condition
factor is increasing (Figure 3) . On day 20, lar-
vae whose initial feeding had been delayed 10
or more days had higher C/N values than larvae
fed earlier; here too, decreasing condition fact-
ors accompanied increasing C/N values. Since
preservation in Formalin has been shown to
affect the C, H, N, and ash levels of copepods

10 13 16

AGE (doys)

Figure 3. — Condition factors and carbon/nitrogen ratios
of fed and unfed larvae. Condition factors were calcu-
lated as [ (mean dry weight, mg) / (mean standard length,
mm)] X 10^. Closed circles = fed larvae, open circles
= unfed larvae.

r

g 1.0

A

o

" ~~ —o^

2 08

^^^..^^^^

z

^~^o^^

o

^^^^^

1- 0.6

^~-->J^^

a

^^^^

z

^^

8 01

.ill 1 1

r

2 '*''

O

o

^ 42

-

/

1

B

CD

1

1 1

1

1 4

7

10

13

16

DAY OF INITIAL FEEDING

Figure 4. — Condition factors and carbon/nitrogen ratios
of 20-day-old larvae with different times of initial feed-
ing. Condition factors calculated as in Figure 3.

420

MAY: EFFECTS OF DELAYED INITIAL FEEDING

(Omori, 1970) , the values given here for larvae
1 and 4 days old, which had been preserved in
Formalin to allow removal of yolk by dissection,
may be somewhat in error.

The level of protein in larval samples was esti-
mated by multiplying the nitrogen level by 6.25
(White, Handler, and Smith, 1968) , and fat was
calculated by difference: 100 - (percent ash +
percent protein) = percent fat. Nonprotein
nitrogen and carbohydrate were assumed to be
present in negligible amounts in this material
(Lasker, 1962). Caloric content was calculated
by multiplying weights of fat and protein in
average larvae by 9.5 cal/mg and 5.7 cal/mg,
respectively (Brody, 1945; Kleiber, 1961).
Table 7 lists the resulting values. The most

Table 7. — Protein, fat, and caloric content of larval
samples. Protein and fat are given as percentages of
total dry weight. Protein was calculated from the nitro-
gen content of samples, fat by difference, and caloric
content by multiplying weights of protein and fat by
standard conversion factors.

Treatment

Protein
(%)

Fat
(%)

Caloric

content

Aga
(days)

cal/mg of

col/mg of
ash-free

dry weight

dry weight

1

63.8

31.1

6.60

6.97

4

fed

65.6

29.0

6.50

6.86

7

fed

65.6

26.5

6.25

6.79

10

fed

67.5

23.9

6.12

6.70

13

fed

70.6

20.8

6.00

6.54

16

fed

68.1

23.2

6.11

6.68

19

fed

66.9

23.9

6.09

6.70

25

fed

68.1

21.9

5.97

6.64

4

unfed

65.0

28.4

6.43

6.89

7

unfed

66.3

25.9

6.26

6.79

10

unfed

69.4

21.2

5-94

6.55

13

unfed

70.0

20.8

5.98

6.60

16

unfed

70.6

22.1

6.13

6.60

20

fed from

day

1

70.6

19.5

5.89

6.54

20

fed from

day

4

69.4

20.8

5.94

6.59

20

fed from

day

7

71.3

19.3

5.90

6.50

20

fed from

day

10

67.5

24,3

6.16

6.71

20

fed from

day

13

68.1

23.1

6.07

6.65

20

fed from

day

16

66.3

22.3

5.89

6.64

notable trends are an increase in protein level
and decrease in fat level, in both fed and unfed
larvae (Table 7). Unfed larvae had lower fat
and about the same or somewhat higher pro-
tein levels than fed larvae. Among 20-day-old
larvae, those for which initial feeding had been
delayed tended to have higher fat and lower
protein levels than those fed early (Table 7).
Reflecting changes in proximate composition.

the caloric content of larval tissue showed an
early decrease and from day 10 on showed no
increasing or decreasing trend, in both fed and
unfed larvae (Table 7). From day 10 on,
starved larvae tended to have a lower caloric
content than fed larvae. The caloric contents
of 20-day-old larvae showed no consistent trend
with time of initial feeding (Table 7).

DISCUSSION

The developmental process requires a nutri-
tional input to supply energy and raw materials.
In larval grunion which receive no food, devel-
opment does not progress beyond the stage
reached when the yolk is absorbed, although the
larvae survive well beyond this point. The pro-
cess of ossification is halted and the upward
flexion of the notochord does not take place in
unfed larvae, while tissue resorption, supplying
energy for metabolic processes during starva-
tion, results in a slow decrease in larval mass.
Fat seems to be utilized most during starvation.
The amount of fat in an average starving larva
decreases by 0.071 mg, or 0.689 cal, during 16
days of starvation, while protein decreases by
only 0.043 mg, or 0.245 cal (Tables 2 and 7).
The fat and protein levels of feeding larvae are
not greatly diff"erent from those of starving lar-
vae (Table 7), but in the former case the ob-
served increase in protein level with time must
be a consequence of rapid protein synthesis in
the growing organism, whereas in the latter it
reflects the utilization of the body's fat reserves.

When food is off'ered to unfed larvae, growth
begins and proceeds at about the same rate as
in larvae fed from day 1 (Figure 2). Weight
and body composition at day 20 in larvae whose
initial feeding was delayed for various periods
is close to that of larvae fed for similar lengths
of time from day 1 (Tables 2, 3, and 7), though
fat is much more depleted in larvae fed for 4
and 7 days starting on days 16 and 13, respec-
tively, than in larvae fed for 4 and 7 days start-
ing on day 1. Larvae fed for a period of 16
days, from day 4 to day 20, gained more weight
and had higher protein levels than larvae fed
from days 1 to 16 (Tables 2, 3, and 7) , suggesting
that a few days' delay in initial feeding caused

421

FISHERY BULLETIN: VOL. 69. NO.

an increase in conversion efficiency. A similar
effect has been found in aduft fish (Ivlev, 1939;
Pandian. 1967) . There is some indication in the
results of the quantitative feeding experiments
that larvae convert food more efficiently after
7 days without food than after 7 days of feeding
(Table 5) , but the data are too meager to justify
any conclusion on this point.

Omori (1970) showed that copepods from
areas poor in food tended to have lower C,'N
ratios than copepods from rich areas. In lar-
val fishes, condition factors have been used in
attempts to assess nutritional state (Hempel
and Blaxter, 1963; Blaxter, 1965). Both meas-
ures were compared in the present study (Fig-
ures 3 and 4). Although starved larvae had
lower C N ratios than fed larvae after day 4,
due presumably to catabolism of fat, the C/N
ratios of growing, fed lai'vae decreased with age
as a consequence of the rapid elaboration of
protein, while their condition factors increased.
Reflecting this same tendency, larvae 20 days
old had higher condition factors but lower C/N
ratios, the longer they had been feeding. Con-
dition factor seems to be somewhat more con-
sistent and reliable as an index of the nutritional
state of larval grunion than C/N ratio.

In sum, larval grunion appear to be extremely
resistant to food deprivation. Under laboratoi\v
conditions it takes 3 weeks for all larvae to die
of starvation at 18° C (Figure 1). No matter
how long initial feeding is delayed, over 40'"r
of the larvae alive when food is offered will sur-
vive, and all larvae which survive 16 days with-
out food can commence feeding at this time and
survive (Table 1). Since grunion larvae hatch
from eggs deposited in the beaches of southern
California and northern Baja California and
must inhabit inshore waters almost exclusively,
and since the abundance of microplankton is ex-
tremely high in inshore as com|iared with off-
shore waters in this region ( Beers and Stewart,
1967), it seems unlikely that these larvae ever
experience high rates of mortality due to star-
vation. Major sources of mortality among
grunion larvae must be sought, rather, in pre-
dation and jihysical damage from waves. Tidal
variations may result in different incubation

periods in grunion eggs from different spawn-
ings (Walker, 1952), but the effect of this on
larval viability has yet to be determined.

These findings differ from results for clupeoid
larvae. In the northern anchovy a delay in in-
itial feeding of 2.5 days after yolk absorption
resulted in nearly complete mortality, even
though many larvae were alive when food was
administered (Lasker et al., 1970). This "point
of irreversible starvation" appears not to exist
for larval grunion, as starvation can in fact be
reversed at any point along the survival curve
of starved larvae (Figure 1).

Larvae of the herring (Clupea harengus)
show a decrease in the percentage of larvae
which commence feeding as the jieriod of food
deprivation is lengthened, and the point at which
the percentage feeding is half that at the start
of the experiment has been termed the "point
of no return" (Blaxter and Hempel, 1963; Blax-
ter, 1965). Again, the grunion larvae show a
different pattern, with at least 80 ''r of the larvae
commencing feeding when food is offered after
periods of starvation ranging from 7 to 16 days
(Table 4). Some larvae which did commence
feeding after 7, 10, and 13 days without food
were nevertheless unable to survive and died
after gorging themselves with Artemia nauplii.
The interesting fact that all of the larvae alive
after 16 days of starvation commenced feeding
and survived, while the percentage feeding was
lower in larvae starved for shorter periods of
time, may be explained as a result of mortality
among the weakest larvae, so that by day 16
only the most hardy individuals were still alive.

Thus, certain types of larvae would be more
likely than others to show a "critical period"
pattern of mortality at sea under conditions of
low food availability. If northern anchovy lar-
vae were not to encounter food within 2.5 days
after yolk absorption, there would ensue a ca-
tastrophic mortality concentrated in time (Las-
ker et al., 1970). In contrast, grunion larvae,
which hatch in a more well-developed and robust
state, would exhibit mortality extending over a
number of days if deprived of food and hence
would not show a "critical period" in the classi-
cal sense of Hjort. Obviously a sudden increase

422

^UY; EFFECTS OF DELAYED INITIAL FEEDING

in mortality at sea could come about after yolk
absorption, or at any other time, owing to factors
other than the availability of food. Hjort was,
of course, not referring to larvae of the atherinid
type when he enunciated his "critical period"
hypothesis, but with the large volume of pub-
lished material now available concerning the lar-
vae of a few commercially important species,
it would be easy to lose sight of the great diver-
sity of larval forms and to apply ideas which
may have validity in some groups to groups
in which they have no place.

ACKNOWLEDGMENTS

I wish to express my sincere thanks to
Reuben Lasker, National Marine Fisheries Ser-
vice, La Jolla, Calif., for advice, encouragement,
and the generous provision of laboratory and
aquarium space during this study. Andrew
Kuljis and David Crear assisted in the collection
of grunion eggs, and Elaine Sandknop prepared
the cleared and stained larvae. The author was
supported by a Bureau of Commercial Fisheries
(now National Marine Fisheries Service) Pre-
doctoral Fellowship during this work.

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424

MAY: EFFECTS OF DELAYED INITIAL FEEDING

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425

THE RELATIVE SAMPLING PERFORMANCE OF 6- AND
10-FOOT ISAACS-KIDD MIDWATER TRAWLS

William A. Friedl'

ABSTRACT

The relative abilities of 6- and 10-ft Isaacs-Kidd midwater trawls (IKMT) to sample macroplankton and
fishes were assessed from comparable hauls taken with graded mesh nets during January and February
1967, in central Puget Sound. The plankton catch, mostly individuals 2 to 2.5 cm long, was dominated
by the mysid, Neomysis kadiakensis. To quantify zooplankton data from the larger trawl, its cross-sec-
tional area effective in filtering macroplankton was estimated for each month. The mean eflfective cross-
sectional area of the 10-ft IKMT is 1.75 m^. This implies a significant funneling of macroplankton by
the forward section of the trawl.

The fishes taken were dominated numerically by Pacific herring, Clupea harengus pallasi; bay gobies,
Lepidogobius lepidus; and plainfin midshipmen, Porichthya notatus. Herring was not taken by the 6-ft
trawl; there was little apparent difference in the ability of the two trawls to capture midshipmen
and gobies. Overall, the 10-ft IKMT caught more fish, more active fish, and larger fish than the 6-ft
trawl. Though the 6-ft IKMT is probably adequate for studies with an emphasis on macroplankton, use
of the 10-ft IKMT to sample fishes in inshore waters is preferable.

Interpretation of net haul data depends upon
the capabihties and limitations of the sampling
gear employed. With the plethora of equipment
presently available for sampling the larger
plankton and smaller nekton, comparative infor-
mation on the relative sampling abilities of dif-
ferent gear is needed to equate results obtained
with different nets.

This report deals with the relative sampling
abilities of two sizes of Isaacs-Kidd midwater
trawl (IKMT), a type of net widely employed
in marine and freshwater investigations. The
results apply to IKMT in general ; the assess-
ment elucidates the degree to which data ob-
tained with different ti'awls are comparable.

METHODS AND MATERIALS

Samples were taken from the University of
Washington 65-ft research vessel Hoh at night
along a N-S track in Port Orchard, a narrow
channel west of Bainbridge Island in central
Puget Sound with a maximum depth of slightly
over 40 m. Comparable IKMT hauls were made

' Marine Biology Branch Code 5042, Naval Undersea
Research and Development Center, San Diego, Calif.
92132.

on two cruises in January and February 1967.
Length frequency data are from five cruises
made each month from November 1966 through
March 1967.

Two sizes of IKMT with graded mesh nets
were compared. The mouth area of the 10-ft
IKMT (Figure 1) is 7.68 m^ and that of the 6-ft
IKMT (Aron, 1959) is 2.94 m^. Mesh sizes
for the various sections of the trawls and other

COLLECTINS BUCKET. 10cm DIAMETER. 0 33 mm SCREEN

COD END- l/B in. (0 32cml MESH KNOTLESS NYLON

mJERMEOiATE SECTION:

I Ve in. (2 9 cm ) MESH NYlON PANELS

1/2 in (13 cm) MESH KNOTLESS NYLON LINER

FORHaRD SECTION:
1 1/2 in 13.8 cm 1 MESH
NYLON PANELS

Manuscript received January 1971.

FISHERY BULLETIN: VOL. 69, NO. 2, 1971.

Figure 1. — Dimensions and construction details of the
10-ft Isaacs-Kidd midwater trawl used in this study
(after Cooney, 1967).

427

FISHERY BULLETIN: VOL. 69. NO. 2

Table 1. — Dimensions and material specifications of the
Isaacs-Kidd midwater trawls compared in this study.

Item

6-ft IKMT 1

10-ft IKMT

Mesh size

Forward section
Intermediate section
Cod end

7.6 cm
1.3 cm
3.2 mm

3.8 cm
1.3 cm
3.2 mm

Cross-section area
Mouth
liner
Cod end

2.94 m2
1.26 m2
0.20 m2

7.68 m'
0.32 m2
0.20 mz

Filtering area
Forward section
Intermediate section
Cod end

14.85 m!
7.02 m2
1.61 m2

51.96 mz
9.81 m2
1.61 m2

dimensional data are presented in Table 1. Dur-
ing each haul, speeds were measured at the
surface with a Tsurami-Seiki-Koshakusho Co.
flowmeter' while trawls were at depth. The
same engine speed was used for all hauls. Gen-
erally, trawls were at depth 10 min and in the
water less than 15 min total. In January, sev-
eral 10-ft IKMT hauls were at depth 15 min.
Net depth was monitored on deck from signals
transmitted through the towing cable by a pres-
sure-activated sensing unit (designed and built
by the Department of Oceanography, University
of Washington) mounted above the trawl. A
Marine Advisers bathykymograph attached to
the trawl bridle was read after each haul to
check sampling depth.

The sampling distance was calculated from
the speed and duration of each haul. This
distance was multiplied by the appropriate trawl
mouth area (Table 1) to determine the maxi-
mum volume of water filtered during each haul;
the volumes so determined were used to calcu-
late the monthly fish concentrations. For deter-
minations of zooplankton concentrations, how-
ever, use of filtered volumes based on trawl
mouth areas would result in concentrations in-
ordinately low (Banse and Semon, 1963). In-
stead, volumes filtered should be based on the
trawl cross-sectional area eff'ective in sampling
zooplankton of the size considered. The effective
cross-sectional area, as used here, may be de-
fined as that area which yields the correct zoo-
plankton concentration, as measured indepen-

' The use of trade names is merely to facilitate de-
scriptions; no endorsement is implied.

dently, when divided into the zooplankton catch
per unit distance of tow. Thus, if the length
of tow is known, the number of animals caught
per unit distance towed can be converted to
concentration if the efl'ective cross-sectional
area is known. Banse and Semon (1963) com-
pared euphausiid catches from a quantitative
high speed catcher with those of the 6-ft IKMT
and determined the effective cross-sectional area
of the trawl to be not significantly diflS'erent
from the area of the opening of the middle
(1.3-cm mesh liner) section of the trawl, namely
1.26 m- (Table 1). This efi"ective area, multi-
plied by the sampling distance for 6-ft IKMT
hauls, produced the effective volume of water
filtered by the smaller trawl. Macroplankton
concentrations were calculated for January and
February from total 6-ft IKMT catch and total
effective volumes filtered each month. Total 10-
ft IKMT macroplankton catch was divided by
the total sampling distance to determine the
monthly macroplankton catch per kilometer by
the larger trawl.

RESULTS AND DISCUSSION

Macroplankton samples from each trawl were
comjiared to determine the effective cross-sec-
tional area of the 10-ft IKMT. The mysid,
Neomysis kadiakensis, represented 80% of the
total catch; the mysid (AcantJiomysis macrop-
sis), the euphausiids {Enphausia pacifica and
Thysanoessa raschii) , and decapods of the genus
Crago made up most of the rest. Most of the
individuals were between 2 and 2.5 cm long.
Plankton concentrations were considerably re-
duced in February (Table 2) and sejiarate esti-
mates of the 10-ft IKMT effective cross-sec-
tional area were made for each month. Using
the method of Banse and Semon (1963), divi-
sion of the 10-ft IKMT catch per kilometer by
the catch per 1000 m-' filtered by the effective
cross-sectional area of the smaller trawl yielded
an estimate of the 10-ft IKMT effective cross-
sectional area for each month (Table 2). The
mean effective area, weighted according to the
number of 10-ft IKMT hauls made each month,
is 1.75 m- (Table 2) . This is con.siderably larger
than the area of the intermediate section open-

428

FRIEDL: PERFORMANCE OF ISAACS-KIDD TRAWLS

Table 2. — Summary of macroplankton catch data used to compute the 10-ft IKMT cross-sectional area effective
in sampling macroplankton. Separate estimates were made for each month. The mean 10-ft IKMT effective area
is computed from the monthly estimates and is weighed according to the number of hauls made with the larger
trawl each month (see text).

6-ft IKMT

10-ft IKMT

Month

Hauls
(no.)

Catch
(no.)

Volume
(10' m=)

Concentration
(catch/ 103 m3)

Hauls 1
(no.) 1

Catch
(no.)

Distance
(km)

Catch/km

Effective
area (m^)

Jan.
Feb.

8
8

588
128

16.16
17.41

36.38
7.35

6
12

774
221

12,95
16.62

59.77
13.30

1.643
1.810

Weighted mean effect

■vearea: ""^^

X 6) + (1.810 X
18

'2) - 1.754

m!

ing (0.32 m=; Table 1) and indicative of a sig-
nificant funneling by the forward section of the
trawl.

The effective macroplankton sampling area of
the 6-ft IKMT corresponds to the area of the
opening of the intermediate section (1.3-cm
mesh liner) ; effects of funneling by the for-
ward section (7.6-cm mesh) of the trawl are
not obvious (Banse and Semon, 1963). My re-
sults indicate that the forward section of the
10-ft IKMT, with 3.8-cm mesh, is relatively more
important a factor in the ability of the net to
sample macroplankton than the corresponding
section of the smaller trawl. Given forward
sections of the same mesh for both trawls, how-
ever, the effective macroplankton sampling area
of the 6-ft IKMT would probably equal or ex-
ceed that of the 10-ft IKMT, for organisms of
the size considered here. The ratio of the ef-
fective cross-sectional area to total trawl mouth
area is 0.43 for the 6-ft IKMT and 0.23 for the
10-ft trawl. Thus, a larger percentage of the
water entering the mouth of the smaller trawl
is filtered for macroplankton. For this reason,
and because the 6-ft IKMT is generally easier
to handle and deploy, the smaller trawl would

be preferred for studies with primary emphasis
on macroplankton or small fishes.

The relative ability to each trawl to sample
fishes was also assessed. Total catch figures
are presented in Table 3. Numerically, Pacific
herring, Chipea harengus pallasi; bay gobies,
Lepidogobius lepidus; and plainfin midshipmen,
Porichthys notatus, dominated the overall catch.
Herring and gobies were common in hauls above
23 m while midshipmen were most abundant in
deeper tows. A few shiner perch, Cymatogaster
aggregata. Pacific cod, Gadus macrocephalus,
spiny dogfish, Sqjialus acanthias, and miscella-
neous flatfishes were also taken and are included
in the category "Others" in Table 3. Though
the total catch of the 10-ft IKMT exceeds that
of the 6-ft IKMT for each category of fishes,
the data are not directly comparable because
the larger trawl filtered more water in each
stratum. To equate catch data between trawls
on the basis of equal volumes filtered, the 10-ft
IKMT catch for each category of fish was
multiplied by the ratio of 6-ft to 10-ft IKMT
volumes filtered for each stratum (0.31 for hauls
above 23 m; 0.47 for deeper hauls. Exact vol-
umes given in Table 3) . The product, expressed

Table 3. — Summary of fish catch data, by trawls, from hauls made in January and February 1967. Total catch fig-
ures are in whole numbers and concentrations of fishes (Individuals/1000 m^ of water filtered) are in parentheses.
Estimated 10-ft IKMT catch for volumes filtered equal to those of the 6-ft IKMT within each stratum is entered
as "Equivalent 10-ft catch" and is directly comparable to the 6-ft IKMT catch data (see text).

10 to

22 m

23 to

31 m

Trawl

Hauls
(no.)

Volume
(103 rv?)

Herring

Boy
gobies

Midship-
men

Others

Hauls
(no.)

Volume
(103 m3)

Herring

Bay

gobies

Midship-
men

Others

10-ft
6-ff

14
11

171.4
53.4

27

(.16)

0

24

(.14)

2

(.04)

4

(02)

0

8
(.05)

1
(.02)

4
5

53.7
25.1

1

(.02)

0

10

(.19)

2

(.08)

48
(.89)

22
(.88)

11

(.20)

1

(-04)

Equivalent

10-ff

catch

8

8

I

3

1

5

22

5

429

FISHERY BULLETIN: VOL, 69. NO. 2

to the nearest whole number, is entered as
"Equivalent 10-ft catch" in Table 3 and is di-
rectly comparable to the catch figures for the
6-ft IKMT in the row above it. Figures for the
overall fish concentrations, from data on total
catch and total volume filtered, are also given
in Table 3.

When the catch data are compared on an equal
volume filtered basis, the superior sampling abil-
ity of the 10-ft IKMT is evident. With the ex-
ception of Porichthys in the lower stratum, the
10-ft IKMT caught more fish of each category
than did the 6-ft trawl and the resulting overall
concentrations estimated by the 10-ft IKMT are
likewise higher (Table 3). Pacific herring, a
major component of the mid-depth sonic scat-
tering layer in Port Orchard (Cooney, 1967;
Friedl, 1970), were not taken by the 6-ft IKMT
and apparently were capable of actively avoiding
the smaller trawl. The less active, Porichthys,
however, was sampled equally by the trawls in
the lower stratum. Though the catch and con-
centrations of Lepidogobius appear much lower
for the 6-ft IKMT in Table 3, the discrepancy
may reflect gear selection and loss through the
7.6-cm mesh of the 6-ft IKMT forward section
more than active avoidance of the trawl by the
fish. The Lepidogobius captured were small,
35 to 50 mm SL, and probably were filtered only
by the 1.3-cm mesh liner of the 6-ft IKMT inter-
mediate section. Assuming all gobies taken by
the 6-ft IKMT were filtered by the intermediate
section only, the concentrations above and be-
low 23 m would be 0.12 and 0.11 fish per 1000 m^
respectively, and would more nearly appro.xi-
mate those of the larger trawl (Table 3). Thus,
as with the macroplankton, the finer mesh of
the forward section of the 10-ft IKMT enhanced
the ability of the trawl to sample small organ-
isms.

The 10-ft IKMT caught more fish and sampled
active fish better than the 6-ft IKMT despite
the fact it was generally towed at lower speeds
(Table 4). The towing speed of the smaller
trawl, though only slightly greater than that
of the 10-ft IKMT, could have increased pres-
sure waves and vibrations associated with the
trawl and evoked greater avoidance responses

Table 4.— Net speed data for 6- and 10-foot IKMT hauls
in January and February 1967. Speeds measured at the
surface while the trawls were at depth. Average speeds
are significantly different at the 99% level when com-
pared with Student's t distribution (Simpson, Roe, and
Lewontin, 1960).

Hauls
(no.)

Trawling speed (m/sec)

Rcngg

Average

Confidence
interval (95%)

10-fr
6-ft

1.64 to 2.13
1.99 to 2.25

1.64
2.14

1.78 to 1.90
2.09 to 2.19

in active fishes such as herring (Chapman, 1964;
Harrisson, 1967). At present, knowledge of
the pressure and vibration characteristics of
IKMT underway is lacking and further con-
clusions regarding the influence of such char-
acteristics on the sampling abilities of trawls
would be speculative and beyond the scope of
this paper.

Comparison of the length frequencies of Por-
ichthys taken in deeper tows during the entire
winter period (November - March) indicates
a selection for larger fish by the larger trawl,
despite its slower towing speeds and finer mesh
(Figure 2). Nearly 70% of the Porichthys
taken between 20 and 35 m by the 6-ft IKMT
in the winter were less than 150 mm long (SL),
while half the Porichthys taken by the 10-ft
IKMT between 25 and 35 m in the same period
exceeded 180 mm SL (Figure 2).

My results indicate the 10-ft IKMT catches
more fish, more active fish, and larger fish than
the 6-ft IKMT used in the study; similar con-
clusions, with respect to the ability of small
and large trawls to samjile mesopelagic fishes,
were reached by Harrisson (1967). Aron and
Collard (1969) studied the influence of net speed
on catch for a 6-ft IKMT fully lined with 1.2-cm
mesh netting and found that faster tows took
larger fish of certain types off the California
coast. My data, for inshore fishes, indicate
mouth size, towing speed, net mesh size, and,
perhaps, the dynamic characteristics of trawls
combined with the behavioral aspects of the or-
ganisms sami)led are all interrelated in a com-
plex way to ultimately determine the sampling
ability of a given trawl.

Standardization of gear and techniques used
to sample midwater organisms would provide

430

FRIEDL: PERFORMANCE OF ISAACS-KIDD TRAWLS

10-FT IKMT

350

250

350

LENGTH,MM-5MM GROUPS

Figure 2. — Porichthys notatus length frequencies (SL)
from hauls made on monthly cruises from November
1966 through March 1967. Ten-ft IKMT catch from
five hauls between 25 and 35 m; volume filtered 57,400
m3. Six-ft IKMT catch from 12 hauls between 20 and
35 m; volume filtered 58,000 m^. Total catch (N) and
mean length (X) given on graphs for each trawl.

data). Thus, discussion of the biolog-ical "uni-
verse" defined by samples from a given trawl
must acknowledge the limitations of the gear
employed and avoid conclusions beyond the
scope of the data available from the sampler.
In general, my results indicate the 10-ft IKMT
to be preferable to the 6-ft IKMT for biological
surveys emphasizing fishes in inshore waters,
provided the vessel employed is capable of han-
dling the large trawl on a regular basis. For sur-
veys of macroi)lankton, however, the 6-ft IKMT
is adequate and generally easier to deploy. The
larger mouth opening and overall finer mesh of
the forward section apparently enable the
10-ft IKMT to sample more fish, larger fish,
and more active fish better than the 6-ft trawl.
Fully lining the trawls with fine-mesh netting
(UNESCO, 1968) would help simplify analysis
of results by eliminating the need for estimating
effective sampling cross-sectional areas when
calculating concentrations of small fishes and
macroplankton. Such lining would probably
also increase the trawls' ability to sample smaller
fishes (Backus et al., 1970), but the overall ca-
pabilities of the trawls to sample large or active
forms would likely change little and utilization
of the 10-ft IKMT would still be recommended.

a more valid basis for comparison of difl'erent
samples, but limitations of resources and equip-
ment often determine the manner and means
by which samples are taken. In this study,
for instance, the strain of towing the 10-ft IKMT
severely taxed the running rigging of the re-
search vessel and prevented the use of the larger
trawl on some cruises. At best, results of stud-
ies, such as this and that of Aron and Collard
(1969), illuminate the limitations and capabil-
ities of sampling gear, characteristics which
must be recognized even with widely employed
equipment such as the 6-ft IKMT. That trawls
may sample only a limited portion of the fauna
present is obvious and must be recognized. For
instance, recent work in Puget Sound with large
trawls indicates concentrations of herring, de-
termined by IKMT hauls in winter sonic scat-
tering layers, may be at least two orders of
magnitude low (T. S. English, unpublished

ACKNOWLEDGMENTS

This project was conducted in partial fulfill-
ment of the requirements for a degree of Master
of Science in the Department of Oceanography,
University of Washington, Seattle, Wash., with
the guidance of Dr. T. Saunders English. The
efforts of the crew of R/V Hoh are gratefully
acknowledged as is the critical review of the
manuscript by Dr. Eric G. Barham, Naval
Undersea Research and Development Center,
San Diego, Calif. Final preparation supported
by the U.S. Naval Ship Systems Command under
SR 104 03 01 Task No. 0588.

LITERATURE CITED

Aron, W.

1959. Midwater trawling studies in the North Pa-
cific. Limnol. Oceanogr. 4: 409-418.

431

FISHERY BULLETIN: VOL 69, NO. 2

Aron, W., and S. Collard.

1969. A study of the influence of net speed on
catch. Limnol. Oceanogr. 14 : 242-249.

Backus, R. H., J. E. Craddock, R. L. Haedrich, and
D. L. Shores.

1970. The distribution of mesopelagic fishes in the
equatorial and western North Atlantic Ocean.
J. Mar. Res. 28: 179-201.

Banse, K., and D. Semon.

1963. On the effective cross-.section of the Isaacs-
Kidd midwater trawl. Univ. Wash. Dep. Ocean-
ogr. Tech. Rep. 88, 9 p.

Chapman, C. J.

1964. Importance of mechanical stimuli in fish be-
haviour, especially to trawls. In Modern fishing
gear of the world 2: 537-540. Fishing News
(Books) Ltd., London.

COONEY, R. T.

1967. Diel differences in trawl catches of some de-

mersal fishes. M. S. Thesis, Univ. Wash., Seattle,
96 p.

Friedl, W. a.

1970. Sonic scattering and its probable causes in
two areas of Puget Sound. In G. B. Farquhar
(editor). Proceedings of an international sym-
posium on biological sound scattering in the ocean,
March 31-April 2, 1970, p. 527-550. Maury Center
Ocean Sci. Rep. 005.

Harrisson, C. M. H.

1967. On methods for sampling mesopelagic fishes.
/)( N. B. Marshall (editor). Aspects of marine
zoology, p. 71-126. Symp. Zool. Soc. London 19.

Simpson, G. G., A. Roe, and R. C. Lewontin.

1960. Quantitative zoology. Revised ed. Har-
court, New York, 440 p.
UNESCO.

1968. Zooplankton sampling. UNESCO (U.N.
Educ. Sci. Cult. Organ.) Monogr. Oceanogr. Meth-
od. 2, 174 p.

432

STUDIES ON THE USE OF CARBON DIOXIDE DISSOLVED IN
REFRIGERATED BRINE FOR THE PRESERVATION OF WHOLE FISH

Harold J. Baknett, Richard W. Nelson, Patrick J. Hunter,
Steven Bauer, and Herman Groninger'

ABSTRACT

Although storing fish in refrigerated seawater has many advantages over storing them in ice, the use
of refrigerated seawater also has several disadvantages, one of vi'hich is the difficulty in controlling
the growth of spoilage bacteria in the fish. Reported here is the effect on the growth of bacteria in
rockfish and chum salmon of dissolving carbon dioxide in brine. Storing the fish in the refrigerated
brine treated with carbon dioxide inhibited the growth of the bacteria, retarded the rate at which the
fish decrease in quality, and increased their storage life by at least 1 week.

Refrigerated seawater as a medium for cooling,
storing, and transporting fish has many advan-
tages, which have been well documented (Idyll,
Higman, and Siebenaler, 1952; Osterhaug, 1957;
Cohen and Peters, 1962; Peters and Dassow,
1965; Roach et al., 1967).

This medium, however, also has disadvant-
ages. These include the excessive uptake of
water by species of low oil content, such as sole
and cod, and an increase in total salt. Con-
trolling the growth of spoilage bacteria in fish
stored in refrigerated seawater also presents a
problem (Roach et al., 1967). This problem
results from the blood, dissolved protein, and
visceral contents accumulated in the seawater
during the storage of the fish. For these reasons,
fish held in refrigerated seawater are not nec-
essarily of better quality than are those held
for the same period in ice. Nor can fish neces-
sarily be held longer in refrigerated seawater
than in ice before spoilage occurs.

This laboratory recently began a study of
methods for increasing the effectiveness of re-
frigerated seawater as a medium for preserving
fish. The investigation is timely because fish-
ermen are finding it increasingly difficult to lo-
cate catches on traditional fishing grounds. This
reduced abundance requires longer stays at sea,
which sometimes result in the landing of fish
of less than optimum quality.

' National Marine Fisheries Service Technological
Laboratory, Seattle, Wash. 98102.

^fanuscript received January 1971.

FISHERY BULLETIN: VOL. 69. NO. 2. 1971.

Use of carbon dioxide gas dissolved in re-
frigerated seawater seemed promising as an in-
hibitor of the spoilage bacteria. Stansby and
Grifliths (1935), for example, found that whole
haddock and haddock fillets stored in an atmos-
phere of carbon doxide kept almost twice as long
as did those stored in air. Castell (1953) dem-
onstrated that carbon dioxide showed promise
of being a useful presei-vative for salted fish held
in 12';r brine. Carbon dioxide has been used
effectively to extend the storage life of refri-
gerated meat and poultry products (Wheaton,
1960) and is known to have bacterial inhibiting
properties (King and Nagel, 1967). Fiskeri-
ministeriets Forsogslaboratorium (1968) noted
that, in limited experiments on holding fish in
tanks, carbon dioxide decreased the rate at
which their quality was degraded. Wayne I.
Tretsven (1968, personal communication)
showed that the shelf life of fresh silver salmon
refrigerated in a mixed atmosphere of carbon
dioxide, oxygen, and nitrogen was significantly
extended beyond that of fresh silver salmon
refrigerated in air.

Rockfish is normally iced aboard the fishing
vessel and may be held for as long as 7 to 10
days before being landed. Chum salmon is fre-
quently held in refrigerated brine aboard can-
nery tenders and may be held aboard the ves-
sel for as long as 7 days. With both methods
of holding, the quality of the fish may be poor
if they must be held for longer periods. This

433

FISHERY BULLETIN; VOL. 69. NO. 2

study is specifically concerned with the effects
that holding in modified refrigerated brine con-
taining dissolved carbon dioxide" has on the
storage life and quality of rockfish and chum
salmon.

PRINCIPLES OF THE MODIFIED
REFRIGERATED BRINE SYSTEM

EFFECTS OF DISSOLVING CO. IN
REFRIGERATED BRINE

Carbon dioxide is a relatively inert chemical
compound. It is almost odorless and, in the gas-
eous form, is colorless. Combined with water,
it forms carbonic acid, a weak acid. Depending
on the conditions, only part of the CO2 added
to the water is dissolved. The undissolved CO2
either rises to the surface of the solution and is
wasted away or else becomes suspended as gas
bubbles, thereby forming carbonated water.
The amount of CO2 that can be dissolved by
water depends on the pressure and temperature.
The higher the pressure of the COl' and the low-
er the temperature of the water (at least, down
to 35° F), the greater the amount of CO2 dis-
solved. (We found that lowering the temper-
ature below 35° F did not increase solubility.)

When chilled brine is saturated with CO2, its
pH is reduced from about 7.5 or higher to about
4.0. This change in pH from the alkaline to
the acid condition helps to inhibit the growth
of bacteria that contribute to sjjoilage ( Wheaton,
1960). But pH control is not the only oper-
ative factor. Dissolved CO2 seems to inhibit
the metabolic processes of spoilage organisms
and, of course, temperature control is important
in slowing growth rate.

Although the modified refrigerated brine tech-
nique produces positive effects with regard to
the control of bacteria, the addition of CO2 can,
under certain conditions, produce undesirable
side effects. These effects are manifested in the
form of accelerated corrosion rates of metals
exposed to seawater containing high concen-
trations of the dissolved CO2.

REFRIGERATED BRINE EQUIPMENT

The equipment we used consisted of two fi-
ber glass-insulated 55-gal epoxy-coated drums
and a brine chiller.

We cooled the drums by circulating refriger-
ated brine from the lirine chiller through 200
ft of 3/i-inch polyvinyl chloride tubing wound
around the outside of the drums in series and
returned to the chiller (Figure 1).

Polyethylene liners with a capacity of about
30 gal were suspended in the drums by clamps.
(The purpose of the liners was to keep the fish
away from the cold sides of the drum, where
they tend to freeze.)

Each drum was equipped with a Moyno° pump
(Figure 2) for recirculating chilled brine (a so-
lution containing 3.3' r sodium chloride) .' The
brine was circulated by the pumps through a
fitting in the bottom of the polyethylene liner.
It was then forced through fish that had been
placed in the liners, whereupon it overflowed
back into the drums. The brine in the drums
was picked up by a suction hose and recycled
through the pumps at the rate of 10 gal/min.
For maximum diffusion into the brine, the CO2
gas was fed into the suction side of the circu-
lating pump at the rate of 0.2 ft\ hr. The brine
in the other drum was left untreated for use
as a control.

STORAGE LIFE AND QUALITY OF

ROCKFISH HELD IN MODIFIED

REFRIGERATED BRINE

OBJECTIVE MEASUREMENTS

Both bacteriological and chemical measure-
ments were made. All measurements reported
here were made in dujilicate.

* In this report, the term "modified refrigerated
brine" will henceforth mean brine containing dissolved
carbon dioxide (CO2).

' The use of trade names is merely to simplify de-
scriptions; no endorsement is implied.

' Sodium chloride brine was u.sed in lieu of natural
seawater because clean seawater was not convenient to
the laboratory. However, this technique has previously
been used by Collins (1950), Davis and Clark (1944),
and others and found to give good results. In compar-
ative experiments conducted by Roach and Harrison
(1954) and more recently by this laboratory (unpub-
lished), the test results showed that fi.sh held in re-
frigerated brine were of equal quality to fish held in
refrigerated seawater.

434

BARNETT ET AL. : USE OF CARBON DIOXIDE IN BRINE

Figure 1. — Arrangement of the brine chiller (on the left) ; the pump is (on the floor) for circulating the chilled
brine through the cooling coils shown wrapped around the uninsulated holding tanks.

Bacteriological Measurements

Materials and methods. — Described here are
the rockfish and brine samples we used and the
methods of making total plate counts.

The rockfish, Sebasfodes flavidus. were caught
in a trawl off the coast of Oregon. In the prepa-
ration of the samples, 130 lb. of the fresh, whole
fish was divided into two equal lots. Each lot
was placed in a polyethylene-lined drum of brine
at a one-to-one ratio by weight of fish to brine.
At this time, the iced fish had been out of the
water 24 hr. The ratio by weight of fish-to-
brine was maintained throughout the experi-
ment by removing a known weight of brine at
each sampling period.

One tank of brine was treated with CO2 gas

before the fish were loaded into it. The brine
in both tanks was cooled to 31° it 0.5° F during
the experiment.

Periodically three fish and a sample of brine
were removed from each of the storage drums
for examination. The fish samples were used
to make both the objective and subjective mea-
surements at each sampling.

Total bacterial plate counts were made on the
fish by the methods described by Pelroy and Ek-
lund (1966). Briefly, the method was as fol-
lows: a slice of flesh was removed from near
the dorsal side of each fish just posterior to the
nape. Each subsequent experimental sampling
was made from the same side and area of each
fish tested. Forty-five grams of fish from the
excised samples was homogenized aseptically

435

FISHERY BULLETIN: \OL, 69. NO. 2

Figure 2. — ArranKement of the Moyno pump for recirculating chilled brine in the holding tank (on the left)
and the CO2 cylinder (in the back) and attached CO2 flow meter (being adjusted by the worker).

with 180 ml of sterile O.l'^r pe])tone solution at
38° F. Serial dilutions in O.l'^.f peptone-water
were prepared for pour plates from the homo-
genate. Total plate counts were made by use of
a TPY medium (0.5'; yeast extract, 1.5'; tryp-
ticase, 0.5% phytone, 0.2% glucose, 0.5% NaCl,
and 1.5% agar) . Counts were made on the brine
by taking 1-ml samples, making appropriate se-
rial dilutions in the 0.1% peptone-water mix-
ture, and plating out onto the TPY medium.
The plates were incubated at 22° C for 5 days.

Results and discussion. — Table 1 gives the re-
sults of the total-])late-count analyses on the
brines and on the flesh of the rockfish. The
data from the untreated brine show that a lag
in bacterial growth occurred during the first 3

days of the storage test. After the third day,
however, the i)oi3ulation of bacteria in the brine
increased rapidly.

Total plate counts made on the brine treated
with CO2 did not show a significant increase
in the numl)er of bacteria during the 17 days
of storage.

Bacterial growth in the flesh of the rockfish
held in the untreated brine was not inhibited
during storage. On the 10th day, the fish were
judged, by ajjpearance and odor, to be inedible
and unlit for testing. At this time, the total
])late counts each exceeded a million organisms
lier gram of flesh. (A total plate count of a
million organisms iier gram usuallv indicates
flesh of poor (luality.)

436

BARNF.TT ET AL : USE OF CARBON DIOXIDE IN BRINE

Table 1. — Chemical and microbiological changes occurring in COj-treated refrigerated brine and in untreated re-
frigerated brine, and in the flesh of rockfish held in these brines.

Data on refrigerated brine

/i/ith added

CO12

Data on refrigerated brine without CO2

Time in
storage

CO2
cone.

pH

Salt

cone.

Total bocteriol
plate count

pH

Salt
cone.

Total bacterial
plate count

Flesh

Brine

Flesh Brine

Flesh

Flesh Brine

Flesh Brine

Flesh

Flesh Brine

Dayl

ppm

ppm

%

najg

nojml

%

no./g

no. /ml

0

119

1,000

6.7

4.0

0.2

1-2x10'

1.3X10'

6.7

6.8

0.2

1.2X10'

1.3X10'

3

562

2.332

5.8

5.3

0.5

--

1.6X10'

6.4

6.9

0.6

7.7X10'

1.2X10'

8

842

1,843

6.4

6.0

1.1

1.6X10'

--

6.5

7.3

1.0

2.4X10"

2.8X10"

10

__

__

60

1.3

__

Spoiled'

>I0"

14

597

1,452

65

6.0

1.4X10'

5.3X10=

__

..

17

-

-

6.4

6 1

1.8

2.0X10'

3.8X10'

--

--

-

--

—

Samples judged by appearance and ador to be inedible ond unfit for tasting.

The storage of rockfish in the refrigerated
brine containing the CO2 was terminated after
17 days. At this time, the results of the total
plate counts made on the flesh of the fish showed
that the microbial poiiulation had not changed
significantly from the initial total plate count
of 10'' organisms per gram of flesh.

Chemical Measurements

pH. — The pH of the flesh of the rockfish and
of the brines was measured by means of a Beck-
man combination electrode. The pH of the flesh
was measured by inserting the tip of the elec-
trode into the flesh (Patashnik, 1966).

Table 1 gives the results of the pH measure-
ments of the fish and the brine. After 8 days
of continuous recirculation, the pH of the con-
trol brine changed from a slightly acid condition
(pH 6.8) to a slightly alkaline condition (pH
7.3). This change coincided with an increase
in the microbial population in the control brine
and was probably due to the formation of ammo-
nia and amines from the bacterial degradation
of proteins dissolved in the brine.

The initial jiH of the brine treated with CO2
shows the eflfect of the dissolved CO2. The
measurement was made before the fish were
loaded into the brine. The subsequent increase
in the pH of the brine in the presence of addi-
tional CO2 may be attributed to the buff'ering
by the soluble proteins in the blood and slime.
After the 8th day of the experiment, the pH
of the brine treated with CO2 did not increase
significantly.

Between the initial examination and that on

the 3rd day, the pH of the flesh of the fish held
in the brine treated with CO2 dropped appre-
ciably. This change was coupled with an in-
crease in the concentration of the CO2 in the
flesh. As storage continued, the pH returned to
the same level (6.4 to 6.5) as that of the flesh
held in the untreated brine.

COa concentration. — The concentration of CO2
in the flesh and brine was measured by the
method of Umbreit, Burris, and Stauff'er (1957).
The procedure was essentially as follows: A
slice of fish was removed from the thickest part
(dorsal side) of the fish. The sample was then
carefully sectioned into horizontal cuts about
i4.-inch thick and the individual cuts analyzed.
A sample of the flesh or of brine was blended
in Tris bufl^er (hydro.xymethyl) aminoethane at
a pH of about 9. Five grams of the mixture
was added to a Warburg flask, and 0.7 ml of 0.5
M citrate buff'er at pH 4.0 was added to the
side arm of the flask. After the flask and its
contents came to equilibrium at 38° F in a water
iiath, the contents of the side arm were tipped
into the flask. The increase in manometric
pressure was recorded at irregular intervals of
time ranging up to 10 min. The amount of CO2
evolved was calculated from a standard curve
prepared by determining the changes in pres-
sure after measured amounts of acid were tipped
into known concentrations of bicarbonate.

Penetration studies carried out on whole rock-
fish showed that CO2 difl'used into the flesh very
slowly. The maximum dejjth of penetration in-
to the flesh was 0.75 inch. This depth was
reached in about 8 days of storage. The highest

437

FISHERY BULLETIN: VOL. 69. NO. 2

concentration of CO2 in the flesh (842 ppm) was
reached at this time.

The retention of CO2 in the flesh was given
consideration as a potential problem in contrib-
uting to an abnormal head-space pressure in
canned salmon and to the separation of breading
on breaded rockfish products. The initial indi-
cations were, however, that the retention of CO2
will not be a problem. As was remarked earlier,
CO2 is not absorbed well at above-normal storage
temperatures. CO2 will therefore likely be dis-
sipated from the flesh during routine cleaning,
heading, and washing operations, which are done
at temperatures considerably higher than those
of storage. In an experiment in which red salm-
on were held in modified refrigerated natural
seawater and commercially canned, no problems
were encountered as the result of CO2 retention.
In canned products such as tuna and shrimp, the
retention of CO2 should not be a problem, be-
cause these products are exposed to relatively
high preprocessing temperatures.

Additional consideration of these potential
problems, however, will be given to the retention
of CO2 in future studies on modified refrigerated
brine.

Salt concentration. — The concentration of so-
dium chloride was measured by the method de-
scribed by Greig and Seagran (1965) . In brief,
a plastic-strip indicator containing a sensitized
capillary element was placed in a filtered extract
of fish and distilled water. After the reading
was taken by means of the indicator, the con-
centration of salt in the extract was read from
a standard curve supplied by the manufacturer
of the device.

During the first 8 days of storage, the uptake
of salt was similar in the fish held in treated
brine to that in the fish held in the control brine.
Concentrations of salt in the fish held in the un-
treated brine for longer than 8 days were not
determined, because these fish spoiled at about
that time. The fish held in the treated brine
were analyzed for concentration of salt on the
10th and 17th days of storage. They showed
somewhat more uptake of salt at each of these
times.

SUBJECTIVE MEASUREMENTS

Raw Rockfish

At each sampling, a trained taste panel de-
termined the eff'ect of storage of the fish in two
kinds of brine water. The fish were also eval-
uated in the round for general appearance and
odor.

During the first 3 to 4 days of storage, fish
held in either of the two brines were of good
color, odor, and texture. By the 5th day, odors
occurred in the fish held in the untreated brine.
Between the 7th and 10th days, the fish were
judged, by appearance and odor, to be unfit for
tasting. During this time, the untreated brine
had a strong odor of putrefaction and was dark
brown.

The fish held in brine treated with CO2 re-
tained good color, odor, and texture for 17 days.
The brine was almost colorless and odorless at
the end of the experiment.

Cooked Rockfish

Cooked rockfish were prepared for taste-panel
evaluation by the method of Miyauchi, Stoll. and
Dassow (1964). The samples of cooked fish
were evaluated for appeai'ance, odor, flavor, tex-
ture, and overall quality, using a 10-point nu-
merical scale.

Table 2 gives the sensory scores for the cooked
samples. The data show that the fish in the
untreated brine spoiled between the 7th and
10th days of storage. Except for an increase
in saltiness, which occurred in the fish in either

Table 2. — Sensory evaluations on the cooked flesh of
rockfish held in COo-treated refrigerated brine and un-
treated brine (control).

Time

Overall sensory
score'

Comments

storage

Brine and
CO3

Brine
(control)

Brine end CO:

Brine (control)

days

0

3

7
10
M
17

9.0
8,0
7.0

7.0
7.0

9.0

8.0

6.0

Spoiled

Slight salty toste
Unobjectionable salty taste
Unobjectionable firm texture
Firm texture

Objectionable solly taste;
texture, color, and odor good

Slight solly taste
Off-odors
Foul off-odors

' A score of 10 denotes a product of highest quality,- one of 5 denotes
a product of borderline quality.

438

BARNETT ET AL, ; USE OF CARBON DIOXIDE IN BRINE

of the two storage environments, the fish held in
the modified brine water were organoleptically
acceptable and of good quality after 17 days of
storage. The subsequent refrigerated shelf life
of this product was not determined.

STORAGE LIFE AND QUALITY OF

CHUM SALMON HELD IN MODIFIED

REFRIGERATED BRINE

OBJECTIVE MEASUREMENTS

Both bacteriological and chemical measure-
ments were made. All the reported measure-
ments were made in duplicate.

Bacteriological Measurements

Materials and methods. — Described here are
the samples of salmon and of brine and the meth-
ods of making total plate counts.

About 300 lb. of fresh seine-caught chum
salmon, Oncorhynchits keta, were obtained in
the round from Bellingham, Wash. The salmon,
which weighed about 10 to 13 lb. each, were di-
vided into two lots of equal size. Each lot was
loaded at a one-to-one brine-to-product ratio by
weight into a drum of circulating brine con-
taining 3.3^; NaCl (see footnote 4). The
salmon had been held in ice and, at this time,
were less than 24 hr out of the water.

The brine was precooled and treated as was
described in the section on rockfish.

Three salmon and a sample of brine were re-
moved periodically for examination. The fish
samples were used to make both the objective
and subjective measurements at each sampling.

Total bacterial plate counts were made of the

bacteria on the skin of the fish. Samples of the
bacteria were obtained by the swab technique
of Tretsven (1968). Briefly, the procedure con-
sisted in swabbing the skin of the fish with a
sterile swab through a 2 cm' hole cut into the
center of a sterilized metal template. The tip
of the swab was broken off in such a way that
it fell into 10 ml of a O.K^ peptone solution,
which was then mixed. Appropriate serial di-
lutions were made from this mixture and were
plated out on the TPY medium (see the bac-
teriological section described under rockfish) for
the determination of total bacterial counts.

In previous experiments at this laboratory,
the swab technique gave results similar to those
obtained from samples of flesh. Because of this
finding and because of the relative simplicity of
the swab technique, we used it in this experi-
ment. Total plate counts of the bacteria in the
brine were made by the method used in the rock-
fish experiment.

Results and discussion.- — Table 3 shows the
total plate counts made on the untreated and
treated brines. In the control brine, the bac-
terial population steadily increased during the
18-day experiment. About the 7th day of stor-
age, the brine evidenced a slight odor of spoilage.
By the 11th day, the untreated brine smelled
intensely putrid. At that time, the total plate
count exceeded 10" organisms per milliliter.

The effect of CO2 is demonstrated by the es-
sentially unchanged bacterial population in the
treated brine during the experiment. The bac-
terial population increased between the 3rd and
9th days but appeai'ed then to stabilize. During
the experiment, the brine remained odorless and.

Table 3. — Chemical and microbiological changes occurring in C02-treated refrigerated brine and in untreated re-
frigerated brine, and on the flesh of salmon held in these brines.

Time

in

storage

Data on refrigerated brine with added CO2

Dato on refrigerated brine without CO2

pH of
brina

Salt

cone.

Total bacterial plate count

pH of

brine

Salt
cone.

Total bacterial plate count

Skin

Brine

Skin Brina

days

%

no. /cm

no. /ml

%

no. /cm

no. /ml

0

4.0

0.3

1.1X10=

1.3X10*

7.1

0,3

1.1X10=

1.3X10*

3

S.S

0.6

7.7X10*

9.3X10'

6.8

0.6

_.

8.1X10'

9

,_

1.3

1.9X101^

1.4X10=

^_

1.2

2.4X1 0«

2.6X10=

11

5.5

3.2X10*

2.1X10=

6.8

1.0X10»

5.0X10=

18

5.5

1.3

3.8X10*

2.0X10'

6.8

1.4

3.3X10=

3.5X10'

439

FISHERY BULLETIN: VOL. 69, NO.

except for a small amount of suspended protein,
remained clear and colorless.

The number of bacteria on the skin of the
salmon held in the untreated brine increased
more than 20 fold. After the salmon had been
in storage for 9 days, the number of bacteria
on the skin increased from its original value of
1.1 X lO'^ to 2.4 X lOVcm-. At 11 days of stor-
age, the salmon were judged, on the basis of
odor, to be spoiled.

Swab tests on the skin of the salmon held in
the brine treated with CO2 showed that essen-
tially no growth of bacteria occurred during the
17 days of storage.

Chemical Measurements

pH. The pH of the brine was measured as

was described earlier. The pH of the flesh was
not measured. Table 3 shows the pH values
for the brines.

Except for the initial value of 7.1, the un-
treated brine had a pH of 6.8 throughout the
experiment. As yet, we do not know if the dif-
ference in pH of the brines used for holding
rockfish and salmon is related to a difference in
the spoilage patterns of the two species.

The pH of the brine treated with CO2 re-
mained in a stable acid condition throughout the
experiment.

CO2 concentration. — No analyses were made
for CO2 in the flesh or in the brine. However
CO2 was continuously metered into the experi-
mental brine at the same rate as that in the
experiment with rockfish.

Salt concentration. — For greater accuracy
than is possible with the simple rapid method
of analysis described earlier, the concentration
of NaCl in the flesh was measured by the Vol-
hard method (Horwitz, 1960). The sample an-
alyzed was taken from both fillets of a single
fish. The fillets were mechanically comminuted
and thoroughly mixed before the sample was
taken, and the analyses were made in duplicate.

As was true with the rockfish, treating the
brine with CO2 had no effect on the rate of salt

uptake. Salmon held in both brines showed
progressive and similar increases in concen-
tration of salt to a maximum of 1.3 Sf to 1.4%
in the flesh at 9 days.

SUBJECTIVE MEASUREMENTS

Raw Salmon

At each sampling, the salmon were examined
in the same manner as had been the rockfish.

At the beginning of the experiment, the un-
treated salmon had a bright appearance and a
thick covering of colorless slime. After 4 to 5
days, however, they had lost their natural
brightness. They remained slimy, but the slime
had begun to turn yellow. By the 11th day,
the salmon looked blanched and smelled spoiled.
At this time, the brine was dark brown and
had an intense odor of spoilage.

The salmon held in the brine treated with CO2
retained most of their natural color during the
experiment. By the end of the first week of
storage, however, only a trace of slime remained
on their skins. On the 18th day, when the ex-
periment was terminated, the salmon still had a
good appearance and were free of off odors.
The brine was almost colorless and almost odor-
less.

Cooked Salmon

The taste-test scores (Table 4) show that the
samples from both storage environments were
equally acceptable through the first 7 days of
storage.

Table 4. — Sensory evaluations on the flesh of chum
salmon held in CO.^-treated refrigerated brine and in
untreated refrigerated brine.

Time in

Overall sensory
score ^

Comments

storage

3rine and
COa

Brino

(control)

Brine and COa

Brine (control)

days

0

9-0

9.0

--

3

8.0

8.0

Slight salty taste

7

8.0

8.0

__

11

7.0

Spoiled Unobjectionable salty taste,
firm texture

Odor of un-
cooked flesh
putrid

la

6.0

Color, odor, and texture
good; objectionable salty
taste

"

* A score of 10 denotes o product of highest quality; one of 5 denotes
a product of borderline quality.

440

BARNETT ET AL.: USE OV CARBON DIOXIDE IN BRINE

By the 11th day, however, the taste panel
rated those held in the untreated brine as being
unacceptable.

In contrast, the salmon held 18 days in the
treated brine were acceptable. The panel judged
that these salmon had good texture and color
but that they had only fair flavor. The deteri-
oration in the flavor may have been due in part
to the presence of absorbed salt (a salt concen-
tration of about 1.0% is generally considered
to be optimum) but was due mostly to chemical
changes that occurred in the flesh during storage.

SUMMARY AND CONCLUSIONS

The purpose of the work reported here was
to determine the effect that holding rockfish
or chum salmon in refrigerated brine treated
with CO2 would have on their storage life and
quality.

Storing rockfish in brine treated with CO2
increased their storage life by at least 1 week.
The CO2 inhibited bacterial growth and retarded
the rate at wliich the rockfish decreased in qual-
ity.

Storing chum salmon in brine treated with
CO2 gave similar results.

This study indicates that the addition of CO2
to refrigerated brine considerably improves the
preservation properties of this medium with re-
spect to bacterial spoilage. The absorption, how-
ever, of water, uptake of salt, loss of soluble
protein, and the as-yet-undetermined subsequent
refrigerated shelf life of the landed product
are problems that remain to be solved. At this
time, we therefore cannot recommend that rock-
fish and chum salmon be held in modified re-
frigerated brine beyond presently accepted stor-
age periods — that is, 8 to 10 days for either
species.

Although we do not at present recommend
extending the holding times, the reader may
wish to keep in mind that the quality of a landed
product held in refrigerated brine is significantly
improved by the addition of CO2.

Future modified brine studies will be directed
at solving the above mentioned problems and the
problems concerned with accelerated corrosion.

LITERATURE CITED

Castell, C. H.

1953. Cool storage of lightly salted fish in kench
and under pickle. Fish. Res. Bd. Can., Progr.
Rep. Atl. Coast Sta. 56: 17-22.
Collins, J.

1960. Processing and quality studies of shrimp
held in refrigerated sea water and ice. Part 1 —
Preliminary observations on machine-peeling char-
acteristics and product quality. Commer. Fish.
Rev. 22(3): 1-5.
Cohen, E. H., and J. A. Peters.

1962. Storage of fish in refrigerated sea water.
1. Quality changes in ocean perch as determined
by organoleptic and chemical analyses. U.S. Fish
Wildl. Serv-., Fish Ind. Res. 2(1): 41-47.
Davis, H. C, and G. H. Clark.

1944. Holding sardines in chilled brine. Pac.
Fisherman 42(9) : 43.
Fiskeriministeriets Fors£<gslaboratorium.

1968. Main experimental results: fresh fish. In
Fiskeriministeriets Forsogslaboratorium, Copen-
hagen, Denmark, Arsberetning fra Fiskerimin-
isteriets Forsogslaboratorium for 1967, p. 44-45.
Greig, R. a., and H. L. Seagran.

1965. Technical note no. 1 — A rapid field method
for determining the salt concentration in fresh
and smoked chub. Commer. Fish. Rev. 27(12) :
18-21.
HORWITZ, W. (editor).

1960. Official methods of analysis. 9th ed. Asso-
ciation of Official Agricultural Chemists, Wash-
ington, D.C. 832 p.
Idyll. C. P., J. B. Higman, and J. B. Siebenaler.
1952. Experiments on the holding of fresh shrimp
in refrigerated sea water. Fla. State Bd. Con-
serv., ML 2738, 23 p. (Processed.)
King, A. D., Jr., and C. W. Nagel.

1967. Growth inhibition of a Pseudomonas by car-
bon dioxide. J. Food Sci. 32: 575-579.
MiYAUCHi, D., N. Stoll, and J. Dassow.

1964. storage life and acceptability studies on the
radiation-pasteurized crab meat and flounder.
hi Application of radiation-pasteurization pro-
cesses to Pacific crab and flounder, final summary
for the period November 1963 thru October 1964,
p. 6-31. U.S. At. Energy Comm. Res. Develop.
Rep. TID-21404.

OSTERHAUG, K. L.

1957. Refrigerated sea water bibliography. U.S.
Fish Wildl. Serv., Technol. Lab., Seattle, Wash.
B-SSU-No. 2. 21 p. (Processed.)
Patashnik, M.

1966. New approaches to quality changes in fresh
chilled halibut. Commer. Fish. Rev. 28(1): 1-7.

441

FISHERY BULLETIN, VOL. 69, NO. 2

Pelroy, G. a., and M. W. Eklund.

1966. Changes in the microflora of vacuum-pack-
aged, irradiated petrale sole (Eopsetta jordani)
fillets stored at 0.5 C. Appl. Microbiol. 14: 921-
927.
Peters, J. A., and J. A. Dassow.

1965. Improved methods of handling fresh fish in
the United States. Part III. - Use of refriger-
ated sea water. Indo-Pac. Fish. Counc, Proc.
11th Sess. Sect. 3: 254-263.
Roach, S. W., and J. S. M. Harrison.

1954. Use of chilled sea water and brines in place

of ice for holding shrimp aboard a fishing vessel.

Fish. Res. Bd. Can., Progr. Rep. Pac. Coast Sta.

98: 23-24.

Roach, S. W., J. S. M. Harrison, and H. L. A. Tarr.

1961. Storage and transport of fish in refrigerated

sea water. Fish. Res. Bd. Can., Bull. 126, 61 p.

Roach, S. W., H. L. A. Tarr, N. Tomlinson, and J. S.

M. Harrison.

1967. Chilling and freezing salmon and tuna in re-
frigerated sea water. Fish. Res. Bd. Can., Bull.
160, 40 p.
Stansby, M. E., and F. P. Griffith.

1935. Carbon dioxide in handling fresh fish - had-
dock. Ind. Eng. Chem. 27: 1452-1458.
Tretsven, W. I.

1963. Bacteriological survey of filleting processes
in the Pacific Northwest. II. Swab technique for
bacteriological sampling. J. Milk Food Technol.
26: 383-388.
Umbreit, W. W., R. H. Burris, and J. F. Stauffer.
1957. Manometric techniques. Revised ed. Bur-
gess Publishing Co., Minneapolis, 338 p.
Wheaton, R. B.

1960. Effects of carbon dioxide on microorganisms
with reference to application in controlled at-
mosphere storage of refrigerated food. Whirl-
pool Res. Lab. St. Louis, Mo., Proj. 2054, Res.
Rep. 1, 34 p. (Processed.)

442

DDT RESIDUES IN SEA WATER AND PARTICULATE MATTER IN
THE CALIFORNIA CURRENT SYSTEM

James L. Cox
ABSTRACT

Continuous samples of seawater and organic particulate material collected along linear transects in
the California current system were analyzed for DDT residues. DDT residue concentrations in whole
seawater, as determined by continuous-flow, liquid-liquid extraction, ranged from 2.3 X W~^^ g/ml off
Oregon and Washington, to 5.6 X 10"'^ g/ml off southern California. Geographical patterns in these
concentration values are discussed in relation to mechanisms of land-sea DDT residue transfer. DDT
residue concentrations in particulate material collected by continuous-flow centrifugation and filtration
of the centrifugal pellet onto GFC-glass-fiber filters, ranged from 1.2 to 5.7 X 10^^ g/g carbon (with
one exception). These values were related to the density of the standing crops. DDT residues in this
particulate fraction accounted for less than 10% of the DDT residues in the whole seawater samples.
Residues which are fixed to particles of less than 1-2 ^ in diameter may account for the balance of the
DDT residues in the whole water samples. Experimental results are described which implicate adsorp-
tion as the uptake mechanism for algal cells; these experiments also support the idea that <l-2 u, di-
ameter particles carry most of the DDT residues in whole seawater.

DDT and its metabolites have dispersed into the
ocean and are found in high concentrations in
the predators of oceanic food chains. Theoret-
ical considerations predict a net transfer of
extant DDT residues to the oceans, via atmos-
pheric and river currents (Smith, 1970). In
view of the well-known chemical stability of the
principal constituents of the DDT complex, j),p'-
DDT, DDD, and especially DDE, it is not sur-
prising that levels of DDT residues in marine
plankton samples have risen during the past de-
cade (Cox, 1970a) . No published data are avail-
able, however, on concentrations of DDT residues
in seawater and in oceanic particulate matter.
Chlorinated pesticides have been found in con-
centrations up to 13 X 10"" g/ml in surface
slicks in Biscayne Bay, Fla., and at concentra-
tions of about "'- g/ml in the surrounding waters
(Seba and Corcoran, 1969). Measurements of
DDT concentration in the open ocean are needed
to construct a systematic account of DDT residue
transport to the pelagic environment of the
ocean, and to estimate the ultimate transport
of DDT residues to the sediments.

' Formerly at Stanford University, Hopkins Marine
Station, Pacific Grove, Calif. 93950; present address:
Department of Biology, Southeastern Massachusetts
University, North Dartmouth, Mass. 02747.

Manuscript received January 1971.

FISHERY BULLETIN; VOL. 59, NO. 2. 1971.

METHODS AND MATERIALS

Samples of water and particulate material
were collected during cruises of the RV Proteus
in May 1970 from Monterey Bay, Calif., to San
Diego, Calif., passing outside the islands off the
southern California coast and returning closer
to shore through the Santa Barbara Channel.
A second cruise was made in September 1970
from Vancouver, British Columbia, to just off
the mouth of San Francisco Bay, Calif. Fig-
ures 1 and 2 show the cruise tracks and the sta-
tion enumeration for these cruises.

Sampling was continuous and was done while
the ship was underway. Water was obtained
from the shipboard seawater system (PVC and
Teflon) which pumped water from about 1-2 m
below the surface. The stream was first fil-
tered through a 0.176-mm mesh net to remove
larger zooplankton from the sampled water.
The stream was then split; part of the water
was directed into a peristaltic pump which me-
tered the flow of particle-bearing water into a
continuous-flow, internal recycle and recovery,
liquid-liquid extracter of the type described by
Kahn and Wayman ( 1964) . Flow rates through
the liquid-liquid extracter averaged 480 ml/hr.

443

FISHERY BULLETIN: VOL. 69, NO. 2

45

40

SEATTLE

PORTLAND

130°

125°

Figure 1. — Chart of the transects from Vancouver,
British Columbia, to San Francisco Bay, Calif. See
Tables 1 and 3 for station data.

Since only one extracter was used for water ex-
traction, the possibility existed for incomplete
recovery of the DDT residues in the water pass-
ing through the device. Repeated tests of the
extraction efficiency using a large carboy of
oceanic seawater labelled with low levels of "C-
DDT (ca. 5 X 10 ~'- g/ml) gave an extraction
efficiency of 83% (±5%) at the flow rate set-
tings which were used with apparatus at sea.
A Variac setting of 70 was used, which produced
an internal recycle rate of 900 ml/hr. The mag-
netic stirrer rate, which affects the degree of
fracture of the solvent droi)lets, was kept con-
stant.

At the end of a particular run, the contents
of the centrifuge tubes were transferred to com-
busted 4.25 cm Whatman GFC filter papers" and
stored in glass petri dishes at — 15° C until anal-
ysis. The samples from one tube were analyzed
for particulate carbon by the wet combustion
method of Strickland and Parsons (1968). The
samples from the other tube were analyzed for
DDT residues according to previously described
methods (Cox, 1970a).

At the end of a water extraction run, the
flask containing about 100 ml of hexane, the
water extract, was removed and stored until
processing. The extract was condensed to 100
jLiliters after dehydration by passage through
an Na2S04 column. The Na2S04 was specially
rinsed with solvent and combusted at 350° C
to remove interfering impurities normally pre-
sent in the reagent salt (Lamar, Goerlitz, and
Law, 1966) . The condensed extract was spotted
on an alumina chromatoplate, which was de-
veloped in 5'^f benzene in hexane, so that the
solvent front moved 10 cm from the origin.
Centimeter wide zones were stripped from the
chromatoplates which corresponded to zones ex-
pected to contain p,;/-DDT, DDD, and DDE ac-
cording to spots on parallel chromatograms with
pure standards. "C-DDT and '^C-DDE were
also used to determine Rf zones. These zones

' The use of trade names is merely to facilitate de-
scriptions; no endorsement is implied.

Figure 2. — Chart of the transects from Monterey Bay,
Calif., to the southern California area. See Tables 2
and 4 for station data.

444

COX: DDT RESIDUES IN CALIFORNIA CURRENT SYSTEM

were eluted with a small amount of 20 ""r ben-
zene in hexane into test tubes. The eluates were
analyzed individually by the same gas chroma-
tographic techniques used for the particulate
samples.

All glassware was combusted at 350° C over-
night to remove interfering contaminants. All
solvents were nannograde or pesticide quality.
A hexane blank was run through the same pro-
cedure to detect systematic errors from any of
the steps after the initial extraction. No cor-
rection was found to be necessary.

RESULTS AND DISCUSSION

WHOLE SEAWATER EXTRACTS

Comparisons of DDT residue concentrations
in the particulate samples obtained by the cen-
trifugation/filtration method described above
(hereafter referred to as the particulate ma-
terial) are meaningless when they purport to
describe geographical differences since these
concentrations change according to the density
of the standing crop of the particulate material
(Cox, 1970a). Comparisons of the concentra-
tions of DDT residues in whole seawater
(Tables 1 and 2) reveal some significant geo-
graphical differences. Water in the southern
California region appears to have a higher DDT
residue concentration. Water off Oregon and
Washington has lower concentrations, and there
is no evidence of high DDT residue levels ad-
jacent to the mouth of the Columbia River. The
relative uniformity of the DDT residue concen-
trations for this northern cruise (Table 1) sug-
gests a diffuse source of the residues, possibly
from atmospheric fallout. Direct measure-
ments of the DDT content of dust in the at-
mosphere over the Atlantic Ocean (Risebrough,
Hugget, Griffin, and Goldberg, 1968) and mea-
surements of DDT residues in rainwater (Tar-
rant and Tatton, 1968; Yates, Holswade, and
Higer, 1970) implicate aerial transport as an
important mechanism of land-sea DDT residue
transfer. Published calculations based on an-
nual rainfall statistics and probable DDT res-
idue concentrations in rainwater predict the
concentration of DDT residues in the surface

mixed layer of the oceans to be 5 x 10^'- g/ml
(Smith, 1970). This estimate is within a factor
range of 0.5 to 1.1 of the results presented in
Tables 1 and 2.

Atmospheric fallout may be important in
areas remote from river systems draining agri-
cultural areas or in areas remote from waste
dumping of highly populated areas. Sewage
outfalls near large centers of population, such as
the southern California area, contribute a large
share of the DDT residue input to the ocean.
When the outfall is below the pycnocline, the
DDT residues in the effluent may settle with
the particles comprising the solid component
of the sewage and thus enter the benthic envi-
ronment. This may account for the high DDT
levels found in the livers of bottom dwelling
fish in the southern California region, as com-
pared to pelagic species (figures released by
the California Department of Fish and Game
in 1970). Sedimentation of organic particulate
material from the surface layers represent an
additional input to the benthos.

Input of DDT residues to the mixed layer is
represented by the following sources: (1) sew-
age input by vertical transport of material from
below the pycnocline or by direct input from
shallower outfalls, (2) input from terrestrial
runoff water which bears fallout particles, and
(3) direct input from fallout of particles over
the water. The relative importance of these

Table 1. — DDT residue concentrations in seawater ob-
tained by liquid-liquid whole water extracts from tran-
sects shown in Figure 1.

Stations

Total volume
extracted (liters)

DDT concentrotions
in water-parts per 10'^

1-2

2.6

2.3

3-8

4.1

2.7

9-10

2.8

2.3

11-14

4.3

2.3

Table 2. — DDT residue concentrations in seawater ob-
tained by liquid-liquid whole water e.xtracts from tran-
sects shown in Figure 2.

Stotions

Total volume
extracted (liters)

DDT
in wot

concentrations
sr-parts per lO*^

4-7

2.8

4.1

10-13

4.0

3.0

14-15

1.6

5.6

16-19

3.3

3.4

445

FISHERY BULLETIN: VOL. 69, NO. 2

sources is not known, but it is quite likely that
sources (1) and (2) account for the higher DDT
residue concentration in the whole seawater
samples taken off southern California.

PARTICULATE MATERIAL

Results of the analyses of the particulate ma-
terial are shown in Tables 3 and 4. Transect
10-11 (Table 4) yielded an abnormally high
value when compared to the other values for
pai-ticulate material. During transect 10-11,
visual observations were made of oil globules
at the sea surface. The abnormally high value
may have been caused by inclusion of a small
globule of this material in the particulate ma-
terial for transect 10-11, after entrainment in
the seawater system of the vessel. This value
has been deleted from further data presenta-
tions.

Table 3. — DDT residue concentrations in organic par-
ticulate material collected by continuous-flow centrifu-
gation and collection of the centrifugal pellet on GFC-
glass-fiber filter papers. Transects shown in Figure 1.

Tronsect
stations

Total volume
filtered (liters)

Wt. of carbon

in centrifugal

pellet (g X lO-S)

DDT concentration

ng DDT resi-

dues/g carbon (ppm)

1-2

48

4,500

1.4

3.4

43

2,980

2.2

S-6

29

2,550

1.8

7-8

17

490

5.7

9-10

39

2,680

2.1

n-i2

24

1,780

2.3

13-14

28

600

8.3

Table 4. — DDT residue concentrations in organic par-
ticulate material collected by continuous-flow centrifu-
gation and collection of the centrifugal pellet on GFC-
glass-fiber filter papers. Transects shown in Figure 2.

Transect
stations

Total volume
filtered (liters)

Wf. of carbon

in centrifugal

pellet (g X 10— «

DDT concentration

ng DDT resi-

dues/g carbon [ppm)

1

(>)

I72S

27.0

2-3

44

4700

1.6

4-S

36

2130

2.4

6-7

37

2750

2.4

8-9

23

2140

2.5

10-11

36

3320

16.0

12-13

19

2330

1.5

14-15

32

2690

1.4

16-17

50

3280

1.6

18-19

60

3030

1.2

20-21

42

4010

1.3

22

(')

3770

1.2

^ These samples were obtained by using a net; see text for details.

On the May cruise to southern California
(Figure 2), two phytoplankton '/t-m net tows
(35-/a effective ai)erture) were taken at stations
1 and 22, and analyzed along with the particulate
material samples. These tows consisted of 10
successive vertical hauls from 1.5 m to the sur-
face at station 1 and one oblique haul from 10 m
to the surface at station 22. The station 1 value
is in approximate agreement with earlier pub-
lished DDT residue concentrations for net phy-
toplankton samples (27 ppm per unit of carbon
converts to 0.27 ppm wet weight; compare to
values given by Cox, 1970a) . This value is con-
siderably higher than the values listed in Tables
3 and 4 for particulate material. At station 22,
the ship was stopped for an investigation of a
dense phytoplankton bloom, which consisted
principally of Rhizosoleuia spp. No measure-
ments of chloro]jhyll were made, but the water
was visibly discolored due to the high concen-
tration of algal cells in parallel streaks at the
surface. The concentration of DDT residues in
net-tow material fi-om this bloom was consider-
ably lower than in the sample taken at station 1
(0.012 ppm wet weight compared to 0.27 ppm).
This may be explained by the fact that the
standing crop density was much higher at sta-
tion 22 than at station 1.

The generally lower values in the particulate
material compared to net-tow material (except
in the case of station 22 as discussed above)
could result from at least three causes: (1)
loss of materials by cells bursting during the
centrifugation (filtration as a cause of bursting
of cells is well known, but cannot account for
a difference in this case since the net-tow samples
[Cox, 1970a and this report] were vacuum fil-
tered through GFC papers as well), (2) inclu-
sion of smaller particulate material having a
lower intrinsic DDT residue concentration, or
(3) exclusion from the centrifuge of larger zoo-
plankters which would be trapped by the phyto-
plankton net.

Cause 1 represents one reasonable source of
loss of DDT residues from the particulate ma-
terial, if in fact they should have higher DDT
residue concentrations than those reported here-
in. However, experiments with the same cen-

446

COX: DDT RESIDUES IN CALIFORNIA CURRENT SYSTEM

trifuge showed that at least 98% of the imr-
ticulate chloropliyll a in the incurrent water is
recoverable from the centrifugal pellet in whole
particulate form (trappable on GFC filters).
This indicates that breakage of cells must be
minimal.

Cause 2 is also a possible explanation. Pfister,
Dugan, and Frea (1969) pointed out that chlor-
inated hydrocarbons showed quantitative dif-
ferences of distribution among particles greater
than 0.1.5 /a which were separable by density
gradient centrifugation. Although they found
no recurrent patterns of distribution among the
DDT metabolites they were able to detect, their
results suggest large diffei-ences in the pesticide
concentrations in the four different density class-
es of particles analyzed. The form in which
their data are presented, however, does not al-
low any conclusions about lower or higher DDT
residue concentrations in the material which
was collected in the centrifuge, but not included
in the net-tow material.

Odum, Woodwell, and Wurster (1969) found
lower DDT residue concentrations associated
with smaller detrital particles in a core taken
from a sprayed marsh, but it is uncertain if
these results may be applied to oceanic seston.

Cause 3 is a possible explanation on the basis
of the mesh size of the zooplankton exclusion
filter used in the centrifugation/filtration pro-
cedure (0.176 mm) compared to the one used
in the processing of the net-tow material both
in this report and the earlier published data
(0.33 mm).

EFFECT OF STANDING CROP DENSITY

The effect of standing crop density, alluded to
above, was observed in the analyses of the par-
ticulate material. Standing crop densities were
calculated for the transects using estimates of
the volume of water filtered during the centri-
fuge running time and the carbon analyses of
the centrifugal pellet. The values for DDT res-
idue concentration are plotted vs. the standing
crop density in Figure 3. The slope of the re-
gression line fitted to the data points from both
cruises is ajjproximately — 1, indicating that
equal amounts of DDT residues were taken \\\)

by the algal materials within a given volume
of water over the range of standing crop den-
sities encountered. This is essentially the same
conclusion mentioned earlier (Cox, 1970a).

PARTICULATE MATERIAL AS A PART
OF WHOLE SEA WATER

Data points from the Vancouver to San Fran-
cisco cruise seem to fit the empirical linear re-
lationship detailed in Figure 3 much more closely
(r — — 0.99) than the data points from the
Monterey Bay to southern California cruise (r —
— 0.54). This variability is undoubtedly due
to the greater variability of the DDT i-esidue
concentrations of the whole seawater from the
southern California region, where most of the
samples were taken. There would be no need
to impute causal relationships between the whole
seawater concentration and the concentration of
DDT residues in the particulate material, if the
particulate material represented a major portion

20 M 60 100 200

STANDING CROP DENSITY (mgC/m'')

Figure 3. — DDT concentrations in the particulate
samples as a function of particulate carbon standing
crop density. Stations 1 and 22 (Table 4) are not in-
cluded, since the density of the standing crops could
not be computed because there were no measurements
of the volume of water filtered in these net-tow samples.
Also, for reasons outlined in the text, they may not
be comparable to the samples collected by the centrifuge.
Transect station 10-11 (Table 4) was omitted because
of the possible interference of oil, as described in the
text. The remaining 16 values from Tables 3 and 4
appear in this figure. Open circles refer to data from
Table 3 ; solid circles refer to data from Table 4.

447

FISHERY BULLETIN: VOL. 69, NO. 2

of the DDT residues in whole seawater. In
fact, the particulate material accounted for
less than 10 ':r of the DDT residues in the
corresponding whole water extracts (range:
1.8^/r to9.99f)- Unless the remaining amount
of DDT residues (<909f of the total present)
is in soluble form, it must be fixed to particles
not collected in the centrifugation/filtration
procedure. Typical natural distributions of
particulate matter in seawater (Bader, 1970;
Beardsley, Pak, and Carder, 1970) suggest that
most of the particulate volume and almost all
of the particulate surface area is accounted for
by particles of less than 2 /x in diameter. Thus it
is quite likely that the balance of the DDT resi-
dues in whole seawater are fixed to these smaller
particles, in view of the hydroi)hobicity and af-
finity for interfaces characteristic of the dif-
ferent metabolites of DDT. The possibility also
exists that it may occur as micelles or aggregates
which cannot be taken up by the particulate
matter.

EXPERIMENTAL EVIDENCE

Two experiments were j^erfoi'med to examine
the distribution of DDT residues between sea-
water and phytoplankton. In both experiments,
'^C-DDT in a 1-ml ethanol carrier was added to
GFC filtered oceanic seawater in a 4-liter glass
carboy which was stirred by a magnetic stirrer.
Repeated subsamples of 25 ml each were taken
from the system until successive samples gave a
constant "C activity. All counts were made on a
Nuclear-Chicago Unilux II scintillation counter.

Aliquots of a dense suspension of Diinaliella
salina culture were added to the carboy from
a large separatory funnel with a 25-ml dispen-
sing chamber, via a tube connected to the carboy.
Sampled and added amounts were such that a
constant volume was maintained. After ad-
dition of an aliquot of culture, one or two ali-
quots of 25 ml each were removed from a tap
at the bottom of the carboy. This amount was
vacuum filtered onto a GFC-glass-fiber filter pa-
per, and counts of '■'C-DDT were made of the
filter and of a petroleum ether extract of the
filtrate. Cumulative '■'C activity in the filter and

filtrate equalled amounts present in the 25 ml
aliquots (both filter and filtrate) before addi-
tion of the algal suspension, when the net
amounts of "C-DDT removed from the system
by sampling were taken into account. A cor-
rection was made for adsorption or possible
trapping of small particles of "C-DDT on the
filter. The correction factor, expressed as per-
cent of total activity per 25-m! aliquot which
was on the filter before addition of the algal
suspension, was constant in the five replicates
taken just before the algal cells were added.
This correction factor may have changed during
the course of addition of the algal cells, but the
techniques used did not allow a distinction be-
tween "C activity on the filter which adsorbed,
associated with trapped small pai'ticles, or asso-
ciated with the algal cells themselves. I be-
lieve that this change was small and did not
materially afl^ect the outcome of the experiments.

Figure 4 shows the results of the two experi-
ments. In Experiment 1, the seawater used in
the carboy was not altered; in Experiment 2,
the seawater was specially prepai-ed to increase
the load of small (<l-2 fi) inorganic particles,
to see what effect this might have on the uptake
function. Nuchar-attaclay, a mixture of finely
divided charcoal and clay pai-ticles (attapulgite) ,
was added to 2 liters of GFC-filtered seawater.
After shaking, the mixture was refiltered
through a GFC filter. It is estimated that only
a tiny fraction of the initially added Nuchar-
attaclay (initially added amount was 0.1 g) ac-
tually got through the filter. The 2 liters of
water i)roduced in this way were mixed with
another 2 liters of GFC-filtered seawater and
jHit into the carboy. Two other conditions were
diff"erent in Experiment 2. The culture of Dii-
naliella salina used was denser (note that the
arrow in Figure 4 indicates that 750 /ng C/liter
is reached at a lower volume of culture added).
The initial concentration of "C-DDT in Exper-
iment 2 was ai)|)roximately 15 ppt.

The first part of the uptake functions in Ex-
l)eriments 1 and 2 aijjieared to be linear, indi-
cating that under the conditions ])revailing at
the beginning of each experiment, each Diinal-
iella cell took up a con.stant amount of the "C-

448

COX: DDT RESIDUES IN CALIFORNIA CURRENT SYSTEM

<

Q
O
I
O

750figmC/l

600 700

-(- ATTAPULGITE/CHARCOAL PARTICLES<l-2|i

-EXPERIMENT 2

- y

o

-750pgniC/i

- /° Y=l.ll +

1 1 1

0034 X

1 1 1 1

18-
16-
14-
12-
10-
8-
6-
It-
2

0 100 200 300 400 500 600 700

VOLUME ALGAL SUSPENSION ADDED (ml)

Figure 4. — Percentage of total "C-DDT in sample
aliquots recovered on GFC filters, plotted as a function
of total volume of Dunaliella salhia culture added to a
constant volume system. See text for detailed discussion.

DDT which was available. Both curves show
inflection points after the density of cells in-
creases beyond 750 ^ug C/1. The fact that the up-
take per cell was constant over the linear range
indicates that each cell has a saturation value
for uptake of DDT, which is independent of the
ambient concentration of DDT available. The
curves presumably begin to level off when the
"C-DDT which was available for uptake is most-
ly associated with the algal mass already added.
If algal cells exhibit a saturation value for
uptake of DDT, then adsorption of DDT to the
cell surface is a more likely explanation for DDT
uptake than phase partitioning of DDT between
seawater and the lipid component of the algal
cell, as has been previously hypothesized (Cox,

1970b). Each Dunaliella salhia cell probably
had a total cell surface area of 240 fjr (Mullin,
Sloan, and Eppley, 1966). The cells in Experi-
ments 1 and 2 took up a mean of 5 X 10~^ pico-
grams '^C-DDT//i-. This value may be near the
asymptotic saturation value for Dunaliella salina
for the experimental conditions described above.
The validity of a saturation value of this kind
needs to be tested with other phytoplankton
species over a wide range of ambient DDT con-
centrations.

A quantitative solution to simultaneous
Freundlich adsorption equations for the algal
cells and the <l-2 ix particles could explain the
uptake curves if the adsorption energy coeffi-
cient were known in each case. Studies such
as those of Weber and Gould (1966) should
therefore be applied to uptake of DDT residues
by phytoplankton and smaller particles to elu-
cidate the relationships discussed here.

No measurements were made of the concen-
tration of the <l-2 fi particles in the untreated
seawater of Experiment 1 or the treated sea-
water of Experiment 2. Thus the differences
can only be explained qualitatively. The higher
concentration of '^C-DDT in Experiment 2
(30 ppt) was appai'ently reflected in the uptake
of '^C-DDT per unit of cell surface area ; Ex-
periment 2 yielded a value of about 6 x 10~^
picograms "C-DDT'/i-, which is higher than the
mean for both experiments quoted above. The
uptake of "C-DDT per unit of cell surface area
in the case of Experiment 2 is probably closer
to the asymptotic saturation value because of
the higher concentration of '^C-DDT in the me-
dium. The main difference between the curves
for Experiments 1 and 2 is the position of the
inflection point. Experiment 2 shows an ap-
parent inflection point which is lower than the
apparent inflection point of Experiment 1,
indicating a lowering of the available percent-
age of total "C-DDT in the system. The total
small particle concentration of the system was
not measured, so this apparent change must be
regarded as a presumptive effect of the Nuchar-
attaclay addition.

If a large percentage of the DDT added to
aqueous systems is fixed to a particle fraction

449

FISHERY BULLETIN: \0L. 69, NO. 2

less than 1-2 /x in diameter, then the experi-
mental DDT uptake results that have been in-
terpreted in terms of a partition coefficient or
a concentration factor using the nominal con-
centration of DDT in the aqueous medium be-
come relatively meaningless without knowledge
of the fraction of the initial amount of DDT
present which is fixed to these small particles
and hence unavailable to the test organism. In
the oceanic environment, it is quite likely that
the amounts of "available" DDT residues are
exceedingly small. Uptake of DDT by the seston
is probably closely coupled with input pulses
which would be largely determined by fallout
conditions at the surface and seasonal runoflF
of DDT residues from land areas. "Available"
DDT residues which may rise during these pe-
riods will be taken up by plankton. A complete
picture of the processes involved in DDT trans-
port to the pelagic environment has yet to be
drawn and will require further experiinental and
analytical work.

ACKNOWLEDGMENTS

I thank David Bracher for technical assist-
ance. Vance McClure, John MacGregor, and
Robin Burnett gave valuable advice in prepara-
tion of the manuscript. The work was support-
ed by NSF Grant GB 8408, a grant from the
State of California Marine Research, Committee,
and an NSF predoctoral fellowship.

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1970b. Low ambient level uptake of i^C-DDT by

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Kahn, L., and C. H. Way'.man.

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Yates, M. L., W. Holswade, and A. L. Higer.

1970. Pesticide residues in hydrobiological environ-
ments. Water, air, and waste chemistry section
of the American Chemical Society Abstracts.

450

EGG LOSS DURING INCUBATION FROM OFFSHORE
NORTHERN LOBSTERS (DECAPODA: HOMARIDAE)

Herbert C. Perkins'

ABSTRACT

Egg loss during incubation from offshore northern lobsters, Homarus americanus Milne Edwards, was
estimated by counting the eggs of 196 females. The lobsters were captured along the continental shelf
off southern New England during October (eggs recently extruded), April, and June (eggs nearly
ready to hatch). Egg loss during the period October to June averaged 36% for females of all sizes
studied.

The exploitation of northern lobsters in the off-
shore canyons of the continental shelf is steadily
increasing (Skud, 1969). Owing to this in-
creased effort, the National Marine Fisheries
Service (formerly the Bureau of Commercial
Fisheries) has initiated a study of the biology
and population dynamics of the stock. As ac-
curate estimates of fecundity are useful for
studying population dynamics, the present study
was undertaken to determine the extent of egg
loss from female Homarus ame7'iccu)us during
embryonic development and the consequential
magnitude of error in estimating fecundity if
any loss occurs. Brunei (1962, 1963) has shown
that female sjiider crabs, Chionoectes opilio, may
lose over half their eggs during the incubation
period. The present paper shows the extent
of egg loss from the northern lobster and the
difference in fecundity estimates depending on
the time during the development period when
the eggs are counted.

according to carapace length. The mean num-
ber of eggs and the range for each 5-mm group
are recorded in Table 1. Carapace length was
measured from the posterior edge of an eye
socket to the distal edge of the carapace.

The females were frozen at sea, later thawed
in the laboratory and their eggs removed from
the pleopods by stripping with small forceps.
The eggs were hardened in Formalin for 24 hr,
then soaked in fresh water before being dried
in an oven at 150° C. Drying time lasted 1 to 2
hr depending on the size of the egg mass. After
drying, the individual egg masses were rubbed
over a 1-mm screen to break up any clusters and
eliminate non-egg material, then counted with
an electronic counter (Boyar and Clifford,
1967). Test runs with the counter produced
a maximum error of ± 29^r. The counts given
represent numbers of viable eggs only (non-
viable eggs are rarely observed in masses of
developing eggs).

METHODS AND MATERIALS

The lobsters were captured with otter trawls
during research and commercial cruises at Hud-
son, Veatch, Oceanographer, Lydonia, and Cor-
sair Canyons. These canyons are located along
the edge of the continental shelf, south and east
of New England. The 196 female lobsters used
in this study were divided into 5-mm groups

' National Marine Fisheries Service Biological Lab-
oratory, West Boothbay Harbor, Maine 04575.

Manuscript received January 1971.

FISHERY BULLETIN: VOL. 69, NO. 2, 1971.

RESULTS AND DISCUSSION

A curvilinear relationship was apparent when
the number of eggs was plotted on the corres-
ponding carapace length. The same result was
noted by Saila, Flowers, and Hughes (1969).
In order to employ covariance analyses in this
study, the data were transformed to natural
logarithms. The lines presented in Figure 1
were plotted from the antilogarithms of the val-
ues calculated from the linear regression equa-
tions (Table 2).

451

FISHERY BULLETIN; VOL 69. NO. 2

Table 1. — Month of capture, range and mean number of eggs for each 5-mm carapace length group for the 196

offshore female lobsters.

Carapace

OCTOBER

APRIL

JUNE

length
groups

Number

of
lobsters

Number of eggs

Number

of
lobsters

Number of eggs

Number

of
lobsters

Number of eggs

(mm)

Mean Range

Mean Range

Mecn Range

80-84

3

10,449

8,286-11,357

1

9,212

__

1

7,890

_.

85-89

10

14,341

8,707-17.428

2

10,518

9.010-12,027

2

7.920

6,400- 9.440

90-94

23

16,317

11,501-21,348

4

13,476

9.578-18.400

5

8,950

6.410- 12.240

95-99

15

19,440

14.425-25.454

3

15.973

12,140-19,310

3

9,887

8,270- 10,700

100-104

15

20,463

13.831-26,832

8

19.355

12.853-23.270

6

14,900

8,470- 17,940

105109

1

24.896

^_

4

19,212

16.161-22.853

4

19.692

10.160- 30190

110-114

3

30,452

27,321-32,309

11

23.789

17.639-28.245

0

__

__

115-119

0

_.

__

7

27,001

18,703 33,160

1

30.602

120-124

2

44.334

42.059-46.610

1

26,628

3

27.743

20,671- 31,789

125-129

2

51,184

50,008-52,361

5

35.757

18.821-40.159

1

42.743

__

130-134

0

__

..

S

32.796

25,180-41.636

4

40.728

33,238- 49,820

135-139

1

55,240

__

2

31.045

26,850-35,240

4

40,092

22,600- 52.956

140-144

0

__

2

51.002

48,526-53,478

4

45.506

32,770- 54,820

145-149

c

..

1

45,928

__

2

68.510

67,660- 69,360

150-154

0

0

5

52.457

44,463- 69,095

155159

0

._

1

78,422

3

51.978

37,400- 66.551

160-164

0

1

66,210

3

64,673

56.302- 73,207

165-169

0

0

2

63.175

62.573- 63,777

170-174

0

..

1

70,178

3

71.831

60,866- 87,303

175-179

0

__

0

1

81,164

--

180-184

0

__

0

3

73,770

56,372-104,541

185-189

0

0

—

—

0

_-

—

190-194

0

__

0

1

78,844

--

195-199

0

-

--

0

--

--

1

90,400

-

Table 2. — Raw sums, sums of squares, sums of cross products, and regression equations derived from transformed
data on carapace lengths and numbers of eggs from 196 berried female lobsters captured during October, April,
and June. (X = loge carapace length, Y ^ lege number of eggs.)

Month

October

April

Juno

75
59
62

ZX

IX'

lY

ZY'

Regression equation
(K = a+bX)

342.8625
279.4272
301 .6997

1568.1306
1324.7648
1471.6059

737.7546
595.6230
640.9857

7267.0013

3375.0329

6026.4485

2824,7918

6666.0539

3130.1578

Y = -5.0202-|-3.2499(X)

Y = -3.2280+2.8132(.V)
f = -5.0231-f3.1569(A-)

The regression lines were all significantly dif-
ferent (P < 0.01) in level (F intercept) from
each other. No significant difl"erence was found
in the slope of any of the lines, indicating egg
loss is consistent between extrusion and hatch-
ing from females of all sizes. The average total
loss from extrusion to hatching throughout the
size range of the females studied was S&'^r , and
the average loss during the last few months
(April through June) was IS*"!.

The eggs obtained in October were all in pre-
naupliar condition (Templeman, 1940) and were
judged to be no more than 4 weeks in age. Those
eggs obtained in June were all within a month
of hatching. Twenty-four berried females,
caught in June, were kept in laboratory tanks
where all egg hatching was completed by the

middle of July. Eggs taken in April showed less
development than those taken in June, and 12
females kept in the laboratory tanks from the
April samples completed hatching by the first
of July. Water temperatures in the laboratory
during April and May were slightly higher than
would be expected in the offshore waters for
the same period.

The offshore waters where the lobsters are
found undergo no great seasonal temperature
fluctuations (Colton et al, 1968) typical of the
coastal waters of New England. I have exam-
ined over 500 berried females from the offshore
area and conclude that extrusion of eggs occurs
in September and October, and that hatching
occurs the following June or July. I have found
no deviation from this pattern; however, slight

452

PERKINS: EGG LOSS DURING INCUBATION

80 90 100 MO 120 130 140 150 160 170 180 190 200
CARAPACE LENGTH (MM)

Figure 1. — Regression lines of egg counts versus cara-
pace lengths for October, April, and June.

variation in the extent of development of eggs
from one year to the next during the same month
has been noted, and from canyon to canyon dur-
ing the same year. These variations among
years and areas are attributed to small differ-
ences in water temperature, while the consistent
year to year reproductive periods are attributed
to the relatively constant thermal environment.

While counts obtained from ovarian or newly
extruded eggs testify to the reproductive poten-
tial of a female, counting eggs that are close to
hatching give more reliable estimates of a fe-
male's potential contribution of larvae to the
population.

ACKNOWLEDGMENTS

I wish to thank Mrs. Gwyneth M. Kensler for
translating the papers by P. Brunei; the captain
and crew of the MV Stanley M. Fisher for sup-
plying me with some of the berried females;
Jack Mahoney and Paul Swain of the National
Marine Fisheries Service Office of Statistical
Services, Gloucester, Mass., for assistance in ob-
taining some of the samples.

LITERATURE CITED

BoYAR, H. C, AND R. A. Clifford.

1967. An automatic device for counting dry fish
eggs. Trans. Amer. Fish. Soc. 96: 361-363.

Brunel, p.

1962. Nouvelles observations sur la biologie et la
bionietrie du crabe araigne'e Chionoecetea opilio
(Fabr.). Sta. Biol. Mar. Grande-Riviere, Que'.
Rapp. Annu. 1961, p. 63-72.

1963. Troisieme serie d'observations sur la biologie
et la biometrie du crabe-araigne'e Chionoecetes
opilio (Fabr.). Sta. Biol. Mar. Grande-Riviere,
Que'. Rapp. Annu. 1962, p. 91-100.

CoLTON, J B., Jr., R. R. Marak, S. R. Nickerson, and
P. R. Stoddard.

1968. Physical, chemical, and biological observa-
tions on the continental shelf. Nova Scotia to Long
Island, 1964-66. U.S. Fish Wildl. Serv., Data Rep.
23, 189 p.

Saila, S. B., J. M. Flowers, and J. T. Hughes.

1969. Fecundity of the American lobster, Homarus
nmericaniis. Trans. Amer. Fish. Soc. 98: 537-539.

Skud, B. E.

1969. Giant lobsters. In F. E. Firth (editor). The
encyclopedia of marine resources, p. 353-357. Van
Nostrand Reinhold, New York.
Templeman, W.

1940. Embryonic developmental rates and egg-lay-
ing of Canadian lobsters. J. Fish. Res. Bd. Can.
5: 71-83.

453

ERRATA

Fishery Bulletin, Vol. 69, No. 1

Rothschild, Brian J., and James W. Balsiger, "A linear-programming solution to salmon man-
agement," p. 117-140.

1) Page 120, left hand column, first line below equation (4) has the inequality in the wrong
direction and should have:

"The constraint is redundant if X' ^ 2 Kj."

i = 1

2) Page 120, right hand column, fourth line below equation (8) should have same script 'V/" as
"■ ^^" in equation 8-

3) Page 120, right hand column, equation (9) has the inequality in the wrong direction and
should be:

E X H

F

4) Page 137, right hand column, line 40 should read:

... a series of years "maximizing" . . .

Seckel, Gunter R., and Marian Y. Y. Yong, "Harmonic functions for sea-surface temperatures
and salinities, Koko Head, Oahu, 1956-69, and sea-surface temperatures, Christmas Island, 1954-
69," p. 181-214.

1) The senior author's name is misspelled. It should be:
"Gunter R. Seckel," rather than "Gunther R. Seckel."

INTERNAL DEFENSES OF CRUSTACEA: A REVIEW

Carl J. Sindermann-

ABSTRACT

Studies of the internal defenses of Crustacea have a discontinuous history, which began in the late 1800's.
Elaborate early studies of phagocytes and humoral factors in the hemolymph have been extended with
renewed vigor during the past decade. As is true for other invertebrates studied, phagocytosis of for-
eign particles by fixed and mobile cells in the crustaceans is augmented by naturally occurring bacteri-
cidins, lysins, and agglutinins. A few instances of experimental enhancement of titers of such hu-
moral factors by previous exposure to foreign protein have been reported. Specificity of natural and
experimentally enhanced humoral factors is much lower than that of vertebrate immunoglobulins, but
probably such factors act synergistically with cellular protective mechanisms, as they do in the vertebrates.
Phagocytosis by fixed and mobile cells in gills, pericardial sinus, and sinuses at the bases of appendages
seems to be a principal defense perimeter in many crustaceans. EflScac.v of phagocytes in destroying in-
vading microorganisms varies, depending on the species of the microorganism, as well as host physiology
and environmental factors. Phagocytic activity is enhanced by hemolymph factors, which, in addition
to immobilizing and agglutinating the invading organisms, also sensitize them to phagocytosis.

Hemolymph factors, most of which seem to be of cellular origin, may also have bactericidal or lytic
activity, leading to extracellular destruction of microbial invaders. A few recent studies indicate that
effects of hemolymph factors may be enhanced e.xperimentally by injection of killed or living micro-
organisms.

The number of known microbial diseases in crustaceans is greater than that known in most other in-
vertebrate groups, with the possible exception of the Mollusca and Insecta. The number and depth of
studies concerned with internal defense mechanisms of Crustacea are similarly greater than those of
most other invertebrate groups — again with the possible exception of the moUusks and insects. One mi-
crobial pathogen of Crustacea that has received adequate attention is daffkya hovinri — a gram-positive
coccus which causes a fatal septicemia in lobsters and is capable of infecting other decapods. An elab-
orate series of studies in several laboratories has elucidated many details of the host-parasite relation-
ship and has also provided extensive information about the internal defenses of a number of the larger
Crustacea. Gaffkya constitutes a test microorganism of choice for future studies of disease processes
in crustaceans.

Thus the available information about cellular and humoral defenses of Crustacea against invasion
by foreign protein constitutes a significant part of what we know about such proces.ses in the inverte-
brates. Phagocytosis, augmented by humoral factors with low specificity, seems to be the fundamental
means of internal protection in the crustaceans and in other groups of invertebrates as well.

Investigations of the internal defense mecha-
nisms of invertebrates against disease have pro-
gressed with renewed vigor in the past decade.
Literature has accumuhited to the point where
condensation and summarization of information
about certain invertebrate groui^s, such as the
Crustacea, seem justified.

' Contribution No. 197, National Marine Fisheries
Service, Tropical Atlantic Biological Laboratory, Miami,
Fla. 33149.

" National Marine Fisheries Service, Tropical Atlantic
Biological Laboratory, Miami, Fla. 33149.

The hirge number of jiubUshed reports on in-
ternal defenses of Crustacea can provide a good
indication of the extent of our knowledge of im-
munity ill marine invertebrates. Beginning with
the pioneering work on phagocytosis and the en-
tire process of inflammation by Metchnikoff
(1884, 1893, and 1905), and on humoral factors
described in the very extensive (but sometimes
poorly documented, in terms of procedux-es and
data) work of Cantacuzene (1912-34), the Crus-
tacea have often been animals of choice in studies
of internal defense mechanisms. A significant

Manuscript accepted February 1971.

FISHERY BULLETIN: \0L. 69, NO, 3. 1971.

455

FISHERY BVLLETIM: VOL. 69. NO, 3

body of literature has accumulated, with conspic-
uous bulges in the early years (1884-1930) and
in the past decade (1960-70), but with a very
narrow waist during the period 1930-60.

Studies of humoral defenses of the larger
Crustacea during the past 5 years (1965-70) are
curiously reminiscent of work reported by Can-
tacuzene and his associates during the period
1912 to 1934, with the very important difference
that most of the modern work includes elements
that were largely missing from earlier reports,
such as details of procedures, sujiporting data,
adequate controls, and attempts at quantitation
of results.

Because so much of the literature produced be-
fore 1940 lacks adequate quantitation and fails
to jn'ovide details of techniques used, it is often
difficult to relate results to those of more recent
studies. Bang (1967b) has deliberately ad-
dressed himself to a rejietition of earlier studies
but has used modern methods in an attempt to
improve the relationship. Other recent reports,
even though based on species other than those
used in earlier studies, constitute ree.xaminations
of the concepts and general findings of the early
investigators.

It is difficult to determine why the early work
on immune responses in invertebrates so effec-
tively begun by JMetchnikoff, Cantacuzene, Cue-
not, Bruntz, and others during the late 19th
century and the early 20th century seemed to
lose impetus and then virtually cease until re-
cently. It is apparent from the literature,
though, that research on invertebrate defenses,
initiated so auspiciously, receded for a number
of decades to the backwaters and eddies of the
mainstream of advances in immunology, which
was concentrated on the homoiothermic vei-te-
brates. This may be explained in part by a
natural and necessary concentration of research
interest on human and mammalian immune re-
sponses (most immunologists wei'e — and still
are — generally associated with medical schools
and hospitals) . Part of the explanation also may
be that earlier work failed to disclose any defense
mechanisms in invertebrates that seemed funda-
mentally or conceptually different from those
that were being elucidated for the vertebrates.
More importantly, the explanation may have

been that much of the earlier work failed to
indicate any immunologic responsiveness in the
invertebrates tested. In spite of occasional suc-
cesses, the "inability of invertebrates to respond
to the introduction of antigen by formation of
antibodies" became a sort of dogma among many
of the early biologists, as was pointed out by
Cantacuzene (1923b). Failures to find responses
may have been due jiartly to choice of inocu-
lum with negligible antigenicity in the experi-
mental invertebrate. Two factors may have
caused the recent resurgence of interest among
biologists in comparative immunology (which
is gradually beginning to include the lower
vertebrates and the invertebrates): (1) an
evident need to reexamine the conceptual and
evolutionary basis of immune responses and (2)
an interest in understanding the internal de-
fenses of invertebrates, which allow them to
survive in a microbe-rich environment even
though they lack the specific antil)ody response
characteristic of most vertebrates.

The subject matter of the present review is
one that has been treated previously (Cantacu-
zene, 1923b: Huff, 1940; Baer, 1944; Bang
1967b; Levin, 1967; Tripp, 1969; Rabin, 1970b;
Bang, 1970). Many of those iiapers, however,
were broad considerations of the invertebrates
as a whole, and discussions of internal defenses
of Crustacea were often more or less incidental.
It is interesting — as Good and Papermaster
(1964) pointed out — that no review of inverte-
brate immunity has em])hasized induced re-
sponses. A recent, and excellent, 2-volume text
on the physiology of Crustacea (Waterman,
1960) does not include a detailed consideration
of the very imjiortant subject of internal de-
fenses, except for reference to hemocytes and
phagocytosis (Maynard, 1960; Parry, 1960),
and a consideration of hemolymph coagulation
(Florkin, 1960).

The general plan for this review is to discuss
some of the early literature, after a brief pre-
liminary statement about concepts and termi-
nology, and a summary of known diseases of
Crustacea. More recent studies will then be
considered by categories of cellular and humoral
systems: phagocytic, bactericidal, lytic, agglu-
tinating, iJrecii'jitating. phage clearing, and anti-

456

SINDERVIANN: INTERNAL DEFENSES OF CRUSTACEA

toxic. A final section will attempt a detailed
review of the demonstrated systems of internal
tlefenses of lobsters and other crustaceans
against the microbial pathog-en Gaffkya homaii
— which is one of the best examples of a test
system for invertebrates for which existing in-
formation is adequate.

CONCEPTS AND TERMINOLOGY

Before proceeding with an examination of in-
ternal defenses of crustaceans, a brief review
of some of the terminology may be relevant.
"Resistance" and "susceptibility" have often been
used interchangeably and reciprocally, but as
Schneider (1951) and Stauber (1961) pointed
out, insusceptibility and resistance should prolv
ably be considered as sejiarate biological phe-
nomena. Insusceptibility refers to those exist-
ing external or internal features of an animal
— morphological and physiological — which deny
access to a potential pathogen, or prevent its
successful establishment and survival. Resist-
ance, on the other hand, has been defined by
Read (1958) as "those changes in the physio-
logical state of the host which represent a re-
sponse to present or jirevious contact with the
parasite or with a similar chemical entity."

Resistance (and its equivalent — "immunity") ,
defined as host response, can then be considered
as "innate" (natural) or "acquired" (induced).
Innate resistance includes responses to primary
contact with a pathogen, and acquired resistance
includes responses that develop after primary
contact. The distinction between the two types
of response is not, however, always as definitive
as might be preferred. Acquired resistance is
often characterized by enhanced responsiveness
to subsequent contact with a pathogen.

Resistance, whether innate or acquired, may
be cellular or humoral. The cellular defense
mechanisms are based largely on activities of
leucocytes (hemocytes of invertebrates) and in-
clude: phagocytosis — engulfment and often di-
gestion of foreign particles, lencocytosis (hemo-
cytosis), and leucocytic (hemocytic) infiltiv-
tion — the mobilization of hemocytes in the lilood
stream and their migi-ation to invaded or injured
tissues; coagnkttion — the formation of cellular

or extracellular clots to close gaps in the circu-
latory system and to immobilize microorganisms;
and encapsulation — the surrounding of large
masses of invading material liy phagocytes and
fibrocytes. Humoral defense mechanisms, which
probably depend on cellular secretions or cell
disrur>tion, and act synergistically with cellular
defenses, include agglutinating, lytic, precipi-
tating, and bactericidal systems, and other ac-
tivities (Figure 1).

POTENTIAL PATHOGEN IN
EXTERNAL ENVIRONMENT

Figure 1. — Mechanisms of internal defense.

Antibodies (in the vertebrate sense of specific
immunoglobulins) have not laeen demonstrated
in invertebrates, although less specific antibody-
like activity is common. Since antibodies have
not been demonstrated, it is probably technically
incorrect to use the term "antigen" with in-
vertebrates. The semantics involved will be con-
sidered in the discussion section, but for con-
venience the term will be used in this paper.
Furthermore, it must be made clear that when
lysins, precipitins, agglutinins, etc. of inverte-
brates are discussed, no af^empt is made to

457

FISHERY BULLETIN: VOL. 69, NO. 3

homolog'ize them with vertebrate factors. The
terms merely indicate the type of activity pro-
duced.

DISEASES OF CRUSTACEA

An imjiressive array of disea.^es atnictinjr the
Crustacea has been described (summarized in
Sindermann, 1970, and Bang, 1970). A number
of these diseases are of microbial etiology, and
Koch's postulates have been satisfied for several
of them. Some of the published reports con-
cerning crustacean diseases include information
about host defenses against infection, others do
not. The literature also contains information
about a variety of experimentally induced infec-
tions in Crustacea, many of them produced by
microorganisms not known as pathogens in
natural populations. Such experimental studies
have been pai-ticularly useful in elucidating pos-
sible internal defense mechanisms — augmenting
studies with known pathogens. The following
summary is just that and is not intended as a
detailed treatment of crustacean diseases. Some
general background information on known di-
seases seems important, however, to any con-
sideration of internal defense mechanisms.

The only virus disease of invertebrates re-
])orted in the scientific literature is one that oc-
curs in crabs, Portunus dejmrator, on the French
Mediterranean coast (Vago, 1966). Disease
signs mentioned in his very brief paper included
progressive darkening of the exoskeleton, paral-
ysis, and death.

Bacterial infections of various Crustacea have
been described, beginning with a disease of beach
hoppers on the French coast caused by lumines-
cent bacteria (Giard and Billett, 1889). Exper-
imental infections were obtained by injecting
cultured microorganisms, and some of the crus-
tacean species tested exhibited varying degrees
of resistance to experimental infection. Another
luminescent disease was reported in sand fleas
(Talorchestia longicornis and Orchestia pluti-
nus) from Woods Hole, Mass., by Inman (1927) .
Luminiscent bacilli were cultured, and experi-
mental infections obtained. Luminiscent bac-
teria were also isolated from the digestive tracts
of nonluminous sand fleas. A bacte)'ial disease

of Gammarus mariiuis was reported from Eng-
land by Tait (1917), in which signs of disease
included change in color of the infected ami^hi-
pods from brown to opaque .vellowish-white, re-
duction in numbers of blood cells, and absence
of coagulation of hemolymph. Among the larger
decapod Crustacea, a severe bacteria! disease of
lobsters caused by gram-po.-itive cocci, Gnffkya
hoinari,- was recognized in 1947 (Snieszko and
Taylor, 1947) and has been the subject of in-
tensive studies since then (to be considered in
detail later in this iKijjer). Experimental in-
fections and resultant mortalities of blue crabs,
CalUnectes sapidua, from Chesapeake Bay were
reported by Krantz, Colwell, and Lovelace
(1969) withVibrio panthenwlyticns. The micro-
organism has been isolated from mollusks, fishes,
and sediments in various parts of the world and
is known as a cause of human gastroenteritis in
the Orient. Additionally, several exam])les of
"shell disease" — erosion of the exoskeleton by
chitin-destroying bacteria — are known in lob-
.sters, crabs, and shrimps (Hess, 1937; Rosen,
1967. 1970; Anderson and Conroy, 1968).

Fungus diseases of Crustacea are surijrisingly
numerous in reports dating back to Metchnikofl"
(1884), who described fatal infections of Daph-
nia caused by Monofijiora hiciisjiidata and who
first emphasized the crucial role of phagocytosis
in determining the outcome of infection. A
yeast infection in sand hoppers, Talitrus, from
the coast of France, was reijorted by Herrmann
and Canu ( 1891 ) . Experimental infections from
exposure to cultured microorganisms were fatal
to Tttlitriis in 20 to 2.5 days. Phagocytosis was
marked in such infections, and the hemolymph
became milky in advanced cases. Crabs (Car-
cinus niaenofs) , jirawns (Paluemonetes varimis) ,
and crayfish (Astacus fiiiriatulis) were not sus-
ceptible to the experimenUil infections. Pixell-
Goodrich (1928) descriljed another yeast infec-
tion which was epizootic in ddnimano; from a
stream in England. The pathogen Cryptococciis
(jammarl repi'oduced in the hemolymph and
rendered it milky in color, coagulation was re-
tarded, and heavil.v infected individuals died.
Phagocyto.sis was active and sometimes success-
ful in overcoming infections. Hypertrophy of
fixed phagocytic cells was common.

458

SINDERMANN: INTERNAL DEFENSES OF CRUSTACEA

One of the most severe, widespread, and long-
continuing epizootics known in invertebi'ates has
affected and still affects European crayfish. It
is caused by the fungus Aphanomyces astaci (al-
though other microorganisms have been var-
iously associated with mortalities). Known as
"Krebspest," the disease swept through cray-
fish populations of Europe beginning about the
turn of the century (Schikora, 1906, 1926;
Schaperclaus, 1935; Nybelin, 1935; Mannsfield,
1942; Unestam, 1965; Gordon, 1966). Appar-
ently resistance differs among species — the
American craj'tishes, for example, seem less seri-
ously affected by the pathogen in experimental
studies.

Other fungus diseases of Crustacea include
a systemic infection of pea crabs. Pinnotheres,
from English sea mussels by Leptolegnia marina
(Atkins, 1929, 1954a); a systemic disease of
cultured prawns, Palaemon serrahis, in England,
caused by Pythium sp. (Anderson and Conroy,
1968) ; a gill infection of pandalid shrimp,
Dichelopandalus leptocenis, from the western
North Atlantic, caused by a chytrid-like micro-
organism (Uzmann and Haynes, 1969) ; and gill
infections of lobsters, Homarus vulgaris and
Palinurus vulgaris, in Italy, caused by Ramularia
hranchialis and Didymaria palinuri — both Fungi
Imperfecti (Sordi, 1958).

Fungi also infect and destroy egg masses of
Crustacea. Eggs of blue crabs, Callinectes sa~
pidiis, from Chesapeake Bay may be infected by
Lageiiidiuin callinectes (Couch, 1942; Newcombe
and Rogers, 1947; Rogers-Talbert, 1948) ; and
eggs of pea crabs are often infected by Plec-
tospira dubia and Pythium thalassium (Atkins,
1954b, 1955).

Among the many protozoan diseases of Crus-
tacea, those caused by microsporidans are prob-
ably the most destructive. Nosema sp. and
Plistophora cargoi destroy body muscles of blue
crabs (Sprague, 1965, 1966); Nosema pulvis
and Thelohania maenadis infect muscles of green
crabs, Carcinus maenas (Perez, 1905a, 1905b,
1907). Other microsporidan infections of body
muscles in Crustacea include those produced in
Gammurus by Theileria sp. and Nosema sp.
Necrotic muscle fibers containing microsporidan
spores were destroyed by phagocytes (Pixell-

Goodrich, 1928). Other pathological effects of
microsporidans on gammarids have been recent-
ly reported by Bulnheim (1967) and Bulnheim
and Vavra (1968). Crayfish muscles are at-
tacked by Microsporida of the genera Thelohania
and Nosema (Sprague, 1950b; Pixell-Goodrich,
1956; Sogandares-Bernal, 1962). Microsporida
are also significant pathogens of shrimps.
Sprague (1950a), Woodburn et al. (1957), Iver-
sen and Manning (1959) , Iversen and Van Meter
(1964), and others have described infections of
body muscles and gonads of shrimps from the
Gulf of Mexico and European waters, caused
by a number of representatives of the genera
Thelohania and Nose7na.

Other protozoan diseases of crustaceans in-
clude those caused by ciliates, an ameba, and
gregarines. A ciliate, Anophrys sarcophaga,
causes a fatal disease in shore crabs, Carcinus
maenas, of Europe. The disease, and host re-
sponses to infection, will be considered in detail
in a later section. Other parasitic ciliates occur
in the hemolymph of Crustacea. Paradinium sp.
and Syndinium sp. occur in calanoid copepods.
Syndinium causes gonad destruction, while Par-
adinium colors the host a deep red (Gordon,
1966) . Hematodinium sp. has also been reported
by Gordon in Carcinus. A suctorian, Ephelota
gemmipara, can seriously reduce production of
lobster larvae (Dannevig, 1928, 1939). An
ameboid parasite, Paramoeba perniciosa, causes
a fatal disease (called "gray crab disease") in
blue crabs from the Atlantic coast of the United
States (Sprague and Beckett, 1966, 1968;
Sprague, Beckett, and Sawyer, 1969; Sawyer,
1969). Hemolymph of infected crabs becomes
cloudy and often incoagulable; in some individu-
als most of the cells in the hemolymph are amebae
(Sawyer, Cox, and Higginbottom, 1970). A
great number of gregarines occur in Crustacea
of all kinds, but their pathogenicity seems slight,
except for some destruction of the digestive
epithelium resulting from heavy infections (Ball.
1938; Theodorides, 1961, 1962; Tuzet and
Ormieres, 1961; Kruse, 1959a, 1959b).

Helminth diseases of crustaceans seem less
abundant and less severe in their effects than
those of microbial etiology. Trematode metacer*
cariae encyst in muscles and hepatopancreas of

459

FISHERY BLLLETIM: VOL. 69. NO. 3

crabs, and larval cestodes, acanthocephalans,
nematodes, and leeches occasionally have been
reported from crabs, shrimps, and lobsters
(Sindermann, 1970).

Crustaceans are frequently parasitized by
other crustaceans — sometimes with serious ef-
fects on the host. Rhizocephalan barnacles are
endoparasites of crabs, causing gonad degener-
ation and other morphological changes. Epi-
caridean isopods may produce similar changes in
crabs and shrimps. Copepods sometimes para-
sitize crab eggs, as well as the gills of lobsters
(Sindermann, 1970).

INTERNAL DEFENSE SYSTEMS

Studies of crustacean internal defenses pub-
lished during the last decade have augmented
earlier studies and have provided additional data
to support generalizations and principles ali'eady
enunciated, but none has yet provided the factual
basis for new or different concejits. Because
additional precision in terminology is now avail-
able, it is possible to consider the internal defense
systems of Crustacea under the following head-
ings: cellular (phagoc.\i:ic), bactericidal, lytic,
agglutinating, precipitating, phage clearance,
antitoxic, and others. It should be obvious that
these systems are not mutually exclusive and
may often interact or even share components
to protect the individual animal from invasion
by potential pathogens. Largely for ease of de-
scription, the systems will be considered con-
secutively, even though many may act either
in concert or simultaneously.

PHAGOCYTOSIS AND OTHER
CELLULAR DEFENSES

The earliest study of lihagoc.vtosis in Crustacea
concerned infections of Daphnia by the fungus
Monospora hicuspidata (Metchnikoff, 1884).
The fungus spores in the haemocoel were i)hago-
cytized and digested; the rapidity and vigor
with which phagocytosis occurred determined
the outcome of the infection. If some spores
escaped phagocytosis, germinated, and formed
conidia, the infection became generalized and the

host died in a few da.vs. If all the fungus spores
were phagoc>i:ized and destroyed, the infection
was arrested. Thus the speed and effectiveness
of phagocj-tic action in some individuals, possibly
mediated by humoral factors, determined sur-
vival. Absence of phagocytosis inevitably led
to death.

Hemocytes of Crustacea were investigated by
Cattaneo (1888b), Cuenot (189r5, 1897. 1905),
and Bruntz (1907). Cattaneo described the
amebocv-tes of Carcinus maenas; Cuenot re-
ported blood forming tissues — nodules of lymph-
oid cells in the blood sinuses — in decapods and
described "jjhagocytic organs" in the hepato-
pancreas of decapods and amphipods; and
Bruntz published an extensive paper on the
hemocj-tes of many of the crustacean groups,
distinguishing granular and hyaline hemocytes.
Bruntz also described a "i^hagocytic organ" in
gammarids; his 1907 paper reviewed an exten-
sive series of his own studies (15 reports) pub-
lished during the jjeriod 1903-1907 by the Societe
Biologique de Paris. Other early studies of crus-
tacean hemocytes include those of Hardy (1892) ,
Tait (1918a, 1918b), and Tait and Gunn (1918).

Following the classical early studies of Metch-
nikoff, Cuenot, Bruntz, and others, which elu-
cidated the critical role of phagocytes in the in-
ternal defenses against microorganisms, phago-
cytic cells have received greatest attention from
vertebrate immunologists. General principles
that have emerged from the more recent studies
of phagoc.\i;osis in vertebrates undoubtedly apply
as well to invertebrates. Among the papers that
have contributed to understanding of phagoc.v-
tosis are those of Wright and Douglas (1903),
Wood, Smith, and Watson (1946), Wood (1953),
Robineaux and Frederic (1955), Suter (1956),
Rowley (1960), Rogers (1960). Evans and
Karnovsky (1961), and Spector and Willoughby
( 1963) . Reviews of phagocj-tosis have been pub-
lished by Hirsch (1965) and Aarum (1967).

The mechanism of intracellular degradation
of phagocjlized microorganisms has been de-
scribed in general terms for the vertebrates
(Figure 2). Lysosomes — graiuiles in the cyto-
plasm of phagocytes — contain antibacterial sub-
stances and hydrolytic enzymes (Cohn, Hirsch,
and Wiener, 1963). The lysosome membrane

460

SINDERMANN; INTERNAL DEFENSES OF CRUSTACEA

fuses with the vacuolar membrane within the
phagocyte, releasing antimicrobial components
into the vacuole (Robineaux and Frederic, 1955;
Hirsch, 1965; Aarum, 1967). Evidence for
comparable intracellular events in invertebrates
is sparse, but Janoff and Hawrylko (1964) re-
ported lysosomal enzymes in clams and starfish,
and Eble (1966) found hydrolytic enzymes in
oyster phagocytes.

Invading microorganisms are subjected to
antimocrobial factors both inside and outside the
jihagocytes. Substances of i)resumed cellular
origin, such as lysozynie, occur in the phagocytes
and the plasma. A great array of such antimi-
crobial factors was identified in vertebrates
(Skarnes and Watson, 1957; Elberg, 1960;
Hirsch and Cohn, 1960; Landy, 1960; Coombs,
Coombs, and Ingram, 1961; Mackaness, 1962;
Miles, 1962), and some counterparts were rec-
ognized in invertebrates. McDade and Tripp
(1967). for e.xample. reported lysozymes in oys-
ter hemolymph.

In the vertebrates, specific and nonspecific
serum proteins increase the speed and effective-
ness of phagocytosis — the opsonizing efl^'ect
(Wright and Douglas, 1903; Suter, 1956; Row-

Figure 2. — Role of cell membrane and lysosome break-
down in phagocytosis. 1-4; phagocytosis; 5-7: lysosome
activities. (Redrawn from Hirsch, 1965.)

ley, 1960) . Sensitization of bacteria with serum
factors is not always a necessary prelude to
phagocytosis, however, as was pointed out by
Wood, Smith, and Watson (1916) and Wood
(1953). In the absence of other host responses,
early phagocyte activity may be important in
IH'eventing infection.

Phagocytosis, then, constitutes the keystone
to resistance. As Aarum (1967) mentioned,
". . . the organism's ability to opjjose infection
in-ecisely follows the phagocytes' ability to func-
tion oijtimally. Resistance is lowered by a low-
ering of phagocytic activity." Phagocytosis can
occur at the site of a lesion, in the filtering tissues
and organs of the circulatory system, and (to a
lesser extent) in the body fluid itself. Groups
of fixed phagocytic cells are present in many
crustaceans, most commonly in the sinuses and
lacunae of the gills and at the bases of the legs.

Phagocytes agglutinate, aggregate, and co-
operate in defense — forming nodules (the "nod-
ules leucocytaires" of Cuenot, 1898), which are
also known in annelids, mollusks, echinoderms,
and other invertebrates. In a number of ani-
mals the nodules are bi'own, due to presence of
large numbers of brown granules in the phago-
cytes, which may be excretion products or de-
composition ]5roducts. In Gammaruti, the phago-
cytes composing the nodules secrete a clear
yellowish chitinoid substance around the para-
sites. This secretion gradually becomes dark
brown. The nodules ajipear as conspicuous
black spots in infected individuals (Pixell-Good-
rich, 1928) and are found frequently in gills and
appendages. It should be clearly understood,
however, that there are few detailed modern
studies of phagocytosis in crustaceans or other
invertebrates. Data from in vitro studies are
imrticularly scarce, so there should be no impli-
cation that the kinetics, energetics, or other as-
liects of i:>hagocytosis are fully understood.

Hemocytes of crustaceans and other inverte-
brates also act in other ways to protect the in-
dividual from overwhelming microbial invasion.
Hemocytosis and hemocytic infiltration have
been described in a number of invertebrate
groups. Manifestations in invertebrates and
vei'tebrates involve proliferation of hemocytes,
changes in permeability of blood vessels, leakage

461

FISHERY BULLETIN: VOL, 69, NO. 3

of blood fluids into tissues, adherence of hemo-
cytes to blood vessel walls, and migration of
hemocytes into tissues around areas of injury
or parasitic invasion.

The involvement of hemocytes in coagulation
or clot formation is a complex one, inasmuch as
either cellular or extracellular clots may be
formed. Intravascular cellular clots adhere to
walls of blood vessels and spaces, producing
stasis, and once they are formed, persist for
some time. Extracellular clots, resulting from
release of constituents of hemocytes, can inhibit
microbial motion and thus render microorgan-
isms more vulnerable to phagocytosis. Since
Fredricq (1879) first pointed out that in Crus-
tacea coagulation of hemol\Tnph involves cell
agglutination as well as plasma coagulation,
others have demonstrated similar characteristics
in a number of invertebrate groups. The release
of a component from hemocytes and the role of
this component in initiating coagulation of plas-
ma were reported by a number of authors be-
ginning with Halliburton (1885). Lowit (1889)
observed the rapid disruption of hemocytes and
the rapid clotting characteristic of most Crus-
tacea and concluded that a causal relation ex-
isted. Hardy (1892), Tait and Gunn (1918),
Tyler and Scheer (1945), and George and Nich-
ols (1948) all provided data which supported
the conclusion that a component from certain
hemocytes acts with fibrinogen of plasma to form
fibrin clots.

Bang (1967c, 1968) demon.strated that in the
hermit crab, Eupaynriis lovgicarpus. clots
formed in at least two stages following injui'y —
first a clumping and stickiness of hemocytes
without change in shape or loss of granulation,
then retraction of the clot and the development
of a network of fibrous cell projections contain-
ing microtubules.

The abundant and elaborate literature on he-
molymph coagulation in Crustacea was admir-
ably summarized and evaluated by Florkin
(1960) . As he pointed out, coagulation has been
considered by some authors to occur in two dis-
tinct phases— cellular coagulation and then jilas-
ma gelation— while other workers view coagula-
tion as a continuous ])rocess in which i)lasma gel-
ation begins around hemocvtes. It was Florkin's

conclusion that plasmatic coagulation was a one-
step process in which fibrinogen of the plasma
was acted upon by a coagulin released by the he-
moc\'tes. It seems equally possible, however, that
more than one type of coagulable protein exists
and that the categories of clots may be complex
rather than simple. Florkin also reviewed the
role of cellular clots in wound repair, emphasiz-
ing the im]5ortance of secretion of a chitin film
over the wound area by underlying coagulated
phagocytes.

Encapsulation is also a common form of cellu-
lar internal protection in invertebrates. Invading
organisms, often relatively large, are surrounded
by phagocytes and fibrocytes. The onset of
encapsulation may be rapid, and the cellular
aggregates may be resolved only very slowly.

In summary, the hemocytes function in a num-
ber of ways beyond phagocytosis, although the
latter must be considered the dominant cellular
defense mechanism:

1. Hemocytes are important in cellular infil-
tration of injured or diseased tissue.

2. They are important in clotting — either as
participants in cellular clots, or by release of se-
cretions or injury products which combine with
plasma components to form extracellular clots.

.3. The hemocytes are of primarj' importance
to encapsulation.

A great variety of crustacean hemocytes have
been described during the past several decades.
Animals studied included crayfishes (George and
Nichols, 1948; Toney, 1958; Wood and Visentin,
1967), blue crabs (George and Nichols, 1948;
Toney, 1958), lobsters (Toney, 1958; Hearing
and Vernick, 1967) , and brine shrimp (Lochhead
and Lochhead, 1941). Except for size differ-
ences, the principal distinction seemed to be pres-
ence or absence of granules in the cytoplasm.
The hyaline hemocytes are usually smaller than
the granular, and some of the hyaline cells
probably develop into the granular types, since
the intergrades have been noted (Cuenot, 1895).
As was aptly pointed out by Rabin (per-sonal
communication), "The developmental relation-
ships of one form of hemocyte to another which
have been made amount to little more than edu-

462

SINDERMANN: INTERNAL DEFENSES OF CRUSTACEA

cated guesses, since they have been based hirsely
on static images which may not even represent
the true cell pictures as they occur in riro." Both
types of cells (hyaline and granular) probably
have physiological subtypes, as suggested by the
work of Fisher-Piette (1931) in which explants
of lobster hemopoetic tissues resulted in multi-
plication of two types of hyaline cells— adhesive
ameboid and non-adhesive non-ameboid. Inclu-
sions of granular cells, in addition to their de-
fensive function mentioned earlier, may also pro-
vide nutrient material— as suggested by release
of this material into the hemolymph during ovar-
ian development (Lochhead and Lochhead,
1941). Hyaline hemocytes may also be trans-
formed into connective tissue or endothelial cells
of blood vessels (Danini, 1925, 1927; Debaisieux,
1952a, 1952b; Demal, 1953). Hemocyte physi-
ology and biochemistry are areas where addi-
tional studies are needed, but the extreme fra-
gility of certain cells once they are removed from
the normal animal has undoubtedly been a major
deterrent.

Phagocytic activity has been ascribed in vary-
ing degrees to most recognized categories of
hemocytes (Haeckel, 1862; Hardy, 1892; Cuenot,
1895; Bruntz, 1905, 1907; Kollman, 1908; Tait
and Gunn, 1918; George and Nichols, 1948;
Toney, 1958; Rabin, 1970b).

In recapitulation, the phagocytes of vertebrate
and invertebrate animals have been investigated
widely since the late 19th century, and the blood
cells of Crustacea have received at least propor-
tionate study. Cellular defenses of Crustacea
and other invertebrates are varied but center on
the phagocyte and its activities. Important also
are the humoral defenses, which will be consid-
ered in the following sections. Before proceed-
ing to considerations of other than cellular de-
fenses, however, it seems relevant to include an
often overlooked perimeter of defense suggested
by Miles (1962). Early suppression of microbial
numbers may be due to microbicidal activity of
the tissue cells themselves, either innate or in-
duced, or to soluble antimicrobial substances in
the intercellular fluid of the integument. As
Miles pointed out, such pre-inflammatory cellu-
lar defenses in no way diminish the importance
of phagocytes and humoral factors, but only pro-

vide an added perimeter of defense. Antimi-
crobial capacities of tissues as a whole, and of
nonphagocytic cells in particular, may be a main-
stay of nonspecific resistance — in both primary
invasion and the determination of subsequent
courses of infection. Tissue defenses of this
nature in the invertebrates may be of great sig-
nificance.

HUMORAL DEFENSE SYSTEMS

Early studies of humoral factors in Crustacea
produced significant, but at times ambiguous,
results. Noguchi (1903) found that sera of
lobsters and horseshoe crabs possessed natural
agglutinins against various vertebrate eiythro-
cytes. After repeated injections, he was able to
demonstrate an induced hemolysin in the horse-
shoe crab but not in the lobster. Fredericq
(1910) . using a variety of antigens, was unable
to demonstrate precipitins in a number of dec-
apods (Homanis vulgaris, Palinurus mdgaris,
' Carcinus maenas, Portunus puher, Cancer pa-
gurus, and Astacus fluviatilis) .

The early literature on humoral mechanisms
of internal defense in invertebrates, and espe-
cially the crustaceans, was clearly dominated by
Cantacuzene and his students. Cantacuzene, in
a period covering almost 3 decades beginning in
1912, examined the broad picture of humoral de-
fences of a large number of marine invertebrates.
His work with Crustacea will be summarized
in the next few pages as background for a con-
sideration of subsequent studies.

Cantacuzene (1912a) reported (in a paper
consisting essentially of a series of statements
but little supporting data) the presence of natur-
al agglutinins, lysins, and precipitins in serum
of the hermit crab, Ervpagurus prideaiixii. He-
molysins for sheep and rabbit erythrocytes oc-
curred in crab serum to a maximum titer of 250
and were destroyed by heat at 55° C. Aggluti-
nins for rabbit erythrocj-tes persisted in dilutions
beyond those at which hemolysis disappeared.
Agglutinins for bacteria (Escherichia coli and
Vibrio cholerae) were also present, as were weak
precipitins against horse and rabbit sera. Can-
tacuzene also stated that comparable agglutinins,
lysins, and precipitins were not present in Pagu-

463

FISHERY BULLETIN: VOL. 69, NO. 3

rus striatum, which is closely related to Eiijxig-
unis prideauxii.

Cantacuzene (19231)), summarizing- a decade
of study of humoral defenses in invertebrates,
found that the serum of the spider crab, Main
squlnado, possessed natural agglutinins for
mammalian red blood cells, with great individual
variation from crab to crab. He observed, rather
significantly, that agglutinins weakened or dis-
appeared completely in crabs held in captivity
for long periods. He noted, on injection of eryth-
rocytes, that agglutinins disappeared com-
pletely during the first days after inoculation
and did not return to their original titer for
several weeks after the last dose. Cantacuzene
also reported that rare individuals of Maia. — in-
variably moulting females — possessed a lysin for
mammalian red blood cells. Maia serum also
possessed a strong lytic factor, but no aggluti-
nins, against cholera vibrios.

Cantacuzene inoculated Maia with coelomic
fluid of Sipimculus midus (4 to 5 injections at
intervals of 3 to 5 days) and found that the crabs
produced first agglutinins and then lysins against
the various injected sipunculid coelomic cells,
including ova. The nature, intensity, and dura-
tion of response varied greatly among indivi-
duals. The lytic ability seemed more pronounced
in females than in males, and more so in fe-
males approaching sexual maturity. Hemolysins
against mammalian erythrocytes were also pro-
duced.

When he comi)ared the lytic ability of Maia
serum after injection with sipunculid fluid and
mammalian erythrocytes, Cantacuzene found
that response was more rapid and stronger with
the former, and he concluded — on the basis of
these and other studies — that mammalian red
cells were only mediocre antigens for marine in-
vertebrates. He attributed this weak antige-
nicity to coating of the injected mammalian
erythrocytes in Maia and other invertebrates
with a serum factor that interfered with sub-
sequent reactions. Cantacuzene a])tly referred
to this as "mummification" of the red cells by
invertebrate body fluids.

Concerning acquired immunity to bacterial
infections in Crustacea, Cantacuzene (1923b)
found that the crab Maia squinado, when inoc-

ulated with killed Vibrio choleme or small doses
of live vibrio, was able — 12 days after the fifth
injection — to survive the challenge with 20 times
the dose of vibrio which had proved fatal to un-
inoculated control crabs.

Cantacuzene also reported on studies of the
responses of Maia squinado to injections of gram-
positive bacteria isolated from the crab's diges-
tive tract. Inoculation was followed by reduc-
tion in numbers of amebocytes and, within 24 hr,
by disappearance of most of the bacteria from
the hemolymph. The bacteria were immobilized
in the various i^hagocytic tissues, particularly
in the branchial lacunae — at first they adhered
to the cell surfaces, then amassed into small
granules, and were finally engulfed by fixed and
mobile phagocytes. The process of digestion of
bacteria was slow, and still incomplete after 7
weeks. Clotting ability of the hemolymph de-
creased immediately after inoculation but re-
turned to normal in 8 days. Xo agglutinins for
the bacteria could be demonstrated in vitro, but
the natural agglutinins for mammalian red blood
cells (discussed earlier) disappeared. In vitro
studies disclosed that the hemagglutinin coated
the bacteria but did not cause their agglutination.
The adherence in vivo of the bacteria to fixed
phagocytic cells undoubtedly was enhanced by
the sensitization. Some evidence for this was
gained by adding macerated hypodermal or peri-
cardial cells to a mixture of bacteria and crab
serum in vitro. The cell fragments acted as
centers for bacterial agglutination and immobili-
zation, but the agglutinating ability was not
conferred on the serum by the addition of cell
fragments.

A diflferent sequence of events was described
for those crabs (Maia) in which the experimental
infections progressed to death. Early immobili-
zation of bacteria in lacunar cells was followed,
in 8 to 15 days, by the appearance of encapsu-
lated forms, invulnerable to destruction by
phagocytes. The encaj^sulated bacteria multi-
plied, phagocyte numbers were reduced, and the
clotting ability of the hemolymph diminished. By
10 to 20 days after inoculation, the hemoljTnph
became incoagulable, the natural agglutinin for
red cells disappeared, the connective tissue be-
came gelatinous, and the animal died.

464

SINDERMANX: INTERNAL DEFENSES OF CRUSTACEA

Caiitacuzene (1923b) also examined the in-
ternal defenses of the hermit crab, Eiii)a(/nnis
prideauxii. which he had reiiorted earlier to
possess strong hemolysins and strong' antibac-
terial agglutinins. Injected gram-negative bacilli
were entrapped and immobilized on the cell sur-
faces of the branchial lacunae, and then phago-
cytized, as was the case with Maia described
]ireviously.

Cantacuzene (1923b) also reported that the
sera of crabs, Carcinus maenas, infected by the
rhizocephalan SacrnUna, contained a factor ab-
sent from normal crabs. Using a standard com-
plement fixation test, with extract of the rhizo-
cephalan as antigen and with ci-ab serum,
Cantacuzene (1925b) was able to demonstrate
an antibody-like response in parasitized crabs.
Sheep cells were lysed in tubes with normal crab
serum but not in those containing parasitized
crab serum. Using a fine suspension of Sarcu-
lina. Cantacuzene found precipitating and agglu-
tinating activity in the serum of parasitized
crabs. The activity was not consistent, however,
in that some sacculinized crabs lacked it. In a
concurrent study. Levy (1923) found that macer-
ated sacculinids wei-e toxic when injected into
crabs, but that no antitoxic activity could be dem-
onstrated in ]iarasitized crabs. Both groups,
normal and parasitized, died at about the same
rate.

In an earlier study Cantacuzene (1913) re-
ported that inoculation of the sacculinid parasite
with gram-negative bacteria resulted in septi-
cemia and death of the parasite within 1 week,
and infection of the crab host by 10 days after
inoculation. At about 5 days after inoculation,
the crab hemolymph became incoagulable, and
agglutinins appeared against the bacteria inoc-
ulated into the parasite. The antibacterial
agglutinins were not present in sacculinized un-
inoculated control crabs.

Appreciable evidence for some degree of spe-
cificity of the natui'al agglutinins of Crustacea
was accumulated by Cantacuzene. An agglutinin
in Maia against mammalian red cells could be
absorbed from crab serum by certain gram-jjos-
itive bacteria but did not agglutinate them, nor
did it agglutinate cholera vibrios. It did, how-
ever, strongly agglutinate typhoid bacilli.

Agglutinins against vei-tebrate erythrocytes and
certain bacteria were found in sera of Homarus
vulgaris, Eupagurus prideauxii, and E. bernhar-
dus, but the same antigens were not agglutinated
by sera of Cancer pagurus, Carcinus maenas,
Portunus puber, or Galathea punctata. The
serum of Eupagurus prideauxii agglutinated
mammalian red blood cells and amebocytes of
Maia and Buccinum, but did not agglutinate
the coelomic cells of sipunculids or ascidians.
And so Cantacuzene set the scene, by the
early 1930's, for the continuation of broad and
elaborate studies of humoral internal defenses
of marine invertebrates — particularly the Crus-
tacea— but the stage, with only a few notable ex-
ceptions, remained curiously empty and dark
until the mid-19.50's. Although research during
the last decade emphasized species other than
those studied by Cantacuzene (except for the
work of F. Bang) , it reinforced many of Can-
tacuzene's findings: that natural agglutinins
and lysins, with some specificity, occur in Crus-
tacea and other invertebrates, and that respon-
ses to foreign antigens can be induced in selected
invertebrate.? — responses which are only par-
tially specific. The increased precision and
quantitation of tests, and the careful attention
to controls, have improved the quality of the
newer data, but have neither provided new con-
cepts nor modified the genei-al conclusions of
Cantacuzene. The more recent literature on
humoral defenses of Crustacea will be summar-
ized by general categories in the following
sections.

Bactericidal Systems

Natural bactericidins have been reported from
a number of marine invertebrates (Bang,
1967b). Recently, increase in titers of bacteri-
cidal activity after inoculation with Formalin-
killed bacteria was noted in West Indian spiny
lobsters, Panidirus argus, and American lob-
sters, Homarus americanus (Evans et al, 1968;
Acton, Weinheimer, and Evans, 1969). A bac-
tericidal assay system described by Schwab and
Reeves (1966) was used to quantitate the degree
of response. In experiments with American
lobsters held in seawater at 5° C, the peak of

465

FISHERY BULLETIN: VOL. 69. NO. 3

bactericidal response against o;ram-negative ba-
cilli was reached within 48 hr after inoculation,
and high titers persisted throughout the obser-
vation period (11 days). In spiny lobsters,
presumably maintained at significantly higher
environmental temperatures at Bimini, the
Bahamas (reported as 26° -28° C in a later pa-
per) , the primary bactericidal response to intra-
cardial injection of living or killed suspensions of
the same gram-negative bacilli (originally iso-
lated from the digestive tract of spiny lobsters)
reached a peak at about 36 to 48 hr after in-
jection, then declined slowly for the following 2
weeks. Partial lack of specificity of the bac-
tericidin was indicated by its appearance follow-
ing injection of gram-positive bacilli and by its
activity against Salmonella typhosa and Esch-
erichia coli, as well as against the unidentified
gram-negative bacillus used as the homologous
test organism. The bactericidin was not active,
however, against Pseudomonas aeruginosa or
against three species of gram-])ositive bacteria.

A subsequent study (Weinheimer, Acton,
Sawyer, and Evans, 1969) of the specificity of
the spiny lobster bactericidin further indicated
that the response was i^artially nonspecific. Low
titers of the bactericidin against gram-negative
bacilli could be demonstrated after injections of
Formalin-killed type 2 pneumococci and bovine
serum albumin. Formalin produced a pro-
nounced adjuvant efl:ect.

Secondary responses — those following rein-
jection of the same antigen after a lapse of time
— of spiny lobsters to killed suspensions of gram-
negative bacilli were also examined by Evans,
Gushing, Sawyer, Weinheimer, Acton, and Mc-
Neely (1969). Titers of bactericidin were
slightly but significantly higher after reinocula-
tion than after primary inoculation, and the rate
of secondary response (the number of hours to
I'each peak titer) seemed somewhat accelerated
when comi)ared with the primary response. Un-
fortunately, the number of animals tested was
small. It seems important that similar obser-
vations be greatly extended — since, as the au-
thors pointed out, the results were reminiscent
of the specific anamnesis or immunological mem-
ory demonstrable in the immunoglobulin
responses of vertebrates.

The spiny lobster bactericidin was apparently
a large molecule, as suggested by resistance to
dialysis and by Sephadex separations. Inacti-
vation occurred at 65° C and activity was not
restored by addition of unheated normal hemo-
lymph. Activity was not reduced by treatment
with EDTA or carageenin. These results indi-
cate dissimilarity with vertebrate comiilement-
based bactericidal systems, but the authors sug-
gested that the bactericidin may represent a
primordial immunoglobulin.

Noteworthy is that all the American lobsters
and a number of the West Indian sjiiny lobsters
used in the studies by Evans, Weinheimer. Paint-
er, Acton, and Evans (1969) had demonstrable
pre-existing titers of bactericidins against the
gram-negative bacillus used in the experiments.
Possibly the remainder of the sijiny lobsters used
in the studies could have had titers of bacteri-
cidins lower than were demonstrable by the
methods used. Thus inoculation may not have
"induced" the bactericidin but instead may have
merely enhanced or increased the titers. A num-
ber of explanations were offered for the pre-ex-
isting titers of bactericidal activit.v, including
trauma because of handling, and response to pre-
vious bacterial infection. Two relevant obser-
vations are that in many American lobsters, a
rapid increase in bactericidal titer preceded
death, and in studies of spiny lobsters, the bac-
tericidal activity was found to be partially non-
specific, in that activity against other gram-
negative bacteria was enhanced.

The conclusions reached by the research group
that examined the spiny lobster bactericidin
(Weinheimer, Acton, Sawyer, and Evans. 1969)
are in accord with findings for other phyla:
"These data suggest that, although invertebrates
appear capable of antigenic recognition, the mol-
ecules synthesized may have broad specificity
covering a wide range of antigenic determinants.
Further studies will be necessary to ascertain
whether these inducible substances represent
primitive immunoglobulins. In any event, it
would be surprising if they did not have a major
role in defense of the animal against pathogenic
microbes."

An important qualification was pointed out by
Aarum (1967) regarding results obtained by ex-

466

SINDERMANN: INTERNAL DEFENSES OF CRLSTACEA

perimental inoculation of large numbers of bac-
teria. Infectious agents are found in large
numbers in the circulatory system only in septi-
cemia, which occurs only after a growth phase
of a virulent pathogen within the host, often
within fixed or immobilized phagocytic cells.
Rapid increase in pathogen numbers in the cir-
culating body fluid is usually a precursor to death
and indicates a failure of host defenses. Thus
the artificial introduction of large numbers of
microorganisms should not be expected to elicit
normal responses in an animal. It should also
be noted that insusceptibility barriers to infec-
tion, operative in the normal animal, may be by-
passed by experimental inoculation, resulting in
massive infection and death from microorgan-
isms not otherwise known as pathogens. A
further qualification mentioned by Aarum is that
even the simplest experimental manipulation
may change phagoc>i;ic abilities, so that the nor-
mal phagocytic response of an animal to path-
ogens may be far diff"erent from responses elic-
ited experimentally.

nns, multiplies and causes death, was immo-
bilized, agglutinated, and lysed in vitro by serum
of several other crabs — particularly Maia squi-
nado, Eupagurus p7-ideauxii ,andPorhmus puber.
Experimental inoculations of ciliates were
cleared usually within several hours. It is in-
teresting that the parasite, when experimentally
introduced in another member of the Portunidae,
Portiinus depumtor, multiplied and killed the
experimental hosts just as it did in Carchms
maenas. Poisson attributed the reactions of
crabs to the ciliate to expressions of a natural
immunity, eflfected by agglutinating and lytic
activity of the hemolymph.

Other lytic systems of Crustacea have received
passing attention. Cantacuzene (1913) found
that hemolymph of the hermit crab, Eupagunis
prideaKxii, possessed a heat-labile hemolysin, as
well as precipitating and agglutinating activities.
Cantacuzene (1921, 1923b) stated that injection
of the spider crab, Maia sqninado, with sheep
erythrocytes produced hemolysins as well as
agglutinins.

Lytic Systems

A natural hemolysin for sheep erj-throcj'tes
in the hemolymph of West Indian spiny lobsters
was reported by Weinheimer, Evans, Stroud,
Acton, and Painter (1969). Low temperatures
(0° and 4° C) inhibited lysis, which was best
demonstrated at 25° and 37° C. Heating the
lobster hemolymph to 52° C destroyed lytic ac-
tivity. The hemolysin could be adsorbed on red
cells or cell stroma at low temperatures. Red
cells with the adsorbed lysin were lysed when
the temperature was raised to 37° C, which in-
dicated a possible enzymatic type of activity of
this hemolytic system. The authors suggested
a multiple step system, analogous to mammalian
hemoljlic systems, consisting of a single protein
species which is first adsorbed on the surface
of the sheep erythrocyte, and then — in one or
more steps — lyses the cell.

A detailed study of the presence or absence
of natui-al immunity to invasion of the hemo-
lymph of crabs by a parasitic ciliate, Anophrys
sarcophaga, was reported by Poisson (1930).
The ciliate, which in shore crabs, Cavciniis viae-

Agglutinating Systems

Natural hemagglutinins of the Australian
freshwater crayfish, Parachaeraps bwarinatus,
were examined by McKay, Jenkins, and Rowley
(1969) . Absorptions of hemolymph by erythro-
cytes of four mammalian and one avian species
disclosed specificity, in that absorption by cells
of one species still left agglutinins for cells of
other species. The crayfish hemagglutinins were
nondialysable and were inactivated at 57° C.
In vitro studies with crayfish phagocytes and
mouse erythrocytes disclosed that the crayfish
hemagglutinins greatly enhanced the adhesion
of the erythrocytes to the phagocytes — a specific
opsonic effect. A similar effect was observed in
vivo, apparently as a prelude to phagocytosis.

The recent studies support earlier reports of
specific hemagglutinins in a number of inverte-
brate phyla (Tyler and Metz, 1945; Tyler, 1946;
Sindermann and Mairs, 1959; Gushing, Cala-
price, and Trump, 1963; Tripp, 1966) with spe-
cificities somewhat comparable to those of verte-
brate natural isohemagglutinins and with some
biological propei'ties (such as enhancement of

467

FISHERY BULLETIN; \'0L. 69. NO. 3

adhesion and phafrocytosis of erythrocytes by
phagocytes) simihu- to those of vertebrate anti-
bodies.

A study of natural agghitinins in the serum of
California spiny lobsters, PanuUrus interruptiis,
for blood and sperm cells of 54 species (repre-
senting 7 phyla) was published in 1945 by Tyler
and Metz, and is still cited as one of the most
comprehensive examinations of its kind for a
marine animal. Agglutination was not found in
37 other species tested. Titers for positive re-
actions ranged from 8 to 256. The most inter-
esting phase of the study was an extensive series
of absorptions of spiny lobster serum by cells
of many of the species tested. In each case, ab-
sorption of serum with cells of any single species
removed agglutinins for all the species tested
that belonged to the same group (Class) but left
agglutinins for the cells of all other gi-oups
tested. Tyler and Metz concluded, on the basis
of absorptions, that at least 10 class-specific
agglutinins were present in the serum of the
spiny lobster. A few cross-reactions occurred,
and some reduction in titers resulted from ab-
sorptions with cells of other species, which sug-
gested the presence of a number of reacting sites
on the cells.

Bang (1967b) examined the resjionses of the
spider crab, Maia sqiiinado, to injections of
Anophrys, a large ciliate pathogenic for shore
crabs, Carchms maenas. as part of a laudable
attempt to repeat with modern methods some of
the early French studies of invertebrate de-
fenses. Sera of some spider crabs strongly
agglutinated the ciliates, but that of others did
not. Agglutination resulted from formation of
a mucoid substance around the tail cilia. Crabs
that lacked the agglutinin died from overwhelm-
ing infections of the hemolymph, whereas those
with the agglutinin survived (Bang, 1962).
When present, the agglutinin was apparently
fairly constant, except that in some crabs it
was lost spontaneously but temiiorarily at time
of molting. Poisson (1930) had noted earlier
that the hemolymph of Maia lysed the ciliates
and that the hemolymph of the hermit crab,
Eupagunis prideauxii, agglutinated them.

An agglutinin in the hemol.vmph of the hermit
crab, Pagitvistes iilreyi, for human type 0 cells,

and to a lesser e.xtent for types A and B, was
reported by Cushing (1967). A number of in-
dividuals lacker the hemagglutinin, and some of
these possessed a serum factor which inhibited
the action in vitro of the positive sera. The
analogy to specific soluble substances found in
sera of certain vertebrates was pointed out by
Cushing, with the suggestion that further studies
of this kind with other invertebrates might prove
instructive. Cohen (1968) found agglutinins
for human and other vertebrate er.vthroc.vtes in
sera from coconut crabs, Birgus latro. Young
crabs lacked the agglutinins.

The serum of the American lobster contains
strong and specific natural agglutinins for an
antigen present on the red blood cells of sea
herring, Clupea harengus (Sindermann and
Mairs, 1959). Detection of blood groups in this
fish was aided by the use of the hemagglutinin —
individual herring either had the antigen or
lacked it. Titers reached as high as 256, and
reactions paralleled those obtained with absorbed
rabbit antisera and plant lectins (Sindermann,
1963). Erythrocytes of other clupeoid fishes
tested were also strongly agglutinated by lobster
sera (Sindermann, 1962).

Precipitating Systems

Production of i^recipitins by invertebrates has
been reported only rarely. Osawa and Yabuubhi
(1963), in a very brief paper, found that the
"Homard americain, Cambarus clarkii" [prob-
ably Homaius america7uis] did not produce
agglutinins or lysins when injected with red
blood cells but did produce weak precipitins (de-
tectible by Immunoelectrophoresis) after in-
jection with serum from rabbits and goats. No
information was given about dosage, injection
schedules, time for response, or titers.

Stewart and Foley (1969) suggested that a
"precipitin-like principle already present in the
hemolymi^h" of the American lobster might be
important in removal of foreign protein. Fluo-
rescein-labelled bovine serum albumin (BSA)
and lobster serum proteins were injected into lob-
sters held at 5° C. and the fluorescence level
checked periodically for 6 days. With lobster
serum proteins, an initial decline in fluorescence

468

SINDERMANN: INTERNAL DEFENSES OF CRUSTACEA

within 2 hr after injection was followed by a
l)lateau that remained constant for the duration
of the experiment; with labelled BSA, however,
the rate of clearance was concentration depen-
dent, but the foreign i)rotein declined to very low
levels by 3 days after injection. Fluorescent
material was apparently excreted in proportion
to its disaiipearance from lobster hemolymjih.
Pinocytosis by phag-ocytes was not demonstrated,
but tiny n-ranular fluorescent accretions were
observed in the hemolymph of lobsters injected
with labelled BSA, beginning- about 8 hr after in-
jection. In vitro studies, in which a standard
ring test with labelled or unlabelled BSA and
lobster serum was used, disclosed a clearly dis-
cernil)le ring after 16 hr at room temjierature,
and a precipitate at the bottom of the tulie after
36 hr. Precipitin titers of individual lobster
sera ranged from 2 to 16 and were independent
of the total protein concentration of the lobster
serum. Dialysis of lobster serum did not change
the titers, but preci]ntin activity was destroyed
by heating above 50° C.

A number of interesting implications in the
study were pointed out by Stewart and Foley.
The clearance mechanism seemed able to dis-
tinguish between foreign and native in-oteins,
and the capacity for clearance seemed high, as
indicated by accelerated clearance of larger doses
of BSA. Attempts to increase the levels of pre-
cipitin by previous injection of lobsters with
BSA did not succeed, and in fact resulted in de-
creased jn-ecipitin levels in some individuals.
The authors suggested that the hemolymph fac-
tor responsible for clearance of foreign protein
may be maintained normally at low levels and
may be supplemented by further secretions when
requii'ed. They also suggested that the precipitin
principle in the hemolymph may be the first of
several steps or possibly the primary removal
factor and that digestion and excretion may take
place elsewhere — i)robal)ly in the hepatopan-
creas.

The results of the studies of Stewart and Foley
are in agreement with those of Teague and Friou
(1964), who observed that injected foreign pro-
tein was rapidly removed fi-om the hemolymph
of the crayfish Camharus virilis. Previous in-
jection of the protein did not increase the clear-

ance rate. Teague and Friou did not observe
precipitin activity against injected bovine and
human serum albumins but concluded that clear-
ance resulted from nonspecific degradation of the
foreign protein.

Other evidence of clearance of injected pro-
teins but failure to induce heightened responsive-
ness in Crustacea was reported by Campbell and
(larvey ( 1961) . They mentioned that "It is also
of interest that we have made many attempts
to induce antibody formation in invertebrates,
e.g., lobsters. We have been unsuccessful so far,
but in every instance the antigens remained un-
digested and unchanged in the circulation and
tissues for many months." Although not men-
tioned specifically, the lobsters were probably
California spiny lobsters and the test antigens
probably included BSA, since this w^as the prin-
cipal antigen used in other studies reported in
the same paper.

Phage Clearance

Taylor, Taylor, and Collard (1964) and Nel-
strup, Taylor, and Collard (1968) presented
some evidence (from two crabs) of an increase
in the rate of secondary clearance of injected
Ti bacteriophage in the shore crab, Carcinus
maenus. Clearance was not complete until after
2 weeks at 16° to 18° C, and no neutralizing
antibody to Ti phage was detected in the hemo-
l.\Tn])h. Primary inoculation with Tu phage did
not increase clearance rates for Ti secondary
injections. The small number of animals used
in these experiments makes the conclusions
highly tentative. The authors suggested the ex-
istence of a "phylogenetically more primitive
type of immune response than the production of
humoral antibody," but did not state clearly what
the response was — except possibly that it was
"an apparently purely cellular secondary re-
sponse."

Studies of phage clearance by Cushing and
McNeely (reported in Cushing, 1967) led to neg-
ative conclusions. Phage Tj persisted for up
to 168 days in the California spiny lobster and
disappeared at a steady rate, uninfluenced by
the size of the original inoculum. Two species
of crabs tested also failed to clear bacteriophage.

469

FISHERY BULLETIN: VOL. 69, NO

Other negfative findings for increased rate of
phage clearance following inoculation in cray-
fish were reported by Teague and Friou (1964) .

Antitoxic Activity

Little definitive information is available about
antitoxic activity in invertebrates. As Huff
(1940) pointed out, "Experimental demonstra-
tion of antitoxic action in invertebrates has
failed for the most part because of lack of
susceptibility of invertebrate cells for known
toxins." Probably the best example of antitoxic
phenomena in Crustacea was described by
Cantacuzene (1925a) and Cantacuzene and
Damboviceanu (1934a, 1934b). The hermit
crab, Eupagin-us prideauxii, exhibited resist-
ance to nematocyst toxin of Adamsia palliata.
a commensal coelenterate commonly found on
the shell of the crab. When injected, the toxin
had no effect on E. prideauxii, but it was lethal
to many other Crustacea and to a number of
other invertebrates tested, including the closely
related hermit crab. E. benthardus. Cantacuzene
also found that serum of E. piideauxii could
neutralize the coelenterate toxin when the two
— serum and toxin — were mixed and injected in-
to crab species susceptible to the toxin. The
development of this antitoxic jsrinciple can be
seen as a logical and necessary concomitant of
the very close relationship of crab and anemone,
but the question of whether this is an example
of innate or acquired resistance has not been
resolved.

Another examjile of coelenterate toxin lethal to
crabs was reported by Lane, Coursen, and Hines
(1961) . Biologically active peptides in Pkysalia
nematocyst toxins were tested, using fiddler
crabs, Uca pugilntor, as assay animals.

Except for the work with coelenterate toxins,
evidence of antitoxins in invertebrates is weak.
Stauber (1961) reported almost immediate re-
moval of dij^htheria toxoid from oyster blood,
but Metchnikoff (190.5) and Bengston (1924)
found that tetanus and botulinus toxins remained
in insect body fluids for several weeks without
loss of toxicity. These studies must, of course,
be viewed as most indecisive, since substances
toxic to humans are not necessarily so to inverte-

brates. Reaction on the part of invertebrates
could be identical to i-eaction against any other
introduced foreign material.

Invertebrate responses to gram-negative bac-
terial endotoxins were the subject of a review
by Levin (1967). The most striking activity
of such endotoxins is the pi-oduction, after ex-
l)erimental inoculation, of intravascular clots
and the ensuing death of various crustaceans
and other invertebrates. Antitoxic immunity
has not been demonstrated, but, as Levin stated:
"Endotoxin appears capable of activating com-
plementary defense mechanisms in inverte-
brates, including aggregation of amoebocytes,
coagulation, bacterial immobilization, and jihago-
cytosis. All these may be operative through
one tyi^e of cell — the amoebocyte."

Other Protective Systems

McKay and Jenkin (1969) examined resist-
ance of the Australian freshwater crayfish, Par-
achaeraps hicarinatus, to a pathogenic Pseudo-
monas sp. and concluded that the animal was
capable of an adaptive immune response. Their
findings indicated lower mortality rates (after
bacterial challenge) in animals inoculated with
heat- and alcohol-killed vaccines as well as with
endotoxin. Inoculation with vaccines prepared
from other gram-negative bacteria also increased
the level of resistance to the Pseudomonas in-
fection, but vaccines from gram-positive bacteria
did not — indicating some degree of specificity.
A positive correlation was found between sur-
vival of challenged animals and the number of
exposures to bacterial antigen; after four inoc-
ulations, the LD,-,n of immunized animals was
nearly 100 times that of controls. Temperature
also played a significant role in the onset, degree,
and duration of protection induced by inocula-
tion of animals with killed bacteria. At 26° C,
onset of protection was rapid ( 1 day) , reached
a iieak at 3 days, and almost disappeared by 12
days; at 19° C, onset was slower (2 days),
reached a maximum at 4 days, and persisted for
12 days (the duration of the experiment); at
14° C, no protection was afl!"orded. Inoculation
of gram-negative endotoxin resulted in protec-
tion similar in appearance and duration to that

470

SINDERMANN: INTERNAL DEFENSES OF CRUSTACEA

produced by killed vaccines. Althoug'h the terms
"immunity" and "resistance" were used, tlie pre-
cise nature of the protection afforded by inocu-
lation of vaccines and endotoxin was not de-
scribed by the authors. In vitro experiments
with hemolymphs of control and resistant cray-
fish disclosed no bactericidal or bacteriostatic
effects, and McKay and Jenkin suggested that
the most important effect of imznunization may
have been to increase the metabolic rate of the
phagocytes [thereby stimulating phagocytosis].

Barker and Bang (1966), extending the ear-
lier studies of Cantacuzene (1925b) with the
shore crab, Carcinus maenas, and its rhizoceph-
alan parasite Sacculina carcini, reported that
inoculations of Vibrio sp. caused the hemolymph
of the parasite to become incoagulable within 24
hr. Masses of gelled material containing bac-
teria were seen within body spaces. Septicemia
and death, first of the parasite, and then often
of the crab host, followed soon after.

Insuscejitibility factors seem operative when
certain parasites of invertebrates fail to develop.
Michajlow (1938) and Baer (1944), for in-
stance, found that larval cestodes, Triaenophorus
and Ligula, penetrated the intestinal wall of a
number of copepods, but developed only in cer-
tain species. In others, the larvae died and were
phagocytized. Hedrick (1935) observed similar
differences in survival of larval nematodes.
Leger and Duboscq (1908) reported earlier that
sporogony of the sporozoan Agregata eberthi
(which occurs in the intestinal wall of crabs
of the genus Portunus) took place readily in all
species except P. puber, in which the parasite
was quickly phagocytized after invading the in-
testinal wall.

INTERNAL DEFENSE MECHANISMS

INVOLVED IN GAFFKAEMIA

OF LOBSTERS

The American lobster, Homanis americanus,
has an effective internal defense system, consist-
ing of active phagocytosis as well as agglutin-
ating and bactericidal (or bacteriostatic) activ-
ity, against a number of injected bacteria. The
protective system seems to fail completely only

when challenged by Gaffkya homari — which is
thus far the only bacterial pathogen known to
develop systemic infections in lobsters and to kill
them. Probably the most extensive series of
reports concerned with responses of inverte-
brates to a particular pathogen is that dealing
with the lobster (and other decapods) and the
highly pathogenic gram-positive micrococcus
G. homari. "Gaffkaemia" — the disease caused
by G. homari — is enzootic in both the American
lobster, Homarus americanus, and the European
lobster, H. vulgaris, and has been reported to
cause epizootics in captive populations of both
species (Roskam, 1957; Goggins and Hurst,
1960; Gibson, 1961; Stewart and Rabin, 1970).
Microorganisms with characteristics of G. hom-
ari have been isolated from shrimp {Penaeus
aztecus from the Gulf of Mexico) and from crabs
{Carcinus maenas and Libinia emarginata from
New England and Cancer irroratus from eastern
Canada), but the disease "gaffkaemia" is known
only in lobsters. Early descriptions of the di-
sease and its etiological agent (Hitchner and
Snieszko, 1947; Snieszkoand Taylor, 1947) have
been followed during the past decade by studies
in several laboratories, which used the lobster
and the pathogen as a test system to elucidate
responses to infection and other aspects of the
host-iiarasite relationship. The possible course
of infection in lobsters is summarized in Table 1.
Snieszko and Taylor (1947) first satisfied Koch's
postulates for the pathogen and demonstrated
high mortality following inoculation of cultured
G. homari. Stewart and MacDonald (1962) and
Stewart et al. (1966) found that 40 to 60%
of lobsters they examined from certain locations
on the Canadian east coast were infected.

Studies by Harvey Rabin at Woods Hole and
The Johns Hopkins University (Rabin, 1965;
Rabin and Hughes, 1968) confirmed that lobsters
inoculated with Gaffkya became septicemic with-
in 2 days and died a few days later. Inoculation
of gram-negative endotoxin 10 hr before ex-
posure to the pathogen did not alter the course
of infection. Prior inoculation of heat-killed
Gaffkya cultures (24 hr before challenge) pro-
duced no protection.

In vitro studies with lobster serum as a cul-
ture medium disclosed that Gaffkya growth was

471

FISHERY BULLETIN: VOL. 69, NO. 3

Table 1. — A proposed hypothesis to explain the course
of Gaffkya homari infections in lobsters at 15° C.

Day

Development of gaffkaemia in lobsters

decrease in
bacterial

hemocyte
numbers.

Bacteria gain access to tissues of lobsters as a result of
injury which destroys the integrity of exoskeleton (or pos-
sibly the gut epithelium). Lobster hemocytes phagocytrze
C. homari.

Phogocytized bacteria may multiply within hemocytes. Hemo-
cytes containing engulfed bacteria lodge in capillary ond
lacunar areas (heart, hepatopancreos, gills) of the lobster.
Hemocytes may be disrupted, releasing C. homari in hemo-
lymph. This may result in rapid
numbers and logarithmic increase

Hemolymph stimulates multiplication of released bacteria.
Hemocyte numbers seem to be graduolly reduced by con-
tinued phagocytosis and disruption of phagocytes.

Clotting mechanism (release of coogulin from hemocytes)
is affected— possibly by reduction of hemocyte numbers—
and clotting time is greatly prolonged.
Lobsters die from depletion of nutrient stores and utilization
of this material by Gafjkya. Injured gaffkoemic lobsters
may bleed to death. (The possibility of exotoxin has not
been entirely eliminoted, but there is no present evidence
to suggest its existence.)

stimulated, while growth of a Vibrio (nonpath-
ogenic to lobsters) was usually inhibited. Serum
from lobsters which had been inoculated 24 hr
earlier with killed Gaffkya still stimulated
growth of the pathogen in vitro.

Rabin and Hughes (1968) tested resistance
to Gaffkya in a variety of studies with lobsters
and other marine arthropods. Findings with
spider crabs (Lihinia emargivata) , rock crabs
(Cancer borealis) , and horseshoe crabs (Limulus
pohjphemiis) were that most of the test animals
cleared inoculated G. homari. In vitro studies
with hemoljTnph disclosed either no apparent
effect or only slight inhibition of growth of the
pathogen by sera of spider and horseshoe crabs,
and a slight stimulation of growth by sera of rock
crabs.

The possible role of exotoxin was tested in
lobsters by Rabin and Hughes with inoculation
of filtrates of G. homari cultures. The filtrate
had no effect when it was injected into the ab-
domen, but injection into the major joint of the
chela induced autotomy or abnormal movements
in over 50 "^r of the lobsters treated.

FA'idence of resistance to gaffkaemia was
noted by Rabin and Hughes in a single lobster,
which had been infected naturally before it was
brought to the laboratory. Twelve days after

capture the lobster was free of the pathogen.
The animal was inoculated twice with increas-
ingly larger dosages of G. homari and cleared
the bacteria within 6 days — but died on the 11th
day following the second challenge. The reac-
tions indicated a partial resistance and an ability
in some individuals to recover from gaffkaemia.
It is interesting that serum from this presum-
ably resistant lobster was similar to that of other
lobsters tested in that it did not inhibit growth
of G. homari in vitro.

Rabin and Hughes stated that the presence
of Gaffkya infections did not damage the clotting
mechanism — an observation quite different from
that of Goggins and Hurst (1960), who found
that reduction in amebocytes and a much pro-
longed clotting time were distinctive features
of the disease. Stewart et al (1969) and Stewart
and Rabin (1970) clarified these seemingly dis-
parate observations by rejjorting that "coagulin"
is released to initiate clotting by rujiture of
hemocytes and that the "concentration of plasma
proteins, including fibrinogen, does not appear to
decline significantly in gaffkaemic lobsters." An
earlier report by Rabin and Hughes (1968)
stated that when extract of lobster muscle was
used as a coagulin source, recalcified clotting
times were the same in diseased and normal
animals. When these facts are combined, it can
be concluded that the abnormally and persistently
low hemocyte content of the hemolymph results
in prolonged clotting time and does not indicate
any deficiency in plasma constituents other than
coagulin (Figure 3).

Studies carried on by James Stewart and his
associates at the Halifax (Nova Scotia) Lab-
oratory of the Fisheries Research Board of Can-
ada have extended the work of Rabin and have
provided the greatest number of contributions
to the literature about the effects of Gaffkya
disease on lobsters. In accord with earlier stud-
ies, infections usually were fatal, although rare
individuals infected with Go//A-i/a-like organisms
did survive (Stewart et al., 1966).

Cornick and Stewart (1968a) provided con-
siderable relevant information about the host-
parasite relationships of Gaffkya and lobsters.
Experimental infections by inoculation, in which
dosages as low as approximately 5 bacteria per

472

SINDERMANN: INTERNAL DEFENSES OF CRUSTACEA

40-

500-1

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BACTERIAL NUMBERS

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DATS AITIR INJKTION

Figure 3. — Relations of hemocyte counts, clotting time,
and bacterial numbers to time from experimental ex-
posure of lobsters to Gaffkyn. (Redrawn from figures
in Stewart, Arie, Zwicker, and Dingle (1969) and Stew-
art and Rabin, 19V0.)

lobster at 15° C were used, killed 90 ^^ of the
test animals within 17 days. The absence of
an effective host defense against Gaffkya was
strongly indicated by the fact that the mean
time to death was almost constant, regardless
of dosage (Figure 4). Cornick and Stewart's
studies disclosed additional facts that help to ex-
plain the pathogenicity of the bacterium to lob-
sters: Gaffkya resisted digestion in phagocytes
and multiplied in the hemolymjih; growth of
Gaffkya was stimulated in vitro by serum of
lobsters while growth of several other bacteria
was inhibited; and Gaffkya was not agglutinated
by lobster serum, though all other bacteria tested
were agglutinated.

Presence in lobster hemolymph of effective de-
fenses against bacteria other than G. homari was
indicated by clearance within 30 days of inocu-
lated suspensions of Micrococcus conglomeratus.
M. sedentarius, Achromobacter thala^sius, and
Gaffkya tetragena. Since several of these bac-
teria are closely related to G. homari (which was
not cleared), some specificity of the phagocytic
or humoral protective mechanisms is strongly
indicated.

Natural agglutinins in lobster serum were
demonstrated against all bacteria tested (six

genera), except for all strains of G. homari.
Such agglutinins were of low titer, nondialy-
sable, inactivated at .56° C, and seemed to be non-
specific (as suggested by the limited observation
that a single absorption of serum by Flavobac-
teriuTn marinum removed agglutinins for all
other bacteria tested except Brerihacterium sp.) .
Cornick and Stewart's observations on phago-
cytosis of G. homari are interesting and war-
rant further investigation. They found no
phagocytized bacteria in hemolymph prepara-
tions 15 min after inoculation, but they did find
fluorescent-dye-labelled bacteria in hemoc>i;es in
heart, liver, and gill tissues of experimental lob-
sters soon after inoculation. Circulating hemo-
cyte numbers were reduced significantly with-
in 15 min after bacterial inoculation but returned
to normal levels after 5 hr. These data are in
agreement with the statements of Maynard
(1960). that phagocytes which have engulfed
foreign material lodge in capillary and lacunar
areas of the crustacean body, resulting in re-
duction in numbers of circulating hemocytes.
Bang (1956) observed in tissues of Limulus in-
jected with gram-negative bacteria a similar re-
duction in circulating hemocytes. In Cornick
and Stewart's study long-term infections of lob-
sters were characterized by the presence of black
nodules containing G. homari in tissue cells in
the gills, swimmerettes, and ventral abdominal

^ 20-
<

< 15-

LOG DOSE (BAOERIA / KG WEIGHT)

Figure 4. — Relation of dosage of Gaffkya to mean time
to death (MTD) in lobsters (calculated line of best fit
for mean time to death, using experimental groups of
10 lobsters each). (From Cornick and Stewart, 1968a.)

473

FISHERY BULLETIN: VOL. 69, NO, 3

sinuses of the lobster. As Parry (1960) had
pointed out earlier, this type of aggregation in
gills is a common phenomenon in Crustacea.
Poisson (1930) observed that, in the few crabs
{Carcinus maenas) resistant to the parasitic
ciliate Anophrys sarcophaga, masses of dead cil-
iates occurred in branchial lacunae, pericardial
sinus, and hepatopancreatic sinuses. Degener-
ating ciliates eventually formed brownish cysts.
Cantacuzene (1923b) observed a similar phe-
nomenon in Maia sqn'nmdo inoculated with bac-
teria. He pointed out that the lacunar tissue of
the branchial lamellae of decapod crustaceans,
with its many fixed phagocytes, acts as an ex-
tensive and effective bacterial filter.

Cornick and Stewart suggested that the devel-
opment of polysaccharide capsules by G. homari
in later stages of infection could be an important
device that prevented destruction of the phagocy-
tized bacteria and allowed multiplication of the
pathogen. They pointed out, as evidence, that
unencapsulated G. homari grown in culture were
actively phagocytized. As Stewart and Rabin
(1970) later reported, however, the unencapsu-
lated cultured bacteria were also virulent. It
may be that the capsule forms soon after the
organisms are injected into the host. This ob-
servation of survival and growth of ])hogocy-
tized encapsulated bacteria in lobsters is a direct
counterpart of the inability of vertebrate phago-
cytes to destroy many encapsulated microor-
ganisms, and parallels the earlier findings by
Cantacuzene (1923b) of a fatal disease in crabs
induced by encapsulated gram-positive bacteria.

Stewart, Dockrill, and Cornick (1969) exam-
ined certain insusceptibility factors affecting
Gaffkya disease in lobsters. Destruction of the
integrity of the integument seemed essential to
transmission of the pathogen. Acidity of the
gastric fluid was bactericidal and appeared to
provide an effective barrier against oral infec-
tion. Previous attempts to infect lobsters by
feeding infected material had been unsuccessful
(Snieszko and Taylor, 1917; Wood, 1965a, 1965b;
Rabin and Hughes, 1968).

Undoubtedly such insuscei)tibility factors are
of definite imiMrtance to the epizootiology of
gaffkaemia for several reasons: lobsters are
cannibalistic; hemolymph of moribund gaffkae-

mic individuals contains about 10' organisms per
ml (Stewart, Arie, Zwicker, and Dingle, 1969);
and Gaffkya can be isolated consistently from lob-
ster pounds, sea water, bottom mud, and slime of
holding containers (Goggins and Hurst, 1960).
A thorough study of the effects of temperature
on experimentally induced Gaffkya infections in
American lobsters was reported by Stewart,
Cornick, and Zwicker (1969). Mean time to
death was inversely related to temperature
(Figure 5). At 1° C no deaths attributable to
experimental infections occurred; at 3° C mean
time to death was 172 days; and at intermediate
higher temperatures mean time to death de-
creased drastically to a minimum of 2 days at
20° C (which approaches the upper lethal tem-

175

150-

5 125

X

I—
<

a
O

z
<

100

75-

50-

25-

O
\

1—
10

I
15

20

25

TEMPERATURE (°C)

Figure 5. — Relation of temijoraturc to mean time to
ileath in lobsters experimentally exposed to Gaffkya.
(From Stewart, Cornick, and Zwicker, 1969.)

