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CALffORNlS
FISH™GAME

California Fish and Game is a journal devoted to the conservation and
understanding of fish and wildlife. If its contents are reproduced elsewhere, the
authors and the California Department of Fish and Game would appreciate
being acknowledged.

Subscriptions may be obtained at the rate of $10 per year by placing an order
with the California Department of Fish and Game, 2201 Garden Road, Monte-
rey, CA 93940. Money orders and checks should be made out to California Fish
and Game. Inquiries regarding paid subscriptions should be directed to the
Editor.

Complimentary subscriptions are granted on on exchange basis.

Please direct correspondence to:

Robert N. Lea, Ph.D., Editor-in-Chief
California Fish and Game
2201 Garden Road
Monterey, CA 93940

]

VOLUME 74

APRIL 1988

NUMBER 2

Published Quarterly by

STATE OF CALIFORNIA

THE RESOURCES AGENCY

DEPARTMENT OF FISH AND GAME

—LDA—

STATE OF CALIFORNIA
GEORGE DEUKMEJIAN, Governor

THE RESOURCES AGENCY
GORDON VAN VLECK, Secretary for Resources

FISH AND GAME COMMISSION

ALBERT C. TAUCHER, President
Long Beach

ROBERT A. BRYANT, Vice President E. M. McCRACKEN. JR., Member

Yuba City Carmichael

JOHN A. MURDY III, Member BENJAMIN F. BIAGGINI, Member

Newport Beach San Francisco

HAROLD C. CRIBBS

Executive Secretary

DEPARTMENT OF FISH AND GAME

PETE BONTADELLI, Director

1416 9th Street

Sacramento 95814

CALIFORNIA FISH AND GAME

Editorial Staff

Editorial staff for this issue:

Editor-in-Chief Robert N. Lea, Ph.D.

Marine Resources Peter L. Haaker, Robert N. Lea,

Paul N. Reilly, and John P. Scholl
Inland Fisheries Timothy C. Curtis

CONTENTS

67
Page

An Innovative Technique for Seeding Abalone and Preliminary Results

of Laboratory and Field Trials Thomas B. Ebert

and Earl E. Ebert 68

The Survival and Growth of Transplanted Adult Pink Abalone, Haliotis

corrugata, at Santa Catalina Island Kristine C. Henderson,

David O. Parker, and Peter L. Haaker 82

Records of the Deep-Sea Skates, Raja (Amblyraja) bad/a Carman, 1899
and Bathyraja abyssicola (Gilbert, 1896) in the Eastern North

Pacific, with a New Key to California Skates Ceorge D. Zorzi

and M. Eric Anderson 87

Differences in Yield, Emigration-Timing, Size, and Age Structure
of Juvenile Steelhead from Two Small Western

Washington Streams John J. Loch, Steven A. Leider,

Mark W. Chilcote, Randy Cooper, and

Thom H. Johnson 106

Allozyme Variation in the California Halibut, Paralichthys

californicus Dennis Hedgecock and

Devin M. Bartley 119

BOOK REVIEWS 128

68 CALIFORNIA FISH AND CAME

Calif. Fish and Came 74 {2): 68-8 1 1 988

AN INNOVATIVE TECHNIQUE FOR SEEDING ABALONE
AND PRELIMINARY RESULTS OF LABORATORY AND

FIELD TRIALS'

THOMAS B. EBERT

Ocean Resource Consulting Associates

P.O. Box 3334

Salinas, California 93912

and

EARL E. EBERT^

California Department of Fish and Game

Marine Resources Division

Marine Resources Laboratory

Granite Canyon, Coast Route

Monterey, California 93940

In recent years the California abalone fishery has undergone a severe decline.
However, present technology provides an opportunity to test rehabilitation and
enhancement techniques for this valuable fishery resource. Because the biology and
technology for producing and cultivating abalone is well developed, sufficient
quantities of juvenile abalone are available for seeding programs. Previous efforts to
rehabilitate once productive abalone fishing grounds have failed, met with limited
success, or have been of questionable value. These enhancement efforts were
conducted by divers who generally hand-planted the abalone in assumed optimal
habitat areas. This method is not only unwieldly and labor intensive; but the planted
abalone are generally stressed, and often are highly vulnerable to predators. In an
effort to rectify this problem a new abalone planting method has been designed,
tested and appears promising. This method employs a "seeding module" which is
designed to serve as an intermediate habitat for the abalone, and retains them for
a predetermined acclimation time prior to their release and dispersal. Evaluation of
this technique indicates that site selection and abalone size are critically important
factors. However, if the appropriate criteria are met then high abalone survivorship
and an enhanced fishery resource could result.

INTRODUCTION

The red abalone, Haliotis rufescens, ranges from central Baja California to
southern Oregon (Cox 1962) and is extensively sought by sport and commer-
cial fishermen. Commercial landings of red abalone have exhibited a steady
decline in recent years. In 1967 nearly 1,228,000 kg of red abalone were landed,
however, by 1986 the catch had dwindled to 120,000 kg (Calif. Dept. of Fish
and Game, landing receipts). Historically, during the peak production years, the
major commercial fishing grounds for red abalone were located along the
central California coast from Monterey to Point San Luis. Morro Bay repre-
sented the center of the fishery and the majority of the catch, exceeding
450,000 kg annually, was landed there (Cox 1962, Miller 1974, Surge and
Schultz 1 973 ) . This fishery persisted through the 1 960's and into the early 1 970's
(Miller 1974, Burge, Schultz, and Odemar 1975). The demise of the central
California fishery was due to the sea otter, a major predator of abalone (Ebert

' Accepted for publication November 1987.

^ Present address: California Department of Fish and Game, Marine Resources Division, 2201 Garden Road,
Monterey, California 93940.

INNOVATIVE TECHNIQUE FOR SEEDING ABALONE 59

1968a, b, Burge and Schultz 1973, Miller 1974, Burge et al. 1975). Presently, no
red abalone are taken commercially from the central California coast, nor are
any landed at Morro Bay.