474

SINDERMANN: INTERNAL DEFENSES OF CRUSTACEA

perature for American lobsters) . It is important
to note (in view of the very low seasonal tem-
peratures of waters in which lobsters live na-
turally) that at 1° C the pathogens i^ersisted
in the host in low numbers but with virulence
unchang-ed, and they produced mortalities when
the temperature increased. Experimentally in-
fected lobsters were also sensitive to and died
from rapid increases or decreases in environ-
mental temperatures — although the temperature
changes used in the experiments were probably
greater than those that would normally be ex-
perienced in nature.

Findings in vivo were paralleled by in vitro
results of growth of Gaffkya in lobster serum —
with a more I'apid increase to a peak of bac-
terial numbers with increasing temperature.
The organism grew in culture at all the exper-
imental tem])eratures (within a range of 1° to
20° C) ; at 1° C the bacterial growth curve was
erratic — it decreased in numbers to the 30th day,
then a log increase progressed to the 60th day,
followed by a substantial decline. The impor-
tant observation, of course, is that G. homari can
survive within the range of environmental tem-
peratures experienced by American lobsters and
that the pathogen causes mortality more rapidly
as temperature increases.

A concurrent physiological and biochemical
study by Stewart, Arie, Zwicker, and Dingle
(1969) and Stewart, Foley, and Ackman (1969) ,
in which an attempt was made to define features
of the infection that lead to death of lobsters,
produced several interesting results. The path-
ogen lacked proteolytic, lipolytic, and fibrinolytic
exoenzymes, suggesting that harmful effects are
not caused by direct destruction of tissue. The
authors observed that although in vitro growth
of G. homari was limited by the carbohydrate
level of the lobster serum medium used, pre-
sumably such a level would be maintained in
vivo at the exiiense of other tissues. Drastic
reductions in hepatopancreatic glycogen and
hemolymph nonprotein nitrogen characterized
later stages of the infection. No evidence of a
toxin was detected, and the conclusion was that
gafTkaemia is largely a wasting type of disease
— that death from the disease was "a result of
an unsuccessful competition on the part of the

lobster for its own readily available storage ma-
terial."

On the basis of experimental inoculations and
subsequent mortalities. Bell and Hoskins (1966)
suggested that Gaffkya might be pathogenic for
the Dungeness crab, Cancer magister, and the
shrimp Panda Ins platyceros from the Pacific
coast. That observation could be important in
view of recent introductions of American lob-
sters (some possibly carrying Gaffkya) on the
Canadian west coast. Other ex])erimenta!
studies (Cornick and Stewart, 1968b) indicated
that the bacterium may also be pathogenic for
east coast crabs (Cancer irroratus, C. borealis,
and Hyas coarctatus) . In vitro growth of the
]iathogen in crab sera was similar to that in
lobster serum, suggesting susceptibility of the
crabs. However, agglutinins for G. homari,
which were demonstrated in the sera of one of
the crab species (C irroratus) , might counteract
the favorable bacterial growth in vivo and reduce
the severity of infections in the crab. Cornick
and Stewart extended their observations by inoc-
ulations of C. irroratus with suspensions of G.
homari. After 49 days the surviving crabs
(three) were found to be heavily infected (10^
organisms/ml hemolymph). Passage through
the crabs did not alter pathogenicity of Gaffkya
to lobsters. A repetition of the crab inoculations
with larger numbers of crabs provided some evi-
dence of greater mortalities in experimental
groups than in controls. Pathogenicity for rock
crabs was less than for lobsters, as indicated by
a mean time to death of 42 days in crabs, against
only 18 days in lobsters. The authors mentioned
the possible role of rock crabs as reservoirs of
infection for lobsters, in view of reduced path-
ogenicity and prolonged mean time to death in
crabs.

From the foregoing, it is apparent that ex-
perimental studies with G. homari have been nu-
merous and vai'ied and have provided significant
insights aljout the internal defenses of Crusta-
cea. Important areas for future study include
determination of whether strains of the pathogen
with different virulences exist, and determina-
tion of whether virulence may be increased by
rapid passage through impounded lobster pop-
ulations.

475

FISHERY BULLETIN: VOL. 69. NO, 3

DISCUSSION

In the development of information and prin-
ciples of invertebrate internal defenses, con-
sistent and entirely natural attempts have been
made to translate findings into the concepts and
compartments constructed for the immune re-
sponses of vertebrates. The effort has led to
some confusion of terminology and even to lack
of agreement about definitions of immunity.

The concept of immunity in vertebrates has
been admirably stated by Good and Papermaster
(1964), who define immunity precisely and nar-
rowly as "a biologic phenomenon embodying pri-
mary and secondary responses, with antibody
synthesis and release, reactions of immediate and
delayed allergy, and homograft immunity."
They state: "To the time of writing [1964],
adaptive immunologic responsiveness has not
been demonstrated in the invertebrates." They
then define adaptive immune responsiveness as
"the ability to respond to antigenic material by
production of specific combining substances, and
to show an anamnestic response to these same
antigens on subsequent exposure." Their con-
tinued exposition of immunity from the verte-
brate point of view includes the following signifi-
cant points:

1. "Adaptive immunity ... is primarily a func-
tion achieving full expression late in phylogeny
and ontogeny."

2. "The l>-mphoid cell family is the primary
cellular basis for adaptive immune response in
vertebrates . . . ."

3. "The possibility that another cell system
may mimic adajitive immune resi)onses in an in-
vertebrate species cannot be excluded at this
time."

A broader, more inclusive, concept of immu-
nity has been suggested recently. If the broader
definitions of terms projiosed by several authors
are accepted, the words "immunity" and "im-
mune response," rather than careful circum-
locutions, can be used with invertebrates. As
an example, McKay and Jenkin (1969) stated
that the Australian freshwater crayfish was ca-
jialjle of an "adaiitive immune resjionse." Such
a capability is not possible within the confines

of Good and Papermaster's definition of adaptive
immunity as the production of specific immuno-
globulins (a capacity which has been correlated
with the occurrence of lymphoid tissue) . Per-
haps their definition is too restrictive and rigid,
since a number of invertebrates do show re-
sponses that protect them from pathogens (hence
they are adaptive) .

Earlier definitions of antibodies and immunity
allowed more latitude for inclusion of inverte-
brate responses. Cantacuzene (1923b) , for ex-
ample, considered as antibodies ". . . toute sub-
stance albuminoide du plasma, douee ou non de
sjiecificite, qui, se fix.mt sur I'antigene, modifie
les relations de contact de ce dernier, soit avec
les cellules, soit avec les autres constituants
chimiques des humeurs."

McKay, Jenkins, and Rowley (1969) stated
". . . to allow comjiarisons to be made between in-
vertebrate phyla and the vertebrates . . . the defi-
nitions of the immune response should be as
broad as possible and emphasis placed on the
functional aspects . . . ." These authors suggest
that such a definition of the immune response
might be "the ability of the animal to respond
to a foreign particle (whether it be truly foreign
or unwanted self) by the iiroduction of s]5ecific
proteins capable of reacting with the inducer,
and the resultant of this reaction leading to
phagocytosis."

Gushing (1967), in an excellent summariza-
tion of invertebrate immune mechanisms, stated
"There is a growing consensus of observations
supporting the view that while vertebrates and
invertebrates may share some basic immune
competences such as 'innate immunities' and
phagocytic cells, it is indeed only within the
vertebrates that the full capacity of adaptive im-
munity exists." This statement seems reason-
able, and fits the confines of Good and Paper-
master's narrow definition of adajitive immunity,
but is too negative if a broader perspective of
immunit.v — such as that proposed by McKay,
Jenkins, and Rowley — is adojjted.

Probably greater emphasis should be jilaced
on the cidaptive aspects of invertebrate internal
defense processes. Substantial numbers of
studies have indicated the existence of adaptive
responses to experimental inoculations of for-

476

SINDERMANN: INTERNAL DEFENSES OF CRUSTACEA

eigfn protein. Whether the response is in the
form of specific immunoglobulin seems less sig-
nificant than the degree of protection afforded
to the individual by the adaptive response. In
the broadest sense, the replacement of a pro-
tective constituent of the hemolymph after its
utilization in preventing infection could be con-
sidered adaptive. For example, the precipitat-
ing factor for foreign jn-otein found by Stewart
and Foley (1969) in lobster serum (which de-
creases following experimental inoculation of
BSA and which is unreactive against injected
lobster serum) would be adaptive.

Considering immune responses of vertebrates
and invertebrates. Good and Papermaster stated
that the presence in vertebrates of lymphoid tis-
sue and cells constitutes a basic distinction. On
this basis, as Chadwick (1967) has pointed out,
"It is highly unlikely that insects [or Crustacea
or other invertebrates] do produce mammalian
type antibody, or that the mechanism of any
acquired response to antigenic stimulus could be
likened to responses in higher animals in terms
of the production of specific antibody globulins."
Analogous tissues and cells exist in a number of
invei'tebrate groups, however, as do analogous
humoral res]3onses without the extreme specifi-
cities of vertebrate globulins. Chadwick (1967)
also stated that the ". . . immune resjionse in an
insect is not the consequence of an antigen-anti-
body-globulin reaction but more likely the result
of the production of some, as yet undefined,
principle in insect hemolymph which may con-
tribute to its resistance." The same statement
might be made about other invertebrates in
which an induced response has been demon-
strated.

Although somewhat beyond the confines of the
present consideration of internal defenses of
Crustacea, it might be well to call attention to
recent tissue transplantation work of Cooper
(1968, 1969a, 1969b, 1969c, 1969d) with an-
nelids, which indicates a high degree of specifi-
city of response and which suggests some sim-
ilarities to vertebrate tissue graft responses.
Cooper's (1969d) concluding statement is sig-
nificant: "Further clarification of anamnestic
responses to tissue transplants would confirm our
views that at least two of the parameters of

adaptive immunity [in the vertebrate sense],
namely specificity and memory, did not evolve
exclusively with the lower vertebrates."

It is obvious that modification, redefinition, or
replacement of some conventional immunological
terminology — particularly toward broader defi-
nitions— is needed if the invertebrates are in-
cluded in comparative immunology. If we re-
move "antibodies" from invertebrate terminol-
ogy we must also remove "antigen," since anti-
body response is part of the definition of antigen.
An eff'ective substitute for "antigen" (as sug-
gested for insects by Hinton) (Chadwick, 1967)
would be "immunogen." Chadwick also sug-
gested replacement of "antibody" with such
terms as "natural bactericidal substance," "spe-
cific inducible substance," and others. Further-
more, as stated earlier, it must be made clear
that when "lysins," "precipitins," "agglutinins,"
and other humoral factors of invertebrates are
discussed, identification with vertebrate factors
is not intended — the terms are used merely to
indicate the kind of activity produced (i.e., "lytic
substance or activity," "precipitating substance
or activity," etc.) regardless of the physiological-
biochemical mechanism (s) involved.

When suitably qualified the "safe" general
terms, therefore, include "resistance," "immu-
nity," "immune response"; terms that can have
general applicability and utility, if accepted in
a general sense, include "agglutinin," "lysin,"
"precipitin"; specific vertebrate terminology,
not applicable to invertebrates includes "anti-
body," "antigen," and "serological."

Beyond the establishment of working defini-
tions of immunity in invertebrates, it seems ap-
propriate to list a number of generalizations that
seem warranted by the admittedly narrow base
of evidence now available. Obviously, any gen-
eralization about a group as evolutionarily di-
verse as the invertebrates — or for that matter
even of the Crustacea — must be in the form of
a tenuous and easily retractable hypothesis
(which may at times border on speculation),
and the following statements are offered with
these qualifications:

1. Resistance in the vertebrates seems pri-
marily related to production of immunoglobulins

477

FISHERY BULLETIN: \'0L. 69, NO. 3

which combine with foreign protein to enhance
the phagocytic process. Although specific im-
munoglobulins have not yet been demonstrated
in invertebrates, an analogous protein system,
of lower specificity but with functions similar to
vertebrate immunoglobulins, is suggested. Na-
tural (and in some cases, partially specific) ag-
glutinins are common in invertebrate body fluids,
and their titers in some species may be increased
by e.xposure to specific antigens.

2. Resistance in the vertebrates, and in some
invertebrates also, includes the production of
bactericidins, lysins, and agglutinins. The ap-
pearance of, or the increase in, titers of such
factors in certain invertebrates following expo-
sure to foreign proteins may account in part for
increased resistance to certain pathogens (Mc-
Kay and Jenkin, 1969; Bang, 1967b).

3. Many of the bactericidal, bacteriostatic,
lytic, and agglutinating properties seem to be
conferred on the hemolymiih of invei-tebrates by
release of materials from hemocytes. The sub-
stances so released often seem not only less spe-
cific in their action than vertebrate antibodies,
but also the stimulation of release may be much
less specific. For example, the release of a lysin
in sipunculids for the ciliate Anophrys can be
stimulated by inoculation of certain bacteria
(Bang, 1967a), and the release of a hemolysin
in Maia sqninado for sheep red blood cells can
be induced by injection of sipunculid coelomic
fluid (Cantacuzene, 1920a, 1923b).

4. Immune response in invertebrates, as best
exemplified in insects and crustaceans, is often
rapid in onset and disappearance — usually a
matter of a few days.

5. As has been observed by a number of
authors (Feng and Stauber, 1968; Stewart,
Cornick, and Zwicker, 1969), environmental
temperature is a critical factor in the host-par-
asite relationships of invertebrates. Temper-
ature has been found experimentally to exert a
significant eflfect on the appearance, degree, and
duration of resistance to infection in certain in-
vertebrates (McKay and Jenkin, 1969), just as
it does in poikilothermic vertel)rates (Bisset,
1946, 1947a, 19471), 1948a, 1948b). Tempera-
ture affects the rate of growth and i-eproduction
of microorganisms, the rate of production of

toxic metabolites, and the utilization of nutrient
derived from the host. Temperature can also
affect the rate of phagocytosis and the rate of
production of humoral defenses against infec-
tion. Thus the progress of infection and the out-
come of disease represents a composite of en-
hancement or inhibition partly mediated by
temperature.

6. Endotoxin has been found (in the verte-
brates) to increase the metabolic rate of phago-
cytes and stimulate phagocytosis (Jenkins and
Palmer, 1960; Whitby et al, 1961). A similar
effect may be produced by endotoxin in the in-
vertebrates. Thus, exposure to gram-negative
bacteria which are so abundant in the sea (or
to their endotoxins) may increase the level of
nonspecific resistance to other gram-negative or-
ganisms or their endotoxins. This "nonspecific
immunity," which is also known in the verte-
brates (Rowley, 1956; Landy and Pillemer,
1956), may be of great significance in the in-
vertebrates— in fact, it may be the basic mech-
anism of internal resistance to bacterial path-
ogens in the invertebrates.

7. Handling and ex])erimental procedures
rapidly induce bacteremias in a number of in-
vertebrates. Rabin (1965), for example, found
that almost half of all American lobsters used
in his studies had bacteremias upon arrival in
the laboratory. Cornick and Stewart (1966)
found that about 20 'r of a large sample of lob-
sters had bacteria in their hemolymph. Isolates
were principally Micrococcus, Pseiidomonas,
Brevibacterium, and Achromobacter — bacteria
commonly found in the marine envii'onment, and
apparently nonpathogenic for lobsters. The acts
of capture, transport, and impoundment of these
and other marine animals may produce stresses
and physiological changes (or mechanical dam-
age) that permit entry of microorganisms com-
mon in the surrounding sea water.

8. There is some limited evidence that the
process of phagocytosis, fully elaborated in the
Protozoa, is enhanced in the vertebrates by non-
specific humoral factors which sensitize, agglu-
tinate, immobilize, or otherwise increase the
susce))tibilily of iiroteins to jihagoc.vtosis by fixed
and mobile phagocytic cells. Although the op-
sonizing substances of invertebrates have not

478

SINDERMANN: INTERNAL DEFENSES OF CRUSTACEA

been adequately characterized and the mecha-
nisms involved have not been adequately eluci-
dated, it may be speculated that in the verte-
brates a greater degree of specificity of humoral
factors has been added to the nonspecific mech-
anisms found in the invertebrates.

The proper role of specific vertebrate anti-
body as a possible augmentation of evolutionarily
older nonspecific internal defenses was alluded
to by Miles (1962). He stated ". . . it is fairly
clear that antibody per se has little effect on
the viability or metabolism of microbes with
which it combines. It is effective in defense
either because it neutralizes toxins, or because
it makes the microbe susceptible to non-specific
defense factors like complement or the phago-
cyte .... We may then properly consider anti-
body as accessory to the more fundamental non-
specific defense mechanisms . . . ." It should be
emphasized, however, that much remains to be
learned about the nonspecific humoral factors
of vertebrates, as well as invertebrates.

9. Brown (possibly chitinoid) bodies or cysts
in gills characterize later stages of a number of
crustacean diseases. The sequence of events,
after invasion by microorganisms, may include
action of toxic or inhibitory factors in hemo-
lymph, accretion of moribund or dead invaders
in gill lacunae, phagocytosis of dead organisms,
and formation of nodules or cysts containing
dead organisms, and gradual phagocytic de-
struction of necrotic material.

10. An important point, as Bang (1967b)
mentioned, is that the probability of discovering
internal defense mechanisms is greater when di-
sease phenomena are studied under natural con-
ditions. In experimental work, microorganisms
pathogenic to marine invertebrates should con-
stitute test organisms of choice; microorganisms
found in the environment (and which may be
facultatively pathogenic) should be next in order
of preference; and microorganisms or proteins
which the mai'ine animal is unlikely to encounter
seem least instructive. There are valid experi-
mental reasons, of course — such as the ease of
recognition of bacteriophages — that often lead
to selection of test microorganisms other than
pathogens or potential pathogens. Whether

these unusual choices are effective antigens is
obviously a most important consideration.

Another extremely pertinent observation
made by Bang (1967b) was: "The limited
amount of information [concerning immunolog-
ical responses of invertebrates] is, I believe, due
mainly to the limited number of studies, and not
to any lack of imagination on the part of evo-
lutionary forces in developing protective mech-
anisms."

11. One final and very significant thought was
proposed by Stauber (1961): "That so few
examples of acquired resistance are known
among invertebrates may even be quite logical.
Because of their relatively short generation
times, their usual small size and often enormous
reproductive capacities, subsequent epizootics
would be much more likely to be circumvented
by the appearance of resistant stocks through
natural selection .... Even with very high mor-
tality rates a residual stock of animals under
favorable conditions later might repopulate an
area .... If this reasoning is adequate to explain
the lack of evidence for the occurrence of ac-
quired resistance in most of the invertebrates,
perhaps those invertebrates with a long life span,
like Liniulus should be investigated more fully,
as likely hosts capable of demonstrating ac-
quired resistance."

It is interesting to note that it is precisely
those invertebrates with a long life span which
have received increased attention during the past
several years, and that a few indications of
acquired resistance have been reported.

Information about the internal defenses of
crustaceans and other invertebrates may be
summarized as follows:

The weight of evidence indicates a major de-
fensive role in invertebrates for phagocytosis,
augmented by relatively nonspecific innate or
acquired humoral factors. Preformed substances
released into the hemolymph from granular
hemocytes seem to play a major role in humoral
defenses of Crustacea, and probably other in-
vertebrates as well. Thus the body fluids of
many invertebrates contain natural bacterici-
dins, agglutinins, lysins, and occasionally pre-
cipitins. Some limited evidence for augmenta-

479

FISHERY BULLETIN: VOL. 69. NO. 3

tion of such defenses by exposure to foreigTi
antigen exists. This evidence is primarily in
form of increased titers following: experimental
inoculation. Specific acquired antibodies (im-
munoglobulins) have not been demonstrated in
invertebrates, but induced antibody-like activity
has been demonstrated in a few^ species. The
fundamental difference seems to be in degree of
specificity of response, which is significantly
higher in the vertebrates. It is obvious that the
synergistic action of phagocytes and humoral
factors in the invertebrates, as well as in the
vertebrates, constitutes the significant defense
perimeter — but the degree of specificity of the
humoral components is lower in the inverte-
bi'ates. The master internal defense plan seems
to be: foreign protein + humoral factor =
recognition of foreignness and phagocytosis.

Cooper (1969c), concluding a very though-
provoking paper, stated: "It seems reasonable
to conclude that invertebrates do possess immune
systems, although the nature of the mechanisms
is decidedly unknown. Reactions may be as
numerous as the varied taxonomic groups, as is
true of most rigorously studied vertebrates. In-
vertebrate cellular immunity may be closer to
vertebrate reactions and may represent the
more primitive responses. In the absence of
classic vertebrate-type immunoglobulin in in-
vertebrates, a real dichotomy would be evident
in the evolution of immune responses. On the
other hand, immunoglobulin precursors may be
present."

Certainly the next decade will prove to be an
exciting one in the study of invertebrate internal
defense systems. The components of classical
vertebrate immunity — present as analogues in
invertebrates, and probably varying widely
among phyla — provide an excellent background
against which new findings may be evaluated.

ACKNOWLEDGMENTS

The author would like to acknowledge with
thanks the helpful comments of Dr. Harvey
Rabin, Institute for Comparative Biology, Zoo-
logical Society of San Diego, San Diego, Calif.;
Dr. James Stewart, Halifax Laboratory, Fish-
eries Research Board of Canada, Halifax, N. S. ;

and Dr. Marenes Trip]3, Department of Bio-
logical Sciences. LIniversity of Delaware, New-
ark, Del. Impetus for this review was provided
in part by an examination of cellular and hu-
moral I'esponses of shrimps and crabs being con-
ducted with Dr. Ben Sloan, Carson-Newman
College, Jefferson City, Tenn. Elizabeth Leon-
ard, Librarian, Tropical Atlantic Biological Lab-
oratory, aided immeasurably in assembling
copies of the extensive body of literature on
which this review is based.

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489

CLEANING SYMBIOSIS AMONG CALIFORNIA INSHORE FISHES'

Edmund S. Hobson''

ABSTRACT

Cleaning symbiosis among shore fishes was studied during 1968 and 1969 in southern California, with
work centered at La Jolla. Three species are habitual cleaners: the senorita, Oxyjidis caUfomica;
the sharpnose seaperch, Phaixerodon atripes; and the kelp perch, Brachyistius frenatus.

Because of specific differences in habitat, there is little overlap in the cleaning areas of these three spe-
cies. Except for juvenile sharpnose seaperch, cleaning is of secondary significance to these species, even
though it may be of major significance to certain individuals. The tendency to clean varies between in-
dividuals. Principal prey of most members of these species are free-living organisms picked from a
substrate and from midwater — a mode of feeding that favors adaptations suited to cleaning.

Because it is exceedingly abundant in a variety of habitats, the senorita is the predominant inshore
cleaning fish in California. Certain aspects of its cleaning relate to the fact that only a few of the many
serioritas present at a given time will clean, and that this activity is not centered around well-defined
cleaning stations, as has been reported for certain cleaning fishes elsewhere. Probably because cleaners
are difficult to recognize among the many senoritas that do not clean, other fishes generally do not at-
tempt to initiate cleaning; rather, the activity is consistently initiated by the cleaner itself. An infest-
ed fish approached by a cleaner generally drifts into an unusual attitude that advertises the temporary
existence of the transient cleaning station to other fish in need of service, and these converge on the
cleaner. Although seiioritas, as a group, clean a number of different fishes, a given individual tends to
initiate cleaning with members of just one species.

The fishes cleaned most often are those which are most abundant and, at the same time, are most
heavily infested with external parasites. The most numerous ectoparasites are caligid copepods, the
most abundant and widespread of which is Caligus hobsoni. These particular parasites, along with
gnathiid isopod larvae, are the major prey of the cleaning fishes. Cleaning is essentially limited to the
external body surface; ectoparasites of the oral and branchial cavities are not ordinarily taken. Clean-
ing effectively reduces the numbef of parasites on fishes that are cleaned, and is an important activity
for the organisms involved. However, there is no basis for the contention that many good fishing grounds
in southern California exist because fishes have congregated in these locations for cleaning.

It has been suggested that many of the better
inshore fishing spots are, in fact, cleaning sta-
tions (Limbaugh, 1961; Feder, 1966). The
contention is that fishes congregate at these lo-
cations so that ectoparasites and other deleteri-
ous material can be removed from their bodies
by resident cleaning organisms. Critics of this
hyjwthesis might well suggest instead that clean-
ers simply are especially active where fishes are
most abundant, or that the cleaners as well as
those they clean occur at these locations for

' Contribution of Scripps Institution of Oceanography.

" National Marine Fisheries Service, Tiburon Sport
Fisheries Marine Laboratory, Tiburon, Calif., and
Scripps Institution of Oceanography, University of Cal-
ifornia, San Diego, Calif. Mailing address: National
Marine Fisheries Service, Fishery-Oceanography Center,
P.O. Box 271, La Jolla, Calif. 92037.

Manuscript accepted March 1971.

FISHERY BULLETIN: VOL. 69, NO. 3, 1971.

reasons that have nothing to do with cleaning.
Regardless of which view is correct in a given
situation, one having witnessed fishes crowded
around a cleaner, vigorously soliciting its ser-
vices, can only conclude that this activity is in-
deed important to the organisms involved.

Cleaning symbiosis has been widely described
in the literature (Longley and Hildebrand, 1941;
Eibl-Eibesfeldt, 1955; Limbaugh, 1955, 1961;
Randall, 1958, 1962; and others) and was re-
viewed by Feder (1966). Youngbluth (1968)
studied activity of the Hawaiian cleaning labrid
Labroides phthirophagus in some detail, and
Losey (1971) analyzed the communicative sig-
nals between this same species and the fishes that
it cleans. But most other reports on cleaning
have been simple treatments based largely on

491

incidental observations. In this report, I de-
scribe cleaning symbiosis among inshore fishes
of southern California and attempt to I'elate ob-
served activity with the incidence of specific
ectoparasites.

Conrad Limbaugh, Scripps Institution of
Oceanography, was among the first to report
cleaning symbiosis among California fishes. In
a study of fishes of the kelp beds, Limbaugh
(1955) described cleaning by the seiiorita, Ox-
yjulis californica, a fish of the family Labridae,
and also by several seaperches of the family
Embiotocidae: the kelp perch, Brachyistius
frenatus; the black perch, Emhiotoca jacksoni;
and the pile perch, Rhacochilus vacca. Subse-
quent observers have described cleaning by the
rainbow seaperch, Hijpsurus cnryi (Gotshall,
1967) ; the sharpnose seaperch, Phanerodon
atripes (Clarke, Flechsig, and Grigg, 1967;
Gotshall, 1967; Hobson, 1969a) ; and the black-
smith, Chromis punctipinnis (Turner, Ebert,
and Given, 1969).

FISHERY BULLETIN: VOL. 69, NO. 3

SPECIES STUDIED

Most of the cleaning observed during this
study was performed by the seiiorita (Figure 1) ,
which by virtue of its great abundance in a va-
riety of habitats is the predominant cleaner in-
shore. The sharpnose seaperch (Figure 2) was
frequently observed cleaning, but its activity is
centered in deeper water. The kelp perch (Fig-
ure 3) may be an important cleaner in the can-
opy region of the kelp forests, where it concen-

FiGURE 1. — Seiiorita.

FiGUKE 2. — Sharpnose seapercli anions: l)ranche.s of a Rorgonian.

492

HOBSON: CLEANING SYMBIOSIS

trates, but this was not determined in this study
because observations in the kelp-canopy habitat
were infrequent. Nevertheless, observations
were sufficient to recognize the kelp perch as a
habitual cleaner. The only other fish seen clean-
ing was the white seaperch, Phanerodon fur-
cntu^, in which cleaning seemed to be only an
occasional incidental activity.

METHODS

During 1968 and 1969, I spent more than 103
hr underwater directly observing cleaning and
related activity in California inshore waters.
Also contributing to the study are many inci-
dental observations of cleaning made during
other work with California fishes between 1961
and 1970.

Supplementing the observations, 421 speci-
mens of 39 species were collected with spear.
These represent most of the species common in
the study area that exceed a length of 100 mm
(all lengths of fishes in this report are standard
length). The ectoparasites were collected from

all specimens and will be reported in detail else-
where in collaboration with R. F. Cressey, U.S.
National Museum. These collections also pro-
vided the material for descriptions of 1 1 species
of copepods formerly new to science (Cressey,
1969a, 1969b, 1970; J. Ho, California State Col-
lege, Long Beach, unpublished manuscript) . Ad-
ditional undescribed species may occur among
a number of copepods from these collections
presently under study by Z. Kabata, Biological
Station, Nanaimo, British Columbia.

In addition to a survey of the ectoparasites,
gut contents of known cleaning species, including
material from .53 seiioritas, 29 sharpnose sea-
perch, and 3 kelp perch, were analyzed.

Many ectoparasites leave their host when it
is in difficulty, and some fishes regurgitate their
stomach contents under stress. To reduce this
loss, all specimens were individually sealed in
plastic bags immediately upon capture, and while
still underwater.

To acquire detailed data on the cleaning in-
teraction, a number of individuals of cleaning
species were kept under surveillance for periods

Figure ',i. — Kelp perch next to giant kelp.

493

FISHERY BULLETIN: VOL, 69, NO. 3

up to 15 min, and a verbal account of their ac-
tivity was recorded on taiie. The attempted
standard of 15 min could not be maintained for
all these observations because sometimes con-
tact with the fish beinjr watched was lost as the
fish swam among vegetation or other fishes. In-
dividuals followed included known cleaners as
well as others that had not shown evidence of
cleaning. In monitoring the activity of known
cleaners, a record was kept of the time during
which they showed an apparent cleaning inter-
est in other fish and also the number of cleaning
bouts in which they became involved. A clean-
ing bout is defined here as any cleaning activity
involving a discrete group of fishes, whether this
group includes one cleaner attending a single
fish, or several cleaners attending a cluster of
40 to 50 fish. On various occasions I also re-
corded the number of times that the cleaner
actually "picked" at the body of another fish, and
I)recisely at what point on the body this action
was directed.

Study Areas

Observations of cleaning symbiosis were made
at many locations throughout southern Califor-
nia, including the Channel Islands, and at the
Coronado Islands, Mexico. However, most of
the data were collected during concentrated work
at La Jolla, Calif. Here, three study sites were
established, each including an area of ai)()ut
100 m-, that lie on a line running northwest off-
shore from La Jolla Point. Moving away from
the beach along this line, the first station lies in 3
to 10 m of water about 200 m ofl'shore, the sec-
ond is in 20 to 25 m of water about 700 ni off-
shore, and the third in 30 to 35 m of water about
1000 m oflfshore. The sea floor at all three sta-
tions is rocky and irregular, with many crevices
and caves. Algae are not conspicuous at the two
deei)er stations, which are similar, but the rocks
supi)ort a heavy growth of gorgonians. On the
other hand, the nearshore region of the 3- to 1 0-m
station is richly carpeted with surfgrass, Phyl-
lospadix, and other parts of the inshore station
are forested by large kelps, particularly giant
kelp, Macrocystis, and feather-boa kelp, E(/re-
(/ia. However, these large kelps are sparse here

in comparison to some areas nearby to the south
and elsewhere in California. Other details of
the ijrincipal study area will be inti'oduced as
they become pertinent.

During all observation periods at the La Jolla
stations a record was kejjt of water temperatures
from surface to bottom, horizontal visibility, and
surge conditions.

OBSERVATIONS

GENERAL ECOLOGY

Scnorita

The seiiorita, which attains a length of about
250 mm, is one of the most abundant fishes in
the inshore waters of southern California, in-
cluding the Channel Islands. It occurs from the
shoreline to depths exceeding 40 m and is re-
corded from central California south to central
Baja California, Mexico (Roedel, 1953). An in-
habitant of water over rocky substrates and
among sea weeds, the seiiorita sometimes swims
singly, Vjut more often in groups of from a few
to many hundreds of individuals. Like other
labrids, it is strictly a diurnal fish, taking shelter
under cover at night.

Food habits. — The senorita feeds on a variety
of benthic organisms from the surface of both
algae and rocks. It also feeds heavily in the mid-
waters, taking small organisms in the jilankton,
as well as forms that are attached to or encrusted
on drifting algal fragments. All this feeding
is accomijlished in a characteristic picking man-
ner, a mode of feeding well suited to its pointed
snout and the several long, curved canine teeth
that project forward at the front of each jaw.

To determine the food habits of this fish in
the study area, 26 specimens. 110 to 195 mm
long, were speared randomly from the population
at large. None of these were cleaning when
collected. Food items in their stomachs, ranked
as percentage of each item in the entire sample,
were as follows: bryozoans encrusted on algae,
43 9f ; caprellid amphijjods, 32Sf ; fish eggs, S'^'r ;
gammarid amphipods, 2.5^^ ; unidentified crus-
tacean fragments, 4Sf ; and pelecypod mollusks,

494

IIOBSON; CLEANING SYMBIOSIS

2.4';. A number of items each made up less
than l''f of the sample, incUidinp: crab frag-
ments, gastropod moUusks, pycnogonids, and a
gnathiid isopod larva. Unidentified material
constituted le^r of the sample. The gnathiid
larva, a single individual from one seiiorita, was
the only evidence of ectroparasites among this
material.

Limbaugh (195.^)) stated that senoritas are
omnivorous carnivores which feed on almost any
animal material. Quast (1968) concluded that
the principal foods of the seiiorita are small
gastropods and crustaceans associated with al-
gae. Because he found no crabs or pistal shrimps
in the diet, Quast suggested that bottom feeding
is infrequent; however, having seen senoritas
frequently picking on the bottom, I believe there
must be some other reason why these prey are
not taken more often. Size may be a factor, as
crabs and pistal shrimps generally are larger and
more heavily shelled than most prey of the
seiiorita.

Movements. — Although individual seiioritas
may range widely over the bottom in a given
locality, they seem to operate within a restricted
range. Individual fish, when followed, always
criss-cross back and forth within a defined area.
Twelve individuals, selected randomly from the
population at large and kept under surveillance
for 11 to 15 min each, showed no evidence of
cleaning.

Senoritas are most abundant at the 3- to 10-m
station and become progressively fewer with in-
creasing depth offshore. Nevertheless, even at
the 30- to 35-m station the species was among
the most numerous present. Fluctuations in
numbers wei'e often apparent with changes in
water temperature. Some of the movement is
vertical. When a layer of colder water moved
in over the bottom — a frequent phenomenon at
the 20- to 2.')-m station — seiioritas were especially
abundant up in the water column above the
thermal interface. Seasonal and other longer
term changes may induce inshore/offshore move-
ments in certain members of the popuk\tion. The
numbers present fall off noticeably when temper-
atures drop much below 13° C, but at least some
.senoritas were present no matter what the con-

ditions. These comments on temperature effects
are based entirely on casual evaluations of rel-
ative abundance under varying conditions.

Sharpnose Seaperch

The sharpnose seaperch is not regarded as a
common species (e.g., Limbaugh, 1955), but was
relatively abundant during this study over rocky
substrates below 20 m in the La Jolla area. It
grows to over 200 mm long and is recorded from
Bodega Bay, central California (Miller, Gotshall,
and Nitsos, 1965), south to the San Benito
Islands, Mexico (Roedel, 1953). Most of those
observed during this study were juveniles less
than about 125 mm long that swam singly or,
more often, in small groups of less than 10 indi-
viduals. Adults were seen only occasionally but
sometimes swam in larger aggregations. All
activity observed in these fish occurred during
daylight. After dark they hover above the sub-
strate and are alert, but their activity at this
time, if any occurs, was not determined.

Food habits. — This seaperch takes a variety
of benthic organisms from the surface of rocks,
algae, gorgonians, and other benthic substrates.
Prey are taken off the bottom in a characteristic
picking manner similar to that of the seiiorita.
However, the seaperch's dentition would seem
less specialized for picking than that of the
senorita; its conic teeth are relatively short and
straight, and those at the front of the jaws are
not notably longer than tho.se on the sides, nor
do they project forward.

To investigate the food habits of this fish in
the study area, 13 individuals, 76 to 170 mm
long, were speared randomly from the popula-
tion at large. None of these were cleaning when
collected. Food items in their stomachs, ranked
as percentage of each item in the entire sample,
were as follows: caprellid amphipods, 56%;
chitons, 9%; planktonic copepods, 9/f ; isopods,
&',r ; limpets, 2%; pelycypodmollusks, 1%; and
sponges, l'''r. Unidentified material made up
14'^; of the sample. There was no evidence of
ectroparasites in this material. One individual
had fed heavily and exclusively on plankton-
ic copepods, showing that this fish is not

495

FISHERY BLLLETIN: VOL. 69. NO. 3

limited to benthic prey. I have found no refer-
ences to food habits of this fish in the litera-
ture.

Movements. — On the basis of limited obser-
vations, these fish do not seem to move around in
their habitat as much as senoritas do. Never-
theless, they do show marked inshore/offshore
movements that may relate to changing water
temperatures. Unlike the ubiquitous senorita,
this fish occurred in limited numbers that al-
lowed assessing relative abundance through ac-
tual counts. It was never seen at the 3- to 10-m
station but was reasonably abundant (10-20 in-
dividuals were counted during 15-min periods)
on all visits to the 30- to 35-m station. At the
20- to 25-m station its appearance was irregular
and closely followed temperature fluctuations.
Generally it was rare or absent at the 20- to 25-m
station when bottom temperatures rose much
above 13° C, and was present (a maximum of
10 was seen during a 20-min ]5eriod) when the
temperature dropped much below this level. As
most of the individuals seen were juveniles, a
seasonal factor inde]3endent of temperature was
probably operating here. Nevertheless, short-
term temperature changes over the critical range
(approximately 12°-14° C at the 20- to 25-m sta-
tion) were consistently accompanied by the
presence or absence of this fish. I emphasize
that these assessments of abundance are relative
to the numbers of the species regularly present.
The senorita was alwa.vs more abundant than
the seaperch at all stations and under all con-
ditions. Thus whereas the seaperch was con-
sidered abundant during a period in which 15
individuals were seen, at no time did I find so few
seiioritas present at any of the three La Jolla
stations.

Kelp Perch

The kelp perch was not abundant in the La
Jolla study area, where it was seen only at the in-
shore station. Its distribution is essentially lim-
ited to the kelp beds, which were not well de-
veloped in the study area at the time of this
work. Nevertheless, it is very numerous in Cal-
ifornia inshore waters that are heavilv forested

with kelp. Attaining a maximum length of about
150 mm, the kelp perch is recorded from Van-
couver Island, Canada, south to central Baja
California, Mexico (Roedel, 1953). The kelp
]Derch occurs near the rocky bottom at the base
of giant kelp, as well as adjacent to the rising
kelp stipes, but is most abundant just under the
kelp canopy, near the water's surface. Tyiii-
cally, this fish occurs in aggregations of a dozen
or more, but larger individuals frequently are
solitary, especially those near the rocky sea floor.
Most of my observations of kelp perch were made
outside the La Jolla study area, the majority
around the Channel Islands.

Food habits. — This perch feeds in a picking
manner, similar to that employed by the senorita
and sharpnose seaperch. It preys on a variety
of organisms from the surface of the surrounding
kelp and also feeds extensively on material sus-
pended in the current. Its pointed snout and
small, upturned mouth, together with a number
of relatively long, curved canine teeth that pro-
ject forward at the front of each jaw, are well
suited to its mode of feeding. The dentition of
this fish is similar to that of the seiiorita, a fact
also noted by Hubbs and Hubbs (1954). I did
not sample kelp perch from the population at
large for food-habit analysis; all those collected
were from known cleaning stations. However,
Limbaugh (1955) stated that they feed on small
crustaceans, particularly those that occur on
giant kelp. Quast (1968), who also reported a
predominantly crustacean diet, with a prepon-
derance of amphipods, noted that some mollusks
and bryozoans are taken as well.

Movements. — Limited observations indicate
that aggregations of kelp perch in the canopy,
and close to large rocks, remain relatively stable.
Several aggregations that were observed over
2 to 3 months did not change appreciably in lo-
cation or in numbers of individuals. Data on
this point are scanty, however.

At night they hover in the same areas in
which they are active in daylight, but their ac-
tivity at this time, if any occurs, was not deter-
mined.

496

HOBSON: CLEANING SYMBIOSIS

CLEANING ACTIVITY OF
THE SENORITA

Unlike some other cleaners (see Feder, 1966) ,
senoi-itas do not establish well-defined stations
at which they receive other fishes seeking to be
cleaned. Rather, the senoritas, as they move
over the local area, approach and clean fishes
wherever they encounter them.

Despite their great abundance, only a small
segment of the seiiorita population seems pre-
disposed to clean at a given time. The cleaning
habit is not limited to any particular stage in
their life history: cleaning senoritas have in-
cluded some of the smallest individuals seen
(< 40 mm) as well as some of the largest
(> 225 mm). In cleaning material from the
bodies of fishes, senoritas employ the same pick-
ing technique they use to take small prey from
a rock or algal substrate. This mode of feeding,
along with their pointed snout and long, for-
ward-projecting canine teeth, are well suited to
the cleaning habit.

Individuals that clean are numerous where
there are many resident fishes, especially of
certain species (as discussed below) , but I found
no evidence that residents of other areas come
to these locations to have parasites removed.
Occasionally a migrating species, such as the
California yellowtail, Seriola dorsalis, will pause
to be cleaned while passing through areas where
cleaners are active, but this is not the same as
a resident of a particular area habitually swim-
ming elsewhere to be cleaned and then returning
to its home ground.

Fishes Cleaned by the Senorita

Casual observation alone show that some fish
species are cleaned far more often than others,
and that many species do not seem to interact
with cleaners at all.

To obtain data on this point, a record was kept
of the species seen being cleaned by senoritas
during 62 observation periods (15 min to 2 hr
long) from June 1968 to January 1969. During
this period, 392 cleaning bouts were witnessed,
385 of which involved senoritas cleaning one or
more individuals of a single species; in only

seven instances were senoritas seen cleaning
members of a mixed-species group. The tabu-
lation of species cleaned (Table 1) does not in-
clude the mixed-species groups because in the
mixed groups it was not determined whether
representatives of all species present were ac-
tually cleaned. All seven mixed groups included
halfmoons, Medialuna calif orniensis, and one or
more fish of other species. In four of these,
halfmoons were mixed with blacksmiths, in one
they were mixed with opaleyes (Girella nigric-
ans), in one with rubberlip perch {Rhacochilus
toxotes), and in one with both rubberlip perch
and pile perch. All of these were incidental
observations. The compilation does not include
data obtained on other occasions when the ac-
tivity of individual cleaners was recorded for
extended periods.

The data clearly indicate that blacksmiths, and
to a lesser extent topsmelt (Atherinops af finis) ,
predominate as recipients of the senorita's clean-
ing efforts in the areas where the observations
were made. Table 1 is not a definitive list of
species cleaned by the senorita ; nevertheless, it
is evident that many species which co-occur with
the senorita are not cleaned. At other times,
in addition to all species noted in Table 1, 1 have
seen Seriola dorsalis and Trachurus symmet-
j'icus being cleaned. But the ratio of species
listed here generally is consistent with observa-
tions made on other occasions and at many dif-
ferent locations.

Table 1. — Fishes observed being cleaned by senoritas
during 62 observation periods betvi'een June 1968 and
January 1969 at La JoUa, Calif, (exclusive of seven
mixed-species groups).

Species

Number

of

cleaning bouts

Percent of

total bouts

observed

Blacksmith, Chromis pitnctipinnis

231

60

Topsmelt, Athcrinop! ajfmis

31

21

Goriboldi, Ilypsypopi rubicunda

22

6

Halfmoon, Medialuna calijornunsis

19

S

Senorita, Oxyjulis catilornica

10

3

Rubberlip perch, Rhacochilus toxotei

8

2

Opaleye, Circlla nisriiani

5

Kelpfish, HcUroslichul roslralus

3

Black perch, Emhiotoca jackioni

1

Pile perch, Rhacochilus vacca

1

Sorgo, Amsotremus davidsoni

1

Blue rockfish, Scbasles mystinus

1

Olive rockfish, Sebastcs scrranoidcs

'

497

FISHERY BULLETIN: VOL 69, NO. 3

Reports in the literature present a comparable
picture. Most published accounts of cleaning by
seiioritas describe the way blacksmiths cluster
around this cleaner to solicit its attentions (Lim-
baugh, 1955, 1961; Feder, 1966; and others).
Limbaugh (1955) observed the following fish
being cleaned by seiioritas: Myliohatis califor-
nica, Stereolepis gigas, Paralahrax clathratus,
Trachurus symmetriciis, Atherinops affinis,
Anisotremtis davidsoni, Hyperprosopon argen-
teum, Rfiacochilus vacca, Chromis punctipinnis,
Hypsypops nibicunda, Girella nigricans, Medi-
aluna californiensis, and Mola mola. Turner et
al. (1969) observed the following fish being
cleaned by seiioritas: Sebastes spp., Atherinops
affinis, Atherinopsis californiensis, Trachunis
symmetriciis, Seriola dorsalis, Chromis ptinctip-
innis, and Mola mola. Neither of these reports
gives data on the relative frequency with which
these different species were cleaned, but it is
significant that many of the same species con-
sistently appear in the reports of independent
observers, while at the same time many other
species that frequent these waters in large num-
bers are not mentioned. No doubt many species
not yet reported are occasionally cleaned by
seiioritas, but there seems little doubt that a
certain few species, the blacksmith in particular,
predominate in this activity.

Specific Cleaning Interactions

The fishes cleaned by the seiiorita vary mark-
edly in their habits and habitat, as well as in
their relative numbers. These fishes do not seek
out cleaning at a "station" established by the
seiiorita, but rather i-eceive the seiiorita on their
own grounds during the course of their regular
activity. Cleaning interactions often proceed
diff'erently with one of these species than with
another. Some of these variations in cleaning
activity are characterized below.

Senorita-blacksmith interactions. — The black-
smith is one of the most abundant fish over rocky
substrates in Califoi-nia inshore waters, where
it swims in large stationary aggregations in mid-
water. It feeds largely on zooplankton (Quast,
1968) and attains a length of about 250 mm.

Generally the first sign of an interaction oc-
curs when a seiiorita swims up alongside a black-
smith in midwater and closely inspects its body.
The blacksmith may then immediately stop swim-
ming and, holding its fins motionless and erect,
drift into an awkward-appearing posture. Usu-
ally the blacksmith is head-down, but sometimes
turns on its sides or is tail-down. On some occa-
sions the blacksmith presents a particular part
of its body to the inspecting seiiorita. The seii-
orita swims about this fish, usually pausing
briefly to pick at its body. Immediately follow-
ing the first sign of this activity other black-
smiths converge on the spot, so that very quickly
10 or more crowd around the cleaner (Figure 4) .
The seiiorita soon leaves the original blacksmith
and may then move on to one of the others. It
may also swim slowly away, whereupon the
group of blacksmiths follows along, each attempt-
ing to position itself in the seiiorita's path. Al-
though the seiiorita shows progressively less in-
terest in the blacksmiths, they continue to crowd
in its way. Soon the seiiorita shows no further
interest in cleaning, and all but a few black-
smiths leave the group. The remaining few
doggedly continue attempting to present them-
selves to the now-unresponsive cleaner. Even-
tually, however, these last blacksmiths lose con-
tact with the cleaner as it swims off" among the
kelp or the many other seiioritas in the sur-
rounding water. Once they have lost contact
with the cleaner the blacksmiths do not attempt
to solicit cleaning from any of the many other
seiioritas around them.

On only two occasions did I note blacksmiths
soliciting cleaning from a seiiorita that did not
seem to have made an initiating gesture. Once
the blacksmiths were very small, about 40 mm
long, and in the other observation, at a depth
of 27 m, little cleaning had been seen and rela-
tively few seiioritas were present. However,
in both instances the seiioritas were known by
me on the basis of earlier observations to be
individuals that clean. It is possible that the
fishes soliciting attention recognized these seii-
oritas as cleaners through some cue not noted
by me. Sometimes when a seiiorita incidentally
passes close to a blacksmith, the blacksmith no-
ticeably pauses in its swimming and looks as

498

HOBSON: CLEANING SYMBIOSIS

Figure 4. — Senorita cleaning the caudal peduncle of one of a group of blacksmiths that

hover to solicit service.

though it is beginning to assume a soliciting
posture; however, when the seiiorita swims on
past, the blacksmith immediately resumes its
original activity. Occasionally members of other
species were seen responding similarly to passing
seiioritas. In most observations of cleaning, my
attention was drawn to activity already in prog-
ress, so that it was not possible to determine
whether cleaner or client had initiated the ac-
tivity.

Individual seiioritas that cleaned blacksmiths
during many short-term observations were not
seen cleaning any other species. This same
situation held true for three individuals, known
to have been cleaning blacksmiths, whose ac-
tivity was monitored in detail on tape for 15
min. When observed for extended periods,
seiioritas were found to become involved in
a succession of separate cleaning bouts. This
activity was not restricted to one location but
continued at various points over a relatively
wide area. Periodically they joined cleaning al-
ready underway, or initiated cleaning themselves

at a number of different locations — always with
blacksmiths. I have no explanation for the fact
that a sefiorita which becomes unresponsive and
leaves one group of blacksmiths that still vigor-
ously solicits its service may soon initiate ac-
tivity again with another blacksmith.

The three individuals whose cleaning activity
was monitored for 15 min joined in a mean of
4 separate bouts (range 2-6) . For a mean of 11
min of this time (range 6.75-13.25 min) they
showed an apparent cleaning interest in black-
smiths, or were accompanied by blacksmiths with
which they had earlier initiated a cleaning inter-
action. When not thus engaged with black-
smiths, they swam in midwater showing no
apparent interest in the fishes around them but
occasionally picked at drifting scraps of debris,
usually algal fragments. During much of the
time that they swam in consort with blacksmiths,
they closely inspected these fish and actually
picked at their bodies a mean of 26 times (range
14-33). Of these picks, 27 9^ were made at the
base of the blacksmith's anal fin, 25% on the

499

MSIM.RV imi.l,l',IlN: vol. l,'l, NO. 3

c.'iuil.il iicdiinclc ())• <Miiilal (in, 22/^ at the base of
the pi'cloral lin, !()'< somewhere on Ifie body
oxclu.sive of ii (iii-ha.se or head, K'^ on the head,
5% at the bust' of I lie pelvic (in.i, and )'.'; .al I he
l)aHO of the dorsal (in.

(Dearly, tlie bases of the (ins (-(^cteive rno:-.( of
(he .■illenlioii ffoni the seiioritas. 'I'hese data
ai(! (;on:;isLeiil with the niatiy more k<'I"''"iI "b-
Hei'vations mHd(! on other occasions. At no time
dnrinj^ this study were senoritas seen to elean
within the or.al or branchial cavities of black
smitlis: ail cleanin)'; w;is dii-ected .'d the liody
snrf.'ice.

Si'iiorila-lDiisiiicll i III (■ nirl !<iiin.- The top-
smelt, which .attains a leiiKlh of .about 200 mm, is
abnnd.inl in ni.aiiy inshoi'e rcKions of Californi.-i
coastal waters, but its flistribution is more spotty
tlian th.at of IIk! ubi(iuitous i)lacksmith. Like
till" blacksmith, it feeds larccly on zoopl.ankton,
whicli it lakes while swinuiiiiiK in larjve schools
at the watcr'.s surface. (Juast ( IIXJK) noted the
simil.arity in dii-l between bipsmelt and bl.ick-
smitlis, and while acknowN-dcinj': th.at (lu'ir feed-
in)C .'irc'is m;iy oM'rl:ip. he puinlcd dut tli.it (op
•smelt norm.ally swim liic.her- in the w.atcr colimm.

In the l,;i ,b)lla study area, topsmelt ;ire con
centr.aled .'it the inshore station over exti^nsive
lields (d' Mirfivr.'e;;; th.al >'.row in I', to ,'"> m of
wat<'r. 'I'liey .'ire nevei' far from the substi'.ate
in this relatively sh.allow water, even thou).','h
they swim in lar^e schools .at the widcr's sur-
face. They are more abund.ant th.an blacksmiths
in this area, and iier(> tiiey predomin.ate in the
sehorita's cleaning activity.

The cleaning'' inter.aclion proceeds in much the
same w.ay as it does with bl.acksmilhs: the ;ic-
tivit.v is iiiili.ated when ;i sehorila swims up \n
.an individu.al topsmelt .and begins b) inspect it
closely, immedi.alely other lopsmell converge
on this p.air to |)lace themselves in the sehorita's
p.alh, thus soliciliniv its .Mtteidion. When pre-
sentinjv themselves nuitionless before seiiorit;is,
topsmelt fre(|ueidly hover l.ail-down, in coidr.ast
to the head-down posture most often assumed
by l)l.acksmiths. I s.aw .sehorit.as cle;iii iinl\- the
external i)o<iy surf.ices of topsmelt. In the rel-
atively shallow water where most of this activity
was observed, sehorit.as bicak o(I' coiit.act with a

Ijroup of lopsmell nioi'e re.adily tli.an they do
with blacksndths, as they need otdy swim down
to the silbsli'ate below, where the topsmelt seem
ri'liict.anl to follow.

These sli;illow ;ir<'as are fre(|uently swept by
.•;ur;-',(', and the lo.ad id' driftinj^' d(!bris in mid-
wat<a' is fre<|ueii1ly heavy. In this area ele.anin)^
senoril.as freiiiienlly leave the j,rrou|)s of topsmelt
they an; atlendin;', to inspect an object driftiuK'
in the water nearby. Sometimes they take the
objec't into their moutfis, sometimes not. Often
w lien (;ikeri it is (|uickly I'ejected.

Attempts at extended observations on individ-
ual senoritas th;il had been clcanintf topsmelt
were largely nnsucce.ssfid. Too often before; the
observ.ation li.ad proj.;r(;ssed far the senoritas
dis.ippe.ired amoiijj the surfjjfrass or other vege-
tation carpeting the .se.a dooi' in this .are.a. How-
ever, two individuals were followed for 10 nnn
e.ich, durinjv which time one; entered irdo four,
the other two, separate cleanin;; bouts. I'etwccn
cli'.inin;^ bouts these two swam over a wile area
.alone in nndwatcr, occasionally |)ickinK a' drift-
in)'; debris. On several occasions they picked at
liciithii' .iljrae. Neilhei' individual showed clean-
ing interest in species other than topsmelt, which
was consist(;nt with observations of other sen-
oril.as lh:il cK'.'ineil topsmelt.

Sciiiirilii-fid rihdiili i II I r rii !■ I ill ii s .■ — The K'ari-
b.aldi, which attains .a length of about ^.SO mm,
is a solitaiy, hi^rhly territori.al (ish that lives
clo.se to tli(> substrate. lOspeci.ally during' the re-
product ive season, when the males aKJrressively
j'.ii.ird their nests anions' the rocks, these bright
oi'anK'e jiom.acentrids norm.ally drive away .all
other (ish Ih.at come ne.ai'. They feed on sessile
bciilliic inx'ertebr.ates .and .are .abunil.ant .at the
.'i- to lO-m station.

(I.arib.aldis fre(|Ueidly .are cleaned by senoritas.
Most of the K'.arib.aldis seen bein^' cleaned were
swinmiinj;' .a metei' or so .above the bottom; I
(til not iibser\-e cleaners .act i\e around the pari-
b.aldis K'l.ardinK' nests amon^ the rocks. All of
the M'.'iiab.aldis seen beiuK cleaned were solit.ary,
which redects their territori.al n.itnre. The sen-
(uit.i swims up to a K'arib.aldi .and closely inspects
its body, thus initiating: the action. Usually the
jv.arib.'ildi lioNcrs motionless in -a norm.d liori-

500

MOIISON: Cl.KANlNc; SYMHIOSIS

/.(iiilal •■illiludc, its liiis soiiiclimcs cfccl. 'I'lir
senorila may pick at a few places on llu' jiari-
haidi's body — most often around the caudal re-
Pfion— -hut usually its attentions are brief, and
soon it swims away. With l)lacksmiths and top-
smelt, each cleaninji' bout is pi-olonn'cd by the
many other individuals that join at the cleaning
site to crowd in tiie senorita's path. Nothing of
this sort hapiiens with the solit;iry garibaldi,
which usually makes no attom|)l to follow the
senorita when it Icaxcs, so that each cIc^aninK'
bout is relatively brief. After leavin^f one pari-
baldi, how(!ver, often IIh' senorita (|uickly ap-
proaches another. In agreement with their
cleaninji; of blacksmiths and topsmelt, senoritas
known to have cleaned jjaribakiis were subs(!-
quently seen cleaning: only other members of that
same species. This was true durinjif sevei'al
short-tei'm observations, and also when one in-
dividual WHS followed foi- 1.^) min, ;u:d a record
of its activity was taped; this particulai' senori1;i
initiated cleaniri^ activity witii 2(i ditferent gari-
baldis durinjr the observation period as it swam
over an irregular cour.se amonjf the rocks in an
area where blacksmiths, topsmelt, anti other spe-
cies also were present. Kach cleaninK bout lasted
a mean of IOs(^c (raii^e 7-25 sec) , lolaliuK 'I min
15 sec of the 15-min period. In nine of these
bouts, th(! senorita inspected tli(! garibaldi liut
did not pick at its body. In the other 17 bouts,
the senorita picked at the ^Jiribaldi's body a
total of 42 times, or a mean of about 2.5 times
per bout.

All cleaninK of K'ai'ibaldi that I observed was
directed at the external body surface.

ScnoriUi-halfmooii inlrracl Johk. — Half moons,
which may exceed a length of 250 mm, usually
swim hijrh in the water column, fre(|uently in
lar^e aKKrej^ations, but just as often in small
Kroui)S or as solitary individuals. They are often
abundant amonj,' risinjr .stands of jfiant kclj).
Th(Mr omnivf)rous diet, which includes a variety
of benthic al^ae, alon>; with bryozoans, sponges,
and crustaceans (I^imbauKh, l955;Quast, 1908),
indicates bottom feeding; however, much of thi.s
material is taken in midwater as drifting debris.

donsiderinj,' their larpe numbers in many
s()uth('rn (California coastal areas, halfmoons are

not, p;ii'ticul;irly abund.inl in the principal study
areas. .Still, they were fre(|uently seen bein^'
cleaned by senoiit.'is dur'in;^ this study. When
iii.iny halftnoons were present, cleaninK hy the;
senorita progressed much as described above; for
blacksmiths. Yet when just one halfmoon was
present, a fre(|U(!nt occurrence, the cleaning:
bouts were brief like tho.se described above for
the ffaribaldi. At k^ast one halfmoon was i)res-
ent in all the mixed-species groups that I re-
corded when collectinji the data [X'esented in
Tabic 1. I .saw seiioritas clean only the external
body surface of halfmoons.

One scMloi-ita, seen cleaning a halfmoon. was
kept under surveillance for 12 min before con-
tact was lost. As the observation period began,
the senorita picked at the halfmoon once and
th(ni moved away, swinnniuK slowly and alone,
2 or :] m over the sub.strate. After an uiuivent-
ful :'. niin, the senorita api)roached a second h.df
moon, which promptly hovered in a head-down
jitlitudc. l''or !.'"> sec the senorita clox'ly in-
sp<!ct(Hl this halfmoon and picked at its body
three times before swimminj": away. It then
continued on alone for the remaining 8-( min
that it was under obsersation, still swimminj.r
slowly over a wide semicircular course 2 or U m
above the rocks. During this time it pa.s.sed
many different (ish without showing interest,
but it did not pa.ss another halfmoon. It did
pick at thr(K! did'eixnit pieces of floatinj^ debris
but rejected all three immediately.

Si'vorHfi-senoritd hitcraclioiis. Scuor'dnH
themselves are cleaned by other members of
their own species. Despite the large numbers
of .senoritas that usually are present, I saw no
groups converging on cleaning individuals, as
regularly occurs with blacksmiths, topsmelt, and
other abundant species. In most of the .seno-
rita's intraspecific cleaning interactions, the
cleanei- attends just a single individual, which
usually hovers motionless in a normal horizontal
attitude!, <!xc(!pt that its fins are erected; some-
times the mouth is opciii wide and gill covers
are distended, but I saw senoritas clean only
the external body surface of these fish. There
was no indication that senoritas which clean
other senoritas ;dso clean othei' species. I fol-

501

FISHERY BULLETIN: VOL. 69. NO. 3

lowed one individual for 10 min after having
seen it clean another seiiorita. After this ini-
tial activity, the individual under surveillance
swam over a wide area, showing interest only
in other senoritas, even though blacksmiths, top-
smelt, and other species were present. Swim-
ming alone, 2 or 3 m over the rocks, it would
assume a position alongside another seiiorita and
follow it for a short distance. Usually these
other fish showed no interest, but some stopped
swimming and erected their fins, whereupon the
cleaner picked at their bodies — usually once, but
occasionally several times. Between cleaning
encounters this seiiorita passed through a school
of very small (< 40 mm) blacksmiths, several
of which hovered head-down in its path; how-
ever, the cleaner showed no interest in these fish.
On two occasions it picked at a piece of drifting
debris.

Senorita-kelpfish interactions. — At least one
species regularly initiates cleaning bouts with
senoritas. Earlier (Hobson, 1965a) I reported
observing a kelpfish, Heterostichus rostratus,
repeatedly soliciting cleaning from unresponsive
senoritas. The kelpfish was concealed among
benthic algae, which is the typical habitat of this
fish. But each time a seiiorita approached in
the water overhead, the kelpfish rose up into
the senorita's path, where it hovered motionless,
fins erect (Figure 5) . A succession of senoritas

Figure 5. — Kelpfish hovering in midwater, fins erect,
to solicit cleaning from a passing seiiorita.

passed by without responding to the kelpfish, and
each time the kelpfish returned to the cover be-
low, where it waited until the next approach.
Finally a passing seiiorita paused briefly and
picked at the kelpfish's side before continuing on
its way. After this brief encounter, the kelp-
fish did not rise from concealment again even
though several more seiioritas subsequently
passed overhead.

During the present study this sequence of
events involving kelpfish and senoritas was wit-
nessed several times at a variety of locations;
indeed, every instance of a kelpfish being cleaned
followed this pattern — obviously it is a regular
pattern in the behavior of the species.

Other interactions — Observations are too few
to recognize distinctive aspects in cleaning in-
teractions involving the many other species that
occasionally are cleaned by seiioritas. Usually
such activity is noted simply as occasional sight-
ings of small clusters of fish, or individual fish,
hovering before a seiiorita. In all such en-
counters, however, only the external body surface
was cleaned.

Notes follow regarding two other species that
are cleaned by senoritas.

A single sehorita was observed cleaning a pile
perch, after which its activity was noted for
15 min. Pile perch are not abundant where these
observations were made, and after leaving the
first individual, the seiiorita swam alone in mid-
water for 14 min. It moved over a wide semi-
circular course during this time and showed no
interest in any of the many fish that it passed,
although none were pile perch. It did pick at
three small items drifting in midwater. After
14 min it made an abrupt course change and,
with slightly accelerated swimming, went di-
rectly to a solitary pile perch that was in mid-
water about 10 m away. The seiiorita swam
about the pile perch, which now hovered head-
down, but after a close inspection lasting about
10 sec it moved on without picking at the pile
perch's body.

Many of the fishes cleaned by seiioritas occa-
sionally start, as if nipped too vigorously. Some-
times such fish dart away, thus terminating the
cleaning. Other times they actively turn on the

502

HOBSON: CLEANING SYMBIOSIS

seiiorita and drive it away. The rubberlip perch
was noted taking the latter course of action per-
haps more often than the other species, even
considering the relatively few times it was ob-
served being cleaned.

Although the kelpfish is the only species that
was observed consistently initiating cleaning
from seiioritas, individuals of several species do
so in at least one situation. This occurs where
exceptionally large concentrations of senoritas,
sometimes thousands, swim above the rocks.
At various times, garibaldis, pile perch, rubbei'-
lip perch, olive rockfish, and others were ob-
served hovering in the soliciting posture amid
these concentrations (Figure (5) until one of the
senoritas approached and cleaned them.

Material Removed from Other Fishes by
the Senorita

Food habits of cleaning senoritas. — An obvi-
ous question is: What do seiioritas remove from
the bodies of fishes they clean? Limbaugh
(19.55) stated that senoritas remove bacteria.

parasitic copepods, and isopods. He was not
more si)ecific than this, nor did he present data.
Various other cleaners reportedly take not only
ectoparasites but also diseased and neci'otic tis-
sue (Feder, 1966, and others.)

To determine just what it is that sefioritas
remove from the bodies of other fishes, I ex-
amined the gut contents of 27 specimens. 111 to
175 mm long, that were speared while they were
cleaning other fishes. Food items in their guts,
ranked as percentage of each item in the entire
sample, were as follows: caligid copepods, 39% ;
gnathiid isopod larvae, 12 S' ; algae with en-
crusting bryozoans, 10 /r ; caprellid amphipods,
5',t ; fish scales, iVr; and fragments of nonpar-
asitic crustaceans, 4',i . Unidentified material
made up 26 "^r of the sample. Of the 27 speci-
mens, ectoparasites occurred among the gut con-
tents of all but two. In most, the ectoparasites
predominated. Even though the data are con-
vincing, they do not fully reflect the extent to
which cleaning oliviously dominated the activity
of these particular fish for at least several hours
leading u]) to their capture. This is because the

Figure 6. — Garibaldi hovering amid a large assemblage of senoritas.

503

FISHERY BL'LLKTIN: VOL 69, NO- 3

parasites are so small (1-3 mm long) in com-
parison with the size of other food items. For
example, 471 gnathiid isopod larvae were present
in one seiiorita gut, but being so small they con-
stituted only 35V' of the material. On the other
hand, a few algal fragments, with encrusting
bryozoans, made up AOV of the material in this
same specimen. However, only seven individ-
uals contained ectoparasites alone, as compared
with 17 that contained both parasites and free-
living prey. In all but one of these, the two
classes of material were sharjily divided in the
gut, usually with the free-living material poster-
iorly in a more advanced stage of digestion. Al-
though most of the ectoparasites in the gut had
undergone extensive damage and would not, by
themselves, have been identifiable to species, this
material usually graded gradually to freshly in-
gested specimens that were readily identified.
This fact, coupled with the circumstance that in-
dividual seiioritas tend to stay pretty much with
a single type of food organism during a given
period, greatly aided the task of analyzing this
material.

Ectoparasites on the fishes. — To assess the sig-
nificance of cleaning in removing ectoparasites,
one must know what parasites occur on the fishes,
as well as the extent of the infestation. Thus
the survey of ectoparasites done in conjunction
with this work included essentially every fish
species exceeding 100 mm long regularly present
in the La Jolla study area, as well as every spe-
cies that was seen being cleaned there. Ecto-
])arasites infesting these fishes include 33 spe-
cies of copepods, one species of brachiuran, two
species of isopods, one species of leech, and one
species of monogenetic trematode. Following is
a brief summary of the information being com-
piled on these parasites in collaboration with R.
F. Cressey.

Copepods are the predominant ectoparasites
on fishes in this area. The 33 species represent
seven families: Bomolochidae (6 species),
Caligidae (13 species), Dichelesthiidae (2 spe-
cies), Lernaeidae (1 species), Chondracanthidae
(5 species) , and Lerneopodidae (6 species) . The
one species of the closely related brachiurans is
a member of the family Argulidae. The bomolo-

chids, which were found on 12 species of the
fishes sampled, are mobile forms about 2 mm
long (all lengths of parasites here and below do
not include egg cases) that occurred mostly on
the gills of their hosts. The caligids, which in-
fested 29 species of the fishes, are mobile forms,
2 to 4 mm long, that occurred mostly on the ex-
ternal body surface of their hosts, although two
species were found only in the oral cavity. The
dichelesthiids are highly modified forms about
2 mm long that were attached to the gills of two
species. The lernaeid is a highly modified form
about 5 mm long that was attached to the fins
of 12 species. The chondracanthids, which in-
fested five species, are highly modified forms, 3 or
4 mm long, that lived attached in the branchial
chamber, including the gills, of their hosts. The
lerneopodids, infesting eight of the fish species,
are highly modified forms, 2 to 5 mm long, mostly
living attached in the branchial and oral cavities,
although one individual fish carried several at-
tached to its dorsal fin. Finally, the argulid
is a mobile form about 2 mm long that was found
on the outer body surface of one species of fish.
The fish species hosting representatives of the
different copepod and brachiuran families are
listed in Table 2, and examples of the six copepod
families are illustrated in Figure 7.

Thus a variety of ectoparasitic copepods occur
on the fishes, but only caligids were found among
the gut contents of the cleaners. Further-
more, although 13 species of caligids (five spe-
cies of the genus Caligus and eight species of
the genus Lepeoiihtheirus) occur on fishes in this
area, only a relatively few of these are significant
as prey of the cleaners, as noted below.

Of the two isopods, one, Livoneca vulgaris, a
large parasite, about 20 mm long, was found in
the branchial chamber of just one species of fish
and was not found to be jirey of the cleaners.
On the other hand, the highly mobile gnathiid
larvae (Figure 8), which are about 2 mm long,
are a major prey of the cleaners. Only one form
of gnathiid was readily recognized, but more
than one species may occur among this material.
Parasites of the body surface of fishes, the gnath-
iid larvae were taken on 11 of the fish species
sampled, l)ut I suspect that they are actually
more widespread and abundant than these data

504

HOBSON: CLEANING SYMBIOSIS

Table 2. — The types of ectoparasites and the fishes they infest, based on a survey of the fishes in the study area.
Where more than one species of parasites is included under a heading, the number in parentheses following
the name of each fish thereunder indicates how many different species of that type are represented on that
fish. For all fish species listed, the number of infested individuals is shown over the number of individuals ex-
amined, followed by the range in numbers of individual parasites of that type which were taken from that species
of fish.

COPEPODS

BOMOLOCHIDAE (6 species of 3 genera)
Fishes infested with members of

this family:
PaTnlakrax dalhralus (t) 2/8: 1-2
P. nrkuliirr (2) 5/11: 1-20
Phanrrodon atripri (1) 1/13: 1
Rhacockilul vacca (1) 3/15: 1
M\iTom£trus minimus (1) 1/7: 1
Hypsypopi rubiiunda (1) 1/20: 1
ScoTpaena guttata (I) 6/14: 2-56
Srbastes myslinus (1) 1/9: 1
S. strrantndts (1) 2/11: 1-8
Uxyltbiui pictus (1) 1/8: 1
Athrrinopi aginis (1) 2/13: 1-4
Pleuronichlhys cornosus (1) 6/10: 1-11

CALIGIDAE (13 species of 2 genera)
Fishes infestecf with members of

this family;
Paralabrax clathratus (2) 4/8: 1-5
P. nrbuliln (3) 4/11: 5-27
Caulolatilus prirufpl (1) 1/4: 2
jintiolrfmus davidsoni (1) 1/8: 1
Chfitotrrma saturnum (I) 2/16: 1
MrdMuna calilarnwniii (2) 12/13; 1-75
Cirrlla ntgricam (3) l/IO; 1-14
Embiotoca ;actiom (2) 2/15; 1-2
Phanerodon atripts (1) 5/13: 1-5
Rhatothilu! toxotr, (3) 10/10: 1-IQ
R vacca (2) 4/15; 1-11
CKromii pitnctipinnis (I) 10/10; 2-39
Hypiypopi rubiitinda (2) 19/20: 1-144
Pimeiomctopon puUhrum (3) 13/14: 1-70
OxyiMs califorixra (3) 13/38; 1-59
Scorpafna guttata (1) 7/14: 1-14
Sebaites atrovirent (3) 6/16; 1
S. carnata, (2) 3/11: I
S, chryiomehi (1) 1/7: 1
S. conitrllatus (1) 2/2: 1-5
S. mmiatus (I) 1/5: 2
S. myitinici (3) 5/9: 1-5
S. pauciipimi (I) 3/3; 1
S. nrranoidt! (3) 8/11: MO
S. srrricrps (2) 15/15: 1-25
Scorpaenichtkyt marmoratui (2) 8/10: 1-42
Heteroitichui mstratus (1) 2/13; 1-2

COPEPODS-Cont.
CALIGIDAE-Cont.
Athirinops aljinis (1) 13/13: 1-23
Pleuronichthys toenasu! (1) 5/10: 1-5

DICHELESTHIIDAE (2 species of 1 genus)
Fishes infested with parasites

of this fomily;
Gymnothorax mordax (1) 1/1: 9
Paralabrax nibuhlcr (1) 5/11; 2-70

LERNAEIDAE (1 species)

Fishes infested by this porosite:
Trachurus symmetricus (1) 1/7; 1
Aniiotrcmus davidsoni (1) 1/8: 1
Ckeilolrema saturniim (1) 2/16; 1-2
Mrdialutta calilorniensis (1) 5/13: 2-7
Brachyiiliui Irenatui (1) 1/5; 1
Embiotoca lackwni (1) 2/15: 1-2
Hypsur^us caryi (1) 2/11: 1-2
Phancrodon iurcalus (I) 3/12; 1-3
Rhacockilus toxotts (1) 1/10; 1
R. vacca (1) 2/15; 1
Micrometrus munmui (I) 5/7; 1-6
.llhcrinops affimi (I) 2/13: 1-4

CHONDRACANTHIDAE (5 species of 5 genera)
Fishes infested with parasites of

this family:
Oxyjulis calijoritua (1) 13/38; 1-4
Scorpaena guttata (1) 2/14: 1-5
Scorpaenichthys marmoratus (I) 4/10; 1-4
Hrtrrosltchui roitratiu (1) 7/13: 1-7
PIrurortuhthys coenoli,, (1) 7/10: 1-47

LERNEOPODIDAE (6 species of 4 genera)

Fishes infested by parasites of
this family:

Cheilotrema ialuriium (1) 1/16: 1

Girrlla nigricans (1) 1/10: 1

Phancrodon atnpcs (I) 5/13: 1-4

Rhacochilus vacca (1) 1/15: 1

Chromis punctipinnis (1) 1/10: 1

Scbastcs atrovirfns (1) 1/16: 4

S, constellates (1) 1/2: 1

S minialus (1) 5/5; 2-8
ARGULIDAE (1 species)

Fish infested with this parasite:

.itkcrinopsis calijornicnsts l/I; 2

ISOPODS
CYMOTHOIDAE (1 species)

Fish infested with this parasite:
Scbastcs mystinus 1/9: 1

GNATHIID LARVAE (number of species not
determined)
Fishes infested with these parasites:
Chromis punctipinnis 1/10: 1
Hypsypops rubicunda 4/20: 1-8
Pimclomctopon pnlchrum 3/14; 1-4
Scbastcs atrovircns 4/16: 1-20
S, carnatus 3/11: 1
S. chrysomclas 1/11: 2
S. constcllatus 1/2: 1
S. scrranoidcs 1/11; 1
S. scrriccps 3/15: 1-5
Oxylcbiu! pictus 3/8: 1-3
Scorpaenichthys marmoratus 3/10; 2-5

MONOGENETIC TREMATODE (1 species)
Fishes infested with this parasite;
Medialuna calijornicnsis 6/13: 2-16
Girclla nigricans 4/10: 1-4
Rhacockilus toxotes 2/10: 1
R. vacca 2/15: 1-18
Hypsypopi rubicunda 1/20: 1
Pimclomctopon pulchrum 10/14: 1-26
Scorpaena guttata 2/14: 5-8
Scbastcs atrovircns 7/16; 1
S. constcllatus 1/2: 1
S. minidtus 2/5; 1-2
S. scrranoidcs 3/11: 1 -26
S. scrriccps 2/15; 1-3
Hctcrostichus roslratus 6/13; 1-7

LEECH (1 species)

Fishes infested with this parasite:
Hypsypops rubicunda 2/20: 1
Scbastcs scrranoidcs l/Il: 4
Hctcrostichus rostralus 2/13; 1-2

FISHES ON WHICH NO PARASITES WERE
FOUND:
Xcnistius calijornicnsis 0/1
Halickocrcs scmicinctus 0/10
Coryphoptcrus nicholsi 0/5

indicate. They are the most mobile of the par-
asites, and probably many escaped when their
host fish was collected. The monogenetic trem-
atode occurred on the outer body surface of 13
species of fishes, and the leech occurred simi-
larly on 3 species. However, neither was found
to be taken by the cleaners. The fish species
hosting the various isopods and also the trema-
tode and leech are listed in Table 2. Listed also
are the three fish-species on which no ectopara-
sites were found.

The above summary of the survey results gives
a general picture of the ectoparasites infesting
the fishes that co-occur with the cleaners and
might be regarded as a list of the potential prey
of the cleaning fishes. The following material
considers the parasites that actually are known
to be ]3rey.

Ectoparasites in the diet of cleaners relative
to ectoparasites on fishes that are clearied. —
Many of the ectoparasites listed above infest

505

FISHERY BUI.LEXrN: VOL, 69. NO. 3

V

V

Figure 7. — Representatives of the families of ectoparasitic copepods found to infest fishes in
the La Jolla area.

A. Bomolochidae (Bomolochus longicaivdiix, female, after Cressey, 1969b) ;

B. Caligidae (Caligus hobsoni, male, after Cressey, 1969a) ;

C. Dichelesthiidae (Hatschckia pacifica, female, after Cressey, 1970) ;

D. Lernaeidae {Peiiiciilus fiss>!>es, female, after Wilson, 1917) ;

E. Chondracanthidae (Chondracanthas gracilis, female, modified after Wilson, 1935) ;

F. Lerneopodidae {Kpibrnnchiella septicaudn, female, after Shiino, 1956).

J06

HOBSON: CLEANING SYMBIOSIS

?»<^'

«'

Figure 8.— Gnathiid larva from the body surface of the
black-and-yellow rockfish, Sebastes chrysomelas.

fishes that rarely or never interact with cleaners.
In considering the ectoparasites found in the gut
of particular senoritas, it would be most mean-
ingful to do so in regard to the ectoparasites
known to be hosted by the species of fishes that
these ]5articular senoritas were cleaning when
collected. Of the 27 cleaning senoritas taken
for the gut-content analysis, 15 (SG'^f) were
cleaning blacksmiths, 8 (SO":;) were cleaning
topsmelt, 2 {T"r ) were cleaning garibaldis, and
2 (1^/r) were cleaning halfmoons. Thus the
selection closely parallels the relative frequency
with which sefioritas were observed cleaning
these same species (Table 1) and is a good sample
of the fishes that are cleaned by senoritas.

Three species of ectoparasites were collected
from 10 blacksmiths, 141 to 199 mm long. Each
of these blacksmiths carried from 2 to 39 indi-
viduals of the copepod Caligus hobsoni on their
body surface. One specimen also carried a single
gnathiid isopod larva on its body surface, and
another the copepod Clavellopsis flexicurvica on
a gill arch. All 15 senoritas that were collected
as they cleaned blacksmiths contained either
Caligus hobsoni or gnathiid larvae, but no other
ectoparasites: one contained gnathiids alone,
seven contained C. hobsoni alone, and seven con-
tained both gnathiids and C. hobsorii. Up to 256
individuals of C. hobsoni and up to 263 gnathiid
larvae were counted from among the stomach
contents of individual seiioritas that had been
cleaning blacksmiths.

Three species of ectoparasites were collected
from 13 topsmelt, 122 to 212 mm long. These

topsmelt each carried from 1 to 23 specimens
of the copepod Caliyus sermtns on their body
surface. Two topsmelt also carried the copepod
Parabomolochus constrictus on their gills, a
single parasite on one, four on the other. Two
topsmelt also carried the copepod Peniculus
fissipes embedded in their fins. Six of the eight
seiioritas that had been cleaning topsmelt when
collected had ectoparasites among their gut con-
tents. Five contained only Caligus serratns —
as many as 73 in each fish. One other contained
only 10 gnathiid larvae, a parasite that was not
seen on the topsmelt themselves; however, as
noted above, I suspect that this parasite is more
widespread than our survey data indicate.

Six species of ectoparasites were collected
from 20 garibaldis, 184 to 240 mm long. Nine-
teen garibaldis each carried 1 to 144 Caligus hob-
soni on their body surface. Thirteen each carried
1 to 4 individuals of an unidentified species of
Lepeophtheinis on their body surface, and one
carried a single Bomnlochus ardeole in its
branchial cavity. In addition, four carried 1
to 8 gnathiid isopod larvae, two carried a single
leech, and one carried a single monogenetic
trematode, all on their body surface. The two
senoritas that were collected as they cleaned
garibaldis had preyed mostly on gnathiid larvae,
with each containing over 400 of these parasites.
In addition, one had consumed six Caligus hob-
soni. and the other had taken five Lepeojihtheirus
sp.

Four species of ectoparasites were collected
from 13 halfmoons, 166 to 295 mm long. Twelve
of the 13 halfmoons each carried 1 to 75 Caligus
hobsoni on their body surface. Each of two also
carried a single Lepeophtheirus sp. on its body
surface, and each of six carried 2 to 7 Peniculus
/issii>es embedded in its fins. In addition, each
of six carried from 2 to 16 monogenetic trema-
todes on its body surface. Of the two seiioritas
collected as they cleaned halfmoons, each con-
tained only Caligus hobsoni in its gut contents,
one a single specimen and the other eight.

Significantly, with the exception of the gnath-
iid larvae in a cleaner of topsmelt, as discussed
above, no parasite was found in the cleaner's
gut contents that did not occur on the species
of fish that was being cleaned by the cleaner

507

FISHERY BULLETIN': VOL 69. NO. 3

when it was collected. This fact further sup-
poi-ts the contention that cleaning tends to be
si:iecies-specific for a jjiven seiiorita.

The data clearly show that the parasites most
frequently taken l)y senoritas are certain mobile
forms that occur on the body surface of their
host. It may be that other parasites on the ex-
ternal body surface are not taken. No leeches or
trematodes were found among gut contents,
even though these forms are abundant on
the garibaldi and halfmoon. Also, the gut con-
tents did not show evidence of the lernaeid
Peniodus fissipes, an immobile form which par-
tially embeds itself in the skin of its hosts —
mostly on the fins. This parasite occurs on top-
smelt, garibaldis, and halfmoons among those
known to he cleaned by seiioritas. However,
negative evidence based on the meager gut-con-
tent data are weak, especially as the cleaning
labrid Lahroides phthirophar/us in Hawaii,
which feeds mostly on caligoid copepods, fre-
quently takes lernaeids (Randall, 1958; Young-
bluth, 1968). I would expect additional study
to show that cleaning seiioritas at least occasion-
ally take P. fissipes. Nevertheless, several
abundant fishes infested by P. fissipes, but not
found to carry caligids, gnathiids, or other mo-
bile external forms, were not seen being cleaned.
For example, the white seaperch is one of the
most abundant species at the 3- to 10-m station
off La Jolla and yet was never seen being cleaned.
Twelve specimens of this fish were examined,
and the only ectoparasites found were one to
four P. fissipes on three individuals. Similarly,
the only parasite found on 11 rainbow seaperch,
an abundant species in the study areas that was
not seen being cleaned, was a single P. fissipes
on one individual and two on another.

However, not all fishes whose external body
surfaces are heavily infested by mobile forms
were observed being cleaned. The sheephead,
Pimelometopon pnlrhrum, is a case in point.
CalifiHS hohsoni occurs on this fish, but onl.v in-
frequently— a single specimen of this copepod
was taken from each of 2 of the 14 sheepheads
that were examined. However, the sheephead
is heavily infested by two s])ecies of Lepeophthei-
rus, a genus of copepods that is closely related
to Caligus. Up to 70 L. parvjis were taken from

the body surface of a single sheephead, and this
fish has not yet been seen being cleaned. Fur-
thermore, up to 4 gnathiid larvae, which cleaners
take from other fish, were found on 3 of the
sheephead. Similarly, the treefish, Sebastes ser-
riceps, which is heavily infested with caligids,
has not yet been seen being cleaned. The tree-
fish is not known to carry C. hohsoni, but 13 of
15 specimens examined carried up to 12 Lepeoph-
theiru.s louglpes on their body surface, and 3
carried up to 5 gnathiid larvae. The significance
of these exceptions to what seems a valid gener-
alization has not l:)een determined. Perhajis it
is significant that these two species of fish are
not heavily infested by copepods of the genus
Caligus, as are the more frequently cleaned
fishes.

The many parasites that infest the oral and
branchial cavities might seem to be potential
prey for cleaners, but I found no evidence that
these iiarasites are taken by seiioritas.
, The principal ectojjarasites on the body sur-
face of the two most frequently cleaned fishes,
the blacksmith and the topsmelt, are the copepods
Caligus hobsoni and C. serratus, respectively,
which are very similar to one another morpho-
logically. With just one exception among the
fishes surveyed (discussed below), C. ser-ratus
seems to be restricted to topsmelt. On the other
hand, C. hobsoni occurs on a wide variety of
species and is also the principal form on gari-
baldis and halfmoons. Interestingly, a list of
the fishes hosting this parasite, ranked by in-
cidence (Table 3), looks much like the ranking
of fishes that were observed being cleaned by the
seiiorita (Table 1).

The importance of cleaning in reducing the
incidence of ectoparasites on fishes. — Certainl.y
cleaners remove many ectoparasites from the
bodies of certain fishes — the numbers in their
diet attest to this fact. But does cleaning in
fact aiijireciably reduce the level of infestation
on these fishes, or do other parasites quickly
replace those that are removed by the cleaners?
Although this question is difficult to answer, some
insight is i)rovided by observatio'iis on the gari-
baldi. When guarding eggs on their nests dur-
ing the reproductive season, male garibaldis be-

508

HOBSON: CLEANING SYMBIOSIS

come especially intolerant of the presence of
other fish species. Clarke (1970) recorded the
number of times garibaldis, in defence of their
territory, attacked fish of various other species
at different times of the year. He found that
when males were guarding eggs their attacks on
senoritas increased elevenfold. Not surpris-
ingly, I saw no cleaning of garibaldis that were
guarding eggs. At other times of the year male
garibaldis do not guard their territory as vigor-
ously against members of other species and are
frequently seen being cleaned. A series of these
males were collected both in and out of the re-
productive season, and the numbers of ectopar-
asites they carried were assessed. Seven indi-
viduals (mean length 228 mm) sampled as they
guarded their eggs carried a mean of 67 Caligus
hobsoni (range 20-144), 2.5 Lepeophtheinis sp.,
1.4 gnathiid isopod larvae, and 0.2 monogenetic
trematodes. These counts contrast strikingly
with those from six males (mean length 219 mn\)
sampled outside the reproductive season, which
carried a mean of only 4.8 C. hobsoiii (range
0-13), 1 Lepeophtheinis sp., 0.8 gnathiid larvae,
and no monogenetic trematodes. These findings
suggest that males which are guarding eggs be-
come heavily infested with C. hobsoni when they
do not allow cleaners to approach them, a con-
clusion strengthened by the fact that over this
same period the relative numbers of this same
]"iarasite were not noted to change on other in-

fested fishes. The samples included too few of
the other parasites to make a meaningful com-
parison. It remains a question why Lepeoph-
theinis sp. and the gnathiid larvae did not show
a pattern of occurrence similar to that of C.
hobsoni, as both of these parasites are known
to be prey of the cleaners. In any event, these
data add to the evidence which indicates that
C. hobsoni is the primary prey of cleaning sen-
oritas in the study areas.

Ectoparasites on Senoritas

Senoritas that were closely observed as they
cleaned other fishes often were noted to have
caligid copepods on their bodies. One seiiorita,
about 120 mm long, was host to an estimated
100 of these parasites concentrated especially
along the dorsal-fin base. These observations
were significant because during the survey for
ectoparasites, most seiioritas taken from the pop-
ulation at large were free of external forms,
although many carried a chondracanthid cope-
pod on their gills.

Twenty seiioritas, 102 to 190 mm long, were
sampled from among those giving no indication
of being cleaners. Eight of these carried 1 or
more of the chondracanthids on their gills, but
only 2, or 10''r, had parasites on their external
body surfaces: one of these carried 10 speci-
mens of Caligus hobsoni and 1 specimen of

Table 3. — Hosts of Caligus hobsoni.

Species

Specimens
examined

Specimens

hosting
C. hobsoni

Number of

C. hobsoni

on eoch

infested fish

mean (range)

Percent
occur-
renca

Blacksmith, Chromis punctipinni!
Topsmelt, Jthfrinops affinis
Gofiboldi, Hypsypops rubicunda
Halfmoon, Mediatuna calijorniensis
Opaleye, Girella nigricans
Olive rockfish, Sfbastes serranoides
Blue rockfish, Sebastes mystinus
Sharpnose seaperch, Phanerodon atripf:
Senorita, Oxyiulis catiiornica
Sheephead, Pimetometopon pulchrum
Rubberlip perch, Rhacotkilus toxoids
Cobezon, Scorpaenichthys marmoratus
Gopher rockfish, Sfbaslc-s carnalus
Pile perch, Rhacochiius vacca
Kelp rockfish, Sehastfs atroi'irfns

10

10

10.6(2-39)

100

13

'13

MC(3-23)

MOO

20

19

31.2(1-144)

95

13

12

19.8(1-75)

92

10

3

5.4(1-14)

80

11

5

2.6(M)

45

9

4

1

44

13

S

2(1-5)

38

36

9

11(1-59)

24

14

2

1

14

10

1

10

10

1

10

11

1

9

15

1

7

16

I

6

* .Ith^rinops affinii does not carry C. hobsoni.
text) of the very similar C. serratus.

but rather is the sole host (with one exception, see

509

FISHERV BULLETIN': VOL, 69, NO. 3

Lepeophtheirus sp.; the other senorita carried
a single Lepeophtheirus sp. Comparative data
were obtained by examining 16 senoritas. 114 to
160 mm long, that had been cleaning. Of these,
11, or nearly 10' r . carried copepod parasites on
their external body surfaces: 6 carried from
1 to 59 Callous hobsntii, 4 carried from 1 to 9 C.
seiratus, and 1 carried 3 Lepeophtheirus sp.

Significantly, those senoritas carrying Caligns
hobso7ii all had been cleaning blacksmiths, those
carrying C. serratiis had been cleaning topsmelt,
and the one carrying Lepeophtheirus sp. had
been cleaning a garibaldi. Thus the ectopara-
sites found on cleaning seiioritas were in all in-
stances forms that also infest the species which
that particular seiiorita had been cleaning. The
occurrence of C. serratus is especially interest-
ing, because these seiioritas are the only fish
other than topsmelt found so far to carry this
parasite.

Alerted to the phenomenon, I inspected the
bodies of many senoritas that incidentally passed
by during various phases of the work under-
water. Ectoparasites were evident on some, but
only on a small minority of the population. That
the vast majority are not infested by such par-
asites accounts for the observation, noted above,
that senoritas do not crowd around cleaners that
initiate activity in their midst, as do blacksmiths,
topsmelt, halfmoons, and others.

On the basis of these data, and on the general
cleaning picture that has developed, I believe that
at least most of the senoritas infested with caligid
copepods are cleaners. Presumably they acquire
these parasites while intimately associated with
the former hosts during cleaning. That a given
cleaner is found to carry parasites similar to
those on the fish it has Ijeen attending, but no
others, is further evidence that cleaning by in-
dividual senoritas tends to be species-specific.

Environmental Factors That Influence Cleaning

Temperature. — As noted above, the numbers
of senoritas present at the 20- to 25-m station
fluctuated in an api)arent response to water
temperature, with the critical level at about 12°
to 13° C. Less cleaning occurred at lower tem-
peratures (Figure 9), which would be ex-

liected with fewer senoritas present. Neverthe-
less, even considering the smaller numbers, the
senoritas present at lower temi^eratures seem
less active than those ])resent at higher temper-
atures. The eff'ect was striking on one occasion
at 25 m when, with an influx of warm water,
the temperatui-e rose suddenly from 11° to
14.5° C. No change was noted in the numbers
of senoritas present over this short period of
time, but where no cleaning had been seen dur-
ing a 20-min survey immediately before, shortly
after the temperature rise six different groups
of fishes being cleaned were in view simultane-
ously.

Turbidity. — When the water is turbid because
of ])lankton or suspended sediment, there is no-
ticeably less cleaning activity than when the
water is clear. The fishes are generally more
wary, and remain closer to cover when visibility
is reduced.

Surge. — When there is a strong surge, a fre-
(]uent occurrence, especially in water less than
10 m dee]), there is far less cleaning activity than
when the water is still.

Day-night. — The seiiorita, a strictly diurnal
sijecies that takes shelter under cover at night,
does not clean after dark.

n=6 "=5

n

61"

so-

59°

58° 57° 56° 55°

54°

53°

52°

51° (°F)

16 !•

ls 6-

150°

144° 139' 133° 128°
TEMPERATURE

12 2°

117°

tl.l°

I06°(°C)

FlGi'RE 9. — Number of sefiorita cleaning bouts seen dur-
ing each of 3.'! observation period.s, 15-25 min long, at
ilifTercnt water temperatures in an area 25 m deep at
La Jolla. Periods during which temperature fluctuated
were not considered, n = number of obser\'ation periods
at that temperature; where n > 1, value given is the
mean.

510

IIOBSON: CLEANING SYMBIOSIS

CLEANING ACTIVITY OF THE
SHARPNOSE SEAPERCH

Unlike senoritas, which clean as adults as well
as juveniles, all of the sharpnose seaperch that I
observed cleaning were juveniles less than about
125 mm long-. Occasionally noncleaning sea-
perch swim in groujis of 15 or more, but those
seen cleaning were always solitary, or in groups
of two or three. In agreement with senoritas,
cleaning seaperch do not establish well-defined
cleaning stations, but instead may clean other
fish at any point as they move from place to
place. I found no evidence that fishes which
are residents of other areas come to where sea-
perch are located for cleaning; rather, cleaning
seaperch occur where resident fishes are nu-
merous. As is true of seiioritas, seaperch use
the same picking technique to clean material
from the bodies of other fish that they use to
take small organisms from a benthic substrate.
Clearly bottom-picking can be preadaptive to
cleaning. Cleaning by seaiierch, as by seiioritas,
usually occurs within 3 m of the substrate. How-
ever, there is little overlap in the cleaning areas
of the two species: generally seaperch clean at
greater depths and or in colder water than
senoritas, where limited observations indi-
cate they may ]iredominate as cleaners even
when senoritas are more abundant. Data
illustrating this distribution of cleaning activ-
ity at a point in time were obtained at the
20- to 25-m and 30- to 3.5-m locations off
La JoUa, where the two species co-occur

Table 4. — Number of bouts in which sharpnose seaperch
and senoritas, respectively, were seen cleaning other
fishes during 1.5-niin observation periods at the 20- to
25-m and 30- to 35-m locations off La Jolla. Two obser-
vation periods, one at each location, and never more than
45 min apart, were made on each of the dates indicated.

Number of cleaning bouts observed

Dote

20- to 25-m location

30- to 35-m location

Seaperch Senorita

Seaperch Senorita

22 Nov.

2

13

17

0

27 Nov,

0

7

1

0

9 Jan.

2

5

9

0

15 Jan.

2

4

8

0

3 feb.

2

12

9

2

(Table 4) . Despite the fact that senoritas were
observed to be far more numerous than perch
throughout the depth range of this study
(3-50 m), seaiierch performed almost all
the cleaning observed at the 30- to 35-m lo-
cation, where cleaning by the much more
abundant seiiorita was limited to a few isolated
instances.

A measure of the incidence of cleaning indi-
viduals within the population of juvenile sharp-
nose seaperch was obtained during 39 observa-
tion periods at the 20- to 25-m and 30- to 35-m
locations at La Jolla. These observations, to-
taling more than 26 hr, were made from Sep-
tember 1968 to February 1969. During this
period, 201 juvenile seaperch were seen, of which
105, over 52 Sf , were cleaning other fishes. Thus
it appears that at least most sharpnose seaperch
are cleaners when they are juveniles, whereas
only a small minority of the seiiorita population
seem to be cleaners.

Fishes Cleaned by the Sharpnose Seaperch

Because sharpnose seaperch were observed
only at depths lielow 20 m, substantially less data
are available on their cleaning activity than on
that of seiioritas. Of the 105 seaperch observed
cleaning during the 39 observation periods re-
ported above, all but one were cleaning black-
smiths; the lone exception was cleaning a soli-
tary blue rockfish, Sebastes mystimis. On two
other occasions, I saw sharpnose seaperch clean-
ing rubberli)! jierch, but otherwise the only fish
seen being cleaned have been blacksmiths (Fig-
ure 10). Undoubtedly additional observations,
especially in other areas, would expand this list.
I observed seiioritas cleaning in many different
areas, but my observations of cleaning seaperch
are limited to La Jolla. Clarke et al. (1967)
saw a sharpnose seaperch cleaning a rockfish at
1.50 m oflf La Jolla, and Gotshall (1967) reported
what he believed to be this species cleaning Mola
mola off Monterey. Yet no matter how many
different species the seaperch may in fact clean,
there seems no doubt that blacksmiths are prime
recipients in southern California, at least in
depths shallow^er than 35 m.

511

FISHF.RV BULLETIN: VOL. 69, NO. 3

Figure 10. — Sharpnose seaperch inspecting a blacksmith,
which hovers to solicit cleaning.

Specific Cleaning Interactions— Seaperch-
Blacksmith

The limited observations on cleaning by sharp-
nose seaperch provide details only on interac-
tions with blacksmiths. As nearly as could be
seen, when sharjinose seaperch clean blacksmiths
the activity proceeds much as it does when black-
smiths are cleaned by senoritas, as described
above. However, the observations were too few
to determine whether or not cleaning activity
is consistently initiated by the cleaner. Several
times blacksmiths hovered in their typical head-
down posture before seemingly unresponsive sea-
perch, but perhaps the sea])erch had earlier made
some initial gesture. Whenever it could be de-
termined, the seaperch initiated the cleaning.

Some details were obtained at the 20- to 25-m
location at La Jolla, where two seai)erch, known

to have been cleaning blacksmiths, were each
kept under surveillance for 15 min, while their
activity was monitored on tape. Both swam on
irregular courses among the rocks but remained
within an area encompassing about 15 to 20 m'.
During this time one entered into 4, the other 5,
separate cleaning bouts, averaging 2.6 (range
0.5-7.5) and 1.8 (range 0.75-3.5) min long, re-
spectively, all with blacksmiths. The cleaner ini-
tiated the activity in each instance, but immedi-
ately thereafter a number of other blacksmiths
converged on the spot. Most of the cleaning
bouts continued after the original blacksmith had
left the group, and a succession of others arrived
and departed before the bout ended. Although
usually they hovered head-down Ijefore the clean-
ers, the blacksmiths nevertheless assumed a wide
variety of attitudes. During much of the time
they swam with the blacksmiths, the two sea-
perch under surveillance closely inspected the
Ijlacksmith's bodies and actually picked at them
18 and 14 times, respectively. Most of the clean-
ing was directed at the fin bases, particularly
the caudal. While in company with the black-
smiths, one of the seaperch broke away from the
group and swam to look closely at the dorsal fin
of a blue rockfish. However, no cleaning oc-
curred: the blue rockfish swam away as though
uninterested in cleaning and the seaperch re-
turned to the blacksmiths. When not in company
with the blacksmiths, the two seaperch swam
alone 1 or 2 m over the substrate. One descended
to the bottom twice and picked at gorgonians:
five times on the first descent, once on the
second.

Once a blacksmith was seen obviously attempt-
ing to present its caudal fin to a seaperch, with-
out success in enticing the seajserch to clean.
Close inspection did not reveal parasites, but
part of the fin was torn away and shredded
flesh was exjiosed. Ajiparently this Ijlacksmith
was presenting a point of irritation to the clean-
er, which in this instance was an injury, not a
parasite. Some cleaners, for example, Abudef-
diif troscheUi, which i)icks molting skin from the
Oalaiiagos marine iguana (Hobson. 1969b).
will clean dead or injured itssue, but at least
(in this occasion the seaperch showed no inter-
est.

512

IIOBSON: CLEANING SYMBIOSIS

Material Removed from Other Fish by the
Sharpnose Seaperch

To determine the food of cleaning' seaperch,
I examined the gut contents of 16 specimens,
74 to 122 mm long, that were speared as they
cleaned blacksmiths. Food items in their guts,
ranked as percentage of each item in the entire
sample, were as follows: caligid copepods, 68'^; ;
caprellid amphipods, IG^r; gnathiid isopod lar-
vae, 9%; algae, I'/r ; and unidentified items,
6'"r. Thus ectoparasitic caligids and gnathiids
made up 77^; of the material. All 16 specimens
contained ectoparasites; in fact, ectoparasites
constituted the vast bulk of the material in all
but one individual, which had fed more heavily
on caprellids. As with senoritas, when an apiire-
ciable amount of free-living material was pres-
ent, it was usually sharply divided from the ecto-
parasites and more digested to the rear in the
digestive tract. All the identifiable caligid cope-
13ods among this material were Califius hohsoni,
which is consistent with what is known of ecto-
parasites on blacksmiths, the sjiecies cleaned by
these seaperch, and indicates feeding habits si-
milar to those of the cleaning senorita, presented
above.

Incidental Cleaning by a Close Relative

Although sharpnose seaperch were not seen
in water less than 20 m deep, the white seaperch,
a very similar species, is frequently abundant
there. Tlie white seaperch was probably the
most numerous of the embiotocids during most
of the observations made at the 3- to 10-m lo-
cation off La Jolla. Underwater the white sea-
perch and the sharpnose seaperch are nearly
identical, but can be distinguished by the dusky
bordered caudal fin of the former and the black-
tipped pelvics and more pointed snout of the
latter.

White seaperch are especially abundant in
groups of 10 or more close to surfgrass in 3 or
4 m of water off La Jolla. Typically they hover
head-down; in this attitude they are not solic-
iting cleaning but rather are intently regarding
the surface of the vegetation, at which they pick
occasionally. Tiny organisms that live on the
surfgrass are prey of these fish: five white sea-

perch, 80 or 81 mm long, speared in this habitat,
were filled with (showing percent of total vol-
ume) caprellid amphipods (80%), gammarid
amphipods (5'"f), isopods (2%), fragments of
algae with encrusting bryozoans (lO^r ) , and un-
identified crustacean parts (3'r ). Quast (1968)
found that specimens from a kelp bed had fed
mostly on small bottom-dwelling crustaceans,
polychaetes and bivalves, as well as kelp frag-
ments, some of which were heavily encrusted
with bryozoans. Thus the bottom-picking feed-
ing habits of the white seaperch are very similar
to the noncleaning habits of the sharpnose sea-
perch.

On one occasion, I saw a white seaperch swim
1 or 2 m above the surfgrass in company with
a lone blacksmith, which hovered head-down in
the manner tyincal of one that desired to be
cleaned. The white perch picked at the black-
smith's body several times, but the bout was
brief, and the perch soon joined a group of 8
to 10 others of its own kind near the surfgrass
below. This seaperch, which proved to be 79 mm
long, was speared, and its gut contents included
58 caprellid amphipods, a single gammarid am-
phipod, one small isopod, plant fragments with
encrusted bryozoans, and some unidentified non-
parasitic crustacean remains. No ectoparasites
were found; its food was similar to that of the
other white seaperch reported above. On an-
other occasion I saw a white seaperch cleaning
several blacksmiths over a sandy bottom in 12 m
of water, but this individual was not collected.
Probably the observed cleaning was no more
than a brief incidental activity for these fish.
At no other time did I see any indication of clean-
ing by this species, but perhaps the activity is
more frequent under appropriate conditions.

CLEANING ACTIVITY OF
THE KELP PERCH

Because the kelp perch is not abundant in the
La Jolla study area, where larger kelps are
sparse, most observations of cleaning by this
fish were made incidentally during other projects
in areas heavily forested with kelp. However,
these other projects generally were centered on
the sea floor, whereas kelp perch concentrate

513

FISHERY BULLETIN: VOL. 69, NO. 3

above in the midwater and canopy regions.
Nevertheless, observations of cleaning were suf-
ficiently frequent to recognize this species as a
habitual cleaner, though probably less so than
either the seiioritas or the juvenile sharpnose
seaperch. In taking material from the bodies
of other fishes, the kelp perch uses the same
picking teclmique that it employs to pick items
from an algal substrate, or that are adrift in
midwater. Its pointed snout and dentition, which
is similar to that of the senorita, as described
above, are well suited to cleaning.

Insofar as an aggregation of kelp perch tends
to remain in one location, these fish can perhaps
be regarded as maintaining a station at which
other fishes are cleaned. But I saw no indication
that more than one or a few members of a given
aggregation clean, or that other fishes come to
these locations from any distance for cleaning.
In fact, I saw only blacksmiths and other kelp
perch being cleaned by this fish. In the one
observation of intraspecific cleaning, a single
kelp perch swam among others of its aggrega-
tion, intently inspecting their bodies. Usually
the subject of this attention moved away, where-
upon the cleaner moved to another fish. A few
responded to the cleaner by erecting their fins
and hovering immobile in a head-down posture,
and these were cleaned. Occasionally a fish be-
ing cleaned suddenly darted away as if the clean-
er had been too vigorous in its attentions. All
blacksmiths being cleaned were solitary indi-
viduals that hovered in head-down soliciting
fashion close to an aggregation of kelp perch.
Whether or not one of the perch had earlier
made an initiating overture was never deter-
mined. Never more than one or two of the perch
in the aggregations wei'e seen cleaning these
blacksmiths. Occasionally a cleaner would close-
ly follow a halfmoon or kelp bass that inciden-
tally i^assed close by, but I saw no evidence that
these fish were interested in the perch, and no
cleaning occurred.

Three kelp perch, 91 to 99 mm long, one of
which had been cleaning a blacksmith, were col-
lected from an aggregation hovering near a
stand of feather-boa kelp. The gut contents of
the individual known to have cleaned the black-
smiths contained (showing the percent of total

volume): gnathiid isopod larvae (50S^), non-
parasitic isopods (STr), gammarid amphipods
(^Vf ) , caprellid amphipods (20''y ) , and uniden-
tified material (20''f). Neither of the two that
were not known to have cleaned contained evi-
dence of ectoparasites: one was full of caprellid
amphipods (90'^'r) and unidentified material
(lO'^r). whereas the other had nothing in its
digestive tract except a few unidentified frag-
ments posteriorly.

Llmbaugh (1955) reported kelp perch clean-
ing kelp bass, opaleyes, garibaldis, blacksmiths,
and walleye surfperch i^nyperprosopon arcjcn-
teum).

DISCUSSION

Various cleaning fishes remove a wide variety
of deleterious material from the bodies of the
animals they service. In addition to ectopar-
asites, this material includes diseased, injured,
or necrotic tissue, fungi, and unwanted food
particles (Feder, 1966; Hobson, 1968, 1969b;
and others) . However, the discussion below con-
siders cleaning only as the removal of ectopar-
asites, because my data indicate that these are
the only items taken in significant amounts from
California fishes by the cleaners considered in
this report.

INCIDENTAL VS. HABITUAL CLEANING

Cleaning is widespread among small-mouthed
marine fishes that characteristically pick minute
organisms from the substrate (Hobson, 1968).
Included are species of the families Chaetodon-
tidae, Pomacentridae, Labridae, Embiotocidae,
Blenniidae, and others. Morphological and be-
havioral characteristics suited to their way of
life have preadapted many species of these fami-
lies for the cleaning habit. Probably some such
fishes iHck ectoparasites only incidentally during
routine foraging when under certain conditions
the body of an adjacent fish, infested with ecto-
pai-asites, becomes accessible as just another
feeding substrate. The relative tendency of a
given si)ecies to clean likely is influenced by both
short-term ;uid long-term environmental
changes. Such changes may be expected to alter

514

IIOBSON: CLEANING SYMBIOSIS

interspecific relations, by affecting not only the
relative availability of various prey organisms
and the incidence of various ectoparasites, but
also the species composition of the interacting
fishes themselves.

In California the white seaperch likely is one
of those species that cleans only occasionally as
an incidental adjunct to regular foraging. Sever-
al other California species reported by Limbaugh
(1955) and Gotshall (1967) clean, including
black perch, pile perch, and rainbow seaperch,
but they have not been seen doing so by me.
The report of cleaning by the blacksmith (Tur-
ner et al. 1969) remains an anamoly. as this fish
does not fit the pattern of a bottom-picking pred-
ator described above. However, it may be sig-
nificant that many of those substrate-picking
predators which clean most frequently are spe-
cies that also feed on material adrift in mid-
water, as do the senorita, sharpnose seaperch,
and kelp perch. Thus this mode of feeding too,
including the taking of plankton, may, in some
species, favor adaptations that are suited to
cleaning. Fishes that are adapted to both sub-
strate-picking and plankton-picking may possess
adaptations especially well suited to cleaning.

Probably many species of fishes clean inci-
dentally on isolated occasions, but relatively few
are habitual cleaners. And even the habitual
cleaners vary greatly in the degree to which they
are specialized for this habit. Species of the
Indo-Pacific labrid genus Labroides are highly
specialized cleaners that feed almost exclusively
on ectoparasitic crustaceans (Randall, 1958;
Youngbluth, 1968). These fishes possess many
specific morphological and behavioral specializa-
tions that are adapted to this way of life (Feder,
1966; Losey, 1971). However, only a small mi-
nority of cleaners are so highly specialized; most
are but part-time practitioners of the cleaning
habit, with much of their food being derived
from other sources.

That some cleaners depend on ectoparasites
for prey, whereas others can subsist equally well
on food from other sources, has led to classifying
various species as either obligate or facultative
cleanei-s (e.g., Youngbluth, 1968) . The senorita,
sharpnose seaperch, and kelp perch may well
resist being so classified because their cleaning

seems to be characteristic not so much of a spe-
cies as of just certain individuals. At least at
a given time, most senoritas do not clean, where-
as some seem to be facultative cleaners, and a
few might even be obligate cleaners. Juvenile
sharpnose seaperch follow a similar pattern, but
with a relatively higher incidence of individuals
that clean. Limited data can only suggest that
the status of the kelp perch may be similar.

CLEANING INITIATED BY THE SENORITA

Usually there seem to be fishes present that
need cleaning, as shown when a seiiorita identi-
fies itself as a cleaner by initiating action with,
say, a blacksmith or a topsmelt, and immediately
is converged upon by many other fish that crowd
in its way seeking attention. That such fishes
generally wait for a senorita to begin the clean-
ing, rather than attempting to initiate activity
themselves with one of the many senoritas
present, likely reflects a low probability of suc-
cess if they make the first move. If, as it seems,
the vast majority of sefioritas are not cleaners,
or at least not currently predisposed to clean,
then random efforts to solicit service would not
seem adaptive.

This situation contrasts with that of the Ha-
waiian wrasse Labroides phthirophagus, of
which all individuals seem to be obligate cleaners
(Youngbluth, 1968), and which is not nearly
as abundant on Hawaiian reefs as the senorita
is in California. In centering their activity
around well-defined stations, the distinctive L.
phthirojihagus can be recognized readily by
others that need cleaning. Thus, not surpris-
ingly, cleaning encounters that involve L. phihi-
rophagns are regularly initi;>.ted by fishes seek-
ing cleaning (Losey, 1971).

We have seen that under certain circumstances
various fishes initiate cleaning encounters
with sefioritas. Some fishes successfully do so
by hovering amid unusually dense concentra-
tions of senoritas, luit the overtures of such fish
are not directed at individuals ; rather, they are
broadcast to the assemblage at large. The suc-
cess of this tactic presumably follows the proba-
bility that an individual predisposed to clean oc-
curs among such a large number of sefioritas.

515

FISHERY BULLETIN: VOL, 69. NO.

Kelpfish regularly solicit cleaning from indi-
vidual senoritas, but the situation is exceptional.
Because kelpfish rise into midwater for cleaning,
it appears that they do not receive satisfactory
service in their regular habitat amid benthic veg-
etation. In their usual surroundings, where they
are extremely difficult to discern, the cryptic
kelpfish may be relatively inaccessible to cleaning
seiioritas. One can see why a fish thus handi-
capped might be required to initiate needed
cleaning itself. The number of unsuccessful at-
tempts experienced by kelpfish before a seiiorita
was finally induced to clean them underscores
the existing problem of locating a cleaning indi-
vidual.

SPECIES-SPECIFIC CLEANING

Because the cleaning seiiorita initiates most
of its activity, it has the opportunity to select
its clients, and the data indicate that a species-
specific choice is exercised. That individual
cleaners tend to limit their selection to members
of only one species may be related to the fact
that they initiate cleaning on the home ground
of the fishes they serve, when these fishes are
engaged in some of their regular activity. As
each of these clients has distinctive habits, a seii-
orita approaching to clean a fish of one species
faces a somewhat difi'erent situation than a seii-
orita approaching to clean a fish of another spe-
cies. The distinctions often are subtle, but may
be significant enough to account for a given
seiiorita's tendency to seek out members of only
one species.

Again we can draw a contrast with the clean-
ing behavior of Lahroides phthirophagus, indi-
viduals of which receive members of many dif-
ferent species at well-defined cleaning stations
(Randall, 1958; Youngbluth, 1968). Probably
such nonspecific cleaning is characteristic of
cleaners whose activity is confined to these estab-
lished locations. Fishes that visit such cleaning
stations enter the cleaner's own territory, and
frequently .join a mixed-species group that hov-
ers in wait for service. In tending these fishes
on its home ground, the cleaner is receiving
them on its own terms, so to speak, so that the
situations surrounding cleaning bouts with

all of the difl^'erent species are essentially the
same.

Cleaning by the seiiorita may not be species-
specific on those few occasions when the cleaning
activity is initiated by the fish in need of such
service, for example by the kelpfish, as described
above. Although they show some diff'iculty lo-
cating a receptive seiiorita, kelpfish nevertheless
seem far more successful at doing so than one
would expect if indeed they are required to find
one that will clean only kelpfish. Thus, although
individual seiioritas seem to be species-specific
when they themselves initiate cleaning, they may
be considerably less so, and perhaps even non-
specific, when the other fish makes the initial
overture. There are no data on this point, how-
ever.

The extent to which these considerations ap-
ply to juvenile sharpnose seaperch and kelp
perch cannot be ascertained because data are
lacking.

SIGNIFICANCE OF POSTURES ASSUMED
BY FISHES THAT SOLICIT CLEANING

\^'Ilen members of an assemblage of fishes like
blacksmiths or topsmelt converge on a cleaning
site that has developed in their midst, probably
their attention was initiall.v alei'ted by the un-
natural-appearing posture assumed by the indi-
vidual first approached by the cleaner. Usually
this posture does not seem to be assumed pur-
posefully, but rather results when the fish, hav-
ing ceased swimming and immobilizing its fins,
passively drifts out of its regular attitude (Hob-
son, 1965b). The posture thus assumed varies,
especially between species, where perhaps dif-
fering centers of gravity are determining fac-
tors. Thus the blacksmith usually hovers head-
down, whereas the topsmelt is more often
tail-down. Sometimes an unnatural-appearing
posture is actively assumed when the fish at-
tempts to present to the cleaner a certain part
of its body, presumably that part carrying an
irritation. By virtue of their unusual appear-
ance, these ijostures in cleaning interactions
serve to draw attention to the fish that is cleaned.
It does not seem necessary that any particular
posture be assumed, only that it look out of the

516

HOBSON': CLEANING SYMBIOSIS

ordinary. Rejiorts are widespread (see Feder,
1966) of cleanino- recipients assuming- these un-
natural-appearing postures.

Attention-getting postures assumed by fishes
being cleaned probably occurred incidentally
during the early development of cleaning sym-
biosis, when fishes hovering to be cleaned quite
naturally stopped moving and passively drifted
out of their regular attitudes. As the various
cleaning relations evolved, apjiarently this ob-
vious cue subsequently assumed a difl'erent role
as a signal in different situations. Generally
these postures are suggested to be signals be-
tween the recipient of cleaning and the cleaner,
indicating a readiness to be cleaned. Quite likely
this is the primary signal-function in activity
involving such cleaners as Labroides phthiro-
phagus. where all members of the siiecies are
cleaners and where activity is centered around
cleaning stations that are well known to other
fishes in the area. In this situation a fish in
need of cleaning- should be reasonably successful
in advertising its condition by assuming the
characteristic soliciting posture before a fish
recognizable as a cleaner. Losey (1971) showed
that various fishes regularly employ this tactic
to induce L. phthimiihagiis to clean them. Ob-
servations in the Gulf of California demonstrated
that the cleaning station itself has played a role
in establishing the soliciting- posture as a cue.
There I have seen the goatfish MuJloidichthys
denfatits hovering head-down at cleaning sta-
tions of the butterflyfish Heniochiis nigrirostris,
when the resident cleaner was itself temporarily
absent. Losey (1971) observed similar behavior
among Hawaiian fishes. In such a situation the
hovering posture probably alerts the cleaner to
fishes that have arrived for cleaning.

However, in cleaning activity involving the
sefiorita, the soliciting- posture usually is assumed
only after cleaning has been initiated by the
cleaner. The pi'oblem of recognizing an indi-
vidual that will clean among the vast majority
of seiioritas that do not clean, coupled with the
absence of well-defined cleaning stations, would
reduce the adaptiveness of the client's soliciting
posture as a cue to initiate cleaning. Probably
the most eflfective way for a fish to obtain needed
cleaning in this situation is to wait until a cleaner

has identified itself by initiating activity with
some fish in the area. Once this has occurred,
one can see the value of the posture, when as-
sumed by the first fish to be approached, as a
cue in alerting other fish that need cleaning to
the presence of a cleaner. In eff'ect, then, the
fish assuming the soliciting posture advertises
the temporary existence of the transient cleaning
"station" to other potential recipients of clean-
ing. Well-defined cleaning stations like those
of Labroides phthirojihagus do not need this sort
of advertisement, as their locations are -well
known to the fishes that visit them. Nor is it
necessary that cleaning individuals of L. phthi-
rophagns be pointed out, as all members of that
distinctive species are cleaners. Despite this,
it is probable that fishes hovering to be cleaned
at a Labroides station themselves create a visual
cue that tends to attract other fishes.

There may also be a maladaptive aspect to
the postures assumed by fishes that solicit clean-
ing. In hovering at an unnatural angle, fins im-
mobile and erect, a fish may enhance its chances
of being cleaned, but it would also seem likely
to draw the attention of predators and to handi-
cap itself in evading attack. Perhaps such an
increased vulnerability accounts at least in part
for the sharp decline in cleaning that occurs
with reduced visibility, when predators can ap-
proach closer undetected. Increased vulnera-
bility may also account for the observation
reported earlier (Hobson, 1965c), where poma-
dasyids in the Gulf of California abruptly broke
away from cleaners when a predator approached.

THE POSSIBILITY THAT FISHES BEING
CLEANED EXPERIENCE STRESS

Being prodded and picked over by an animal
of another species would seem to require a dif-
ficult adjustment for a fish. It may well be that
fishes experience stress under this circumstance,
even when the behavior is well established. Cer-
tainly observations have shown that this exper-
ience can be uncomfortable, judging from how
often fishes being cleaned suddenly bolt forward,
and swim away, apparently having been nipped
too vigorously by the attending cleaner. Some-
times too, a fish approached by a cleaner clearly

517

FISHERY BLXLETIM; VOL, 69. N'O. J

experiences conflicting responses, one moment
tolerating or even soliciting the cleaner's atten-
tions, and the next moment chasing it awaj' on
each approach. Such ambivalent behavior was
especially evident in rubberlip perch. Losey
(1971) noted that Labroides phthirophagus in
Hawaii is sometimes attacked by fishes that it
attempts to clean, and suggested that this may
occur when the cleaning is painful to the host
fish.

The color changes shown by many fishes being
cleaned (Randall, 1958; and others) may in fact
be manifestations of stress. It is well known
that many fishes experience color changes in re-
sponse to stress. Earlier (Hobson, 1965a) I dis-
cussed the striking color change of the goatfish
Mulloidichthys dentatns when it solicits cleaning
in the Gulf of California, and pointed out that
this fish shows the same color change in other
situations that are obviously stressful. Such
color changes have been regarded as signals be-
tween the fishes being cleaned and the cleaners,
(e.g., Feder, 1966), functioning in the cleaning
interaction much like the soliciting attitudes
discussed above. As with the attitudes, any role
such color changes may now have assumed as a
signal probably evolved from an incidental by-
product of early cleaning. I have no data on this
point relating to the California species, as such
color changes are not especially evident in fishes
that were observed being cleaned there.

ARE CLEANERS IMMUNE FROM
PREDATION.'

Reportedly some cleaners are immune from
pi'edation because of the service they provide
the predators (Feder, 1966; and others). Lim-
baugh's (1961) belief that the senorita enjoys
such immunity is based on observations of this
labrid entering the open mouth of kelp bass to
clean and on not finding it among the stomach
contents of predators during a food-habit study.
However, Quast (1968) found seiioritas in the
stomachs of kelp bass, and H. Geoffrey Moser,
U.S. National Marine Fisheries Service (unpub-
lished data), found sefioritas in stomachs of the
bocaccio, Sebastes paucispinis, and the starry
rockfish, S. constellatiis.

I doubt that cleaners enjoy immunity in
the sense that predators, recognizing them as
benefactors, actively avoid preying on them.
Cleaners may recognize those predators which
are not at that time intent on feeding and may re-
strict their cleaning to such individuals. A preda-
tor that assumes a soliciting posture may effec-
tively advertise this situation, and no doubt other
cues exist. Such mechanisms would reduce the
chance of cleaners placing themselves in vulner-
able situations while cleaning. In addition, clean-
ers probably are not as vulnerable while cleaning
large predators as might be expected simply be-
cause cues characteristic of feeding situations
are not present. In associating themselves so
intimately with predators, cleaning fishes show
behavior that is so unlike that of prey that preda-
tors probably do not regard them as food. How-
ever, even if such factors do reduce the danger
that might seem inherent in the cleaning act,
I doubt that their cleaning role affords these
fishes any security from being eaten in non-
cleaning situations.

PARASITES AS PREY OF THE
CALIFORNIA CLEANERS

It is hardly surprising that the fishes which
are cleaned most frequently in California are
those which are the most abundant and at the
same time carry the most ectoparasites. Thus
the blacksmith, topsmelt, halfmoon, and gari-
baldi are the fishes cleaned most frequently,
and the survey of ectoparasites showed them to
be among the most heavily parasitized. The
vast majority of ectoparasites on these particular
fishes are mobile forms, mostly caligid copepods
and gnathiid isopod larvae, that occur on the
body surface of their hosts. That these same
parasites were found to make up the diet of the
cleaners attending these fishes is consistent with
the observation that only the exteriors of fishes
were seen being cleaned during this study.

Although the forms infesting the external
body surface are the most numerous ectopara-
sites on the fishes available to the California
cleaners, many other types were found to infest
the oral and branchial cavities. One might ques-
tion why these other parasites do not seem to be

518

HOBSON: CLEANING SYMBIOSIS

taken, especially as Limbaugh (1955, 1961) re-
ported senoritas entering the mouth of the kelp
bass and cleaning beneath the gill covers of the
garibaldi. Furthermore, such behavior has been
widely reported for some other cleaners, such as
species of Labroides (Eibl-Eibesfeldt, 1955;
Randall, 1958; and others), and some echeneids
are known to habitually feed on copepods from
the branchial cavities of sharks (Cressey and
Lachner, 1970) . Nevertheless, any such activity
by seiioritas must be relatively rare. In discuss-
ing this situation I limit my remarks to the
senorita, because data are jiresently insufficient
to determine whether the same may apply to
the sharpnose seaperch and kelp perch.

Senoritas would not be expected to take par-
asites from the oral or branchial cavities as often
as species of Labroides or echeneids if for no
other reason than they simply are too large rel-
ative to most of the fishes they clean. Whereas
species of Labroides or the echeneids are small
enough to enter the oral and branchial cavities
of most of the fishes they service, the seiiorita
is nearly as large, and sometimes even larger,
than most of its clients. Significantly, Limbaugh
observed seiioritas cleaning within the oral and
branchial cavities of kelp bass and garibaldis,
both of which are relatively large species. Most
of the senorita's cleaning is directed toward
smaller species, like the blacksmith and the
topsmelt.

The specialized techniques that would be re-
quired to prey on the parasites of the oral and
branchial cavities would probably pose another
problem to the senorita. In its regular habit
of taking parasites from the external surfaces
of fishes, the cleaning senorita concentrates on
just a few forms that not only are numerous
on many of the most abundant fishes, but also
are not too dissimilar from free-living prey of
the species. Sometimes these external forms
also occur in the branchial cavity, and some
similar forms, e.g., bomolochids (Figure 7), ha-
bitually occur there and in the oral cavity. But
the majority of parasites characteristic of the
branchial and oral cavities are aberrant forms,
e.g., dichelesthiids, chondracanthids, and lerne-
opodids (Figure 7), and these are unlike anj--
thing else encountered bv the seiiorita. No one

type predominates; rather, they occur in a wide
variety of forms, none widespread among the dif-
ferent species of fishes, and none especially
abundant (except on an occasional individual
fish) . Thus a cleaner probably could not subsist
on one type alone but would have to master a
repertoire of specialized techniques in order to
exploit enough of these varied forms to make
it worthwhile. And before access is gained to
the site of infestation, a much more refined clean-
er-host interaction must have evolved than is
necessary when parasites are simply cleaned
from the external body surface. No such re-
lation would evolve unless the cleaner acquired
the precise manipulations necessary to pick at-
tached pai-asites ofl" the gills without damaging
the delicate gill membranes. Obviously the
cleaning relation would not be adaptive if such
damage occurred. In short, to feed habitually
on parasites from the oral and branchial cavities
would seem to require a higher degree of spe-
cialization than has been demonstrated by the
seiiorita. It seems unlikely that such special-
ization would develop as long as the more abun-
dant and readily available forms on the body
surfaces continue to satisfy the cleaning needs
of the species. Certainly judging from the way
blacksmiths, topsmelt, and other fishes vigor-
ously compete to have their external parasites
removed, it would seem that there is little imme-
diate chance of these parasites falling into short
supply.

CLEANING SYMBIOSIS AND THE
DISTRIBUTION OF SHORE FISHES

In his often-cited report on cleaning symbiosis,
Limbaugh (1961: 48) stated:

In my opinion it is the presence of the senorita and
kelp perch that brings the deep-water coastal and
pelagic fishes in.shore to the e<ige of the kelp beds
on the California coast. Most concentrations of reef
fishes may similarly be understood to be cleaning
stations. Cleaning stations would therefore account
for the existence of such well-known California sport-
fishing grounds as the rocky points of Santa Catalina
Island, the area around the sunken ship Valiant off
the shore of Catalina, the La Jolla kelp beds and sub-
marine canyon and the Coronado Islands.

Presumably this conclusion was intuitive, as no

519

FISHERY BULLETIN: VOL. 69, NO. 3

data were presented. In his review of cleaning
symbiosis, Feder (1966: 368), basing his con-
clusion on Limbaugh's work, similarly stated:
"In all probability, many good fishing grounds
are such primarily because they are cleaning
stations." I believe that this contention is un-
founded. Seiioritas are the major cleaners in
California inshore waters, so that if cleaning
symbiosis does account for most concentrations
of reef fishes in this region, as Limbaugh sug-
gested, then seiioritas would be the cleaner large-
ly responsible. Cleaning occurs wherever seii-
oritas are concentrated but clearly is not a major
activity of the population, even though it may
be so for a relatively few individuals. In any
event, it seems safe to conclude that cleaning
is not among the major factors determining the
distribution of seiioritas. And if cleaning does
not determine the distribution of seiioritas them-
selves, it seems unlikely that it would determine
the distribution of other species.

Undoubtedly many factors contribute to cre-
ating situations that draw concentrations of
fishes to certain locations. Where a number of
different species have similar requirements, as-
semblages will develop where conditions satis-
fying these requirements are optimum. The
presence of these fishes increases the complexity
of the environment, thus creating situations that
support still other species, and so on. Often
it is apparent that certain features are especially
significant as a basis for these concentrations.
Consider, for example, the rocky points that Lim-
baugh included in his list of "well-known Cali-
fornia sport-fishing grounds." The flora and
fauna of these locations are generally rich, a
fact probably related to such local features as
converging currents that frequently produce up-
welling and nutrient-rich waters. Plankton is
commonly abundant here, along with plankton-
feeding fishes like the blacksmith. Seiioritas
and other species frequently are numerous here
too, but the main attraction seems to be a gen-
erally rich food supply rather than available
cleaning. Similarly it is unrealistic to attribute
concentrations of fishes around sunken ships to
cleaning activity. Where a wreck has settled
on an open expanse it becomes a haven for fishes
that require a nearby structure for cover or a

spatial reference point. Obviously such fishes
will center themselves here, because the sur-
rounding featureless substrate does not meet
their requirements. I am describing a well-
known phenomenon, one that is the rationale be-
hind constructing artificial fishing reefs. Thus
food and a suitable substrate often appear to be
key features in a habitat that supports large
numbers of fishes. Of course to cite just one or
the other would be an oversimplification, as re-
quirements in both must be satisfied, along with
many other perhaps more subtle needs. The var-
ious s])ecies assembled at such locations inter-
act in a variety of ways; cleaning symbiosis is
one such interaction, and undoubtedly an impor-
tant one, but hardly the prime reason for them
being there.

CHANGES IN HABITS WITH TIME

Uncertainty remains regarding changes in
habits with time. The picture of activity devel-
oped in this report was derived directly by ob-
serving activity and also indirectly by examining
both digestive-tract contents and the specific
ectoparasites that infest the various fishes. But
these methods only define situations that exist
over a relatively brief span of time. Data on
individual activity over longer periods are need-
ed. Certainly habits of individuals change with
time, but how much change and over how much
time? The fact that material in the digestive
tracts frequently occurs in sharply delimited
homologous blocks indicates that these fishes
often feed heavily or even e.xclusively on one
particular type of prey, and then abruptly shift
to something else. Are habits such as a relative
tendency to clean and to clean members of just
one species immutable characteristics of indi-
viduals, or have the observations described in
this report simply defined temporary situations
that the various individuals just happened to be
experiencing at the time they were singled out
for study? It is possible that all seiioritas clean
at one time or another, though not all at once,
and only a few at a time. It is also possible that
a seiiorita, which tends to clean members of just
one species during a given period of cleaning,
may select members of another species during

520

II0B30N: CLEANING SYMBIOSIS

a subsequent period of cleaning. Despite these
questions, the conclusions drawn in this report
are dependent only on an accurate assessment
of the immediate situation, so that their validity
is not affected by whether or not the habits of
individuals under study remain basically un-
changed over time.

A NOTE ON INDIVIDUAL VS.
SPECIES HABITS

Information on variations in feeding behavior
among individual fish under natural conditions
is difficult to acquire. Typically a given behavior
is described as a species characteristic, and the
extent to which this behavior varies among the
different members of the species is unknown.
Observations of cleaning by the senorita dem-
onstrate that different individuals in a popula-
tion may react differently to a given situation.
Unquestionably this phenomenon e.xtends beyond
cleaning behavior to other facets of the animal's
activity. If, as is probable, some of the charac-
teristics of individual fish result from early im-
printing, then dift'erent members of the same
population could be expected to react differently
in certain situations throughout life. In any
event, it seems unquestionable that the behavior
of an individual is considerably more limited than
that descriptive of its species, or even its own
population.

CONCLUSIONS

1. Three inshore species of fishes in southern
California are habitual cleaners: the senorita,
the sharpnose seaperch, and the kelp perch. A
number of other species clean occasionally as
an incidental adjunct to their regular feeding.

2. The seiiorita may clean throughout its post-
larval life, whereas cleaning by the sharpnose
seaperch is an activity largely of juveniles. The
life-history period during which kelp perch clean
has not been defined.

3. Cleaning is of secondary significance to
these species, although it may be of major sig-
nificance to certain individuals. Only a few of
the many seiioritas present at a given time clean,

and the same seems to be true of the kelp perch.
The incidence of cleaners is much higher among
juvenile sharpnose seaperch, but the adults of
this species do not seem to clean regularly. The
major food of all three species is free-living or-
ganisms which they pick from a substrate and
midwater.

4. There is little overlap between the cleaning
areas of the three species. The seiiorita is the
major cleaner in southern California inshore
waters by virtue of its great abundance in a
variety of rocky habitats. However, the kelp
perch may be the predominant cleaner in the
canopy region of the kelp beds, where the spe-
cies concentrates, and the sharpnose seaperch
is the predominant cleaner where it occurs at
depths below about 20 to 30 m and/or water
under 12° or 13° C, even though the senorita
may be more abundant.

5. The seiiorita and sharpnose seaperch do not
establish well-defined stations at which they re-
ceive other fishes seeking to be cleaned — a situ-
ation frequently described for other cleaner
fishes. Rather, as they move from place to place,
individuals of these species approach and clean
other fishes in various different locations.

6. Cleaning activity by these species is essen-
tially limited to removing ectoparasites from the
external body surfaces of fishes. They do not
ordinarily take parasites of the oral and branch-
ial cavities. The dentition of the senorita and
kelp perch, which is similar and which includes
a number of long, curved canines that project
forward at the front of each jaw, seems espe-
cially suited to pick ectoparasites.

7. The major prey taken by these fishes
through cleaning are caligid copepods and gnath-
iid iso]3od larvae. The species of pai-asite taken
most often by the seiiorita and sharpnose sea-
perch is Caligus hohsoni.

8. Some species of fishes are cleaned far more
often than others, and many species that co-
occur with these cleaners are not cleaned at all.
The fishes most frequently cleaned are those
which at the same time are most abundant and
most heavily infested with ectoparasites. The
most numerous ectoparasites on these fishes are
caligid copepods, the most abundant of which is
C. hohsoni.

521

FISHERY BULLETIN: VOL. 69. NO. 3

9. Cleaning effectively reduces the number of
ectoparasites that infest the external body sur-
faces of fishes that interact with the cleaners.

10. At any given time, many individuals of
the more frequently cleaned species are in need
of cleaning. Nevertheless, in activity involving
the seiiorita, infested fishes do not ordinarily
attempt to initiate cleaning but instead wait for
cleaning to be initiated by the cleaner. Because
the vast majority of sefioritas are not cleaners,
or at least are not currently predisposed to clean,
i-andom efforts to solicit cleaning from sefioritas
in the population at large would not be adaptive.

11. When initiating its cleaning activity, a
given individual seiiorita tends to approach and
clean members of only a single species of fish.

12. Because the vast majority of sefioritas are
not currently predisposed to clean and because
there are no well-defined cleaning stations, the
unnatural-appearing posture assumed by a fish
approached by a cleaner is an important cue in
advertising the location of available cleaning to
other fish in need of this service.

13. Fishes being cleaned probably experience
some degree of stress. The color changes ex-
hibited by some fishes when being cleaned are
essentially manifestations of this stress; sec-
ondarily, they may have assumed a signal-func-
tion in certain cleaning interactions.

14. While intimately associated with the fishes
they clean, sefioritas frequently become infested
themselves by the same parasites they are at-
tempting to remove from these other fishes.

15. Cleaning activity is sharply curtailed when
visibility is reduced by turbid water or when
there is strong water movement, such as a heavy
surge.

16. Cleaning activity among these fishes is a
diurnal phenomenon. There is no evidence that
it continues after dark.

17. Any so-called "immunity" from predation
that a cleaner may enjoy probably relates (1) to
an ability to recognize predators that are not in-
tent on feeding and to limit cleaning to such indi-
viduals, and (2) to the fact that behavior exhib-
ited by a cleaner servicing a predator is so unlike
that of pi-ey that the predator does not regard the
cleaner as food. However, their role as cleaners
probably does not afford these fish any security

from being eaten during noncleaning situations.

18. Cleaners are widespread among small-
mouthed marine fishes that characteristically
pick tiny organisms from a substrate. This mode
of feeding, especially when combined with the
capacity to pick tiny prey that are adrift in mid-
water, preadapts fishes to the cleaning habit.

19. There is no basis for the contention that
many of the good fishing grounds in southern
California are such because fishes have congre-
gated to be cleaned by resident cleaners.

20. Feeding behavior varies significantly
among individuals of at least some species. Thus
the habits of an individual can be more limited
than those descriptive of its species or even its
own population.

ACKNOWLEDGMENTS

Lloyd D. Richards assisted me in collecting
the data for this study. I thank Roger F. Cressey
and Thomas Bowman, U.S. National Museum,
who identified the parasitic copepods and iso-
pods, respectively, around which much of this
study is centered. I thank, too, Carl L. Hubbs
and Richard H. Rosenblatt, Scripps Institution
of Oceanography, and John R. Hunter, U.S. Na-
tional Marine Fisheries Service, for helpful com-
ments on a draft of the manuscript.

REFERENCES

Clarke, T. A.

1970. Territorial behavior and population dynam-
ics of a pomacentrid fish, the garibaldi, Hypnypops
ruhicunda. Ecol. Monogr. 40: 189-212.
Clarke, T. A., A. 0. Flechsig, and R. W. Grigg.

1967. Ecological studies during Project Sealab II.
Science (Wash., D.C.) 157: 1381-1389.
Cressey, R. F.

1969a. Caligus liobsoni, a new species of parasitic
copepod from California. J. Parasitol. 55 : 431-
434.

1969b. Five new parasitic copepods from California
inshore fish. Proc. Biol. Soc. Wash. 82: 409-427.

1970. Hatschekia pacified new species (Copepoda:
caligoida) a parasite of the sand bass, Paralebrax

522

HOBSON: CLEANING SYMBIOSIS

nebulifer (Giard). Proc. Biol. Soc. Wash. 82:
843-846.
Cressey, R. F., and E. a. Lachner.

1970. The parasitic copepod diet and life history
of diskfishes (Echeneidae) . Copeia 1965 : 310-318.

ElBL-ElBESFELDT, I.

1955. Uber Symbiosen Parasitismus und andere
besondere zwischenartliche Beziehungen tropis-
cher Meersfische. Z. Tierpsychol. 12: 203-219.
Feder, H. M.

1966. Cleaning symbiosis in the marine environ-
ment. In S. M. Henry (editor), Symbiosis, Vol. 1,
p. 327-380. Academic Press, New York.

Gotshall, D. W.

1967. Cleaning symbiosis in Monterey Bay, Cali-
fornia. Calif. Fish Game 53: 125-126.

HOBSON, E. S.

1965a. Forests beneath the sea. Animals 7: 506-

511.
1965b. A visit with el barbero. Underwater Nat.

3(3): 5-10.
1965c. Diurnal-nocturnal activity of some inshore

fishes in the Gulf of California. Copeia 1965:

291-302.

1968. Predatory behavior of some shore fishes in
the Gulf of California. U.S. Fish Wildl. Serv.,
Res. Rep. 73, 92 p.

1969a. Comments on certain recent generalizations
regarding cleaning symbiosis in fishes. Pac. Sci.
23: 35-39.

1969b. Remarks on aquatic habits of the Galapagos
marine iguana, including submergence times,
cleaning symbiosis, and the shark threat. Copeia
1969: 401-402.

HUBBS, C. L., AND L. C. HUBBS.

1954. Data on the life history, variation, ecology,
and relationships of the kelp perch, Brachyistms
frenatiis, and embiotocid fish of the Californias.
Calif. Fish Game 40: 183-198.

LiMBAUGH, C.

1955. Fish life in the kelp beds and the effects of
kelp harvesting. Univ. Calif. Inst. Mar. Resour.
IMR Ref. 55-9, 158 p.

1961. Cleaning symbiosis. Sci. Am. 205: 42-49.

LONGLEY, W. H., AND S. F. HiLDEBRAND.

1941. Systematic catalogue of the fishes of Tor-
tugas, Florida. Pap. Tortugas Lab. 34. Carnegie
Inst. Wash. Publ. 535, 331 p.
LosEY, G. S., Jr.

1971. Communication between fishes in cleaning
symbiosis, hi T. C. Cheng (editor), Aspects of
the biology of symbiosi.s, p. 45-76. Univ. Park
Press, Baltimore.
Miller, D. J., D. Gotshall. and R. Nitsos.

1965. A field guide to .some common ocean sport
fishes of California. 2d revision. California De-
partment of Fish and Game, 87 p.

QUAST, J. C.

1968. Observations on the food of the kelp-bed
fishes. In W. J. North and C. L. Hubbs (editors),
Utilization of kelp-bed resources in southern Cal-
ifornia, p. 109-142. Calif. Dep. Fish Game, Fish
Bull. 139.

Randall, J. E.

1958. A review of the labrid fish genus Labroides,
with descriptions of two new species and notes on
ecology. Pac. Sci. 12: 327-347.
1962. Fish service stations. Sea Frontiers 8:
40-47.

ROEDEL, P. M.

1953. Common ocean fishes of the California coast.
Calif. Dep. Fish Game, Fish Bull. 91, 184 p.
Shiino, S. M.

1956. Copepods parasitic on Japanese fishes. 12.
Family Lernaeopodidae. Rep. Fac. Fish. Prefect.
Univ. Mie 2: 269-311.
Turner, C. H., E. E. Ebert, and R. R. Given.

1969. Man-made reef ecology. Calif. Dep. Fish
Game, Fish Bull. 146. 221 p.

Wilson, C. B.

1917. North American parasitic copepods belonging
to the family Lernaeidae with a revision of the
entire family. Proc. U.S. Natl. Mus. 53: 1-150.

1935. Parasitic copepods from the Pacific coast.
Am. Midi. Nat. 16: 776-797.

YOUNGBLUTH, M. J.

1968. Aspects of the ecology and ethology of the
cleaning fish, Labroides phthirophagus Randall.
Z. Tierpsychol. 25: 915-932.

523

GRAY WHALES, Eschrkhtius robustus, AVOID THE UNDERWATER
SOUNDS OF KILLER WHALES, Orcinus orca

William C. Cummings and Paul 0. Thompson'

ABSTRACT

Underwater sound playback experiments were undertaken to determine if gray whales would avoid the
sounds of killer whales. When presented killer whale "screams" from an underwater projector, the
gray whales swam directly away from the sound source. Controls of no intended stimulus, pure tones,
and random noise generally failed to induce an avoidance. It appeared that gray whales localized the
killer whale sounds and avoided them as a sign of potential danger.

Killer whales, Orcimis orca, are known to attack
large marine mammals, including gray whales,
Eschric.hthis robustus (Scammon, 1874; More-
john, 1968). Several accounts of such attacks
were related to the first author by observers who
witnessed these events. Among these were Dr.
Carl L. Hubbs of Scripps Institution of Ocean-
ography, University of California, and Alan
Baldridge, Hopkins Marine Station, Stanford
University. In January 1952, Dr. Hubbs saw a
gray whale that swam into the thick kelp beds
off La Jolla, Calif., apparently fleeing from a
group of killer whales. Off the Point Lobos
State Reserve, Carmel, Calif., Baldridge ob-
served a gray whale calf being eaten by six to
seven killer whales. Other observers had seen
the initial attack which also involved the mother
whale. When Baldridge arrived, the killer
whales were chewing on the lips, tongue, and
throat of the dead young gray whale.

Killer whales produce a variety of underwater
phonations, including high pitched "screams"
and trains of well-separated clicks (Schevill and
Watkins, 1966). Underwater sounds have been
recorded from about one-half of the known spe-
cies of marine mammals, and probably all are
capable of some vocal behavior. However, ex-
cept for the echolocating abilities of porpoises
and a few of their own behaviors associated with
sound pi'oduction, very little is known about the

* Naval Undersea Research and Development Center,
San Diego, Calif. 92132.

significance of underwater sound to marine
mammals — virtually nothing where the large
whales are concerned.

Taking advantage of the gray whales' migra-
tion in nearby waters, we conducted underwater
sound playback experiments to find out if they
would react to the underwater sounds of killer
whales, possibly avoiding them as a sign of
danger.

METHODS

The experiments took place off Point Loma,
San Diego, Calif., during successive migrations
of gray whales in January 1969 and 1970. Each
year about 11,000 of these whales pass San Diego
on their southward migration to the breeding
grounds off Baja California and the Mexican
mainland (Rice, 1970). The whales, some with
calves, return to our waters in the early spring
on their way back to the Bering Sea and the
Arctic Ocean.

Field work was done from a large catamaran,
RV Sea See, which served as a stable and roomy
platform, moored in 30 m of water, 33 m sea-
ward of an extensive kelp bed. The ship held
a northerly heading at the mooring. Gray whales
normally funneled through this location staying
relatively close to the coast, but avoiding the
thick kelp.

Three kinds of acoustic stimuli were prepared
on magnetic tape — a natural sequence of
"screams" from killer whales, originally record-

Manuscript accepted March 197],

FISHERY BULLETIN; VOL. 69, NO. 3. 1971.

525

FISHERY BULLETIN: VOL. 69, NO. 3

ed off Dabob Bay, Wash.; a matching sequence
of two simultaneous pure tones of 500 and 2000
Hz that resembled the major frequency com-
ponents in most of the recorded killer whale
"screams" and with the same on-off times as
the "screams"; and a similarly timed sequence
of random noise in the band fiom 500 to 2000
Hz. Random noise and pure tone were used
as control stimuli in addition to a third control
wherein there was no playback or any intended
stimulus, and the whales were allowed to pass
relatively undisturbed. The ship's equipment
was silenced throughout the experiments and
we made no unnecessary noises.

The sound projector (designed and built at
our laboratory) was lowered to 12 m below the
surface of the water. It was powered with a
250-w amplifier (Optimation)' connected to the
tape recorder (Uher 4200) used for playback.
We monitored the output from a receiving hydro-

phone ( Wilcoxon, Type M-H90-A) located at the
same depth as the projector, 12 m away. Cal-
deron and Wenz (1967) have described this cal-
ibrated monitoring system. Underwater signals
picked up by the receiving hydrophone led to
one track of another Uher stereo tape recorder.
The other track carried our running commentary
of the whales' behavior. Peak source level of
the killer whale signals (Figure 1) and the play-
back control stimuli was nearly constant- — 151 db
re 1 /xNewton m' ( = 51 db i-e 1 dyne'cm') at 1 m
in the 1969 experiments, and 176 db in 1970.
Because of the natural propagation losses mea-
sured in the area, we expected sound pressure
levels of the projected sounds to reach the pre-
vailing ambient sea noise level in the third-oc-
tave band at 500 Hz, at about 1100 to 1400 m.

' The use of trade names is merely to facilitate de-
scription; no endorsement is implied.

3-

N2.

w

— 0

::^^-

T — I — I — I — i — I — I — I — I — i — I — I — I — I — i — I — I — r— 1 — r

1 2 0

-\ — i — I — I — r

Time [seconds ]

Time [seconds]

FiGl'RE 1. — Spectrograms of killer whale "screams" that were played back to migrating gray whales. Of 141
signals on the playback, 83 were very similar to the one at top, left. The othcr.s shown are in clockwise order
according to their frequency of occurrence on the tape (30, 19, 9). The analyzing filter bandwidth was 20 Hz.

526

CUMMINGS and THOMPSON: GRAY WHALES

Besides no playback, used in the 1969 exper-
iments, random noise and pure tone served as
additional controls in 1970.

Gray whales come by Point Loma at any time
during the migration season, day or night, as
individuals or in small groups of two to five
animals. However, for the total of 5 weeks
at sea, we had to work in bright daylight, 0830
to 1630 hr, because of earlier difficulty in seeing
the whales in subdued light. Undisturbed whales
moved along in a southerly course at average
speeds of 10 km/hr, blowing from one to three
times every 1 to 14 min. We have also seen
killer whales off Point Loma.

Migrating gray whales produce underwater,
low-frequency moaning sounds in a band from
20 to 150 Hz (Cummings, Thompson, and Cook,
1968) . These sounds last 1.0 to 1.7 sec.

We began an experiment upon seeing an on-
coming whale or group of whales that was not
encumbered with small boat traffic. Playbacks
were generally started when the whales were
150 to 450 m away, toward the north. The ex-
periments were alternated so that successive
contacts would not encounter the same situation.
Sessions lasted 30 to 100 min, after which the
whales had passed the ship or disappeared.
There were 77 experiments (77 contacts) in-
volving a total of 132 gray whales. The ap-
pearance of "whale-watching" or fishing boats
invalidated our work with numerous other con-
tacts. They not only interfered with the whales'
progress, but their underwater sounds consider-
ably reduced the playback signal-to-noise ratio.

EXPERIMENTAL RESULTS

The reactions of gray whales to the projected
killer whale sounds were spectacular. Blowing
whales, or those running at the surface, imme-
diately swirled around and headed directly away
from the killer whale sound source. We have
no idea of how quickly the submerged whales
reacted, but subsequent surfacings were away
from the killer whale sound source.

Most whales fled towards the north. How-
ever, if their previous southerly course had taken
them seaward of the ship and the sound source,

they turned and swam toward the open sea.
Gray whales coming from the general direction
of the kelp, or those very close to it, fled into
this heavy growth and stayed in one general lo-
cation until we stopped the killer whale stimulus.

Whales came about and resumed a southerly
course for Mexico 5 to 30 min after the killer
whale sound stopped. If we renewed the play-
back, before the whales passed by, they again
fled northward from the sound source. On sev-
eral occasions, we repeated the experiments on
the same contact up to three times, each with
similar results.

Of the 36 contacts principally involving killer
whale playback, 30 avoided the sound source,
3 were questionable because we never saw them
after playback, and 3 passed the ship as normal,
without an apparent avoidance (Table 1) . How-
ever, one of the last-mentioned was a single
whale that had already come very close to the
east-west line arbitrarily set on the projecting
transducer. This whale could have just as easily
avoided the sound source by swimming to the
south.

Table 1. — Reaction of gray whales contacted on 77

occasions to various stimuli.

[1-4 whales in a contact; 132 whales in all.]

Random
noise

Pure
tones

No
ploybock

Killer

whole

"screams"

Avoidance
No ovoidance
Questionable

0
21
0

30
3
3

All 21 contacts not encountering an intended
stimulus (no playback) moved along towards
the south in normal fashion. Two contacts of
the 10 that received pure tone avoided the sound
source. However, 1 of these 2 turned only mo-
mentarily. It then resumed the southerly course,
still in the presence of the playback stimulus.
Of the 10 contacts presented with random noise,
2 avoided by turning towards the north for a
very short distance. However, both of these
gray whales seemed to be startled only for the
moment; then quickly turned a second time and
swam down past the random noise sound source.

Two of the 8 contacts that did not avoid
random noise and 2 of the 8 that did not avoid

527

FISHERY BULLETIN: VOL. 69, NO. 3

pure tone (Table 1) did flee the killer whale
source when we projected it to them before they
passed by the sound projector. We did not pro-
ject killer whale sound to the other contacts
that did not avoid random noise and pui-e tone.

Observers on board noted how little of the
avoiding whales' bodies showed above the sur-
face and their unusually small surface distur-
bance. In many instances their blows were in-
visible and even blows at close range were
scarcely audible. In contrast, the surfacing of
undisturbed whales involved the simultaneous
appearance of head and blow accompanied by
a well-defined surface wake. Their blows were
generally visible, and they were audible at close
range. After their first appearance, the undis-
turbed whales showed their backs and sometimes
tossed their flukes high into the air. On the
other hand, it was diflicult to spot the fleeing
whales.

We thought that if gray whales associated
the projected killer whale "screams" with po-
tential danger, they would have left the area
silently to lessen their chance of detection. For
example, Schevill (1964) noted that belugas,
Delphinapterus leucas, became silent in the
vicinity of two killer whales. Upon analyzing
our data, it turned out that only 2 gray whale
phonations appeared on the tapes during killer
whale periods, whereas 47 occurred during the
control periods.

Gray whales on the breeding grounds fre-
quently exhibit a behavior termed "spying-out"
(Gilmore, 1961) wherein the head comes ver-
tically out of the water for several seconds. "Spy-
ing-out" in the breeding lagoons seems to be
associated with searching for channels; it is also
done when the whales are pressed by small boats
(communication from Dr. Joseph R. Jehl, San
Diego Natural History Museum) . Since we have
seen this behavior over the past 6 years only
three times, we assume that migrating gray
whales rarely "spy-out." However, gray whales
in the present experiments inevitably "spied-
out" after fleeing into the thick kelp following
killer whale playbacks.

As a result of these experiments we conclude
that gray whales apparently recognize the voice
of a killer whale, that they can easily localize

the sounds underwater, and that they flee killer
whale phonations probably as a sign of potential
danger. Such avoidances consist of several be-
haviors that appear to function as protective
mechanisms — sound localization, silence, rapid
escape, i-educed exposure, and visual search.

DISCUSSION

Walker (1971) has expressed the opinion that
the function of "spy-hopping" ("spying out")
by gray whales is not that ". . . the whale looks
around, spying out possible dangers such as
ships, or even spotting shore landmarks as aids
to navigation." In reply he points out that "In
the vertical posture the law of gravity takes
over, conveying food from the whale's mouth to
a capacious four-chambered stomach. Although
a gray whale can swallow when horizontal, the
vertical position allows it to clean entangled de-
bris from the filter and to wash food down to the
throat for quick ingestion." Walker further re-
ported ". . . that in the 'spy-hopping' position
their [gray whales'] range of vision is limited
and that they navigate mostly by echolocation,
. . . ." On the other hand, in the same report is
the following portion of a caption to a photo-
graph showing a breaching gray whale. "The
catapulting action, he [Dr. Walker] believes,
enables the animals to scan the waters around
them and make course corrections when inter-
fering noises prevent them from navigating by
echo-location."

We ai-e not aware of any experimental evi-
dence that shows whether a gray whale "spy-
hops" to look around or to swallow food. Nor
is there any substantial evidence that migrating
or breeding gray whales feed very much. To
the contrary, there is hard evidence (summa-
rized by Gilmore, 1968) that gray whales fast
on their way to the breeding grounds, at the
grounds, and on the return triii north.

Relative to the killer whale attack cited earlier,
Baldridge reported that the mother frequently
"spy-hopped" from a distance as the killer whale
chewed on her dead calf.

In view of the above, the context of "spy-
hopping" exhibited by gray whales during our
experiments would seem to imply that this be-

528

CUMMINCS and THOMPSON: GRAY WHALES

havior had a visual function, i.e., they were
probably looking for killer whales. This impli-
cation does not necessarily exclude swallowing,
but we doubt that the gray whales were feeding
under these circumstances.

Moreover, concerning Walker's assertion that
gray whales "navigate mostly by echolocation,"
although it has been clearly demonstrated that
porpoises can echolocate underwater objects (re-
viewed by Norris, 1969) , it is not known whether
they normally navigate at sea by this means.
"Echolocation-like" (Asa-Dorian and Perkins,
1967) and "echolocation" sounds (Poulter, 1968)
were recorded in the presence of gray whales,
but there was little evidence that the sounds
actually were from the whales. There are in-
numerable sounds in the ocean and many pos-
sible sources, but the matching correlations are
often difficult to achieve. In any event, we pre-
fer not to use the term "echolocation" in de-
scribing the underwater sounds of animals un-
less they are known to have such a function.
Although we have recorded a few clicklike sounds
during five seasons of work with gi'ay whales,
we have never been able to associate them with
the whales. The clicklike sounds that were re-
corded, while using an array of hydrophones and
a technique of computing sound source locations,
originated from an area where, apparently, there
were no gray whales.

Bioacousticians are not in a position to say
with any certainty that gray whales do not
echolocate; future experimental work could pos-
sibly show that they do. However, our own
research with 7 of the 10 species of mysticate
whales has yet to reveal any data to suggest that
a member of this order uses underwater echolo-
cation.

Whales normally exhale at the surface of the
water with the blowholes exposed, but Hubbs
(1965) has reported underwater blows by four
species of whales — humpback, Megaptera no-
vaemigliae; fm., Balaenopter a phy solus; striped
dolphin, Lagenorhynchus obliquidens; and the
gray whale. In addition, he noted gray whales
to refrain from spouting, skip an inhalation, or
barely protrude their blowholes in the presence
of killer whales. In the same report, Hubbs
associated these behaviors with "strange or

frightening stimuli." We were not close enough
to see if fleeing gray whales exhaled underwater,
but our other cited observations of gray whales
covertly avoiding the killer whale sounds cer-
tainly parallel Hubbs' observations.

Unfortunately, there was no record of the
killer whales' behavior during the original re-
cordings of the phonations used for playback.
We advise others who may be involved with
sound playback to use appropriately meaningful
signals, whenever possible. For example, under-
water sounds that are part of an animal's re-
productive behavior may have little or no effect
on nonbreeding animals. Likewise, feeding
sounds may not affect animals that are in a
state of alarm. If possible, we would have com-
pared the results of playing back two sets of
killer whale sounds in the present experiments
— one recorded from attacking whales in a pred-
ator-prey situation, if indeed killer whales utter
sounds at this time, and another from killer
whales that apparently were not feeding or
preying.

Based on the methods of this study, our co-
workers. Dr. James F. Fish, and John S. Vania
subsequently used killer whale sound playback
to keep white whales, Delphinapterus leucas,
from entering the Kvichak River, Alaska, where
they eat young salmon before the fish can get
to the open sea (Fish and Vania, 1971).

ACKNOWLEDGMENTS

We thank Dr. James F. Fish for helping with
the field work and reviewing the report; Bruce
C. Parks and Robert Z. Hester for operating
the research vessel; Richard N. Bray, George
E. Lingle, and John B. Webster for assisting
with the data analysis; and Shelley L. Steahl
for helping to prepare the manuscript.

LITERATURE CITED

Asa-Dorian, P. V., and P. J. Perkins.

1967. The controversial production of sound by the
California gray whale, Eschrichtius gibbosiis.
Nor. Hvalfangst-Tid. (Norw. Whaling Gaz.)
56(4) : 74-77.

529

FISHERY BULLETIN: VOL. 69, NO. 3

Calderon, M. a., and G. M. Wenz.

1967. A portable, general-purpose underwater
sound measuring system. Nav. Undersea Warf.
Cent, San Diego, Calif., TP 25, 46 p.

CuMMiNGS, W. C, P. 0. Thompson, and R. Cook.

1968. Underwater sounds of migrating gray
whales, Eschrichtius glaucus (Cope). J. Acoust.
Soc. Am. 44: 1278-1281.

Fish, J. F., and J. S. Vania.

1971. Killer whale, Orchins orca, sounds repel white
whales, Delpliinapterus leiicas. Fish. Bull., U.S.
69: 531-535.
GiLMORE, R. M.

1961. The story of the gray whale. Pioneer Print-
ers, San Diego, Calif., 17 p.
1968. The gray whale. Oceans Mag. 1(1): 9-20.
HuBBS, C. L.

1965. Data on speed and underwater exhalation of
a humpback whale accompanying ships. Hval-
radets Skr. 48: 42-44.
MOREJOHN, G. V.

1968. A killer whale — gray whale encounter. J.
Mammal. 49: 327-328.

NORRIS, K. S.

1969. The echolocation of marine mammals. In
H. T. Andersen (editor), The biology of marine

mammals, p. 391-423. Academic Press, New York
and London.

POULTER, T. C.

1968. Vocalization of the gray whales in Laguna
Ojo de Liebre (Scammon's Lagoon) Baja Cali-
fornia, Mexico. Nor. Hvalfangst-Tid. (Norw.
Whaling Gaz.) 57(3): 52-62.

Rice, D.

1970. Long distance swimmers of the East Pacific,
gray whales. Pac. Search 4(8): 2-3.

Scammon, C. M.

1874. The marine mammals of the north-western
coast of North America. John H. Carmany and
Company, San Francisco, Calif., 319 p.

SCHEVILL, W. E.

1964. Underwater sounds of cetaceans. In W. N.
Tavolga (editor). Marine bio-acoustics, proceed-
ings of a sjTnposium held at the Lerner Marine
Laboratory, Bimini, Bahamas, April 11 to 13, 1963,
p. 307-316. Pergamon Press, Symposium Publi-
cations Division.

SCHEVILL, W. E., AND W. A. WATKINS.

1966. Sound structure and directionality in Orcinus
(killer whale). Zoologica 51: 71-76.
Walker, T. J.

1971. The California gray whale comes back.
Natl. Geogr. Mag. 139(3) : 394-415.

NOTICE THIS MATERIAL MAY BE
PROTECTED BY LAW
(TITLE 17 U.S. CODE)

530

KILLER WHALE, Orcinus orca, SOUNDS REPEL WHITE WHALES,

Delphiiiapterus leucas

James F. Fish' and John S. Vania"

ABSTRACT

This study was conducted to determine if the migration of white whales up the Kvichak River, Bristol
Bay, Alasl<a, could be stopped by playing high-intensity underwater sounds to them. While in the
river the whales feed on salmon smolt migrating down to the sea. Transmission of killer whale sounds
was found to be an effective means for keeping the whales out of the river. During control periods
when sound was not projected, the whales moved freely in and out of the river. A permanent play-
back system could be installed with little difficulty and would result in a significant reduction in the
number of smolts consumed by belugas in the Kvichak River.

White whales, or belugas, Delphinapteriis leu-
cas, commonly travel 20 to 30 km up Alaska's
Kvichak River (Figure 1) on the flood tide and
back down on the ebb, foraging on available food

Figure 1. — Location of the study area.

' Naval Undersea Research and Development Center,
San Diego, Calif. 92132.

^ Alaska Department of Fish and Game, Anchorage,
Alaska 99502.

organisms along the way. This twice-daily
movement of from 50 to over 500 whales occurs
during May and throughout most of June. It
ceases only after boat traffic from the seasonal
salmon fishery becomes heavy.

The Kvichak River supports the most exten-
sive run of red salmon, Oncorhynchus nerka, in
the world. These runs range from 1 to 45 million
fish per year. Lake Iliamna, the largest lake in
Alaska, located about 80 km up the Kvichak,
is the principal rearing area for the young salm-
on before they migrate to the sea as 1- or 2-year
olds. The annual migration of smolt occurs dur-
ing the end of May and the first 2 weeks in June
with the peak of migration occurring about the
first of June.

Field studies by the Alaska Department of
Fisheries (1956) in the early 1950's showed that
beluga predation on the salmon smolt occurred
when the young fish were migrating to sea and
appeared to be most extensive in the confines
of the river. As the smolt moved into Kvichak
Bay, they scattered and became less vulnerable
to predation. Attempts were made to keep the
belugas out of the river by chasing them with
motorboats and by dropping small charges of
explosives into the river. These methods were
not very successful and were difficult to use dur-
ing inclement weather or at night.

From 1963 to 1968 Vania projected various
sounds, including killer whale sounds, noise, and
music, underwater to the belugas in an attempt

Manuscript accepted March I97I.

FISHERY BULLETIN: VOL. 69. NO. 3, 1971.

531

FISHERY BULLETIN: VOL, 69, NO. 3

to keep them out of the river. There was no
reaction to the noise or music. The killer whale
sounds were only partially successful, appar-
ently because the playback level was too low.
His equipment was not designed for underwater
sound transmission. Most other woi-kers at-
tempting to influence the movement of wild
whales with sound have been unsuccessful. How-
ever, in nearly all of these experiments the
projected sounds did not exceed 140 to 150 db,
re 1 ^Newton/ m" ( = 40 to 50 db, re 1 dyne/cm')
at 1 m. One exception was a sound playback ex-
periment on California gray whales, Eschrich-
tius robustus, by Cummings and Thompson (this
issue of Fishery Bulletin) where a high-power
transmitting system was used and the whales
did react to the sounds. Their transmitting sys-
tem was similar to the high-power system de-
scribed here which we used to transmit killer
whale sounds to belugas in the Kvichak River
in June 1970.

METHODS

The primary high-jjower transmitting system,
operated from Station A (Figure 2) , consisted of
a Uher tape recorder," a small impedance-match-
ing preamplifier, a 250-w Optimation power
amplifier, and a sound projector developed and
built by the Naval Undersea Research and De-
velopment Center. Frequency response of this
system was ±3 db from 250 to 4000 Hz, limited
by the projector. A secondary, battery-operated
playback system, operated from a small boat at
Station B (Figure 2), utilized a Uher tape re-
corder, a 40-w Bogen amplifier powered by a
motorcycle battery, and a J-9 sound projector;
system response was =t3 db from 200 to 6000 Hz.

A calibrated recording .system, consisting of
a Wilcoxon hydrophone, a Uher tape recorder,
a sonar calibration box, and a modified GR
Octave-Band Analyzer, was used to measure the
sound pressure level of the playback signals at
various points throughout the river and to record
the vocalizations from the belugas. This system
was described by Calderon and Wenz (1967).

" The use of trade names is merely to facilitate de-
scriptions; no endorsement is implied.

Figure 2. — Enlarged drawing of the study area. Trans-
mitting stations were located at A and B. The regions
indicated by numerals are locations where playback
sound pressure levels were measured.

We selected killer whale, Orcimis orca. vocal-
izations for transmission because of their out-
standing acoustic properties and because killer
whales are known to kill and eat the relatively
slow-swimming white whales (Scammon, 1874:
92; Dergerbol and Nielsen, 1930; Kleinenberg
et al., 1964: 292). A long-play tape was made
from "screams" and clicks recorded from killer
whales at sea. We do not know, however, what
behavior was associated with their sound pro-
duction.

In the first 10 playback trials, the sound, trans-
mitted only from Station A, was not turned on
until the approaching belugas were sighted.
But in subsequent trials, when we transmitted
from both A and B, we started the playback
as soon as the tide changed. Weather and light
permitting, a new trial started with each flood
tide and lasted from 15 min to 2 hr — as long as
necessary to either move the whales back down
the river (in those trials where they were per-
mitted to move part way up before the sound

532

FISH and VANIA: KILLER WHALE SOUNDS

was turned on) or keep them from moving- up
the river (when the sound was turned on before
the whales started upriver) .

We had an excellent view of the river from
the third floor of a building about 25 m above
the water at Station A. Frequent low-altitude
flights in small planes provided a check on the
exact location of the whales when they could
not be seen from the building. The white-col-
ored whales were easy to see in the muddy brown
river.

In all, there were 14 playback trials plus 7
control trials in which the whales were observed
but sounds were not transmitted. The number
of whales involved in each trial ranged from 50
to near 500 with about 100 being the average
group size. Because several years of observa-
tions indicated the belugas move up the river on
every incoming tide, we did not feel it was nec-
essary to have an equal number of transmission
and control trials. Consequently, we introduced
a control after no more than four successive
transmissions, primarily to determine if the be-
lugas had stopped using the river as a result of
the sound playbacks.

The sound pressure level of the playback
sounds transmitted from Station A was mea-
sured at 6 locations in the river within 4 km of
the source (Table 1). All levels reported in
this paper are in db, re 1 fiN/m'. Sandbars pre-
vented good transmission across the river, par-
ticularly during the early stages of the flood
tide when some of the bars were covered by less
than 0.5 m of water. For example, the sounds
projected from Station A were below the back-
ground noise level at Location 6 (Figure 2) . The

Table 1. — Sound pressure level (db re 1 /xN/m') of
playback signals and ambient noise at the indicated
locations.

Location,
Fig. 2

Signal
broad-
band

Ambient noise

Broad-
bond

500-5000
Hz bond

1 m from

Source A

170

120

No data

I

115

103

96

2

132

90

84

3

107

91

85

4

103

95

90

6

Below

ambient

98

95

best transmitting channel was downriver toward
Telephone Point (Location 2), where a level of
132 db was measured for the playback signals.
Beyond this area, the signal level dropped off
quickly because of the shallow water which ex-
tended out a considerable distance from the
Point. Most of the energy of the playback
sounds occurred in a frequency band from 500
to 5000 Hz; thus we measured ambient levels
in this band in addition to making broadband
ambient measurements.

RESULTS OF PLAYBACK EXPERIMENTS

In the first seven transmission trials, we let the
whales move up the river on the west side to
within approximately 2 km of the sound source
before turning on the playback. The first six
times, the animals turned immediately when the
sound began and swam directly out of the river
against the strong incoming tide. Their rate
of blowing increased and they spent more time
at the surface of the water, making it very easy
for us to observe their course. On the 7th trial,
some of the animals crossed to the opposite side
of the river when the sound started and swam
downstream along the sandbar (Location 4).
The others remained just ofi" Telephone Point
for an hour, then moved out of the river.

It was difl^cult to see the approaching belugas
on the 8th trial because of low light, and they
had already moved up to Location 6 before we
started transmitting. About half of the 100
whales continued up the river; the others turned
and swam back out along the sandbar. On the
next trial, the animals were first seen moving
up the river along the sandbar. Possibly they
learned from the previous eight transmissions to
avoid the side of the river where the sound pro-
jector was located. They continued up to the
end of the bar, even after the sound was turned
on, but then rounded it and moved back down the
river on the other side of the bar (Location 5).

The belugas similarly rounded the upriver end
of the sandbar on the 10th trial; but, instead
of turning around, they swam to the shore (Lo-
cation 7) and continued up the river very close
to the bank. Poor transmission to this location

533

FISHERY BULLETIN: VOL. 69, NO. 3

from Station A and the reaction of the whales
during the 10th trial made it necessary to use
a second transducer simultaneously at Station B.
A copy of the Station A playback tape was used
at Station B, but it was not possible to synchro-
nize the playback sounds from the two projec-
tors. In the subsequent four trials, we turned
on the playback as soon as the tide changed,
thus eliminating the possibility of the whales
going by us unnoticed before the start of trans-
mission. The whales stayed at least 1.5 km down
the river from the sound sources during the four
transmissions using both projectors.

In each of the seven control trials, when no
sound was played, the whales moved directly
up the river with the incoming tide, past the
transmitting stations. They behaved the same
as they did before any of our experiments, with
many individuals passing near the pier at Station
A. However, we could see very few whales from
the viewing station during the killer whale play-
baclis. Low-altitude reconnaissance flights con-
firmed our suspicion that numerous whales were
remaining well down the river out of view dur-
ing the transmissions.

Belugas vocalize extensively (Schevill and
Lawrence, 1949; Fish and Mowbray, 1962).
We recorded their sounds many times at various
places throughout the river, often under ideal
conditions of flat-calm water with no boat traflic.
Once, we drifted in a small boat for over 2 hr
during a no-playback control with a group of
about 500 whales and recorded a spectacular va-
riety of vocalizations from this relatively un-
disturbed herd. The belugas emitted very few
sounds, however, when the killer whale signals
were being transmitted. Quieting of belugas
in the presence of killer whales was noted bj'
Schevill (1964).

CONCLUSIONS AND
RECOMMENDATIONS

Our experiments showed that playback sounds

of killer whales can be used to keep belugas out

of Alaska's Kvichak River. This method was

very effective and practical. Installing and

^maintaining such a playback system for 2 to 3

weeks each year would seem to be an economi-
cally feasible way of reducing beluga predation
on red salmon smolts. Such a system could be
started automatically at the beginning of the
flood tides and, if necessary, left on for their
duration, both day and night. It would not be
seriously affected by adverse weather conditions,
except for a possible reduction in the range over
which the belugas could hear the sounds — be-
cause of higher ambient noise levels in the river
from wind and rough water.

We recommend using two sound projectors,
properly situated to provide good signal levels
all the way across the river. Initially, our trials
with one projector stopped the whales, but the
belugas eventually learned to go up the opposite
side of the river where the playback signals
were very weak or nonexistent. There were
too many sand bars in the river to achieve good
signal levels across the river with one projector,
regardless of its source level.

Although we only used the two-projector sys-
tem for four trials, we do not feel the whales
would habituate and ignore the playback sounds
with continued use. The avoidance of the belu-
gas to this system was striking. The fact that
the whales began swimming up the river again
after nine trials using the single projector was
due, we feel, to their learning to avoid the
source, rather than to habituating to the sounds.
With sound projectors located on both sides of
the river there is probably no channel where
the whales can go up the river without hearing
the playback sounds. On the other hand, even if
the belugas were to habituate after 2 weeks of
playback, this would not significantly affect the
usefulness of the technique. Playback could be
timed to coincide with the 2-week peak of the
smolt run.

After completing this experiment with killer
whale playbacks, we projected a 2500-Hz con-
tinuous tone and 2500-Hz randomly pulsed tones.
The belugas continued up the river during the
continuous-tone playback, but turned back on
the two occasions when pulsed tones were trans-
mitted. Since these playbacks were tried after
the white whales had been subjected to the kill-
er whale sounds for 2 weeks, we cannot spec-
ulate on how naive whales would have reacted.

534

FISH and VANIA: KILLER WHALE SOUNDS

More experiments are necessary before we can
conclude whether or not the belugas recognized
the killer whale sounds as such.

ACKNOWLEDGMENTS

We thank Dr. William C. Cummings for his
suggestions on the manuscript, George E. Lingle
and John B. Webster for assisting with the data,
and the New England Fish Company for pro-
viding laboratory space and aiding with the field
work. Fish's work was supported by Indepen-
dent Research funding of the Naval Undersea
Research and Development Center during his
appointment as a NRC-NUC Postdoctoral Re-
search Associate, and Vania's in part by Fed-
eral Aid to Wildlife Restoration Funds, Project
W-17-R.

LITERATURE CITED

Alaska Department of Fisheries.

1956. Beluga investigation. In 1955 Annual Re-
port, Alaska Fisheries Board and Alaska Depart-
ment of Fisheries, p. 98-106. Rep. 7.
Calderon, M. a., and G. M. Wenz.

1967. A portable, general-purpose underwater
sound measuring system. Nav. Undersea Warf.
Cent., San Diego, Calif., TP 25, 46 p.

Cummings, W. C, and P. O. Thompson.

1971. Gray whales, Eschrichtius robiistus, avoid
the underwater sounds of killer whales. Orchitis
orca. Fish. Bull., U.S. 69: 525-530.
Dergerbol, M., and N. L. Nielsen.

1930. Biologiske lagttagelser over og maalinger af
Hvidhvalen og dens Fostre. Medd. Gronland
77(3): 117-144.
Fish, M. P., and W. H. Mowbray.

1962. Production of underwater sound by the white
whale or beluga, Delphixapterus leucas (Pallas).
J. Mar. Res. 20: 149-162.
Kleinenberg, S. E., a. V. Yablokov, B. M. Bel'kovich,
AND M. N. Tarasevich.

1964. Beluga (Delphinapterus leucas) , investiga-
tion of the species. Translated from Russian by
Israel Program for Scientific Translations for
Smithsonian Institution, IPST No. 1923, 1969,
376 p.

SCAMMON, C. M.

1874. The marine mammals of the north-western
coast of North America. John H. Carmany and
Company, San Francisco, Calif., 319 p.
Schevill, W. E.

1964. Under^vater sounds of cetaceans. In W. N.
Tavolga (editor). Marine bio-acoustics, proceed-
ings of a sjTnposium held at the Lerner Marine
Laboratory, Bimini, Bahamas, .\pr. 11-13, 1963,
p. 306-316. Pergamon Press, Symposium Publica-
tions Division.
Schevill, W. E., and B. Lawrence.

1949. Underwater listening to the white porpoise
(Delphinapterus leucas). Science (Wash., D.C.)
109: 143-144.

\

<^m.

<^

535

DEVELOPMENTAL ABNORMALITIES OF THE FLATFISH Achirus lineatus
REARED IN THE LABORATORY'

Edward D. Houde-

ABSTRACT

Of 31 Achirus lineatus juveniles reared in a single experiment, 26 were abnormal. Abnormalities in-
cluded incomplete eye migration, hooked dorsal fins, the presence of a left pectoral fin, ambicoloration,
and partial albinism. The abnormal specimens have been described and photographed. A single re-
versed specimen, preserved as a nearly metamorphosed individual, also is described. Most of the
abnormal conditions were interrelated. Possible effects of the rearing tank environment on abnormal
development are discussed.

Larvae of lined soles, Achirus lineatus (Lin-
naeus), were reared in the laboratory from
fertilized eggs collected in plankton tows from
Biscayne Bay, Fla. Development and details of
metamorphosis were described by Houde, Futch,
and Detwyler (1970). No developmental ab-
noimalities were detected until metamorphosis
was nearly complete. At 50 days after hatching,
the 31 survivors were examined and 26 (84 SO
were found to be abnormal.

The unique metamorphosis of flatfishes
(Pleuronectiformes) may be responsible for the
high percentage of abnormal specimens reported
for this group in the literature (Norman, 1934;
Hubbs and Hubbs, 1945; Dawson, 1962). Most
of the described abnormal conditions in flatfishes
were encountered in lined soles from this rear-
ing experiment. Abnormalities included, in
order of frequency, (1) ambicoloration (25
specimens), (2) retention of left pectoral fin,
normally lost after metamorphosis (23 speci-
mens), (3) partial or no migration of the left
eye (17 specimens), (4) hooked dorsal fin, (same
17 specimens), (5) partial albinism (1 speci-
men), and (6) reversal (1 siiecimen). Similar
abnormalities have been described previously in

' Contribution No. 198, fi-om the National Marine
Fisheries Service, Tropical Atlantic Biological Labora-
tory, Miami, Fla. 33149.

' Present address: University of Miami. Rosenstiel
School of Marine and Atmospheric Science, Division of
Fishery Sciences, 10 Rickenbacker Causeway, Miami,
Fla. 33149.

Manuscript accepted March 1971.

FISHERY BULLETIN: VOL. 69, NO. 3. 1971.

flatfishes, but are rare in the famil.v Soleidae
(Dawson, 1962) . None have been reported pre-
viously for A. lineatus. The extremely high
percentage of abnormal individuals among lab-
oratory-reared specimens from this experiment
apparently reflects some eff'ect of the aquarium
environment on the development of A. lineatus.
A high proiJortion of pigment-deficient individ-
uals of plaice (Pleuronectes platessa) was as-
sociated with high densities of metamorphosed
specimens in rearing tanks and with low food
levels in the tanks (Shelbourne, 1964, 1965;-
Riley, 1966), but other abnormalities were not
discussed. Although the exact nature of the
influence of the rearing tank on the production
of abnormal specimens of lined soles is unknown,
it is possible that harmful effects are created by
(1) frequent contact with sides of small rearing
tanks, (2) unnatural lighting, and (3) high
concentrations of metabolites. Seshappa and
Bhimachar (1955) reported failure of eye mi-
gration in the tongue sole Cynoglossus semifas-
ciatus (Cynoglossidae) when postlarvae were
kept in the dark. Two of my previous rearing
experiments with A. lineatus also produced ab-
normal individuals. Some juvenile specimens
of other flatfishes, Paralichthys alhigutta (Bo-
thidae) and Gymnachirus ynelas (Soleidae), also
developed abnormally when reared from eggs
hatched in my laboratory. The high incidence
of abnormalities in the reared lined soles sug-
gests that these conditions in flatfishes are not

537

FISHERY BULLETIN: VOL. 69, NO. 3

necessarily genetically controlled. When present
in significant numbers, abnormalities may have
important implications for those considering
flatfishes in aquaculture.