Red abalone populations have declined elsewhere in California principally
due to human-related factors such as over-exploitation and habitat degradation
(Burge et al. 1975, Tegner et al. 1981, Hardy, Wendell, and DeMartini 1982). A
limited entry commercial abalone fishery and further restrictions on the sport
fishery were instituted in 1976 (Hardy et al. 1982, Schultz 1984).

To augment this valuable but declining resource the California Department of
Fish and Game (CDFG), university scientists, and commercial abalone fisher-
men have conducted various enhancement projects (Cox 1962, Ebert and Houk
1984, Tegner and Butler 1985). Enhancement efforts included the seeding of
small sized hatchery-reared abalone or of transplanting mature adult stocks.
Unfortunately, although relatively large numbers of abalones have been seeded
or transplanted in California, on an experimental basis, their survivorship, and
ultimate contribution to the resource has been difficult to assess (Tegner and
Butler 1985). Therefore, abalone seeding and transplanting as a means to
enhance the resource remains questionable from a biological standpoint.

In general, previous efforts to seed small abalone for population enhance-
ment, in California, were conducted by divers who hand-planted the abalone
into rocky crevices or artificial habitats (e.g. concrete blocks). More recently,
to reduce handling stress seed abalone were put on adult shells (i.e. abalone,
oyster, scallop) and hand-planted. These methods were not only unwieldy and
labor intensive but the abalone may have been stressed by handling, and as a
consequence, more vulnerable to predation before acclimating to their new
environment. These factors served as an impetus for us to develop a more
efficient approach to seed small sized abalone. Herein we describe an
innovative, expedient method to transport and seed relatively large numbers of
small abalone that can acclimate in an intermediate habitat (seeding module),
free from predation, preparatory to dispersal into the natural environment.
Abalone dispersal rates and movement patterns from the seeding module, and
short-term behavior and survivorship are also described for laboratory tests and
a field trial.

METHODS AND MATERIALS

Abalone Seeding Module Design and Operations

The seeding module consists of a concrete utility box, commercially
available, that is commonly used in water and gas meter applications. The utility
box dimensions are 70 X 46 X 30 cm high (Figure 1). It was modified by
adding a 5 cm thick concrete base, and by cutting-out a 5 X 22 cm section at
each end to provide abalone egress. A PVC casement was fitted around both of
these passageways using 0.6 cm thick PVC 90° angle stock that was glued
directly to the concrete. These passageways were partitioned into four
openings, each measuring 5 X 4 cm high, using 0.6 cm thick PVC strips. These
partitions serve to restrict large predators from entering the seeding module, yet
allow egress of abalones up to 6 cm in length.

CALIFORNIA FISH AND CAME

■* BUOYS ► '<C?p>l

MAGNESIUM
LINK

LATEX

'tubing

10 CM

FICURE 1. The abalone seeding module with cut-away section showing the temporary door
interior with Astroturf, and the magnesium link attachment.

Temporary doors were fitted in both passageways using 0.6 cm thick
perforated PVC plastic sheeting and were 30 X 8 cm high. Astroturf was
cemented to the door interiors to inhibit abalone attachment. Thereby the
abalone could not impede water circulation by covering the door perforations,
nor could they block the doors from opening by adhering to the door jambs.

Both doors were held in place under tension (~ 60 newtons), with two 20
cm lengths of latex rubber tubing. This was done by fastening one end of each
tubing length to opposite doors, then pulling the "free" ends of the tubing
lengths together, and innerconnecting them with a magnesium link. Plastic cable
ties were used to fasten the tubing ends to the doors and the magnesium link.
The dissolution rate of magnesium in seawater is a function of temperature and
salinity. Foreknowledge of these two parameters enabled us to select a proper
sized link. Dissolution of the magnesium link in seawater ultimately releases the
doors. A buoy was attached to each door exterior via a 0.6 cm diameter nylon
line 0.5 m long. Between the buoy and door the nylon cord passes through a
nylon lifting loop that is attached to the lid (1 lifting loop/buoy). When the
doors are released they float up, away from the module passageway, and are
retained by the lifting loops (Figure 1 ). The temporary doors are installed just
before the abalone are introduced to the seeding module.

Abalone Collector-Transporter

An abalone collector-transporter was designed and fabricated to provide an
attachment surface for the abalone while in transit and in the seeding module.

INNOVATIVE TECHNIQUE FOR SEEDING ABALONE y\

The collector-transporter was made from four, 50 cm long PVC pipe sections,
of four diameters (10, 1 5, 20 and 25 cm), that were cut in half lengthwise. These
were stacked one directly above the other (smallest diameter pipe on the
bottom), and fastened together near either end using 2 X 13 cm PVC bolts.
This configuration provided about a 2 to 3 cm space between each pipe section
for the abalones (Figure 2). Astroturf was affixed to the collector-transporter
base. This served two purposes; (i) it prevented abalone from adhering to the
base whereby they could be crushed when the collector-transporter was
positioned in the seeding module following transit and (ii) it presented a good
friction surface with the concrete. This minimized the shifting of the collector-
transporter in the seeding module, particularly when subjected to severe
seawater surge conditions, and thus reduced potential damage to the contained
abalone. The abalone collector-transporter was designed to accommodate 500
to 1000 juvenile abalone of 15 to 30 mm shell lengths. A seeding module
accommodates only one collector-transporter.

FIGURE 2. The collector-transporter used for translocating abalones from the laboratory to the
field. Not to scale. Dimensions, overall, are 50 X 31 X 19 cm high.

Abalone Species Selection and Shell Color

The red abalone was selected for testing because it was readily available,
economically is the most valuable to the fishery resource, and because stocks
have been seriously depleted in some areas. The animals used for this study
were hatchery-reared and supplied by the CDFG, Marine Resources Laborato-
ry, Granite Canyon (MRL).