METHODS

Rearing techniques were briefly described and
larval development through metamorphosis re-
ported by Houde et al. (1970). Methods used
to rear A. lineatus were similar to those de-
scribed in detail by Houde and Palko (1970).
The 31 juveniles of lined sole were maintained
in two 75-liter aquariums and fed on frozen
brine shrimp {Artemia salina). Before meta-
morphosis larvae were fed wild zooplankton
which consisted mostly of copepods. Beginning
50 days after hatching and at approximately
1-month intervals, growth was determined by
measuring fish to the nearest millimeter total
length (TL) and then returning them to the
aquariums. Individuals were recorded as nor-
mal or abnormal when they were measured, the
distinction being based on whether the dorsal
fin was hooked.

Beginning 137 days after hatching, some fish
were sacrificed and preserved for detailed ex-
amination. Radiographs were made to study
skeletal structures. Specimens were accessioned
into the fish collection at the Tropical Atlantic
Biological Laboratory.

NORMAL SPECIMENS

Only five specimens were normal in all respects
(Figure 1). Meristics and morphometries of
normal individuals fell within the range of var-
iation for the species (Jordan and Evermann,
1898).

GROWTH AND MORTALITY

Growth was compared between grossly de-
formed specimens with hooked dorsal fins and
normal specimens or those whose only anomalies

Figure 1. — Left side (upper photo) and right side (lower
photo) of 45.8 mm TL normal Achinis lineatus reared
in the laboratory. Dorsal fin was bent when specimen
was preserved but it is normal.

consisted of unusual pigmentation and the pres-
ence of a left pectoral fin. SiJecimens with ab-
normal pigmentation or with left pectoral fins
were classified as "normal" at the time they
were measured because such conditions could
not always be detected in small living juveniles.
Although "normal" individuals initially were
longer than abnormal ones, some compensation
apparently occurred, and little diflference in
lengths was apparent between specimens still
living from the two categories at 250 days after
hatching. Both "normal" and abnormal speci-
mens averaged about 52 mm TL at this time.
No natural mortality occurred for either normal
or abnormal lined soles between 50 and 275 days
after hatching.

538

HOUDE: DEVELOPMENTAL ABNORMALITIES OF Jchirus lineatus

Table 1. — Abnormalities of AchUiis lineatus reared in the laboratory.
A plus symbol indicates the presence of the abnormality and a minus
s\Tnbol indicates its absence.

Specimen
number

Total
length

Pigment on
bfind side

Body

Lef»
pectoral

Hooked
dorsal

fir>

Left eye
migration

mm

%

%

64

32.6

100

100

+

+

incomplete

65

27.5

100

100

+

+

incomplete

6B

29,5

100

100

+

+

incomplete

69

39.6

100

100

+

+

incomplete

72

45.8

100

100

+

+

incomplete

73

41.6

100

100

+

+

incomplete

84

42.7

100

100

+

+

incomplete

85

48.0

100

100

+

+

incomplete

88

60.0

100

100

+

+

incomplete

91

52,0

100

100

+

+

incomplete

92

500

100

100

+

+

incomplete

93

53.0

100

100

+

+

incomplete

67

34.8

100

100

+

+

nearly complete

83

438

100

100

+

+

nearly complete

87

61.0

100

100

+

+

nearly complete

90

77.0

100

100

+

+

nearly complete

75

58.4

100

100

+

—

complete

79

56.3

100

100

+

—

complete

89

69.0

100

100

+

-

complete

66

45.5

100

-70

+

—

complete

74

54.8

100

-70

+

-

complete

63

39.1

100

-10

+

—

complete

78

52.1

100

-10

+

-

complete

70

48.1

100

-10

—

—

complete

77

54.5

-90

0

-

-

complete

■86

66.0

0

0

-

+

no eye migration

71

45.8

0

0

—

—

complete

76

63.6

0

0

—

—

complete

80

42.6

0

0

—

—

complete

81

40.3

0

0

—

—

complete

82

52.9

0

0

—

—

complete

* This specimen had a small albinistic area on the right side of its head.

ABNORMALITIES

PIGMENTATION

Among the many abnormally pigmented speci-
mens (Table 1) four major categories could be
distinguished. Three were types of ambicolora-
tion and the fourth was partial albinihm: (1)
Nineteen specimens were completely pigmented
on both sides (Figures 2 and 3). (2) Two speci-
mens were completely pigmented except for the
mouth region on the left (blind) side (Figure 5) .
(3) Four specimens were completely or almost
completely pigmented on the body of the blind
side but not on the head, which had little (10% )
or no pigment (Figure 6). (4) One specimen
was partially albinistic on the right side of the
head, but other pigmentation was normal. The

eye completely failed to migrate in this speci-
men (Figure 7). Normal coloration (five speci-
mens) consisted of a lack of pigment on the blind
side, except for tiny melanophores scattered over
the posterior third of the body (Figure 1). All
except two ambicolored individuals had some
other associated abnormality, but normally pig-
mented specimens were always normal in other
respects.

LEFT PECTORAL FIN

The left pectoral fin disappeared from normal
lined soles when metamorphosis was nearly com-
plete (Houde et al., 1970). A fin with 1 to 6
rays remained on 23 of the 31 juveniles from
the rearing experiment. All specimens with a
left pectoral fin also were abnormally pigmented.

539

FISHERY BULLETIN: VOL. 69. NO. 3

Figure 2. — Left side (left photo) and right side (right photo) of head of 39.6 mm TL abnormal Achirus lineatiis
reared in the laboratory. Ambicoloration, hooked dorsal fin, incomplete eye migration, and presence of a left
pectoral fin.

Usually the fin was associated with a hooked
dorsal fin and failure of eye migration (Figures
2 and 3), but a pectoral fin also was present on
some individuals without those abnormalities
(Figure 5).

HOOKED DORSAL FIN

Seventeen specimens had a hooked dorsal fin.
In normal metamorphosis, the left eye of A.
lineatus migrates across the dorsal midline under
the projecting dorsal fin ; the "hook" of the
dorsal fin subsequently grows down toward the
snout, eventually becoming adnate to the head.
Development of the dorsal fin during metamor-

phosis was described for normal A. lineatus by
Futch, Topp, and Houde. ' In normal lined soles
the first five dorsal fin pterygiophores articulate
with serrations in the supraoccipital bone. The
three anteriormost pterygiophoi-es are dii-ected
anteriad, lying nearly parallel to the axis of the
neurocranium. A fleshy connection is estab-
lished between the dorsal fin and the prefrontal
complex of the neurocranium. Radiographs of
abnormal lined soles revealed that rotation of
the frontal and prefrontal bones was incomplete
during metamorphosis. The anteriormost pter-

" Futch, C. R., R. W. Topp, and E. D. Houde. De-
velopmental osteology of the lined sole, /lc/i/n(s lineatus
(Pisces: Soleidae). (Unpublished manuscript.)

540

HOUDE; DEVELOPMENTAL ABNORMALITIES OF ^rhirus linealus

Figure 3. — Left side (upper photo) and right side (lower
photo) of 32.6 mm TL abnormal Acliirus tineatus reared
in the laboratory. Abnormalities include ambicolora-
tion, hooked dorsal fin, partial eye migration, and
presence of a left pectoral fin.

Figure 4. — Right side of head of 34.8 mm TL abnormal
Achirus lineatus reared in the laboratory. Abnormal-
ities include ambicoloration, hooked dorsal fin, and
presence of a left pectoral fin. Eye migration nearly
complete.

ygiophores appeared normal and articulated with
the supraoccipital serrations, but were directed
away from the neurocranium at an angle of
about 20°. No fleshy connection was established
between the doi'sal fin and the incompletely ro-
tated prefrontal complex. Hooked dorsal fins
and eye migration failure are associated (Fig-
ures 2 and 3), but the hooked condition can
also be present when eye migration is nearly
normal (Figure 4).

ranged from almost total failure of migration
(Figures 2 and 7) to various stages of partial
or nearly complete migration (Figures 3 and 4) .
All individuals with this abnormality also had
hooked dorsal fins and were ambicolored or par-
tially albinistic. In normal A. lineatus eye mi-
gration began at about 3.5 mm TL and was com-
plete at 6.5 mm TL (Houde et al., 1970).

REVERSAL

EYE MIGRATION

Migration (rotation) of the left eye was in-
complete in 17 specimens. The abnormality

A single reversed specimen was reared. This
specimen was not included among the 31 treated
in Table 1 because it was preserved before meta-
morphosis was completed. Reversals among the

541

FISHERY BULLETIN: VOL. 69, NO. 3

Figures. — Leftside (upper photo) and right side (lower
photo) of 45.5 mm TL abnormal Achirus Uneatus reared
in the laboratory. Abnormalities include ambicoloration
and the presence of a left pectoral fin.

Figure 6. — Left side (upper photo) and right side (lower
photo) of 48.1 mm TL abnormal Achmis lineatus reared
in the laboratory. Specimen is ambicolored but other-
wise normal.

Soleidae are extremely rare' (Hubbs and Hubbs,
1945). The specimen was a nearly metamor-
phosed individual of 5.5 mm TL (Figure 8),
that appeared normal in other respects when
compared with other postlarvae of the same
length. Internal organs were not examined to
determine whether they were reversed. Normal
A. lineatus of the same length have been illus-
trated and described by Houde et al. (1970).

* The photograph in Herald (1961; fig. 139) should
not be mistaken as a reversed Gymnachirii a nnlliamsoni,
because in actuality this photograph was produced by an
accidental reversal of a Kodachrome slide during prepa-
ration of the text.

SUMMARY

Most abnormalities of the laboratory-reared
A. lineatus appeared related to each other. The
presence of related anomalous conditions in in-
dividual specimens of flatfishes often has been
reported, and the apparent association of ambi-
coloration, hooked dorsal fins, incomplete eye
migration, and the tendency toward symmetry
in paired fins has been discussed (Dawson, 1962;
Gudger and Firth, 1936; Norman, 1934). The
26 aberrant juvenile specimens in my series
of 31 were examined to determine the associ-
ation of abnormal conditions in individual fish.
p]xamination of Table 1 shows that the abnor-
malities are associated. Sixteen specimens had

542

HOUDEi DEVELOPMENTAL ABNORMALITIES OF Achiru, l^ratus

Figure 7.— Leftside (upper photo) and right side (lower
photo) of 66.0 mm TL abnormal Achirus lineatus reared
in the laboratory. Partial albinism, hooked dorsal fin,
no eye migration.

all four major anomalies and 16 to 23 specimens
had two or three coexistent aberrancies. The
"rule" of Gudger and Firth (1936), that was
supported by extensive data on flatfishes (Daw-
son, 1962), stated that specimens with complete
pigmentation of the body and pigmentation cov-
ering at least one-quarter to one-third of the head
on the blind side will have a hooked dorsal fin
and incomplete eye migration. Five of my lined
soles fitted that category of ambicoloration but
had neither a hooked dorsal fin nor incomplete
eye migration (Table 1 and Figure 5). All but
two ambicolored specimens also were abnormal
in some other respect. Ambicolored individuals
in which the body and more than 10 ^f of the

head on the blind side were pigmented retained
a pectoral fin on the blind side. Eye migration
never was complete in those specimens with a
hooked dorsal fin.

A single specimen (Figure 7; *86 in Table 1)
was unique in that the left eye completely failed
to migrate. A portion of the right side of its
head was unpigmented making it the only par-
tially albinistic specimen in the series. The left
side, which was unpigmented and lacked a pec-
toral fin, was similar in these respects to the
blind side of normal lined soles. A well-devel-
oped hooked dorsal fin was present. Similar
abnormalities were present in a naked sole
(Gymnachmis melas Nichols) that was reared
at the laboratory.

The high percentage of abnormalities in lab-
oratory-reared A. lineaUis must have been in-
fluenced by rearing conditions, since abnormal
lined soles apparently are extremely rare in
nature. Further controlled experiments should
make it possible to determine what factors cause
abnormal metamorphosis of lined soles and per-
haps other flatfishes. These experiments also
might test the common assumption that survival
of abnormal flatfishes is lower than that of nor-
mally metamorphosed individuals, since no ad-
vantages in either survival or growth of normal
juveniles of A. lineatus were detected in the ini-
tial rearing experiment.

ACKNOWLEDGMENTS

Assistance in rearing the larvae was provided
by Barbara Palko and Robert Detwyler. Charles

Figure 8. — Left side of a reversed, nearly metamor-
phosed, 5.5 mm TL specimen of Achirus lineatus reared
in the laboratory.

543

FISHERY BULLETIN: VOL. 59, NO. 3

Futch, William J. Richards, and C. R. Robins
have reviewed and criticized the manuscript.
The reversed specimen was illustrated by Grady
Reinert. Photographs were taken by Andrew
Ramsay and Anna Delor.

LITERATURE CITED

Dawson, C. E.

1962. Notes on anomalous American Heterosomata
with descriptions of five new records. Copeia
1962: 138-146.

GUDGER, E. W., AND F. E. FiRTH.

1936. Three partially ambicolorate four-spotted
flounders, Paralichthys oblongus, two each with
a hooked dorsal fin and a partially rotated eye.
Am. Mus. Novit. 885: 1-9.
Herald, E. S.

1961. Living fishes of the world. Doubleday and
Co., Inc., Garden City, N.Y., 304 p.
HouDE, E. D., C. R. Futch, and R. Detwyler.

1970. Development of the lined sole, Achirus
lineatus, described from laboratory-reared and
Tampa Bay specimens. Fla. Dep. Nat. Resour.,
Tech. Ser. 62, 43 p.

HOUDE, E. D., AND B. J. PALKO.

1970. Laboratory rearing of the clupeid fish

Harengula pensacolae from fertilized eggs. Mar.
Biol. 5: 354-358.

HL'BBS, C. L., AND L. C. HUBBS.

1945. Bilateral asymmetry and bilateral variation
in fishes. Pap. Mich. Acad. Sci. Arts Lett. 30:
229-310.
Jordan, D. S., and B. W. Etormann.

1898. The fishes of North and Middle America.
U.S. Natl. Mus. Bull. 47, Part III: 2183-3136.
Norman, J. R.

1934. A systematic monograph of the flatfishes
(Heterosomata). Vol. I. Psettodidae, Bothidae,
Pleuronectidae. British Museum (Natural His-
tory), London, viii + 459 p.
Riley, J. D.

1966. Marine fish culture in Britain VII. Plaice
(Pleiironectes platessa) post-larval feeding on
Artemia salina L. nauplii and the effects of vary-
ing feeding levels. J. Cons. 30: 204-221.
Seshappa, G., and B. S. Bhimachar.

1955. Studies on the fishery and biology of the
Malabar sole, Cynoghssus semifasciatus Day.
Indian J. Fish. 2: 180-230.
Shelbourne, J. E.

1964. The artificial propagation of marine fish.
In F. S. Russell (editor), Advances in Marine
Biology, Vol. 2, p. 1-83.

1965. Rearing marine fish for commercial pur-
poses. Calif. Coop. Oceanic Fish. Invest., Rep. 10:
53-63.

544

THE EARLY LIFE HISTORY OF SKIPJACK TUNA, Katsuwonus pelamis,

IN THE PACIFIC OCEAN

Howard 0. YosHroA'

ABSTRACT

This study investigates the early life history of skipjack tuna, including the distribution, abundance, age,
and growth. The study is based on 1,742 juvenile skipjack tuna that were found in the stomachs of
6,867 billfishes caught in Hawaiian waters and in the South Pacific by commercial longline boats. The
smallest juvenile taken near Hawaii was 5.9 cm in standard length, and in the South Pacific 1.6 cm
in standard length. Regressions describing the relations between the standard length and lengths of
(1) the vertebral column, (2) the precaudal vertebrae, (3) caudal vertebrae, (4) the Ist-lOth verte-
brae, and (5) the 21st-30th vertebrae of juvenile skipjack tuna were determined. The regressions pro-
vided estimates of the standard length of fragmentary specimens. Juvenile skipjack tuna were widely
distributed between lat 5° and 32° S, and long 137° W and the 180th meridian. North of the equator,
the commercial longline boats fished close to the main Hawaiian Islands, and thus only a limited pic-
ture was obtained of the areal distribution of juvenile skipjack tuna. Juvenile skipjack tuna were
found in almost all months in Hawaiian waters. They were most numerous in July and August. In
the South Pacific, juveniles were also found in almost all months between lat 5° and 20° S. Peaks
in the apparent abundance were evident in April and October in the area north of lat 10° S. Juvenile
skipjack tuna appeared to be more numerous in the South Pacific than around Hawaii.

Length-frequency distributions of juvenile skipjack tuna from Hawaii showed well-defined modes,
which progressed with time. The growth of the juveniles was estimated by using the modal lengths
determined from the monthly length-frequency distributions. Skipjack tuna between 9 and 40 cm
around Hawaii are estimated to grow 2.0 cm per month. One-year-old fish are estimated to be 31
cm in standard length.

In 1968, 70,746 metric tons of skipjack tuna,
Katsmcotnis pelamis, were landed in the eastern
Pacific ( Inter- American Tropical Tuna Commis-
sion, 1970) and 109,018 metric tons were landed
in Japan (Japan. Fisheries Agency, Research
Division, 1970). Because of its commercial im-
portance much knowledge has been accumulated
on the biology of the skipjack tuna. Information
on early life history, however, is incomplete.
Matsumoto (1958) described skipjack tuna lar-
vae and their temporal and spatial distribution
in the central Pacific. Ueyanagi (1969) report-
ed on the distribution of larval skipjack tuna
in the Pacific Ocean between 1960 and 1967,
and Higgins (1967) summarized the distribu-
tional records of juvenile skipjack tuna in the
Pacific.

' National Marine Fisheries Service, Hawaii Area
Fishery Research Center, Honolulu, Hawaii 96812.

The present study is based on immature skip-
jack tuna between 1.6 and 40 cm taken from the
stomachs of billfishes near Hawaii and in the
South Pacific. Included are observations on geo-
graphical and seasonal distribution, length-fre-
quency distributions, and age and growth rates.

MATERIALS AND METHODS

The stomachs of 6,867 billfishes" were exam-
ined in this study. Those examined included
4,118 striped marlin, Tetrapturus audax; 1,606
blue marlin, Makaira nigricans; 383 shortbill
spearfish, T. angustirostri^; 216 sailfish, Istio-
phoms platypterus; 196 swordfish, Xiphias
gladius; 171 black marlin, M. indica; and 177
billfishes that were not identified to species.

Manuscript accepted February 1971.

FISHERY BULLETIN: VOL. 69, NO. 3, 1971.

' The term billfishes as used in this paper includes
swordfish.

545

FISHERY BULLETIN: VOL. 69, NO. 3

Sixty-six percent of the stomachs came from
billfishes captured near Hawaii' between July
1962 and April 1966. These stomachs were used
previously in an early life history study of al-
bacore, Thunnus alalunga ( Yoshida, 1968) . Most
of these billfishes were caught within 37 km (20
nautical miles) of the main islands. A few were
caught as far as 740 km (400 nautical miles)
from Oahu. Thirty-four percent of the stomachs
came from billfishes caught in the South Pacific
between lat 5° and 32° S, and between long 135°
W and 179° E (Figure 1). These were caught
on longline gear by boats operating out of Amer-
ican Samoa between January 1964 and July 1966.
The fishery has been described by Otsu and
Sumida (1968).

Arrangements were made with the crews of
several boats to have billfish stomachs collected
on the fishing voyages. Each cooperating crew
was provided with a stainless steel tank, form-
aldehyde solution, labels, and collecting bags.
The crew was paid 50 cents for each stomach.

In the laboratory at Honolulu, all tuna and
tunalike specimens were sorted from the stomach
contents and identified. Skipjack tuna were
identified by skeletal characters (Godsil and
Byers, 1944). Standard length was recorded
for all intact specimens. Following a technique
used earlier (Yoshida, 1968), a method was de-
vised to estimate the standard length of frag-
mentary specimens. Relations were determined
between the standard length and the length of:
(1) the complete vertebral column (41 verte-
brae), (2) the precaudal vertebrae (vertebrae
1-20), (3) the caudal vertebrae (vertebrae 21-
41), (4) Ist-lOth vertebrae, and (5) 21st-30th
vertebrae, based on 77 intact juvenile skipjack
tuna specimens from around Hawaii and the
South Pacific. All the relations appeared to be
linear and straight lines were fitted to the data
by the method of least squares. Combining the
samples from Hawaii and the South Pacific
should not adversely affect the results. A plot
of the data for all five relations did not indicate
any differences between the North Pacific and
South Pacific samples. A covariance analysis
applied to the relation between the standard
length and the length of the complete vertebral
column for Hawaiian and South Pacific juvenile

^^

y^

W///////////7//,

'■'///?/^'/7//, V/???///^

♦t^i-':*-'^"--'^* h'fi'^'-'-:y^^^ ,, MARQUESAS

^ •.?t SAMOA IS. L "' WMmm

Figure 1. — The location of capture of billfishes (shaded
area) and the distribution of juvenile skipjack tuna
(dots) in the South Pacific.

skipjack tuna confirmed the lack of significant
diffei'ences between the samples. No significant
differences were found in the regression coeffi-
cients {F = 0.105; df = 1, 73) and in the in-
tercepts {F = 0.053; df = 1, 74). The re-
gressions of the standard length on the various
vertebral segments are presented in Table 1.
The lengths of most of the specimens were
estimated by using a suitable regression. For
22 ""f of the specimens the relative position of
the fragments could not be determined, and the
regressions were not used. For these specimens
the standard length was estimated by comparing
the average length of the vertebrae in the frag-
ment with the average length of the vertebrae

546

YOSHIDA: EARLY LIFE HISTORY OF SKIPJACK TUNA

of the specimens used to calculate the regres-
sions.

Table 1. — Regressions describing the relations between
the standard length and lengths of the vertebral column,
precaudal vertebrae, caudal vertebrae, Ist-lOth vertebrae,
and 21st-30th vertebrae of juvenile skipjack tuna [I =
standard length (cm) , L = length of vertebral fragments
(cm)].

Segment of vertebral
column

Regression

Standard deviation
from regression

Complete vertebral
column

/ =

0.0693 + 1.2262i

0.435

Precaudal vertebrae

/ =

0.6544 + 2.4926i

0.439

Caudal vertebrae

( =

-0.4414 + 2.41 96Z.

0.445

Ist-lOfh vertebrae

/ =

0.4280 + 5.2938i

0.515

21st-30th vertebrae

( =

-0.2637 + 4.6942i

0595

DISTRIBUTION AND ABUNDANCE

Seasonal and areal coverage was spotty, but
sampling was extensive enough to permit mean-
ingful analysis for the present study. In the
following sections I will discuss the distribution
and the seasonal and annual apparent abundance
of juvenile skipjack tuna in the South Pacific
and near Hawaii.

AREAL DISTRIBUTION

Commercial longline boats engaged in collect-
ing billfish stomachs in the South Pacific ranged
over a wide area, and juvenile skipjack tuna, as
indicated by their presence in billfish stomachs,
also were widespread (Figure 1). Around
Hawaii fishing was restricted to a relatively
small area, and so a more limited picture was
obtained of the areal distribution of juvenile
skipjack tuna.

Skipjack tuna larvae are widely distributed
in the Pacific Ocean (Matsumoto, 1966; Ueya-
nagi, 1969). Ueyanagi (1969) reports that lar-
vae were taken across the entire South Pacific
between the equator and lat 10° S. Also, west
of long 140° W larvae were taken as far south
as lat 32° S. My study shows that the distribu-
tion of juvenile skipjack tuna is similar to the
distribution of the larvae. In the North Pacific,
skipjack tuna larvae have been found around
Hawaii and across the entire Pacific between the
equator and lat 20° N. In the western North
Pacific, between long 160° W and the Asian

continent, larvae have been taken almost as far
north as lat 35° N (Ueyanagi, 1969).

My study indicates that gaps in the distribu-
tion of juvenile skipjack tuna in the Pacific re-
flect a lack of sampling. Higgins (1967) has a
somewhat similar viewpoint. It is likely that
the juveniles are as widely distributed as larval
skipjack tuna in the North Pacific.

The distribution of juvenile skipjack tuna in
the South Pacific by quarters of the year (all
years combined) is shown in Figure 2. This is
only the apparent distribution, however, because
it reflects the operations of Samoa-based vessels.
These vessels primarily seek albacore, and there-
fore they fish the areas where albacore catch
rates tend to be high. In the first half of the
year, vessels generally operate north of lat 20° S,
and in June or July they move as far south as
lat 30° S before heading north again (Otsu and
Sumida, 1968). Samples were available mostly
from north of lat 20° S, and juvenile skipjack
tuna were found throughout the sampling range.
In the third and fourth quarters, samples were
available from a wider area, and again juvenile
skipjack tuna were taken from almost the entire
area sampled. Although seasonal coverage was
incomplete throughout the total area, synoptic
sampling would probably produce juveniles in
all seasons and throughout the total area.

SEASONAL APPARENT ABUNDANCE
Hawaii

Apparent abundance is expressed here as
number of skipjack tuna per 100 billfish stom-
achs. The apparent abundance of juveniles
around Hawaii, all years combined, is shown in
Figure 3. The juveniles were more numerous
during July, August, and September. A peak
in abundance usually occurred in August. These
observations confirm Matsumoto's (1966) con-
clusion that skipjack tuna in the Hawaiian
Islands spawned during the summer. He showed
that the abundance of larval skipjack tuna
peaked in July.

The apparent abundance of juveniles in 1963,
1964, and 1965 oflfers interesting contrasts. For
example, in August 1963 the apparent abundance
peaked sharply to 100 juveniles per 100 bill-

547

FISHERY BULLETIN: VOL. 69, NO. 3

ORJI IS

•r SAMOA IS.

MARQUESAS IS.

JAN. -MAR.

TAHITI

^Jr^vv.-- V >.

4

OFIJI IS.

SAMOA IS

APR.- JUNE

■r/.

,,, '^, MARQUESAS IS

TAHITI

"W::

^'

MARQUESAS IS

X SAMOA IS.
a, ".J

OFIJI IS.

-9^

">?//■

1^:

OCT. - DEC.

■//.-v. % :5^
TAHITI

Figure 2. — Distribution of juvenile sl<ipjack tuna (dots) by quarters of the year in the South Pacific. The
shadings show the billfish sampling area.

fishes. Only small number.s were taken between
January and June and between October and
December. In 1964 and 1965 the summer
peak in abundance was not so high; however,
juveniles were more numerous in other months.
The apparent abundance of juveniles was
highest in 1964 when an average of 21.3 ju-
veniles per 100 billfishes was taken. In 1965,
an average of 19.1 juveniles was taken, and in
1963 the average was 12.4.

South Pacific

To examine the seasonal apparent abundance
of juvenile skipjack tuna in the South Pacific,
the area north of lat 10° S was considered sep-
arately from the area between lat 10° and 20° S
(Figure 4). Because the coverage was poor in

any one year, the data for all years were
combined.

Juvenile skipjack tuna were taken through-
out the year north of lat 10° S. Peaks in the
apparent abundance were evident in April and
October. Larvae have been taken throughout
the year in the equatorial waters (lat 10° N to
10° S) of the central Pacific (Matsumoto, 1966).
They were most numerous between April and
July. Thus, the apparent abundance of the
juveniles differs somewhat from that of the lar-
vae in that a peak was absent in larval abundance
in the latter half of the year. The diff"erence
in apparent abundance between the larvae and
juveniles may not be real. The small number
of stomachs collected in the latter half of the
year may not have been adequate to reveal the
true abundance of juveniles.

548

YOSHIDA: EARLY LIFE HISTORY OF SKIPJACK TUNA

NUMBER OF BILLFISH STOMACHS EXAMINED
264 373 558 442 436 507 238 303 183 279 567 418

slightly more numerous north of lat 10° S than
between lat 10° and 20° S. In 1965, however,
juveniles were more numerous between lat 10°
and 20° S than north of lat 10° S. Also they
appeared to be more numerous in the South Pa-
cific than near the Hawaiian Islands.

About 12 ''r of the billfish stomachs from
Hawaii contained one or more juvenile skipjack
tuna, while 19 ''r of the billfish stomachs from the
South Pacific contained one or more juveniles.
In both areas the largest number of juvenile
skipjack tuna per stomach was 11; most of the
stomachs from both areas had only one juvenile.

AGE AND GROWTH

The length-frequency distribution of juvenile
skipjack tuna from Hawaii and the South Pa-
cific is shown in Figure 5. Near Hawaii the
smallest juvenile taken was 5.9 cm SL (standard

JAN FE8 MAR APR MAY JUNE JULY AUG SEPT OCT NOV DEC

FiGUBE 3. — Apparent abundance of juvenile skipjack
tuna in Hawaiian waters, 1962-66.

Juveniles were taken in all months except
July between lat 10° and 20° S. Here also the
uneven sample sizes make the analysis of ap-
parent abundance difficult. It appears, however,
that juveniles were numerous from November
to February. No comparable data on larval skip-
jack tuna in this area are available.

The apparent abundance of juvenile skipjack
tuna was higher in 1964 than in 1965 in the
South Pacific (Table 2) . In 1964, juveniles were

Table 2. — Annual apparent abundance of juvenile skip-
jack tuna in the central Pacific Ocean.

Number

of
billfishes

Number of

juvenile

skipjack tuna

juveniles
per 100
billfishes

1963

Hawaii

1,351

167

12.4

1964

Hawaii

1,608

342

21.3

Equator-tO' S

579

268

46.3

10"'-20° S

216

92

42.6

1965

Hawaii

1,008

193

19.1

Equalor-10° S

208

60

28.8

10°-20° S

537

191

35.6

5 60

O 20

"^ \ r

NORTH OF «• S

124) 1 ^

M

(212)

<23)

(16)

10*

-20

•s

(4)

(5)

m

(5)

1

'

-1

4

172)

(32)

(6)"

(160)

w

(222)

r

(122)

(5)

(25)

n

(71)

JAN FEB MAR APR MAY JUNE JULY AUG SEPT OCT NOV DEC

Figure 4. — Apparent abundance of juvenile skipjack
tuna in the South Pacific. The figures in the parentheses
are the number of billfish stomachs that were e.xamined.

549

FISHERY BULLETIN: VOL. 69, NO. 3

HAWAI 1

t'

?^

r 1

1

P^-

r

Tltr ' f

^ia

SOUTH PACIFIC

N'867

tUTh^ rv^-EmiTV

"0 10 20 30 40

STANDARD LENGTH {CM )

Figure 5. — Length-frequency distribution of juvenile
skipjack tuna.

length) . A prominent mode was located at the
14-14.9 cm size class, a lesser mode at 25-25.9 cm,
and a relatively obscure mode was evident be-
tween 30 and 40 cm. The length frequencies
of juvenile skipjack tuna from the South Pacific
were similar to those from Hawaii. The smallest
juvenile taken in the South Pacific was 1.6 cm
SL. A prominent mode was evident at the 12-
12.9 cm length class, a lesser mode between 20
and 30 cm, and a relatively obscure mode was
apparent between 30 and 40 cm.

The monthly length-frequency distributions of
the juveniles near Hawaii show well-defined
modes in the summer and fall ( Figure 6) . Some
of the length distributions have two or more
well-defined modes. These modes probably rep-
resent progeny from two or more sj^awnings
spaced more or less closely in time. An increase
in size of the juveniles, as indicated by a pro-
gression of the modes, was evident in the
monthly length distributions. In contrast, Hig-
gins (1970) found that modal groups of juvenile

skipjack tuna taken in midwater trawls did not
show an increase in length with time.

Because the modal lengths increased with
time, an attempt was made to describe the
growth of the juveniles. To facilitate the des-
ignation of modes, the length data were smoothed
by a moving average of three. Modes were not
considered in samples that had fewer than 10
fish, nor in length groups containing fewer than
5 fish. The selected modes are given in Figure 7
and Table 3. Using the method of least squares,
straight lines were fitted to groupings of modal
points to represent the apparent growth of the
juveniles. The slope of the lines for 1962, 1964-
65, and 1965-66 indicates that juvenile skipjack
tuna grow about 2.0 cm per month. The slope
of the line for 1963-64 indicates a growth of 1.2
cm ]3er month. These data suggest annual dif-
ferences in the growth of the juveniles. I be-
lieve that an increment of 2 cm per month is the
best estimate of the growth rate of juvenile
skipjack tuna within the length range covered
in this study. Rothschild (1967) used data from
tag and recapture experiments and the von Bert-

Table 3. — Modes in the length-frequency distributions
of juvenile skipjack tuna from Hawaii (from Figure 6).

Year Month Standard length (cm)

1964

August

13.0

19.0

September

20.0

October

27.0

November

22.0

June

I3.S

July

13.5

August

9.5

15.5

September

15.5

22.0

November

23.5

December

24.0

April

30.0

May

19.0

25.0

Juno

15.5

25.5

July

8.5

13.5

August

II.O

18.5

September

12.5

October

14.5

23.5

November

23.5

December

25.0

April

35.5

May

12.5

26.5

June

9.5

July

15.5

August

10.5

145

October

13.0

19.5

November

18.5

April

32.5

550

YOSHIDA: EARLY LIFE HISTORY OF SKIPJACK TUNA

. _j5r!-frtT.HT-(3-- >a

-B~

"■^l^^^Hffk

I— FrfeB=i

^ftv-~-

AUG

SEPT ^ I

_«,-rTTHflTWfH4. ifK»-»_

^<fefl— n-

STANDARD LENGTH (CM )

STANDARD LENGTH (CM )

STANDARD LENGTH I CM )

Figure 6. — Monthly length-frequency distribution of skipjack tuna from Hawaii.

JJASQND|JFMAMJJASOND|JFMAMJJASONOJFMAMJJASOND|JFMAMJ

1963 1964 1965

Figure 7. — Growth of juvenile skipjack tuna from Hawaii.

alanffy growth function to estimate skipjack
tuna growth. He indicated that skipjack tuna
between 44 and 72 cm grew about 16.6 cm per
year or 1.4 cm per month. The deceleration in

tuna between 9 and 40 cm to 1.4 cm per month

for fish between 44 and 72 cm is to be expected.

It is useful to determine the growth rate of

skipjack tuna from hatching to 9 cm SL. These

growth from 2.0 cm per month for skipjack and other data may make it possible to estimate

551

FISHERY BULLETIN: VOL. 69, NO. 3

the age of skipjack tuna at various sizes. The
growth rate of a related species, bhick skipjack,
Euthynnus lineatus, between 17 and 75 mm SL
has been determined (Clemens, 1956). In ex-
periments conducted in shipboard aquaria Clem-
ens showed that black skipjack grew 36.8 mm in
295 hr, which would be about 9 cm in a month.
Houde and Richards (1969) reared larval little
tunny, E. alletteratus, under laboratory condi-
tions and reported similar growth rates. It was
recently found that larval skipjack tuna have
similar growth rates (personal communication,
William J. Richards, Supervisory Zoologist,
NMFS Tropical Atlantic Biological Laboratory,
Miami, Fla. 33149, August 18, 1970). If larval
skipjack tuna grow at the same rate (9 cm per
month) for the first month and 2 cm per month
for the next 11 months, then skipjack tuna 1 year
old would be 31 cm SL.

Brock (1954) assumed that the modal sizes
of fish between 40 and 50 cm FL (fork length)
that appear in the Hawaiian skipjack tuna fish-
ery during the summer represented 1-year-old
fish. Forty to fifty centimeters for 1-year-old
fish seems too high. Modal lengths typical of
winter skipjack tuna in the Hawaiian fishery are
35, 50, and 70 cm FL (Rothschild, 1965). My
data indicate that the 35-cm modal group that
appears in the winter represents 1-year-old fish.

SPAWNING

In the Hawaiian area, juvenile skipjack tuna
smaller than 10 cm were found during 7 months
in 1963 and during 5 months in 1964 and 1965
(Figure 6). This suggests a protracted spawn-
ing season and nearly continuous recruitment
of juveniles. The catch of larvae indicates that
spawning begins in March, peaks in July, and
declines sharply in September and October
(Matsumoto, 1966).

The Hawaiian ski|5jack tuna fishery peaks in
the summer when the bulk of the catch is com-
posed of "season-size" fish larger than 60 cm
(Rothschild, 1965). Larval and juvenile skip-
jack tuna also are most numerous during the
summer, which suggests that the large fish
spawn in Hawaiian waters. The presence of

juveniles in the spring and fall, although in lesser
numbers, indicates that spawning also takes
place then. Rothschild (1965) has hypothesized
that at least one subpopulation spawns in Ha-
waiian waters. The protracted spawning sea-
son may indicate that more than one subpopu-
lation spawns here.

In the South Pacific between lat 5° and 20° S,
the spawning season is more protracted than in
Hawaiian waters. Juveniles smaller than 10 cm
SL were taken in almost every month north of
lat 10° S. Between lat 10° and 20° S they were
taken in all months except March, April, June,
and July (Figure 8); the reason for their ab-
sence in these months may be inadequacy of
samiiling. The area south of lat 20° S was some-
what different. Although sampling was sparse,
the length-frequency distribution consistently
showed few small juveniles, which indicates little
or no spawning in this area.

The length-frequency distribution of juvenile
skipjack tuna north of lat 10° S and between lat
10° and 20° S indicated a progression of modes
(Figure 8). However, a plot of the modal
lengths indicated no growth. The cause of this
may be a protracted spawning season and in-
adequacy of samples. Also juveniles appear to
migrate southward as they grow. Only small
numbers of juveniles largei' than 20 cm SL were
taken north of lat 20° S, and most of the ju-
veniles taken south of lat 20° S were larger than
20 cm SL.

ACKNOWLEDGMENTS

Thanks are due the research assistants at the
NMFS Hawaii Area Fishery Research Center
who examined the billfish stomach contents for
juvenile skipjack tuna and aided in summarizing
part of the data. The portion of the study in
the South Pacific would not have been possible
without the cooperation of the crews of the many
fishing vessels from Jajian and the Republic of
Korea. I thank William J. Richards, NMFS,
Miami, Fla.; Walter T. Pereyra. NMFS, Seattle,
Wash.; and Witold L. Klawe, Inter-American
Tropical Tuna Commission, La Jolla, Calif, for
reviewing the manuscript.

552

YOSHIDA: EARLV LIFE HISTORY OF SKIPJACK TUNA

NUMBER
24

20

16
12
8
4
0

NORTH OF 10°
1964

FEB

MAR

N--6'

" APR
NOlO

W

MAY

"fftv-.

JUNE
N = 39

"FOrfisb. _»..7~- !

JULY

^^__j^

SEPT

OCT

n 1

FEB

MAR

N-.6

APR

MAY

N'l

Rv,

JUNE
N=2

JULY

N'3

AUG

N'2

L_

SEPT

N.5

OCT

fftw^i^

NOV

N = 2

DEC 1

N = 2 1
" "

-Jm^

FEB

N^2B

MAR p-^

APR

^..-Jilkife^

1966

JAN

N = 36

Jk4

i

%

FE8

MAR ^

N=2 1

41. _

APR

N'4

MAY

SOUTH OF 20° S
1963

NOV

N = l

1964

AUG

N<I4

" -^tttF

SEPT

N=I9

>f^mbs^

OCT

N = 5

1965

FEB 1

N.I

.<^fl'W,^,

STANDARD LENGTH ICM )

STANDARD LENGTH (CM)

Figure 8. — Monthly length-
frequency distribution of ju-
venile skipjack tuna north of
lat 10° S, lat 10°-20° S, and
south of lat 20° S in the South
Pacific.

553

FISHERY BULLETIN: \0L. 69. NO. 3

LITERATURE CITED

Brock, V. E.

1954. Some aspects of the biology of the aku,
Katsuwonus pelamis, in the Hawaiian Islands.
Pac. Sci. 8: 94-104.
Clemens, H. B.

1956. Rearing larval scombrid fishes in shipboard
aquaria. Calif. Fi.sh Game 42: 69-79.
GODSIL, H. C, AND R. I). Byers.

1944. A systematic study of the Pacific tunas.
Calif. Div. Fish Game, Fi.sh Bull. 60, 131 p.
HiGGINS, B. E.

1967. The distribution of juveniles of four species
of tunas in the Pacific Ocean. Indo-Pac. Fish.
Counc, Proc. 12th Sess., Sect. 2: 79-99.
1970. Juvenile tunas collected by midwater trawl-
ing in Hawaiian waters, July-September 19G7.
Trans. Am. Fish. Soc. 99: 60-69.
HouDE, E. W., AND W. J. Richards.

1969. Rearing larval tunas in the laboratory.
Commer. Fish. Rev. 31(12): 32-34.

Inter-American Tropical Tuna Commission.

1970. Annual report of the Inter-American Tropi-
cal Tuna Commission, 1969. La Jolla, Calif., 117 p.

Japan. Fisheries Agency, Research Division.

1970. Annual report of effort and catch statistics
by area. Japanese skipjack baitboat fishery, 1968.
136 p.
Matsumoto, W. M.

1958. Description and distribution of larvae of four

species of tuna in central Pacific waters. U.S.
Fish Wildl. Serv., Fish. Bull. 58: 31-72.

1966. Distribution and abundance of tuna larvae
in the Pacific Ocean. In T. A. Manar (editor) ,
Proceedings, Governor's Conference on Central
Pacific Fishery Resources, State of Hawaii,
p. 221-230.

Otsu, T., and R. F. Sumida.

1968. Distribution, apparent abundance, and size
composition of albacore (Thimmis alahniga) taken
in the longline fishery based in American Samoa,
1954-65. U.S. Fish Wildl. Serv., Fish. Bull. 67:
47-69.

Rothschild, B. J.

1965. Hypotheses on the origin of exploited skip-
jack tuna (k'atsuwomis pelamif:) in the eastern
and central Pacific Ocean. U.S. Fish Wildl. Serv.,
Spec. Sci. Rep. Fish. 512, 20 p.

1967. Estimates of the growth of skipjack tuna
(Katsuiro7ins pelamis) in the Hawaiian Islands.
Indo-Pac. Fish. Counc, Proc. 12th Sess., Sect. 2:
100-111.

Ueyanagi, S.

1969. Observations on the distribution of tuna
larvae in the Indo-Pacific Ocean with emphasis
on the delineation of the spawning areas of alba-
core, Tlituiniis alalunga. [In Japane.se, English
synopsis.] Bull. Far Seas Fish. Res. Lab. (Shimi-
zu) 2: 177-256.

YOSHIDA, H. O.

1968. Early life history and spawning of the al-
bacore, Thuvrms nlnlnnga, in Hawaiian waters.
U.S. Fish Wildl. Serv., Fish. Bull. 67: 205-211.

554

DISTRIBUTION OF TUNA LARVAE (PISCES, SCOMBRIDAE) IN THE
NORTHWESTERN GULF OF GUINEA AND OFF SIERRA LEONE'

William J. Richards and David C. Simmons^

ABSTRACT

Investigations of tuna larvae distributions in the northwestern Gulf of Guinea and off Sierra Leone
were made during February-April 1964, August-October 1964, and February-April 1965. Larvae of
the yellowfin tuna, bigeye tuna, skipjack tuna, little tunny, and frigate mackerels were collected and
studied. Analyses of the data indicated that larvae of yellowfin tuna and bigeye tuna migrate to the
surface during the day, skipjack tuna migrate to the surface during the night, and frigate mackerels
do not seem to migrate at any time. Our data for little tunny were inconclusive. All species were
widely distributed over the area but larvae of the commercially important tunas — yellowfin, bigeye,
and skipjack — were restricted to waters where surface temperatures were higher than 24° C.

The distribution of tunas varies seasonally in
the eastern Atlantic Ocean (Richards, 1969).
In 1964 and 1965, the Bureau of Commercial
Fisheries research vessel Geronlmo (cruises 3,
4, and 5) collected tuna larvae in the northwest-
ern Gulf of Guinea and off Sierra Leone. These
collections were part of extensive investigations
intended to relate the spatial and temporal dis-
tributions of tunas to the environment. Cruise
3 was in the northwestern Gulf of Guinea be-
tween 10 February and 26 April 1964, which
is within the winter-spring "warm season" in
the Gulf of Guinea, when sea-surface tempera-
tures are higher than during summer and fall.
Cruise 4 was in the northwestern Gulf of Guinea
between 5 August and 13 October 1964, which
is within the summer-fall "cool season" in the
Gulf of Guinea, when sea-surface temperatures
are lower than during winter and spring. Dur-
ing cruise 5. collections were made in two areas:
the northwestern Gulf of Guinea and off Sierra
Leone. The northwestern Gulf of Guinea area
was generally the same as that covered in
cruises 3 and 4 and collections were made from
14 March to 19 April 1965 within the winter-
spring "warm season." The area off Sierra

' Contribution No. 185, National Marine Fisheries
Service, Tropical Atlantic Biological Laboratory, Miami,
Fla. 33149.

- National Marine Fisheries Service, Tropical Atlantic
Biological Laboratory, Miami, Fla. 33149.

Leone, which is immediately northwest of the
areas covered in cruises 3, 4, and part of 5, was
studied from 10 February to 2 March 1965 (see
Figure 1).

Figure 1. — Reference map for the areas studied. The
shaded area east of long 10° W was surveyed on
Geronimo cruises 3, 4, and part of 5; the shaded area
west of long 10° W was surveyed on part of cruise 5.

The purposes of this study are to (1) analyze
the time the collections were made, (2) describe
the distribution of the tuna larvae, and (3) dis-
cuss the relations of the tuna larvae to oceano-
graphic featui'es. In addition to the collecting
of larvae on each cruise, sightings of surface

Manuscript accepted February 1971,

FISHERY BULLETIN: VOL. 69, NO. 3, 1971.

555

FISHERY BULLETIN.- VOL. 69. NO. 3

schools of tuna were recorded and several ocean-
ographic features — temperature, salinity, and
dissolved oxygen — were measured. The distri-
butions of these oceanographic features were
published in a series of atlases (Goulet and
Ingham, 1968; Ingham, Goulet, and Brucks,
1968; Brucks, Ingham, and Leming, 1968a,
1968b).

The northwestern Gulf of Guinea is affected
by the general meteorological and oceanic condi-
tions of the Gulf of Guinea and by some unique
local features. Ingham (1970) concluded that
two types of upwelling occur in this region —
a seasonal wind-driven upwelling (.July through
October) and a current-induced upwelling that
is present most of the time. The mi.xed surface
layer is rather thin in the coastal area (less than
10 m near the coast, grading to 30 to 40 m off-
shore) and is influenced by current-induced up-
welling, wind-driven upwelling, and advection.
Ingham (1970) reported that during the period
of Geronimo cruises 3, 4, and 5, advection was
the most effective of the three factors.

The species collected were the yellowfin tuna,
Thunnus albacares (Bonnaterre) ; the bigeye
tuna, Thunnus obesiis Lowe; the bluefin tuna,
Thunniis thynmis (Linnaeus); the skipjack
tuna, KatsMivonus pelamis (Linnaeus) ; the little
tunny, Euthynnus cdletterattts (Rafinesque) ; and
the frigate mackerel, Aiixis sp. Larvae of the al-
bacore, Thunnus alalunga (Bonnaterre) were
not collected. Numbers of larvae, their location,
and the methods used to collect, sort, identify,
and compute the numbers of larvae have been
treated by Richards et ai. (1969a, 1969b, 1970)
for each cruise. Larvae were collected by an
ICITA (International Cooperative Investiga-
tions of the Tropical Atlantic) 1-m plankton net.
towed at the surface.

ANALYSIS OF COLLECTION TIME

The relative apparent abundance of some fish
larvae is complicated by diel variations. Oblique
plankton collections that samjiie the entire ver-
tical distribution of a species tend to catch fewer
fish larvae during the day (Ahlstrom, 19.'59),
presumably a result of increased net avoidance.
In sui'face collections, such as those taken dur-

ing Geronimo 3, 4, and 5, diel vertical migrations
also could be an important factor in abundance
variations.

We used the Mann-Whitney U test (Siegel,
1956) to determine the probability of equal
catches of tuna larvae in day and night surface
tows. A ranked test such as this should min-
imize the effects of patchiness. Tows with local
apparent midtimes from 0600 through 1759 hr
were designated as day tows and those with local
a]3parent midtimes from 1800 through 0559 hr
as night tows. Included in our calculations were
all successful tows (those that captured tuna
larvae) and unsuccessful tows (those that did
not capture tuna larvae) , except those unsuccess-
ful tows outside the temperature-salinity ranges
of the species (Table 1). These temperature-sa-
linity ranges are a composite from Richards
(1969) and the present study and should not
be considered absolute. The unsuccessful tows
were included because of the implication that
larvae were not cajjtured for some reason other
than intolerance to temperature or .salinity. In
calculating the statistics, a correction for the
tied (equally ranked) unsuccessful tows was
used (Siegel, 1956).

Table 1. — Temperature-salinity ranges for larvae of
yellowfin tuna, bigeye tuna, skipjack tuna, little tunny,
and Auxis sp. These data are a composite from Richards
(1969) and the present study.

Species

Temperature
range

Salinity
range

Yellowfin tuna
Bigeye tuna
Skipjack tuna
Little tunny
Auxit sp.

° C
23.6-29.7
23.6-30.5
23.4-29.7
22.7-29.3
21.6-30.5

33.5-36.8
31.8-36.4
31.4-36.9
32.7-35.4
33.2-359

The resulting probabilities (Table 2) indicate
that yellowfin and bigeye tunas were collected
more often at the surface during the day, and
skijijack tuna and little tunny more often at the
surface at night. No difference was ai^parent
between day and night tows for Auxis.

Also analyzed was whether tuna larvae were
better able to dodge the plankton net during the
day than at night. The question was considered
because we naturally assumed that tuna larvae
should be able to see a plankton net more clearly
during the day and therefore avoid it more

556

RICHARDS AND SIMMONS: DISTRIBUTION OF TUNA LARVAE

Table 2. — Probabilities of equal catches of larvae in day and night

plankton tows.

Species

Number of
day tows

Number of
night tows

Total number of standard-
ized larvae per number of
successful tows

Day

Night

Probability
of equal
catches

263

194

1701,7/113

645,8/57

<0.01

Bigeye tuna

265

197

409,6/63

186,4/32

= 0.02

Skipjack tuna

267

206

33,3/12

364,7/38

<0.01

274

209

303.5/28

362.2/36

= 0.03

Auxii sp.

280

218

3637.8/128

2812.3/93

= 0.99

easily. We also reasoned that large larvae, be-
ing better swimmers than smaller larvae, should
have been captured less frequently in day col-
lections than in night collections. Thus, if net
avoidance was demonstrable, the lengths of
larvae caught during the day should have been
smaller.

Percent length frequencies of each species of
larvae collected in the day and night were plotted
from the following data: Yellowfin tuna, 1,009
day-caught larvae, 340 night-caught larvae (Fig-
ure 2); bigeye tuna, 271 day, 84 night (Figure
3) ; skipjack tuna, 22 day, 197 night (Figure 4) ;
little tunny, 134 day, 72 night (Figure 5) ; and
Auxis, 1,636 day, 1,082 night (Figure 6).

The length frequencies of night-caught larvae
tended to be skewed more toward the larger
sizes than did the day-caught larvae. The bi-
modal frequency of skipjack tuna captured dur-
ing the day could have been due to the small
sample size. The Mann-Whitney U test (Siegel,
19.56) was applied to the frequencies to deter-
mine if night-caught larvae were significantly
larger than day-caught larvae. Probabilities of
less than 0.01 that larvae were the same length
were found for yellowfin tuna, little tunny, and
Auxis; bigeye and skipjack tunas had probabil-
ities of 0.06 and 0.22, respectively. It should be
noted also that the largest larvae of every spe-
cies but bigeye tuna were captured at night.
We tentatively conclude that there was greater
net avoidance during the day for yellowfin tuna,
little tunny, and Auxis, but little net avoidance
for bigeye and skipjack tunas.

A differential vertical migration on the basis
of size also should be considered as a possible
explanation for the capture of larger larvae at
night. Certain evidence causes us to reject this
possibility, however. Ueyanagi (1969) found

30-

»^

20-

O

O

^ 10

0-

o-o DAY
•— • NIGHT

2.0
2A

I I I I I I I I I I I I I I I I I
4.0 6.0 8.0 10.0

4.4 6.4 8.4 10.4
STANDARD LENGTH (mm)

Figure 2. — Percent length frequencies of yellowfin tuna
larvae captured during the day (broken line, 1,009
specimens) and night (solid line, 340 specimens).

that the size composition of tuna larvae taken in
night surface tows resembled the size composi-
tion of those taken during both day and night
at depth. Smaller larvae were more numerous
in catches made at the surface during the day.
The implication is that net avoidance of larger
larvae is greater at the surface during the day,
and there is no indication of a vertical migration
of the two size groups in opposition to one an-
other.

557

FISHERV BULLETIN: \0L, 69. NO. 3

30-

i«

20-

O

10-

0-

o-o DAY
•— • NIGHT

2.0
2'.4

« I ' " ' I I

4.0 6.0

I I

4.4 6.4

II''
8.0

8A

STANDARD LENGTH (mm)

Figure 3. — Percent length frequencies of bigeye tuna
larvae captured during the day (broken line, 271 speci-
mens) and night (solid line, 84 specimens).

Analyses of our data show that yellowfin tuna
larvae were more successfully captured in day
tows than at night, even though greater net
avoidance during the day was indicated. Had
net avoidance been the major factor in day-
night differences in abundance, more larvae
should have been captured at night. Apparently
—since the opposite is indicated — yellowfin tuna
larvae migrate to the surface in the day and net
avoidance is of minor imi)ortance, in terms of
numbers collected. Ueyanagi (19(51) suggested
that istiophorid larvae behave similarly; other
workers (Wade, 1951 ; Strasburg, 1960; Klawe,

1963; Ueyanagi, 1969) found no decisive evi-
dence to show that yellowfin tuna larvae perform
a vertical diel migration to the surface.

Our study indicated that bigeye tuna larvae
— like those of yellowfin tuna — migrate verti-
cally to the surface in the day, but the proba-
bilities were not as significant (P = 0.02 com-
pared with P <0.01 for yellowfin tuna). Net
avoidance was negligible for bigeye tuna larvae.
Ueyanagi (1969) reported a greater larval ocur-
rence of bigeye tuna at the surface during the
day than at night.

Our evidence showed that skipjack tuna
larvae migrate vertically to the surface at night
and that net avoidance was apparently negligi-
ble. A vertical migration to the surface at night
also was suggested by Wade (1951) and Stras-
burg (1960). Ueyanagi (1969) reported a
scarcity at the surface during the day, but in-
creased abundance at night.

&^

20-

O

«. ^o-\

o

>-

0-

° ■

o

■ t

I

"A

n

ii/i

M

o-o DAY

' V

1 >>

/

\ "

•—•NIGHT

i

1 1

I I ' I I ' ' ' I ' ' ' I '
2.0 4.0 6.0 8.0

I I I I

2.4 4.4 6.4 8.4

STANDARD LENGTH (mm)

T— r

FlGURE 4. — Percent length frequencies of skipjack
larvae captured during the day (broken line, 22 ;
mens) and night (solid line, 197 specimens).

558

RICHARDS AND SIMMONS: DISTRIBUTION OF TUNA LARVAE

30H

20-

o
o

i: 10

0-

2.0
24

' I '
40

6.0

4.4 6.4
STANDARD

' " I '
8.0

I
8/4

LENGTH

T-r-r-rA/T-r

10.0 22.0

104
(mm )

224

Our night tows caught little tunny larvae
more successfully than day tows, but differences
were not as pronounced as they were for skip-
jack tuna larvae (P = 0.03 compared with
P <0.01 for skipjack tuna larvae). Since a
greater ability to dodge the net during the day
was indicated, day-night differences could have
been caused by migration to the surface at night,
net avoidance, or a combination of both. Among
larvae of yellowfin tuna, bigeye tuna, skipjack
tuna, and Auxis, net avoidance was negligible
or ineffective in detecting day-night differences
in abundance. The higher frequency of night
captures of little tunny larvae, therefore, was
probably caused primarily by vertical migration
to the surface at night. Vertical migration to
the surface at night also was suggested for the
closely related Eidhynnus yaito (=E. affinis)
by Wade (1951).

Figure 5. — Percent length frequencies little tunny larvae
captured during the day (broken line, 134 specimens) and
night (solid line, 72 specimens).

^20-

O

10-

o

oc 0-

o-o

o-o DAY
NIGHT

I I I I I I ' ' I ' '
2.0 4.0 6.0

I I I

2.4 4.4 6.4

I I I I I I I I I I I I I I I I I I I I I I ''' I '

8.0 10.0 12.0 14.0 16.0 18.0 20.0

I I I I I I I

8.4 104 124 14.4 16.4 18.4 >

STANDARD LENGTH (mm)

Figure 6. — Percent length frequencies of Auxis larvae captured during the day (broken line, 1,636 specimens)

and night (solid line, 1,082 specimens).

559

FISHERY BULLETIN: VOL. 69, NO. 3

Auxis larvae wei-e equally abundant in day
and night tows, indicating that this species does
not migrate to the surface. The indication of
net avoidance during the day had no detectable
effect on apparent abundance, but if Anxis
larvae were more abundant at the surface dur-
ing the day and net avoidance had a significant
effect on abundance, the same results could be
obtained. Larval Auxis were almost equally
abundant at the surface in day and night col-
lections according to Wade (1951). Strasburg
(1960) captured more Auxis larvae in 0 to 60 m
tows at night and stated that Matsumoto (1958)
also captured more specimens in night surface
tows. Klawe (1963) reported greater success
in catching Auxis larvae at night in surface and
300-m oblique tows but not in 140-m oblique
tows; he suggested that net avoidance may be
primarily responsible for decreased day catches.
In a more recent study, Klawe, Pella, and Leet
(1970) concluded that Auxis larvae did not ex-
hibit a diel vertical movement; they also found
no indication of net avoidance.

DISTRIBUTION OF LARVAE

Because all our collections were made by
surface tows, it was not possible to directly com-
pare our totals with the number of larvae col-
lected during the Equalant surveys (Richards,
1967, 1969). The two multiship Equalant sur-
veys covered most of the tropical Atlantic Ocean.
Equalant I took place at the same time of year
as Geronimo cruises 3 and 5 ("warm season"),
Equalant II corresponded to the time of Gero-
nimo cruise 4 ("cool season"). The average
number of tuna larvae collected per 1,000 m^ of
water strained on each Geronimo cruise herein
discussed and the average under 1 are (100 m-)
of sea surface for Equalant I and Equalant II
(Richards, 1969) are shown in Table 3. The
average numbers of larvae collected on the
Geronimo cruises were corrected for diel var-
iations in abundance. This was computed by
the following formula:

where a = total number of standardized
day-caught larvae
a' = total number of standardized

night-caught larvae
h = total number of day tows
h' — total number of night tows.
The correction was applied to all species except
Auxis because that species was equally abun-
dant in day and night collections. The averages
for Auxis were obtained by dividing the total
number of standardized larvae by the total num-
ber of tows. The Equalant averages were not
corrected for diel variations in abundance be-
cause most of the collections were oblique and
sampled the entire vertical range of all tuna
larvae. Calculations for the average number of
larvae collected were similar to those used for
Auxis but were expressed as the number under
1 are of sea surface. In the following separate
accounts we report on our detailed findings con-
cerning each species of larval tuna.

Table 3. — The average number of tuna larvae col-
lected on Geronimo cruises 3, 4, and 5 and the two
Equalant surveys.

Species

Geronimo

cruise

Equalant

survey

3

4

1

'S

25

1 II

\timbfr

P"

WOO m3

Numhfr undfr 1 are

Yellowfin tuna

11.4

5-2

I.l

1.0

7.82

5.05

Bigeye tuna

2.9

0.9

0.4

0.6

3.00

1.24

Skipjack tuna

2,3

0.3

0.1

0.2

13.71

7.85

Little tunny

3.5

0.8

0.4

0.4

_,

„

Auxit sp.

12.6

9.9

6.5

18.8

-

—

a/h

/6'

1 14 March to 19 April 1965 in northwestern Gulf of Guinea.
- 10 February to 2 March 1965 off Sierra Leone.

YELLOWFIN TUNA LARVAE

The distribution of yellowfin tuna larvae in
the northwestern Gulf of Guinea is shown in
Figure 7. During Geronimo cruise 3, yellowfin
tuna larvae were common throughout most of
the area, averaging 11.4' larvae per 1000 m^ of
water strained. During cruise 5 (in the Gulf of
Guinea a year later), a smaller area was sam-
pled and an average of 1.1 larvae was collected
per 1000 m'' of water strained. During Equalant
I, no larvae were found north of about lat 2° N in
the same area, in contrast to the distribution
found during Geronimo cruise 3. We presume

560

RICHARDS AND SI\LMO.\S; DISTRIBITION OF Tl NA LAR\AE

GE-3

GE-5

GE-5

LARVAE PER 1000 m^

o 0 • 1-10

• 11-50 • 51 And Over

Figure 7. — The distribution of yellowfin tuna larvae in the northwestern Gulf of Guinea based on collections
during Geronimo cruises 3 (10 February to 26 April 1964), 4 (5 August to 13 October 1964), 5 (14 March to
19 April 1965), and cruise 5 off Sierra Leone (10 February to 2 March 1965).

561

FISHERY BL'LLETIN: VOL. 69, NO. 5

that the difference was because of increased sam-
pling intensity on Geronimo cruise 3. Wide-
spread spawning was seen near the equator, liow-
ever, on both Equalant I and Geronimo cruise 3.
An indication of this equatorial spawning is evi-
dent in cruise 5 (Figure 7). During Geronimo
cruise 4, the distribution of larvae was reduced
from that seen on cruise 3, averaging 5.2 larvae
per 1000 m^ of water strained. Again the situ-
ation differed from that found in Equalant II
during which almost no larvae were taken,
probably because of light sampling.

Richards (1969) found no yellowfin tuna
larvae in waters with temj^eratures lower than
26° C, and indicated that the presence of yellow-
fin tuna larvae may depend on water tempera-
ture. During the Geron imo cruises, with one ex-
ception, yellowfin tuna larvae were collected in
waters warmer than 24° C. Hence, the lower
limit of 26° C for surface temperature set for
the presence of yellowfin tuna larvae by Richards
(1969) should be lowered to 24° C. Surface
water temperatures were above 27° C at all sta-
tions sampled during cruise 3, and yellowfin tuna
larvae were found between 27.9° and 29.7° C.
During cruise .5 (also the "warm season") , sur-
face tem])eratures ranged from 22.5° to 29.9° C
but yellowfin tuna larvae were found within a
range of 24.9° to 29.5° C. During cruise 4 (the
"cool season"), surface temperatures ranged
from 19.3° to 25.5° C; yellowfin tuna larvae were
found only in water with temperatures higher
than 24° C except at one station with a temper-
ature of 23.6° C. During cruises 3, 4, and 5,
surface salinity values ranged from SS'/i, to 36',,^.
The yellowfin tuna larvae were rarely encount-
ered when salinity fell below 34/i, but were
common between 34'/;, and 36%c.

In the area off Sierra Leone, yellowfin tuna
larvae were encountered in water tempei-atures
higher than 25° C (Figure 7), the area south of
the 25° C isotherm. That area was not covered
during the "cool season" by Geronimo crui.ses
hut did receive minor coverage on Equalants I
and II, which resulted in the collection of some
tuna larvae, particularly on Equalant II. Water
temperatures were 26° C or higher at the Equal-
ant stations where collections wei'e made. Co-
nand (1970) found yellowfin tuna larvae in

waters warmer than 27° C off Senegal.

The Gulf of Guinea and contiguous waters ac-
count for much of the Atlantic tuna catch.
Beardsley's (1969) discussion of the relation of
oceanographic features to adult yello\vfin tuna
distributions in that area is of interest to the
present study. In his summary charts of adult
yellowfin tuna distributions, some catch rates
are high in areas of cool water where the larvae
do not occur, which indicates that an abundance
of adults may not indicate abundance of larvae.
Surface fishing was carried out by the Geronimo
during cruises 3, 4, and 5 and it was interesting
to note that there was no apparent relation be-
tween sightings of surface schools and location
of larvae.

BIGEYE TUNA LARVAE

The distribution of bigeye tuna larvae in the
northwestern Gulf of Guinea approximated that
of yellowfin tuna larvae (Figure 8), but the
average number per 1000 m^ of water strained
was less than for yellowfin tuna larvae. (A
similar pattern was noticed on the Equalant
surveys) . Off Sierra Leone, the species was col-
lected as often as yellowfin tuna (29 bigeye tuna
stations compared with 28 yellowfin tuna sta-
tions), but the average number of bigeye tuna
larvae collected was less than that of the yellow-
fin tuna. Larvae of bigeye tuna — like the yellow-
fin tuna larvae — were collected offshore, south
of the 25° C isotherm. The apparent abundance
of bigeye tuna larvae, compared with yellowfin
tuna larvae, closely resembles that of the adults,
as shown in the Japanese Atlantic longline data
( Wise') . During the Equalant surveys, 3.0 times
more yellowfin tuna larvae than bigeye tuna lar-
vae were captured. In 1963 (the year of Equal-
ants I and II) 3.4 times more yellowfin tuna
adults than bigeye tuna adults were captured by
Jai)anese longliners in the same general area
(Wise, see footnote 3). During the Geronimo
surveys 3.9 times more yellowfin tuna larvae than
bigeye tuna larvae were captured. In 1964 (the

' Wise, .1. P. 1969. .'^ome basic stati.stics of the .At-
lantic tuna fi.shrrie.s. B.C.F. Tropical Atlantic Biological
Laboratory, [Miami, Fla.,] Data Summary No. 8, 14 p.
[Processed.]

562

RICHARDS AND SIMMONS; DISTRIBUTION OF TUNA LARVAE

GE

-3

8-

o

•

1

1

4°-

^

°^^

•
•
o

•

0°-

o

o

•
•
o
o

•

•

0

• o
o

o

0 •
o

0
0
0

•
•

•

•
o

0

° •

4°-

1-

0-

5^'

12=

10°

GE-4

• K?>^°°*^ .••o°od'

0*„ «• O i„r(P

0°

GE-5

LARVAE PER 1000 m^

0 • 1-10

• 11-50 • 51 And Over

Figure 8. — The distribution of bigeye tuna larvae in the northwestern Gulf of Guinea based on collections
during Geronimo cruises 3 (10 February to 26 April 1964), 4 (5 August to 13 October 1964), 5 (14 March
to 19 April 1965), and cruise 5 off Sierra Leone (10 February to 2 March 1965).

563

FISHERY BULLETIN: VOL. 69, NO. 3

predominant year of the Geronimo surveys) , 3.7
times more adult yellowfin tuna than adult big-
eye tuna were captured by Japanese longliners
in the same general area (Wise, see footnote 3) .

SKIPJACK TUNA LARVAE

Richards (1969) found that distributions of
skipjack tuna larvae differed from those of yel-
lowfin and bigeye tunas, particularly when
surface temperature values were below 26° C.
Apparently skipjack tuna larvae are able to
tolerate lower temperatures than the other two
tunas. In the area covered by Geronimo cruise 3,
distributions of larval skipjack tuna (Figure 9)
were similar to those of yellowfin tuna larvae,
but fewer were caught. The lesser quantities
may have resulted from the sampling method
used; surface collections may not adequately
sample the species.

On Geronimo cruise 3, skipjack tuna larvae
were collected in water temperatures that ranged
from 27.6° to 29.7° C and salinities from 34.4^*.
to 35.5';V. On Geronimo cruise 4 (Figure 9) the
species was infrequently collected, although
larvae had been commonly collected in the same
region on Equalant II. Skipjack tuna larvae
were found in the warmer water (24.4°-25.8° C)
on Geronimo cruise 4, which was also true of
Equalant II (see Richards, 1969: 298). On
Geronimo cruise 5 (Figure 9) larval skipjack
tunas were taken at only four stations, presum-
ably an artifact of the sampling method. Off
Sierra Leone, these larvae were found at only
seven stations, perhaps again an artifact of
sampling.

LITTLE TUNNY LARVAE

also noticeably different from that of the other
tuna species. The temperatures for the larvae
ranged from 22.7° to 29.3° C and the salinities
from 32.7^',r to 35.4;,,. Apparently little tunny
larvae can tolerate a wider range of physical
conditions than can the larvae of the more
oceanic tunas — skipjack, yellowfin, and bigeye.

Auxis sp.

Larvae of Auxis (frigate mackerels) are un-
questionably the most abundant scombrid larvae
found in these tropical waters. This abundance
holds true for the eastern Pacific (Klawe, 1963) ,
as well as for the eastern Atlantic (Figure 11).
(We are aware that Auxis may be two species,
but as yet methods for distinguishing their
larvae have not been satisfactorily developed.)
In the northwestern Gulf of Guinea, Auxis larvae
were collected mostly nearshore, though a few
specimens were found offshore. Auxis was the
only species widely distributed off Sierra Leone.
One reason for its abundance may be the wide
tolerance of the larvae for temperature and sa-
linity— Auxis larvae were found in water with
temperatures as low as 21.6° C and as high as
30.5° C, the widest temperature range found for
any tuna larvae we studied. The salinity range
of the species was 33.2/,'r to 35.9/,c.

ACKNOWLEDGMENTS

This manuscript was reviewed by Elbei't H.
Ahlstrom, National Marine Fisheries Service,
La Jolla, Calif.; Witold L. Klawe, Inter-Amer-
ican Tropical Tuna Commission, La Jolla, Calif. ;
and Walter M. Matsumoto, National Marine
Fisheries Service, Honolulu, Hawaii. We appre-
ciate their effoi-ts in our behalf.

Little tunny larvae were collected during the
Equalant surveys but the data have not yet been
evaluated. In the northwestern Gulf of Guinea
and off Sierra Leone, little tunny larvae were
collected during each Geronimo cruise (Figure
10). Unlike the other species, they were not
collected on the outer ti-ansects near the equator.
The distribution of the larvae of this species,
as it related to temperature and salinity, was

LITERATURE CITED

Ahlstrom, E. H.

1959. Vertical distribution of pelagic fish eggs and
larvae off California and Baja California. U.S.
Fish Wildl. Serv., Fish. Bull. 60: 107-146.
Be.ard.sley, G. L., Jr.

19C9. Distribution and apparent relative abundance
of yellowfin tuna (Tluinniis albacares) in the east-
ern tropical Atlantic in relation to oceanographic
features. Bull. Mar. Sci. 19: 48-56.

564

RIC}IARDS AND SIMMONS; DISTRIBUTION OF TUNA LARVAE

GE-3

GE-4

ff-

10'

10^

GE-

5

lOf-

"^

*■

0

o

0 o

o
o

^^^^^1

O

o

O O

o

o o
0 o

^H

o

o o

o °

^^H

r-

8

o

0

o o
o o

°°o

^M

•
o
o

o o
o o
0 o

o 0 0 ^■^M

O ° ° § O

o

R °

O 0

o o o o °

o o

o

O 0

o 0 oo 0

6°-

o

^ o

o S

° o ° "P
o° o o

° §*° 0

• 0 o

0 o

o o

• 0

4-

20°

ir

16

14

4-

0-

12

GE-5

?°8oO°o

O O O O o OO^

§°8o8o^

4) °oo o o o

-r-
0°

LARVAE PER 1000 m^

o 0 . 1-10

• 11-50 • 51 And Over

Figure 9. — The distribution of skipjack tuna larvae in the northwestern Gulf of Guinea based on collections
during Geronimo cruises 3 (10 February to 26 April 1964), 4 (5 August to 13 October 1964), 5 (14 March to
19 April 1965), and cruise 5 off Sierra Leone (10 February to 2 March 1965).

565

GE-3

8-

[^^H^^HH

^^^^^^^^^^^^^^^^^^^^^^^i^^^^^^^^^^i

4-

0 0 ° o-

(f-

0 0 0

0 0
0 0 0 0
0 0 0
0 0 0

0 0

0

0 0 0 0 0

4°-

12°

(f-

FISHERY BLLLETIN': VOL. 69, NO. .1

GE-4

GE-5

LARVAE PER 1000 m^

0 • 1-10

• 11-50 •SI And Over

Figure 10. — The distribution of little tunny larvae in the northwestern Gulf of Guinea based on collections dur-
ing Geronimo cruises 3 (10 February to 26 April 1964), 4 (5 August to 13 October 1964), 5 (14 March to 19
April 1965), and cruise 5 off Sierra Leone (10 February to 2 March 1965).

566

RICHARDS AND SIMMONS: DISTRIBUTION OF TINA LAR\ Ali

0-

GE-3

12

—r—
0

GE-4

GE-5

GE-5

4-
2-

O

0

o

o
o

o

o

si:

O Q (

DO #0 •
0 o °

• o
o

o

0

o
o
o
o
o
o

o
o

0-
2-

o

I

o

1 r

12 6 4 2 tf 2°

LARVAE PER 1000 m^

o 0 . 1-10

• 11-50 • 51 And Over

FiGlRE 11. — The distribution of frigate mackerel larvae, Aiixis sp., in the northwestern Gulf of Guinea based
on collections during Geronimo cruises 3 (10 February to 26 April 1964), 4 (5 August to 13 October 1964),
5 (14 March to 19 April 1965), and cruise 5 off Sierra Leone (10 February to 2 March 1965).

567

FISHERY BULLETIN: VOL 69. NO. 3

Brucks, J. T., M. C. Ingham, and T. D. Leming.

1968a. Oceanic conditions in the northwestern
Gulf of Guinea, 14 to 30 March 1965 (part of
Geronimo cruise 5). U.S. Fish. Wildl. Serv., Data
Rep. 27, 46 p.

1968b. Oceanic conditions off Sierra Leone, 10 Feb-
ruary to 2 March 1965 (part of Geronimo cruise
5). U.S. Fish Wildl. Serv., Data Rep. 28, 43 p.
Conand, F.

1970. Distribution et abondance des larves de
quelques famille et especes de poissons des cotes
Senegambiennes en 1968. ORSTOM Dakar, Doc.
Sci. Prov. 26, 52 p.
GouLET, J. R., Jr., and M. C. Ingham.

1968. Oceanic conditions in the northwestern Gulf
of Guinea, Geronimo cruise 3, 10 February to 21
April 1964. U.S. Fish Wildl. Serv., Data Rep.

25, 46 p.
Ingham, M. C.

1970. Coastal upwelling in the northwestern Gulf
of Guinea. Bull. Mar. Sci. 20: 1-34.
Ingham, M. C., J. R. Goulet, Jr., and J. T. Brucks.

1968. Oceanic conditions in the northwestern Gulf
of Guinea, Geronimo cruise 4, 5 August to 13 Oc-
tober 1964. U.S. Fish Wildl. Serv., Data Rep.

26, 48 p.
Klawe, W. L.

1963. Observations on the spawning of four species
of tuna (Neothumiiis macropteriis, Katsuwoniis
pelamis, Auxis thazard and Euthynnus lineatiis)
in the eastern Pacific Ocean, based on the distribu-
tion of their larvae and juveniles. Inter-Am. Trop.
Tuna Comm. Bull. 6: 447-540.
Klawe, W. L., J. J. Pella, and W. S. Leet.

1970. The distribution, abundance and ecology of
larval tunas from the entrance to the Gulf of Cal-
ifornia. Inter-Am. Trop. Tuna Comm. Bull. 14:
505-544.
Matsumoto, W. M.

1958. Description and distribution of larvae of four
species of tuna in central Pacific waters. U.S.
Fish Wildl. Serv., Fish. Bull. 58: 31-72.
Richards, W. J.

1967. On the distribution and abundance of tuna
larvae. (Abstr. ) Proceedings of the Symposium
on the Oceanography and Fisheries Resources of
the Tropical Atlantic. FAO (Food Agr. Organ.
U.N.) Fish. Rep. 51: 60.

1969. Distribution and relative apparent abun-
dance of larval tunas collected in the tropical At-
lantic during Equalant surveys I and II. Pro-
ceedings of the Symposium on the Oceanography
and Fisheries Resources of the Tropical Atlantic,
Abidjan, 1966. UNESCO (U.N. Educ. Sci. Cult.
Organ.), Paris, p. 289-315.

Richards, W. J., D. C. Simmons, A. Jensen, and W. C.
Mann.

1969a. Tuna larvae (Pisces, Scombridae) collected
in the northwestern Gulf of Guinea, Geronimo
cruise 3, 10 February to 26 April 1964. U.S.
Fish Wildl. Serv., Data Rep. 36, 18 p.

1969b. Larvae of tuna and frigate mackerel
(Pisces, Scombridae) collected in the northwestern
Gulf of Guinea, Geronimo cruise 4, 5 August to 13
October 1964. U.S. Fish Wildl. Serv., Data Rep.
37, 16 p.

1970. Larvae of tuna and frigate mackerel (Pisces,
Scombridae) in the northwestern Gulf of Guinea
and off Sierra Leone, Geronimo cruise 5, 10 Feb-
ruary to 19 April 1965. U.S. Fish Wildl. Serv.,
Data Rep. 40, 23 p.

SlEGEL, S.

1956. Nonparametric statistics: for the behavioral
sciences. McGraw, New York, xvii -|- 312 p.
Strasburg, D. W.

1960. Estimates of larval tuna abundance in the
central Pacific. U.S. Fish Wildl. Serv., Fish.
Bull. 60: 231-255.
Wade, C. B.

1951. Larvae of tuna and tuna-like fishes from
Philippine waters. U.S. Fish Wildl. Serv., Fish.
Bull. 51: 445-485.
Ueyanagi, S.

1964. Description and distribution of larvae of five
istiophorid species in the Indo-Pacific. Proceed-
ings of the Sjnuposium on Scombroid Fishes held
at Mandapam Camp from Jan. 12-15, 1962. Mar.
Biol. Assoc. India, Sympos. Ser. 1: 499-528.
1969. Observations on the distribution of tuna
larvae in the Indo-Pacific Ocean with emphasis
on the delineation of the spawning areas of al-
bacore, Tliunviifi alalnnga. [In Japanese, English
synopsis.] Bull. Far Seas Fish Res. Lab. (Shi-
mizu) 2: 177-256.

568

RANDOM VARIABILITY AND PARAMETER ESTIMATION
FOR THE GENERALIZED PRODUCTION MODEL'

William W. Fox, Jr.^

ABSTRACT

Three alternative statistical models are proposed for estimating the parameters of the generalized pro-
duction model by the method of least squares. A stochastic representation of the generalized produc-
tion model is consti'ucted and simulation (or the Monte Carlo Method) is employed to infer the effects
of random variability on the variation in catch. The use of residuals examination for selecting the
appropriate statistical model for least-squares estimation of the generalized production model param-
eters is demonstrated for the yellowfin tuna fishery in the eastern tropical Pacific Ocean. In both the
simulation and actual fishery, statistical Model 3 — assuming catch residual variance is proportional to
the catch squared — best fulfills the assumptions of least-squares theory and should, therefore, provide
the best least-square parameter estimates.

Mathematical models are powerful tools which
are being used increasingly in resource man-
agement. A knowledge of mathematics allows
a resource manager to construct from gathered
data a representation of the real system and,
coupled with statistical theory, allows estima-
tion of the parameters of his model. Then, as
is impossible in the real system, a manager may
experiment on his model and derive outcomes
which aid decisions about management of the
real system. Results of model experimentation
usually depend greatly on the formulation of the
model and to some degi-ee on the accuracy of
the parameter estimates. Often precise statisti-
cal parameter estimation lags behind mathemati-
cal formulation, primarily because many math-
ematical models are robust, i.e., decisions are
independent of parameter accuracy. This is one
reason for the development of detei-ministic
rather than stochastic models. However, it
seems that it is always desirable to obtain the
best possible parameter estimates from the data
at hand.

' Quantitative Science Paper No. 16. A series pre-
pared under the general sponsorship of the Quantitative
Ecology and Natural Resource Management Program
supported by Ford Foundation Grant Number 68-183.

- Center for Quantitative Science in Forestry, Fish-
eries and Wildlife, University of Washington, Seattle,
Wash. 98105.

A simple case of Bernoulli's equation has been
suggested as a model for the growth of an or-
ganism by Richards (1959), Chapman (1961),
and Taylor (1962)

dx/dt

Ha-,'" — Kxt

(1)

where x, represents either weight or length at
time t, and H, K, and m are parameters which
may be given some physiological significance.
Recently equation (1) has been advanced inde-
pendently by Chapman (1967) and Pella and
Tomlinson (1969) as a simple model for assess-
ing the relation between exploitation and yield
(or catch) from a living resource

dP/dt = HPr — KP, — qfP, for m < 1

(2)
dP/dt = — HP,'" + KP, — qfP, for m > 1

where P, is the population size (biomass or num-
bers), / is the amount of fishing effort, q is the
coefficient of catchability, and H, K, and m are
parameters. It is assumed that / is constant
over the time period that equation (2) is used.
Therefore, qf = F, the instantaneous fishing
mortality coefficient, and qfP, = C, the catch.
Equation (2), referred to herein as the gener-
alized production model after Pella and Tomlin-
son (1969), includes the logistic model used by

Manuscript accepted February 1971.

FISHERY BULLETIN: VOL. 69, NO. 3, 1971.

569

FISHERY BULLETIN: VOL, 69, NO. 3

Graham (1935), Schaefer (1954, 1957), and
others when m = 2, and the exponential model
discussed by Fox (1970) if the limit is taken
as m -> 1.

This type of production modeling is a stock
assessment approach which has extreme math-
ematical and data requirement simplicity.
Therein lies its primary virtue; for example,
equation (2) contains only four parameters
whereas the simplest Beverton and Holt (1957)
type of model providing the same relation con-
tains at least nine parameters. Estimation of
the parameters of equation (2) requires only
catch and fishing effort data while at the very
least, the Beverton and Holt approach addition-
ally requires age structure information. Dis-
cussion of the different assumptions for imple-
menting each approach can be found in Schaefer
and Beverton (1963). The generalized produc-
tion model provides for a wide variety of shapes
for the production curve and thus coupled with
its mathematical simplicity represents an im-
portant tool for successfully managing exploi-
tation.

Procedures for estimating the parameters of
production models can be found in Schaefer
(1954, 1957), Ricker (1958), Chapman, Myhre
and Southward (1962), Gulland (1969), and
Pella and Tomlinson (1969). However, it ap-
pears that in all cases, except Schaefer (1957),
random variation about the deterministic pre-
dictions of the production model has been largely
ignored in choosing a statiMical model for esti-
mating the parameters. Perhaps this is because
of the apparent formidable nature of such var-
iation. On the other hand, such variation may
often be approximated in a simple manner to
allow better estimates of the parameters than
if ignored altogether. It is conceded that the
generalized production model is at the very best
only a good approximation of the actual biologi-
cal dynamics, but this should not imply that
better parameter estimates are unwarranted, un-
less its prime vii'tue of mathematical simplicity
is compromised in the course of such action.

Several statistical models for estimating the
parameters of mathematical models of biological
I'elationships have been discussed variously by
Zar (1968), Glass (1969), Hafley (1969), and

Pienaar and Thomson (1969). While to the
nonstatistician these papers may bear a strong
resemblance to quibbling over apparent minor
differences of results in the face of large data
variability, the improper statistical model can
lead to misleading conclusions or to significant
errors, as several of the above authors demon-
strated. Statistical models differ on the assump-
tion about the manner in which variation or
error enters the deterministic biological model.
The technique employed by Pienaar and Thom-
son (1969) to assess fulfillment of the assump-
tions about variation is the graphing and ex-
amination of i-esiduals, the differences between
the observed data and those predicted by the
model. Extensive discussion on the examination
and analysis of residuals can be found in Ans-
combe (1961), Anscombe and Tukey (1963),
and Draper and Smith (1966).

This paper presents a discussion of the nature
of simple random variability and its relation to
estimating the parameters of the generalized
production model. An illustration of residuals
examination in selecting the appropriate sta-
tistical model for the parameter estimating
technique of Pella and Tomlinson (1969) is in-
cluded. Data from the fishery for yellowfin tuna,
Thunnus albacares, in the eastern tropical Pa-
cific Ocean were utilized in the illustration.

STATISTICAL MODELS

Schaefer (1957) recognized that the produc-
tion model is not deterministic and represented
environmentally induced variation as an additive
term consisting of a random variable tj multi-
plied by population size. In terms of the gen-
eralized production model

dP/dt = KPt — HPt — qfP, + rjP, . (3)

His parameter-estimating procedure used a finite
difference approximation of equation (3) di-
vided through by Pt for the case when m = 2.
By summing over many time periods the effects
of variation are eliminated since the expected
value (or mean) of -q is zero. Schaefer's form-
ulation of the error term, while rea.sonable and
convenient for his estimating technique, pro-

570

FOX: RANDOM VARIABILITY AND PARAMETER ESTIMATION

duces a complex statistical model on integrating
equation (3). Therefore, his statistical model
was given no further consideration.

Pella and Tomlinson (1969) also mentioned
that the generalized production model is not
deterministic. They pointed out several sources
of error in Schaefer's finite difference approxi-
mation of population change and estimation pro-
cedure, and advanced a "least-squares" searching
procedure as an alternative. In doing so, how-
ever, apparently no consideration was given to
statistical implications of their technique. The
Pella-Tomlinson procedure integrates equation
(2) over the time period during which the fish-
ing effort is assumed constant, A(, to give

X e

_, I

-IK (*) g/) (1-m) t 1-""

(4)

where Po is the population size at the beginning
of the time period, and the upper signs applying
when TO < 1 and the lower when to > 1. Start-
ing with initial guesses of the parameter values,
an estimated catch history, { C, } where i =
1 . . . n time periods, is calculated from the known
fishing effort history, \ fi} , by the formula

N . ^ ^
Ci = qfi- 2 ^(Pui + Pi.i + i) • ^t,/N (5)
3 = 1

where Pi„- are found from equation (4) over
j = 1 . . .N subintervals of each time interval /.
The fitting criterion, S, is computed from the
known catch history, \Ci], of /( time periods as

n
S = 2 (C.
i = 1

i = 1 '

(6)

where the £; are residuals. The initial parameter
guesses are then modified in a searching routine
with their computer program GENPROD until
those parameter values which minimize S are
located.

The statistic S is a "least-squares" criterion.
For the parameters of a nonlinear model which
minimize S to be the best least-squares estimates,
the residuals, ti, must: 1) be independent, 2)

have an expected value (or mean) of zero, and
3) have^ constant variance (i.e., not correlated
with t, C„ or /,).' Consequently, the proper sta-
tistical model for the Pella-Tomlinson fitting
technique must both fulfill the three assumptions
and be biologically rational. It is also important
that the statistical model be simple, i.e., one
which requires no additional parameters to be
estimated.

Ignoring for the moment that equation (5)
is an approximation, the choice of equation (6)
as the least-squares estimate criterion tacitly
assumes

givmg

Ci = Ci

P, = P, + (l/qf,) . ei

(7)
(8)

where P =

n

P dt for ease of notation. Equa-

tion (7), referred to hereafter as statistical
Model 0, is biologically tantamount to assuming
random variation in population size approaches
being infinitely great in an unexploited popula-
tion. This denies the concept of an environ-
mentally limited maximum population size or
"carrying capacity" which is usually a founda-
tion of the production model. Therefore, Model 0
assumed by Pella and Tomlinson is intrinsically
unattractive even though it may be a reasonable
approximation at intermediate exploited pop-
ulation levels.

There are three simple statistical models
(among many) which are commonly assumed,
biologically reasonable, and involve calculating
S as a weighted sum of squares or from trans-
formed data.

Model 1. Additive Error

so

Pi = Pi + eii (9)

Ci = Ci + (qf,) ■ e,i (10)

' Additionally, if the g, are normally distributed then
it can be shown that the least-squares estimates are
also the maximum likelihood estimates which have min-
imum variance as the number of data grows large —
hence are global best estimates (e.g., see Draper and
Smith, 1966).

571

FISHERY BULLETIN: VOL. 69, NO. 3

giving

Si = J [(C, - C,)/7,]- (11)

I = 1

as the appropriate criterion to be minimized.
Model 2. Multiplicative Error

Pi = Pi ■ en (12)

so

or

C, ^ Ci ■ 621

(13)

In Ci = In C, + In e.. (14)

giving

2 (In Ci
I = 1

In C,)- (15)

as the appropriate criterion to be minimized.
Model 3. Additive Proportional Error

P. = Pi + Pi ■ esi (16)

so

giving

Ci= Ci + C, ■ €zi

(17)

Sa = 2 [(Ci - C,)/C,]- (18)
i = 1

as the appropriate criterion to be minimized.

Model 1 assumes constant variation at all pop-
ulation levels. This is perhaps the least biologi-
cally reasonable of the three suggested alterna-
tive statistical models since it is easier to conceive
that under equilibrium conditions a population
will fluctuate more radically near its environ-
mentally limited maximum size than at smaller
sizes under constant exploitation. Model 1 is
usually employed as a statistical model when
variation is expected to arise from experimental
or measurement error. Assuming adequate sta-
tistics of catch and fishing effort exist, it is more
likely that variation will arise from environ-
mental influences on the parameters of the model.
Models 2 and ?> assume that variation in pojui-

lation size decreases with population size and
that variation in catch increases with the size
of the catch. Models 2 and 3 approximate the
stochastic representation of equation (2) sug-
gested by Pella and Tomlinson [their equation
(14)]

dP/dt = 7), l{±)HPt'

(^) AT,]

(19)

where ?ji and tj2 are continuous random variables.
Other statistical models obviously could be
constructed, such as

Pi = Pi

Pi

(20)

where c could assume any value — Models 1 and
3 are actually special cases with c = 0 or 1
respectively. However, this would introduce
another parameter to be estimated. The four
previously described statistical models will
suffice.

Returning to the point that equation (5) is
a numerical approximation of integration, equa-
tions (7), (10), (13), (14), and (17) are not
strictly true for the Pella-Tomlinson procedure.
Accurate representations would include an ad-
ditional error term due to linear approximation.
However, as provided for, the linear approxi-
mation error may be reduced by increasing the
value of A' in equation (5). As will be dem-
onstrated later, this error is very small in re-
lation to the magnitude of the €i even at small
values of A^. The choice of N, on the other hand,
can be critical to obtaining good estimates of
several parameters.

We now have three alternative statistical
models which fulfill the goals of simplicity and
biological rationality to various degrees. It re-
mains to be determined which of them fulfills
the assumptions of least-squares theory for ob-
taining the best pai-ameter estimates.

STOCHASTIC SIMULATION

An analytical solution for the approi)riate sta-
tistical model is not possible since the actual
causes of variability and the relationships to
their effects on the generalized production model

572

FOX: RANDOM VARIABILITY AND PARAMETER ESTIMATION

are unknown. However, a commonly used ap-
proach, simulation (or the Monte Carlo method) ,
may be employed to infer probable eflfects of
variability and lead to selection of the "best"
statistical model. This simulation study con-
sisted of constructing a stochastic (or proba-
bilistic) analogue of the generalized production
model and then simulating the catches at var-
ious levels of constant fishing effort. Inferences
will be drawn about the propriety of all four
statistical models from residual variation pro-
duced in the catches. Also, the sensitivity of
catch residual variation to parameter variation
will be demonstrated.

The generalized production model can be writ-
ten in a form that is more easily discussed bio-
logically

dP/dt = P,K[{P„
— qfPt

— F,'"-') /•?«"'-']

(21)

The signs ( + or — ) are set for convenience
assuming m > 1. The usual biological in-
terpretation of the constants is as follows:
K is "the intrinsic rate of natural increase",
P = (K/H)''""~^^ is the asymptotic environ-
mentally limited maximum population size or
"carrying capacity", and m is the determinant
of the pi'oportion of P^ at which the maximum
rate of production occurs. The stochastic an-
alogue of equation (21) is

dP/dt

PtK{(TT^-

- yfP.

— P,--') /tt^-']

(22)

|. are stochastic variables with
m, q\ re-

where [k, tt, (jl, y ^

expected values (or means) \K, P

spectively, and distributions and variances to

be specified. The parameters of equation (21)

were considered to be stochastic variables since

they are actually average conditions determined

by many environmental inter-relationships.

The distributions and variances of the sto-
chastic variables are unknown as are their
expected values to be estimated from the fishery
data. Some broad inferences about the distri-
butions can be made, however, from biological
and mathematical implications of the production
model. The "intrinsic rate of natural increase",

K, was assumed to be approximately normally
distributed [■~N (K.a-i)], because K is the re-
sultant rate of a linear combination of rates-—
birth rate — death rate (P in numbers) , or birth
rate + growth rate — death rate (P in biomass)
— so may be either positive or negative at any
given time. Negative values for tt and y are
biologically and physically meaningless so they
were assumed to be approximately log-normally
distributed [~logN(P^, 0--2) and ~logN(f/,cr^3)
respectively]. The integrated forms of equa-
tions (2), (21), or (22) do not exist for ni = 1;
therefore /x was assumed to be given by [1 -f
(m — 1 ) ^] where ^ was assumed to be approx-
imately log-normally distributed with a mean
of one [~logAMl, o-'4)]. This resulted in fi
having a mean of m with a range of minus in-
finity to one, or one to plus infinity, depending
on whether m is less or greater than one.

Integrating equation (22) from Po to Pt yields

— Po'-"

„U— ,/) (1-1,

(23)

this is the stochastic analogue of equation (4).
Expected values and arbitrary variances
(tr-i, ah, 0-^3, o-'i) were chosen to allow:

Stochastic

Expected

Approximate

variable

value

99% range

K

5.60

5.30-5.90

M

2.00

1.95-2.06

n (108)

1.40

1.07-1.83

7 (10-5)

7.00

6.63-7.39

The expected values were rounded approximate
values obtained in the example following this
section. In the same manner as the previously
described Pella-Tomlinson technique, equations
(5) and (23) were used to simulate a 48-year
catch history at each of 13 levels of fishing effort.
The continuous stochastic variable case was ap-
proximated by setting A'' = 10 in equation (5).
At each iteration, the stochastic variables
i^ K, n, IX, y \ were drawn at random from their
respective probability distributions, produced

573

FISHERY BULLETIN: VOL. 69, NO. 3

with a random number generator by the multi-
plicative congruential method (subroutine
RAND, University of Washington Computer
Center) . The variances and means of residuals
and log-residuals were calculated at each fishing
effort level.

The results of the simulation trials are given
in Table 1. It was obvious from the formulation
of equation (23) that Model 0 — assuming con-
stant residual variance — was inappropriate, the
simulation trials add confirmation. Model 1 —
assuming residual standard deviation propor-
tional to fishing efl'ort — is also rejected over any
moderate range of fishing effort. A close approx-
imation, however, is obtained for / ^ 22,000.

Model 2 — assuming constant log-residual var-
iance— appears to be valid up to .58,000 ^ / <
65,000, where a trend of increasing variance be-
gins. The hypothesis of common log-residual
variance for / ^ 65,000 was tested by Bartlett's
f-test (Snedecor and Cochran, 1967) . The result
is not significant (uncorrected x' = 7.72, 9 df,
Pr >0.50). Including the log-residual variance
for / = 70,000, however, significance is ap-
proached (corrected x^ = 16.35, 10 df,
Pr <0.10).

Model 3 — assuming residual standard devia-
tion proportional to catch — fulfills the assump-
tion about as well as Model 2. The proportional
relationship between the residuals standard de-
viations and deterministic catch (Figure 1) ap-
pears to be different between catches given by
fishing effort below and above that which pro-

■o 4

50 100 150

Deterministic Cotch (x lO')

200

Figure 1. — Standard deviation of the^ residuals, €3,
plotted against the deterministic catch, C, for statistical
Model 3. • = fishing effort below maximum sustainable
yield (MSY) level. A = fishing effort above MSY level.
® = fishing effort at MSY level.

duces the maximum sustainable yield (MSY)
(C = 196 X 10*). Regression analysis reveals
that variance about regression, Sy^^, is highly
significantly different between below and above
MSY levels (F r= 9.90; 4, J df; Pr <0.01), but
the regression coefficients, b, are not significantly
diff-erent (t = 1.47; 5 df; Pr >0.20)-Table 2.
The "above MSY" regression has a i/-intercept,
which must be zero, significantly different from
zero {t = 3.30; 4 df ; Pr <0.05). It appears
that Model 3, like Model 2, is valid up to
58,000 ^ / < 65,000 (Figure 1).

Table 1. — Results of the stochastic catch simulation trials of the generalized production model.

Fishing

Deterministic
catch

(I0«)
C

Deterministic

population

size

(}0«)

P

Mean residual

Residual variance

effort

(IW

In e
(lQ-«)

(10l»)

SSdn e)
(10-«)

1,000

96775

138.25

-0.0706

-0.7765

0.0844

9.1231

5,000

45.9375

131.25

-0.0599

-0.1713

1.7538

8.3187

10,000

85-7500

122.50

0,0143

-0.0218

5,7506

7.8882

15,000

119.4375

113.75

0.2155

0.1357

13,0288

9.0945

22,000

156.3100

101.50

-0,7088

-0.4956

20,4779

8.3884

29,000

181.1775

89.25

-1.1161

-0.6551

24.6701

7.5760

40,000

196.0000

70.00

-0.6563

-0.3646

22.6228

5.9845

51,000

181.1775

50.75

0.5173

0.2404

30.1457

9.1269

58.000

156.3100

38.50

-0.1051

—0.1044

18.4686

7.6021

45.000

119.4375

26.25

0.5438

0.3927

18.1894

12.5489

70,000

85.7500

17.50

0,2865

0.2577

11.5283

15.4564

75,000

45.9375

8.75

-0.3734

-0.9846

7.2114

34.2285

79,000

9.6775

1.75

-0.2770

-3.4017

0.8834

102.6439

574

FOX: RANDOM VARIABILITY AND PARAMETER ESTIMATION

Table 2. — Regression analysis for statistical Model 3 of standard deviation of catch residuals, S{ea), on determin-
istic catch, C, with levels of fishing effort below and above that which produces the maximum sustainable yield (MSY) .

Effort

level

regression

Degrees

of
freedom

S«2

S^y

ly'

J

Degrees

of
freedom

Sum

of

squares

S'y/x

Below MSY
Above MSY

5
5

21421.9
21421.9

601.047
498.146

16.9475
12.4109

0.028058
0.023254

4
4

0.083566
0.826986

0.020892
0.206746

In conclusion, the assumption of statistical
Models 0 and 1 were rejected by the simulation
study. Statistical Models 2 and 3 were found
to be valid over a wide and similar range of
fishing effort. Their range of validity includes
up to and well beyond the level of fishing effort
producing the MSY (/ = 40,000) , the most likely
range in which a fishery would operate. Em-
ploying Model 3 has a theoretical advantage over
Model 2 in a least-squares estimating procedure.
With Model 3, the actual residual variance is
minimized. Whereas with Model 2 the log-re-
sidual variance is minimized and the parameters
are best least-squares estimates only in the trans-
formed model. The theoretical advantage of
Model 3 may serve as a criterion for choosing it
when no other criteria exist.

Several additional simulation trials were made
to demonstrate the relative degree of influence
that random variability in each parameter ex-
erts on the variance of the catch residuals. The
upper two standard deviations of each stochastic
variable was set equal to 25 '^r of their mean,
the level of fishing effort was set at 40,000 ( MSY-
producing level), and four trials of 500 time
periods each were made. Each parameter in turn
was allowed to vary with the remaining three
constant (Table 3). The variation in catch was
most sensitive to varying the exponent, m, and
least sensitive to varying the catchability coeffi-
cient, q. This, of course, implies the relative
precision of the parameters if they had been ac-

Table 3. — Catch residual variance produced by variation
in each stochastic variable of the generalized production
model.

Stochastic
variable

Expected
value

Approximate
95% range

Residual

variance

S2 (c)
(10'2)

S2 (In e)
(10-4)

u

2.00

1 .67-2.50

46.0834

11.9100

K

5.60

4.20-7.00

36.8604

9.7958

T (108)

1.40

1.12-1.75

30.7556

8.1498

y (10-5)

7.00

5.60-8.75

17.1333

4.4781

tual estimates. One should not, however, gener-
alize on the order of precision since these results
obtain specifically for the assumed probability
distributions and expected values. This exercise
does demonstrate a frequently employed method
for implying which parameters, given their esti-
mates, are most critical and perhaps deserving of
additional independent estimation.

RESIDUALS EXAMINATION:
AN EXAMPLE

The data of catch, catch per unit effort, and
fishing effort from the eastern tropical Pacific
yellowfin tuna fishery (Pella and Tomlinson,
1969; Table 6) are plotted in Figure 2. Appar-
ently the population and fishery dynamics are
250r . A

E 200

150

.= 100

if 50

t

_L

_L

J_

_L

10 20 30 40 50

Fishing Effort (Thousands of Boat Days)

60

1— o

— DO

t'f

B

60

"0 10 20 30 40 50

Fishing Effort (Thousands of Boat Days)
Figure 2. — Data from the eastern tropical Pacific yellow-
fin tuna fishery, 1934-67, plotted as (A) catch vs. fishing
effort, and (B) catch per unit effort vs. fishing eflTort.

575

FISHERY BULLETIN: VOL. 69, NO. 3

well described by a production model — good re-
lationships are observed in Figure 2. These data
were used by Pella and Tomlinson in exempli-
fying their technique ; for comparative purposes
the same data are utilized here. The results of
this section, however, should be considered as
just an example and not a recommendation on
management.

The parameters of the generalized production
model for the tuna fishery were estimated by the
Pella-Tomlinson computer program, GENPROD,
replacing the fitting criterion, S, with those of
each alternative statistical model [equations
(11), (15), and (18)]. Each parameter was
searched to five digits or until the improvement
in S was less than 0.01 Cr at three levels of nu-
merical approximation in equation (5) —
M= 1,3,5- — (Table4). Increasing the precision
of numerical approximation greatly changed the
parameter estimates between N = 1 and 3, but
only slightly between N = S and 5. The most
sensitive parameter is H, followed in order by
K, q, m, and r. Consequently, the estimates
of the average environmentally limited maxi-
mum population _size, P„ , and average optimum
population size Poi,t, vary with the level of pre-

cision. Pella and Tomlinson indicated that un-
reasonable estimates were obtained for the
catchability coefficient, q, (presumably with
A'' = 1) and made an arbitrary selection of a
"reasonable" estimate. "Reasonable" catcha-
bility coefficients are obtained here with N = B,
making unnecessary the arbitrary selection of
a reasonable estimate. The management impli-
cations of maximum equilibrium catch, Cunx, and
optimum fishing efl'ort, /opt, are surprisingly
robust to the degree of precision of the numerical
approximation. Schaefer (1957) mentioned
previously, however, that these two management
implications are robust to changes in the esti-
mate of q in his estimating method; Pella and
Tomlinson also mentioned the phenomenon for
their technique. The S criteria values were re-
duced about Tyi- or less by choosing A'^ = 3, as
against A'' = 1 and reduced a negligible 0.2%
or less by choosing N = 5 (Si and S2 increased
minutely due to the level of precision chosen for
S) . Obviously, the error due to approximation
in equation (5), as previously stated, is negli-
gible for these data with A'' ^ 3.

Turning to the eff'ects of the alternative sta-
tistical models (with N = 5), it may be seen

Table 4. — Parameters and management implications of the generalized production model for the eastern tropical
Pacific yellowfin tuna fishery, 1934-67, estimated with the Pella-Tomlinson technique (GENPROD) using four dif-
ferent statistical models and three levels of precision, A^, in equation (5).

H
(10-5)

(10-

Management implications

Pounds
(10«)

Pounds
(10»)

/opt

Boat
days

Pounds
(10«)

Criterion

20

1.4

45._-

_.

182.6

35,300

1.78_-X10>«

0

1.4

2900-1

33,26

.820

27.00

44.6

182.6

35,200

19.2

I.7858X10"

1

1.9

0.17064

15.21

.904

21.69

52.7

186.2

33,210

25.8

4.7140X10'

2

1.6

34,502

16.65

.879

18.10

64.0

182.5

34,500

29.2

8.2214X10-

3

2.0

0.00748

7.57

.865

11.50

101.2

191.5

32,900

50.6

7.8762X10-

N = 3

0

1.5

59.999

7.65

.842

7.36

162.7

184.5

34,660

72.3

1.7197X101'

I

22

0.00013

5.90

.921

10.00

113.0

188.6

32,200

58.6

4.5291X10'

2

1.8

0,17092

5.86

.952

7.70

147.4

184,0

33,800

70.7

8.0355x10-1

3

2.0

0,00408

5.59

.835

8.50

136.9

191.5

32,900

68.5

7.3769X10-1

N = S

0

1.5

55,802

7.28

.843

7.10

170.4

183.9

34,200

75.7

1.7185X10>«

I

2.2

0,00010

5.38

.921

9.11

124.0

188.7

32,210

64.3

4,5296X10'

2

l.S

0.15820

5.61

.926

7.40

153.9

184.1

33,700

73.8

8.0371 X 10-'

3

2.1

0.00054

5.06

.845

8.10

142.7

192.6

32.700

72.7

7.3608X10-1

' Pella and Tomlinson (1969; Table 5).

576

FOX: RANDOM VARIABILITY AND PARAMETER ESTIMATION

that the most sensitive estimate is H, followed
in succession by the estimates of m, K, q, and r.
The estimates of the management implications
Cmax and /opt are, for all practical purposes, the
same among statistical models, but less similar
than among levels of precision. This may be
offered as an argument against considering al-
ternative statistical models. But consider the
plot of the data in Figure 2; one could draw
an average line by eye through the data and
arrive at estimates of Cmax and /opt just as ac-
curate as those estimated by the sophisticated
least-squares search technique. The point is that
with good data most rational statistical pro-
cedures should provide similar estimates of Cmax-
and /opt. One cannot be certain that this will
be so with data of lesser quality or different
range. The values of m which determine the
shape of the yield curve, on the other hand, are
very different between Models 0 and 3. This
could have a significant effect on an economic
analysis of the yield curve.

In the absence of other criteria for choosing
a particular statistical model, the "fit" — least
sum of squared residuals — is often selected
(Glass, 1969), and is perhaps a reasonable cri-
terion if the goal is interpolation. The goal here
is to obtain the best possible parameter estimates
in oi'der to make, in essence, extrapolations or
predictions. In the latter case the best criterion
is not the "fit", but the degree of assumption
fulfillment. Statistical Model 3 provided esti-
mates that were least influenced by the addition
of error — comparing the parameters' precision
between A'^ equalling 1 and 5 — inferring the
greatest confidence in its estimates. It was also
seen from the simulation study that Model 3
best fulfilled the assumptions of a least-squares
procedure. Model 3, ironically, "fits" the data
the worst, although only by about 6 /r .

Pienaar and Thomson (1969) have suggested
the utilization of an important tool for selecting
a statistical model which best fulfills the as-
sumptions of the estimating procedure — resid-
uals examination. Various plots of the residuals
suggested by Draper and Smith (1966) were
made for the four statistical models (Figure 3).
Each statistical model gives a mean residual
near zero fulfilling one of the least-squares as-

sumptions (Figure 3A). Plots of residuals
against time (Figure 3B) indicate: 1) variation
increases with time in Model 0 from 1934
through 1961, violating the assumption of con-
stant residual variance; 2) Model 1 tends to
over-correct as there is a propensity for var-
iation to decrease from 1940 through 1967; and
3) Models 2 and 3 are nearly identical in con-
trolling time-oriented variation. Runs — consec-
utive residuals of the same sign — are evident
in all four models, indicating violation of the
assumption of residual independence. There
are only ten runs in Model 3 giving a proba-
bility less than 0.01 that the arrangement of
signs is random (Figure 3B) . Draper and Smith
(1966) suggest, however, that unless the ratio
of degrees of freedom to number of observations
is small (here 29/34) , the effect can be ignored.
The dependence of consecutive residuals is un-
doubtedly due to vitiation of the assumption of
no time lags in the fish population. With changes
in fishing effort the age structure of the popu-
lation is altered as well. It might be possible
to average out these effects by considering a
time pei'iod longer than one year, say the aver-
age life-span of an individual. That would be
about 3 years for a yellowfin tuna, the approx-
imate mean length of the runs. However, that
would also reduce the number of observations
to eleven and the fishing effort, assumed con-
stant in integration of the model, would vary
considerably.

An increase in residual variation with deter-
ministic catch is obvious for Model 0 (Figure
3C), again violating the assumption of constant
residual variance. As in the time plot. Model 1
tends to over-correct for the phenomenon ex-
hibited by Model 0. Models 2 and 3 stabilize
the variance as might be expected. In the final
plot, residuals against fishing effort, the same
conclusions may be reached (Figure 3D) .

Models 2 and 3 apparently fulfill the assump-
tions of the least-squares procedure while Models
0 and 1 violate the assumption of constant re-
sidual variance. Invoking the previously men-
tioned criterion for choosing between Models 2
and 3, the best statistical model for this fishery
is Model 3.

577

Model 0 Co =0.00184 «I0'

ilX

X-i_

-5-4-3-2-1012345
Model I €| =-0.00658 « 10'

.ill

-3-2-1 0 I 2 3
€| X 10"'

Model 2 irri2 = 0.01555x10''

. 1 1 i 1 1 i .

-4-3-2-101234
InCjX 10

Model 3 ij =-0.20674x10-'

. i I I I. .

-3-2-10123
€,x 10

4|-
2

Model 0

FISHERY BULLETIN: VOL. 69, NO. 3

• B

-*-•"«--

2

7 I
2 0

-2

4
Q 2

~ Oh^-
= -2

Model

A^A^

^"a^

^A

-A.-.

Aa ^

.A-£i^e^

^ A
A

-4L

Model 2

A ^ AA

A A^

4
O 2

W -2
-4

Model 3

Aa

0 hv^-"-^----e— ^-.-^/-"-— --.-— -n-----

^ A
A

A A ^^

A ^^

I I I I I I I

D 5 10 15 20 25 30

t (Years)

r 21-

e 0

2 -

-3
-4

° 2

= -2
-4
4

9 2

« 0

w ^

-4

Model 0

Model I

_| V'-

• c

r Model 0

c^

2 Qf^s—

2 ^

A_.A

Model 2

A AA 5

AAA
^ A A^

• • •!

0 __- -.^^ • A__.A^

Model I

^

1^-

2 - ^

Model 3
^:iA A ^

^A ^A

A A

A

A ^A

-3

"* r Model 2
O 2 - ^

i;„ Q : *• '__jL. _•-

c "2 - • •

-4^ •

4
O 2

A A

_A_ fji^

/\\ A A

A A ^

-4

Model 3
Aa ^

0 -— <^-;2,-— '
11 -2 - A A

A

A^

L.

_L.

I L-

_L_

50

200

10 15 20 25 30 35 40
f (Thousands of Bool Days)

_^I00 150

C (Millions of Pounds)

Figure 3. — Plots of residuals, e,, for statistical Models 0, 1, 2, 3, from the generalized production model for the
eastern tropical Pacific yellowfin tuna fishery, 1934-67. A. Frequency distributions. B. Residuals against time.
C. Residuals against deterministic catch, (?;. D. Residuals against fishing effort, /,.

578

FOX: RANDOM VARIABILITY AND PARAMETER ESTIMATION

The referee of this paper has raised an im-
portant point regarding- application of the var-
ious statistical models to actual fishery data.
In a non-overexploited fishery, generally, the
quality and level of catch and effort values in-
crease with time. Eelatively speaking, Model 0
in this case places greater weight on more recent
data than do Models 1, 2, or 3, and in the ab-
sence of any other criteria it might represent
the intuitive choice. However, if the quality
of the data were a more significant contributor
to unequal residence variance than the statistical
model, one would expect, in this case, a decrease
in the residuals plotted for Model 0 against time,
catch, and fishing effort in contrast to the appar-
ent increase for the yellowfin tuna fishery (Fig-
ure 3) . If one has reason to suspect a significant
difference in quality of the data, as would be
suggested by a decrease in the residual plots
of Model 0, perhaps a solution is to partition
the data at the point in time where a significant
quality increase occurs. Then fit each set of
data individually placing greater weight on the
parameter estimates for the more recent set.
The specter of the suitability of employing pro-
duction models over long time periods is also
raised by this point. But it is outside the scope
of this paper and the reader is referred to the
papers cited previously.

SUMMARY

In using a least-squares procedure for esti-
mating parameters of a mathematical model,
such as the Pella-Tomlinson technique, there are
three assumptions about the residuals for ob-
taining the best least-squares estimates: 1) the
residuals are independent, 2) the residuals have
an expected value of zero, and 3) the variance
of the residuals is constant (Anscombe and
Tukey, 1963; Draper and Smith, 1966; Snedecor
and Cochran, 1967). We have observed from
the simulation study that two (of four alterna-
tive) simple statistical models which are bio-
logically sound — Model 2 (using a logarithmic
transformation) and Model 3 (weighting by the
inverse of the squared deterministic catch) —
fulfill the statistical assumptions for obtaining

good least-squares estimates of the generalized
production model parameters over a wide range
of fishing effort.

On applying these four statistical models in
estimating the parameters of the generalized
production model for the eastern tropical Pacific
yellowfin tuna fishery, residuals e.xamination re-
vealed that the same two statistical models.
Models 2 and 3, fulfilled the least-squares esti-
mation assumptions. Models 0 (assumed by
Pella and Tomlinson, 1969) and 1 did not. Model
3 was selected as the best model since it involves
the direct minimization of the actual residual
variance, and is therefore considered to be theor-
etically superior to Model 2.

Finally, anyone using the generalized pro-
duction model and the Pella-Tomlinson estimat-
ing technique should be aware of, in addition
to the proper statistical model, the effect of the
value of A'^ in equation (5) on the parameter
estimates.

ACKNOWLEDGMENTS

I wish to express my appreciation to Dr.
Douglas G. Chapman, Director of the Center for
Quantitative Science in Forestry, Fisheries and
Wildlife, University of Washington, for the con-
siderable consultation he gave during the course
of this study and for his review of the final
manuscript. Many others, especially the referee,
who offered suggestions on clarification and im-
provement of the value of this study, are also
extended my gratitude.

LITERATURE CITED

Anscombe, F. J.

1961. Examination of residuals. Proceedings of
the Fourth Berkeley Symposium on Mathematical
Statistics and Probability. 1 : 1-36.
Anscombe, F. J., and J. W. Tukey.

1963. The examination and analysis of residuals.
Technometrics 5: 141-160.
Beverton, R. J. H., AND S. J. Holt.

1957. On the dynamics of exploited fish populations.
Fish. Invest. Min. Agr. Fish. Food (G.B.), Ser. II,
19, 533 p.

579

FISHERY BULLETIN: VOL. 69, NO. 3

Chapman, D. G.

1961. Statistical problems in dynamics of exploited
fisheries populations. Proceedings of the Fourth
Berkeley Symposium on Mathematical Statistics
and Probability. 4: 153-168.

1967. Statistical problems in the optimum utiliza-
tion of fisheries resources. Int. Stat. Inst, Bull.
42(1) : 268-290.
Chapman, D. G., R. J. Myhre, and G. M. Southward.

1962. Utilization of Pacific halibut stocks : estima-
tion of maximum sustainable yield, 1960. Rep. Int.
Pac. Halibut Comm. 31, 35 p.

Draper, N. R., and H. Smith.

1966. Applied regression analysis. Wiley, New
York, 407 p.
Fox, W. W., Jr.

1970. An exponential surplus-yield model for op-
timizing exploited fish populations. Trans. Am.
Fish. Soc. 99: 80-88.
Glass, N. R.

1969. Discussion of calculation of power function
with special reference to respiratory metabolism
in fish. J. Fish. Res. Board Can. 26: 2643-2650.
Graham, M.

1935. Modern theory of exploiting a fishery, and
application to North Sea trawling. J. Cons. 10:
264-274.
Gulland, J. A.

1969. Manual of methods for fish stock assessment.
Part 1. Fish population analysis. FAO (Food
Agr. Organ. U.N.) Man. Fish. Sci. 4, 154 p.
Hafley, W. L.

1969. Calculation and miscalculation of the allo-
metric equation reconsidered. BioScience 19:
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PELLA, J. J., AND P. K. TOMLINSON.

1969. A generalized stock production model. Inter-
Am. Trop. Tuna Comm., Bull. 13: 419-496.

PlENAAE, L. v., AND J. A. THOMSON.

1969. Allometric weight-length regression model.
J. Fish. Res. Board Can. 26: 123-131.
Richards, F. J.

1959. A flexible growth function for empirical use.
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Richer, W. E.

1958. Handbook of computations for biological sta-
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SCHAEFER, M. B.

1954. Some aspects of the dynamics of populations
important to the management of the commercial
marine fisheries. Inter-Am. Trop. Tuna Comm.,
Bull. 1: 25-56.
1957. A study of the dynamics of the fishery for
yellowfin tuna in the Eastern Tropical Pacific
Ocean. Inter-Am. Trop. Tuna Comm., Bull. 2:
245-285.
ScHAEFER, M. B., and R. J. H. Beverton.

1963. Fishery dynamics — their analysis and inter-
pretation. In M. N. Hill (editor) , The sea. Vol. 2,
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Taylor, C. C.

1962. Growth equations with metabolic parameters.
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1968. Calculation and miscaculation of the allomet-
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580

ADDITIONAL DATA ON THE SPAWNING OF THE HAKE

John S. MacGregor'

ABSTRACT

In January 1970 samples of hake were taken off southern and central Baja California to study fecundity.
In the southern area female hake as small as 130 mm standard length contained developing eggs, and
all females longer than 140 mm contained such eggs. There is a marked cline in size at first maturity
of hake along the Pacific Coast (hake in the Pacific Northwest exceed 400 mm before reaching maturity).
Seventeen female hake 130 to 202 mm long taken in the southern area contained from 3,400 to 19,500
eggs or 229 per gram of fish; 11 females 222 to 305 mm from the central area contained from 3,500
to 110,000 eggs or 243 per gram of fish. In previously published data 22 female hake 346 to 688 mm
from northern Baja California contained from 33,000 to 496,000 eggs or 192 eggs per gram of fish.
There are no significant differences in fecundity among the three areas. The hake spawns once a year
with over 98% of the spawning taking place between January and April.

In 1966, I published data on the fecundity of 22
female hake taken off northern Baja Cahfornia.
In 1970, additional samples of hake were ob-
tained from central and southern Baja California
to determine if there were geographic differ-
ences in hake fecundity in the offshore waters of
Baja California.

The hake samples taken off southern and
central Baja California in January contained
prespawning females from which estimates of
fecundity were obtained.

The hake from northern Baja California for
which fecundity data have been published (Mac-
Gregor, 1966) appear to be identical to those
taken off southern and northern California,
while those taken farther to the south are dif-
ferent with respect to growth rate and size at
first maturity and, in fact, have been described
as a different species (Ginsberg, 1954).

The female hake for which fecundity deter-
minations were made were taken by trawl from
the research vessel David Star?- Jordan. Station
J-45-13 at lat 26°07' N, long 113°07' W was
sampled January 11, 1970. Station J-45-27 at
lat 28°44' N, long 115°15' W was sampled Jan-
uary 16, 1970. Methods for estimating fecundity
of the samples were essentially the same as used
previously (MacGregor, 1966).

' National Marine Fisheries Service, Fishery-Ocean-
ography Center, La Jolla, Calif. 92037.

Previous data on hake fecundity (MacGregor,
1966) were obtained from samples taken by the
research vessel John N. Cobb (Berry and Per-
kins, 1966). Station C-58-23 at lat 31°49' N,
long 117°53' W was sampled March 21, 1963.
Station C-58-29 at lat 29°46' N, long 116°01' W
was sampled March 23, 1963. Station C-58-31
at lat 29°35' N, long 116^00' W was sampled
March 25, 1963.

FECUNDITY

The range for fecundity data for samples
J-45-13 (Table 1) and J-45-27 (Table 2) com-
pare with Cobb 1963 samples (MacGregor, 1966)
as follows:

J-45-13
Standard length (mm) 130 to 202
Weight (g) 22.1 to 57.0

Gonad weight (g) 0.928 to 4.002
Advanced eggs 3.419 to 19.564

Eggs per gram of fish 141 to 343

1-4 S -27
222 to 303
88.0 to 221.0
3.279 to 22.710

Cobb 1963
346 to 688
300 to 2,750
13.1 to 196.8

3.496 to 110,017 33,000 to 496,000
38 to 498

Manuscript accepted February 1971.

FISHERY BULLETIN: VOL. 69, NO. 3, 1971.

83 to 556

There is no overlap in the ranges of standard
length and fish weight of the samples from the
three localities. The number of advanced eggs
in the ovaries tends to increase with size of fish
both within and between samples. However, be-
cause of the great variation in the numbers of
advanced eggs among the individual fish, there is
considerable overlap in gonad weight and num-
bers of advanced eggs between successive
samples.

581

FISHERY BULLETIN: VOL. 69. NO. 3

Table 1. — Fecundity data for 17 female hake taken at Station J-45-13 (lat 26°07' N,
long 113°07' W) January 11, 1970.

Standard
lengfh

Weight

Gonad

weight

Gonad
index

Advanced eggs

Size rang©

Eggs per
gram of fish

mm

:

S

mm

130

22.1

0 928

4.2

0.50-0.67

3,419

155

131

23.3

1.345

5.8

.57-

.73

7,049

303

13S

25.2

1.320

5.2

.57-

.77

3,564

141

137

22.4

1.518

6.8

.50-

.67

6,469

289

137

29.3

1.795

6.1

.53-

.70

7,139

244

138

24.8

0.987

4.0

.53-

.70

4,048

163

140

28.8

1.350

4.7

.53-

.70

4,956

172

140

34.5

2.241

6.6

.57-

.77

7,926

230

141

30.5

1.222

4.0

.50-

.70

4,534

149

150

21.2

1.198

5.7

.53-

.73

4,257

201

ISO

37.1

2.481

6.7

.53-

.73

10,864

293

160

31.5

1.875

6.0

.53-

.73

6,447

205

162

30.3

1.957

6.5

.57-

.73

7,633

252

170

32.3

2.000

6.2

.50-

.70

8,741

271

172

37.7

1.863

4.9

.47.

.70

10,731

285

174

37.7

2.000

5.3

.50-

.70

7,559

201

202

57.0

4.002

7.0

.50-

.67

19,564

343

Table 2.— Fecundity data for 11 female hake taken at Station J-45-27 (lat 28°44' N,
long 115°15' W) January 16, 1970.

Standard
length

Weight

Gonad
weight

Gonad
index

Advanced eggs

Size range

Number

Eggs per
gram of fish

mm

t

S

mm

222

100

8.663

9.7

0.50-0.67

29,399

294

230

88

7.011

8.0

.50- .73

23,253

264

233

104

8.488

8.2

.60- .77

29,450

347

238

91

3.279

3.6

.57- .73

3,496

38

245

105

6.292

6.0

.50- .70

17,511

168

247

120

5.956

5.0

.60- .80

18,264

152

252

no

9.341

8.5

.53- .77

43,014

391

263

147

5.308

3.6

.60- .80

13,747

94

275

146

1 1 .860

8.2

.57- .83

38,959

286

287

176

12.972

7.4

.67- .83

24,877

141

305

221

22.710

10.3

.57- .80

110,017

493

The mean number of advanced eggs per gram
of fish is 229 for sample J-45-13, 243 for sample
J-45-27, and 192 for the Cohh 1963 samples.
Owing to the great range of individual values
in each of the samples, there is no significance
in the differences between the means. The mean
for the 50 fish in the three samples is 216 eggs
per gram of fish. The standard error of the
mean is 15 eggs or about l'''r . In spite of some
rather low fecundities, the distribution of eggs
per gram of fish approximates a normal distri-
bution indicating that these low counts are with-
in the limits of expected variation.

Eggs /gram

Pfrcent JTtq

< so

2

100

24

200

38

300

30

400

2

500

2

>SSO

2

The low counts apparently did not result from
partial spawning of the advanced mode because
they were found in fish that were not yet ripe.

RATIOS

To obtain estimates of the numbers of ad-
vanced eggs in the hake ovary, first about 100
yolked eggs in the sample were measured in
order to delimit the distributions of advanced-
and small-yolked eggs. Then the additional ad-
vanced-yolked eggs in the weighed sample were
counted. An estimate of the numbers of small
eggs was obtained from the ratio of large to
small eggs in the measured frequency distribu-
tion, but' because this estimate is based on rel-
atively few eggs it is less accurate than the esti-
mates of advanced eggs. Estimates of the num-
bers of small eggs per gram of fish ranged from

582

MacGREGOR: ADDITIONAL DATA ON SPAWNING OF HAKE

33 to 766 and averaged 248. This compares with
38 to 556 with an average of 216 for the ad-
vanced eggs for all samples.

The correlation obtained by MacGregor
(1966) between percentage of eggs in the ad-
vanced mode and advanced eggs per gram of
fish has no mathematical significance because
both variables are related. Actually there is
no relation between the number of advanced eggs
and the number of small eggs. Ovaries con-
taining either high or low numbers of advanced
eggs per gram of fish may contain either high
or low numbers of small-yolked eggs. How-
ever, the conclusion that the great variation in
the ratios of large to small eggs makes multiple
spawning unlikely seems to be valid.

Of 366,093 hake larvae taken on monthly
cruises in the 6 years 1951 through 1956, 87%
were taken in January, February, and March,
11.5% in April, and the remaining 1.5% in the
remaining 8 months. Several large samples of
hake taken off California in April 1970 showed
that the advanced eggs were no longer present
in the ovaries of the females while the smaller
yolked eggs were. Because there is no evidence
of further egg development in the ovaries and
no evidence of heavy spawning subsequent to
April in the plankton, we must assume that these
small-yolked eggs are resorbed following spawn-
ing of the advanced mode.

SIZE AT FIRST MATURITY

One hundred thirty-six hake from sample
J-45-13 (southern Baja California) were ex-
amined for stage of sexual maturity. Eighty
hake from sample J-45-27 (central Baja Cali-
fornia) and an additional seven hake taken in
1961 near Cedros Island (central Baja Cali-
fornia) were also examined (Table 3).

In sample J-45-13 the largest immature male
was 127 mm in length, and the largest immature
female 138 mm. The smallest maturing male
was 119 mm. and the smallest maturing female
125 mm. All males 129 mm and longer and all
females 140 mm and longer were maturing.

In sample J-45-27 the range of fish length was
not as good for determining size at first maturity.
The smallest maturing male was 137 mm long,
and it appeared that all males 159 mm and long-
er were matui-e. The smallest mature female
was 222 mm in length, and all females of this
length and longer were maturing. However,
on the basis of the 1961 sample it appears that
all females were maturing at some length be-
tween 202 and 222 mm.

It is difficult to determine the size at first ma-
turity for hake off northern Baja California and
California because very few fish of suitable size,
taken during the spawning season, were avail-
able. For off-season hake the gonad index may

Table 3.— Size at first maturity. Southern Baja California, sample J-45-13, lat 27°07' N, long 113°07' W, January
11, 1970. Central Baja California (Cedros Island area), sample J-45-27, lat 28°44' N, long 115°15' W, January 16,
1970, and sample B-6111-3, Cedros Island, November 25, 1961. Males judged mature or immature by size and appear-
ance of testes. Females judged immature if largest eggs in ovary were 0.20 mm or less in diameter (not yolked) ;
probably maturing if ma.ximum egg diameter was 0.23 to 0.47 mm; mature if maximum egg diameter was 0.50 mm
or larger. Immature, not sexed: gonads not developed enough so that se.\ can be determined by gross examination.

Males

Females

Not sexed

Sample

Standard
length

Immaturo

Mature

Standord
length

Maximum egg diameter (mm)

Standard
length

Immature

0-0.10 0.30-0.47 0.50-0.77

J-45-13

119-127

6

6

122-124
125-128

6

8

0

I

0
0

129-166

0

50

130-138

9

4

6

140-202

0

0

21

137-140
159-307

Maximum egg diameter (mm)

0-0.20

0.37

0.67-0.83

172-197

3

0

0

222-228

0

1

1

230-305

0

0

10

42

583

FISHERY BULLETIN: VOL. 69, NO. 3

indicate maturity. Generally, hake with gonad
indices of less than 0.5 (i.e., the gonad weight
is less than 0.5^/r of the fish weight) do not con-
tain yolked eggs in their ovaries. There is no
yolk in eggs up to 0.20 mm diameter, and fish
containing such eggs a few months before or
after the spawning season may be considered
immature. Eggs in an ovary having a gonad
index of 0.8 have a maximum diameter of about
0.34 mm and at a gonad index of 1.5, about 0.43
mm maximum diameter. The eggs generally are
not large enough to count (over 0.65 mm diam-
eter for the largest eggs in the ovary) until
the gonad index is about 3.5, and then only for
fish having a fecundity of less than 100 eggs
per gram of fish. If we apply the same criterion
(a gonad index of less than 0.5 as indicating an
immature fish) to the males, we can roughly
estimate the size at maturity for off-season hake.

Applying this criterion of maturity to a num-
ber of miscellaneous hake samples taken in the
off-season for spawning off northern Baja Cal-
ifornia and southern California, it appears that
all males 285 mm and longer and all females
340 mm and longer were mature.

Best (1963) estimated that all hake, both
males and females, taken off northern California
were mature at 400 mm total length (about 360
mm standard length) . The length at which all
fish are mature could be somewhat less as he
had a limited number of smaller fish in his
samples.

Nelson and Larkins (1970) found that all fish
of 450 mm total length (about 405 mm standard
length) were mature in the Pacific Northwest.
Apparently they also had few smaller fish to
work with, and the length at which all fish are
mature could be somewhat less.

DISCUSSION

The mean number of eggs per gram of fish
was not significantly different among the three
samples, ,1-45-13, J-4.5-27, and Cobb 1963. These
three samples were taken in widely separated lo-
calities, and although they were similar with
respect to relative fecundity, questions have been
raised as to the distinctness of the north Pacific
hake with respect to race or even species.

Ginsberg (1954) assigned the north Pacific
hake to two species based on morphometric and
meristic characters. His descriptions were
based on 12 specimens of Merlucchis productus
taken off Washington, Oregon, and California,
as far south as San Diego, and eight specimens
of M. angustimamis taken in the Gulf of Panama,
the Gulf of California, off the Pacific Coast of
Baja California, and off Del Mar, Calif.

Ahlstrom and Counts (1955) could find no evi-
dence of more than one species of hake in their
extensive collections of eggs and larvae taken
Ijetween San Francisco and the southern tip of
Baja California. All of the small fish that had
fully developed dorsal and anal fins had fin ray
counts that fell within the range of M. productus
but outside of the range of M. angustimanus as
given by Ginsberg.

F. H. Berry (unpublished data) studied nu-
merous additional specimens of hake from Baja
California and California. He concluded that
M. jyvoductus and M. angusthnanus were the
same species and the differences in meristic and
morphometric characters, used by Ginsberg to
separate the species represented a latitudinal
cline.

There was certainly a marked cline in size at
maturity for the hake used in this study, espe-
cially when these data are compared with data
given by other authors. The size at which all
fish were mature was as follows:

Southern Baja Californi,!

Ccmral Baja Californi;

Sex Standard

Imgth

males 129 mm

females 140 mm

males 1S9 mm

females 202-233 mm

NortKeni Baja California and southern California males 385 mm

females 340 mm

Norlhcrn California (Best. 1%3)

Pacific Northwest (Nelson and Larkins. 1970)

both
both

360 mm
40? mm

The difl^'erences between areas are so great that
the roughness of some of the estimates does not
affect the conclusion that these differences are
very real.

The distribution and growth jiatterns of the
European hake, M. merlucciiis, is similar to that
of M. prndKcfus in many ways. The Euroiiean
hake ranges from Norway to at least Mauritania
ill Africa (Hart, 1948) while .1/. productiis

584

MacGRF-GOR: ADDITIONAL DATA ON SPAWNING OF HAKE

ranges from Alaska to at least the southern tip
of Baja California. Both species grow to much
larger sizes in the northern parts of their ranges,
but are much smaller in their southern ranges.
M. merluccius in the Mediterranean Sea is small-
er than the north Atlantic form, and both the
southern Baja California and African coasts
apparently produce dwarf races of their respec-
tive hake species.

Most recent information from the Guinean
Trawling Survey (Williams, 1968) shows that
there are continuous populations of hake from
Norway to South Africa. However, the hake
taken off the west coast of Africa are ascribed
to several species other than M. merluccius. The
West African hake, M. poUi and unidentified M.
spp. were taken throughout the survey area from
the Gambia border to the Congo. The Senegal
hake M. senegalensis was taken in the northern
areas between the Gambia border and southern
Liberia with one questionable record from Ni-
geria, and the South African hake M. cape7isis
was taken in the southern areas between Came-
roun and the Congo. A sample of 50 M. sene-
galensis averaged 26.3 cm total length (range
18 to 27) , and a sample of M. poll! averaged 41.7
cm total length (range 35 to 49).

SUMMARY

The north Pacific hake, Merluccius producfus,
ranges from Alaska to at least southern Baja
California.

The fecundity of individual hake varied
greatly ofi" Baja California and southern Cal-
ifornia, but there was no significant difference
in average fecundity among the samples taken
from widely separated sampling stations in this
area. Estimates of the number of advanced

eggs contained in 50 prespawning hake averaged
216 eggs per gram of fish.

Average size at first maturity for female hake
varied from 133 mm standard length off southern
Baja California to about 340 mm off northern
Baja California and southern California. Males
appeared to mature at smaller sizes 128 mm in
the south to 285 mm in the north.

LITERATURE CITED

Ahlstrom, E. H., AND R. C. Counts.

1955. Eggs and larvae of the Pacific iial^e, Mer-
luccius productus. U.S. Fish Wildl. Serv., Fish.
Bull. 56: 295-.329.
Berry, F. H., and H. C. Perkins.

1966. Survey of pelagic fishes of the California
Current area. U.S. Fish Wildl. Serv., Fish. Bull.
65: 625-682.
Best, E. A.

1963. Contribution to the biology of the Pacific
hake, Merluccius productus (Ayres). Calif. Coop.
Oceanic Fish. Invest., Rep. 9: 51-56.
Ginsberg, I.

1954. Whitings on the coasts of the American conti-
nents. U.S. Fish Wildl. Serv., Fish. Bull. 56:
187-208.
Hart, T. J.

1948. The distribution and biology of hake. Biol.
Rev. (Cambridge) 23: 62-80.
MacGregor, J. S.

1966. Fecundity of the Pacific hake, Merluccius
productus (Ayres). Calif. Fish Game 52: 111-116.
Nelson, M. 0., and H. A. Larkins.

1970. Distribution and biology of Pacific hake:
A sjTiopsis. In Pacific hake, p. 23-33. U.S.
Fish" Wildl. Serv., Circ. 332.
Williams, F.

1968. Report on the Guinean Trawling Survey.
Volume I. General report. Organisation of
African Unity, Scientific, Technical and Research
Commission, Lagos, Nigeria. OAU/STRC Publ.
99, 828 p.

585

THE LOW-TEMPERATURE THRESHOLD FOR PINK SALMON EGGS
IN RELATION TO A PROPOSED HYDROELECTRIC INSTALLATION

Jack E. Bailey' and Dale R. Evans'

ABSTRACT

A proposed hydroelectric installation in southeastern Alaska would alter the seasonal pattern of stream
temperatures and pose a threat to the natural production of pink salmon, Oiicorhynchus gorbuscha.
Analysis of experiments reported in the literature indicated that such an installation might lower stream
temperatures below the threshold normal for the embryonic development of pink salmon. Our experi-
ments with pink salmon eggs incubated in refrigerated water showed that the epgs required initial
temperatures above 4.5° C for normal embryonic development. An increase in mortalities and in alevins
with spinal deformities occurred when initial incubation temperatures were 4.5° C and lower; ini-
tial incubation at 2° C resulted in complete mortality. The proposed hydroelectric installation could
result in temperatures as low as 4.5° C during spawning and initial incubation and could therefore be
expected to cause an increase in mortality and the occurrence of deformed alevins. The low temperature
would be followed by higher than normal winter incubation temperatures, which would have an unknown
effect on the time of emergence of fry. A tunnel intake designed to draw water of a desirable temper-
ature on demand would be required to protect salmon.

In 1964 the Bureau of Reclamation (now the
Alaska Power Administration) started feasibil-
ity studies on a hydroelectric installation on Lake
Grace, 51 km northeast of Ketchikan, Alaska.
Grace Creek, the lake's outlet stream, enters the
sea 4 km from Lake Grace. An impassable falls
2 km above tide water prevents migrating fish
from reaching Lake Grace. Below the falls, the
creek provides important spawning, incubation,
and rearing areas for salmonids, especially pink
salmon, Oncorhynchus gorbuscha.

The proposed dam would divert practically
all of the water from Grace Creek through a
hydroelectric plant and back into Grace Creek
about 1.2 km from tide water. Because of the
design of the dam and of the water intake, the
temperature of the lower 1.2 km of the creek
could be changed to lower than normal in sum-
mer and fall and higher than normal in winter.

Analysis of the studies by Combs and Bur-
rows (1957) and Combs (1965) on the relation
between temperature and the development of
salmonid embryos indicated that when the hy-

' National Marine Fisheries Service, Biological Lab-
oratory, Auke Bay, Alaska 99821.

° National Marine Fisheries Service, Office of Water
Resource Studies, Juneau, Alaska 99801.

droelectric facility is constructed, water tem-
peratures in the principal spawning areas of
Grace Creek might be too low for normal em-
bryonic development. We therefore estimated
the temperatures likely to occur in Grace Creek.
Because these temperatures seemed critically
low, we conducted laboratory experiments to de-
termine i^recisely the low-temperature thresh-
old or minimum temperature for the normal
development of embryos of pink salmon, the
major species in Grace Creek.

In this report we analyze the effects of the
proposed installation on the temperature regime
of Lake Grace and Grace Creek and describe
the threshold temperatures for development of
])ink salmon embryos, and then relate the two
studies and discuss their implications.

EFFECTS OF PROPOSED INSTALLATION

ON TEMPERATURE REGIME
OF LAKE GRACE AND GRACE CREEK

To consider the effects of the installation on
the temperature regime, we compared the sea-
sonal temperature pattern of Grace Creek under
normal conditions with the temperatures likely

Manuscript accepted February 1971.
FISHERY BULLETIN: VOL. 69, NO.

587

FISHERY BULLETIN: VOL- 69, NO. 3

to occur when the proposed power plant is in
operation.

The daily maximum and minimum temper-
atures for Grace Creek (U.S. Geological Survey,
1966: 15; 1967: 17; 1968: 16) for the first and
second half of each month between April 16,
1965, and March 31, 1967, were averaged to de-
termine the annual temperature pattern under
normal conditions (Figure 1 ) . The highest tem-
perature for this period was 17.8° C and the low-
est was 0.6° C. Normally, Grace Creek temper-
atures reach a maximum of about 15° C at the
start of the spawning season in mid-August,
and decline to 10° C at the end of the spawning
season the first week of October. After the
spawning season, stream temperatures continue
to fall, reaching about 6° C by late November
and about 1.5° C in midwinter, when ice cover
forms on Lake Grace during most years. The
average stream temperature is about 1.5° C from
the end of December until the end of March.

If the proposed power development on Lake
Grace is completed, it would significantly change
the physical dimensions and waterflow of the
lake. The dam at the outlet of Lake Grace would
raise the lake surface from the present eleva-
tion of 131.1 m (mean sea level) to a maximum
elevation of 152.4 m and increase its surface
area from 668 to 1,046 ha. Water would be di-
verted through a pressure tunnel and exposed
penstock to a powerhouse on Grace Creek, 1.21

a 7

BEFORE INSTALLATION

AFTER INSTALLATION, LOW RAINFALL

AFTER INSTALLATION. HIGH RAINFALL

I I I I I I I I I 1 I I I I I I I I I M I I I I I I I I I I 11 I I I I I I I I I I I I I I I I I M I I

JLT ' AUG ' SEPT ' OCT ' NOW ' OEC ' JAN ' FEB ' MAR ' APR ' MAY JUNE

Figure 1. — Average annual temperature pattern of
Grace Creek, based on temperature records from April
16, 1965, through March "1, 1!)67, and temperature pat-
terns that might prevail during year.s of extreme high
and low rainfall if water is drawn from a reservoir at
the 125.0-m elevation.

km downstream from the dam. The intake ele-
vation of the diversion tunnel would be constant
at 125.0 m, but the elevation of the reservoir
surface would change from 131.4 to 152.4 m
as the active reservoir capacity of 1.84 x 10' m'
is used. The maximum depth of the natural lake
is 129.5 m.

Most of the water in the stream below the
powerhouse would come through the powerhouse
and would therefore be similar in temperature
to the water at the tunnel intake level of the
lake. To predict the temperature of this water,
we obtained temperature-depth jirofiles from
Lake Grace during the freshwater phase of the
reproductive cycle of pink salmon. Profiles were
taken on July 27, 1961, August 12, 1965, Sep-
tember 16, 1965, October 8, 1965, November 18,
1965, and March 25, 1965 (Figure 2). In addi-
tion to the temperature-depth profiles, we ob-
tained thermograph records which indicated
surface water temperatures attained 4° C No-
vember 28, 1965, and again May 28, 1966. These
thermograph records provide our best estimate
of the dates of autumn and spring overturn of
Lake Grace. Although these data were not all
taken during a single reproductive cycle of pink
salmon, we feel they are representative. These
pi-edicted estimated temjieratures of the lake
waters that would enter the intake are probably
higher than would actually occur because in-
creasing the depth of the lake increases its
thermal capacity and results in colder deep water
(Hutchinson, 1957). No correction was made
for the cooling eflFect of deeper water.

The actual surface elevation of the reservoir
and therefore the depth of the tunnel intake
would depend on operational requirements of
the power plant and the flow of water into Lake
Grace. The fixed tunnel intake at the 125.0-m
elevation could be under 6.4 to 27.4 m of water
because the proposed active reservoir elevation
varies from 131.4 to 152.4 m. We allowed for
these fluctuations in using the temperature-depth
profiles as an indication of water tempei-atures
at tunnel intake depth.

The project development plan for Lake Grace
included a graphic model of simulated reservoir
water surface elevations for each month from

588

B.\ILEV and EVANS: LOW-TEMPERATURE THRESHOLD

5 10 15 20

5 10 15 5 10 15 5

TEMPERATURE ( *" C t

Figure 2. — Temperature-depth profiles from Lake Grace
during months of the freshwater reproductive cycle of
pink salmon.

January 1928 through December 1964.' The
basis of the model included records of streamflow
and climate from Grace Creek and several near-
by streams and also a computer study of the
monthly operation of the power plant. We have
chosen the year of lowest water level (1948) and
the year of highest water level (1934) from the
surface elevation model to illustrate the range
of temperature patterns that might be caused
by fluctuating water levels (Figure 1). The
simulated water levels and depth of water above
the entrance to the intake tunnel at 125.0 m used
to predict water temperatures are shown in
Table 1.

In Grace Creek, the probable result of the
power plant would be lower than normal tem-
peratures during summer and fall when salmon
eggs are beginning their development and higher
than normal temperatures during the winter
when eggs and alevins are completing their de-
velopment. Temperatures of Grace Creek dur-
ing the normal spawning season currently range
from 15° to 10° C, but under the conditions of
power plant operation, temperatures would be
from 7° to 5° C. During the first month after
spawning, temperatures normally range from

10° to 6° C, but under the altered conditions
they may be reduced to only 6° to 4.5° C. The
predicted temperatures for the winter incuba-
tion period, 3° to 4° C, would be consistently
higher than the 1° to 3° C in the unaltered
stream.

LOW-TEMPERATURE THRESHOLD

FOR NORMAL DEVELOPMENT

OF EMBRYOS

Several workers have studied the low-temper-
ature threshold for normal development of em-
bryos of fishes. In this section we review their
findings and describe our laboratory experiments
with pink salmon.

EXPERIMENTS BY OTHER WORKERS

An important aspect of the effects of low tem-
peratures is the stage of development at the time

Table 1. — Estimated water temperatures that would
have prevailed at the 125. 0-m elevation (mean sea level)
of the proposed tunnel intake of Lake Grace if the pro-
posed power plant had been in operation during the year
of lowest water level (1948) and the year of highest
water level (1934) from 1928 to 1964.

Water surface

elevation

(m)

Depth of water

above

tunnel intake

(m)

Water temperature

at tunnel intake

(° C)

Month

194a

1934

1948 1934

1948 1934

July

135.6 152.4

10.4 27.4

5.6 3.9

August

134.1 152.4

9.1 27.4

7.2 5.0

September

137.2 150.9

12.2 25.9

7.2 5.6

October

141.7 152.4

16.8 27.4

6.1 5.0

November

143.2 152.4

18.3 27.4

5.6 4.4

March

135.6 149.4

10.7 24.4

2.8 3.3

' Alaska Povifer Administration. 19G8. Lake Grace
Project, Alaska. On file, Alaska Power Administration,
Federal Building, Juneau, Alaska 99801.

the critical temperature is imposed on the em-
bryo. Combs and Burrows (1957) associated
high mortalities and gross anomalies in embryos
of Chinook salmon with low temperatures during
the pregastrula stages; they used a significant
rise in mortality in defining the low-temperature
threshold. Combs (1965), Efimov (1962), and
Price (1940) found that salmonid eggs were
most sensitive to low temperature in the blastula
and early gastrula stages. These authors dem-
onstrated that once gastrulation is well under-
way, the embryos can tolerate temperatures close
to freezing.

589

FISHERY BULLETIN: VOL, 69. NO. 3

Adverse effects of low temperatures during-
certain stages of development were also ob-
served for other fishes. KinneandKinne (1962)
exposed embryos of the cyprinodont Cyprinodon
maculavis to different temperature-salinity-oxy-
gen combinations and found a period of "low
thermal stability," which we presume to mean
low resistance, in embryos exposed to critically
low tem])eratures during early development
(fertilization to gastrulation) . Stockard ( 1921 )
conducted a number of experiments with eggs
of the cyprinodont Fundulus heteroclitus which
he placed in a refrigerator at 5°, 7°, and 9° C
for various lengths of time and at various stages
of development. Development was almost, if
not completely, stopped at 5° C and greatly
slowed at 9° C. Exposure to 5° C just after gas-
trulation commenced was not noticeably injur-
ious, but exposure to low temperatures during
earlier stages resulted in increased mortalities
and gross anomalies among survivors.

Piavis (1961) incubated sea lamprey eggs at
various constant temperatures and learned that
viable burrowing larvae could be produced at
15.6° C but not at 12.8° C. McCauley (1963)
also explored the lethal temperature limits of
embryonic sea lamprey. He found that the nar-
row range of constant temperature, 15.0° to
25.0° C, necessary for successful hatching may
be extended to 12.2° to 25.6° C if gastrulation
is completed before the eggs encounter temper-
atui'e extremes.

The work of Taning (1952) on the effects of
temperature on the development of Sahno trntta
trutta supports Stockard's conclusion that the
earlier the stage of development is arrested, the
moi'e severe will be the effect.

The lowering of temperatures in Grace Creek
by the proposed hydroelectric plant would be
greatest just before and during gastrulation of
the pink salmon embryos (Figure 1).

EXPERIMENTS IN LABORATORY ON
PINK SALMON

We conducted an experiment in the laboratory
to determine if iiink salmon eggs could survive
and develop normally under the projected ther-
mal regime for Grace Creek. The eggs for the

study came from two pink salmon collected Sep-
tember 7, 1966, from Grace Creek. The eggs
were thoroughly mixed and fertilized by sperm
from two males in the field.

Embryonic development had begun before
the eggs were placed in the experimental array
because the temperature in the transporting
container ranged from 7° to 12° C (average,
10.8° C) during the 10-hr trip to the laboratory.
According to Soin (1954) the first cleavage di-
vision occurs in pink salmon eggs about 7 hr
after fertilization at 11° C. Knight (1963)
showed that about 2.5 hr elapse between suc-
cessive cleavage divisions in rainbow trout eggs
at 12.2° C. Therefore, we estimate, but did not
confirm, that the Grace Creek pink salmon eggs
completed two cleavage divisions before they
were transferred to the controlled temperatures
of the experiment.

The eggs were incubated in 55- and 42.5-mm
diameter Buchner funnels with perforated
plates. Each of the large funnels was stocked
with 120 eggs and each of the small ones with
25 eggs. The water M'as introduced through the
stem of the funnel to produce an upwelling flow
through the plates that supported the eggs. The
water was not recirculated, and flow rates' were
set to deliver an apparent velocity of about 200
cm hr to the eggs. Dissolved oxygen content
of the water as it entered the funnels was above
8 ppm at all times.

The experiment involved 16 treatments con-
sisting of four initial incubation temperatures
each with four exposure periods. The four tem-
peratures were ambient," 4.5°, 3.0°, and 2.0° C;
and the four exposure periods were 15, 27, 37,
and 103 days. All of the exposure periods be-
gan 10 hr after fertilization on September 7,
1966. When the experimental cold treatment
for each lot was completed, the eggs were trans-
ferred to ambient temperature to complete their
incubation. Temperatures were recorded con-
tinuously; the daily means (Figure 3) were
usually within ±0.5° C of the planned levels. In-

' Apparent velocity was obtained by dividing the rate
of flow to the egg container in cubic centimeters per hour
by the cross-sectional area of the container in square
centimeters.

° Ambient temperature is the unmodified temperature
of the laboratory water supply. See Figure 3.

590

BAILEY md EVANS: LOW-TEMPERATURE THRESHOLD

9,0

l/l

AMBIENT

8.0

1

7.0

uP^VA

\

6.0

-

\

5.0

\

4.0

^n^^

.^

.

0.0

I

4.5°

C5.0

; J^ A

0

A r /

-\.A /V^.

^4.0

-M v^ '-y vu

-^

3
*-

a. 3.0

: \vVvA^

UJ

Q.

s

[^ 0.0

3.0°

4,0

I L L 1 A,

—

3.0

W1]WVVA%.1

2.0

w] |f| V w v\/\

1.0

^ 1

1

0.0

, . /sL ,1 .^A A. H , ^■°°

2.0

UAlA^tv^^W^Aj^^^

1 0_

1

■ 0 15 27 37 103

EXPOSURE PERIOD (DAYS)

Figure 3. — Four initial incubation temperatures to which
pink salmon eggs were subjected for four exposure per-
iods in laboratory experiments on effects of low tem-
perature on growth and development. Dashed lines in-
dicate when individual lots were transferred to ambient
temperature (see footnote 5).

frequent variations as great as ±2° C for 1 day
were observed. Mean temperatures for the 37-
day period September 7 through October 14
were within ±0.2° C of the planned levels. Am-
bient temperature, initially 6.9° to 8.7° C,
dropped gradually to the usual winter level of
4.0° C by mid-November.

We made no direct observations of the stages
of development of the embryos when they were

transferred to ambient temperature (on days
15, 27, 37, and 103), but in a separate exper-
iment we observed development of pink salmon
embryos in relation to temperature. At tem-
peratures approximating ambient in the present
experiment, the eggs began gastrulation about
the 10th day and completed gastrulation about
the 26th day. Eggs incubated initially at 4.5° C
began gastrulation about the 21st day and com-
pleted gastrulation about the 45th day. Eggs
incubated initially at 3.0° C began gastrulation
about the 34th day and completed gastrulation
about the 62d day.

We controlled water temperatures during in-
cubation by mixing chilled and unchilled water
in the intake line to each incubation funnel. A
continuous flow of fresh water chilled to 1.0°
±0.3° C was obtained by operation of a 1/3-hp
refrigeration unit. The cooling coils and agi-
tator propeller were suspended in an insulated
20-gal fiberglass tank. Unchilled or ambient
water was introduced through Y fittings to pro-
duce the required temperature for experimental
lots of eggs.

Eggs incubated entirely at ambient temper-
ature were first to hatch — the midpoint of hatch-
ing occurred December 9, 1966, 94 days after
fertilization. The last eggs to hatch were from
the group that was incubated initially at 3.0° C
for 103 days. The survivors of the prolonged
cold treatment hatched February 8, 1967, 154
days after fertilization.

Mortalities were inversely related to initial
incubation temperatures. None of the eggs in-
cubated at 2.0° C survived (Table 2) ; at 3.0° C,
about 75% died; and at 4.5° C, about 10% died.
Average moi'tality of eggs incubated entirely at
ambient temperature was only 3%.

The occurrence of developmental anomalies
was also associated with severity of the initial
cold treatments. No alevins were produced in
the 2° C treatment lots. Mild spinal defoi'mities,
various degrees of spinal curvature in the verti-
cal plane, occurred in the 3.0° C and 4.5° C lots.
The spinal flexures were not always severe
enough to be easily recognized as deformities,
but the deformity caused the lengths of alevins
in these lots to be less uniform than the lengths
of alevins in the ambient temperature lots.

591

FISHERY BULLETIN: VOL. 69. NO. 3

Table 2. — Percentage mortality from fertilization to
hatching of pink salmon in relation to initial incubation
at low temperatures (number of eggs in each lot in
parentheses).

Exposure period

Percenl

mortality at temperature

treatment'

idayl)

Ambient

4.5° C

3.0° C

2.0° C

15

4

12

71

100

(24)

(24)

(24)

(24)

27

0

12

77

100

(25)

(25)

(22)

(25)

37

5

10

60

100

(20)

(21)

(20)

(21)

103

2

7

82

100

(41)

(41)

(40)

(40)

* See Figure 3 for temperature regime for each treatment.

Range in lengths among alevins in the ambient
temperature lots was 20.9 to 22.9 mm, but range
in length in the 3.0° C lots was 15.1 to 22.3 mm
(Table 3).

Because of the increased mortality and ab-
normal embryonic development of Grace Creek
pink salmon eggs at temperatures of 4.5° C and

Table 3. — Ranges in lengths (millimeters) of alevins
from eggs treated at four temperatures (number of
alevins measured in parentheses).

Ro

-iges in total length {mm) at—

Exposure
period
I.Jays)

Ambient
temperature

4.5° C

3.0° C

2.0° C

15

21.3-22.6

20.8-23.2

18.4-21.9

(10)

(10)

(7)

27

21.1-22.8

21.0-23.1

20.5-21.7

(10)

(10)

(5)

37

20.9-22.3

19.3-22.3

19.4-22.3

(10)

(10)

(8)

103

21 .0-22.9

20.2-22.4

15.1-20.3

(10)

(10)

(7)

lower, we conclude that initial incubation tem-
perature for these eggs should be higher than
4.5° C. This is in agreement with the 4.4° to
5.9° C threshold for normal development of sock-
eye and Chinook salmon eggs found by Combs
(1965).

DISCUSSION

The proposed Grace Creek hydroelectric pow-
er plant focuses attention on a fishery problem
that may become increasingly imjiortant if more
hydroelectric plants are to be built on Alaska

streams. Where water for power generation is
drawn only from the deeper and colder waters
of reservoirs, the resulting stream temperatures
would be lower than normal during the salmon
spawning season and initial incubation period
(Figure 1).

At Grace Creek the expected changes in water
temperature could affect salmon in several ways.
Delay in ripening of gonads of the adults after
they enter the streams because of the lowered
temperatures (Reingold, 1968) might result in
late spawning. The low initial incubation tem-
peratures would further delay development of
embryos, but if normal cleavage were not dis-
rupted this delay could be offset by the higher
winter temperatures. The net effect on time
of emergence and seaward migration of the fry
is not known. The predicted initial incubation
temperature of 4.5° to 7.2° C (Figure 1) for
pink salmon eggs at Grace Creek includes the
temperature 4.5° C, at which we detected ab-
normal development and increased mortality of
the embryos. Measures should therefore be
adopted to prevent deleterious temperature
changes. Provision of an intake designed to
draw water of a desirable temperature on de-
mand is suggested as minimum action to protect
the salmon.

ACKNOWLEDGMENTS

Theodore R. Merrell, Jr., generously gave of
his time and thoughts in discussions of the
problem. Charles J. DiCostanzo critically re-
viewed the manuscript and made suggestions to
improve clarity of presentation.

LITERATURE CITED

Combs, B. D.

1965. Effect of temperature on the development of
salmon eggs. Prog. Fish-Cult. 27: 134-137.
Combs, B. D., and R. E. Burrows.

1957. Threshold temperatui-es for the normal de-
velopment of Chinook salmon eggs. Prog. Fish-
Cult. 19: 3-6.
Efimov, V. I.

1962. Vyzhivaemost' gorbushi v period embrional'-
nogo razvitiya. (Survival rate of pink salmon
(Oncorhynchus gorbuscha) during embryonic de-

592

BAILEY and EVANS: LOW-TEMPERATURE THRESHOLD

velopment.) Polyarn. Nauchn.-issled. Inst. Morsk.
Rybn. Khoz. Okeanogr., Nauchn.-Tekh. Byul. 4 :
25-26. (Abstr. in Biol. Abstr. 45: 7142, Abstr.
No. 89708.)
Hutchinson, G. E.

1957. A treatise on limnology. Volume I, Geog-
raphy, physics, and chemistry. Wiley, New York,
1015 p.

KtNNE, O., AND E. M. KiNNE.

1962. Rates of development in embryos of a cyprin-
odont fish exposed to different temperature-salini-
ty-oxygen combinations. Can. J. Zool. 40: 231-253.

Knight, A. E.

1963. The embryonic and larval development of the
rainbow trout. Trans. Am. Fish. See. 92 : 344-355.

McCauley, R. W.

1963. Lethal temperatures of the developmental
stages of the sea lamprey, Petromyzon marinus
L. J. Fish. Res. Board Can. 20: 483-490.
PlAVTS, G. W.

1961. Embryological stages in the sea lamprey and
effects of temperature on development. U.S. Fish
Wildl. Serv., Fish. Bull. 61: 111-143.
Price, J. W.

1940. Time-temperature relations in the incubation
of the whitefish, Coregonus clupeaformis (Mitch-
ill). J. Gen. Physiol. 23: 449-468.

Reingold, M.

1968. Water temperature affects the ripening of
adult fall Chinook salmon and steelhead. Prog.
Fish-Cult. 30: 41-42.
SoiN, S. G.

1954. Zakonomernosti razvitiya letnei kety, gor-
bushi i simy. (Pattern of development of sum-
mer chum, masu, and pink salmon.) Tr. Soveshch.,
Ikhtiol. Kom. Akad. Nauk SoSR 4: 144-155.
Stockard, C. R.

1921. Developmental rate and structural expres-
sion: An experimental study of twins, 'double
monsters' and single deformities, and the inter-
action among embryonic organs during their or-
igin and development. Am. J. Anat. 28: 115-277.
Taning, a. V.

1952. Experimental study of meristic characters
in fishes. Biol. Rev. (Cambridge) 27: 169-193.
U.S. Geological Survey'.

1966. Water resources data for Alaska, 1965. Part
2. Water quality records, 73 p.

1967. Water resources data for Alaska, 1966. Part
2. Water quality records, 81 p.

1968. Water resources data for Alaska, 1967. Part
2. Water quality records, 64 p.

593

PRIMARY PRODUCTION IN THE MID-SUBARCTIC
PACIFIC REGION, 1966-68

Jeery D. Larrance'

ABSTRACT

Primary productivity, chlorophyll a, net zooplankton, nutrients, and associated physical variables were
measured on seven cruises in the mid-Subarctic Pacific Region in 1966-68. Most of the data were col-
lected between lat 46° N and the central Aleutian Islands, although several measurements were made
as far south as lat 40° N. Primary productivity and chlorophyll were higher in Aleutian coastal waters
than in areas to the south, but no other major differences among upper zone domains were consistent
seasonally. Production was low in winter, high in spring, and intermediate throughout the summer.
Annual productivity was between 80 and 100 g C/nfi. Chlorophyll a concentrations changed only slightly
except in March when chlorophyll was high during the early part of the phytoplankton bloom.

Low light intensities limited primary production during the winter, and zooplankton grazing appeared
to limit production in summer and part of spring. Nutrients and light were always sufficient to sup-
port high productivity during spring and summer except in late summer when some nutrients, particu-
larly nitrate, were very low south of lat 44° N; however, the productivity did not appear severely
limited. The main source of phosphate replenishment in the upper layers during spring and summer
was probably in situ regeneration by zooplankton rather than upwelled deep water.

The pelagic biota of the Subarctic Pacific Region
has long been recognized as distinct from that
in the Subtropical Region, and the Subarctic is
thought to be generally more productive. Until
the introduction of the carbon-14 technique by
Steemann Nielsen (1952) , however, no adequate
means existed for directly measuring primary
productivity in the open ocean. Since that time
thousands of measurements of primary produc-
tion have been made throughout the Tropical
and Subtropical North Pacific. Measurements
in the Subarctic Pacific have been fewer and
more localized.

Koblents-Mishke (1965), who summarized
data from the Pacific Ocean, estimated that pri-
mary productivity in the mid-Subarctic Region
averaged about 150 to 250 mg C/m- per day
or 55 to 91 g C/m^ per year. She estimated
average production in the Gulf of Alaska and
along the Washington and Oregon coasts to be
between 250 and 650 mg C/m^ per day (90-240 g
C/m- per year) and in the transition area of
the southern Subarctic to be 100 to 150 mg C/m-

' National Marine Fisheries Service, Biological Lab-
oratory, Seattle, Wash. 98102.

Manuscript accepted February 1971.

FISHERY BULLETIN: VOL. 69. NO. 3, 1971.

per day (35-55 g C/m^ per year). As discussed
by Koblents-Mishke, these estimates are rather
imprecise because productivity at most of the
stations was measured only at the surface and
not throughout the euphotic zone and because
many of the measurements were made in artifi-
cial light of various intensities. Comprehensive
analyses of annual cycles were seldom possible
because surveys have been made during all
seasons in only a few studies.

From detailed year-round surveys, Anderson
(in press) estimated annual primary produc-
tion in oceanic waters off^ Washington and Ore-
gon to be 125 g C/m-. Mean annual primary pro-
duction at Ocean Station "P" (lat 50° N, long
145° W) in the Gulf of Alaska was 48 g C/m=
in 1960-66 (McAllister, 1969). Although pri-
mary productivity has been measured on several
individual cruises through the region (McGary
and Graham, 1960; Faculty of Fisheries, Hok-
kaido University, 1961; Doty, 1964; Koblents-
Mishke, 1965), no previous time-series studies
of productivity have been made in the central
Subarctic Region west of Station "P."

Primary productivity, zooplankton abundance,
and related physical and chemical oceanographic

595

FISHERY BULLETIN: VOL. 69. NO. 3

variables were measured on several cruises in
1966-68 within the Subarctic Region in con-
junction with studies of abundance and distribu-
tion of Pacific salmon (genus Oncorhynchus) .
Productivity data are listed in Larrance (1971),
zooplankton is discussed by Day (1970),' and
physical data are listed in Ingraham and Fisk
(1970). The objectives were to obtain an esti-
mate of annual productivity and to detect what
differences in levels of productivity, if any,
occurred among several oceanographic areas
identifiable by physical characteristics.

METHODS

Primary productivity and related variables
were measured on cruises of the RV George B.
Kelez in March, June, and September 1966;

' Day, D. S. 1970. Distribution of zooplankton from
the mifl-Subarctic Region of the Pacific Ocean, 1966-67.
Natl. Mar. Fish. Serv., Biol. Lab., Seattle, Wash. Unpubl.

manuscr.

January-February, June-July, and August 1967;
and May 1968 ; and on a cruise of the MV Par-
agon in June 1966 (Table 1). Measurements
in 1966-67 were south of Adak Island (long
176°25' W) except in January-February 1967
when the cruise track was along long 162° W
and in May 1968 when it was along long 165° W
( Figure 1 ) . Primary productivity was measured
by the carbon-14 method introduced by Stee-
mann Nielsen (1952) and modified by Strick-
land and Parsons (1965) . Productivity stations
were normally taken shortly before dawn and
local apparent noon (LAN); incubation periods
were for one-half the daylight period, i.e., from
dawn to LAN and from LAN until about twi-
light. Seawater was sampled with 6-liter plastic
water bottles at depths determined from the
penetration of light below the sea surface. These
"light depths" were 100, 61, 35, 18, and V/( of
the surface intensity according to the fractions
of light transmitted by neutral-light filters used
in the productivity incubations. The depths

Table 1. — Summary of areas, dates, and stations on which primary pro-
ductivity was measured, 1966-68'.

Cruise no.

Vessel

Dales

Number of stations

Area

1966

Kl-««

Kiln

March 18-28

Productivity - 6

Chlorophyll end

nutrients - 9

Total - 9

Adak Is. to lot 41° N

P2-66

Paragon

June 10-21

Productivity - 8
Chlorophyll and
nutrients - 10
Total - 10

Adak Is. to lot 41° N

K3-«6

Keltz

Sept. 8-20
1967

Productivity . 1 1

Chlorophyll and

nutrients - 19

Surface productivity - 14

Totol - 28

Adak Is. to lot 40° N

K1-<S7

Ktliz

Jan. 30-Feb. 15

Productivity - 10
Total - 10

Along long 162° W
between lot 54° and
46° N

KS-67

Kiln

June 24-July 3

Productivity - 10
Total - 10

Adak Is. to lot 46° N

'<&&7

Ktin

July 8-July 11

Productivity (Vb
day only) - 4

Alaskan Stream

K7-(57

Ktln

Aug. 21-Aug. 28
1968

Productivity - 7
Total - 7

Adak Is, to lot 46° N

K2-68

KtIn

May 9-15

Chlorophyll and

nutrients - 5

Total - 5

Along long 164° W
between lot 53° and
49° N

* Only portions of cruises discussed in this report are included in Table I.

^ Data from cruise 6-67 were averaged with data from station 5-67 for this report.

596

LARRANCE: PRIMARY PRODUCTION IN MID-SUBARCTIC REGION

I70°E 180° I70°W

Figure 1. — Tracks of Bureau of Commercial Fisheries cruises in 1966-68 in the Subarctic Pacific Region during

which primary productivity was measured.

were calculated from Secchi disk readings con-
verted to extinction coefficients (Poole and At-
kins, 1929). Sampling depths of the morning
stations were computed from the preceding day's
Secchi-disk readings. Duplicate light-bottle
samples under the neutral-light filters were in-
cubated on deck in daylight and cooled with
running sea water. After incubation, samples
were filtered through Millipore' filters, pore size
0.45 fi. for radioassay.

Stock solutions of Na2"C03 were prepared ac-
cording to Strickland and Parsons (1965) but
were standardized by using liquid-scintillation
techniques. A 1.00-ml portion from an ampoule

containing the stock carbonate solution was in-
troduced in 10 ml of a suitable phosphor solu-
tion, and its count rate determined in a Packard
Tri-Carb' scintillation spectrometer. One liter
of phosphor solution contained 800 ml toluene,
200 ml Sterox" (a surfactant required to make
the water miscible in toluene) , 5.0 g PPO (2, 5-
diphenyl-oxazole), and 0.3 g bis-MSB (p-bis-
(o-methylstyrl) -benzene) . Counts of an external
radium standard were also recorded and the ab-
solute activity (dpm) was determined from a
quench correction curve relating efficiency to the
count rate of the external standard (Wang and
Willis, 1965). Although scintillation counting

^ Millipore Corp., Ashby Rd., Bedford, Mass. 01730.
References to trade names in this publication do not imply
endorsement of commercial products by the National Ma-
rine Fisheries Service.

' Packard Instrument Co., Inc., 2200 Warrenville Rd.,
Downers Grove, 111. 60515.

" Jefferson Chemical Co., P.O. Box 53300, Houston,
Tex.

597

FISHERY BULLETIN: VOL. 69, NO. 3

is more efficient than planchet counting, produc-
tivity samples were routinely counted on plan-
chets in a gas-flow geiger detector for conven-
ience. The efficiency of the geiger counter was
determined by counting a standard source of
known activity so that absolute activity of the
samples could be related to those of the stock
solution.

Samples for chlorophyll a, phosphate, silicate,
and nitrate-nitrite were also drawn from the
water bottles. Nutrient samples were frozen
in plastic bottles and returned to Seattle for anal-
ysis. Phosphate and silicate concentrations
were determined by methods given by Strickland
and Parsons (1965), and nitrate-nitrite samples
were analyzed by the method of Wood, Arm-
strong, and Richards (1967).

Four liters of water from each sampler were
filtered through glass-fiber filters (Gelman, type
A) ,° stored in a dark desiccator at about 0° C,
and returned to Seattle for chlorophyll a anal-
yses. A layer of MgCOa was added to the filter
prior to filtration. Chlorophyll a concentrations
were determined by the method of Richards with
Thompson (1952) but were computed with equa-
tions given by Parsons and Strickland (1963).
Chlorophyll samples on the glass-fiber filters
were ground in a tissue grinder as suggested
by Yentsch and Menzel (1963). The resulting
suspension was filtered through a very-fine-por-
osity (VF) fritted-glass disk under pressure,
and the cake of residue remaining on the disk
was stirred with a few ml of 90 ''r acetone and
refiltered. Absorbances at 750 ni/u, which in-
dicate turbidity, of the resulting effluents were
seldom more than 0.010 per cm of light path
and then only in the more highly colored sam-
ples. A series of 20 tests showed no more than
traces of pigment remaining in the residue after
the first wash. The above treatment for separat-
ing residue from samples was preferable to cen-
trifugation because it resulted in generally lower
turbidity and more complete recovery of extract.

Total incident solar and sky radiation (over
the wavelength range 0.3 to 3 n) was continu-
ously measured and graphically recorded by a

" Gelman Instrument Co., P.O. Box 1448, Ann Arbor,
Mich. 48106.

pyranometer. Although the photosynthetically
active portion of the spectrum is roughly half
the total radiation (Edmondson, 1956), total
radiation values were used in productivity cal-
culations. Salinity and temperature were mea-
sured and standard weather observations were
recorded near the productivity stations (Lar-
rance, 1971).

Measurements of productivity, chlorophyll a,
and nutrients at various depths were integrated
to the bottom of the euphotic zone (designated
here as that depth where light intensity is 1%
of the surface intensity), or other specified
depth, and the integrated values expressed per
square 'meter of sea surface. Mean values for
several oceanographic domains were computed
by weighting the values according to distances
between stations. Details of the calculations
were given in Larrance (1971).

PHYSICAL OCEANOGRAPHY

The physical oceanography of the Pacific Sub-
arctic Region has been described by Fleming
(1955) , Dodimead, Favorite, and Hirano (1963) ,
and Tully (1964). On the basis of data from
Ocean Station "P" (lat 50° N, long 145° W),
Dodimead etal. (1963) divided the upper 1,000 m
of the Subarctic Pacific Region into three perma-
nent zones: an upper zone from 0 to about
100 m depth; a halocline from about 100 to 200 m
through which the salinity increases downward
by about l%c; and a lower zone from about 200
to 1,000 m. During the spring and summer,
warming of the surface layers causes a tempo-
rary thermocline in the upper zone which is
subsequently destroyed by cooling in the autumn.
Consequently the lower limit of the wind-mixed
upper layer ranges from about 30 to 60 m in
the spring and summer and extends to the top
of the permanent halocline at 100 m during
winter. The upper zone in the Subarctic Pa-
cific has been divided by Dodimead et al. (1963)
into Coastal, Alaskan Stream, Central Subarctic,
Western Subarctic, and Transitional Domains
(Figure 2).

The Coastal Domain south of the Aleutian
Islands lies over the continental shelf and is
strongly influenced by Bering Sea water mixed

598

LARRANCE: PRIMARY PRODUCTION IN MID-SUBARCTIC REGION

l40O 150° 160° 170° £ 180° 'Z°l"'_

150°

130°

>^^^^'

/,a

NORTH PACIFIC OCEAN

SCHEMATIC DIAGRAM OF
UPPER ZONE DOMAINS

^///////-^

'''''^m^''

<^^£^^

oo^]^

^^^$$^// ■•'//// <(''''' g^y'R£/'>^^''^/,w'''=: CENTRAL SUBARCTIC DOMAIN

OOM^N

ia^:^?imeiiiife

UMSuJARgiCBOUND^P^,

tffsr wwz? £i/?//^r

/::■!.; TRANSITIONAL DOMAJN '•'^i''-;-?^

""-n,;

•••.,

:^=*

■»—— — MM W1

-M.»IM»»»i»IHJ«MMMM1JBMMM»IMI« -M-M-JI »l ■ B P ■ M ■ ItJ
liO'' 160° 170° E 180° r7(?W 160° I;

Figure 2. — Diagram of upper zone domains in the Subarctic Pacific Region (after Dodimead, Favorite, and

Hirano, 1963).

through passes between the islands. To distin-
guish the Coastal from Alaskan Stream Domains,
coastal water was arbitrarily defined by sui'face
salinities greater than 32.9'-,',. The Alaskan
Stream, described in detail by Favorite (1967),
flows westward out of the Gulf of Alaska with
velocities as high as 100 cm/sec. It is diluted
by runoff from Alaska and can be detected by
low salinity (less than S2.6'/t() at the surface.
The Central Subarctic Domain is an area of
weak and variable currents bounded on the north
by the Alaskan Stream and on the south by the
Subarctic Current, which flows eastward at ve-
locities between 5 and 20 cm/sec (McAlister
et al., 1970) . The Subarctic Current separates
the Central Subarctic Domain from the Tran-
sitional Domain, which extends southward as
far as the northern boundary of the Subtropical
Region and is also an area of weak eastward
flow. The nomenclature given by McAlister et al.

(1970) was slightly diff'erent from that applied
to the upper zone domains of Dodimead et al.

(1963), but it was based in part on features

below the upper zone. For purposes of the
present paper, the definitions of the upper zone
domains as given in Dodimead et al. (1963) were
used; the Subarctic Current, which originates
in the Western Subarctic Domain, was thus in-
cluded in the Central Subarctic Domain.

The Transitional Domain has been further di-
vided into two areas (T-1 and T-2) on the basis
of the salinity in the upper 50 m. The division
between areas T-1 and T-2 was set in August
1967 at lat 47° N, where surface salinity was a
maximum and decreased to the north and to the
south at least as far as lat 46° N. The Transi-
tional Domain was also divided in September
1966, when the northern area (T-1) extended
from lat 47°05' N to a relatively sharp hori-
zontal salinity gradient at lat 43°35' N. The
southern area (T-2) extended to lat 40°45' N,
where the boundary between transitional and
subtropical waters was found. These divisions
of the Transitional Domain are somewhat ar-
bitrary but tend to be corroborated by biological
and chemical characteristics.

599

FISHERY BULLETIN: VOL. 69, NO. 3

PRIMARY PRODUCTIVITY ESTIMATES

ADJUSTED FOR DIFFERENCES

OF LIGHT INTENSITY

Because productivity was measured in natural
light which differed (by as much as fivefold)
in total insolation from day to day, productivity
values were adjusted by two methods to permit
comparison of productivity estimates under
similar lig^ht conditions for purposes of detecting
possible differences in productivity among ocean-
ographic areas. One method applied the relation
given by Ryther (1956) and Ryther and Yentsch
(1957) of relative daily productivity beneath
a unit of sea surface to total daily surface ra-
diation. The measured daily light intensities
were averaged for each cruise and the corres-
ponding values of R (photosynthetic rate rela-
tive to photosynthesis at light saturation),
defined by R>i;her and Yentsch (1957), were de-
termined for the cruise mean of daily light and
for the light observed on the particular day in
question (K,,, and R,,,, respectively). Adjusted
productivity was then com])uted by Pr = P,„ y
Rav'Rm where Pr and P,„ are the adjusted and
observed productivities integrated through the
euphotic zone and have the units of mg C 'm-
per day. This ]irocedure amounts to using the
shape of Ryther's (1956) curve but not his ab-
solute values for estimating productivity.

Since Ryther derived his curve from photosyn-
thesis measurements of phytoplankton from
Woods Hole Harbor, that relationship is likely
to differ from similar curves based on measure-
ments from other areas. An attempt was made,
thei'efore, to establish a simple emi)irical rela-
tion to estimate productivity in the mid-Sub-
arctic Pacific Region from chlorophyll and light
data obtained during the Kelez cruises. The
regression of measured daily productivity (P,,,)
per unit of chlorophyll a (C„) in the euphotic
zone

(where Pm/Ca ^

,mg C as.similated/m- per day,
mg chloroi)hyll a m-

on daily light intensity measured on the ship's
deck was computed (Figure 3) . Only data from
those stations where a full day's productivity and
light were measured were used for the relation.

• From Stotions south

45

of 46° N - not
included m the regression

40

•

35

•

50

• /

-"-'

o /

o /

25

/•

o / °

20

o o /

o/°o

o /

15

o .A °o^ o

/ On
0 / ' "

10

°y 0 o

o«ft./^

o o /

5

/

/ Pm/Ca =0 0574 X SOLAR RADIATION

0

1 1 1 1 1 1

0 100 200 300 400 500 600

SOLAf R4DI4TI0N (col/cm^ p«r do»)

Figure 3. — Relation between the ratio of daily primary
productivity to chlorophyll a (P,n/Ca) in the euphotic
zone and daily solar radiation above the sea surface in
the Subarctic Pacific Region, 1966-67.

The intercept of the regression and the axes was
not significantly different from the origin. The
variability was generally large, as might be ex-
pected from data of this kind, and was especially
high for stations in the southern portion of the
study area (transitional and subtropical water).
This variability suggests that productivity re-
sponses to the environment in the Transitional
Domain and subtropical water were probably
different from tho.se north of about lat 46° N.
Furthermore, relatively few measui-ements were
taken south of lat 46° N — not enough for seasonal
comparisons. For these reasons, the regression
was computed for only those stations north of
lat 46° N.

Productivities under average daily light in-
tensities for each cruise (Pk) were estimated by
multiplying the chlorojihyll a measured in the
eu|)hotic zone at a station by tlie estimate, from
the regression, of P Ca corresponding to the

600

LARRANCE: PRIMARY PRODLCTIONJ !N MID-SL BARCTIC REGION

average daily light intensity for the cruise. Al-
though the relation was based on data tal<en
north of lat 46° N, it was used to estimate pro-
ductivity in June 1966 for stations as far south
as lat 44° N (Figure 4).

These methods give rough approximations at
best but probably indicate productivity responses
to seasonal-average light conditions more accu-
rately than those given by measured produc-
tivity values affected by large day-to-day fluc-
tuations of light. The means of Pu for each
cruise were higher than means of Pk except in
September (Table 2, Figure 5). The higher Pr
values may mean that the photosynthetic effi-
ciency of the subarctic Pacific phytoplankton is
lower than the average efficiency of populations
represented in Ryther and Yentsch's (1957)
analysis. Other ]30ssible explanations might in-
volve differences between our experimental pro-
cedures and Ryther's (1956).

AREAL AND SEASONAL

DISTRIBUTIONS OF PRIMARY

PRODUCTIVITY AND CHLOROPHYLL ^4

Differences in ])roductivity and chlorophyll a
among the upper zone domains do not appear
to be consistent from season to season except
that mean values in the Coastal Domain and
Adak Bay were higher than those farther from
shore (Figure 4, Table 2). The Coastal and
Alaskan Stream Domains can be compared only
in June- July 1967 because both areas were not
sampled on any other single cruise. Productivity
and chlorophyll o were substantially higher in
coastal water than in the Alaskan Stream. Un-
like other times of the year, productivity and
chlorophyll values were similar in nearshore and
offshore areas in March 1966 and January-Feb-
ruary 1967, probably because low light inten-
sities in these months limited production to about
similar levels throughout the northern Subarctic
Region. This effect was especially pronounced
at Adak Bay, where productivity estimates in
March were between 350 and 460 mg C/m- per
day but ranged between 840 and 2,400 mg C m-
per day in late spring and through the summer.
The lowest productivity during each cruise was
in the Central Subarctic Domain except in win-

ter, when productivity was uniformly low
throughout the region. The mean ijroductivity,
however, was lower in the Central Subarctic
Domain than in the other areas only in March
1966 and June 1967.

Daily carbon assimilation was normalized
(,P/C„) above to estimate productivity from
chlorophyll and light measurements. The com-
monly used P 'Ca ratio may also be considered
as an index of the capacity of a population to
photosynthesize under natural light and ambient
nutrient and temperature conditions, and pro-
vides a basis for seasonal and areal comparisons.
This ratio is similar to "turnover rate" (Cushing
et al., 1958) and to the ratio discussed by Currie
(1958), except that Currie used the concentra-
tion of the total complement of plant pigments
instead of only chlorophyll 0. Piatt (1969) used
an efficiency index (productivity/light energy)
to normalize productivity measurements for
comparison at designated chlorophyll concentra-
tions by means of a regression of the efficiency
index on chlorophyll. His method was similar
to that used here except he could estimate pro-
ductivity at individual depths. For analysis in
this study, ratios of P 'C„ were computed for
measured productivities (P,,,) and productivities
adjusted for differences in light (Pr) by the
curve of Ryther and Yentsch (1957).

Ratios of Pr 'C, were high at four of the nine
stations at or south of lat 46° N (Figure 6).
The southernmost stations in March and Sep-
tember 1966 were in subtropical water. In
March, Pr (515 mg Cm- per day) and Pr /Ca
(39) were high, suggesting conditions of a phy-
toplankton bloom, whereas in September, Pn/Ca
was lowest (10) of any observed during summer
(Table 2). At lat 44° N in June 1966 and at
lat 42°50' N in September, Pr/C, ratios were
high (41 and 49), but Pr values were moderate
(232 and 275 mg C/m- per day) and chlorophyll
values were unusually low (5.6 mg 'm- in each
case) . This combination of high Pr/Co and low
chlorophyll may be due to high carbon to chlor-
ophyll ratios in the cells. At lat 46° N in August
1967, however, Pr and chlorophyll a were both
relatively high (664 mg C 'm= per day and 16.8
mg/m') ; thus the high productivity and photo-
synthetic capacity (Pr/Cu = 40) of the popu-

601

FISHERY BULLETIN: VOL. 69, NO. 3

< < tr

o _J 1-

< <X (Tl

I i

Z 03

MARCH 1966

I48SI

1170 =

SEPTEMBER 1966

; T-2

S 500

0
700

dtm^

Figure 4. — Primary productivity in the mid-Subarctic Pacific Region, 1966-68.

602

LARRANCE: PRIMARY PRODUCTION IN MID-SUBARCTIC REGION

Table 2.— Chlorophyll a in the euphotic zone, measured and estimated primary productivity values, and ratios of
productivity to chlorophyll a in the mid-Subarctic Pacific Region (averaged within upper zone oceanographic do-
mains) 1966-68.

Chlorophyll a

Primary productivity

Date and cruise no.

(mg/m2)

(mg C/m

per day)

and area

c„

P^

Pr

Pk

Pm'C^

Pr/C,

PK/Ca'

Morch 1966 {ICl-66)

Adok Boy

24.9

187

460

351

7.5

18.5

Alaskan Stream

23.2

229

392

327

9.9

16.9

Centrol Subarctic

17.8

305

265

251

17.1

14.9

Transitional

19.6

317

317

276

16.2

16.2

tr*

Subtropic

13.2

612

515

—

46.4

39.0

r

46°-jl°40'

19.3

292

303

272

15.1

15.7

14.1

June 1966 (P2-66)

Adak Bay

64.3

1485

1492

1061

23.1

23.2

Alaskan Stream

25.0

--

412

—

—

Central Subarctic

14.5

422

429

239

29.1

29.6

Transitional

9.4

324

328

155

34.5

34.9

46°-5l°40'

14.4

431

426

238

29.9

29.6

16.5

September 1966 (K3-66)

Adak Bay

42.4

914

—

827

21.6

—

Coastal

23.8

345

464

14.5

—

Central Subarctic

11.9

195

199

232

16.4

16.7

Tronsitional 1

11.7

222

197

228

19.0

16.8

Transitional 2

6.9

187

217

—

27.1

31.4

Subtropia

15.0

165

150

—

11.0

10.0

46°-il °40'

12.8

204

201

250

15.9

15.7

19.5

Jonuory-February 1967 CKl-67)

Alaskan Stream

9.1

71

80

60

7.8

8.8

Central Subarctic

12.4

93

108

82

7.5

8.7

Transitional

10.1

94

82

67

9.3

8.1

46°-53°53'

11.2

83

96

74

7.9

8.6

6.6

June-July 1967 (KJ-67 and K6-67)

Adak Bay

99.4

2068

2396

1889

20.8

24.1

Coastal

22.8

945

680

433

41.5

29.8

Alaskan Stream

14.0

290

265

266

20,7

18.9

Central Subarctic

11.1

165

193

211

14.9

17.4

Transitional

13.2

171

299

251

13.0

22.6

46°-5r40' - ,

12.7

202

248

241

15.9

19.5

19.0

August 1967 (K7-67)

Adak Boy

60.6

643

878

867

10.7

14.5

Coastal

41.8

661

483

598

15.8

11.6

Central Subarctic

6.3

118

138

90

18.7

21.9

Transitional 1

7.2

127

127

103

17.6

17.7

Transitional 2

1 6.8

598

664

240

35.6

39.5

46°-51 °40'

10.7

238

247

153

22.2

23.1

14.3

May 1968 (K2-68>

Alaskan Stream

41.3

710

Central Subarctic

10.6

182

Tronsitionol

14.3

246

48°50'-53°

14.3

246

1 Mean values for each cruise.

lation were undoubtedly real. From these re-
sults, productivity and photosynthetic capacity
south of lat 46° N appear to be neither char-
acteristically high nor low, except in spring
during bloom conditions, but fluctuate over a
wide range.

Because relatively few measurements were
made south of lat 46° N and the Pr/Ch ratios
varied rather widely, only the data between lat

46° N and the Aleutian Islands were compared
to determine seasonal patterns of production.
If all the data are treated as if taken in the
same calendar year, a seasonal pattern of pro-
ductivity can be approximated (Figure 5) . Pro-
ductivity in winter was uniformly low through-
out the area (Pr =96 and Pk = 74 mg C/m^
per day). The mean chlorophyll o concentra-
tion (11.2 mg/m-), however, was similar to

603

FISHERY BULLETIN: VOL. 69, NO, 3

500

400

:300

b200

o
o

IT

Q.

>- 100

a:

<

or

a

JAN

FEB

MAR

APR

MAY
MONTH

JUN

JUL

AUG

SEP

Figure 5. — Seasonal pattern of primary productivity ami chlorophyll o in the mid-Subarctic Pacific Region be-
tween the Aleutian Islands and lat 46° N.

summer means. As might be expected, primary
productivity was limited by low available light
energy in the winter. The mean daily light in-
tensity was low (116 cal/cm-), and the avail-
ability of light to the cells was further limited
by their being distributed throughout the surface
mixed layer, which reached well below the eu-
photic zone to the halocline at about 100 m.

In March, daily light intensities averaged 274
cal/cm- and thermal stratification had developed
sufficiently to decrease the mixed-layer depth —
thereby increasing exposure of the cells to light
at shallower depths and consequently stimulating
growth. The mean chlorophyll a concentration
(19.3 mg/m-) was clearly higher than for any
other season, and Pr and Pk (303 and 272 mg
C/m- per day) were more than three times as
high as in January and February (Figure 5,
Table 2). The Pr/C„ and Pk/Co ratios (16
and 14) were roughly twice those in midwinter,
indicating that productivity was no longer lim-
ited by low light intensities. Although measure-
ments in May 1968 were made at a considerable
distance east of the Adak Line and may not be
directly comparable, mean Pk values were re-

markably similar in June 1966 and 1967 and
May 1968 (238, 241, and 246 mg C/m^ per day,
respectively) as were the mean chlorophyll val-
ues (14.4, 12.7, and 14.3 mg/m-, respectively).

In August, the mean Pk and Pr values differed
significantly {Pk = 153 and Pr = 247 mg C/m^
per day) . A large part of this difference may be
attributed to high productivity measured at lat
46° N in transition area T-2 (Pk- = 240 and
Pr = 664 mg C/m- per day) . These estimates
strongly influenced the means because the
weights assigned to each in the averaging pro-
cess were relatively large. The mean chlorojjhyll
a concentration (10.6 mg m') was slightly less
than in June, and the mean Pr/Cu (23) was
higher than in June. In September, mean Pb
and Pk were 201 and 2.50 mg Cm- per day,
and the mean chlorophyll o was 13.0 mg/m'.
These values were somewhat similar to the other
summer values, as were the ratios Pw/Ca (16)
and Pk/C„ (20).

The general time-distributional pattern of pro-
ductivitj' and chloroi)hyll a between lat 46° and
51°40' N from January through September was
drawn from the above results (Figure .5). Pro-

604

LARRANCE: PRIMARY PRODUCTION IN MID-SUBARCTIC REGION

. Pr/Co

pk/Co

SEPTEMBER 1966

JANUARY
FEBRUARY 1967

JUNE JULY 1967

Figure 6. — Ratios of Pr/C„ and Py^/C^ in the Subarctic
Region along long 175°-17G° W, 1966-67.

duction was low in the winter, increased sig-
nificantly in March, and was relatively steady
at intermediate levels throughout the summer.
Chlorophyll a also increased between February
and late March as a consequence of high pro-
duction but decreased significantly during the
spring and decreased slightly throughout the
summer. Some reasons for these changes can
be inferred from the nutrient and zooplankton
data and are discussed later.

Although primary production apparently con-
tinued at a high rate through the spring, chloro-
phyll a concentrations were significantly less in
May and June than in March. Two probable
reasons for this decrease are a decrease in cell
chlorophyll content and an increased loss rate,
primarily due to grazing. It is impossible to
ascertain from the data which one of these
causes was most important, but some trial cal-

culations can help explore the problem. The
standing stock (Si) at t days (time between
consecutive cruises) was predicted by the simple
growth equation

S, = Soe""-""

where So is the initial standing stock and « and h
are growth and loss coefficients. Standing stock
was expressed in mg chlorophyll a/m^, and P/Ca
ratios were multiplied by \/F (ratio of cell
chlorophyll a to cell carbon) to give growth co-
efficients (o) in units of day^'.

The growth rate (a) varied with time be-
cause P/Ca varied and \/F was assigned values
according to those reported elsewhere (Strick-
land, 1960; Eppley, 1968; and Strickland et al,
1969). Populations in nutrient-rich water
under suboptimum light intensities, conditions
extant in February and March, contain larger
amounts of chlorophyll per unit carbon than
those in nutrient-poor water under brighter
light. Eppley (1968) found F values of about
30 for deep nutrient-rich water and 90 for shal-
low water depleted of nutrients. Values of \/F,
therefore, were assumed to be 0.04 in February
and March and 0.01 in June. The June value
is probably too low because the water still con-
tained ample nutrients (although lower than in
March) for vigorous growth, but was selected
to maximize the decrement afl^orded to decreas-
ing cell chlorophyll content and therefore min-
imize St in June.

Results of the calculations show (Table 3) that
changes in cell chlorophyll content could account
for only part of the decrease in chlorophyll con-
centration between March and June. The loss
coefficient ( b ) was computed for the period Feb-
ruary to March and assumed to remain constant
through June. The computed standing stock
{S,i) in June was 1096, about 80 times as high
as the observed value. (For comparison, stand-
ing stocks were also computed for X/F = 0.04
and \/F = 0.01, Table 3.) Since this (1096)
is the minimum that could be expected from a
loss of cell chlorophyll, grazing must have in-
creased during the period to further decrease
the chlorophyll concentration to its observed
level. A concomitant increase in zooplankton
corroborates this conclusion (discussed later).

605

FISHERY BULLETIN: VOL. 69, NO. 3

Table 3.— Computed standing stock (S,), expressed in units of chlorophyll,
for various cell chlorophyll to carbon ratios (l/F) during spring 1966 in
the mid-Subarctic Pacific Region.

l/F

P/C^

la

Feb. -Mar.
Mar.-June
Mar. -June
Mar.-June

11.2
19.3
19.3
19.3

50
80
80
80

S,

.04

.04-0)

.04

.01

7-15
15-20
15-20
15-20

0.433
0,472
0.701
0.398

20.422
0.422
0.422
0.422

19.3
21096.
29.3X10'°
228.0

ifl is the mean growth coefficient calculated by assuming that />/Ca varied linearly with time
as did ]/f in the second computation.

: e-l

: "0 +

where Aa= AP/C„ [(:/F)„ -|- 1/f • Al/F]

the initial and final values for the period.
2 Computed values.

A g
t

S .

= 1

AREAL AND SEASONAL DISTRIBUTION
OF NUTRIENTS

Nutrient concentrations were always higher
in Adak Bay and the Coastal Domain than in
the other areas and generally decreased toward
the south (Table 4, Figure 7). Average con-
centrations of nutrients in the Central Sub-
arctic water exceeded those in the Alaskan
Stream only in June 1967. In winter of 1967,
the nutrients were relatively high and varied
little throughout the cruise ai-ea. Low nutrient
concentrations at a few stations to the south
in September correspond to lower PR/Ca ratios.
The lowest average phosphate concentration in
the upper 50 m, 10 mg-at/m-, was in subtropical
water. Nitrate-nitrite was undetectable in the
upper 10 m at one station in area T-2 (lat 43° N)
and totaled only 12 mg-at/m- in the upper 50 m,
whereas the minimum silicate observed was 187
mg-at/m- at the same station. Apart from the
low nutrient values measured south of about lat
44° N in September and possibly in subtropical
water in Mai-ch, nutrients appeared to be in
sufficient abundance to support vigorous phyto-
plankton growth. Even for these areas of low
concentrations, productivity did not appear to
be severely limited, as evidenced by the Pr/C„
ratios, but was probably somewhat suppressed.

To obtain a seasonal pattern of changes, the
data on nutrients, like those on productivity,
were ti'eated as composite measurements from
the same year. The changes of mean nutrient
concentrations between lat 46° and 51°40' N
from season to season were not large. In mid-

(P/Ca)a ' Al/F and A is the difference between

winter all nutrients were relatively abundant,
as were phosphate and silicate in March. (Ni-
trate was not measured in March.) Phosphate
decreased between March and June 1966 from 78
to 56 mg-at/m-, the largest fractional change
measured during this study for any of the nu-
trients. In June 1967, nitrate and phosphate
concentrations were nearly equal to those in
winter, but concentrations of silicate were lower.
The apparent difference in the phosphate fluc-
tuations between the 2 years could be the result
of a shift in timing of the periods of high pri-
mary productivity, differences in supply by
circulation, or an overall net difference in the
balance between phosphate assimilation and
supply for the year. By August phosphate and
silicate had increased to quantities considerably
higher than those in winter, but in September
phosphate was lower and silicate was only slight-
ly higher than in winter.

The low nutrient concentrations to the south
in the summer lend support to the proposal by
Anderson (1969) that a trans- Pacific band of
chlorophyll occurs between the seasonal and
permanent pycnoclines in the summer. His
measurements indicate that the algae are pro-
duced in situ at these depths (50 to 75 m) which
receive less than 1 % of the light energj' at the
sea surface. This band lies between lat 35° and
45° N and is coincident with and could explain
the occurrence of a layer of maximum oxygen
content (Reid, 1962). Anderson also found that
nitrate in the surface mixed layer above the
chlorophyll band was nearly absent, having been
used up in the spring during high primary pro-
duction. A nitrate gradient through the deep

606

LARRANCE; PRIMARY PRODUCTION IN MID-SUBARCTIC REGION

Table 4. — Dissolved nitrate, phosphate, and silicate in
upper 50 m of mid-Subarctic Pacific Region (averaged
within upper zone oceanographic domains), 1966-68.

So: z ti

-It- UJ ^

Cruise no.
and area

Kl-66
Adak Bay
Alaskan Stream
Central Subarctic
Transitional
Subtropic
46*-5r40'

P2-66
Adak Bay
Alaskan Stream
Central Subarctic
Transitional
46='-5t»40'

K3-66
Adak Bay
Coastal

Central Subarctic
Transitional I
Transitional II
Subtropical
46''-51 "Afy

Kl-67
Alaskan Stream
Central Subarctic
Transitional
46 "-53 "53'

K5-67
Adak Bay
Coastal

Alaskan Stream
Central Subarctic
Transitional
46*-51''40'

K6-67

Alaskan Stream
Central Subarctic

K7-67

Adak Bay

Coastal

Central Subarctic

Transitional 1

Transitional II

46'-5r40'

K2-68
Alaskan Stream
Central Subarctic
Transitional

Nitrate
mg-at/m'^

Phosphoto
mg-at/m^

954

£83

492

64

76

S79

571
661
599
627

772
1,1(50
534
790
248
579

554

800

1,111
1,020
596
724
276
610

104.6
88.8
81.2
60.2
29.2
77.8

94.9
81.2
56.9
49.6
56.0

90.4
88.7
75.4
56.7
16.8
10.0
72.0

83.4
82.0
69.0
79.0

101.7
117.4
65.8
89.0
42.2
78.6

56.9

90.6

113.6
120.7
88.2
97.3
49.2
86.4

60.0
63.1
105.7

Silicate
mg-at/m^

2,849
1,990
1,903
1,195
512
1,754

2,871
1,978
1,491
1,155
1,480

2,499
2,331
1,692
1,143
280
335
1,597

1,594
1,665
1,314
1,561

2,192
2,806

811
1,704

588
1,247

942
2,026

3,012
2,666
1,854
1,883
792
1,725

868
1,022
1,415

chlorophyll maximum suggested that nitrate
diffused toward the surface from deeper water
was completely assimilated in the deep layer.
During the present study, chlorophyll maxima
were found at 50 m in June 1966 at lat 44° N and
at 100 m in September at lat 43° N. Nitrate was
not measured in June but it was undetectable in

ic

MARCH 1966

PHOSPHATE
--ft NITRATE
- - SILICATE

SEPTEMBER 1966
; T-2

---^-.,,-.i-.. "^'^ '- "^'2 AUGUST 1967

Figure 7. — Dissolved nitrate-nitrite, phosphate, and
silicate in the upper 50 m of the mid-Subarctic Pacific
Region, 1966-68.

607

FISHERY BULLETIN: VOL. 69, NO. 3

the upper 10 m at lat 43° N in September. The
deep chlorophyll layer at other stations could
easily have been missed because sampling below
the 1% light level was at standard depth.

PHOSPHATE CHANGES AND THEIR
RELATION TO PRIMARY PRODUCTION

An attempt was made to draw qualitative in-
ferences from phosjjhate data about the relative
levels of primary production between cruises to
obtain a somewhat more detailed picture of the
seasonal productivity pattern. The major fac-
tors generally affecting changes in dissolved
phosphate concentration in the oceans are: (1)
utilization by primary producers (P„), (2) re-
generation by zooplankton and bacteria (Pr) ,
and (3) advective changes (P„). The relation
among these factors is given by the formula:

Po

P„ + Pr + Pa,

where P,> is the net change of phosphate con-
centration with time, P„ is negative, Pr is posi-
tive, and Pa can be of either sign. Estimates
of Pu between cruises were calculated by apply-
ing a ratio of carbon to phosphorus (C:P) to
the carbon-14 data as discussed below, Pa was
estimated from calculations of vertical velocities
and phosphate concentrations measured at depth,
and Po was calculated from measurements of
phosphate concentrations; however, no adequate
estimate of Pr was possil)le. Two major assump-
tions were necessary to evaluate the above
parameters:

1. The uptake ratio of C:P = 40 by weight
(Strickland and Parsons, 1965) . This value re-
lates the C and P content of cells, but not the
amounts assimilated. It is applied here, how-
ever, to carbon-assimilation rates measured by
the carbon-14 method, which measures rates be-
tween net and gross production. The resulting
estimate of phosphorus uptake, therefore, will
be larger than the actual amount of phosphorus
retained in new cell material.

2. Phosphate concentrations and their in situ
changes were uniform within individual u])per-
zone domains. This assumjjtion permits us to
neglect the effect of horizontal advection.

Since nutrients were generally abundant in
the Subarctic Region and changes were small
during the year, circulation and regeneration
must have supplied dissolved nutrients to the
upper zone at rates sufficient to keep pace with
their utilization, despite high assimilation rates
by the algae during spring and summer. The
amounts of phosphate supplied to the upper 50 m
by upwelling were estimated from calculations
of monthly mean vertical velocities (Wickett,
1966, 1968)' and observed phosphate concen-
trations at 50 m (Table 5). Wickett listed
meridional components of Ekman and total
transport for alternate points on a grid of 5-
degree units of latitude and longitude. To ob-
tain the phosphate estimates, the average of
monthly mean vertical velocities for grid points
at lat 45° N, long 175° W and at lat 50° N, long
180° W were used as single monthly estimates
applicable to the Adak line of stations north of lat
45° N. To obtain the net amount of phosphate ex-
changed through the 50-m surface, the net verti-
cal displacement of water during each month
was multiplied by mean phosphate concentra-
tions at 50 m. The computed vertical velocities
refer to the bottom of the Ekman layer which
extends to the halocline at 100 m in winter but
is limited by the thermocline in summer to as
shallow as 30 m. The error incun-ed, however,
by applying the velocities to 50 m rather than
any other level was probably within the range
of precision of the estimated velocities.

Such estimates of vertical transport of phos-
phate must be considered minimal, because the
turbulent flux of properties across a surface
cannot be computed by using mean velocities.
That is, mean vertical velocities indicate net
upward flow, although water and its associated
jiroperties actually move up and down across
horizontal surfaces. When phosphate concen-
tration increases with depth (as it usually does) ,
the shallower water loses less phosphate by
downward flux than it gains by equivalent up-

' Wickett, W. P. 1966. Fofonoff transport com-
putations for the North Pacific Ocean, 1966. Fish. Res.
Board Can., Manuscr. Rep. Ser. (Oceanogr. Limnol.)
229, 92 p. (Processed.)

1968. Transport computations for the North Pacific
Ocean, 1967. Fi.sh. Res. Boanl Can., Tech. Rep. 53, 92 p.
(Processed.)

608

LARRANCE: PRIMARY PRODUCTION IN MID-SUBARCTIC REGION

Table 5. — Changes of dissolved phosphate in upper 50 m of mid-Subarctic
Pacific Region (attributable to vertical transport and assimilation by
phytoplankton) and their relation to measured concentrations (shown
in parentheses).

mg ?/m~ per day
(mg P/m-)

mg P/m2 per day
(mg P/m-)

mg P/m2 per doy
(mg P/m2)

Residual change

of P'

mg P/m2 per day

(mg P/m2)

1966

March-ear

ly June

-8.1
(-680)

1.0

(80)

-6.4 to -9.3
(-530 to -760)

-2.7 to 0
(-230 to 0)

Late June

-Sept.

5.4
(500)

1.5
(MO)

-5.5 to -8.4
(-500 to -770)

9.4 to 12.3

(860 to 1130)

1967

Feb.-June

0

(0)

2.7

(310)

-4.0 to -4.3
(-570 to —620)

1.3 to 1.6
(260 to 430)

July-Aug.

4.3
(240)

-1.7
(-100)

-4.9 to -6.2
(-280 to -350)

10.9 to 12,2
(620 to 690)

1 See text for definition.

ward motion; the net upward flux of phosphate,
therefore, is underestimated when mean vertical
velocities are applied.

Values of P,, for the periods between cruises
were estimated from productivity data. The
lesser values of the two productivity estimates
(Pk or Pr) from each of two succeeding cruises
were averaged, as were the greater values.
These averages represented the limits of the
range of mean productivity during the period
between cruises. For example, in the summer of
1966 (when in June, Pk = 238 and Pr = 426 mg
C/m^ per day, and in September, Pk = 2-50 and
Pr = 201 mg C/m- per day) , the range of mean
productivity during the period was from 220
(the average of 238 and 201) to 338 (the average
of 426 and 250) mg C/m^ per day. The limits
of the ranges were divided by the C:P ratio
(40) to obtain the daily rate of phosphorus up-
take in milligrams within a 1-m- cross-sectional
column of the euphotic zone (Table 5). This
rate was considered equivalent to the uptake in
the upper 50 m. No error was incurred by this
approximation when the euphotic zone was no
deeper than 50 m. The "residual changes" of P
were the changes unaccounted for by P„ and P„ ;
thus they included regeneration, other changes
not evaluated, and measurement errors:

residual change

Po — (Pa + P„).

Although the accuracy of these estimates was
low, the direction that Pa and P„ are likely to be
in error is known and the direction of error of the

residual changes can be deduced. As the absolute
values of Pa were minimal and those of P„ were
too large (and P„ was either positive or negative
and P„ was always negative) , the sum Pa + Pu
tended to be underestimated. The residual
changes, therefore, tended to be overestimated.

The residual changes during similar seasons
in the 2 years indicate similar trends (Table 5).
Negative values during spring 1966 show that
phosphorus assimilation, and hence primary
in-oductivity, must have averaged more than
that calculated, even if no regeneration occurred.
If phosphate regeneration is assumed to be
zero, the productivity during spring 1966 could
have been as much as 40 ''r higher than that
calculated to account for the changes in measured
phosphate. Although regeneration rates were
probably lower than in summer, some regener-
ation probably occurred, and therefore the re-
sidual change would have been greater and the
productivity even higher. Clearly, spring phy-
toplankton production in 1966 must have been
substantially greater than the measured pro-
ductivities.

Larger residual changes in the summer in-
dicate higher phosphate regeneration rates than
in spring. Phosphate turnover times ranging
from about one to several months have been re-
ported (Ketchum, 1962). According to Ketch-
um, excretion by zooplankton accounts for large
portions of regenerated phosphate as well as in-
organic niti'ogenous compounds. The residual
changes were correlated with zooplankton

609

FISHERY BULLETIN: VOL. 69, NO. 3

biomass in the Subarctic Region, which was
roughly three times higher in summer than in
February or March (Donald S. Day, unpublished
data) .' If phosphate regeneration accounted for
all the residual changes in summer, 45 to 50 ""f of
the phosphate in the water would be renewed by
regeneration in 3 months. In contrast, the
upwelled phosphate supplied only about 6'^f of
the total concentration in summer of 1966 and
phosphate was lost from the upper layers in 1967
by mean velocities downward. According to the
computed values (Table 4) , however, in the sum-
mer the residual change of phosphate was
roughly twice that removed from the water by
plants. If the residual change is assumed to
be mostly due to regeneration, therefore, the
zooplankton would have had to release twice as
much phosphorus as was taken up by the algae
during the same period. A more likely expla-
nation is that more phosphate was supplied from
below than is indicated by the P,, values and the
consequent residual changes would be less. In
either case, in situ regeneration by zooplankton
appears to be a major source of nutrients sup-
plied throughout the summer in the mid-Sub-
arctic Pacific Region.

At Ocean Station "P" primary productivity
accounted for the entire loss of phosphate be-
tween March and August (Parsons, 1965),° sug-
gesting that regeneration was negligible. But,
since zooplankton at Station "P" was sufficiently
abundant to graze the phytoplankton to a stable
level (McAllister, Parsons, and Strickland,
1960), it would seem that some phosphate re-
generation should have occurred.

RELATION OF ZOOPLANKTON

BIOMASS TO CHLOROPHYLL AND

PRIMARY PRODUCTION

Data on zooplankton abundance and chloro-
phyll were compared to determine if these two

' Donald S. Day, Oceanographer, Natl. Mar. Fish.
Serv. Biol. Lab., Seattle, Wash.

" Parsons, T. R. 1965. A general description of some
factors governing primary production in the Strait of
Georgia, Hecate Strait and Queen Charlotte Sound,
and the N.E. Pacific Ocean. Fish. Res. Board Can.,
Manuscr. Rep. Ser. (Oceanogr. Limnol.) 193, 34 p.
(Processed.)

variables were correlated. The smaller zoo-
plankters were sampled by raising a y^-m NOR-
PAC net (mesh opening 0.33 mm) vertically
from 150-m depth to the surface at about 1 m/sec.
Displacement volumes of the catches weighted
for distance between stations were averaged be-
tween lat 46° N and 51°40' N for each cruise.
The mean volumes in February and March were
about 0.070 ml/m'' of water strained and ranged
from about 0.250 to 0.280 ml /m^ in summer,
except in August 1967 when the mean volume
was 0.550 ml/m^ (Day, see footnote 8). Thus,
the zooplankton standing stock increased to about
four times its winter level sometime after the
phytoplankton increase in March. Grazing by
the zooplankton apparently occurred early
enough to crop down the algae, thereby limiting
])rimary productivity before it reached suffi-
ciently high levels to deplete the nutrients from
the upper layers. A relatively steady state of
grazing pressure and phytoplankton standing
stock seemed to hold during the summer (at least
in summer 1966). These findings agi-ee with
the conclusion of McAllister et al. (1960) that
zooplankton grazing limited primary production
at Ocean Station "P" by maintaining the phyto-
plankton standing stock at relatively low con-
centrations.

The relation between zooplankton displace-
ment volumes and chlorophyll a concentrations
(Figure 8) shows a negative correlation, further
corroborating the above conclusion. The regres-
sion of chlorophyll a on zooplankton includes only
those stations north of lat 46° N, except in coastal
water and Adak Bay, and excludes all winter
data. As shown previously the nearshore and
transition waters exhibit chemical and biological
features, which indicate ecological areas some-
what distinct from the area between. The winter
data were also excluded from the regression be-
cause productivity was limited by insufficient
light. Chlorophyll a concentrations south of lat
46° N showed no apparent relation to the amount
of zooplankton present. Chloi-ophyll in Adak
Bay and coastal waters was always significantly
higher than estimated from the regression, ex-
cept in March in Adak Bay. All of the high
chlorophyll values were near shore and associ-
ated with intermediate quantities of zooplankton.

610

LARRANCE: PRIMARY PRODUCTION IN MID-SUBARCTIC REGION

.

• C-SW.AI St.T-l

210

-

K Adok Boy, Coastal
4 South of 46" N
D Winter doto, 1967

110

.

.

R

70

-

"e

ESO

- \

E
O

\

= 50

• N,

\

UJ

Q.

O.
3

•\

A

Z40

* \

ol

V •

\

\.

*

_J

\

\

_)

\

ix

. \ o

'

X • \

(L

"=\

\ \

\ •

T

^'A „\

\

>^ •

\ .

<J 20

&

a

\

V- \

N

10

1

\

'o 100 200 300 400 500 600 700

ZOOPLANKTON (ml/IOOOm^)

Figure 8. — Relation of chlorophyll a to net zooplankton
in the upper 150 m of the Subarctic Pacific Region,
1966-68. Dashed lines represent 95% confidence limits.

The zooplankton value at the only nearshore
station (Adak Bay) in March was the lowest
observed. These data suggest that the zooplank-
ton increase occurred later in the spring in
coastal areas than farther offshore, a condition
which could have permitted the phytoplankton
bloom to reach much higher levels near shore
before being controlled by grazing.

ANNUAL PRIMARY PRODUCTION

The annual primary production between lat
46° and 51°40' N was estimated from values of
Pk, Pr, and Pm. The data from all cruises were
combined into a single composite year for ap-
portioning productivity to time periods. The
lowest estimate was for Pk (72 g C/m- per year) ;
Pm and Pr were somewhat higher (82 and 85 g
C/m- per year). If the estimate of primary
productivity from phosphate changes is correct,

annual productivity could be as high as 100 g
C/m^. These estimates are considerably higher
than those reported by McAllister (1969), mod-
erately higher than those of Koblents-Mishke
(1965), and lower than those of Anderson (in
press).

No reason is apparent from the quantitative
data for the difference between annual produc-
tivity at station "P" (48 g C/m^ per day; Mc-
Allister, 1969) and that in the mid-Subarctic
Region. If zooplankton is the main factor lim-
iting productivity, more zooplankton and less
chlorophyll should be expected at station "P"
than south of the Aleutians; however, zooplank-
ton density was lower and chlorophyll a concen-
trations were about the same or slightly higher
at station "P." More detailed seasonal obser-
vations from the mid-Subarctic, as well as a
comparison of plankton communities in the two
locations, will probably be necessary to explain
the observed differences in annual productivity.

CONCLUSION

The main conclusions drawn from the primary
productivity and related data are listed below:

1. No significant differences in primary pro-
ductivity were found consistently among the var-
ious oceanographic domains or other waters of
the Subarctic Pacific Region except that Adak
Bay and the Coastal Domain south of Adak
Island were generally more productive than
areas farther south.

2. The annual cycle of productivity is typical
for temperate oceans: productivity is low in win-
ter, increases in the spring until more or less of
a bloom develops, and declines by summer to rel-
atively steady intermediate levels. Productivity
in autumn and early winter was not studied.

3. Light limits productivity during winter;
less light penetrates the surface than during
other seasons, and the greater thickness of the
mixed layer in the upper zone further reduces
the light available to the algae.

4. During spring and summer, nutrients and
light are plentiful, but zooplankton appears to
graze the standing stock of phytoplankton to
relatively low levels — thereby limiting produc-
tivity of phytoplankton.

611

FISHERY BULLETIN: VOL. 69, NO. 3

5. The main mechanisms of dissolved-phos-
phate supply in the upper 50 m of water during
summer are in situ regeneration by zooplankton
and upwelling. Regeneration supplies signifi-
cant amounts of phosphate (perhaps more than
is provided by upwelling) in the summer, but in-
creased turbulence and upwelling in winter
maintain high levels of nutrients throughout the
upper 100 m of water.

6. The seasonal cycle and factors limiting pro-
ductivity are similar to those at station "P" (lat
50° N, long 145° W), but some significant dif-
ferences exist. Productivity in the study area
is nearly twice that at station "P," and zooplank-
ton biomass is also much greater. The change
in measured phosphate concentrations at station
"P" over the productive season can be accounted
for by phosphate utilized by the algae and by
phosphate supplied by upwelling. South of the
Aleutian Islands, however, phosphate regener-
ated in situ must be invoked to balance the phos-
phate budget.

7. Annual primary production in the area
studied is about 80 to 100 g C/m^.

ACKNOWLEDGMENTS

I am especially indebted to Thomas Elwel! and
Frederick Galassi for their technical assistance,
particularly for their efforts at sea. I thank
Dr. F. A. Richards for volunteering the services
of chemists at the Department of Oceanography,
University of Washington, to analyze the nitrate-
nitrite samples. I wish also to express my appre-
ciation to Dr. G. C. Anderson and Dr. Karl Banse,
Deinirtment of Oceanography, University of
Washington, for their many helpful criticisms
of the manuscript.

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1965. A manual of sea water analysis. 2d ed.,
revised. Fish. Res. Board Can., Bull. 125, 203 p.
TULLY, J. P.

1964. Oceanographic regions and assessment of
temperature structure in the seasonal zone of the
North Pacific Ocean. J. Fish. Res. Board Can. 21:
941-970.

Wang, C. H., and D. L. Willis.

1965. Radiotracer methodology in biological science.
Prentice-Hall, Englewood Cliffs, N.J., 382 p.

Wood, E. D., F. A. J. Armstrong, and F. A. Richards.
1967. Determination of nitrate in sea water by
cadmium-copper reduction to nitrite. J. Mar.
Biol. Assoc. U.K. 47: 23-31.
Yentsch, C. S., and D. W. Menzel.

1963. A method for the determination of phyto-
plankton chlorophyll and phaeophytin by fluo-
rescence. Deep-Sea Res. Oceanogr. Abstr. 10:
221-231.

613

lago, A NEW GENUS OF CARCHARHINID SHARKS, WITH
A REDESCRIPTION OF /. omanensis

Leonard J. V. Compagno' and Stewart Springer"

ABSTRACT

A new genus, lago, is proposed for Eugaleiis omanensis Norman, 1939. /. omanensis, originally de-
scribed from a single specimen, is redescribed from 16 additional specimens from the northern Arabian Sea
continental shelf and slope between the Gulf of Oman and the Gulf of Kutch. Its presence in areas
of low oxygen and the possibility of its occurrence in deeper waters of the Red Sea are discussed.

Norman (1939) described Eugaleus omanensis
from a 280-mm female specimen, taken at 210-m
depth in the Gulf of Oman. He placed it in
Eugaleus Gill, 1864 ( = Galeorhinus Blainville,
1816) with reservations because omanensis dif-
fered from all other species of Eugaleus in den-
tition and absence of a pronounced ventral
caudal lobe. Norman noted that omanensis did
not fit Hemigaleus Bleeker, 1852 because of den-
tition differences and lack of precaudal pits but
he declined to establish a new genus for it.

Fowler (1941) overlooked Eugaleus omanen-
sis in his review of Indo-Pacific elasmobranchs
but later (1956) gave a description of the species
condensed from Norman's account and allocated
it to the genus Galeorhinus. Misra (1949) had
earlier placed it in the same genus but this was
not mentioned by Fowler.

Smith (1957) revised Galeorhinus but also
overlooked G. o?nanensfs. Compagno (1970) re-
viewed the systematics of Hemitriakis, Galeo7'-
hinus, and related genera. He considered G.
omanensis generically distinct from Galeorhinus
but did not propose a new genus in deference
to this paper.

During the International Indian Ocean Expe-
dition (IIOE) in 1963, the RV Anton Bruun on
Cruise 4B conducted 109 trawling stations in
ti'ansects along the continental shelf of the Arab-
ian Sea between Bombay and the Gulf of Oman
at depths from 15 to 375 m (Woods Hole Ocean-

' Stanford University, Stanford, Calif. 94305.
" National Marine Fisheries Service, National Center
for Systematics, Washington, D.G. 20560.

Manuscript accepted February 1971.
FISHERY BULLETIN: VOL, 69, NO.

ographic Institution, 1965). Sixteen specimens
of a small carcharhinid were included in these
collections and sent to us through the Smith-
sonian Oceanographic Sorting Center. They
were tentatively identified by us as Galeorhinus
omanensis (Norman).

Marshall and Bourne (1964, 1967), in photo-
graphic surveys of benthic fishes, collected 30
photographs of a small carcarhinoid shark
(about 2 ft long) at depths between 1115 and
2195 m in the Red Sea. They noted that their
shark might be either a triakid or a carcharhinid
but was not identifiable to genus or species. Com-
parison of Marshall and Bourne's photographs
and sketch of their "mystery shark" with our
specimens and Norman's account of G. omanen-
sis led us to suspect that the "mystery shark"
might be omanensis.

We then sent two specimens of the IIOE series
to Dr. N. B. Marshall at the British Museum
( Natural History) . At our request he compared
them with the holotype, the hitherto only known
specimen of Galeorhirms omanensis, and con-
firmed our identification of the IIOE specimens.
He also agreed that the IIOE omanensis are very
similar to the Red Sea "mystery shark" of the
photographs, but noted that final identification
of the Red Sea species must await capture of
specimens.

Differences between "Galeorhinus" omanensis
and members of Galeorhinus, Hypogaleus, Hem-
itriakis, and all other carcharhinid genera war-
rant the erection of a new genus for "Galeor-
hinus" omanensis.

615

FISHERY BULLETIN: VOL. 69, NO. 3

\-

Figure 1. — lago omanensis, from a 565-mm female deposited in U.S. National Museum. Drawing by Mildred

H. Carrington.

lago GENUS NOVUM

Eiigaleus omanensis NORMAN, 1939,
TYPE-SPECIES

Etymology

This shark, a namesake of the villain of
Shakespeare's Othello, is a troublemaker for
systematists and hence a kind of villain.

Diagnosis (Terminology Follows Compagno,
1970)

lago (Figure 1) differs from most carchar-
hinoids in the extremely anterior origin of its
first dorsal fin. Only Isogomphodon oxyrhyn-
chus, a few species of Carcharinus, and the
sphyrnid Eusphyra blochii rival lago in this
respect.

lago is morphologically intermediate bet\veen
the families Triakidae and Carcharhinidae as
defined by Bigelow and Schroeder (1948) and
Garrick and Schultz (1963). The characters
of lago strengthen the evidence presented by
Compagno (1970) against separation of these
families on simple nictitating lower eyelid and
dental characters advocated by these writers.

We follow Compagno in uniting, at least provis-
ionally, the two families. lago thus falls into
the family Carcharhinidae (sensu lato).

lago is far from the advanced and intermediate
carcharhinid genera discussed by Compagno
(1970). These genera include Hemigaleus,
Hemipristis, Galeocerdo, Scoliodon, Rhizoprioiv-
odon, Loxodon, Negaprion, Triaenodon. Lamiop-
sis, Isogomphodon, Carcharhinus, Hypoprion,
and Aprionodon. lago differs from all of these
in having a transitional, not internal, nictitating
lower eyelid with edge nearly horizontal; shal-
low subocular pouch; teeth with strong basal
ledges and grooves; teeth at symphysis only
slightly smaller than adjacent ones; no precau-
dal pits; pectoral fin skeleton projecting less than
halfway into fin ; distal pectoral radials only as
long as proximals, with parallel edges and trun-
cate tips (not tapered and acute); caudal fin
without projecting ventral lobe and lateral un-
dulations of its dorsal margin in adults; cran-
ium with a complete supraorbital crest (absent in
advanced forms); and a spiral, not scroll, in-
testinal valve (Hemigalejis and Hemipristis are
exceptional in also having spiral valves).

lago differs from Galeorhinns and HypogaJeus
as delimited by Compagno (1970) in having a
transitional rather than internal nictitating low-

616

COMPAGNO and SPRINGER: NEW GEN'LS OF CARCHARHINID SHARKS

er eyelid in adults, with nearly horizontal edge;
anterior nasal flap not greatly reduced; teeth
without postlateral cusplets; an interdorsal
ridge present; lateral trunk denticles much long-
er than wide in adults (about as long as wide
in Hypogaleus and Galeorhinus) ; and no ventral
lobe on caudals of adults.

From the curious Le.pfocharias, logo differs
in having a transitional rather than internal
nictitating lower eyelid in adults; much larger
spiracles; no nasal barbel; very weak gynandric
heterodonty; teeth with primary cusps oblique,
not erect, and lacking cusplets; sharp-edged,
bladelike cutting teeth; fewer total vertebrae,
130 to 147 (198 to 214 in Leptocharias) ; spiral
intestinal valve with about 5 turns (14 to 16 in
Leptocharias) ; and an entire supraorbital crest
(reduced in Leptocharias to isolated preorbital
and postorbital processes) .

lago can be distinguished from Hemitriakis,
Furgaleus, Scylliogalens, the Triakis-Miistelns
complex, Proscyllium, and Eridac^us by its more
lateral eyes, in dorsal view nearly touching head
rim, and its sharp-edged, monocuspidate teeth.
In addition, lago differs from He>nitriakis in
having a transitional rather than external nic-
titating lower eyelid, noncarinate posterior teeth,
more tooth rows (only 18 to 36/29 to 34 in
Hemitriakis) , weak transverse notches on teeth,
and no ventral caudal lobe. lago lacks the short,
thick, rounded snout, nasoral grooves, and molar-
iform teeth of Scylliogalens and also has fewer
tooth rows and series of teeth functional. Un-
like Furgaleus, lago lacks nasal barbels, erect
cusps on its lower anterolateral teeth, and a
ventral caudal lobe; also, lago (Figure 2) has
the nostrils definitely closer to the mouth than
the snout tip (about equidistant in Furgaleus) .
lago differs from most members of the Triakis-
Mustelus complex in having fewer tooth rows and
series of teeth functional; however, Triakis sem-
ifasciata rivals lago in these respects. lago does
not have a pavement of molariform teeth as in
Mustelus; also, its pelvic anterior margins are
less than half the length of pectoral anterior
margins (over half as long in Triakis-Mustelus) .
Finally lago contrasts with Proscyllium and
Eridacnis by its transitional, not rudimentary,
nictitating lower eyelid; monocuspidate poster-

FiGURE 2, — lago omnnensis. A. Ventral side of head.
B. Dor.sal side of head.

ior teeth (not comblike) ; dorsal fin base mid-
point closer to pectoral base termination than
pelvic origins (vice-versa in Proscyllium and
Eridacnis) ; second dorsal origin anterior (not
over or posterior) to anal fin origin; interme-
dialia of vertebral centra strong wedges (not
wedgelike in Proscyllium and Eridacnis) ; large
papillae absent from gill arches and buccal cavi-
ty; and nostrils farther apart. lago also lacks
the clasper hooks, scyliorhinoid color pattern, and
apparently the oviparous reproduction of Pros-
cyllium.

GENERIC DESCRIPTION

Head flattened, its length from snout tip to
fifth gill opening about i/i. total length.

Eye openings dorso-lateral, not visible in
ventral view of head, openings elongate, about
twice as long as high, with a well-developed
posterior notch ; nictitating lower eyelid trans-
itional (Figure 3B), its edge nearly hoi'izontal;
secondary lower eyelid strongly differentiated,
its edge thin; subocular jjouch shallow, its lateral
surface bare of denticles.

Slitlike spiracles, length about J'- eye length,
located about -- eye length behind and slightly
below posterior eye notch; external gill slits mod-
erately short, lengths in adults nearly equal, the
longest 1,4 to % eye length; nostrils located
about one-half as far from mouth as from snout
tip, well separated, without nasoral grooves,
widths about 1% to 2 times internarial dis-
tance, anterior nasal flap a short truncate lobe.

617

FISHERY BULLETIN: VOL, 69, NO. 3

Mouth opening subtriangular, broad, 2 to 214
times as wide as long ; labial furrows extending
around mouth corners, the upper furrows longer,
extending anteriorly only to below eye pupils;
large papillae absent from buccal cavity.

Teeth small (Figures 3A and 4), largest with
greatest width at root about 1.5 mm in 457-mm
female; tooth rows 46 to 55/37 to 45; 2 to 3
series functional along edges of jaws; teeth
in mixed alternate and imbricate overlap pattern
of Strasburg (1963); no serrations; premedial
edge of crown in anteroposteriors convex, post-
lateral edge deeply notched forming a low post-
lateral blade on crown foot; all teeth with a
strong basal ledge and groove, transverse ridges
on crown foot; roots low, deep, with transverse

Figure 3. — lago omanensis. A. Typical teeth: upper,
buccal surface ; lower, labial surface. B. Eye. C. Cross
section of trunk vertebra; thoroughly calcified areas
shown in black. D. Valvular intestine, one side cut away.
Drawing by L. J. V. Compagno.

groove on attachment surface but transverse
notch weak; teeth not noticeably protruding
when mouth is closed.

Dignathic heterodonty very weak, with upper
anteroposteriors having slightly higher crowns
than lower ones; disjunct monognathic heter-
odonty indicated by differentiation of medials
in one row on upper jaw and about 3 in lower;
medials smaller, with erect primary cusps, large
premedial and postlateral blades, and no cusi^Iets;
larger anteroposteriors are sharji-edged, com-
pressed, bladelike cutting teeth witli an oblique

Figure 4. — lago omanensis. Teeth of right side of upper
and lower jaws; labial aspect. Dotted lines indicate
jaw symphysis.

primary cusp and no cusplets; anteroposteriors
show moderate gradient monogrnathic hetero-
donty, with teeth becoming smaller, more
oblique-cusped, and lower-crowned towards ends
of dental band ; posteriormost teeth with strong
primary cusps; ontogenic heterodonty not known
at present; gj'nandric heterodonty indicated
only by slightly more erect cusp tips on antero-
posteriors of adult males.

Trunk not markedly compressed, less than
twice as high as wide, subtriangular in cross
section; a low interdorsal ridge present; lateral
dermal keels and precaudal pits absent from
caudal peduncle.

Dermal denticles of trunk below first dorsal
longer than wide, crown with a high, narrow
ridge extending to tip of posteriorly directed
cusp; a pair of lateral ridges weakly developed
or absent, lateral cusps weak or absent.

Pectoral fins larger than first dorsal fin in
area, their anterior margins about 11,4 times as
long as combined base and inner margin lengths;
distal tip of adpressed pectoral about over its
free rear tip when pectoral inner margin is held
parallel to body axis; origin of pectoral below
or slightly in advance of fourth gill opening;
pectoral skeleton projecting less than halfway
into fin, its longest distal radials about equal
in length to corresponding proximal ones; distal
radials with truncate tips and parallel edges.

Pelvic anterior margins less than half length
of pectoral anterior margins; pelvic bases equi-
distant between first and second dorsal bases.

Claspers with pseudoperae, pseudosiphons,
cover rhipidia, true rhipidia, and exorhipidia
(Figures 5B and 5C) ; siphon sacs large, extend-
ing anteriorly to level of pectoral free rear tips
(Figure 5A); margins of clasper cartilage
rolled, with margins overlapping to form a tube;
clasper hooks absent.

618

COMPAGNO and SPRINGER: NEW GENL'S OF CARCHARHINID SHARKS

Origin of first dorsal fin far forward, varying
in position from above fourth gill opening to
slightly before pectoral axilla; midpoint of first
dorsal base much closer to pectoral axilla than
to pelvic origins; free rear tip of first dorsal
anterior to pelvic fin origins.

Second dorsal nearly as large as first, its height
about 70 '"r of first dorsal height; its posterior
margin strongly concave.

Anal smaller than second dorsal, slightly more
than half its height, its base about % of second
dorsal base length; its posterior margin nearly
straight or shallowly concave; its origin poster-
ior to second dorsal origin by about i/-) to \A of
second dorsal base length; posterior ends of sec-
ond dorsal and anal bases opposite.

Caudal without projecting ventral lobe-tip in
adults, preventral margin slightly more than I/3
of dorsal margin length; subterminal margin
long, over half length of terminal margin ; cau-
dal dorsal margin length about i/o of total
length; terminal sector of caudal about 1/3 of
dorsal margin length; vertebral axis of caudal
only slightly raised above body axis.

Figure 5. — lago omanensis. A. Ventral aspect of trunk
of mature male to show size and position of clasper
siphons. B. Dorsal surface of left clasper. C. Partially
expanded tip of left clasper. AP, apopyle ; C, connection
between rhipidion and cover rhipidion; CR, cover rhipi-
dion; EG, epirhipidial groove; ER, exorhipidion; HP,
hypopyle; P-2, pelvic fin; ESA, pseudoperal aperture;
ESP, pseudopera; PSP, pseudosiphon pouch; R, rhipi-
dion; S, siphon sac; SG, subrhipidial groove.

Vertebrae moderately numerous, 129 to 147
in total count {N = 16). Monospondylous pre-
caudal (MP) centra 24.5 to 27.6 ^r of total count;
diplospondylous precaudal (DP) centra 33.6 to
36.1; and diplospondylous caudal (DC) centra
37.2 to 40.1 (N =8). A ratios 120 to 162, B
ratios 102 to 137 (N = 11 ) . DP and DC centra
more numerous than MP centra and nearly equal
to each other, DP MP ratio 1.22 to 1.46 and
DC/MP ratio 1.38 to 1.63 (/V = 8). Transition
between MP and DP centra easily delimited on
radiographs, over pelvic region. Posteriormost
MP centra not greatly hypertrophied. DP cen-
tra of relatively uniform length throughout, not
forming a stutter zone of alternating long and
short centra.

Vertebral calcification pattern a modified ver-
sion of White's (1937) "Maltese cross" pattern,
without diagonal calcified lamellae; notochordal
canal unusually large (Figure 3C); wedgelike
intermedialia strongly developed.

Supraorbital crest of cranium strongly devel-
oped and entire.

Intestinal valve of spiral type, with about five
turns.

lago is apparently livebearing (see section in
Reproduction below) , but whether or not a yolk-
sac placenta is formed cannot be determined
from available specimens.

lago omanensis (NORMAN, 1939)

Eugaleus omanensis Norman, 1939, p. 11, Fig.
3 (type-locality. Gulf of Oman); Compagno,
1970 (generic systematics) .

Galeorhinus omanensis Misra, 1949, p. 21 (in
list of Indian elasmobranchs, name only) ; Fowl-
er, 1956, p. 17 (description, after Norman);
1967, p. 363 (in list of fishes of the world, name
only).

MATERIAL

Seven males, 224 to 365 mm; nine females,
358 to 582 mm (Table 1); holotype, British
Museum (Natural History) Reg. No. 1939.5.24.9,
a 280-mm female from Gulf of Oman. Speci-

619

FISHERY BULLETIN': VOL. 69, NO. 3

Table 1. — Oceanographic data for lago omanensis from Final Cruise Report, Anton Bruun Cruise 4B, Woods Hole

Oceanographic Institution (1965).

Lenglh
specimen

Sex

IIOE
station
number

Dale

Lot
N

Long
E

Bottom
temperotura

Oa at
bottom

Depth

mm

' C

ml/liter

m

312

<i

227A

11/19/63

22°38'

67°11'

22.39

0.77

no

224

e

231A

1 1 /20/63

23

13'

66°40'

19.89

0.24

183-155

457

9

255A

11/30/63

2i

SO-

57°07'

24.47

2.40

92-95

427

9

255A

11/30/63

25

SO'

57°07'

24.47

2.40

92-95

440

9

264A

12/02/63

25

02'

56"'52'

20.02

0.60

291-272

480

9

264A

12/02/63

25

02'

56° 52'

20.02

060

291-272

472

9

264A

12/02/63

25

02'

56°52'

20.02

060

291-272

343

d

264A

12/02/63

25

02'

56"52'

20.02

0 60

291-272

358

9

268A

12/03/63

24

12'

57=26'

16.24

0.28

364-368

565

9

26BA

12/03/63

24

12'

57°26'

16.24

0.28

364-368

582

9

268A

12/03/63

24

12'

57«26'

16.24

0 28

364-368

335

<f

268A

12/03/63

24

12'

57°26'

16.24

0.28

364-368

3<U

rf

268A

12/03/63

24

12'

57»26'

16.24

0,23

364-368

395

9

279B

12/09/63

24

13'

65°52'

19.34

022

170-192

304

rf

2798

12/09/63

24-

13'

65°52'

19.34

0.22

170-192

295

e

2798

12/09/63

24°

13'

65-52'

19.34

0.22

170-192

mens are deposited in the collections of the U.S.
National Museum, California Academy of Sci-
ences, and the British Museum (Natural His-
tory) .

DESCRIPTION

Proportional dimensions as percentages of
total length are given for our 16 specimens in
Table 2.

In lateral view head outline slightly convex
dorsally and ventrally, its outline tapering
smoothly to snout tip; outline of head in dorsal
view parabolic in shape, the sides converging
at a narrow angle from gill openings to nostrils
but then converging at a much wider angle to
snout tip; head broad, width at spiracles about
half its length; interocular slightly less than
width of head at eyes; head subquadrate in
transverse section at eye pupils.

Snout tip narrowly rounded in dorsal view,
bluntly pointed in lateral view; preoral length
1.1 to 1.4 in mouth width.

Eye length equal to or slightly longer than
distance between nasal apertures; eye openings
subelliptical, rounded anteriorly.

Nictitating lower eyelid (NLE) a variety of
Compagno's (1970) transitional type, interme-
diate in form between "nictitating folds" and
"nictitating membranes" of authors (Figure
2B); its anterior edge smoothly confluent with

edge of upper eyelid ; secondary lower eyelid
( SLE ) originating beneath origin of NLE ; post-
eriorly NLE merges with SLE and continues as
single edge to notch; subocular pouch or pocket
between NLE and SLE extends beneath anterior
two-thirds of eye; SLE edge sharp and thin with
NLE is artificially raised to the limits of its
travel; dermal denticles present on outer face
of NLE. The structure and the kinetics of the
NLE in [a(jo omanensis suggest that it cannot
cover the potserior third of the eye when raised
as it can in adults of Galeorhinus and higher
carcharhinoids.

Spiracles open below level of posterior eye
notch and are posterior to eye by distance about
equal to their own length.

Gill openings increasing in size from first to
third by small increments, with fourth slightly
shorter than third and fifth about half length of
fourth, becoming more dorsally situated from
anterior to posterior, with upper origin of first
opposite midpoint of fifth. Definite gill rakers
not developed, but small dermal mounds are
jn-esent on gill arches.

Nostrils relatively large, their openings
obliquely directed anterolaterad; anterior nasal
flap varying from subtriangular to lobate; a
small inner nasal flap present dorsal to anterior
nasal flap and concealed by it; posterior nasal
margin with an elongated process (.stiffened by
ala nasalis) that projects obliquely dorsomedially
into nasal cavity.

620

COMPAGNO and SPRINGER; NEW GENUS OF CARCHARHINID SHARKS

Table 2. — Proportional measurements of lago omanensis expressed as percentages of
total lengths; measurement method follows Bigelow and Schroeder (1948).

Mala

Range in

Female

Range in

335 mm

7 males

565 mm

9 females

Tip of snout to:

Front of mouth

7.2

6.1-7,6

5.8

5.7-6.4

First gill opening

19.1

17.4.20,0

16.8

16.2-17.8

Lost gill opening

24.2

24,2-27,5

23.4

23,0-24,5

Origin pectoral fin

23.3

23,3-25,9

22.7

21,2-23,5

Origin first dorsal fin

25.9

25,3-29,5

24.8

24,0-27,1

Origin pelvic fins

42.8

41,6-45,9

43,9

42,7-46,5

Origin second dorsal fin

56.8

56,8-60,6

58.4

57,8-59,9

Origin anal fin

58.3

58,3-63.4

59,2

59,2-63,3

Anus

44.7

43.5-49,1

45,1

44,5^7.4

Distance between fin base:

First and second dorsals

23.5

21.4-25,3

24,2

21,9-24,6

Pectoral and pelvic

16.1

13,7-16,1

18.6

16,8-20,0

Pelvic and anal

ll.O

11.0-12,3

n.5

11,0-13,2

Anal and lower caudal

8.9

7.2-10,5

8.5

7.5-9.7

Length eye opening

5.1

4,2-5.1

4.1

3.3-4.1

Least internasat distonce

4.0

3.6^.2

3.7

3.3-3.9

vVidth mouth

7.2

7,7-9,4

7.1

6,4-8.4

Length upper labial furrow

1.5

1 ,5-2.0

1.2

1.1-1,2

Length lower labial furrow

09

0.8-1,4

0,9

0,6-1.1

Diameter spiracle

0.6

0,4-0.8

05

0.2-0,6

Distance, spiracle to eye

0.7

'0.7-1.1

1.1

'0.7-1.2

Fin measurements:

Base first dorsal

8.9

8,9-11,2

9,4

8.3-11.6

Height first dorsal

6.0

6,0-7,8

7,8

7.0-8.8

Base second dorsal

8.9

8,0-9.7

7.3

7.3-9.1

Height second dorsal

4,8

4,5-6,1

5.5

5.2-6.5

Base anal

6,0

5,5-6,6

5,3

4,9-6.4

Height anal

3.0

2,6-3,4

3,5

2,8-4.0

Width pectoral base

4.8

4.7-5.6

4.8

4,5-5,6

Anterior margin pectoral

14.3

12,7-14,3

15,3

13,4-16,6

Overall length pelvics

8.6

18.3-9.9

9.6

'8,5-9,6

Upper margin caudal

22.4

20,1-22,4

21,9

20,8.22,7

' In 4 moles or 6 females.

Mouth width about two-thirds of width of
head at mouth corners; edge of lower jaw
convex.

Teeth show modest gradient heterodonty;
from symphysis to mouth corner teeth become
lower relative to their root lengths; tooth size
changes also along this gradient, starting from
small to largest in about four rows from medials
and gradually becoming smaller towards ends
of dental band.

Body moderately slender, trunk rather high
anteriorly, almost humped above pectorals,
sloping posteriorly to pelvics and caudal origins;
caudal peduncle long, slender, subquadrate in
cross section, a weak postdorsal ridge extending
medially from just after second dorsal to caudal
origin; an ill-defined predorsal ridge extending
for a shoi't distance anterior to first dorsal fin;
distance from snout tip to cloaca somewhat less
than distance from cloaca to caudal tip.

Dermal denticles small, those of dorsal sur-
face below first dorsal fin base 0.04 to 0.08%
of total length in two specimens, 0.15 to 0.35 mm
in 457-mm female; anterior edges and posterior
cusps of adjacent denticles somewhat overlap-
ping, skin visible between denticles; denticles
transparent, without pigment and more or less
invisible when wet; chromatophores of skin be-
tween denticle bases visible through denticles;
bases of denticles short, subquadrate, with rel-
atively short pedicels; medial ridge of crown
not subdivided longitudinally (Figure 6) ; con-
cave depression present on either side of medial
ridge, with its lateral boundary deflected slightly
outward to form an incipient lateral ridge that
may or may not terminate in a short lateral cusp;
lateral cusps generally absent from denticles of
caudal and ventral surfaces ; denticles below first
dorsal becoming wider relative to their lengths
with increase in specimen size; small denticles

621

FISHERY BULLETIN: VOL. 69, NO. 3

Figure 6. — lago omanensis. Dermal denticles from side
of trunk below first dorsal fin, 582-mm female, scanning
electron microscope photomicrograph, scale line at lower
left equals 100 ^.

(less than 0.1 mm long) present on anterior part
of palate and inner surfaces of branchial arches,
also irregularly and rather sparsely scattered
on tongue.

Pectoral fins broad, subangular, with their
anterior margins convex, apexes rounded, post-
erior margins slightly convex, free rear tips
rounded, and inner margins convex, relatively
short, their anterior margins about an eye di-
ameter shorter than distance from snout tips
to first gill opening; pectoral inner margins long,
about 11/2 to 11/;! times pectoral base length;
posterior margin about ll/ij to iy-> times in
anterior margin; free rear tip of pectoral vary-
ing in position from below posterior end of first
dorsal base to last third of first dorsal base.

Pectoral fin skeleton, as studied on radio-
graphs, somewhat similar to that of Galeorhiniis;
propterygium with 1 radial, mesopterygium with
3 or 4, segmented metapterygial axis with 10 to
12; metapterygial axis elongate, much larger
than anterior basals, with a distal set of seg-
ments; radials mostly divided into three seg-
ments (proximal, intermediate, and distal),
intermediates shorter than jiroximals or distals,
which are equal in length.

Pelvic fins somewhat larger than anal but
smaller than second dorsal in area; pelvics in
some males relatively smaller than those of fe-
males; pelvics triangular, with anterior margins
slightly convex to nearly straight, apexes broadly
rounded to subangular, posterior margins nearly
straight, free rear tips acute (slightly attenuate
in some specimens) , inner margins straight;
pelvic anterior margins 2.6 to 2.8, posterior
margins 1.7 to 1.9, and inner margins 1.4 to 1.6
in comparable margins of pectorals.

Claspers and associated secondary sexual
structures of males generally similar in basic
plan to those described for Galeorhimis galeus
(as "Galeiis mdgar-is") by Leigh-Sharpe (1921),
but differing in several details; claspers long,
more slender and more angular distally than
those of Galeorhmus with bluntly pointed, flat-
tened tips (Figure 5A) ; claspers of adult males
extending well beyond free rear tips of pelvics;
clasper groove roofed over and closed by its
overlapping sides from apopyle to hypopyle;
small pseudosiphon present mediodorsally, its
pouch extending anteriorly on clasper. Unlike
Galeorhimis, the pseudosiphon aperture is much
less prominent and is located relatively farther
from the clasper tip. Cover rhipidion very large
(scarcely developed in Galeorhinus) , formed as
a rounded flap completely covering rhipidion;
rhipidion evenly rounded (wedge-shaped in
Galeorhinus); pseudojjera present, dorsolateral
and opposite to the rhipidion edge (as in Galer-
hinus) ; unlike Galeorhinus, the pseudopera is
partially covered by another flap, here termed
the exorhi])idion, which originates laterad to the
pseudopera and extends posteriorly to cover part
of the rhipidion. Hypopyle opening at level of
pseudopera, cover rhipidion, and anterior third
of rhipidion.

Clasper skeleton studied from radiographs of
six males. Terminology is modified from Junger-
son (1899) and White (1936, 1937). One basal
cartilage connecting clasper cartilage to pelvic
basipterygium; a small beta cartilage present
at the junction of basal cartilage and clasper
cartilage; details of terminal cartilages not
clear, but at least two terminals, a dorsal and
a ventral, are in'esent; clasijer cartilages heavily
calcified in adult males.

622

COMPAGNO and SPRINGER: NEW GENUS OF CARCHARHINID SHARKS

First dorsal fin triangular with height much
less than length from origin to free rear tip;
origin ill-defined, grading into predorsal ridge;
anterior margin slightly concave basally but con-
vex towards fin apex, with a 45 degree slope
relative to body axis; apex acutely rounded,
posterior margin somewhat concave, free rear
tip slender, elongate, acute; base much longer
than fin height, inner margin about 60 to 70%
of fin height; end of first dorsal base about
over adpressed apex of pectoral; pectoral free
rear tip anterior to pelvic origins by a distance
nearly or quite equal to lengths of pelvic bases.

Second dorsal fin generally similar in shape
to first dorsal; its height about half length from
origin to free rear tip; fin base about 1.4 to 1.5
times height; inner margin about 0.5 to 0.7 of
height; origin of second dorsal posterior to mid-
point between anal origin and posterior end of
pelvic base; free rear tip of second dorsal op-
posite or slightly posterior to that of anal; sec-
ond dorsal over twice area of anal.

Anal fin a low triangle, with height about 0.4
in length, anterior margin broadly convex, apex
rounded, posterior margin moderately concave,
free rear tip slender and acute, and inner margin
concave; inner margin almost or quite equal in
length to height; fin base 1.4 to 1.6 times fin
height.

Dorsal margin of caudal nearly straight, pre-
ventral margin broadly convex, and junction of
preventral and postventral margins rounded;
postventi-al margin long, concave anteriorly but
nearly straight posteriorly and curving abruptly
upward into subterminal notch; subterminal
margin nearly straight, terminal margin invar-
iably frayed but apparently moderately concave.

Vertebral counts given in Table 3.

Vertebral calcification pattern was studied
from transverse sections and radiographs of
centra from below first dorsal fin. Terminology
for vertebral parts follows Ridewood (1921).
Primary double cone without diagonal calcified
lamellae; solid dorsal, lateral, and ventral inter-
medialia present, separated by uncalcified areas
for the basidorsals and basiventrals (Figure
3C) ; notochordal canal at constricted portion of
double cone unusually large (as in many other

deepwater sharks, a feature possibly correlated
with habitat).

The chondrocranium was dissected out in one
specimen but is not described here. It is similar
in structure to the crania of Galeorhiniis and
Mustelus described by Gegenbaur (1872) but
differs in numerous details from both.

Stomach very large, subdivided into a sack-
like fundus and a long slender pylorus. The
fundus extends posteriorly over two-thirds the
length of pleuroperitoneal cavity, then reverses
direction as the pylorus to continue anteriorly
nearly to root of liver, where it joins the spiral
intestine. The latter is fusiform, with a spiral
valve of about five turns (Figure 3D). The nar-
row rectum has a slender rectal gland attached
distally to the epigonal organ in both sexes.
Liver only moderately large, with paired lat-
eral lobes concealing small medial lobe, posterior
ends of lateral lobes extending only one-half to
two-thirds of distance to posterior end of pleuro-
peritoneal cavity. Spleen elongate, not nodular,
originating dorsally on distal end of fundus and
coursing anteroventrally on pylorus to spiral in-
testine, where it extends posteroventrally to be-
low the first intestinal valve. Pancreas elongate,

Table 3. — Vertebral numbers in male and female lago
omanensis.

Monospondylous

Diplospondylous

Caudol

Total

precaudals

precauda

Is

vertebrae

vertebrae

Moles

34

48

48

130

34

47

48

129

36

49

58

143

36

47

52

135

37

49

51

137

37

45

51

133

37

51

Females

44

132

37

51

50

138

37

47

50

134

37

51

58

146

37

51

52

140

37

51

50

138

33

51

51

140

38

51

51

140

39

52

53

144

42

49

56

147

single, located anterior to spiral intestine and
dorsal to stomach. Ovaries well-developed only
on right side, with long epigonal organ extending
posteriorly to rectal gland; both oviducts well-de-

623

FISHERY BULLETIN: VOL, 69. NO. 3

veloped and functional in all adult females ex-
amined, with small nidamental •glands almost
obsolete on the right side in some specimens;
both testes apparently functional, subequally de-
veloped in three males examined, with a single
epigonal organ attached to left testes. Semi-
lunar valves of conus arteriosus in two rows,
the anterior one with three valves, the posterior
with three much smaller valves located each on
the posterior base of an anterior valve.

Color brownish or grayish above and lighter
below, with no conspicuous markings or abrupt
color changes from dorsal to ventral; expanded
chromatophores in the darkest specimen give a
peppered appearance; small areas of darker pig-
mentation present near tips of both dorsal and
caudal fins and in some specimens extending
along leading edges of fins; lining of buccal
cavity and peritoneum whitish.

VARIATION

The variation in morphometries among our 16
specimens is substantial, unusually so for a series
of adult sharks. Most of the difl'erences do not
follow sex, but it is apparent that the abdominal
section is longer in females than in males. Thus
the distance between pectoral and pelvic bases
ranges from 13.7 to 16.1% of total length in
seven males but is 16.8 to 20.0% in nine females.
This is similar to the situation reported for the
squaloid Euprotomicrus bispinatus by Hubbs,
Iwai, and Matsubara (1967) and in Carcharhhuis
leucas by Thorson, Watson, and Cowan (1966).
Large variations in tooth row and vertebral
counts were noted also. Despite the range of
variation between individuals and the sexual
dimorphism in our sample, we find nothing to
indicate that more than one species is repre-
sented or that the variation can be attributed
to known geographical or environmental influ-
ences.

REPRODUCTION

One 440-mm specimen in our series has par-
tially developed and uncalcified claspers but has
eggs with very early embryos in the oviducts.

Thus the specimen is, at least functionally, a
female. Histological examination of the ovaries
was not made, but gross examination revealed
one ripe ovary of normal appearance but little
development of the other gonad. A similar in-
stance of the partial development of claspers by
a functional female Centrophoriis bisitanicus
was reported by Cadenat (1960). A more ex-
treme example, recorded by King (1966), was
of a hermaphroditic Scyliorhinus canicuhis with
a single immature clasper, a ripe ovotestis (with
ovarian follicles at all stages and seminiferous
tubules with mature sperm), and functional
nidamental glands, oviducts, vasa deferentia, and
seminal vesicles (with sperm). King also listed
another S. caniculus specimen with two imma-
ture claspers, a ripe ovotestis, and oviducts, but
no seminal vesicles and vasa deferentia. The
opposite condition was found in a field-dissected
specimen of Mustelus higmani by Dr. John
Thompson (Springer and Lowe, 1963) . This in-
dividual lacked claspers but had a pair of en-
larged testes.

It may be significant that in the above cases
the size of each shark was within the range of
its functional sex at maturity regardless of ex-
ternal characters belonging to the opposite sex.
The lago and Centrophoriis females with clasp-
ers were larger than would be expected for ma-
ture males of the species, but the clasperless
male Mustelus was smaller than mature females
of its species. Both hermaphroditic Scyliorhinus
were the size of adult females of their species
despite the presence of claspers.

Our smallest male, 224 mm long, is immature
with uncalcified claspers but six others from
295 to 363 mm are mature. We did not examine
internally a 358-mm female, the smallest of its
series, but eight others from 395 to 582 mm are
mature and have eggs in their oviducts. The
eggs are for the most part not large, having
yolks not more than 10 mm in diameter, and
in our specimens, embryos, when present, are
in a very early stage of development. In the
oviducts each egg is encased in a thin and soft
membranous shell which closely adheres to the
oviduct lining. The nidamental glands vary in
size from scarcely visible enlargements of the
anterior oviduct to about 10 mm in diameter,

624

COMPAGNO and SPRINGER; NEW GENUS OF CARCHARIIINID SHARKS

but all are far smaller than those present in
oviparous scyliorhinids. The condition of nida-
mental glands and eggshells indicate that lago
omanensis is livebearing, with oviductal egg
counts suggesting a litter of 2 to 10 young. The
relatively small size of egg yolks implies that a
maternal source of nourishment is provided the
embryos unless the young are extremely small at
birth.

SIZE

lago is one of the smaller carcharhinids. In
the Carcharhinidae, ScoUodon, the Protozygaeyia
group in Rhidoprionodon, and Mustelus have spe-
cies nearly or quite as small as /. omanensis,
though Eridacnis species are even smaller. One
of the latter, E. radcliffei, is apparently the smal-
lest carcharhinid and one of the smallest sharks,
with males mature at 186 mm and females at
216 mm.

Size disparity between the sexes is a common
phenomenon among elasmobranchs, in all known
cases with females larger than males. In lago
omanensis this disparity is very marked ; our
largest male (365 mm) was only 63% as long
as the corresponding female (582 mm) and
weighed but one-sixth as much.

FOOD

Stomachs of two specimens contained remains
of unidentified fish, in one a fish head 32 mm
long and in the other a 50-mm section of the
posterior trunk of a fish estimated to have been
more than 200 mm long.

DISTRIBUTION

Table 1 shows the distribution of 16 of 17
known specimens of lago omanensis, all except
the holotype from IIOE Cruise 4B. Only three
other shark specimens, all Mustelus sp., were
collected during Cruise 4B from 81 trawling
stations in the northern Arabian Sea. This total
of only 19 shark specimens of two species is much
lower than the expected catch for comparable
gear in many other areas of continental shelf
and slope.

A possible explanation for the low incidence of
sharks in the catches lies in frequent presence

of ijoorly oxygenated water near the bottom
along the coast between the Gulf of Kutch and
the Gulf of Oman (See Banse, 1968, for a gen-
eral account of the hydrography of part of this
area). Sharks of species commonly held in ma-
rine aquaria are thought to require a high dis-
solved oxygen level for survival although studies
to verify this for particular species have not
been made.

Low oxygen concentration in water at the bot-
tom, 0.22 to 0.77 ml/liter, is associated with five
of the six IIOE stations at which lago omanensis
was taken. It appears that this species may be
exceptionally tolerant to low oxygen levels, even
at the moderately warm (16.24° to 22.39° C, or
about 61.3° to 72.4° F) water it apparently in-
habits. In the Red Sea, Marshall and Bourne
(1964) reported that their unidentified carcharh-
inoid (which may be lago omanensis or a close
relative) occurred at depths down to 2195 m.
As this area and these depths may have oxygen
concentrations lower than 1 ml/liter at the end
of summer (Richards, 1957), the Marshall and
Bourne shark may be able to survive oxygen
levels as low as known lago omanensis appar-
ently does in the Arabian Sea.

Gibbs and Hurwitz (1967) regarded the great-
er development of gill lamellae in the stomiatoid
fish, Chauliodus pammelas compared with that
in C. sloani as an adaptation to the low oxygen
habitat of C. pammelas. We looked at struc-
tures having respiratory functions in lago oman-
ensis but found nothing to suggest such an
adaptation. /. omanensis, however, has no
closely allied species as a basis for comparison.

ACKNOWLEDGMENTS

We thank Dr. N. B. Marshall, British Museum
(Natural History) for assistance in comparisons
of the holotype with specimens of the IIOE ser-
ies, Maarten Korringa, Stanford University, for
suggesting the generic name, and Mrs. Martha
J. Mitchill of Kent Cambridge Scientific Inc.,
and Stanford University, for permitting one of
the writers (Compagno) to use a Cambridge
Stereoscan scanning electron microscope in her
care.

625

FISHERY BULLETIN: VOL. 69. NO. 3

LITERATURE CITED

Banse, K.

1968. Hydrography of the Arabian Sea shelf of
India and Pakistan and effects on demersal fishes.
Deep-sea Res. Oceanogr. Abstr. 15: 45-79.

BiGELOW, H. B., AND W. C. SCHROEDER.

1948. Sharks. In Fishes of the western North
Atlantic, p. 59-546. Mem. Sears Found. Mar. Res.
Yale Univ. 1, Part 1.
Cadenat, J.

1960. Notes d'Ichtyologie ouest-africaine. XXXII.
— Sur un cas d'intersexualite chez un Requin de
I'espece CentropJiorus lusitanicus Bocage et Capel-
lo 1864. Bull. Inst. Fr. Afr. Noire, Ser. A, 22:
1428-1430.

COMPAGNO, L. J. V.

1970. Systematics of the genus Hemitriakis (Se-
lachii: Carcharhinidae), and related genera.
Proc. Calif. Acad. Sci., Ser. 4, 38: 63-98.
Fowler, H. W.

1941. The fishes of the groups Elasmobranchii,
Holocephali, Isospondyli, and Ostarophysi obtained
by the United States Bureau of Fisheries Steamer
"Albatross" in 1907 to 1910, chiefly in the Phil-
ippine Islands and adjacent seas. U.S. Natl. Mus.
Bull. 100, Vol. 13, 879 p.

1956. Fishes of the Red Sea and Southern Arabia,
I. Branchiostomida to Polynemida. Weismann
Science Press, Jerusalem, 240 p.

1967. A catalogue of world fishes (VII). Q. J.
Taiwan Mus. 20: 341-366.

GaRRICK, J. A. F., AND L. P. SCHULTZ.

1963. A guide to the kinds of potentially dangerous
sharks. In P. W. Gilbert (editor). Sharks and
survival, p. 3-60. D. C. Heath, Boston.
Gegenbaur, K.

1872. Untersuchungen zur Vergleichenden Anato-
mic der Wirbelthiere. Drittes Heft. Das Kopf-
skelet der Selachier, ein Beitrag zur Erkenntnis
der Genese des Kopfskeletes der Wirbelthiere.
Wilhelm Engelmann, Leipzig, 316 p.
GiBBS, R. H., Jr., and B. A. Hurwitz.

1967. Systematics and zoogeography of the stomia-
toid fishes, Chauliodus pammelas and C. sloani, of
the Indian Ocean. Copeia 1967: 798-805.
HuBBS, C. L., T. Iwai, and K. Matsubara.

1967. External and internal characters, horizontal
and vertical distribution, luminescence, and food
of the dwarf pelagic shark, Euprotomicrus bi-
spinatus. Bull. Scripps Inst. Oceanogr. Univ.
Calif. 10, 64 p.
Jungerson, H. F. E.

1899. On the appendices genitales in the greenland
shark, Soinniosus microcephalus (Bl. Schn.), and
other selachians. Dan. Ingolf-Exped. 2(2), 88 p.
King, A. D.

1966. Hermaphroditism in the common dogfish

(Scyliorhinus caniculus) . J. Zool. 148: 312-314.

Leigh-Sharpe, W. H.

1921. The comparative morphology of the second-
ary sexual characters of elasmobranch fishes.
The claspers, clasper siphons, and clasper glands.
Memoir II. J. Morph. 35: 359-380.

Marshall, N. B., and D. W. Bourne.

1964. A photographic survey of benthic fishes in
the Red Sea and Gulf of Aden, with observations
on their population density, diversity, and habits.
Bull. Mus. Comp. Zool. Harvard Univ. 132:
223-244.

1967. Deep-sea photography in the study of fishes.
In J. B. Hersey (editor) , Deep-sea photography,
p. 251-257. Johns Hopkins Oceanogr. Stud. 3.
Misra, K. S.

1949. A check list of the fishes of India, Burma &
Ceylon. Part I. Elasmobranchii and Holocephali.
Rec. Indian Mus. Calcutta 45: 1-46.
Norman, J. R.

1939. Fishes. John Murray Expedition of 1933-34,
Sci. Rep. 7(1) : 1-116. British Museum (Natural
History), London.
Richards, F. A.

1957. Oxygen in the ocean. In J. W. Hedgpeth
(editor) , Treatise on marine ecology and paleoe-
cology. Vol. 1, p. 185-238. Geol. Soc. Am., Mem.
67, Vol. 1.
Ridewood, W. G.

1921. On the calcification of the vertebral centra
in sharks and rays. Philos. Trans. Roy. Soc.
London, Ser. B., Biol. 210: 311-407.
Smith, J. L. B.

1957. A new shark from South Africa. S. Afr.
J. Sci. 53: 261-264.
Springer, S., and R. H. Lowe.

1963. A new smooth dogshark, Mustebis higmani,
from the equatorial Atlantic coast of South Amer-
ica. Copeia 1963: 245-251.
Strasburg, D. W.

1963. The diet and dentition of Isistivs brasiliensis,
with remarks on tooth replacement in other sharks.
Copeia 1963: 33-40.
Thorson, T. B., D. E. Watson, and C. M. Cowan.
1966. The status of the freshwater shark of Lake
Nicaragua. Copeia 1966: 385-402.
White, E. G.

1936. Some transitional elasmobranchs connecting
the Catuloidea with the Carcharhinoidea. Am.
Mus. Novit. 879, 22 p.

1937. Interrelationships of the elasmobranchs with
a key to the order Galea. Bull. Am. Mus. Nat.
Hist. 74, Artie. 2, p. 25-138.

Woods Hole Oceanographic Institution.

1965. U.S. program in biology. International In-
dian Ocean Expedition. Final cruise report,
Anton Dniun cruises 4A and 4B. Manuscr. Rep.
W.H.O.I. 1-2, tables, mimeo.

626

UPTAKE, ASSIMILATION, AND LOSS OF DDT RESIDUES BY
Euphausia pacifica, A EUPHAUSIID SHRIMP

ABSTRACT

James L. Cox'

Euphausia pacifica Hensen, an abundant euphausiid shrimp from the California Current, can acquire
sufficient DDT residue from its food to account for amounts found in its tissues. Assimilation effii-
ciencies for DDT in ingested food are similar to published figures for assimilation of carbon from
food. The concentration vs. size function suggested by gas-liquid chromatographic analyses of DDT
residues in E. pacifica, however, was quite different from the function predicted by a theoretical food
assimilation model. Direct uptake of '"iC-DDT from water was rapid and partially reversible by re-
turning animals to unlabelled flowing seawater. Uptake equilibrium was reached within 72 hr for smaller
animals (<3 mg dry weight) ; larger animals apparently equiliberated after a longer period. '■'C-DDT
present in animals after 2 weeks exposure to unlabelled flowing water was retained in higher amounts
in larger animals (>3 mg dry weight). The possible effects of dietary changes, moulting, and surface
to volume ratios on observed natural levels are discussed.

DDT and its congeners are manmade substances
which have achieved global distribution. This
fact has produced w^idespread concern over their
long-term impact in ecosystems and has stim-
ulated efforts to study DDT transport from a
systems analysis viewpoint (Harrison et al.,
1970). Indirect evidence (Cox, 1970) suggests
an accretion of DDT residues in oceanic food
chains and underscores the need to produce in-
formation about mechanisms and rates of DDT
acquisition and loss by plankton organisms.
This paper reports the results of an experimental
study of the euphausiid crustacean Euphausia
pacifica dealing with quantitative aspects of
DDT acquisition from food and water, rates of
loss of acquisition from food and water, rates
of loss of acquired DDT, and factors affecting
equilibration with the surrounding water.

Euphausiid crustaceans are among the most
abundant zooplankters in many oceanic regions.
They are the food of commercially important
fishes and in general represent an important link
of oceanic food chains. E. pacifica is the most
abundant euphausiid of the California Current.
Ponomareva (1954, 1955, 1959, 1963) has sum-

' Department of Biology, Southeastern Massachusetts
University, North Dartmouth, Mass. 02747.

marized behavioral and population data on this
species, and Lasker (1966) has made extensive
laboratory studies of its feeding, growth, res-
piration, and carbon utilization.

METHODS AND MATERIALS

Laboratory maintenance of E. pacifica has
been described by Lasker and Theilacker ( 1965) .
Animals were maintained in a 40-liter capacity
tub with flowing seawater at 10 to 12° C and
fed daily rations of freshly hatched Artemia
nauplii. Individuals were kept long enough dur-
ing the course of the experimental work for
noticeable growth. Mortality was extremely
low after the first day that the animals were
kept in the tub.

In direct uptake experiments, '^C-DDT was
added in small carrier volumes of ethanol (ca.
100 /xliter) to GFC glass fiber filtered seawater
(voluriies from 1 to 10 liter) under constant
stirring from a magnetic stirrer. Animals were
introduced in groups from a small net or turkey
baster. At the completion of an uptake run,
animals were removed, rinsed briefly with fresh
water, and placed in a desiccator for 6 days at

Manuscript accepted March 1971.

FISHERY BULLETIN: VOL. 69, NO. 3, 1971.

627

FISHERY BULLETIN: VOL. 69, NO.

room temperature. Losses of "C-DDT during
desiccation were insignificant. Dried animals
were removed, weighed on a Cahn electrobal-
ance to ± 0.01 mg, placed in scintillation vials
with equal volumes of NCS solubilizer (Nuclear-
Chicago) , and digested 1 hr at 70° C before in-
troduction of scintillation fluid and subsequent
counting on a Nuclear Chicago Unilu.\ II scin-
tillation counter.'

Loss experiments were done by taking labelled
animals, subsampling them for initial "C-DDT
levels, and placing them back in a flowing sea-
water tank. Water in the tank had a turnover
time of less than 10 min, so lost '^C-DDT was
rapidly removed from the system. Groups of
animals were removed from the tank at inter-
vals and analyzed as described above.

In addition to work with '■'C-DDT, freshly
caught E. iiacifica were processed and analyzed
for naturally occurring levels of DDT residues
according to published methods (Cox, 1970),
except that whole eujihausiids were ground in
the homogenizer, rather than algae on filters.

All direct uptake work was done at concen-
trations less than 33 ppt (parts per 10'^)
'*C-DDT in seawater, ranging down to 5 ppt.
In uptake and loss experiments, individual
samples were taken by removing about 10 to 15
animals from the experimental system, pro-
cessing them, and plotting the results on log-
log (full logarithmic) paper and fitting a least-
squares regression line to the logarithmically
transformed data. Depending upon the extent
of the dry weights of the animals taken in each
of the described groups, points corres])onding
to 1.0, 2.0, 3.0, or 10.0 mg dry weight were taken
from the regression line for comparisons.

RESULTS

UPTAKE

Since the lipid constituents of planktonic or-
ganisms are not in direct contact with seawater,
it is necessary to postulate a two-step process
of uptake of DDT residues — first, adsorption on-

to surfaces in contact with seawater and second,
diff'usion or transport of the adsorbed residues
into the lipid constituents of the organism. Ini-
tial uptake by E. pacifica was rapid; Figure 1
shows the results of a 2-hr uptake experiment.
Approximately equal numbers of animals were
added to two 7-liter jars containing "C-DDT at a
low ppt concentration. Two hours later, ani-
mals were removed and analyzed. The concen-
tration vs. dry weight functions were found to
be exponentials, yielding a straight line on the

100

XI
Q.

.p..

<

S '0

u

z

S 100

a
a

-

T! < "1 T~ '7'-T'l Mil

\

1 ■ T'— 1 — r-

LIVE ;

1 1 1

V LOGY =

:^%

2.09- 0.98

LOGX'

1 ill

\,

V

HEAT KILLED

LOG Y= 2.13-0.97 LOGX

\

\

-J I I I i I I I

- Reference to trade name in this publication does not
imply endorsement of commercial products by the Na-
tional Marine Fisheries Service.

1.0 K)

DRY WEIGHT (mg)

Figure 1. — Uptake of '^C-DDT by Euphausia pacifica
of different weights after 2 hr of exposure to labelled
medium.

log-log plot. Initial uptake appeared to be un-
related to the animals' activity or respiration
since heat-killed animals had the same total
uptake as live animals. The amounts of ''C-DDT
taken up per animal were almost identical in
these experiments (exactly equal amounts would
yield a slope of — 1 in the regression function).
In a diflFerent series of exijeriments, the slopes
of the log-log concentration vs. dry weight func-
tions changed from — 1.05 at 2 hr and — 0.99 at
8 hr to — 0.67 at 24 hr. This change resulted
from increased uptake by larger animals after
longer exposure. Figure 2 summarizes the over-

628

COX: UPTAKE, ASSIMILATION. AND LOSS OF DDT RESIDUES

all patterns of uptake for the 72-hr period. Three
arbitrary dry weights of animals (2.0, 3.0, and
10.0 mg) were chosen to illustrate different
weight effects during uptake. The points cor-
responding to these dry weights were taken
from regression lines like those shown in Fig-
ure 1. The values on the ordinate were con-
verted from concentration to total picograms
(g X 10-'2) of "C-DDT. After 72 hr of ex-
posure, the 10-mg animal did not reach equilib-
rium; the 2 and 3 mg animals did reach equi-
librium after 72 hr.

=^ 560

TIME (hr)

Figure 2. — Uptake of '^C-DDT by Enphruisia pacifica
in a closed system. Equilibrium concentration of '''C-
DDT in the water was 20 parts per trillion. The three
dry weight values were taken from log-log regression
lines for subsamples of 10 animals or more. See text
for details.

EFFECT OF TEMPERATURE

Temperature appeared to have little effect on
initial uptake rates. The Qio for short-term (2
hr of exposure) uptake between 5° and 15° C for
an animal of a given dry weight was computed
by comparing log-log regression functions for
two groups of animals exposed to the same nom-
inal concentrations of "C-DDT in the medium —
one group at 5° C and the other at 15° C. This
procedure yielded a Qio of 1.11 for an animal
of 2.0 mg dry weight and a Qm of 1.29 for an
animal of 10.0 mg dry weight. Both figures
suggest a physical process as the limiting step
for direct uptake of DDT; the higher figure for

larger animals may reflect a higher Qio for
transfer into the lipid reservoir of the larger
animal.

Del Nimmo (personal communication, 1970)
has evidence that DDT residues are transported
to internal sites of accumulation by a protein
fraction in the haemolymjih of penaeid shrimps.
If E. pacifica is comparable in this regard to the
penaeid shrimp, then transport of DDT in the
circulatory system must not be the rate-limiting
step in uptake, since circulatory rates may be
expected to have a higher On, than those found.
Respiratory rates, which are directly dependent
upon circulatory rates, exhibit Qm values in ex-
cess of 2.2 in E. pacifica (Paranjape, 1967).

CONCENTRATION FACTORS

The short-term uptake concentration factors
(the ratio of the concentration of DDT in the
animals to the concentration in the water after
brief exposure) for "C-DDT changed little over
the range of concentrations employed. Table 1
summarizes data that were taken from log-log
jjlots for animals of 1.0 and 3.0 mg dry weight.
It is evident that short-term uptake of DDT for
an animal of a given size is proportional to the
concentration of the DDT in water.

Table 1. — Concentration factors after 2 hr e.xposure.

Equilibrium concentration
of •''C-DDT in seawater

Concentration factor X 103
Concentration in animal (dry):
concentrotion in water (w/v)

Parts per trillion

i.n mt

3.0 ms

5

4.4

I.I

120

3,2

1.1

26

4.1

1.2

33

4.1

1.2

1 This includes data from one-half hour run.

LOSS

If short-term exposure to DDT in the seawater
medium of E. pacifica results in surface adsorp-
tion, one expects that these adsorbed residues
will be lost to the medium if the ambient con-
centration of the DDT is lowered. If all the
labelled DDT in a short-term experimental ex-
posure is adsorbed, the animals would be ex-
])ected to lose eventually all of their label when
returned to unlabelled flowing seawater.

629

FISHERY BULLETIN: VOL. 69. NO. 3

Figure 3 shows the results of 2 weeks of
"rinsing" on animals originally exposed to "C-
DDT for 2 hr. The lower data points show that
a fraction of the "C activity was retained, al-
though the size vs. estimated i-iC-DDT concen-
tration function was altered considerably by the
treatment. Figure 4 shows a loss curve con-
structed from a series of log-log plots such as
those in Figures 1 and 3. The 10.0 mg animal
apparently neared equilibrium at the end of the
2-week period, but the 2.0 and 3.0 mg animals
were still declining. Presumably, the '^C-ac-
tivity loss occurred by diffusion of the parent
compound ('■'C-DDT) or metabolites into the
flowing seawater medium. Some loss may have
occurred through moulting. Unfortunately, the
conditions of the experiment did not allow any
record of moult production.

ASSIMILATION FROM FOOD

Animals were isolated in Carolina dishes and
kept at 10° C in the dark in 200 ml of GFC
filtered seawater and fed known numbers of
freshly hatched Artemia nauplii previously
labelled with "C-DDT (2.7 ± 0.02 X 10-'= g
"C-DDT nauplius, on the average for groups
of 10 to 50) . After 24 hr, animals were removed
to new dishes and fed daily rations of unlabelled
nauplii to ensui'e flushing of the undigested re-
mains of the labelled nauplii from the guts of
the experimental animals. After 2 days, the
animals were removed, rinsed, dried in a desic-
cator, and weighed. Amounts of "C-DDT ac-
tivity retained were comjiuted by measuring the
activity of the dried animals as described in the
section on methods. Amounts of labelled nauplii
eaten were calculated by counting the numbers
left in the dishes after the 24-hr feeding ])eriod.
Table 2 summarizes the results of the experiment.

100-

<

O

o

>-
o
a
I
o

? M I 1

1 I 1 1 1 1 1 I M II

-

°o\ LOGY =2.31-

-058 :

-

LOG x:

-

-

-

•

t
• •

-

-

:^'*

=

1 1 1 1

1 I 1 1 1 1 J 1 1 1 1

1 1 1

1.0

DRY WEIGHT (mg)

Figure 3. — Loss of "C-DDT from Etiphausia pacifica
kept in a flowing water system. Values for the different
dry weights were obtained as indicated in the methods
section of the text. The solid dots indicate "C-DDT
concentrations after 2 weeks of exposure to unlabelled
flowing seawater. The open dots are for animals ex-
posed to "C-DDT for 2 hr, then "rinsed" in the flowing
seawater system for 2 hr before sampling.

Animal 5 may have had a higher assimilation
efliciency because of delayed excretion of the gut
contents, presumably attributable to the post-
moult condition, i.e., passivity and lack of feed-
ing or swimming movements (Paranjape, 1967).
Consequently animal 5 was excluded from fur-
ther calculations. Animal 1 may have had a
lower assimilation efliciency because some loss
of labelled material with the moult. The avei'age
"C-DDT assimilation efliciencies for animals
2 to 4 is only slightly lower than Lasker's (1966)
estimates of carbon incorporation efficiency for
E. pacifica.

Table 2. — •■'C-DDT assimilation from labelled Arteinia nauplii by Eiiphausia pacifica.

Nauplii eoten

nauplii offered

(lobelled)

Percent
consumplion

Ami. "C-DDT

ingested

picogroms

is X IO->2)

Amf. "C-DDT
assimilated
picograms
(S X 10-U)

Percent

assimilation

efficiency

1

30/30

100

81

28

2

44/53

83

119

70

3

38/38

100

103

81

4

49/rs

65

132

106

5

21/62

34

62

58

34
58
78
80
93

1 Premoult means moult was recovered after feeding on labelled nauplii. Postmoult means moult was recovered after feeding on unlabelled nauplii

630

COX: UPTAKE, ASSIMILATION. AND LOSS OF DDT RESIDUES

In another experiment, 12 animals were placed
in a vessel and fed "C-DDT labelled nauplii for
1 hr. Six animals were taken and processed for
"C activity, and the remaining six were allowed
to feed on unlabelled nauplii, for 2 days before
they were processed. The assimilation efficien-
cies were computed as a ratio of '•'C activity in
the animals processed after 2 days to the "'C
activity in the animals processed immediately
after the 1-hr feeding period. This method
yielded an assimilation efficiency of 76 '"r.

For calculations, I took a mean of the first
four animals' assimilation efficiencies. It is un-
certain whether this figure (62*;; ) adequately
reflects the influence of moulting on DDT assim-
ilation efficiency. Moulting probably plays an

<J
§80

V

?60

:\

V

^V

10.0 mq

< AO

1—

^

o

-

1 1

2.0 mg

aOmg~~—

1 1

o-

1 1

3

2

TIME

6

(days)

14

Figure 4. — Loss curve constructed from data such as
that presented in Figure 3. See text for details.

z
o

-OA

-3.0

,17

zz *-^

t-^

—

►< 1

< *

*

-2fl

>-

-1.5

z «

_ Q

*,

/

O E

E

-1.0

" -- 26

4 /'

z 9-
o Q-

Q.
O.

*c 1

__b^

o

^-1

-0.5

1 i

r

1 1 1 1 1 1 1 1 III

0

1

1

10

DRY WEIGHT (mg)

Figure 5. — DDT residue concentrations in different sizes
of Eiiphausia pacifica. The numbers next to the data
points indicate the numbers of animals in the pooled
sample analyzed; horizontal brackets indicate the range
of weights of individual animals within the groups.

important role in DDT loss from the organism;
DDT incorporated into the moult is lost when
the moult is shed.

NATURAL LEVELS OF DDT

Figure 5 shows the results of gas chromato-
graphic analyses of E. pacifica samples collected
in August 1970, the same time that most of the
experimental animals were collected. On the
basis of DDT acquisition from food, a rising
trend in the DDT residue concentrations would
be expected as animals grew and aged. In order
to examine the discrepancy between the observed
DDT values and that which might be expected
from cumulative assimilation of DDT residues
from food, a model was constructed.

Woodwell, Wurster, and Isaacson (1967)
found 0.04 ppm in plankton hauls from a polluted
estuary; I have found 0.25 ppm in large, pooled
samples of copepods from Monterey Bay. The
mean weight of these copepods, 0.95 mg, was
only slightly higher than for those eaten by E.
pacifica. E. pacifica also feeds on phytoplankton.
The concentrations of phytoplankton, when the
density of the standing crop of phj-loplankton
is high enough to stimulate feeding, are probably
below 0.1 iipm, wet weight (Cox, 1970). An
intermediate figure can be taken as representa-
tive of the DDT concentration of the food of E.
pacifica. I chose 0.1 ppm as the mean concen-
tration of DDT i-esidues in food.

Employing the carbon budget parameters
published by Lasker (1966) and the estimate of
DDT residue concentration in food organisms,
I calculated the cumulative DDT content of the
ingested food of animals of three diflferent dry
weights (Table 3). The computed values are
compared with values interpolated from the ar-
biti'arily drawn dotted line in Figure 5.

Two conclusions may be drawn from a com-
parison of columns 7 and 8 in Table 3. First,
the estimated values are close enough to the ob-
served values to indicate that ingestion is a suf-
ficient source of DDT residues in E. pacifica.
Second, the concentration vs. size function of
the observed values is quite different from that
of the calculated values, indicating that processes
other than simple accumulation of a fraction of

631

FISHERY BULLETIN: VOL. 69, NO. 3

Table 3. — Calculation of expected DDT residues in different sizes of Eiiphausia pacifica.

Dry
weight

Equivalent
weight
carbon

Carbon

growth

incorporation

efficiency^

Cumulative
amount
nauplius
carbon
required

DDT
equivalent^
(S X 10-8)

Assumed
DDT

incorporation
efficiency

Parts per 10^ — dry

Expected

DDT

concentrotion

OBserved

DDT

concentrotion

1.0
2.0
3.0

0.42
0.84
1.26

0.30
0,15
0.10

mi;
1.4
4.2
8.4

1.4
4.2
8.4

0.62
0.62
0.62

0.9
1.3
1.7

0.75
0.55
0.S<5

' Corbon growth incorporation efficiencies were taken from Table 2 of Lasker (1966); the figures shown ore not means of the values presented by
Lasker but are round-figure approximations which take account of the trends shown and of the different range of sizes of animals used in the lab-
oratory experiments which yielded these figures.

2 The DDT equivolent of the food was calculated from nauplius carbon assuming a wet weight DDT concentration in the food of 0.1 ppm, and a
carbon weight to wet weight ratio of 0.1.

ingested DDT determine DDT residue concen-
trations in E. pacified.

DISCUSSION

For E. pcwitica. there are two important
sources of DDT residues — direct uptake from
water and assimilation from food. Short-term
direct uptake is rapid and appears to be at least
partially reversible, suggesting adsorption of
DDT to exposed surfaces. Over longer periods,
these initially acquired residues are transferred
to internal deposition sites. The long-term
uptake and loss experiments show that larger
animals tend to retain more of the initially
acquired DDT, possibly because of greater
lipid content. Direct uptake from water is
a possible mechanism for accumulation of res-
idues if the initially adsorbed residues are con-
tinually transferred to internal dejrosition sites.
The rate of initial uptake will depend upon the
concentration in seawater (Table 1); retention
of these initially acquired residues apparently
depends on other factors, judging from the lower
set of data points in Figure 3. One determina-
tive factor may be lipid content; values given by
Mauchline and Fisher (1969) indicate that lipids,
expres-sed as percentage of body weight, can vary
by as much as an order of magnitude in Euphmis-
ia spp., according to the body weight of the ani-
mal. The four lipid values listed by Mauchline
and Fisher (1969) for E. pociticu correspond
closely to the DDT concentration values after 2
weeks rinsing shown in Figure 3. However, in
the absence of concurrent lijiid values for the
animals of the lower data points shown in Figure
3, no conclusion can be drawn about the relation-

.ship between retention of '^C-DDT and the per-
centage lipid composition of the animals. It is
reasonable to assume, nonetheless, that the
changes in the lipid content of E. pacifica which
accompany reproductive cycles and seasonal
feeding changes will have some impact on the
DDT residue content, regardless of the source
of the DDT residues.

The second possible source of DDT residues,
as previously discussed, is from food. In this
case, DDT is almost certainly transported di-
rectly in the fat of the food organisms to the fat
reservoir of the consumer. Numerous studies
indicate that marine organisms do not alter lipids
from ingested food (Lasker and Theilacker,
1962; Jezyk and Penicnak, 1966; Jeffries, 1970;
and others). Comparison of published values
of fatty acid comjwsition for E. pacifica (Ya-
mada, 1964) with values for its food, micro-
zooplankton and j)hytoplankton (Jeffries, 1970),
suggests that mass assimilation of fatty constitu-
ents along with DDT residues is taking place.

As has been suggested, food is probably a suf-
ficient source of DDT residues in E. pacifica
(Table 3). Direct uptake may contribute to
DDT residues in E. pacifica, but its role cannot
be assessed because of the lack of seasonal data
on DDT concentrations in seawater as well as
uncertainties about DDT's availability to or-
ganisms in the natural environment (Cox, 1971).

Some basis must be sought to explain the un-
expected higher concentrations of DDT residues
in the smaller animals. Three possibilities exist:
( 1 ) the food of immature E. pacifica may have
higher DDT concentrations, (2) direct uptake
from water is more important for the smaller
animals because of their higher area: volume

632

COX: UPTAKE, ASSIMILATION, AND LOSS OF DDT RESIDUES

ratios, or (3) smaller animals have not used
any of their lipid reserves, which use may cause
loss of some DDT residues. The data presented
here do not allow conclusions on the relative im-
portance of these possibilities.

LITERATURE CITED

Cox, J. L.

1970. DDT residues in marine phytoplankton: In-
crease from 1955 to 1969. Science (Wash., D.C.)
170: 71-73.

1971. DDT residues in seawater and particulate
matter in the California Current system. Fish.
Bull. U.S. 69: 443-450.

Harrison, H. L., O. L. Loucks, J. W. Mitchell, D. F.

P.ARKHURST, C. R. TR.ACY, D. G. WaTTS, AND V. J.

Yannacone, Jr.

1970. Systems studies of DDT transport. Science
(Wash., D.C.) 170: 503-508.
Jeffries, H. P.

1970. Seasonal composition of temperate plankton
communities: Fatty acids. Linmol. Oceanogr.
15: 419-426.
JEZYK, p. F., AND A. J. Penicnak.

1966. Fatty acid relationships in an aquatic food
chain. Lipids 1: 427-429.
Lasker, R.

1966. Feeding, growth, respiration, and carbon
utilization of a euphausiid crustacean. J. Fish.
Res. Board Can. 23: 1291-1317.

Lasker, R., and G. H. Tiieilacker.

1962. The fatty acid composition of the lipids of
some Pacific sardine tissues in relation to ovarian
maturation and diet. J. Lipid Res. 3: 60-64.

1965. Maintenance of euphausiid shrimps in the
laboratory. Limnol. Oceanogr. 10: 287-288.
Mauchline, J., and L. R. Fisher.

1969. The biology of euphausiid.s. hi F. S. Russell
and M. Younge (editors), Advances in marine
biology. Vol. 7, 454 p. Academic Press, London.
P.-\ranjape, M. a.

1967. Molting and respiration of euphausiids. J.
Fish. Res. Board Can. 24: 1229-1240.
Ponomareva, L. a.

1954. Euphau.siids of the Sea of Japan feeding on
copepods. Dokl. Acad. Sci. U.S.S.R. (Zool.) 98:
15.3-154.

1955. Nutrition and distribution of euphausiids in
the Sea of Japan. Zool. Zh. 34 : 85-97.

1959. Reproduction of Euphausiidae of the Sea of
Japan and development of their early larval
stages. [In Russian, English summary.] Zool.
Zh. 38: 1649-1662.

1963. The euphausiids of the North Pacific, their
distribution and mass species. [In Russian,

yjt' English summary.] Moscow, 142 p.

WotoWELL, G. M., C. F. WURSTER, JR., AND P. A.

Isaacson.

1967. DDT residues in an east coast estuary: A
case of biological concentration of a persistent in-
secticide. Science (Wash., D.C.) 156: 821-824.
Yamada, M.

1964. The lipid of plankton. [In Japanese.] Bull.
Jap. Soc. Sci. Fish. 30: 673-681.

633

A KEY TO THE AMERICAN PACIFIC SHRIMPS OF THE GENUS

Trachypeiiaeus (DECAPODA, PENAEIDAE),

WITH THE DESCRIPTION OF A NEW SPECIES

Isabel Perez Farfante'

ABSTRACT

Study of American Pacific members of the genus Trachypertaetis reveals that variation in armature of
the telson includes not only movable spines, but also fixed spines and even no spines at all. It also con-
firms that the eighth somite bears two arthrobranchiae instead of one arthobranchia and one pleuro-
branchia. A new species, Trachypcnaeus fuscina, is described, the specific features of T. faoea Loesch
and Avila are presented, and a key to the five members of the genus occurring in the region, together
with their ranges, is included.

Along the Pacific coast of Latin America species
of Penaeiis are the inainstay of the shrimp fish-
eries; however, members of various other genera
contribute to the catches in significant quantities.
Among the latter, three Trachypevaeus have
been previously recognized: T. byrdi Burken-
road, T. shnilis pacificus Burkenroad, and T.
faoea Loesch and Avila. A fourth, noncommer-
cial species, T. hrerisutume Burkenroad, is also
found in the region. Burkenroad ( 1934a, 1938) ,
presented detailed descriptions of the taxa he
described, but the characters cited for T. faoea,
except color pattern, have not proven to be diag-
nostic. Since the commercial Trachypenaeus are
indiscriminately known by the common names
of "tigre" and "cebra," a definition of T. faoea
is needed.

The study of collections of American Pacific
Trachypenaeus has shown that yet another com-
mercial species of this genus occurs in the area.
It also pointed out a previously undescribed var-
iation in the armature of the telson, and con-
firmed the identity of the gills on the eighth
somite.

The measurement of total length is the linear
distance from tip of rostrum to posterior end of
telson, and that of carapace length is the distance
from orbital margin to midposterior margin of

' National Marine Fisheries Service Systematics Lab-
oratory, U.S. National Museum, Washington, D.C. 20560.

carapace. The ratio, length of posteriormost
pair of telsonic spines to width of terminal por-
tion of telson, is presented in the following man-
ner: length of spine/width of terminal portion
= average ratio {N, number of specimens:
range of variation).

GENUS Trachypenaeus ALCOCK

Trachypeneus Alcock, 1901: 15. — Burkenroad,

1934a: 49.— Burkenroad, 1934b: 73, 94.
Trachypeiiaeus.— Kuho, 1949: 391.— Ball, 1957:

202.
Type-species by original designation, Penaeiis

anchoralis Bate, 1881.

The telson of the genus Trachypenaeus was
described by Kubo (1949) as lacking fixed spines,
and by Ball (1957) as possessing several pairs
of lateral movable spines. Previously, Burken-
road (1934b) had proposed a grouping of the
genera of the subfamily Penaeinae in four series;
he defined the series Trachypenaeus as having
a variable number of mobile lateral spines on
the telson and characterized the series Parape-
naeus as possessing one to three pairs of movable
spines in addition to a fixed posterior pair, con-
sidering the presence of fixed spines on the telson
as a unique character for the latter series.

In the species of Trachypenaeus described be-
low, however, the posteriormost of the four pairs
of spines on the telson is fixed, and in Trachy-

Manuscrlpt accepted March 1971.
FISHERY BULLETIN: VOL. 69, NO. 3,

685

FISHERY BULLETIN': VOL. 69, NO. 3

penaeiis byrdi Burkenroad the telson lacks
spines. The telson of the members of the genus,
thus, must now be more broadly characterized
as having several pairs of lateral movable spines,
or several pairs of movable spines anteriorly and
a fixed posterior pair, or unarmed. Furthermore,
the evidence presented here indicates that the
character of the posteriormost pair of telsonic
spines is not a unique character of the series
Parape7iae2is.

The branchial formula of Trachypenaeus was
given by Dall (19.57) as follows: pleurobranch-
iae on somites IX to XII; a rudimentary arthro-
branchia on somite VII, anterior and posterior
arthrobranchiae on VIII to XII, and a posterior
arthrobranchia only on XIII; mastigobranchiae
(ejnpodites) on VII, VIII and XII [first, second
maxillipeds and third pereiopod] , sometimes also
on X and XI [first and second pereiopods] . All
American species possess this combination of
branchiae, including epipodites on the first and
second pereiopods, and, in addition, a vestigial
anterior arthrobranchia on somite XIII.

In Trachypenaeus. the anterior arthrobranch-
ia on somite VIII is considerably disiilaced dor-
sally, and appears to occupy the position of a
pleurobranchia; however, its attachment is on
the arthrodial membrane. In Figure 1 the open-
ings of the branchiae on somites VIII and IX,
together with the proximal parts of the second
and third maxillipeds, are depicted ; this figure
clearly shows that the two arthrobranchiae on
somite VIII are attached to the arthrodial mem-
brane, like those on somite IX, whereas the
pieurobi'anchia on the latter somite has its origin
on the pleural membrane.

Burkenroad (1934a; see also 1934b) divided
the genus Trachypenaeus into two subgenera,
Trachypenaeus and Trachysahtmbria, the latter
possessing epipodites on the first and second
pereiopods, and a thelycum with a median pocket
on sternite XIV; the former lacks these char-
acters. Later, Burkenroad (19.59) observed that
some members of Trachysalambria lack such
epipodites and, thus, questioned the "usefulness"
of his division. Recently, a number of species
from the Indo-Pacific have been described which
bear ejnpodites on the first two i)airs of i)ereio-
pods but the thelyca, as indicated by Racek and

Dall (1965) , difi'er fi'om that Burkenroad attrib-
uted to the members of Trachysalambria. Con-
sequently, more investigations are needed to in-
terpret the interrelationships of the species of
the genus. It should be i)ointed out, however,
that all American species of Trachypenaeus ex-
hibit the characters given by Burkenroad for
T rachysalamb ria.

Figure 1. — Trachypenaens fi(sciiia sp. n., 9 3.3 mm car-
apace length, off Barra de San Marcos, Chiapas, Mexico.
Dorsal view of proximal part of second and third maxilli-
peds and attachments of gills on arthrodial and pleural
membranes of somites VIII and IX (second maxilliped
has been displaced laterally), a. Podobranchia. b, b'.
Anterior arthrobranchiae. c, c'. Posterior arthrobran-
chiae. d. Pleurobranchia.

The spelling of the generic name used here,
Trachypcymeus instead of Trachypcnen.H as was
originally iniblished, is based on the decision
reached by the International Commission on Zoo-
logical Nomenclature, Opinion 864, 1969, Bull.
Zool. Nomencl. Vol. 25, Parts 4-5, \^. 138-147.

636

PEREZ FARFANTE: KEY TO AMERICAN PACIFIC SIIRIXU'S, GENUS Traihypmarm

Trachypenaeus jusciua SPECIES NOVA

FIGURES 1, 2, 3A, 4A-F, 5A, 6
•PINTO," "CEBRA," "TIGRE,"

Tmchypeneiis faoe Lindner, 1957 [part], women
nudum: 48, 49, 81, 145.— Crocker, 1967 [part] :
8, 57.

MATERIAL

Holotype.— 5, USNM 135403, off Cocodrilo,
Chiapas, Mexico, 22 m, October 31, 19G9, H. Ro-
mero and G. Gomez, 35.25 mm carapace length,
135 mm total length, ratio length of spine/width
of terminal portion of telson = 0.55.

Allotype.— d, USNM 135404, off La Tapada.
Chiapas, Mexico, 22 m, July 31, 1970, D. Palacios,
26 mm carapace length, 108 mm total length,
ratio length of spine'width of terminal portion
of telson = 0.80.

Paratypes.— Mexico. Oa.xaca. 8 $, IBUNM-
USNM,"Salina Cruz, May, 1961, E. Martin F.
1 S, INIBP, Santa Maria Xadani, Laguna Su-
perior, July 23, 1970, L Perez Farfante. 1 2,
USNM, off Las Chiches, 24 m, August 6, 1966,

Z. Ortiz and G. Gomez. 2 3 1V, USNM, Golfo
de Tehuantepec, July 14, 1963, I. Mayes. Chia-
pas. 32, USNM, off Barra de San Marcos, 27 m,
March 18, 1964, A. Guerra. 3 2 , INIBP-USNM,
off mouth of Rio Suchiate, 7-13 m, February 12,
1968, Romero, Ortiz, Sanchez, and Arias. 1 9,
USNM, off La Tapada, 7-9 m, February 5, 1968,
Romero, Ortiz, Sanchez, and Arias. 4 3 5 2,
INIBP-USNM, off La Tapfida, 22 m, July 31,
1970, D. Palacios. 5 2, INIBP-USNM, off Co-
codrilo, 22 m, October 31, 1969, H. Romero, and
G. Gomez. Ecuador. 1 2, USNM, off Playas,
September 2, 1962, fishermen. Perii. 2 2,
USNM, Caleta La Cruz, Tumbes, 70 m, E. M.
del Solar.

DESCRIPTION

Carapace pubescent (Figure 2) ; dorsum den-
sely covered by setae; paired bands of longer
setae flanking postrostral carina, from rostrum
to various levels in posterior third of carapace;
another band on dorsal side of antennal carina;
longer setae also along cervical, hepatic and
branchiocardiac sulci, and others forming patch-
es on orbital region and posteroventral portion

Figure 2. — Trachypenaeus fuscina sp. n. Lateral view, 9 33 mm carapace length, off Cocodrilo, Chiapas, Mexico.

637

FISHERY BULLETIN: VOL. 69, NO. 3

of anteniial carina; branchial region covered
with short setae; pair of small, bare, crescent-
shaped to semicircular areas- at anterior end of
posterior third of carapace, flanking postrostral
carina. Abdomen naked, except for elongate
patches of long setae on each side of mid-dorsal
carina on third to sixth somites, and two addi-
tional paired patches often present on sixth so-
mite, one dorsal and other ventral to cicatrices.
Telson (Figure 3A) with two pairs of longitudi-
nal bands of long setae, one along walls of median
sulcus, and other along lateral sulci.

Rostral teeth 6-7, first tooth situated imme-
diately behind orbital margin; epigastric tooth
at posterior end of anterior fourth of carapace.
Rostrum reaching as far as proximal fourth of
dorsal flagellum; basal portion ascending well
above level of carapace, and apical one-third, un-
armed portion, decreasing progressively in
height, and curving upward. Adrostral carina
slightly sigmoidal, ending about midway between
first rostral and epigastric tooth. Postrostral
carina strong, long, reaching almost to posterior
margin of carapace, higher anteriorly, bearing
elongate fossette, immediately behind midlength,
and several pits posteriorly. Orbital angle pro-
duced into rather broad orbital spine. Gastro-
orbital carina and orbito-antennal sulcus absent.
Postocular sulcus deep, extending posterovent-
rally to about level of orbital angle. Longitudinal
suture well marked, long, extending along two-
thirds of carapace or slightly more. Ti'ansverse
suture short, clearly distinct, situated at level
of coxa of third pereiopod. Antennal and hepatic
spines long and strongly acuminate. Antennal
carina prominent, extending to below hepatic
spine. Cervical sulcus shallow and short, not in-
tercepting longitudinal suture. Hepatic carina
and hepatic sulcus well marked, and inclined
anteroventrally, their length about one-third that
of carapace. Postcervica! line sinuous, extend-
ing from postrostral carina to near posterior end
of hepatic carina. Branchiocardiac sulcus feeble,
marked ventrally by obtuse carina. Pterygosto-
mian angle obtuse, its ventral margin sloping
posteroventrally before turning backwards.

Antennular flagella subequal, shorter than
either antennular ])eduncle or carajiace, slightly
longer in males than in females of same length,

and proportionally longest in subadult; ratio of
flagellar length to carapace length about 0.66 in
shrimp of 1.5 mm carapace length, ratio decreas-
ing with increasing length of shrimp to about
0.40 in shrimp with carapace length of 40 mm.
First .'egment of antennular peduncle with disto-
median boi'der produced into heavy, scalelike
projection densely covered with long setae; dis-
tolateral spine prominent, slender and sharp;
prosartema long, extending to distal end of seg-
ment; stylocerite attaining midlength of seg-
ment.

Antennal flagellum long, almost twice total
length of shrimp; scaphocerite reaching distal
end of antennular peduncle, elongate, its length
2'/-; times maximum width; lateral, thickened
margin ending anteriorly in strongly pointed
spine.

Third maxilliped surpassing carpocerite by as
much as dactyl and one-fourth of propodus; first
pereiopod reaching, at most, base of carpocerite;
second pereiopod surpassing distal end of car-
pocerite by as much as three-quarters of dactyl;
third pereiopod exceeding carpocerite by as much
as projiodus and one-tenth of carpus; fourth per-
eiopod extending to about same level as first; fifth
pereiopod very long and slender, exceeding car-
pocerite by entire length of dactyl, and surpass-
ing fourth by projiodus and four-fifths length of
carpus. Spine on basis of third maxilliped, and,
as in all members of genus, on first and second
pereipods. Epipodites on first and second
pereiopods deeply bifurcate, epipodites on second
maxilliijed and third pereiopod unfurcate; ves-
tigial anterior arthrobranchia on somite XIII.

Abdomen with middorsal carina extending
from posterior half of second to sixth somite,
carina low and rounded on second, rather acute
on third, and forming high and sharp keel from
fourth to sixth somites; fourth and fifth somites
with ])osteromedian V-shaped notch; sixth so-
mite bearing middorsal spine posteriorly, small
spine at posteroventral angles, and two cicatrices
on each side, anterior one sensibly longer. Telson
(Figure 3A) shorter than inner ramus of uropod,
with median sulcus deep anteriorly and well
marked posteriorly to base of terminal portion;
paired rounded carinae flanking median sulcus,
and sharp carinae bordering oblique, lateral

638

PEREZ FARFANTE: KEV TO AMERICAN PACIFIC SHRIMPS, GENUS Trathypiitratu!

5 mm

Figure 3. — Telsons. A. Trachypenaeus fuscina sp. n.,
5 33 mm carapace length, off Cocodrilo, Chiapas, Mexico.
B. Trnchypenaeus faoea Loesch and Avila, 9 37 mm car-
apace length, Ensenada de Garachine, Golfo de Panama,
Panama.

sulci; terminal portion (from mesial base of
posteriormost spine to apex) from relatively
short to long, its length relative to its width at
base ranging from 1.60 to 3.70; telson armed
with four pairs of lateral spines, posteriormost
pair fixed and long, ratio length of spine/width
of terminal portion = 0.70 (iV27: 1-0.50); other
spines movable and strong, posterior pair (lo-
cated at lateral base of longer fixed spines) rel-
atively long, anterior two pairs (located poster-
ior to midshoulder of telson) small, but usually
visible with naked eye.

Petasma (Figure 4 A, B) with large, hornlike,
distolateral projections, broad at base, curving
laterally, and opening dorsally near anterior
margin by long, transverse slit; posteroventral
wall of horns reflexed dorsally and produced for-
ward into membranous flap; distomedian projec-

tions short, overhanging distoventral aperture
of petasma. Ventrolateral lobule of petasma al-
most entirely cornified, including ventral wall
of horns and dorsally reflexed lateral margin;
proximomedian portion of lobule with rather
flexible strip, tapering to base of distal two-fifths
of median margin, there ending where corneous
sclerite, curving mesially, reaches margin; soft
elliptical area immediately distal to corneous
section of margin. Dorsolateral lobule bearing
narrow rib along proximomesial third, rib broad-
ening proximally and turning mesially at prox-
imal extremity resembling golf club. Dorso-
median lobule with narrow, distally bifurcate rib
at base of distomedian projection, its length
about one-third that of lobule. Length of pe-
tasma— from apex of distomedian projection to
proximal margin of dorsolateral lobule — almost
one and one-fifth times its width at level of disto-
lateral projections.

In males, posterior margin of sternite XIII
(Figure 4F) bearing large, elongate, subellipti-
cal to ovate median plate, latter with obtuse to
acute tip, and numerous marginal setae; anterior
half of sternite XIV with strong, subpyramidal
prominence, its anterolateral, ventromedially in-
clined edges often forming shelflike ridges.

Appendix masculina (Figure 4C-E) thick,
subcircular in outline, its length along midline
subequal to maximum width, and produced into
two proximolateral prominences; dorsal wall
cornified, except for distal and lateral margins,
these, together with ventral wall, rather soft;
entire, broad, median border setiferous, setae
continuing on distal margin forming narrow
band. Dorsal base of endopod with corneous,
roughly trapezoidal sclerite, bearing strong me-
dian rib articulating distally with appendix
masculina; rib with small setiferous depression
on distal portion of ventral surface. Accessory
sclerite on dorsolateral margin of endopod.

Thelycum (Figure 5A) with posterior part
bearing anterolateral, subtriangular, heavily
sclerotized projections; anterior part of sternite
XIV, with platelike base, projecting as median
prominence, and produced forward into pair of
lateral, elongate, tonguelike flaps, extending al-

639

FISHERY BULLETIN: VOL. 69, NO. 3

most to anterior margin of median plate; bases
of flaps strongly inclined dorsomedially, form-
ing depression limited posteriorly by promin-
ence; margins of flaps often reflexed ventrally.

Platelike portion of sternite XIV naked; its lat-
eral margins pronouncedly curving posterome-
sially, forming deep emarginations with pro-
jections fi-om posterior part; basal portions of

2 mm

J

1 mm

2 mm

J

Figure 4. — Trachypenaeus fuscina sp. n., r! 20 mm carapace length, off Cocodrilo, Chiapas, Mexico. Petasma:
A. Ventral view. B. Dorsal view. Appendix masculina and proximal portion of endopod: C. Dorsal view. D.
Ventral view (endopod displaced). E, Ventromedial view of appendix masculina. F. Sternites XIII and XIV.
G. Trachypenaeus faoea Loesch and Avila, f, 18 mm carapace length, Playa Rella Vi.sta, Panama, sternites XIII
and XIV.

640

PEREZ FARFANTE: KEY TO AMERICAN PACIFIC SHRIMPS, GENUS Trachypintatus

2 mm

Figure 5. — Thelyca. A. Trachypenaens fuscina sp. n., 9 34.5 mm carapace length, off Barra de San Marcos,
Chiapas, Mexico. B. Trachypenaens faoea Loesch and Avila, $ 32.5 mm carapace length, Ensenada de Garachine,
Golfo de Panama, Panama.

flaps setose. Median plate of sternite XIII large,
oval, strongly concave ventrally, with margin
tumid, and bearing setae; plate extending poster-
iorly joining dorsal wall of flaps, thus giving
rise to median pocket; latter bearing paired aper-
tures of internal seminal receptacles laterally
(Figure 6B). In impregnated females, median
pocket occupied by sclerotized, sperm-free,
brownish component of spermatophores, extend-
ing almost to anterior margin of median plate.
Hardened, glutinous material, extruded with
spermatophores, protruding through slit between
flaps, forming plug on ventral surface of flaps.
Internal seminal receptacles (Figure 6A, B)
consisting of paired, longitudinally arranged,
trilobed, membranous sacs: single, large, post-
erior lobe, dorsal to median pocket, extending
caudally almost to posterior margin of sternite
XIV; and two small lobes, one directed antero-
mesially, dorsal to median plate, and the other
laterally, dorsal to small hood of sternite XIV.

2 mm

2 mm

Figure 6. — Trachypevaeus fuscina sp. n. A. Seminal re-
ceptacles (dorsal view), 9 39.5 mm carapace length, off
Salina Cruz, Oaxaca, Mexico. B. Left seminal receptacle
(ventral view), 9 31 mm carapace length, mouth of Rio
Suchiate, Chiapas, Mexico.

641

FISHERY BLXLETIN: \0L. 69. NO. 3

Seminal receptacles derived from paired, deep
invaginations at anterolateral extremities of
sternite XIV. In impregnated females, seminal
receptacles enclosing main component of sperm-
atophores, consisting of thin walled sac contain-
ing subspherical masses of spermatozoa.

COLOR

Juveniles recently caught in inshore water of
Oaxaca, Mexico, light buff with brownish red
suffusion; transverse, dark reddish brown bands
on posterior part of abdominal somites; bands
convex anteriorly, with widest portion on mid-
dorsal line, extending ventrally and forming
patch on posterior half of pleuron. Preserved
adults (fresh ones not observed by me) with
distinct dark abdominal bands, similar to those
in juveniles.

SIZE

Largest specimen examined, ? 40.5 mm car-
apace length, about 150 mm total length, from
off La Tapada, Chiapas, Mexico, depth 7-9 m.
Males smaller than females, largest observed
i allotyije, 26 mm carapace length, 108 mm total
length.

DISTRIBUTION

T. ftiscina has been found in the Golfo de
Tehuantepec, along the coasts of Oaxaca and
Chiapas, Mexico, and in the Golfo de Guayaquil,
as far south as Tumbes, Perii. Although this
species and T. faoea are sympatric in the Golfo
de Guayaquil, apparently T. fuscina ranges
farther north, since T. faoea has not been found
along the southwestern coast of Mexico.

REMARKS

T. fnscina is veiy closely related to T. faoea,
but differs from it in several aspects — mainly
in features of the telson (Figure 3A). In T.

fuscina the posteriormost pair of spines is longer,
and fixed instead of movable, this being the only
member of the genus Trachypeyuieus with im-
movable spines on the telson; the anterior three
pairs of telsonic spines are stronger than in T.
faoea, particularly those spines at the lateral
base of the posteriormost pair; also the median
sulcus is well marked as far as the base of the
terminal portion of the telson. In T. fuscina the
platelike base of the anterior part of sternite XIV
in females (Figure 5A) is naked, and its lateral
margins curve strongly posteromesially, giving
rise to a deep emargination at the junction of
the plate with the posterior part of the thelycum
(sternite XIV). In males, the median plate of
sternite XIII narrows anteriorly, usually taper-
ing to a point (Figure 4F).

It should be pointed out that during copulation
in this species, as well as in T. faoea, the male
transfers to each seminal receptacle a very thin
sac containing the spermatozoa, which are
grouped into subspherical masses. These masses
are not individually transmitted to the seminal
receptacles as believed by Burkenroad (1934b),
a phenomenon considered by him to be typical
of the genus TrcLchypenaeiis.

ETYMOLOGY

Fuscina, h., = three-pronged foi"k — referring
to the trifid appearance of terminal portion of
telson.

Trachypenaeus faoea LOESCH AND AVILA

FIGURES 3B, 4G, 5B
"CEBRA," "TIGRE," "INDIO," "CARABALI"

T rachypeneus faoe Lindner, 1957 [part], nomen
nudum: 34, 35, 42, 43, 48, 49, 60, 61, 133, 134.
—U.S. Fish and Wildlife Service, 1962: 2, 6.—
Croker, 1967 [part] : 8, 19, 30, 39, 47, 57.

Trachypeneus faoea Loesch and Avila, 1964:
4-8, 16, 21, 24-28, fig. 8b, 13b.— Avila and
Loesch, 1965: 3, 5, 6, 9, 10, 16, 19, 20, 23, 24,
fig. 4b.

Trachypenaeus face. — Food and Agriculture Or-
ganization of the United Nations, 1965: 10.

642

PEREZ FARFANTE: KEY TO AMERICAN PACIFIC SHRIMPS, GENUS Traihyprnrarus

MATERIAL

Neotype.— ? , USNM 135398, Playas, Ecuador,
January 7, 1964, Ortiz, 28 mm carapace length,
110 mm total length, ratio length of spine/width
of terminal portion of telson = 0.25.

Panama. 7 <i 21 9 , USNM, Playa Bella Vista,
March 20, 1955, M. D. Burkenroad. 3 5 , USNM,
Ensenada de Garachine, Bahia San Miguel, 16 m,
April 18, 1967, Sliimada Sta. 14. 3 9, USNM,
4 km W of Punta Garachine, 24 m, April 18, 1967,
Shlmada Sta. 78. Colombia. 7 9 , USNM, Tor-
tugas Grounds, S of Buenaventura, 9 m, Sep-
tember 19, 1969, L. W. Knapp, Cacique Sta.
LK69-24. Ecuador. 22 9, USNM, Playas, Jan-
uary 7, 1964, Ortiz. 1 ci 4 9 , USNM, Boca de
Tenguel, April 14, 1966, Ansaldo.

TYPE MATERIAL

Loesch and Avila (1964) did not cite any ma-
terial in particular; however, as the title of their
work indicates, the specimens studied and illus-
trated in their keys were from Ecuador. Because
of the close similarities between T. faoea and T.
fiischm it seems mandatory that a neotype of
T. faoea be selected, so that no confusion will
arise as to the identity of the species of Loesch
and Avila. Therefore, a neotype is here desig-
nated from a lot of females of Trachypenaens
faoea collected in Playas, Ecuador, which was
identified and sent to me by the authors of the
species. Inasmuch as the combination of spe-
cific morphological characters of this species
have not been indicated previously, they are pre-
sented here.

"Trachypeneus faoe" first appeared in the
literature in the report of a survey of the shrimp
fisheries of Central and South America by Lind-
ner ( 1957) . This author grouped it with T. byrdi
as one of the "larger zebra shrimp," noting the
"blue-black" stripes on the abdomen and citing
various other common names. Lindner, obvi-
ously, did not intend to describe the species, and
did not include any specific character. He re-
ported "T. faoe" in the shrimp fisheries of the
American Pacific, from Mexico to Peru, includ-
ing El Salvador, Costa Rica, Panama, Colombia,
and Ecuador. Later (U. S. Fish and Wildlife

Service, 1962) the species was cited as one of
"medium and small" shrimp found in the catches
of Guatemala.

The original description of the species ap-
peared in the keys to the commercial penaeid
shrimps of Ecuador by Loesch and Avila (1964) ,
and was mistakenly ascribed to Burkenroad. As
stated by Avila and Loesch (1965), Burkenroad
had planned to describe the species, but had not
done so prior to the publication of their keys, nor
has his description appeared since. T. faoea was
distinguished from other penaeids found in the
Ecuadorian catches on the basis of four morpho-
logical characteristics and color pattern. The
following characters were cited: "No teeth on
ventral ]3ortion of rostrum. ... No well-devel-
oped dorsolateral sulcus on the posterior part of
the last abdominal segment. . . . Backward-
pointing dorsal spine on last abdominal segment
only. . . . Telson not armed with lateral arma-
ture." The first two characters are shared by
many species treated in their keys, and are actu-
ally supraspecific; the third character is common
to all but one (T. byrdi Burkenroad) of the
American Pacific Trachypenaeus, and the fourth
is inaccurate: T. faoea does possess small lat-
eral spines on the telson.

The color of the species was described as fol-
lows: "Tail section light anteriorly and dark
posteriorly on each abdominal segment .... No
distinctive patterns on second and third abdom-
inal segments, each segment similarly colored
with wide dark band covering % the width of
]iosterior part of each abdominal segment. More
than 1/2 of color of tail is dark (dark brown)."
An entire animal and a separate abdomen were
figured. In both illustrations the telson appears
unarmed. The figure of the entire animal is
accompanied by the rostral tooth formula.

—FT-. Of the characters cited, color is the only

one that appears to be typical of the species, and
it can only be applied to identification of fresh
or recently preserved animals. It is unfortunate
that circumstances prevented Loesch and Avila,
who dealt with large numbers of specimens, from
publishing a detailed description of T. faoea.

T. faoea is very closely related to T. fuscina,
and except for the following, the above descrip-

643

FISHERY BULLETIN: VOL. 69, NO. 3

2 mm

I I

Figure 7, — Thelyca. A. Ti-achypeitaeus brevistiturae Burkenroad, 5 21.5 mm carapace length, off Zacapulco, Chia-
pas, Mexico. B. Trachypenaeiis hyrdi Burkenroad, 9 27 mm carapace length, Golfo de Panama, Panama (syn-
type). C. Trachypenaeus similis pacificus Burkenroad, 9 25 mm carapace length, Archipielago de las Perlas,
Golfo de Panama, Panama (syntype).

tion of T. fuscina also applies to T. faoea: the
armature of the telson, the shape and pubescence
of the platelike base of the anterior part of
sternite XIV in females, the marginal contour
of the median plate of sternite XIII in males, and
perhaps color.

In T. faoea the posteriormost of the four pairs
of spines on the telson (Figure ."jB) are movable
instead of fixed, and shorter than those of T.
fuscina, the ratio length of spine/width of term-
inal portion = 0.40 (A^47: 0.75-0.20); the other
three pairs of movable spines, including those
located at the lateral base of the posteriormost
spines, are minute, actually microscopic. In T.
faoea the median sulcus of the telson is deep
anteriorly but hardly perceptible or indistinct
posteriorly.

In males of T. faoea the median plate at the
posterior margin of sternite XIII (Figure 4G)
usually varies from subtrajjezoidal (widest an-
teriorly) to suhorbicular. In females, the struc-
ture of the thelycum (Figure 5B) is similar to
that of T. fuscina; however, lateral margins of
the platelike base of the anterior part of sternite
XIV are almost straight, not or barely curving
posteromesially, forming about 90° angles with

projections of the posterior part; furthermore,
the lateral areas of that platelike portion are
studded with rather densely set setae, the latter
extending onto basal portions of the flaps.

Avila and Loesch (1965) described the color
of recently preserved juvenile specimens of T.
faoea as dark blue or purple with light uropods.
They noticed that specimens preserved for 2 days
in b'/r Formalin exhibit a clear, horse-shoe
shaped band on the first three abdominal somites,
which is open anteriorly. These observations
were based on material from Ecuador and differ
from those made by me on T. fuscina. Recorded
notes on color are so limited that conclusions in
regard to differences in this character between
the two species must await further obsei'vations
throughout their ranges.

DISTRIBUTION

Although this species has been reported from
as far north as the coasts of Guatemala, El Sal-
vador and Costa Rica, the collections available
to me are limited to the area from Panama to
Ecuador. Examination of additional samples of

644

PEREZ FARFANTE: KEY TO AMERICAN PACIFIC SHRIMPS. GENUS Traihyprnratui

"cebra," or "tigre" shrimp from Central and With the discoveiy of an additional species

South America will be necessary to establish the of Trachypenaens in the American Pacific, it

actual distribution of T. faoea as well as that of seems appropriate to present a key to the five

T. fuscina, both known by the same common members of the genus occurring in the region,

names. together with the range of each.

KEY TO THE AMERICAN PACIFIC SPECIES OF Trachypenaeus

1. Carapace with longitudinal suture short, not extending to hepatic spine. Third ma.xilliped
lacking spine on basis; first pereiopod bearing spine on ischium. Thelycum with median
plate armed with small anteromedian spine (clearly distinct in juvenile, barely perceptible
in adult) ; anterior part of sternite XIV shorter than posterior part, and not produced as
paired flaps (Figure 7A). Petasma with dorsal spinelike projection near apex of horn . .
T. hrevisuturae Burkenroad

(From off Punta Arenas, Golfo de California, to El Salvador).

Carapace with longitudinal suture long, extending posteriorly beyond hepatic spine. Third
maxilliped bearing spine on basis; first pereiopod lacking spine on ischium. Thelycum with
median plate lacking anteromedian spine; anterior part of sternite XIV longer than poster-
ior part, and produced as paired flaps. Petasma without projection near ajjex of horn .... 2

2. Spine present on posterior end of middorsal carina of last two, three, or four abdominal
somites. Telson unarmed. Thelycum with slit between flaps never reaching posterior part

of sternite XIV, and with median plate short, not reaching gonopores (Figure 7B)

T. byrdi Burkenroad

(From Guatemala to Golfo de Guayaquil)

Spine present only on posterior end of middorsal carina of last abdominal somite. Telson
ai'med with lateral spines. Thelycum with slit between flaps reaching posterior part of
sternite XIV, if not, with median plate long, reaching, or almost reaching, gonopores . . 3

3. Rostral teeth 7 to 10, usually 8 or more. Telson with proximal triangular patch of long
setae on each side of median sulcus. Thelycum with median ]3late not excavated, short,
and protruding ventrally on midportion. Anterior part of sternite XIV lacking platelike
base and bearing subrectangular flaps, extending only to posterior part of median plate
(Figure 7C) T. similis pacifinis Burkenroad

(From Bahia Concepcion, Golfo de California, to Tumbes, Peru)

Rostral teeth 6 or 7. Telson lacking proximal, triangular patches of long setae. Thelycum
with median plate strongly excavated. Anterior part of sternite XIV with platelike base,
and bearing paired, much elongate, tonguelike flaps, extending well beyond midlength of
median plate 4

4. Telson with posteriormost pair of lateral spines fixed. Thelycum with platelike base of an-
terior part of sternite XIV lacking setae on each side, its lateral margins strongly curving
posteromesially, forming deep emargination with posterolateral projections (Figure 5A) . .

T. fuscina sp. n.

(Golfo de Tehuantepec and Golfo de Guayaquil)

Telson with posteriormost pair of latei-al spines movable. Thelycum with platelike base of
anterior part of sternite XIV setose, its lateral margins almost straight, forming about

90° angles with posterolateral projections (Figure 5B) T. faoea Loesch and Avila

(From Guatemala to Golfo de Guayaquil)

645

FISHERY BULLETIN: VOL. 69, NO. 3

ACKNOWLEDGMENTS

In addition to the collections in the United
States National Museum (USNM), Smithsonian
Institution, material was obtained from the Ins-
titute de Biolog-ia, Universidad Nacional Auto-
noma de Mexico (IBUNM), through Alejandro
Villalobos F. and Jorge A. Cabrera, and the Ins-
titute Nacional de Investigaciones Biologico-
Pesqueras, Secretaria de Industria y Comercio
de Mexico (INIBP), through Amin Zarur and
Hector Romero. I wish to thank the above men-
tioned persons for their assistance and cooper-
ation. The two collections from Mexico have
been divided, one part deposited in the corres-
ponding Mexican institution and the other at the
USNM. I am indebted to Quinto Avila and
Harold Loesch for critical material from Ecua-
dor, and to Leslie W. Knapp for making avail-
able to me specimens from Colombia. Horton
H. Hobbs, Jr., Fenner A. Chace, Jr., and Bruce
B. Collette offered critical comments that con-
siderably improved the manuscript. The illus-
trations are by the artist Maria M. Dieguez,
National Marine Fisheries Service Systematics
Laboratory.

LITERATURE CITED

Alcock, a.

1901. A descriptive catalogue of the Indian deep-
sea Crustacea Decapoda Macrura and Anomala, in
the Indian Museum. Being a revised account of
the deep-sea species collected by the Royal Indian
Marine survey ship Investigator. Indian Museum,
Calcutta, V + 286 p., 3 pis.
Avila, Q., and H. Loesch.

1965. Identificacion de los camarones (Penaeidae)
juveniles de los esteros del Ecuador. (Identifica-
tion of the juvenile shrimp (Penaeidae) of the
Ecuadorian estuaries.) Bol. Cient. Tec. (Guaya-
quil) 1(3), 24 p.
Bate, C. S.

1881. On the Penaeidea. Ann. Mag. Nat. Hist.,
Ser. 5, 8: 169-196, pis. 11-12.

BURKENROAD, M. D.

1934a. Littoral Penaeidea chiefly from the Bing-
ham Oceanographic Collection with a revision of
Penaeopsis and descriptions of two new genera

and eleven new American specie.s. Bull. Bingham
Oceanogr. Collect. Yale Univ. 4, Artie. 7, 109 p.

1934b. The Penaeidea of Louisiana with a discus-
sion of their world relationships. Bull. Am. Mus.
Nat. Hist. 68: 61-143.

1938. The Templeton Crocker Expedition. XIII.
Penaeidae from the region of Lower California
and Clarion Island, with descriptions of four new
species. Zoologica 23 : 55-91.

1959. Addenda et corrigenda au Memoire XXV.
Penaeidae par Martin D. Burkenroad (pages 67-
92). In Mission Robert Ph. Dollfus en Egypte
(decembre 1927 — mars 1929), S. S. "Al Sayad."
Resultats scientifiques, S'^ Partie [contributions]
(XXIII-XXXIV), p. 285. Centre national de la
recherche scientifique, Paris.
Croker, R. S.

1967. The shrimp industry of Central America, the
Caribbean Sea, and northern South America. U.S.
Fish Wildl. Serv., Foreign Fish. Leafl. 74, 127 p.
Dall, W.

1957. A revision of the Australian species of Pe-
naeinae (Crustacea Decapoda: Penaeidae). Aust.
J. Mar. Freshwater Res. 8: 136-231.
Food and Agriculture Organization of the United
Nations.

1965. Informe al gobierno de El Salvador sobre la
pesqueria de camarones y los recursos camaro-
neros de El Salvador. Basado en el trabajo de
Robert W. Ellis, biologo de pesca de la FAO/
PAAT. Rep. FAO/EPTA 1936, 46 p.
KUBO, I.

1949. Studies on penaeids of Japanese and its ad-
jacent waters. J. Tokyo Coll. Fish. 86(1), 467 p.
Lindner, M. J.

1957. Survey of shrimp fisheries of Central and
South America. U.S. Fish Wildl. Serv., Spec.
Sci. Rep. Fish. 235, 166 p.
Loesch, H., and Q. Avila.

1964. Claves para identificacion de camarones
peneidos de interes comercial en el Ecuador.
(Identification keys for commercial Ecuadorian
penaeid shrimp.) Bol. Cient. Tec. (Guayaquil)
1(2), 29 p.

Racek, a. a., and W. Dall.

1965. Littoral Penaeinae (Crustacea Decapoda)
from northern Australia, New Guinea, and adja-
cent waters. Verh. K. Ned. Akad. Wet. Afd.
Natuurkd. Sect. 2, 56(3): 1-116, 13 pis.

U.S. Fish and Wildlife Service.

1962. Fisheries survey of shrimp fisheries in Guate-
mala, El Salvador and Nicaragua. U.S. Fish
Wildl. Serv., Mark. News Leafl. 74, 13 p.

646

ARTIFICIAL RIPENING OF MAATJES-CURED HERRING WITH THE AID
OF PROTEOLYTIC ENZYME PREPARATIONS

T. M. RiTSKES'

ABSTRACT

For manufacturing maatjes-cured herring, the herring caught in the North Sea or Irish Sea is suitable
only during months when the proteolytic activity of the appendices pyloricae is sufficiently high. For
instance, only North Sea herring caught from May to July has sufficient proteolytic activity for the man-
ufacture of a well-ripened product. For herring caught in other areas, this period may differ consider-
ably. The present work shows that it is possible to use herring caught in other seasons if protease
preparations are added to the fish together with salt. The herrings were examined organoleptically,
whereas the brines were examined by chemical analysis and by chromatography on Sephadex G-25. No
significant differences were found between naturally ripened herring and herring cured by the aid of
enzyme preparations. The lipase content of the preparation should be low enough in order to avoid the
formation of a fatty acid taste in the cured fish.

Maatjes-type cured herring, the fish product that
has been made for centuries aboard Dutch fish-
ing vessels, is usually made from North Sea
herring (Clupea harengus L.), and in latter
years from Irish Sea herring as well.

After being caught, the herring is gibbed and
salted promptly. "Gibbing" means the removal
of some of the intestines through an incision
below the left gill. It is essential that, at this
procedure, the appendices pyloricae are left in
the fish; according to Luijpen (1959) this organ
plays an important role in the formation of the
characteristic organoleptic properties of the
product. The particular taste and the soft con-
sistency are due to the action of proteolytic en-
zymes from the appendices pyloricae on the fish
flesh.

Since the content of proteolytic enzymes in
the fish varies with the seasons, the fish is suit-
able for the manufacture of maatjes-cured her-
ring only for a few months. Other variables
like age and size of the fish or its source may
also influence the protease content and in this
way restrict the suitability of herring for the
maatjes-curing process. For these reasons,
there is a demand for a manufacturing method

' Institute for Fishery Products TNO, IJmuiden, the
Netherlands.

Manuscript accepted March 1971-

FISHERY BULLETIN: VOL. 69, NO. 3, 1971.

which is less dependent upon the protease ac-
tivity of the appendices pyloricae.

The aim of our investigation was, therefore,
to find the conditions for obtaining an acceptable
maatjes-cured herring by the addition of pro-
tease preparations. In this way a product with
the desired organoleptic properties might be
manufactured from herring which have rel-
atively inactive appendices pyloricae and which
consequently cannot ripen in a natural way.

MATERIALS AND METHODS

Artificially ripened herring was made by add-
ing protease preparations and salt to gutted
fresh or frozen herring. The enzyme prepara-
tions were mixed with the salt before salting
the herring in the usual way, viz. mixing the
herring with a certain quantity of dry salt.
Shortly after the addition of salt, a brine is
formed which covers the fish entirely. After
storage from 7 to 31 days the fish was examined
organoleptically and the brines chemically. In
most cases the enzyme-treated herring was com-
pared with naturally ripened herring and with
eviscerated ("gutted") herring to which no en-
zyme preparations were added.

The purpose of the chemical analyses was to
gather information about possible differences

647

FISHERY BL'LLETIN: VOL, 69, NO. 3

between the natural and the artificial ripening-
process. These analyses included: assay of
total soluble nitrogen by the Kjeldahl method,
protein determination by the biuret method, and
determination of amino nitrogen (as a rough
measure for the amino acid content) . Assuming
that the soluble matter is evenly distributed be-
tween the fish and the brine formed, most of
the analyses were carried out in the latter.

Some of our experiments are described below.
Other experiments gave similar results and are
omitted here for ease of survey.

NATURAL RIPENING PROCESS

Frozen maatjes herring that had been caught
in the North Sea at the end of May were used.
The protein content was 16.49;^ and the fat con-
tent IS.S^r . Herring in this stage is normally
used for the preparation of maatjes-cured her-
ring.

The protein content was determined by the
Kjeldahl method; for the fat determination, the
Bligh and Dyer (19.59) method was used in a
modification according to Ederzeel and Ritskes
(1966).

Part of the herring was gibbed and part was
gutted. One part of salt was added to 20 parts
of herring (light salting). The fish was kept
at 3° C for 1 week.

In order to remove proteins which are assumed
to be of less importance in the study of the ripen-
ing process, the brines were heated for about 15
min at 80° C and then filtered warm over a
fluted filter paper. All analyses were carried out
with these clarified brines. In this experiment,
these analyses included a Kjeldahl nitrogen de-
termination, a measurement of the biuret value
according to Strickland, Freeman, and Gurule

(1961) and a determination of the amino nitro-
gen content according to the method of the Dutch
Food Law (1963). This latter method is based
upon two alkalimetric titrations to different end
points. The salt content in the brines was de-
termined by the Volhard method.

In order to elucidate the protein breakdown
process during ripening, gel chromatography
of the brine was applied; 0.8 ml of a clarified
brine was chromatographed on a Sephadex G-25
column- (length 44 cm, diameter 1.44 cm; frac-
tion volume 3.4 ml, elution rate 19.8 ml/h), dis-
■tilled water being used as an eluant. In each
fraction the biuret value and the absorbence at
280 nm (nanometers or millimicrons) were
measured. The results of the organoleptic eval-
uations and the chemical analyses are shown in
Table 1. The results of gel chromatography are
plotted in Figures 1 and 2. As could be ex-
pected, the values found in the brine of the gibbed
herring were considerably higher than in that
of the gutted herring.

TESTING OF TWO ENZYME
PREPARATIONS

Frozen spawning herring, caught at the end
of August in the North Sea were used. The
]irotein content was IT.Q'? and fat content

18.2';r.

Two enzyme preparations, Pr 8 and TG 21/63,
were tested. Their proteolytic activities were
determined according to Anson (1938), with
denatured hemoglobin as a substrate. Lipol>-tic
activity was determined on olive oil according
to Marchis-Mouren, Sarda, and Desnuelle

- Reference to trade names in this publication does not
imply endorsement of commercial products by the Na-
tional Marine Fisheries Service.

Table 1. — Results of organoleptic evaluation of naturally ripened maatjes-cured
herring and of analyses of brine in which herring ripened.

Organolept

c evaluotion

Analyses of the brine^

Variation

of the herrmg

Biuret value
(EsM X 1000 X
dilution factor)

Total N
(mg N/ml)

Amino N
{% w/v)

Flavor

Texture

Gutted Nontyptcal Moderately firm 900 4.4 0.133

Gibbed Good Optimal (soft) 1720 6.9 0.255
maatjes-flavor

' Solt conlent of brine was 10.5 ± 0.5% w/v.

648

RITSKES: ARTIFICIAL RIPENING OF MAATJES-CURED HERRING

;.o

t

-

(

1.6

-

(

Absorbonce ^^^

-

z 1-2

00

<

z
< 0,8

in

a
o

in

m
<

-

t

J

i

-

0.4

1

naaaiii

•

FRACTION NUMBER

Figure 1. — Chromatogram of the clarified brine of gutted
maatjes herring on Sephadex when herring were ripened
naturally.

( 1959 ) . Pr 8 had a proteolytic activity of 5.3 X
10^ U/mg and a lipolytic activity of 0.04 Des-
nuelle units/mg; for TG 21/63, these values were
9.1 X 10-^ and 18.7, respectively. These prepa-
rations, like all others used in this study, were
supplied by N. V. Organon, Oss, the Netherlands.
Details concerning these preparations are sum-
marized in Table 2.

The proteolytic activity of the preparations
was found by measuring the caseinolytic activity
at pH 7.5 and 35° C (Ruyssen, 1969) . The NF-
pancreatin reference standard was used (see
National Formulary XIII, 1970, p. 514). The
potency of the protease preparations is expressed
in terms of the minimum activity required by
NF XIII. The lipase activity was measured
by potentiometric titration of fatty acids hydro-
lyzed in an olive oil emulsion at pH 8.0 (Marchis-
Mouren, Sarda, and Desnuelle, 1959). The In-
ternational F.I. P. standard for pancreas lipase
was used as a standard (Ruyssen, 1969). One

unit forms 1 /umol fatty acid per minute under
the conditions of the assay.

In order to eliminate the effect of the intestinal
enzymes, the fish was gutted before the enzyme
preparations were added.

One part of salt was added to seven parts of
herring (w/w). The fish was kept at 15° C
for 3 weeks. Analyses were taken after 1, 2,
and 3 weeks; organoleptic evaluation took place
after 2 weeks.

Four variations were tested: (a) gutted; (b)
gibbed; (c) gutted and 2.0 g of Pr 8 per kg
herring added; (d) gutted and 1.2 g of TG 21/63
per kg herring added.

^ft^<^'

FRACTION NUMBER

Figure 2. — Chromatogram of the clarified brine of gibbed
maatjes herring on Sephadex when herring were ripened
naturally.

Table 2. — Enzyme preparations used in the e.xperiments.

Code No.

Origin and description

TG 21/63

Porcine pancreas powder

Pr 8

Porcine pancreas protease mixture with

low Itpase activity

Pr 34

Pancreas protease from sheep

Pr 35

Beef pancreas protease mixture

Pr 11/66

Same quality as Pr 8

W

Beef pancreas protease concentrate

CH 32/67 A

Same quality as Pr 8

649

FISHERY BULLETIN: VOL, 69, NO. 3
Table 3. — Results of organoleptic evaluations and chemical analyses from experiment using two enzj-me preparations.

Analyses of the brine'-

Voriation

Biuret value

Totol nitrogen

Flavor

Texture

After
1 week

2 weeks 3 weeks

After
1 week

2 weeks

3 weeks

Gutted

Salty; not ripened

firm

856

1,105

1,305

5.1

6.0

6.0

Gibbed

Not fully ripened

firm

__

1,320

8.1

„

Gutted + Pr 8

Ripened flovor

soft

2,620

3,670

4,320

10,0

11.8

13.4

Gutted + TG 21/63

Ripened flavor but
with an unpleosant
fatty acid flavor

soft

2,740

3,950

4,630

10.4

13.1

15.0

The salt content in the brine was 20 ± 2% w/v

The brine was analyzed as described earlier,
but with the omission of the amino-N determina-
tion.

The results of the organoleptic evaluations and
the chemical analyses are shown in Table 3.
They show that, by the addition of enzyme
preparations to gutted herring, it is possible to
obtain a product with "maatjes-cured" organ-
oleptic properties. A high lipolytic activity,
however, seems to be undesirable.

Both the biuret value and the total nitrogen
content in the brine increase during the ripening
period. There seems to be a relation between
the values found and the degree of ripening.

ARTIFICIAL RIPENING OF

FRESH SPENT HERRING WITH

ENZYME PREPARATIONS LOW IN

LIPASE ACTIVITY

After the herring has spawned, the uptake of
food steps and the fat content decreases grad-
ually to relatively low values, e.g., 5 to 8"^^ . Since
the proteolytic activity of the appendices plyo-
ricae is low in this ijeriod, the fish as such is un-
suitable for the manufacture of maatjes-cured
herring.

Fresh, spent herring, caught in February in
the Irish Sea were used. The protein content
was 17.1% and the fat content 5.2 '"^ .

Activity of the enzyme preparations tested is
shown in Table 4.

In view of the results obtained in the exper-
iment on spawning herring, the proteolytic ac-
tivity in the artificial maatjes-cured herring was
reduced in this experiment.

Six variations were tested: (a) gutted; (b)

gibbed; (c, d, e, f) gutted and added respec-
tively: 1.0 g Pr 34, 1.0 g Pr 35, 1.0 g Pr 11/66
and 55 mg W per kg of fish. The fish was kept
at 3° C for 3 weeks. One part of salt was added
to 10 parts of herring.

The brine was analyzed as described earlier.
In analyses of the herring, 30 g of ground her-
ring fillets were homogenized with 100 ml of
water in an Ultra-Turrax mixer. The mixture
was heated to 80° C and, after cooling to room
temperature, filtered through fluted filter paper.
In the extract thus obtained, the same analyses
as earlier described for the brine were carried
out. Gel chromatography was performed as de-
scribed earlier.

The results of the organoleptic evaluations
and the chemical analyses are shown in Table 5.

The brines of the variations "gutted" and
"gutted + Pr 35" were chromatographed. The
results are plotted in Figures 3 and 4.

With the preparations Pr 35 and Pr 11/66,
an acceptable product was obtained. W gave
rise to a good texture but developed le.ss flavor.
Pr 34 caused some ofll'-flavor, probably because
of the comparatively high lipolytic activity. It
seems to us that a lipolytic activity lower than
1 U/mg is desirable for a preparation which has
a protease activity equivalent to the minimum
activity required by NF XIII.

Table 4. — Proteolytic and lipase activities of enzyme
preparations.

Enzyme
preparotion

Proteolytic octiv
according to NF

ty
XIII

lipaso activity:
Desnuelle U/mg

Pr 34

1.6 X NF

1.8

Pr 35

1.0 X NF

02

Pr 11/66

3.0 X NF

02

W

20 X NF

0.6

650

RITSKES: ARTIFICIAL RIPENING OF MAATJES-CLRED HERRING

Table 5. — Results of organoleptic evaluations and chemical analyses from experiment with the artificial ripening
of fresh spent herring with enzyme preparations low in lipase activity.

Organoleptic evaluation

Chemical analyses

Flavor

Texture

In the brines^

In the extracts

Biuret
value

Total N

Amino N

Biuret
value

Total N

Amino N

Gutted

Nontyplcal

Moderately

firm

1,345

5.6

0.138

Gibbed

Nontypical

Moderately

firm

1,665

7.8

0.1 78

Gutted + Pr 34

Fair, but with
some off-flavor

Soft

2,690

8.8

0.255

Gutted + Pr 35

Fair

Too soft

2,900

9.1

0.252

Gutted + Pr 11/66

Fair

Soft

2,355

7.3

0.210

Gutted + W

Nontypical

Soft

2,460

8.2

0.224

0.017

* The salt content in the brines was 12 ± 1% w/v.

I »tt9*»

7S 30 3S

FRACTION NUMBER

Figure 3. — Chromatogram of the clarified brine of gutted
herring, without the addition of enzymes on Sephadex
G-25, in experiment on artificial ripening of fresh spent
herring with enzyme preparations low in lipase activity.

There exists a relation between the texture
of the herring and the biuret value found in the
brine. Between texture and total amount of
nitrogen in the brine no apparent relation was
shown. The ratio total N to amino N is about
the same in the brine and in the herring extract,
indicating that analysis of the brine give infor-
mation about the ripening process in the herring.

The chromatograms show that, in the brine
of the ripened herring, the amount of biuret-
positive material with larger retention times has
increased. This indicates that the amount of
small protein fragments increased.

The chromatographic pattern of the brine of
an artificially ripened herring (Figure 4) does

I »»t88ir'

■ »1»»§nnr

FRACTION NUMBER

Figure 4. — Chromatogram of the clarified brine of gutted
herring, with the addition of the enzjTne Pr 35, on Sepha-
dex G-25, in experiment on artificial ripening of fresh
spent herring with enzjTne preparations low in lipase
activity.

651

FISHERY' BULLETIN: VOL, 69, NO. 3

not differ essentially from that of the gibbed
herring brine (Figure 2). With the methods
used, no obvious difference was found between
the natural and the artificial ripening pro-
cess.

THE ARTIFICIAL RIPENING OF LEAN

HERRING AND ITS RELATION TO

CHANGES IN THE RESULTS OF BRINE

ANALYSIS

Fresh herring caught in the North Sea at the
beginning of April were used. The protein
content was 16.7%; fat content, 10.6%.

Two variations were studied: (a) gutted;
(b) gutted and with 1.0 g of Pr 35 per kg of
herring added. One part of salt was added to
10 parts of herring. The fish was kept at 3° C.
Samples for analysis were taken after 11, 17,
24, and 31 days. Organoleptic evaluation was
carried out after 24 days.

The brine was analyzed as described ear-
lier.

After 24 days at 3° C, organoleptic evaluation
showed: variation (b) had a soft texture and a
well-ripened flavor, whereas variation (a) was
still firm and had less flavor.

Results of chemical analysis of the brine are
plotted in Figure 5 and summarized in Table 6.

The salt content in the brines was 16 ± 2%
w/'v.

During the ripening process there is a steady
increase in biuret value, total N, and amino N
in the brine. This finding demonstrates again
the relation between these values and the degree
of ripening.

THE ARTIFICIAL RIPENING OF FRESH

LEAN HERRING WITH DIFFERENT

AMOUNTS OF A PROTEASE

PREPARATION

Fresh spent herring caught near the Hebrides
in August was used. This herring contained
17.4% of protein and 8.2% of fat.

In this experiment an enzyme pi-eparation
CH 32/67 A was tested, with a proteolytic ac-
tivity of 1.93 times NF XIII units and a lipolytic
activity of 0.3 Desnuelle units per mg.

One part of salt was added to 10 parts of fish.
Six variations were tested: (a) gutted; (b)
gibbed; (c, d, e, f) gutted and 0.5, 1.0, 2.0, and
5.0 g of CH 82/67 A added, respectively. The
fish was kept at 3° C for a month, then evaluated
and analyzed.

The brine was analyzed as discussed earlier.
Results are shown in Table 7.

J 8o 2500

7.0 itm.

z 6.0 > 1500

< a

° S.O m 1000

Total n
biuret value

AMINO N

Figure 5. — Results of analyses
of clarified brines of gutted her-
ring with and without addition
of Pr 35, in experiment on the
artificial ripening of lean herring
and its relation to changes in the
result of brine analysis.

30
DAYS STORED

652

F.ITSKES: ARTIFICIAL RIPENING OF MAATJES-CURED HERRING

Table 6. — Chemical analyses of the brines' in experiment
on artificial ripening of lean herring.

Brines

Gutted

Gutted + Pr 35

Biuret value:

after 1 1 days

625

1,915

after 17 days

1,010

2,320

after 24 days

840

2,520

after 31 days

960

2,820

Total N:

after 1 1 days

4.5

6.8

after 17 doys

5.2

7.6

after 24 days

5.1

8.3

after 31 days

5.7

9.3

Amino N:

after 1 1 days

0.131

0.183

after 17 days

0.165

0.215

after 24 days

0.146

0.238

after 31 days

0.160

0.282

^ The salt content in the brines was 16 ± 2% w/v.

An addition of 0.5 g of CH 32/67 A per kg
of herring is too low to obtain a well-ripened
product under these conditions. An addition of
1.0 g per kg, however, seems somewhat too high.
A suitable dose is probably the amount of pro-
tease that corresponds with a proteolytic activity
of 2000 mg-eq NF XIII powder per kg of herring.

In the brines (b) and (d) the same amino-
N contents were found, but the biuret value in
(d) was considerably higher than in (b). This
suggests that the action of the enzyme prepa-
ration is particularly the breakdown of muscle
protein to larger fragments, whereas the en-
dogenous enzymes show more peptidase activity.
This is in accordance with the observation that
an overdose of the enzyme preparation results
in a very soft rather than in a strong-tasting
herring.

SUMMARY

The addition of a certain quantity of a protease
preparation to herring which is unsuitable for
maatjes curing has a favorable effect on both
flavor and texture of the herring.

An addition of 2000 mg-eq NF XIII powder
per kg of herring is pi'oposed. Doubling or
halving this amount had a pronounced effect on
the organoleptic properties of the cured herring.
The lipase activity should be low.

In the brines the biuret value, the total N
content and the amount of amino N increase
gradually. There appears to be a distinct re-
lation between the biuret value in the clarified
brine and the consistency of the herring; the
same is true for the amino N content in the brine
and the flavor of the herring.

The ratio biuret value: amino N content
found in the brine was higher for artificially
ripened herring than for the naturally ripened
product. This finding indicates that the enzyme
preparations are poorer in peptidase activity
than the appendices pyloricae from the herring.

The protein breakdown in the artificially ri-
pened herring, however, does not seem to be
essentially diff'erent from that in the naturally
ripened herring. The patterns obtained by
chromatography of the brines over Sephadex
G-25 did not show any essential diflference.

ACKNOWLEDGMENTS

The author wishes to thank A. Ruiter and
L. G. Heeringa for their valuable assistance in
writing the manuscript.

Table 7. — Results of organoleptic evaluations and chemical analyses from experiment on artificial ripening of
fresh lean herring with different amounts of a protease preparation.

Variation

Organoleptic evaluation

Gutted

Gibbed

Gutted + 0.05% CH 32/67 A

Gutted + 0.10%

Gutted + 0.20%

Gutted -I- 0.50%

Chemical analyses of brines^

Biuret value

' The salt content in the brines was 12 ± 1% w/'

Total N

Salty; no ripened flavor

Firm

1,300

5.4

0.195

Nontypical

Moderately firm

1,640

9.0

0.328

Fair

Moderately soft

2,320

8.0

0.274

Fair

Optimal (soft)

2,875

9.2

0.334

Strongly ripened

Too soft

3,210

10.7

0398

Not tasted

Too soft

3,650

11.9

0.465

653

FISHERY BULLETIN: VOL. 69, NO. 3

LITERATURE CITED

Anson, M. L.

1938. The estimation of pepsin, trypsin, papain
and cathepsin with hemoglobin. J. Gen. Physiol.
22: 79.
Bligh, E. G., and W. J. D\-ER.

1959. A rapid method of total lipid extraction
and purification. Can. J. Biochem. Physiol. 37:
911-917.
Netherlands Government, "Warenwet."

1963. W.E.J. Tjeenk Willink, ZwoUe. 1.5th print.
Vol. 2: 5.
Ederzeel, L. p., and T. M. Kitskes.

1966. The fat content of fish meals. Some Dutch
studies. Fish. News Int. 5(6) : 48.

LuiJPEN, A. F. M. G.

1959. De invloed van het kaken op de rijping van
gezouten maatjesharing. Thesis, Utrecht.
Marchis-Mouren, G., L. Sarda, and P. Desnuelle.
1959. Purification of hog pancreatic lipase. Arch.
Biochem. Biophys. 83: 309-319.

R. RUYSSEN.

1969. Pharmaceutical enzymes and their assay.
International Commission for the Standardization
of Pharmaceutical Enzymes. A modified NF XIII
method is described. Universitaire Pers, Gent:
134-146.
Strickland, R. D., M. L. Freeman, and F. T. Gurule.

1961. Copper binding by proteins in alkaline solu-
tion. Anal. Chem. 33 : 545-552.

654

LABORATORY STUDIES OF PREDATION BY MARINE COPEPODS

ON FISH LARVAE

Kurt Lillelund'- - and Reuben Lasker'

ABSTRACT

A variety of marine copepods have been shown to fatally injure or capture and ingest young anchovy
larvae in the laboratory. Labidocera jollae, L. trit^piyiosa, and Pontellopsis occidentnlis (family Pontel-
lidae), species common to surface waters of the California Current, are effective predators of larval fish.
The copepods can be attracted by the vibrations of the larval tail beat and react by biting or capturing
the fish larvae. Cruising speeds for these copepods varies from 1.5 to 4 body lengths per second which,
coupled with continuous swimming behavior, results in extensive searching by the copepod for prey.
In laboratory experiments, when the ratio of larval fish prey to L. jollae female individuals was low
(<10:1 in 3500 ml), all of the larvae were killed in 24 hr where "killing" refers to both capture-in-
gestion and biting resulting in a fatality. If the ratio was higher, killing increased but rarely reached
100% mortality of the larvae. L. trispinosa males and females never killed all the larvae offered to
them in 24 hr in 3500 ml although more larvae were killed as the number offered was increased. In-
creased swimming and escape ability developed as anchovy larvae became older and were not caught or
bitten as effectively as younger ones by copepods. However, killing of larvae by P. occidentalis was un-
affected by the age of the larvae up to 3.5 days old.

When Arteinia salina nauplii were substituted for larval fish as prey for L. tri<spinosa, the amount
of grazing was proportional to the ratio of nauplii to copepods. If the number of Artemia nauplii was
less than 11-14/liter per copepod in 3500 ml all the nauplii were killed in 24 hr. When the density of
nauplii was increased, more were killed but never all of them. In experiments where nauplii and yolk-
sac larvae were offered together as prey the mortality of the larvae due to predation declined in pro-
portion to the increase in the number of nauplii provided.

Caloric requirements were calculated from oxygen consumption measurements and showed that only
1 to 4 anchovy lar\'ae are required per day per copepod to satisfy the metabolic needs of Labidocera,
depending on the species and the sex. This number is far less than can be killed or captured if the
density of larvae is high enough.

In large (140 cm) vertical cylinders larvae and L. trispinosa were distributed within 25 cm of the
surface in the dark. Data are presented which show that L. trispinosa and anchovy larvae also co-
occur in the upper few meters under the surface of the sea. This is probably also true for P. occident-
alis and L. jollae. No data are yet available on the relative density of predatory copepods and fish
larvae where they co-occur or their possible predator-prey interactions in the sea.

Huge mortalities of larval fish are known to oc-
cur in the sea. From the time of Hjort (1914)
these have been attributed mainly to the lack
of the proper food when the larvae begin to feed
(see review by Blaxter, 1969). Undoubtedly
other biotic and abiotic factors are also involved

' Institut fiir Hydrobiologie und Fischereiwissen.schaf t
der Universitat Hamburg, 2 Hamburg 50, Olbersweg 24,
Germany.

" This research was supported in part by a Grant
from the Deutsche Forschungs Gemeinschaft.

' National Marine Fisheries Service, Fishery-Ocean-
ography Center, La Jolla, Calif. 92037.

Manuscript accepted April 1971.

FISHERY BULLETIN: VOL. 69. NO. 3, 1971.

in larval fish mortality, but com])aratively little
work has been done to measure their effect.
Among the possible causes of larval-fish mortal-
ity, predation by other zooplankters may be an
important factor. Freshwater aquarists have
known for some time that copepods must be elim-
inated from fish rearing tanks or high mortal-
ities of young larvae or fry will occur (Davis,
1959). Lillelund (1967) reviewed the literature
pertaining to predation by freshwater copepods
on fish larvae and described the predatory be-
havior of cyclopoid copepods as he observed them

655

FISHERY BULLETIN: VOL, 69, NO. 3

in the laboratory. Zooplankters in general and
copepods in particular have been seen to devour
marine fish larvae. For example, in an early
study on the rearing of marine fish, Garstang
(1900) noted that the harpacticoid copepod Idya
furcata (= Tisbe furcata) was a larval-fish
predator. Subsequently Lebour (1925) from
her examination of living marine plankton,
concluded that a variety of zooplankters eat fish
larvae and noted that "many jellyfishes and
Pleurobrachia besides Sagitta and Tomopteris
will readily eat small fishes." Lebour also il-
lustrated the capture of an anglerfish larva
(Lophius piscatorius) by the copepod Anomalo-
cera Patterson i (family Pontellidae).

Despite this information on the predatory be-
havior of copepods, there is virtually no behav-
ioral information available on the ability of ma-
rine copepods to capture and ingest or fatally
injure fish larvae, although many marine cope-
pods are known to be carnivorous (Gauld, 1966)
and other incidental reports of copepods preda-
tory on marine fish larvae have been made
(Wickstead, 1965; Petipa, 1965). Furthermore,
the possible importance of predation on fish lar-
vae as it affects the determination of year class
strength through larval fish mortality has been
generally ignored, probably because of the lack
of pertinent quantitative laboratory and field
information.

In this study we present the results of exper-
iments designed to measure quantitatively the
ability of three jiontellid marine copepods, La-
hidocera trispi7iosa, L. jollae, and Pontellopsis
occidentalis, to capture or fatally injure larvae
of the northern anchovy, EngrauUs mordax, an
important commercial fish of the California Cur-
rent. The behavior of copepods and larvae
which bears on the susceptibility of the latter to
predation is also described in detail.

METHODS

Copepods and anchovy eggs were captured
with a 0.5-m-mouth-diameter plankton net
(0.333-mm mesh) towed at the surface in coastal
water off' San Diego, Calif., between March and
August 1970. The copepods were separated

from other plankton with a large bore pipette on
shipboard, diluted with surface water in liter
jars, and kept at sea water temiierature (about
15° C) in an insulated chest until returned to
the laboratory.

All experiments were ])erformed in 3500-ml
beakers in the dark because Lnbidocera were
]3hototactic and attracted to the light source and
Pontellojjsifi was inhibited in its attacks on lar-
vae in the light. In an earlier study on fresh-
water cyclopoid cope]5ods, Lillelund (1967) used
a constant level, continuous flow device which
we used also for maintaining marine copepods
in good condition in the laboratory (Figure 1).
However, it was more convenient to do all pre-
dation experiments in static water over a 20- to
24-hr period, since the copepods we investigated
swim continuously throughout the small volume
(3500 ml), obviating the need for continuously
circulated water. A constant temjjerature of
18° C was maintained in the beakers by placing
them in a running seawater bath.

Mortality of the larvae was measured by
taking the difference between the number of
larvae at the beginning of the experiment and
those remaining alive at the end. Some mor-
tality not associated with predation always oc-
curred, hence control vessels containing larvae
alone were always provided and the results of
experiments corrected for larvae dead of other
causes. In all experiments, this natural mor-
tality never exceeded 10';;.

Anchovy eggs were sorted in the laboratory
according to their stage of development and
newly hatched larvae were used as prey in the
predation experiments. When older larvae were
required they were reared according to the meth-
od of Lasker et al. ( 1970) , except that the rotifer
Brachionus plicatilis was substituted for snail
veligers as larval-fish food (Theilacker and Mc-
Master, in press).

Oxygen consumi>tion measurements were
made by Warburg manometry. Usually 18 to 22
copepods were put into 3 ml of seawater in a
Warburg flask and oxygen uptake monitored for
8 hr at 18° C. Dry weight of individual cojie-
])()ds was measured with an electrobalance

to ± 2 jLtg.

656

LILLELUND and LASKER: PREDATION BV MARINE COPEPODS

ii-D'

Figure 1. — Constant level device for maintaining copepods and fish larvae. The temper-
ature of the 3500-ml beaker (B) was kept constant with running seawater in a water
table (A) whose capacity was 610 liters. Plankton netting (0..333-mm mesh) was held
over the mouth of the 500-ml funnel (C) with a section of bicycle tire tube. Rubber
tubing showing constrictions as D and D' had screw-type clamps to regulate flow. E is
the drain. Note that the level of seawater is higher in the beaker than in the bath. The
drawing is not to scale.

MARINE COPEPODS CAPABLE OF
KILLING ANCHOVY LARVAE

Euaetideus acutus
Candacia bipinnata

Before choosing Labtdocera and PonteUopsis
for experimental work we tested a number of
copepod species for their ability to capture or
fatally injure newly hatched yolk-sac larvae of
the northern anchovy. For each test, five fish
larvae were isolated in 200 ml of seawater in a
Petri dish at room temperature (20° C) usually
with two or three copepods of a particular species
to be tested. Of the local copepod species ob-
served, the following fatally injured anchovy
larvae by biting them or captured and ingested
them:

Acartia dana and A. tonsa
Eiichirella rostvata and E. sp.
Labidocera jollae and L. trispinosa
Pleuromamma borealis
PonteUopsis occidentalis
Euchaeta acuta

Because the two species of Labidocera listed
above are common to waters adjacent to San
Diego and were readily available, most of our
experimental work was done with them. When
PonteUopsis occidentalis became abundant, we
also collected some information about its preda-
tory behavior relative to fish larvae.

Although capture and ingestion of fish larvae
was commonplace under laboratory conditions,
it is rare to find a copepod with a captured fish
larva in Formalin-preserved plankton. This may
be the result of the Formalin preservation com-
mon on shipboard which, we have observed, usu-
ally causes copepods to drop larvae.'

' We have found that if a copepod has captured a
larva it will retain the larva if both are transferred to-
gether to a slight melted depression in an ice cube with
a pipette and preserved with a drop of 3% Formalin.

657

FISHERY BULLETIN: VOL. 69. NO. 3

SWIMMING AND FEEDING BEHAVIOR
OF Labidocera

REACTION TO THE LARVAL TAIL BEAT;
BITING AND INGESTION OF LARVAE

We noted that individual Labidocera ignored
motionless fish larvae or floating eggs. How-
ever, when a larva beat its tail in the close vi-
cinity of a swimming labidoceran, the copepod
swam immediately toward the beating tail and
grasped the larva. The tail beat of the larva
was often stimulated by the chance touch of a
copepod's antenna. Figures 2a and 2b show a
L. jollae female which caught a 3-day-old ancho-
vy by the tail and partially ingested it. Figure 3
shows another larva caught behind the head

Figure 2. — (a) Labidocera jollae female, 3 mm long,
and a 3-day-old anchovy larva 6 mm long which was
captured by the tail and half ingested, (b) Enlarge-
ment of the head and setae of the copepod shown in 2a.