It is well known that diet influences the shell coloration of abalone (Leighton
1961, Olsen 1968). Since the hatchery-reared abalone used during this study
were fed predominantly giant kelp, Macrocystis spp., their shell color was
typically aquamarine. By contrast, native red abalone typically exhibit a sepia
shell color. Therefore, the shell coloration of hatchery-reared abalone used for
this study served as a useful "tag" for field identification from the natural
population, and also could be used for subsequent growth rate information.

CALIFORNIA FISH AND GAME

Laboratory Studies

Laboratory studies with the abalone seeding module were conducted in a
circular, 2.4 m diameter, fiberglass tank. Ambient temperature seawater
(12-15°C) was provided. To simulate the natural environment, cobbles and
boulders, with attached biota, were distributed on the tank floor. Additional
substrate consisted of four hollow concrete blocks that were spaced equidistant
around the tank floor perimeter. Sand patches fronted each concrete block, and
giant kelp fronds were anchored to two of the concrete blocks. This
arrangement of substrates and kelp (Figure 3) was used to determine abalone
dispersal patterns, substrate preferences, and the influence of forage (kelp).

CONCRETE

BLOCK

FIGURE 3. A schematic diagram of the 2.4 m diameter tank floor layout used to measure abalone
dispersal rates and patterns.

INNOVATIVE TECHNIQUE FOR SEEDING ABALONE 73

Two abalone size groups were used, with one exception, for laboratory trials.
These averaged 10 mm (range = 8-1 2 mm), and 20 mm (range =18-22 mm)
shell lengths, and 250 of each size group were used per trial. The one variant
abalone size group trial comprised 554 individuals with a mean length of 32 mm
(range = 24-45 mm). The abalone used for all trials were first contained and
acclimated in the seeding module through 2 nocturnal periods. A magnesium
link size was selected that would decay, separate, and release the seeding
module doors in the late afternoon-early evening period, just prior to the third
nocturnal period of abalone containment. This release time was selected
because it corresponds to a known rise in abalone activity that has been
observed in laboratory and field populations.

An initial series of seven trials were made in the tank to measure abalone
dispersal rates and movement patterns from the seeding module according to
abalone size. They spanned 1,2,2,4,5,7 and 8 nocturnal periods post-abalone
release. The second 2 day release period (noted above) was conducted for the
larger abalone size group (x = 32 mm). All abalone were recovered at the end
of each trial and their location plotted diagramatically on a data sheet.

Following the initial series of trials a longer term trial (28 days) was
conducted. Only the 10 mm and 20 mm mean length abalone size groups were
used for this trial; 250 of each size group. The tank was drained daily and all
abalone were counted according to size and location inside and outside of the
seeding module for the trial duration. This trial was duplicated using two "fresh"
abalone size groups.

Field Studies

Field studies were conducted in Carmel Bay, California (lat 36°34'N, long
12r56'W). These studies were designed principally to compare abalone
behavior and survivorship according to seeding method and abalone size. The
study area was comprised of two sites 50 m apart, in 7 m depths. Each study site
area was circular and encompassed about 28 m ^. A 3 m radius line was used
to delimit each study site. An abalone seeding module was placed at one site,
while the other site (control) lacked a seeding module. Abalone seeded at the
control site were allowed to attach to adult abalone shells in the laboratory,
about 10-15 per shell, transported to the control site where the shells were
hand-planted in rock crevices. The abalone collector-transporter was used to
hold and transport abalone to the seeding module.

The biota in the general study area was characterized with respect to abalone
ecology. Macrocystis was the major canopy forming algae present, and is
important nutritionally for abalone. Predominant phaeophytes in the understory
were Laminaria spp. and Pterygophora californica while Botryoglossum farlo-
wianum, Gigartina spp. and Rhodymenia spp. were the most conspicuous
rhodophytes. Articulated and crustose coralline algae were major turf compo-
nents.

Known juvenile abalone predators in the general study area, although not
necessarily documented during surveys, included the cabezon, Scorpae-
nichthys marmoratus; crabs. Cancer spp.; Loxorhynchus crispatus, Paguristes
spp.; various sea stars, Pisaster spp., Orthasterias koehleri, and Pycnopodia
helianthoides; and octopuses. Octopus spp.

74 CALIFORNIA FISH AND CAME

To assess the octopus population, traps were designed, fabricated and
deployed. These consisted of PVC pipe sections, about 36 cnn long, of three
dianneters (about 2.5, 3.8 and 5.1 cm), capped at one end, with a coupling
inserted near the capped end to facilitate octopus removal. Three traps, one of
each size, were deployed at each study site.

One field trial was conducted using 1000 abalone of two size groups
accordingly:

Abalone size group and no. of abalone

10 mm 20 mm

Site (range = 8-12 mm) (range = 18-22 mm)

Control 250 250

Seeding module 250 250

The abalone were transported from the laboratory to the study site,
out-of-water, in styrofoam containers following procedures developed at the
MRL. These consist of putting the abalone and their substrates (adult abalone
shells or collector-transporter) in a plastic bag, adding seawater moistened
sponges, filling the plastic bag with pure oxygen and sealing it. One or two
refrigerant bags (BLUE ICE®) are placed on the bottom of each chest, followed
by 5-6 layers of newspaper to insulate the abalone from close contact with the
refrigerant. Transit time from the laboratory to the study site, and placement of
the abalone in the seeding module was about 2 h.

Field observations began two days after the abalone were seeded, just prior
to the separation of the magnesium link in the seeding module. A second survey
was made just following magnesium link separation and door release. Obser-
vations were made at both sites weekly thereafter with a minimum of
distrubance. These surveys included, (i) a general qualitative assessment of the
biota, (ii) qualitative and quantitative observations of abalone distributions and
dispersal patterns, (iii) removal of dead abalone (empty shells) and noting
when possible, the cause of mortality, (iv) opening the seeding module lid to
determine abalone dispersal rates and to check for abalone predators, and (v)
examination of octopus traps. Four weeks post-release both sites were
destructively surveyed. This entailed thorough examination and disturbance of
all abalone habitat, where physically possible, throughout the 28 m ^ study site.
All live abalone found were noted according to position and examined for
growth. A less intensive extralimital survey was made for seeded abalone that
extended out to approximately 10 m from each site reference point. This survey
focused on areas with turnable rocks (15 cm diameter and larger), because they
are a preferred habitat of cryptic abalone in the area.

RESULTS

Seeding Module Performance

The seeding module performed well during laboratory and field trials.
Magnesium links separated as planned, and the buoys lifted the doors clear of
the module passageways on all trials. The configuration and weight of the
module enabled it to remain stable at the relatively shallow depth of the study
site, even during moderately strong surge conditions. Seawater quality inside the
seeding module apparently was adequate for the abalone since there were no

INNOVATIVE TECHNIQUE FOR SEEDING ABALONE 75

mortalities or evidence of stress. The grate affixed to the door passageway was
sufficient to preclude observed abalone predators, yet there was no evidence
that abalone egress from the module was inhibited.

The abalone collector-transporter proved to be an efficient method to collect,
hold, and transport abalone to the seeding module. Abalone readily crawled on
the collector-transporter when it was placed in a laboratory tank containing
abalone, and there were no mortalities during the 2 h transit (out-of- water)
period, for the field trial.

Laboratory Trials

Initial Trial Series

Fifty percent or more of all abalone size groups had left the seeding module
following two nocturnal periods (Table 1). A direct relationship was evident
between abalone size and dispersal rate from the seeding module. The largest
abalone size group (x = 32 mm) traveled further, faster, than other size groups.
The smallest abalone size group (x = 10 mm) dispersed the slowest.

TABLE 1. Dispersal Of Red Abalone From The Seeding Module, During Laboratory Trials, N (%).

Size Nocturnal periods and abalone, n (%), found outside

group No. seeding modules following release

(mm) seeded 1 2 4 5 7 8 28 28

10 250 96(38) 143(57) 176(70) 184(74) 180(72) 152(61) 220(88) 232(93)

20 250 130(52) 127(51) 200(80) 149(60) 235(94) 215(86) 230(92) 248(99)

32 554 281(51)

The two larger abalone size groups preferred the concrete blocks with kelp
rather than the blocks without kelp (Table 2). Observations of the largest
abalone size group revealed that following two nocturnal periods post-release,
281 (50.7%) were outside the seeding module, of which 143 (50.9%) were
observed on the concrete blocks with kelp, while only 10 (3.6%) were
observed on the concrete blocks without kelp. This preference of the larger size
abalone for concrete block habitats with giant kelp progressively increased with
time. By contrast, the smallest abalone size group (x = 10 mm) was not
observed on concrete blocks until seven nocturnal periods had elapsed, and
very few were present (Table 2). All abalone size groups formed clumped
distributions, irrespective of habitat type.

TABLE 2. Number of Red Abalone Observed On Concrete Block Habitats With And Without Giant Kelp.

Size

group Nocturnal periods and no. of abalone on habitats (kelp/ no kelp) following release

(mm)

0/0

111

2/0

19/9

24/13

14/0

20/2

32/6

34/5

65/7

56/6

63/13

89/15

143/10

Second Trial Series

Abalone dispersal rates from the seeding module compared closely with the
first trial series through eight nocturnal periods. Also, no significant difference
was apparent between the duplicate test runs (comparison of simple linear
regressions, 0.1 < P < 0.2). Following release of the doors from the seeding
module passageways, the exodus of abalone was initially high, then leveled and
remained at a uniform rate (Figure 4). After 14 nocturnal periods post-door

CALIFORNIA FISH AND CAME

release approximately 50 abalone remained in the module, but very few were
on the collector-transporter and it was removed. Also, it became evident
through day-to-day counts that some abalone that had left the module returned.

250

li.
O

200

• tOmm size group
o 20mm size group

150

[

100

—

I 1

1 1 1 1 1 1 1

2 4 6 8 10 12 14 16 18 20 11 24 26 28
NOCTURNAL PERIODS

FIGURE 4. Dispersal rate of the red abalone from the seeding module during laboratory trials.

Observations made three nocturnal periods after the doors were released
revealed a correlation between abalone movement and photoperiod. Sightings
made at midday (1200 h and bright sun), 1.5 h before sunset, at sunset, and 45
min. later revealed 2,8,41, and 150 emergent abalone, respectively. Also,
observations made at sunset and later revealed a high activity level for the
emergent abalone as they traversed the rock substrate.

Field Trial

This trial was conducted during the summer (August-September) period
when algal assemblages in Carmel Bay typically attain maximum seasonal
lushness (Foster and Schiel 1985). Sea surface temperatures averaged 13.7°C.
The octopus traps were examined, at each site during each survey, but no
octopuses were caught.

Seeding Module Site

When the collector-transporter and contained abalone seed was placed in the
seeding module no conspicuous abalone predators were observed within 3 m
of it. Also, abalone predators were not observed just prior to, and immediately

INNOVATIVE TECHNIQUE FOR SEEDING ABALONE TJ

following door release. Only one masking crab, L crispatus, was found within
the study site during the trial. Weekly observations revealed that the abalone left
the seeding module at a rate comparable to that documented during laboratory
trials. After 4 weeks no abalone remained in the seeding module. Prior to the
destructive survey, abalone were observed under rocks and in crevices at
distances up to 10 m from the seeding module. After 4 weeks at liberty 178 live
abalone, comprised of almost a 50:50 size group ratio, were located (Table 3).
The majority of these abalone were evenly distributed out to 3 m from the
module. A cursory survey beyond the site limits uncovered one 20 mm size
group abalone about 8 m from the module. In general, most abalone were found
under rocks that were 15 cm and larger in diameter. All but six of the abalone
(five 10 mm and one 20 mm size group) exhibited recent shell growth. Very
few empty shells were found (Table 4).