Figure 3. — The head of a Labidocera jollae female show-
ing a newly captured 3-day-old anchovy larva caught
behind the head.

by another female. Response to the larval tail
beat is typical of all the copepods we have ob-
served which attack fish larvae.

Often a copepod would capture, then drop a
larva, inflicting a wound by biting the thin epi-
thelium. The anchovy larval skin is only about
2 to 3 /i thick in the finfold and tail regions and
appears to be easily injured. In every instance,
a bite which damaged the larval skin resulted in
the death of the larva. Therefore, in our experi-
ments mortality due to a copepod was the result
of either actual capture and ingestion of a larva
or biting that resulted in damage fatal to the
larva. Hence, the number of larvae reported as
"killed" in an experiment is the sum of fatalities
due to biting and the number of larvae actually
ingested. For both sexes of each Labidocera
species the time of ingestion of anchovy larvae
varied between 6 and 25 min. In one instance
an L. trispinosa male caught and completely con-
sumed two larvae in 1 hr. If we increased the
number of larvae to six or more in a 200-ml
Petri dish containing two copepods, mortality
through biting alone increased and the time dur-
ing which a larva was held by a copepod varied
from a few seconds to minutes. For example, an
L. jollae female attacked six larvae in 50 min.
The individual larvae were held only 10 to 60 sec
and not ingested. All six larvae died subsequent
to the attack.

658

LILLELUND and LASKER: PREDATION BV MARINE COPEPODS

POSITIVE PHOTOTAXIS AND SWIMMING
SPEED

Labidocera jollae and L. trisplnosa are posi-
tively phototactic, and when confined to a beaker
of seawater illuminated from above, concentrate
at the water surface-beaker interface which is
the brightest area. Copepods were induced to
swim in the main body of water by wrapping
the beaker with black paper with 1 cm lapped
around the rim. This effectively eliminated the
bright area and resulted in random swimming
movements of the copepods near the surface.

Swimming distances of copepods were traced
for 3 min in two dimensions on a clear acetate
sheet laid over a glass plate on top of a 3.5-liter
beaker. The distances were measured with a
map measurer. Vertical movements were very
slight, thus negligible, in these experiments be-
cause of the highly phototactic behavior of the
individuals. Labidocerans can swim continually
over relatively large areas in short periods of
time (Vlymen, 1970). Comparative speeds for
individuals are shown in Figure 4 ; on the aver-

80r

o
O

Ql
UJ

a.
o
o

60-

40

E
u

20

-62

= =-22

-37

z^33

r

Figure 4. — Swimming speeds for individuals of Labido-
cera. Each small horizontal bar represents the speed
of one animal; the large bar is the mean speed.

age a L. jollae female swims 62 cm/min (3-4
body lengths/sec) and the male swims 22 cm/min
(1.5-2 body lengths/sec) . Both sexes of L. tris-
plnosa swim 33 to 37 cm/min (2-3 body lengths/
sec) . Although L. jollae females swim in a seem-
ingly random pattern, the males usually swim
in straight lines for a few seconds then swim
in circles and cover a small area intensively.

KILLING EFFICIENCY OF Labidocera

We discovered that if the ratio of anchovy
larvae to L. jollae females was low (<10:1),
all or almost all the larvae in 3500 ml would be
killed within 20 to 24 hr in the dark. Two ex-
periments were done which illustrate this. In
the first, 30 anchovy larvae were confined with a
variable number of L. jollae females (Figure 5)
resulting in concentrations of larvae to copepods

2 4 6 8 10 12 14
LARVAE PER COPEPOD

Figure 5. — Mortality of Engraulis mordax larvae, 0 to
1 day old, resulting from predation by different numbers
of Labidocera jollae females. In each experiment 30
larvae were presented to 2 or more copepods in 3500 ml
for 21 hr. Thus where 3 larvae per copepod is indicated
on the abscissa, 30 larvae and 10 copepods were used;
at the other extreme 15 larvae per copepod indicates 30
larvae and 2 copepods. The unbroken line is the theor-
etical 100% lax'val mortality curve.

659

FISHERY BULLETIN: VOL. 69. NO. 3

of 3: 1 to 15: 1. In the other, only single L. jollae
females were tested and the number of larvae
varied to provide ratios of larvae to copepods
of 5:1 to 40:1 (Figure 6). The results were

- 30

5r

o

_J
o

>-
<

20

/

100% MORTALITY^/

o

/ 0

o

o

/ \ 1 1 1 1

D 10 20

30

40

§1

I-

_l -J

>- ^
> >-

o m

5°

5 lu

LARVAE PER COPEPOD

Figure 6. — Mortality of Engrmdis mordax larvae, 0 to
1 day old, resulting from predation by single Labidocera
jollae females. In each experiment 1 copepod was con-
fined with 5 to 40 larvae in 3500 ml for 20 hr. The un-
broken line is the theoretical 100% larval mortality curve.

similar in the two experiments; when the ratio
was approximately 10:1 or less, it was usual
for all larvae to be killed. When more than 10
larvae were available per copepod, more larvae
were killed per copepod but the mortality
dropped below lOOSf. In similar experiments
two L. trispinosa females were tested with larvae
to copepod ratios varying from 2: 1 to 15: 1. L.
trispinosa females were much less efficient than
L. jollae females and never killed all the larvae
presented to them in 24 hr (Figure 7). Males
of both species were similar in killing efficiency
to L. t)-ispinosa females. Based on these results,
further predation experiments were performed
over 20 to 24 hr using 30 larvae with two L. jollae
females or five males; experiments performed
with either sex of L. trispinosa had 30 larvae
and 5 copepods. The comparative predatory
ability of labidocerans is shown graphically in
Figure 8. The mean number of anchovy larvae
killed by L. jollae females was 15. L. trispinosa
males and females had mean kills of 4 and 2

liJ
<
>

DC
<

>-
>

O

X

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O
CVJ

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Q.
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CL
O
O

a:

LJ
CL

< Q
iij

oo

X

/

y'

/

/

/

/

/

/

/

/

.6
/
/
/

/ °

h /o
/
/
/
/
I l_

0 5 10 15

LARVAE PER COPEPOD

Figure 7. — The effect of increasing the density of larval
anchovies on the predatory behavior of Labidocera tris-
pinosa females. Each dot represents a separate experi-
ment with 2 or 3 copepods and from 5 to 45 larvae.

larvae respectively in 24 hr, markedly less than
L. jollae females. The high killing rate by L.
jollae females reflects the longer distances and
greater volume covered by them owing to tiieir
larger size. L. jollae females are approximately
0.2 mg dry weight, and males, 0.1 mg. Female
L. trispinosa average about 0.1 mg dry weight;
males, 0.09 mg.

EFFECT OF THE AGE OF THE LARVA ON
PREDATION BY Labidocera

We noted in our experiments that Labidocera
became less efficient in killing anchovy larvae as
the larvae aged. The anchovy larva is 2.5 mm

660

LILLELUND and LASKER: PREDATION BY MARINE COPEPODS

^30

-

CVI

*-^

o

0

o

Q.

-

UJ

o

o

Q.

(

)

O

O

<

!

(K 20

UJ

Q.

Q

(

>

UJ

_l

\

!

iC

^ 10

>

>

(T

<

0

_l

>-

>

O

c

s

X

^ 0

^

<

L jollc

7e i

h I6r

■15.4

-^"

L trispinosa %
L. jollae di L trispinosa <?

Figure 8. — Predation by individual Labidocera jollae and
L. trispinosa under comparable prey density. Experi-
ments were conducted in the dark for 24 hr in 3500 ml.
Each circle represents the results of one experiment.
The horizontal bar is the mean value for each series of
experiments.

long when it hatches from the egg. Yolk-sac
anchovy larvae have unpigmented eyes, lack a
mouth and gills, and the yolk is invested with
lipid (Bolin, 1936) ; when newly hatched the an-
chovy larva is very slightly buoyant. The newly
hatched larva remains motionless most of the
time at this stage and swims only sporadically.
As it develops, swimming activity increases, oc-
curring about 5 9r of the time at hatching to 25'^r
on the second day and 50 '^r by the third (John
R. Hunter, personal communication). Figure 9
indicates a rapid decline in predation in the dai-k
by L. trispinosa and L. jollae females as the larva
grows older, presumably as a result of the latter's
increased swimming and sensory ability. Ef-
fective predation is restricted therefore to yolk-
sac larvae.

14

12

10

I-

o
o

Q.
liJ
Q.
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cr

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UJ 8

<
>

q:
<

_i

>

o

X

L. jollae

L. trispinosa %

(2) (2)
o

"0 24 48 72 96 120 144
AGE OF ANCHOVY LARVAE (hr)

168

Figure 9. — The effect of the age of the anchovy larva
on predation by Labidocera jollae and L. trispinosa fe-
males. Each open circle is the mean of the number of
experiments shown in parentheses. The age of the larva
at the beginning of each experiment is given on the
abscissa.

EFFECT OF LARVAL ANCHOVY DENSITY
ON L. jollae PREDATION

Given 2 to 3 days, single L. jollae females can
kill by capture or biting all of 30 young anchovy
larvae in 3500 ml. This is shown in a mortality
curve (Figure 10) constructed from the results
of a series of experiments, each of which had a
number of newly hatched larvae (30 or less)
at the start confined with a single L. jollae fe-
male. The density of larvae per unit volume
(within the limits of these experiments) seemed
to have little or no effect on the kill rate until
there was only one larva remaining per 700 ml,
when the rate due to predation by the copepod
declined drastically. Our experience with pre-
dation experiments in 3500 ml volumes suggested
that anchovy larvae were randomly distributed
in this relatively small volume and that in the
dark, at least, each L. jollae female could almost

661

FISHERY BULLETIN: VOL. 69. NO. 3

35 r

24 48

HOURS

Figure 10.— Survival of 0- to 1-day-old anchovy larvae
in the presence of a single Labidocera jollae female.
The curve is a composite from a series of experiments
in 3500 ml starting at different larval densities per
copepod where the time was noted after the capture of
a number of larvae. The numbers in parentheses indi-
cate the number of experiments ending at each point.

completely search half this volume in 24 hr, re-
sulting in continuing random contact with and
killing of most, although not all, of the suspended
larvae when two or more L. joUae females were
present.

THE EFFECT OF AN ADDITIONAL PREY
ON LARVAL PREDATION BY Labidocera

Recent experiments by Brooks (1970) with
Labidocera trispinosa showed that this copepod
selects Artemia salina nauplii over copepod nau-
plii from the plankton. She concluded that Ar-
temia nauplii are selectively grazed because they
are relatively less mobile, hence more easily
captured.

We tested predation by L. trispinosa on Arte-
mia nauplii and found that grazing corresponded
roughly to the results we obtained when fish
larvae alone were killed, i.e., up to a certain
concentration all Artemia nauplii were killed
in the experimental container in the dark over
24 hr. Survivors were found only if the number
of nauplii exceeded 11-14 nauplii 'liter 'copepod.
As the density of nauplii was increased more
were killed. This result was the same whether
experiments were performed in 3500-ml beakers
or in 200-ml Petri dishes (Figure 11).

When Artemia nauplii in various concentra-
tions and 30 anchovy larvae were offered to-
gether to five L. jollae males or five L. trispinosa
males or females, larval mortality decreased in

100

CM

Q
O
0.
LlJ
Q.
O
<J

cr
iij

Q.

0 20 40 60 80 100

Artemia NAUPLII PER COPEPOD

Figure 11. — Mortality of Artemia nauplii due to Labido-
cera trispiiiosa female predation at different densities
of nauplii per copepod. Closed circles indicate experi-
ments done in 200-ml Petri dishes.

662

LILLELUND and LASKER: PREDATION BY MARINE COPEPODS

proportion to the number of Artemia nauplii
present. The results of these experiments are
shown in Figure 12. There was a 50% decrease
in mortality of larvae with L. trispinosa females,
L. jollae males, and L. trispinosa males when
the nauplii concentration was approximately 220,
150, and 100 nauplii /liter, respectively. The de-
crease in larval mortality is accentuated if Ar-
temia nauplii are offered to Labidocera when
older larvae are present. Fewer Artemia nauplii
need to be present to depress the predation mor-
tality on older larvae (Figure 13). The ease
with which Labidocera can captui'e Artemia may
make it less likely that fish larvae will be at-
tacked. As the larvae age, this effect is com-
pounded since it has become even more difficult
to catch larvae and hence relatively less taxing
for the copepod to take Artemia nauplii.

L. trispinosa $
L. jollae ^
L trispinosa a'

d 0 50 100 150 200 250

^ Artemia NAUPLII PER LITER (seawater)

Figure 12. — Predation by Labidocera jollae males and
both sexes of L. trispinosa on anchovy larvae when
Artemia nauplii were also available to the copepods.
Fifty percent reduction in larval mortality occurred
when Artemia nauplii numbered 220/liter with L. tris-
pinosa females, approximately 150/liter with L. jollae
males and 100/liter with L. trispinosa males.

CALORIC REQUIREMENT OF L. jollae
AND L. trispinosa

We noted that the vigor of Labidocera indi-
viduals declined with time if they were not fed
or fed only Artemia nauplii. For example, after
1 week in the laboratory the activity of copepods
fed only Artemia was diminished so that a cope-
pod's ability to capture larvae was about one-

50 100 150 200 250 300

Artemia NAUPLII (1 day old) PER LITER

Figure 13. — The effect of the age of the anchovy larva
and the addition of an extra prey (Artemia nauplii) on
larval mortality due to predation by Labidocera tris-
pinosa females.

half that of a newly caught copepod. Labidocera
died after 2 or 3 days of starvation. This was
preceded by a decrease in swimming activity
which was reflected in a lower respiration rate
and dry weight of individuals. In Figure 14 we
give comparative respiration rates and dry
weights for L. jollae females (a) newly caught,
(b) larval-fish fed, and (c) starved for 2 days.
These results show an enhanced respiratory rate
for fed and presumably healthier animals and a
drastic decline due to short term starvation.

STARVED FOR 2 DAYS

FRESH ANIMALS

FED ANCHOVY AND SARDINE LARVAE 2 DAYS

00 02 0.4 0.6 08 10 1,2

is\ Og/COPEPOD PER HOUR

STARVED 2 DAYS

FRESH ANIMALS

FED ANCHOVY AND SARDINE LARVAE FOR 2 DAYS

000 0.10 Oil 012 013 014 015

DRY WEIGHT (mg)

016

Figure 14. — Comparative oxygen consumption and indi-
vidual dry weight measurements of Labidocera jollae
females under starved and well-fed conditions at 18° C.

663

FISHERY BULLETIN: VOL. 69, NO. 3

Further comparisons of respiration rates were
made only between newly caught and larval-
fish fed L. jollae females, males, and L. tris-
pinosa males and females (Figure 15). In
each instance there was an increase in res-
piratory rate after feeding on anchovy larvae.
The caloric requirement of Lubidocera jollae and
L. trispinosa was calculated from oxygen con-

sumption data to estimate the number of larvae
which could sustain the copepod in a healthy
condition at 18° C (Table 1). In spite of La-
hklocera's ability to kill large numbers of fish
larvae or Artemia in a day, actual caloric re-
quirements may be met by ingestion of only a
few (1-4) larvae or nauplii (4-16).

2.5

•=> 2.0
O

1.5

cr

UJ

a.

o
o

Q.
UJ
Q.

o
o

CM

O 0.5

0.0

♦
0

J .^

,f(5P ,f,5P

Figure 15. — Oxygen consumption by newly caught (open
symbols) and larval-fish fed (closed symbols) labidocer-
ans at 18° C.

PREDATION ON FISH LARVAE AND
Labidocera BY Potitellopsis occidetitalis

Poiitellopsis adults and copepodites stages IV
and V can kill by biting or capture and ingestion
of anchovy larvae; older larvae (up to 3.5 days
old in our test) were killed by this copepod as
easily as yolk-sac larvae. Each stage V copepo-
dite killed three larvae per day on the average
and each adult female killed about 11 per day
(Figure 16) . We observed also that Pontelloijsis
attacked and ate Labidocera spp. when they were
confined to the same beaker.

CO-OCCURRENCES OF PREDATORY
COPEPODS AND FISH LARVAE IN THE SEA

In the laboratory we noted that 30 to 40%
of the Labidocera individuals resided in the up-
per 5 to 25 cm of 140-cm-deep, 17.5-cm-diameter
tanks — both in darkness and in the light. Yolk-
sac anchovy larvae occupied a similar stratum
because they are slightly buoyant. In the sea,
spawning by anchovies occurs mostly in the
upper 10 m but occasionally may occur relatively
deeply (Ahlstrom, 1959). This prompted us to

Table 1. — Oxygen consumption and the calculated number of
anchovy larvae required to sustain the respiratory requirements of
Labidocera jollae and L. trispinosa per day at 18° C. The oxycal-
orific equivalent of 1 jaliter of oxygen is 0.005 calorie. Yolk-sac
anchovy larvae weigh 0.01 mg dry weight and contain 0.054 calorie.
These data assume 100% digestive assimilation and an RQ ^ 0.8
for each copepod. Approximately four Artemia nauplii are cal-
orimetrically equivalent to one anchovy larva.

Species
and sex

Q Oj

/tliter/mg dry
weight/nr

Oa consumption
^liter/copepod/hr

Average dry weight
per copepod

Anchovy

larvae

required/day

Labodocera jollae .
/.. jollat
L. trijpinosa '•
L. trispinosa

11

II
7.7
4.3

2.0
1.0
0.94
0.40

0.19
0.095
0.12
0.092

664

LILLELUND and LASKER: PREDATION BY MARINE COPEPODS

I5r

g J^ 10

in o

lO o

I Q.

o ui

n

< UJ

id

o —
z ^

<

10.9

oo
o

3.1

ego

o

8
8o

oc'

,c»'

de

0'

_Q-

.-^^

=5^^

&^

^'

-d?'

,cje'

.^0'

l>5

Figure 16. — Predation by Pontellopsis occidentalis on
anchovy larvae 0 to 3.5 days old. Each horizontal line
indicates the mean value of the experiments shown with
open circles ; 30 larvae were provided to 1 to 6 copepods
in 3500 ml at the beginning of each experiment.

measure the rate of ascent of anchovy eggs to
determine the maximum depth at which spawn-
ing could occur and yet insure the presence of
yolk-sac larvae at the surface. In La Jolla sea-
water, salinity 33^;, and 17° C, anchovy eggs
rise 5 cm/min or 3 m/hr. Thus, with time from
spawning to hatching at 2 days, eggs spawned
as deep as 144 m would hatch at or near the
surface of the ocean, although spawning that
deeply is rare (Ahlstrom, 1959). During de-
velopment and, as they use up their yolk, an-

chovy larvae become almost neutrally buoyant
and start to sink very slowly in laboratory con-
tainers. Even so, after 2 days of development,
50 ""f of the laboratory-reared larvae were still
above the 30 to 40 cm depth.

Ahlstrom (1959) reported closing-net cap-
tures of anchovy larvae at a variety of stations
and depths in the California Current off Cali-
fornia and Baja California. He has kindly pro-
vided us with length distributions of anchovy
larvae taken at two stations, a night station,
5206-90.28, where over 500 larvae were taken,
and a day station, 5504-120.50, where over 5000
lai'vae were captured. The length of the larva
is roughly indicative of its age (Kramer and
Zweifel, 1971), and we have tabulated the depth
distribution of anchovy lai'vae at these stations
by length and age (Table 2) .

The depth distributions by age and length of
anchovy larvae indicate that 50 Cr or more of
anchovy larvae up to 3 weeks old are above 10 m
in depth. Fifty percent of the youngest class,
3 to 4.5 mm and 1 week old or less, were above
3.5 m during the day, and were slightly more
than 2 m deep in the night. Ahlstrom's data
also suggest that larvae of the Pacific sardine,
Sardinops caendea, Pacific mackerel. Scomber
japoniciis. and jack mackerel, Trachunis sym-
mefricus. all pelagic fish of the California Cur-
rent, may be similarly distributed.

Labidocerans are not diurnal vertical migrants
and seem to be confined near the surface of the
sea. Oblique tows with a plankton recorder
(Longhurst et al., 1966) were taken in an area
where Labidocera trispinosa and anchovy larvae
are known to occur. The results are shown in
our Table 3. The volume of each discrete sample
at a particular depth was small (4-6 m°) and the
zeros may simply indicate relatively low abund-
ance below the surface. Both tows, taken a day
apart in close pro.ximity to one another, showed
that L. trispinosa was mainly present above
10 m, as were anchovy larvae. Simultaneously
10-min neuston tows were taken which filtered
463 m" no deeper than 30 cm at the surface of
the sea (Table 4). The large number of Labi-
docera trispinosa and anchovy larvae in these
tows suggests that the upper 30 cm of the ocean

665

FISHERY BULLETIN: VOL. 69, NO. 3

Table 2. — Depth distribution of anchovy

larvae by

age and length at two stations.

5504-120.50

(day) and

5206-90.28 (ni

ght);

collected by

Ahlstrom (1959).

Length and age

of lorvoe

Average depth
of catch (m)

3.0-4.5 mm
0-7 days old

5.0-7.5 mm
8-14 days old

8.0-1 1.0 mm
15-21 days old

11.5-f-
214- do

mm
,'s old

no.

% of
total

no.

% of
total

no.

% of
total

no.

% of
total

Station 5504-120.50 (doy)

2

515

42

505

17

283

37

64

36

7

317

26

820

28

216

28

52

29

18

138

11

596

20

78

10

31

17

27

96

8

138

5

31

4

5

3

44

105

9

509

17

62

8

19

11

60

61

5

324

11

95

12

7

4

74

1

0

70

2

1

0

0

0

Total

1233

2962

766

178

Station 5206-90.28 (night)

2

65

50

52

40

44

20

35

36

7

54

42

48

37

73

34

25

26

17

10

8

15

12

50

23

14

14

27

0

0

15

12

49

23

23

24

Total

129

130

216

97

Table 3. — Vertical distribution of Labidocera trispinosa
adults and anchovy larvae at 32°55.1' (Station 1 at 0100)
June 3, 1970, and 32°45.8' (Station 2 at 2340) June 3.
Volume of water filtered for each discrete depth sample
in oblique tows were: Station 1, 6 m^; Station 2,
4.35 m^. No L. jollae or Pontellopsis occidentalis indi-
viduals were caught in these samples.

Depth (m)

Number of

L. trispinosa

adults

Number of

En^raulis mordax

lorvaa

Stotion I

0- 3

13

5

(7-11

mm long)

3- 7

0

I

7-15

0

1

15-60

0

0

Station 2

0-2

A

17

(7-10

mm long)

2- 7

17

n

(9-10

mm long)

7-15

2

1

15-25

0

1

25-60

0

0

is the area which should be examined for further
elucidation of this predator-prey relation-
ship.

The observations presented in this paper in-
dicate that marine copepods may be effective
predators on larval fish, at least in the sense that
a predator need not devour its prey but is equally
effective if it injures it mortally. Younjj pelagic
fish larvae are particularly susceptible to biting
zooplankters because they have an extremely
thin skin and are unable to survive once the skin
is punctured. Pontellid copepods, in particular
Labidocera spp., appear to have a well-developed

Table 4. — Numbers of Labidocera jollae, L. trispinosa,
Pontellopsis occidentalis, and Engraulis mordax eggs and
larvae taken in 463 m^ within 30 cm of the surface simul-
taneously with the oblique tows described in Table 3.

Species

Station 1

Station 2

L_ trispinosa

L. jollae

P. occidentalis

E. mordax

1152
336
112
226
(5-10 mm long)

6400

104

128

36

(10-12 mm long)

vibration sense which serves to orient the cope-
pod toward its swimming prey although this is
preceded by random searching. A fish larva
with its beating tail provides the right stimulus
to the copepod to initiate an attack when the
latter is close enough to detect the beat.

We have called attention to the vertical distri-
bution of Labidoceru in the sea and the apparent
co-occurrence of larval anchovies in the same
depth stratum. Unfortunately, quantitative
data on the density of predatory copepods or
other zooplankters as related to fish larvae have
yet to be made. It is our opinion that pontellid
copepods and fish larvae are concentrated in the
upper few meters and probably the ui)i)er few
centimeters of the sea and that observations of
this oceanic fine structure may reveal densities
of fish larvae to copepods which would implicate
predatory copepods (and possibly other zoo-
plankters) as important causes of larval fish
mortality.

666

LILLELUND and LASKER: PREDATION BY MARINE COPEPODS

ACKNOWLEDGMENTS

We thank James E. Smith and Donald L.
Seibert of the Scripps Institution of Oceanogra-
phy and Michael McMaster, Mrs. Gail Theilacker,
and Raymond E. Shuey of the National Marine
Fisheries Service, Fishery-Oceanography Cen-
ter, for their generous assistance during this
study.

LITERATURE CITED

Ahlstrom, E. H.

1959. Vertical distribution of pelagic fish eggs and

larvae off California and Baja California. U.S.

Fish Wildl. Serv., Fish. Bull. 60: 107-146.
Blaxter, J. H. S.

1969. Development: Eggs and larvae. In W. S.
Hoar and D. J. Randall (editors), Fish physiol-
ogy, Vol. 3, p. 177-252. Academic Press, New York.

BOLIN, R. L.

1936. Embryonic and early larval stages of the
California anchovy. Calif. Fish Game 22: 314-321.
Brooks, E. R.

1970. Selective feeding of some adult female cope-
pods on an array of food including Artemia and
naturally-occurring nauplii. U. Calif. Inst. Mar.
Resour., Res. Mar. Food Chain Prog. Rep., July
1969 - June 1970, Part 2, p. 56-74.

Davis, C. C.

1959. Damage to fish fry by cyclopid copepods.
Ohio J. Sci. 59: 101-102.
Garstang, W. R.

1900. Preliminary e.xperiments on the rearing of
sea-fish larvae. J. Mar. Biol. Assoc U.K. 6:
70-93.
Gauld, D. T.

1966. The swimming and feeding of planktonic
copepods. hi H. Barnes (editor), Some contemp-
orary studies in marine science, p. 313-334. Allen
and Unwin Ltd., London.

Hjort, J.

1914. Fluctuations in the great fisheries of north-
ern Europe viewed in the light of biological re-
search. Cons. Perm. Int. Explor. Mer, Rapp P.-
V. Reun. 20: 1-228.
Kramer, D., and J. R. Zvveifel.

1970. Growth of anchovy larvae (Engraulis mor-
dax Girard) in the laboratory as influenced by
temperature. Calif. Coop. Oceanic Fish. Invest.,
Rep. 14: 84-87.
Lasker, R., H. M. Feder, G. H. Theilacker, and
R. C. May.

1970. Feeding, growth, and survival of Engraulis
mordax larvae reared in the laboratory. Mar.
Biol. 5: 345-353.
Lebour, M. V.

1925. Young anglers in captivity and some of their
enemies. A study in a plunger jar. J. Mar. Biol.
Assoc. U.K. 13: 721-734.
LiLLELUND, K.

1967. E.xperimentelle Untersuchungen iiber den

Einfiuss carnivorer Cyclopiden auf die Sterblich-

keit der Fischbrut. Z. Fisch. Deren Hilfswiss 15:

29-43.

Longhurst, a. R., a. D. Reith, R. E. Bower, and D. L.

R. Seibert.

1966. A new system for the collection of multiple
serial plankton samples. Deep-Sea Res. Oceanogr.
Abstr. 13: 213-222.
Petipa, T. S.

1965. The food selectivity of Calaniis helgolandicus.
Invest. Plankton Black Sea, Sea of Azov. Akad.
Sci. Ukrainian. SSR, 102-110. Ministry of Agri-
culture and Fisheries Trans. N.S. No. 72.
Theilacker, G. H., and M. F. McMaster.

In press. Mass culture of the rotifer Brachionus
plicatilis and its evaluation as a food for larval
anchovies. Mar. Biol.
Vlymen, W. J.

1970. Energy expenditure of swimming copepods.
Limnol. Oceanogr. 15: 348-356.
Wickstead, J. H.

1965. An introduction to the study of tropical
plankton. Hutchinson and Co., London, 160 p.

667

TROPHIC INTERACTION BETWEEN THE SEA STAR Pisaster giganieus
AND THE GASTROPOD Kelletia kelletii

Richard J. Rosenthal^

ABSTRACT

The sea star Pisaster giganteus and the gastropod Kelletia kelletii are conspicuous inhabitants of the
sublittoral zone off San Diego, Calif. Diving observations over a period of 2'/2 years indicate that the
two species are trophically interrelated. P. giganteus, an opportunistic predator, and K. kelletii, a car-
nivorous scavenger, have been observed feeding together on common food items. The sea star appears
to be a major predator of the whelk, even though K. kelletii made up less than 10% of the diet of the
sea star. The whelk does not display an avoidance response in the presence of P. giganteus. Coexis-
tence between the two species is believed possible as long as K. kelletii does not become more preferred
prey of the asteroid.

Available information on the behavioral respons-
es of marine miollusks in the presence of preda-
tory sea stars has increased markedly within the
past few decades (Bullock, 1953; Feder, 1963,
1967; Margolin, 1964a, 1964b; Feder and
Christensen, 1966; Montgomery, 1967). How-
ever, most of these investigations have been lim-
ited to laboratory or intertidal observations.
Except for a recent study by Mauzey, Birkeland,
and Da>i;on (1968), the interactions between
mollusks and sea stars in the eastern Pacific
subtidal waters have not been investigated. Di-
rect sublittoral behavioral observations off the
west coast of north America have been hampered
by cold water and limited underwater observa-
tion time.

Assessment of predator-prey relationships be-
tween subtidal organisms has been limited
mainly to recording interactions between two
organisms under laboratory conditions. A spe-
cies-specific avoidance reaction or escape re-
sponse by a mollusk to a sea star is considered
one indication of a predator-prey relationship.
The evolution of such responses, and the recog-
nition of chemical stimuli emanating from either

' Westinghouse Ocean Research Laboratory, Annap-
olis, Md.; present address: Scripps Institution of Ocean-
ography, tjniversity of California, San Diego, Calif.
92037.

organism, suggests a long standing predator-
prey association. Mauzey et al. (1968) found,
however, that biochemical similarities between
a predator and other organisms could cause a
prey species to avoid the nonpredatory species
as well as the predator.

Gastropods which displayed no avoidance re-
sponses in the presence of specific sea stars have
been observed by Bullock (1953), Margolin
(1964b), and Feder (1967). Bullock (1953)
even suggested that nonresponsive mollusks are
characteristic of ecological situations where star-
fish predation on these species must be rare.

This paper examines laboratory and field data
obtained on the behavioral interactions between
the sea star Pisaster giganteus (Stimpson) and
the gastropod Kelletia kelletii (Forbes). In-
cluded are observations on the feeding, species-
specific responses, and predator-prey interaction
between the two species.

P. giganteus is reported from Vancouver
Island, British Columbia, to northern Baja Cal-
ifornia, Mexico (Fisher, 1930), while K. kelletii
has been found from Santa Barbara, Calif., to
San Quintin Bay, Baja California, Mexico (Ab-
bott, 1954). Both species are conspicuous and
abundant inhabitants of the nearshore subtidal
reefs off southern California. Bathymetric dis-
tribution appeared to be somewhat similar for
K. kelletii and P. giganteus off San Diego County,

Manuscript accepted March 1971.

FISHERY BULLETIN: VOL. 69, NO. 3, 1971.

669

FISHERY BULLETIN: VOL. 69, NO. 3

BAJA
V CALIFORNIA

Figure 1.— Location of the four subtidal observation areas off San Diego County, Calif.

670

ROSENTHAL; TROPHIC INTER.ACTION BETWEEN SEA STAR AND GASTROPOD

with the greatest concentrations of each between
2 and 40 m in depth.

The laboratory portion of the study was con-
ducted in the experimental seawater aquarium
of the National Marine Fisheries Service, Fish-
ery-Oceanography Center, La Jolla, Calif. I
made direct subtidal observations during day-
light hours while scuba diving off San Diego
County during the period January 1968-July
1970.

DESCRIPTION OF SUBTIDAL
STUDY AREAS

Four widely separated nearshore locations
within San Diego County were selected as field
study sites (Figure 1). These sites were se-
lected because they varied in depth, substratum,
and species composition.

DEL MAR

The study area was located within a stand of
giant kelp, Macrocystis pyrifera, which lies in
15 to 20 m of water about 1 km offshore from
Del Mar, Calif, (lat 32° 57' N, long 117n6' W).
The kelp bed is characterized by having a rel-
atively flat sea bottom with intermittent sand
patches and low profile siltstone ledges. The sea
floor is relatively homogeneous in appearance
except for the occurrence of these ledges, which
are less than 1.5 m in height. Pterygophora cal-
ifornica, a low standing brown algae, occurs
abundantly on the seaward edge of the M. pyrif-
era bed.

POINT LA JOLLA

The observation site off Point La Jolla (lat
32°51' N, long 117°16'30" W) was between 150
and 300 m due west of Point La Jolla. The area is
characterized by large boulders and undercut
sandstone ledges. It is a topographically heter-
ogenous substrate containing many microhabi-
tats. Portions of the area contain large sand-
stone formations which rise vertically to within
a few meters of the sea surface. The tops of

these formations are often covered by surf grass,
Phyllospadix torreyi. The observation area
ranged between 5 and 16 m deep because of
such pronounced vertical changes in relief.
Scattered throughout the area are two species
of perennial brown algae, Egregia laevigata and
Eisenia arbor ea.

QUAST ROCK

Quast Rock is situated on an offshore reef
about 630 m northeast of Point La Jolla (lat
.32°51'30"N; long 117°17' W). The observation
area encompassed approximately 225 m^ of this
reef. The rock is a sandstone formation with a
deep undercut and a cave on the northern end.
The substratum supports an extremely diverse
benthic invertebrate fauna, largely because of
the complexity of the habitat. The area is de-
void of giant kelp and only two species of brown
algae, Cystoseira osnmndacea and Agarum fim-
briatum, were common along the reef. The ob-
servation area ranged from 17 m on the top of
the rock to approximately 27 m on a lower
terrace.

POINT LOMA

The study site was located approximately 1.5
km offshore from Point Loma, Calif, (lat 32°42'
N; long 117° 16' W). The area is within a M.
pyrifera stand and the bottom is between 13
and 18 m deep. The substratum is predominant-
ly rock, siltstone, and sand. Portions of the
bottom are interrupted by channels and low re-
lief ledges. The shade area under the giant kelp
canopy supports an algal undergrowth composed
primarily of P. calif ornica, C. osmundacea, and
Laminaria farlowii.

FEEDING BEHAVIOR OF

Pisaster giganteus

P. giganteus appears to be an opportunistic
predator on the nearshore subtidal reefs off San
Diego County. It feeds primarily upon live
animals, although it has been observed scaveng-
ing on dead fishes and invertebrates. Thirty-
two identifiable species of invertebrates, with
pelecypods and gastropods making up about 80%

671

FISHERY BULLETIN: VOL. 69. NO. 3

of the total, were seen being preyed on by this
sea star at the four study areas (Table 1) . The
diet of P. giganteus is remarkably variable or
generalized over the four subtidal observation
areas, but within each habitat the diet is more

Table 1. — A list of prey species eaten by Pisaster gigan-
teus and Kelletia kelletii from January 1968 to July 1970.

Prey

(Closs)

Pilaster giganteus

Kdlctia kelUtii

Anomia peruviana (pelecypod)

+

Astraea gibberoia (gastropod)

+

Astraea undosa (gastropod)

+

Balanus tintinnabulitm (crustacean)

+

Botula (Adula) lalcata (pelecypod)

+

Bursa californica (gastropod)

Ceratostoma nuttallii (gastropod)

+

Chama pelludda (pelecypod)

+

Conus californicus (gastropod)

+

Diopatra ornata (polychaete)

+

Hinnit£s mtiltirugosus (pelecypod)

+

Jaton festivus (gastropod)

+

Kelletia kelletii (gastropod)

+

Lithophaga plumula (pelecypod)

+

Loligo opalescens (cephalopod)

+

(S)

Maxwellia gemma (gastropod)

+

Mitra idae (gastropod)

+

Mytiltis calijornianus (pelecypod)

+

Mytilus edulis (pelecypod)

+

Netastoma rostrata (pelecypod)

+

Ostrea lurida (pelecypod)

+

Panulirus interruptus (crustacean)

+

(S)

Paralabrax nebulifer (osleichlhyes)

+

(S)

Parapkolas californica (pelecypod)

+

Pelagia panopyra (scyphozoon)

+

(S)

Phyllochaetopterus prohfica (polychaete)

Pisaster giganteus (asteroid)

Platyodon cancellatus (pelecypod)

+

Pododesmus cepio (pelecypod)

+

Pterynotus trialatus (gastropod)

+

Pyura haustor (ascidian)

+

Serpulorbus squamigerus (gastropod)

+

Sphyraena argentea (osteichthyes)

+

(S)

Strongylocentrotus jranciscanus {ecW\r\o\6)

+

(S)

Strongylocentrotus purpuratus (echinoid)

+

(S)

Styela montereyensis (ascidian)

+

Taliepus nuttallii (cruslocean)

Ventricolaria fordii (pelecypod)

+

+ (S)i

+

+

+ (S)
+ (S)

+

+

+ (S)
+ (S)

+
+ ts)

+ (S)

+ (S)

+ (S)

-1-
+ .(S)

+ (S)

+

+ (S)

+ (S)

+ (S)

+

+ (S)

+ (S)

^ (S) = Scavenge.

selective or restricted (Figure 2). Variations
in the diet of P. giganteiis with each habitat
or microhabitat are attributed to the availability
and abundance of prey organisms, and prefer-
ences in the feeding behavior of the sea stars
in these four locations.

Predator success may, in many instances, be
dependent upon the predator's ability to feed
upon what is available in a given habitat. The
prey must be abundant enough to be utilized as
a food source and the predator must be capable
of selecting these forms. Variability in diet

120

I lO-
100-

90

30

n B ■ 1

,^^-^^'^^^'^^^^^^''

5TP'

ON^

PREY

Figure 2. — Comparison of the feeding behavior of
Pisastei- giganteus as observed in the four study sites
from August 1969 to July 1970.

with changes in sea star habitat has been dis-
cussed by Mauzey et al. (1968). Feder (1959)
suggested that differences in the diet of the
sea star P. ochraceus can largely be attributed
to changes in prey availability.

Evidence for opportunistic or adaptable pre-
dation by P. giganteus is drawn from variability
in diet within each habitat and a temporary
alteration in the feeding behavior of the Quast
Rock sea star population. On February 20, 1970,
12 out of 43 P. giganteus observed on or around
Quast Rock were found to be feeding. Six of
these individuals were eating Chama pellucida;
two, Balanus tintinnahulum; two, Se7'pulorbis
squamigems; and one, Pyura haustor. Altera-
tion in feeding was observed with the sudden
appearance of a potential food source during the
spring of 1970. Thousands of spawning squid,
Loligo opalescens, were observed in the proxim-
ity of Quast Rock on March 12, 1970. Spawning
had been reported to occur each year in the La
Jolla area (Fields, 1965), although "spent" in-
dividuals had not been sighted in the Quast Rock
location during the previous 12 months. Num-
bers of dying or dead squid were lying along the
bottom off Quast Rock. A total of 52 P. gigant-
eus was examined around Quast Rock ; of these,

672

ROSENTHAL. TROPHIC INTERACTION BETWEEN SEA STAR AND GASTROPOD

42 were feeding on dead L. opalescens. The P.
giganteus population had temporarily switched
from active predators to scavengers with the
availability of this abundant, though temporary,
food source. I returned to the study site on
April 10, 1970, and noted 6 out of 41 P. giganteus
to be feeding equally on C. pellucida, B. tintin-
nahulum. and H'mnites multirugosiw. With the
dead squid no longer present, the sea star pop-
ulation returned to feeding on the available prey
organisms of the reef.

Feeding preference experiments by Mauzey
et al. (1968) and Landenberger (1968) indi-
cated that the sea star P. ochmceus preferred
mussels to alternative food items offered the
sea stars. Landenberger (1968) also showed
that P. giganteus preferred the mussels Mytihis
edulis and M. calif oi-nianus to five other mollus-
kan species. Additional observations by Paine
(1969) suggest that few other prey are con-
sumed as long as mussels are readily available
to P. ochraceus. However, mussels were rarely
available to P. giganteus in the four subtidal
locations examined. If P. giganteus has a spe-
cific food preference in these subtidal locations,
then it must be adaptable or capable of change,
since each habitat or microhabitat varies some-
what in prey availability.

P. giganteus appears to exhibit a feeding
preference for prey that is either immobilized
or sedentary in habit, since these organisms
were eaten more frequently than motile forms.
Attached or boring bivalves, balanoid barnacles,
and sessile tube-dwelling mollusks were "pre-
ferred" or eaten most often by P. giganteus.

P. giganteus preys on K. kelletii more often
than any other motile gastropod, and yet the
whelks do not appear to be eaten in proportion
to their abundance or accessibility in these lo-
cations. Abundance and distribution of K. kel-
letii was determined by random sampling along
150 m transect lines in two of the locations.
The following densities were determined: Del
Mar 1.82/m2, and Point Loma O.TS/m^. Distri-
bution and movement of K. kelletii is, at least,
sometimes nonrandom, for the whelks were
found to be in an aggregated distribution pattern
in each of these areas during late spring of 1970.
The distribution pattern of a motile organism

may reflect spawning or feeding interactions;
therefore, these results were compared with and
found to coincide with earlier data obtained
from the Del Mar kelp bed during the fall of
1968. During the reproductive season (Rosen-
thal, 1970) , numbers of K. kelletii occur in com-
munal spawning groups, and yet predation by
P. giganteus did not appear to increase with the
availability of the whelks in these locations.

FEEDING BEHAVIOR OF

Kelletia kelletii

K. kelletii is basically a carnivorous scavenger,
although it has been observed feeding on live
sedentary polychaetes. As a scavenger, it ap-
pears to be attracted to almost any injured or
dead animal occurring on the sea floor (Table 1) .
Often, large numbers of K. kelletii have been
observed moving towards and/or feeding upon
a common food item in subtidal areas. The
food-finding ability of K. kelletii by distance
chemoreception has, on more than one occasion,
been a nuisance to spiny lobster fishermen in
some areas off southern California. These fish-
ermen usually bait traps with dead fish to attract
the spiny lobster Panulirus interruptus. Many
times, however, a single lobster trap may con-
tain dozens of K. kelletii which were attracted
to the trap by the "scent" of the bait.

K. kelletii feeds with an extensible muscular
proboscis which can be extended from the head
region during feeding. Food is ingested by a
muscular sucking action of the proboscis and a
rasping of the radula. The proboscis is capable
of extending approximately twice the length of
the whelk's shell; it is this extension which al-
lows K. kelletii to reach food items in depressions
or within the substratum. Pearce and Thorson
(1967) found that the proboscis of the gastropod
Neptunea antiqua can be everted and may be
extended to 21/4 times the length of the snail's
own shell.

The proportion of the whelk's diet which re-
sults from preying on live animals versus scav-
enging on carrion or dying organisms was not
determined. An aggregation of K. kelletii feed-
ing on a dead fish or mollusk attracts the atten-
tion of an underwater observer more often than

673

FISHERY BULLETIN: VOL. 69, NO. 3

Figure S.—Pisnster gi(janieus and Kelletia kelletii jointly feeding on a date mussel, Botula (Adula) falcata.
Note: The sea star's tube feet are touching the whelk's foot.

an isolate feeding. In many instances the snails
were believed to be feeding since the proboscis
was extended into a hole or within the substra-
tum, and yet rarely was the food item identified.
Most of the scavenger feedings by K. kelletii
attract more than one individual. In one in-
stance, 8.5 K. kelletii were clustered around and
feeding on a dead bass, Paralabrax sp., off Point
Loma. Aggregate feedings on carrion or dying
animals appeared to be the usual mode of feeding
in these subtidal areas.

CONVERGENT FEEDING BEHAVIOR

A unique and yet reoccurring behavior pat-
tern has been observed in those subtidal habitats
where both species are found. P. giganteus and
K. kelletii converge and attempt to feed on a
common prey organism at the same time ( Figure
3). Usually P. giganteus began to feed first,
with the whelks grouped around the sea star
(Figure 4). In many instances K. kelletii were

674

ROSENTHAL: TROPHIC INTKRACTIOX BETWEEN SEA STAR AND GASTROI'On

Figure 4. — Convergent feeding behavior between Pinaster giganteus and Kelletia kelletii
21 m underwater off Point La Jolla, Calif. Tlie sea star is eating a Chama pellucida,
while three whelks are attempting to get to the prey.

675

FISHERY BULLETIN: VOL. 69, NO. 3

partially underneath or even crawling over the
sea star attempting- to get to the food item, and
at times a feeding sea star would also be grasping
from one to four K. kelletii. A few of these
interspecific feedings were quite distinct in ap-
pearance, especially when both species were
scavenging larger prey such as dead fishes.
Three P. gigante.us and 28 K. kelletii were ob-
served feeding simultaneously on a dead barra-
cuda, Sphyraena argoitea, off Quast Rock on
December 31, 1968. However, most of the feed-
ing convergences observed were not as obvious
as this; usually they involved only a single sea
star and two or three whelks. Convergent
feeding behavior has been noted 65 times in
these four locations over a 2-year period. On
one occasion, five separate convergent groups
were observed within a 400 m- area off" Point
Loma.

Direct competition for food was most evident
when both species were scavenging carrion or
moribund organisms. However, in situations
where P. gigantens had captured or killed live
prey, K. kelletii was rarely observed with its
proboscis extended into the prey. It is probable
that feeding by the whelk usually takes place
on a secondary basis after the sea star has de-
parted. The percentage of prey that is left un-
eaten by P. giganteus following a feeding is
unknown.

These convergent feeding groups were not
limited to K. kelletii and P. giganteiis. K. kelletii
has been observed feeding interspecifically with
two other sea stars, Dennasterias imbricata and
Pisastei- brevispimis. Other scavenging or car-
nivorous types of epibenthic invertebrates which
have been found in these sea star-whelk feeding
groups include the gastropod Mitra idae and the
hermit crab Pagvristes ulreyi.

PREDATION ON Kelletia kelletii

There have been few natural predators of
K. kelletii rejiorted in the literature. The moon
snail, Polinices leivisii, was observed by Mac-
Ginitie and MacGinitie (1949) to have drilled
and eaten a live K. kelletii in a laboratory tank.
Juvenile K. kelletii were found in the stomachs

of young pile perch, Rhacochilus vacca, by Lim-
baugh (1955) . Three predators of K. kelletii ob-
served during diurnal hours in these subtidal lo-
cations were Pisaster brevispinus, P. giganteics,
and the cephalopod Octopus bimaculatus. How-
ever, only predation by P. giganteus is considered
at this time.

P. giganteus is a major predator of K. kelletii
on the nearshore reefs that I studied. During
the 214-year study i^eriod, 42 separate feedings
were observed in which, the sea star was in the
act of digesting a whelk; and 53 other times,
P. giganteus were found attacking K. kelletii.
Five separate attacks by P. giganteiis on K.
kelletii were observed in a single dive off middle
Coronado Island, Baja California (lat 32°25' N,
long 117°16' W) on December 3, 1969.

The sea star usually fed by attaching tube feet
to the substratum and the shell and the oper-
culum of the K. kelletii. P. gigaiiteus was usually
observed in a humped or arched position while
attacking and feeding on the whelk. In this
feeding position, a sea star can bring into play
a greater number of tube feet and exert max-
imum pull on the operculum and shell of the
whelk while still remaining attached to the sub-
stratum (Feder and Christensen, 1966). K. kel-
letii were not swallowed or ingested whole by
P. giganteus; instead, digestion appeared to take
place extraorally as is the case with other food
items. The whelk's operculum was either torn
away or pulled out of the shell opening by the
tube feet, and the sea star's stomach was inserted
into the shell. Bullock (1953) suggested that
predation on the intertidal snail Acanthina spi-
rata by carnivorous asteroids was slight, and that
possibly po.ssession of a heavy operculum ac-
counted for the nonresponsive behavior the snail
displayed in the presence of predatory sea stars.
The operculum of K. kelletii does not eliminate
sea star predation; however, the structure ap-
parently does increase the time necessary for an
asteroid to complete the feeding process.

The A', kelletii which were attacked by P.
giganteus ranged between 18 and 120 mm in
shell length (siphonal canal to the apex) ; how-
ever, approximately lO'i of these feedings in-
volved K. kelletii greater than 60 mm in length.
This size class, greater than 60 mm, was com-

676

ROSENTHAL: TROPHIC INTERACTION BETWEEN SEA STAR AND GASTROPOD

posed primarily of sexually mature individuals
(Rosenthal, 1970). K. kelletii less than 40 mm
in length were rarely preyed on by P. giganteus.
These smaller individuals are more secretive in
habit than larger mature A', kelletii. and they
characteristically burrow in the substratum.
Possibly the burrowing and cryptic behavior of
smaller A', kelletii decreases sea star predation
by reducing the number of contacts with preda-
tory P. giganteus. K. kelletii is considered to be
what Paine (1969) referred to as "secondarily
preferred prey," since invertebrate species other
than K. kelletii were found to be numerically
more predominant in the diet of P. giganteus at
these four locations (Figure 2).

Seasonal changes in K. kelletii predation by
P. giganteus was not considered to be a factor
in these subtidal regions. P. giganteus was ob-
served feeding on whelks throughout the year
with no noticeable change in the incidence of
predation.

RESPONSE OF Kelletia kelletii TO
Pisaster giganteus

From the number of reports of mollusks re-
sponding to predatory sea stars (Feder and
Christensen, 1966), I initially expected to ob-
serve an avoidance reaction by K. kelletii in the
presence of P. giganteus. To test this, 150 K.
kelletii between 15 and 138 mm in shell length
were brought into the laboratory and maintained
in either standing or circulating seawater. The
seawater temperature ranged between 16.0° and
19.9° C throughout the entire experiment. K.
kelletii were tested for any reaction which might
be exhibited in the presence of, or while touching,
P. giganteus. At times, the whelks responded
by siphon extension, shell rocking, or twisting,
and a slow sliding movement away from or in
the direction of P. giganteus. Many times no
shell movement was noted within a 10-min pe-
riod. Tests were conducted on whelks that were
inactive and on others that were moving, feeding,
or spawning. Each K. kelletii was used only
once or twice so that continual contact with the
sea star would not affect the whelk's reaction.

At no time did I note an escape or avoidance
response by A. kelletii in the presence of the
sea star.

Field observations were similar to those in the
laboratory; either A', kelletii did not respond
or, at times, they actually were attracted to P.
giganteus. The two species were usually found
close to one another on these subtidal reefs, and
contacts between the two probably are frequent.
During convergent feeding, the two species
touched or even crawled over one another ; how-
ever, at other times the A', kelletii and P. gigant-
eus occurred within a few centimeters of each
other even though neither species was engaged
in feeding. Paine (1969) found a perplexing
intimacy of association between three intertidal
gastropods and their major predator, the sea
star P. ochraceus. In contrast to these two sit-
uations, Bullock (1953: 137), stated that "In
those seashore situations where predatory stai'-
fish and gastropods both occur, it is notable that
the two are generally not seen close together."

One of the routine field experiments was to
pick up a P. giganteus underwater and place
it on or within a few centimeters of an indi-
vidual or group of A', kelletii. On only one occa-
sion was a reaction exhibited in K. kelletii out
of the hundreds of attempts to stimulate an active
response. In this one instance, a group of 11 A.
kelletii, which appeared to be searching for food,
was encountered 20 m underwater off Del Mar on
November 6, 1968. A large P. giganteus was
placed approximately 30 cm from the group of
whelks, and within a few minutes the sea star ap-
proached the K. kelletii. All of the whelks
moved away from the approaching sea star;
however, two of the K. kelletii were captured
by the sea star while the others moved off in a
similar direction. This reaction appeared to be
an avoidance response although it could have
been only random or chance movement on the
part of the whelks, regardless of the presence
of the sea star.

CONCLUSION

The existence of a predator-]jrey relationship
between a gastropod and a sea star is not un-
usual; however, the continual nonresponsive or

677

FISHERY BULLETIN: VOL. 69. NO. 3

at times even attractant behavior the whelk dis-
plays in the presence of this potential predator
appears to be unique. P. g if/an tens and K. kelletii
are trophically interrelated. Trophic interaction
is based on a predator-prey relationship and simi-
larities in the diet of both species. The prey
species consumed by P. giganteiis and K. kelletii
are similar; however, the method of feeding-, as
well as the physical condition of the prey, is
usually dissimilar.

These observations leave many unanswered
questions on the behavioral relationship between
a potential pre.v organism and a predatory sea
star. K. kelletii is preyed upon by P. giganteiis;
however, the whelk does not respond to sea star
contact as has been reported in other gastropod-
asteroid interactions. The sea star is a major
predator of A', kelletii. although the whelk makes
up less than 10 S^ of the sea star's diet. The
factors which limit predation of K. kelletii by
P. giganteus are unknown, since both species
are such conspicuous and extremely abundant
inhabitants of the sublittoral zone off San Diego
County. Feder (1963) studied intertidal sea star
predation on gastropods and noted that species
which exhibited avoidance responses in the
presence of asteroids were not preyed upon in
proportion to their abundance or availability in
the intertidal. K. kelletii does not exhibit avoid-
ance or escape responses in the presence of P.
giganteus, and yet it does not appear to be eaten
in proportion to its accessibilit.v or abundance
in subtidal areas off San Diego. A general feed-
ing preference by the sea star for attached or
nonmotile prey is thought to limit predation
on K. kelletii in these locations. The cryptic and
burrowing habits of juvenile K. kelletii may
further reduce ]3redation on the smaller whelks
by limiting the numl)er of contacts with j^reda-
tory sea stars. Paine (1969) suggested that co-
existence between a major predator and prey
is possible as long as the prey species does not
reach a more preferred status in the diet of the
I)redator.

It can only be speculated that the escape re-
sponse of K. kelletii in the presence of the sea
star has either not evolved or possibl.v was lost
through continual contact and convergence on
a similar trophic level. Perhaps other behavioral

activities such as feeding may be of greater se-
lective value to K. kelletii than is a species-spe-
cific avoidance response. Quite possibly the
whelk benefits more by not actively avoiding
P. giganteus than it would by continually run-
ning from this potential predator. The chances
for K. kelletii to feed on moribund or dead or-
ganisms would be increased, since both species
are attracted to these food items.

SUMMARY

1. Trophic interaction between the sea star
P. gigantens and the gastropod K. kelletii is
based on a predator-prey relationship and simi-
larities in the diet of both species.

2. P. giganteus, a highly opportunistic in-eda-
tor, was observed feeding on 32 identifiable spe-
cies of invertebrates. The sea star exhibited
a preference for prey which was either immo-
bilized or sedentary in habit, since these forms
were preyed upon most heavily.

3. K. kelletii, a carnivorous scavenger, usually
feeds on moribund or dead organisms that it
finds resting on the sea floor.

4. K. kelletii and P. giganteus feed together
on common food items. Convergent feeding be-
tween these two species was a recurring behav-
ioral pattern which was observed repeatedly in
the four subtidal areas.

5. P. giganteus is the major identifiable pred-
ator of A', kelletii off San Diego County; how-
ever, the whelk makes up less than 10 9f of the
prey observed to be captured by the sea star.
The whelk is believed to be of secondary im-
portance as food of the sea star, since inverte-
brates other than K. kelletii were utilized more
often.

6. A', kelletii did not display a species-si)ecific
avoidance or escape response in the presence of,
or while in contact with, P. giganteus.

7. Both species appear to be highly successful
and abundant organisms of the sublittoral zone,
and coexistence is believed possible as long as
predation by the sea star on A', kelletii is not
excessive.

678

ROSENTHAL: TROPHIC INTERACTION BETWEEN SEA STAR AND GASTROPOD

ACKNOWLEDGMENTS

I am grateful to the National Marine Fisheries
Service, La Jolla, Calif., for providing laboratory
facilities. This manuscript has benefited from
the critical reviews of J. R. Chess, W. D. Clarke,
and H. M. Feder. Thanks are expressed to R. E.
Bower and J. R. Chess for the help and assistance
they rendered in the field while diving.

LITERATURE CITED

Abbott, R. T.

1954. American seashells. Van Nostrand Co., Inc.,
Princeton, N.J., 541 p.
Bullock, T. H.

1953. Predator recognition and escape responses
of some intertidal gastropods in the presence of
starfish. Behaviour 5: 130-140.
Feder, H. M.

1959. The food of the starfish, Pisaster ochraceus,
along the California coast. Ecology 40: 721-724.
1963. Gastropod defensive responses and their ef-
fectiveness in reducing predation by starfishes.
Ecology 44: 505-512.
1967. Organisms responsive to predatory sea stars.
Sarsia 29: 371-394.
Feder, H. M., and A. M. Christensen.

1966. Aspects of asteroid biology. In R. A. Booloo-
tian (editor), Physiology of Echinodermata, p.
87-127. Interscience Publishers, New York.
Fields, W. G.

1965. The structure, development, food relations,
reproduction, and life history of the squid LoUffo
opalescens Berry. Calif. Dep. Fish Game, Fish
Bull. 131, 108 p.
Fisher, W. K.

1930. Asteroidea of the North Pacific and adjacent
waters. Part III, Forcipulata. U.S. Natl Mus.
Bull. 76: 1-356.

Frisch, K. V.

1941. Uber einen Schreck.stoff der Fischhaut und
seine biologische Bedeutung. Z. vgl. Physiol. 29 :
46-145.
Landenberger, D. E.

19G8. Studies on selective feeding in the Pacific
starfish Pisaster in Southern California. Ecology
49: 1062-1075.
Limbaugh, C.

1955. Fish life in the kelp beds and the efl^ects of
kelp harvesting. Univ. Calif., Inst. Mar. Resour.,
Ref. 55 - 9, 158 p.
MacGinitie, G. E., and N. MacGinitie.

1949. Natural history of marine animals. Mc-
Graw-Hill. New York, 473 p.
Margolin, A. S.

1964a. The mantle response of Diodora aspera.

Anim. Behav. 12: 187-194.
1964b. A running response of Acmaea to seastars.
Ecology 45: 191-193.
Marler, p., and W. J. Hamilton III.

1966. Mechanisms of animal behavior. Wiley, New
York, 771 p.

Mauzey, K. p., C. Birkeland, and P. K. Dayton.

1968. Feeding behavior of asteroids and escape
responses of their prey in the Puget Sound region.
Ecology 49: 603-619.

Montgomery, D. H.

1967. Responses of two haliotid gastropods (Mol-
lusca), Haliotis assimilis and Haliotis rufescens,
to the forcipulate asteroids (Echinodermata),
Pycnopodia helianthuides and Pisaster ochraceus.
Veliger 9: 359-368.

Paine, R. T.

1969. The Pisaster-Teguta interaction: Prey
patches, predator food preference, and intertidal
community structure. Ecology 50: 950-961.

Pearce, J. B., and G. Thorson.

1967. The feeding and reproductive biology of the
red whelk, Neptimea antiqua (L.) (Gastropoda,
Prosobranchia). Ophelia 4: 277-314.
Rosenthal, R. J.

1970. Observations on the reproductive biology of
the Kellet's whelk, Kelletia kelletii (Gastropoda:
Neptuneidae). Veliger 12: 319-324.

679

VARIABILITY OF NEAR-SURFACE ZOOPLANKTON OFF SOUTHERN
CALIFORNIA, AS SHOWN BY TOWED-PUMP SAMPLING

Charles P. O'Connell'

ABSTRACT

Variations in the density of near-surface populations of small copepods, large copepods, euphausiids, and
chaetognaths are described for an area of 6,000 square miles off the coast of southern California from
three cruises in the autumn of 1961 and two cruises in the autumn of 1962. Samples were collected with
a towed pump at a depth of 5 m. Approximately 162 samples, each representing a 1-mile transect, were
collected on each cruise.

Median densities for the cruises showed some significant differences for each species group. The fre-
quency distribution of densities within the area on individual ci-uises varied from positive skewness at
low general levels to relative symmetry at liigh general levels for the three crustacean groups, but was
skewed at all levels for chaetognaths. Within sampling blocks of 20 square miles, the range of density
varied with the median as log R = 0.35 + 0.8 log /!/. Range is greater than the median when the latter
is less than 50, but less than the median when it is higher than 50.

Euphausiids and large copepods showed greater diurnal change than small copepods and chaetognaths.

Dry weight concentration of samples, averaged over all cruises, was 17.3 mg/m^ for the day period
(0600-1800) and 25.1 mg/m^ for the night period. Most of the nighttime increase is attributable to the
euphausiid group.

The three crustacean groups, and dry weight, showed significant inverse trends with temperature, but
not with distance from land. The trends with temperature reflect events in 1961 but not in 1962.

These variations suggest that food potential of plankton for pelagic fishes may be appreciably greater
than indicated by general averages for the area, depending on the degree of selectivity and orientation
to small-scale features of distribution by the fishes.

Little is known about the effects of plankton
variability on the distribution, movements, or
rate of feeding of pelagic fishes which feed on
plankton. It has been demonstrated experi-
mentally (Ivlev, 1961) for some fishes that rate
of feeding varies not only with average density
but also with the degree of aggregation of food
organisms in an area. Plankton density is
known to vary diurnally (Gushing, 1951; King
and Hida, 1954) as well as seasonally and an-
nually, and there is evidence of aggregation in
the variation for both small and broad spatial
scales (Barnes and Marshall, 1951; Cassie, 1959,
1962, 1963). The plankton pump surveys re-
ported here were undertaken to obtain informa-
tion on variability and trends in variability for
four iilankton species groups commonly present
in near-surface waters along the southern Cal-
ifornia coast. Though surveys were limited to

' National Marine Fisheries Service, Fishery-Ocean-
ography Center. La Jolla, Calif. 92037.

the autumn seasons of 2 consecutive years, the
data should be a useful guide in evaluating the
food potential of near-surface plankton distri-
butions in the region.

COLLECTION OF SAMPLES

Samples were collected with the towed pump
and shipboard filtering system described by
O'Connell and Leong (1963). The 1.9-cm
(%,-inch) orifice of the pump pointed forward
to achieve a coring orientation, and the rate of
pumping (98 liters min) exceeded the passive
coring rate to produce in effect a 5.8-cm (2-inch)
diameter coring cross-section. Operation of the
system was essentially a matter of leaving the
pump in tow and running throughout a cruise
pattern with the incoming water stream diverted
to the scuppers except while traversing sampling
blocks, at which time the flow was directed
through the filtering apparatus. The stainless
steel filtering screen (105/li mesh) retained

Manuscript accepted April 1971.

FISHERY BULLETIN: VOL. 69, NO. 3, 1971.

681

FISHERY' BULLETIN: VOL. 69, NO. 3

virtually all organisms as small as 200/li in length
(O'Connell and Leong, 1963) or lOO/x in diameter
(Leong, 1967). The upper, size limit was less
easily defined, but organisms as long as 14 mm
were delivered at the filtering apparatus, though
the large individuals were often mutilated.

Five cruises were carried out, three in Sep-
tember to November 1961 and two in the same
period of 1962. For each cruise a pattern of
18 sampling blocks was selected from a possible
281 that covered an area of almost 6,000 square
miles (Figure 1). To insure reasonably good
coverage of the entire area, the ])opulation of

blocks was divided into three approximately
equal subareas and a set of six blocks was se-
lected at random from each. The blocks were
occupied by the shortest practical track from
northwest to southeast. Each cruise pattern
required about 2.5 days of vessel time.

Each sampling block was 51.8 km- (20 square
miles) in area, the only exceptions being some
of the blocks adjacent to the coast or to islands.
Nine 1.6-km (1-mile) samples were collected at
each block in a continuous series along two con-
necting sides (Figure 1, insert) and were pre-
served in Formalin for laboratory processing.

^

PT DUME

1

2

3

4

5

6

7

8

9

10

1

2

3

\

II

12

13

14

15

16

17

18

19

20

4

5

6

7

K

21

22

23

24

25

26

27

28

29

30

8

9

10

II

y

31

32

33

34

35

36

37

38

39

40

12

13

14

15

16

r" "^

41

42

43

44

45

46

47

48

49

50

17

18

19

20

21

22

23

24

25

Y

CALIFORNIA

51

52

53

54

55

56

57

58

59

60

27

28

29

30

31

32

33

34

35

36 137

^

K

61

62

63

64

65

66

67

68

69

70

39

40^^

h^

-^

42

43

44

45

46

47

48

49

^

h

71

72

73

74

75

76

77

78

79

80

51

52

53

r^'

54

55

56

57

58

59

60

61

"1

r\

Q^

81

82

83

84

85

86

87

88

63

64

65

66

L

69

70

71

72

73

74

75

76

77

\

89

90

91

92

93

94

95

96

78

79

80

81

82

83

84

85

86

87

88

89

90

91

92

93

K

1

2

3

4

5

6

7

8

9

10

11^

\

TYPICfl

startX

L TRANSECT PATTE

RN

12

13

14

15

16

17

18

19

20

21

22

\

1 ' 2 ' 3 ' 4
5

6

7

e

9

\

23

24

25

26

27

26

29

30

31

32

33

,1

35

36

37 38

39

40

41

42

43

44

45

46

47

48

49

50

51

52

53

54

55

56

57

5ffl^

59

60

61 62

63

64

65

66

67

68

69

70 1|

71

72

73

74

75

76

77

78

79

80

61

62

63

64

8J

86

87

88

89

90

91

92

EN

>*.

UN DIEGO

34°

33°

119*

118°

117°

Figure 1. — The sampling area and entire population of .sampling blocks;. Six blocks were randomly selected from
each of the three subareas for each cruise and occupied by the shortest route from north to south. Sampling
blocks are 4X5 miles and the insert shows the manner of transect sampling. Four of the nine samples from
each block were .selected randomly for organism enumeration.

682

O'CONNELL: XARIABILITY OF NEAR-SURFACE PLANKTON

Consecutive 1.6-km samples were separated by
shifting the incoming stream to a new filter every
6.5 min. Water volume, recorded for each sample
from a meter in the incoming line, averaged 636.7
liters (standard deviation 47.8) . Water temper-
ature of the incoming stream was recorded at
approximately the midpoint of each series of
block samples. Continuous thermograph records
indicated that surface water temperature did
not change appreciably during the sampling of
individual blocks.

SAMPLE PROCESSING

Four of the nine samples from each block were
randomly selected for the estimation of numbers
of organisms. Of the remaining five, one was
chosen at random to be reserved for special
purposes such as length and dry weight measure-
ments of species groups, and the other four were
pooled to obtain a dry weight value for the block.
Estimates were standardized as quantities per
m^ on the basis of the actual volumes of water
filtered in the samples.

Estimates for two size categories of copepods,
0.2 to 0.9 mm in length and all over 1.0 mm long,
and for euphausiids and chaetognaths, were
made by volumetric subsampling with replace-
ment, i.e., each subsample was returned to the
sample before the next subsample was drawn.
The volumetric subsampling technique yields
estimates of satisfactory precision only if or-
ganisms are randomly distributed in the sample
container prior to the removal of each sub-
sample. Simple stirring accomplished this for
all species groups except the small copepods,
probably because they were entangled in ph>i;o-
plankton present in the samples. Random distri-
bution was assumed to exist where the value sVx
did not exceed x'/^-l for a series of subsamples
(Holmes and Widrig, 1956). A random distri-
bution was achieved for the small copepods by
subjecting the sample to a few 1-sec bursts of
rapid stirring in a Waring Blender." However,
because this treatment fragmented some larger
organisms a two-step jn-ocedure was emiiloyed:

" The use of trade names is merely to facilitate de-
scriptions; no endorsement is implied.

all organisms except the small copepods were
estimated by subsampling following gentle stir-
ring; the sample was then agitated in the War-
ing Blender, after which the small copepods were
estimated by subsampling.

Estimates for the small copepods were always
based on subsamjjle counts totaling 200 to 300
from the sample. With the assumption of ran-
dom distribution, the number in the sample
should in all ca-ses be within 15'^ r of the estimate
for j) = 0.05 (Holmes and Widrig, 1956). More
than half of the sample estimates for the other
three species groups were based on counts of
30 or more, for which the number in the sample
should have been within 40'^r of the estimate.
For the remainder, where numbers counted
were low, examination was not extended beyond
subsamples totaling one-third the volume of the
sam|)le container, 2,000 ml.

In addition to the four species groups counted,
the samples contained larvaceans and small in-
vertebrate eggs (0.15-0.35 mm diameter), some-
times in moderately high numbers. Larvacean
tails and heads were separated, however, and in-
vertebrate eggs were not readily distinguishable
from the latter. Cladocerans and polychaetes
were generally absent or low in number, though
each occurred in high numbers in a few samples.
Fish eggs occurred rarely and in low numbers.

SIZE OF ORGANISMS

Length measurements for 10 day samples
(0600-1800) and 10 night samples are summa-
rized in Table 1 and Figure 2. Measurements
were total length except for euphausiids, which
were measured from the carapace behind the
eye to the junction of the abdomen and telson.
Data from day and night samples were pooled
for small copepods and chaetognaths but not for
large copepods and eujihausiids, which showed
appreciable size frequency differences for the
two periods.

The length-frequency distribution for the small
copepod group, composed largely of naupliar
and copepodite stages, is nearly symmetrical,
with the mean and the median close to the mid-
])oint of the ]3redetermined size range (0.20-0.99
mm long). Almost one-third of the organisms

683

FISHERY BULLETIN: VOL. 69, NO. 3

Table 1. — Length data for species groups.

■■

Mean
length

Median
length

Minimum
length

Maximum
length

mm

mm

77: m

777 771

Small copepods

0 58

0 56

020

0.99

Large copepods:
Day

Night

1.94
1.75

1 90
1.61

1.00
1.00

5.30
4.20

Euphousiids:
Day
Night

2.3
5.7

2 1
59

0.6
1.1

97
10.6

Choetognoths

6.4

5.5

20

14.5

were between 0.5 and 0.6 mm in lenjrth. It i.s
possible that the decline in numbers below the
median length was partly the result of increasing-
escapement with diminishing size, but the escap-
ing fraction, known to be negligible for sizes
above 0.4 mm, is assumed to be relatively small
for sizes down to 0.2 mm (O'Connell and Leong,
1963) . On this assumption the length-frequency
distribution is considered representative for this
size range of copepods.

The large-copepod group shows a modal shift
to smaller sizes at night, although the size range
and degree of skewness are not markedly dif-
ferent for the two periods. Organisms less than
1.5 mm in length were largely copepodites, while

SMALL COPEPODS

LARGE COPEPODS

40

n

30 -p

r 1 — 1

20. -

10-

n

r"

10

4 16 2

2 2

6 I

0 34 38 42 +

CHAETOGNATHS

0 12 :4 16

FiGliRK 2. — Length-frequency histograms of organisms
in four species groups, as determined from selected
samples. For large copepods and eu|)hausiids the wide
bars show day frequencies and the narrow Itars night fre-
quencies.

those between 1.5 and 3.0 mm were adult Calanus
helgolandiciw and Pamcalanus sp., with Centro-
payes sp. also present in the night samples.
Those larger than 3.0 mm were largely Rhincal-
anus s\). in both day and night samples.

The euphausiid group, which ai)peared to be
composed largely of Euphaiisia pacifica, though
Nyctiphanes simplex and Nematoscells dlfficlUs
were also in evidence, showed a marked shift
to larger sizes at night, obviously the result of
vertical migration. It is ai^ijarent from the sizes
involved that the day samples were composed
mostly of larval stages and the night samples
of .larval stages and juveniles, with few if any
adults. The largest individuals in the samples
were considerably smaller than the maximum
total length for the species, 25 mm (Boden,
.lohnson, and Brinton, 1955).

The i)ump samjiles did show some evidence of
fragmentation of larger euphausiids, and for this
reason the size frequency distribution for the
night period might be slightly biased in favor
of the smaller sizes, and estimates of numbers
sampled might be a little low.

Fragmentation probably involved far more
juveniles than adults. Samples from opening-
closing nets 1 m in mouth diameter taken in
sjiring and summer off southern California
(Brinton, 1962) showed adults to be scarce or
absent in the upper 10 m during the night as well
as the day. -Juveniles were predominant at this
stratum. Even at depths where adults were
most abundant at night — 40 m in one case and
140 to 280 m in another — they were only one-fifth
and one-tenth as numerous as juveniles. Night-
time obli(|ue hauls with nets 1 m in mouth di-
ameter off central Baja California indicated
essentially the same kind of vertical distribution
for euphausiid species in that area (Ahlstrom
and Thrailkill, 1963) . On the basis of such evi-
dence it seems probable that the size-frequency
distriljutions shown by the pump samples are
reasonably representative of the day and night
pojiulations near the surface, though certainly
not of the population in the entire water column.

The chaetognath group was composed largely,
if not entirely, of Scu/lttu eiuierltlca. and the size
range is jiroljably representative for the near-
surface population samiilcd. The size range for

684

OCONNELL: VARIABILITY OF NEAR-SURFACE PLANKTON

the species is 1.0 to 15.5 mm in lenj>-th ( Alverino,
1961), and the samples contained individuals
from 2.0 to 14.5 mm long.

VARIATION BETWEEN CRUISES

Table 2 shows characteristics of the frequency
distributions of all 1.6-km samples by cruise and
period of the day for the four species groups.
Median densities are lower than mean densities
in every instance but one, the nighttime period
for small copepods on cruise 5, indicating that
distributions for virtually all arrays show some
degree of positive skewness. Differences be-
tween cruises are described in terms of the me-
dians to avoid undue effects of extreme values
that can arise in moment measures on nonnormal
populations.

Nighttime median densities are higher than
daytime medians on all cruises for small cope-
pods and euphausiids, and on all but the fifth
cruise for large copepods. However, variation
was such that day and night medians differed
significantly (p<0.05, Tate and Clelland, 1957)
in only one instance for small copepods, three
instances for large copepods, and two instances
for euphausiids. Though none of these groups
can be considered to show consistently higher
densities at night for the area as a whole, real
differences occurred more often for the large
copepods and euphausiids than for the small
copepods. Day and night median densities for
chaetognaths do not differ significantly for any
of the cruises.

Daytime median densities do not differ sig-
nificantly between cruises for chaetognaths or
euphausiids, but those for small copepods and
large copepods differ significantly (?j<0.05) for
about half the comparisons. Nighttime medians
(Figure 3) show a pattern similar to the day-
time sets for the two copepod groups but show,
in addition, a number of significant differences
between cruises for the euphausiids and one dif-
ference for chaetognaths. Median densities of
the small copepods were significantly higher for

Figure 3. — The nighttime cruise medians for four species
groups shown by cruise date. Vertical bars indicate the
95% confidence intervals.

60

30

1 NOV. 1 DEC.

1 DEC.

1 OCT. 1 NOV.

CHAETOGNATHS
1962

1 DEC.

1 OCT

1 NOV.
MONTH

1 DEC.

685

FISHERY BULLETIN: VOL. 69. NO. 3

Table 2. — Summary of density estimates (no/m-') of 1.6-km samples by cruise, constituent group, and period of day.

Confidence limits^

P =

0.95

Mean

J

Median

Lower

Upper

Minimum

Maximum

C

ruiso 1, September 26-28, 1961, .V =

= 32 day, 40 night

Small copepods:

Day

2,569.7

987.4

2,275.5

2,023

2,552

1,210

5,233

Night

2,983.9

1,356.2

2,542.0

2,252

2,792

1,075

7,103

Lorge cope pod s:

Day

6.4

16.0

1.0

0

5

0

83

Night

72.8

95.5

42.5

22

73

a

500

Euphausiids:

Day

6.7

9.4

3.0

2

8

0

38

Night

52.2

37.1

41.5

32

57

10

172

Chaetognaths:

Day

84.2

122.9

21.0

S

105

2

488

Night

123.6

244.2

33.0

10

63

2

1,153

Cruise 2, October 9-11, 1961, .V =

24 day, 40 night

Small copepods:

Day

3,379.0

1,773.1

3,034.5

2,217

3,527

1,550

7,532

Night

3,953.0

1,620.0

3,325.0

2,942

4,257

2,142

8,118

Large COpepods:

Day

47.3

104.5

1.0

0

17

0

440

Night

102.7

67.3

101 0

60

128

S

250

Euphausiids:

Day

109

19.7

1.0

0

15

0

88

Night

48.2

31.7

42.5

35

50

7

145

Chaetognaths:

Day

132.7

135.3

121.5

3

198

0

420

Night

51.8

61.9

21.0

13

47

2

280

Cruise 3, November

6-18, 1961. A'

= 28 day, 40 n

ght

Small copepods:

Day

8,679.0

3,969.7

7,381.5

6,107

10,208

3,752

19,368

Night

10,577.8

3,060.7

10,281.0

8,673

11,812

4,948

17,568

Large copepods:

Day

18,3

21.1

10.0

5

18

0

92

Night

83.0

42.9

77.0

63

95

10

183

Euphausiids:

Day

15.5

13.9

13.0

S

22

0

48

Night

39.5

50.8

23.0

17

28

2

243

Chaetognaths:

Day

73.5

104.5

36.0

32

42

12

470

Night

44.5

38.8

32.5

23

50

3

188

Cruise 4, October 1.3, 1962, .V =

43 day, 26 night

Small copepods

Day

2,718.1

1,748.8

1,993.0

1.739

2,771

456

8,190

NighT

3,524.1

1,087.1

3,504.0

2,854

4,179

1,477

5,560

Large copepods:

Day

21.3

19.6

18.0

10

22

0

90

Night

33.6

29.5

21.5

11

50

3

99

Euphausiids:

Day

8.2

9.1

4.0

3

10

0

39

Nighr

16.0

14.3

13.0

6

19

1

58

Chaetognaths:

Day

116,7

164.6

57.0

35

133

9

993

Night

86.9

71.6

60.0

38

113

13

257

Cruise 5, November

9-21, 1962, .V

= 32 doy, 31 n

ght

Small copepods:

Day

3,728.2

2,277.8

3,487.0

2,235

4,328

1,654

11,613

Night

3,505.3

1,962.1

3,750.0

2,054

4,223

796

9,476

Large copepods:

Day

121.5

252.0

49.5

29

70

0

1,220

Night

41.1

35.6

30.0

19

52

1

154

Euphausiids:

Day

9.8

11.0

6.5

1

13

0

48

Night

24.4

34.4

12.0

5

21

0

163

Chaetognaths:

Day

32.2

20.8

28.5

19

41

3

94

Night

21.0

20 2

12.0

7

25

0

72

* Confidence limtls are for medians (Tote and Clelland, 1957).

686

O'CONNELL: VARIABILITY OF NEAR-SURFACE PLANKTON

each successive cruise in 1961, and the median
for the last cruise in this year was more than
three times as high as any of the others. Median
densities of the large copepods were two to four
times as high for the last two cruises in 1961
as for the other cruises. Euphausiid medians
were about twice as high for the first two cruises
of 1961 than for the other cruises. The chaeto-
gnath median for the last cruise of 1962 was sig-
nificantly lower than for the first cruise of that
year, but no other difl'erences can be distin-
guished.

In summary, the three crustacean groups
showed real differences in density near the
surface at night for the area as a whole. All
showed differences of three to four times be-
tween the 2 successive years. The euphausiids
and small copepods also showed real differences
of about two and three times within the first
of the 2 vears.

VARIATION WITHIN THE AREA

The 1.6-km samples were taken in block
clusters so that small-scale variability could be
described in respect to variability over the entire
area. The possibilities of comparison are lim-
ited, however, because parametric analyses were
avoided. The necessary assumptions about fre-
quency distribution of sample estimates could
not be satisfied for the present data. Frequency
distribution of block medians (or means) is var-
iable between cruises.

FREQUENCY DISTRIBUTION OF
BLOCK MEDIANS

Table 3 shows the frequency distribution of
block medians for the day and night periods of
each cruise. The distributions for each species
group vary noticeably, but there are similarities

Table 3. — Frequency distribution of block medians by cruise and day (D) or night (N) period.

Class

(no/m')

ID

IN

2D

2N

3D

3N

4D

4N

5D

5N

Small copepods:

1-3,000

6

7

3

4

._

__

8

3

4

4

3,001-6,000

2

3

2

5

__

3

4

4

5

6,001-9,000

__

1

1

5

__

__

9.001-12,000

1

__

__

1

__

12,000-15,000

--

—

—

—

1

—

—

—

Category

1

1

2

2

3

1

2

2

2

Large copepods:
0
1-50

3

5

3
2

5

3

7

"i

11

5

6

7

51-100

3

__

2

__

..

2

1

1

101-150

__

1

3

__

2

..

__

1

151-200

_.

2

__

„

..

_.

1

._

201-f

—

1

1

—

—

—

—

—

I

—

Cotegory

1

3

I

4

1

4

1

2

3

2

Euphausiids:

0

2

2

1

2

1

1-25

5

2

3

2

5

5

9

6

8

7

26-50

1

3

1 ■

4

1

3

__

1

_.

1

51-75

3

3

1

__

76-100
101-125
126-150
ISl-f

-

2

-

I

-

-

-

-

-

1

-

-

-

~

-

1

-

-

-

-

Cctegory

1

3

I

3

I

2

1

2

1

2

Chaetognaths:

1-50

5

6

2

7

5

7

4

2

8

9

51-100

1

2

1

1

1

2

3

2

1

__

101-150

__

_.

1

1

1

3

2

_.

._

151-200

__

2

1

__

201-250

1

1

__

_.

_.

1

..

__

251-300

1

..

1

_.

._

_.

._

__

_.

..

300-f

—

1

—

—

—

—

I

—

—

—

Category

1

I

3

2

2

2

3 •

3

2

2

687

FISHERY BULLETIN: VOL. 69, NO. 3

among them suggestive of trends with tlie gen-
eral level of density. To define the trends, the
distributions for each specie^ group wei'e pooled
into three or four categories on the basis of the
extent of concentration in specific frequency
classes and the extent of dispersion over all
classes. Category designations are indicated in
the table, and percentage frequency histograms
are shown for each category in Figure 4. Num-
ber of blocks, number of night and day periods,
and the range of cruise medians (from Table 2)
are given for each histogram.

The histograms suggest the same kind of trend
for the three crustacean groups: a shift from
distribution almost entirely restricted to the low^-
est classes when general area level is low,
through distribution of greater positive skew-
ness for intermediate levels of area density, to
symmetrical distril)ution as blocks of low me-
dian value disappear at the higher levels of area
density. The chaetognath distributions were
more difficult to classify, but it appears that fre-
quency distribution is appreciably skewed at all
levels of area density for this group.

The differences in the trends for the four spe-
cies groups are also illustrated by the extent of
the overlap between the distributions for the
highest and lowest categories in the figui'es.
There is no overlap for small copepods, perhaps
50 to 75 'r overlap for large copepods and eu-
phausiids, and complete overlap for chaeto-
gnaths. These differences suggest that when the
overall area median is at one extreme, the possi-
bility of blocks with medians at the other ex-
treme is greatest for the chaetognaths, least for
the small copepods, and intermediate for the
large copepods and euphausiids.

The existence of such trends in frequency dis-
tribution indicates that, at least for the crusta-
ceans, no one statistical distribution would satis-
factorily fit all the data sets; nor would any
single normalizing transformation be uniformly
effective for the different data sets. Without
normalized distributions, even the iiiterin-etation
of coefficients of variation would be diflicult in
comparing cruise periods. It may be noted, how-
ever, that when all frecjuency distribution cate-

gories are pooled, the distributions for the four
species groups show similar degrees of skewness.
The total block array for each species group is
approximately normalized by log transformation.

SMALL COPEPODS

LARGE COPEPODS

£^0^.000 [ riV^

C= 4

P= 2 NIGHT
M=77-I0I

1 — '

C= 3

■

n= 7
P: 1 DAY

■

M= 6,000-9

1 1 . , .

CATEGORIES POOLED
0=87

0 3 6 9 12 15 18 21 24
NUMBER/m' X lO'

EUPHAUSIIDS

rm^"

c- 3

n-20

P= 2 NIGHT
41-43

lOOr

C= 2
n=26

P= 3 NIGHT
M= 12-23

n:4I
P= 5 DAY
M= 1-13

CATEGORIES POOLED

25 50 75 100 125 150 175

number/m'

n

XI

P= I DAY, I NIGHT
M=42-50

P = 2 DAY. 3 NIGHT
M= 5.000-6000

P= 2 NIGHT
M=2l-30

n-. 29

P=2DAY, I NIGHT
M^BELOW 3.000 50-

CATEGORIES POOLED
n=e7

50 100 150 200

NUMBER/M*

CHAETOGNATHS

C= 3

n= 24

P: 2 DAY, I NIGHT

M-57-I2I

P= 2 DAY, 3 NIGHT
M= 12-36

P: I DAY, I NtGHT
M= 21-33

CATEGORIES POOLED
n=e7

50 100 150 200250300

number/m'

Figure 4. — Percent frequency distribution histograms
for four species groups as pooled on the basis of simi-
larity. Range of sample medians (M) (from Table 2),
number of day and night periods (P), and number of
sampling blocks (n) represented by each histogram
category (C) is shown. The histogram at the bottom
of each set shows the distribution of all block medians
from all cruises.

688

OCONNELL: VARIABILITY OF NEAR-SURFACE PLANKTON

RELATION OF RANGE TO MEDIAN
IN SAMPLING BLOCKS

Within block variation is indicated for eacli
species group and for all species groups together
by regression log R = a + b log M (Table 4),
where R = block range and M = block median.
The slopes, b. for the five equations do not differ
significantly from each other (p = 0.05). All
are significantly greater than 0 (p = 0.01), and
all but that for small copepods are significantly
less than 1.0 (/) = 0.05). The intercepts are
all significantly greater than 0, again except for
the small copepods, but they do not diflfer sig-
nificantly from each other (p = 0.05). In view

Table 4. — Estimated coefficients for regressions of log
block range on log block median for each species group
and all species groups combined."

Species group

Small copepods

87

-.18

.95"

.40

.53**

Lorga copepods

31

.51

.72"

.36

.74"

Euphousiids

79

.38

.72"

.30

.79"

Chaetognaths

86

.26

.87**

.33

.82"

Combined

333

.35

.80"

.35

93"

^ N = number of sampling blocks;
= stondord deviation about the line;
" p = 0.01.

= intercept; b = slope;
correlation coefficient.

of the similarities, the regression for all groups
combined (Figure 5) is a satisfactory descrip-
tion of the average relation of block range to
block median for each of the species groups.

The regression for all groups combined indi-
cates that average block range increases with
block median but not proportionately. The ex-
pected ranges for difl["erent medians are:

1,000 10,000
562 3,548

Median 1 10 50 100
Range 2 14 51 89

Thus range will tend to be greater than the me-
dian when the latter is below 50, but appreciably
less than the median when the median is above
100. Small copepods are the only group with
consistently high medians, and they also have
the greatest standard deviation about the line.
This suggests that, while the ratio of range to
median is lower, on the average, for this group,
it also tends to be more variable than for the
other groups.

The relation of block range to the total varia-
tion within the area is suggested by the mag-
nitude of block ranges relative to the class in-

tervals of the frequency distributions shown
earlier (Table 5) . In the case of small copepods,
block ranges only slightly exceed the size of class
intervals for the two highest classes in the distri-
bution. For the other three species groups, block
ranges exceed the class intervals for all but the
lowest class. Ranges tend to be spread over
three or more class intervals for the upper halves
of the euphausiid and chaetognath distributions.
Even though the highest classes tend to be rare,
it can be seen that ranges extending over two
or more class intervals would not be uncommon
for large copepods, euphausiids, and chaeto-
gnaths.

Table 5. — The number of class intervals encompassed
by the range for the midpoint of each class interval in
the frequency distribution for each species group. The
0-1 class is excluded and other classes are numbered con-
secutively.

Frequency
class

Small
copepods

Large
copepods

Euphousiids

Chaetognaths

0.1
0.3
0.9

1.2
1.5

0.6
1.4

2 1
28

3.4

0.7
1.6
2,4
3.2
3.9
4.6
5.2

0,6
1.4
2 1
2.8
3.4
4.0
4.6

DIURNAL VARIATION

It is evident from the differences in day and
night sets of data that density level near the
surface is influenced by diurnal vertical move-
ments, pai-ticularly for the larger crustacean
groups. The pattern of change is indicated for
each of the species groups by medians for 4-hr
time intervals (Figure 6). A sequence of change
is most apparent for the large copepods and
euphausiids, the lowest medians occurring be-
tween 1000 and 1400 hr and the highest between
1800 and 0200 hr. The increase in the evening
appears to be more rapid than the decrease in
the morning for both groups.

The small copepods show a pattern similar to
that for large copepods, but much weaker. The
highest time interval median is almost 10 times
the lowest for large copepods but less than 2
times the lowest for small copepods.

Chaetognaths show only slight evidence of
diurnal change. The peak between 0600 and

689

FISHERY BULLETIN: VOL. 69, NO. 3

10*

o

c

LlJ
O

<

I0>

SMALL COPEPODS
LARGE COPEPODS
CHAETOGNATHS
EUPHAUSIIDS

Q □ c

10"

10'

IC^ 10"

MEDIAN (no/m')

Figure 5. — The relation of sampling block range to sampling block median for the four species groups combined.

1000, which is obviously responsible for the gen-
erally higher day-period densities shown else-
where, may indicate an upward and a downward
movement in the morning.

The spread of block medians tended to be as-
sociated with the time-interval medians for
euphausiids but not for the other siiecies groups.
The euphausiids showed both high and low block
medians at night Imt only low medians during
the middle of the day. Large copepods showed
a similar distril)ution excei)t that three of the
highest four block medians in the series occurred
between 1000 and 1S(K) hr. Small copepods and

chaetognaths showed high and low medians in
all time periods.

CORRELATIONS BETWEEN DENSITIES
OF THE FOUR SPECIES GROUPS

The data were examined for association be-
tween the densities of species groujis over the
area by calculating rank-difference correlation
coefficients (Tate and Clelland, 1957) for the
nighttime block medians of each cruise (Table
(■)) . Daytime blocks were excluded to reduce the
component of correlation that would result from

690

O'CONNELL: VARIABILITY OF NEAR-SL'RFACE PLANKTON

in

z

CHftETOGNftTHS

SMALL COPEPODS/IOO

LARGE COPEPODS

EUPHAUSMOS

06 10 14 18 22 02 06

HOUR

Figure 6. — The relation of median density to time of day
for four species groups. The points are medians for
block densities in 4-hr intervals. The small copepod
medians were divided by 100 to put them on the same
scale as the others.

Table 6. — Rank difference correlation coefficients for
median block densities of four species groups for the
night periods of five cruises.

Cruise

\

2

3

4

5

Small copepods : large copepods

-AS

.31

.75

.71

,20

Small copepods : euphausiids

-09

-.20

.59*

.14

.87"

Small copepods : chaetognoths

.26

-.36

-.43

-.42

.30

Large copepods : euphausiids

.10

.04

.71*

.14

29

Large copepods : chaetognoths

.02

.29

.20

.21

.73-

Euphausiids : chaetognoths

.42

.12

-.23

.00

.53

Number of night blocks

10

10

10

7

9

* p = 0.05.
•• p = 0.01.

the parallel patterns of diurnal change in the
crustacean groups.

The coefficients for each of the six species
group combinations varied widel.y among the
five cruises, with only four of the entire 30 co-
efficients indicating significant correlations. It
appears that, while occasional correlations can
be expected to occur over the area, consistent
trends of association in density do not occur
among these four species groups near the surface
at night.

DRY WEIGHT VARIATION

Dry weight concentrations are summarized
by cruise period in Table 7 and by weight class
for all cruises in Figure 7. Low and high values
occur both night and day, but there is clearly
a shift to higher values at night.

The sample concentrations may underestimate
the true concentrations by as much as 15 or 20%.
Ahlstrom and Thrailkill (1963) showed that for
copepods dry weight decreased about 15% after
Formalin preservation. Lasker (1966) showed
that dry weight of euphausiids was about 35%

15 25 35 45 55

DRY WEIGHT (mg/m')

Figure 7. — Dry weight frequency distribution of all
sampling blocks. The wide bars .show day frequencies
and the narrow bars night frequencies.

Table 7. — Summary of sample dry weight concentration (mg/m^) by cruise and day (D) or night (N) period.

ID

IN

2D

2N

3D

3N

4D

4N

5D

5N

Mean

13.04

20.87

18 02

22.24

22.94

34.01

22.67

24.51

18.44

25.58

Median

1500

18.32

14.51

21.03

22.76

31.80

1524

24.72

15.27

23.23

Minimum

5.81

9.36

5.54

13.54

14,17

25.79

7,02

968

8.46

9.54

Maximum

20.85

34.00

43.74

30.57

30.42

49 59

56.90

34.62

32.11

52.42

Number blocks

7

9

6

7

7

9

II

7

9

9

691

FISHERY BULLETIN: VOL. 69, NO. 3

lower for preserved than for fresh material.
These groups were prominent in the inimp sam-
ples, and dry weight determinations were made
after long Formalin preservation. The pump
samples undoubtedly contained a higher propor-
tion of small copepod forms than the net samples
of Ahlstrom and Thrailkill (1963) , and it is pos-
sible that dry weight loss in Formalin is less
for the smaller than for the larger individuals
of this group.

As a basis for estimating the contributions
of different species groups to dry weight con-
centration, dry weight factors were determined
for large copepods, euphausiids, and chaeto-
gnaths by sorting known numbers of each from
a few representative samples for drying and
weighing. The resulting values are given in
Table 8. The factor given for small copepods,
which would have been difficult to separate in
sufficient numbers and purity for a direct de-
termination, was inferred from data given by
Marshall and Orr (1955) for Calanus finmarchi-
ctis and C. helgolandkiis in eastern Atlantic
waters. They showed that Calamis stage V, at
an average length of 2.5 mm, have a dry weight
of about 300 mg 1000 organisms, and that ac-
cording to Bogorov (1938) one stage V organism
is equal in dry weight to two stage IV, 11 stage
III, 42 stage II, and 60 stage I organisms. The
average lengths of these stages are given as
2.1 mm, 1.65 mm, and 0.94 mm, and the average
length of nauplii is given as 0.585 mm, which
is the same as that of small cojiepods in the
present study. Large copejjods from the present
study show an average length intermediate be-
tween those given for stages IV and III above.

Table 8.— Dry weight (DW) and ash weight (AW)
determinations (mg/1000 organi,sms) for species groups
in selected samples.

AW

Small copepods

mi/1000
■2.5

mg/1000

%

Lorge copepods:
Doy
Night

54.64
49.88

3.48
2.94

6.36
5.89

Euphousiids:
Doy
Night

42.03
293.26

3.29

11 51

7.82
4.95

Chaetognaths

23.5

1

5.51

suggesting a ratio of six large copepods to one
stage V, or a dry weight of 50 mg 1000 organ-
isms, which is very close to the actual determina-
tions. No dry weight equivalent is given by
Bogorov for nauplii, but extrapolation of his
series against average lengths suggests that 120
nauplii per stage V Calanus, or 2.5 mg 1000
nauiJJii, would be a conservative estimate.

Dry weight concentrations were calculated
for each species group in each block from the
dry weight factors and from the medians of nu-
merical estimates for the blocks. The values
for sjjecies groups were summed to produce a
"calculated" dry weight concentration for each
block. These are compared to the measured dry
weight concentrations in Figure 8. All the data
together tend to cluster around the line of equal
value (slope 1.0), and each of the different

80r

• Not determined by direct meoiurenienl. See text.

10 20 30 40 50
MEASURED DRY WEIGHT (mg/m')

FiGL'RK 8. — The relation of calculated to measured dry
weight concentration for all sampling blocks. Calcu-
lated dry weights were derived from species group
density estimates and dry w^eight factors (Table (>).
The line indicates equality of the two scales C Cruise 1;
O Cruise 2; A Crui.se ;i; ▲ Cruise 4; • Cruise 5.

692

O'CONNELL: \AR1 ABILITY OF NEAR-SURFACE PLANKTON

cruise sets has slopes similar to the line. Varia-
tion is wide, but there are only four serious dis-
crepancies. Whatever the reasons for these
discrepancies, the four blocks were excluded
from calculation of the relative contributions of
species groups to dry weight concentrations for
day and night cruise periods.

Table 9 shows the averages of dry weights
calculated for each species group for each cruise
period, and for all cruise periods pooled by day
and night. "Calculated" sample concentrations,
obtained by summing the values for the four spe-
cies groups, are compared with the average
measured concentrations for the cruise periods
in the last two columns. Though the calculated
concentrations are lower than the measured con-
centrations for all day periods, and higher than
the measured concentrations for three of the
night periods, the two sets show reasonably good
agreement, as do the day and night averages
for all cruises together.

The measured sample concentrations for all
cruises pooled suggest that, on the average, dry
weight was 31 '~f higher at night than during
the day. The calculated concentrations suggest
that it was 48 '^r higher. Calculated values for
the species groups show that the dry weight
increase at night is largely attributable to in-
creases in the euphausiid group, with lesser in-
creases in the large copepods and also the small
copepods. Euphausiids were responsible for
more than one-third of dry weight concentration

at night, on the average, and small copepods for
less than half of it. During the day, on the
other hand, small copepods accounted for about
three-fourths of dry weight concentration, with
most of the remainder divided between large
copepods and chaetognaths.

VARIATION WITH TEMPERATURE
AND DISTANCE FROM LAND

The data for each of the four species groups,
and for dry weight, were examined for possible
relationships with the independent variables,
temperature, miles from nearest land (including
islands), and miles from nearest point on the
mainland. Regressions were in the form log
Y = a + bX, where X — the independent var-
iable and Y = the dependent variable. Small
copepods, large copepods, and dry weight showed
significant trends with temperature, and chaeto-
gnaths showed significant trends with distance
from land (Table 10). For euphausiids, night
values alone, as well as day and night values
together, were tested but neither demonstrated
significant trends.

The two copepod groups and dry weight all
show an inverse relation with temperature, but
in all cases the trends are largely attributable
to changes occurring in 1961, as a comparison
of nighttime cruise medians with average cruise
temperature shows (Table 11). The decline in

Table 9. — Calculated average dry weight fractions (mg/m^) and percentages for species groups by cruise and day

(D) or night (N) period.

Average sample
dry weight

Small
ms/m3

copepods
%

Large

copepods
%

Euphau

siids
%

Chaetognaths

Calculated

Measured

ID

6.46

70.9

0.26

2.9

026

2.9

2.13

23.4

9.11

13.04

IN

7.70

26.1

3.49

11.8

14,88

50.5

3.41

11.6

29,48

20.87

2D

8.54

61.4

2.18

15.7

0,36

2.6

2.84

204

1392

18.02

2N

9.29

35.7

4.08

13.7

11,83

45.5

0 79

3.0

25,99

22.24

3D

20-07

88.3

0.73

3.2

063

2.S

1.29

5.7

22,72

22.94

3N

25.74

68.7

370

9.9

6,99

18.7

1.03

2.7

37.46

34.01

4D

6.05

62.6

0.97

10 0

0,35

3.6

2 30

23.8

9.67

15.66

4N

8,88

Sl.O

1 50

8.6

4.95

28.4

2.07

11.9

17.40

24.51

5D

7.56

66.4

2,93

25.7

0.28

2.5

0.61

5.4

11-38

16.72

5N

8.52

47.7

2.09

11.7

6.86

38.4

0.41

2.3

17.88

24.09

Averoge D

974

72.9

1,41

10.6

0 38

2.8

1,83

13.7

13.36

17.28

Average N

12.03

469

2,97

11.6

9.10

35.5

1,54

6.0

25-64

25.14

693

FISHERY BULLETIN: VOL. 69. NO. 3

Table 10. — Regressions of median bloctc densities and
dry weight concentrations on temperature and distance
from land.'

Regression

N

a

b

J

r

Small copepods
on temperature

83

5.38

-.105'

.23

.54"

Large copepods
on temperature

78

3,23

-.101"

.52

.26-

Dry weight on
temperature

78

2. -16

-.067"

.22

.40"

Choetognaths on
distance to
moinlond

85

1.99

-.013"

.53

.31"

Choetognaths on
distance to
nearest lond

85

2.02

-.020*

.54

.22-

^ N = number of sampling blocks;
= standard deviation about tne line;
* p = 0,05.
•• p = O.OI.

= intercept; h = slope;
correlation coefficient.

Table 11. — Average temperatures, median copepod den-
sities, and median dry weight concentrations for the
night periods of each cruise.

Cruise
dots

Temperature

Small
copepods

Large
copepods

Dry

weight

° C

no./m'

no /m»

mj/m-l

9/27/61

18.9

2.542

42

18

10/10/61

18.2

3,325

101

21

11/17/61

15,9

10,281

77

32

10/ 2/62

13.6

3,504

21

25

11/20/62

16.1

3,750

30

23

water temperature was approximately the same
in both years. The copepod values and dry
weight consequently show a strong inverse re-
lation with temperature and date for 1961 but
not for 1962.

The chaetognaths show inverse trends with
distance from the mainland and from nearest
land, but the former is the more significant of
the two. The relationship with distance to
nearest land includes many of the distance
measurements to the mainland, of course, and it
is possible that these are largely responsible for
the significant relationship with distance to
nearest land. The geographical distribution of
all chaetognath block medians (Figure 9) shows
that distance from the mainland is the more
pertinent independent variable. Low densities
occurred at all distances beyond 7 miles, where-
as the highest densities did not occur farther off-
shore than 14 miles, with a single exception. It
can be .seen that density was far more variable
near the mainland than offshore.

DISCUSSION

The food potential of plankton for pelagic
fishes depends on the relation between the aver-
age density of some or all species groups over
an area and the rate at which the fishes can feed
on these species groups. Since median density
of the more common species groups varies widely
within the space of a few months for the area
surveyed in this study, it is in'obabie that food
potential of near-surface plankton off southern
California fluctuates appreciably within short
time intervals. However, there were marked
small-scale variations in the distributions of den-
sities associated with the general area levels, and
the general level would not be an appropriate
index of food potential if fishes tend to orient
to small-scale features of distribution.

Although the association of range with median
for sampling blocks of 51.8 km^ demonstrates
that densities vary, sometimes widely, within the
blocks, the medians of blocks of this or some
similar size probably constitute a scale of suf-
ficient resolution for assessing the food potential
of plankton over a large area. Maximum values
within the blocks are not likely to be imjiressively
greater than the median. If the median of large
copepods is 175 /m^, the block can be expected
to have, on the average, a maximum density of
245 /m-' representing an area of 2.6 km- ( 1 square
mile) within the block. If the median of
eu]jhausiids is 90 m\ the block can be expected
to have a maximum density of 130/m^ for
2.6 km-. Blocks with such medians are usually
rare, and the medians, as well as the maximum
values, are likely to be considerably higher than
the densities in most blocks in the area. The
medians would slightly underestimate the food
potential of such blocks only if plankton feeding
fishes tend to orient to the highest densities with-
in the space of 20 square miles.

The distributions of .sampling block medians,
which were skewed unless general area level
was ver.v high, suggest that even under the
poorest general conditions relatively high den-
sities of organisms are likely to exist in some
small portion of the survey area. Small cope-
l)()ds, for example, showed a few occui'rences
of blocks with medians above 6000/m'', and one

694

O'CONNELL: VARIABILITY OF NEAR-SURFACE PLANKTON

-^Z^

••• r.

CALIFORNIA

Q^

MEDIAN DENSITY/m'
• 1-25
# 26-75

A 76-150

151 +

DIEGO

34°

-33°

119° 118°

Figure 9. — Geographical distribution of chaetognath medians for all blocks on all cruises.

117°

with a median above 9000 m'', when the general
area median was about 3000 m''. Large co]ie-
pods showed a few occurrences of blocks with
medians well above 200 when the general area
median was 50/'m^ or less. Euphausiids showed
occurrences of blocks with medians above 75 m''
when the general area median was between 25
and 40/m^. It seems probable, in other words,
that high crustacean densities are always present
somewhere in the area. At the lower general
levels they would be scarce but perhaps as much
as three times higher than densities over most
of the area.

The data indicate that higher densities of
chaetognaths are most likely to occur near the
mainland, but they failed to demonstrate such
trends for the three crustacean groups. They

indicate only that the crustaceans, and dry
weight, may sometimes be at higher levels where
and when temperatures are relatively low. Re-
gressions with temperature show, for example,
that the density of small copepods was 6400/m'^
in 15° C water, on the average, as compared with
2400, m'' in 19° C water, and that dry weight
concentration was 29 mg/m-' in 15° C water, but
only 15 mg/m'' in 19° C water. Since variation
associated with these trends is wide, it can only
be concluded that water of low temperature may
sometimes, though not always, contain much
higher standing crops of zooplankton than are
likely to be found in warmer water in the survey
area.

Dry weight factors were determined for the
different species groups because it is impossible

695

FISHERY BULLETIN: VOL. 69, NO. 3

to estimate the relative nutritional value of such
groups in the plankton on the basis of organism
counts alone. In general, the near-surface zoo-
plankton had a dry weight equivalent of about
25 mg/m^ at night, which was approximately
30 Sr greater than the average daytime level.
Small copepods were the dominant fraction dur-
ing the day and increased only slightly at night.
Most of the nighttime increase in dry weight is
attributable to the appearance of euphausiids,
which were estimated to have a dry weight
equivalent of 9 mg/m^, on the average, as com-
pared with less than 1 mg m^ during the day.
There was some deviation from this general pat-
tern among the five cruises. DiflFerences be-
tween and within sampling blocks were not de-
scribed in terms of dry weight. The general
differences are enough to show that the nutri-
tional potential of the plankton, in terms of dry
weight for any set of samples, would depend
on the extent to which fishes do or do not feed
selectively.

However they are interpreted, it must be noted
that the dry weight equivalents of the samples
taken in this survey, aside from the possible
loss of weight in Formalin preservation, may not
represent the whole of the biomass utilized by
some plankton feeding fishes near the surface.
They contained almost no zooplankters smaller
than 0.2 mm in length and relatively little phy-
toplankton. The comparison in Table 12 indi-
cates that such smaller organisms may constitute
a considerable fraction of the biomass.

Beers and Stewart (1967) sampled the eupho-
tic zone with a towed pump on a line of stations
off" San Diego. Water was strained successively
through 202-, 103-, and 35-fj. cloths to estimate
quantities below each cloth. Leong and O'Con-
nell (1969) estimated from the resulting data

Table 12. — Comparison of dry weight values (nig/m')
for different lenprth ranges of planktonic organisms in
two towed pump studies.

Period

Group

Length rang© (mm)

<0.2 0.2-1.0 >1.0

Beers and Stewart Day only Phytoplankton 25.1
(1967) Zooplankton 2.9

Present survey

Doy
Night

Crustocean
Crustacean

0

8.9

9.7
12.0

0
0

1.8
12.1

that phytoplankton and zooplankton passing
through the 105-fj. cloth represented average dry
weight concentrations of 25 and 3 mg/ml The
103-/X cloth was approximately the same mesh
size as the filtering screens used in the present
survey. The material retained between the 103-
and 202-;a cloths of Beers and Stewart is here
judged to approximate the size range, 0.2 to 1.0
mm, and the numerical estimate for their inner-
most station, when converted to dry weight by
the constant, 2.5 mg/1000 organisms, yields a
concentration similar to the daytime average for
crustaceans in this size range in the present
surveys.

It appears that material smaller than that col-
lected in the present survey might represent a
dry weight ap])roximately two to three times as
great as that that was collected. Adjustment
for the smaller organisms in questions of nu-
tritional potential would depend on selectivity
in the feeding of various fishes.

It is difficult to judge whether the dry weight
values attributed to organisms larger than 1 mm
in the above comparison fully represent the bio-
mass of larger plankton organisms near the
surface that can be utilized by plankton feeding
fishes. Such fishes probably take crustaceans
larger than collected by the pump when oppor-
tunity arises. It can only be restated that euphau-
siids larger than those sampled are relatively
rare close to the surface. Five of the 1-m-mouth-
opening-net tows taken by Ahlstrom and Thrail-
kill (1963) through the upper 100 m or so were
composed largely of crustacean material. From
the data given they were estimated to represent
dry weight concentrations averaging 3.5 mg m'.
The figure is in the range of day and night con-
centrations for the pump samples, but the com-
parison is uncertain because of differences in
the location as well as the depth of sampling.

The above discussion implies that estimating
the food potential of jilankton for fishes must de-
I)end as much on information concerning the
feeding behavior of the fishes as on information
concerning the abundance and variability of the
plankton. The data given here on i)lankton var-
iability are intended as a basis for interpreting
hypotheses that may arise from laboratory or
field studies of feeding behavior.

696

0-CONNELL; VARIABILITY OF NEAR-SURFACE PLANKTON

LITERATURE CITED

Ahlstrom, E. H., and J. R. Thr-^ilkill.

1963. Plankton volume loss with time of preserva-
tion. Calif. Coop. Oceanic Fish Invest., Rep. 9:
57-73.
Alverino, a.

1961. Two new chaetognaths from the Pacific.
Pac. Sci. 15: 67-77.
Barnes, H., and S. M. Marshall.

1951. On the variability of replicate plankton
samples and some applications of "contagious"
series to the statistical distribution of catches over
restricted periods. J. Mar. Biol. Assoc. U.K. 30:
233-263.
Beers, J. R., and G. L. Stewart.

1967. Micro-zooplankton in the euphotic zone at
five locations across the California Current. J.
Fish. Res. Board. Can. 24: 2053-2068.
BoDEN, B. P., M. W. Johnson, and E. Brinton.

1955. The Euphausiacea (Crustacea) of the north
Pacific. Bull. Scripps Inst. Oceanogr. Univ. Calif.
6: 287-400.
Bogorov, B. G.

1933. Modifications in the biomass of Calanus
finmarclncus in accordance with its age. [In
Russian, English summary.] Bull. State Ocean-
ogr. Inst., Moscow, 8: 1-16.
Brinton, E.

1962. The distribution of Pacific euphausiids.
Bull. Scripps Inst. Oceanogr. Univ. Calif. 8(2):
51-270.
Cassie, R. M.

1959. Micro-distribution of plankton. N. Z. J.
Sci. 2: 398-409.

1962. Frequency distribution models in the ecology
of plankton and other organisms. J. Anim. Ecol.
31: 65-92.

1963. Microdistribution of plankton. Oceanogr.
Mar. Biol. Annu. Rev. 1 : 223-252.

Gushing, D. H.

1951. The vertical migration of planktonic Crus-
tacea. Biol. Rev. (Cambridge) 26: 158-192.
Holmes, R. W., and T. M. Widrig.

1956. The enumeration and collection of marine
phytoplankton. J. Cons. 22: 21-32.
IVLEV, V. S.

1961. Experimental ecology of the feeding of fishes.
(Translated from the Russian by Douglas Scott.)
Yale Univ. Press, New Haven, 302 p.
King, J. E., and T. S. Hida.

1954. Variations in zooplankton abundance in
Hawaiian waters, 1950-52. U.S. Fish Wildl.
Serv., Spec. Sci. Rep. Fish. 118, 66 p.
Lasker, R.

1966. Feeding, growth, respiration, and carbon
utilization of a euphausiid crustacean. J. Fish.
Res. Board Can. 23: 1291-1317.

Leong, R.

1967. Evaluation of a pump and reeled hose sys-
tem for studying the vertical distribution of small
plankton. U.S. Fish Wildl. Serv., Spec. Sci. Rep.
Fish. 545, 9 p.

Leong, R. J. H., and C. P. O'Connell.

1969. A laboratory study of particulate and filter
feeding of the northern anchovy {EngrauUs mor-
dax). J. Fish. Board Can. 26: 557-582.
Marshall, S. M., and A. P. Orr.

1955. Biology of a marine copepod. Oliver and
Boyd, Edinburgh and London, vii -|- 188 p.
O'Connell, C. P., and R. J. H. Leong.

1963. A towed pump and shipboard filtering system
for sampling small zooplankters. U.S. Fish Wildl.
Serv., Spec. Sci. Rep. Fish. 452, 19 p.
Tate, M. W., and R. C. Clelland.

1957. Nonparametric and shortcut statistics. In-
terstate Printers and Publishers, Inc., Danville,
111., ix -I- 171 p.

697

NOTE

PREDATION ON JUVENILE PACIFIC

SALMON BY A MARINE ISOPOD

Rocinela bellkeps pugettensis

(CRUSTACEA, ISOPODA)

Observations were made of predation by a ma-
rine isopod on both captive and wild Pacific
salmon. Pacific salmon are known to be hosts
to a number of ectoparasites, esjiecially the
Copepoda. However, we have been unable to
find any reported incidents of predation or para-
sitism of Pacific salmon by the Isopoda.

In July 1969, we began a series of experiments
in Pug-et Sound to evaluate the feasibility of
saltwater rearing of Pacific salmon within float-
ing pens. Stocks of young salmon were weighed
and measured several times during the year at
the Manchester, Wash., e.xperimental station of
the National Marine Fisheries Service and rou-
tinely examined for ectoparasites visible to the
naked eye. A large Branchiuran parasite, Ar-
gtdus sp., was found on a 600-g chinook salmon
{OncorhyncMis tshaivytscha) ; the Branchiuran
was removed from the fish and kept for study.
Later, another Branchiuran was found in the
same body position on this fish. There were no
other visible ectoparasites.

In March 1970, we began collecting zooplank-
ton to provide live food for both salmon fry and
newly metamorphosed flatfish. Collections were
made during the night; a surface light was used
to attract the plankton and an airlift pump to
draw them into a net suspended at the sea
surface.

The collected organisms were poured into a
tank containing over 1000 young pink salmon ( 0.
(jorbiischa) , 30 to 45 mm long. Among the un-
sorted plankton were 8 or 10 isopods of the same
species. The pink salmon fed vigorously on large
numbers of amphipods in the tank, whereas the
isopods alternately rested on the sides of the tank
and swam about in random patterns. One iso-
pod quickly attached itself to a young pink

salmon. Within minutes, two more of the young
salmon were similarly attacked. The fish be-
came distressed, swam erratically about the tank,
and drifted listlessly to the bottom, where they
died within a few miiuites after settling. The
point of attack by the isopod on each young
salmon was lateral, just above or slightly poste-
rior to the pelvic fin. Small, but deep wounds
that penetrated the body wall were found on
each aflfected fish. The gut of each of the isopods
removed from the dead fish contained blood.

One of the isopods was placed in another tank
containing several dozen coho salmon (0.
kisntch), slightly larger than the pinks (100-
140 mm long). An hour later, the isopod was
found firmly attached to the head of one fish,
immediately posterior to and between the eyes.

Isopods are now removed before any plankton
are fed to our fish. If we should overlook even
the smallest of these isopods, we can expect
either death or injury to some fish.

We examined several specimens of the hun-
dreds of isopods we have collected and have
identified them as Rocinela belliceps pugettensis
(Stimpson), a subspecies of Rocinela belliceps.
R. belliceps is widespread in northern coastal
areas of the North Pacific Ocean, from the Be-
ring Strait southward along the North American
coast to California and southward along the
Asian coast to Korea (Pavlovskii, 1955) . Hatch
( 1947) feels that most of the specimens in Puget
Sound are the subspecies, pugettensis. He as-
signs subspecific rank on the basis of the number
of spines on the propodite of the prehensile legs
— six spines on the propodite of pugettensis,
whereas belliceps has three to four. A zone of
mixed populations of R. belliceps belliceps and
R. belliceps pugettensis exists near the entrance
to Hood Canal, just inside the Strait of Juan de
Fuca. All of the specimens we examined from
our collections at the Manchester station (which
is on the western side of central Puget Sound)
had six spines on the propodite of the prehensile
legs.

699

Rocinela sp. belongs to the family Aegidae.
Members of this family are widely recorded
ectoparasites of fishes. The first three pairs of
walking legs are prehensile and are used effec-
tively for attachment.

We originally felt that the attacks on our
salmon fry and fingerlings by R. belliceps puget-
tensis might have been the result of confinement
and would not be likely to occur with such fre-
quency in open waters. However, on at least
three occasions, we have observed wild chum
salmon (O. keta) and pink salmon fry and finger-
lings attacked by R. belliceps pngettensis. These
attacks occurred at night, under a light, that
probably attracted larger numbers of fish and
isopods than would normally occur in open
waters. In each instance, an isopod attached
itself at a point just posterior to the dorsal fin
and on, or slightly below, the lateral line. Af-
flicted fish could not maintain a normal swim-
ming position in a school and darted about in
erratic patterns. On one occasion, an afflicted
fish was seen to leave the school and disappear.
Even if a wound inflicted by an isopod were not
fatal, it is possible that the erratic behavior of
a fish trying to dislodge the parasite might at-
tract predators.

On another occasion, in one of our large float-
ing pens, we found a juvenile coho salmon with
R. belliceps pugettensis attached anterior to the
dorsal fin and just above the lateral line (Figure
1). This pen was not near our night light and
there was a large amount of free space compared
with our tanks or cages.

Also, in a cage that had a submerged light to
attract plankton, we found R. belliceps puget-
tensis on an immature coho salmon weighing
about 200 g. The fish appeared to be in some
distress, but perhaps because of its size, the
wound was not fatal.

Aral (1969) reported on (i8 taxa of parasites
recovered fi-om 61 species of fish in British Co-
lumbia, but these did not include R. belliceps
belliceps. Aral's collections were made by seine
and trawl; we found that R. belliceps pugettensis
will release its grasp if the host is forced into

a restrictive net. Hatch (1947) states that R.
belliceps belliceps is found in 9 to 1250 m of
water and that it is an ectoparasite of cod,
sculpin, halibut, skate, and other bottom fish.
At Manchester, \\'here our observations were
made, the water depth is 9 to 13 m. The abun-
dance of R. belliceps pugettensis varies between
seasons, with the greatest abundance from April
through August.

Although we have no way to judge the extent
of natural predation of Pacific salmon by R. bel-
liceps belliceps or R. belliceps pugettensis in the
wild, we think that, especially under the con-
fined conditions of pen rearing, the fry and ju-
veniles of Pacific salmon should be included as
possible prey of R. belliceps pugettensis and
probably R. belliceps belliceps.

The present instance clearly points up the
possible misapplication of the term "parasitism"
in certain cases of specialized predation. The
isopod R. belliceps pugettensis is not a permanent
symbiont of a fish and is thus not properly re-
ferred to as a parasite.

Figure 1. — Rocinela belliceps pugettensis on a juvenile
coho salmon in one of the large growing pens. This
specimen was anterior to the dorsal fin, whereas most
of the others w-ere attached in a posterior position.
Note the blood-filled gut of the isopod.

The authors would like to thank Dr. Paul Ilg
of the Department of Zoology, University of
Washington, for his suggestions on terminology
and Dr. Thomas E. Bowman of the National
Museum of Natural History, Washington, D.C.,
for verifying our identification of the isopod.

700

Literature Cited

Arai, H. p.

1969. Preliminary report on the parasites of
certain marine fishes of British Columbia. J.
Fish. Res. Board Can. 26: 2319-2337.
Hatch, M. H.

1947. The Chelifera and Isopoda of Washington
and adjacent regions. Univ. Wash. Publ. Biol.
10(5) : 155-274.
Pavxovskii, E. N. (editor).

1955. Atlas bespozvonochnykh dal'nevostochnykh
morei SSSR (.Atlas of the invertebrates of the

Far Eastern seas of the USSR). Izdatel'stvo
.•Vkademii Nauk SSSR, Moscow-Leningrad, 243 p.
(Transl., 1966, 457 p., avail. Clearinghouse Fed.
Sci. Tech. Inform., Springfield, Va., as TT 66-
51067.)

Anthony J. Novotny and
Conrad V. W. Mahnken

Nafio7ial Marine Fi-ihcries Service
Biological Laboratory
Seattle, Washington 98103

GPO 999-072

701

MEASUREMENTS OF FISH TARGET STRENGTH: A REVIEW

Richard H. Love'
ABSTRACT

The concept of target strength and its application to the quantitative assessment of fishery resources
are discussed. Methods of determining the echo characteristics of fish are reviewed and a number of
results presented. Among the more important of these results are: (1) practically every case of in-
terest to the fishing industry is in an acoustic region in which the target strength varies widely with
fish size and aspect and acoustic frequency, (2) the major contributors to target strength in this region
have been determined to be the swim bladder, flesh, and skeleton, and (3) the average maximum side-
aspect and dorsal-aspect target strength of an individual fish have been determined for this region.

Quantitative assessment of fishery resources is
a difficult task, and many groups have turned to
acoustic techniques to conduct assessment sur-
veys. Present acoustic techniques can give an
estimate of the number and dimensions of fish
schools in a geographic area and, by estimating
the density of the fish in a school, the number of
individual fish in the area can be approximated.
Measurements of fish target strength are being
made by various investigators in an effort to en-
able the direct acoustic estimation of the number
and size of individuals in a school and to enable
the direct identification of those individuals by
acoustic methods. This paper discusses the
concept of target strength and its application
to the quantification and/or identification of fish
schools, reviews target strength measurement
techniques, and discusses some results which
have been obtained utilizing these techniques.

TARGET STRENGTH

Active sonars project acoustic energy into the
water in an effort to detect objects by the echoes
they return, the intensity of the echo depending
on the proportion of the sound reflected back to
the receiver. The target strength of the echo-
producing object is a quantitative measure of its
reflecting characteristics and is defined as

10 log

a)'

(1)

' U.S. Naval Oceanographic Office, Washington, D.C.
20390.

Manuscript accepted April 1971

FISHERY BULLETIN: VOL. 69. NO. 4, 1971.

where h is the intensity of the sound striking
the target and /i is the intensity of the reflected
sound measured at 1 m from the acoustic center
of the target. If h is the intensity of the re-
flected sound measured at some distance r from
the target, then, assuming that the sound spreads
spherically, and there are no losses, h will be
directly proportional to h:

Ir

V47r/ ?■=

(2)

o- is defined as the acoustic cross-section of the
target, and inr- is the spherical surface area
through which all the incident energy is reflected,
cr depends on the size, shape, and orientation
of the target, and, in general, will vary with the
angle between the incident direction and the
direction of the receiver. In all present fish-
eries work, this angle is zero and therefore in
this paper cr will be the acoustic cross-section
of a target for the case in which the source and
receiver are located at the same point.

By letting r in equation (2) be equal to 1 m
and combining equations (1) and (2),

10 log

fe)

(3)

Now if Is is the intensity of the projected sound
1 m from the source,

h = ll

and therefore,

(4)

703

FISHERY BULLETIN: VOL. 69, NO. 4

(5)

01- in logarithmic form,

10 log /, = 10 log (-2L\ + 10 log h — 40 log r.

(6)

Defining the echo level (E) as 10 log Ir and the
source level (S) as 10 log /,„ and rearranging,

T r= E — S

40 log r.

(7)

Equation (7) can be used to compute target
strength in an ideal medium. In a real medium,
however, the actual transmission loss will in-
clude effects due to absorption, scattering, re-
fraction, and the boundaries. Hence, in a real
medium

E — S

2H

(8)

where H is the one way transmission loss. H
takes into account spreading loss, absorption,
and any anomalies. In actual practice H cannot
always be reliably predicted and must be mea-
sured unless the ranges involved are small.
Equation (8) is known as the active sonar equa-
tion and is always used in the computation of
target strength since it involves only directly
measurable quantities — echo level, source level,
and transmission loss.

It is impossible for more sound to be reflected
from a target than is incident upon it, and it is
therefore seemingly impossible for any object
to have a positive target strength, yet many large
targets do. This is a consequence of the refei--
ence distance being 1 m, and the measurements
being made at greater distances, with spherical
spreading assumed in order to calculate the
target .strength. However, the spreading loss
very close to a target is less than the spherical
spreading loss which is assumed, and hence pos-
itive target strengths can be obtained for large
targets.

The imiwrtance of the target strength of a po-
tential target is obvious from the sonar equation
(equation (8)). The maximum range at which
a target can be detected in any given environ-
ment depends on its target strength and the
characteristics of the transmitting and receiving

systems. Therefore, an estimate of target
strength is essential to the effective design and
operation of any active sonar system.

The quantification of a fish school, knowing its
target strength, is possible because the target
strength of a school depends on the average size,
number, distribution, and aspect of the individ-
uals in the school. In order to quantify fish
schools using target strenglh information, it is
first necessary to determine the size and number
of individuals required to produce a given target
strength. The initial step in this process is the
determination of the target strenglh of an in-
dividual fish. The application of this knowledge
to studies on the acoustic intei'actions of arrays
of scatterers will eventually produce accurate
predictions of school target strength. The great
majority of work done up to this time has been
on individual fish, and quite a bit more must be
done before this initial step is completed. De-
finitive work on the quantification and identifi-
cation of fish schools utilizing target strenglh
information awaits completion of this step.

Reflection of sound from an object in water
occurs when the oliject has an acoustic impedance
which differs from that of the water. Acoustic
impedance is defined as the product of the den-
sity (p) of a substance and the velocity of sound
(c) in that substance. The proportion of sound
reflected from or transmitted into an object in
water depends on the magnitude of the imped-
ance mismatch between the object and the water.
The simplest case of reflection occurs when a
plane wave is normally incident upon a plane
boundary between two semi-infinite media. The
pressure amplitude reflection coeflicient is de-
fined as the ratio of the reflected pressure ampli-
tude to the incident pressure amplitude, and for

this case it is found to be P-^- P'^', where

p2C2 + PlCl

piCi is the impedance of the medium in which
the incident wave is traveling and pjC; is the
impedance of the medium upon which the wave
is incident. If the second medium is reduced to
finite thickness and a third medium is i)laced
behind it (the third medium may or may not be
the same as the first), the jiroblem l)ecomes
slightly more complicated. When the incident
\vave arrives at the first boundary, some energy

704

LOVE: MEASUREMENTS OF FISH TARGET STRENGTH

is reflected and some is transmitted. After this
ti-ansmitted portion reaches the second boundary,
some of the energy is transmitted into the third
medium and some is reflected back into the sec-
ond medium, where it is again partially reflected
from the first boundary. This process continues
until a steady state is reached. The solution of
this problem is relatively easy, but it is inter-
esting because the resultant am])litudes of the
transmitted and reflected waves depend on the
phases of the component waves. The component
waves add vectorially and whether the amplitude
of the initially reflected wave is increased or de-
creased depends on the thickness of the second
medium and the wavelength of the incident wave.

The reflection of sound from an infinite plate
poorly approximates the reflection from a fish,
and it is useful to examine the reflection from a
finite object such as a sphere. When the sphei-e
is large compared to the acoustic wavelength,
the echo originates from specular reflection, in
which the part of the sphere near the point
where the sound wave is normally incident pro-
duces a coherent reflected wave. When the size
of the sphere is comijarable to a wavelength, in-
terfei-ence effects similar to those mentioned for
the plate with finite thickness will cause the
acoustic cross-section to vary. When the sphere
is small compared to a wavelength, scattering
takes place and the acoustic cross-section of a
sphere of radius o is proportional to a'^/X* where
X is the wavelength. This solution was obtained
by Lord Rayleigh and hence this region is called
the region of Rayleigh scattering.

For objects other than spheres, analysis be-
comes difficult, if not impossible. However, as
long as the object is not highly compressible,
the concept of the regions of Rayleigh scattering,
interference effects, and geometric reflection is
valid. For a fish, the distinctions between these
regions becomes unclear because of the fish's
internal structure. When the fish is very small
compared to the acoustic wavelength, Rayleigh
scattering can be expected. However, if the fish
has a gas-filled swim bladder the gas bubble will
resonate at some wavelength in this region,
greatly increasing the target strength over that
predicted by Rayleigh scattering. When the size
of the fish is comparable to the wavelength, in-

terferences will occur among the fish flesh and
organs, the skeleton, the gas in the swim bladder,
and the boundaries of the fish. When the fish
is larger than the wavelength, the dimensions of
many of these parts will be comparable to the
wavelength and the region of interference effects
will be greatly extended into what would be the
region of geometric reflection for a homogeneous
body.

Gushing et al. (1963) have assumed that the
region of interference effects extends from L/\
= 8 to L/\ = 100, where L is the fish length,
and \ is the acoustic wavelength, and they sug-
gest that for quantitative results this region
should be avoided. Neglecting the fact that they
have ignored the effects of swim bladder reso-
nance, the limits they have jilaced on the inter-
ference region will now be examined. For a rigid
sphere of radius a the limits of the interference
region are approximately 1 ^ 27ra/\ ^ 10, and
for any other object these limits will probably
be farther apart. Measurements on individual
fish indicate that interference effects occur at
values of L'k -- 0.7 (Love, 1971) and this can
be taken as a lower limit. (This is not to say
that it is the lower limit, only that this is as low
as measurements have been made.) Haslett
(1962a) examined a small number of whiting to
determine their "standard dimensions." He
found that the diameter of the backbone was
about 0.01 the length of the fish. Assuming that
the backbone of a fish is the smallest part of a
fish which contributes to its echo, this m.eans
that if interference effects occur in the back-
bone until its circumference is something near
10 times as large as the wavelength, as in the
case for the sphere, then the upiier limit of the
interference zone for a fish will be at least Lk
— 200. Again, measurements have been made
which indicate that the upper limit will be at
least this high (Haslett, 1969). Therefore, it
may be assumed that the limits of the interfer-
ence region are at least 0.7 ^ L/K ^ 200.

If it is assumed that fish of interest to com-
mercial fishermen range from 10 cm to 150 cm,
and that fish-finding sonars have frequencies
ranging from 10 kHz to 200 kHz, then the range
of interest for fisheries applications will be 0.7 ^
L/k < 200, the limits set for the interference

705

FISHERY BULLETIN: VOL. 69, NO. 4

region. Therefore, although it would be advan-
tageous to avoid the interference region, it is
apparent that this is the region in which the
worl< must be done.

METHODS OF TARGET STRENGTH
JVIEASUREMENT

Analytical methods are of limited value in this
interference region and experimental methods
must be utilized to obtain any valid answers.
It is possible to conduct the needed experiments
either at sea or in the laboratoiy, with each type
of measurement having its limitations. Whether
the measurements are made at sea or in the lab-
oratory, target strength will be determined from
the sonar equation, meaning that the source level
of the transmitter, the sensitivity of the receiver,
and the propagation loss must be known. The
calibration of the transmitting and receiving
systems is a standard procedure, but propagation
loss is much more diflicult to determine if long
ranges are involved. One way to avoid the prop-
agation loss problem is to make measurements
at short ranges, and this is what is done in the
laboratory. This, of course, is impossible with
large targets. Another method is to use a ref-
erence target for which the target strength is
known. In this method neither the transmitting
nor receiving systems have to be calibrated and
the propagation loss does not have to be measured
because all echo levels are compared to the ref-
erence level. One of the best reference targets
is a thin-walled air-filled rubber sphere, although
for large targets buoyancy becomes a problem.
Another good reference target, which can be
used for large targets, is a tri-i)lane, three mu-
tually perpendicular planes, for which it can be
shown that any incident ray will be reflected in
a direction exactly opposite to the incident di-
rection. Hence a tri-i>lane acts as a single plane
])erpcndicular to the incident rays and reflects
a large, calculable percentage of the incident
energy. It is possible to measure propagation
loss directly and this is fairly simi)le if a trans-
mitting and a receiving ship are utilized. Propa-
gation loss measurements can also be made by
placing a calibrated transponder in the vicinity
of the target.

Along with the problem of accurately measur-
ing propagation loss, there are other jiroblems
associated with target strength measurements
at sea, the most critical of these being relative
motion between the sonar beam and the fish
target. Roll or pitch of the ship can be over-
come by using a stabilized sonar beam, hut drift
can cau.se the axis of the beam to move off target.
Care must also be taken so that the target sup-
port structure does not interfere with the mea-
surements. Other problems that can arise are
poor weather, high ambient noise levels, and ex-
traneous targets swimming into the beam.

Of course, there are problems associated with
laboratory measurements also, the chief one
being the limitation on the size of the target.
The fish must be ]ilaced at a range great enough
to insure that the incident sound energy is ap-
proximately equal over the complete fish and to
insure that the fish is not in the near-field of the
transmitter nor the receiver in the near-field of
the fish. However, the range must not be so
great that reflections from the boundaries or fish
supiiort interfere with the measurements.
Nevertheless, by judicious choice of measure-
ment range and by using short pulse lengths,
unambiguous work can be done in a laljoratory
tank. In order to obtain a true value of target
strength the pulse lengths of the discrete fre-
quency pulses most often utilized by fisheries
sonars must be at least twice the length of the
target in the direction of projiagation, so that
an echo can be obtained from all parts of the
target simultaneously.

A tyiiical block diagram of the electronics re-
quired for target strength measurements is
shown in Figure 1. The transmitting system
consists of a signal soui'ce of known frequency,
a means to generate puLses, amplifiers, a trans-
mitting transducer, a system to match the elec-
trical impedances of the amplifier and transduc-
er, and a means to measure the outgoing signal.
The receiving .system consists of a receiving
tiansducer, amplifiers, a means to gate out un-
wanted echoes, iiossibly a filter, and a means to
measure the received signal. The electronic
system is basically the same whethei' it is used
in the laboi'atory or at sea.

If all fish were composed of the same homoge-

706

LOVE: MEASUREMENTS OF FISH TARGET STRENGTH

FREQUENCY _ osrii LATOR
COUNTER ' I OSCILLATOR

AMPLIFIER »

TRANSMIT
GATE

POWER

AMPLIFIER

IMPEDANCE
MATCH

RECEIVE
GATE

_, TWO CHANNEL
RECORDER

(projector)

(receiver)

Figure 1. — Typical target strength measurement system
electronics.

neous material and had the same shape, it would
take a comprehensive measurement program to
determine the target strength of a fish at all
aspects and frequencies because of the complex
shape of the body. Since fish are definitely not
homogeneous and different species of fish have
different shapes and internal structures, the
problem of determining the target strengths for
all species becomes immense. Considering the
differences among individuals of the same spe-
cies due to age, sex, condition of health, etc., it is
obvious that an experimental program to pre-
dict completely the target strength of any given
fish is impossible. Since the complete determi-
nation of the target strength of all fish is im-
possible, the most that can be hoped for is that
experimental techniques will eventually lead to
empirical results which can be generalized to
apply to any species of importance.

RESULTS OF MEASUREMENTS OF
INDIVIDUAL FISH

Most of the early experiments conducted dur-
ing the 1950's investigated a specific situation.
For example, if a researcher had an echo sounder
which operated at a given frequency, he would

measure the dorsal-aspect target strengths of a
number of fish of the commercial species found
in his geographic area, in order to obtain an
average dorsal-aspect target strength vs. fish
size for those species. This information was
valuable to anyone designing or using an echo
sounder of the same frequency to find these
species, but it was of minimal value to anyone
else.

A second technique used is just an extension
of the earlier technique. With it, different spe-
cies of fish have been examined at many aspects
and/or frequencies in attempts to determine how
target strength varies with fish size, species,
aspect, and frequency. Figure 2 shows some
typical results of this technique. The results
are from a live 21-cm black crapjne which was
rotated about its dorsiventral axis and insonified
with frequencies of 30 kHz and 130 kHz. It
is seen that the maximum target strength occurs
very near the side aspect, where the insonified
area is a maximum. At 130 kHz the number of
lobes in the pattern is substantially greater, and

® A

:^

4 f\ ^^„,^

f

y

-50«^^

5

-sbdB ^^

-""^^^^ /

\ /

f^ -50dB

\

\

>

-«clB J
/ t

1

/

■ 50dB -40118 ^*^-30dB

Figure 2. — Target strength of a 21-cm black crappie
versus aspect, (a) 30 kHz. (b) l.'iO kHz. (From Love,
1969.)

707

FISHERY BULLETIN: VOL. 69. NO. 4

the maximum target strength slightly greater
than at 30 kHz. Although these measurements
have produced some useful results on the gen-
eral changes of target strength with fish size
and frequency for aspects of special interest,
little has been learned about the fine-scale
changes or about the differences among species.

The use of a third technique jiermits investi-
gation into the nature of the echo-formation
process either by dissection or modeling. By dis-
section, researchei's have discovered which parts
of a fish are the major acoustic reflectors. By re-
moving the swim bladders from a number of
perch, Jones and Pearce (1958) determined that
the gas-filled swim bladder accounts for approx-
imately .'50 ''r of the dorsal and side-aspect target
strengths of perch at L \ = 4. Hence, the swim
bladder is an imi)ortant contributor to target
strength for L/\ values in the interference re-
gion. By systematically removing various parts
of a skipjack tuna, Volberg (1963) found that
appreciable echoes could be obtained from either
the skeleton or a piece of flesh. Diercks and
Goldsberry (1970) have indicated the possibility
that scales may also be an imiiortant contributor
to the target strength of a fish at certain fre-
quencies. Unfortunately, they did not remove
any scales and their hypothesis is based on con-
siderations of the directivity of the scales as an
array of scatterers.

An adjunct to the determination of the parts
of the fish which are acoustically imjjortant is
the determination of the acoustic impedance or
reflection coeflicient of these parts. The reflec-
tion coeflicient is defined as it was previously for
two semi-infinite media. The impedance of the
gas in the swim bladder is readily determined,
and the reflection coefficient for the swim bladder
is approximately — 1. Determination of the
acoustic impedance of fish bone or flesh is dif-
ficult and care must be taken to insure valid
measurements. Shishkova (1958) measured the
density of and speed of sound in flesh from a few
species of fish and determined the reflection co-
eflicient in fresh water to be about 0.05. Haslett
(1962b) used a different technique to indirectly
measure the reflection coeflicieiits of flesh and
bone from haddock and cod. He found the re-
flection coeflicient of flesh in fresh watei- to be

about 0.05, in seawater to be about 0.02, and the
reflection coeflicient of bone to be about 0.25.

Using these values for the reflection coefll-
cients and his "standard fish dimensions," Has-
lett (1962c, 1964) has modeled fish bodies, back-
bones, and swim bladders. Utilizing rubber
ellipsoids to model the fleshy body of the fish,
he found that the number of lobes obtained in
polar plots for the ellipsoids and for actual fish
agreed fairly well, that is, with less than 509f
error, but that the target strengths obtained for
the models were considerably lower than those
obtained for the fish. Using rubber and plastic
cylinders to model the backbone and copper cyl-
inders to model the swim bladder, Haslett has
examined variations in the target strength of
these models as frequency, size, and aspect are
varied. A brief summary of Haslett's work for
side aspect is shown in Figure 3. Along with
his data for the acoustic cross-sections of stickle-
backs and guppies, apjM'oximations to the
acoustic cross-sections of the swim bladder, body,
and backbone are given. The various curves for
each component were determined by Haslett
(1965) using his reflection coeflicients and the
results of his modeling experiments and depend

10

FiGl'Rlv 'A. — Sido-aspect acoustic cross-sections dptprmincd
by Haslett.

708

LOVE: MEASUREMENTS OF FISH TARGET STRENGTH

on how the component is approximated and on
the limits of that ai^proximation. Hence the
curves are a function of whether the swim blad-
der is approximated by a spherical bubble or a
rigid cylinder; what the limits of the geometric
and Rayleigh scattering regions are for the body
and the backbone; and whether the body is
approximated by an ellipsoid or a plane in the
geometric region. These curves indicate that
the swim bladder jiredominates over most of the
given L/\ range, but that the body and backbone
become significant at the higher L/X's. It is
apparent that Haslett's measurements of the
acoustic cross-sections of sticklebacks and gup-
pies vary widely and do not follow any of his
curves. This variability is not fully explained
by any of his experiments on fish or models.
Obviously, the nature of the echo-formation pro-
cess is quite complex if Haslett cannot explain
this variability after such comprehensive work.

In attempting to quantify fish resources the
objects of interest are usually fish schools rather
than individual fish. When the target strength
of a school is measured, the question to be an-
swered is "What is the average size and number
of fish required to produce this target strength?"
The answer will depend on the average target
strength of the fish in the school, and any vari-
ations among the individuals will be of minor
importance. If a forward-looking sonar is used
for quantification, the minimum size and number
of fish required to produce a given target
strength will occur at the aspect for which the
target strength of an individual fish is a max-
imum. This aspect will be near the side aspect
of the fish. Thus, average values for the max-
imum side-aspect target strength of an individual
fish are important for quantification of fish
schools with a forward-looking sonar. If a down-
ward-looking sonar, or echo sounder, is used for
quantification, average values for the dorsal-
aspect target strength of an individual fish are
important.

For these reasons the author has made max-
imum side-aspect (Love, 1969) and dorsal-aspect
(Love, 1971) target strength measurements as
a function of fish size, species, and frequency.
The measurements were made in the laboratory,
and hollow rubber spheres were used as refer-

ence targets for calibration. It was found that
the magnitude of the variation in target strength
for one species was of the same order as it was
for all species. Therefore the data for all spe-
cies were combined with all other available per-
tinent data and a regression line was calculated
for each aspect using the method of least squares.
Figure 4 shows all the dorsal aspect data. The
data were obtained using fish from Ifi families
in 8 different orders: Clupeiformes, Cyprini-
formes. Gasterosteiformes, Cyprinodontiformes,
Mugiliformes, Gadiformes, Beryciformes, and
Perciformes. The fish ranged in length from
about 1 cm to 1 m. Some had swim bladders
while others did not. Insonifying frequencies
ranged from 8 kHz to 1480 kHz. Note that the
parameters used here are a/X- and L/\, which
diff"er slightly from those used by Haslett. The
equation for the regression line calculated from
these data is

o-A^ = 0.041 (L/X)i94, (9)

and the dorsal-as]iect target strength is

r„ = 19.4 log L + 0.6 log \ — 24.9 (10)

Equation (10) is for T,, at 1 m and L and \ in
meters and is valid in the range 0.7 ^ L X ^ 90.
Figure 5 shows all the maximum side-aspect
data. The data were obtained using fish from
13 families in 7 different orders: Cypriniformes,
Gasterosteiformes, Cyprinodontiformes, Gadi-
formes, Beryciformes, Perciformes, and Pleuro-
nectiformes. Fish size and acoustic frequency
ranges were approximately the same as those for
dorsal aspect. The equation for the regression
line calculated from these data is

0-/X2 = 0.064 (L/\y\ (11)

and the maximum side-aspect target strength is

Ts = 22.8 log L — 2.8 log X — 22.9 (12)

Equation (12) is valid in the range 1 ^ L/X
:^ 130, and again Ts is at 1 m and L and X are in
meters.

Figure 6 is a nomogram solving equations
(10) and (12), given the acoustic frequency, /,
in kHz, and the fish length, L, in cm.

709

FISHERY BULLETIN: VOL. 69, NO. 4

10°

10'

10=

1 1 1

1

1 .

1

1

LEGEND
0 YUOANOV, GAN'KOV,

AND SHATOBA (1966)
A HASLETT (1962 d, 1965,1969)
D V0LBERG(I963)

^)

A

^ DIERCKS AND

GOLDSBERRY (1970)

V HASHIMOTO AND
MANIWA 11956b)

TO "^

-

> SMITH (1954)

l^ JONES AND PEARCE (1958)

n

D c

[

f "

-

-

+ LOVE (1969)

/

A
A

-

(r/X'-0 064

(L/X)»»« ^

\

i /

A
A

D \

V /

^

\

. rf/ A

D t

r

-

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1

V A

—

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A

—

V

-

-

:0*

A

-

+
+

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cudf ■•■ A^i

^7^ A A

S^ ^ A

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» A

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A

Va a

i A

-

* * 7*

A

—

+

1 1 ^f 1

1 1

1

1

1

10
L/X

10'

Figure 4. — Dorsal-aspect
acoustic cross-section of an
~\ individual fish.

10'

710

LOVE: MEASUREMENTS OF I-ISU TARGET STRENGTH

10'

10'

10==

to

IQ-

10"

FiGURE 5. — Maximum side-
aspect acoustic cross-sec-
tion of an individual fish.

10"

I

1 1

1

I

1

□

LEGEND

o

YUDANOV, GAN'KOV,
AND SHATOBA (1966)

B

a

A

HASLETT (I962d,l9€5)

a

V0LBERG(I963)

0

SHISHKOVA (1964)

V

V

HASHIMOTO AND

A

^

^

MANIWA (1955, 1956 a,b)

A

""

t>

SMITH (1954)

<

MIDTTUN AND H0FF(I962)

0* AA^„

;

^

«

JONES AND PEARCE(I958)
MCCARTNEY AND

STUBBS (1970)

>

+

LOVE (1971)

•^^?

■ I"^^

V \

^

X

(T/X' =0041 (L/X)

0

• 4

> A

—

^^^

-

§^f^

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'*nHe%^,^ . «A

A
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A

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'iA A

+ '*-x X X "

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A

* ' " X x"

—

" « ■ «

0

—

1

X

1 1

1

1

1

10

10'

10'

711

FISHERY BULLETIN: VOL. 69. NO. 4

r

TARGET STRENGTHS

or AN
INDIVIDUAL FISH

FOR DORSAL ASPECT*
I00< Lf £14000

FOR SIDE ASPECT-

150 < LI < 20000

Figure 6. — Nomogram for calculating the dorsal-aspect
and maximum side-aspect target strengths of an indi-
vidual fish.

QUANTIFICATION AND
IDENTIFICATION OF SCHOOLS

Since estimates for the maximum side-aspect
and dorsal-aspect targret strengrths of individual
fish are available, the determination of the
target strengths of fish schools at these aspects
will depend on the detei-mination of the efl^ects
of the number of fish in the school and their
distribution. If the fish are widely spaced, or
in a plane perpendicular to the sonar beam, so
that there is no acoustic interaction among the
individuals, the target strength of the school is
equal to the average tai'get strength of an indi-
vidual ])lus 10 times the logarithm of the number
of fish. The probability of finding a school that
meets these qualifications is quite small and
therefore the effects of interactions among the
fish must be taken into account.

Little exjierimental work on the acoustic inter-
actions of fish in a school has been done, although
some measurements of the target strengths of
groups of fi.sh have been made, usually with
little concern for the distribution of the indi-
viduals (e.g., Thorpe and Ogata, 1967; Shishko-
va, 19(50). Some theoretical work on distribu-
tions of scatterers has been done, the scatterers
usually being point scatterers or small bubbles
(e.g., Foldy, 191."); Weston, 196(5). Weston
( 1967) has applied the results for bubbles to fish

schools and has estimated reflection coefiicients
for regions well-below and well-above resonance.
Since there is no interference region for a bubble,
he does not concern himself with interference
efl'ects, and his results are of limited value in the
interference region. Boyles (1969) has dis-
cussed the mathematical theory of multiple scat-
tering from fish schools, but to obtain results
in the interference region the complete spatial
scattering and absorption pattern of an individ-
ual fish must be known.

The identification of a school of fish utilizing
target strength information is obviously much
more difficult than its quantification, and since
it is not yet possible to quantify fish schools with
this information, it is surely not yet possible
to identify them.

Figure 3, which summarized Haslett's work,
seems to indicate that no reasonable pattern of
target strength vs. frequency can be found for
any s]iecies due to the rapid fluctuations of target
strength. Haslett's measurements were made
at three widely spaced frequencies. Measure-
ments made by the author at a larger number
of more closely spaced frequencies indicate that
for individual fish these fluctuations are not so
rapid and that possibly individual fish may be
identified through the use of target strength vs.
frequency (a L-vs. L X) curves. Dorsal aspect
target strength measurements made on six bay
anchovies, Anchoa mitchilU, one Atlantic men-
haden, Brevoortia tyraymus, five goldfish, Caras-
shcs auvatiis, and six Atlantic silversides, Menid-
ia meniditt, revealed that all of these fish had
similar or/Lr vs. L \ curves (Love, 1971). The
most notable feature of these curves is a deep
minimum in the neighborhood of L/\ = 10. This
minimum is easily seen in the average curves
for each species shown in Figure 7. Similar
measurements on three mummichogs, Fundulns
heterocUtiis, five striped killifish, Funduhts
majiilis. six black crappies, Pomoxis n'niromacu-
latiis. and four si)otted seatrout, Cynscion nehn-
losus, revealed that the cr/L^ vs. L/k curve for
any individual of these species bears no easily
discernible relation to that of most, or all, of
the other individuals of that species, or to the
average curve for that species.

The anchovies, goldfish, and menhaden are

712

LOVE: MEASUREMENTS OF I-ISII TARGET STRENGTH

malacopterygians, the more primitive teleosts;
the crappies and seatrout are acanthoi)teryg'ians,
the more advanced teleosts; and the mummi-
choo;s, killifish, and silversides belong to inter-
mediate orders which have characteristics of
l)oth groups (Berg, 1947; Bertin and Arambourg,
1958). In general, the malacopterygians have
physostomous swim bladdei's, osseous bone tis-
sue, intermuscular bones, comparatively many
vertebrae, fins without siiines, and cycloid scales.
In general, the acanthopterygians have physo-
clistous swim bladders, osteoid bone tissue, no
intermuscular bones, comjiaratively few verte-
brae, fins with spines, and ctenoid scales. Con-
sidering that the swim bladder, bones, and
possibly scales of a fish contribute to its acoustic
cross-section, it is obvious that the malacopter-
ygians and the acanthopterygians have signifi-
cant structural differences in components which
have been shown to be acoustically important.
Why the malacojiterygians and one intermediate
species display the characteristic minimum in

CRAPPIES

0 02

001

0 005

0 002

00005

GOLDFISH

FiGl'RE 7. — Average measured dorsal-aspect acoustic
cross-sections for different species of fish. (From Love,
1971.)

(t/L- near L X = 10, or why the acanthopter-
ygians and the other two intermediate species
have no distinctive cr/L- vs. L/\ curve cannot
be answered, given the present limited knowl-
edge of echo-formation by fish.

Although these differences cannot be presently
exjjlained it seems probable that if there were a
geograjjhic area in which two species with about
the same size and habits predominated, and if
one species were a Clupeiform and the other a
Perciform, a ship with a wide-band sonar could
differentiate between individuals of each species
by examining their target strength vs. frequency
curves. This hypothetical example indicates how
very limited the present capability to identify
fish by determining target strength is. Hope-
fully, more measurements at many frequencies,
with dissection and removal of various compo-
nents of the fish, and more sophisticated model-
ing techniques will exjilain the features of the
target strength vs. frequency curves for indi-
viduals of a few species. This could then lead
to the prediction of curves for other species,
which in turn could greatly increase the ability
to differentiate between individuals of different
species. This information could then be applied
to the difl'erentiation of schools of different spe-
cies, although it is to be expected that the man-
ner of distribution of the fish in the school will
cause significant differences between the target
strength vs. frequency curve obtained for the
school and the average curve for the individuals
in the school.

SUMMARY

Some of the more important results of mea-
surements of fish target strength to date are:
( 1 ) it has been determined that practically every
case of interest to the fishing industry is in the
region of interference effects, (2) the major con-
tributors to the target strength of a fish in this
region have been determined and their acoustic
impedances measured, (3) the variations of tar-
get strength with aspect for an individual fish
have been examined, (4) estimates of the dorsal-
aspect and maximum side-aspect target strength
of an individual fish have been made, (5) there

713

FISHERY BULLETIN: VOL. 69. NO. 4

are indications that the identification of individ-
ual fish based on target strenjjth vs. frequency
curves is possible for limited cases.

The two goals of fish target strength measure-
ments, namely quantification and identification
of fish schools, have not yet been attained. The
quantification of fish schools and the identifica-
tion of many individual fish should be ho]iefully
accomplished in the next few years. The iden-
tification of schools will require the information
on quantification of schools and identification of
individuals, and therefore will probably not be
accomplished for some time.

LITERATURE CITED

Berg, L. S.

1947. Classification of fishes, both recent and fossil.
J. W. Edwards, Ann Arbor, Mich. 517 p.
.Bektin, L., and C. Arambourg.

1958. Supre-ordre des Teleosteens. In P.-P. Grasse
(editor), Traite de Zoologie, Agnathes et Poissons
1.3: 2204-2500. Ma.sson et Cie., Paris.
BOYLES, C. A.

1969. Preliminary report on the mathematical the-
ory of the multiple scattering of an acoustic pulse
from a random collection of volume scatterers
with application to scattering from fish schools.
Tracor, Inc. Doc. RL/69-074 U, Rockville, Md.,
83 p.

Gushing, D. R., F. R. H. Jones, R, B. Mitson, G. H.
Ellis, and G. Pearce.

1963. Measurements of the target strength of fish.
J. Br. Inst. Radio Eng. 25, p. 299-303.
DiERCKS, K. J., and T. G. Goldsberry.

1970. Target strength of a single fish. J. Acoust.
Soc. Am. 48(1, Part 2): 415-416.

FOLDY, L. L.

1945. The multiple scattering of waves. I. General
theory and isotropic scattering by randomly dis-
tributed scatterers. Phys. Rev. (Second Serie-s)
67: 107-119.
Hashimoto, T., and Y. Maniwa.

1955. Ultrasonic reflection loss of fish shoal and
characteristics of the reflected wave. Tech. Rep.
Fishing Boat No. 6, p. 113-139. [English transl. :
Ministry of Agriculture, Fisheries and Food, Fish-
eries Laboratory, Lowestoft, England (1957)].

1956a. Study on reflection loss of ultrasonic wave
on fish-l)ody by millimeter wave. Tech. Rep. Fi.sh-
ing Boat No. 8, p. 113-118. [English tran.sl.:
Ministry of Agriculture, Fisheries and Food, Fish-
eries Laboratory Lowestoft, England (1957)].

1956b. Study on reflection loss of ultrasound of mil-
limeter wave on fish-body, (2). Tech. Rep. Fish-
ing Boat No. 9, p. 165-173. [English tran.sl. : Min-
istry of Agriculture, Fisheries and Food, Fish-
eries Laboratory, Lowestoft, England (1957)].
Haslett, R. W. G.

1962a. Measurement of the dimensions of fish to
facilitate calculations of echo-strength in acoustic
fish detection. J. Cons. 27: 261-269.

1962b. The back-.scattering of acoustic waves in
water by an obstacle II: Determination of the
reflectivities of solids using small specimens.
Proc. Phys. Soc. 79: 559-571.

1962c. Determination of the acoustic scatter pat-
terns and cross-sections of fish models and ellip-
soids. Br. J. Appl. Phys. 13: 611-620.

1962d. Determination of the acoustic back-scatter-
ing patterns and cross sections of fish. Br. J.
Appl. Phys. 13: 349-357.

1964. The acoustic back-scattering cross sections
of short cylinders. Br. .J, Appl. Phys. 15: 1085-
1094.

1965. Acoustic backscattering cross sections of fish
at three frequencies and their representation on a
univei-sal graph. Br. J. Appl. Phys. 16: 1143-1150.

1969. The target strengths of fish. J. Sound Vib.
9: 181-191.
Jones, F. R. H., and G. Pearce.

1958. Acoustic reflexion experiments with perch
(Perca fliiviatilis Linn.) to determine the pro-
portion of the echo returned by the swimbladder.
J. Exp. Biol. 35: 437-450.
Love, R. H.

1969. Maximum side-aspect target strength of an
individual fish. J. Acoust. Soc. Am. 46: 746-752.

1971. Dorsal aspect target strength of an individ-
ual fish. J. .A.coust. Soc. Am. 49: 816-823.
.McCartney, B. S., and A. R. Stubbs.

1970. Measurements of the target strength of fish
in dorsal aspect, including swimbladder resonance.
In G. B. Farquhar (editor). Proceedings of the
International Symposium on Biological Sound
Scattering in the Ocean, p. 182-214. Maury Cen-
ter for Ocean Science Report 005, Preliminary ed.

Midttun, L., and I. HOFF.

1962. Measurements of the reflection of .sound by
fish. Rep. Norw. Fish. Mar. Invest. 13(3), 18 p.
Shishkova, E. V.

1958. An investigation of the acoustic properties
of fish. Tr. Vses. Nauchn.-issled. Inst. Morsk.
Rybn. Khoz. Okeanogr. 36: 259-269. [Engli.sh
transl.: Associated Technical Services, Inc., East
Orange, N.J. (I960).]

714

LOVE: MEASUREMENTS OF FISH TARGET STRENGTH

1960. Sound reflecting capacity of pelagic and ben-
thic fish. Rybn. Khoz. 36 (10): 56-63. [English
transl.: in Translations on USSR fishing industry
and marine resources No. 12, Clearinghouse Fed.
Sci. Tech. Inf., JPRS 44,174 (1968).]

1964. Study of acoustical characteristics of fish.
In Modern Fishing Gear of the World 2, p. 404-
409. Fishing News (Books) Ltd., London.
Smith, P. F.

1954. Further measurements of the sound scat-
tering properties of several marine organisms.
Deep-Sea Res. 2: 71-79.
Thorpe, H. A., and C. T. Ogata.

1967. Hydroacoustic reflections from captive an-
chovies. Lockheed Calif. Co. Rep. 20989, San Di-
ego, 45 p.

VOLBKRG, H. W.

1963. Target strength measurements of fish.
Straza Industries Rep. R-101, El Cajon, Calif.,
146 p.
Weston, D. E.

1966. Acoustic interaction effects in arrays of small
spheres. J. Acoust. Soc. Am. 39: 316-322.

1967. Sound propagation in the presence of bladder
fish. In V. M. Albers (editor) Underwater acou-
stics 2(Ch. 5) : 55-88. Plenum Press, New York.

YUDANOV, K. I., A. A. Gan'kov, and O. E. Shatoba.
1966. Reflection of sound by commercial fish of the
Northern Basin. Rybn. Khoz. 42(12): 57-60.
[English transl.: Clearinghouse for Fed. Sci.
Tech. Inform. Document TT-67-61940.]

715

DISTRIBUTION AND BIOLOGY OF MYSIDS (CRUSTACEA, MYSIDACEA)

FROM THE ATLANTIC COAST OF THE UNITED STATES

IN THE NMFS WOODS HOLE COLLECTION

Roland L. Wigley and Bruce R. Burns'

ABSTRACT

Nineteen species of marine mysids, representing 16 genera, liave lieen assembled at the NMFS Biolo-
gical Laboratory, Woods Hole, Mass. These specimens were collected between 1953 and 1969 from the
continental shelf and slope off the east coast of the United States between Canada and southern Flor-
ida. The species represented are: Eiicopia grimaldii, Borcomysis tridcns, Bowmanidla portoriceiisis,
Anchmlina typica, Erythrojis crythrophthalma, Meterytlirops rohiista, Hypererytlirops caribbaea,
Pseudomma affine, Pseudnmma sp., Amblyops abbreviata, Dathymynis renoculata, Mysidopsis bigelowi,
M. furca, Promysis atlantica, Mysis mixta, M. stenolepis, Piaunns flexuosus, Neomysis americana, and
Heteromysis formosa.

Geographic and bathymetric distributions, relations with liottom sediments, and other ecological in-
formation are given for all species. Biological data such as spawning season, clutch size, body length
at maturity, and similar information are reported for 11 species. More detailed accounts of the life
history and ecology of Erytlirops crytlirophtlialma , My^idniii^iis bigelowi, and Ncdiiiysis americtma are
made possible by the large numbers of specimens of these species.

This repoi't is based on the collection of my-
sids assembled by the Food Habits Project
and the Benthic Invertebrates Project at the
National Marine Fisheries Service (NMFS),
Biologfical Laboratory — formerly known as the
Bureau of Commercial Fisheries (BCF) — Bio-
loffical Lalwratory, Woods Hole, Mass. Mysids
were not specifically sought in assembling this
collection; they were acquired from biological
samjiles collected for ecological studies pertain-
ing to various kinds of demersal fishes and
assemblages of benthic invertebrates. Estua-
rine and inshore species are few because nearly
all sampling was conducted in offshore areas.

The known mysidacean fauna off the eastern
coast of the United States is not extensive.
Tattersall (1951) made a thorough review of
the literature and the mysid specimens in the
U.S. National Museum. He reiiorted only 11
shallowwater (less than 200 m) species occur-

^ National Marine Fisheries Service, Biological Lab-
oratory, Woods Hole, Mass. 02543.

Manuscript accepted July 1971

FISHERY BULLETIN: \'0L. 61, NO. 4. 1071.

ring in the area between Maine and Florida.
This includes estiiarine and shore forms as well
as middle and outer continental shelf species.
Although a few additional species have been
found in this area since the time of Tattersall's
study (Klawe, 19.5.5; Bowman, 1957, 1964;
Wigiey, 1963; Bacescu, 19(58; Haefner, 1968;
and others) and undoubtedly some species re-
main undetected, it is reasonable to conclude
that only a modest number of different kinds
of mysids occur in this region.

A substantial portion of the sjiecies in the
NMFS samples from the western Atlantic also
occur in European waters. They are: Eucopia
(jrimaldii, Borenmysis tridens, Eiythrops ery-
fhmphthalma. Meterythrops rohnsta, Pseudom-
ma (if fine, Amblyops abbreviata, Mysis mixta,
Praumis flexuosiis, and Heteromysis formosa.
Those sjiecies that do not have an amphi-Atlantic
distribution are largely indigenous to the west-
ern North Atlantic, namely: Bowmaniella por-
toricensis, Hypererythrops caribbaea, Pseudom-
ma sp., Bathymysis renoculata. Mysidopsis big-
elowi. M. furca, Mysis .'iteuolepis. and Neomysis

717

FISHERY BULLETIN: VOL. 69, NO. 4

americana. These indigenous species are all
inhabitants of warm-temperate to troi)ical areas;
none are subarctic or boreal. Presumably mem-
bers of this group have been unable to bridge
the ocean because of unfavorable water tem-
peratures across the northern rim of the At-
lantic Ocean where water depths are favorable.
Amblyops abbreviata and Metenjthrops robmta.
in addition to having an amphi-Atlantic distri-
bution, are also widely distributed in the North
Pacific Ocean. Only Aiirhidliiid tijpica, which
occurs in the Atlantic and Pacific Oceans, and
Promysis atldjificd, which occurs in the North
and South Atlantic Oceans, do not fall into the
two main categories above.

The Euroi^ean si)ecies Praiuuis flexHonuti.
now well established in the coastal waters of
New England, may have been introduced rather
recently by the activities of man (discu;:sion on
pages 735 and 73G).

The information presented herein supple-
ments our scanty knowledge of the biology of
individual sjiecies and also ])rovides a general
review of the kinds of mysids in the western
Atlantic, their distribution, relative abundance,
and relations with some environmental char-
acteristics.

MATERIALS AND METHODS

Three million specimens i'ei)resenting 19 spe-
cies and 16 genera were collected during 19.53-69
from the continental shelf and slope off the east-
ern coast of the United States between Canada
and southern Florida.

Two-thirds of the samples were collected from
the offshore New England region, between Nova
Scotia, Canada, and Long Island, N.Y. (Figure
1). About 2,000 samples were analyzed from
this region. Sparse sampling (1,000 samples)
was conducted between New York and Key
West, Fla. Most of the collections were taken
by six oceanograiihic research vessels: Alba-
tross III, Albatross IV. Blueback, and Delaware,
all operated by the National Marine Fisheries
Service; and Asterias and Gosnold, operated by
the Woods Hole Oceanographic Institution,
Woods Hole, Mass. Collection data and biologi-
cal information for each sample of nivsids in

the NMFS collection are given in Burns and
Wigley." The collection data include: latitude
and longitude, water depth, date, sampling gear,
vessel name, cruise and station number. The
biological information consists of the number
of specimens, summary of body length by spe-
cies, sex, and stage of maturity.

The 12 kinds of sampling instruments used
in collecting mysids were: bottom skimmer,
Cam!)bell gral:>, diii net, 30-cm ring net, 1-m
i-ing net, plankton net, naturalists dredge, otter
trawl, sled-mounted ring net, Smith-Mclntyre
grab, shrimj) trawl, and Van Veen grab. A few
sjiecimens were obtained from fish stomachs.
The kinds of gear mo.st successful in catching
mysids were ring nets, grab samjjlers, the bot-
tom skimmer (a combination dredge and plank-
ton net), and dredges with fine-mesh nets. Only
occasional siiecimens were obtained with bot-
tom trawls and dredges with coarse mesh
nets.

Mysids were preserved in Formalin at sea
and transferred to ethyl alcohol at the time
the sami)les were sorted in the laboratory
ashore.

In classifying larvae according to their
stage of development, we have followed Nair
(1939).

A total of 5,-566 specimens were examined
under low-power magnification with a binocular
microscojie to determine sex and stage of
maturity and to measure size. Body length
was measured from the anterior margin of the
carapace to the posterior end of the telson,
using an ocular micrometer in the micro-
scope.

SYSTEMATIC ARRANGEMENT

For the .systematic arrangement and termi-
nology we have followed Tattersall and Tatter-
sall (1951). The list of species in their respec-
tive groupings are as follows:

= Burns, Bruce R., and Roland L. Wigley. 1970. Col-
lection and bioloRical data pertaining to my.sids in the
collection at the BCF Biological Laboratory, Woods Hole.
Lab. Ref. No. 70-2, 36 p. Bur. Comnicr. Fi.sh. Biol.
Lab., Wood.s Hole, .Mass. (Unpublished manuscript.)

718

WIGLEY and BURNS.- DISTRIBUTION AND BIOLOGV OF MYSIDS

/ '< '^'^ NOV*

, SCOIIA^ , .

^. .•.••. •.-••'•r-'t' •'c-T.'

Figure 1. — Chart of the Atlantic Continental Shelf and adjacent area showing the
location of sampling stations. A. Samples collected with dredges and similar types
of collection instruments. B. Samples collected by means of grab samplers.

719

Order MYSIDACEA

Suborder LOPHOGASTRIDA

Family EUCOPIIDAE

Eticojiia grhnaldil Nouvel, 1942

Suborder MYSIDA

Family MYSIDAE

Subfamily BOREOMYSINAE

Boreomysis tridens G. 0. Sars,
1870

Subfamily GASTROSACCINAE
Boirmaniella portoricevsis

Bacescu, 1968
Avrhialiiia tyjiica (Kroyer, 1861)

Subfamily MYSINAE

Tribe ERYTHROPINI

Erythrops enjfhrophthahnd

(Goes, 1861)
Meterythrops robiisfa S. I. Smith.

1879
Hypereryfhni/i.s rariblxtca Tatter-

"sall, 1937
PHeudoinma uffliie C. O. Sars,

1870
Psendomma sp.
Ambiyops abbreviata (M. Sars,

1869)

Tribe LEPTOMYSINI

Bathymysis venocnluta Tattersall,

1951
Mysidops;is bifiplovl Tattersall.

1926
Mysidopsis fnrca Bowman, 1957
Projnysis atlantira Tattersall,

1923

Tribe MYSINI

Mysis mixta Lilljebor<r, 1852
Mysl.s stenolepis S. I. Smith, 1873
Pmunna flexuosus (O. F. Mtiller,

1776)
Neomysis americawi (S. I. Smith,

1873)

Tribe IIETEROMYSIXI

Heteromysis formosa S. I. Smith,
1873

FISHERY BULLETIN: VOL. 69. NO. 4

SPECIES ACCOUNTS

Order MYSIDACEA
Suborder LOPHOGASTRIDA

Family EUCOPIIDAE
Eucopia grimaldii Nouvel, 1942

This mysid is a moderately large bathypelagic
species that occurs most commonly at depths
of about 2,000 m and has not been found at less
than 300 m. Its nfeoKraphic distribution is cos-
mopolitan, it having- been reported from the
North and South Atlantic, Pacific, and Indian
Oceans. The majority of records are from tem-
loerate and tropical waters, but it has been re-
corded from as far north as Iceland and southern
Greenland and as far south as South Africa and
New Zealand (Fage, 1942; Tattersall, 1951).

There is only one specimen of E. gthnaldii in
our collection (Burns and Wigley, Table 2).
taken at a dce|)\vater station (700 m) along the
continental slope off southern New England
(Figure 2). This siiecimen was caught in a
12.2-m shrimj) trawl equipijed with a coarse-
mesh (6.5 cm extension measure) net. Al-
though the net was fished on bottom, it cannot
be determined at what depth the specimen oc-
curred. The low fishing efiiciency of this trawl
during setting and retrieval, however, lends
support to the belief that it was caught on or
near the ocean bottom.

This is only the second record of this species
from off the eastern coast of the United States,
even though it is moderately common in other
areas and widely distributed throughout the
world. Its occurrence in deej) water over bot-
tom sediments compo.sed of silts and clays is
typical for this species.

Suborder MYSIDA

Family MYSIDAE

Subfamily BOREOMYSINAE

Boreomysis tridens G. O. Sars, 1870

This is a moderately large species that is
known to occur only in the Noiih Atlantic
Ocean. It is distributed along the eastern At-
lantic Continental Sloite frum the Bay of Biscay

720

WIGLEY and BL RNS, DISTRIBUTION AND BIOLOC.V OF MYSIDS

f

NEW
YORK

Boreomysis tridens

Eucopia grimaldii

FiciRE 2. — (ieographic distribution of Eucopia grimaldii
and rioreomysis tridevs based on specimens in the col-
lection at the NMFS Biological Laboratory, Woods Hole.

north to Norway, across to the Faroe Ishxnds,
south and west of Iceland and Greenland, south-
ward along the continental slope of North Amer-
ica (Tattersall and Tattersall, 1951). Tattersall
(1951) lists over 20 records from off the north-
east coast of the United States, ransingr as far
south as Delaware (lat 38°27' N).

This species was reported by Verrill (1885)
as being common on the continental slope in the
western Atlantic. The collections of this mysid
reported by Tattersall (1951), all made by the
research vessels Albatross, Fish Hairk. and
Challenger, reflect its deepwater habitat.

Our collection contains one sample of this
species consisting of three specimens (Burns
and Wigley, Table 3). They were taken on the
west side of Hydrographer Canyon, located
about 130 km southeast of Nantucket, Mass.
(Figure 2). The dejjth of water at this loca-
tion is 102 m. Its occurrence at this depth and
on bottom sediments of silty sand are charac-
teristic for this species. Two specimens 15.0

and l(i.5 mm in length are immature; a 26-mm
specimen is an adult male.

Subfamily GASTROSACCINAE
Bowmaniella portoriceiish Bacescu, 1968

B. portorkensis is morphologically very sim-
ilar to B. johnsoiii (Tattersall). A close exam-
ination of pleopod 3 in male specimens and of
the uropod and the jjosterior part of the caraiiace
in all s]Decimens was required for reliable dif-
ferentiation of these two species. B. portori-
censis is a subtropical species that has Ijeen re-
ported by Bacescu (1968) off the southeastern
coast of the United States between Beaufort,
N.C., and northern Florida. Although this spe-
cies was known in only a few locations at the
time of Bacescu's report, it is undoubtedly more
common than these few i)ublished i-ecords sug-
gest, as indicated by the relatively large number
of sami)les in the NMFS collection. Its rather
small size (up to 11-mm body length) and its
occurrence in areas that have not yet been thor-
oughly studied jiresumably have contrilnited to
the paucity of collections.

The NMFS collection contains 100 specimens
of B. portoriceiiHis from 46 samples, all of which
are from off the southeastern coast of the United
States (Figure 3; Burns and Wigley, Table 4).
The northernmost samiiles were taken ai^proxi-
mately 90 km north of Cape Hatteras, N.C., at
lat 36° N. The southei'n limit of our samples is
15 km south of Ft. Pierce, Fla., at lat 27°20' N.
All of these samjiles were collected within 125 km
of the shoreline. Water depths at which they
occurred I'ange from 9 to 56 m, and most of them
were t;'.ken at dejiths between 15 and 39 m.

Body lengths average ().9 mm; the range in
length is 3.1 to 10.0 mm.

This species is chiefl.y an inhabitant of sandy
sediments. Sand was present at all stations.
Shell was a major component at T,r of the sta-
tions and a minor component at 26 ''r of the
stations where B. portoricensis occurred.

Seven females, 7.9 to 10 mm in length, from
the May and June samples were carrying larvae
in the brood iiouch. The numl)er of larvae i)er
clutch ranges from 1 (obviously an incomplete
Ijrood) to 30. Only the relativel.v advanced

721

1-rSIII.RV ISLLLliTIN; VOL. 6'>, NO. 4

Bowmaniella portoricensis

Figure '.i. — (ieographic distribution of Bowinaniella
portoricensis based on specimens in the collection at the
NMFS Biological Laboratory, Woods Hole.

larval stas'es — V, VI, and VII, with lengths from
1.0 to 1.2 mm — are represented. The jiresence
of larvigerous females as well as immature spe-
cimens in May and Jime samjiles reveals that
/>*. portoricevslf! si)awns not only in early sum-
mer, but in the spiMnfjtime as well.

The NMFS collection contains :'A males and
47 females, a ratio of 0.7 male to 1 female.

Auchialiiia typica (Kr0ycr, 1861)

This moderately small, stout mysid is widely
distributed in both the Atlantic and Pacific
Oceans. It has been reported from the Pacific
near the central (Hawaii and Gilbert Islands)
and southwestern (China Sea to (Jreat Barrier
Reef) res'ions. According to Tattersall (19.")])
it is abundant in the region of the Philijjpine
Islands and the East Indies. Though it has been
reiiorted in the North Atlantic from south of
Newfoundland (Nouvel, 1943), records from
the vicinity of the Bahama Islands and Cuba are
the most common. Many occurrence records
in the literature are ba.sed on siiecimens collected
in surface waters.

The NMFS collection contains three speci-
mens from thi'ee difi^'erent stations (Figure 4;

Anchialina typica

Klia lii-: 1. — (it'ogi'apliic distribution of Aiicliialiiia typica
based on specimens in the collection at the NMF.S Rio-
logical Laboratory, Woods Hole.

WIGLEY and BIRNS. DISTRIBUTION AND BIOLOCi' OF MVSIDS

Burns and Wigley, Table 5) . The southernmost
sample is from off northern Florida. The other
two samples were taken 60 to 70 km east of
Georgetown, S.C. All specimens are males 4.5
to 5.0 mm long. They were all collected with the
Campbell grab in rather shallow water, between
32 and 38 m. Bottom sediments at these sta-
tions are composed of fine and medium sand.
These are the first records of this genus and this
s]iecies from the shallow shelf region off the
eastern coast of the United States.

A closely related species, .4. a g ills, is an active
swimmer that migrates to surface waters at
night and descends to deep water before day-
break (Russell, 1925). Based on NMFS rec-
ords of ^. typica reported herein, and on Tatter-
sail's (1951) records, it appears likely that A.
tijl)ica in the shallow and moderately shallow
regions of the continental shelf may also dwell
on bottom during the day and rise to surface
or near surface waters at night.

Subfamily MYSINAE

Tribe ERYTHROPINI
Erythrops erythrophthalma (GiJes, 1864)

Geographic Distribution

This colorful mysid species has a widespread
distribution on the continental shelf and upper
portion of the continental slope in Arctic seas
and the North Atlantic Ocean. In eastern At-
lantic waters it extends from the Arctic south-
ward to the British Isles. In the western At-
lantic it has been reported from off Greenland,
eastern Canada, and off the northeastern United
States as far south as Delaware (Gardiner, 1934;
Bigelow and Sears, 1939; Tattersall, 1951;
Tattersall and Tattersall, 1951).

The NMFS collection contains 187 samples to-
taling 4,573 specimens of this species (Figure 5;
Burns and Wigley, Table 6). These sami)les
were collected on the continental shelf and slope
between southeastern Nova Scotia and Long
Island, N.Y. By far the largest number of sam-
ples is from the southei'n part of Georges Bank.
A moderate number of samples were taken in
the offshore southern New England area south

^- yi^f NOVA \ \ >\

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0 KM 100- ^ f ;|[ SCOTIA^ ' ^ V )

X

v-;^

\ J ^'' ' K .^.^ 5 '' '"' -^'' /

} ' ^s 1 » ' ^ 1

A ^- -•-,-' /

<"V ^J >\'.-^J

V%' '' "*' I

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sJ* V • •n \

A •' • • .-^ ••.! 1

^5* ^ ^ •^V 1

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\\ •/ 'wA

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Portland') « / • /

V^ • .••••/

) • .* . . -*" /

J- ' r.t'\<:-'"/

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^

/l.!^ S- /

f

^' f// ' / ^-^

//// ''' (''

w u

vo«i3^ \ 1 Erythrops erythrophtha

ma

Figure 5. — Geographic distribution of Erythrops ery-
tJirnphthaJnia based on specimens in the collection at the
NMFS Biological Laboratory, Woods Hole.

of Rhode Island and eastern Massachusetts. The
common occurrence of this species on Georges
Bank was somewhat unexpected in view of the
fact that W'hiteley (1948) found it to be a minor
component in plankton samjjles collected there
in 1939-41.

Bathymetric Distribution

This is an offshore species that occurs chiefly
in mid- to outer-shelf depths. The shallowest
record in published accounts that we have seen
is 12 m, reported by Procter (1933) for speci-
mens collected on the coast of Maine. Deepest
record previously reported is 275 m, from the
Gulf of St. Lawrence (Tattersall, 1957). Depth
range for samples in the NMFS collection is 18
to 421 m (Table 1).

A large proportion (78'^ of the samples and
90^^^ of the specimens) were taken at midshelf
depths, 60 to 100 m. The sample from unusually

723

FISHERY BL'LLETIN: VOL. 69. NO. 4

Table 1. — Bathymetric distribution of Erythrops ery-
throphthalma, based on the NMFS collection.