TABLE 3. Live Red Abalone Recovered, Percent Showing Shell Growth, And Percent Unaccounted For,
After Four Weeks, From The Field Study Sites In Carmel Bay.

Size

Live abalone New shell Abalone

:)ite

group (mm)

no. % growth (%) unaccounted (%)

Seeding

87 34.8 94.3 64.4

module.

91 36.4 99.6 61.2

Control . . .

26 10.4 34.6 84.8

81 32.4 84.0 50.4

TABLE 4.

Red Abalone Mortalities Recovered During Weekly Surveys At The Field Study Sites In Carmel

Bay.

Abalone size

Shell recoveries (no. /condition *)

Site

group (mm)

week 1 week 2 week 3 week 4 total

Seeding

01— 0/- 0/— 2/1 2

module

2/1 0/- 1/F 2/F 6

1/1

Control . . .

2/1 3/1 2/1 5/1 12

2/1 2/1 2/1 5/F
8/F 2/CE 3/CE 8/1

11 /CE 43

* 1 = intact.

F = fragment,

CE = chipped edges

Control Site

No obvious large abalone predators were observed while seeding the
abalone, although small crabs (eg. Paguristes spp., and Mimulus spp.) were
seen. However, 2 days post-abalone seeding two L. crispatus and one P.
brevispinus were observed at the site but not removed. Shell fragments of two
20 mm size group abalone were observed along with the majority of the live
seeded abalone still attached to the adult abalone shells that had served as their
seeding substrate. A cursory examination of the undersides of several smaller
rocks that were adjacent to the seeding substrates revealed several clumps of
seeded abalone.

During each weekly survey predatory sea stars were observed within the
study site. Additionally, a cabezon was seen on one occasion and masking crabs
were common. Many of the seed abalone appeared to remain on the shells
used as a planting substrate for the duration of the study. After 4 weeks at liberty
107 seed abalone were located and marked with a grease pencil (Table 4).

78 CALIFORNIA FISH AND GAME

Most abalone (97%) were found on the original planting shells or next to them,
while no abalone were found beyond the study site limits. In comparison to the
seeding module site, a smaller percentage of both seed abalone size groups
showed growth. Surveys disclosed a greater number of empty shells at this site
compared to the seeding module site (Table 4) . These mortalities were typically
found where they had been planted.

DISCUSSION

Abalone seeding projects in California, prior to this study, generally required
too many divers who expended considerable time and effort hand-planting
abalones. This resulted in disturbance of the physical habitat at the seeding site,
and frequently attracted abalone predators (Fox and McMullen, unpubl. data;
Tegner and Butler 1985). The use of "mother" shell (adult abalone, scallop or
oyster shells) as an attachment surface for seed abalone did serve to reduce
seeding time and effort, and probably stress on the abalones. Data compiled
from several CDFG Cruise Reports show that an average of 529 abalone were
seeded per diver h (range = 200-1027). This average coincides with the time
( 1 h) needed to seed 500 abalone at the control site. In contrast, we seeded 500
abalone in 5 diver min in the seeding module, with a minimum of site
disturbance, and without attracting predators. Moreover, this seeding rate can
be increased several fold simply by increasing the seeding module size and
number of contained abalones.

The abalone containment period in the seeding module prior to door release
(minimum of 48 h) was arrived at through deductive reasoning and seems
satisfactory. We hypothesized that this time period was sufficient for the
abalone to acclimate, and a lack of forage (kelp) would serve to hasten their
departure from the module. This starvation period, based on laboratory
observations, would not cause stress. No tests were performed at shorter or
longer durations and it is possible that some other containment duration could
prove more optimum.

There is strong evidence from laboratory and field observations (pers.
obser.), and reinforced by this study, to indicate that twilight (early evening) is
an optimum time for seeding module door release and abalone dispersal. The
abalone activity level sharply increases at this time and does not diminish until
just before dawn.

Initially we were concerned about possible poor water circulation within the
seeding module, particularly during laboratory trials, where water flow rates
were considered low. However, there was no evidence of hypoxic conditions
(no stressed or dead abalone). This suggested that the seeding module possibly
could accommodate a greater abalone density. We confirmed this by routinely
holding 1,000 red and pink abalone, H. corrugata, averaging about 20 mm long,
in a seeding module with a collector-transporter. These were 48 h tests,
performed in the laboratory, and without any abalone mortalities.

During laboratory and field trials the dispersal rate of abalone from the
seeding module appeared to be fairly rapid. For example, during laboratory
trials approximately 50% of all abalone had left the seeding module following
two nocturnal periods. Initial field observations disclosed that after one week
post-release only 11% of the abalone remained. The results of all laboratory and
field trials showed that 90% or more of all abalone had left the seeding module

INNOVATIVE TECHNIQUE FOR SEEDING ABALONE 79

within two weeks. Most abalone observed in the seeding module after two
weeks exhibited growth, which suggests that these individuals used the module
as a habitat and foraged outside nocturnally.

Fox and McMullen (unpublished data) found that potential abalone preda-
tors were attracted to the seeding area while the abalones were being seeded,
and observed predation of just-seeded abalones. Tegner and Butler (1985)
noted that abalone predators rapidly returned to an abalone seeding area
following their removal, and that seeded and hence stressed abalones, were
also vulnerable to the whelk; Kellettia kelletti. This whelk does not prey on
healthy abalone. It was clearly evident from our field study that the control site
abalone attracted predators. In contrast, the abalone seeded at the module did
not attract obvious potential abalone predators, or other reef fauna during the
field trial; either before or after door release.

The more rapid egress and dispersal of the larger size group (20 mm) abalone
from the seeding module during laboratory trials and their preference for
concrete blocks with kelp was not unexpected. Momma et al. (1980) and
Miyamoto et al. (1982) reported that larger abalone seed sizes dispersed more
rapidly. The 20 mm size abalone probably were attracted to the blocks with kelp
because they prefer macroalgae, while their smaller size cohorts ( < 15 mm)
prefer a diatom diet; and a diatom film covered most exposed surfaces.

Principally, we tested two abalone size groups to compare dispersal rates
from the seeding module and survival. Underlying these tests was the obvious
and direct implication to the economics of seeding abalone for fishery
enhancement (i.e. cost effectiveness). It requires about six months to cultivate
red abalone to 10 mm shell lengths, and another five months for them to attain
20 mm lengths. There is a direct relationship between seed size and cost. The
main objective is to optimize abalone seed size with survivorship. Some
investigators report better abalone survival at larger seed sizes (Inoue, 1976;
Momma et al., 1980; Miyamoto et al., 1982). But, Tateishi et al. (1978) found
a survival rate of 48.6% nine months after abalone averaging 14.4 mm were
released into the wild, and attributed this high survivorship to the physical and
biological conditions present at the release site. Tegner and Butler (1985)
reported no difference in survivorship, after 1 year, for two red abalone size
groups that averaged 45 and 71 mm when seeded. We found more 20 mm than
10 mm live abalone after four weeks at liberty at both sites. However, due to
the difficulties of locating small sized abalone, and the length of the field trial no
conclusions can be made.

A high percentage of "unaccounted for" abalone has plagued the interpre-
tation of results of most seeding projects in California, including this one.
Although we observed a significant difference in survivorship according to
seeding method, over 90% of the seeded abalone, overall, were not relocated.
Abalone < 5 cm long are difficult to locate because of the cryptic refuges they
inhabit during daylight hours. It follows that fewer small size abalone are apt to
be observed where optimum habitat exists. Yet, abalone are known to move
extensively at night. Momma and Sato (1969) found that H. discus hannai
moved 56.2 m during one night of foraging. The foregoing suggests that another
method may be needed to assess the short-term as well as long-term results of
abalone seeding projects.

80 CALIFORNIA FISH AND GAME

One method that may be useful for estimating abalone seed survivorship is
based on empty seed shell recoveries. Empty shells are easily seen because their
nacreous interior is reflective and often exposed. Small empty abalone shells are
not subject to extensive transport by prevailing currents and the majority of the
shells are usually recovered (T. Ebert unpubl. data, Mines and Pearse 1982,
Schmitt and Connell 1982). Shells could be transported by predators (e.g. 5.
marmoratus and Octopus spp.) or destroyed by crustaceans (e.g. L. crispatus).
Using this criterion (no. empty abalone shells found = l<nov;'n mortality), our
seed survivorship, after 4 weeks, was 98.4% and 89.0% at the seeding module
and control sites, respectively. This survivorship seems inordinately high.

Efforts to enhance California's abalone populations, either by transplanting
mature adult stock, or by seeding smaller size, hatchery-reared abalone, have
spanned a 30 year period. But, the results of either method has been difficult to
assess. The transplant method generally employs a relatively small number of
large abalone which are ready to spawn and presumably do so. The success of
the transplant may not be dependent upon long-term adult survivorship, but
survivorship of their offspring. Adult transplants are conducted at the "expense"
of one region of the fishery to enhance another. This practice may not be
prudent given that the fishery is being fully exploited. Field studies (Giorgi and
DeMartini 1977), and laboratory studies (Ebert and Houk 1984) show that the
onset of sexual maturity in the red abalone occurs at about a 4 cm shell length.
These smaller size red abalone exhibit greater sexual vigor in the laboratory,
when compared to larger adults (>15 cm), and may spawn thrice annually
(Ebert and Houk 1984). Presumably this sexual vigor occurs in nature and may
serve to enhance recruitment through broadcasting gametes during most or all
annual oceanographic regimes. Laboratory and field observations made over
several years indicate that hatchery-reared abalone respond similarly to natural
population abalone with respect to predator-prey relationships. For these
reasons we suggest that small hatchery-reared abalones be seeded in future
programs rather than the transplantation of larger abaione. The red, green, and
pink abalone species are routinely cultivated, and available.

CONCLUSIONS

The results of this study indicate that the use of an abalone collector-
transporter, seeding module method offers:

(i) An efficient method to collect, transport, and seed relatively large

numbers of abalone;
(ii) Reduced handling stress on abalone;

(iii) An acclimation period for abalone free from potential predators;
(iv) A timed-release mechanism that permits abalone dispersal from the

seeding module at an optimum time.

Further research is needed on optimizing abalone seed size and survivorship,
and the development of a reliable method to assess the results of a seeding
program.

INNOVATIVE TECHNIQUE FOR SEEDING ABALONE 81

ACKNOWLEDGMENTS

We are thankful to D. Ebert, J. Houk and D. VenTresca for their diving
assistance and helpful suggestions. The California Department of Fish and
Game's Marine Resources Laboratory at Granite Canyon supplied the abalone
seed and provided laboratory space and general assistance throughout this
study.

LITERATURE CITED

Burge, R. T. and S. A. Schultz. 1973. The marine environment in the vacinity of Diablo Cove with special reference
to abalones and bony fishes. Mar. Res. Tech. Report No. 19. 433p.

Burge, R., S. Schultz and M. Odemar. 1975. Draft report on recent abalone research in California with

recommendations for management. State of California. The Resources Agency, Depart. Fish and Game. 62

PP-
Cox, K. W. 1962. California abalones, family Haliotidae. Calif. Dept. Fish and Came, Fish Bull. (118) 1-133.
Ebert, E.E. 1968a. California sea otter-census and habitat survey. Underwater Naturlist, Winter: 20-23.
1968b. A food habits study of the southern sea otter, Enhydra lutris nereis. Calif. Fish and Game,

54(1):33^2.
Ebert, E. E. and J. L. Houk. 1984. Elements and innovations in the cultivation of red abalone Haliotis rufescens.