Water depth

Samples

Specimens

m

Number

Number

0- 19

1

1

20- 39

1

2

40- 59

13

277

60- 79

73

1,676

80- 99

72

2,422

100-119

12

133

120-139

4

6

140-159

4

33

160-179

3

17

180-199

I

1

200-219

1

2

220-239

1

1

420-439

1

2

Total

187

4,573

deep water was collected at the head of Lydonia
Canyon, along the southwestern edge of Georges
Bank. This sample consisted of two specimens,
one adult female and an immature, collected in
a stramin-mesh ring net towed 1 to 2 m above
the sea bottom.

In summary, the available evidence from the
NMFS material suggests that only a small part
of the population spawns at one time and that
spawning takes place throughout a large part of
the year — possibly from spring through fall or
longer.

Sex Ratio

The NMFS collection contains 1,536 males and
1,692 females, a ratio of 0.91 male to 1 female.

Body Size

The eggs are nearly sj^herical and average
0.4 mm in diameter. Larvae of stage V are

1.2 mm long, and stage VII are 1.4 mm. Imma-
tures range in length from 3.0 to 6.1 mm. Ma-
ture specimens have an overall size range from

4.3 to 9.6 mm. Size range during various sea-
sons, separated by sexes, are:

Spawning

Seven ovigerous specimens fre present only
in the August samples, and 11 larvigerous spec-
imens are present in August and September
samples. This is an unusually small number of
specimens (about fr) in spawning condition
compared with the total number of adult fe-
males. Furthermore, the spawning females are
not especially large. Their average length is
6.4 mm, range .5.7 to 7.1 mm. Larger specimens
taken during the same month and at other sea-
sons are not in spawning condition. The i)re-
sence of immature specimens of about 4 to 5 mm
in length throughout the period from June
through December implies an e.xtended spawn-
ing season during the warmer part of the year,
plus the possibility of spawning during other
seasons as well. The absence of well-defined
length modes from month to month also supports
the hypothesis of a lengthy sjiawning period.

The number of eggs per clutch ranges from
1 to 6, and the number of larvae from 2 to 15.
The lower values apiiear to represent incom-
jjlete broods that resulted from losses incurred
during the catching and processing procedures.

Season

Males
6.4

Females

Mar. -Apr.

6.1

May -June

5.2-7.5

5.8-7.0

July -Aug.

5.1-8.3

5.0-9.0

Sept.-Oct.

4.8-9.6

4.3-8.7

Nov. -Dec.

5.1-8.9

5.0-8.9

A size comparison of mature males with ma-
ture females from the same samples discloses
that males are 0.3 to 0.4 mm larger than females.

The minimum size of adults is generally larger
in the early summer, decreases in late summer
and fall, then increases again in early winter.
This is due to an earlier maturation of immature
individuals dui'ing the period when water tem-
lieratures are comparatively high. The trend for
maximum size of adults is just the opposite.
Maximum length is smallest in early summer,
increases in the late summer and fall, and (the
males only) decreases again in early winter. It
is not clear whether this sequence in size dif-
ferences results solely from f;ister growth dur-
ing the warm season, or whether a summer
generation has reached the culmination of its
life span in September-October.

724

WIGLEY and BURNS: DISTRIBUTION AND BIOLOGY OF MYSIDS

Length of Life

An analysis of body length measurements did
not disclose trends in growth or separate length-
frequency modes that indicated year classes.
Immature specimens with an average length of
roughly 4.5 mm are present in June, August,
September, November, and December. The ma-
ture grouijs of both males and females in these
same months are mostly between 5 and 7 mm
long and do not exhibit the expected increases
in size as the seasons progress. Our tentative
conclusion is that E. enjfhrojihthalma has a
short life span, a rai)id growth rate, and a
lengthy spawning season.

Relation to Bottom Sediments

Members of this genus are considered to dwell
on or near the sea bottom, and our catch records
substantiate this view. It is uncommon in plank-
ton samples collected in the upper water layers,
but is regularly taken in hauls collected near
bottom. It occurred most frequently and in
greatest abundance on sand sediments (Table 2) .
Seventy-seven i^ercent of the samples and over
90% of the specimens were taken on, or over,
sand sediments. A moderate number of samjjles
(lO'^r ) were taken in areas of fine-grained sed-
iments. Furthermore, it should be added that
most of the sediments along southern Georges
Bank, where the majority of sami)les were taken,
contain modest amounts of silt, generally be-
tween 1 and 10'^. These quantities are insuffi-
cient to be incorporated in the bottom type ter-

Table 2. — Frequency of occurrence of Erythrops ery-
throphthalma in variou.s types of bottom sediments,
based on the NMFS collection.

Bottom type

Samples

Specimens

Number

Number

Rock-grovel

6

122

Grovel-sond

6

13

Glociol till

2

12

Sand

144

4,224

Sond-silt

12

iO

Silt-cloy

17

152

Total

187

4,573

minology (Shepard, 1954) . Although these are
small quantitities, the presence of silt on the
sediment surface makes it readily available to
the mysids. Furthermore, this species is com-
mon on the silty sediments in the region south
of Martha's Vineyard, Mass. Thus E. erythroph-
thalvia appears to inhabit sediments containing
a small to moderate amount of silt, in contrast
to N. amei-icaiia and M. bir/elmvi, which are
more common in sediments having a very low
silt content.

Meterythrops robusta S. L Smith, 1879

This rather large but uncommon species has
a wide distribution in boreal and subarctic wa-
ters. In the Atlantic region it has been reported
from the Kara Sea, Spitsbergen, Norway, Green-
land, Gulf of St. Lawrence, and in the Gulf of
Maine as far south as Cape Cod, Mass. In the
Pacific it occurs in the area between Alaska and
Washington. Moreover, assuming that M. mi-
crojihthalma is a synonym for M. robusta (.see
Banner. 1951), then its distrilnition also includes
the region off the east coasts of Japan and Korea
(Tattersall, 1951).

The NMFS collection contains nine specimens
from six stations, all from the ]ieriphery of the
Gulf of Maine (Figure (5; Burns and Wigley,
Table 7). Four siiecimens were collected at one
station in the channel north of Browns Bank;
three sjiecimens were from three stations north
of Gi-eat South Channel; and two specimens
were taken off eastern Mas.sachusetts.

Bathymetric distribution ranged from 64 to
150 m, and all specimens except one were from
depths between 110 and 150 m.

The type of bottom sediments inhabited by
this species is distinctive. The bottom sediments
contained gravel at five of the six stations where
M. rohni<tu occurred. Three of the samjiles were
taken on glacial till; one sample was from sandy
gravel; one sample was from gravel; and one
sample was from silt-clay. All other offshore
s])ecies of mysids in the NMFS collection are as-
sociated with sand or finer grained sediments.

All specimens of M. robusta in the NMFS
collection were caught in stramin nets or iiatu-

725

FISHERY BULLhTIN: \0L. 69, NO. 4

.<^

NEW
YORK

Meterythrops rofausta

Figure 6. — Geographic distribution of Meterythrops ro-
busta based on specimens in the collection at the NMFS
Biological Laboratory, Woods Hole.

ralists dredges towed alongf the sea bottom.
From this we infer that this species probably
inhabits the sea bottom or the water stratum
closely adjacent to bottom.

Body length of immature specimens ranged
from 6.6 to 7.5 mm, young males 8.5 to 12.0 mm,
and young females 8.6 to 9.3 mm. There were
no large specimens in the NMFS collection that
comi)are in size with the 28.5-mm adult male re-
ported by Smith (1879) from the Gulf of Maine.

The six adult specimens included four males
and two females, a ratio of two males to one
female.

No definite information pertaining to spawn-
ing is available from the material in our col-
lection. Both females are young and without
external eggs. The only evidence on this sub-
ject is the presence of immature and young sjie-
cimens in the August collections, which implies
a spring spawning season.

Hypererythrops caribbaea Tattersall, 1937

This species is distributed along the east coast
of North America from Maine to the Caribbean
Sea. It has been reported from the outer conti-
nental shelf and upper slope at depths between
214 to 402 m (Tattersall, 1951). Apparently it
is an uncommon species, since it has been re-
ported previously from only seven stations.
Body size is moderately small; lengths range
from about 8 to 13 mm.

The NMFS collection contains three specimens
from three locations (Figure 7; Burns and
Wigley, Table 8) , between the southern Gulf of
Maine and the continental shelf margin south
of Rhode Island. This southernmost sample is
from a depth of 179 m; the others are from 168
to 179 m. The .smallest specimen, 5.5 mm body
length, is immature; the other two, 9.5 to
11.0 mm, are adult females. The largest spec-
imen is larvigerous with an incomplete brood

.^

9

f

NEW
YORK

Hypererythrops caribbaea

Figure 7. — Geographic distribution of Hypererythrops
cariblinea based on specimens in the collection at the
NMFS Biological Laboratory, Woods Hole.

726

WIGLEY an,l BURNS: DISTRIBUTION AND BIOLOGY OF MYSIDS

of only two young in the brood pouch. Collec-
tion of this specimen in August indicates a sum-
mei- spawning season for this sjiecies. This
larvigerous specimen was found in the stomach
of a Gulf Stream flounder, Citharkhthys arctif-
rons Goode. Since H. caribbaea. is found in
warm-temperate waters, its occurrence in the
Gulf of Maine may be restricted to the deeper
basin areas where water temperatures are ameli-
orated by the intrusion of relatively warm, high-
salinity slope water.

Pseudomma affine G. O. Sars, 1870
The geographic distribution of this species
extends from the Bay of Biscay northward to
Norway, westward to Iceland, Greenland, and
North America. We found only two records of
its occurrence in North American waters. Tat-
tersall (1951) recorded one specimen taken by
the research vessel Fhh Hawk at station 999,
located 153 km south of Rhode Island (lat
39°45' N, long 71°30' W) at a depth of 487 m.
Klawe (1955) reported taking this species 2 km
off Campobello Island, New Brunswick, Canada.

.^

f

f

Pseudomma affine

Bathymetric range of all records from the North
Atlantic Ocean is 80 to 914 m.

Our collection contain;; 119 specimens from 22
samples (Figure 8; Burns and VVigley, Table 9) ,
all from the Gulf of Maine, except one from just
south of Georges Bank. They were collected at
moderate water depths: 146 to 329 m. Bottom
sediments at these collecting sites contain large
projiortions of fine particles, chiefly silts, clays,
and fine sands. Only two samples were taken
in areas having gravel or coarse sand bottom.

Body lengths range from 4.0 to 13.1 mm; the
majority are between 8 and 11 mm.

Evidence of an extended spawning season is
provided by the presence of ovigerous, larviger-
ous, and small juvenile specimens in the col-
lection. A 10.9-mm ovigerous specimen was
taken in December (Albatross III, cruise 70,
station 41) with 11 eggs and an average egg
diameter of 0.4 mm. One 11.0-mm larvigerous
specimen taken in August {Albatross IV, cruise
65-11. station 56) contains one larva 1.2 mm
long. Additionally, juveniles 5 mm or less in
length were taken in August, November, and
December. Spawning thus takes place during
summer and winter and may also occur in the
spring and fall.

Sex ratio of the specimens in the NMFS col-
lection is 2.3 males (68 specimens) to 1 female
(29 specimens).

Several morphological features in our speci-
mens differ slightly from published descriptions
of this species. In Table 3 are listed the number
of spines on the telson and relative length of the
antennal scale apex and relative width of the
antennal scale. Specimens in our collection have
fewer apical spines (nearly always 6) on the
telson, and a greater number of spines (9-24,
average 17) on the lateral margins of the telson,
than specimens from the eastern Atlantic. Also,
the antennal .scales on Gulf of Maine sjiecimens
have a proportionately longer apex (that portion
of the scale between the spine cleft and the an-
terior end) than eastern Atlantic specimens.
Spination of the telson and shape of the antennal

Figure 8. — Geographic distribution of Psendoinma af-
fine based on .specimens in the collection at the NMFS
Biological Laboratory, Woods Hole.

FISHERY Bl'LLETIN: VOL. 69, NO. 4

Table 3. — Number of spines on the telson and the pro-
portional measurements of the antennal scale for indi-
vidual male and female specimens of Pseudoynma affine
of various sizes.

Body
length

Spines

on telson

Antennal

scale

Apex

Lateral"

Relative
length of apex*

Relative
widtha

mm

Number

Number

%

%

Males

8.0

6

15

31

29

10.0

6

17

34

25

10.3

6

19

3«

27

13.0

8

24

37

29

Females

4.3

6

9

28

32

7.0

6

13

33

33

7.3

6

..

36

31

10.4

6

21

40

29

10.S

6

19

44

30

12.0

6

18

42

30

1 Total count of lateral spines from both sides of the telson.

2 Measurements expressed as percentages of the antennal scale length.

scale change as the specimens increase in size.
The number of lateral sjjines on the telson in-
creases with body length, particularly in males.
In both males and females the apex of the an-
tennal scale is proportionately longer in larger
specimens.

Sexual dimorphism is rather slight in the
characters listed in Table 3. Females have a
relatively larger antennal scale apex and a
slightly broader antennal scale than males.

The close affinity of P. affine with P. roseum
G. O. Sars necessitated considerable effort to
establish the identity of the specimens at hand.
In addition to the taxonomic characters men-
tioned above, sijecimens in our collection were
distinguished from P. i-oscum l)y: the relatively
broad telson and an ocular plate that has a broad,
gently rounded anterolateral "corner" with serra-
tions extending along a large portion of the later-
al margins. The practice of using morphological
characters that change with size or vary accord-
ing to sex or stage of maturity has led to confu-
sion between these species. Further taxonomic
studies of these two species are clearly in order.

Pseudomma sp.

Ten specimens of Pseudomma that do not cor-
respond morphologically to any known species

are represented from three localities off southern
New England. A description of this species and
notes on its ecology is being prepared and will
be reported elsewhere.

Amhlyops abbreviata (M. Sars 1869)

This widely distributed boreal mysid occui-s
in both the North Atlantic and North Pacific
Oceans. In the Pacific it has been found off
Japan and off the west coast of North America
from Washington to Alaska. In the Atlantic it
ranges from the Bay of Biscay north to Scandi-
navia, west to Greenland and North America.
Previous records from the northeastern coast
of the United States consist of 38 specimens
from 7 offshore stations situated between Cape
Cod, Mass., and northern New Jersey. These
specimens were collected by the U.S. Fish Com-
mission between 1879 and 1881 at water depths
between 238 and 838 m.

Our collection contains 34 specimens from 8
samples taken in the Gulf of Maine, primarily
in the southern part of the Gulf (Figure 9;
Burns and Wigley, Table 10). Water depths
at these localities range from 183 to 329 m. The
bottom sediments where these specimens were
taken are composed predominantly of silts, clays,
and fine sands; one excei)tion is a sandy gravel
bottom off the eastern end of Georges Bank
where one juvenile specimen was obtained. Body
length ranged from 4.7 to 15.0 mm. The size
of adults is 10 to 15 mm; the males tend to be
slightly larger (average length 12.9 mm) than
females (average length 12.3 mm).

Spawning occurs during winter and possibly
in other seasons as well. One ovigerous female
collected in December (Albatross III. cruise 70,
station 25) had 29 eggs in the marsupium, each
0.4 mm in diameter. The presence of juvenile
specimens 4 to 6 mm in length in August and
an 8-mm specimen in December suggests that
spawning also takes place in summer and fall.

Sex ratio of the specimens in the NMFS col-
lection is 0.65 male (11 specimens) to 1 female
(17 specimens).

728

ttlGLEY and BLRNS : DISTRIBUTION AND BIOLOGY OF MYSIDS

0 XM .00

^ ,

fj' ' ^'P NOVA
-' '11 SCOTIA .

.^

^

/

/

•

•

PORTLAND^ \

fx

\
1
1
1 ,

9

^. \

? ^

*S. '~^->

/ /
/ /

y /
/ /

/ J

BOSTON

ly -u

v^

I \

.T

/ /
/ /
/ /

'■ /^

>'

if

f

NEW U^^
YORK^*^

I J

Ambtyops abbreviata

\

\

Figure 9. — Geographic distribution of Amblyops abbre-
viata based on specimens in the collection at the NMFS
Biological Laboratory, Woods Hole.

between Hudson Canyon and Hydrographer
Canyon — in the same area where they were
found to be most common by the Fis:h Hawk
and Albatross (Figure 10; Burns and Wigley,
Table 11) . The depth range of their occurrence
is 220 to 366 m. Because two samples were col-
lected with the bottom skimmer, it is certain
these specimens were present on the sea bottom
at the time of capture. Their presence on the
bottom during hours of low light level, 1600 to
2200 hr, suggests they may not undertake a
diurnal vertical migration. Five specimens are
adults, 13.0 to 16.2 mm long, and thi-ee specimens
are immature, 4.0 to 6.0 mm long. We have no
information on spawning other than the pre-
sence of 4- to 6-mm specimens in June, from
which a spring spawning may be inferred. Bot-
tom sediments at the collecting sites are fine-
grained types: sand, silt, and silt-clay.

Tribe LEPTOMYSINI
Bathymysis renoctilata Tattersall,

1951

This large-eyed species of Bathymysis, which
occurs only in the western Atlantic Ocean, has
been reported from southern New England to
the southern tip of Florida (Tattersall, 1951).
The principal area of occurrence is along the
outer continental shelf and upper slope between
Hudson Canyon and Hydrographer Canyon
(southeast of Nantucket, Mass.). The bathy-
metric range reported for this species is 220 to
483 m. These records are based on collections
made b.v the research vessels Fish Hawk and
Albatross during the latter part of the last
century.

The NMFS collection contains eight specimens
from three stations off southern New Eng-land

Figure 10. — Geographic distribution of Bathymysis re-
nocalata based on specimens in the collection at the
NMFS Biological Laboratory, Woods Hole.

>^

9

Bathymysis renoculata

729

FISHERY BULLETIN: VOL. 69, NO. 4

Mysidopsis higelowi Tattersall, 1926
Geographic Distribution

M. higelowi is a small American species that
occurs along the Atlantic and Gulf coasts of
eastern and southern United States from New
England to Louisiana.

The NMFS collection contains 2,031 specimens
out of 54 samples (Figure 11; Burns and Wig-
ley, Table 12) collected from northeastern
Georges Bank southward along the coast to the
vicinity of Jacksonville, Fla. Georges Bank is
the principal area represented in the sampling;
the results extend the known range of this spe-
cies a considerable distance to the northeast.
Only five samples were from localities south of
the Nantucket Shoals region: these were taken
off New Jersey, Virginia, North Carolina, and
northern Florida.

It is interesting to note this species is not
listed as present in the plankton samples col-
lected from Georges Bank between 1939 and
1941 (Whiteley, 1948). Although the absence
could have been due to annual fluctuations in
abundance in this northern sector of its range,
our results show the species was present each
year we conducted moderate or heavy sampling:
in 1955 through 1958, and in 1964 through 1967.
More likely the absence in the 1939-41 samples
resulted not from temporary fluctuations but be-
cause these earlier collections were primarily
from middle and upper water levels, whereas
most of the NMFS collections were taken on or
near the sea bottom.

Bathymetric Distribution

M. higelowi is a shallow-shelf species that has
been reported from inshore localities such as the
inlet to Indian River Bay, Del., and Calcasieu
Pass, La., and from offshore waters as deep as

Figure 11. — Geographic distribution of My-
sidopsis higelowi based on specimens in the
collection at the NMFS Biological Labora-
tory, Woods Hole.

S

JACKSONVIILEO

730

WIGLEV and BURNS ; DISTRIBUTION AND BIOLOGY OF MYSIDS

77 m (Tattersall, 1951; Grice and Harf; Hop-
kins, 1965).

Depth range of the NMFS samples is from
13 to 179 m. By far the largest number of
samples (73rf ), greatest number of specimens
(91 "^r ), and highest densities occur between 30
and 80 m (Table 4). One collection taken at
an unusually deep locality, 179 m, is from the
northern edge of Georges Bank. The water
circulation in this area and its proximity to
shallow waters commonly inhabited by this spe-
cies may account for its presence at that rela-
tively great depth.

Table 4. — Bathymetric distribution of Mysidopsis bigel-
owi, based on the NMFS collection.

Water depth

Somples

Specimens

10- 19
20- 29
30- 39
40- 49
SO- 59
60- 69
70- 79
80- 89
90- 99
100-109
170-179

Number
4
3
9
8
9
7
6
4
2
I
1

Number

28

10

557

493

640

73

85

22

116

1

6

Total

54

2,031

Spawning

This species spawns from April to November
in the coastal areas of Delaware (Hopkins,
1965) . There is no information about spawning
habits of the offshore and northern populations,
and we did not find a single ovigerous or lar-
vigerous specimen in the NMFS collection. We
do, however, have immature specimens repre-
sented in samples collected in May, August, Sep-
tember, November, and December. This is in-
dicative of a long spawning season, probably
from early summer through fall.

The large size of immatures, 4.0 to 5.0 mm,
in May samples is believed to represent the over-
wintering young. The absence of ovigerous fe-

^ Grice, George D., and Arch D. Hart. 1962. The
abundance, seasonal occurrence and distribution of the
epizooplankton between New York and Bermuda. Ap-
pendix to Ref. 62-4, Woods Hole Oceanogr. Inst. (Un-
published manuscript.)

males in the many large samples collected in
December is evidence that spawning most likely
has terminated by that time of year.

Sex Ratio

The NMFS collection contains 313 males and
195 females, a ratio of 1.6 males to 1 female.

Body Size

This species is the smallest mysid in the
NMFS collection. A summary of body length
data by month of capture for males, females,
and immatures is given in Table 5. Range in
body length among all specimens in the col-
lection is 2.4 to 6.6 mm. The average length
of immatures is 3.8 mm, males 4.9 mm, and fe-
males 5.1 mm. Members of this species were
found to mature at 3.5 mm, smaller than any
other species in the NMFS collection.

Table 5. — Means and ranges of body length of Mysi-
dopsis bigeloici by months and se.xes.

Body length

Month

Immatures

Males

Females

Mean

Range

Mean Range

Mean Range

mm

mm

mm

mm

mm

mm

May

4.6

4 0-5 0

5 1

4.9-5.7

5.5

5.4-5.7

Aug.

4.0

^.

4.9

4.2-6.6

4.5

3.8-5.8

Sept.

3.0

4.6

5.0

Nov.

3.8

2 4-4.1

5.2

4.6-5.7

5.1

4.0-6.3

Dec.

3.5

2.4-4.5

4.8

3.5-5.8

4.5

3.5-5.6

Length of Life

Our samples are inadequate to give an accu-
rate estimate of the length of the life cycle. The
few available clues, such as the presumably long
spawning season and the large size of the over-
wintering immatures, are suggestive of a life
cycle similar to Neomysis americnna: a short-
lived summer generation and a long-lived winter
generation.

Relation to Bottom Sediments

Many specimens in the NMFS collection were
taken with bottom samplers (Smith-Mclntyre,
Van Veen, and Campbell grabs) or gear that

731

FISHERY' BULLETIN; VOL. 69, NO. 4

sampled water layers adjacent to the sea bed
(sled net). These results suggest M. bigeloivi
lives in or on the bottom sediments during much
of its life.

An analysis of the types of bottom sediments
at the collecting sites reveals a high incidence
of this mysid on various grades of sand (Table
6), usually sand containing little or no silt or
clay. They tend to avoid fine-grained sediments
as further evidenced by their absence in several
hundred samples taken from a 1,000 square km
area of predominantly silt and sandy-silt sedi-
ments south of Martha's Vineyard, Mass., on
research vessel Delaircrre cruise 62-7.

Table 6. — Frequency of occurrence of Mysidopsis bigel-
owi in various t>-pes of bottom sediments, based on the
NMFS collection.

Bottom type

Samples

Specimens

Number

Ntimher

Rock-gravel

4

177

Gravel-sond

1

1

Shell-sond

1

1

Sond

44

1,847

Sand-silt

1

1

Unclassified

3

4

Total

54

2,031

Relation to Water Temperature

M. bigeloivi inhabits water temperatures from
about 2° C in the northern part of its range to
summer water temperatures of about 30° C in
the Florida and Louisiana areas. The annual
change in temperature is slightly less than 20° C
in the north and slightly more than 20° C in the
south.

Mysidopsis ftirca Bowman, 1957

This species was de.scribed by Bowman (1957)
from a sample containing 23 specimens collected
in 1953 by the research vessel Theodore N. Gill.
The specimens were obtained at one station
(number 57) located 40 km from shore off the
northern coa.st of South Carolina. Depth of
water at the collecting site is 22 m. It was later
reported by Brattegard (19(59) from off south-
eastern Florida at depths of 1 to 48 m.

The NMFS collection contains one specimen,
a female 4.2 mm long, taken with the Campbell

FiGiRE 12. — Geographic distribution of Mysidopsis furca
based on a specimen in the collection at the NMFS Bio-
logical Laboratory, Woods Hole.

grab 50 km east of Georgetown, S.C, (Figure
12; Burns and Wigley, Table 13) about 50 km
southwest of the type locality. The specimen
was taken at a depth of 22 m on sediment com-
posed of fine sand. This small species has a
reported size range of 4.6 to 6.1 mm (Bowman,
1957). Neither the size nor the develojimental
stage of the NMFS specimen provides any indi-
cation of sjiawning season or size at maturity.

Promysis atlantica Tattersall, 1923

This rare species was described from an im-
mature female specimen collected off Rio de Ja-
neiro, Brazil, in 1910 (Tattersall. 1923). It
was not reported again until Clarke (1956) de-
scribed the male and adult female, and gave
new records of occurrence for specimens col-

732

WIGLEY and BURNS: DISTRIBUTION AND BIOLOGY OF MYSIDS

lected off the coasts of Louisiana, South Caro-
lina, and North Carolina.

The NMFS collection contains three specimens
from three stations located off the southeastern
coast of the United States (Figure 13; Burns
and Wig-ley, Table 14). Their geographic dis-
tribution is from just north of Cape Hatteras,

N.C., to Fort Pierce, Fla. Size range is 4.5 to
5.0 mm; all are females. They were taken in
shallow water, 8 to 26 m, on sandy sediments.
Little is known about the biology of this species,
and the few specimens in the NMFS collection
provide no additional information on spawning
or length of life.

^-^<^

N\

^

"^ NORFOLK^;

c3

> ^8

^- /

/ \
/ \
1 \

/

/
/

/

■§>

CHARlESTONdt

1
1

\
/

\ f

0 KM lOO [((

^

%

\
\
\
\
\
\
\
\

\

JACKSONVIllEO \

'~ T. S

MIAMlttiv^

Promysis atlantica

"■■^^

■■ 1

^

Figure 13. — Geographic distribution of Promysis atlant-
ica based on specimens in the collection at the NMFS
Biological Laboratory, Woods Hole.

Tribe MYSINI
Mysis mixta Lilljeborg, 1852

This boreal mysid occurs in the Eastern At-
lantic region from the White Sea, Spitsbergen,
Scandinavia and southward to the Baltic Sea,
and westward to Iceland. In the Western At-
lantic region it has been reported from Green-
land, eastern Canada, and the eastern coast of
the United States as far south as Cape Cod,
Mass. In the Gulf of Maine it has been most
frequently reported from off the eastern coast
of Massachusetts and from a few localities off
the Maine coast (Smith, 1879; Rathbun, 1905;
Tattersall, 1951; and others).

This species is represented by 382 specimens
from 45 samples in the NMFS collection (Fig-
ure 14; Burns and Wigley, Table 15). The ma-
jority of specimens, including all adults, were
taken in the western part of the Gulf of Maine
between Cape Cod, Mass., and the central Maine
coast. The first records of this species from
south of Cape Cod were collected in the region
off Rhode Island and southeastern Long Island,
N.Y. The location of the southernmost sample
is lat 40°36' N and long 71°33' W, approximately
55 km southeast of Montauk Point, N.Y. All 26
specimens from these six southern samples are
immatures 10.5 to 20.1 mm in length ; they were
collected in June and September.

Water depths at all NMFS collecting sites
range from 29 to 159 m. Bottom sediments at
these localities consist of a variety of types
ranging from fine-textured clays to gravel. Most
of the samples, however, come from intermediate
types of sediment: silt-clay ( 38 '^ f ), glacial till
(27'"r), and sand (22%). Only a small per-
centage of samples represent other bottom
types: silt-sand (7/^), gravel (4Cr), and clay
(1%).

733

FISHERY BULLETIN: VOL. 69. NO. 4

C^

NEW
YORK

Hysis mixta

Body Size

Body lengths range from 5.0 to 25.0 mm. Im-
mature specimens are a common comi^onent,
accounting for 69'' r of all specimens caught.
Many of these immature specimens are large
(15 to 20 mm). Also noteworthy is that many
large males and females do not possess fully
developed secondary sex characteristics. A
summary of body length measurements by
months and stage of development is listed in
Table 7.

Table 7. — Means and ranges of body length of Mysis
mixta by months and stages of development.

Body

length

Month

Immotures

Adults

Mean Range

Mean

Range

mm

mm

mm

mm

May

6.9

5.0- 8.5

20.6

19.0-21.3

Jun.

10.5

Aug.

13.6

10.3-20.0

22 0

20.0-24.2

Sept.

18.8

17.2-20.1

__

Oct.

16.7

14.0-20.0

23.4

22.0-25.0

Figure 14. — Geographic distribution of Mysis mixta
based on specimens in the collection at the NMFS Bio-
logical Laboratory, Woods Hole.

The occurrence of specimens at the surface
(Albatross IV, cruise 66-14, station 24) and in
several samples between middepths and surface
(Albatross IV, cruise 66-14, stations 35, 36, 39,
and 40), as well as those taken on the sea bot-
tom, indicates a diurnal vertical migration. Spec-
imens at the surface were collected at 0300 hr
and midwater samples were taken between 2100
and 0900 hr. This imijlies inhabitance of upper
waters during hours of darkness and a bottom
habitat in the daytime.

Sex Ratio

The NMFS collection contains 119 females
but only 2 males, which is a ratio of 0.017 male
to 1 female. Whether males occur in a habitat
different from females, or are actually so much
less abundant than females, is unknown. This
is the only species in the collection having such
a grossly unbalanced sex ratio.

Length of Life and Spawning

Although Smith (1879) suggested this spe-
cies might be an annual that spawns during the
winter, our analysis of the maturity status and
size frequency data of the NMFS specimens
leads us to believe that M. mixta has a 2-year
life span and spawns in winter or early spring.

Our material is scanty for purposes of deter-
mining length of life, but the data do indicate
a clear trend in growth and development (Table
7). The specimens reveal two definite age
groups in both spring and fall. In May the im-
matures average 6.9 mm and the adults 20.6 mm.
In Octol)er the immatures average 16.7 mm and
the adults 23.4 mm. Juveniles increase in length
at a rate of about 2 mm per month until winter
when the growth rate slows apjireciably. They
mature and spawn in the winter or early spring.

None of the NMFS specimens are ovigerous.
The only indication of spawning season is the
presence of small (5.3 to 6.3 mm) specimens in
Ma.v, which suggests a late winter or early
spring spawning.

734

WIGLRV and BURNS: DISTRIBUTION AND BIOLOGV OF MVSIDS

Myst's stenolepis S. I. Smith, 1873

This large American mysid is distributed in
coastal waters of northeastern North America
from the Gulf of St. Lawrence to New Jersey.
Though very common to this regfion it is rep-
resented by only a few specimens in the NMFS
collection because biological samples were rarely
collected in the intertidal and shallow subtidal
zones.

The NMFS collection contains 13 specimens
from six samples (Figure 15; Burns and Wigley,
Table 16) . all from a rather small area off east-
ern Massachusetts and eastern Rhode Island.
The specimens were collected with a dip net
along shore in water dejiths of about 1 m. Four
samples were taken in beds of Zostem or algae,
and one sample was from a sandy tjottom (bot-
tom type for the other sample is unknown).

M. stevolepis is one of the largest shallowwater
species in the NMFS collection. Body lengths

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Mysjs

stenolep

s

of these specimens range from 13.0 to 2(5.0 mm,
and average 20.4 mm.

According to Smith (1879) the life span of
this species is one year. Their life cycle is as
follows: (1) adults spawn in winter and early
spring, (2) the young ap]iear in late sjiring and
summer, and (3) they mnture in the fall and
winter. Material in the NMFS collection sub-
stantiates this life-cycle plan. Body lengths of
specimens, by months, are:

Month

Average body

Stage of

collected

length (mm)

maturity

September

14.2

Immature

October

20.0

Mature

November

24.2

Mature

February

25.3

Mature

]\Iarch

25.0

Mature

April

26.0

Mature

Figure 15. — Geographic distribution of Mysis steiiolriiis
based on specimens in the collection at the NMFS Bio-
logical Laboratory, Woods Hole.

Three larvigerous specimens collected in Feb-
ruary and March range in size from 25.0 to
25.5 mm.

Fecundity of this species is very high com-
pared with other east coast mysids. An oviger-
ous-larvigerous specimen 25.0 mm long, collected
in late February, held 94 eggs and 50 stage III
larvae in the brood pouch. Average diameter of
the eggs is 0.4 mm and average length of the
larvae is 1.4 mm. A 25.5-mm long larvigerous
female from the same sample was carrying 188
stage IV larvae; their average length is 1.4 mm.
A 25.0-mm larvigerous female collected in March
was carrying 171 stage VII larvae; their aver-
age length is 1.86 mm.

A rather high water temperature was noted
when the September 4, 1961, sample of M. ste-
nolopis was collected. The temperature was
23.9° C at a depth of 1 m in an eelgrass bed in
Waquoit Bay, Falmouth, Mass. This is the
highest temperature recorded for the NMFS
samples of this species.

Prautius flexuosus (O. F. Miiller, 1776)

This species is very common in shallow coastal
waters of Great Britain and along the northern
coast of France, Holland, and southern Scandi-
navia (Tattersall and Tattersall, 1951). In 1960
it was discovered in the harbor at Barnstable,

735

FISHERY BULLETIN: VOL. 69. NO. 4

Mass., (Wigley, 1963) the first report of its
occurrence outside the north European area.
It has also been collected in large numbers from
the coast of New Hampshire by Dr. William F.
Black (personal communication), and from the
Penobscot River (Maine) estuary by Haefner
(1969).

The NMFS collection contains 15 specimens
from five samples (Figure 16; Burns and Wig-
ley, Table 17), including four specimens from
the original seven taken at Barnstable in 1960.

0 KM 100 i^ :"

'•? NOVA \ \ ^^'•;

|I SCOIIA J ;'|^^ \^j

/ .^

\ ^ '*":'

\-^ ^ j

PORTLAND^ ' ^

) \

1 1

f

^. Ta '^--.^^

\ ' 1
\ 1 }

1 ^ 1
1 ^ /

BOSTONO-'~~~J^|rA

/ \

#

' f// ,

T

NEWVy/ (
YORKOP^ \

j Praunus

flexuosus

Figure 16. — Geographic distribution of Praunus flexu-
ostis based on specimens at the NMFS Biological Lab-
oratory, Woods Hole.

[The other three specimens from this collection
were sent to Dr. Olive S. Tattersall, who very
kindly examined them and verified the identi-
fication (Burns and Wigley, Table 17; footnote
2).] The other samples are also from coastal
areas north of Cape Cod, Mass. These were
collected along shore at Manomet, Mass.; in the
harbor at Nahant, Mass. (by Dr. Nathan W.
Riser); at Rye Harbor, N.H. (by Mr. John A.

Lindsay) ; and from a tide pool on Appledore
Island, Isle of Shoals, N.H. (by Mr. Stephen
Tonjes).

This is a shallowwater species commonly
found in tide pools and associated with algae or
Znstera. All samples in the NMFS collection
are from nearshore localities at depths of 5 m
or less. The majority of samples were collected
by means of a dip net.

Size range of all NMFS specimens is 15.0 to
28.0 mm; males are 15.5 to 19.0 mm and females
16.5 to 28.0 mm. Only three immature speci-
mens, ranging in length from 15.0 to 16.5 mm,
are represented in the collection. Sex ratio of
the 12 adult specimens is one male to one female.

The spawning season for this species in New
England waters, based on the one ovigerous and
two larvigerous females in the collection, is at
least April through November. It may, how-
ever, spawn in this region throughout the year,
as it does in Europe. The 25.0-mm female from
Barnstable. Mass., held 44 eggs in the brood
pouch. The 21.0-mm female from Isle of Shoals,
N.H., held 39 stage V larvae in the brood pouch.
Although the larvigerous female in the Rye
Harbor sample contained 19 larvae, the ooste-
gites were separated and it appeared to be an
incomplete clutch.

W^hen this species was discovered in North
America in 1960, the question arose whether it
was a recent immigrant from Europe, or wheth-
er it had inhabited this region for hundreds of
years but had been overlooked. After the first
capture of only seven specimens most considered
it a rare species with only a local distribution in
New England. Additional information obtained
since 1960, however, indicates it is rather widely
distributed between Maine and Cape Cod, Mass.,
and that it is abundant in the Maine-New Hamp-
shii'e region. In view of this, and considering
the intensive collecting in shallow coastal waters
of New England by A. E. Verrill, S. I. Smith,
W. Stimpson, and numerous other scientists dur-
ing the latter half of the nineteenth century,
it is our con.iecture that P. flexnotiu-a is a com-
paratively new addition to the New England
fauna. Possibly it was transported from Eurojie
to a New England port, such as Boston or Ports-
mouth. N.H., among fouling organisms on the

736

UIGLIlV ai,d BURNS: DISTRIBLTION AND BIOLOGY OF MYSIDS

bottoms of ships durins' World War II when
convoys of merchant sliips were making fre-
quent and rather regular transoceanic voyages.

Neomysis americana (S. I. Smith, 1873)
Geographic Distribution

N. americana is the most common mysid in-
habiting the northeastern coastal waters of the
United States and undoubtedly the most abun-
dant mysid in the western North Atlantic Ocean.
It is strictly a North American species, having
been reported only from the Gulf of St. Law-
rence south to Virginia. It is much more abun-
dant and widely distributed between Virginia
and New England than in the northern part of
its range.

The NMFS collection originally contained
over 2 million specimens of this species — more
numerous than any other mysid in the collection,
but for purposes of analysis the larger lots were
subsampled. Subsamples totaling 8,451 spec-
imens from 168 samples (Figure 17; Burns
and Wigiey, Table 18) were examined. The
geographic distribution of specimens in this col-
lection ranges from off Nova Scotia, near the
mouth of the Bay of Fundy, south to Chesapeake
Bay.

Most of the specimens are from two regions
(Figure 17): (1) eastern Georges Bank to
Rhode Island, and (2) from northern New Jer-
sey to Chesapeake Bay. The gap in distribution
between these two areas (off Long Island) ap-
pears to be more pronounced in offshore waters
than inshore. Bigelow and Sears (1939) also
encountered a Ijroad hiatus in the occurrence of
this species in the offshore waters of eastern
Long Island. Yet, inshore in the New York re-
gion it has been reported from Great South Bay,
Long Island (Smith, 1879) and from Long Is-
land Sound (Verrill, Smith, and Harger, 1873;
Smith, 1879; and Richards and Riley, 1967).
The only record from offshore Long Island
known to us is that rejiorted by Grice and Hart
(see footnote 3) which indicated the presence
of this s])ecies in two plankton samples taken
at station 13 located at lat 40°44' N and long
71°41' W (water depth, 64 m). The above rec-

0 "M 100 Pi -^

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]|1 SCOTIA J j ^^^ \^j

y '^

p

4fk

PORTLAND^ \ ^

BOSTONO-^"X^

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americana

^' NORFOIK^

^

FiGUEE 17. — (ieographic distribution of Ncnmyxis amer-
icnna haseA on specimens in the collertion at the NMFS
Biological Laboratory, Woods Hole.

ords indicate merely a restricted occurrence or
low aljundance in the offshore New York region,
not a complete break in distribution.

Samples from the Georges Bank area during
summer and winter revealed a similar distrilni-
tion of N. americana in both seasons. The spe-
cies was pre.sent over most of the bank, with
highest concentrations in the central part, the
same area where Whiteley (1948) also found
them to be most abundant.

737

FISHERY BULLETIN: VOL. 69. NO. 4

Bathymetric Distribution

A'', americana is a shallowwater species most
commonly reported from the intertidal zone to
depths of 60 m. However, it appears to inhabit
somewhat deeper water in the Georges Bank
region as indicated by the records of occurrence
in Figure 17. Whiteley (1948) reported it from
a number of plankton samples taken at stations
where the water depth was 75 m, but at very few
localities where depths were greater than 100 m.
Greatest depth reported for this species is 214 m
(Wigley, 1964).

Depth range for the samples in the NMFS
collection is 1 to 232 m. Fretiuency distribution
for these samples is listed in Table 8. This spe-
cies is common from the intertidal zone out to
90 m but is most abundant at dejjths between
30 and 60 m.

Table 8. — Bathymetric distribution of Neomysis ameri-
cana, based on tlie NMFS collection.

Water depth

Samples

Specimens

m

jWmber

Number

0- 9

S

147

10- 19

14

139

20- 29

20

361

30-39

19

3.289

40- 49

38

1,998

50- 59

32

1,619

60- 69

13

299

70- 79

12

308

80- 89

4

220

90. 99

2

2

100-109

3

6

150-159

1

3

230-239

1

'

Unclassified

4

59

Total

168

8,451

A^. amerkanu undertakes I'egular vertical mi-
grations between the sea bottom and the upper
water layers. Light intensity is the primary
controlling element to which the mysids are re-
sponding. The.v move to deeper, darker regions
during daytime and upward toward the surface
at night (Ilurlbut, 1957; Herman, 1963). The
NMFS samples jirovide veiy little information
on this asjiect other tiian to substantiate i)robable
vertical migration in shallow water. At depths
of less than 50 m on Georges Bank this si)ecies
is more common in bottom samples collected dur-
ing the davtime than at night.

Spawning

Though spawning of coastal populations of .V.
americana takes place throughout the year, it is
much more intensive during the warmer months
of April through October (Smith, 1879; Fish,
1925; Cowles. 1930; Herman, 1963; Hopkins,
1965). The Georges Bank population was re-
ported by Whiteley (1948) to spawn in the
spring. S])ecimeiis in the NMFS collection indi-
cate spawning of Georges Bank stocks from
March through October and possible spawning in
all months of the year. There appear to be two
major spawning jieriods, one in the sirring
(March through June) and another in the late
summer and fall (August through October).
Of the ovigerous or largiverous specimens pi-e-
pent in samples collected every month from
March to October the largest numbers occurred
in March through June and August through
October. Immature specimens were particularly
numerous in August and December. The small
number of immature specimens collected in late
winter and early spring may indicate occasional
small-scale spawning in winter.

Two distinct size groups (summer generation
and overwintering generation) of s]iawning fe-
males are discernable; one grouji spawns in the
spring, the other in the fall (Figure 18) . Spring
spawnei's have an average length of 11 to 12 mm,
and ]iroduce a clutch containing about 26 eggs.
Fall spawners have an average length of 6 to
8 mm, and their clutch contains only about six
eggs. Additional information about these two
generations is given below.

Eggs are spherical, 0.38 to 0.42 mm in dia-
meter, in both the summer and overwintering
generations.

Size of the larvae varies according to their
stage of development. Average lengths in milli-
meters for the following stages are: stages I and
H— 0.39, stage HI— 0.55, stage IV— 0.85, stage
V— 0.96, stage VI— 1.15, and stage VII— 1.34.

Sex Ratio

The NI\IFS collection contains 1,574 males
and 1,669 females; the ratio is 0.94 male to 1
female.

738

WIGLEY ana BLRNS: DISTRIBUTION AND BIOLOGV OF MYSIDS

'^ (MMATUflEj' -FmMATURE

_j I I i_

JAN MAR. MAY JULY SEPT. NOV, JAN. MAR MAY JULY SEPT

MONTHS

Figure 18. — Schematic diagram of the age-size-maturity
composition of Neoriiysis americatia populations from off-
shore New England.

Length of Life

The Georges Bank population of .V. (uneticdna
appears to consist of two generations: (1) a
short-lived summer generation and (2) a long-
lived overwintering generation (Table 9, Figure
18). The summer generation stems from eggs
that hatch in late winter to late spring. They
grow rajsidly and mature in late summer and
autumn. Length of life of this generation is

Table 9. — Range in body length of the (1) summer and
(2) overwintering generations of Neomysis americana,
by sexes and periods.

Ronge in length

Male

All
specimens

Ovigerous

ond
lorvigerous

mm

mm

mm

mm

Summer generation

May -June

3.0- 6.8

5 9- 7.4

6.0- 7.4

_..

July -Aug.

5,0-(9.C)

5.1-19.0)

60- 8.9

Sept. -Oct.

—

5,7-10.0

6.0- 9.6

6.6- 8.3

Overwintering

generation

Sept.-Ocf

3.0- 7.0

._

Nov. -Dec.

3.1- 7.4

5.5- 9.6

5.6- 9.6

_.

Jon. -Feb-

8.3-105

10.6-12.9

11.5-14.7

__

Mor. -Apr.

6.0-10.9

9.3-12.1

9.3-13.3

10.7-12.4

May -June

9.5-14.0

9.5-14.0

11,4-14.0

July -Aug.

—

ca.(9)-13.0

ca.(9)-(14,0)

—

estimated to be 6 to 10 months. They are the
]irogeny of the overwintering group, the dom-
inant groui^ in the offshore New England area.
The overwintering generation originates from
eggs that hatch during the summer and autumn,
and perhaiJS even from late spring eggs. They
grow at nearly the same rate as the summer
generation but do not reach maturity until the
following spring. Thus, they are substantially
larger than the summer generation. Adults of
the overwintering generation are 10 to 15 mm
long, compared with 6 to 10 mm lengths for the
summer generation adults. Estimated length of
life of this overwintering group is 10 to 14
months.

Relation to Bottom Sediments

Although A', americana make daily excursions
from the sea bottom to upper water levels
(see BathiiTnetric Distribution), a substantial
amount of their time is spent on bottom, and
they appear to be selective in the type of bottom
they inhabit. The bottom type with which they
are most commonly associated is sand (Table
10). Kinds of sands they inhabit, in decreasing
order of importance are: fine, medium, and
coarse. One explanation for the scarcity of N.

Table 10. — Frequency of occurrence of Neomysis ameri-
cana in various types of bottom sediments, based on the
NMFS collection.

Bottom type

Somples

Specimens

Rock-gravel

Gravel-sand

Glacial till

Shell-sand

Sond

Sill-sand

Silt-clay

Unclassified

Totol

Number
5
10
0
4
131
7
7

Number

262

37

0

51

7,987

30

25

59

8,451

' Immotures less than 3 to 4 mm length usually passed through the
meshes of the sampling and processing equipment.

americana in the middle and outer shelf areas
south of Rhode Island and New York may be
unsuitable sediments. The bottom over much
of this area is Ijlanketed with silty sands and
sandy silt, whereas on Georges Bank and much

739

FISHERY BULLETIN: VOL. 69, NO. 4

of the nearshore coastal areas where N. ameri-
cana is common, the bottom types are predomi-
nantly sands with low silt content (Wigley,
1961; Uchupi, 1963).

Relation to Water Temperature

This mysid is eurythermic and the extremes
of temperature in shallow New England waters
(0° to over 20° C), in shallow portions of
Georges Bank (2°-18° C), and in the vicinity of
the Chesapeake Bay (over 25° C) , do not appear
to inhibit survival of this species. Reproduc-
tion and other life processes, however, are af-
fected by temperature. Also, the sequence, tim-
ing, or duration of temperature regimes may be
important. For example, in the offshore region
south of Rhode Island and Long Island, N.Y.,
where there is a low abundance of this species,
the presence of a layer of cold bottom water (the
so-called "cold bubble") may have a pronounced
influence in repelling immigi-ants or retarding
reproduction.

Tribe HETEROMYSINI

Heteromysis formosa S. I. Smith, 1873

H. formosa is an amphi-Atlantic species that
has been reported in the eastern Atlantic from
the northern coast of France, British Isles, and
Norway. In the western Atlantic it is known
to occur along the eastern and southern coasts
of the United States from Maine to the Gulf of
Mexico. All except three of the western At-
lantic records are from the northeastern sector,
between Maine and New Jersey. The three
southern records are all from relatively deep-
water (48 to 227 m) localities. Specimens from
48 m were collected by Brattegard (1969) off
Fort Pierce, Fla. The other two records,
reported by Tattersall (19.51), are based on col-
lections of the research vessel Albatross at a
depth of 227 m off the coast of North Carolina
(lat 34°38' N, long 75°34' W) and in eastern
Gulf of Mexico (lat 28°36' N, long 85°.34' W)
at a depth of 203 m. (One additional deepwater
sample was collected in the northern region by
the research vessel Fish Hairlc at station 917,
located south of Martha's Vineyard. Mass., at lat
40°22' N. long 70°42' \V at a depth of 81 m.)

The NMFS collection contains 72 specimens
from 15 samples (Figure 19; Burns and Wigley,
Table 19) . The geographic distribution of these

.^

NEW
YORK

Heteromysis formosa

FiGl'RE 19. — Geographic distribution of Heteromysis
farmusa based on specimens in the collection at the
NMFS Biological Laboratory, Woods Hole.

samples extends from southwestern Georges
Bank (1 sample) and southern Massachusetts
(12 samples) to northern New Jersey (2
samples).

Although the bathymetric range for the
NMFS samples is 2 to 84 m, only one .sample
containing a single sjjecimen was taken at 84 m.
All others were collected at depths of 26 m or
less. This species customarily inhabits the shal-
low (1-20 m) inshore areas, such as harbors,
bays, and estuaries, where it is much more com-
mon than on the outer i)ortion of the continental
shelf. The presence of only a single specimen
in the NMFS collection from moderately deep
water on the outer continental shelf, in contrast
to the 71 specimens from inshore locations, illus-

740

WIGLEV and BURNS: DISTRIBUTION AND BIOLOCV OP MVSIDS

trates the relative scarcity of this species off-
shore.

Based on NMFS samples, spawning; takes
place from June to September. Ovigerous or
larvigerous females are 5.0 to 8.0 mm long and
the number of young per brood is 13 to 15. The
average diameter of eggs is 0.4 mm; the length
of stage VI larvae is 1.0 mm and of stage VII
larvae is 1.7 mm.

The NMFS collection contains 27 males and
31 females, a ratio of 0.9 male to 1 female.

Immature specimens within the size range of
3.4 to 4.5 mm are present in samples from Oc-
tober through January. Body lengths of adults
range from 4.7 to 8.9 mm.

This species was collected from a variety of
different bottom types (gravel, sand, coarse
sand, glacial till, and silty sand). Apiiarently
it has no special affinity for any one kind of sedi-
ment, but ap])ears to be more commonly associ-
ated with coarse-textured sediments. Members
of this species congregate in dead shells of bi-
valves such as Mercciiaria and Spwiila.

Sizes of adult specimens from coastal areas
are approximately 5 to 9 mm, whereas the off-
shore specimens reportedly reach lengths of
15 mm. Owing in part to this difference in size,
and partly to their deepwater habitat, Tattersall
(1951) considered the possibility that the large
offshore specimens collected by the research ves-
sels Albatross and Fish Haivk might represent
a new species closely related to H. formosa. He
concluded, however, that both groups were sim-
ilar and only one species was represented.

The deepwater specimen in the NMFS col-
lection is a female only 6.5 mm long. A mor-
])hological comparison of this specimen with
inshore specimens revealed no major differences
that we could detect.

SUMMARY

GENERAL

The princii:)al biological and ecological char-
acteristics for each of the 19 species in the
NMFS collection are summarized in abbreviated
form in Table 11. This tabulation provides a
condensed comijarison of one species with an-

other within the NMFS collection and can be
used for comparing NMFS information with
data from other sources.

TAXONOMIC AFFINITY AND ENDEMISM

The taxonomic affinities of mysids in the
NMFS collection are most closely allied with the
boreal and subarctic species in the North At-
lantic; however, a high degree of endemism is
evident.

Nine species having an amphi-Atlantic dis-
tribution are: Eucopia grhnaldU, Boreomysis
tridens, Eiythrops erythrophthalma , Metery-
throps robusfa, Pseudomma affine, Amhlyops
abhreciata, Mysis mixta, Pmunus flexuosus, and
Heteromysis formosa. The eight species that
are indigenous to the western North Atlantic
are: Bowmnniella portoricensis, Hypereryth-
rops caribbaea, Pseudomma sp., Bathymysis re-
noculata, Mysidopsis bigelorvi, M. furca, Mysis
stenolepis, and Neomysis americana. These in-
digenous species are all inhabitants of warm-
temjierate to tropical waters. Only one species
in the NMFS collection (Eucopia grimaldii) is
cosmo]Mlitan. Four species (Eucopia grimaldii.
Anchialina typica, Meterythrops robusta, and
Amhlijojis abbreviata) occur in the Pacific Ocean
as well as in the western Atlantic. One species
(Promysis atlantica) occurs in the South At-
lantic and North Atlantic Oceans.

GEOGRAPHIC DISTRIBUTION

The geographic distribution of sjjecies repre-
sented in the NMFS collection differs in scope
from .single records (of which there are three)
to wide-ranging multiple records. Mysidopsis
bigeloiri has the greatest range, extending from
northern Georges Bank southward to northern
Florida. Neo^nysis americana has a moderate
range, extending from northern Gulf of Maine
south to Chesapeake Bay. Bowmaniella portor-
icensis and Promysis atlantica have widespread
ranges in the southern area, with distributions
extending from Virginia to Florida. All re-
maining species were collected within rather
limited geographic areas along the eastern coast
of the United States, mostly off New England.

741

FISHERY BL'LLETIN: VOL. 69. NO. 4

Table 11. — Summary of biological and ecological information, by species, pertaining only to mysids in the

NMFS collection.

Body

length

Number

Geographic

Bothymetric

Bottom

Spowning

of eggs

Species

distribution

range

type

Range

Smallest

adult

season

per
clutch'

m

mm

mm

Eucopia grimaldii

Slope off southern New England

700

(Silt-clay)

32-0

32.0

Boreomysis tridens

Slope off southern New England

402

Silt-sand

15,0-26.0

26.0

BowmanieUa portoricensii

Inner shelf Virginia to Florida

9- 56

Sand

3.1-10.0

6.1

Spring and summer

30

Anchialina typica

Inner shelf South Carolina
to northern Florida

32- 38

Sand

4.5- 5.0

4.5

--

--

Erytkrops erythrophthalma

Inner ond outer shelf and upper
slope off New Englond

18-421

Sand

3.0- 9.6

4.3

(May-Oct.)=
Aug. ond Sept.

15

Meterytkrops robusla

Gulf of Maine

64-150

Gravel-sand

6.6-12.0

8.5

{Possibly spring)^

Hypfrerythrops caribbaea

Outer shelf off New England

168-179

Sand

5.5-11.0

9,5

Aug.

Pseudomma afjine

Outer shelf and upper slope off
New England

146-329

Sill-sond

4.0-13.1

7.3

July-Dec.=

11

Pseudomma sp.

Outer shelf off New England

Silt-sand

__

__

Amblyops ahbrrviata

Gulf of Maine

183-329

Silt-clay

4,7-15.0

10.0

Dec.

29

Bathymysis renoculata

Slope off southern New England

220-366

Silt-cloy

4.0-16.2

13.0

(Possibly spring)-

Mytidopsii bigflovji

Inner and outer shelf Georges
Bank to Florida

13-179

Sand

2.4- 6 6

3.5

(Possibly June-
Oct.)=

--

Mysidopiis furca

Inner shelf off South Carolina

22

Sand

4.2

4.2

Promysis atlantica

Inner shelf Virginia to Florida

8- 26

Sand

4.5- 5.0

4.5

Mysis mixta

Inner shelf off New England

29-159

Various

5.0-25.0

19.0

(Possibly winter or
eorly spring)^

-

Mysii stenoUpis

Shores of southern Massachusetts
ond Rhode Island

I

Sond and
Zoitera

13.0-26.0

20.0

Feb. and Mor.

188

Praunus flfxuosus

Shores of New Hampshire and
eastern Massachusetts

]

Various

15.5-28.0

15.5

Apr. -Nov.

44

Neomysii ameruana

Inner and outer shelf off New
England; inner shelf New Jer-
sey to Virginio

1-232

Sand

3.0-14.7

5.5

Mor.-Ocr. (possibly
also in winter)

»6
'26

HetiTomysis formosa

Inner ond outer shelf Massa-
chusetts to New Jersey

2- 84

Vorious

3.4- 8.9

A.6

June-Sept.

IS

1 A lorge proportion of ovigerous femoles hod an incomplete clutch. The values given here refer only to those
^ Deduced from the presence of immature specimens at a somewhat later season.

* Clutch size of the summer generation.

♦ Clutch size of the overwintering generation.

'ith a full complement of eggs.

The presence of 15 species in the New England
region (Table 12) , compared with only 3 species
in the Middle Atlantic and 5 species in the South-
ern area, is due, in part, to more intensive sam-
pling in the New England waters. However, the

Table 12.-

-Geographic classification of species, based
on the NMFS collection.

New England
(Nova Scotia south
to Hudson Canyon)

Middle Atlantic Southern

{Hudson Canyon south {Northern Virginia

to northern Virginia south to Florida)

Eucopia grimaldii
Boreomysis tridens
Erythrops erythrophthalma
Melerylhrops robusta
Hypererythrops caribbaea
Pseudomma ajfine
Pseudomma sp.
Amblyops abbreviate
Bathymysis renoculata
Mysidopsis bigelowi
Mysis mixta
Myjis stenolepis
Praunus flexuosus
Seomysis americana
Heteromysis formota

Bowmaniella portoricensis
Anchialina typica

Mysidopsis bigelowi

Seomysis ametieana
Heteromysis formosa

Mysidopsis bigelowi
Mysidopsis furea
Promysis atlantica

recovery of five species in samples from the
southeastern coast of the United States where
the sampling was sparse, indicates a relatively
diverse mysid fauna inhabits that region. Thor-
ough sampling will undoubtedly disclose a num-
ber of additional species (new species plus new
records for presently recognized species) in all
sections of the coast, though the Middle Atlantic
region can be expected to contain the fewest
species of mysids.

BATHYMETRIC DISTRIBUTION

The overall bathymetric range at which
NMFS mysids were collected is from 1 to 700 m
(Table 11). In general all depth zones are
rather evenly represented without a preponder-
ance in any one zone. In Table 13 the species
are listed under five categories based on the
watei' depths from which they were most fre-
quently caught. Two sjiecies were found only
in the intertidal zone. Five species are typically

742

WIGLEV anJ BIRNS: DISTRIBITION AND BIOLOGY OF MVSIDS

Table 13. — Bathymetric classification of species, based
on the NMFS collection.

1. Shore Species (occur in the intertidal zone, minimum and maximum
depth 0 and 1 m):

Mysii stfnoli'pis
Pranuus flfxuosus

2. Shallow Shelf Species (occur predominantly at depths less than 50 m,
minimum and maximum depth 2 and 84 m):

Boumaniella portoncensis
Anthialina typica
Mysidopsis furca
Promysis atlantiea
Hi-lrTomysis formosa

3. Eurybathic Shelf Species (occur over a broad range of depth on the
continental shelf, minimum and maximum depth 1 and 421 m):

Erythropf erythrophthalma
Mftfrylkrops robusta
Myiidopsis bigelozvi
Mysis mixta
Neomysis americana
Psfudomma sp.

4. Deep Shelf and Upper Slope Species (occur on the continental slope
and outer shelf, minimum and maximum depth 98 and 329 m);

HyprTfTythrops caribbaea
Pseudomma ajfinf
.Imblyops ahbreviala

5. Slope Species (occur predominantly on the continental slope, min-
imum and maximum depth 220 and 700 m):

Eucopia grimaldn
BoTfomysis tndfns
Bath\m\fii renoculala

Shallow Shelf (less than HO m) inhabitants.
Heternwysis formosa is included in this category
even though one specimen was taken at a depth
of 84 m. This is the only New England species
in this bathymetric category; all other Shallow
Shelf species are warm-water forms collected
in the southern region. Six species are listed
under the heading "Eurybathic Shelf Species."
They were each taken over a broad de])th range
(for example, Neomysis americana, 1-232 m) on
the continental shelf and occasionally on the
upper continental slope. Three species that live
along the outer margin of the continental shelf
are listed under the category "Deep Shelf and
Upper Slope Species." Depth range for these
species is 98 to 329 m. Three si^ecies were taken
at depths beyond the outer margin of the conti-
nental shelf, from 220 to 700 m. They are listed
under the category "Slope Species."

females is the most convincing evidence; this
was obtained for eight species. Additionally,
indirect evidence from catch records of imma-
ture specimens provides clues to possible spawn-
ing seasons of seven species, including four spe-
cies for which direct evidence is lacking.

Spawning of most species for which informa-
tion is available takes place during the warmer
months — May through October. Species that
spawn in this season are: Boivmaniella portor-
icensis, Erythrops erythrophthalma, Hyperery-
throps caribbaea, Pseudomma affine, Ambhjops
abbreviata, Prannus flexuosus, Neomysis amer-
icana, Heteromysis formosa, and possibly Buthy-
mysis renoculata and Mysidopsis bigeloivi.
One species, Neomysis americana, probably
.spawns in all seasons of the year with maximum
l^roduction in s])ring. Amblyops abbreviata and
Pseudomma affine spawn in winter and summer;
Meterythrops robusta, Mysis mixta, and M. ste-
nolepif: jirobably spawn in winter or early spring.

The number of eggs or larvae per clutch was
counted for eight species. Although the average
number per clutch for different species ranges
from 6 to 188, these extremes are rare. For
most sjjecies the average brood contains between
11 and 30; exceptionally small clutches (6 eggs)
were produced only by the summer generation
of Neomysis americana. Unusually large
clutches (average of 188 eggs) were tyjjical for
one species, Mysis stenolepis. A moderately
large number of eggs (average of 44) was pro-
duced by Prauniis flexuosus. Both of the latter
species are relatively large inshoi-e inhabitants.
Small species commonly brood as many eggs as
moderately large species; within a species, how-
ever, the smaller specimens have fewer eggs
than large siiecimens. The diameter of eggs of
ovigerous mysids in the collection was surpris-
ingly uniform. Both large and small sjiecies
produced eggs that were approximately 0.4 mm
in diameter.

SPAWNING

Information pertaining to the siKiwning sea-
sons of 13 mysid sjiecies in the NMFS collection
is summarized in Table 11. Direct information
based on the cajjture of ovigerous or larvigerous

BODY SIZE

The smallest and largest s]iecimens (excluding
larvae) in the NMFS collection are 2.4 and
32.0 mm in body length. Body lengths were
measured for 18 of the 19 species represented

743

FISHER V BULLETIN; VOL. 69. NO. 4

in the collection. (Siiecimens of Pseiidomma sp.
have not yet been measured.) They have been
classified as small, medium, or large. Two cri-
teria were used for determining the appropriate
size category: (1) the maximum length of spec-
imens of each species rei)resented in the col-
lection and (2) the length of the smallest adult
of each species.

Small species are those with a maximum
length of 6.6 mm or less and with the smallest
adult 4.5 mm or less. There are four species
in this category: Anchialina typica, Mysidopsis
bigelou'i, M. furca, and Pro»(2/.s/.s athnificu. My-
sidopsis bic/elowi is the smallest species encount-
ered; it matures at a body length of 3.5 mm.

Medium size species are those having a max-
imum length between 8.9 and 16.2 mm and with
the smallest adult 4.6 to 13.0 mm long. There
are nine species in this category: Bowynuniella
portoricensis, Erythrops erythrophthalma, Me-
tei-ythrojis robnsta, Hypererythiops caribhaea,
Psendommn affine. Amblyops abbreviata. Bathy-
mysis renocidata, Neomysis americana, and
Heteromysis formosa.

Large species are those with a maximum
length of 25.0 mm or more and with the smallest
adult more than 15.0 mm long. There are five
species in this category: Eucopia grimaldii,
Boveomysis tridens. Mysis mixta. M. stenolepis,
and Praunus flexuosiis.

RELATION TO BOTTOM SEDIMENTS

A large majority of mysid species in the
NMFS collection live on bottom sediments com-
posed of sand or silty sand. They were least
abundant and seldom encountered in gravel and
rocky areas. (Eucopia giimaldii is excluded
from this discussion of mysids in relation to bot-
tom sediments, because it is a bathypelagic spe-
cies.) Eleven of the 18 benthic species were
most commonly associated with sand and silty
sand. The sand-dwelling species are: Bowma-
niella, po)'forirensis, Avchialina hjpica, Enj-
throps erythrophthalma, Hypererythrops carib-
haea, Mysidopsis bigelowi, M. furca, Promysis
atlantica, and Neomysis americana. The two
most common species are both included with the
sand-dwelling inhabitsints, but there are signifi-

cant differences in the habitats they occupy.
Neom.ysis americana are occasionally taken on
silty sand bottoms, but typically inhabit sand
sediments that are silt free or contain very little
silt. Conversely, PJrythro/is erythrnjihthalina
have their center of abundance in areas of sand
sediments that contain small to moderate quan-
tities of silt. However, the silt content of the
sands they occupy is usually insufficient to classi-
fy them as silty sands according to the standard
classification established by Shepard (1954).
Silty sand inhabitants are: Boreomysis tridens,
Pseudomma affine. and Pseudomma sp. The
only species that is frequently associated with
gravels and other coarse substrates is Metery-
throps robusta.

Species associated with fine-textured sedi-
ments or with various tyiies of bottom materials
were usually less abundant and present at fewer
localities than the species listed above. Species
that were associated with silt-clays are: .Ambly-
ops ahbreriafa and Bafhymysis renocidata. Both
species are deepwater inhabitants. Their over-
ail depth range is 183 to 366 m. Fine-grained
sediments blanket a large portion of the sea floor
at these de])ths. S]iecies that were found occu-
pying a wide variety of difl^erent kinds of bottom
sediment types are: Mysis mixta, Praunus
flexuosus, and Heteromysis formosa. These are
shallowwater species and the most common
bottom types they inhabited were: sand,
gravel, silt-clay, glacial till, algae, and eelgrass
{Zostera) .

CO-OCCURRING SPECIES

The catch records reveal a high incidence of
co-occurrence of the Atlantic coast mysids.
Listed in Table 14 are 15 species, 79''f of the
total number of species collected, taken in the
same sample with one or more other species of
mysids. The presence of difl'ei-ent species of
mysids in dredges, trawls, ring nets, and similar
sami>liiig instruments that are towed along the
ocean bottom for relatively long distances
(hundred meters to several kilometers) reveals
a rea.sonably close spatial occurrence. Unfortu-
nately, the spatial separation between specimens
of the different species in such samples prior to

744

WIGLEV and BURNS: DISTRIBUTION AND BIOLOGY OF MYSIDS

collection are unknown. It was especially in-
teresting to find two species in the same grab
sample (Campbell sampler or Smith-Mclntyre
sampler), for example, Bowmanielki portoricen-
sis with Anchialina typira or Mysidopsis furca.
This is good evidence that within an area of
0.48 m- of sea bottom B. }fortoricensis lives with
A. typica or M. furca. Also, Neoinysis ameri-
cona and Mysidopsis bigelowi were caught in the
same grab (Smith-Mclntyre sampler) samples,
but in this case both species were taken from an
area of bottom only 0.1 m-. These examples, of
course, do not mean that these species are com-
petitors. They are strong indicators, however,
of close habitation and possible competition for
space or other living requirements.

Table 14. — A list of co-occurring species. Species in
column B were present in one or more samples with the
corresponding species listed in column A.

Bowmaniella portoricensis

.Inchialina typica
ErytkTops frythrophthalma

Pseudomma afjine

Pfeudomma sp.
Amblyops abbreviata
.\fysidopsis bigelowi

Meterytkrops rohusta
Hypenrythrops carihbaea

Myjidopsis furca
Myiis mixta

.Xtysis stenoUpis
Praunus flcxuosus
Neomysii amfrtcana

hieteromysii jorn.

Anchialina typica
Mysidopsis juna

BotvmanieUa portoricensis

ifypererythrops caribhaea
Pseudomma afjine
Pseudomma sp.
Mysidopsis bigelowi
Mysis mixta
\'fomysis americatia
lleteromysis formosa

Erylkrops erythrophthalma
flypererytlirops caribbaea
Amblyops abbreviata

Erythrops erythrophthalma

Pseudomma affinf

Erythrops cTythrophthatma
llypererylhrops caribbaea
A'eomysis americana

Mysis mixta

Erythrops erythrophthalma
Pseudomma affine

BotvmanieUa portoricensis

Erythrops erythrophthalma
Meterylhrops robusta
Neomysis americana

Praunus flexuosus

Mysis stenolepis

Erythrops erythrophthalma
Hypererythrops caribbaea
Mysidopsis bigelowi
Mysis mixta

Erythrops erythrophthalma

ACKNOWLEDGMENTS

We thank our associates and former associ-
ates, particularly Gilbert L. Chase, Jr., Harriett
E. Murray, Evan B. Haynes, Thomas L. Morris,
Ruth R. Stoddard, and Rober B. Theroux, and
other staff members of the NMFS Biological
Laboratory, Woods Hole, for assistance in col-
lecting: and processing samples; members of
the scientific staff at the Woods Hole Oceano-
graphic Institution and U.S. Geological Survey,
Woods Hole, for assistance in collecting samples;
crewmen aboard the research vessels; and Prof.
Arthur G. Humes, Boston University, Boston,
Mass., who read the manuscript and provided
helpful comments.

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716

ESCAPEMENT LEVELS AND PRODUCTIVITY OF THE NUSHAGAK
SOCKEYE SALMON RUN FROM 1908 TO 1966"

OLE A. Mathisen'^

ABSTRACT

Since the inception of a commercial fishery for soclteye sahnon in the Nushagak District, Bristol Bay,
Alaska, the annual yields have followed a definite pattern. Catches increased during a relatively short
development phase of the fishery, then stabilized for some years and then declined in two steps separated
by periods of relative stability.

For years the cause of the decline had been thought to be overfi-shing, and various measures of cur-
tailment had been placed upon the fishing industry.

Evidence is presented in this paper that the average escapement or the potential egg deposition re-
mained about the same during each of three periods (1908-1919, 192.5-1945, and 1946-1966) ; hence
the diminution in the runs was due not to lack of spawners but to a decline in the rate of return per
spawner.

So that the cause or causes of the present low reproductive potential can be ascertained, the effects
of fishing on the stocks of salmon must be examined. Besides removing part of the run, the yearly
commercial fishing operation may have altered either the age composition or the distribution of the
escapement.

Available historical records were examined for evidence of these types of changes but largely with
a negative result; therefore, the hj^pothesis was advanced that the observed declining rate of return
per spawner is caused by a declining basic productivity of the nursery areas. The latter is then ascrib-
able to the cumulative effect of relatively little enrichment of bioenergetic elements from salmon carcas-
ses since the instigation of commercial fishing operations in comparison with the prefishing era when
the entire virgin run escaped to the spawning grounds.

Suggestions are made for future field testing of this hypothesis.

In the development of the salmon fishery along
the eastern perimeter of the Pacific Ocean, the
most southern stocks were utilized first. As de-
mand increased and certain stocks declined, the
fishery shifted northward until the runs of the
entii-e southeastern Alaska and soon thereafter
those of the western districts were exploited.
The rapidity of growth of the salmon fishing in-
dusti'v in Alaska is astonishing. The firstcannery
was built in southeastern Alaska at Klawak in
1878 (Rich and Ball, 1928), and only 6 years later
exploratory fishing was conducted in Bristol Bay.
The early Bristol Bay catch records show that,
from 1884 to 1891, fishing was conducted only
in Nushagak Bay (Figure 1). Four years later,
salmon was harvested in the other watersheds
of Bristol Bay, the Kvichak-Naknek, the Egegik,

' Contribution No. 346, College of Fisheries, University
of Washington.

' Fisheries Research Institute, College of Fisheries,
University of Washington, Seattle, Wash. 98195.

Manuscript accepted April 1971.

FISHERY BULLETIN: VOL. 69, NO. 4. 1971.

and the Ugashik Districts. The patterns were
initially alike, with a continuous and steady rise
in production for at least 10 years in the smaller
districts of Egegik and Ugashik and 20 years
or more in the Nushagak District and even longer
in the Kvichak District where on the average
more than 60 'r of the Bristol Bay harvest is
made annually.

As these four fisheries developed, annual var-
iations became more and more aijparent, but the
overall iiroduction was fairly stable until 1919,
when it declined drastically all over Bristol Bay
in spite of no decline in fishing effort. The catch-
es in Ugashik, Egegik, and Kvichak Districts
soon thereafter rebounded to their former pro-
duction level, but the catches in the Nushagak
District did not. From this point on, the pattern
of development in Nushagak difl^ered from that
of the other fishing areas in Bristol Bay, primar-
ily in a more severe and persistent decline of the
stocks making up the entire run.

747

FISHERY BULLETIN: VOL. 69. NO. 4

In an effort to reverse this downward trend
by providing for larger escapements, fishing ef-
fort was reduced by restrictions on fishing time,
gear, and location. The effect of these measures
can be gauged from three principal sources of
information: (1) A counting weir was oper-
ated in the Wood River of the Nushagak District,
the principal trunk stream, during the years
1908-1919. (2) Biological studies were con-
ducted in subsequent years that provided data
on the age, length, and size composition of the
catch and in jiart of the escapement. (3) The
salmon canning iiidusti'y itself has kept meticu-
lous records on daily catches, number of fishing
units, and type of gear operated.

The various sources of data indicated above
were utilized to reconstruct the levels of escape-
ments in the Nushagak District during the last
50 years in an effort to determine whether the
magnitude of the yearly escapements is corre-
lated with the declining salmon production in
Nushagak Bay. If this were not the case, the
fishery may have changed the age and size com-
position of the stock or the distribution of the
various stocks in time and space. These factors
will be examined in a search for a logical expla-
nation of the decline of the Nushagak fishery.

NUSHAGAK BAY AND WATERSHED

Nushagak Bay includes the waters between a
line drawn from Nichol's Spit to Etolin Point
and the confluence of the Wood and Nushagak
Rivers (Figure 1). These streams serve as the
trunk streams of the Wood River lakes and the
Tikchik lakes, respectively. Two other trunk
streams drain into Nushagak Bay, namely, the
Snake River and the Igushik River. The entire
watershed comjn-ises a drainage basin of
10,207 km-. The morphometric parameters of
some of the more important salmon-producing
lakes are given by Gadau (1966).

Although sockeye salmon occur in more north-
erly latitudes, the Nushagak River system rep-
resents the northern boundaries of large sockeye
salmon runs. The reason may be the absence
of large lakes in more northern stream systems,
which would i)rovide sullicient nursery grounds.
Thus, in the Tikchik system there are six lakes

with five accessible to the salmon, but only the
three lower ones, indicated on Figure 1, are im-
portant for sockeye salmon production.

NUSHAGAK SOCKEYE CATCHES,
1884-1966

The commercial fishery for sockeye salmon in
Bristol Bay began in Nushagak Bay in 1884 after
the schooner Neptune made an exploratory salt-
ing expedition (Moser, 1902). Prior to that
time, some salting, from 800 to 1200 barrels each
year, was done by fishermen operating a simple
trap in the Wood River.

The most recent account of catch data was pub-
lished by Kasahara (1963). His figures differ
in some years from those given in Tables 1 and 2
of this paper, compiled in part from original
sources, but the discrepancies are mostly minor
in nature, and they do not change the overall
picture in catch level and trend. Derivation of
the Nushagak catch figures used in this report
is given in the footnotes and comments to the
mentioned tables.

When the Nushagak catches are plotted, they
exhibit strong annual variations, as in most sock-
eye salmon runs (Figure 2). A small part of
the variability can be explained by differences in
fishing effort, which reflected economic condi-
tions or inaccurate predictions by the cannery
superintendents as to the actual size of the run.
Viewed over longer time periods, however, there
can be no doubt that the annual catches reflect
changes in stock strength. This conclusion is
amply brought out by the construction of a trend
line by a moving average of 5's because of 5-year
cycle.

Three distinct periods are discernible. The
first period spans the years 1900-1918, the sec-
ond one covers the years 1921-1945, and the last
period includes the years 1946-1966. The aver-
age annual catches during these jieriods were
5,134,156; 2,888,726; and 1,183,485 salmon, re-
spectivel.y.''

Transition from one level to the next took

' If the estimated forpipfn catches made since 1956
were included with the domestic catches for the third
period, the average annual catch would be raised about
25%.

748

MATHISEN: NUSHAGAK SOCKEYE SALMON FISHERY
159°

158°

157°

60°

LAKE
CHAUEKUKTULI

60°

59°

158°

Figure 1. — The Nushagak District of Alaska showing (from north to south) the Tikchik, Wood River,

Snake River, and Igushik River lake systems.

749

FISHERY BULLETIN: VOL. 69, NO 4

Table 1. — Commercial catches of sockeye salmon, Nu-
shagak Bay, 1893-1945.

Nushogaii Sockeye Calc^
1 893 -1966

Number
of f-sh

Number
of fish

1893

640,000

1921

3.717,284

1894

860,000

1922

3,408,358

1895

938,946

1923

1,921,874

1924

2,168,154

1896

1,262,690

1925

3,903,125

1897

1,240,080

1898

1,890,092

1926

4,022,328

1899

2,517,436

1927

657,467

1900

4,234,533

1928

4,957,096

1929

3,851,479

1901

5,401,051

1930

1,610,568

1902

4,725,715

1903

6,319,189

1931

2,260,541

1904

5,345,659

1932

3,083,615

1905

7,387,935

1933

3,753,230

1934

4,575,049

1906

5,427,512

1935

649,093

1907

2,627,351

1908

6,092,031

1936

1,560,138

1909

4,906,635

1937

4,561,298

1910

4,469,755

1938

2,322,704

1939

4,169,121

1911

2,957,073

1940

1,519,082

1912

3,993,428

1913

5,409,933

1941

1,897,869

1914

6,457,815

1942

2,465,779

1915

5,904,862

1943

3,373,643

1944

3,513,241

1916

3,744,551

1945

2,296,019

1917

5.847,239

1918

6,296,702

1919

1,477,336

1920

2,682,056

Sources:

I884-]927 - Rich and Boll (1928).

1929-1945 — Annual District Management Reports, District Agents. Bu-
reau of Fisheries and Fish ond Wildlife Service.

Comments:

The catches for 1884-1892 are only given in cases and therefore are not
included. , ,

For the years 1925-1946, Alaska Salmon Industry gathered dolo on the
catch, the pack, and expended effort by the major fishing coniponies.

The number of fish per case is computed from the information collected
by Alaska Salmon Industry. It was used for conversion of the cose pock
into number of fish for the years 1929, 1930, 1931, 1932, and 1941. since
only the case pack is recorded for these years in the Reports of the Man-
agement Agencies.

One 200-lb. barret of salted salmon has been set equal to 54 fish and
one 350-lb. barrel equal to 95 salmon.

The official recorcis for the year 1928 list only canneries thot operated
in Nushogak in this year. The catch figure usea is based on records sub-
mitted to Alaska Salmon Industry from all but two canneries. The catch
in the latter case was extracted from the sworn reports submitted by the
fishing industry to the tax authorities.

place within 2 to 3 years. Althouofh the other
districts in the Bristol Bay region have experi-
enced a decline in production, this decline has
been neither so distinct nor so drastic in nature
as in the Nushagak District.

FISHING GEAR AND AREAS IN
NUSHAGAK BAY

Three types of fishing gear have been utilized
in Nushagak Bay — traps, drift gill nets, and

80

Coieh eu>.e, unsmooiheo

72

s

Coleh co>»e.smooihe<1 Dy

movnq ovetoqe Dl S s

he

':■':'■ ■ i'' A

c 4fl

T 'A'^y'^ '\-

l«

'J '.'^': i\L

■5

/ M iY

■oiA

'i ,' ' I; ''.

|..

/ '••

'■ / 1 i* VtT\ '■

16

/ '

;j

1 ' ' \ ''"'

08

' t . t

f

J tw^

i

1890 169^ 1898 I9(H I90« 1910 I9W I9IS 1922 1926 1930 1934 1938 I9« I9« 1950 I9M 1958 1962 1966

Figure 2. — Catches of sockeye salmon in the Nushagak
fishery, 1893-1966.

stationaiy gill nets (set nets). Traps were not
used to any great extent in the Nushagak fishery
or in Bristol Bay as compared with other areas
of Alaska, in which they were in widespread use.
The main factor which discouraged the use of
traps undoubtedly was the strong tidal currents
in Bristol Bay, where tidal differences reach as
high as 25 ft or more and peak water velocities
reach 4 to .5 knots. These conditions permitted
trap operations only in a restricted number of
places. Since gear records became available in
190 1 and until traps were outlawed in 1923, their
number in Nushagak Bay varied from 3 to 11
(Rich and Ball, 1928).

Apiuirently set nets were not commonly used
during the period when traps were legal. The
first documented set net catches were taken in
1924, and set nets are mentioned in the 1926
regulations. A maximum length of 7.5 fm was
set in 1926, but in 1931 maximum length was
reduced to 50 fm, as is the case today. Since the
advent of yearly reports by the management
agent in 1929, accurate records have existed as
to the distribution of eff"ort between these two
ty|ies of geai'.

Uj) to and including 1922, no restrictions were
placed on mesh size and length of the drift gill
nets. In 1924, tiie maximum length of drift nets
was set at 200 fm and mesh size of at least 5%
inches, stretched measure, between knots. After
the 1925 season, minimum size was set at S'/j
inches. No other changes in mesh regulations

750

MATHISEN: NUSHAGAK SOCKEVE SALMON FISHERY

Table 2. — Catches and escapements of sockeye salmon in Nushagak District, 1946-1966.

Sources:

1946-1959 - Mathlsen, Burgner, and Koo (1963)-
1960-1966 — Alaska Department of Fish and Game, Div

Catch

Escapement by river syste

m

Estimoted
total run

Escapement

Year

Wood
River

Other
streams

Total

as percent
of fotol run

1946

2.028.144

3.717,000

1,002,000

4,719,000

6,747,144

70.0

1947

2.767.287

1,782,000

725,000

2,507,000

5,274,287

47.5

1948

2.805.793

1,483,250

608,000

2,091,250

4,897,043

42.7

1949

800,123

101,025

37,000

138,025

938,148

14.7

1950

1.212.091

451,600

121,000

572,600

1,784,691

32.1

1951

436.950

457,600

82,000

539,600

976,550

55.3

1952

698.071

226,800

207,000

433,800

1,131,871

38.3

1953

449,341

515,542

313,000

828,542

1,277,883

64.8

1954

315.357

570,624

121,000

691,624

1,006,981

68.7

1955

1.054,978

1,382,755

551,000

1,933,755

2,988,733

64.7

1956

1,263,186

773,101

439,000

1,212,101

2,475,287

49.0

1957

491,498

288,727

210,000

498,727

990,225

50.4

1958

1,092,156

960,455

317,478

1,277,933

2,370,089

53,9

1959

1,719,687

2,209,266

832,619

3,041,885

4,761,572

63.9

1960

1,517,988

1,016,073

657,185

1,673,258

3,191,246

52.4

1961

511,483

460,737

398,896

859,633

1,371,116

62.7

1962

1,461,766

873,888

63,810

937,698

2,399,464

39.1

1963

842,744

721,404

342,452

1,063,856

1,906,600

55.8

1964

1,420,941

1,076,112

262,892

1,339,004

2,759,945

48.5

1965

793,323

675,156

424,110

1,099,266

1,892,589

58.1

1966

1,170,271

1,208,682

422,044

1,630,726

2,800,997

58,2

Total

24,853,178

20,951,797

8,137,486

29,089,283

53,942,421

-.

Average

1946-1966

1,183,485

997,705

387,499

1,385,204

2,568,689

51.9

jion of Commercial Fisheries, Bristol Bay Area, Annuol Management Report 1966, 59

were made until 1961, when 5%-inch nets were
permitted.

The length of drift nets was reduced to 150 fm
per boat in 1929 and has remained unchangfed.
However, the industry did not necessarily always
feel compelled to observe these maximum and
minimum limits. The g-iU net fishery developed
before such regulations were introduced and en-
forced. The necessity of observing a corres-
pondence between the pull of the boat and the
drag of the gill net had more or less standardized
the gear. Length of the drift net and mesh size
as actually used can be studied from two other
sources (Table 3).

For the period 1902-1925, the mesh sizes and
lengths of the drift nets used were given in the
yearly reports of two canneries belonging to
Alaska Packers Association in Nushagak.

Since 1926 reports have been submitted by the
operators to the Federal government concerning
their canning activities. These sworn state-
ments give the lengths of nets used by the dif-
ferent companies. Since the advent of state-
hood, gear regulations have been published
annually.

There has been a gradual but steady decline
of the mesh size to 5% inches, stretched mesh.
In contrast, the length of the drift nets has been
remarkably constant. Even when an upper limit
of 200 fm was introduced in 1924, many oper-
tors used nets half this size or 100 fm. Since
1928, all drift nets have measured 150 fm long,

Table 3. — Mesh sizes and lengths of drift gill nets used
in the Nushagak sockeye salmon fishery, 1902-1966.^

Stretched

Length of
drift net

mesh size

inches

jathomi

1902

61/8-61/4

1903

6%

120

1904

6-6'/e

150

1905

6<A

ISO

1906

6-i%

150

1907

6<A6-6<A

160

1908-1912

6

160

1913-1925

5%

150b

1926-1927

SVi-S'A

100-200C

1928-1960

S'h

150d, e

1961-1966

S'M

150

a Information prior to 1925 taken from records of the Alaska Packers
Association and for subsequent years from onnounced regulations of the
Federal Authorities.

b A maximum legal length of 200 fm ond minimum mesh size of 5%
inches specified for 1924 and 1925.

c A minimum mesh size of 5V2 inches set for new nets.

d A maximum length 150 fm set in 1929.

e A maximum length of 100 fm set for 1937 only.

751

FISHERY BULLETIN: VOL. 69, NO. 4

except for the year 1937, when the maximum
size was reduced to 100 fm for 1 year and only
for Nushagak Bay.

Powered fishing boats were outlawed in 1922
and not permitted again until 1951. However,
in the 30's the canning companies started to use
small tug boats to tow the fish boats fi'om one
place to another, or most commonly to assist in
bringing a boat to the delivery scow. Conse-
quently, the efficiency of one boat increased with
this added mobility. In part, it was offset by
the movement of fishing boundaries over the
years farther and farther out from the river
mouth and thereby reduction in efficiency of the
fishing gear.

In 1899, fishing above tidewater was prohib-
ited in streams less than 500 ft in width. In
the tidewater of smaller streams, gear could only
cover one-third of the stream width.

In 1907, fishing in the Wood and Nushagak
Rivers was prohibited within 500 yards of the
mouth of Wood River. Over the years, gradu-
ally, restrictions of fishing area have been im-
posed, which resulted in a transfer of fishing
operations away from the river and river mouth
and into the open Nushagak Bay. In Figure 3
are indicated locations of canneries in operation
shortly after the turn of the century. Only three
plants remain actively canning in Nushagak Bay
today.

THE NATURE OF THE SOCKEYE
SALMON RUNS

All sockeye salmon runs to Bristol Bay have
a very distinct and regular time schedule. His-
torically, the period from June 25 to July 25
has been considered as the time when the salmon
are present in Nushagak Bay in catchable quan-
tities. Records accumulated since 1955 indicate
that, on the average, peak catches in Nushagak
Bay were made on July 5 (Royce, 1965).

The entry is of a i)ulse tyjie with exponential
declining departure curves for the trunk streams
and the spawning grounds (Mathisen, 1969).
Bi- or trimodal catch curves, especially in earlier
years, undoubtedly were created by changes in
frequency or I'ehilivc strength of the individual
pulses. We do not know the racial composition

NUSHAGAK RIVER DISTRICT

Figure 3.— Copy of an old map (probable date 1907)
with the locations of canneries and salteries in Nushagak
Bay. Canneries in operation today are the Columbia-
Wards Cannery at the site of North Alaska Salmon
Company Cannery, a Queen Fisheries plant near Co-
lumbia River Packers Association plant, and Pacific
Alaska Fisheries Dillingham plant at the site of Alaska-
Portland Packers Association.

of the individual pulses, but some tagging data
(Straty, 1969) jjoint to a fairly random mixing
of individual races.

Basically, the juvenile salmon spend 1 or 2
years after emergence in the nursery areas of
the freshwater lakes. They return from ocean
feeding after 2 or 3 years. Thus, four different
age groups will make up a year's run, namely,
1.2, 1.3, 2.2, and 2.3 (after Koo's [1962] nota-
tion). The number of fish in other age groups
is insignificant and can be disregarded. The
Nushagak District differs from other districts
in Bristol Bay in having a preponderance of 1-
freshwater check salmon.

ESCAPEMENT LEVELS IN THE
NUSHAGAK DISTRICT

The history of the Nushagak fishery was di-
vided earlier into three periods. Within each
of these periods data exist in regard to escape-

752

MATHISEN: NUSHAGAK SOCKEYE SALMON FISHERY

ment levels, althoiiofh they differ in completeness.
Naturally the best records have been assembled
duririg the last period, while the most incomplete
records exist from the middle period. The
escapement records are discussed in order of
completeness.

THE PERIOD 1946-1966

and escapement level, rather in the overall ratio
of catch to escapement over the entire jjeriod.
The average catch amounted to 1,183,485 sock-
eye salmon and the average escapement to
1,385,204 spawners. The ratio is almost one to
one; or on the average, a pair of spawners pro-
duced a progeny of four fish. In terms of fishing
mortality, the rate of exploitation has averaged

The records for this period are complete in
the sense that escapement estimates were made
for all streams draining into Nushagak Bay
(Table 2). Estimates were based originally on
ground or aerial surveys. In 1953, the Wood
River escapement was estimated from tower
counts in the trunk stream. In 1958, this tech-
nique was adopted for assessment of the Igushik
escapement, and in 1959 for that of the Nuyakuk
River. From 1960 to 1964, tower counting was
conducted in the Snake River system and inau-
gurated in the Nushagak-Mulchatna River in
1966. Otherwise, escapement estimates were
made by the less reliable aerial survey. The
earlier estimates based on ground surveys all
have in common a much larger variance, but they
gain in consistency because of the fact that large-
ly the same personnel conducted spawning sur-
veys in all years, even after introduction of tower
counts (Gilbert, 1968).

In the present context, we are not jjrimarily
interested in the year-by-year changes in catch

THE PERIOD 1908-1919

No total escapement estimates exist for this
period, except for the Wood River system where
a counting weir was operated from 1908 to 1919
with the exception of the 1914 season. Daily
counts and comments on weir building and main-
tenance are found in Reports of the Commis-
sioner of Fisheries for the years in question
(Table 4).

On the assumption that the ratio of the Wood
River escapement to the total Nushagak escape-
ment was the same for the years 1908-1919 as
was observed during the period 1946-1966, when
estimates were available of the Wood River
escapement as well as of the total Nushagak
escapement, then this ratio can be used to esti-
mate the total Nushagak escapement for the
years 1908-1919 from the weir counts.

The ratio of the total Nushagak escapement
to the Wood River escapement has been computed
in two ways from data in Table 2. The first ratio

Table 4.— Total Nushagak escapement 1908-1919.

Wood River
weir count

Estimated
Nushagak
escapement

Estimated
total run

Escapement

OS percent

of total

run

1908

2,603,655

3,758,636

6,092,031

9,850,667

38,2

1909

893.244

1,289,487

4,906,635

6,196,122

20.8

19)0

670,104

967,362

4,469,755

5,437.117

17.8

1911

354,299

511,466

2,957,073

3,468,539

14.7

1912

325,264

469,551

3,993,428

4,462,979

10.5

1913

753,109

1,087,188

5,409,933

6,497,121

16.7

1914

No count

6,457,815

__

1915

259,341

374,385

5,904,862

6,279,247

6.0

1916

551,959

796,808

3,744,551

4,541,359

17.5

I9I7

1,081,508

1,561,265

5,847,239

7,408.504

21.1

191S

943,202

1,361,606

6,296,702

7,658,308

17.8

1919

145,114

209.487

1,477,336

1,686,823

12.4

Total

8,580,799

12,387,241

57,557,360

63,486,786

—

Average

1908-1919

780,073

1,126,113

4,796,447

5,771,526

19.5

Sources: Reports of the Commissioner of Fisheries for the fiscal years 1908 through 1919 and special papers. Government Printing Office, Washington,
D.C., 1910-1921.

753

FISHERY BULLETIN: VOL. 69, NO. 4

is based on the data for the years 1946-1957,
when the escapement estimates were made
largely from ground and aerial surveys. Pre-
sumably this estimate is less reliable -than the
second estimate based on the years 1958-1966,
when the escapement estimates were based
largely on very reliable tower counts. The two
ratios are 1.4438 and 1.4433.

Thus the average Wood River escapement has
formed a remarkably constant proportion of the
total Nushagak escapement regardless of which
years are used for calculation. Consequently,
the ratio 1.4436, based on data for all the years
1946-1966, has been used to enlarge the early
Wood River weir counts from 1908 to 1919 to
reflect the Nushagak escapement for the same
years.

Estimated in this manner, the annual Nusha-
gak escapement for the period 1908-1919 aver-
aged 1,126,113 spawners, and the total Nushagak
sockeye run averaged 5,771,526 salmon, or a rate
of exploitation of 80.5%.

THE PERIOD 1925-1945

No weir counts exist for these years, and quan-
titative stream surveys were not conducted.
However, escapement estimates can be made
from available data on the catch, size distribution
of the fish, sex ratio, and expended effort.

From 1926 on, the legal minimum mesh size
was 51/2 inches, and from 1927 the maximum
length of the drift gill nets i-emained unaltered
at 150 fm. An exception must be made for 1937,
when the maximum length was reduced to 100 fm
for this one year in the Nushagak fishery. There-
fore, given a measure of the catch and the in-
stantaneous rate of fishing for each centimeter
group by the 5i/.>-inch gill nets and an estimate
of expended fishing effort, the escapement can
be calculated by centimeter groups from the
formula for competitive fishing units and
summed over the size range observed in a year
to give the total escapement:

E

h

e '"i

1

where E = the unknown total escapement,

Cj = the known catch for size group /,

Qi = the coefficient of catchability for

size group ./,
/ = the number of standardized fish-
ing units, and
a and b = lower and ui)per bounds of the
size range.

No natural moi'tality has been assumed during
the fishing season.

Because of the different selection curves for
males and females by 5V2-inch mesh size, these
calculations must be done separately for each
sex. The necessary data for this calculation
follow.

Sex Ratios

It has been assumed that no selection for sex
was exerted in the collection of samples for size
and age composition. Consequently, the num-
bers of males and females measured in a day
provide an estimate of the sex ratio in the catch
for that particular day. This procedure was
necessitated by the absence of specific sex ratio
samples.

Size Composition of the Catch

During the years considered here, the Bureau
of Fisheries stationed biologists at selected can-
neries for collection of scale samples and length
measurements. At other times, resident people
were hired for the same purpose and paid a fixed
amount for each scale book collected.

Generally the type of length measurements
made is not indicated in the records; but it
has been assumed that the procedure was to
measure length from the tip of the snout to the
fork of the tail. This assumption was verified
by a comparison of the resulting length-fre-
quency curves with the mean lengths of 2- and 3-
ocean fish in postwar years.

Since 1946, the common procedure has been
to measure the length of the sockeye salmon
taken in the fishery from the middle of the eye
to the fork of the tail. The Fisheries Research
Institute took a series of double measurements
in 1946 to provide a basis for constructing a i-e-
gression line between the two types of measure-
ments, and a conversion can be made from one

754

MATinSEN: NL'SIIAGAK SOCKEVE SALMON FISHERY

measurement to the other by means of the two
following equations:

S : ME-TF = 536.772 + 0.8279
[(snout-TF) — 592.340]

5 : ME-TF =. 527.481 + 0.8946
[(snout-TF) — 569.724]

Commonly, length measurements were collect-
ed throughout the fishing season. These mea-
surements were grouped by fishing periods or
by time periods for which catch records exist.
Finally, a seasonal weighted length-frequency
distribution was computed by the use of the
period catches as weighting factors.

Expended Fishing Effort

Batts and Fischler (1967) have summarized
the fishing regulations promulgated during the
years 1924-1945. A summary of the allowable
fishing time is given in Table 5, without consid-
eration for the stage of the tide in relation to
closed and open periods. Although the largest
or smallest tides generally are inferior fishing-
periods compared with the medium-sized ones,

no correction was attempted on the premise that
the plus and minus deviations tended to cancel
each other over the entii-e season.

The number of fishing boats that operated each
year for the period 1929-1945 is recorded by the
management agents in their annual reports and
copied in Table 5. The size of the Nushagak
fishing fleet in 1925-1928 was estimated from the
data collected by the Alaska Salmon Industry.
More than 60% of the total Nushagak catches
during these 4 years were made by the reporting
canneries, which also submitted records on the
number of boats employed. By direct propor-
tionality an estimate was derived for the total
number of fishing boats and set nets that op-
erated from 1925 to 1929 (Table 5).

So that a common unit of eff'ort could be de-
rived, the fishing power of set nets was expressed
in terms of that for drift nets according to a
method by Robson (1961) .' The conversion was
made separately for each year by consideration

* Robson, D. S. 1961 . Estimation of the relative
fishing power of individual .ships. Cornell Univ., Bio-
metrics Unit, Plant Breeding Dep., BU-133-M. (Un-
published manuscript.)

Table 5. — Registered fishing effort in Nushagak Bay, Bristol Bay, Alaska, 1925-1950.

Total
fishing

time
in days

Total

number

boats

(drift nets)

Total

boot doy

units

Total
number
set nets

Total

set net

day

Relative

efficiency

set nets/boots

converted

to boat

units

Total

effort in
boat days

1925

22.000

337

7,414

66

1,452

.0717

104.0

7,518

1924

21.000

256

5,376

44

924

.1153

106.5

5,483

1927

19.500

292

5,694

63

1,326

.2796

370.7

6,065

1928

22.500

264

5,940

39

878

.3283

288.7

6.229

1929

21.000

311

6,531

115

2,415

.3613

872.5

7,404

1930

15.250

335

5,109

112

1,708

.1640

280.1

5,389

1931

13.500

351

4,739

152

2,052

.3264

669.8

5,409

1932

18.333

276

5,060

208

3,813

.1151

438.9

5,499

1933

18.688

280

5,233

167

3,121

.1617

504.7

5,738

1934

19.666

279

5,487

221

4,346

.0833

362.0

5,849

1935

9.000

65

585

154

1,386

.2981

413.2

998

1936

17.750

298

5,290

263

4,668

.5129

2,394.2

7,684

1937

19.500

236

4,602

173

3,374

.1594

537.8

5,140

1938

19.500

99

1,931

96

1,872

.2426

454.1

2,385

1939

19.000

235

4,465

144

2,736

.3217

880.2

5,345

1940

14.000

129

1,806

128

1,792

.5773

1,034.5

2,841

1941

19.000

125

2,375

116

2,204

.1803

397.4

2,772

1942

27.500

96

2,640

53

1,458

.2827

412.2

3,052

1943

21.500

119

2,559

98

2,107

.3850

811.2

3,370

1944

24.000

118

2,832

103

2,472

.2889

714.2

3,546

1945

20.000

82

1,640

164

3,280

.2134

700.0

2,340

1946

16.500

198

3,267

119

1,964

.3077

604.3

3,871

1947

21.000

181

3.801

190

3,990

.2650

1,057.4

4,858

1948

16.000

198

3,168

216

3,456

.4709

1,627.4

4,795

1949

10.400

192

1,997

272

2,829

.2255

637.9

2,635

1950

13.500

108

1,458

270

3,645

.1728

629.9

2,088

755

FISHERY BULLETIN: VOL. 69, NO. 4

of 5 days during the peak of the fishing season.
This procedure eliminated some of the variability
present at the beginning or the end of the fishing
season due to irregular entries or departures of
the salmon. The choice of 5 days was made in
order to avoid too complicated a scheme, and
often more than half of the total Nushagak catch
was taken during the time period considered.

In this two-way classification with two rows
corresponding to drift net and set net and five
columns corresponding to the time periods, the
catch in 1 day and by a given type of gear is:

Cii = fij ■ n ■ Nj ■ e,j ,

where fa = the number of fishing units of
type i operated on day ;,

n = the coefficient of catchability of
gear type (' for all size groups,

Nj = the average stock of salmon en-
countered by the gear on day j,
and

en = error term.

If r . . is the coefficient of catchability of a unit
of a theoretical average of all types of gear,
one can write ai = n/r . . Similarly, if the av-
erage stock size encountered by the gear during
the entire period is defined as N . ., one has
Pj = Nj/N . . Finally, the error term was con-
sidered log-normal (Beverton and Holt, 1957).

The random variable Yn — log {dj/fn) can
be written then as

Yij = m + ai + bj + e,j.

Since we have only two types of gear, log r-y —
log Vi ~ a2 — ai. An estimate of ai can be ob-
tained directly from a linear hypothesis program,
such as BMD 05V (Di.xon, 1965) , under the con-
straint tti + a2 = 0. The results expressed
as arithmetic ratios are listed in Table 5.

Fishing Power of 5J^-Inch Gill Nets

Two size groups of fish iiredominate in all
Bristol Bay sockeye salmon fisheries (Mathisen,
Burgner, and Koo, 1963). The 3-ocean fish
measure on the average from 5 to 6 cm longer
than the 2-ocean fish, and the males of both size
groups are between 2 and 3 cm larger than the
females.

Between years there are i)ronounced differ-

ences in the proportion of 2- and 3-ocean fish and,
to a much smaller extent, in the sex ratio of the
total runs. Since during the middle part of the
Nushagak fishery considered here, the mesh size
of the gill nets remained stable at 51/2 inches,
the total fishing mortality generated by one unit
of gear changed from year to year primarily
with changes in the relative proportion of 2-
and 3-ocean fish and males and females. Con-
sequently, the coefficient of catchability must be
determined by length or age groups, and sep-
arately for males and females. There are only
5 years, 1946-1950, with records of catch and
escapement when sailboats were used together
with linen gill nets. Conversion to powered fish-
ing boats was largely accomplished by 1954, al-
though a shift in boat types continued. At the
same time nylon gill nets came into universal use.
Added to these changes were modifications of
boundary lines of the fishing districts. There-
fore, the rate of the present-day fishing of the
gear in Bristol Bay is not comparable with that
which prevailed during the middle period of the
Nushagak fishery.

Data on catch and escapement and the cor-
responding length-frequency distributions for
Nushagak from 1946-1950 are available (Math-
isen et al.. 1963). The escapements were esti-
mated visually and may not be too accurate.
But in 1 year, 1946, when an independent esti-
mate could be made from a tagging experiment,
the correspondence was remarkably great
(Mathisen, 1969) . Effort during the same years
is listed in Taljle 5. On the assumption that set
net effort can be converted into drift net effort
and that all units of gear were fishing simul-
taneously on the same stock, it is a straightfor-
ward matter of computing the coefficient of
catchability for each centimeter group and sep-
arately for males and females from the expres-
sion on page 754 used in reverse.

There were rather large year-to-year varia-
tions; therefore the following smoothing process
has been applied to the data. An arithmetic
mean value for each centimeter grou]) was found
for the 5 years considered. A moving average
of 5's of these arithmetic means provided the
final values in the selection curves in Figure 4.
The (lip in the selection curve for males is con-

756

MATHISEN: NUSHAGAK SOCKEVE SALMON FISHERY

lOOi

Table 6. — Age composition in trap and gill net catches
in Nushagak, July 1 and 5, 1919.

I ■ ■ ' ■ I ■ ■ ' ' I
40 45 50 55 60

Total length (cm)(ME-FT)

65

70

Figure 4. — Instantaneous rate of fishing by centimeter
groups.

sidered due to statistical variability introduced
by the rather small escapements in 1949 and
1950. It was further demonstrated by similar
calculations for recent years with exact catch
and escapement data that once the males become
vulnerable to the gear, the coefficient of catch-
ability increases only slightly from 2- to 3-ocean
fish. Whereas in the lower part of the selection
range, the curves are fairly similar for males
and females, the rate of fishing on 3-ocean fe-
males was several times that of 2-ocean females
based on the average lengths of these two groups
given by Mathisen et al. (1963). As a result,
in years when 2-ocean fish predominated in the
run, a large preponderance of females was pre-
sent in the escapement as in 1946, when there
were 68% males in the catch and only 35% males
in the escapement. In 1948, when there was a
predominance of 3-ocean fish, the corresponding
figures were 44% and 49%.

The selective action of the gill nets on the 3-
ocean fish can be demonstrated further by com-
parison of age composition of gill net and trap
catches made in the same year (Table 6). The
traps can be considered nonselective and were
placed close to the upper boundary line of the
fishing area (Moser, 1902). Therefore, the age
composition of the trap catches can be used as
an estimate of the age composition of the escape-
ment. Whereas the 2- and 3-ocean fish were
present in about the same numbers, the catch
by 5%-inch gill nets contained more than five
times as many 3-ocean fish as 2-ocean fish.

Traps

Gill

nets

Age
group

Number
of
fish

Percent

Number
of
fish

Percent

1.2

65

M

2.2

33

15

2-ocean

98

51.9

29

15.5

1.3

83

150

2.3

8

8

3-oceon

91

48.1

158 .

84.5

Total

189

187

Source: Clark, Frances N. 1933. Red salmon in the Nushagak District
of Bristol Boy Alaska. (U.S. Bureau of Fisheries) Nafl. Mar. Fish. Serv.,
Biol. Lab., Auke Bay, Alaska. (Unpublished manuscript.)

ESTIMATED ESCAPEMENTS, 1925-1945

When the calculations outlined above are ex-
ecuted, an estimated escapement for each of the
years from 1925 to 1945 is obtained (Table 7).
Two years, 1932 and 1938, were not included
in the computation of an average escapement
level since no length measurements were taken
in these years. No measui-ements were taken
in the fishery in 1931; instead, scales and mea-
surements were collected in the Wood River,
and this length-frequency distribution has been

Table 7. — Calculated escapements and total runs in
Nushagak District, 1925-1945.

Total
catch

Total
escapement

Estimated
total
rurt

Escapement
as percent
of total run

1925

3,903,120

285,081

4,188,201

6.8

1926

4,022,333

697,730

4,720,063

14.8

1927

657,468

803,643

1,461,111

55.0

1928

4,957,072

1,383,130

6,340,202

21.8

1929

3,851,482

754,125

4,605,607

16.4

1930

1,610,568

3,158,751

4,769,319

66.2

1931

2,260,539

491,877

2.752,416

17.9

1932

3,083,165

—

—

1933

3,753,230

1.995,688

5,748,918

34.7

1934

4,575,043

1,791,481

6,366,524

28.1

1935

649,093

2,277,858

2,926,951

77.8

1936

1,560,135

1,816,382

3,376,517

53.8

1937

4,561,297

10,118,033

14,679,330

68.9

1938

2,322,704

__

--

1939

4,169,122

361,356

4,530,478

8,0

1940

1,519,082

990,237

2,509,319

39.5

1941

1,897,870

1,197,981

3,095,851

38.7

1942

2,465,779

1,586,861

4,052,640

39.2

1943

3,373,650

1,762,232

5,135,882

34.3

1944

3,513,236

1,335,734

4,848,970

27.6

1945

2,296,020

1,614,470

3,910,490

41.3

Total

61,002,458

34,422,650

90,018,789

—

Average

1925-1945

2,904,879

1,811,718

4,737,831

38.2

757

FISHERY BULLETIN: VOL. 69, NO. 4

used. Since the fish in the escapement average
smaller than in the catch, it will result in an
overestimate of the total run for this year.

Unquestionably, the computed escapements
are subject to many sources of error, and they
reflect only the general magnitude of the escape-
ments. In genera! there are some measurements
from each fishing period that can be weighted by
the corresponding catches, and any unrepresent-
ativeness of the sampling was in part corrected.
It therefore appears that the greatest bias arises
from the way in which fish were selected and
measured. In 1930, for example, there were few
measurements taken, and they included a rather
high proportion of suspiciously small 2-ocean fe-
males, which resulted in the rather large esti-
mated total escapement. Almost 12,000 mea-
surements were made in 1937, but largely of fish
from the resident set net fishery near the upper
fishing boundary. The result is an underestimate
of the mean average length in the commercial
catches, since the run at this point had been sub-
jected to the selection of the drift net fishery;
the calculated escapement is substantially in-
flated. In 1939 no 2-oceaii fish were measured
in drift net catches, and therefore the low rate
of escapement may be substantially correct.

The International North Pacific Fisheries
Commission (1962) has published estimates of
Nushagak escapements for the period considered
here. A fishing rate common for all size groups,
and with no distinction between males and fe-
males, was computed from Bristol Bay catch and
escapement data for 1955-1957. Furthermore,
nylon gill nets were used and were operated
from power boats. Because of the selective ac-
tion of the gill nets for males and females, and
for 2- and 3-ocean fish, it is easy to understand
that these estimates are entirely different from
those presented here.

SUMMARY OF RESULTS

On the previous pages, escapement levels were
calculated for the three distinct periods of the
Nushagak fishery shown by the catches on Fig-
ure 2. These results have been summarized in
Table 8.

Table 8. — Rate of exploitation in three periods of the
Nushagak fishery.

Average
escapement

Average
catch

Exploitation

1908-1919
1925-1945
1946-1966

Thouiandl
1,126
1.812
1,385

Thoujattds
A.TX,
2,905
1,183

%
81
62
48

During the early period of the fishery, the
runs sustained a fishing mortality of more than
80''7 until 1919 when all runs to Bristol Bay
suff'ered a drastic decline. The universality of
this decline in many sockeye salmon systems
suggests that the causes must be sought in
changes in the environment and not in the mode
of fishing operation. The Nushagak runs never
returned to their former level, in contrast to
those of the other systems in Bristol Bay, notably
those to the Kvichak River.

During the middle period, here defined as the
time from 1925 to 1945, the amplitude of the
year-to-year oscillation increased (Figure 2).

Following the last World War, not only did
the Nushagak and other Bristol Bay sockeye
salmon runs decline, but many of the Kamchatka
.salmon runs did too (Krogius and Krokhin,
1956). The widespread decline suggests again
that environmental and probably oceanographic
conditions not related to fishing depressed the
survival. In the third period of the Nushagak
fishery the runs remained at a very low level,
compared with levels of the two previous periods.

Concomitant with this stepwi.se decline in aver-
age yield, there has been a decrease of the re-
productive potential of the Nushagak sockeye
salmon runs. Whereas during the early period
of the Nushagak fishery, the runs were exposed
to an ex|)!oitation rate of nearly BO'';, during
the middle period of the Nushagak fishery, the
runs were exposed to an exploitation rate of
around 60%. During the last period, the exploi-
tation rate was around 50''; . largely set by the
regulation. The runs are maintaining them-
selves, but so far no substantial increase is
apparent.

Thus the rate of return per sjiawner has fallen
from five to less than three and finally to two
mature fish. As a result, there has been no in-
crease to former run levels in spite of the reduced

758

MATHISEN: NUSHAGAK SOCKEYE SALMON FISHERY

exploitation rates. This situation is in contrast
to the situation in the Fraser River, where the
removal of the Hell's Gate blockade and increased
escapements initiated almost an immediate in-
crease in the returns in some river systems.

Therefore, it remains for us to explore if any
changes have occurred in the Nushagak runs that
can explain the described reduction in reproduc-
tive potential.

DISCUSSION

No visible changes have taken place in the
Nushagak environment since fishing commenced
there before the turn of the century. Even today
there are no dams or any other obstruction to
the migrating salmon. The resident population
still remains so low that pollution problems or
any form of industrial waste are nonexistent.
Neither has the subsistence fishery increased in
volume and an estimated 30,000 or more of all
species are harvested today. Other freshwater
fishes were not or were lightly harvested until
recent years, when a recreational fishery for
trout and char has developed.

A sockeye salmon run to a watershed such as
the Nushagak District is made up of a great
number of races that difl'er in morphological
features, age structure, time and place of spawn-
ing, and reproductive rate. The most direct ef-
fect of overfishing would be the disappearance
of certain races, or at least a reduction in their
numerical size to the point where they cease
to be important contributors to the commercial
catches. If this were true, it could manifest it-
self on the spawning grounds after the various
races have segregated. The number of spawners
per unit of nursery area reflects the stock
strength on a spatial basis.

There are some river systems within the
Nushagak District with low spawning density
relative to that of others. For 1955-1962 the
average number of spawners per square kilom-
eter of lake rearing area in the Tikchik Lakes
was 280 and in Lake Nunavaugaluk 290. In
contrast, the spawning density in the Wood River
lakes was 2,340 fish per square kilometer of lake
rearing area and 4,360 fish in the Igushik system
(Burgner et al., 1969). There is no evidence

available to indicate that this was different in
the early history of the Nushagak fishery. While
there are relatively more 3-ocean fish in the
Tikchik runs than elsewhere in the Nushagak
system and hence a higher fishing mortality, the
scarcity of spawning beaches and streams pre-
cludes both here and in the Nunavagaluk system
the possibility of a large population prior to com-
mercial exploitation.

The possibility still remains that the individual
races may pass through the fishery at diff'erent
times and thereby be exposed to diff"erent fishing
rates. If this were so, one might expect to see
some shift in time when peak abundance oc-
curred. This was studied by plotting the dates
when 10, 50, and 90 ""^ of the commercial catches
were made (Figure 5). From 1895 to 1947, the
two first points were reached at the same time
aside from simultaneous year-to-year variations.
There are some indications in Figure 5 that
salmon were present longer in Nushagak Bay
in years prior to 1920, but when one considers
the exponential rate of departure to the spawning
streams from the fishing grounds, the larger total
runs dui'ing these years would account for such
a prolongation of the fishing season. Added to
this consideration is the fact that the canneries

'^^A.Ov-

' I II I I 1 I I I M M I I I 1 I I II I I I 1 M I I 1 1 I I I Tl ri I I I I I I I 1 M I II

(OO'OO'OO'oO'OOT)

'..,^.-, — .-~^^ — ^"^^-^^ — ^^^ ^— ^^

Year

Figure 5. — Data on which 10, 50, and 90% of the Nu-
shagak catch was made, 1895-1947. (Subsequent years
omitted since a progressively stricter curtailment of fish-
ing time prevented direct comparison with forrner years.)

759

FISHERY BULLETIN: VOL. 69. NO. 4

usually set production goals in this period and
extended fishing until these goals were reached.

As a result, one may conclude that 70 years of
intensive harvesting have not drastically affected
the timing of the Nushagak runs. All tagging
experiments conducted in Bristol Bay point to
a complete mixing of all races in the fishery and
exposure to the same fishing pressure in a spe-
cific river system (Smith, 1964; Mathisen, 1969;
Straty, 1969) . Thus there is very little evidence
of a differential rate of removal in time among
all the races that constitute the Nushagak sock-
eye salmon run. The only exception seems to
be the races bound for the Igushik system. Their
migration path follows the west side of Nushagak
Bay past Nichol's Spit. In earlier years when
the main fishing activities were concentrated
closer to the confluence of the Nushagak and
Wood Rivers than they are today, the fishing
pressure on the Igushik races during those years
was lower.

A differential fishing pressure could arise from
the selectivity of the gill nets if some Nushagak
races consisted primarily of 3-ocean fish while
in others 2-ocean fish predominated. Burgner
(1964) has pointed out the ])reponderance of 3-
ocean fish to the Tikchik as one example. How-
ever, if a diminution of such races were of any
real consequence, it must manifest itself in
changes of the age composition through the re-
corded history of the Nushagak fishery. The
figures in Table 9 are based on the age composi-
tion in the commercial catches. Because of the
larger net sizes used up to 1926, a bias is intro-
duced in favor of 3-ocean fish and only the last
two periods are directly comparable.

Throughout all years the majority of the fish
migrated to sea as age 1 smolts and returned in
somewhat the same proportion of 2- and 3-ocean

fish. Over the years one can notice a shift,
with less 3-ocean fish in the catches of males in
recent years. If similar data were available
for the escapement, and thereby of the total runs,
one would in all probability see more of a con-
trast in the shift from 3- to 2-ocean female fish,
especially in the years when mesh sizes were
larger than 5\U inches. A mesh size experiment
conducted in 1928 by the Bureau of Fisheries
illustrates this point. The log ratio of catches
made with nets of .51 o-inch and 6-inch mesh sizes
are plotted by centimeter groups in Figure 6
and form an expected straight line. The aber-
rant points toward the upper size range are due
to a much larger sampling error because of the
very few fish present at these sizes.

The essential element of an escapement is not
the total number of fish present but the poten-
tial egg deposition they represent. During the
first period of the Nushagak fishery, when net
sizes ranged from 6Vi to 5% inches, escapements
of the same numerical magnitude as in later
years must have represented a substantially
higher potential egg deposition since a much
higher proportion of 3-ocean females was in-
cluded in those escapements than in years with
.51/2-inch mesh size. On the average, 3-ocean
females produce 650 eggs more per female than
2-ocean fish. The mean fecundity of these two
groups are 3,639 and 4,290 eggs, respectively
(Mathisen. 1962).

This net selection has another, more intangible
aspect. Not only is fecundity greater in the
larger 3-ocean females, but egg size is also a
function of the size of the females (Mathisen,
1962). Thus there may be a higher survival of
the progeny in this case than from eggs pro-
duced by 2-ocean females in the same environ-
ment. This concern was expressed in 1927 by

Table 9. — Summary of age in the commercial catches of sockeye salmon in Nushagak.

Sei

Period

Age-groups

No. of
years

sampled

2-ocean

3-oceari

1.2

2.2

1

1.3 1

2.3

Others

Mile

1912-1919
I92S-1945
1946-1966

21.32
35.77
42.19

8.66
8.95
9.55

S7.08
48.16
40.77

11.11
5.38
4.12

1.83
1.59
3.37

6
18
21

21.98
44.82
51.74

68.19
53.54
44.89

Female

1912-1919
I92S-194S
1946-1966

27.1!

25.42
27.12

9.80
7.05
5.91

51.25
60.48

56.62

1108
4.97

5.57

0.76
1.43

4.78

6
18

21

36.91
32.47
33.03

62.33
65.45
62,19

760

MATHISEN: NUSHAGAK SOCKEYE SALMON FISHERY

7.0

SO-

SO

■5 «

c —

2.0-

to

T3

1.0-

0.7

•5 ""0.5

!0.3-

0.2-

0.1

I
50

I — I — r-

55

Total

1 — I — I — I — I — r

60
length (cm)

65

Figure 6. — Log ratio of catches made in Nusliagak, 1928,
by 6- and 5 y2-inch gill nets. Males and females combined
by centimeter groups.

tivity, by a shift to smaller net sizes over the
years which reduced the potential egg deposition
rather than the numerical size of the escape-
ments. Such an explanation would be most ap-
propriate for the transfer from the first to the
second major period of the Nushagak fishery in
1919. But this argument loses some strength
when other sockeye salmon systems outside
Bristol Bay are considered.

The given description of the Nushagak fishery
and reduction of reproductive rate are almost
identical to that described for the Karluk sock-
eye fishery by Rounsefell (1958) . A major por-
tion of the Karluk River catches were taken in
beach seines at the river mouth or in adjacent
traps, both of which are nonselective for size.
Gill nets never played a dominant part in harvest
of the Karluk sockeye salmon. In spite of the
absence of gear selective for size, a selection
from the middle part of the run was present
(Thompson, 1951).

The Chignik fishery offers another example.
Recently Dahlberg (1968) and others before him
have pointed out the almost identical catch
curves for the Chignik and Nushagak fishery.
In the Chignik fishery one can distinguish three
major production levels, and the relative posi-
tion of these are the same as observed in Nu-
shagak (Figure 7). The only difference is that
the fall from an initial high production level to
an intermediate one came a few years later,
1926-1927, in the case of the Chignik fishery.
Traps were for a long time the principal fishing

Gilbert, who wrote in a letter to Commissioner
H. O'Malley:

As a result of this screening process, we are selecting
for breeding purposes predominantly the younger or
less robust members of the colony, those that are
dwarfed by reason of early maturity or lack of growth
vigor. The effect of such continued breeding from the
least fit of the community must result, it would seem,
in the gradual impoverishment of the race and the
reduction in size and value of the individuals composing
it.

The inference may be made that the observed
shifts in run strength and productivity in Nu-
shagak are associated with changes in gear selec-

JOn

;6A-

18

32

16

.s.Chignik

<?) O) O^ Oi

O^ O) c^i ^ Oi ^h

I 35
09-

Figure 7. — Comparison of catches of sockeye salmon in
the Chignik and Nushagak fisheries. Curves smoothed
by a moving average of 5's.

761

FISHERY BLLI.ETIN: \0L. 69, NO. 4

gear at Chignik, later supplemented with seines,
which today are the only gear operated. Gill-
netting never became effective at Chignik be-
cause of the clear water there and the narrow
channel. But as in the case of the Karluk fishery,
there has been a selection and domination of
certain races (Dahlberg, 1968).

In three important sockeye-producing systems,
the historical development has been the same
and resulted in a continuous decline of return
per spawner. Dahlberg sees the cause as dif-
fei-ential fishing mortality on the Chignik Lake
and Black Lake races with an overfishing on the
latter ones. Rounsefell (1958) suspects the ef-
fect of predation and stabilization of predator
populations in the alisence of the former large
contrast between off and peak years as the prin-
cipal cause. The evidence presented for the
Nushagak fishery points to various effects of net
.selectivity as a major contributing factor.
Viewed by themselves, each of the presented e.\-
planations may appear i^lausible, but the almost
identical happenings in three unrelated systems
suggest that a common underlying cause also
may be operating.

In all three cases the decline started two dec-
ades or so after large-scale commercial harvest
had been in operation. Provided the initial rate
of reproduction remained the same the spawning
stock or the potential egg dei)osition was suffi-
cient to maintain the runs, or rebuild them after
stringent regulations were put into effect.

One might conclude that the primary produc-
tion of the nursery areas, which all are oligo-
trophic lakes in the three mentioned systems,
started a slow decline from the moment fishing
began, and the enrichment from salmon carcasses
was substantially reduced relative to the situ-
ation which pi'evailed prior to commercial
harvest.

Clearly, a hypothesis of this type cannot be
demonstrated from the data presented. Rather,
conclusive evidence must be sought from other
sources. One is descriptive and involves a study
of the sedimentation rates in prefishing years
and in recent ones from bottom cores. Great
changes in basic lake productivity should bo re-
flected in the yearly sedimentation rate of diatom
shells. Donaldson (1967) has demonstrated

that changes in escapement level are indicated
by phosphorus content of corresponding bottom
sediments.

Experimental evidence on the role of the bio-
genic enrichment from salmon carcasses can be
obtained from a lake fertilization similar in con-
tent, volume, and mode of dispersion to that
])rovided by the dying spawners themselves.

ACKNOWLEDGMENTS

The basic data for this paper were assembled
in 1961-1963 under Contract No. 14-17-0007-20
with the Bureau of Commercial Fisheries. The
author acknowledges with thanks a valuable re-
view of the manuscript by Dr. C. DiConstanzo
and many fruitful discussions with Dr. R. L.
Burgner, Director of the Fisheries Research In-
stitute, and with my colleagues, Drs. D. E. Rogers
and B. J. Rothschild.

LITERATURE CITED

Batts, B. S., and K. J. FiscnLER.

1967. Historical data on the sockeye salmon runs
to NushaKak District, Bristol Bay, Alaska. Univ.
Wash., Fish. Res. Inst. Circ. 67-10, 6.3 p.

Beverton, R. J. H., AND S. J. Holt.

1957. On the dynamics of exploited fish populations.

Fish Invest. Minist. Agric. Fish. Food (G. B.),

Ser. II 19, 53.3 p.
Burgner, R. L.

1964. .Age composition of Nushagak red salmon.
Univ. Wa.sh., Fish. Res. Inst. Circ. 219, 62 p.

BtRGNER, R. L., C. J. niCoSTANZO, R. J. ELLIS, G. Y.

Harry, .Jr., W. L. Hart.man, O. E. Kerns, Jr., 0. A.
Mathisen, and W. F. Royce.

1969. Biological studies and estimates of optimum
escapements of sockeye salmon in the major river
systems in southwestern Alaska. U.S. Fish Wildl.
Serv., Fish. Bull. 67: 405-459.
Dahlberg, M. L.

1968. Analysis of the d>Tiamics of sockeye salmon
returns to the Chignik Lakes, Alaska. Ph.D.
Thesis, Univ. Washington, Seattle, 337 p.

Dixon, W. J.

1965. Biomedical computer programs. Revised ed.
Univ. California, Los Angeles, 620 p.

Donaldson, J. R.

1967. The phosphorus budget of Iliamna Lake,
Alaska, as related to the cyclic abundance of sock-
eye salmon. Ph.D. Thesis, Univ. Washington,
Seattle, 141 p.

762

MATHISEN: NL'SHAGAK SOCKEYE SALMON FISHERY

Gadai", E. L.

1966. Mineral study of the four lake systems in

the Nushagalv District of Alaska. M.S. Thesis,

Univ. Washington, Seattle, 229 p.
Gilbert, J. R.

1968. Surveys of sockeye salmon spawning popu-
lations in the Nushagak District, Bristol Bay,
Alaska, 1946-1958. Univ. Wash. Publ. Fish., New
Ser. 3: 200-267.

International North Pacific Fisheries Comjiission.

1962. The exploitation, scientific investigations and
management of salmon (genus Oncorlty^ichus)
stocks on the Pacific Coast of the United States
in relation to the abstention provisions of the
North Pacific Fisheries Convention, Vancouver,
Canada. Int. North Pac. Fish. Coram., Bull. 10:
1-160.

Kasahara, H.

1963. Catch statistics for North Pacific salmon.
Int. North Pac. Fish. Coram., Bull. 12: 7-82.

Koo, T. S. Y.

1962. Age designation in salmon. Univ. Wash.
Publ. Fish., New Ser. 1: 41-48.
Krogius, F. v., and E. M. Krokhin.

1956. Resultaty issledovanie biologii nerki-krasnoi,
sostoianiia ee saposov i kolebanii chislennosthi v
vodakh Kamchatki. Vopr. Ikhtiol. 7: 3-20.
Mathisen, 0. A.

1962. The efl^ect of altered se.x ratios on the spawn-
ing of red salmon. Univ. Wash. Publ. Fish., New
Ser. 1: 137-222.

1969. Tagging experiments in Bristol Bay, Alaska,
in 1946 and 1947. Univ. Wash., Fish. Res. Inst.
Circ. 69-1, 15 p.

Mathisen, O. A., R. L. Burgner, and T. S. Y. Koo.

1963. Statistical records and computations on red
salmon (Oticorhynchiis nerka) runs in the Nu-
shagak District, Bristol Bay, Alaska, 1946-1959.
U.S. Fish Wildl. Serv., Spec. Sci. Rep. Fish. 468,
32 p.

Moser, J. F.

1902. Alaska salmon investigations in 1900 and
1901. In Annual bulletin of the Commissioner of
Fish and Fisheries for 1901, p. 173-398.
Rich, W. H., and E. M. Ball.

1928. Statistical review of the Alaska salmon fish-
eries. Part I. Bristol Bay and the Alaska Penin-
sula. Bull. U.S. Bur. Fish. 44: 41-95.

ROUNSEFELL, G. A.

1958. Factors causing decline in sockeye salmon
of Karluk River, Alaska. U.S. Fish Wildl. Serv.,
Fish. Bull. 58: 83-169.
RUYCE, W. F.

1965. Almanac of Bristol Bay sockeye salmon.
Univ. Wash., Fish. Res. Inst. Circ. 235, 48 p.
S.MITH, H. D.

1964. The segregation of red salmon in the escape-
ments to the Kvichak River system, Alaska. U.S.
Fish Wildl. Serv., Spec. Sci. Rep. Fish. 470, 20 p.

Straty, R. R.

1969. The migratory pattern of adult sockeye
salmon (OncorJiynchiis nerka) in Bristol Bay as
related to the distribution of their home-river
waters. Ph.D. Thesis, Oregon State Univ., Corval-
lis, 243 p.
Thompson, W. F.

1951. An outline for salmon research in Alaska.
Univ. Wash., Fish. Res. Inst. Circ. 18, 49 p.

763

CHANGES IN CATCH AND EFFORT IN THE ATLANTIC MENHADEN

PURSE-SEINE FISHERY 1940-68

William R. Nicholson'

ABSTRACT

The catch, number of vessel weeks, and catch per vessel week in the Atlantic menhaden fishery increased
during the 1950's. During this period fishing methods improved and the efficiency of vessels increased.
Improvements included use of airplanes for spotting schools, aluminum purse boats, nylon nets, power
blocks, and fish pumps for catching and handling fish, and larger and faster carrier vessels that could
range farther from port. The catch and catch per vessel week began declining north of Chesapeake Bay
in the early 1960's. By 1966, fish north of Chesapeake Bay had become so scarce that plants either
closed or operated far below their capacity. In Chesapeake Bay the number of vessel weeks increased,
and the catch and catch per vessel week decreased through the early and mid 1960's. Variations in
catch, effort, and catch per unit of effort showed no trends in the South Atlantic. The annual mean
number of purse-seine sets per day varied in different areas and ranged from about 2.0 to 4.5. The
annual mean catch per set ranged from about 11 to 25 metric tons.

Catch and effort statistics are important in eval-
uating and managing any fishery. They may be
used in measuring changes in actual or apparent
abundance, estimating population sizes and mor-
tality rates, and determining optimum fishing
rates.

When investigations of the Atlantic menhaden
(Brevoortia tyrannus) fishery were begun in
1955 by the Bureau of Commercial Fisheries,
provisions were made for collecting and com-
piling catch and effort statistics. The number
and locations of daily purse-seine sets were ob-
tained from logbooks placed aboard vessels at
the beginning of the fishing season, and daily
catches of individual vessels were copied from
plant records.

The objectives of the present study were:
(1) to analyze logbook data and vessel landing
records to determine differences and changes in
the number of purse-seine sets, mean number
of sets per day, and the mean catch per set, both
between and within geographical divisions of the
fishery, (2) to develop a method of measuring
fishing effort, and (3) to document changes that
have occurred in the fishery.

' National Marine Fisheries Service, Center for Est-
uarine and Menhaden Research, Beaufort, N.C. 28516.

Manuscript accepted April 1971.

FISHERY BULLETIN: VOL. 69. NO. 4, 1971.

BRIEF HISTORY OF THE FISHERY

Atlantic menhaden are found from central
Florida to Nova Scotia and at one time or an-
other have been exploited over most of this
range. Fishing began in the early part of the
19th century in waters off Massachusetts and
Maine. Following improved methods of fishing,
extracting oil, and processing meal, the fishery
expanded in this area in the latter part of the
19th century. When the scarcity of menhaden
in waters north of Cape Cod caused the collapse
of the fishery in that area, about 1895, the in-
dustry shifted to the Middle and South Atlantic
coast. By the 1930's processing plants were lo-
cated in approximately the same areas where
they occur today (Figure 1).

Although in some areas pound nets capture
menhaden incidentally with other species, purse
seines catch nearly all of the fish that are reduced
for meal and oil.

Purse seining began in the late 19th century
and by present standards was inefficient and la-
borious. Purse boats were rowed and carrier
vessels were sailed. Gradually, sailing vessels
were replaced by larger, coal burning steam
ships, purse boats were equipped with gasoline

765

FISHERY BULLETIN: VOL. 69, NO. 4

enjjines, and seines were made larger. Follow-
ing World War I, diesel and gasoline engines
gradually replaced steam engines in the carrier
vessels. Methods of catching and processing
menhaden, however, changed very little between
World Wars I and II.

After World War II the increased demand for
fish meal and oil initiated changes in the industry.
Numl)ers and sizes of vessels increased, methods
of fishing changed, ])rocessing facilities expand-
ed, and processing efficiency increased.

A major change in fishing methods occurred in
194(3 when airplanes were introduced to locate
concentrations of fish. Plant operators found
this practice so successful that they rapidly added
more planes in following years (Table 1). In-
itially, airplanes scouted wide areas and directed
vessels to places where menhaden were abundant.
Later, after captains wei'e given portable radios,
the airplane pilot directed the actual setting of
the net. Since about 1950 airplanes have been
an inte.gral part of fishing operations (Robas,
1959; June, 1963).

Fish inimps, initially installed on carrier ves-
sels in 1916, were the first significant advance

Table 1. — Number of airplanes used in the Atlantic
menhaden fishery.^

Figure 1. — Ports and major fishins areas, Atlantic men-
haden fishei-y.

Year

Norlh

Middle

Chesapeoke

South

Total

Atlontic

Atlantic

Bc3y

Atlantic

1945

0

0

0

0

0

1946

0

1

0

2

1947

0

7

2

10

1948

1

8

2

12

1949

1

11

2

15

1950

1

10

3

15

1951

1

10

3

15

1952

2

11

4

18

1953

4

11

4

20

1954

4

12

3

4

23

1955

5

15

5

4

29

1956

6

15

8

4

33

1957

8

15

9

4

36

1958

8

17

10

4

39

1959

7

17

12

5

41

1960

5

16

7

4

32

1961

6

16

8

4

34

1962

6

16

9

3

34

1963

5

16

11

3

35

1964

4

18

13

4

39

1965

3

6

18

4

31

1966

1

4

18

4

27

1967

0

2

16

4

22

1968

1

2

16

4

23

a Exact dota ore not availoble for the North Carolina fall fishery.
Estimates indicate that 20 to 25 were used each year after about 1955.

766

NICHOLSON: ATLANTIC MENHADEN TURSE-SEINE FISHERY

in fishing methods after World War II (Robas,
1959). Pumping fish directly from the purse
seine to the hold replaced the time-consuming
method of brailing and left more time for scout-
ing and making additional sets. By 1955 nearly
all vessels were equipped with fish pumps
(Table 2).

Before fish in the seine can be pumped or
brailed aboard the carrier vessel, they must be
concentrated, or "hardened-up." This can be
done by crewmen in the purse boats pulling in
the net by hand, but it is a laborious process that
requires approximately 22 men. A mechanical

Table 2. — Percent of vessels equipped with fish pumps
and power blocks in the Atlantic menhaden purse-seine
fi.shorv.

Middle

^tlantic^

Chesapeake Bay

South Atlantic

Year

Fish
pumps

Power
blocks

Fish
pumps

Power
blacks

Fish
pumps

Power
blacks

1946-49

0

0

10-20

0

0

0

1950

6

0

24

0

0

0

1951

13

0

25

0

0

0

1952

32

0

31

0

0

0

1953

44

0

22

0

9

0

1954

43

0

25

0

10

0

1955

81

0

90

0

11

0

1956

78

2

92

0

23

0

1957

91

2

88

16

23

0

1958

96

100

100

57

25

0

1959

100

100

100

68

45

0

1960

100

100

100

95

45

0

1961

100

100

100

74

45

0

1962

100

100

100

66

50

31

1963

100

100

100

83

69

31

1964.68

100

100

100

100

64-74

42-69

a Includes Amogansett from North Atlantic Area,

device, or "power block," for "drying-up" the net,
used experimentally in 1955, became operational
in 1956 (Schmidt, 1959a). Its use reduced the
crew by 6 to 10 men and the average time to
"harden-up" the fish by about 6 min (Schmidt,
1959a, 1959b), and enabled the crew to retrieve
the net quickly if the fish were missed. Power-
blocks were used extensively for the first time
in 1958 and by 1966 were installed on nearly all
vessels from Long Island southward (Table 2).

Large sets are sometimes lost when the net
cannot be raised manually or mechanically to
concentrate the fish so that they may be pumped.
But the pump head, if positively charged with
electricity, becomes an electrode that attracts and
concentrates menhaden without the necessity of
raising the bunt (Kreutzer 1959). Such a de-
vice, commonly called a "fish shocker," was first
installed on vessels in 1956, but its use did not
spread beyond the Middle and North Atlantic
areas. By 1966 it had fallen into disuse
(Table 3).

Beginning in 1954, nylon nets gradually re-
placed cotton or linen nets (Table 3) . Although
moi-e expensive initially, nylon nets last longer
and do not split or tear when filled with fish
as other nets sometimes do.

Aluminum purse boats began replacing wood-
en purse boats in 1957 (Table 3) . Being lighter,
more maneuverable, and more stable than wood-
en boats, they can encircle a school of fish easier

Table 3. — Percent of vessels equipped with fish shockers, nylon nets, and aluminum purse boats in the Atlantic

menhaden purse-seine fishery.

Middle Allcjntic

a

Chesapeake Bay

South Atlantic

Year

Fish
shockers

Nylon
nets

Aluminum

purse
boats

Fish
shockers

Nylon
nets

Aluminum
purse
boots

Fish
shockers

Nylon

nets

Aluminum
purse
boots

1954

0

2

0

0

0

0

0

0

0

1955

0

5

0

0

0

0

0

0

0

1956

47

19

0

0

4

0

0

0

0

1957

45

18

0

0

44

0

0

13

0

1958

85

100

66

0

82

4

0

14

0

1959

85

100

85

0

94

23

0

20

0

1960

82

100

82

0

100

32

0

45

0

1961

82

100

82

0

100

30

0

58

0

1962

82

100

89

0

100

63

0

81

33

1963

82

100

100

0

100

83

0

100

50

1964

78

100

100

0

100

100

0

100

50

1965

86

100

100

0

100

100

0

100

58

1966

0

100

100

0

100

100

0

100

69

1967

0

100

100

0

100

100

0

100

100

1968

0

100

100

0

100

100

0

100

100

a Includes Amogansett from North Atlantic Area.

767

FISHERY BULLETIN; VOL. 69, NO. 4

and faster, and can operate more easily in rough
seas.

Three jet-propelled purse boats were intro-
duced in 1962. Adjustable jet nozzles on each
end gave the boats e.\cellent maneuverability,
and there was no propeller or guard to entangle
nets. They lacked the power to close up the seine
rapidly, however, and were abandoned.

With the exception of airplanes for spotting,
none of the improvements were adopted by ves-
sels in the Point Judith, Gloucester, or Portland
fleets. All vessels fishing from these ports were
small to medium-sized otter trawlers that were
converted to purse seining for only about 2
months during the summer.

DESCRIPTION OF THE FISHERY

The purse-seine season for menhaden extends
from late spring through fall, but the time varies
in different localities. South of Cape Hatteras,
N.C., it begins in April or May and lasts until
late December or early January. From Chesa-
peake Bay to the southern shore of Long Island
it begins in late May and usually ends about the
third week in October. North of Cape Cod the
season lasts only from about late June to early
September.

To facilitate summarizing and discussing an-
nual changes in the fishery, June and Reintjes
(19.59) divided the range of Atlantic menhaden
into four areas, the North Atlantic, Middle At-
lantic, Chesapeake Bay, and South Atlantic (Fig-
ure 1). Although the boundaries are arbitrary,
they were drawn to take advantage of natural
separations in the fishing areas. Similarities
in age and size composition of the catches, time
and duration of fishing, and range of vessels from
the home port tended to .set each area apart.
The North Carolina fall fishery, a specialized
fishery that occurs only during November and
December from Cape Hatteras to Cape Fear, is
distinct from the summer fishery in the South
Atlantic and was treated as if it were an area.
This classification, which jirovides a convenient
way of expressing statistics of the fishery, is used
in the present analysis. Poits in the South At-
lantic area are Fernandina Beach, Fla.; Yonges
Island, S.C; and Southport and Beaufort, N.C.;

in the Chesapeake Bay area — Reedville, Va.; in
the Middle Atlantic area, Lewes, Del.; and Wild-
wood, Tuckerton, and Port Monmouth, N.J.; in
the North Atlantic area — Amagansett, N.Y.;
Point Judith, R. I.; Gloucester, Mass.; and Port-
land, Maine; and in the North Carolina fall fish-
ery— Beaufort and Morehead City, N.C.

A disadvantage of the fishery area concept is
that all of the fish landed at a port in a partic-
ular area may not have been caught in that area.
The problem is not serious, however, because ves-
sels seldom fish in areas other than the one in
which their home port is located. Port Mon-
mouth vessels, which sometimes go through the
East River to fish in western Long Island Sound,
and Amagansett vessels, which sometimes fish
ofl" the northern New Jersey coast, contradict this
general lule more often than do vessels at other
ports.

The number and location of daily purse-seine
sets each year from 19.5.5 to 1966 were obtained
from logbooks placed aboard vessels at the be-
ginning of each fishing season. Port samplers
were instructed to pick up cojiies of each page
every 2 weeks, answer questions pertaining to
the methods of keeping the logs, and stimulate
interest of the pilots to keep the logs complete
and up to date. From 25 to 100 '^r of the boats
fishing at each port kept logs. Although gen-
erally over 60 ''r of the fleet was covered each
year, many vessels did not keep complete records.

Daily landings of each vessel were copied from
plant records. Although some records extended
back as far as 1912, records at most plants were
not available for years prior to 1940.

ANNUAL CATCH

No trends were evident in the annual catches
in the South Atlantic area or North Carolina
fall fishery, but the catches in the other three
areas i-eflected an increase in fishing effort after
1945 and a decline in abundance after 1956
(Table 4). After reaching a peak in 1956 of
378,300 metric tons in the Middle Atlantic area
and 98,500 tons in the North Atlantic area, the
catch declined to 6,000 and 1,800 tons, respec-
tively in 1966. In the Chesapeake Bay area the
catch decreased from 196.800 metric tons in

768

NICHOLSON: ATLANTIC MENHADEN PURSE-SEINE FISHERY

1959 to 115,600 tons in 1966. In the North At-
lantic area, the Point Judith, Gloucester, and
Portland fleets, which began menhaden fishing
about 1949, accounted for most of the increases
between 1950 and 1960. Menhaden were not
landed at Portland after 1957 or at Gloucester
and Point Judith after 1962.

CALCULATION OF FISHING EFFORT

In any searching fishery where the sizes and
types of vessels vary, the unit of fishing effort
is diflncult to define. Marr (1950) found a pos-
itive linear relation between mean catch per boat
week and boat length in the Pacific sardine
{Sardlnoi)s sagax) fishery off Oregon. He se-
lected the modal boat-length group as a standard,
calculated the catch per boat week of boats in
this group for each year, and based his estimates
of apparent abundance on this index. He was
unable, however, to estimate total effort except

by dividing the total catch of all vessels by the
catch per unit of the standard group.

Silliman and Clark (1945), studying the Pa-
cific sardine fishery off California, linked groups
of identical vessels and estimated apparent
abundance from the catch per boat week of these
groups. They estimated the total effort by di-
viding the total catch by the catch per boat week
of the linked grouji, assuming that the catch per
boat week of the selected vessels was represent-
ative of the catch per boat week of the fleet, and
using a base season for each of the three areas
they studied. Recognizing the effect of differ-
ences in vessel size on catch per unit of effort,
they used a standard multiple regression to esti-
mate total effort in each area by relating in a
single equation the length and horsepower of each
vessel, the number of vessels, and the number of
weeks.

Clark and Daugherty (1950) extended the
study by Silliman and Clark through the 1948-49

Table 4. — Atlantic menhaden purse-seine catch by year and area.

North
Atlantic

Middle
Atlantic

Chesapeoke
Bay

South
Atlantic

North Corolino
fall fishery

Total

1940

16.8

91.1

— — — thouiands oj metric tons

35.3 37.9

36.6

217.7

1941

33.5

104.1

60.2

45.2

34.9

277.9

1942

14.6

77.7

21.9

32.9

20.1

167.2

1943

9.8

96.S

42.1

59.7

28.8

237.2

1944

27.5

122.6

32.2

46.9

28.7

257.9

1945

34.0

136.4

35.1

58.5

31.9

295.9

1946

42.9

183.8

57.6

40.8

37.3

362.4

1947

44.2

185.8

81.2

34.2

329

378.3

1948

44.4

137.4

68.3

55.8

40.6

346.5

1949

52.2

149.8

62.8

59.3

39.7

363.8

1950

49.3

143.0

63.1

20.0

21.8

297.2

1951

510

168.6

56.1

54.6

31.1

361.4

1952

58 1

193.7

45 7

86.0

26.4

409.9

1953

59.7

363.2

77.8

52.8

39.7

593.2

1954

64.9

335.7

126.0

39.6

41.9

608.1

1955

83.3

317.6

132.7

43.4

644

641.4

1956

98.5

378.3

94.0

68.6

72.7

712.1

1957

83.5

304.5

126.4

36.4

52.0

602.8

1958

36.0

211.1

151 3

41.3

70.3

510.0

1959

66.0

250.9

196.8

63.1

82.3

659 1

1960

66.4

256.0

108.5

36.7

62.2

529.8

1961

58.6

274.6

128.7

44.1

69.9

575.9

1962

64.7

249.9

155.1

42.2

25.8

537.7

1963

35.2

111.7

104.0

34.2

62.8

347.9

1964

15.0

3S.2

134.1

46.5

38.4

269.2

1965

119

45.8

126.1

36.7

52.9

273.4

1966

1.8

6.0

115.6

24.5

71.7

219.6

1967

0

17.1

911

34.1

51.2

193.5

1968

6.7

26.2

115.5

33.6

52.8

234.8

769

FISHERY BULLETIN: VOL. 69, NO, 4

season. They also used linked groups of vessels,
but simplified calculations by using catch per
lunar month rather than catch per week.

June and Reintjes (1957), studying the men-
haden fishery off Delaware Bay, used the linkage
method to determine the catch per boat week
for selected boats from 1939 to 1953. They esti-
mated the total number of boat weeks by dividing
the total catch by the catch per boat week.

In the yellowfin tuna (Thunmis albacares)
bait-boat fishery in the eastern tropical Pacific,
Shimada and Schaefer (1956) grouped vessels
by carrying capacity. They computed the catch
per days absence from port for each grouji and
established one group as a standard. They
standardized effort by dividing the catch per days
absence of the standard group by the catch per
days absence of each other group. Broadhead
(1962) related the catch per day of bait boats to
the catch per day of purse-seine vessels by using
regression analysis.

Menhaden i^lant records, while showing the
date and amount of fish landed by each vessel,
do not list days when vessels fish and catch
nothing, and do not indicate whether a catch
represents 1 or more days' fishing. While ves-
sels generally land their catch daily, quite often
in the Middle and North Atlantic areas they
land 2 or 3 days' catch at one time, particularly
in late spring and early fall, a jjractice which
has increased in recent years as fish have become
scarce and daily catches smaller.

There is no satisfactory way of getting the
complete daily history of each vessel. Even if
port samplers recorded each vessel's daily ac-
tivity, the records still would be incomplete be-
cause not all ports are sampled and because no
ports were sampled prior to 1955. Logbook
records also are incomjilete. Any eflFective meth-
od of measuring efl!'ort. therefore, must use ves-
sel landings as they are recorded at the plants.

Fortunately, menhaden vessels generally op-
erate continuously throughout all or part of the
fishing season and fish every day that weather
permits, unless in port for repairs. Except in
the North Carolina fall fishery, which lasts only
6 to 8 weeks, the number of days that had weather
I)rohil)its menhaden fishing is relatively small
and is relatively constant from year to year.

Any time period, therefore, that assumes con-
tinuous fishing and accounts for unproductive
fishing days should be a satisfactory unit of basic
fishing effort. Because the vessel week satisfies
these conditions and may be readily computed,
it was selected as the basic unit.

Because variations in the catch per unit of
effort among vessels may necessitate ad.justing
the basic unit to a common standard, the rel-
ative efficiency of vessels fishing from each port
was examined.

No clear correlation could be shown between
catch per week and vessel length or weight, so
the relation between mean catch per week and
vessel carrying capacity was explored. Carry-
ing capacity, determined for each vessel by aver-
aging the 10 largest catches for 3 consecutive
years, ranged from about 100 to 350 short tons
(90-317 metric tons). Vessels were grouped,
according to their carrying capacity in short
tons, into six cla.sses:

Class

1
2
3

4
5

6

Carrying capacity

<141
141-180
181-220
221-260
261-300

>300

The relative efficiency of vessels at each port
was examined by plotting the mean catch per
week of each vessel and by plotting the catch
lier week against carrying capacity.

In the South Atlantic area all vessels were
class 3 at Fernandina Beach, Yonges Island, and
Southiiort. and class 1 or 3 at Beaufort. Vari-
ation in the catch per week among vessels was
evident at all jjorts, but there was no distinct
tendency for any group to have larger or smaller
catches per week than another.

Until about 1963 nearly all vessels in Ches-
apeake Bay were class 3, although a few were
class 2, 4, or 5. After 1961 the number of class
5 vessels increased. Although the large capacity
vessel tended to have greater mean catches per
week than small capacity vessels, the variation
was extreme among all vessels, both between and
within years. As the catch per week declined
after 1 961 , the variation between vessels of small
and large capacities decreased.

770

NICHOLSON; ATLANTIC MENHADEN PURSE-SEINE FISHERY

In the Middle Atlantic area vessels ranged
from class 2 to 6, but no more than two classes
occurred at any port. At Port Monmouth and
Tuckerton, class 6 vessels did not show sub-
stantially greater catches per week than class 5
vessels. Class 5 vessels at Lewes clearly had
greater catches per week than class 3 vessels,
while class 5 vessels at Wildwood had greater
catches per week than class 2 vessels.

Because the increases in the catch per vessel
week that accompanied the increases in vessel
carrying capacity were small and inconsistent
and the variability between ports was great, no
vessel class was designated as a standard for the
fishery. Effort was simply left unadjusted at
all excejst five ports — Lewes, Wildwood, Point
Judith, Gloucester, and Portland.

Effort at Lewes and Wildwood was adjusted
because the differences in the catch per unit of
effort between the two classes at each port were
large. At these ports the 10-year mean of the
ratio of the catch per week of the group of larger
vessels to that of the group of smaller vessels
was computed for 1950-59. Annual effort of
the smaller vessels was adjusted by multiplying
the total number of weeks fished each year by
the mean ratio, 0.610 for Wildwood and 0.573
for Lewes.

Efl^ort at the other three ports was adjusted
because many of the vessels, which were small
to medium-size otter trawlers temporarily con-
verted to purse seinei's during the summer, fished
intermittently, usually only when menhaden were
plentiful. Because effoi't could not be measured
very precisely under these conditions, it was esti-
mated in terms of Amagansett units by dividing
the annual catches at these ports by the mean
catch per week of Amagansett vessels.

Most menhaden vessels were class 3, 4, or 5.
At most ports the relative proportions of one
class to another changed very little each year and
the number of vessels remained fairly constant
(Table 5). LTnder such conditions the number
of vessel weeks, with minor adjustments, was
as precise an estimate of total fishing effort as
was possible to obtain. Various other adjust-
ments might have been made, but with doubtful
improvement in the overall estimate of fishing
effort.

Henceforth, vessel weeks will refer to units of
fishing eflfort and will include these adjustments.

NUMBER OF VESSEL WEEKS

After World War II ended in 1945, the number
of vessel weeks rose shar]5ly in the Chesapeake
Bay, Middle Atlantic, and North Atlantic areas
(Table 6) . The increase resulted from the addi-
tion of vessels in all areas and from an increase
in the number of weeks that plants in the North
and Middle Atlantic operated.

After 1959 in the North Atlantic and 1962 in
the Middle Atlantic, the number of vessel weeks
droi)iied sharjjly. Much of the deci'ease in the
North Atlantic between 1959 and 1962 can be
attributed to a reduced number of converted
trawlers at Portland, Gloucester, and Point Ju-
dith, where no menhaden were landed after 1962.
After 1962 the number of vessels at Amagansett
also declined. Reduced effort in the Middle At-
lantic after 1962 was due to a decrease in the
number of vessels. The Tuckerton plant and one
of the Lewes plants closed during the 1964 season
and never reopened. The Wildwood plant op-
erated only a few weeks each year after 1964,
and the boats were transferred to plants in Ches-
apeake Bay. The remaining plant at Lewes
closed after the 1965 season.

Effort in the Chesapeake Bay area fluctuated
between approximately 300 and 400 vessel weeks
from 1944 to 1954; thereafter it generally in-
creased (except when fishing was restricted in
1960 because of a poor market) until about 800
vessel weeks were reached in 1964-66. Addi-
tional vessels accounted for most of the increase
through 1963. In 1964-68, fishing terminated
approximately 7 weeks later (mid-November)
than in pi-evious years.

Ill the South Atlantic area, effort fluctuated
between 245 and 530 vessel weeks from 1941
to 1968. Although some fluctuation was due to
variation in the length of the fishing season, par-
ticularly in Florida, most was due to variations
in the number of vessels. The annual number of
vessels, and vessel weeks, generally was less from
1960 to 1968 than in previous years.

In the North Carolina fall fishery, the number
of vessel weeks varied from 97 to 457 and

771

FISHERY BULLETIN: VOL. 69, NO. 4

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772

NICHOLSON: ATLANTIC MENHADEN PURSE-SEINE FISHERY

Table 6.-

—Number of vessel weeks per season in the Atlantic menhaden fishery,
by year and area.

Area

Year

North
Atlantic

Middle
Atlantic

Chesapeake
Bay

South
Atlantic

North
Corolina

fall
fishery

Total

1940

a

337

329

a

a

a

1941

141

392

417

506

227

1,683

1942

89

323

251

376

194

1,233

1943

49

287

202

419

166

1,123

1944

84

397

296

316

224

1,317

1945

89

477

302

394

234

1,496

1946

132

528

294

343

291

1,588

1947

134

552

4)8

322

333

1,759

1948

130

675

405

430

288

1,928

1949

156

691

385

473

457

2,162

1950

155

614

403

322

187

1,681

1951

157

676

369

379

222

1,803

1952

150

580

333

474

220

1,747

1953

161

819

376

474

244

2,074

1954

189

838

408

488

262

2,185

1955

334

890

451

475

342

2,492

1956

298

888

466

530

391

2,573

1957

262

949

527

412

311

2,461

1958

227

734

559

354

380

2,254

1959

301

897

668

474

312

2,652

1960

280

854

410

292

163

1,999

1961

249

946

482

395

224

2,296

1962

264

990

582

327

97

2,260

1963

238

823

666

264

286

2,277

1964

134

376

803

277

249

1,839

1965

96

300

786

359

259

1,800

1966

79

87

795

254

220

1,435

1967

0

124

757

253

212

1,346

1968

23

113

601

245

246

1,228

a Records not available.

depended primarily on the number of vessels,
the season generally lasting about 7 or 8 weeks.

CATCH PER VESSEL WEEK

Despite sharp fluctuations that occurred an-
nually, there were pronounced trends in the
catch per vessel week in three areas (Table 7).
In the North Atlantic area, the catch per vessel
week remained at a high level through 1957,
dropi)ed sharply in 1958 and continued to decline
thereafter. From a peak of 385 metric tons per
week in 1952, it dropped to 23 in 1966. The high
figure for 1968 (292) reflects the fact that two
vessels, one fishing from late June until mid-
October and another during August and early
September, caught most of the fish available.

The most significant changes occurred in the
Middle Atlantic and Chesapeake Bay areas.
From 348 metric tons per week in 1946, the

catch per vessel week in the Middle Atlantic area
dropped to 203 in 1948, and thereafter rose
steadily, attaining 444 tons in 1953. From 1954
to 1957 It remained high, between 320 and 426
tons. Between 1958 and 1961, it declined rela-
tive to the previous 4 years, but still remained
between 279 and 299 tons. It dropped to 253 tons
in 1962, and 70 tons in 1966. By contrast, the
catch per vessel week in the Chesapeake Bay area
was low from 1943 to 1953, fluctuating between
109 and 207 tons, and high from 1954 to 1962,
fluctuating, except for 1956, between 239 and
309 tons. In 1963 the catch per week dropped
to 156 tons and then continued a downward
trend.

In the South Atlantic the catch per vessel week
showed no trends. The figures generally ranged
from about 86 to 136 metric tons, with extreme
fluctuations of from 39 to 180 tons.

In the North Carolina fall fishery the catch
per vessel week from 1941 to 1954 fluctuated

773

FISHERY BULLETIN: VOL. 69, NO. 4

Table 7. — Mean catch of Atlantic menhaden per vessel week, in metric
tons, Atlantic menhaden fishery.

Area

Yeor

North
Atlantic

Middle
Atlontic

Ctiesopeoke
Boy

South
Atlantic

North
Corolino

fall
fishery

1940

a

273

107

a

a

1941

237

266

144

89

154

1942

164

240

88

88

104

1943

200

337

208

142

173

1944

327

309

109

149

123

1945

383

286

116

148

136

1946

325

348

196

119

128

1947

329

336

194

106

93

1948

342

203

169

130

141

1949

335

217

163

125

87

1950

313

233

157

62

117

1951

325

249

137

144

140

1952

387

333

136

181

120

1953

371

444

207

111

162

1954

343

401

309

81

16C

1955

249

357

294

91

188

1956

330

426

201

130

186

1957

319

320

239

88

167

1958

159

288

270

117

185

1959

219

279

295

133

263

1960

237

299

265

126

381

1961

235

290

267

111

312

1962

245

253

267

129

266

1963

148

135

156

130

220

1964

112

93

167

168

154

1965

124

152

161

102

203

1966

23

69

145

96

326

1967

0

138

121

135

241

1968

292

232

192

137

215

a Records not available.

between 87 and 173 metric tons and averaged
132 tons, and from 1955 to 1968 fluctuated be-
tween 156 and 381 and averaged 239 tons. The
increased use of airplanes and other improve-
ments in fishing methods, rather than any in-
creases in the al)undance of menhaden, probably
were responsible for the large catches per vessel
week in the later years.

While the catches per vessel week were lower
for ports in the South Atlantic area than for
ports in the Middle Atlantic, the variation be-
tween ports in each area was of about the same
magnitude (Table 8). In the South Atlantic
the figures for Southport and Fernandina Beach
were about ecjual to each other but higher than
for Beaufort. In the Middle Atlantic the catch
per ves.sel week usually was highest at Tuckerton.

The monthly catch-per-vessel-week figures
were computed for each area, but they showed
no consistent trends or variation worth noting.

NUMBER OF PURSE-SEINE SETS

The number of purse-seine sets was estimated
from logbooks and reduction plant i-ecords by
the formula:

S,

L,(S^ U)

where:

St = number of estimated monthly
sets,

Si = number of sets from logbooks,

Li = number of days for which num-
ber of sets is known,

Lt = total number of landings days
from plant records.

Vessels at each port were stratified by months
and by loading capacity, on the assumi)tion that
the number of sets per day varied with both
lime and capacity. The number of monthly
sets was estimated for vessels in each stratum.

774

NICHOLSON: ATLANTIC MENHADEN PURSE-SEINE FISHERY

Table 8. — Mean catch of Atlantic menhaden per vessel week, in metric tons, landed at ports in the South and

Middle Atlantic areas.

Fernandina
Beach, Flo., and
Yonges Is., S.C.

Southport,
N.C.

Beaufort,
N.C.

Lewes,
Del.

Wildwood.
N.J.

Tuckerton,
N.J.

Port

Monmouth,

N.J.

1940

a

73

27

255

165

b

318

1941

106

88

36

292

211

b

257

1942

109

84

34

261

243

b

217

1943

170

119

51

337

309

b

344

1944

170

148

107

319

269

b

302

1945

134

164

97

331

309

198

256

1946

121

181

80

413

331

306

278

1947

73

180

103

382

234

343

252

1948

129

158

118

189

210

216

226

1949

78

207

no

238

200

213

186

1950

71

54

57

256

164

270

188

1951

193

82

70

266

140

279

233

1952

247

154

75

367

177

412

259

1953

140

98

75

444

505

524

374

1954

100

93

72

433

359

457

327

1955

85

107

80

404

333

433

253

1956

138

148

103

436

346

518

399

1957

86

104

73

301

255

368

377

1958

63

193

74

366

268

221

194

1959

194

161

70

301

253

252

273

1960

184

143

86

346

259

278

259

1961

157

132

64

332

259

258

258

1962

180

133

92

247

240

254

269

1963

149

108

127

115

150

137

155

1964

129

227

140

34

80

61

56

1965

105

137

69

131

103

b

187

1966

137

67

72

50

238

b

48

1967

173

172

192

b

171

b

122

1968

122

260

189

b

175

b

261

a Records not avo

lable.

b Plant closed.

Monthly totals at each port were obtained by
summing the estimates for each stratum, sea-
sonal totals by summing- the monthly estimates,
and ai'ea totals by summing the totals of each
port. The mean number of sets per day for
either month or season was calculated by di-
viding the total number of estimated sets by the
total number of fishing days.

Because of the difficulty of maintaining good
logbook records in recent years, the analysis
was not continued beyond 1966. By that time
little fishing was done north of Chesapeake Bay.

At ports where more than one size class of
vessels fished, the larger vessels generally aver-
aged slightly more sets per day than the smaller
ones (Table 9). The differences were greater
at ports where the vessel classes were not adja-
cent (Lewes and Wildwood) than they were at
ports where the vessel classes were adjacent
(Amagansett, Port Monmouth, and Tuckerton) .
Because data were insufficient to calculate the

mean catch per set for each vessel class in Ches-
apeake Bay, the data were combined for classes
2 and 3, and 4 and 5. After 1964 the lack of
data made meaningful comjjarisons impossible.

The slightly greater mean number of sets per
day for the larger vessels may reflect the ability
of these vessels to steam faster and range farther
from their home port, and to carry more fish
when fully loaded. More than likely, these fig-
ures reflect the ability and aggressiveness of the
vessel captains, since the better ones generally
are assigned to the larger vessels.

The annual or monthly number of sets (Table
10) reflected the abundance of fish and the
amount of fishing effort. Excluding the North
Carolina fall fishery, the most sets per season
through 1963 were usually made in the Middle
Atlantic area and the fewest sets in the South
Atlantic. After 1963, following the drastic de-
cline of the fishery and the decrease in effort in
the Middle and North Atlantic areas, the number

775

FISHERY BULLETIN: VOL. 69, NO. 4

Table 9. — Mean number of purse-seine sets per day, Atlantic menhaden fishery, by port and vessel class.

Amagansetr,
N.Y.

Port

'w^onmouth,
N.J.

Tuckerton,
N.J.

Lewes,
Del,

Wildwood,
N.J.

Reedvil
Va.

e.

Year

Class

Class

Class

Class

Class

Class

5

1

6

5

1

6

5

6

3

5

2

5

2.3

4-5

1955

2.49

2.91

3.23

3.71

..

„

3.46

3.93

3.07

3.93

1956

2.82

2.88

3.43

4.03

4.41

4,68

3.38

3,98

3,15

3-99

1957
1958
1959
1960
1961

3.34
2.63
2.72
2.79
3.00

3.17
2.83
3.06
2.81
3.35

3.98
3,26
3,75
3.69
3.40

4,00
2.71
3.58
3.54
3.85

4.44
2.78
3.86
4.29
3.98

4.54
3.67
4.21
4.57
3.75

3.67
3.79
3.19

3.28

4,52
3.07
3.92
4,84
4.21

3,22

2.88
3.61
3.07

3.75

3,43
3.96
3.50

4.56
4.12
4.40
3-86
3.92

5,25
3.76
4.84
4.38
4.40

1962
1963

2.78
2.51

3.29
3.03

3.49
2.60

3.85
3.17

3.49
3.16

3.61
3.27

3,53
2.14

3.46
3.34

2.74
2.96

3.09
2.95

2.86
3.09

3.42
3.39

1964

2.30

2.91

2,41

2.65

__

3.85

..

__

._

2.95

3.62

Mean
Difference

2.74

0.28

3,02

3.32

0.19

351

3.80

0.22

4.02

3.31

0.61

3.92

3.09

0.49

3,58

3,72

0.41

4.13

of sets in Chesapeake Bay, reflecting the increase
in effort, was more than double the number in
any other area.

There also were differences in the mean num-
ber of sets per day between areas (Table 11).
Generally, the greatest number of sets per day
was made in Chesapeake Bay, where vessels
averaged about 0.10 set per day more than ves-
sels in the Middle Atlantic. The fewest sets per
day were made in the South Atlantic, where the
tendency of schools to disappear by midday
limited fishing to the forenoon, and in the North
Carolina fall fishery, where the huge schools of
fish enabled the vessels to load with relatively
few sets.

CATCH PER SET

The mean catch per set varied monthly and
annually in each area (Table 12). In all areas
except the North Atlantic, it tended to be smaller
during the middle part of the season than during
the early or later part. In the Middle and North
Atlantic areas, it averaged 9 tons more in Octo-
ber than in any other month. Annually, it fluctu-
ated randomly in all areas except the Middle
Atlantic, where it decrea.sed after 1962.

Since purse seines tend to capture an entire
school, the mean catch per set is an estimate of
mean school biomass.

The school biomass apijears to increase as the
average age of the fish constituting the .school
increases. The catch per set in the North At-

lantic, where 3-year and older fish constitute the
bulk of catch, was higher than in the South At-
lantic and Chesaijeake Bay, where 1- and 2-year-
old fish compose most of the catch (Nicholson
and Higham, 1964). In the South Atlantic in
1960 and 1961, and in Chesapeake Bay in 19-58,
1960, and 1961, when 2- rather than 1-year-old
fish composed an unusually high percentage of
the catch (Nicholson and Higham, 1964), the
mean catch per set was relatively high. In the
Middle Atlantic area in 1955 and 1956, when the
catch contained a large percentage of fish older
than age 2 (June and Reintjes, 1959, 1960), the
mean catch per set was relatively high. Both
the mean catch per set and the average age were
low in the North Atlantic in 1957 and 1958. In
the Middle Atlantic both the average age and
the mean catch per set tended to decrease fi'om
June to September and then increase sharply
in October, while in the North Atlantic both
tended to increase from June to October.

Except for the South Atlantic area, where
the disapiiearance of schools by midday limits
the number of sets, the mean number of sets
per day (Table 11) and the mean tons per set
(Table 12) were inversely correlated, implying
that fewer sets were necessary to load a vessel
in areas where the school biomass was large, that
schools became more numerous as their biomass
decreased, or that heavy fishing pressure tended
to keep school size small.

Relative abundance also aiipears to influence
school biomass, but the relationship is not clear.
When the catch per vessel week, a measure of

776

ATLANTIC MENHADEN PURSE-SEINE FISHERY

-Estimated number of purse-seine sets in the Atlantic menhaden fishery, by year, month, and area.

Month

North

Year

Total

Carolina

foil
fishery

Area

Apr.-
May

Juno

July

Aug.

Sept.

Oct.

Nov.

South

1955

640

1.422

716

303

77

196

0

3,354

1.477

Atlantic

1956

1,421

817

463

572

411

197

0

3,881

2,358

and North

1957

606

761

435

564

315

85

0

2,766

1,556

Carolina

1958

704

708

574

365

561

118

0

3,030

2,354

fall fishery

1959

812

1.260

1,129

847

506

225

0

4,779

1,827

1960

126

506

590

847

131

105

0

2,305

1,408

1961

310

512

420

512

457

131

0

2,342

1,316

1962

432

648

454

573

806

259

0

3,172

2,568

1963

513

354

380

606

449

140

0

2.442

2,121

1964

403

634

540

496

216

__

0

2.289

1,412

1965

270

531

392

393

309

246

0

2.141

1.826

1966

120

298

257

387

235

62

0

1.359

1.603

Chesapeake

1955

__

—

--

--

—

—

Bay

1956

0

2.025

1.485

2,444

1,361

376

0

7.691

1957

0

2.697

2.501

2.880

2,292

762

0

11.132

1958

0

1.916

2.093

2.208

2,423

550

0

9.190

1959

0

3.060

3.036

2.914

2,657

1,328

0

12.995

1960

0

1.450

1.468

1.878

1,525

899

0

7.220

1961

0

2.376

1.713

1.874

1,257

802

0

8.022

1962

0

1,306

2,751

1.346

1,491

1,227

0

8.121

1963

0

2,150

1,374

1.567

1,411

979

0

7,481

1964

0

2.253

1,798

1.925

1,747

1,334

1,037

10,094

1965

0

1.927

1,137

1.912

1,633

1,533

795

8,937

1966

0

1,473

1,484

2,460

1,386

1,550

888

9,241

Middle

1955

0

3,857

3,483

2.693

2,304

920

0

13,257

Atlantic

1956

0

3.740

3,258

4.264

2,130

950

0

14,342

1957

0

3,589

3,991

4,637

2,641

2,045

0

16,903

1958

0

1. 2 16

2,352

3,098

2,919

243

0

9,828

1959

0

2,884

3,496

3,184

2,448

805

0

12,817

1960

0

2,894

3,889

4,707

2,162

1,556

0

15,208

1961

0

3,529

3,780

5,085

2,233

888

0

15,515

1962

0

5,243

1,987

2,732

1,839

1,088

0

12,889

1963

0

3,086

1,952

2,083

1,025

618

0

8,764

1964

0

1,035

832

663

576

111

0

3,217

1965

0

1,083

733

937

432

152

0

3,337

1966

0

359

168

162

63

-

0

752

North

1955

0

647

1,319

881

413

198

0

3,458

Atlantic

1956

0

579

1,195

1,228

557

302

0

3,861

1957

0

590

1,435

1,332

689

340

0

4,386

1958

0

1B4

519

654

432

280

0

2,069

1959

0

350

1,085

996

764

265

0

3,460

1960

0

611

800

1,092

382

236

0

3,121

1961

0

584

750

1,259

403

269

0

3,265

1962

0

624

344

419

409

347

0

2,143

1963

0

453

422

624

301

217

0

2,017

1964

0

94

233

183

125

30

0

665

1965

0

171

190

198

150

0

0

709

1966

0

9

19

125

70

0

0

223

abundance, declined drastically in the Middle
Atlantic area in 1963, the mean tons per set also
declined. But in the North Atlantic area, where
the catch per vessel week also dropped sharply
in 1963, the mean tons per set did not drop until
1965. Where the decline in the catch per vessel
week was not so severe, no changes in the catch
per set were noted. Perhaps population density
must reach a rather low level before it can cause
a significant decrease in school size. A factor
which may contribute to an ostensible decrease

in school size is selectivity by vessel captains, who
have a tendency to pass by the smaller schools
when fish are abundant. When fish are scarce,
captains are less discriminate.

VARIATION IN ABUNDANCE

Atlantic menhaden are pelagic, but they rarely
range far from shore. Most are caught within
20 miles of the coast. People have speculated
that a large population, unavailable to the fishery,

777

FISHERY BULLETIN: VOL. 69, NO. 4

Table 11. — Mean number of purse-seine sets per vessel day in the Atlantic menhaden fishery, by year, month, and
area. Raw means are weighted, column means are unweighted.

Month

North
Carolina

foil
fishery

Area

Year

Apr..
Moy

June

July

Aug.

Sept.

Oct.

Nov.-
Dec.

Mean

South

1955

2.42

2.54

2.04

_.

0

2.40

2.14

Atlantic

1956

2,00

2.64

1.36

2.00

3.00

._

0

2.07

2.49

and North

1957

1.65

2.44

__

2.30

1.67

1.20

0

1.97

2.79

Corohna

1958

3.12

2.75

2.00

1.54

2.36

__

0

2.47

2.35

fall

1959

2.30

2.67

2.43

2.46

2.60

0

2.50

2.42

fishery

I960

2.36

2.45

2.82

2.97

..

..

0

2.70

2.76

1961

2.69

1.79

2.88

0

2.20

2.11

1962

2.65

2.69

3.24

2.85

3.60

2.88

0

2.88

2.39

1963

2.32

2.21

2.50

3.00

3.40

3.50

0

2.41

2.62

1964

2.25

2.43

2.40

2.35

2.63

0

2.41

2.60

1965

1.71

2.39

2.23

1.90

2.32

3.33

0

2.17

2.78

1966

1.72

2.24

1.95

2.51

2.06

2.00

0

2.09

2.76

Mean

2.25

2.43

2.40

2.36

2.62

2.58

0

2.36

2.52

Chesapeake

1955

__

__

._

..

__

._

__

__

Bay

1956

0

3.70

3.49

3.98

3.82

3,33

0

3.72

1957

0

4.43

4.81

4.72

4.89

3.10

0

4.56

1958

0

3.45

3.89

4.08

5.08

2.85

0

3.99

1959

0

4.13

4.10

5.32

5.27

3.73

0

4.50

I960

0

3.82

4.19

3.95

4.34

3.72

0

4.00

1961

0

4.57

4.00

3.68

3.65

3.48

0

4.01

1962

0

2.93

3.15

3.30

2.76

2.71

0

2.98

1963

0

3.75

2.34

2.82

3.20

3.69

0

3.25

1964

0

3.21

3.00

3.75

3.63

3.09

4.03

3.38

1965

0

3.22

2.69

3.08

2.88

3.31

4.07

3.06

1966

0

2.67

2.92

3.53

2.79

3.05

3.07

3.03

Mean

0

3.62

3.51

3.84

3.85

3.28

3.72

3.68

Middle

1955

0

3.38

4.15

3.83

3.38

2.68

0

3.61

Atlantic

1956

0

3.79

4.17

4.40

3.51

2.41

0

3.87

1957

0

3.50

4.50

4.67

4.03

3.21

0

4.07

1958

0

2.63

3.19

3.41

3.89

2.53

0

3.33

1959

0

3.30

3.93

4.16

3.45

2.65

0

3.68

I960

0

4.22

4.68

4.51

4.00

2.89

0

4.26

1961

0

3.24

4.04

4.48

3.68

2.96

0

3.82

1962

0

3.84

3.03

4.21

3.15

2.12

0

3.45

1963

0

3.15

3.13

3.30

3.20

1.96

0

3.07

1964

0

2.41

3.19

3.56

3.01

0

2.98

1965

0

3.35

3.28

4.01

2.78

3.62

0

3.40

1966

0

2.79

__

3.95

2.75

0

3.08

Mean

0

3.30

3.75

4.04

3.40

2.70

0

3.55

North

1955

0

2.49

3.23

2.45

1.98

2.28

0

2.48

Atlantic

1956

0

2.63

2.89

3.41

2.53

2.25

0

2.84

1957

0

3.80

3.55

2.96

2.89

2.97

0

3.28

1958

0

2.13

2.93

2.83

2.66

2.37

0

2.70

1959

0

2.14

2.53

3.46

2.60

1.97

0

2.73

1960

0

2.70

2.74

3.64

2.07

2.11

0

2.79

1961

0

2.75

3.24

3.77

2.54

2.60

0

3.12

1962

0

3.06

2.77

3.56

2.73

2.61

0

2.96

1963

0

2.54

3.42

2.96

2.61

1.67

0

2.75

1964

0

1.87

3.26

2.48

2.33

1.92

0

2.58

1965

0

2.87

2.96

2.54

2.39

0

2.71

1966

0

1.40

2.78

5.00

__

0

2.24

Mean

0

2.53

3.03

3.26

2.48

2.28

0

2.77

may occur far offshore. There is no available
evidence to support this view.

There is evidence, however, that the entire
population is fished. Since 1945 Atlantic men-
haden have been exploited from northern Florida
to the Gulf of Maine, an area constituting nearly
their entire range. With the advent of airplanes
that could search larger areas and vessels that

could range up to a hundred miles from port,
no areas have been unsearched or unfished, ex-
cept where prohibited by local restrictions.

Under these conditions changes in the catch
per unit of effort are assumed to reflect changes
in actual, rather than aijjiarent, abundance.
Even though the figures have been influenced
by changes in vessel efficiency, they are sensitive

778

NICHOLSON: ATLANTIC MENHADEN PURSE-SEINE FISHERY

Table 12. — Mean catch per purse-seine set of Atlantic menhadpn, in metric tons, by year, month, and area.

means are weighted, column means are unweighted.

Row

Mo

nth

North
Carolina

fall
fishery

Area

Yeor

Apr.-
Moy

June

July

Aug.

Sept.

Oct.

Mean

South

1955

16.4

11.9

11.3

7.4

15.9

16.9

12.6

44.4

Atlantic

1956

19.4

21.9

16.1

12.7

13.6

13.6

17.7

31.2

and North

1957

10.7

17.3

14.5

10.0

12.2

11.1

13.1

35.6

Carolina

1958

10.4

15.3

21.4

8.4

9.1

21.4

13.5

29.8

fall

1959

16.8

16.9

11.2

10.0

9.5

9.7

13.2

44.8

fishery

1960

13.2

12.0

13.8

16.5

13.0

48.7

16.0

44.2

1961

22.6

24.9

15.4

14.6

17.9

15.3

18.6

53.3

1962

14.2

15.3

12.4

16.4

9.3

13.4

13.2

45.5

1963

16.4

18.5

18.9

13.4

7.5

3.2

14.0

28.3

1964

25.6

22.5

23.6

15.5

3.6

20.0

27.6

1965

17.4

25.7

17.2

15.0

10.7

10.3

17.2

28.8

1966

20.2

15,3

19.2

18.4

21.1

12.3

18.2

44.7

Mean

17.0

18.1

162

13.2

12,0

16.0

15.6

33.2

Chesapeake

1955

__

__

Boy

1956

__

12.6

14.3

10.8

12.9

9.1

12.2

1957

__

11.8

11.9

9.6

13.1

11.1

11.4

1958

11.9

20.7

18.9

16.0

8.8

16.4

1959

__

15.3

13.2

14.8

16.0

18.1

15.2

1960

21.8

14.2

14.1

11.2

14.0

15.1

1961

__

16.1

20.0

12.2

16.9

11.1

16.1

1962

__

29.1

15.2

16.9

13.2

23.6

18.5

1963

__

12.9

16.2

15.8

12.4

11.9

13.9

1964

14.2

13.4

13.3

9.3

15.3

13.2

1965

__

15.9

15.7

13.6

11.9

13.0

13.9

1966

__

11.9

H.7

8.4

10.5

13.8

12.6

Mean

—

15.8

15.1

13.5

13.1

13.6

14.4

Middle

1955

23.0

23.8

21.3

23,3

37.4

24.0

Atlantic

1956

__

29.1

25.7

25.6

22.2

30.7

26.4

1957

__

16.5

18.4

15.5

14.6

30.0

18.0

1958

18.1

19.1

24.0

22.7

15.0

21.5

1959

__

22.8

18.1

18.8

16.6

26.1

19.6

1960

15.6

17.3

16.2

15.3

21.7

16.8

1961

__

19.4

22.8

15.2

12.7

15.5

17.7

1962

22.6

16.8

8.3

15.1

48.7

19.8

1963

__

17.2

9.5

6.3

10.1

16.5

12.7

1964

10.7

10.8

13.3

11.2

11.0

11.3

1965

__

13.0

10.2

14.2

17.1

27.2

13.7

1966

7.0

4.7

10.3

16.3

8.0

Mean

—

18.0

16.4

15.8

16.4

25.4

17.4

North

1955

12.9

21.2

31.2

26.9

41.6

24.0

Atlantic

1956

__

23.2

24.4

25.1

26.8

33.9

25.5

1957

._

17.7

15.4

18.1

24.1

29.6

19.1

1958

14.4

10.5

16.9

18.6

16.7

15.4

1959

..