Aquaculture, 39: 375-392.

Foster, M. S., and D. R. Schiel. 1985. The ecology of giant kelp forests in California: a community profile. U.S. Fish
and Wildl. Serv. Biol. Rep. 85(7.2): 152 p.

Giorgi, A. E. and J. D. DeMartini. 1977. A study of the reproductive biology of the red abalone, Haliotis rufescens
Swainson, near Mendocino, California. Calif. Fish and Game, 63(2):80-94.

Hardy, R., F. Wendell and J. D. DeMartini. 1982. A status report on California shellfish fisheries. Pages 328-340
in B. Cicin-Sain, P. M. Grifman and J. B. Richards, eds. Social science perspectives on managing conflicts
between marine mammals and fisheries.

Hines, A. H., and ). S. Pearse. 1982. Abalones, shells and sea otters: dynamics of prey populations in central
California. Ecology, 63 (5) :1 547-1 560.

Inoue, M. 1976. [Abalone.] Pages 19-60 in Suisan Zoyoshoku Deeta Bukku. [Fisheries Propagation Data Book.]
Published by Suisan Shuppan. Translation by M. Mottet, State of Washington, Department of Fisheries.

Leighton, D. L. 1961. Observations of the effect of diet on shell coloration in the red abalone, Haliotis rufescens
Swainson. The Veliger 4(1):29-32.

Miller, D. J. 1974. The Sea Otter Enhydra lutris Its Life History, Taxonomic Status, and Some Ecological
Relationships. Calif. Dept. Fish and Came, Mar. Res. Leafl. (7):1-13.

Miyamoto, T., K. Saito, S. Motoya, and K. Kawamura. 1982. Experimental studies on the release of the cultured
seeds of abalone, Haliotis discus hannai Ino in Oshoro Bay, Hokkaido. Sci Repts. Hokkaido Fisheries
Experimental Station, No. 24:59-89. (English abstract, figures and tables).

Momma, H. and R. Sato. 1969. The locomotion of the disk abalone, H. discus hannai Ino, and the Seibold's
abalone H. seiboldii Reeve, in the fishing grounds. Tohoku ) Agric Research 29 (3) :1 50-1 57.

Momma, H., K. Kobayashi, T. Kato, Y. Sasaki, T. Sakamoto, and H. Murata. 1980. [On the artificial propagation
method of abalone and its effects on rocky shores. I. Remaining ratio of the artificial seed abalone (Haliotis
discus hannai Ino) on latticed artificial reefs.] Suisan Zoshoku [The Aquaculture], 28(2) :59-65. Translation by
M. Mottet, State of Washington, Department of Fisheries.

Olsen, D. A. 1968. Banding patterns in Haliotis. II. Some behavioral considerations and the effect of diet on shell
coloration for Haliotis rufescens, H. corrugata, H. sorenseni and H. assimilis. Veliger 11 (2):135-139.

Schultz, S. A. 1984. Status of abalone resource. Odyssey, 7(2):4-5.

Schmitt, R. J. and J. H. Connell. 1982. Field evaluation of an abalone enhancement program. Pages 172-176 in

California Sea Grant College Program 1980-1982 Biennial Report, Institute of Marine Resources, University

of California, La Jolla.

Tateishi, M., M. Tashiro, and T. Yada. 1978. Place of releasing and survival rate of artificially raised young abalone,

Haliotis discus. Suisan Zoshoko (The Aquaculture], 26(1):1-5. Translation by M. Mottet, State of Washington,

Department of Fisheries.
Tegner, M. |., ]. H. Connell, R. W. Day, R. J. Schmitt, S. Schroeter, and ). B. Richards. 1981. Experimental abalone

enhancement program. Pages 114-116 in California Sea Grant College Program 1978-1980 Biennial Report,

Institute of Marine Resources, University of California, La Jolla.
Tegner, M. |. and R. A. Butler. 1985. The survival and mortality of seeded and native red abalones, Haliotis

rufescens, on the Palos Verdes Peninsula, Calif. Fish and Game, 71 (3):150-163.

82 CALIFORNIA FISH AND GAME

Calif. Fish and Came 74 ( 2 ) ; 82-86 1 988

THE SURVIVAL AND GROWTH OF TRANSPLANTED

ADULT PINK ABALONE, HAUOTIS CORRUGATA, AT

SANTA CATALINA ISLAND^

KRISTINE C. HENDERSON, DAVID O. PARKER, and PETER L. HAAKER

California Department of Fish and Game

Marine Resources Division

1301 West 12th Street

Long Beach, California 90813

Pink abalone, Haliotis corrugata, populations, once abundant at Santa Catalina
Island, have declined drastically. During January and April 1983, 517 adult pink
abalone were experimentally transplanted from San Clemente Island to Emerald
Bay on the northeast side of Santa Catalina Island as a potential concentrated
spawning stock.

By February 1984, the shells of 91 (18%) dead abalone had been recovered, and
only 24 (5%) live abalone could be located at the transplant site. The loss of the
remaining 402 (78%) tagged abalone is believed due to illegal take. Changes in
length of 12 of the live abalone ranged from —8 to +7 mm (x = 0 mm), with only
three showing growth. Growth was affected by the disappearance of the local kelp,
due to an influx of warm water associated with an El Nino event.

INTRODUCTION

The pink abalone, Haliotis corrugata, is a valuable commercial and recre-
ational species in southern California. Once abundant on the mainland south of
Pt. Conception and around some of the Channel Islands, their numbers have
greatly declined. California commercial landings of pink abalone peaked at
1,507,593.6 kg (in the shell) in 1952, and fell to 25,812.6 kg by 1984 (California
Department of Fish and Game landing receipts). Commercial passenger fishing
vessel (CPFV) records shov^ a high of 16,292 abalone taken at Santa Catalina
Island in 1973 and only 2,296 in 1983, the bulk of the harvest being pink and
green abalones.