19.5

18.9

18.9

17.1

26.0

19.0

1960

24.3

19.2

18.8

19.8

34.7

21.2

1961

._

14.3

19.5

18.9

16.7

24.9

18.0

1962

22.9

21.3

17.6

22.8

44.7

25.1

1963

__

18.6

9.4

20.1

19.7

19.9

17.4

1964

22.8

30.2

19.3

23.8

34.3

25.1

1965

..

13.2

14.3

20.8

18.5

16.7

1966

4.4

4.3

8.5

9.5

__

8.3

Mean

-

17.3

17.4

19.5

20.3

30.6

19.6

enough to reflect real differences in population
abundance.

Variations in year-class strength have con-
tributed to fluctuations in population abundance.
Estimates of year-class strength prior to 1952
have been based on catch-per-unit-of effort fig-
ures and since 1952 on catch samples. From
1950 to 1958 there were four exceptionally large

year classes, the largest occurring in 1958 (June
and Reintjes, 1959; Nicholson and Higham,
1964) . Most of the year classes after 1958 have
been smaller than any of the year classes prior
to 1958. This series of small year classes oc-
curred simultaneously with the general decline
in abundance, which began about 1956 and be-
came more noticeable in 1963, after the large

779

FISHERY BULLETIN: VOL. 69. NO. 4

1958 year class had nearly passed from the
fishery.

The greatest decline in abundance has been
in the Middle and North Atlantic areas, where
older fish constitute the bulk of the catches.
Fish pumps and airplane spotters, two of the
improvements having the most impact on fishing
effectiveness, increased sharply in both areas
after 1949. Yet the catch per vessel week, after
reaching a peak in about 1952, declined there-
after in both areas, despite other fishing improve-
ments added in the middle 1950's. In the North
Atlantic, the catch per vessel week, except for

1952 and 1953, was no greater from 1950 through
1962 than it had been from 1941 to 1950. In the
Middle Atlantic, the catch per vessel week, al-
though being substantially greater from 1952 to
1962 than it had been up until 1951, began a
steady decline in 1957, and from 1963 to 1966
was much lower than in the years prior to 1950.
From these data one may conclude that the
abundance of menhaden in these two areas was
no greater from 1950 to 1962, and considerably
less after 1962, than it had been prior to 1950.

The decline in abundance in Chesapeake Bay,
where 1- and 2-year-old fish compose most of
the catches, has not been as great as in the
North and Middle Atlantic. The catch per vessel
week was substantially greater from 1954 to 1962
than it was prior to 1954 or after 1962. Since
the major improvements in fishing methods came
a few years later than in the Middle and North
Atlantic, the higher catches per vessel week after

1953 probably reflect an increase in fishing effi-
ciency, although they could reflect an increase in
menhaden abundance. The decrease after 1962
probably resulted from a true decrease in men-
haden abundance.

Abundance in the South Atlantic, where age-1
fish compose most of the catch, appears to have
remained unchanged. The catches per vessel
week varied widely, but showed no trend. In
this area the fisheries at the three ports are
small, geographically distinct, and dependent on
relatively small numbers of fish, principally of
one age group, that are dispersed over a large
area. If the carrying capacity is less in the South
Atlantic than in other areas, the abundance of
fish in the area is less likely to reflect changes

in the total Atlantic menhaden population than
is the abundance of fish in areas of high density
and high carrying capacity, such as Chesapeake
Bay.

In the North Carolina fall fishery menhaden
nearly always will appear to be abundant, be-
cause they are concentrated in a small area for
a short period of time and are easy to catch.
But since weather is more variable than in other
areas, it influences the catch per vessel week
more than it does elsewhere. The wide fluctu-
ations in the catch per vessel week, therefore,
do not necessarily reflect variations in abun-
dance.

The relation between the decline in abundance
and the high levels of fishing effort can be under-
stood only if the spawning age, the age and size
distribution, and the seasonal movements of the
fish are considered. Atlantic menhaden spawn
after they have completed three growing seasons
(Higham and Nicholson, 1964), and rarely sur-
vive past seven growing seasons. Their age and
size distribution and seasonal movements have
been described by June and Nicholson (1964)
and Nicholson,' and are briefly summarized here.

During the fishing season from about May to
October, the population from Florida to Chesa-
peake Bay is composed primarily of age-1 and
age-2 fish. Although the proportion of each age
group varies with the strength of individual year
classes, age-1 fish are usually more abundant,
particularly south of Cape Hatteras. From the
mouth of Chesapeake Bay to Long Island, age-2
fish gradually replace age-1 fish as the dominant
age group. Age-3 fish, dominant in Long Island
and Nantucket Sounds, become less abundant
north of Cape Cod, where age-4 to age-7 fish
predominate. A southward movement begins
among fish at the northern end of the range
in late summer and extends to all fish north of
Cape Hatteras by early November. By mid-Jan-
uary nearly all menhaden have moved into the
offshore area between Cape Lookout and north-
ern Florida. In late winter these fish begin a
northward movement.

' Nicholson, William R. Movements of Atlantic men-
haden as inferred from changes in age and size distri-
bution. (Unpublished manuscript.)

780

NICHOLSON: ATLANTIC MENHADEN PURSE-SEINE FISHERY

As older fish decreased in abundance, fisheries
dependent on them declined. No menhaden were
landed after 1958 at Portland, after 1962 at
Gloucester, or after 1963 at Point Judith. After
the 1958 year class ceased to contribute largfe
numbers to the catch, the Amagansett, Port Mon-
mouth, and Tuckerton catches dropped sharply.
As catches declined and plants closed or reduced
fishing, effort also dropped. By 1968 only 136
vessel weeks were expended in the North and
Middle Atlantic, as compared with 1,265 in 1962.

Effort in areas where age-1 and -2 fish were
predominant continued to be high. In 1968, 846
vessel weeks were expended in the South Atlantic
and Chesapeake Bay, as compared with 909 in
1962.

Changes in the catch and the catch per vessel
week suggest that the decline in numbers of fish
older than age 2 was much greater than the de-
cline in numbers of fish younger than age 3.

If recruitment is dependent on spawning popu-
lation size, and spawning population size is de-
pendent on the escapement of pres])awning age
fish, the total yield will be limited by the amount
of escapement. Schaaf and Huntsman" have
shown that with present levels of fishing effort,
the spawning stock of Atlantic menhaden is in-
adequate for recovery of the population.

LITERATURE CITED

Broadhead, G. C.

19fi2. Recent changes in the efficiency of vessels
fishing for yellowfin tuna in the Eastern Pacific
Ocean. Inter- Am. Trop. Tuna Comm., Bull. 6:
283-316.
Clark, F. N., and A. E. Daugherty.

1950. Average lunar month catch by California
sardine fishermen, 1932-33 through 1948-49. Calif.
Div. Fish Game, Fish Bull. 76, 28 p.
HiGHAM, J. R., Jr., and W. R. Nicholson.

1964. Sexual maturation and spawning of Atlantic
menhaden. U.S. Fish Wildl. Serv., Fish. Bull. 63:
255-271.
June, F. C.

1963. The menhaden fishery. In M. E. Stansby

" Schaaf, William E., and Gene R. Huntsman. Pop-
ulation dynamics of the Atlantic menhaden: An analy-
sis of the purse seine fishery, 1955-69. (Unpublished
manuscript.)

(editor) , Industrial fishery technology, p. 146-159.
Reinhold Publishing Corp., New York.

June, F. C, and W. R. Nicholson.

1964. Age and size composition of the menhaden
catch along the Atlantic coast of the United States,
1958; with a brief review of the commercial fish-
ery. U.S. Fish Wildl. Serv., Spec. Sci. Rep. Fish.
46, 40 p.

June, F. C, and J. W. Reintjes.

1957. Survey of the ocean fisheries off Delaware
Bay. U.S. Fish Wildl. Serv., Spec. Sci. Rep. Fish.
222, 55 p.

1959. Age and size composition of the menhaden
catch along the Atlantic coast of the United States.
1952-55; with a brief review of the commercial
fishery. U.S. Fish Wildl. Serv., Spec. Sci. Rep.
Fish. 317, 65 p.

1960. Age and size composition of the menhaden
catch along the Atlantic coast of the United States,
1956; with a brief review of the commercial fish-
ery. U.S. Fish Wildl. Serv., Spec. Sci. Rep. Fish.
336, 38 p.

Kreutzer, C. O.

1959. The use of electricity in commercial fi.shing
in the sea. Proc. Gulf Caribb. Fish. Inst. 11:
50-52.
Mark, J. C.

1950. Apparent abundance of the pilchard {Sardi-
nops caerulea) off Oregon and Washington, 1935-
43, as measured by the catch per boat. U.S. Fish
Wildl. Serv., Fish. Bull. 51: 385-394.

NiCHOL.SON, W. R., AND J. R. HiGHAM, jR.

1964. Age and size composition of the menhaden
catch along the Atlantic coast of the United States,
1959; with a brief review of the commercial fish-
ery. U.S. Fish Wildl. Serv., Spec. Sci. Rep. Fish.
478, 34 p.
ROBAS, J. S.

1959. Menhaden purse seining. In H. Kristjonsson
(editor). Modern fishing gear of the world, p. 394-
399. Fishing News (Books) Ltd., London.
Schmidt, P. G., Jr.

1959a. New purse-seining techniques in the men-
haden fishery employing the power block. Proc.
Gulf Caribb. Fish. Inst. 11: 46-50.

1959b. The Puretic power block and its effect on
modern purse seining. In H. Kristjonsson (edi-
tor) , Modern fishing gear of the world, p. 400-413.
Fishing News (Books) Ltd., London.

ShIMADA, B. M., AND M. B. SCHAEFER.

1956. A study of changes in fishing effort, abun-
dance, and yield for yellowfin and skipjack tuna
in the Eastern Tropical Pacific Ocean. Inter-
Am. Trop. Tuna Comm., Bull. 1: 351-421.

SiLLIMAN, R. P., AND F. N. ClARK.

1945. Catch per-unit-of-effort in California waters
of the sardine (Sardinops caerulea) 1932-42.
Calif. Div. Fish Game, Fish. Bull. 62, 76 p.

781

ABUNDANCE AND DISTRIBUTION OF YOUNG ATLANTIC MENHADEN,
Brevoortia tyratinus, IN THE WHITE OAK RIVER ESTUARY,

NORTH CAROLINA

E. Peter H. Wilkens' and Robert M. Lewis-

ABSTRACT

The effect of salinity, temperature, tide, turliidity, and illumination on the distribution of larval, preju-
venile, and juvenile menhaden in an estuary was investigated. Most menhaden larvae entered the estuary
in March after the water had warmed to about 10° C, and moved upstream to the low-salinity-freshwater
zone where they transformed into juveniles. More larvae were caught in the lower estuary on flood tide.
After transformation to juveniles they were caught in schools throughout the estuary. Turbidity and
illumination did not affect the distribution of menhaden, but illumination affected catchability, since
more menhaden were collected during night tows.

In this study we investigrated the effects of tem-
perature, salinity, and light on the distribution
and abundance of larval, prejuvenile, and juve-
nile menhaden in a single estuary, the White Oak
River in North Carolina. As the strength of
individual year classes of Atlantic menhaden
fluctuates widely, we were interested in deter-
mining what effect these environmental factors
had on menhaden during their first year in an
estuary. This information could be helpful in
assessing and predicting the strength of indi-
vidual year classes. Estimates of the strength
of individual year classes before they enter the
fishery would be valuable to the commercial
fishery. A single estuary was selected so that
a better understanding of these variables could
be achieved before being applied to a coastwise
fishery.

Atlantic menhaden, found along the eastern
coasts of the United States and Canada from
Nova Scotia to southern Florida (Hildebrand,
1964; Reintjes, 1964), spawn in almost every
month in some part of their range (Higham and
Nicholson, 1964). Menhaden are spawned in

' National Marine Fisheries Service, Southeast Fish-
ery Center, Miami, Fla. 33149; formerly National
Marine Fisheries Service, Center for Estuarine and
Menhaden Research, Beaufort, N.C.

" National Marine Fisheries Service, Center for Estu-
arine and Menhaden Research, Beaufort, N.C. 28516.

Manuscript accepted May 1971.

FISHERY BULLETIN: VOL. SO, NO. 4.

the ocean and enter an estuar.y as larvae. Once
strong enough to swim against the tidal currents,
they move ujistream towards fresh water (Lewis
and Mann, 1971) where they transform into ju-
veniles. They remain in the estuary for their
first growing season, gradually moving down-
stream in the summer and reaching the lower
estuary or open sea by autumn (June and
Chamberlin, 1959; Massmann, Ladd, and Mc-
Cutcheon, 1954).

STUDY AREA, SAMPLING LOCATIONS,
PROCEDURES, AND NETS

The White Oak River estuary is a bar-built
estuary (Pritchard, 1967) which drains forest
lands in the upstream part and salt marshes in
the downstream part (North Carolina State
Board of Health. 1954) . The Intracoastal Water-
way crosses the mouth of the estuary near Bogue
Inlet.

We selected this estuary because: (1) We
knew from preliminary sampling that larval
menhaden entered the lowei- section from the
ocean in the winter and early spring and that
juveniles occurred in the upper section in the
summer; (2) its small size (28sqkm) permitted
ample sampling coverage; and (3) its proximity
to the Beaufort laboratory made frequent sam-
pling easy.

783

FISHERY BULLETIN: VOL. 69. NO. 4

We assumed that few or no larvae moved from
other estuaries into the White Oak River estuary.

We collected larval, pre.juvenile, and juvenile
menhaden at 14 sampling locations extending
34 km upstream from Bogue Inlet (Figure 1).
The distance between stations varied from 2 to
5 km and averaged about 3 km. The type of gear
we used, frequency of sampling, and date of
sampling are listed in Table 1.

Table 1. — The White Oak River estuary sampling
schedule.

Sompling location

Sompl

freque

ng

ncy

Gear

Sampling period

Swonsboro Bridge

(Station 2)

2-3 days/

week

Channe

net

Nov. 1967-Apr. 1968
Nov. 1968-Apr. 1969

Upstream stations 6-12

Monthly

Surface

trawl

July-Sept. 1968

Upstream stations 6-12

Weekly

Channel

net

Feb.-Apr. 1969^

Upstream stations 6-12

Biweekly

Channel

net

May 1969

Upstream stations 6-12

Monlhly

Channel

net

June-Sept. 1969=

^ Stations 1, 3, 4, and 5 were sampled irregularly in this period.
^ A few samples were taken upstream with the surface trawl in this
period.

We sampled larvae entering the estuary at the
Swansboro Bridge (station 2) 2 or 3 days per
week from November through April in 1967-68
and 1968-69. During July, August, and Sep-
tember 1968, we sampled at several of the up-
stream stations. Starting in February 1969 we
collected menhaden throughout the river and
estuary, although our efforts were concentrated
on the upstream section (stations 6 through 12) .
In March and April we visited these stations
every week; in May, every 2 weeks; and from
June to September, every month.

During the 1967-68 and 1968-69 seasons, we
sampled for larvae with a channel net described
by Lewis, Hettlei', Wilkens, and Johnson (1970).
The net, with a 1 by 3 m opening, had a tail bag
constructed of 0..5-mm mesh. At Swansboro we
attached the net to the bridge and made four
to six 30-min sets per day. At the other loca-
tions, we towed the net between two 16-ft alum-
inum boats and made a 1.5-min set when the
larval and i)rcju\enile menhaden were scarce and
a I3-miii .set when they were abundant.

During July, August, and September 1968, we
sampled juveniles with a 6.1-m surface trawl

WHITE OAK
RIVER

Figure 1. — Sampling locations for young menhaden on
the White Oak River estuary, N.C.

having a 6.2-mm bar mesh. We towed it in the
same manner as the channel net. During the
corresponding months in 1969, most of the col-
lections were made with the channel net.

In all the collections, the number of menhaden
caught was expressed as an index (/ = number
of young menhaden per 100 m' water strained).

We recorded surface temjjerature and salinity
at the start and end of each set at the bridge
and at the end of each tow at the other sites.
We measured the amount of water strained by
the net during each set with a flowmeter. Dis-
solved oxygen and turbidity readings were taken
only in July, August, and September 1968.

784

WILKENS and LEWIS: YOUNG ATLANTIC MENHADEN

TEMPORAL DISTRIBUTION

Larval menhaden entered the White Oak River
from November until early May. Two peaks of
abundance occurred each year, one in November
and December and the second and major peak in
February and March (Figure 2).

soo.o
200.0

/^^

100.0

/ \

50.0

20.0

10.0

5 0

2.0

1.0

\

1

0.5

■

/

\

V ^

i

0.2

4

/\
/ \
/
/
/

J

/

\.

0.1

NOV. 1

DEC.

"T

JAN.

■ FEB. ■ MAR.

APR. '

Figure 2. — The mean biweekly abundance indexes at
Swansboro Bridge in 1967-68 (solid line) and 1968-69
(dashed line).

The entrance of large numbers of larvae in
February and March probably resulted from the
migratory schools of menhaden that spawned off
the North Carolina coast during the winter.
Higham and Nicholson (1964) found that during
November and December most of the females in
the landings were nearly ripe. Reintjes (1969)
reported finding hundreds of thousands of de-
veloping menhaden eggs off the North Carolina
coast in December 1966.

Those larvae that entered the estuary during
November and December were probably the

1969

Figure 3. — The relative abundance of larval (solid line) ,
prejuvenile (dashed line) , and juvenile menhaden (dotted
line) in the White Oak River estuary. (The larval in-
dexes are from the bridge, and the prejuvenile and juve-
nile indexes are from the upstream zone where the fresh
and salt water mix. Larval and prejuvenile indexes are
biweekly means, but the juvenile index is a monthly mean
plotted on the day the sample was obtained.)

progeny of fish that either had inhabited North
Carolina waters in the summer or had moved
into North Carolina waters from other areas in
early autumn.

Prejuvenile menhaden were first caught in
March and became abundant in late March and
A])ril (Figure 3). After the peak in April the
number of prejuveniles decreased, and by the
beginning of May most had transformed into
juveniles.

Juvenile menhaden, collected in relatively low
numbers from May until September, occurred
with maximum abundance in late May and June.
As young menhaden got above 45 mm fork length
during the summer of 1968, we caught fewer
fish during the day. To determine if illumina-
tion was a factor that resulted in greater net
avoidance by juvenile menhaden, we scheduled
a series of day-night sampling trips. We col-
lected larger samples of menhaden during night-
time tows, which indicated that some fish were
able to avoid our net during the day. Fish from
day and night tows were similar in length. In
addition, we caught more menhaden on overcast
or moonless nights than on clear, moonlight
nights. As a result of our findings in 1968, we
sampled for juveniles in 1969 only at night in
order to increase our sampling efficiency.

785

FISHERY BULLETIN: VOL. 69, NO. 4

EFFECT OF SALINITY, TEMPERATURE,

AND TIDE ON THE DISTRIBUTION

OF YOUNG MENHADEN

SALINITY

Larval menhaden, after entering: the lower
estuai-y, move upstream into lower salinities to
metamorphose. They seek the zone of the river
from 1 '/,, salinity to fresh water. This zone ex-
tends a short distance upstream from the inter-
face between fresh and salt water. Larval and
prejuvenile menhaden were most abundant in
this zone where metamorphosis occurs (Figure
4). They api)arently range into fresh water for
only a short distance since they were absent or
present only in small numbers in our samples
farther upstream.

After the menhaden have transformed from
prejuveniles to juveniles, they appear to seek
higher salinity water. In late May when most
of the prejuveniles had metamorphosed, we
found juveniles in low-salinity water. As the
season progressed the juveniles were present in
the low-salinity water upstream, but they tended
to be more abundant in water downstream.
Schools of juvenile menhaden generally moved
out of the estuary in the fall.

Both the position and length of the upstream
zone where young menhaden concentrated are
influenced by tidal excursion, rainfall, and wind
dii'ection and strength. A northeast wind causes
unusually high tides and pushes salt water far-
ther upstream than during normal flooding and
ebbing tides.

We do not understand why low-salinity water
is important to young menhaden, but one expla-
nation is that they cannot metamorphose prop-
erly in either fresh or high-salinity water.
When larvae were held in salinities ranging from
15 to 40 ';, , about one-third of the flsh in each
salinity group develojied abnormalities of the
spine (Lewis, 19(i6). Juveniles may also con-
gregate in low-salinity areas at times because
food may be more abundant.

In some estuaries turbidity may vary with sa-
linity. We measured the turl)idity at the Swans-
boro site in March, April, and May 1968 and at
our upstream sites during the summer of 19fi8 to

determine if it afl^ected the number of young
menhaden caught by our net, and to see if there
was any relation between salinity and turbidity.
At Swansboro, where the water remained rela-
tively clear (light transmittance ranged from 89
to 96 ' r ) , no correlation existed between turbi-
dity and the catch of larvae. At our upstream tow
areas, where the water also was clear, light
transmittance ranged from 68 to 9.5 ""r . We also
found no relation between turbidity and catch
of young menhaden. We concluded therefore
that turbidity was too low to affect catchability
in the White Oak River. As there were no
marked differences between up- and downstream
turbidities, we concluded also that there was no
relation between salinity and turbidity.

TEMPERATURE

Larval menhaden are sensitive to low temper-
atures, particularly if the salinities are high or
low. They have the best chance for survival in
an estuary if the temperature remains above
4° C and the salinity ranges between 10 and 20 '/,c
(Lewis, 1966) . Below 4° C they sui'vive for only
a short time. Lewis (1965) determined that the
number of hours to 50";^ mortality at 2.0° C
varied from 3.2 to 38.5 hr depending on the ac-
climation temperature.

We compared the temperatures in the estuary
during the 2-year study with temperature tol-
erances of larval menhaden determined in the
laboratory by Lewis (1965, 1966). The water
temperature in the White Oak River went below
4° C for several days in January and December
1968 and January 1969. Except for two sam-
pling days in 1968 and one in 1969, the water
temperature did not get over 10° C from the be-
ginning of January to mid-March ; it stayed at
2° C for 2 days during this period in 1968, and
1 day in 1969. We caught few menhaden larvae
during the jjeriods of low water temperature.

Most larvae that enter the estuary before the
lethal cold water temperatures in the winter
probal)ly do not survive, while those that enter
during the late winter and early spring probably
remain in the downstream area because of the
colder water upstream. As the water warms
in the spring to above 10° C thev move towards

786

WILKENS and LEWIS: VOUNG ATLANTIC MENHADEN

o

6
o

o
o

<

O

March 17

:1dDd_

1.5 0.2 0.0 0.0
March 27

0.0 0.0 0.0 0.0 0.0

April 1

May 1

Ud

D

□

1.5 0.2 0.0 0.0 0.0

April 9

m

4.1 0.1 0.0 0.0 0.0

April 16

8.0 3.8 0.0 0.0 0.0

^

•
a
E
o

o

Z

5.2 1.8

0.0 0.0

May 14

a 1=] 1=1 O _
13.7 7.4 4.2 1.5 0.0

May 27 i

tDoiDD

15.4 11.7 4.4 0.6

June 26

:nDl

1.8 0.2 0.0 0.0

July 16

a
E
o

[DD

3.0

August 27

10.2 3.0 0.0 0.0

E

0

15.1 8.9 0.5 0.0

16 18 21 24 28

16 18 21 24 28

KILOMETERS

Figure 4. — The distributioii of menhaden by date, kilometer, and salinity in the White Oak River, March-
August 1969. (Number below each bar is salinity at station.)

787

FISHERY BULLETIN; VOL. 69, NO. 4

the low-salinity freshwater zone. Those that
enter later in the season, after the water has
warmed, move upstream in a shorter time. Once
menhaden had moved upstream, salinity and food
supiily probably affected their distribution more
than temperature.

Since dead menhaden larvae do not float, we
probably would not notice if kills occurred when
the temperature droijped below 4° C. However,
we did observe many dead young and adult bay
anchovy (Anchoa mitchiUi) and pinfish (Lagod-
on rhomboides) floating on the surface on Jan-
uary 10 and 12, 1968, when the water temper-
ature was 2° C. Some of the floating fish revived
when placed in warmer water, but most did not.
We assume that many of the species present in
the estuary either died from or were subject to
cold stress. Thus any cold weather that occurs
during the time larval fish are present in the
estuary can have an important effect on the num-
ber of individuals surviving in the ])opulation.

Although high water temperature does kill
juvenile menhaden, it did not appear to cause
any mortality in the White Oak River estuary.
In laboratory tests, juvenile menhaden died in
water temperatures above 33° C (Lewis and
Hettler, 1968). In the White Oak River the
temperature remained below 33° C except for a
short period when it rose to 34.1° C.

TIDE

Velocity of water current affects the abun-
dance and distribution of fish larvae in an estu-
ary. Bishai (1959) found that herring larvae
(6-8 mm total length) maintained themselves
in a current of 0.58 to 1.03 cm/sec and that at
higher velocities they drifted with the current
but at a rate less than the current.

During our sampling in the field we noticed
that larval menhaden also held their jiositions
only in weak currents. The menhaden larvae
collected at the Swansboro bridge were larger
(10-30 mm total length) than the herring tested
by Bishai and seemed able to maintain their
position at velocities less than 10 cm/sec. Above
this velocity they were carried by the current.
One would expect, therefore, to obtain large
larval indexes during peak tidal flows at midflood

Table 2. — Number of menhaden larvae per 100 m' of
water at hourly flood and ebb-tide stages, Swansboro,
N.C., February-March 1969.

Stage

Hour

Mean
velocity

Abundance
index

Range

Number of
collections

m/src

Flood

1

o.m

33.6

17.2- 45.2

3

2

0.17

216.0

16.0- 591.4

4

3

0.15

94.9

0.8- 578.4

8

4

0.18

74.0

4.0- 338.8

7

5

0.15

894.9

1.5-3,582.0

7

Ebbi

1

0.22

65.6

20.6- 110.6

2

2

0.27

168.0

25.6- 365.4

3

3

0.23

43.1

7.2- 121.1

5

4

0.21

26.4

0.4- 90.5

6

5

0.19

17.8

2.2- 82.9

7

6

0.16

6.5

1.9- 13.0

8

7

0.11

8.7

1.4- 14.4

7

The ebb-tide stoge generolly lasted about 2 hr longer than flood.

and at early ebb. Larval indexes during these
periods varied considerably, but in general were
larger than indexes during late ebb and early
flood tide stages (Table 2). The variability in
abundance indexes arises, in part, from day-to-
day changes in menhaden distribution in the low-
er estuary during the 2-month period. A 24-hr
study in March 1968 at Beaufort, N.C., showed
that larval abundance varied with the tide, cur-
rent, and time of day (Lewis and Wilkens, 1971).

Tides affect the movement of larvae in and out
of an estuary as well as within an estuary.
Flooding currents carry larval menhaden into
the estuary where, before heading upstream,
they move back and forth with the changing
tides. At the Swansboro bridge station more
larvae were caught on flood tide than on ebb.
During February and March 1969, larval indexes
greater than 10 occurred in 81 'r of the sets made
on flood tide but only in 51 ""f of the sets on ebb
tide. June and Chamberlin (1959) reported sim-
ilar results at Indian River, Del. Some of the
larger catches of the season occurred on late
flood. The early hours of ebb tide had higher
larval indexes than late ebb. As more larvae
enter than leave, the number of larvae in the
estuary reaches a maximum by midsiiring.

Tidal stage and current velocity affected the
catchability of larvae. In the lower estuary these
forces either concentrated the larvae in one lo-
cation or spread them over a large area. In the
u)iper e.stuary the location and width of the low-

788

WILKENS and LEWIS: YOUNG ATLANTIC MENHADEN

salinity-freshwater zone, which was influenced
by the tide, affected the distribution of larvae
and prejuveniles.

SUMMARY

Larval menhaden were present in the White
Oak River estuary from November to May but
were most abundant in February and March.
Prejuveniles were abundant in late March and
April, and by the beginning of May most had
transformed into juveniles. Our largest catches
of juveniles occurred in May.

Larvae progress upstream to the zone where
the salt and fresh water mix (0-1 ;„ salinity).
Large catches of prejuvenile and larval men-
haden occurred within this zone. We did not
find juvenile menhaden in the zone until the end
of May when most prejuveniles had transformed
to juveniles.

Laboratory tests from other studies showed
that menhaden died when the water temperature
fell below 4° C and rose above 33° C. Even
though young menhaden encountered both ex-
tremes of water temperature in the White Oak
River, we saw no evidence of any deaths.

Catches of larval menhaden at the Swansboro
bridge were more abundant on flood tide than
ebb. The early hours of ebb tide had higher
larval indexes than late ebb.

Illumination affected the catches of juvenile
menhaden at our upstream stations as we caught
more menhaden on overcast or moonless nights
than on clear, moonlight nights or during the
daylight hours.

LITERATURE CITED

BisHAi, H. M.

1959. The effect of water currents on the survival
and distribution of fish larvae. J. Cons. 25: 134-
146.
Hicham, J. R., and W. R. Nicholson.

1964. Sexual maturation and spawning of Atlantic

menhaden. U.S. Fish Wildl. Serv., Fish. Bull.
63: 255-271.
HiLDEBRAND, S. F.

1964. Family Clupeidae. In Fishes of the western
North Atlantic, p. 257-454. Mem. Sears Found.
Mar. Res. Yale Univ. 1, Part 3.

June, F. C, and J. L. Chamberlin.

1959. The role of the estuary in the life history
and biology of Atlantic menhaden. Proc. Gulf
Caribb. Fish. Inst. 11th Annu. Sess., p. 41-45.

Lewis, R. M.

1965. The effect of minimum temperature on the
survival of larval Atlantic menhaden, Brevoortia
tyrannus. Trans. Am. Fish. Soc. 94: 409-412.

1966. Effects of salinity and temperature on sur-
vival and development of larval Atlantic men-
haden, Brevoortia tyrannus. Trans. Am. Fish.
Soc. 95: 423-426.

Lewis, R. M., and W. F. Hettler, Jr.

1968. Effect of temperature and salinity on the sur-
vival of young Atlantic menhaden, Brevoortia
tyrannus. Trans. Am. Fish. Soc. 97: 344-349.

Lewis, R. M., W. F. Hettler, Jr., E. P. H. Wilkens,
AND G. N. Johnson.

1970. A channel net for catching larval fishes.
Chesapeake Sci. 11: 196-197.

Lewis, R. M., and W. C. Mann.

1971. Occurrence and abundance of larval Atlantic
menhaden, Brciwortia tyrannus, at two North
Carolina inlets with notes on associated species.
Trans. Am. Fish. Soc. 100: 296-301.

Lewis, R. M., and E. P. H. Wilkens.

1971. Abundance of Atlantic menhaden larvae and
associated species during a diel collection at Beau-
fort, North Carolina. Chesapeake Sci. 12: 185-187.
Massmann, W. H., E. C. Ladd, and H. N. McCutcheon.
1954. Postlarvae and young of the menhaden
{Brevoortia tyrannus) in brackish and fresh
waters of Virginia. Copeia 1954 : 19-23.
North Carolina State Board of Health.

1954. The White Oak River Basin. N.C. State
Board Health Pollut. Surv. Rep. 2, 122 p.
Pbitchard, D. W.

1967. What is an estuary: Physical viewpoint. In
G. H. Lauff (editor). Estuaries, p. 3-5. Am.
Assoc. Adv. Sci., Publ. 83.

Reintjes, J. W.

1964. Annotated bibliography on the biology of
menhadens and menhadenlike fishes of the world.
U.S. Fish Wildl. Serv., Fish. Bull. 63: 531-549.

1969. Synopsis of biological data on Atlantic men-
haden, Brevoortia tyrannus. U.S. Fish Wildl.
Serv., Circ. 320, 30 p.

789

histius bmsiliensis, A SQUALOID SHARK, THE PROBABLE CAUSE OF
CRATER WOUNDS ON FISHES AND CETACEANS

EVERET C. Jones'

ABSTRACT

Evidence is presented that bites inflicted by the small squaloid shark, Isistius brasiliensis (Quoy and
Gaimard) , are the causes of crater wounds, crescentic wounds, and related scars on large pelagic
fishes and cetaceans. This evidence consists of a ci-escentic "wound" experimentally produced on the
side of a dead fish by a living Isistiu.s; specialized morphology of the shark's basihyoid cartilage and
coracohyoideus muscles, lips, labial cartilages, and spiracles, that, together, enable the shark to form
an oral vacuum on a smooth surface; an experiment in which a living Isistin.'i formed such a vacuum;
specialized morphology and arrangement of the mandibular teeth ; close agreement between the range
of reported wound widths and the estimated range of bite widths of Isif^titis; agreement between the
geographical ranges of Isistius and those fishes and cetaceans which bear crater wounds; and, finally,
the presence in Isistius stomachs of hemispheroidal plugs of fish flesh. Speculation on the circumstances
that may enable a small, slow shark to make contact with large, swift fishes and cetaceans is included.
Isistius apparently qualifies as a temporary parasite.

Probably the earliest account of the existence
of small, round or oval, scooped-out wounds on
the sides of large pelagic fishes is contained in
an ancient legend of Samoa (A. Utu, personal
communication), which states that atu (skip-
jack tuna, S^^f/ii/z^/nts /*e^a>H/s (Linnaeus)) en-
tered Palauli Bay, and, upon approaching the
beach, left small round pieces of their flesh as
gifts to Tautunu. chief of that community. Evi-
dence of this sacrifice was found by the people
who caught the atu and observed fresh, round
wounds on their sides.

This legend provides one of many explanations
that have been advanced regarding the causes
of such wounds on large pelagic fishes as well
as on whales and porpoises. This paper jjresents
evidence that many crater wounds, crescentic
wounds, and the resulting scars on pelagic fishes
(Figure 1), and open pit wounds and resulting
scars on cetaceans are the results of bites in-
flicted by the small squaloid shark, Isistius bra-
siliensis (Quoy and Gaimard). (A second spe-
cies, Isistiits phitodns, was described by Garrick
and Springer (1964) from the Gulf of Mexico.
Although nothing is known of the behavior of

' National Marine Fisheries Service, Hawaii Area
Fishery Research Center, Honolulu, Hawaii 96812.

Manuscript accepted June 1971.

FISHERY BULLETIN: VOL. 69, NO. 4.

this species, which is based on one specimen,
it is probable that its feeding habits are similar
to those of I. brasiliensis.)

Such wounds on fishes have been reported by
Nemoto (1955), Iversen (1959), Guitart M.
(1964), Klawe (1966), Bane (1969), and Ma-
chado Cruz (1969). The literature on open pit
wounds and related scars on cetaceans is much
more extensive, apparentl.v beginning with the
work of Collett ( 1886) . Mackintosh and Wheel-
er (1929) and van Utrecht (1959) presented
thorough discussions of these wounds and proba-
ble causes, and summarized the previous litera-
ture. Nemoto (1955) noted that some of the
wounds observed on whales are similar to and
Ijrobably have a common origin with those on
fishes. He further stated that a cause other than
lamprey attacks, the most commonly advocated
agent, must be found to account for crescent-
shaped scars and open pit wounds on cetaceans
and fishes.

It was not always jjossible for me to determine
whether published photograijhs and descriptions
were of wounds and scars of the types which I
attribute to Isistius bites. I have never seen
wounds known to have been produced by lam-
preys and therefore cannot comment with any

791

FISHERY BULLETIN: VOL. 69, NO. 4

Figure 1. — Crater wounds on a large dolphin from the
central Pacific.

authority on them. I believe, however, that
Pike (1951) unknowingly but accurately de-
scribed the differences between lamprey bites
and Isistius bites on whales when he wrote:
"The lampreys seem to leave two distinct types
of wounds .... The first consists of a circular
area in which the epidermis is completely abrad-
ed by the teeth of the sucking disc. In the center
of this is a hole through the skin caused by the
rasping tongue. In the other type the lamprey
apparently rasps away the skin over the entire
area with the result that there is a circular sore
right down to the blubber and no jieriphery of
skin which has been damaged but not eaten
away." The second type and some of the wounds
and scars illustrated by Pike are, I believe, at-
tributable to Isistius bites.

Crater wounds have been reported in the lit-
erature cited on skipjack tuna; yellowfin tuna.

Figure 2. — A crater wound on the side of a swordfish
caught in the Gulf of Mexico. (Photo by Martin
Bartlett.)

Thunytn^ alba^'ares (Bonnaterre) ; dolphin, Cor-
yphaena hippunis Linnaeus; opah, Lampris re-
gius (Bonnaterre); and swordfish, A'/p/i/«s g/«-
diiis (Linnaeus) (Figure 2). In addition to
these, I have seen crater wounds on albacore,
Thunnus alalunga (Bonnaterre), and wahoo,
Acanthocyhinm solandri (Cuvier) , in the central
Pacific. Biologists and fishermen in Hawaii have
reported to me having seen them on kawakawa,
Enfhyruius affinis (Cantor) ; large jacks, Car-
anx sp.; rainbow runners, Elagatis sp.; and
various species of marlins, Istiophoridae.

The cetaceans upon which crater wounds,
crescentic wounds, or resultant scars have been
reported were listed by van Utrecht (1959). In-
cluded were beaked whales, sperm whales, var-
ious species of porpoises, and nearly all of the
baleen whales (order Mysticeti) except the right
whales (family Balenidae) which apparently do
not migrate out of cold polar waters. In Ha-
waiian waters, wounds and scars (Figure 3)
are commonly seen on porpoises of the genera
Tursiops and StcneUa, and have been observed
on a beaked whale, Ziphias sp., stranded on
Oahu.

Dr. Donald W. Strasburg, during discussions
several years ago, i)lanted the idea that Isistiiis
might be the cause of crater wounds on fishes.
He had found (Strasburg, 1963) that the man-

792

lON'ES ; PROBABLE CAUSE OF CRATER WOUNDS

Figure 3. — Crescentic scar on a living porpoise, Stenella
roseiventris Wagner, The Oceanic Institute, Makapuu,
Hawaii.

dibular teeth of Isistius are shed as a unit and
that the next set of replacement teeth are al-
ready erect and immediately functional when
the previous set is shed. He wondered "...
which aspects of Isistius biology require such a
safeguard."

OBSERVATIONS

An opportunity to test the idea came in July
1969, during cruise 44 of the RV Toirn^end
Cromwell of the NMFS, HAFRC (National Ma-
rine Fisheries Service, Hawaii Area Fishery
Research Center). Nightly midwater trawl
hauls were made along long 145° W between
lat 14° N and 3° S in the central Pacific. The
trawl catches contained occasional specimens of
Isistius, some of which were alive but moribund
when brought on board. I stated that this spe-
cies of shark might be responsible for the crater
wounds which we had observed on tunas a few
hours earlier. This led John D. Fowler, Jr., re-
search assistant aboard the Toirnsend Cromwell,
to iiress the mouth of a moribund Isistius against
the side of a dead fish, Cubiceps sp. The shark
made a biting motion, producing a crescentic
wound (Figure 4) that if completed would have
been similar in size and shape to crater wounds
observed on tunas. That shark could not be in-
duced to repeat its performance, but Fowler's
experiment led to further attempts to determine

Figure 4. — A crater "wound" produced on the surface
of a nectarine by pushing the teeth of a dead Isistius
into the fruit and then rotating the body of the shark
around the point of attachment. In the center is a
crescentic "wound" produced by a living Isistius when
its mouth was pressed against the side of the dead fish.

whether adaptations in structure for specialized
feeding behavior existed in Isistius.

The basihyoid cartilage or "tongue" of Isistitts
was large and thick in contrast to that structure
in galeoid sharks. It was also unusually mov-
able; with a pencil I was able to push the tongue
caudad to a point just anterior to the first ex-
terior gill opening (Figure 5). In that position
the posterior margin of the tongue was elevated
(dorsad) until the tongue was nearly vertical,
fitting closely against the roof of the mouth, and

Figure 5. — A demonstration of the movability of the
tongue of Isistius.

793

FISHERV BULLETIN: VOL. 69, NO. 4

completely separating the mouth from the phar-
ynx. Two ridges in the roof of the mouth cor-
responded to two grooves in the posterior margin
of the tongue. This structural correspondence
suggested that vertical positioning of the tongue
was a normal occurrence. The movability of the
tongue, as well as several other attributes de-
scribed below, can only be demonstrated with
specimens of Isistius that have not been fixed.
Observations of these anatomical characters
led to the hypothesis that Isistius is capable of
achieving a vacuum with its mouth on a smooth
surface. Concurrently with the retracted, verti-
cal positioning of the tongue, the lips protruded
completely around the mouth. The fleshy lateral
lips contained well-developed labial cartilages
that caused them to be semirigid and, when pro-
truded, to complete an ovoid of labial margins
in a single plane (Figure 6). Such a structure
in contact with a smooth surface enables the

Figure 6. — A demonstration of the coraoohyoideus mus-
cles of Isistitis. Note also the protruded lips, the in-
ternal openings of the spiracles, and the mandibular
teeth.

shark to form a vacuum when the spiracles are
closed and the tongue then retracted.

In order to further determine if behavioral
retraction of the tongue was probable, dissec-
tions were made of the ventral surface of the
.shark ju.st posterior to the mandible. The
paired coracohyoideus muscles that insert on the
tongue were unusually large in Isistius (Figure

Fir.URE 7. — Exposed coracohyoideus muscles of a large
whitetip shark, central Pacific.

6). A comparative dissection of a large, fresh,
whitetip shark, Carcharhinus longimanus
(Poey) was made (Figure?); the cross section-
al areas in Isistius were estimated to be four
times those of the same muscles in the whitetip
shark, both relative to the total lengths of the
sharks. Pulling caudad on the exposed coraco-
hyoideus muscles of Isistius caused the tongue
to retract to the nearly vertical ])Osition noted
before; concurrently, the mouth gaped and the
lilJs protruded. The tongue of the whitetip
shark was not movable and pulling on the cor-
acohyoideus muscles did not retract it.

Later I attemtited to repeat Fowler's experi-
ment by holding the mouth of a living Isistius
against the side of a gempylid fish. In this case,
the shark did not make a biting motion but. in-
stead, the spiracles closed, the head flattened
slightly, and an oral vacuum was formed by
means of which I was able to lift the gempylid
from the table with no other support.

It seemed that the remaining evidence needed
to indict Isistius would be the presence of hemi-
spheroidal i^lugs of fish flesh in their stomach
contents. This evidence was found when two
IsistiN.<; caught subsequently on the same cruise
were found to contain single plugs of flesh of
aiipropriate size and shai)e. One of these jilugs
was from a relatively large fish, judging from
the thickness of the myomeres; the other was
from a squid. During a later cruise in the same
area, Reginald M. Gooding, fishery biologist,

794

JONES: PROBABLE CAUSE OF CRATER WOUNDS

Figure 8. — A hemispheroidal plug of unidentified fish
flesh from the stomach of an Isistiiis, central Pacific.

found a very fresh plug of fish flesh complete
with integument and some scales (Figure 8).
The fishes from which these plugs were bitten
have not been identified. In order to find such
plugs, it is necessary to examine Isistins imme-
diately after capture because digestion will usu-
ally continue for a time after the specimen is
placed in formaldehyde or a freezer.

DISCUSSION

Further evidence relating Isistins to wounds
on fishes may be present in a photograph (Fig-
ure 9) of a crescentic wound on the caudal fin
of a swordfish (M. R. Bartlett, personal commu-
nication). The deep crescentic cut is opposed
by an arc of small dents and scars. The size
and arrangement of these correspond to the
small, hooked upper teeth of Isistius (Figure 6) .
In addition, a series of white scratches extending
from the small arc toward the crescentic cut ap-
pear to have been made by the upper teeth as
the shark backed away from the incomplete bite.
In this case, the shark's mandibular teeth must
have encountered the large, bony ray in the edge
of the caudal fin. The same fin bore an entire,
cut-out wound near the posterior border (Fig-
ure 10).

The geographical distribution of records of
Isistius brasilie7isis (Strasburg, 1963; Parin,
1964) corresponds well with the general distri-
butions of the s]iecies of fishes which bear crater
wounds. Several authors (Mackintosh and

Figure 9. — A crescentic wound on the caudal fin of a
swordfish caught in the Gulf of Mexico. Note the arc
of small dents opposite the cut, and the scratches pro-
duced by the shark's upper teeth as it backed away from
the incomplete wound. (Photo by Martin Bartlett.)

Wheeler, 1929; Pike, 1951; Nemoto, 1955; van
Utrecht, 1959) have noted that fresh wounds
were seen only, or more frequently, on cetaceans
caught in the warmer waters of their migrations
and that those caught more poleward bore only
healed or partially healed scars. This was evi-
dence, they stated, that the animal producing
the wounds was an inhabitant of warm water.

Some wounds on cetaceans described in the
literature were undoubtedly produced by lam-
preys (Pike, 1951). The majority of catch
records of lampreys in both the Pacific and At-
lantic, however, are near shore and in temperate
or cold waters which fits poorly the distribution
of fishes and whales bearing fresh crater
wounds.

The largest crater wounds recorded (Mack-
intosh and Wheeler. 1929) were 4 or 5 cm by
7 cm. The smallest I have seen were 1.2 cm
by 2 cm. The smaller diameters of these cor-
respond well with the bite-widths I have esti-
mated for Isistiws at the extremes of the known
range of 14 to 50 cm, total lengths (Strasburg,
1963).

All of the Isistius stomachs examined aboard
the Town-send Cromn'ell contained squid beaks
and pieces of squid pens. Strasburg (1963) also

795

FISHERY BULLETIN: VOL. 69, NO. 4

Figure 10. — The caudal fin of a swordfish caught in the
Gulf of Mexico, showing a crescentic wound and a com-
pleted wound cut through the trailing edge of the fin.

found squid remaiiLs in most of the stomachs
of preserved specimens he inspected, and calcu-
lated that the squids which were eaten were as
large or larger than the sharks. He wondered
how small sharks that apparently swim slowly
could catch and capture such large, swift prey.
This question is also pertinent in considering
how IsLstius succeeds in contacting fast-swim-
ming animals such as tunas, marlins, or por-
poises. It would appear to be no problem for
Isistius to approach and make contact with
basking or drifting whales or fishes. In the case
of tunas, however, there is no evidence that they
ever drift or stop swimming (Magnuson. 1970).

A possible sequence is that the potential prey,
seeing Isistius as an object apparently suitable
for food, makes the initial approach, identifies it
at a short distance, rejects it as food, and veers
off. At that instant, the shark may be able to
achieve contact by means of a short dash.

It is also possible that the shark, to some de-
gree, simulates other organisms such as squids
in the pattern of its luminous ventral surface.
A more remote possibility is that Isistius is mis-
taken by large teleosts for a cleaner, and is in-
vited to make contact.

Large squids appear to be killed by Isistius
more often than merely deprived of plugs of
flesh. It may be that squids also make an ini-
tial approach but, unlike teleosts, do not veer
off from their attack and are subsequently bested
in the encounter.

Isouchi (1970) provided the only record of
an Isistius eaten by a large teleost when he found
a living shark in the stomach of Scomheromorus
sp. This record indicates that Isistius is a po-
tential food item; on the other hand, records
of teleosts having ingested any species of small
or young sharks are limited to five or six (S.
Springer and M. R. Bartlett, personal commu-
nications) . This certainly supports a hypothesis
of usual rejection. Rejection of the young as
food by teleosts, in fact, may account for the
survival of most elasmobranch species, consider-
ing their extremely low reproduction rates and
relatively low swimming speeds.

It may not be necessary to assume any compli-
cated behavior patterns of Isistius or its prey;
perhaps contacts by means of short dashes can
be made during chance proximities. Thomas
Dohl, The Oceanic Institute, Hawaii, has in-
formed me that young porpoises of sizes that are
assumed to be still nursing do not bear wounds
or scars, but those which are larger do. Similar
restriction of wounds and scars to older por-
poises is suggested by the data of van Utrecht
(1959). This may be simply a matter of an
increased jirobability of encounter with time;
but it may, on the other hand, indicate that
porpoises are not attacked by Isistiiis until the
pori)oises become predatory on fish.

Several crescentic wounds which I have exam-
ined on tunas were made from a frontal attack

796

JONES; PROBABLE CAUSE OF CRATER WOUNDS

Figure 11. — An excised crescentic wound superimposed
over a diagram of a skipjack tuna to indicate that the
wound was made from a frontal attack, central Pacific.

position, that is, the shark and its prey were
going in opposite directions when the wound was
inflicted (Figure 11). Such crescentic wounds,
as previously pointed out, are apparently the re-
sult of circumstances which do not allow the
shark to complete the scooping out process. Be-
sides providing support for the suggestion that
the teleost makes the initial approach, the evi-
dence of frontal attacks may explain the occur-
rence of wounds in which the plug of flesh is
still attached to the bottom of the wound by a
peduncle. Such wounds are common on ceta-
ceans (Mackintosh and Wheeler, 1929; van
Utrecht, 1959) . In a frontal attack, the drag of
water on the shark's body would cause it to ro-
tate, in the manner of the hand of a clock, around
the point of attachment until the shark was ori-
ented in the same direction as its prey. This
movement would cause the mandibular teeth to
act in the manner of a melon-ball cutter and, if
penetration was adequate, the crater wound
would be completed.

To explore this possibility, I employed a nec-
tarine (Persicum sp.) from the ship's galley
since no large, dead fish was available at the mo-
ment. I pushed the teeth of a fresh, dead Isisthis
into the fruit and then rotated the body around
that point. The result (Figure 4) was a neat,
round, crater "wound" and the hemispheroidal
"plug" in the shark's mouth with the small,
hooked upper teeth securing it. If tooth penetra-
tion had been inadequate during such a sequence,
the integument would be cut completely around
but the plug would remain attached by a central
peduncle. Necrosis of the plug would probably

follow, resulting in conditions described by
Mackintosh and Wheeler (1929). They present-
ed a hypothetical sequence beginning with a
crescentic wound which developed, by gradual
erosion of the flesh, to the open pit stage. The
"flabby" pedunculate plug, they believed, was a
stage in the healing process and was sloughed
off near the completion of healing.

They pointed out that the most obvious cause
of crescentic and open pit wounds was the bite
of some fish, but no fish known to them possessed
teeth or a mouth structure which would produce
such wounds. They, therefore, returned to the
assumption that the wounds were a result of
microbial infections.

Except in the cases of attacks on squids when
the prey is killed, it appears that Isistiiis, in bit-
ing pieces out of living cetaceans and fishes,
qualifies as a temporary parasite in the same
sense that a mosquito does.

ACKNOWLEDGMENTS

I want to acknowledge the contributions of
many persons who provided unpublished rec-
ords, specimens of wounds and scars, photo-
graphs, as well as ideas and encouragement
during the preparation of this manuscript. My
special thanks are extended to John D. Fowler,
Jr., NMFS, HAFRC, who initiated the important
experiments at sea.

LITERATURE CITED

Bane, G. W.

1969. Parasites of the yellowfin tuna, Thunnus
albacares, in the Atlantic Ocean. Wasmann J.
Biol. 27: 163-175.

COLLETT, R.

1886. On the external characters of Rudolphi's
rorqual (Balaenoptcra borealis). J. Zool. (Lon-
don), p. 24.3-265.
Gakrick, J. A. F., AND S. Springer.

1964. Isistius plutodus, a new squaloid shark from
the Gulf of Mexico. Copeia 1964: 678-682.
GlIITART M., D.

1964. Biologia pesquera del Emperador o Fez de
Espada, Xiphias gladius Linnaeus (Teleostomi:
Xiphiidae) en las aguas de Cuba. [In Spanish,
English synopsis.] Poeyana, Ser. B 1, 37 p.

797

FISHERY BULLETIN: VOL. 69, NO. 4

ISOUCHI, T.

1970. A cigar shark, Isistins brasiliensis from
tropical water of the eastern Pacific. [In Jap-
anese, English abstract.] Jap. J. Ichthyol. 17:
124-125.

IVERSEN, E. S.

1959. Pelagic puzzle. Sea Frontiers 5: 175-178.

Klawe, W. L.

1966. Observations on the opah, Lampi-is regiiis
(Bonnaterre). Nature (London) 210: 965-966.
Machado Cruz, J. A.

1969. Tentativa de diagnostico etiologico de feridas
em atuns - Thnnniis albacares (Bonnaterre) -
de Angola. [In Portuguese, English synopsis.]
Junta Invest. Ultramar Estud. Ensaios Doc. 15,
8 p. + 6 fig.

Mackintosh, N. A., and J. F. G. Wheeler.

1929. Southern blue and fin whales. Discovery
Rep. 1: 257-540 -f 64 plates.
Magnuson, J. J.

1970. Hydrostatic equilibrium of Euthynmts af fin-

is, a pelagic teleost without a gas bladder. Copeia
1970: 56-85.
Nemoto, T.

1955. White scars on whales. (1) Lamprey marks.
Sci. Rep. Whales Res. Inst. Tokyo 10: 69-77.
Parin, N. V.

1964. Data on biology and distribution of pelagic
sharks Enprotomicrus bispinatus and Isistius
brasiliensis (Squalidae, Pisces). [In Russian,
English summary.] Akad. Nauk SSSR Tr. Inst.
Okeanol. 73: 163-184.
Pike, G. C.

1951. Lamprey marks on whales. J. Fish. Res.
Board Can. 8: 275-280.
Strasburg, D. W.

1963. The diet and dentition of Isistius brasiliensis,
with remarks on tooth replacement in other
sharks. Copeia 1963: 33-40.
Van Utrecht, W. L.

1959. Wounds and scars on the skin of the com-
mon porpoise, Phocaena phocaena (L.). Mam-
malia 23: 100-122.

798

THE RELATIVE IMPORTANCE OF NANNOPLANKTON AND
NETPLANKTON AS PRIMARY PRODUCERS IN THE CALIFORNIA

CURRENT SYSTEM

Thomas C. Malone'

ABSTRACT

Nannoplankton and netplankton primary productivity and standing crop were measured on a seasonal
basis in Monterey Bay (October 1969 to February 1971) and along four transects of the California Cur-
rent between lat 35° and 50° N. Nannoplankters accounted for 60 to 99% (mean =: 86%) of the ob-
served productivity and standing crop both inshore and offshore under oceanic conditions. Seasonal
and geogi-aphical variations in the nannoplankton fraction were remarkably stable, and variations in
phytoplankton productivity and standing crop were due primarily to the netplankton. The assimilations
ratios of both fractions were relatively constant.

Increases in the netplankton fraction were closely coupled with the occurrence of coastal upwelling,
and netplankton productivity and standing crop e.xceeded that of the nannoplankton only during the
strongest upwelling pulses. These increases were probably due to the suspension effect of positive ver-

tical advection and to increases in ambient NO<,-N concentrations above 1 to 3

/i"

Decreases were in

response to increases in grazing pressure and downward water movements. A model is suggested to ac-
count for the following observations: (1) the nannoplankton fraction varied within narrow limits com-
pared with the netplankton; (2) nannoplankton assimilation ratios (and presumably growth rates)
were consistently high and twice those of the netplankton; and (3) netplankton productivity and stand-
ing crop increased relative to the nannoplankton during periods of upwelling. The model is based on the
response of particles of varying sinking rates to vertical and horizontal advection, and on the degree of
coupling between the production of organic matter by primary producers and grazing by primary con-
sumers.

The phytoplankton can be divided into two size
classes based on their retention by fine mesh
nets (aperture size 20 to 90 /x) . Those retained
are commonly called "netplankton" while those
which escape are referred to as "nannoplank-
ton." Seasonal and geographic variations in
netplankton and nannoplankton primary produc-
tivity and standing crop are neither well docu-
mented nor understood. Previous investigations
in both temperate (Yentsch and Ryther, 1959;
McAllister et al., 1959; Gilmartin, 1964; Ander-
son, 1965) and tropical marine environments
(Steeman Nielsen and Jensen, 1957; Holmes,
1958a; Teixeira, 1963; Saijo and Takesue, 1965;
Malone, in press a) have demonstrated that the
nannoplankton are usually responsible for 80 to
100% of the observed phytoplankton productiv-
ity and standing crop. Netplankton produc-

' Department of Biology, The City College, City Uni-
versity of New York, New York, N.Y. 10031.

Manuscript accepted June 1971.
FISHERY BULLETIN: VOL. 69, NO.

tivity is often higher in neritic than in oceanic
waters (e.g., Steemai^Nielsen and Jensen, 1957;
Malone, in press a) but rarely exceeds that of the
nannoplankton. However, neritic phytoplank-
ton communities dominated by the netplankton
in terms of cell number (Digby, 1953) and chlo-
rophyll concentration (Subrahmanyan and Sar-
ma, 1965) have been reported.

The ecological significance of these two size
classes lies in the role of cell size and surface
area-to-volume (A/V) ratios in the dynamics of
phytoplankton productivity and energy flow
through pelagic food chains. Small cells gen-
erally have shorter generation times and higher
growth rates in a given environment than do
larger cells (Findenegg, 1965; Williams, 1965;
Eppley and Sloan, 1966; Eppley and Thomas,
1969; Eppley et al., 1969). Recent observations
on the kinetics of nutrient uptake by phytoplank-
ton (Eppley et al., 1969) indicate that the half-
saturation constants (Ks) for nitrate and ammo-

799

FISHERY BULLETIN: VOL. 69, NO. 4

nium uptake vary in proportion to cell size, pre-
sumably a consequence of the high A/V ratios
of smaller cells (Munk and Riley, 1952). Some
evidence is also available that niaximum uptake
rates ( Vm) , while not species specific, do increase
with increasing cell size (Dugdale, 1967; Ep-
pley et al., 1969) so that netplankters with high
Ks and Vm values would be favored when nitrate
concentrations are high while nannoplankters
with low Ks and V,„ values would be favored
when nitrate concentrations are low.

High A/V ratios facilitate suspension (Munk
and Riley, 1952; Smayda and Boleyn, 1966a,
b; Eppley et al., 1967) increasing the potential
residence times of cells in the photic zone under
stratified conditions. Also, since sinking rates
generally increase as cell size increases, larger
cells will tend to be concentrated in regions of
upward water flow while smaller cells will be
distributed along a gradient toward regions of
downward water flow (Stommel, 1949; Semina,
1968). In this way, small cells will tend to be
spread over a greater volume than larger cells,
and motile cells seeking to maintain their po-
sition in the water column will be concentrated
in regions of downward flow (Hutchinson,
1967).

In addition, the distribution of productivity
and biomass among diff'erent size classes of phy-
toplankton should be reflected in the distribu-
tions and abundances of herbivores which
selectively graze on the basis of particle size.
Nannoplankters appear to be the preferred food
of many planktotrophic larvae (Bruce et al.,
1940; Thorson, 1950) and microzooplankton
(Beers and Stewart, 1969; Parsons and Le Bras-
seur, 1970), while herbivorous copepods actively
select netplankton species (Harvey, 1937; Mul-
lin, 1963; Conover, 1966; Mullin and Brooks,
1967; Richman and Rogers, 1969). Phytoplank-
ton cell size may also aflfect the efliciency of ener-
gy transfer to large predators, since nannoplank-
ton-based food chains appear to require one or
two additional energy transfers to reach a given
sized consumer than do netplankton-based food
chains (Ryther, 1969; Parsons and Le Brasseur,
1970).

The California Current system and Monterey
Bay provide ideal environments in which to

study variations in netplankton and nannoplank-
ton productivity and standing crop, since nu-
trient concentrations and vertical water move-
ments vary markedly both seasonally and geo-
graphically. The California Current system is
discussed by Reid et al. (1958) , and the monthly
mean charts of geostrophic flow have been pre-
pared by Wyllie (1966). The southerly flow of
the California Current is typically strongest
during the spring and summer when northerly
winds are best developed. At this time the
coastal boundary of the Current is marked by
upwelling. During the fall and winter northerly
winds are weak or reversed, and a coastal coun-
tercurrent (the Davidson Current) often devel-
ops between the California Current proper and
the coast. Thus, the hydrography of the coastal
region off' California is generally characterized
by upward water movements and high nutrient
concentrations during the spring and summer,
and downward water movements and low nutri-
ent concentrations during the fall and winter.
The annual cycle of hydrographic conditions
in Monterey Bay has been described by Bolin
and Abbott (1961) and Bolin (1964). Skogs-
berg (1936) divided the annual cycle in the up-
per 100 m into three hydrographic periods:

1. An Upwelling Period (March to Septem-
ber) characterized by low surface temper-
atures (9.5° to 11.5° C), high salinities
(33.2 to 33.9;^f), and high nutrient concen-
trations (>2.0 fxM POj-P, >5.0 /iM NOs-N,
and >10.0 fiU SiO^-Si).

2. An Oceanic Period (September to Novem-
ber) characterized by high surface temper-
atures (12.0° to 15.0° C), decreasing salin-
ities (33.0 to 33.6',',) and low nutrient
concentrations (0.2 to 2.0 jjlm PO^-P, 0.0 to
0.5 fiM NOs-N, and 1.0 to 10.0 /liM SiO.,-Si).

3. The Davidson Current Period (November
to March) characterized by decreasing tem-
peratures (11.0° to 13.5° C), low salinities
(32.4 to 33.2:^,), and low nutrient condi-
tions.

Water of oceanic origin is brought into the Bay
during both Oceanic and Davidson Current Pe-
riods, at first passively as the high density up-
welled water begins to subside and then actively

800

MALONE: RELATIVE IMPORTANCE OF NANNOPLANKTON AND NETPLANKTON

when southerly winds prevail. Since both pe-
riods are characterized by a downward flux of
water (subsidence and downwelling) and low
nutrient concentrations in the upper half of the
photic zone, they will be consolidated and re-
ferred to as the "Oceanic Period."

The purpose of this study is to document tem-
poral and spatial variations in nannoplankton
and netplankton productivity and standing crop
and to evaluate these variations with respect to
dissolved inorganic nitrogen concentrations,
vertical water movements, and grazing pres-
sure.

METHODS AND MATERIALS

Measurements of netplankton and nanno-
plankton primary productivity and standing
crop were made at 17 stations in the California
Current system between lat 35° and 50° N dur-
ing July, August, and November 1970, and at
California Cooperative Oceanic Fisheries Inves-
tigations (CalCOFI) station 3 in Monterey Bay
from October 1969 to February 1971 (Figure 1).
The latter station is located over the Monterey
Submarine Canyon in about 1000 m of water
(lat 36°46.8' N, long 122°01' W) . All data were
collected during cruises of the RV Proteus (Stan-
ford University).

Netplankton and nannoplankton photosyn-
thetic capacities (rate I of carbon fixation as
measured by the carboi>14 technique at light
saturation), chlorophyll-a concentrations, and
cell numbers were estimated from duplicate
water samples collected from 2 m below the
surface with two Van Dorn bottles. The dupli-
cate Van Dorn bottle samples were taken 3 hr
before local apparent noon and again 3 hr after
local noon. Four light and two dark bottles
(a total of 12 125-ml Pyrex bottles) were
drawn from each sample, inoculated with hfic
of Na2"C03, and incubated under fluorescent
light (about 0.06 langley/min) for 2 to 3 hr at
sea-surface temperatures (Doty and Oguri,
1958). Following incubation, half of the light
and dark bottles from each Van Dorn sample
were fractionated by passing the water first
through Nyte.x-net discs with 22-/n apertures
(netplankton) and then through HA Milli-

FlGURE 1. — stations occupied along transects (1-A, B,
2, and 3) of the California Current during July and
August (G) and during November (□), 1970; the
shaded area represents the transition zone between off-
shore and inshore regions.

pore' filters (nannoplankton). The remaining
four light and two dark bottles were HA Milli-
pore filtered directly as controls. The filter discs
were washed with about 30 ml of filtered sea-
water, dried in a CO2 free atmosphere, and their
activity measured with a Nuclear Chicago scalar
(model 161 A) equipped with a model D47 gas
flow chamber with a micromil window. Each
filter was counted for at least 5 min, and rates
of carbon fixation were calculated as described
by Doty and Oguri (1958) after averaging du-
plicate light bottle values. Mean coeflicients of
variation between duplicate light bottles were
6 ± I'^f for the nannoplankton and 26 ± 5%
(95';f confidence limits) for the netplankton.
The mean coefficient of variation between phy-
toplankton productivity values calculated from
the sum of the nannoplankton and netplankton
fractions and the unfractioned controls was 10

± 29r.

' The use of trade names is merely to facilitate de-
scriptions; no endorsement is implied.

801

FISHERY BULLF.TIN: VOL. 69, NO. 4

Samples for pigment analysis were also col-
lected 2 to 3 hr before local apparent noon
from 13 depths between the surface and 100 to
200 m. The upper 6 to 10 depths sampled were
within the photic zone, depending on its depth,
and were chosen on the basis of the thermal
structure of the water column. Sample depths
were evenly spaced through the mixed layer and
evenly but more closely spaced across the ther-
mocline. Samples were always taken at the base
of the photic zone and at two depths below to
at least twice the photic zone depth. Chloro-
phyll-a and phaeopigment concentrations were
determined by a fluorometric technique (Strick-
land and Parsons, 1968). Water samples were
fractionated by the same procedure described
for the carbon-uptake experiments except What-
man GF/C glass fibre filters coated with 2 ml
of I'yr MgCOs suspension were used in place of
membrane filters, and the netjilankton chloro-
l)hyll fraction was calculated from the difference
between fractionated and unfractionated values.
Duplicate values for each fraction were averaged
(mean coefficients of variation were 10 ± 2'"f for
the nannoplankton and 22 ± 8/r for the net-
plankton fraction) . The use of glass filters may
have led to no more than a 10 /f underestima-
tion of nannoplankton chlorophyll-a (Malone,
in press a).

Samples for phytoplankton enumeration and
identification were preserved with Lugol's so-
lution made basic with sodium acetate in place
of acetic acid. Aliquots of 100 ml were placed
in Nessler tubes and the cells allowed to settle
for 72 hr. Depending on the concentration of
cells, from 50 to 90 ml of the supernatant was
then siphoned off and 2 ml aliquots were added
to settling chambers. After 48 hr the samples
were counted by the inverted microscope tech-
nique of Utermohl (Lund et al., 1958). All or-
ganisms longer than about 30 jjl were counted
at 100 V while smaller cells were counted in 100
random fields at a magnification of 400 x . For
lack of better criteria, phytoplankton having di-
mensions of 30 X 22 (U, or less were classified
as nannoplankton and those with larger dimen-
sions as netplankton. This did not present
much of a problem, however, because the nanno-
plankton fraction was dominated by cells whose

longest dimension was in the range of 2 to 15 /n,
while the netplankton fraction was dominated
by chain-forming diatoms with cell lengths of
40 fjL or more, e.g., Nitzschia pacifica. Dominant
netplankton forms were identified to species, and
less numerous forms to genus. The remaining
phytoplankters were cla.ssified as pennate or
centric diatoms, thecate or nonthecate dinoflag-
ellates, coccolithophores, silicoflagellates, or
"others." Mean coefficients of variation be-
tween duplicate samples were 14 ± 4Sf for the
nannoplankton fraction and 27 ± 11 Tl for the
netijlankton fraction.

Standard hydrographic and bathythermo-
graph casts were made 2 to 4 hr before local
apparent noon in conjunction with productivity
and standing crop measurements to estimate the
vertical distributions of dissolved inorganic ni-
trogen compounds, temperature, and density in
the water column. Additional hydrographic
casts made for the CalCOFI Program in Mon-
terey Bay are utilized in this paper. Nitrate con-
centrations were determined by the manual
procedure described by Strickland and Parsons
(1968) and ammonium by the phenolhypochlo-
rite method (Solorzano, 1969). A Secchi disc
was used to estimate photic zone depths (3.5 X
Secchi disc reading) .

The ratio of phaeopigments-to-chlorophyll in
the water column (to 100 m for inshore stations
and to 200 m for offshore stations) was used
as a rough index of relative grazing pressure on
the phytoplankton standing crojj (Lorenzen,
1967; Beers and Stewart, 1969). In the pre-
sent study, a highly significant (P = 0.01) re-
gression of phaeopigment concentration on logio
transformed zooijlankton wet weights was found,
and it was concluded that the phaeopigment-
chlorophyll ratio could be used as a first order
index of grazing pressure.

TEMPORAL VARIATIONS IN
MONTEREY BAY

ENVIRONMENTAL FACTORS

The hydrographic conditions observed at
CalCOFI 3 from October 1969 to February 1971
are summarized in Figure 2 and Table 1. Sur-

802

MALONE: RELATIVE IMPORTANCE OF NANNOPLANKTON AND NETPLANKTON

O N D J

O N D J

Figure 2. — a. Vertical distribution of temperature (°C)
at CalCOFI 3 from October 1969 to February 1971.
b. Vertical distribution of NO3-N (yaM).

Table 1. — Environmental factors monitored at the sur-
face, concurrently with measurements of productivity
and standing crop at CalCOFI station 3 in Monterey
Bay.

Temper-
ature

Salinity

NO3-N

Mixed Photic
layer zona

28 Oct. 69

2 Dec.
26 Feb. 70

5 Mor.
10 Mar.
18 Mar.

°C

14.20
14.68
13.10
13.20
13 17
12.06

33.51
33,39
32.68
32,99
32.98
33.11

1.7
0.3
0.3
0.4
C.l
0.4

li.M

0.3
0.6
0,2
0.4

30
30
50
30
25
15

60
55
60
50
65
30

31 Mar.

11.17

33.49

7.8

0.3

0

25

8 Apr.

10.45

33.65

14.5

0.1

30

45

18 Juno

12.44

33.81

6.5

0.5

10

15

2 July

n.02

33.71

13.9

1,5

0

40

26 July

12.95

33.82

6.5

3.3

0

40

12 Oct.

13.56

33.53

I.l

0.6

0

70

26 Oct.

13.03

33,41

3.1

0.8

30

65

6 Nov.

13.59

32 99

0.7

0,2

40

65

18 Nov.

14,29

33,26

0.2

__

15

60

30 Nov.

13.40

33,28

2.4

45

55

7 Dec .

13,24

33 02

1.3

__

50

55

17 Jan. 71

11.50

33-43

6,6

0,4

50

60

27 Jon.

10.84

33.52

8.7

0,8

20

30

3 Feb.

11.79

33.33

3.8

0.4

15

50

face water of oceanic origin was found in the
Bay from October 1969 to mid-March 1970. The
intrusion of oceanic water and the general sub-
sidence of the water mass are evidenced by the
descending isotherms and nitrate isopleths, high
surface temperatures, and low salinities. Mixed
layer and photic zone depths were about 30 and

60 m respectively, and NO3-N concentrations
were less than 0.5 fiM throughout most of the
photic zone.

Upwelling was initiated in March as indicated
by the ascending isotherms and nitrate isopleths,
NO3-N concentrations in excess of 5.0 fiM over
the entire photic zone, low surface temperatures,
and high surface salinities. With the exception
of a minor intrusion of oceanic water late in July
and early August, upwelling continued uninter-
rupted into September with peaks in early April
and early September. "Mixed layer" depths
varied between 0 and 30 m, and at no time ex-
ceeded the depth of the photic zone, which
ranged from 15 to 45 m.

From September through December the hy-
drography of the Bay was confused and neither
oceanic nor upwelling conditions ever predomi-
nated. Weak upwelling surges bracketed by in-
fluxes of oceanic water occurred during late Oc-
tober and late November (Figure 2). Surface
NO3-N concentrations were variable (0.2 to 3.1
jLiM) reflecting the indecisiveness of the system.
Then, following a period of oceanic water during
December and early January, a strong upwelling
pulse occurred which was about as intense as
the upwelling during late March and early April
of the previous year.

Hydrographically, three periods can be dis-
tinguished in the Bay during the period of this
study:

1. A stable Oceanic Period from October 1969,
into March 1970,

2. A stable Upwelling Period from March into
September,

3. A "Mixed" Period from September through
December punctuated by a strong upwell-
ing pulse in January.

The grazing pressure index declined during
the transition from oceanic to upwelling condi-
tions to a low of 0.03 in early April (Figure 3) .
Grazing pressure then increased rapidly during
the steady upwelling of June and July to an an-
nual maximum of 2.03 which was followed by
a gradual decline during the Mixed Period end-
ing with a sharp rise in late January to a peak
in early February.

803

FISHERY BULLETIN: VOL. 69, NO. 4

Figure 3. — Temporal variations in the ratio of phaeo-
pigments-to-chlorophyll-a (P/C) integrated over the up-
per 100 m at CalCOFI 3.

A s o N D J r

SURFACE PRIMARY PRODUCTIVITY
AND STANDING CROP

Seasonal variations in surface productivity
and standing crop are shown in Figure 4. Since
a significant difference (F-test, P<0.01) w^as
not observed between morning and afternoon
values (see Malone, in press b), only data col-
lected during the morning sampling will be con-
sidered.

Phytoplankton productivity and standing
crop remained below 5.0 mgC m"^ hr~S 1.00
mgChl-a m~^, and 3.5 X 10^ cells/liter during
the Oceanic Period. Values above 10.0, 1.50,
and 10.0 x 10° were observed only during the
Upwelling Period and the January Upwelling
pulse. The Mixed Period was characterized by
intermediate levels of productivity and standing
"■crop. Three peaks were observed, of which the
two greatest coincided with the two most intense
upwelling pulses: (1) 50.4 mgC m"^ hr~', 7.92
mgChl-a m"^ and 24.2 x lO'* cells/liter on the
last day of March, and (2) 43.4, 10.46, and 23.9
X 10'^ during the last week of January. The
third, less pronounced peak, was in mid-June
^during steady upwelling.

Figure 4. — a. Temporal variations in surface netplank-
ton ( ■ ) and nannoplankton ( □ ) productivity (mgC
m-3 hr-i) and the net/nanno ratio (O) at CalCOFI 3.
b. Temporal variations in surface chlorophyll-a (mg
m^') and the net/nanno ratio, c. Temporal variations
in surface cell numbers, the net/nanno ratio, and the
ratio of dinoflagellates-to-diatoms ( A ) .

804

MALONE: RELATIVE IMPORTANCE OF NANNOPLANKTON AND NETPLANKTON

Phytoplankton assimilation ratios (mgC hr~'
mgChl-a"') were relatively constant, with most
values falling between 5 and 10 (mean =r 7.4
± 1.0, 95'^'e confidence limits). Fluctuations in
the amount of chlorophyll-a per cell (10~^ fig)
were also within comparatively narrow limits.
Values varied from 0.85 to 6.97 with a mean of
2.62 ± 0.66.

Surface levels of nannoplankton productivity
and standing crop were remarkably stable
through the year. Productivity and standing
crop values were less than 8.0 mgC m~^ hr^S
0.80 mgChl-a m-^ and 3.3 x 10= cells/liter dur-
ing the Oceanic Period. During the Upwelling
Period productivity ranged from 6.6 to 18.6,
chlorophyll-a from 0.46 to 2.44, and cell numbers
from 5.1 to 14.4 X 10^ Thus, while nanno-
plankton productivity and standing crop were
lower under oceanic than upwelling conditions,
the diflferences were not marked.

In contrast, netplankton productivity and
standing crop varied tremendously during the
year, from less than 0.6 mgC m"^ hr~*, 0.14
mgChl-a m~', and 0.1 X 10= cells/liter during
the Oceanic Period to greater than 2.8, 0.40, and
0.6 X 10= during the Upwelling Period. Two
prominent peaks were observed (31.8 mgC m~^
hr-', 6.76 mgChl-a m-^ and 36.8 and 9.83), both
in association with the two most intense upwell-
ing pulses. A secondary peak occurred in mid-
June. Netplankton cell numbers reached suc-
cessive peaks of 24.2, 27.1, and 23.8 x 10= cells/
liter which coincided with peaks in productivity
and chlorophyll-a. During the fall and early
winter Mixed Period, intermediate values were
observed with small peaks associated with each
short burst of upwelling. Thus, netplankton
productivity and standing crop varied from an
order of magnitude less than that of the nan-
noplankton during the Oceanic Period to an
order of magnitude greater during the Upwell-
ing Period. Comparison of mean squares and
ranges of variation (Table 2) clearly demon-
strates that temporal variations in phytoplank-
ton productivity and standing crop were pri-
marily due to the netplankton fraction with the
nannoplankton maintaining a relatively stable
background level.

Variations in the ratio of netplankton-to-nan-

noplankton (net/nanno) are also shown in Fig-
ure 4. The net/nanno productivity ratio never
exceeded 0.3 during intrusions of oceanic water
(either during the Oceanic Period or the Mixed
Period), and was greater than 1.0 on only two
occasions: during the strong upwelling pulses
of late March and late January. The same pat-
tern was found for the net/nanno chlorophyll
and cell number ratios except the chlorophyll
ratios were consistently higher and the cell num-
ber ratios lower than the productivity ratios.
This is reflected in the assimilation ratios and
cell chlorophyll-a content of the two fractions,
both of which were relatively constant during
the study. The mean nannoplankton assimila-
tion ratio of 9.4 ± 1.5 was significantly higher
than the netplankton mean of 4.7 ± 1.3. Simi-
larly, the nannoplankton had more cells per unit
chlorophyll-a than did the netplankton. The
mean chlorophyll-a content per netplankton cell
was 23.6 ± 13.1 x 10" Vs which is significantly
higher than the nannoplankton mean of 1.9 ±
0.5 X 10 -« ng.

Peaks in the ratio of netplankton-to-nanno-
plankton cell numbers coincided with peaks in
netplankton cell number, but the ratio exceeded
1.0 only during the January bloom. This prob-
ably reflects the dominance of the small-celled
(<20 fjL in length), chain-forming diatoms
Chaetoceros socialis and Skeletonema costatum
in the netplankton fraction. In contrast, the net-
plankton blooms of late March and mid-June
were dominated by large-celled (>40 fi in
length) chain-forming diatoms Nitzschia pacif-
ica and Rhizosolenia fragilissima, respectively.
Nitzschia spp., Skeletonema costatum, Leptocyl-
indricus sp., and Chaetoceros spp. accounted for

Table 2. — Mean squares and range factors (maximum/
minimum) for nannoplankton and netplankton produc-
tivity (PP = mgC m-3 hr-'), chlorophyll-a concentra-
tion (mg m~3, m~2)_ and cell numbers (no./liter) at
CalCOFI station 3.

Fraction

Mean squares

nannoplankton
netplankton

PP

16
109

mg m— 3 no./liter
0.2 17
6.5 32

ms m-2

86

1,680

Range factors

nannoplankton
netplankton

9

1,800

12 13
4,200 4,400

4

120

805

FISHERY BULLETIN: VOL. 69, NO. 4

70% of the netplankton in the March bloom. In
mid-June Rhizosolenia spp. and Nitzschia spp.
made up 809 of the netplankton. The nanno-
plankton fraction was dominated by small mo-
nads 2 to 15 jLt in length in all but one of the
samples examined. The one exception occurred
at the peak of the March-April netplankton
bloom when small diatoms dominated the nan-
noplankton fraction. When the net/nanno ratio
was high (during upwelling), diatoms were
more numerous than dinoflagellates; but when
the ratio was low (during oceanic conditions),
dinoflagellates were more numerous (Figure
4c).

VERTICAL DISTRIBUTION OF PIGMENTS

The chlorophyll-a content of the water column
(0 to 100 m) varied between 14 and 30 mg m"-
during the Oceanic Period and between 24 and
152 mg m~2 during the Upwelling Period (Fig-
ure 5). The seasonal pattern of variation was
much the same as that observed for surface

chlorophyll concentrations, but the range of var-
iations was less.

Variations in netplankton and nannoplankton
chlorophyll content of the water column were
also similar to the surface pattern. Nanno-
plankton chlorophyll-a values fluctuated between
the low of 9.6 mg m~^ observed during the
Oceanic Period and the high of 44.2 observed
during the Mixed Period. Water column levels
of netplankton chlorophyll-a, however, were less
than 8.0 during the Oceanic Period and sur-
passed 110 during both strong upwelling pulses.
Again, changes in the phytoplankton chlorophyll
content of the water column and in the net/nan-
no ratio were due primarily to variations in the
netplankton fraction with the nannoplankton
fraction remaining comparatively constant
(Table 2).

The vertical distribution of chlorophyll-a al-
ways exhibited a maximum which was in the
photic zone above or in association with the
phaeopigment maximum. The netplankton max-
imum was always located below the nannoplank-
ton maximum except during strong upwelling
when both maxima occurred in the upper 10 m
of the photic zone (Figure 6). Four stations
have been selected to illustrate the different types
of vertical pigment distributions encountered
(Figure 7). Two basic patterns were observed,
a stable oceanic distribution with low chlorophyll
concentrations and low net/nanno ratios (Fig-
ure 7a) , and an upwelling distribution with high
chlorophyll concentrations and high net/nanno
ratios (Figure 7b). Under oceanic conditions,
the nannoplankton maximum was found in the
upper half of the photic zone, near the bottom of
the mixed layer and in nitrate-poor water

O N D J F

Figure 5. — Temporal variations in netplankton ( B ) and
nannoplankton ( Q ) chlorophyll-a content of the water
column (mg m-~, 0 to 100 m) and the net/nanno ratio
( G ) at CalCOFI 3.

Figure 6. — Temporal variations in the depths of the
nannoplankton { "^ ) and netplankton ( A ) chlorophyll-a
maxima at CalCOFI 3.

806

MALONE: RELAT1\E IMPORTANCE OF NANNOPLANKTON AND NETPLANKTON

90 no laO liO T.mpl^Ct

mg Chl-am-3
■ 40 30 30 10 0 10

90 no 130 ISO i.mprcl
^^ 20 30 NOj-NluMl

110 130 150 T.mp*-^)

20 30 NO3-N

DO 130 T.mpnci

!£L_, 10 NO,-N

Figure 7. — Vertical profiles of netplankton ( D ) and nannoplankton (□) chlorophyll-a (mg m"^), NO3-N
(^m), and temperature (°C) at CalCOFI 3: (a) Oceanic Period (10 March), (b) Upwelling Period (31 March),
(c) Upwelling Period with peak grazing pressure (26 July), and (d) Mixed Period during post-upwelling sub-
sidence (6 November).

( <0.5 fjiM NO3-N) ; while the netplankton max-
imum was located in the lower half of the photic
zone, in the thermocline, and in nitrate-rich
water (>5.0 fiU NO3-N). Maximum phaeopig-
ment concentrations occurred in association with
or just below the netplankton maximum. With
the onset of upwellincr, the netjilankton maxi-
mum gradually shifted from a depth of 75 m
to the surface (Figure 6). Initially, upwelling
had a dilution effect which was followed by a
rapid increase in the netplankton fraction and
later by a slight increase in the nannoplankton
fraction (Figure 5). The upwelling distribution
observed on March 31 is shown in Figure 7b.
Both netplankton and nannoplankton chloro-
phyll maxima were at the surface and nitrate
concentrations were high (>5.0 (iM NO.-i-N)
throughout the photic zone.

The remaining two examples represent special
cases which evolved from an upwelling distribu-
tion such as the one just described. Figure 7c
shows the distribution observed during late July
that developed over the period of steady upwell-
ing during which the grazing pressure index
increased markedly (Figure 3) . Note that both
netplankton and nannoplankton maxima were
in the upper 10 m, and NO3-N concentrations
were in excess of 5 (jlM throughout the photic
zone; but that the concentration of netplankton
chlorophyll has been greatly reduced and the
net/nanno ratio was low. Phaeopigments were
high with a maximum just below the netplankton
chlorophyll maximum. The distribution shown
in Figure 7d (November 6) developed during
a period of subsidence following an upwelling
pulse. At this time, the netplankton maximum

807

FISHERY BULLETIN: VOL. 69, NO. 4

was near the bottom of the photic zone 30 m
below the nannoplankton maximum; the net-
plankton chlorophyll concentration and net/nan-
no ratio were still high; and NO3-N concentra-
tions were greater than 2 /jlU throughout most
of the photic zone.

GEOGRAPHIC VARIATIONS IN THE
CALIFORNIA CURRENT

ENVIRONMENTAL FACTORS

Four transects across the core of the Current
were made for this study (Figure 1). Tran-
sects 1-A, 2, and 3 were made during late July
and August 1970, and transect 1-B was made
during the first week of November 1970. Cal-
COFI station 3 in Monterey Bay was the inshore
station for transects 1-A and B. The hydro-
graphic conditions observed along these tran-
sects are summarized in Table 3 and Figures 8
and 9.

The July-August transects were made during
a period of coastal upwelling and were charac-
terized by shoreward rising isotherms and ni-
trate isopleths. Based on the upward slope of
these isopleths, upwelling was least intense at

the southernmost inshore station and most in-
tense at the northernmost station, which is typi-
cal for this time of year (Reid et al., 1958).
Nitrate concentrations were high in the upper
half of the photic zone at the three inshore sta-
tions and low at the two outermost stations of
each transect. Ammonium concentrations were
relatively high (>1 /ixM NH4-N) in the photic
zone at the stations of transect 1-A but were
low (typically 0.1 to 0.5 fiM) throughout the
water column at most of the remaining stations.
The surface mixed layer was never observed to
extend below the photic zone, inshore or oflfshore.
An undercurrent was present below the thermo-
cline between stations 5 and 8 of transect 1-A
as indicated by the spreading isotherms (cf.
Wooster and Gilmartin, 1961). Based on the
temperature (Figure 8) and nitrate profiles
( Figure 9 ) , the stations along each transect were
divided into three groups:

1. Stations within about 100 km of the coast
were classified as inshore (stations 3, 61,
and 63),

2. Stations between 100 and 250 km offshore
were classified as transitional (stations 8,
55, and 67),

Table 3. — Environmental factors monitored concurrently with measurements of productivity and standing crop in
the California Current system between lat 35° and 50° N.

Stotion

Date

Di stance
from
land

Temper,
oture

Salinity

NO3-N

NHi-N

Mixed
layer

Photic
zone

km

°C

%.

llM

^M

m

m

03a

24 July 70

15

12.95

33.82

6.5

3.3

0

40

08

27 July

155

14.88

33.11

1.3

1.4

20

65

15

29 July

470

17.69

32.95

0.2

1.8

30

105

24

31 July

675

18.49

32.88

O.I

1.7

20

100

33

2 Aug.

535

18.03

32.51

0.0

0.4

0

115

61

9 Aug.

30

11.98

33.38

8.8

0.7

10

40

SS

7 Aug.

130

16.04

31.88

0.1

0.0

10

65

A6

5 Aug.

310

17.25

32.08

0.1

0.4

15

105

38

3 Aug.

485

18.25

32.79

0.1

0.3

15

95

63

IS Aug.

70

11.55

33.00

0.3

0.5

10

15

67

16 Aug.

150

14.91

32.62

0.7

0.2

30

75

73

18 Aug.

315

1724

3204

0.1

0.5

20

55

84

20 Aug.

450

17.07

3257

0.2

0.1

30

90

88

22 Aug.

280

15.82

3247

0.1

0.3

20

80

03a

6 Nov.

15

13.59

32.99

0.7

0.2

40

60

14

5 Nov.

90

14.58

32.98

0.0

0.5

20

65

05

2 Nov.

150

14.38

3281

0.1

0.7

20

50

12

4 Nov.

225

14.74

32.62

0.2

0.1

15

60

08

3 Nov.

290

15.31

32.46

0.1

1.0

15

60

a CalCOFI station 3.

808

MALONE: RELATIVE IMPORTANCE OF NANNOPLANKTON AND NETPLANKTON

0>»(onc« from lond (I"")
200 300 400

20

i! ^ .vv'* ^»

38

^

^^:^

-17____

'0

^^=^

— '«— — ^
15-

60

x-<:^

^

13

--.„,___^ C

80

^\ 1

^~-~~12 (

100

\

V ^\

^^M

120
UO

A

a

9

^""^10,^^

Figure 8. — Vertical distribution of temperature (°C)
along four transects of the California Current system
with the depths of the nannoplankton ( O ) and net-
plankton ( A ) chlorophyll-a maxima: (1-A) along lat
37° N in July, (2) along lat 40° N in August, (3)
along lat 44° N in August, and IB along lat 36°40' in
November. Vertical lines represent stations.

(l-A)

Figure 9.— Vertical distribution of NO3-N (fiM) along
four transects of the California Current system with the
depths of the nannoplankton ( O ) and netplankton ( A. )
chlorophyll-a maxima.

809

FISHERY BULLETIN: VOL. 69, NO. 4

3. Stations greater than 250 km from the
coast were classified as offshore (stations
15, 24, 33, 46, 38, 73, 84, and 88).

Transect 1-B was made at a time when the
Davidson Current is usually developed (Bolin,
1964). The inshore station (CalCOFI 3) was
occupied during an oceanic phase of the Mixed
Period, and subsidence is evidenced by the down-
ward trend of the isotherms and nitrate iso-
pleths (Figures 2, 8, and 9). Surface temper-
atures were comparatively high and nitrate
concentrations low. The Davidson Current was
developed at stations 3 and 14, and the transition
from Davidson to California Current Water oc-

curred between stations 14 and 12 with a surface
divergence probably located between stations 5
and 12. Station 8, the outermost station, was
in the California Current proper.

SURFACE PRIMARY PRODUCTIVITY
AND STANDING CROP

During the July-August transects, when coast-
al upwelling dominated the hydrographic regime
of the California Current system, phytoplankton
productivity and chlorophyll-a concentrations
decreased markedly with distance from land
(Figure 10). Inshore, productivity and chlo-
rophyll ranged from 6.62 to 61.6.5 mgC m^^ hr~'
and from 0.8 to 11.5 mg m~^, respectively. Pro-

15 24 33 46 38 73 84 88
Offshore

Figure 10. — a. Inshore-offshore variations in surface netplankton ( ■ ) and nannoplankton ( □ ) productivity
(mpC m~5 hr~') during tlie .July-August transects and the Novcmljer tran.scct (inset), b. Inshore-offshore
variations in surface netplankton and nannoplankton chlorophyll-a (mg m~^).

810

MALONE: RELATIVE IMPORTANCE OK NANNOPLANKTON AND NETPLANKTON

ductivity and chlorophyll concentrations off- it was located near the boundary between the
shore, however, exceeded 1.0 mgC m^^ hr"' and Davidson and California Currents which is
0.10 mgChl-a m-^ only once. The highest levels marked by a surface divergence and associated
of productivity and chlorophyll were found at upwelling. In this connection, it is also note-
inshore station 63 and were equivalent to the worthy that nannoplankton productivity and
maximum values observed at CalCOFI 3 during chlorophyll levels were about twice those ob-
the two most intense upwelling pulses. served previously for transitional and offshore

This inshore-offshore decrease in surface pro- regions,

ductivity and chlorophyll was not observed over Phji;oplankton assimilation ratios were simi-

the first 225 km of the November transect when lar to those observed at CalCOFI 3, most values

subsidence rather than upwelling characterized. falling between 5 and 10. Excluding inshore

the coastal hydrographic regime. Productivity stations, the mean assimilation ratio was 7.7 ±

and chlorophyll concentrations were relatively 1.1, which is not significantly different from the

constant out to station 12 (Figure 10) and cor- mean observed at CalCOFI 3. Nannoplankton

responded with the minimum values observed ratios averaged 8.3 ± 1.2 v.'hich is twice the ob-

at CalCOFI 3 during the Oceanic Period. served mean netplankton ratio of 4.1 ± 0.8.

Both nannoplankton and netplankton produc- Both means are equivalent to those observed at

tivity and chlorophyll decreased markedly be- CalCOFI 3.
tween inshore and offshore stations along the

July-August transects (Figure 10). Nanno- VERTICAL DISTRIBUTION OF PIGMENTS
plankton values fell by as much as an order of

magnitude from above 4.0 mgC m-^ hr-> and Inshore-offshore variations in the chlorophyll-

0.60 mgChl-a m-^ to less than 1.2 and 0.18, re- ^ content of the water column (0 to 200 m) dur-

spectively. The netplankton, however, exhibited i„or the July-August transects were similar in

the greatest decline. Netplankton productivity trend but less in amplitude than that observed

decreased by 2 to 3 orders of magnitude from ^t the surface. Inshore, chlorophyll varied from

1..5 to 51.3 mgC m-3 hr"' to offshore levels of 27.32 to 217.68 mg m-^ compared with the
0.01 to 0.26. Similarly, netplankton chlorophyll
values were 0.12 to 10.14 mg m~' inshore and

0.002 to 0.052 offshore. This decline in the net- ^ , ., ,

,,, J. .. ,,. iii iii Table 4. — Netplankton-nannoplankton ratios in the Cal-

plankton fraction relative to the nannoplankton :f^^„:^ r„rv»„t c„o+ ■ ^ *• ■! Vdd

' ,. rr \ ^ A\ iiornia Current system: primary productivity (PP =:

is reflected m the net/nanno ratios (lable 4). ^igC m-3 hr-'), chlorophyll-a m-^ and chlorophyll-a

Inshore productivity ratios ranged from 0.23 to m-2.

4.95, while offshore ratios varied from 0.02 to ^;^„ i ^ \ —, 1 ~,

0.36. Chlorophyll ratios followed the same pat- 03 023 ^ ^-j^

tern but tended to be higher. os 0.30 o.48 0.36

The pattern observed in November was quite 24 0 02 0 05 oh

different. Levels of netplankton productivity ~ ~ ^3 o.n 0.22 006

and chlorophyll were low along the entire tran- "^i '^^ --^

sect and were within the range commonly found ss 0.09 0.19 0.I6

offshore and during oceanic phases inshore (Fig- 33 g,, °27 H^

ure 10). Nannoplankton productivity declined ^ ■^9"] 73"; -g-

slightly from an inshore maximum of 3.20 to <>^ 0.03 o.is 0.33

an offshore minimum of 1.21. Variations in sur- 34 03^ °'32 g^^

face chlorophyll were similar except the maxi- 83 00"^ ^^ ~^

mum of 0.40 was observed at station 5 which is 03 0.07 017 T12

150 km from shore. Station 5 is particularly in- 11 002 010 0 is

teresting because netplankton productivity and 12 o!o3 0 1^ 0I0

chlorophyll also exhibited small peaks here, and °3 om oj7 0 16

811

FISHERY BULLETIN: VOL. 69, NO. 4

offshore range of 10.72 to 25.96 mg m-^ (Figure
11). In November the pattern was much the
same, with an inshore maximum of 66.64 and an
offshore level of 23.20.

Nannoplankton chlorophyll in the water col-
umn showed little variability (Figure 11). In-
shore levels of nannoplankton chlorophyll varied
from 17.49 to 31.94 mg m -, while offshore levels
ranged between 9.63 and 21.76. The netplank-
ton fraction underwent much greater fluctua-
tions (Figure 11). Inshore concentrations
ranged between 3.26 and 185.74 in contrast to
the offshore range of 1.00 to 4.97. The latter
range is equivalent to that observed at Cal-
COFI 3 during the Oceanic Period and the for-
mer to that observed during the Upwelling Peri-
od. Excluding inshore stations, the mean chloro-
phyll-a concentration of the nannoplankton f rac-

3 61 63
Inshore

Figure 11. — Inshore-offshore variations in the netplank-
ton ( ■ ) and nannoplankton ( □ ) chlorophyll-a content
of the water column (mg m~-, 0 to 200 m) during the
July-August transects and the November transect
(inset).

tion was 16.55 ± 2.38 which is significantly
higher (P — 0.05) than the netplankton mean
of 3.08 ± 0.81.

The vertical distributions of chlorophyll-a and
phaeopigments at the offshore stations of the
July-August transects were characterized by a
subsurface maximum located at the base of the
photic zone, in the lower part of the thermocline,
and near the upper reaches of the nitrate-rich
layer (Figure 12). Netplankton and nanno-
plankton chlorophyll maxima were usually locat-
ed near each other, but the netplankton maxi-
mum was not always deeper than the nanno-
plankton maximum. Netplankton chlorophyll
was more evenly distributed and concentrations
were much lower than in inshore waters (com-
pare Figures 7 and 12) . Both maxima gradually
decreased in depth shoreward from between 80
and 100 m offshore to 10 m or less at the inshore
stations paralleling the upward trend of the iso-
therms (Figure 8) and nitrate isopleths (Fig-
ure 9).

The pattern was much different during the
November transect (1-B). The netplankton
maximum was always located below the nanno-
plankton maximum, especially at the inshore
station where the netplankton maximum was
30 m below the nannoplankton maximum (Fig-
ure 7d). Both maxima decreased in depth sea-
ward to station 5 (Figures 8 and 9) where the
vertical distribution conformed to the upwelling
distribution (Figure 12), i.e., netplankton and
nannoplankton maxima were in the upper 10 m
and nitrate concentrations were relatively high
throughout most of the photic zone. Farther off-
shore the depth of the chlorophyll maxima in-
creased once again. This up and down move-
ment of the maxima closely i^aralleled the depth
variation of the isotherms and nitrate isopleths
just as during the July-August transects.

DISCUSSION

The constancy of the phytoplankton assimila-
tion ratios both inshore (7.4 ± 1.0) and off-
shore (7.7 ± 1.1) suggests that nutrients were
rarely limiting to primary productivity (Dick-
man, 1969) . The mean assimilation ratios found
are close to the value of 7.3 reported by Holmes
(1958b) in the nutrient-rich waters of the Costa

812

MALONE: RELATIVE IMPORTANCE OF NANNOPLANKTON AND NETPLANK.TON

mg Chl-o m^ 9 11

2 10 1 2

01 m I (,.^)

Sio 15

/

1

Photic

\ Zone

/

\

\

mg Chl-o m^
2 10 12

mg Chl-o

1 _0 L

(1-B)
Slo 5

TempCc)

Temp(°C)
.^Oj-NCmM)

Temp(^)
S03-N(/uM)

Phoeo mg m*^

Figure 12. — Vertical profiles of netplankton ( D ) and nannoplankton ( □ ) chlorophyll-a (mg m-3),
phaeopigments (mg m"'), NO3-N (^m), and temperature (°C) : transect 1-A, station 15, off-
shore region; transect 3, station 84, offshore; transect 1-B, station 5, transition zone.

813

FISHERY BULLETIN: \'0L. 69. NO. 4

Rica Dome (incubator light intensity about 0.0(5
langley/min) and are not sig-nificantly different
from the mean of 8.6 ± 1.3 found by Curl and
Small (1965) at light saturation based on in situ
measurements. Anderson (1964), working off
the Washington and Oregon coasts, obtained ra-
tios of 1.6 to 9.8 (at about 0.02 langley/min)
with low values occurring during the summer
when nutrient concentrations were low and high
values during the spring bloom when nutrient
concentrations were high. In the eastern trop-
ical Pacific, Thomas (1970) andMalone (in press
a) found that assimilation ratios were signifi-
cantly less in nitrogen-poor than in nitrogen-rich
waters. These results are consistent with the ob-
servations of Curl and Small (196.5), supported
by McAllister et al. (1964), which suggest that
ratios below 3 are indicative of a nutrient defi-
ciency while those above 5 indicate nutrient-
rich waters.

Both the nannoplankton and the netplankton
exhibited relatively constant assimilation ratios,
but mean nannoplankton ratios were signifi-
cantly higher (9.4 ± 1.5 inshore, 8.3 ± 1.2 off-
shore) and twice as great as those of the net-
plankton (4.7 ± 1.3 inshore, 4.1 ± 0.8 off-
shore). The constancy of these ratios over a
wide range of productivity values in spite of
large variations in ambient nitrogen concentra-
tions indicates that nutrient concentration was
not an important limiting factor and that the
phytoplankton were adapted to about the same
light intensity over the entire year. This is
conceivable since seasonal variations in day
length and light intensity tend to be dampened
by the seasonal pattern of cloud coverage, i.e.,
the summer months are usually foggy while the
winter months are usually clear. The situation
is similar to that found off La Jolla (Strickland
et al., 1970).

Increases in the productivity and standing
crop of the netplankton fraction and in the net/
nanno ratio were closely coupled with the occur-
rence of upwelling. Each new upwelling pulse,
regardless of duration (CalCOFI 3) or location
(transect 1-B) was marked by an increase in
net/nanno ratios and netplankton standing croj).
Potentially, upwelling can affect phytoi)lankton
productivity in at least two ways: (1) by in-

creasing the residence time of cells in the upper
reaches of the photic zone and (2) by increasing
the rate at which nutrients are supplied to the
photic zone. The settling velocities of phyto-
plankton cells range between 0 and 10 m day~'
(for a review see Smayda, 1970), with most
values falling between 0.5 and 2 m day"' (Ep-
pley et al., 1967; Strickland et al., 1969) . Aver-
age upwelling velocities are of the order of 10 m
day ' (Hidaka, 1954), which is quite sufficient
to inhibit the sinking of negatively buoyant cells.

Since the netplankton fraction was primarily
composed of nonmotile diatoms and the nanno-
plankton fraction of flagellates, it is probable
that vertical water movements will have a great-
er effect on the vertical distribution of netplank-
ton than on the nannoplankton. It is not sur-
prising, therefore, that the depth of the net-
plankton maximum was more closely tied to the
u])ward and downward trends of the isotherms,
both seasonally at CalCOFI 3 (Figure 6) and
along inshore-offshore transects of the Califor-
nia Current (Figure 8). The netplankton max-
imum at CalCOFI 3 was always found below that
of the nannoplankton except during strong up-
welling when both maxima occurred in the upper
10 m. During periods of subsidence the net-
plankton minimum was depressed to greater
depths than the nannoplankton maximum was.
This was observed during the Mixed Period even
though NOa-N concentrations in the surface lay-
ers were still high (>1.0/LiM). The reverse was
observed along transect 1-B in that the netplank-
ton maximum decreased in depth as the zone of
ofli"shore upwelling was approached, moving in
the process from a nitrate-rich layer (>5.0 yuM
NO.i-N) into a nitrate-poor layer (<0.5 yuM
NO:!-N) . The depth distribution of nannoplank-
ton chlorophyll (Figures 6 and 7) was more in-
dependent of vertical water movements and
maximum chlorophyll concentrations were often
found at the su)-face during influxes of oceanic
water (during both Oceanic and Mixed Periods)
when subsidence was most pronounced.

Most of these trends in the depth distriljution
of netplankton and nannoplankton chlorojihyll
could be explained in terms of the vertical dis-
triljution of nitrate in the photic zone. How-
ever, during the early stages of upwelling in

814

MALONE: RELATIVE IMPORTANCE OF NANNOPLANKTON AND NETPLANKTON

March, the iietplankton maximum moved pro-
grressively toward the surface while the chloro-
phyll concentration of the maximum and in the
water column steadily decreased. If this change
in depth was due solely to the upward movement
of the nitrate-rich layer in the photic zone, some
increase in netplankton would have been ob-
served during the time taken for the maximum
to move from a depth of 75 m to 5 m. In addi-
tion, measurements made in the Peru Current,
where vertical advection was not in evidence and
the photic zone was well stratified (Malone,
in press a), support the hypothesis that upward
water movements, in addition to high nitrate
concentrations, are necessary prerequisites for
netijlankton productivity to approach or exceed
that of the nannoplankton. Netplankton pro-
ductivity and the net/nanno productivity ratio
were low despite high nitrate concentrations
(Figure 13).

Two lines of evidence indicate that the net-
plankton and nannoplankton respond differently
to varying nitrate concentrations. The first is

Figure 13. — Mean netplankton ( A ) and nannoplankton
( G ) productivity as a function of mean NO3-N concen-
trations with 95':'i confidence limits: 0.1 ^M, offshore
oceanic region; 0..3 ju.M, CalCOFI 3, Oceanic Period;
1.5 fiM, CalCOFI 3, Mixed Period; 9.2 ^M, inshore up-
welling.

based on the relationship between productivity
and nitrate concentrations encountered in dif-
ferent environments (Figui'elS). Nannoplank-
ton productivity increased rapidly as NO3-N in-
creased from about 0.0 to 0.5 (jlU. Above 0.5
fjLU nannoplankton productivity increased a-
symptotically. In contrast, netplankton produc-
tivity increased slowly over concentrations of
0.0 to 1.5 /AM and then increased rapidly with
concentrations in excess of 1.5 /uM (California
Current system). The netplankton, therefore,
tend to have higher half-saturation constants
and maximum uptake rates for nitrate than the
nannoplankton, so that NO3-N concentrations
above 1 to 3 /xu are necessary before the net-
plankton can effectively compete with the nan-
noplankton. This agrees with the results of
Maclsaac and Dugdale (1969) and Eppley et al.
(1969), which indicate that small-celled oceanic
species in oligotrophic waters have Ks values for
nitrate uptake of less than 0.5 jj-M while large-
celled neritic species in eutrophic waters have Ks
values greater than 1.0 ^iM.

The observed inshore vertical distributions of
netplankton and nannoplankton chlorophyll
were also consistent with these observations.
The netplankton chlorophyll maximum was al-
ways found at depths where NO3-N concentra-
tions were greater than 2 /xm, while during non-
upwelling periods (when concentrations less
than 2 /aM were found in the photic zone) the
nannoplankton maximum occuri'ed at depths
where the NO.rN concentration was between 0.2
and 2.0 fiM. Similar observations were made by
Eppley (1970) who found that diatoms were as-
sociated with relatively high nitrate concentra-
tions at depths where light intensities were high
enough for growth to occur.

Based on these observations, netplankton pro-
ductivity and standing crop will increase relative
to the nannoplankton only when NOa-N concen-
trations above 1 to 3 ;u,M are found in the upper
half of the photic zone and when the netplankton
standing crop is supported in the photic zone by
vertical advection, i.e., upwelling.

Decreases in netplankton standing crop and
net/nanno ratios were related to influxes of
oceanic water and increases in grazing pressure
in Monterey Bay. Variations in phytoplankton

815

FISHERY BULLETIN: VOL. 69. NO. 4

productivity and grazing conformed to what
Gushing (1959) has referred to as an unbal-
anced seasonal cycle of primary production and
primary consumption. Neritic regions in tem-
perate waters are generally characterized by
about a 2-month time interval between peaks
in phytoiilankton and zooplankton biomass
(Gushing, 1959; Heinrich, 1962), with a time
lag of about 1 month between the onset of the
spring bloom and the increase in zooplankton
standing crop. Martin (1965) found a 2-month
lag between the maximum phytoplankton stand-
ing crop and the increase in zooplankton stand-
ing stock.

In Monterey Bay, about 2 months elapsed be-
tween the March-April phytoplankton bloom and
the rapid increase in grazing pressure observed
during June and July (Figure 3) . Although up-
welling was in progress (NO.i-N concentrations
were greater than 5 fj.u throughout the photic
zone and the netplankton chlorophyll maximum
was in the upper 10 m), the phytoplankton chlo-
rophyll content of the water column declined as
grazing pi'essure increased. The netplankton
fraction fell continuously while the nannoplank-
ton dropped at first and then increased (Figure
5). The reduction in standing crop was accom-
panied by a steady decline in the ratio of net-
plankton-to-nannoplankton chloro])hyll in the
water column, from 1.1 near the beginning of
the increase in grazing pressure to 0.1 at its
peak. Thus, it appears that (1) the phyto-
plankton bloom was ultimately limited by graz-
ing; (2) the netplankton fraction, dominated by
Nitzschia spp. and Rhizosolenia spp. {&0'/c of
the netplankton by number), was selectively
grazed; and (3) the cycle of netplankton pro-
duction and animal grazing was unbalanced.

Variations in the net/nanno chlorophyll m~^
ratio were significantly related to concurrent
changes in the nitrate content of the photic zone
(an indicator of upwelling) and to grazing pres-
sure (F = 5.56, P = 0.05) by the multiple re-
gression equation:

net/nanno = 1.76 + 0.003 (NO3-N)
— 2.53 (Phaeo/Chl-a).

This equation is based on 20 sets of data (Cal-
COFI 3), and the partial correlation coefficients

for the interactions between the net/nanno ratio
and nitrate concentration (r = + 0.51) and be-
tween the ratio and grazing pressure (r =
— 0.56) are significant at the 0.05 level. The
evidence suggests, therefore, that upwelling is
a necessary precondition for netplankton pro-
ductivity and standing crop to approach or ex-
ceed that of the nannoplankton in marine en-
vironments where water depth greatly exceeds
the maximum depth of wind-driven turbulent
mixing.

The relative constancy of the nannoplankton
relative to the netplankton fraction, in spite of
marked changes in the concentration of inor-
ganic nitrogen, the intensity and direction of
vertical water movements, and grazing pressure,
is puzzling. The assimilation ratios of both
fractions exhibited little variability, but on the
average nannoplankton ratios were twice as
great as those of the netplankton. Since this
ratio is an index of growth rate (cf. Eppley and
Strickland, 1968), the nannoplankton must have
been limited primarily by "cropping" factors
(Dicknian, 1969), at least during those periods
when netplankton productivity was increasing
relative to nannoplankton productivity. This is
supported by the observation that the chloro-
phyll content of nannoplankton and neti:)lankton
cells also exhibited little variability during the
period of study. During upwelling, two pro-
cesses could selectively remove nannoplankton
cells from upwelling regions: (1) grazing and
(2) horizontal advection.

If nannoplankton grazers were predominantly
protozoans (Beers and Stewart, 1969) with
short generation times and netplankton grazers
were crustaceans and fishes with long genera-
tion times, the coupling between primary pro-
ductivity and grazing would be much closer for
nannoplankton-based food chains than for net-
plaiikton-based food chains. The cycle of nan-
noplankton productivity and animal grazing
would be balanced (Gushing, 1959; Heinrich,
1962) in contrast to the unbalanced character
of netplankton-based food chains. This would
tend to dami)en fluctuations in the nannoplank-
ton fraction relative to the netplankton fraction.

Similarly, if nannoplankton cells were selec-
tively removed from sites of upwelling by mass

816

MALONE: RELATIVE IMPORTANCE OF NANNOPLANKTON AND NETPLANKTON

transport normal to the coast because of their
lower sinking rates, netplankton cells would
have a greater tendency to remain closer to the
region of upward water movement than nanno-
plankton cells (Stommel, 1949). Both of these
processes, selective grazing by organisms with
short generation times and horizontal advection
away from upwelling sites, would limit increases
in nannoplankton standing crop during upwell-
ing and could compensate for the growth rate
differential between the netplankton and nanno-
plankton fractions. This would set the stage
for netplankton productivity and standing crop
to exceed that of the nannoplankton during up-
welling, and also explain the discrepancy be-
tween nannoplankton growth rates and their
response to photic zone enrichment. Decreases
in nannoplankton standing crop due to "exces-
sive" grazing or removal from the photic zone
by downward water movements would be damp-
ened by the short generation times (and, there-
fore, potentially rapid response time) and mo-
tility of the nannoplankton species.

Comparisons of the Oceanic Period in Mon-
terey Bay with the offshore oceanic environment
of the California Current reveals an interesting
pattern of netplankton and nannoplankton vari-
ation which is consistent with the above model.
The productivity and standing crop of the net-
plankton fraction did not vary significantly
between the Oceanic Period inshore and the off-
shore oceanic zone. In contrast, the nannoplank-
ton were significantly higher inshore than off-
shore (Table 5). This "inshore enhancement"
effect during intrusions of oceanic water could
arise in response to the overall pattern of circu-
lation. The vertical distribution of nannoplank-
ton chlorophyll compared with that of the net-

Table 5. — Mean netplankton and nannoplankton produc-
tivity and standing crop with 95 7r confidence limits for
the Oceanic Period at CalCOFI 3 and the oflFshore oceanic
region of the California Current.

Oceanic
region

Measuremeni

Nanno

Net

Offshore

mgC m — 3 hr— l

0.69 ± 0.20

0.08 ± 0.05

Inshore

3.90 1.53

0.25 0.20

Offshore

mgChl-o m — 3

0,093 0.036

0.019 0.010

Inshore

0.477 0.227

0.068 0.047

Offshore

mgChl-a m— *

15.60 3.22

2.58 0.92

Inshore

18.14 5.15

371 2.17

plankton indicated that nannoplankters are more
independent of vertical water movements and
are better able to maintain their position in the
water column. This ability, probably a conse-
quence of motility, will result in a concentration
of nannoplankton in regions of downward flow
(Hutchinson, 1967). In addition, the ability of
nannoplankton to maintain their position in the
photic zone could give rise to a situation anal-
ogous to the "island mass effect" described by
Doty and Oguri (1956). The former is more
likely, however, since assimilation ratios were
equivalent in both inshore and offshore environ-
ments, i.e., the increase in primary productivity
was a consequence of higher standing crops
rather than an increase in growth rates.

SUMMARY AND CONCLUSIONS

Phytoplankton productivity and standing crop
were low under oceanic conditions, both inshore
and offshore. During the Oceanic Period in
Monterey Bay the nannoplankton accounted for
60 to 99 '"r of the observed productivity and
standing crop, while offshore this fraction was
responsible for 75 to 99 9r . The productivity and
standing crop of the netplankton fraction were
exceedingly low and constant under these condi-
tions, but the nannoplankton fraction was signi-
ficantly higher inshore than offshore. Netplank-
ton productivity and standing crop exceeded
that of the nannoplankton only during periods of
strong upwelling.

The netplankton fraction was composed al-
most exclusively of diatoms while the nanno-
plankton fraction was dominated by flagellates.
Similar, but more detailed observations off La
Jolla, Calif., (Reid et al, 1970) showed the nan-
noplankton to be composed primarily of naked
dinoflagellates, "monads" (e.g., Chilomonas ma^
rina and Eidreptia sp.), and coccolithophores
(e.g., Coccolithis hiixleyi) .

The nannoplankton fraction was surprisingly
stable both seasonally in Monterey Bay and geo-
graphically in the California Current system.
Variations in phytoplankton productivity and
standing crop were due primarily to the net-
plankton with the nannoplankton maintaining
a comparatively stable background level.

817

FISHERY BULLETIN: VOL. 69. NO. 4

Increases in netplankton productivity and stand-
ing crop were closely related to upwelling, both
as a consequence of the positive vertical advec-
tion and the entrainment of nitrate into the
upper half of the photic zone. The requirement
for positive vertical advection was probably re-
lated to both cell size and motility so that the
vertical distribution of nannoplankters was more
independent of vertical water movements. The
relationship between cell size and A/V ratios
probably accounted for the higher nitrate re-
quirements of the netplankton. Decreases in the
netplankton were primarily due to grazing and
to removal from the photic zone by downward
water movements.

The stability of the nannoplankton compared
to the variability of the netplankton is inter-
esting, especially in light of the marked changes
observed in the concentration of inorganic nitro-
gen compounds and the direction and intensity
of vertical water movements. Since nanno-
plankton assimilation ratios were consistently
high and twice as great as netplankton assimi-
lation ratios, the nannoplankton must have been
limited primarily by cropping factors during up-
welling periods when netplankton standing crop
was increasing relative to that of the nanno-
plankton. Under these conditions increases in
the nannoplankton fraction will be dampened by
selective removal from u])welling sites by mass
transport away from the coast and grazing by
organisms with short generation times (e.g.,
protozoans). Decreases in nannoplankton
standing crop due to "excessive" grazing or re-
moval from the photic zone by downward water
movements will be limited by the motility and
short generation times of nannoplankton species.
The motility of nannoplankters in combination
with onshore mass transport and downward
water movements will also favor an offshore-
inshore increase in nannoplankton productivity
and standing crop.

Finally, it is clear that the nannoplankton and
netplankton components of i)h.vtoplankton com-
munities respond differently to changes in their
environment; that cell size, surface-to-volume
ratios, and motility play important roles in me-
diating these resi)onses; and that changes in
netplankton and nannoplankton productivity rel-

ative to each other have definite consequences
with respect to energy flow through phytoplank-
ton-based food chains.

ACKNOWLEDGMENTS

I am grateful to M. Gilmartin, D. P. Abbott,
and B. Robison for their criticisms and encour-
agement, and to M. S. Doty for his timely advice
during the preparation of this paper. I thank
Peter Davoll and David Bracher for the hydro-
graphic and nutrient chemistry data, and M.
Youngbluth for the zooplankton data.

This research was supported in part by NSF
Grants GB 8408 Al, GB 8374 A2, GD 27254,
and in pai't by NIH Predoctoral Fellowship 5
FOl GM 44364-02, and was submitted in partial
fulfillment of the Ph.D. dissertation requirement,
Stanford University.

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820

DISTRIBUTION, APPARENT ABUNDANCE, AND LENGTH COMPOSITION

OF JUVENILE ALBACORE, Thunnus alalunga,

IN THE SOUTH PACIFIC OCEAN

Howard 0. Yoshida'

ABSTRACT

The distribution, apparent abundance, and length composition of juvenile albacore, Thunnus alalunga,
were deduced from 127 specimens found in the stomachs of 2,297 billfishes collected in the South Pacific
between January 1964 and July 1966. Juvenile albacore were found in the South Pacific from lat 5° to
31° S, between long 153° and 179° W. Billfish stomach samples were collected from as far east as long
135° W, but juveniles were not in the stomachs east of long 153° W. The juveniles were consistently
more numerous between lat 10° and 20° S than in the area farther north. The mean length of the ju-
veniles increased from north to south but not from east to west (or vice versa). A southward migra-
tion of juveniles is postulated.

In April 1963, the National Marine Fisheries
Service (formerly the Bureau of Commercial
Fisheries) , Hawaii Area Fishery Research Cen-
ter established a field station in Pago Pago,
American Samoa, to collect information on the
longline fishery based there. A fleet of vessels
from Japan, the Republic of Korea, and the Re-
public of China has supplied two American-
owned canneries with albacore, Thunnus ala-
hinga, and other tuna. In 1965 the fleet was
composed of 154 vessels which landed 15,588
metric tons of albacore (Otsu and Sumida, 1968) .

The field station was established primarily to
study the eff'ects of the fishery on albacore. As
part of this study an investigation was started
to determine the early life history of albacore
in the South Pacific.

Beginning in 1964, arrangements were made
with several longline fishing vessels based in
American Samoa to collect stomachs of billfishes,
which are known to prey on juvenile tunas (Yo-
shida, 1965, 1968). The distribution, apparent
abundance, and length composition of juvenile al-
bacore, here defined as fish smaller than 400 mm
standard length, were determined by specimens
found in the stomachs of the predators.

MATERIALS AND METHODS

The longline vessels based at American Samoa
fished primarily for albacore; billfishes were
taken only incidentally. The crews of the co-
operating longline vessels collected 2,297 bill-
fish' stomachs between January 1964 and July
1966. These stomachs were also used in a study
of juvenile skipjack tuna, Katsuwonus pelamis
(Yoshida, 1971).

In the laboratory, all the tunas and tunalike
specimens were first sorted from the stomach
contents. The juvenile tunas were identified by
the use of skeletal characters; juvenile albacore
were easily identified by their definitive skeletal
characters (Matsumoto, 1963; Yoshida, 1965).
Standard length (SL) was taken for all intact
juveniles and is the measurement used through-
out. For fragmentary specimens, the standard
length was estimated from previously determined
relations between standard length and various
vertebral segments (Yoshida, 1968). A total of
127 juvenile albacore was found in the billfish
stomachs (Table 1).

' National Marine Fisheries Service, Hawaii Area
Fishery Research Center, Honolulu, Hawaii 96812.

Manuscript accepted June 1971.

FISHERY BULLETIN: VOL. 69. NO. 4, 1971.

'' For the purpose of this paper the term billfish, in
addition to the Istiophoridae, includes the swordfish,
Xiphias gladius.

821

FISHERY BULLETIN: VOL. 69, NO. 4

Table 1. — Juvenile albacore found in billfish stomachs from the South Pacific.

Date

Positi

on

Stondard
length

Data
1965

Po

ition

Stondard
length

Dote
1966

Posit

on

Standard

1964

Lot S

Long W

Lot S

Long W

Lot S

Long W

length

mm

mm

mm

3/9

07''00'

170-00'

143

1/5

14-00'

174-00'

122

1/7

15-00'

175-00'

107

3/20

06°00'

164-00'

116

1/5

14-00'

174-00'

97

1/9

15-00'

174-00'

89

3/21

05°00'

165-00'

67

1/22

14-00'

175-00'

96

1/9

15-00'

174-00'

83

4/4

oa-oo-

175-00'

102

1/22

14-00'

175-00'

78

1/9

16-00'

174-00'

110

4/5

08°00'

175-00'

136

1/22

14-00'

175-00'

84

1/9

16-00'

174-00'

113

4/9

07"00'

178-00'

78

1/24

14-00'

174-00'

102

1/9

16-00'

174-00'

133

4/9

07°00'

178-00'

137

1/25

14-00'

174-00'

109

1/17

12-00'

175-00'

106

4/12

07°00'

178-00'

26

1/26

11-00'

162-40'

81

1/23

12-40'

171-00'

133

4/16

07° 00'

179-00'

57

1/27

14-00'

174-00'

116

2/8

09-00'

172-00'

130

4/19

O/'OO'

178-00'

102

1/29

14-00'

175-00'

110

2/8

09-00'

172-00'

137

4/20

07»00'

179-00'

66

1/30

14-00'

175-00'

102

2/8

09-00'

172-00'

130

4/20

07°00'

179-00'

66

4/4

07-10'

164-13'

123

2/8

09-00'

172-00'

93

4/20

07°00'

179-00'

106

4/12

07-10'

170-20'

102

2/13

07-02'

171-30'

102

4/24

09''00'

176-00'

115

4/22

07-00'

174-45'

86

3/7

06-35'

162-20'

58

4/25

08°00'

176-00'

67

4/22

07-00'

174-45'

86

3/14

07-20'

161-15'

89

4/26

oe-oo'

177-00'

119

9/1

13-00'

171-00'

96

3/16

08-10'

165-13'

67

5/8

07°54'

165-32'

118

11/7

16-30'

159-20'

152

3/22

11-32'

168-29'

104

S/B

07-54'

165-32'

113

11/7

16-30'

159-20'

158

3/22

11-32'

168-29'

116

5/8

07°54'

165-32'

104

11/7

16-30'

159-20'

142

3/28

09-10'

153-00'

168

5/8

07-54'

165-32'

113

11/8

16-20'

159-09'

152

5/5

08-13'

175-42'

63

5/8

07°54'

165-32'

88

11/22

17-00'

168-00'

105

5/5

08-13'

175-42-

92

5/8

07°54'

165-32'

106

11/29

17-07'

170-43'

119

5/5

08-13'

175-42'

97

5/8

07°54-

165-32'

125

11/29

17-07'

170-43'

115

5/7

08-00'

175-45'

94

5/10

07°46'

165-29'

121

11/29

17-07'

170-43'

91

5/9

08-26'

175-57'

53

5/10

07°46'

165-29'

88

12/14

17-50'

159-30'

137

6/8

07-15'

164-42'

74

5/19

05-29'

170-06'

48

12/14

17-50'

159-30'

148

6/29

30-49'

166-13'

314

5/19

06-00'

172-00'

47

12/17

16-11'

157-27'

100

7/12

28-50'

156-03'

297

5/23

06-00'

173-00'

58

12/21

17-52'

158-20'

138

7/15

28-05'

155-24'

317

5/26

06-23'

173-59'

99

12/22

10-00'

174-00'

159

7/23

28-44'

154-15'

321

6/1

05-52'

174-41'

48

12/25

18-00'

163-00'

130

7/23

28-44'

154-15'

316

6/1

05-52'

174-41'

73

12/25

18-00'

163-00'

164

7/24

28-22'

154-24'

301

6/20

06-43'

171-26'

53

12/28

17-30'

162-10'

162

6/25

07-18'

172-53'

86

12/29

12-00'

171-00'

93

8/18

26-00'

175-00'

357

12/30

12-00'

171-00'

115

8/21

26-00'

176-00'

358

12/31

12-00'

171-00'

93

9/4

24-00'

174-00'

328

9/5

25-00'

174-00'

343

9/9

25-00'

171-00'

333

9/9

25-00'

171-00'

301

9/13

18-00'

170-00'

230

9/13

16-00'

170-00'

230

9/13

16-00'

170-00'

223

9/19

16-00'

173-00'

110

10/4

09-00'

179-00'

93

10/4

09-00'

179-00'

116

10/4

15-00'

173-00'

93

10/8

19-00'

173-00'

146

10/9

17-00'

173-00'

185

10/18

13-00'

174-00'

62

10/22

15-00'

174-00'

83

10/22

15-00'

174-00'

93

10/22

15-00'

174-00'

78

11/11

16-00'

171-00'

79

11/13

16-00'

171-00'

62

11/13

16-00'

171-00'

128

11/14

16-00'

171-00'

133

11/15

)6°00'

175-00'

150

11/16

16-00'

172-00'

no

11/16

16-00'

172-00'

150

12/18

14-00'

174-00'

102

12/31

14-00'

175-00'

133

822

YOSHIDA: JUVENILE ALBACORE IN SOUTH PACIFIC OCEAN

LENGTH OF JUVENILES

The juvenile albacore in the billfish stomachs
ranged from 26 to 358 mm (Figure 1). Two
length groups were apparent in the' length-fre-
quency distribution: one with a mode at 110 mm
and the other at 310 mm; another length group
was suggested between 200 and 250 mm.

In the course of the study it became apparent
that the larger juveniles were being taken be-
tween lat 20° and 30° S. To determine if dif-
ferences existed in juvenile sizes by latitude,
lengths were plotted against latitude of capture
(Figure 2) . The smallest individuals were taken
north of lat 10° S and the largest south of lat
20° S. No specimens smaller than 290 mm were
taken south of lat 20° S. The juveniles between
lat 10° and 20° S were slightly larger (mean SL
120 mm) than those taken north of lat 10° S
(mean SL 94 mm). The mean standard length
of those from south of lat 20° S was 324 mm.

In contrast to the latitudinal differences in
juvenile length, no longitudinal trends in length
were evident. Juveniles larger than 300 mm
were taken in the eastern as well as the more
westerly portion of the area sampled.

MIGRATION OF JUVENILES

The differences in the lengths of the albacore
in the three latitudinal bands may be caused
by the migration of the juveniles. The increase
in length of juveniles from north to south and
the absence of any longitudinal trends in length
suggest a southward migration. After attain-
ing a length of nearly 200 mm the juveniles that
originate between the equator and lat 10° S prob-
ably start migrating south. They apparently
continue to move southward as they grow. This
migration would explain the absence of large
(>250 mm) juveniles north of lat 20° S.

These observations on the suspected migration
pattern of juvenile albacore fit well with the
accumulated information on the biology of al-
bacore in the South Pacific. Observations on
the length composition of commercial catches
of albacore in the South Pacific indicate latitu-
dinal differences in the size of albacore. Adult
albacore tend to be small north of lat 15° S and

NUMBER
18

— i-J

1

?

■■ ?

n '

" :;

1

^

::].M n

pt

F

imi

0 50 100 150 200 250 300 350

STANDARD LENGTH (mm)

Figure 1. — Length-frequency distribution of juvenile al-
bacore in the South Pacific.

s»

'.. • . •

1

. f* .T,.*.*. .

• • • • •

10°

•• ••• •• •

IS"

• "T-.r. v."*-. .

•

20"

•

25»

•

• • —

30°

-

-

S

1 1 1 i 1

1

1

1

120 160 200 240

STANDARD LENGTH (mm)

Figure 2. — The length of juvenile albacore plotted
against latitude of capture.

largest between lat 20° and 25° S. They are
smaller again south of lat 25° S (Otsu and Su-
mida, 1968) . Length-frequency data published by
the Nankai Regional Fisheries Research Labora-
tory ( 1959) show that albacore as small as 490 to
500 mm are caught on longlines south of lat
30° S. Thus, it could be that the juveniles move
southward as they grow and are first taken by
the longline fishery as preadults in the higher
latitudes in the South Pacific. A similar pat-

823

FISHERY BULLETIN! VOL. 69, NO. 4

tern has been deduced for albacore in the North
Pacific. Otsu and Uchida (lOfsS) hypothesized
that the juveniles in the North Pacific migrate
from tropical and subtropical waters into tem-
perate waters and are recruited into the adult
population in higher latitudes, presumably north
of lat 30° N. Generally speaking, then, the al-
bacore in the North and South Pacific, which
are believed to constitute separate subpopula-
tions, follow similar migration patterns within
their respective hemispheres. The adults are
believed to spawn in lower latitudes, between the
equator and lat 20° where the eggs hatch and
the larvae develop into juveniles. The juveniles
then migrate into higher latitudes as they grow
and they join the adult population in the higher
latitudes.

AGE AND GROWTH

Information on age and growth is useful in
determining certain vital statistics for fish pop-
ulations and it would be useful if the growth
of juvenile albacore in the South Pacific could
be determined. Around Hawaii juveniles (60-
350 mm SL) were estimated to grow about
31 mm per month (Yoshida, 1968). It would
have been interesting to compare this growth
with that of juveniles in the South Pacific. A
plot of juvenile albacore length by time of cap-
ture, however, did not indicate that the length of
the juveniles was increasing with time.

DISTRIBUTION AND ABUNDANCE

Because the data for any one year were sparse,
the data for all years were combined to deter-
mine the quarterly distribution of juvenile al-
bacore (Figure 3). The apparent distribution
of juvenile albacore may reflect the operations
of the longline boats. The longline vessels based
at American Samoa primarily were seeking al-
bacore and selecting areas where albacore catch
rates tended to be high. The vessels generally
fished north of lat 20° S in the fir.st half of the
year and beginning in June or July moved south-
ward to as far south as lat 30° S (Otsu and
Sumida, 1968). The data indicated that the co-
operating vessels generally followed this pattern.

In spite of this shortcoming the data suggest
some interesting features of the seasonal distri-
bution of juvenile albacore.

In the first quarter billfish stomach samples
were collected between long 150° and 178° W
and lat 5° and 16° S. The juveniles were gen-
erally found throughout the sampling area west
of long 153° W.

In the second quarter the longitudinal range of
sampling was slightly greater but the juveniles
were restricted to the west between long 165° and
179° W. Latitudinally, most of the stomach
samples were from north of lat 10° S except
for a few samples from about lat 31° S. Ju-
veniles were taken between lat 5° and 9° S and
at lat 31° S.

In the third quarter stomach samples were
available from long 140° W to 178° E between
lat 5° and 31° S. The juveniles were absent in
samples from north of 14° S.

In the fourth quarter the sampling area was
bounded by long 135° W and 178° E and lat 6°
and 21° S. Juveniles were absent from the east-
ermost portion of the area. They were taken
between long 157° and 179° W and lat 9° and
20° S. These observations suggest that the cen-
ter of the spawning area is closer to the area
between long 160° W and the 180th meridian
than farther to the east.

Variations were also evident in the apparent
abundance of juvenile albacore as indicated by
the number of juveniles found monthly per 100
billfish stomachs (Figure 4).

Juvenile albacore were found in all months
except July and August. Peaks in apparent
abundance occurred in January, April, and No-
vember.

The data for all years were pooled because
billfish stomachs were unavailable for some
months in some years. Also, estimates of ap-
parent abundance may be biased by the small
sample sizes. The shortcoming of combining
data for all years and considering a large area
as an entity is that annual and areal variations
in apparent abundance are ob.scured. For ex-
ample, in 1965. except in April when four ju-
venile albacore were taken, no juveniles were
found in billfish stomachs from north of lat 10° S.

The ovei'all abundance of juveniles was greater

824

YOSHIDA: JUVENILE ALBACORE IN SOUTH PACIFIC OCEAN

Figure 3. — The quarterly distribution of juvenile albacore in the South Pacific, all years combined. The shadings
show areas from which billfish stomachs were collected. The dots show where juvenile albacore were taken.

o

NUMBER OF BILLFISH STOMACHS EXAMINED
99 48 92 157 167 248 196 240 218 224 237 183

w

v''---\

n

1

'Rfl

'

JULY AUG SEPT OCT NOV DEC JAN FEB MAR APR MAY JUNE

Figure 4. — Apparent abundance of juvenile albacore in
the South Pacific.

between lat 10° and 20° S than in the area north
of lat 10° S. Combining the data for all years,
7.5 juveniles per 100 billfishes were taken be-
tween lat 10° and 20° S, and 4.5 juveniles per
100 billfishes were taken north of lat 10° S.
(Near Hawaii between July 1962 and April 1966,
juvenile albacore were taken at a rate of 0.8 per
100 billfishes [Yoshida, 1968]. Thus, juvenile
albacore are apparently more numerous in the
South Pacific than around Hawaii.)

SPAWNING

Variations in seasonal and geographic distri-
bution and apparent abundance of juvenile al-
bacore may be related to the spawning of the

825

FISHERY BULLETIN; VOL. 69, NO. 4

adults. Several investigators have made obser-
vations on the spawning of albacore in the South
Pacific. On the basis of an examination of ova-
ries, Otsu and Hansen (1962) concluded that
peak albacore spawning occurs in the southern
hemisphere summer between the equator and lat
20° S. Their results also suggest a spawning
season of at least 5 months. Ueyanagi (1969),
who based his study on the distribution of larvae
and on the stage of maturity of ovaries of adults,
also suggested a southern summer spawning
season. The seasonal apparent abundance of
juvenile albacore does not disagree with the
above conclusions. The fact that juveniles were
found in all but 2 months of the year suggests
a long spawning season. The presence of juve-
nile albacore during and beyond the southern
hemisphere summer indicates some spawning
during the summer. My data also suggest an-
nual variations in adult spawning. The virtual
absence of juvenile albacore north of lat 10° S
in 1965 indicates little or no spawning in this
area during that year.

COMPARISON WITH
SKIPJACK TUNA

A comparison of the distribution and abund-
ance of juvenile albacore and skipjack tuna of-
fers some interesting contrasts. Although bill-
fish stomachs were sampled from long 135° W
to 177° E, juvenile albacore were found only
between long 153° and 179° W (Figure 5). The
juveniles were found throughout the latitudinal
range of sampling between lat 5° and 31° S. Ju-
venile skipjack tuna are distributed over a wider
area: between long 137° W and the 180th mer-
idian from lat 5° to 32° S ( Yoshida, 1971 ) . These
distributional patterns indicate that skipjack
tuna spawn over a wider area than the albacore
in the South Pacific.

Comparing the abundance of the two species,
in 1964 juvenile skipjack tuna were more nu-
merous north of lat 10° S than from 10° to 20° S,
but in 1965 they were more numerous between
10° and 20° S than in the area to the north (Yo-
shida, 1971 ) . Juvenile albacore were consistently
more abundant between lat 10° and 20° S than to

the north. Also, juvenile skipjack tuna appar-
ently were from 4.5 to 15 times more numerous
than juvenile albacore between the equator and
lat 20° S (Table 2). It is also interesting that
the apparent abundance of both species declined
from 1964 to 1965.

Table 2. — Apparent abundance of juvenile albacore and
skipjack tuna in the South Pacific. The apparent abun-
dance is e.xpressed as number per 100 billfishes. Data for
juvenile skipjack tuna are from Yoshida (1971).

North of lot 10' S

Skipiack tuna

Lot 10°-20° S

Albacore Skipjack tuna

1964
1965

6.7
1.9

46.3
28.8

9.3

5,8

42.6
35.6

FiciiRE 5. — The distribution of billfishes (shading)
sampled by the cooperating longline vessels and the dis-
tribution of juvenile albacore (dots) found in the billfish
stomachs.

826

YOSHIDA: JUVENILE ALBACORE IN SOUTH PACIFIC OCEAN

LITERATURE CITED

Matsumoto, W. M.

1963. Unique shape of the first elongate haemal
spine of albacore, Thunnns alalunga (Bonnaterre).
Copeia 1963: 460-462,
Nankai Regional Fisheries Research Laboratory
(editor).
1959. Average year's fishing condition of tuna long-
line fisheries. 1958 ed. [In Japanese with Eng-
lish figure and table captions.] Federation of
Japan Tuna Fishermen's Co-operative Associa-
tions, Tokyo, 414 p. te.xt + atlas.
Otsu, T., and R. J. Hansen.

1962. Sexual maturity and spawning of albacore
in the central South Pacific Ocean. U.S. Fish
Wildl. Serv., Fish. Bull. 62: 151-161.
Otsu, T., and R. F. Sumida.

1968. Distribution, apparent abundance, and size
composition of albacore (Thunnus alalunga) taken
in the longline fishery based in American Samoa,

1954-65. U.S. Fish Wildl. Serv., Fish. Bull. 67:
47-69.
Otsu, T., and R. N. Uchida.

1963. Model of the migration of albacore in the
North Pacific Ocean. U.S. Fish Wildl. Serv.,
Fish. Bull. 63: 33-44.
Ueyanagi, S.

1969. Observations on the distribution of tuna
larvae in the Indo-Pacific Ocean with emphasis
on the delineation of the spawning areas of alba-
core, Tliiinnus alalunga. [In Japanese, English
synopsis.] Bull. Far Seas Fish. Res. Lab. (Shi-
mizu) 2: 177-256.
YOSHIDA, H. 0.

1965. New Pacific records of juvenile albacore
Thunnus alalunga (Bonnaterre) from stomach
contents. Pac. Sci. 19: 442-450.

1968. Early life history and spawning of the al-
bacore, Thunnus alalunga, in Hawaiian waters.
U.S. Fish Wildl. Serv., Fish. Bull. 67: 205-211.

1971. The early life history of skipjack tuna, Ka-
tsuwonus pelamis, in the Pacific Ocean. Fish.
Bull., U.S. 69: 545-554.

827

COMPARISON OF PHYTOPLANKTON PRODUCTION BETWEEN
NATURAL AND ALTERED AREAS IN WEST BAY, TEXAS'

Jane Corliss and Lee Trent"

ABSTRACT

Phytoplankton production was compared between an undredged marsh area, a bay area, and an adja-
cent marsh area altered by channelization, bulkheading, and filling. Average gross production (mg
carbon/liter/day) in the altered area (canals) was 8% higher than in the marsh and 48% higher than
in the bay during June, July, and August 1969. Gross and net production were significantly higher
in the canals and marsh than in the bay; differences between the canals and marsh were not significant.

Large areas of shallow bays and marshes are
being dredged, bulkheaded, and filled for water-
front housing sites along the Gulf of Mexico
coast. When these sites are developed, shallow
marsh and bay areas are deepened or filled with
spoil, thus changing the environment for marine
organisms. Major changes to the bayshore en-
vironment as a result of these alterations in-
clude: (1) reduction in acreage of natural
shore zone and marsh vegetation; (2) changes
in marsh drainage patterns and nutrient inputs;
and (3) changes in water depth and substrates.
The effects of these environmental changes on
the productivity of estuarine organisms are
poorly understood.

Basic production in estuaries results from four
types of plant life: phytoplankton, attached
algae, sea grasses, and emergent vegetation.
Production of sea grasses and emergent vege-
tation is reduced or lost when natural marsh
areas are dredged and filled for housing sites.
Whether or not this reduction in primary pro-
duction by sea grasses and emergent vegetation
is compensated for by an increase in production
by phytoplankton and attached algae is not clear.
The objective of this study was to compare ph.y-
toplankton production between housing develop-
ment canals, natural marsh areas, and the open
bay in a shallow Texas estuary.

' Contribution No. 319, National Marine Fisheries
Service Biological Laboratory, Galveston, Tex. 77550.

" National Marine Fisheries Service, Biological Lab-
oratory, Galveston, Tex. 77550.

Manuscript accepted June 1971.
FISHERY BULLETIN: VOL.

69, NO. 4, 1971.

STUDY AREA AND METHODS

The study area in West Bay, Texas, included
a natural marsh, an open bay area, and the canals
of a waterfront housing development ( Figure 1 ) .
The developed area, which included about 45
hectares of emergent marsh vegetation, inter-
tidal mud flats, and subtidal water area prior
to alteration, was reduced to about 32 hectares
of subtidal water by dredging and filling. The
water volume (mean low tide level) was in-
creased from about 184,000 to about 394,000
kliter.

Sampling stations were established in dead-end
canals in a housing development, natural marsh
ai-eas, and an open bay area (Figure 1) . Water
depths at mean low tide at stations 1 through 5
were 1.6, 2.6, 0.5, 0.2, and 1.0 m respectively.

Primary production was measured on six
occasions at each station between June 18 and
August 14, 1969. Measurements were made
using the light- and dark-bottle technique de-
signed by Gaarder and Gran (1927). Water
samples were taken 15 cm below the surface at
all stations. A 4-liter bottle having a vent at
the bottom with a 30-cm rubber tube attached
was used to take the subsurface samples. Num-
ber 10 netting (0.060-mm mesh) was placed over
the mouth of the bottle and the bottle was sub-
merged, mouth down, until the container filled.
The netting was used to eliminate most of the
zooplankton from the samples.

829

FISHERY BULLETIN: VOL. 69, NO. 4

Figure 1. — Study area and sampling locations in the
Jamaica Beach area of West Bay, Tex.

For each station, six biological oxygen demand
(BOD) bottles (300 ml)— two wrapped with
black rubber tape and four unwrapped — were
filled (gravity flow) from the 4-liter water sam-
ple by inserting the rubber tube down to the
bottom of each bottle. About 300 ml of water
was permitted to overflow after the bottle was
full. Two of the unwrapped bottle samples were
fixed immediately for oxygen determination.
The remaining bottles were stoppered and sus-
pended 15 cm below the surface. The time of
sampling was recorded for each station and the
bottles were recovered 24 hr later and fixed for
oxygen determination.

Water temperature -( ° C) and turbidity in
Jackson turbidity unit — JTU (American Public
Health Association, 1962) — observations were
made just before the water samples for plankton
were taken (Table 1); in.solation was measured
with a recording jjyrheliometer located at sta-
tion 1.

Table 1. — Water temperatures and turbidities observed
just before each incubation period.

Station

Dat8

Average

1

■'

3

4

5

Temperature

June 18

29.0

29.0

29.0

29.0

29.0

29.0

June 25

31.5

31.0

30.5

30.5

31.0

30.9

July 9

31.5

31.5

31.0

31.0

31.5

31.3

July 24

30.5

29.5

30.0

29.5

29.0

29.7

July 30

32.0

31.0

31.5

31.5

31.0

31.4

Aug. 13

31.5

31.0

30.5

30.5

32.0

31.1

Average

31.0

30.5

30.4

30.0

30.6

30.6

Jcukion tut

hidity un

.

Turbidity

June 18

9.0

8.0

16.0

16.0

12.0

12.2

June 25

11.5

13.0

29.0

24.5

53.0

26.2

July 9

9.5

8.0

18.0

24.0

14.0

14.7

July 24

12.5

10.0

29.5

24.5

27.0

20.7

July 30

9.0

8.5

21.0

18.5

17.0

14.8

Aug. 13

9.5

6.5

19.0

12.0

18.5

13.1

Average

10.2

9.0

22.1

19.9

23.6

16.9

Dissolved oxygen was measured using a mod-
ified Winkler method (Carritt and Carpenter,
1966) . Oxygen determinations were made with-
in 3 hr after fixing the water samples. Changes
in dissolved oxygen were converted to changes
in organic carbon using the relation formulated
by Ryther ( 1956) : 1.0 mg oxygen is equivalent
to 0.30 mg carbon.

Net production (NP), respiration (R), and
gross production (GP) were determined using
the carbon values from the initial (/), light (L),
and dark (D) bottle values as follows:

NP = L — I,R = I — D, and GP = NP + R.

ENVIRONMENTAL AND
HYDROLOGICAL DATA

Surface water temperature varied no more
than 1.5° C between stations on any sampling
date and no more than 3° C between dates at

830

CORLISS and TRENT: PHYTOPLANKTON PRODUCTION

any station (Table 1). Surface water temiier-
atures were slightly higher in the canals and
bay than in the marsh.

Turbidity values of surface water samples
varied as much as 41.5 JTU between stations
on June 25 and as much as 41 JTU between
dates at station 5 (Table 1). Average turbidity
values from the marsh and Ijay stations were
about double those from the canal stations. On
June 25, however, turbidities in the bay were
about twice those in the marsh and about four
times those in the canals.

Insolation was similar on all sampling dates.
The daily averages ranged from 0.82 to 0.85
cal/cmVday.

Overproduction of phytoplankton, in terms of
oxygen balance, occurred in some canals of the
development. Plankton blooms that reduced
oxygen to zero at night, and caused fish kills at
station 1, occurred at least three times during
the study period. These blooms were observed
on July 4, July 18, and August 7.

PRODUCTION AND RESPIRATION

Average gross production ranged from 1.17
at station 5 to 2.25 mg carbon/liter/day at sta-
tion 1 during the study (Table 2 and Figure 2).
Average values at the two canal stations were
almost identical. Likewise, there was almost no
difference between average values at the two
marsh stations. Average production in the ca-
nals was slightly higher (B'r ) than in the marsh
and much higher (48^^^^) than in the bay. In
similar studies in Boca Ciega Bay, Fla., Taylor
and Saloman (1968) reported that primary pro-
duction of phytojilankton did not differ consis-
tently between development canals and open bay
areas.

Average net production ranged from 0.84 at
station 5 to 1.74 mg carbon/liter/day at station 1.
Like gi'oss production, the values were about
the same among canal stations and among marsh
stations. Average net production in the canals
was 13''r higher than in the marsh and 51 "^r
higher than in the Bay.

Respiration averaged 0.51 mg carbon/ liter/
day, or 27.7 ^v of gross production and ranged
from 23.4 to 34.4% between stations (Table 2).

Tahuc 2. — Net production (NP), re.spiration (fi), gross
production (GP), and percent respiration (%R) by
station and date in West Bay, Tex.

Data

Vorioblo

Station

Average

1

2

1 ^

4

1 *

-

mj; carl

on/litfr/day —

Juno 18

.\P

2.01

0.91

0.70

1,08

0.54

1.05

R

0.23

0.69

0.58

0.31

0.34

0.43

GP

2.24

1.60

1.28

1.39

0.88

1.48

%R

10-3

43.1

45.3

22.3

38.6

31.9

Juna 25

NP

1.33

1.75

0.87

1.04

0.74

1.15

R

0.39

1.07

0.63

0.52

0.37

0.60

GP

1.72

2.82

1.50

1.56

1.11

1.74

V,R

22.7

37.9

42.0

33.3

33.3

33.8

July 9

.\P

1.80

1.08

1.61

1.34

0.84

1.33

R

0.37

0.56

0.53

0.43

0.31

0.44

GP

2.17

1.64

2.14

1.77

1.15

1.77

%R

17.0

34.1

24.8

24.3

26.9

25.4

July 24

NP

2.57

3.04

1.77

2.40

0.94

2.14

R

0.43

0.38

0.44

0.70

0.32

0.45

GP

3.00

3.42

2.21

3.10

1.26

2.60

%R

14.3

n.i

19.9

22.6

25.4

18.7

July 30

NP

0.81

1.30

1.82

2.12

0.74

1.36

R

0,74

0.46

1.19

0.40

0.32

0.62

GP

1.55

1.76

3.01

2.52

1.06

1.98

9f«

47.7

26.1

39.5

15.9

30.2

31.9

Aug. 13

NP

1.94

1.90

1.43

1.57

1.26

1.62

R

0.87

0.33

0.77

0.44

0.31

0.54

GP

2.81

2.23

2.20

2.01

1.57

2.16

%R
NP

30.9

14.8

35.0

21.9

19.7

24.5

Average

1.74

1.66

1.37

1.59

0.84

1.44

R

0.50

0.58

0.69

0.47

0.33

0.51

GP

2.25

2.24

2.06

2.06

1.17

1.95

T<R

23.8

27.8

34.4

23.4

29.0

27.7

Distinct differences in the percents of gross pro-
duction attributable to respiration between canal,
marsh, and bay areas were not apparent.

Averages of gross and net iiroduction in the
canals and marsh were significantly greater
than in the bay; differences between the canals
and marsh were not significant (Table 3).

The differences in production between stations
were related to turbidity. The correlation co-
efficient (r) between average gross production
and average turbidity at each station was — 0.70.

Table 3. — Compari.sons of net productivity, respiration,
and gross productivity between stations (one-way anal-
ysis of variance).

Compar

"sor

between

Stot

ons 1-5

Stations

M

df

f-value^

df

/"-value

Net production
Respiration
Gross production

4,25
4,25
4,25

4,06'

2.30

5.05-

3,20
3,20
3,20

0.72
0.97
0.25

1 Significance lev
• 5%
•• 1%

el

831

FISHERY BULLETIN: VOL. 69, NO. i

2 -
I -

JUNE 18-19

JULY 9-10

E-.

m

AA

JULY 24-25

W;

JULY 30-31

'//y.

//..

;.

AUGUST 13-14

m

JUN 18-AUG 14

RESPIBiTION
I

I 2 6 7 10

STATION

Figure 2. — Gross and net production and respiration by
station and date, and average values for all sampling
dates.

DISCUSSION

It is probable that eutrophic conditions will de-
velop more frequently in housing development
canals than in natural marsh areas because of
differences in phytoplankton production, water
circulation, water exchange, and high nutrient
levels. In this study, gross production of phy-
toplankton in surface waters was higher in the
canals than in the marsh or bay. We did not
obtain information for computing production per
unit area, but it is iirobable that production per
unit area was significantly greater in the canals
than in the other two areas, the reasons being
the greater depths and lower turbidities in the

canals. Wind-driven circulation responsible for
reaeration of the waters in the development is
less than in the natural area because of houses
blocking and diverting prevailing winds and be-
cause many of the canals are narrow and per-
pendicular to the direction of prevailing summer
winds. Water depths at mean low tide in the
development averaged about 1.5 m but were
often much greater, sometimes over 3 m, whereas
depths in the natural ai'ea averaged about 0.6 m
but were always less than 1 m. With the average
tide level change of 0.3 m, this means that only
about one-fifth of the volume of water in the
development exchanges with the bay during a
normal tidal cycle, whereas about one-half ex-
changes per cycle in the natural area. Nutrient
levels were about the same (nitrogen) or slightly
higher (phosphates) in the canals than in the
natural area (Moore and Trent, 1971). It is
possible, however, that because of reduced water
exchange, nutrient levels in parts of the devel-
opment were too high to maintain a balanced
ecological system.

LITERATURE CITED

American Public Health Association.

1962. Standard methods for the examination of
water and wastewater. 11th ed. Am. Public
Health Assoc, Inc., New York, 626 p.
Carritt, D. E., and J. H. Carpenter.

1966. Comparison and evaluation of currently em-
ployed, and modification of the Winkler method
for determining dissolved oxygen in seawater;
NASCO Report. J. Mar. Res. 24: 286-318.
Gaarder, T., and H. H. Gran.

1927. Investigations of the production of plankton
in the Oslo Fjord. Cons. Perm. Int. Explor. Mer.,
Rapp. P.-V. Reun. 42, 48 p.
Moore, D., and L. Trent.

1971. Setting, growth and mortality of Crassostrea
virijivica in a natural marsh and a marsh altered
by a housing development. Proc. Natl. Shellfish.
Assoc. 61: 51-58.
Rytiier, J. H.

1956. The measurement of primary productivity.
Limnol. Oceanogr. 1: 72-84.
Taylor, J. L., and C. H. Saloman.

1908. Some effects of hydraulic dredging and
coastal development in Boca Ciega Bay, Florida.
U.S. Fish Wildl. Serv., Fish. Bull. 67: 213-241.

832

THERMAL TOLERANCE OF JUVENILE PACIFIC SALMON AND
STEELHEAD TROUT IN RELATION TO SUPERSATURATION OF

NITROGEN GAS

Wesley J. Ebel, Earl M. Dawley, and Bruce H. Monk'

ABSTRACT

Thermal tolerance of juvenile chinook salmon (Oncorhynchus tshawytscha) , echo salmon (O. kisutch) ,
and steelhead trout (Salmo gairdneri) that had been held at various acclimation temperatures was low-
ered when test water was supersaturated (125-130% of saturation) with nitrogen gas. Increasing the
depth of the test tank allowed the fish to compensate somewhat for the supersaturation by sounding,
but substantial mortalities still occurred. A comparison of tolerance among the species tested revealed
that coho salmon were the most tolerant, chinook salmon next, and steelhead trout the least tolerant to
temperature increases in the presence of supersaturation of nitrogen.

During the past several decades, a number of
investigators have examined temperature as a
lethal factor by use of the classic pharmacolog-
ical assay method. Fry, Hart, and Walker
(1946) recognized the importance of acclimation
temperature in determining the tolerance of a
fish to high and low temperatures and estab-
lished upper and lower levels of tolerance at
various acclimation temperatures. Brett (1952)
listed maximum temperatures for survival of
young Pacific salmon (Oncorhynchus spp.) be-
tween 23.8 and 25.1° C. In later work (Brett,
1958), he emphasized temperatures below those
at which a fish dies and constructed hypothetical
temperature polygons which described lower
levels of temperature tolerance where activity,
growth, and spawning would be aflfected.

More recently, investigators have emphasized
the response of fish to temperature changes
under multivariate conditions. Many factors
such as dissolved oxygen deficits, carbon dioxide
increases, and increases in toxic substances all
affect an aquatic organism's tolerance to tem-
perature increases. Mihursky and Kennedy
(1967) stressed the importance of multivariate
experiments for establishing more realistic
standards for temperature regulation.

' National Marine Fisheries Service, Biological Lab-
oratory, Seattle, Wash. 98102.

Manuscript accepted June 1971.

FISHERY BULLETIN: VOL. 69. NO. 4, 1971.

Several nuclear power plants have been pro-
posed for the Columbia River. The National
Marine Fisheries Service (NMFS) is particu-
larly concerned about the effect that heated ef-
fluents from these plants might have on juvenile
Pacific salmon and steelhead trout (Salmo gaird-
neri) migrating downstream, particularly
while they are stressed by supersaturated nitro-
gen gas. High levels of nitrogen gas (over 125%
saturation) occur within large areas of the Co-
lumbia from about early May until mid-August
(Ebel, 1969). This period coincides with the
downstream migration of most juvenile salmon
and trout. Although the effect of supersatura-
tion of gas on juvenile salmon and trout has
not been examined in great detail, preliminary
studies by Ebel (1969) clearly show that Co-
lumbia River juvenile salmon have considerably
lower tolerance to temperature increases when
stressed by supersaturation of nitrogen than the
tolerance indicated by Brett (1952).

The Federal Water Quality Administration
(FWQA) recognized that supersaturation of
dissolved nitrogen could be a significant factor
in establishing water quality criteria for the
Columbia River. It therefore contracted the
Bureau of Commercial Fisheries (BCF; pres-
ently designated as NMFS) to determine the
changes in tolerance of juvenile salmon and
trout to temperature increases at different levels

833

FISHERY BULLETIN: VOL. 69, NO. 4

of temperature acclimation and supersaturation
of nitrogen. In the experiments described in
this report, BCF personnel sought to determine
the change in tolerance of juvenile salmon and
trout to temperature increases when stressed by
supersaturation of nitrogen and to determine
possible changes in tolerance if they had the
option to sound to different depths. Ebel (1969)
reported that the depth at which fish migrate
influences the effect of supersaturation of nitro-
gen because the gas remains in solution at a
much higher concentration when under pres-
sure; we therefore considered depth as well as
temperature increase and supersaturation of
nitrogen to be important.

Our first series of experiments describe the
effect of supersaturation of nitrogen and tem-
perature increases at surface pressures. Later
experiments show how depth changes the above
effect.

METHODS

The general approach used to determine the
effect of nitrogen supersaturation on the tol-
erance of juvenile salmon and trout to increased
temperature was similar to that used by Brett
(1952). Stocks were acclimated to tempera-
tures identical to those used by Brett; test tem-
peratures encompassed the ranges Brett used
in his lethal temperature determinations. These
test and acclimation temperatures were purpose-
ly selected so that changes in tolerance caused
by the stress of supersaturated nitrogen could
be compared with Brett's well-established levels
of temperature tolerance.

Groups of 20 test fish, each acclimated to a
given temperature, were placed simultaneously
in control and test situations involving identical
test temperatures at treatments of high (125-
130 o; ) and normal (100';; ) nitrogen saturation.
Two acclimation groups were used in each set
of tests — one that had a normal acclimation
history and one that had been exposed to super-
saturated nitrogen for 720 min. Observations
of behavior and mortality were made continu-
ously for the first 6 hr, then every hour for the
remainder of an 18-hr period. Events recorded
were times to first indication of stress, to loss

of equilibrium, and to death. The numbers of
live and dead fish with obvious external symp-
toms of gas bubble disease were recorded at the
termination of tests. All tests were then re-
peated (most tests were duplicated, some were
done three times) ; the data given in this report
are derived from the average value of the du-
plicated tests.

Hatchery and wild stocks of fish were tested.
Hatchery fish were from the following stocks:
coho salmon (0. kisutch) reai-ed at Leavenworth
National Fish Hatchery, Leavenworth, Wash.;
spring Chinook salmon {0. tshairytscha) reared
at Little White Salmon National Fish Hatchery,
White Salmon, Wash.; and steelhead trout
reared at the Washington State Fish Hatchery
at Green River, Cumberland, Wash. The wild
fish (spring Chinook salmon) were collected from
the turbine intake gatewells at McNary Dam on
the Columbia River. Because of time limitations
and lack of sufficient populations of fish, only
the coho were tested through the entire range
of acclimation temperatures (5, 10, 15, and
20° C). Hatchery-reared steelhead trout and
hatchery and wild spring chinook were tested
only after exposure at selected acclimation tem-
peratures— steelhead at acclimation tempera-
tures of 10° and 15° C and wild chinoOk at 10° C.

The experimental temperatures (test and ac-
climation) , lengths of time that the various
groups of fish were in holding and acclimation
tanks, and size of fish at time of testing are
summarized in Table 1. Water in test tanks
was adjusted to the appropriate test tempera-
tures established for each acclimation temper-
ature. Temperatures were maintained within
±0.2° C in both test and acclimation tanks.
When the test series required stressing of the
acclimated fish with supersaturated nitrogen, an
acclimation tank at the appropriate temperature
was saturated at 115 to 120*;; nitrogen and about
114 to 120' ; oxygen. The fish were then trans-
ferred from the normally saturated tank ( 100 "^r )
to the supersaturated tank and stressed for 720
min. When supersaturated water was needed
in the test tanks, the supersaturating equipment
was activated, and each tank was adjusted to
maintain between 125 and ISO'/r nitrogen. To
ensure stability, the temperatures and satura-

834

EBEL. DAWLEV. and MONK: THERMAL TOLERANCE

Table 1. — Holding time and temperature of water before transfer to acclimation tanks,
acclimation conditions, and mean size at time of testing of three species of salmon and
trout.

Species and

origin of

fish

T ■„. . Water
Lwtn^ temperature

Acclimation conditions

Mean size of fish
of time of test

Days

Temperature

Length

Weight

days

° C

• C

mm

S

Hatchery coha

28

8.8

35

5.0a

117

17

28

88

17

10,0a

118

18

28

8.8

23

10,0

134

22

28

8.8

4

12.5

134

22

28

8.8

48

15.0a

134

22

28

8.8

3

11.7

118

18

28

8.8

4

14.0

118

18

28

8.8

16

15.0

118

18

28

8.8

4

17.5

118

18

28

8.8

3

20.0a

118

18

Wild spring Chinook

0

15.0

4

10.0a

129

19

Hatchery spring chinoolc

90

8.8-13,0

4

15.0a

134

23

90

88-13.0

3

15.0

134

23

90

88-13.0

3

17.0

134

23

90

8.8-13.0

3

20.0a

134

23

Hotchery steelheod

10

12.0

5

10,0a

179

54

10

12.0

3

14.0

179

54

10

12.0

42

15.0a

179

54

a Final acclimation temperature.

tion levels were then measured for 24 hr before
introduction of the test fish.

The source of supersaturation of nitrogen gas
in the Columbia River was entrained air. We
used pumps to entrain air in our test and accli-
mation tanks. Oxygen, therefore, was also su-
persaturated; the ratio of oxygen to nitrogen
supersaturation was similar to that recorded in
the river (Beiningen and Ebel, 1971). Oxygen
saturation varied from about 114 to 120 '?f.

Facilities used for tolerance tests in relation
to supersaturation of nitrogen at surface pres-
sures were designed to provide a continuous
supply of fresh water. Sufficient cooling and
heating capacity was available from a water
heater and chiller to continuously supply 227
liters/min of either heated or chilled water from
5° to 40° C. Ten cylindrical fiber glass acclima-
tion tanks, about 1 m high x 214 m in diameter,
provided sufficient space to maintain 2000 fish
at each of five acclimation temperatures without
crowding. The test tanks were rectangular fi-
ber glass tanks of 113.6-liter capacity. A flow of
approximately 11.5 to 30.0 liters/min was main-
tained in acclimation tanks and 3.5 liters/min
in test tanks.

Supersaturation of nitrogen and oxygen was
achieved in the acclimation tanks by metering

air into the intake of two high-pressure recircu-
lating pumps with 42 kg/cm- back pressure on
the discharge side of the pump. About 0.75 liter/
min air in each pump created the desired satura-
tion of nitrogen (115-120Sr). Supersaturation
of nitrogen and oxygen in the test tanks was
achieved by metering 0.05 liter/min into an-
other high-pressure recirculating pump with
32 kg/cm^ back pressure, which recirculated the
water in the coldwater supply tank to the test
tanks. (Source of water was from Seattle mu-
nicipal supply; chlorine was eliminated by char-
coal filters.) The final saturation value for each
tank was then achieved by manipulating the
number of equilibrating screens through which
the water flowed before entering the tanks.

The test tank (9 m deep) used for our ex-
periments concerning water depth has been de-
scribed by Pugh, Groves, and Ebel (1969).
When tolerance tests were conducted in the deep
tank, the saturation levels of nitrogen and oxy-
gen were conti-olled in the above manner (by
injecting air into a recirculating pump). Be-
cause of the large volume of water (66,648
liters) , a continuous flow of fresh water was not
needed and the existing water was recirculated.
Time limitations precluded testing more than
two populations (hatchery coho and wild spring

835

FISHERY BULLETIN: VOL. 69, NO. 4

Chinook salmon) at 10° C acclimation temper-
ature.

EFFECT OF SUPERSATURATION OF
NITROGEN GAS ON TOLERANCE OF
FISH TO TEMPERATURE INCREASES

Supersaturation of nitrogen (125-130%) in
the test tanks lowered the tolerance of all fish
to temperature increases at all acclimation tem-
peratures when tested below 26° C (Tables 2-
10). More than 50% mortality occurred within
18 hr even with no temperature increase when
the test tanks were supersaturated at this level.
Time to death of fish was accelerated regardless
of acclimation temperature.

A comparison of LE.^^o (e.xposure time when
50% of the population is dead) curves developed
under the four treatment levels indicates that a
prior stress of 115 to 120% saturation for 12 hr
did not greatly affect the fish when they were
subjected to temperature increases in water sat-
urated at 100% (Figure 1). When these

Table 3. — Mean values" of lethal exposure time (in min-
utes) for coho salmon that had been acclimated to 10° C
water temperature and then subjected to various in-
creases in water temperature and saturation of nitrogen
gas.

Dead fish
in sample

Level

of
gasb

Lethal exposure time at
various temperatures (° C)

27

One fish

Three fish

Half of sample

Ail of sample

NN
NS
SN
SS

NN
NS
SN
SS

NN
NS
SN
SS

NN
NS
SN
SS

773

413

360

215

770

407

340

155

877

472

517

297

960

480

382

225

.. 1,085
960 480

130
130
135
125

100
152
67
95

167
192
232.5
480 282.5 193.5

215
255
255

540

550

1,050 750 395

4
6
4
12

< 5

16
7.5
15

15
23
16.5
35.5

32.5
72.5

35
70

a Mean of replicated tests.

b NN = normal saturation (100%) of nitrogen gas in acclimation and
test tanks,-
NS = normol saturotion in acclimation tank and supersaturation

(125-130%) in test tanks;
SN = supersoturotion in acclimation tank and normal saturation in

test tonks;
SS = supersaturation in acclimation and test tanks.

Table 2. — Mean values'" of lethal exposure time (in min-
utes) for coho salmon that had been acclimated to 5° C
water temperature and then subjected to various in-
creases in water temperature and saturation of nitrogen

Table 4. — Mean values" of lethal exposure time (in min-
utes) for coho salmon that had been acclimated to 15° C
water temperature and then subjected to various in-
creases in water temperature and saturation of nitrogen
gas.

Dead fish
in sample

Level

of
gasb

Lethal exposure time at
various temperatures (° C)

Dead fish
in sample

Level

of
gasb

Lethal exposure time at
various temperatures {" C)

5

10

IS

20

23

25

15

20

23

26

27

28

One fish

NN

125

15.5

One fish

NN

..

._

..

..

26.5

8.5

NS

525

412

380

230

85

14

NS

420

265

2,325

222.5

38.5

7

SN

..

_.

__

__

102

8

SN

__

255

23

10

SS

250

330

197

112

35

10

SS

70

36

45

29.5

17.5

12.5

Three fish

NN

167

20.5

Three fish

NN

50

10.5

NS

615

457

405

270

108

16.5

NS

430

295

297

245

51.5

14

SN

__

__

270

12

SN

705

30

14

SS

483

435

315

128

137

13

SS

175.5

78.5

62.5

38.5

32.5

18

Half of sample

NN

300

27

Half of sample

NN

62

13.5

NS

810

605

577

390

266

21.5

NS

555

502.5

517.5

645

79

20.5

SN

__

20

SN

__

_,

__

855

70

24.5

SS

626

580

435

229

186

20

SS

247

115

124.5

86

52.5

38

All of sample

NN

M

All of sample

NN

__

_.

..

..

93

37

NS

._

990

._

1,080

420

58

NS

_.

115

46

SN

60

SN

460

520

930

910

115

48

SS

—

—

—

840

450

445

SS

519

450

465

312.5

96

36

a Mean of replicated rests.

b NN = normol saturation (100%) of nitrogen gas in occlimotion and
test tanks;
NS = normal soturotion in acclimation tank and supersaturation

(125-130%) in test tanks;
SN = supersaturation in acclimation tonk ond normal soturotion in

test tanks;
SS = supersaturation in acclimation and test tonks.

a Mean of replicated tests.

b NN = normal soturotion (100%) of nitrogen gas in acclimation and
test tanks;
NS = normal saturation in acclimation tank and supersoturotion

(125-130%) in test tonks;
SN = supersaturation in acclimation tank and normal saturation in

test tanks;
SS = supersaturation in acclimation and test tanks.

836

EBEL, DAWXEY, and MONK : THERMAL TOLERANCE

Table 5. — Mean values^ of lethal exposure time (in min-
utesT for coho salmon that had been acclimated to 20° C
water temperature and then subjected to various in-
creases in water temperature and saturation of nitrogen
gas.

Table 7. — Mean values^ of lethal exposure time (in min-
utes) for hatchery spring chinook salmon that had been
acclimated to 20° C water temperature and then sub-
jected to various increases in water temperature and
saturation of nitrogen gas.

Dead fish
in sample

Level

of
gasb

Lethal exposure timft of
various temperatures (" C)

20

27

Dead fish
in sample

Level

of
gosb

Lethal exposure time at
various temperatures (" C)

27

One fish

NN

..

__

_.

93

35

14

One fish

NN

__

__

720

34

33.5

5

NS

375

558

400

130

29

11

NS

255

ISO

71.5

38.5

9.5

SN

130

..

15

47

17

7.5

SN

__

__

41.5

6

8.5

5.5

SS

89

20

135

45

13

9.5

SS

30

30

7.5

15

10.5

3

Three fish

NN

._

..

104

47

14

Three fish

NN

84.5

44.5

6.5

NS

497

510

510

152

38

13

NS

360

345

372

86

43.5

14.5

SN

._

__

82

34

13

SN

__

__

795

39.5

16

7.5

SS

180

300

165

69

30

12

SS

45

67.5

30

28

16.5

4.5

Half of sample

NN

_.

..

..

121.5

60

20

Half of sample

NN

__

,.

..

95

51.5

8

NS

810

780

840

197

43

20

NS

450

435

570

97

48.5

17

SN

__

..

__

115

53.5

22

SN

__

__

620

66

23

8.5

SS

317,5

570

266

115

42.5

16

SS

75

176

42.5

44

22

6.5

All of sample

NN

..

.,

..

.,

93.5

37

All of somple

NN

_

_

__

153.5

63.5

13.5

NS

920

1,040

930

910

115

48

NS

780

690

750

133

66

27.5

SN

__

..

115

46

SN

__

__

820

110

46.5

19

SS

619

450

465

307

97

38.5

SS

397

675

600

97.5

52.5

13.5

a Mean of replicated tests.

b NN = normal saturation (100%) of nitrogen gas in occlimation and
test tanks;
NS = normal saturation in acclimation tank and supersoturotion

(125-130%) in test tanks;
SN = supersoturotion in acclimation tank and normal saturation in

test tanks;
SS = supersaturation in acclimation and test tanks.

a Mean of replicated tests.

b NN = norma! saturation (100%) of nitrogen gas in acclimation and
test tanks;
NS = norma! soturation in acclimation tank and supersoturotion

(125-130%) in test tanks;
SN = supersoturotion in acclimation tank ond normal soturotion In

test tanks;
SS = supersoturotion in acclimation and test tanks.

Table 6. — Mean values" of lethal exposure time (in min-
utes) for hatchery spring chinook salmon that had been
acclimated to 15° C water temperature and then sub-
jected to various increases in water temperature and
saturation of nitrogen gas.

Dead fish
in sample

Level

of
gasb

Lethal exposure time at
various temperatures (° C)

20

23

25

27

One fish

Three fish

Half of sample

All of sample

NN
NS
SN
SS

NN
NS
SN
SS

NN
NS
SN
SS

NN
NS
SN
SS

510
450
32.5

585
30

375

390

30

510

735

510

217

190

110

675

820

540

315

165

123

900

1,080

755

525

90.5
210
30
20.5

255

198

245

80

360
255
370
122.5

1,020
275
700
399

28

22
16 5
75
6.5

55

45

9

II

66
52.5
39.5
16.5

88.5
97
78.5
50

5

4.5
4
3

9

8.5
6.5
4

115
10.5
9
6

30.5
25
19.5
40.5

a Mean of replicated tests.

b NN = normol saturation (100%) of nitrogen gas in acclimation and
test tanks;
NS = normal soturotion in acclimation tank ond supersaturation

(125-130%) in test tanks;
SN = supersaturation in occlimation tank and normal soturotion in

test tanks;
SS = supersaturation in acclimation and test tanks.

Table 8. — Mean values" of lethal exposure time (in min-
utes) for wild spring chinook salmon that had been
acclimated to 10° C water temperature and then sub-
jected to various increases in water temperature and
saturation of nitrogen gas.

Dead fish
in sample

Level

of
gasb

Lethal exposure time at
various temperatures {° C)

20

23

25

Three fish

Half of sample

All of sample

NN
NS
SN
SS

NN
NS
SN
SS

NN
NS
SN
SS

NN
NS
SN
SS

-

—

—

720

660

660

600

780

--

--

780

405
1,080

495

187

150

58
900

870

660

27

61 118 9 4

645 463 163 17 3

98 312 4 2 1

35 68 10 3 I

192.5 27

465 43

80 9

71.5 6

82.5 5

195 4

7.5 2

7.5 3

193 27

165 43

80 9

600 780 71 6

a Mean of replicated tests.

b NN = norma! soturotion (100%) of nitrogen gas in acclimation and
test tanks;
NS = normal soturotion in occlimation tank and supersaturation

(125-130%) in test tanks;
SN = supersaturation in occlimation tank and normal saturation in

test tanks;
SS = supersoturotion in acclimation and test tanks.

837

FISHERY BULLETIN: VOL. 69. NO. 4

Table 9. — Mean values^" of lethal exposure time (in min-
utes) for steelhead trout that had been acclimated to
10° C water temperature and then subjected to various
increases in water temperature and saturation of nitro-
gen gas.

Dead fish
in sample

Level

of
gasb

Lethol exposure time at
various temperatures (° C)

25

One fish

NN

930

458

60

4.5

NS

195

172.5

230

230

60

8.5

SN

360

._

10

6

6

SS

57.5

15

6

6

8.5

5.5

Three fish

NN

..

__

200

10

NS

280

217

367

320

112

15

SN

__

__

206

9

SS

76

50

71

52

19

11

Half of sample

NN

__

__

225

14

NS

307

340

493

450

165

17

SN

__

366

14

SS

104

75

105

74

38

15

All of sample

NN

__

..

675

34

NS

660

660

780

690

465

80

SN

_.

52.5

SS

347.5

307.5

202.5

202.5

95

30

a Mean of replicated tests. ,

b NN = normal saturation (100%) of nitrogen gas in acclimation and
test tanks;
NS = normal saturation in acclimation tank and supersaturotion

(125-130%) in test tanks;
SN = supersaturotion in acclimation tank and normal saturation in

test tanks;
SS = supersaturotion in occlimotion and test tanks.

Table 10. — Mean values^ of lethal exposure time (in
minutes) for steelhead trout that had been acclimated
to 15° C water temperature and then subjected to var-
ious increases in water temperature and saturation of
nitrogen gas.

Dead fish
in sample

Level

of
gasb

Lethal exposure time at
various temperatures (" C)

26

28

One fish

NN

NS

SN

SS

Three fish

NN

NS

SN

SS

Half of sample

NN

NS

SN

SS

All of sample

NN

NS

225

570

480

480

207

7

15

25

14

14
660

645

570

600

390
151.5

30

56

30

21,5

840

630

645

435
495

45

94

52.5

43

320

870

900

720
840

SS

690

452.5 157.5 225

23

18

37.5

15

9.5

6

8

4,5

62.5

21

53.5

20

16.5

11.5

14

11

75

24

58

23.5

23.5

15

19

19

107.5

42

81.5

34.5

127.5

32.5

57.2

24.5

a Mean of replicated tests.

b NN = normol saturation (100%) of nitrogen gas in acclimation ond
test tanks;
NS = normol soturotion in acclimation tank and supersoturotion

(125-130%) in test tanks;
SN = supersaturotion in occlimotion tank and normal saturation in

test tanks;
SS = supersaturotion in acclimation and test tanks.

stressed fish were subjecte(i to temperature in-
creases in water supersaturateci at 125 to 130%,
however, the prior stress significantly (decreased
their tolerance at temperatures below 26° C.
Figure 1 shows only the data from populations
acclimated to 15° C (Tables 3, 6, and 10), but
similar cui-ves that clearly show the effect of
supersaturation can be constructed from the
data on populations acclimated to the other tem-
peratures.

Populations of echo salmon, steelhead trout,
and Chinook salmon acclimated to higher tem-
peratures were able to tolerate higher temper-
atures for longer periods in supersaturated
water as well as in normally saturated water.
A comparison of our LEso curves for coho with
those of Brett (1952) indicates that tolerance
to higher temperatures in supersaturated water

PERCENTAGE SATURATION NITROGEN

Tsti Wdltr

100 %

(GO % A

115-120

100 A

100

125-150 o

1 15-120

IZS-130 .

240 360 460

TirriE (minutes)

Figure 1. — Comparison of i,E;,(| curves of hatchery-reared
juvenile coho salmon, spring chinook salmon, and steel-
head trout acclimated at 15° C and stressed at various
levels of nitrogen saturation.

838

EBEL, DAWLEY, and MONK: THERMAL TOLERANCE

was considerably lower at exposures over 100
min for the same acclimation temperature than
at normal saturation levels (Figure 2).

A comparison of the NN and SN curves (Fig-
ure 1) indicates that the prior stress of super-
saturation of nitrogen had little effect on the
fish when they were subjected to test water that
was not supersaturated. This suggests that mi-
grating salmon and trout under stress from su-
persaturation of nitrogen gas could recover from
the effects of supersaturation if there were
river areas where water would equilibrate.
These data also show that salmon and trout pop-
ulations acclimated at 15° C and subjected to
nitrogen saturation of 125 to 130% will probably
have about 50% mortality in less than 360 min
with no temperature increase when stressed for
12 hr before testing and that subjecting the pop-
ulations to temperature increases merely re-
duces the time to death.

In comparing the tolerance to temperature in-
creases between coho and spring chinook salmon,
we found that the results from the control tests —
where both acclimation and test water were at
100% saturation — were similar to the results of
Brett (1952). That is, coho were more tolerant
than chinook and the respective upper lethal tem-
peratures were 25 to 26° C. Brett did not study
steelhead trout. We found that steelhead trout
were nearly identical to coho in their tolerance

200 300

TIME TO DEATH (minutes)

Figure 2. — Median-resistance-time (LE50) plotted from
temperature tolerance tests with coho salmon fingerlings
acclimated at 5°, 10°, and 20° C and stressed for 12 hr
at 115-120% saturation of N2, then subjected to temper-
ature increases in water supersaturated at 125-130%.
Brett's LE51) curves for fish acclimated at 5° and 20° C —
without N2 stress — are shown for comparison.

to temperature increases when supersaturation
of nitrogen was not present (control tests) but
were the most vulnerable species when super-
saturation was entered as a factor. Figure 3
compares the tolerance of three species to tem-
perature increases when acclimation water and
test water were supersaturated. Coho were the
most tolerant, wild spring chinook next, and
steelhead the least tolerant.

30

s-+-~

25

0 XV ^ " — -J^__^^^

z

\~^ ^

_________^

-20

■+—

\

K

3

< 15

E

a.

S

K 10

-*■ COHO Y = Z7716-00I624X

0 CHINOOK T = 26 095 -0 042 X

X STEELHEAD r = 26 095 -0 042 X

5

ACCLIMATION TEMreHATURE I0*C

0

1 1 1 i 1 1 1

1 1 1

Figure 3. — Comparison of LE50 values between species
of salmonid juveniles (acclimated at 10° C) in tolerance
to tempei-ature increases when stressed by 115-120%
saturation of nitrogen gas for 12 hr, then subjected to
temperature increases in supersaturated water at 125-
130% nitrogen.

Size of fish at time of testing could influence
the comparison between species. Coho and wild
spring chinook acclimated at 10° C were nearly
the same size at time of testing (Table 1), but
steelhead acclimated at 10° C were larger than
the other species when tested. There is evidence
that extremely small chinook fry are more sus-
ceptible to nitrogen supersaturation than finger-
lings; then, as the fingerlings increase in size,
they become more susceptible than the small
fingerlings but less susceptible than the fry
(Meekin, 1969).' If this occurs with steelhead
also, it could account for their lower tolerance.
During one test with coho acclimated at 15° C,
we found no differences in susceptibility within
the size range tested (101-151 mm) at 125 to
130% saturation.

' Personal communication, Thomas Meekin, Washing-
ton State Department of Fisheries. Experiments at
Priest Rapids Dam.

839

FISHERY BULLETIN: VOL. 69, NO. 4

We intended to compare hatchery-reared Chi-
nook salmon with wild or naturally migrating
spring Chinook salmon acclimated to the same
temperature. Wild fish were available only when
they were acclimated to temperatures near 10° C.
The hatchery population had deteriorated by
then, however, so we compared wild fish accli-
mated at 10° C and hatchery fish acclimated to
15° C (Figure 4). As expected, the hatchery
population — acclimated at the higher tempera-
ture— was able to tolerate the highest temper-
atures for a longer period, but when the LEso
curves — which include the effect of nitrogen —
are compared, little difference can be noted. This
indicates that results achieved in the laboratory
with hatchery stocks can be applied to wild Co-
lumbia River stocks with reasonable accuracy.

SPRING CHINOOK (WILD)
10° C ACCLIMATION

SPRING CHINOOK I HATCHER'T REARED)
I5°C ACCLIMATION

PERCENTAGE SATURATION NITROGEN

_l L I L.

100 X

106% a

115-120

too •

(00

125-150 o

I(S-I20

240 360 480

TIME |minul«>)

FlGllKE 4. — Comparison of le-,q curves between juvenile
wild and hatchery spring chinook salmon at various tem-
peratures and levels of saturation of nitrogen gas.

EFFECT OF DEPTH ON RELATION

BETWEEN SUPERSATURATION OF

NITROGEN AND TOLERANCE OF

JUVENILE FISH TO TEMPERATURE

INCREASES

Examination of fish in cages at the forebay of
Priest Rapids Dam (Ebel, 1969) indicated that
juvenile coho and chinook salmon would not con-
tract gas bubble disease if held at a sufficient
compensating depth (5 m). This finding sug-
gests that fish subjected to temperature in-
creases in addition to nitrogen supersaturation
would also be less affected if they remained at
sufficient depth when they encountered a tem-
perature increase.

To test this hypothesis, we subjected coho
salmon acclimated at 10° C to three temper-
atures above acclimation in water supersatur-
ated at 130^f in the 9-m (deep) tank where they
could select any depth from the surface to 9 m ;
we then compared LEioo curves in the 20-cm
(shallow) tanks with those in the deep tank
(Figure .5). These curves definitely indicate
that the coho benefited by having the option to
sound in the deep tank. The LEioo level never
was reached during the 18-hr observation period
when the fish were subjected to 20° C (10° C
increase) in the deep tank, but occurred after

, -t 23° C

360 480

TIME

600 720
t mtnulti)

Figure 5. — Comparison of lEiqq curves for coho salmon
acclimated at 10° C and subjected to three temperatures
(15°, 20°, and 23° C) in 20-cm and 9-m deep tanks
containing water supersaturated with nitrogen gas at
130'/' saturation. Oxygen concentrations varied from
115 to 125% saturation.

840

EBEL, DAWLEY, and MONK: THERMAL TOLERANCE

about 17 hr in the shallow tank. Similarly at
15° C (5° C increase), the LEso level was never
reached in the deep tank but was reached in
about 12.5 hr in the shallow tank. No benefit
from depth is indicated in the curves at 23° C ; in
this comparison, the fact that temperature in the
deep tank was 0.8° C higher (23.8° C) than that
in the shallow tank could account for the lack
of difference.

Wild juvenile spring chinook salmon from the
gatewells at McNary Dam also were tested in
the deep and shallow tanks. These fish were
acclimated at 10° C and then subjected to a 5° C
increase (15° C) with supersaturation of nitro-
gen gas at 130 '/f saturation. The fish also were
stressed for 12 hr before the test in 10° C water
supersaturated at 120% saturation. Again, chi-
nook tested in the deep tank survived at a higher
rate than those in the shallow tanks; the LEso
was never reached in the deep tank, whereas
100% mortality was reached in approximately
11 hr in the shallow tanks (Figure 6).

Observations in the deep tank during tests
with the coho and chinook salmon indicated that
most fish remained between about 1 and 4 m
of the surface. Light intensity and turbidity
possibly influenced the depth distribution. Dur-
ing these tests, artificial light at an intensity of
about 100 footcandles was present at the surface
of the water. Turbidity in the tank was min-
imal; a Secchi disc was visible at the bottom
of the tank and the Jackson turbidity unit
measurement was 0.

It is difficult to relate tests in the tank to na-
tural conditions because turbidity in natural
water varies greatly. In the Snake River, tur-
bidity as measured by a Secchi disc varies from
0.2 to 8.0 m, depending on season and location.
Turbidity usually is high during the spring run-
off in both the Snake and Columbia Rivers; read-
ings are seldom over 1 m on the Snake River
(Ebel and Koski, 1968). This high turbidity
limits visible light penetration to a maximum of
about 1.5 m (observation verified by scuba div-
ing). We therefore believe that juveniles as
observed in the tank were at greater depths than
they might be in the Snake or Columbia Rivers
during the spring migration. Durkin, Park, and

100

^.

15*

C

^

"

MPTM Of TW*K

90

,

'

9M TANN

t

-

'

- - ZOCM TROUGH

4

O 60

/

Z

.:

<»

/

S ""

/

___,

a

1

, ■"

20
0

■ 1/

-•— T '

_

i-

—

^'^

1 1 1 1

Figure 6. — Comparison of le,„q curves of wild spring
chinook salmon acclimated at 10° C and subjected to a
5° C increase (15° C) in tanks 20 cm and 9 m deep that
were supersaturated with nitrogen gas at 1307c satura-
tion. Oxygen concentrations varied from 115 to 125%
saturation.

Raleigh (1970) found that most juvenile salmon
were near the surface as they entered Brownlee
Reservoir. Fish in the Columbia and Snake
Rivers apparently do not sound to a depth suf-
ficient to compensate for nitrogen saturation
levels exceeding 130% ; hence the mortalities re-
ported herein are probably on the conservative
side. We also emphasize that even though the
option of having sufficient depth reduced the
mortality rate, substantial mortalities occurred.

TEMPERATURE STANDARDS

FOR RIVERS WITH

NITROGEN SUPERSATURATION

Our test temperatures and experimental de-
sign were purposely selected so that these data
could be compared with the results reported by
Brett (1952). Brett cautions that the informa-
tion he presents should not be applied verbatim
to other environments. Because of the excel-
lence of his work and the lack of later findings
concerning temperature tolerance of Pacific
salmon, the upper lethal levels established in his
paper are widely quoted and used for setting
temperature tolerance standards for rivers and
streams containing salmon — without regard to
other physical and chemical characteristics of
the water. The changes in Brett's tolerance
curves caused by the stresses of supersaturation
of nitrogen gas were obvious.

841

FISHERY BULLETIN: VOL. 69, NO. 4

Although complete statistical analysis of our
data are not presented in this paper, the dif-
ferences shown between tolerance cui'ves of fish
tested in water with and without supersatura-
tion of nitrogen are so great that conclusions
concerning the effect of supersaturation can be
made with relative confidence.

Substantial mortalities will occur to migrating
juvenile salmon and trout in the Columbia and
Snake Rivers — even if no thermal plume or in-
crease in temperature is encountered — when-
ever the populations must pass through large
areas where 125 to 1309^ saturation of nitrogen
occurs. Studies of vertical distribution (e.g.,
Smith, Pugh, and Monan, 1968; Durkin et al.,
1970) indicate that the majority of migrants
are in surface waters, with substantial numbers
in waters less than 2 m deep. This is too shallow
to compensate for nitrogen levels as high as
ISO^/c Surveys of nitrogen levels by Ebel
(1969), by Beiningen and Ebel (1971), and by
NMFS and State fisheries personnel of Wash-
ington and Oregon during the 1970 spring mi-
gration, verify that nitrogen in large areas of
both rivers exceed 130 9f saturation. Exami-
nation of fish in cages suspended on the surface
and at various depths revealed that mortalities
caused by nitrogen often exceeded 40''/r in a deep
(4.5 m) cage where the fish could sound at their
volition. Periodic checks of juveniles in the
Snake River by NMFS personnel in 1970 indi-
cated that 25 to 45 ';r of the chinook salmon and
30 to 58% of the steelhead trout migrants arriv-
ing at Ice Harbor Dam had external symptoms
of gas bubble disease. We made similar obser-
vations of migrants at The Dalles and McNary
Dams in 1968 and 1969 and recorded similar
findings.

Obviously the migrating juvenile salmon and
trout in the Columbia and Snake Rivers are
under stress during periods of nitrogen super-
saturation. Any increase in temperatui-e over
the ambient river temperature, then, will harm
these populations. Mortalities already occur-
ring will be accelerated even with minimal tem-
perature increases. Our data show that LE.-.n
levels of temperature (Figures 1-4) are far high-
er than could be accepted as standards for ui)per
limits of rivers containing trout and salmon even

at normal concentrations of dissolved nitrogen.
The time to first mortality of wild spring chinook
salmon, for example, that were acclimated to
10° C and tested in supersaturated water at 23°
and 25° C was 10 and 3 min, respectively (Table
8). Temperatures and temperature increases
such as these occur in thermal effluents (Cou-
tant, 1969), and substantial mortalities could
occur to juvenile salmon and trout passing
through thermal plumes.

During spring and summer when flows are
low, increases in temperature of the Columbia
River from Priest Rapids Dam to the forebay
of McNary Dam have been as high as 2.5° C
(Ebel, 1969). Increases in temperature over
the acclimated temperature greatly accelerated
time to death of juveniles when supersatura-
tion of nitrogen gas was present in the test
water whether the fish were held in shallow or
deep tanks. However, during the low flow peri-
ods when temperature increases such as this
occur, nitrogen saturation levels are usually low
and mortalities such as indicated in the tests
would not occur.

The obvious results of these tests are that
supersaturation of nitrogen must be considered
when setting temperature standards and that
any increase allowed over the ambient temper-
ature of the river during periods when the river
is supersaturated with nitrogen will be detri-
mental to salmon and trout populations.

CONCLUSIONS

1. Supersaturation of nitrogen drastically af-
fects the tolerance of juvenile coho salmon, chi-
nook salmon, and steelhead trout to temperature
increases. Tolerance to increases below 26° C
is lowered and mortality rates are accelerated.

2. Acclimation to higher temperatures will en-
able the three species to tolerate higher temper-
atures longer when nitrogen supersaturation is
a factor; however, 50% mortality will be
reached in loss than 18 hr at all acclimation
temijeratures with supersaturation of nitrogen
at 125 to 130%. No temperature is suitable at
the 125 to 130''^ level of nitrogen supersatura-
tion.

3. Dei)th is an important compensating factor

842

EBEL. DAWLEY, and MONK: THERMAL TOLERANCE

when supersaturation of nitrogen is present.
Tests in the deep (9-m) tank, where fish were
free to roam from the surface to the bottom,
revealed that mortality rates were much lower
and tolerance to temperature increases was in-
creased if the juveniles had the option to sound
when subjected to temperature increases.

4. Coho were the most tolerant, chinook next,
and steelhead the least tolerant to temperature
increases when the water was supersaturated
with nitrogen. When supersaturation was not
a factor, coho and steelhead were about equally
tolerant to temperature increases and chinook
the least tolerant.

5. Any increase in temperature allowed over
the ambient temperature (whether high or low)
of the river during periods of supersaturation
of nitrogen will be detrimental to migrating ju-
venile salmon and trout. Temperature stan-
dards should account for the effect of supersatu-
ration of nitrogen gas.

LITERATURE CITED

Beiningen, K. T., and W. J. Ebel.

1971. Dissolved nitrogen, dissolved oxygen, and
related water temperatures in the Columbia and
lower Snake Rivers, 1965-69. Natl. Oceanic
Atmos. Admin., Natl. Mar. Fish. Serv., Data Rep.
56, 60 p.
Brett, J. R.

1952. Temperature tolerance in young Pacific

salmon, genus Oncorhynchus. J. Fish. Res. Board
Can. 9: 265-323.
1958. Implications and assessments of environ-
mental stress. In P. A. Larkin (editor). The in-
vestigation of fish — power problems, p. 69-83.
H. R. MacMillan Lectures in Fisheries, Inst. Fish.,
Univ. B.C., Vancouver, B.C.
COUTANT, C. C.

1969. Temperature, reproduction and behavior.
Chesapeake Sci. 10: 261-274.

DuRKiN, J. T., D. L. Park, and R. F. Raleigh.

1970. Distribution and movement of juvenile
salmon in Brownlee Reservoir, 1962-65. U.S.
Fish Wildl. Serv., Fish. Bull. 68: 219-243.

Ebel, W. J.

1969. Supersaturation of nitrogen in the Columbia

River and its effect on salmon and steelhead trout.

U.S. Fish Wildl. Serv., Fish. Bull. 68: 1-11.
Ebel, W. J., and C. H. Koski.

1968. Physical and chemical limnology of Brovioilee
Reservoir, 1962-64. U.S. Fish Wildl. Serv., Fish.
Bull. 67: 295-335.

Fry, F. E. J., J. S. Hart, and K. F. Walker.

1946. Lethal temperature relations for a sample

of young speckled trout, (Salvelinus fontinalis).

Univ. Toronto Stud., Biol. Ser. 54 (Publ. Ont.

Fish. Res. Lab. 66) : 9-35.
MiHURSKY, J. A., and v. F. Kennedy.

1967. Water temperature criteria to protect
aquatic life. Am. Fish. Soc, Spec. Publ. 4: 20-33.

PuGH, J. R., A. B. Gro\'es, and W. J. Ebel.

1969. Experimental tank to simulate certain res-
ervoir conditions. J. Fish. Res. Board Can. 26 :
1956-1959.

Smith, .1. R., J. R. Pugh, and G. E. Monan.

1968. Horizontal and vertical distribution of ju-
venile salmonids in upper Mayfield Reservoir,
Washington. U.S. Fish Wildl. Serv., Spec. Sci.
Rep. Fish 566, 11 p.

843

CONTRIBUTION TO THE POPULATION DYNAMICS OF ATLANTIC
ALBACORE WITH COMMENTS ON POTENTIAL YIELDS'

Grant L. Beardsley-

ABSTRACT

Length-frequency data on Atlantic albacore from the Bay of Biscay surface fishery and the Atlantic
longline fishery were analyzed. Lengths at age were estimated and the von Bertalanffy growth param-
eters wei-e calculated: K = 0.141, Loo = 140 cm, and tp = —1.63 years. Instantaneous rates were
computed on an annual basis. The total instantaneous mortality coefficient was estimated as 0.96 for
albacore in the Bay of Biscay fishery and 0.79 in the longline fishery. Analysis of catch and effort data
suggested that greater yields are available from the North and South Atlantic longline stocks though
stock identification in the South Atlantic is not clear. Estimates of population structure in the North
Atlantic were made by utilizing total instantaneous mortality rates of 0.50, 0.96, and 1.40 and an in-
stantaneous natural mortality rate of 0.23. The population based on a total mortality coefficient of 0.96
appeared to be the most reasonable.

The albacore, Thunnus alalunga, has become in-
creasingly important to the Atlantic tuna fish-
eries in recent years. From 1956 to 1961 the
Japanese longline fishery in the Atlantic was
primarily directed at yellovvfin tuna, T. albacares,
but rapidly declining catch rates for yellowfin
soon forced a shift of fishing into primarily al-
bacore areas (Wise, 1968). As a result of de-
creased yellowfin catches and a corresponding
shift in fishing toward albacore, the average
number of albacore caught yearly by the Jap-
anese in the Atlantic increased from 228,000 in
the years 1956-61 to 1,332,857 in the years 1962-
68. The percentage of albacore in the combined
catch of albacore and yellowfin in the Atlantic
by the Japanese rose from an average of about
18.7^; in 1956-61 to 67.7% in 1962-68
(Figure 1).

Since 1965 the Japanese have significantly cur-
tailed their longline fishing in the Atlantic. From
a high of almost 100 million hooks in 1965, they
set slightly over 30 million hooks in 1967 and
again in 1968. This decrease, however, has been
offset by the entry of China (Taiwan) and South
Korea into the fishery as well as small amounts

' Contribution No. 203, National Marine Fisheries
Service, Southeast Fishery Center, Miami, Fla. 33149.

- National Marine Fisheries Service, Southeast Fish-
ery Center, Miami, Fla. 33149.

100
90-
80
70

S 60-

50-
^ 40
30
20

10

-2

percent albacore
no. albacore

-f^

p

o

o

Manuscript accepted June 1971.

FISHERY BULLETIN: VOL, 69. NO, 4, 1971

1 I I — 1 — I — I — I — 1 — I — I — I — r
1956 '60 65 68

YEAR

Figure 1. — Total number of albacore caught and the
percentage of albacore in the combined yearly albacore-
yellowfin tuna catch by Japanese longliners in the At-
lantic Ocean, 1956 through 1968.

845

FISHERY BULLETIN: VOL. 69. NO. 4

of fishing by Cuba and Venezuela. In 1968 the
combined landings of albacore by China and
South Korea were about 15,500 metric tons,
which was only 1000 tons less than the Japanese
catch for 1968. Recent estimates have placed
the Atlantic albacore catch for 1969 by China
and South Korea at 19,300 meti-ic tons.

Worldwide demand for tuna is increasing
every year, and there is growing concern over
the condition and well being of Atlantic tuna
stocks. Catch rates of yellowfin tuna in the
longline fishery suffered severe declines in the
1960's. Wise (1968), Food and Agriculture
Organization (1968), Wise and Fox (1969),
Hayasi and Kikawa (1970), and others have
examined the problem and have concluded that
the longline stocks of yellowfin tuna have been
fished beyond their maximum capacity.

This paper is an analysis of some aspects of
the population dynamics of Atlantic albacore
with comments on potential yields and stock size.

AGE AND GROWTH

There have been few studies on the age and
growth of Atlantic albacore. Distinct modes
appear in length-frequency distributions of al-
bacore samples from the Bay of Biscay surface
fishery, and these modes probably represent age-
groups. There is considerable disagreement,
however, over the assignment of absolute ages
to Atlantic albacore (Table 1).

Le Gall (1949, 1952) worked with length fre-
quencies from the Bay of Biscay. He stated
that age-group I was less than 48 cm in length,
and that the first group that appeared in the
fishery was age-group II (56 cm). Figueras
(1957) used vertebrae from 67 fish in his anal-
ysis and concluded that 56- to 57-cm albacore
were 4 years old and that 17- to 18-cm albacore
were 1 year old. Yang (1970) estimated that
56-cm albacore were approximately 3 years old
based on results of his analysis of annular mark-
ings on scales. Otsu and Uchida (1959b), how-
ever, concluded from their study of vertebrae,
scales, and other hard parts of Pacific albacore
that there were no markings that could be con-
sidered age marks.

I used data from the Bay of Biscay for 1967,
1968, 1969, and 1970 (Allain and Aloncle, 1968;
Philippe Serene and Jean-Claude Dao, Centre
National pour I'Exploitation des Oceans, person-
al communication) (Figure 2) as well as long-
line data (Figui-e 3) and estimated lengths at
age for Atlantic albacore (Table 1).

Lengths at ages 1, 2, 3, and 4 wei-e estimated
by modes in length-frequency histograms from
Bay of Biscay samples. The first mode distin-
guishable in the length frequencies (Figure 2,
1968) is at approximately 44 cm, and I assume
that it represents age-group I. There is su])port
in the literature for the assignment of this ap-
proximate length to 1-year-old albacore. Otsu
and Uchida (1963) indicated that 30- to 35-cm

Table 1. — Summary of age and growth investigations on Atlantic albacore.

Method

Sample
size

Age (years)

1

2

3

4

5

6

7

8

9

10

Scales
(total length)

50

Priol (1944)

50-58

59-74

74-86

86-94

94-98

Le Gall (1949)

Length frequencies
(total length)

<25

25-46

46-60

60-74

74-88

Le Gall (1952)

Length frequencies
(total length)

50,000

<48

56

68

81-82

>93

_.

..

..

..

Figueras (1957)

Vertebrae
(total length)

67

17-18

31-32

44-45

56-57

69-70

81-82

91-93

_

Yang (1970)

Scoles

(fork length)

159

20.3

39.6

56.1

71 2

80.9

90.3

98.1

Beardsley

(present study)

Length frequencies
(fork length)

152,602

44

55

64

75

87

95

100

104

108

112

846

BEARDSLEY: POPULATION DYNAMICS OF ATLANTIC ALBACORE

^1

196i
N:M40

»'

i

«■

r

1 J

1

_A_

"U "k

, . J^

If

T^

i

!969

1970
l( = IS717

»o-

0'

, r.^ ,

]#k..„,

rfi

1 n

? s s s s s

lOliK lEKGIH ICM>

Figure 2. — Albacore length-frequency distributions from
the Bay of Biscay surface fishery, 1967-70. Estimated
ages in years are shown above the histograms.

>-

Z
-; 4

5

4

N. 31,707

r

'78

, mTfl 11,111 _

lio

FORK LENGTH (CM)

Figure 3. — Albacore length-frequency distribution from
the Atlantic longline fishery, several years combined.
Estimated ages in years are shown above the histograms.

albacore occasionally appear in the Japanese live-
bait fishery in spring, and they assume that these
fish are approximately 1 year old. On this basis
they assign 2, 3, and 4 years of age to 55-, 65-,
and 76-cm albacore respectively in the United
States west coast fishery. Yoshida (1968)
studied age and growth of juvenile albacore
based on 35 specimens recovered from stomachs
of billfishes in the Pacific. He derived a hatch-
ing date of May 1 based on a regression analysis
of length of the juveniles against month of cap-

ture and concluded that 1-year-old albacore are
approximately 38 cm standard length. Although
I have assigned a length of 44 cm to age-group
I, a more practical approach would probably be
to accept Le Gall's (1952) statement that 1-year-
old albacore are "less than 48 cm in length."

Longline length frequencies were used to esti-
mate ages 5 and older (Figure 3). The assign-
ment of ages beyond age 5 is somewhat subjec-
tive. I assigned ages 7 and 8 to the modes ap-
pearing at 100 to 101 and 104 to 105 cm. Other
ages were assigned mostly by extrapolation. My
estimates agree in most cases with those made
for Pacific albacore by Otsu and Uchida (1963).
No attempt was made to assign ages beyond age
10 although undoubtedly some albacore in the
Atlantic live to be older than 10.

The two modes which correspond to ages 3 and
4 in the longline samples (68-69 and 78-79 cm)
are located at a length of 3 to 6 cm greater than
the same age in the Bay of Biscay samples. Yang
(1970) stated that ring formation on albacore
scales occurred in February-March for North
Atlantic albacore. The Bay of Biscay samples
were taken in summer, and the albacore had
completed approximately a half year's growth.
Most 3- and 4-year-old albacore captured by
longliners are taken in winter when they are
first recruited to the fishery. These 3- and 4-
year-old fish are at the end of a year's growth
or just beginning a new year's growth, and the
disparity in the position of the modes between
the longline samples and the Bay of Biscay
samples represents growth during the period be-
tween the summer fishery and the winter fishery.

GROWTH PARAMETERS

I constructed a Walford line (Figure 4) using
the lengths at age from this study (Table 1) and
took the intercept of the 45° diagonal as an initial
trial value for L„ in the expression for growth
(von Bertalanfl'y, 1938):

lege (L„

Lt) = logeL,

KU — Kt.

A best fit was obtained with L„ = 140 cm. K
was calculated as 0.141, and U was — 1.63 years.
Yang (1970) found L = 135 cm and K = 0.19

847

FISHERY BULLETIN: VOL, 69, NO. 4

0 ■ 40 60 80 100 120 MO 160 180 200

FORK LENGTH (AGE I)

Figure 4. — Walford transformation of length in centi-
meters at age t + 1 against length at age ( for Atlantic
albacore.

from his analysis of albacore growth. The
growth curve based on my calculations is shown
in Figure 5.

AGE (YEARS)
Figure 5. — Growth curve for Atlantic albacore.

LENGTH-WEIGHT

De Jaeger (1963), de Jager, Nepgen, and
van Wyk (1963), van den Berg and Mat-

thews (1969), and Nepgen (1970) published in-
formation on the length-weight relation of
Atlantic albacore. All gave separate equations
for males and females although de Jaeger (1963)
was unable to detect any significant differences
in his samples. I combined data from the long-
line fishery and the Bay of Biscay fishery and
calculated a length-weight equation for both
sexes combined since sex information was not
available for most of the samples at the smaller
sizes:

W = 6.303 X 10-« X L328253

Weight is in kilograms and length is fork length
in centimeters (Figure 6).

30-

,;:■

2S-

^l^'

O'O-

■ ' •-■■ -

f

1-

i

UJ

y ^•

10-

X/'

s-

Jb{Rv

0

V —

T r

T r

1 1

Figure 6.-

FORK LENGTH (CM)

-Length-weight relation of Atlantic albacore,
both se.xes combined.

SEX RATIO

Five hundred ninety-eight albacore were
measured and sexed at canneries located in
Puerto Rico from December 1969 to September

848

BEARDSLEY: POPULATION DYNAMICS OF ATLANTIC ALBACORE

66' ?? 76 80 84 88 v: 96 100 104 108 112

69 73 77 81 85 89 93 97 101 105 109 11*3

FORK LENGTH (CM)

Figure 7. — Length-frequency distribution of 598 male
and female albacore measured at canneries in Puerto
Rico from December 1969 to September 1970. All were
caught in the Atlantic by longline gear.

1970. Males constituted 61% of the samples
and were more abundant at the larger sizes
(Figure 7). Few females appear to attain a
length of much over 100 cm. This dominance
of males both in numbers and at the larger
sizes has been reported for Pacific albacore
by Otsu and Uchida (1959a, 1959b) and Otsu
and Hansen (1962) and for Atlantic albacore
by de Jaeger (1963) and Talbot and Penrith
(1963).

MORTALITY

There have been no mortality estimates for
Atlantic albacore that I am aware of. Suda
(1963) stated that the total instantaneous mor-
tality coefficient of North Pacific albacore is
probably around 0.4. He later estimated that
the natural mortality coefficient for the same
stock is about 0.2 (Suda, 1966). I estimated
the total instantaneous mortality coefficient (Z)
for Atlantic albacore using Bay of Biscay length
frequencies (Figure 2) and longline length fre-
quencies (Figure 3). All mortality rates in
the following discussion are instantaneous rates
unless specifically designated as annual.

BAY OF BISCAY

If we assume that the 1967, 1968, 1969, and
1970 samples from the Bay of Biscay are reason-
ably representative of the total catch which is

in turn an accurate estimator of the true rel-
ative abundance of the different age groups in
the fishery, we can calculate a total mortality
coefficient from the decline in abundance of a
given year class from one year to the next, be-
ginning with the first year it is fully recruited
(age 3). This method requires weighting the
frequencies by catch per unit of eflfort (CPUE) .
Accurate estimates of CPUE for the entire Bay
of Biscay fishery are not available, although re-
cent research suggests that a slight decline in
CPUE has occurred at selected ports in France
in the late 1960's (Jean-Claude Dao, personal
communication). I have assumed a constant
CPUE over the 4 years in question for the pur-
pose of this analysis since complete figures are
not available.

I have also assumed equal i-ecruitment for ages
3 and 4 though this is not likely. Any mortality
estimates based on the relative abundance of ages
3 and 4 in the fishery will be affected by relative
differences in recruitment. Some 3-year-old al-
bacore and many 4-year-olds are recruited to the
winter longline fishery in the North Atlantic;
however, for the 4 years, 1965-68, the average
number of 4-year-old albacore caught in the
North Atlantic winter fishery was only about
40,000. This is a relatively insignificant number
when compared with the total number of 4-year-
olds available in the Bay of Biscay fishery. It
is not known if all the survivors return to the
Bay of Biscay the following summer although it
is probable that most of them do. If 4-year-old
albacore do not all return to the Bay of Biscay
from the winter longline grounds then mortal-
ities will be slightly overestimated.

Mortality coefficients were calculated from the
decline in abundance from age 3 to age 4 only,
and the frequency polygons were divided in the
following manner. Where there was an obvious
null between age classes, for example at 70 to 71
cm in the 1967 plot, the number of fish in that
length group were evenly divided, half were as-
signed to the age above and half to the age below.
Where there was no obvious null, as between ages
2 and 3 in the 1969 plot and between ages 4 and 5
in almost all the plots, the dividing point was
placed at a length approximately half way be-
tween the assigned lengths at age obtained from

849

FISHERY BULLETIN: VOL. 69, NO. 4

Table 1. Using this method I obtained the fol-
lowing values of Z:

Year class Z

1964 (3 years old in 1967) 0.73

1965 (3 years old in 1968) 1.04

1966 (3 years old in 1969) 1.12

The average total mortality coefficient over the
3 years was estimated to be 0.96.

LONGLINE FISHERY

A total mortality coefficient was calculated for
albacore in the longline fishery using a formula
derived by Beverton and Holt (1956):

Z = K {L.

L)

L — Lr

where L is the average length of the fish in the
catch that are as large as or larger than the first
fully recruited length, Lr.

Using: L«,
K
L

Lr

then:

140 cm
0.141
94.2 cm
86 cm

0.79

The total mortality coefficient is not incom-
patible with the average Bay of Biscay estimate
if we consider that the longline is probably rel-
atively inefficient compared with surface gear;
hence fishing mortality in the longline fishery
and consequently total mortality (assuming nat-
ural mortality stays nearly the same throughout
the life span of the fish) is probably less than in
the surface fishery.

The albacore samples used to estimate mor-
tality in the longline fishery were taken over
several years from different areas in the Atlantic.
It is very likely, however, that the composite
length-frequency distribution in Figure 3 is not
a completely accurate picture of the length com-
position of albacore in the Atlantic. Size distri-
bution in the winter fishery, for example, is en-

tirely diflS'erent from that in the summer fishery,
and suitable samples from each fishery would
have to be taken to ensure a representative pic-
ture over the entire ocean.

YIELD ESTIMATES

There are five major areas in the Atlantic
where longliners concentrate on albacore. I
have designated these areas A through E in
Figure 8 and for ease of discussion will sub-
sequently refer to these areas by their letter
designation. Areas A, B, C, and D were de-
scribed by Beardsley (1969) and Koto (1969)
as major fishing areas. Area E off the coast
of Argentina, Uruguay, and southern Brazil has
only recently developed into a relatively major
albacore fishing area. Of the four areas dis-
cussed by Beardsley and Koto, only area C has
shown a decline over the years in catch rate
(Figure 9). Areas A and D produce fish that
are relatively small for longline fish and pre-
sumably are recruits to the longline fishery.
Recent size data obtained from albacore landed
in Puerto Rico and caught in area E reveal that
small albacore are also a large part of the catch
in this area.

60»W

FiGiiRE 8. — The ma.ior lonKline fishing areas for albacore
in the Atlantic Ocean.

850

BEARDSLEY; POPULATION DYNAMICS OF ATLANTIC ALBACORE

o H
o

Q

Z
D
X

X
U

u

4-
2-

Area A

CPUE -
EFFORT-

- 8

Area B

12 OO

X

» z

Area C

Area D

Area E

'" O

•24 2

20

-16

12

X

O
O
7<;

YEAR

Figure 9. — Total longline effort and catch per unit of
effort (CPUE) for the five major albacore fishing areas
in the Atlantic Ocean, 1956-68.

NORTH ATLANTIC

The North Atlantic supports two different al-
bacore fisheries, the longline fishery and the Bay
of Biscay surface fishery, while the South Atlan-
tic has only the longline fisheiy. The Bay of Bis-
cay fishery, conducted primarily by the French
and Spanish, has yielded about 45,000 metric
tons annually since 1963. The fishery catches
primarily 3- and 4-year-old albacore before they
are fully recruited into the longline fishery.

There is evidence that albacore stocks in the
North and South Atlantic are separate ( Beards-
ley, 1969; Koto, 1969; Yang, Nose, and Hiyama,
1969) . Koto indicates, however, that there may
be some mixing of immature albacore between
the South Atlantic and Indian Oceans. I com-
bined catch and effort data from the two major
albacore fishing areas in the North Atlantic and

from the three areas in the South Atlantic and
treated each group as separate stocks.

From 1957 through 1965 I used only Japanese
data (Shiohama, Myojin, and Sakamoto, 1965;
Fisheries Agency of Japan, 1966, 1967a, 1967b)
since the longline fishery during those years was
almost exclusively Japanese. For 1966, 1967,
and 1968 I used Japanese data (Fisheries Agen-
cy of Japan, 1968, 1969, 1970) as well as esti-
mated Chinese and Korean catch data (Wise,
1970) . Catch per unit of eflfort (CPUE) in this
discussion is the number of albacore caught per
hundred hooks fished. CPUE was calculated by
summing the number of albacore caught in a
given ai'ea in a given year, multiplying by 100,
and dividing by the number of hooks fished in
that area during the year. Only the catch data
were available from the Chinese and Korean
fishery. Total Chinese and Korean fishing effort
for 1966, 1967, and 1968 was obtained by using
Chinese and Korean albacore landings and Jap-
anese CPUE and back calculating to the number
of hooks fished. This procedure assumes that
CPUE for the Chinese and Korean fleets was the
same as for the Japanese fleet. This is probably
not true; however, the difference is not likely
to be large. The Chinese and Korean fishing
effort in the Atlantic was not great until 1968
and by then their fishing efficiency was probably
comparable to that of the Japanese.

One of the more common mathematical models
used to express yield from a stock of fish is the
equilibrium-yield model used by Graham (1935) ,
Schaefer (19-54, 1957), and others. One of the
major advantages of this ty]5e of model is that
it requires only catch and effort data. Assuming
a fishery that has attained equilibrium condi-
tions, a plot of CPUE against effort should show
a linear decline which will produce a parabolic
curve of yield when plotted against effort. Fox
(1970) has argued that the relationship between
CPUE and effort is more nearly exponential than
linear. Both models, however, predict almost
identical yields for the ascending limb of the
yield curve. The major difference in the two
models occurs after theoretical maximum yields
have been exceeded. I chose to limit my analysis
to the linear model. The Atlantic longline fish-
ery, however, has never been under equilibrium

851

FISHERY BULLETIN: VOL. 69, NO. 4

conditions. I adjusted for this by using a method
suggested by Gulland (1961) whereby effort is
an average of the current year's effort {Xi) and
the effort from some number of preceding years
(Xi-i, Xi^2, Xi-i ), depending on the av-
erage number of years a year class is available
to the fishery. I used for North Atlantic alba-
core an average of effort in the current year
and the two preceding years:

X =

Xi + Xi-i + X-

The results (Figure 10) show that in the North
Atlantic there has been only a slight decline in
CPUE over the history of the fishery. When
actual catch and effort data are plotted on the
predicted yield curve, only in 1964 did yield ex-
ceed even 50 '^r of the predicted maximum. It
is likely, therefore, that an analysis using an
equilibrium-yield model for the North Atlantic
albacore longline fishery is not feasible since the
population abundance (as represented by
CPUE) has apparently not declined sufficiently
to effectively describe the dynamics of the stock
in relation to fishing. Consequently, maximum
sustainable yield from the North Atlantic long-
line fishery is not estimable at this time. It
appears, however, that increased fishing will re-
sult in increased yield with no major decline in
CPUE.

SOUTH ATLANTIC

The albacore longline fishery in the South
Atlantic is concentrated in three main areas
(Figure 8). During the late 1950's and early
1960's fishing was excellent in area C and fishing
effort increased rapidly to a peak of about 22
million hooks in 1964. CPUE declined sharply,
however, from a high of 10.0 albacore per hun-
dred hooks, and in recent years has stabilized at
about 2Jy. In 1961 the Japanese fished in area D
for the first time, and this area quickly became
the major producer of albacore in the South
Atlantic. Fishing is excellent almost year round,
and CPUE has remained fairly constant at about
8.0 albacore per hundred hooks over the past 5
years. Area E has recently developed as a good

0 20 40 60 80

FISHING EFFORT (MILLIONS OF HOOKS)

Figure 10. — Linear relation between catch per unit of
effort (CPUE) and effort (upper panel) and theoretical
equilibrium yield curves (lower panel) predicted for the
North Atlantic albacore longline fishery. The effort
figures in the upper panel are means of the current
year's effort and the two preceding year's effort. Effort
figures in the lower panel are actual yearly values.

albacore area although effort is still relatively
low.

I combined catch and effort data from the
Japanese, Chinese, and Korean longline fishery
and plotted CPUE against effort in the same
manner as for the North Atlantic (Figure 11).
The decline in CPUE is more pronounced than
for the North Atlantic. The yield curve indi-
cates a theoretical maximum yield of about
1,100,000 albacore from an effort of about 32
million hooks. This yield was equaled in 1964
and surpassed in 1966 and 1968 with an effort
of about 25 million hooks.

The South Atlantic albacore fishery has under-
gone two rather sei^arate and distinct phases.
The first phase was from 1956 to 1964 when
most fishing effort was in area C. This area
produced excellent catches for several years;
then catch rates declined rapidly. In 1965 the
Japanese increased their fishing in area D in
response to excellent catch rates in this area.

852

BEARDSLEY: POPULATION DYNAMICS OF ATLANTIC ALBACORE

10-

I

8-

/ \

.60

^ 6-

1958

1968

& 4-

» —

— -♦•-
63

"m"65

2-

0-

I

1 1

1

1 1

X
to

4

8 12

16

20 24

{T 2,000-

u-

o

^

1968

9

Q

z

/>

<

to

//l^

2 1,000-

O

''/y^'

s,^^

X

'/bl/

^\

1—

67^

0/

\

X

/?'

«63

\

^

60/,-
5V^61

\

<

\

•^ n-

/i95e

\

u-
c

)

1

10

1 1

20 30

1

40

1 1

50 60

FISHING EFFORT (MILLIONS OF HOOKS)

Figure 11. — Linear relation between catch per unit of
effort (CPUE) and effort (upper panel) and theoretical
equilibrium yield curves (lower panel) predicted for the
South Atlantic albacore longline fishery. The effort fig-
ures in the upper panel are means of the current year's
effort and the two preceding year's effort. Effort figures
in the lower panel are actual yearly values.

When the data are combined from areas C, D,
and E, a decline in CPUE is evident to about
1963 (Figure 11). This decline is primarily in
area C. From 1963 to 1968 a steady increase
in CPUE is evident which represents the de-
crease in effort in area C and the increase in
effort in area D where excellent catches were
being made. It appears from the overall pic-
ture of CPUE versus effort that the albacore
population in the South Atlantic has declined
only slightly in relative abundance as a result
of longline fishing.

This may be misleading. I suggested (Beards-
ley, 1969) that the small albacore in area D
formed the recruitment to the South Atlantic
population. This hypothesis was based on size
differences between the two areas; albacore from
area D were small, often averaging as little as

10 to 12 kg, while those caught in area C usually
averaged 18 to 20 kg or larger. The monthly
distribution of catch rates also indicated seasonal
movement between the two areas.

Eecent size information obtained from alba-
core landed in Puerto Rico and caught in area E
show that small albacore are a large part of the
catch. Recruitment to the South Atlantic pop-
ulation may take place in this area. Koto's sug-
gestion that small albacore move between the
Indian and South Atlantic Oceans lends support
to this hypothesis. The small albacore in area D
may well be transients in the South Atlantic,
and any population analysis would have to treat
them as a separate stock.

Until the problem of stock identification in the
South Atlantic is resolved, any estimates of yield
are to be considered tentative. Consistently high
CPUE values in area D over the past 5 years
suggest that even greater yields are possible from
this area. The pronounced decline in CPUE in
area C demonstrates a significant response of the
population to heavy longline fishing pressure,
and any large increase in fishing effort probably
would not result in a significant increase in yield.

POPULATION ESTIMATES

I obtained the approximate average number
of albacore caught from each age-class in the
Bay of Biscay from 1963 through 1968 in the
following manner.

Each length-frequency sample from the Bay
of Biscay (Figure 2) was separated into age-
groups in the same manner as described earlier.
The number of albacore in each age-group was
then divided by the total number of fish in the
respective sample to obtain the percentage con-
tribution of each age-group to the sample. This
percentage was considered as being representa-
tive of the contribution of that age-group to the
total catch for that year. An average percentage
contribution over the 4 years, 1967-70, was then
calculated for each age-group (Table 2).

I then calculated the total weight of a cohort
of 1000 albacore using weights at age (Figure 5)
and average percentages obtained above (Table
3). The average annual catch from the Bay of

853

FISHERY BULLETIN: VOL. 69, NO. 4

Table 2. — Percentage contribution (in number of fish)
of each age-group in the Bay of Biscay from 1967
through 1970.

Age-group

Year

1967

1968

1969

1970

Mean

00.0
01.9
78.0
16.3
03.8

01.1
05.6
54.9
37.5
00.9

00.0
03.9
74.6
19.5
02.0

00.0
32.5
34.7
24.3
08.5

00.3

no

60.5
24.4
03.8

100.0

Table 3. — Calculated numbers of fish and corresponding
weights for a cohort of 1,000 albacore and estimated aver-
age annual catch in number and by age groups from
1963 through 1968 from the Bay of Biscay. See text
for explanation of procedures.

Age

Cohort

Weight

Estimates for an
average year's cotch

Weight

no.

*5

no.

metric torn

1

3

5.4

21,327

34.1

2

110

363.0

781,999

2.580.6

3

605

3,267.0

4,300,992

23,225.4

4

244

2,196.0

1,734,615

15,611.5

5

38

554.8

270,145

3,944.1

Total

1,000

7,109,078

45,394.7

Biscay from 1963 through 1968 was 45,400 met-
ric tons (data from Food and Agriculture Or-
ganization, 1969). I assumed that the average
percentages obtained for 1967 through 1970 were
also representative of the years 1963 through
1968.

I used proportion to estimate the average an-
nual catch from the Bay of Biscay in number
of fish using the total weight of the cohort, the
number in the cohort, and the average annual
weight of the Bay of Biscay catch. This total
was then separated into age-groups (Table 3)
using the percentages in Table 2.

I used these figures to reconstruct three theo-
retical albacore populations in the North Atlantic
based on total mortality coefficients of 0.50, 0.96
(determined from length frequencies), and 1.40
(Tables 4, 5, and 6). In each case I began the
calculations using the estimated number of 3-
year-old albacore landed. I assumed a natural
mortality coefficient (M) of 0.23 and obtained
the fishing mortality coefficient (F) by subtrac-
tion. I used the number of 3-year-olds landed
(Ls), fishing mortality (F), and total mortality

Table 4. — Theoretical albacore population in the North
Atlantic, ages 1 through 5, based on a total mortality
coefficient (Z) of 0.50 from age 3 through 5. See text
for procedures.

Age

Number
of fish

Total
deaths

Natural
deaths

Fishing

deaths

(surface

only)

thousands
33,372

26,514

20,241

12,276

7,445

thoujandl ol fi'h

0.23 6,858 6,837 21

0.27 6,273 5,491 782

0.50 7,965 3,664 4,301

0.50 4,831 3,096 1,735

0.50 2,930 .. 270

Table 5. — Theoretical albacore population in the North
Atlantic, ages 1 through 5, based on a total mortality
coefficient (Z) of 0.96 from age 3 through 5. See text
for procedures.

Age

Number

Z

Totol

Notural

Fishing
deaths

of fish

deaths

deaths

(surface

only)

thousands

th

usands of fish ■

I

15,578

0 23

3,201

3,180

21

2

12,377

0.30

3,208

2,426

782

3

9,169

0.96

5,659

1,358

4,301

4

3,510

0.96

2,166

431

1,735

5

1,344

0.96

830

270

Table 6. — Theoretical albacore population in the North
■Atlantic, ages 1 through 5, based on a total mortality
coefficient {Z) of 1.40 from age 3 through 5. See text
for procedures.

Fishing

Age

Number

Z

Total

Natural

deaths

of fish

deaths

deaths

(surface

only)

thousands

th

ousands ol

fish

1

11,841

0.23

2,433

2,412

21

2

9,408

0.32

2,577

1,795

782

3

6,831

1.40

5,146

845

4,301

4

1,685

1.40

1,269

1,735

5

416

1.40

313

270

854

BEARDSLEY: POPULATION DYNAMICS OF ATLANTIC ALBACORE

(Z) to determine the number of 3-year olds that
died (Ds):

U X Z
Ds = -^ .

Simple back calculation using the annual mor-
tality rates gave the original number of 3-year-
olds present. I was then able to work forward
and backward from this figure to obtain esti-
mates at other ages.

Adjustments were necessary, however, in or-
der to obtain reasonable estimates. I used much
lower total mortality coefficients for 2-year-olds,
for example, than for 3-year-olds. Two-year-
olds were not fully recruited, and they constitute
only about W;? of the total catch. I also as-
sumed total mortality for 1-year-olds was equal
to natural mortality since very few 1-year-olds
are captured.

Only one of the total mortality coefficients
proved to be completely unreasonable. The esti-
mated number of 4-year-olds present was less
than the estimated annual catch of 4-year-olds
when Z = 1.40, which is obviously an impossible
situation. In estimating the other two popula-
tions, Z = 0.96 appeared to be more reasonable
than Z = 0.50. When the number of 4-year-old
albacore that die of natural causes is obtained
by subtracting the estimated fishing deaths from
the estimated number of total deaths the result
corresponds to an M of 0.20 when Z = 0.96,
which is close to the assumed natural mortality
coefficient of 0.23 (based on Suda's (1966) esti-
mate) estimated for ages 1 through 3. When
Z = 0.50, the number of natural deaths of 4-
year-olds corresponds to an M of 0.32.

If we use the figures in Table 5 and apply a
total mortality coefficient of 0.96 from age 5 to
age 6 and 0.79 (fi'om longline data) from age 6
through age 10, we can reproduce what theoret-
ically occurs in the North Atlantic longline fish-
ery in an average year. Table 7 shows that the
longline fishery should capture about 718,000
albacore, ages 5 through 10, in the North At-
lantic each year. The actual average number
of albacoi-e captured annually from 1963 through
1968 is estimated at 513,000 (data from Wise,
1970). This difference is large, but a relatively

Table 7. — Theoretical yields from ages .5 through 10
based on the population in table 5 with natural mortality
coefficient 0.23, and total mortality coefficient 0.96 from
age 5 to age 6 and 0.79 from age 6 to age 10.

Age

Number
of fish

Told
deaths

Natural
deaths

Fishing
deaths

.

- thousands

0/ Ush

5

1,344

829

199

360 (longline)

6

515

270 (surfoce)

281

82

199

7

234

127

37

90

8

107

58

17

41

9

49

27

8

19

10

22

12

3

9

Total

2,271

718 (longline
only)

small adjustment in the number of recruits at
age 5 would bring the figui'es closer together.
For example, by decreasing the number of re-
cruits to 1,100,000 the potential longline catch
was calculated as 533,000 fish, much closer to the
6-year average of 513,000.

ACKNOWLEDGMENTS

Jean-Claude Dao and Philippe Serene, Centre
National pour I'ExpIoitation des Oceans, France,
supplied length-frequency data from the Bay of
Biscay fishery. John A. Gulland, Food and Agri-
culture Organization, Rome, Italy, and Ralph P.
Silliman, National Marine Fisheries Service,
Seattle, Wash., critically reviewed the manu-
script, and I am grateful for their suggestions.

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1969. Proposed migrations of albacore, Thunnus
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De Jaeger, B.

1963. Synopsis of biological data on bluefin tuna
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1957. Datos sobre le edad y crecimiento de la al-
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1968. Report of the meeting of a group of experts
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1970. An exponential surplus-yield model for op-
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Koto, T.

1969. Studies on the albacore-XIV. Distribution
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1970. Exploratory fishing for tuna off the South
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BEARDSLEY: POPULATION DYNAMICS OF ATLANTIC ALBACORE

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1965. The catch statistic data for the Japanese
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1963. Catch variations in the North Pacific alba-
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1968. The Japanese Atlantic longline fishery, 1964,

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1969. The Japanese Atlantic longline fishery, 1965,
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1970. Studies of age and growth of Atlantic al-
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857

PLANKTON POPULATIONS AND UPWELLING OFF THE COAST

OF PERU, JUNE 1969

John R. Beers,' Merritt R. Stevenson," Richard W. Eppley,'
AND Elaine R. Brooks'

ABSTRACT

Plankton populations associated with upwelling areas and the changes with time of upwelled patches
were studied off the coast of Peru near Supe in June 1969. Two patches, detected by their higher
nutrient levels, greater chlorophyll pigment concentrations, and lower surface temperatures than sur-
rounding waters, were each monitored for several days, during which time they gradually lost their
identity. Actively photosynthesizing phytoplankton crops (doubling time ca. 1.4 days) of predominantly
small monads and other flagellates were found in both patches. The zooplankton populations in the
patch areas were estimated to be consuming no more than about 25% of the daily phytoplankton pro-
duction. Direct determination of physical mechanisms affecting the patches showed a relatively high
level of vertical instabilit.v in Patch 1 which would allow for turbulent mixing and the carrying of phy-
toplankters below the compensation depth. A horizontal divergence was associated with Patch 2 and
would also have the effect of dissipating the patch. Approximate estimates of upwelling suggested ver-
tical velocities of about 2 X 10~~ cm/sec in both patches.

Interest in biological production in Peruvian
coastal waters has been high in recent years.
The prosperous fish-meal industry developed
around the anchovy, Engrmdis ringens, has stim-
ulated numerous investigations by Peruvian sci-
entists of the food chain leading to this commer-
cially valuable fish (see, for example: Guillen
and Izaguirre de Rondan, 1968; Zuta and Guillen,
1970; and various "Informes" of the Instituto del
Mar del Peru). In addition, massive upwelling
and its associated biological activities along the
Peru coast has been of concern to investigators
from other countries and has resulted in several
international cruises which have added to our
knowledge of the pelagic ecology of the area.

The distribution of upwelled water at the
surface is often in somewhat discrete "patches,"
perhaps the result of dynamic physical forces
such as currents and/or eddies acting in the area.
In March-April 1966, Strickland, Eppley, and
Rojas de Mendiola (1969) observed low standing

' Institute of Marine Resources; University of Cal-
ifornia, San Diego; La Jolla, Calif. 92037.

^ Inter-American Tropical Tuna Commission, Scripps
Institution of Oceanography, University of California,
San Diego, La Jolla, Calif. 92037.

Manuscript accepted July 1971.

FISHERY BULLETIN: VOL. 59, NO. 4,

1971.

crops of phytoplankton (chlorophyll a, <2 fig/
liter) in high-nutrient patches (e.g., surface
N0.3-N, 20 fig at./liter or higher). In other
similarly rich water phytoplankton abundance
was high (chlorophyll a, 15 /.ig/liter). Barber
et al. (1971) reported the surface water in an
area of recent upwelling showed a lack of the
"organic conditioning compounds" which may
be needed for phytoplankton growth. However,
in the nutrient-rich but low-chlorophyll patches
examined by Strickland et al. (1969) relatively
high growth rates (ca. 0.8 doubling/day aver-
aged over the euphotic zone) were found for the
phytoplankton. Similar rates (ca. 0.6 doubling/
day) can be calculated from the '^N (nitrate and
ammonium) assimilation studies done in this
area by Dugdale and co-workers (University of
Washington Department of Oceanography,
1970).

A high grazing pressure exerted by the pelagic
animal populations was considered by Strick-
land et al. (1969) as a possible underlying cause
for the low standing crops in the nutrient-rich
patches with active phytoplankton populations.
Ryther et al. (1970) also proposed grazing as
an important mechanism for the reduction of the

859

FISHERY BULLETIN: VOL. 69, NO. 4

phytoplankton stock in a patch of upwelled water
they observed continuously for 5 days in April
1966, south of Callao. Both zooplankton and the
anchovy must be considered as potentially impor-
tant direct grazers of the phytoplankton. Rojas
de Mendiola et al. (1969) found the stomach con-
tents of anchovies collected in February-March
of 1968 in the area of this study (i.e., off Supe)
to be predominantly phytoplankton whereas
those from the south (Tambo de Mora) were
mainly zooplankton remains. At that time
the phytoplankton crop off Supe was princi-
pally diatoms while diatoms were of much
less importance in the phytoplankton popula-
tions off Tambo de Mora. Rojas de Mendiola
et al. (1969) also reported they had some evi-
dence that adult anchovies may prefer phyto-
plankton while animal plankters are the choice
of juveniles (65-70 mm anchoveta).

In May-June of 1969 the Food Chain Research
Group of the Institute of Marine Resources, Uni-
versity of California, in cooperation with the
Instituto del Mar del Peru studied various as-
pects of the physical processes and biological
populations associated with upwelling along the
Peruvian coast during austral fall. This work
was carried out as Leg 7 of the PIQUERO Cruise
of the RV Thomas Washington. A complete
description of these studies is recorded in two
"unpublished" data records on file with the Uni-
versity of California, Institute of Marine Re-
sources (1970,° 1971'). From these studies the
coastal current system along Peru was also de-
scribed (Stevenson, 1971). During PIQUERO
Leg 8 the work was extended north to the
Equator where the zonal circulation was studied
(Stevenson and Taft, 1971). Anchovy studies
(abundance, schooling, stomach contents, etc.)
were carried out by Villanueva, Jordan, and

' University of California, Institute of Marine Re-
sources. 1970. Research on the marine food chain;
progress report, July 1969 - June 1970. Part III. Data
record. Cruise PIQUERO, Leg 7. Section 1. Physical,
chemical and production measurements off the coast of
Peru, 28 May - 22 June, 1969 aboard the RV THOMAS
WASHINGTON. IMR Rep. 70-5. (Unpublished man-
uscript.)

' University of California, Institute of Marine Re-
sources. 1971. Research on the marine food chain;
progress report, July 1970 - June 1971. Part III. Data
record. Cruise PIQUERO, Leg 7. Section 2. The plank-
ton. IMR Rep. 71-10. (Unpublished manuscript.)

Burd (1969) on board the Peruvian research
vessel SNP-1 during the first week of PIQUERO
7 in an area south of Callao.

Since neither Strickland et al. (1969) nor
Ryther et al. (1970) provided quantitative evi-
dence to support the hypothesis that grazing
may be an important means of regulating the
phytoplankton crop in these waters, one purpose
of our present studies was to determine the
abundance of the zooplankton — both micro-
zooplankters (see Beers and Stewart, 1970) and
larger forms — and to relate this to observations
on phytoplankton abundance, growth rates, and
taxonomic composition. In addition, we were
interested in the "disappearance" of the patches
with time. Evidence is examined for a sugges-
tion that patches may dissipate through physical
mechanisms such as horizontal and vertical mix-
ing. The detailed study of physical variables
has provided insight into factors affecting bio-
logical production in the waters off Peru which
would not have been appreciated by the biologist
working independently.

MATERIALS AND METHODS

Studies were conducted between 13 and 22
June 1969, in the approximate area bounded by
lat 10° and 12° S and long 78° and 79° W off
Supe. Extensive "surface" mapping operations
at various times throughout this period with
underway continuous analysis of inoi'ganic nu-
trients, phytoplankton pigment fluorescence, and
temperature allowed for the detection and sur-
veillance of two patches of upwelled water in
this area. Water for the mapping as well as
for other "surface" sampling described below
was taken with a pump fitted into the ship's
hull about 3 m below the sea surface. This unit
delivered 10 to 11 liters/min through plastic
piping. A series of 57 discrete stations were
made during the period of observing the patches
for sampling the microzooplankton and macro-
zooplankton populations, obtaining water for
primary i)roduction measurements and phyto-
plankton enumeration, and for determining
temperature and salinity profiles. These were
taken from various depths in and below the
euphotic zone within and outside of the patches.

860

BEERS ET AL,: PLANKTON AND UPWELLING OFF PERU

Our purpose was to return to the same patch of
water, sampling it on successive days as it
"evolved." In general, the temperature and
fluorescence of the surface water were used to
determine the desired location of sampling after
the navigational capabilities of the ship had been
used to locate the general area.

Physical measurements, i.e., temperature and
salinity, were either by continuous vertical pro-
files generally from the surface to the bottom,
or 500 m, using a STD (Salinity-Temperature-
Depth Measuring System, The Bissett-Berman
Corp. Model 940) "■ or at the surface (3 m) using
a thermo-salinograph (The Bissett-Berman
Corp. Model 6600T). Both systems were elec-
tronically interfaced to a shipboard IBM 1800
computer.

Vertical profiles of cun-ent velocity were made
at Stations 99 and 101 using a Hydro Products,
Model 502, meter having a precision Savonius
rotor to sense current speed and a direction vane
coupled with a magnetic compass. The instru-
ment, lowered on the hydrowire, measured the
currents for 15 min at each of a series of depths
through the upper 200 or 500 m. At each station
the current direction and speed were referenced
to the deepest observation. The lower practical
current threshold is considered to be about 2.5
cm/sec.

Phytoplankton nutrient concentrations (i.e.,
PO4, NO3 + NO2, and SiO:i) in water from the
surface pump or taken by water bottles from
various depths were determined using an Auto-
analyzer and methods described in Strickland
and Parsons (1968). A Turner fluorometer
with a continuous flow-through cell (Lorenzen,
1966) was used for mapping surface phyto-
plankton pigment distribution. Vertical profiles
of extracted chlorophyll and phaeophytin were
done following the procedure of Holm-Hansen
et al. (1965).

Levels of primary production through the
euphotic zone were measured by the radiocar-
bonate uptake method at seven stations (see
Table 3). Stations 59, 68, 77, and 87 were
associated with Patch 1 while Stations 88, 93, and

° The use of trade names is merely to facilitate de-
scriptions; no endorsement is implied.

99 were in the second mass of upwelled water
(Patch 2) followed. Water was collected by
Van Dorn bottles from depths corresponding to
80, 30, 20, 15, 5, and 1.5^; of the surface irra-
diance at each location. These depths were es-
timated from Secchi disc depths. Incubation of
samples in deck incubators cooled by surface
seawater was for 6 (noon to sunset) or 24 hr.

At each site where primary production was
measured, water samples were taken for anal-
ysis by the inverted microscope method of Uter-
mohl (1958) of the phytoplankton species com-
position, numerical abundance, and estimates of
biomass (volume and organic carbon). Gener-
ally aliquots from the several depths sampled at
each site were integrated to provide a composite
sample over the euphotic zone, preserved with
5^; Formalin (pH 8.2 it 0.2), and studied as
described in University of California, Institute
of Marine Resources (1971, see footnote 4) and
Reid, Fuglister, and Jordan (1970).

Unconcentrated samples for study of the cil-
iate populations were taken along with the phy-
toplankton as above. In addition, the ciliates
of the euphotic zone were studied at eight addi-
tional sites where the larger zooplankton abun-
dance was measured and they were also deter-
mined in integrated samples from depth inter-
vals, generally 20 to 30 m sampled at 5-m
intervals, below the photosynthetic compen-
sation point (1.5';r surface irradiance) at 10
stations.

Samples of the microzooplankton populations
concentrated on 35-/u, mesh cloth after excluding
larger material on 202-;tt mesh filters were col-
lected from the surface (3 m) using the intake
in the ship's hull at most stations where biologi-
cal sampling was carried out and during certain
of the mapping operations. These samples pro-
vided material for study of all microzooplankton
groups other than the ciliates, many of which
are too small to be retained by this size mesh.
An unconcentrated pump sample taken for total
ciliates is not considered here as there were in-
dications the pump was damaging the non-lori-
cate forms. Methods of analysis of the total
microzooplankton and ciliate populations includ-
ing conversion from a volume estimate to or-
ganic carbon are given in Beers and Stewart

861

FISHERY BULLETIN: VOL, 69. NO. 4

(1970) and University of California, Institute
of Marine Resources (1971, see footnote 4).

Larger zooplankton abundance was studied at
21 sites including the four stations associated
with Patch 1 but only at one location. Station 93,
where productivity was measured in Patch 2.
Samples were taken by vertical tows from ap-
proximately 100 m to the surface using paired
0.5 m nets having 103 fi mesh. The volume of
water filtered was determined by a flowmeter
mounted in the mouth of one of the nets. At
some stations wire angles of 10° to 25° developed
during the sampling. The numerical abundance
and biomass of all developmental stages of the
copepod Calanus chilensis Brodsky were deter-
mined. An estimate of the biomass of the total
Formalin-preserved net material divided into
fractions of >505 /x and <505 /i was obtained
as dry weight and converted to organic carbon
by multiplying by 0.40. For the discussion the
total material is considered to be zooplankton
although there was undoubtedly a small fraction
of phytoplankton and detritus associated with
the net sample.

RESULTS

UPWELLING PATCHES

Periodic changes in position and configuration
of the two patches as determined from surface
mapping of phytoplankton pigments is shown
in Figures 1 and 2. Patch 1, when detected on
13 June, appeared relatively compact and had
a ma.ximum surface pigment (Chi a and "phaeo-
pigments") concentration of 6 to 8 /xg/liter.
Surrounding waters showed 1 to 2 ;ng/liter. The
patch was bounded on the south and west by a
well-defined front. Surface temperature and sa-
linity within the patch were 19.5° C and 35.15// 1,
respectively, while values reached 21.0° C and
35.25'/, on moving out of the patch. The levels
of temperature and salinity at the surface of
the patch were similar to those found at depths
of 35 to 45 m and 50 m, respectively. Surface
nitrate and silicate concentrations of 16 and 13
/LiM, respectively, were found in the patch, drop-
ping abruptly to about 10 and 7 ^^.u on crossing
the thermal front bordering the patch. A de-

cline of surface pigment and nutrient levels was
observed over the period 13 to 21 June. By
June 17 it was apparent that this patch was dis-
appearing and a more extensive mapping oper-
ation revealed a clearly defined patch. Patch 2,
about 16 miles (25 km) south of Patch I (Fig-
ure 2). Patch 2 surface parameters included:
maximum pigment concentration of 6 /iig liter;
temperature, 19.5° C; salinity, 35.15',, ; nitrate,
10 jaM ; and silicate, 13 /aM. A distinct front
bordered the patch on the west. Somewhat cold-
er water (19.0° C) but with a lower pigment
concentration (~3 /xg/'liter) was on the eastern
side. A transect from east to west across Patch
2 passed through water with temperatures from
19° to 21.5° C. Variations of surface chlorophyll
with temperature for Patch 2 are shown dia-
grammatically in Figure 3. This patch was no
longer recognizable by 21 June. Mapping oper-
ations late in the cruise period revealed the
presence of additional patches in the area but
time did not allow for their study.

WATER MOVEMENT IN AND AROUND
PATCHES

Calculations of dynamic topography suggested
that Patch 1 occurred in a cyclonic eddy of the
Peru Coastal Current (Figure 4). Based on
the displacement of the chlorophyll pigments at
the surface, the patch was being shifted to the
west at about 23 cm/sec. Beneath the surface
the dynamic computations suggested a poleward
flow of about 15 cm sec at 50 m (Table 1, Sta-
tions 54, 59, and 78). Cool surface water of
relatively low salinity (35.15J^f) was found on
the nearshore side of the meander.

The limited data available for calculation of
the dynamic topography around the second patch
(Patch 2) suggested a northward flow of surface
water along the western boundary of the front
(Figure 4). Direct measurements with a cur-
rent meter at Stations 99 and 101 in this patch
showed a flow of 18 cm/sec to the ENE at 10 m,
a stronger southerly flow of 30 cm/sec at 50 m
and little current, i.e., less than 5 cm/sec, below
100 m (Table 2). Beyond the temperature-sa-
linity front on the west of the patch, the velocity
of the water was about 5 cm/sec toward the ENE

862

BEERS ET AL. : PLANKTON AND UPWELLING OFF PERU

nT8

w

PIOUERO 7
Part n

14-15 June
CHLOROPHYLL a
1?- pq/L

x

\

iW

^%'

r

?^ Supe

V^

^STA68

'

1 10* M \

Figure 1. — The time sequence of changes in the config-
uration of Patch 1 as shown by the mapping of the total
chlorophyll a and phaeopigments concentration (^g)
liter) in the surface (i.e., 3 m) waters. In Figures 1
and 2, all chlorophyll pigment values are less than
10 jug/liter and are shown with one figure to the right
of the decimal point. The decimal point is often difficult
to see.

863

FISHERY BULLETIN: VOL. 69, NO. 4

PIQUERO 7
Part I

19 Jung

CHLOROPHYLL 0.

J"S/L

2 3

0^

Figure 2. — The time sequence of changes in the config-
uration of Patch 2 as shown by the mapping of the total
chlorophyll a and phaeopigments concentration {fig/
liter) in the surface (i.e., 3 m) waters.

19 20 21 22

TEMPERATURE °C

Figure 3. — Variation in total chlorophyll a and phaeo-
pigments concentration with temperature noted in an
east to west transect across Patch 2.

at 10 m (Figure 4). At greater depths at this
location flow was generally eastward at velocities
up to 4 cm/sec. A small northerly component
was seen at 50 m. A horizontal divergence was
aijparent between the two stations from the
zonal components of the velocity measured at
10 m.

In addition to indicating the horizontal direc-
tion of water flow, measurements from current
meters can be used to estimate vertical shear
(Table 2). Shear on the west side of Patch 2
was generally low because of fairly uniform flow
toward the east. Maximum vertical shear in-
side the patch and to the east of the front was
up to seven times greater than the maximum
to the west of the patch. The large negative
meridional (north-south) shear in the patch sig-
nified a change from weak northerly flow to
strong southerly flow at 49 m.

864

BEERS ET AL.: PLANKTON AND UPWELLING OFF PERU

Figure 4. — Dynamic topography (in dynamic meters)
of the sea surface referenced to the 300 db surface.
Patch 1 was observed 13-21 June 1969; Patch 2, 18-21
June 1969. Data from a detailed analysis of stations
designated by a square ( H ) are given in Tables 1 and 2.

In order to obtain information on the turbu-
lent activity of the water in the vicinity of each
patch, the Vasaila frequency, N, an indicator of
static instability, and the Richardson number,
Ri (Phillips, 1966), an indicator of dynamic in-
stability, were calculated at various depths for
the three stations in Patch 1 and the two current
meter stations associated with Patch 2 (Table 1
and 2). The Vasaila frequency, based on the
vertical density gradient, is often used as an in-
dication of the vertical stability in a water col-
umn assuming static conditions, i.e., no vertical
shear. Small positive values for N imply the
possibility of weak vertical mixing and negative
values indicate the probable overturn of the
water layer being studied. For the purpose of
comparison it was assumed a Vasaila number
less than 1 X 10"^ see"' signified the start of
static instability. Since the effects of a pos-
sible vertical shear are not considered, this
measure will give an inaccurate estimate of the

likelihood of significant turbulence in the pres-
ence of nonuniform horizontal currents. The
Richardson number, Ri, is generally used to esti-
mate whether turbulent mixing is an important
factor for consideration. A Richardson number
less than 0.25 is considered indicative of dynamic
instability and the development of turbulent
mixing. Owing to a lack of current meter data
for Patch 1 it was necessary to estimate the
shear used for determination of Ri from geo-
strophic currents.

In Patch 1 conditions of static instability are
specifically indicated at a depth of 30 to 50 m
for Station 54 (Table 1). The water columns
at the other two stations associated with this
patch were weakly stable. Dynamic instability
was also indicated between 30 and 50 m at Sta-
tion 54. In addition, the upper 10 m of Station
59 showed dynamic instability. Although static
stability was greater at Station 78 than at the
other two stations, the water column was dy-
namically unstable from the surface to 50 m
because of the larger vertical shear present.

Conditions in Patch 2 (Table 2) contrasted
with those in Patch 1. Vertical shear was gen-
erally much less than in Patch 1. This, how-
ever, may be pai'tly attributable to diflferences
arising between direct measurements of currents
(Patch 2) and estimates of currents based on
the horizontal distribution of mass (Patch 1).
Compared with Patch 1, the water column in
Patch 2 was more stable. The Richardson num-
bers from the west side of the front on Patch 2
are all very high and indicate conditions that
are not favorable for vertical turbulent mixing.
In Patch 2 the meridional component of Ri is
smaller and suggests that, while the water col-
umn is not dynamically unstable in the upper
50 m, turbulent mixing might not subside as
quickly as if the water column was highly strat-
ified.

Direct current measurements to the east and
west of the front (Patch 2) were made to 200 m
and 500 m, respectively. If water motion within
the patch at 200 m, however, was similar to the
measurements at that depth on the west side
of the front, the change in current velocity would
be to increase the velocity in the eastward di-
rection by about 4 cm/sec and thereby increase

865

FISHERY BULLETIN t VOL. 69. NO. *

Table 1. — Vertical shear and stability in Patch 1.

Stations

Depth
(m)

Vdsatid

frequency,

'A'

(10-3 s'ec-l)

Velocity,
(cm sec— 1)

Vertical
shear,

dv

32

(10-s sec-l)

Richardson

number,^

Ri

Station 54

0

-20

10°5I.O' S

2.5

2.0

1.53

78° 13.0- W

10

-22

13 June 1969

20
30
50
75

100

4.0
2.5

4

12.0
8.3

-25

-24
-17

- 8

— 17

3.0
-1.0
-3.5
-3.6

3.6

1.74

6.10

-1.69

10.95

5.34

Station 59

0

18

10°52.5' S

2.5

7.0

0.124

78° 19.6' W

10

12

14 June 1969

20
30
50
75

100

5.0
14.0
14.0
8.1
8.3

10

7
- 6
-28
-24

2.0
3.0
6.0
8.4
-1.6

6.30

21.9
5.08
0.921

27.0

Station 78

0

134

10°54.2' S

11.0

31.0

0.116

73°23.1' W

10

103

16 June 1969

20
30
50
75

100

10.0
9.1

13.0
9.8
8.3

74

37

-23

-40

-27

29.0
37.0
30.0
7.2
-5.2

0.120

0.060

0.205

1.85

2.56

(g3p s^\i/2
— ^ -I ' (Phillips 1966) where s = acceleration af gravity, p = density

of sea woter, c = velocity of sound, and : = distance below sea surface.

2 Velocities in this column represent component velocities in the NW-SE direction and ore based on geostrophic
computotions between the individual stations and the adjacent station to the west.

a The Richardson number, Ri = N''/(—Y (Phillips (1966) where f/ = Vasdiici frequency and ~- = vertical

\ 05 ' at

shear using the component of horizontal velocity, V.

* The argument of the Vasoila equation was negative for this loyer ond signifies static instability.

the difference in zonal (east-west) velocities
across the patch. Water motion in the vicinity
of the patch suggests a divergent front with
greater eastward water motion found on the
nearshore side. The lower surface temperatures
and salinity values, relative to offshore salinity,
are evidence for localized upwelling and such a
mechanism could provide the water needed for
replacement owing to horizontal divergence near
the surface.

The source for the u])welled water in the two
patches we studied a])pears to be a poleward flow
associated with a high-salinity core found at
50 m depth (Stevenson, 1971). Some of the
transport from this Coastal Undercurrent is lost
through upwelling as the water moves down
the coastline. The undercurrent has been traced
southward to lat 15°30' S where it was still
present at 50 m. The salinity in the core, how-
ever, had decreased to about 35.12;,, and the

866

BEERS ET AL.: PLANKTON AND UPWELLING OFF PERU

Table 2. — Vertical shear and stability in Patch 2.

Stations

Depth
(m)

Vdsaild
frequency,

N

(10-3 sec-1

Velocity
{cm sec — '

Verticol

sheor

00-3 sec-i)

Richardson
number^

Station 99

10

17

5

ir20.0' S

12.2

-0.266

7.69

2,100

2.5

78° 14 8' W

49

18

-25

20 June 1969

99

10.9

-1

-4

3.80

-4.20

8.2

6.7

5.2

-O.IOI

-0,404

2,681

168

198

=0

=0

Station 101

10

5

I

11°20.0' S

14.3

1.00

-0.250

205

3,280

78°30.0' W

50

1

2

20 June 1969

99

11.8

4

0

-0.612

0.408

368

829

5.7

0,200

0,000

822

149

3

0

4.6

-0,204

-0,204

514

514

198

4

1

4.2

0.100

0,100

1.950

1,952

298

3

0

4.7

0.150

0.000

995

..

498

=0

!>0

' Component velocities, u and v, are from current meter measurements and are positive to the east and north,
respectively.

2 Ri , Ri = Richardson numbers using the east and north velocity components, respectively.

^ The deepest observations ore used for reference and are shown with zero velocity.

measured velocity of about 15 cm/sec was about
half that seen in this study around lat 11° S.
From the PISCO Cruise of the University of
Washington, April-May 1969, Smith et al.
(1971) were able to estimate upwelling in a
narrow coastal region near lat 15° S. They de-
termined the vertical velocity to average 2 X
10 ~2 cm/sec over the period of the investigation
and estimated it to decrease with increased
distance from shore so as to become zero at 20 km
offshore.

PHYTOPLANKTON DYNAMICS IN THE
PATCHES

Photosynthetic carbon assimilation measure-
ments (Table 3) showed that the phytoplankton
crop was physiologically active in both patches
throughout the periods of observation even
though the patches, as defined by their surface
characteristics, were gradually becoming more
difficult to recognize (see Figure 5). The de-
cline in the abundance of phytoplankters at the

Table 3. — Phytoplankton standing crop as carbon, photosynthetic rate, specific growth rate, chlorophyll a and
carbon/chlorophyll a ratio for plankton patches off Peru, June 1969. (See Table 4 for positions of stations.)

Static

Euphotic
zone
depth

Phytoplankton

standing crop

(g C/m2)

Photosynthetic

rate
(g C/mVday)

Specific growth

rate T/i)
(doublings/day)

Chlorophyll ,
(mg/m2)

Ratio
carborVchl a

(g/9)

59
68
77
87

14 June 1969

15 June 1969

16 June 1969
18 June 1969

IB
28
30
42

2.16
1.39
1.40
1.91

1.19
0.83
1.09
1.01

Value probobty low, judged from the high fi or low C/chI a ratio.

0.64
0.68
0.83
061

S0.3
45.7
39

40.8

42.8
30.4
36
46.7

88

18 June 1969

2

20

2.56

1.26

0.58

46.8

55

93

19 June 1969

2

27

'1.33

1.79

1.23

60.3

22.0

99

20 June 1969

2

30

2.27

1.03

0.54

52.9

42.9

867

FISHERY BULLETIN: VOL. 69. NO. 4

Polch 1

- A

A

-

«

■

O

■

A

A

A

•

A

-

O

O

A

A

~

A

A

■

A

.

O

-

-

I

1

-

Figure 5. — Decline with time in surface nitrate ( A )
and chlorophyll pigments concentration ( © ) in Patch 1.
Solid triangles ( A ) are maximum nitrate values found
by automatic analysis (Autoanalyzer) during under-
way mapping. Open triangles ( A ) are discrete nitrate
samples collected on station. Pigment values are max-
ima of fluorescence found in the mapping area.

surface was compensated for by a deepening of
the euphotic zone such that chlorophyll a, stand-
ing crop as carbon, and photosynthesis showed
little variation (<twofold) when integrated
over the increasing euphotic zone depth. The
specific growth rate, ja, of the crop averaged 0.7
doubling/day over the euphotic zone indicating
it should double in 1.4 days if grazers could be
eliminated. Similar measurements of jx in
March-April 1966 off Peru (Strickland et al..
1969) averaged 0.8 doubling/day for four sta-
tions.

The ratio of phytoplankton carbon/chloro-
phyll ft (Table 8) averaged 40: 1 and was similar
to that reported by Lorenzen (1968), using dif-
ferent methods, for a phytoplankton bloom off
Peru. The ratio of photosynthetic rate (g C/mV
day) to chlorophyll a (g/m=) averaged 28 day"',

about one-half that observed by Lorenzen
(1968).

As the phytoplankton crop decreased the ratio
of phaeopigments to chlorophyll a also declined.

SPECIES COMPOSITION OF THE
PHYTOPLANKTON CROPS

Taxa with volumes less than that of 10 fi
spheres accounted for an average 73 /t (range:
46*:; , Station 68 to 93 ^r , Station .59) of the total
plant carbon. The dominant forms in both
patches were small (2-4 fj. and 5-7 fx) cells, often
flagellates, and probably cryptomonads or chry-
sophytes although positive identification was im-
possible in the Formalin-preserved material.
Diatoms never contributed more than 10 to 12%
(average pennates -)- centrics, 5.2%) of the
carbon content of the crop. Of the diatoms two
species, Coveihmn hystrix and Nitzschia delica-
tissima curva, were the most abundant at all
sites. The Corethron was one of the very few
large taxa that would be retained by phytoplank-
ton nets (35 ju mesh). The "photosynthetic"
ciliate, Mesodinium rnbrtim (Taylor, Black-
bourn, and Blackbourn, 1969) , occurred at all
stations but was relatively more abundant in
Patch 1 where numbers reached 3000 'liter at
Station 68. Dinoflagellates contributed 5 to 21 %
of the total phytoplankton carbon. Unidentified
naked forms of cell size <15 /x (equivalent
sphere) were the most common of the dinoflag-
ellates. Coccolithophorids (e.g., Coccolithus
huxleyi and Syracosphaera quadricomum) were
quite numerous when the patches were disap-
pearing, totaling u]) to 1 1 to 14 fxg C liter or 31 %
(Station 87, Patch 1) and 15% (Station 99,
Patch 2) of the plant carbon.

MICROZOOPLANKTON POPULATIONS

Ciliates dominated the microzooplankton pop-
ulations of the two patches in terms of both num-
bers and biomass. No marked diff"erences in the
;ibundaiice of ciliates were noted between the
patches. Their standing stock was greatest
early in our samijling of each patch (i.e.. Station
59, Patch 1; Station 88, Patch 2) owing to rel-
atively large numbers of nonsheathed oligo-

868

BEERS ET AL,: PLANKTON AND UPWELLING OFF PERU

trichs, and was correlated with the generally
highest chlorophyll a and or phytoplankton or-
ganic carbon level observed. The relatively small
number of samples obtained, however, did not
allow us to determine the variability within the
patch at any given time.

Average ciliate abundance over the euphotic
zone at the 15 stations studied ranged from 2400
to 18,000 liter (average, 6200/liter) (Table 4).
Oligotrichous forms were at least 75 "Tr of the
average numbers. Small (10-20 /x) oligotrichs
without well-developed sheaths, e.g., Lohman-
niella oviformis, were generally in much greater
number than larger sheathed species, e.g., Strom-
bidium conicum. Tintinnid ciliates, of which
AcanfhostomeUa ohtusa, Craterella urceolata,

Codonellopsis contracta, and Epiplocylis brandti
were common, composed an averaged of 1% of
the total numbers. Estimated total ciliate or-
ganic carbon levels (Table 4) ranged from 0.7
to 4.8 /Ag/liter (average, 1.9 /ag/liter) of which
n^f and 78*;^, at least, were accounted for by
the tintinnids and oligotrichs, respectively.

The abundance of ciliates dropped significant-
ly below the euphotic zone. In the approximately
20-m depth interval beneath the compensation
point (10 stations observed. Table 4) ciliate or-
ganic carbon was an average 16% of that in the
upper waters whereas the average chlorophyll
level was still 43% of the average concentration
within the euphotic zone. Ciliate abundance
over the upper 100 m comparable to the water

Table 4. — Ciliate standing stock abundance.

Station

Date

Position

Ciliate

standing

stock numbers,

euphotic zone

(no. /liter)

Ciliate

standing

stock biomoss,

euphotic zone

(M9 C/liter)

Ciliate

standing

stock biomoss,

below (20-m

depth interval)

euphotic zone

iltg C/liter)

>59

M June 1969

10°52.5' S
78° 19 6' W

10,000

3.3

-

177

16 June 1969

10»48.1' S
78° 16.2' W

5,300

2.0

0.27

187

18 June 1969

10°51.2' S
78°20.4' W

3,800

1.9

-

•88

18 June 1969

n°19.5' S
78° 18,6' W

18,000

4.8

0.25

89

18 June 1969

11°19.8' S
78°03.6' W

5,600

1.2

0.16

193

19 June 1969

iri8,8' S
78° 1 1.8' W

2,900

0.9

0.38

94

19 June 1969

11°18.8' S
78° 11.8' W

2,400

0.7

0.38

95

19 June 1969

ir20' S
78°12' W

3,800

1.2

0.52

9«

20 June 1969

11°20' S
78° 12' W

4,300

1.0

0.49

97

20 June 1969

ll°20' S
78° 12' W

4,000

1.3

0.43

199

20 June 1969

11°20' S
78°14.8' W

6,500

2.0

~

100

20 June 1969

11°20' S
78°25' W

11,000

4.0

~

>102

21 June 1969

10°55.0' S
78°24.6' W

3,300

0.9

0.09

103

21 June 1969

10°54.2' S
78° 19.8' W

4,700

0.9

~

104

21 June 1969

10°51.2' S
78° 20.4' W

6,700

2.4

0.31

^ Stations with primary productivity and phytoplankton crop taxonomic composition data.
2 Surface chlorophyll a level <1.5 /ig/liter.

869

FISHERY BULLETIN: VOL. 69. NO. 4

column sampled for the "net" zooplankton was
examined at Station 77. Expressed as a per-
centage of the average ciiiate organic carbon
concentration within the euphotic zone, the ver-
tical distribution was 30 to 50 m, 14%; 55 to
75 m, T'r ; and 80 to 100 m, 6%. Chlorophyll
levels over the same depth intervals were 20%,
8%, and 1% of the euphotic zone average. Cii-
iate organic carbon estimate for the 100-m col-
umn was more than 20 ^,r of that of the total
103-/X net sample.

The numbers of small shelled sarcodinan pro-
tozoa, i.e., Foraminifera and Radiolaria, were
relatively low. Numbers counted in the samples
integrated over the euphotic zone were too small
to provide a good estimate but suggested less
than 10 foraminiferans and radiolarians/liter.
At the surface, the average abundance of Sar-
codina for the 12 stations was low — 5.3 organ-
isms/liter or 0.032 jjig C/liter.

The metazoan microzooplankters, principally
juvenile copepods, were also few in numbers.
Less than one metazoan/liter was found, on the
average, in + 35 sample from the surface. Aver-
age numbers in the unconcentrated samples over
the euphotic zone were higher (up to 40/liter)
but the very few counted puts wide confidence
limits on the figure. The size of the "average"
individual copepod, both naupliar and post-nau-
pliar, was significantly greater than seen pre-
viously (Beers and Stewart, 1970) and this sug-
gests the relative absence, at least at this time
of year, of the smaller species and their devel-
opmental stages compared with nutrient-rich
coastal areas off California.

LARGER ( + 103 /x) ZOOPLANKTON

Standing stock zooplankton at five stations
where productivity was measured (Station 59,
()8, 77, 87, and 93) averaged 2.4 mgC/m' over the
upper 100 m and showed less than a twofold
diff'erence between sites (Table 5). For the
twenty-one 103-/x net samples collected, average
zooplankton organic carbon was calculated to be
4.9 mg/m^. Zooi)Iankters small enough to pass
505 fi mesh were 30% of the total at the "pro-
ductivity" sites and 2b'^r overall. Calamis chil-
ensis (NVI-adults) constituted approximately

Table 5. — The standing stock biomass, as dry weight,
of the 103 fj, net zooplankton samples, 100 m to surface
tows.

Station

Data

+103 li zooplankton

dry weight

{mg/m2)

<505 li >505 li Total

58

13-14 June

1969

228

789 1,017

59

14 June

1969

155

273 428

65

15 June

1969

420

933 1,353

66

15 June

1969

384

886 1,270

67

15 June

1969

142

147 289

63

15 June

1969

254

586 840

70

15 June

1969

594

2,410 3,004

73

15 June

1969

433

1,284 1,717

74

16 June

1969

459

1.740 2,199

75

16 June

1969

249

756 1,005

76

16 June

1969

538

1,030 1,568

77

16 June

1969

275

503 778

85

18 June

1969

399

894 1,295

86

18 June

1969

473

911 1,384

87

18 June

1969

83

351 434

93

19 June

1969

13C

398 528

95

19 June

1969

145

1,169 1,314

97

20 June

1969

106

685 791

25% of total net organic carbon at the produc-
tivity sites. At other stations its estimated
abundance as a percentage of the total ranged
from <4% to more than 100%. It appeared
as though the Calunus population associated with
Patch 1 was staying with the patch and growing
as evidenced by following a cohort of NV and
NVI individuals into CI at Day 3 (June 15)
and CII at Day 6 (June 18) (see University of
California, Institute of Marine Resources, 1971;
footnote 4).

DISCUSSION

Many of the specialized studies of biological
populations and production in Peruvian coastal
waters have been done during the late summer
or early fall months of the southern hemisphere,
i.e., February to April. The relatively large
amount of data available from the Instituto del
Mar del Perii provides seasonal coverage of the
important food chain variables and allows us
to place the conditions we found in this study
during austral late fall-early winter in their pro-
per perspective. The transport of nutrient-rich
water to the surface through upwelling occurs
throughout the year but it is generally most in-
tense in winter (.see Wooster and Reid, 1963;
Zuta and Guillen, 1970). However, biological
production, mainly as evidenced by standing crop

870

BEERS ET AL.: PLANKTON AND UPVVELLING OFF PERU

and stock abundance, and primary production
levels (Guillen and Izaguirre de Rondan, 1968),
appears to be highest during the summer period.
Anchovy abundance near the coast is greatest
during spring and summer, the time of the most
active fishing (Sanchez, 1966).

Strickland et al. (1969) and Ryther et al.
(1970) as well as others have pointed out the
relatively large variation in upwelled patches
at the surface. During the present cruise ex-
tensive majjping both to the north and south
of Callao failed to show the very high pigment
patches (chlorophyll a, >10 jUg/liter) reported
by Strickland et al. (1969) in March-April 1966.
Further, the two patches we followed did not
have the visually brown coloration described by
Strickland et al. (1969) for patches with phyto-
plankton in bloom conditions. The phytoplank-
ton population of high-chloi'ophyll, brown-water
patches has been found to be principally diatoms
whereas the dominant forms in "blue" water
areas were generally small flagellates (coccolith-
ophorids and "monads"). In the regions where
Rojas de Mendiola et al. (1969) reported the
diet of anchovies to be phytoplankton, the crop
was principally diatoms and these were the main
forms, although not necessarily the same species,
recognized in the gut contents of the fish. Even
though the cell size of many of the diatom species
reported from the brown-water patches is small
they are often chain-formers which would pro-
vide a size and/or configuration that could be
more easily retained on the gill rakers of the
anchovy.

The size of most plant cells in the populations
found during the present study is relatively small
compared with the chain-forming diatoms and,
therefore, these may not be efficiently utilized
by the anchovy if they pass through their filter-
ing mouthparts. If this size limitation is im-
portant, then it is plausible to suggest the an-
chovy will prey on larger organisms such as
many of the zooplankters which in turn have
grazed the small algal cells. At the time of year
of this study juvenile anchovies (i.e., peladilla)
of length 65 to 70 mm and of age 4 to 6 months
are generally abundant, having been si)awned
during the spring and early summer months
(see Sanchez, 1966). Rojas de Mendiola

(1959)" and Rojas de Mendiola et al. (1969)
have shown the stomach content of this size class
of fish to be mainly zooplankton and have sug-
gested a preference for this food. It would ap-
pear this could possibly be due to a lack of the
diatoms or other appropriate-sized plant cells.
At such times as this when the diatoms are not
abundant the food chain leading to the anchovy
would necessarily be lengthened by at least one
extra trophic level and therefore "efficiency" of
utilization of primary production in terms of pro-
duction of anchovy carbon would be lessened.
Growth rate (i.e., increase in length) of ancho-
vies during these winter months is less than half
that at other times of the year (Sanchez, 1966).
This may be a reflection of the lower abundance
of their "food" at this time of year and the need
for expending a greater amount of energy to
obtain the same or a lesser amount of food.

While some of the diatoms that have been
reported in bloom proportions at other times of
the year (e.g., Ryther et al., 1970) were present
during this study, the absolute abundance of
diatoms was low and they were a relatively un-
important component of the total phytoplankton
crop. This could be the result of a low rate of
production for these forms or may suggest they
are being kept down by grazing.

Obvious possible limiting variables of the
chemical and physical environment to diatom
production do not seem to be relevant here. Even
though these observations were made at the
winter solstice, light at a location so near the
Equator is probably not limiting to production,
although at the time of this study the near-
coastal region of Peru was often obscured by a
persistent cloud cover. And, in fact, photosyn-
thesis was saturated at an irradiance about 20 %
of that at the surface. Basic nutrient require-
ments of the diatoms should be met with the
levels present. Silicate-Si at four of the five sta-
tions Vi-here productivity was measured was
8 to 10 ixg at. /liter or greater through the
eu])hotic zone. Nitrate + nitrite-N levels were

° Rojas de Mendiola, R. 1959. Breve informe los
habitos alimenticios de la anchoveta (Evgrnvlis ringens
Jennys) en los anos 1954-1958. A report presented to
the Cia. Administradora del Guano, 30 April 1959. (Un-
published manuscript.)

871

FISHERY BULLETIN: VOL. 69, NO. 4

generally in excess of 12 to 15 (lU and PO4-P
above 1 (jlM. It is possible, however, that a nu-
trient requirement of the diatoms may not be met
because of the lack of "conditioning compounds"
or some similar mechanism as postulated by
Barber et al. (1970). Temperature is of doubt-
ful significance as many of the abundant species
in the "blooms" enumerated by Ryther et al.
(1970) and Strickland et al. (1969) might be
expected to grow equally well at both winter and
summer surface temperatures.

Thus, at this time of year the food chain lead-
ing to the anchovy probably consists of an inter-
mediate zooplankton step. Villanueva et al.
(1969) found stomach contents of anchovies
collected 6 to 8 June during this study in an area
off Punta San Juan and San Nicholas to be pri-
marily zooplankton. Since no measure of the
anchovy standing stock was made, it is not pos-
sible to estimate the predation of the anchovy
on the zooplankton, but it is possible with our
data to evaluate the importance of zooplankton
grazing on phytoplankton as a mechanism for
preventing their "blooming." The standing
stock of zooplankton in the Peruvian coastal
waters is generally high (Reid, 1962) although,
as pointed out by Gulland (1970), there is pro-
bably a marked degree of seasonal and geograph-
ical variation in their abundance. Gushing
(1969) noted an inverse correlation marked by a
short lag between anchovy egg numbers and
zooplankton abundance off the Peru coast during
the spawning .season. He implicated the spawn-
ing fish as either the direct or indirect causative
agent for this. In either case it was suggested
that the low zooplankton stocks and hence their
reduced grazing pressure at the end of the
spawning season allows for another cycle of
biological production. Initially this would be of
principally primary production during late sum-
mer-early fall followed by an increase in sec-
ondary production in the fail. The latter would
be available to the juvenile anchovies. While
this is simply speculation at the moment, hope-
fully it will become clearer when more data on
the seasonal variation, including small-scale var-
iations, of plankton populations are tabulated
(see Gulland, 1970).

A striking feature of the zooplankton popula-

tions we observed off Peru was the great ab-
solute and relative abundance of ciliates. The
ciliates may be essential elements for the utili-
zation of the small phytoplankton species pre-
sent, and, if preyed upon in turn by the zooplank-
ton, may represent still an additional trophic
level and lengthening of the "food chain" be-
tween the primary producers and the harvestable
anchovy. The average ciliate organic carbon
level over the euphotic zone was about an order
of magnitude greater than that found for 12
equidistantly spaced stations from lat 10° N to
12° S along long 105° W in the eastern tropical
Pacific (Beers and Stewart, 1971). Ciliate
abundance off Peru was similar to the average
estimated for a site 1 mile off the coast of La
Jolla, Calif., from weekly samples over a 5-month
period in the spring and summer of 1967 (Beers
and Stewart, 1970). However, oflf La Jolla the
tintinnids accounted for almost three-quarters
of the ciliate biomass. Also, just 5 to 6 miles off
the California coast the average ciliate abun-
dance (as organic carbon) over the same period
had decreased to a level about one-quarter of that
recorded for the present set of stations which
were generally between 10 and 20 miles off the
coast.

Despite their prominence in the zooplankton
populations the standing stock of ciliates as or-
ganic carbon in the euphotic zone was an average
of only 3.2 9f of the phytoplankton standing crop
(6 stations with productivity data). The aver-
age daily phytoplankton production over the
euphotic zone at these six sites was 49 mg C/m^.
The ciliate carbon was only approximately 5%
of the new phytoplankton crop being added daily.
An estimate of the fraction of the daily primary
production that might be consumed by the cili-
ates can be made assuming the ciliates require
three times their bodily carbon per day. Lab-
oratory culture studies of pelagic ciliates (un-
published) have suggested that tintinnids may
be dividing every 1 or 2 days and that the doub-
ling time may be even shorter for the oligotrichs
(see also Beers and Stewart, 1970) . Values for
possible ciliate consumption of new phytoplank-
ton production ranged from 5'^i (Station 93)
to 24'; (Station 87), averaging 15^^. Other
microzooplankton consumption would, on the

872

BEERS ET AL,, PLANKTON AND UPWELLING OFF PERU

average, be a very small addition to the total.
If the ciliate populations found off Peru with
their dominance of oligotrichous forms i-eceive
much of their nutritional requirements through
functional chloroplasts in their endoplasm, their
direct consumption of phytoplankton would prob-
ably be lower than assumed. The gymnostome
ciliate, Mesodhuum rubnim, for which good evi-
dence of endocellular chloroplasts exists (Taylor,
Blackbourn, and Blackbourn, 1969) was not in-
cluded in this calculation.

The Cahinus standing stocks at the four sta-
tions associated with Patch 1 (0-100 m) were
estimated to be consuming an average of 22 mg
C m-/day. These estimates were derived using
the data of Mullin and Brooks (1970) on inges-
tion by the various developmental stages of Cal-
anus helgolandicus. The average net primary
production over the euphotic zone at these four
stations was found to be 1035 mg C/m2/day.
Thus the Cakinus population, which was an aver-
age of 21 Vf of the total 103 /x net biomass was
consuming only a little more than 2''/> of the
plant production. Even if the remaining 73%
of the zooplankton population were migrating
to the euphotic zone and consuming phytoplank-
ton at the same rate as Calanus the total con-
sumption estimate would still be less than 10 "Jr
of the daily production. Of course, a significant
number of the zooplankters may not be herbi-
vores and also many are much larger forms than
Calamis and it is probable that their daily in-
gestion as a percentage of their bodily carbon
would be lower than that of Calanus. The zoo-
plankton populations below 100 m which might
migrate vertically to feed have not been con-
sidered here. The majority of tows taken on
this cruise were during daylight hours but no
significantly greater abundance was evident in
the few tows taken during the hours of darkness.
The level of dissolved oxygen at 100 m and below
in Peruvian coastal waters is low (usually
<1 ml/liter). However, Mullin (1966)' found

' Mullin, M. M. 1966. Vertical distribution of zoo-
plankton occurring in the oxygen minimum layer off
Peru. In University of California, Institute of Marine
Resources, Research on the marine food chain, Progress
report, January 1966 - December 1966, p. 359-369. (Un-
published manuscript.)

numerous zooplankton species inhabiting the
o.xygen-poor waters off Peru, and some species
even showed their greatest abundance at these
depths. Nevertheless, in terms of total zoo-
plankton biomass the upper 100 m would probab-
ly be of much greater importance than lower
depths.

In summary, our estimates call for no greater
consumption by the zooplankton than about 25%
of the daily primary production. Coupling this
with the fact there was no indication that the
actively photosynthesizing phytoplankton crop
in either patch was increasing with time but, in
fact, was actually disappearing, indicates some
mechanism other than grazing must be at least
partly responsible. Likewise, the fact that there
was no significant increase in the phaeophytin
level or in the chlorophyll/phaeophytin ratio as
the patch was monitored with time argues
against zooplankton grazing as a principal cause.
Dugdale and Goering (1970) in their study of
biological production in the Peru Current during
a period of high diatom levels indicated grazing
was not the principal source of "loss" of phyto-
plankton and that the combined anchovy and
zooplankton grazing was at a daily level of about
20 "^r of the standing crop. It was further sug-
gested that, of these, the anchovy were a quan-
titatively more important grazer than the zoo-
plankters.

Strickland et al. (1969) suggested three al-
ternate hypotheses to grazing which implicated
physical factors as mechanisms for patch dis-
appearance. In the present study, estimates of
vertical shear and stability indicated that turbu-
lent mixing was occurring in the upper 50 m in
Patch 1.

Although a lack of current measurements lim-
its our ability to accurately determine local mo-
tion within Patch 1, an order of magnitude
estimate for the rate of upwelling in the patch
is possible from a consideration of the size of the
patch and associated biological productivity.
From Figure 4 the patch size was found to be
10 km by 5 km by 50 m, in the east-west, north-
south and vertical dimensions, respectively. The
corresponding volume of the patch is 25 X lO'""
cm^. The patch is assumed to be 50 m thick,
below which a subsurface poleward flow is

873

FISHERY BULLETIN: VOL. 69, NO. 4

present. If the doubling rate for plankton is
1.4 days, then to maintain a constant concen-
tration level requires that the water in the patch
is removed at a rate of 2.1 x 10'° cmVsec. The
southward transport of the undercurrent be-
neath the patch is estimated at 20.2 x 10>° cmV
sec, or about 10 times the flow required for re-
placement of water in the patch. Upwelled water
is required to replace the water being- removed
along the outer boundary of the patch. Since
we assume that most, if not all of the water used
to replace water lost from the patch, passes
through the bottom of the patch at 50 m, the
ascending velocity of water at 50 m is estimated
to be 4.1 X 10~- cm/sec for the patch. This is
probably an upper limit since other processes
also act to reduce the biomass. Unfortunately,
only one sub-euphotic zone sample (30-50 m)
from Patch 1 is available, and it shows a chloro-
phyll level only 20 ^r of the average in the up-
per layer. However, if the ciliate and other
zooplankton populations were grazing this ma-
terial in which no new organic carbon was being
produced, it would only be a relatively short time
before a marked diminution of the chlorophyll
level would be expected. In addition, chlorophyll
levels above and below the compensation depth
may not be a comparable index to phytoplankton
abundance as there is an ai)parent decrease in
chlorophyll level in many jihytoplankters when
kept in the dark for any period of time. Thus,
the plant cell population in the sub-euphotic
waters may be underestimated. The phytoplank-
ton cells near to the compensation depth had a
lower photosynthetic rate, g C/g Chi o/hour
(University of California, Institute of Marine
Resources, 1970, see footnote 3), than those
higher in the water column. Eppley, Holmes,
and Strickland (1967) showed that cells in such
a physiological state sink at a more rapid rate
than faster growing phytoplanktei's. While
sinking or upwelling alone may not result in
moving material out of the euphotic zone and
preventing a "bloom" from developing, this com-
bined with the turbulence may be a significant
contributing factor. Dugdale and Goering
(1970) following a high chlorophyll patch of
water over 5 days, concluded that approximately
85% of the phytoplankton production at that

time v/as being lost through sinking and mixing
processes. At one site examined more closely,
IB'^r of the standing crop was lost daily.

Continued upwelling with the consequent
spreading out and or sinking of the surface
waters is another mechanism which would re-
sult in masking any bloom that might have de-
veloped had the upwelled water mass remained
more localized. This was suggested as a means
of "preventing" blooms in regions of divergences
in the Antarctic (Beklemishev, 1958). Hori-
zontal divergence of Patch 2 with a relatively
greater eastward water motion of the nearshore
side was indicated by our current measurements.
Water on the nearshore side would appear to
"stretch" in the horizontal plane and be supple-
mented by ascending subsurface water. Exam-
ination of the graphic reconstruction of chlor-
ophyll distribution (Figures 1 and 2) suggests
a spreading out of the chlorophyll patches, be-
coming diluted in the surrounding area with
time. Since dynamic vertical mixing is not in-
dicated by the Richardson numbers for Patch 2,
the decrease in chlorophyll may be largely attrib-
uted to the divergence and associated upwelling.
Horizontal mixing, however, is undoubtedly an
important dispersing mechanism in both
Ijatches. A rough estimate of upwelling based
on the horizontal divergence was made by using
the current measurements from Patch 2. Up-
welling in the ])atch is assumed to be confined to
a surface layer 50 m thick, where the vertical
velocity is a maximum at 50 m (the same depth
as the poleward flow of the coastal undercur-
rent). The resulting estimate of vertical veloc-
ity at 50 m is 2.5 x IQ-^ cm/sec and compares
favorably with the upwelling rate computed with
greater accuracy for a nearby coastal zone
(Smith et al., 1971). The surface concentration
of nitrate declined in the patches over time as
did the total chlorophyll pigments concentration
(Patch 1, Figure 5). Nitrate consumption by
the phytoijlankton was calculated, assuming 1 g
nitrate assimilated per 6 g of carbon fixed in
photosynthesis, and the indicated plant consump-
tion was only about one-third of the observed
nitrate decline. This observation again suggests
mixing of water in the patches with surrounding
less rich water.

874

BEERS ET AL.: PLANKTON AND UPWELLING OFF PERU

We are left with a system that is undoubtedly
the result of a combination of interacting factors
— both biological and physical — which can be
sorted out only semiquantitatively. Apparently
a loss equivalent to about 25 Cf of the phytoplank-
ton production may have been due to grazing
by zooplankters. As measured here, diffusive
mixing of the patches with adjacent waters and
sinking of the phytoplankton would account for
considerable additional loss of phytoplankton
material. In addition other avenues of possible
loss such as the direct consumption by the an-
chovies exist but were not evaluated here. That
the relative significance of the different variables
may change on a very small scale in time and
location at this time of year can be suggested.
Such complexity would lead to the variety of
conditions that have been described from the
coast of Peru.

ACKNOWLEDGMENTS

This study was stimulated by the interest and
earlier observations of the late Dr. John D. H.
Strickland and several other colleagues from the
Food Chain Research Group. Plans for the
present cruise were coordinated by Dr. Strick-
land, and he participated in this as Chief Scien-
tist until forced by illness to return home mid-
way during the project. His enthusiasm and
devotion to this and similar field studies of
marine food chains have been of great inspira-
tion to us.

We are grateful to members of the staff of the
Instituto del Mar del Perii and, in particular,
0. Guillen, Dr. Romulo Jordan, and Sra. B. Rojas
de Mendiola, for their interest and aid in making
plans for the cruise.

The work of Mrs. Freda M. H. Reid in the
phytoplankton taxonomic studies and Gene L.
Stewart for some of the microzooplankton
quantitative analyses are appreciatively ac-
knowledged. Nutrient analyses were carried out
by Miss Lucia Solorzano and chlorophyll a anal-
yses by J. B. Jordan aboard ship. Miss Betsy
Fuglister was responsible for the computer pro-
gramming of the data. Computational time pro-
vided by the Scripps Shipboard Computer group
is acknowledged with thanks. Assistance in the

preparation of the calculation of dynamic topog-
raphy was provided by Miss Christine Dall.

These studies were supported under AEC
Contract No. AT(11-1)GEN 10, P.A. 20 and
National Science Foundation (Oceanography
Section) Grant GB 12127.

LITERATURE CITED

Barber, R. T., R. C. Dugdale, J. J. MacIsaac, and
R. L. Smith.

1971. Variations in phytoplankton growth associ-
ated with the source and conditioning of upwelling
water. Invest. Pesq. 35: 171-193.
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1970. Numerical abundance and estimated biomass
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1971. Micro-zooplankton in the plankton communi-
ties of the upper waters of the eastern tropical
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Beklemishev, K. V.

1958. The dependence of the phytoplankton distri-
bution on the hydrological conditions in the Indian
sector of the Antarctic. [In Russian.] Dokl.
Acad. Nauk SSSR 119: 694-697.

Gushing, D. H.

1969. Upwelling and fish production. FAO Fish.
Tech. Pap. 84, 40 p.

Dugdale, R. C, and J. J. Goering.

1970. Nutrient limitation and the path of nitrogen
in Peru Current production. In E. Chin (editor),
A collection of manuscripts on the biological
oceanography of the southeast Pacific Ocean. U.S.
Gov. Print. Off., Wash., D.C.

Eppley, R. W., R. W. Holmes, and J. D. H. Strickland.

1967. Sinking rates of marine phytoplankton mea-
sured with a fluorometer. J. Exp. Mar. Biol.
Ecol. 1: 191-208.

Guillen G., O., and R. Izaguirre de Rondan.

1968. Produccion primaria de las aguas costeras
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Gulland, J. A. (editor).

1970. The fish resources of the oceans. FAO Fish.
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1965. Fluorometric determination of chlorophyll.
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1966. A method for the continuous measurement of
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1968. Carbon/chlorophyll relationships in an up-
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MuLLiN, M. M., AND E. R. Brooks.

1970. Production of the planktonic copepod, Cal-
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ber, 1967, p. 89-103. Bull. Scripps Inst. Oceanogr.
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Phillips, 0. M.

1966. The dynamics of the upper ocean. Univer-
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Reid, F. M. H., E. Fuglister, and J. B. Jordan.

1970. Phytoplankton taxonomy and standing crop.
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Reid, J. L., Jr.

1962. On circulation, phosphate-phosphorus con-
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LORENZEN, and N. CoRWIN.

1970. Production and utilization of organic matter
in the Peru Coastal Current. ANTON BRUUN
Report 4, Southeastern Pacific Biological Ocean-
ographic Program of the National Science Foun-
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Sanchez, J. E.

1966. General aspects of the biology and ecology
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1971. The circulation in an upwelling ecosystem:
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1971. New evidence of the equatorial undercurrent
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Strickland, J. D. H., R. W. Eppley, and B. Rojas de
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1969. Phytoplankton populations, nutrients and
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Strickland, J. D. H., and T. R. Parsons.

1968. A practical handbook of seawater analysis.
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1969. Ultrastructure of the chloroplasts and asso-
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224: 819-821.

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1970. Biological production in upwelling ecosys-
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876

NOTES

OBSERVATIONS ON TWO SPECIES OF

DOLPHIN (Coryphaena) FROM THE

TROPICAL MID-ATLANTIC

Large numbers of adult do\\-A\m, Coryphaena
hippnnis Linnaeus, aggregated at night around
the U.S. Coast and Geodetic Survey Ship Dis-
coverer as it drifted in the tropical mid-Atlantic
Ocean in February 1969 (see Stoner, 1969).
Only juveniles of Coryphaena equlselis Linnae-
us, however, were caught under the night light.
This note presents additional details of colora-
tion and meristic counts of juvenile C. equiselis
and reports on mid-oceanic concentrations of
adult C. hippurus.

The drift track of the RV Discoverer on the
Atlantic Trade Wind Expedition (ATEX)— lat
13M8' N long 39°03' W to lat 09°55' N long 44°
3.5' W, February 5 to 22, 1969 — is shown in Fig-
ure 1 (see also PotthofF, 1969). The surface
temperature of the water during the drift pe-
riod ranged from 25.3° C to 26.8° C and the
water depth from 1,757 fm to 2,753 fm.

Gibbs and Collette (1959) reported that very
small juvenile C. hippurus resembled miniature
feathers with dark and light bars alternating
along their bodies and dorsal and anal fins. Very
small C. equiselis, in contrast, tended to be uni-
formly dark along their sides, sometimes dis-
playing weak bars along their fins. During the
drift, 78 juvenile dolphin were caught by dip net;
all were identified as C. equiselis on the basis of
pigmentation on the caudal and pelvic fins
(Giljbs and Collette, 1959) and vertebral counts
(Collette et al., 1969). In the present sample,
specimens ranging from 25 mm SL to 90 mm SL
all had dark vertical bars on their bodies; the
bars were most pronounced over the anal fin on
the ventral half of the fish (Figure 2). The
smallest C. equiselis juveniles (less than 25 mm
SL) tended to be darker, with less pronounced

50"

-r— I — I — I — I — TTT — I — I — r
45° 40° W 35°

Figure 1. — Drift track of the- RV Discoverer during the
Atlantic Trade Wind Expedition (ATEX). The square
on the insert map represents the area covered by the
map.

' Contribution No. 194, National Marine Fisheries
Service, Tropical Atlantic Biological Laboratory, Miami,
Fla. 33149.

Figure 2. — Coryphaena equiselis, 40 mm SL from the
tropical mid-Atlantic Ocean, caught aboard the RV
Discoverer, 19 February 1969.

bars or no bars on the body, and specimens
larger than 90 mm SL had no bars on their
bodies. A single specimen of 230 mm SL ex-
hibited no juvenile coloration. The caudal fork
margin was dark, as were the pelvic fins; how-
ever, the vertebral count (14 + 19 = 33) was
that of C. equiselis not C. hippurus (Collette
et al., 1969). Sixty-three of the juvenile speci-
mens were cleared and stained to obtain verte-
bral counts (Table 1), leading to their positive
identification as C. equiselis. In counting

877

vertebrae, any vertebra associated with a pair
of pleural ribs was counted as precaudal, any
vertebra lacking pleural ribs was counted as
caudal.

In the cleared and stained juveniles, the modal
group of dorsal-fin elements was 55 to 57 (Table
1), which is more similar to the modal group
of 56 to 60 for Atlantic C. hippurus (Gibbs and
Collette, 1959) and of Pacific C. hippimis (Roth-
schild, 1964) , than to that of C. equiselis (51-55)
which these authors reported. The higher mode
in these specimens of C. equiselis from the trop-
ical mid-Atlantic may be representative of an
oceanic population, diff"erent from that sampled
by Gibbs and Collette (1959) who may have in-
cluded specimens from more than one popula-
tion. On the other hand, I may have counted
elements in the cleared and stained specimens
that were not visible to Gibbs and Collette
(1959) in their untreated specimens.

Counts of the anal-fin elements of the speci-
mens from the tropical mid-Atlantic (Table 1)
were not appreciably different from those re-
ported by Gibbs and Collette ( 1959) . However,
the mode was one fin ray higher than those from
the Pacific reported by Rothschild (1964) . Total
gill raker counts (Table 1) of my specimens
were not appreciably different from those re-

ported by Gibbs and Collette (1959) for young
C. equiselis, but differed from Rothschild's
(1964) total counts on adult specimens by two
or three rakers. My gill raker counts were
made on cleared and stained juvenile specimens
and did not include tooth patches on the epi-
branchial and hypobranchial bones; the gill
raker in the epi-ceratobranchial angle was in-
cluded in the ceratobranchial count. Total
counts tended to decrease as fish size increased,
which led me to believe that the rakers over the
epibranchial and hypobranchial bones are grad-
ually transformed into tooth patches. In spe-
cimens below 30 mm SL, the gill rakers over the
epibranchial and hypobranchial bones were very
small with many minute teeth. In intermediate-
sized specimens (40-60 mm SL) some tooth
patches could be counted over the two bones
along with gill rakers. The epibranchial and
hypobranchial bones of juveniles above 80 mm
SL were all covered with fine teeth; the hypo-
branchial bone had no gill rakers associated with
it, whereas the epibranchial usually had one gill
raker.

Size distribution of juvenile C. equiselis caught
during the drift period is shown in Figure 3.
The mode is from 40 to 44 mm SL. From size

Table 1. — Frequency distribution of some meristic characters of juvenile Coryphaena equiselis from the tropical
mid-Atlantic and data on juvenile and adult C. equiselis from Gibbs and Collette (1959) and Collette et al. (1969).

Fins

dorsal fin rays

Anol fin rays

46 47

48

49

50 51 52 53

54 55 56 57

58 59

60 N

X

23 24 25 26 27 28 29

N

X

Tropical mid-Atlantic

__ -_

_-

—

— ..21

9 15 13 15

6

2

63

55,8 _. 1 6 23 21 12 ..

63

26.6

Gibbs and Collette (1959)

1 —

4

10

15 26 31 40

35 22 9 1

1 195

52.6 5 24 62 86 38 6 1

222

25.7

Vertebrae

Precaudal

Caudal

Total

13

14

19 20 21

33 34

Tropical mid-Atlantic

55

8

8 55 _.

63

Collette et al. (1969)

67

12

12 66 t

78 1

Gill rakers

Tropical mid-Atlantic
SL [mm)

Epibranchial
1 2

Cerot
9

obranchial
10 11

0

Hypobranchia
1

2

Total
11 12 13

14

<30

3

12

1

12 2

.-

11

4.-37

5

30-50

13

19

1

28 3

5

23

4 2 13 13

4

51-80

8

4

1

11

6

6

- 5 4 3

-

>80

3

—

—

I 2

2

1

3

-

878

SIZE -FREQUENCY DISTRIBUTION
C. [QUISIUS

I

N:78

PI n

m,nn.,,nmM

so 90 100 no no

STANDARD LENGTH (mm)

Figure 3. — Size-frequency distribution of Coryphaena
equiselis which were attracted to the night light and
caught in dip net during ATEX aboard the RV Discover-
er, February 1969.

data, I infer that the species spawns in the trop-
ical mid-Atlantic during January and February.

My specimens are presently stored at the Troi)-
ical Atlantic Biological Laboratory, Miami, Fla.

I thank Drs. Bruce B. Collette, Robert H.
Gibbs, Jr., and Robert V. Miller for reviewing
the manuscript, and Grady W. Reinert for pre-
paring the illustrations.

Literature Cited

Collette, B. B., R. H. (iiBBS, Jr., and G. E. Clipper.
1969. Vertebral numbers and identification of the
two species of dolphin (Coryphaena). Copeia
1969: 6.30-6.31.
Gibbs, R. H., Jr., and B. B. Collette.

1959. On the identification, distribution, and biology
of the dolphins, Coryphae^ia hippuriis and C. equi-
selis. Bull. Mar. Sci. Gulf Caribb. 9; 117-152.

POTTHOFF, T.

1969. Searching for tuna. Commer. Fish. Rev.
31(7): 35-37.
Rothschild, B. J.

1964. Observations on dolphins (Coryphaena spp.)
in the central Pacific Ocean. Copeia 1964: 445-
447.
Stoner, R. B.

1969. A dryland sailor tries deep sea cruising.
Ensign 57(11) : 28-33.

Thomas Potthoff

National Marine Fisheries Service
Tropical Atlantic Biological Laboratory
Miami, Fla. 3311,9

RESPIRATORY, BEHAVIORIAL, AND

ENDOCRINE RESPONSES OF A TELEOST

TO A RESTRICTED ENVIRONMENT

It is common practice when measuring fish res-
]3iration or activity to allow a varying length of
time for the fish to become accustomed to the
restrictions imposed by the apparatus and to
allow time for any oxygen debt to be repaid
(Fry, 1957). The following observations indi-
cate that such a procedure may introduce com-
plications in the interpretation of results since
the acclimation process results in changes in res-
piration, behavior, and endocrine activity.

Poecilla reticulata males were placed in
groups of 10 in the 100-ml chamber of a con-
tinuous flow respirometer. Animals were main-
tained at 25° C with a 12-hr daylength and fed
daily at the start of the light period. Measure-
ments of oxygen were made with the wide bore
dropping mercury electrode (Briggs, Dyke, and
Knowles, 1958) or by the micro Winkler method
(Fox and Wingfield, 1938).

A daily cycle of routine respiratory activity
in such an apparatus has already been described
(Sage, 1968). The minimum of oxygen con-
sumption occurs at the end of the dark period
23 hr after the last feed and this rate approx-
imates to the standard metabolic rate. Measure-
ment of this rate at daily intervals indicates a
progressive fall in standard o.xygen consumption
(Table 1). A similar fall in respiratory rate

Table 1. — Effect of number of days in respirometer on
standard rate of o.xygen consumption of a group of 10
fish.

Days

Oxygen uptake mmVg/hr

212
156
126
109

to a base line of approximately 100 mmVg/hr
was observed with four other groups of fish
whereas control animals from large containers

879

maintained a standard respiratory rate of ap-
proximately 200 mmVg/hr.

On removing these fish from the apparatus,
their behavior was seen to be very different from
control animals kept in 30-liter aquaria and sim-
ilar to the previously described behavior of fish
treated with thyroxine (Sage, 1968). Thus all
fish jumped during a 15-min period after trans-
fer from the respirometer to a 50 X 25 cm aquar-
ium with a depth of 2.5 cm of water while only
179r of control animals jumped (Table 2). Sim-
ilarly all fish kept for 7 days in 500-ml contain-
ers and fed ad libitum jumped when transferred
to shallow water. The response was therefore
to the restricted containers and not to the abnor-
mal once-per-day feeding regime imposed in the
respirometer.

Table 2. — Effect of maintenance conditions or thyroxine
on frequency of jumping.

Percenlage jumping
(number of individuals)

4 days in ]00-ml respirometer

100 (30)

7 days in 500-ml container

100 (30)

28 days with thyroxine ( 1 in 2 X 10«)
in 30-liter container {Sage, 1968)

37 (28)

Control fish in 30-liter container

17 (28)

Sections through the proximal pars distalis
showed a degranulation of the TSH cells in the
pituitary glands of both groups of fish that had
been kept in restricted environments. This was
not seen in control animals. Stimulation of the
thyroid gland is thus a probable cause of the
observed changes in behavior and may also ac-
count for the respiratory changes. A fall in
standard respiratory rate has been previously
observed and attributed to progressive starva-
tion (Fry, 1957). This cannot explain the pres-
ent results since all respiratory measurements
were made an equal time after a feed.

The responses reported here were obtained
with container to fish volume ratios of 100 and
500: 1. These are larger than the chambers used
in most fish respiration studies. Thus Geyer and
Mann (1939) suggested a ratio of at least 10:1
for Perca.

The present observations indicate that accli-
mating fish to a restricting apparatus may stim-
ulate the TSH cells and thyroid and produce

changes in behavior and respiration. This may
be particularly confusing where seasonal changes
are being investigated since thyroxine has been
implicated in processes of acclimation (Hoar,

1959) and seasonal changes in fish thyroid ac-
tivity are widespread (Matty, 1960; Swift,

1960) and may be related to seasonal changes
in respiratory rate (Fisher, 1958).

Literature Cited

Bbiggs, R., G. V. Dyke, and G. Knowles.

1958. Use of the wide-bore dropping-mercury elec-
trode for long-period recording of concentrations
of dissolved oxygen. Analyst 83: 304-311.

Fisher, K. C.

1958. An approach to the organ and cellular phy-
siology of adaptation to temperature in fish and
small mammals. In C. L. Prosser (editor). Phys-
iological adaptation, p. 3-49. American Physio-
logical Society, Washington, D.C.

Fox, H. M., AND C. A. WiNGFIELD.

1938. A portable apparatus for the determination
of oxygen dissolved in a small volume of water.
J. Exp. Biol. 15: 437-445.

Fry, F. E. J.

1957. The aquatic respiration of fish. In M. E.
Brown (editor). The physiology of fishes, vol. 1,
p. 1-63. Academic Press, New York.

Geyer, F., and H. Mann.

1939. Beitrage zur Atmung der Fi.sche. IV. Die
Bedeutung der Grosse der Atemkammer fiir den
Sauerstoffverbraueh in fliessendem Wasser. Z.
vgl. Physiol. 27: 443-444.

Hoar, W. S.

1959. Endocrine factors in the ecological adapta-
tion of fishes. In A. Gorbman (editor). Compar-
ative endocrinology, p. 1-23. Wiley, New York.

Matty, A. J.

1960. Thyroid cycles in fish. Symp. Zool. Soc.
London 2: 1-15.

Sage, M.

1968. Respiratory and behavioral responses of
Poecilia to treatment with thyroxine and thiourea.
Gen Comp. Endocrinol. 10: 304-309.
Swift, D. R.

1960. Cyclical activity in the thyroid gland of fish
in relation to environmental changes. Symp.
Zool. Soc. London 2: 17-27.

Martin Sage

University of Texas
Marine Science Institute
Port Aransas, Tex. TS373

880

OCCURRENCE OF THE BARRACUDINA,

Paraleph atlantica KR0YER,

IN THE CENTRAL NORTH PACIFIC OCEAN

The barracudina, Paralepis atlantica Kroyer,
is a bathypelagic fish that has rarely been taken
by fishing gear in the North Pacific Ocean; most
specimens have been recorded from waters off
California in the stomach contents of predators
such as whales, fur seals, and scombroid fishes
(Rofen, 1966; Kajimura, 1969). Kajimura
(1969) extended the known range northward on
the eastern Pacific to the Washington coast (lat
46°35' N, long 124°58' W) with a specimen taken
from the stomach of a northern fur seal, Cal-
lorhimis iirsinus. Maruyama (1958) and Ueno
and Abe (1964) reported on three specimens
taken by gill net and trawl from the western Pa-
cific Ocean near Hokkaido, Japan (between lat
42° and 43° N and near long 144° E).

The specimen reported here extends the known
range of the species northward and to the central
Pacific Ocean (lat 48°00' N, long 165° 00' W).
It was captured on 6 May 1969 in surface waters
of 4.5° C with a gill net fished by the RV George
B. Kelez of the National Marine Fisheries Ser-
vice. Meristic characters for the specimen are
given in Table 1 with ranges for the species as
reported by Rofen (1966).

The specimen was torn in half when it was
removed from the gill net, preventing accurate
measurements; its estimated standard length
was 420 mm. It is deposited in the collection of
fishes (Catalog no. 20569) at the University of
Washington, Seattle.

Table 1. — Meristic characters of the specimen compared
with those given by Rofen (1966).

Meristic
charocters

Specimen

Range for
species

Fin rays
Dorsal
Anal
Pectoral

9

■23
16

9-n

20-26
15-17

Gill rokers
Above angle
Below angle

10
29

7-10
25-31

Vertebrae
Total
Prehaemol

«1
35

60-73
28-38

Literature Cited

Kajimura, H.

1969. Northern range extension for Paralepis at-
lantica (Kreyer) in the eastern North Pacific.
Calif. Fish Game 55: 246-247.
Maruyama, K.

1958. Rare deep-water fishes from ofi" Tohoku and
adjacent regions. III. Record of a rare species
of family Paralepididae. Jap. J. Ichthyol. 7: 67-70.
ROPEN, R. R.

1966. Family Paralepididae, Barracudinas. In
Fishes of the western North Atlantic, p. 205-259.
Mem. Sears Found. Mar. Res. 1, Part 5.
Ueno, T., and K. Abe.

1964. Studies on deep-water fishes from off Hok-
kaido and adjacent regions, IV. Second record
of a southern California species of paralepid fish,
Magniaudis barysoma Harry from off the Pacific
coast of Hokkaido. Bull. Hokkaido Reg. Fish.
Res. Lab. 28: 9-12.

Richard G. Bakkala

National Marine Fisheries Service
Biological Laboratory
Seattle, Wash. 9S102

881

INDEX

Fishery Bulletin, Vol. 69, Nos. 1-4, 1971

Abnormalities, developmental

of laboratory-reared lined sole 537

"Abundance and distribution of young Atlantic
menhaden, Brcvoortia tyrannus, in the White
Oak River estuary. North Carolina," by E.
Peter H. Wilkens and Robert M. Lewis 699

Achirns lineatus — see Lined sole

"Additional data on the spavkfning of the hake,"

by John S. MacGregor 581

"(An) adult bluefin tuna, Thunnus ihynnus,
from a Florida west coast urban waterway,"
by Robert W. Topp and Frank H. Hoff 251

AHLSTROM, ELBERT H., "Kinds and abun-
dance of fish larvae in the eastern tropical Pa-
cific, based on collections made on EASTROPAC I" 3

Alaminos — see Vessels

Alaska

Grace Creek 587

Kvichak River 531

Lake Grace 587

Naknek-Kvichak system 122

Nushagak Bay 748

Albacore

Atlantic

age and growth 846

Bay of Biscay surface fishery 846

longline fishery 847

mortality 849

population dynamics 845

potential yield 850

Pacific, juveniles in South

apparent abundance 824

distribution 824

length composition 823

migration 823

time of spawning 825

Amblyops abbreviata — see Mysids

AMBROSE, MARY E.— see DUBROW et al.

Ammonium

concentrations, eastern tropical Pacific 87

Anchialina typica — see Mysids

ANDERSON, WILLIAM W., and MILTON J.
LINDNER, "Contributions to the biology of the
royal red shrimp, Hymenopenaeiis 7-obustus
Smith" 313

Apogonidae — see Fish larvae

Arabian Sea, sharks 615

Argentinidae — see Fish larvae

Argo — see Vessels

Argopecten gibbus — see Calico scallop

"Artificial ripening of maatjes-cured herring
with the aid of proteolytic enzjTne prepara-
tions," by T. M. Ritskes 647

Astronesthidae — see Fish larvae

Atlantic coast

mysids from U.S 717

Atlantic menhaden

purse-seine fishery, 1940-68

annual catch 765

description 768

effort 768

history 769

variation in abundance 777

young, eff'ect of salinity, temperature, tide,
turbidity, and illumination on abundance and
distribution in White Oak River estuary.
North Carolina 783

Auxis sp. — see Frigate mackerel

BAILEY, JACK E., and DALE R. EVANS,
"The low-temperature threshold for pink salmon
eggs in relation to a proposed hydroelectric in-
stallation"

BAKKALA, RICHARD G., "Occurrence of the
barracudina, Paralepis atlantica Kroyer, in the
central North Pacific Ocean"

587

881

Bairdiella icistia — Gulf croaker

BALSIGER, JAMES W.-
and BALSIGER

-see ROTHSCHILD

BARNETT, HAROLD J., RICHARD W. NEL-
SON, PATRICK J. HUNTER, STEVEN
BAUER, and HERMAN GRONINGER, "Stud-
ies on the use of carbon dioxide dissolved in
refrigerated brine for the preservation of whole
fish"

Barracudina

occurrence, central North Pacific

433

881

Bathylagidae — see Fish larvae

883

Bathymysis renociilata — see Mysids

BAUER, STEVEN— see BARNETT et al.

BEARDSLEY, GRANT L., "Contribution to
the population dynamics of Atlantic albacore
with comments on potential yie'.d" 845

'BEERS, JOHN R., MERRITT R. STEVEN-
SON, RICHARD W. EPPLEY, and ELAINE
R. BROOKS, "Plankton populations and upwell-
ing off the coast of Peru, June 1969" 859

Bigeye tuna

larvae, northwestern Gulf of Guinea and off

Sierra Leone 562

Billfish

albacore in stomachs of, South Pacific 821

skipjack tuna in stomachs of, Pacific 545

Bluefin tuna

adult from Florida west coast urban waterway 251

Boreomysis tridens — see Mysids

Bothidae — see Fish larvae

Bottlenosed dolphin

from St. Vincent Island 305

Bowmaniella porturicensif! — see Mysids

Brachyistius frenatus — see Kelp perch

Bregmacerotidae — See Fish larvae

Brevoortia tyrannus — see Atlantic menhaden

Brine, refrigerated

carbon dioxide dissolved in, for preservation

of whole fish 433

BROOKS, ELAINE R.— see BEERS et a!.

BROWN, NORMAN L.— see DUBROW et al.

Brown shrimp

early developmental stages 223

laboratory-reared 223

BULLIS, HARVEY R., JR.— see ROE et al.

BURNS, BRUCE R.— .see WIGLEY and BURNS

CALDWELL, DAVID K., MELBA C. CALD-
WELL, WARREN F. RATHJEN, and JOHN
R. SULLIVAN, "Cetaceans from the Lesser
Antillean island of St. Vincent" 303

CALDWELL, MELBA C— see CALDWELL et al.

"Calico scallop distribution, abundance, and
yield off eastern Florida, 1967-68," by Richard
B. Roe, Robert Cummins, Jr., and Harvey R.
BuUis, Jr 399

Calico scallop

abundance 403

age and growth 401

distribution 403

mortality 401

off eastern Florida, 1967-68 399

spawning 400

yield 404

California

cleaning symbiosis among inshore fishes 491

Monterey Bay 799

plankton variability off southern 681

Salton Sea fishery for Gulf croaker 158

whales off Point Loma 525

California Current system

copepods as predators on fish larvae 655

DDT residues 443, 627

nannoplankton and netplankton 799

California, southern

variabilit.v of near-surface zooplankton, as

shown by towed-pump sampling 681

Cancer ayiteyinariiis — see Crabs

C. anthonyi — see Crabs

Carangidae — see Fish larvae

Central America

shrimps from 635

"Cetaceans from the Lesser Antillean Island of
St. Vincent," by David K. Caldwell, Melba C.
Caldwell, Warren F. Rathjen, and John R.

Sullivan 303

Cetaceans

Alaska 531

California 525

St. Vincent Island, Lesser Antilles

Feresa attcnuata 307

Globiceiiliala macrorhyncha 308

Grampus /jriseus 305

Megaptera novaeangliae 304

Orcinus orca 309

Phyxrfcr catodon 310

Pseiidnrca vrassidens 308

Stenella 305

Steno hredancnsis 304

Tiirsio])K tridicatus 305

unrecorded but expected species 310

Ziphius cavirostris 310

Chaetognaths

off southern California, variability 681

"Changes In catch and effort in the Atlantic
menhaden purse-seine fishery 1940-68," by Wil-
liam R. Nicholson 765

884

"Characteristics of sea-surface temperature an-
omalies," by L. E. Eber 345

Chauliodontidae — see Fish larvae

"Chemical and nutritional characteristics of fish
protein concentrate processed from heated
whole red hake, Uroplujcls chuss," by David L.
Dubrow and Bruce R. Stillings 141

Chesapeake Bay

menhaden fishery 765

Chlorophyll

concentrations in eastern tropical Pacific 87

Chlorophthalmidae — see Fish larvae

Christmas Island, sea-surface temperatures 181

Chinook salmon

thermal tolerance of juveniles in relation to
supersaturation of nitrogen gas 833

Chum salmon

predation on juveniles by marine isopod 700

preservation 433

"Cleaning symbiosis among California inshore
fishes," by Edmund S. Hobson 491

Cleaning symbiosis

among California inshore fishes 491

Clupea harengus pallasi — see Pacific herring

Clupeidae — see Fish larvae

CLUTTER, ROBERT I., and GAIL H. THEI-
LACKER, "Ecological efiiciency of a pelagic
mysid shrimp; estimates from growth, energy
budget, and mortality studies" 93

John N. Cobb — see Vessels

Coho salmon

predation on juveniles by marine isopod 699

thermal tolerance of juveniles 833

COMPAGNO, LEONARD J. V., and STEW-
ART SPRINGER, "logo, a new genus of car-
charhinid sharks, with a redescription of 7.
omanensis" 615

"Comparison of phytoplankton production be-
tween natural and altered areas in West Bay,
Texas," by Jane Corliss and Lee Trent 829

"Contribution to the population dynamics of At-
lantic albacore with comments on potential
yield," by Grant L. Beardsley 845

"Contributions to the biology of the royal red
shrimp, Hijmoiopciincus robi(stiis Smith, by
William W. Anderson and Milton J. Lindner .... 313

COOK, HARRY L., and M. ALICE MURPHY,
"Early developmental stages of the brown
shrimp, Penaeiis aztecus Ives, reared in the lab-
oratory" 223

Copepods

Labidocera, predators on fish larvae 655

predation by marine, on fish larvae 655

southern California, variabilitv 681

CORLISS, JANE, and LEE TRENT, "Compar-
ison of phytoplankton pi'oduction between na-
tural and altered areas in West Bay, Te.\as" . . . 829

Coryphaena equiselia, C. equisetis — see
Dolphin (fish)

C. hipimrvs — see Dolphin (fi.sh)

Coryphaenidae — see Fish larvae

' COX, JAMES L., "DDT residues in seawater
and particulate matter in the California Cur-
rent system" 443

' , "Uptake, assimilation, and loss

of DDT residues by Eiiphausia pacifica, a eu-
phausiid shrimp 627

Crabs

male, sex pheromone activity of molting hor-
mone, crustecdysone, on Pncliygrnpstis cras-
sipes, Cancer antennarius, and C. anthonyi .... 337

CREAR, DAVID, and IRWIN HAYDOCK,
"Laboratory rearing of the desert pupfish,
Cyprhiodon macidarius" 151

Crustacea — see Copepods; Crabs; Lobster;
Mysids; Shrimp
internal defenses 455

Crustecdysone

sex pheromone activity, on male crabs 337

CUMMINS, ROBERT, JR.— see ROE et al.

CUMMINGS, WILLIAM C, and PAUL O.
THOMPSON, "Gray whales, Eschrichtius ro-
6i(.sf)(.s, avoid the underwater sounds of killer
whales, Orcinns area" 525

Cynoglossidae — see Fish larvae

Cyprhiodon macularius — see Desert pupfish

DAWLEY, EARL M.— see EBEL et al.

"DDT residues in seawater and particulate
matter in the California Current system," by
James L. Cox 443

DDT residues

in seawater and particulate matter in the
California Current system 443

885

DDT residues — cont.

uptake, assimilation, and loss by euphausiid

in California Current system 627

Delaware

menhaden fishery 765

Delphinapterus leucas — see White whale

Desert pupfish

laboratory rearing 151

potential for research 151

spawning methods in laboratory 154

"Developmental abnormalities of the flatfish
Achirus lineatus reared in the laboratory," by
Edward D. Houde 537

Discoverer — see Vessels

Diseases

of Crustacea 458

"Distribution, apparent abundance, and length
composition of juvenile albacore, Thunnus ala-
limga, in the South Pacific Ocean," by Howard
O. Yoshida 821

"Distribution and biology of mysids (Crusta-
cea, Mysidacea) from the Atlantic coast of the
United States in the NMFS Woods Hole collec-
tion," by Roland L. Wigley and Bruce R. Burns . 717

"Distribution of tuna larvae (Pisces, Scombri-
dae) in the northwestern Gulf of Guinea and off
Sierra Leone," by William J. Richards and
David C. Simmons 555

Divergence

off coast of Peru 859

Dolphin (fish)

gill raker apparatus and food selectivity 361

two species from tropical mid-Atlantic 877

DUBROW, DAVID L., NORMAN L. BROWN,
E. L. PARISER, HARRY MILLER, JR., V. D.
SIDWELL, and MARY E. AMBROSE, "Effect
of ice storage on the chemical and nutritive
properties of solvent-extracted whole fish — red
hake, Urophycis chiiss" 145

, and BRUCE R. STILLINGS,

"Chemical and nutritional characteristics of fish
protein concentrate processed from heated
whole red hake, Urophycis chuss" 141

"Early developmental stages of the brown
shrimp, Penaeux aztecus Ives, reared in the lab-
oratory," by Harry L. Cook and M. Alice Murphy 223

"Early life history of skipjack tuna, Katauwon-
us pelamis, in the Pacific Ocean," by Howard
O. Yoshida 545

Eastern tropical Pacific

estimating phytoplankton production 87

fish larvae in 3

yellowfin tuna fishery 569

EASTROPAC

fish larvae from Cruise 1 3

EBEL, WESLEY J., EARL M. DAWLEY, and
BRUCE H. MONK, "Thermal tolerance of ju-
venile Pacific salmon and steelhead trout in
relation to supersaturation of nitrogen gas" .... 833

EBER, L. E., "Characteristics of sea-surface
temperature anomalies" 345

"Ecological efficiency of a pelagic mysid shrimp ;
estimates from growth, energy budget, and mor-
tality studies," by Robert I. Clutter and Gail H.
Theilacker 93

Ectoparasites

of California inshore fishes 505

Eel leptocephali — see Fish larvae

"Effect of dietary fish oil on the fatty acid com-
position and palatability of pig tissues," by
Robert R. Kifer, Preston Smith, Jr., and Edgar
P. Young 281

"Effect of ice storage on the chemical and nutri-
tive properties of solvent-extracted whole fish —
red hake, Urophycis chuss," by David L. Du-
brow, Norman L. Brown, E. R. Pariser, Harry
Miller, Jr., V. D. Sidwell, and Mary E. Ambrose . 145

"Effects of delayed initial feeding on larvae of
the grunion, Leurestties tenuis (Ayres)," by
Robert C. May 411

"Egg loss during incubation from offshore
northern lobsters (Decapoda: Homaridae),"
by Herbert C. Perkins 451

EMILIANI, DENNIS A., "Equipment for hold-
ing and releasing penaeid shrimp during mark-
ing experiments" 247

Engraulidae — see Fish larvae

Engraulis mordax — see Northern anchovy

Enzyme preparations

use of proteolytic in artificial ripening of
maatjes-cured herring 647

EPPLEY, RICHARD W.— see BEERS et al.

"Equipment for holding and releasing penaeid
shrimp during marking experiments," by Den-
nis A. Emiliani 247

Erythrops erythropthalma — see Mysids

886

"Escapement levels and productivity of the Nu-
shagak sockeye salmon run from 1908 to 1966,"
by Ole A. Mathisen 747

Eschrichtius robustus — see Gray whale

"Estimating phytoplankton production from
ammonium and chloropliyll concentrations in
nutrient-poor water of the eastern tropical Pa-
cific Ocean," by William H. Thomas and Robert
W. Owen, Jr 87

Eucopia grimaldii — see Mysids

Engnleus omancnsis Norman

new genus, lago, proposed 615

Eupkausia pacifica — see Euphausiids

Euphausiids

growth rates 81

off Oregon 79

size structure 80

uptake, assimilation, and loss of DDT resi-
dues by Euphat(sia pacifica 627

variability off southern California 681

EVANS, DALE R.— see BAILEY and EVANS

Evermannellidae — see Fish larvae

Exocoetidae — see Fish larvae

False killer whale

from St. Vincent Island 308

FARFANTE— see PEREZ FARFANTE, ISABEL

Feresa attenuata — see Pygmy killer whale

FISH, JAMES F., and JOHN S. VANIA,
"Killer whale, Orcinus orca, sounds repel white
whales, Delphinapterus leucas" 531

Fish larvae

Atlantic menhaden 783

eastern tropical Pacific

Apogonidae 37

Argentinidae 13

Astronesthidae 20

Bathylagidae 13

Bothidae 40

Bregmacerotidae 34

Carangidae 38

Chauliodontidae 20

Chlorophthalmidae 21

Clupeidae 12

Coryphaenidae 38

Cynoglossidae 42

eel leptocephali 33

Engraulidae 13

Evermannellidae 32

Exocoetidae 35

Gempylidae 35

Gonostomatidae 13

Idiacanthidae 21

Istiophoridae 37

Malacoteidae 21

Melamphaidae 34

Melanostomiatidae 21

Myctophidae 22

Nomeidae 38

Paralepididae 31

Pleuronectiformes 40

Scombridae 36

Scopelarchidae 32

Scopelosauridae 33

Sternoptychidae 20

Stomiatidae 21

Synodontidae 21

Tetragonuridae 40

Trichiuridae 35

grunion 411

Gulf of Guinea and off Sierra Leone

bigeye tuna 562

frigate mackerel 564

little tunny 564

skipjack tuna 564

yellowfin tuna 560

laboratory studies of predation by

marine copepods on 655

Fish oil

effect on fatty acid composition

and palatahility of pig tissues 281

masking undesirable flavors in 215

Fish protein concentrate (FPC)

chemical and nutritional qualities of,

processed from red hake 141

protein autolysis rates at various pH's and
temperatures in hake and Pacific herring and

effect on yield in preparation of 241

Fish target strength

review of measurements 703

Flavors

undesirable, masking in fish oil 215

Florida

bluefin tuna from waterway 251

Boca Ciega Bay, turtle grass 273

calico scallops off eastern 399

menhaden fishery 765

royal red shrimp off east 313

Food selectivity

and gill rakers among mackerels, tunas, and

dolphins 361

FOX, WILLIAM W., JR., "Random variability
and parameter estimation from the generalized

production model" 569

887

Free radicals

nature of, in freeze-dried fishery products and

other lipid-protein systems 371

Freeze-dried fishery products

nature of free radicals in, and other lipid-
protein systems 371

FRIEDL, WILLIAM A., "The relative sam-
pling performance of 6- and 10-foot Isaacs-Kidd
midwater trawls" 427

Frigate mackerel

larvae in northwestern Gulf of Guinea and

off Sierra Leone 564

FUSS, CHARLES M., JR.— see KELLY et al.

Gaffkaemia

internal defense mechanisms

involved in, of lobsters 471

Gempylidae — see Fish larvae

Genus, new

lago (carcharhinid shark) 615

Geronimo — see Vessels

"Gill raker apparatus and food selectivity
among mackerels, tunas, and dolphins," by John
J. Magnuson and Jean G. Heitz 361

Gill rakers

and food selectivity among mackerels, tunas,

and dolphins 361

Globicephala macrorhyncha — see Short-finned
pilot whale or blackfish

"Gonad maturation and hormone-induced

spawning of the Gulf croaker, Bairdiella icis-

tia," by Irwin Haydock 157

Gonostomatidae — see Fish larv'ae

Goose-beaked whale or Cuvier's beaked whale

from St. Vincent Island 310

Grace Creek, Alaska 587

Grampus griseus — see Risso's dolphin

Gray grampus — see Risso's dolphin

"Gray whales, Esckrichtius robiistus, avoid the
underwater sounds of killer whales, Orcinus
orca," by William C. Cummings and Paul O.
Thompson 525

Gray whale

avoid underwater sounds of killer whales .... 525

GRONINGER, HERMAN— see BARNETT et al.

Grunion

effects of delayed initial feeding on larvae .... 411

Gulf croaker

gonad maturation 157

hormone-induced spawning 157

Salton Sea fishery for 158

Gulf of Guinea

tuna larvae in 555

Guppy

respiratory, behavioral, and endocrine re-
sponses to a restricted environment 879

Hake — see Pacific hake; Red hake

HALL, JOHN R.— see KELLY et al.

"Harmonic functions for sea-surface tempera-
tures and salinities, Koko Head, Oahu, 1956-69,
and sea-surface temperatures, Christmas Island,
1954-59," by Gunter R. Seckel and Marian Y. Y.
Yong 181

Harmonic functions

for sea-surface temperatures and salinities,
Koko Head, Oahu; temperature, Christmas
Island 181

Hawaii

early life history of skipjack tima 545

Koko Head, Oahu 181

HAYDOCK, IRWIN, "Gonad maturation and
hormone-induced spawning of the Gulf croaker,
Bairdiella icistia" 157

, — see CREAR and HAYDOCK

HEITZ, JEAN G.— see MAGNUSON and HEITZ

Herring — see Pacific herring

Herring, maatjes-cured

artificial ripening with aid of proteolytic en-

z>Tne preparations 647

Heteromysis formosa — see Mysids

HOBSON, EDMUND S., "Cleaning symbiosis

among California inshore fishes" 491

HOFF, FRANK H.— see TOPP and HOFF

Homarus americanus — see Northern lobster

Hormone, molting — see Crustecdysone

HOUDE, EDWARD D., "Developmental abnor-
malities of the flatfish Achirus lineatus reared
in the laboratory" 537

Humpback whale

from St. Vincent Island 304

HUNTER, JOHN R., "Sustained speed of jack
mackerel, Trachurus symmetricus" 267

888

, and JAMES R. ZWEIFEL,

"Swimming speed, tail beat frequency, tail beat
amplitude, and size in jack mackerel, Trachurus
symmetricus, and other fishes" 253

, — see PRITCHARD et al.

HUNTER, PATRICK J.— see BARNETT et al.

Hymenopenaeus robustus — see Royal red shrimp

Hypererythrops caribbaea — see Mysids

"lago, a new genus of carcharhinid sharks, with
a redescription of /. omanensis," by Leonard
J. V. Compagno and Stewart Springer 615

lago

generic description 617

/. omanensis

specific description 619

Ice storage

effect on chemical and nutritive properties of
solvent-extracted whole fish — red hake 145

Idiacanthidae — see Fish larvae

Illumination

effect on distribution of young Atlantic men-
haden 783

"Induced spawning of the northern anchovy,
Engraulis viordax Girard," by Roderick Leong . . 357

"In memoriam — Wilbert McLeod Chapman and

Milner Baily Schaefer," by Philip M. Roedel 1

Inshore fishes

cleaning symbiosis among California 491

ectoparasites on California 505

"Internal defenses of Crustacea: a review,"

by Carl J. Sindermann 455

Internal defenses

mechanisms of, in Crustacea 457

Isaacs-Kidd midwater trawl — see
Midwater trawl

"Isisttus brasiliensis, a squaloid shark, the
probable cause of crater wounds on fishes and
cetaceans," by Everet C. Jones 791

Isopod, marine

predation on juvenile Pacific salmon by spe-
cies of 699

Istiophoridae — see Fish larvae

Jack mackerel

relation between exercise and biochemical
changes in red and white muscle and liver . . . 379
swimming speed and size 253

swimming speed, sustained 267

tail beat amplitude and size 253

tail beat frequency and size 253

JELLINEK, GISELA, and MAURICE E.
STANSBY, "Masking undesirable flavors in
fish oils" 215

JONES, EVERET C, "Isistius brasiliensis, a
squaloid shark, the probable cause of crater
wounds on fishes and cetaceans" 791

David Starr Jordan — see Vessels

Katsmvonus pelamis — see Skipjack tuna

George B. Kelez — see Vessels

Kelletia kelletii (whelk)

trophic interaction between, and sea star
Pisaster giganteus 669

KELLY, JOHN A., JR., CHARLES M. FUSS,
JR., and JOHN R. HALL, "The transplanting
and survival of turtle grass, Thalassia testudin-
um, in Boca Ciega Bay, Florida" 273

Kelp perch

cleaning activity 513

general ecology 496

"(.A) key to the American Pacific shrimps of
the genus Tracliypenaeus (Decapoda, Penaei-
dae) , with the description of a new species,"
by Isabel Perez Farfante 635

KIFER, ROBERT R., PRESTON SMITH, JR.,
and EDGAR P. YOUNG, "Effect of dietary fish
oil on the fatty acid composition and palatability
of pig tissues" 281

"Killer whale, Orcinus orca, sounds repel white
whales, Delphinnpterus leucas," by James F.
Fish and John S. Vania 531

Killer whale

from St. Vincent Island 309

gray whales avoid underwater sounds of 525

underwater sounds repel white whales 531

"Kinds and abundance of fish larvae in the east-
ern tropical Pacific, based on collections made on
EASTROPAC I," by Elbert H. Ahlstrom 3

KITTREDGE, JAMES S., MICHELLE
TERRY, and FRANCIS T. TAKAHASHL "Sex
pheromone activity of the molting hormone,
crustecdysone, on male crabs (Pachygrapsns
crassipes. Cancer antenyinrius, and C. anthonyi)" . 337

Koko Head, Oahu, Hawaii 181

KOURY, BARBARA, JOHN SPINELLI, and
DAVE WIEG, "Protein autolysis rates at var-

889

ious pH's and temperatures in hake, Merhiccius
productas, and Pacific herring, Cliipea liarengtis
pallasi, and their effect on yield of fish protein
concentrate" 241

Kvichak River, Alaska
whales in 531

Labidocera — see Copepods

"Laboratory rearing of the desert pupfish,
Cyprinodon macularius," by David Crear and
Irwin Haydock 151

"Laboratory studies on predation by marine
copepods on fish larvae," by Kurt Lillelund and
Reuben Lasker 655

Lake Grace, Alaska 587

- LARRANCE, JERRY D., "Primary production
in the mid-Subarctic Pacific Region, 1966-68" ... 595

Larvae, fish — see Fish larvae

LASKER, REUBEN— see LILLELUND and
LASKER

, — see PRITCHARD et al.

LEONG, RODERICK, "Induced spawning of

the northern anchovy, Engrauli>; mordax Girard" 357

Lesser Antilles

St. Vincent Island 303

Leuresthes tettuis — see Grunion

LEWIS, ROBERT M.— see WILKENS and LEWIS

LILLELUND, KURT, and REUBEN LASKER,
"Laboratory studies on predation by marine
copepods on fish larvae" 655

Lined sole

developmental abnormalities of laboratory-
reared 537

LINDNER, MILTON J.— see ANDERSON and
LINDNER

"(A) linear-programming solution to salmon
management," by Brian J. Rothschild and James
W. Balsiger 117

Linear programming solution to salmon man-
agement 117

Little tunny

larvae in northwestern Gulf of (iuinea and off

Sierra Leone 564

Lobster — see Northern lobster

Long-snouted or spinner dolphin

from St. Vincent Island 305

LOVE, RICHARD H., "Measurements of fish

target strength : a review" 703

"(The) low-temperature threshold for pink
salmon eggs in relation to a proposed hydroelec-
tric installation," by Jack E. Bailey and Dale
R. Evans 587

MacGREGOR, JOHN S., "Additional data on

the spawning of the hake" 581

Mackerel

gill raker apparatus and food selectivity 361

Mackerel, jack — see Jack mackerel

MAGNUSON, JOHN J., and JEAN G. HEITZ,
"Gill raker apparatus and food selectivity
among mackerels, tunas, and dolphins" 361

MAHNKEN, CONRAD V. W.— see NOVOTNY and
MAHNKEN

Malacoteidae — see Fish larvae

MALONE, THOMAS C, "The relative impor-
tance of nannoplankton and netplankton as pri-
mary producers in the California Current system" 799

"Masking undesirable flavors in fish oils," by

Gisela Jellinek and Maurice E. Stansby 215

MATHLSEN, OLE A., "Escapement levels and
productivity of the Nushagak sockeye salmon
run from 1908 to 1966" 747

MAY, ROBERT C, "Effects of delayed initial
feeding on larvae of the grunion, Leurestlie^
tenids ( Ayres) " 411

"Measurements of fish target strength: a re-
view," by Richard H. Love 703

Megaptera noi'aeaiigliae — see Humpback whale

Melamphaidae — see Fish larvae

Melanostomiatidae — see Fish larvae

Menhaden — see Atlantic menhaden

Menhaden oil

effect on pig tissues 282

Merluccius productus — see Pacific hake

Metamysidopsis elongata — see Mysids

Meterythrops robitsta — see Mysids

Mid-Subarctic Pacific region

primary productivity in 595

Midwater trawl

Isaacs-Kidd, relative sampling performance

of 6- and 10-foot 427

890

MILLER, HARRY, JR.— see DUBROW et al.

Mixing

off coast of Peru 859

MONK, BRUCE H.— see EBEL et al.

Monterey Bay, California

nannoplankton and netplankton in 799

MURPHY, M. ALICE— see COOK and MURPHY

Murre II — see Vessels

Myctophidae — see Fish larvae

Mysidopsis bigelowi — see Mysids

M. furca — see Mysids

Mysids

Atlantic coast

Amblynps abbrei'iata 728

Anchialina typica 722

Bathymysis renoculata 729

Boreomysis tridens 720

Bowmaniella portoricensis 721

Erythrops erythrophthalma 723

Eucopia grimaldii 720

Hypererythrops caribbaea 726

Heteromysis formosa 740

Meterythrops robusta 725

Mysidopsis bigelowi 730

Mysidopsis furca 732

Mysis mixta 733

Mysis stenolepis 735

Neomysis americana 737

Praunus flexuostis 735

Prnmysis atlantica 732

Pseudomma affine 727

Pseudo7nma sp 728

Metamysidopsis elongata

body composition 104

culture methods 94

ecological efficiency 93

energy content 107

fecundity 100

growth and maturation 97

molting 95

oogenesis and incubation 94

reproduction 100

respiration 103

Mysis mixta — see Mysids

M. stenole]>is — see Mysids

Naknek-Kvichak system 122

Nannoplankton

compared with netplankton in California Cur-
rent system 799

"Nature of free radicals in freeze-dried fishery

products and other lipid-protein systems," by
William T. Roubal 371

NELSON, RICHARD W.— see BARNETT et al.

Neomysis americana — see Mysids

Netplankton

compared with nannoplankton in California
Current system 799

New Jersey

menhaden fishery 765

New York

menhaden fishery 765

NICHOLSON, WILLIAM R., "Changes in catch
and effort in the Atlantic menhaden purse-
seine fishery, 1940-68" 765

Nitrogen supersaturation

thermal tolerance of juvenile Pacific salmon

and steelhead trout in relation to 833

Nomeidae — see Fish larvae

North Carolina

menhaden fishery 765

young menhaden 783

North Pacific Ocean

Sea-surface temperature anomalies in 345

Northern anchovy

induced spawning of 357

predation on larvae by copepods 656

Northern lobster

egg loss during incubation from offshore 451

NOVOTNY, ANTHONY J., and CONRAD V. W.
MAHNKEN, "Predation on juvenile Pacific
salmon by a marine isopod Rocinela bclliceps
ptigcttcnsis (Crustacea, Isopoda) 699

"Observations on two species of dolphins from

the tropical mid-Atlantic," by Thomas Potthoff . . 877

"Occurrence of the barracudina, Paralepis at-
lantica Kroyer, in the central North Pacific
Ocean," by Richard G. Bakkala 881

O'CONNELL, CHARLES P., "Variability of
near-surface zooplankton off southern Califor-
nia, as shown by towed-pump sampling" 681

Oncorhynciis gorbuscha — see Pink salmon

O. keta — see Chum salmon

O. kisutch — see Coho salmon

0. iierka — see Red salmon, Sockeye salmon

Orciiius orca — see Killer whale

891

Oregon

euphausiids

79

Oxyjulis califomica — see Seiiorita

OWEN, ROBERT W., JR.— see THOMAS and OWEN

PachygrapsHs C7'assipes — see Crabs

Pacific hake

fecundity 581

protein autolysis rates at various pH's and
temperatures and effect on yield of fish pro-
tein concentrate 241

size at first maturity 583

spawning 581

Pacific herring

protein autolysis rates at various pH's and
temperatures and effect on yield of fish pro-
tein concentrate 241

Paragon — see Vessels
Paralepididae — see Fish larvae
Paralepis atlantica — see Barracudina

Parameter estimation

random variability and, for generalized pro-
duction model 569

PARISER, E. R.— See DUBROW et al.

PEARCY, WILLIAM G.— see SMILES and PEARCY

Penaeus aztecus — see Brown shrimp

PEREZ FARFANTE, ISABEL, "A key to the
American Pacific shrimps of the genus Trachy-
penaeus (Decapoda, Penaeidae), with the de-
scription of a new species" 635

PERKINS, HERBERT C, "Egg loss during
incubation from offshore Northern lobsters
(Decapoda: Homaridae)" 451

Peru

plankton populations and upwelling 859

Phanerodon atripcs — see Sharpnose seaperch

Physeter catodon — see Sperm whale

Phytoplankton

and upwelling oflF coast of Peru 859

estimating production of, from ammonium

and chlorophyll concentrations 87

production in natural and altered areas 829

Pig tissues

effect of dietary fish oil on fatty acid com-
position and palatability of 281

Pink salmon

low-temperature threshold for eggs 587

predation on juveniles by marine isopod 699

Pisaster giganteiis (sea star)

trophic interaction between, and gastropod
Kelletia kelletii 669

Plankton — see Nannoplankton; Netplankton;
Phytoplankton ; Zooplankton

"Plankton populations and upwelling off the
coast of Peru, June 1969," by John R. Beers,
Merritt R. Stevenson, Richard W. Eppley, and
Elaine R. Brooks 859

Pleuronectiformes — see Fish larvae

Poecilia reticulata — see Guppy

POTTHOFF, THOMAS, "Observations on two
species of dolphins from the tropical mid-At-
lantic" 877

Praunus flexuosus — see Mysids

"Predation on juvenile Pacific salmon by a
marine isopod Rocinela belliceps pugettensis
(Crustacea, Isopoda)," by Anthony J. Novotny
and Conrad V. M. Mahnken 699

"Primary production in the mid-Subarctic Pa-
cific Region, 1966-68", by Jerry D. Larrance 595

Primary production

in mid-Subarctic Pacific Region 595

PRITCHARD, AUSTIN W., JOHN R. HUNTER,
and REUBEN LASKER, "The relation between
exercise and biochemical changes in red and
white muscle and liver in the jack mackerel,
Trachurus symmetricus" 379

Proinysis atlantica — see Mysids

"Protein autolysis rates at various pH's and
temperatures in hake, Merluccius jyroductics,
and Pacific herring, Cliipea hareiigus pallasi,
and their effect on yield in the preparation of
fish protein concentrate," by Barbara Koury,
John Spinelli, and Dave Wieg 241

Pseudomma affine — see Mysids

Pscudorca crassidens — see False killer whale

Pygmy killer whale

from St. Vincent Island 307

QU.\ST, JAY C, "Sehastes variegatiis sp. n.
from the northeastern Pacific Ocean (Pisces,
Scorpaeni(lae) " 387

"Random variability and parameter estimation
for the generalized production model," by Wil-
liam W. Fox, Jr 569

Random variability

and parameter estimation for the generalized
production model 569

RATIIJKN, WARREN F.— see CALDWELL et al.

892

Red hake

chemical and nutritional characteristics of

fish protein concentrate from 141

effect of ice storage on chemical and nutritive
properties of solvent-extracted whole fish 145

Red salmon

in Kvichak River, Alaska 531

Red Sea, sharks 615

"(The) relation between exercise and biochem-
ical changes in red and white muscle and liver
in the jack mackerel, Tracluiriis sytnmetricus,"
by Austin W. Pritchard, John R. Hunter, and
Reuben Lasker 379

"(The) relative importance of nannoplankton
and netplankton as primary producers in the
California Current system," by Thomas C. Malone 799

" (The) relative sampling performance of 6- and
10-foot Isaacs-Kidd midwater trawls," by Wil-
liam A. Friedl 427

"Respiratory, behavioral, and endocrine respon-
ses of a teleost to a restricted environment,"
by Martin Sage 879

RICHARDS, WILLIAM J., and DAVID C.
SIMMONS, "Distribution of tuna larvae
(Pisces, Scombridae) in the northwestern Gulf
of Guinea and off Sierra Leone" 555

Risso's dolphin

from St. Vincent Island 305

RITSKES, T. M., "Artificial ripening of maat-
jes-cured herring with the aid of proteolytic
enzyme preparations" 647

Rocinela helliceps jnigettensis

(marine isopod) predation on juvenile Pa-
cific salmon 699

Rockfish

preservation with use of carbon dioxide dis-
solved in refrigerated brine 433

Sebastes variegntus, new species from north-
eastern Pacific Ocean 387

Rockaway — see Vessels

ROE, RICHARD B., ROBERT CUMMINS,
JR., and HARVEY R. BULLIS, JR., "Calico
scallop distribution, abundance, and yield off
eastern Florida, 1967-68" 399

ROEDEL, PHILIP M., "In memoriam— Wil-

bert McLeod Chapman and Milner Baily Schaefer" 1

ROSENTHAL, RICHARD J., "Trophic inter-
action between the .sea star Pisaster giganteits
and the gastropod Kelletiu kelletii" 669

ROTHSCHILD, BRIAN J., and JAMES W.
BALSIGER, "A linear-programming solution
to salmon management" 117

ROUBAL, WILLIAM T., "Nature of free
radicals in freeze-dried fishery products and
other lipid-protein systems" 371

Rough-toothed dolphin

from St. Vincent Island 304

Royal red shrimp

age classes 322

biology 313

habits 317

larval, postlarval, and juvenile stages 318

latitude and depth distributions 319

reproductive systems 316

size and age at recruitment 323

size at maturity 320

spawning 321

SAGE, MARTIN, "Respiratory, behavioral,
and endocrine responses of a teleost to a re-
stricted environment" 879

St. Vincent Island
cetaceans from 303

Salinity
sea-surface

Koko Head, Oahu 181

effect on young Atlantic menhaden 786

Salino gairdneri — see Steelhead trout

Salmon — see Chinook salmon; Chum salmon;
Coho salmon; Pink salmon; Red salmon;
Sockeye salmon

Salmon management

linear-programming solution to 117

Scombridae — see Fish larvae

Scopelarchidae — see Fish larvae

Scopelosauridae — see Fish larvae

Scorpaenidae

Sebnstes variegatiis, sp. n 387

Sea star — see Pisaster giganteus

"Sebastes variegatus, sp. n. from the north-
eastern Pacific Ocean (Pisces, Scorpaenidae),"
by Jay C. Quast 387

Sebastes variegatus, sp. n 387

SECKEL, GUNTER R., and MARIAN Y. Y.
YONG, "Harmonic functions for sea-surface
temperatures and salinities, Koko Head, Oahu,
1956-69, and sea-surface temperatures, Christ-
mas Island, 1954-69" 181

893

Senorita

cleaning activity 497

general ecology 494

"Sex pheromone activity of the molting hor-
mone, crustecdysone, on male crabs (Pnchy-
grapsus crassipes, Cancer antemiarius, and C.
aiithonyi)" by James S. Kittredge, Michelle
Terry, and Francis T. Takahashi 337

Shark

Isistius hrasiliensin, probable cause of crater

wounds on fishes and cetaceans 791

new genus, lago carcharhinid 615

Sharpnose seaperch

cleaning activity 511

general ecology 495

Short-finned pilot whale or blackfish

from St. Vincent Island 308

Shrimp — see Brown shrimp: Royal red shrimp

Shrimp

equipment for holding and releasing penaeid,

during marking experiments 247

key to American Pacific, of genus Trachypenaeus 635

SIDWELL, V. D.— see DUBROW et al.

Sierra Leone

tuna larvae off 555

SIMMONS, DAVID C— see RICHARDS and

SIMMONS

SINDERMANN, CARL L., "Internal defenses

of Crustacea : a review" 455

Size

in relation to swimming speed in jack mack-
erel and other fishes 253

in relation to tail beat amplitude in jack mack-
erel and other fishes 253

in relation to tail beat frequency in jack
mackerel and other fishes 253

"Size structure and growth rate of Euphmisia
pacifica off the Oregon coast," by Michael C.
Smiles, Jr., and William G. Pearcy 79

Skipjack tuna

Atlantic

larvae in northwestern Gulf of Guinea and

off Sierra Leone 564

Pacific

age and growth 549

distribution and abundance 545

early life history 545

time of spawning 552

SMILES, MICHAEL C, JR., and WILLIAM
G. PEARCY, "Size structure and growth rate
of Euphausia pacifica off the Oregon coast" .... 79

SMITH, PRESTON, JR.— see KIFER et al.

Sockeye salmon

escapement levels and productivity of Nusha-

gak run from 1908 to 1966 747

Sole, lined — see Lined sole

South America
shrimps from 635

South Carolina

menhaden fishery 765

South Pacific

distribution, apparent abundance, and length

composition of juvenile albacore 821

early life history of skipjack tuna in 545

Species, new
Sebastes variegatus (Pisces: Scorpaenidae) . . 387
Trachypenaeus fuscina (Decapoda: Penaeidae) 635

Sperm whale

from St. Vincent Island 310

SPINELLI, JOHN— see KOURY et al.

Spotted or bridled dolphin

from St. Vincent Island 305

SPRINGER, STEWART— see COMPAGNO and
SPRINGER

STANSBY, MAURICE E.— see JELLINEK and
STANSBY

Steelhead trout

thermal tolerance of juveniles in relation to
supersaturation of nitrogen gas 833

Stenella — see long-snouted or spinner dolphin;
spotted or bridled dolphin

Steno bredanensis — see Rough-toothed dolphin

Sternoptychidae — see Fish larvae

STEVENSON, MERRITT R.— see BEERS et aL

STILLINGS, BRUCE R.— see DUBROW and
STILLINGS

Stomach contents

juvenile albacore found in billfishes, South

Pacific 821

juvenile skipjack tuna found in billfishes of

Pacific 545

Stomiatoidei — see Fish larvae

"Studies on the use of carbon dioxide dissolved
in refrigerated brine for the preservation of
whole fi.sh," by Harold J. Barnett, Richard W.
Nelson, Patrick J. Hunter, Steven Bauer, and
Herman Groninger 433

894

SULLIVAN, JOHN R.— see CALDWELL, D. et al

".Sustained speed of jack mackerel, Trachtirus
syiinnetricits." by John R. Hunter 267

"Swimming speed, tail beat frequency, tail beat
amplitude, and size in jack mackerel, Trachurus
symmetricus, and other fishes," by John R.
Hunter and James R. Zweifel 253

Swimming speed

and size in jack mackerel and other fishes 253

sustained, of jack mackerel 267

Synodontidae — see Fish larvae

Tail beat amplitude

and size in jack mackerel and other fishes 253

Tail beat frequency

and size in jack mackerel and other fishes . . . 253

TAKAHASHI, FRANCIS T.-see KITTREDGE et al.

Target strength

of fishes: a review of measurements 703

Temperature

effect on distribution of young Atlantic men-
haden 787

effect on uptake of DDT by euphausiid 629

low, threshold for pink salmon eggs 587

sea-surface

anomalies in North Pacific 345

Koko Head, Oahu, 1956-69 181

Christmas Island, 1954-69 181

TERRY, MICHELLE— see KITTREDGE et al.

Tetragonuridae — see Fish larvae

Texas

phytoplankton production. West Bay 829

Thalassia testudinum — see Turtle grass

THEILACKER, GAIL H.— see CLUTTER and
THEILACKER

"Thermal tolerance of juvenile Pacific salmon
and steelhead trout in relation to supersatura-
tion of nitrogen gas," by Wesley J. Ebel, Earl
M. Dawley, and Bruce H. Monk 833

THOMAS, WILLIAM H., and ROBERT W.
OWEN, JR., "Estimating phytoplankton pro-
duction from ammonium and chlorophyll con-
centrations in nutrient-poor water of the eastern
tropical Pacific Ocean" 87

THOMPSON, PAUL 0.— see CUMMINGS and
THOMPSON

Thunnus alaliinga — see Albacore

T. thynnus — see Bluefin tuna

Tide

effect on distribution of young Atlantic men-
haden 788

TOPP, ROBERT W., and FRANK H. HOFF,
"An adult bluefin tuna, Thunnus thynnus, from
a Florida west coast urban waterway" 251

Trncliurus symmetricus — see Jack mackerel

T7'achype7iaeus
key to American Pacific 635

T. fuscina
new species, description 635

"(The) transplanting and survival of turtle
grass, Tlialassia testudinum, in Boca Ciega Bay,
Florida," by John A. Kelly, Jr., Charles M. Fuss,
Jr., and John R. Hall 273

TRENT, LEE— see CORLISS and TRENT

Trichiuridae — see Fish larvae

"Trophic interaction between the sea star
Pisasfer giganteus and the gastropod Kelletia
kelletii," by Richard J. Rosenthal 669

Tuna — see Albacore; Bigeye tuna; Bluefin
tuna; Frigate mackerel; Little tunny;
Skipjack tuna; Yellowfin tuna

gill raker apparatus and food selectivity 361

larvae in northwestern Gulf of Guinea and

off Sierra Leone 555

Turbidity

effect on distribution of young Atlantic men-
haden 786

Tursiops truncatus — see Bottlenosed dolphin

Turtle grass

transplanting and survival in Boca Ciega

Bay, Florida 273

Underwater sounds

of killer whales, Kvichak River, Alaska 531

of killer whales. Point Loma, California 525

"Uptake, assimilation, and loss of DDT residues
by Euphausia pacifica, a euphausiid shrimp,"
by James L. Cox 627

Upwelling

and plankton populations off coast of Peru,

June 1969 859

Urophycis chuss — see Red hake

VANIA, JOHN S.— see FISH and VANIA

895

"Variability of near-surface zooplankton off
southern California, as shown by towed-pump
sampling," by Charles P. O'Connell 681

Vessels

Alaminos °

Argo 3

John N. Cobb 581

Discoverer ° ' '

Geronimo 555

David Starr Jordan 3, 581

George B. Kelez 596, 881

Murre II 387

Paragon 596

Rockaway 3

Virginia

menhaden fishery '^65

West Bay, Texas 829

Whelk — see Kelletia kelletii

White Oak River estuary, North Carolina 783

White whale

repelled by underwater sounds of killer whales . 531

WIEG, DAVE— see KOURY et al.

WIGLEY, ROLAND L., and BRUCE R.
BURNS, "Distribution and biology of mysids
(Crustacea, Mysidacea) from the Atlantic coast
of the United States in the NMFS Woods Hole
collection" 717

WILKENS, E. PETER H., and ROBERT M.
LEWIS, "Abundance and distribution of young

Atlantic menhaden, Brevoortia iyrannus, in the

White Oak River estuary. North Carolina 783

Woods Hole

mysids in NMFS collection at 717

Wounds, crater

squaloid shark probable cause of 791

Yellowfin tuna

eastern tropical Pacific fishery used to illus-
trate random variability and parameter esti-
mation for the generalized production model .
larvae in northwestern Gulf of Guinea and off
Sierra Leone

569
560

YONG, MARIAN Y. Y.— see SECKEL and YONG

YOSHIDA, HOWARD O., "Distribution, ap-
parent abundance, and length composition of
juvenile albacore, Thunnus alalunga, in the
south Pacific Ocean" 821

, "The early life history of skip-
jack tuna, Katsuwonus pelamis, in the Pacific
Ocean"

YOUNG, EDGAR P.— see KIFER et al.

545

Ziphiiis cavirostris — see Goose-beaked whale
or Cuvier's beaked whale

Zooplankton

and upwelling off coast of Peru 859

daylight and night hauls compared 7

variability of near-surface off southern Cal-
ifornia as shown by towed-pump sampling .... 681

ZWEIFEL, JAMES R.— see HUNTER and ZWEIFEL

896

ERRATA

Fishery Bulletin Vol. 69, No. 1

Seckel, Gunter R., and Marian Y. Y. Yong, "Harmonic functions for sea-surface temperatures
and salinities, Koko Head, Oahu, 19.56-69, and sea-surface temperatures, Christmas Island, 1954-69,"
p. 181-214.

1) Page 202, upper left panel, in the drafting process the coordinates on the left side were not
properly lined up with the computer drawn curve for the 19.56 salinity; therefore, 0.25'Xo
should be subtracted from the 19.56 salinity values obtained from the curve. The salinity
curves for all other years are correct, and, of course, the harmonic coefficients for 1965 are
correct.

No. 2

Hunter, John R., and James R. Zweifel, "Swimming speed, tail beat frequency, tail beat ampli-
tude, and size in jack mackerel, Trachnrus symmetricus, and other fishes," p. 253-266.

1) Page 253, Abstract, correct equation to read:

V - F„ = L [K(f'-Fo)]

2) Page 260, i-ight column, correct equation to read:

V Vn

^ " = K(F - Fo)

3) Page 263, Table 6, correct equation to read:

V - V„ = L [K(F~Fo)]

No. 3

Houde, Edward D., "Developmental abnormalities of the flatfish Achinis Uneatiis reared in the
laboratory," p. 537-544.

1) Page 541, Figure 4 was published with the image reversed; the figure should appear:

Fishery Bulletin

U.S. DEPARTMENT OF COMMERCE

National Oceanic and Atmospheric Administta||jgpj^g Biologinal Laboratory
National Marine Fisheries Service u i b s^ a -

MAY 171971

WOODS HOLE, iviASS.

Volume 69
Number 1

Vol. 69, No. 1

January 1971

ROEDEL PHILIP M. In Memoriam-Wilbert McLeod Chapman and Milner Baily Schaefer . 1

AHLSTROM, ELBERT H. Kinds a-d abund-« "^ f^ ^"^^^ '^ '''' ^^^^"^ '''°''"^' 3

Pacific based on collections made on EASTEOi'AO l

smiles'. MICHAEL C, JR., and WILLIAM G. PEARCY. Size structure and growth ^^

rate of Euphausia pacifica off the Oregon coast

THOMAS WILLIAM H., and ROBERT W. OWEN, JR. Estimating phytoplankton
p?orcL from ammonium and chlorophyll concentrations in nutnent-poor water of ^^

the eastern tropical Pacific Ocean

PTTTTTFR ROBERT I and GAIL H. THEILACKER. Ecological efficiency of a pelagic

"^ S fhrimpfesdm^tes'from growth, energy budget, and mortality stud.es 93

ROTHSCHILD, BRIAN J., and JAMES W. BALSIGER. A linear-programming solu- ^^^
tion to salmon management

fhiiss ,..•••■••••**''•*'* •••**•'*'

nilBROW DAVID L NORMAN L. BROWN, E. R. PARISER, HARRY MILLER JR.
V D liDWELL a^d MARY E. AMBROSE. Effect of ice storage on the chemical and

lutStive properties of solvent-extracted whole fish-red hake. Urophyc. ckuss 145

CREAR, DAVID, and IRWIN HAYDOCK. Laboratory rearing of the desert pupfish, ^^^

Cyprinodon maeularius

HAYDOCK, IRWIN. Gonad maturation and hormone-induced spawning of the gulf ^^^

croaker, Bairdiella icistia

^■o-n,.-,?-, r-TiMTTTT? R and MARION Y. Y. YONG. Harmonic functions for sea-surf ace
'^S^^ikZr^naS:{^:^L'!^iS^n..,, Oahu. 1956-69, and sea-surface temperatures, ^^^

Christmas Island, 1954-69

JELLINEK, GISELA, and MAURICE E. STANSBY. Masking undesirable flavors in^ ^^^

fish oils

COOK HARRY L. and M. ALICE MURPHY. Early developmental stages of the brown

shrimp, Petmeus azteccs Ives, reared in the laboratory

KOTTRY BARBARA JOHN SPINELLI, and DAVE WIEG. Protein autolysis rates at

Trl^u's'pH's'tnd^Ceratures in hake ^^r.,c^Z'^^:;ir:^n':^'^^
Clupea harengua pallasi, and their effect on yield in the preparation ot ns p

concentrate

Notes

EMILIANI, DENNIS A. Equipment for holding and releasing penaeid shrimp during ^^^
marking experiments

TOPP, ROBERT W., and FRANK H. HOFF. An adult bluefin tuna, Thunnus thynnus, _^_^
from a Florida west coast urban waterway

223

241

U.S. DEPARTMENT OF COMMERCE

Maurice H. Stans, Secretary
NATIONAL OCEANIC AND ATMOSPHERIC ADMINISTRATION

NATIONAL MARINE FISHERIES SERVICE
Philip M. Roedel, Director

FISHERY BULLETIN

The Fishery Bulletin carries technical reports on investigations in fishery science. The Bulletin of the
United Staites Fish Commission was begun in 1881; it became the Bulletin of the Bureau of Fisheries in 1904
and the Fishery Bulletin of the Fish and Wildlife Service in 1941. Separates were issued as documents through
volume 46; the last document was No. 1103. Beginning with volume 47 in 1931 and continuing through volume
62 in 1963, each separate appeared as a numbered bulletin. A new system began in 1963 with volume 63 in which
papers are bound together in a single issue of the bulletin instead of being issued indi%'idually.

Bulletins are distributed free to libraries, research institutions, State agencies, and scientists. Some Bulle-
tins are for sale by the Superintendent of Documents, U.S. Government Printing Office, Washing^ton, D.C. 20402.

EDITOR

Dr. Reuben Lasker

Scientific Editor, Fishery Bulletin

National Marine Fisheries Service

Fishery-Oceanography Center
La Jolla, California 92037

Editorial Committee

Dr. Elbert H. Ahlstrom
National Marine Fisheries Service

Dr. William H. Bayliff

Inter-American Tropical Tuna Commission

Dr. Daniel M. Cohen

National Marine Fisheries Service

Dr. Howard M. Feder
University of Alaska

Mr. John E. Fitch

California Department of Fish and Game

Dr. Mars'in D. Grosslein
National Marine Fisheries Service

Dr. J. Frank Hebard

National Marine Fisheries Service

Dr. John K. Hunter

National Marine Fisheries Service

Mr. John C. Marr

Food and Agriculture Organization of
the United Nations

Dr. Arthur S. Merrill

National Marine Fisheries Service

Dr. Virgil J. Norton
University of Rhode Island

Mr. Alonzo T. Pruter

National Marine Fisheries Service

Dr. Theodore R. Rice

National Marine Fisheries Service

Dr. Brian J. Rothschild
University of Washington

Dr. Oscar E. Sette

National Marine Fisheries Service

Mr. Maurice E. Stansby
National Marine Fisheries Service

Dr. Maynard A. Steinberg
National Marine Fisheries Service

Dr. Roland L. Wigley

National Marine Fisheries Service

Mlil Wlllll I inHAKY

UH nvv z