In 1975 the California Department of Fish and Game (CDFG) identified six
major causes for the decline in abalone populations. The causes were sea otter
range expansion, mortality of sublegal sizes, over harvesting, competition from
sea urchins, illegal harvesting, and loss of habitat (Burge et al. 1975).
Encouraged by Japanese reports of successful abalone enhancement, one of the
recommendations made by CDFG was to embark on an experimental abalone
enhancement program. Ocean outplant of hatchery raised juvenile abalone and
transplantation of native adult spawning stocks were two methods selected by
the CDFG and Scripps Institution of Oceanography for further study and
evaluation.

Successful transplants of adult green abalone, H. fulgens, have been made by
CDFG and Scripps biologists in recent years (Tegner in press). Also two
transplants of adult pink abalone were made at Laguna Beach; 375 were planted
there in 1975 and 109 in 1976. After one year, good survival and growth were
observed. No inter-island transplanting was undertaken.

' Accepted for publication November 1987.

SURVIVAL AND GROWTH OF PINK ABALONE

In 1982 we selected an area of good abalone habitat, which supported few
native (pink and green) abalone, within an area closed to the take of
invertebrates on the northeast side of Santa Catalina Island. Early in 1983 two
groups of tagged and measured adult pink abalone were transplanted from San
Clemente Island to Santa Catalina Island. Here we report on the survival and
growth of these transplants.

STUDY AREA

Santa Catalina Island is approximately 37 km offshore of the southern
California mainland. The northeast side of the island between Lion Head Pt. and
Arrow Pt. is closed to the take of invertebrates between the high tide mark and
304.8 m (1000 ft) seaward beyond the low tide mark. The transplant site (lat 33°
28'N, long 118° 31.5'W) consists of 2024 m^ of rocky bottom, 3-12 m deep,
west of Indian Rock. The substrate is good pink abalone habitat with rocky
outcrops, boulders, low lying vertical relief and sediment/ rock interfaces. The
Indian Rock area is surrounded by sandy substrate, which restricts abalone
movement (Cox 1962), and is located inside Emerald Bay at the western end
of the closure area (Figure 1). Emerald Bay is a popular anchorage for
recreational boaters and CPFV dive boats. A bed of giant kelp, Macrocystis
pyrifera, with a red algal understory was present at the start of the study.

Santa Catalina
Island

INVERTEBRATE CLOSURE AREA

•« ^

V^"^ Transplant Site

E m e r ia
Bay

t
0 1

NAUTICAL MILES

FIGURE 1. Transplant site at Indian Rock, Santa Catalina Island.

84 CALIFORNIA FISH AND GAME

MATERIALS AND METHODS

Adult pink abalone were collected from various locations at San Clemente
Island. The abalone were tagged, measured, and then placed on a thick net
lining the flooded stern well of the R/V KELP BASS. The tags, imprinted stainless
steel washers strung on stainless steel wire, were threaded through the two most
anterior, complete respiratory pores of each abalone. Length and width of each
animal were measured to the nearest mm with vernier calipers, and any injuries
were noted. The net prevented the abalone from firmly attaching to the smooth
deck, thereby reducing the chance of injury when the abalone were removed
for replanting. Seawater was continuously pumped in at the rate of 38 litre/s. At
Santa Catalina Island, each individual abalone was replanted on a rocky surface
suitable for attachment, and observed briefly to ensure attachment to the
substrate.

We returned several times to the transplant area and collected tagged shells
to attempt to quantify mortality. A one-year post plant survey to determine
survival and growth of the transplanted animals was carried out. The transplant
site was thoroughly searched for one hour, and all tagged abalone encountered
were measured, unless their removal would have resulted in fatal injury.

RESULTS

Five-hundred seventeen adult pink abalone, which averaged 141 mm (range
95 to 183 mm), were transplanted in two groups in early 1983 (Table 1 ). Cuts
and abrasions received during collection were greater (29% vs. 14%) in the
January group, as was the observed total mortality (27% vs. 10%). The
transplanted abalone were in good condition when checked in April, July, and
December 1983, and were noted to be feeding and responding normally,
although their numbers appeared to be decreasing. During the study 91 tagged
abalone shells were recovered by CDFG personnel and the public. After an
intensive search in February 1984, we found 24 tagged abalone, 12 of which
were measured underwater and replaced. The other 12 abalone were not
measured because of the risk of injury. The measured animals ranged in size
from 117 to 149 mm. Growth (change in shell length) ranged from minus 8 to
7 mm (x = 0 mm; SD = ± 4 mm), with only three abalone showing an
increase in length. The remaining 402 abalone (78% of the transplant) were not
located as live animals or shells.

TABLE 1. Transplant of Adult Pink Abalone at Santa Catalina Island, California, 1983.

Transplant Date
January April

f0-j4 4-8 Total Percent

Abalone Planted Initially 237 280 517

Transplant Injuries 69 40 109 21.1

Observed Mortality 64 27 91 17.6

One-Year Post Plant Survey

Live Abalone 24 4.6

Abalone Unaccounted For 402 77.8

DISCUSSION

The one-year post transplant survey documented an unexpectedly low
number of 24 surviving abalone. The disappearance of 78% of the animals

SURVIVAL AND GROWTH OF PINK ABALONE 85

cannot be attributed to injury, predation, starvation, migration, or other natural
factors. Green abalone have been successfully established on the mainland
under similar conditions by CDFG/Scripps transplants (Tegner in press), and
the CDFG transplant of pink abalone to Laguna Beach was considered
successful based on a 34% recovery rate after one year. Hence a pink abalone
transplant to Santa Catalina Island was considered viable. A large portion of the
transplanted pink abalone were expected to successfully adapt to their historic
habitat.

Despite special care, abalone are sometimes cut or abraded during collection.
These injuries, or stress induced by handling, will often attract predators or
scavengers and result in the death of the abalone (Tegner and Butler 1985).
Based on previous tagging studies, initial mortalities of 10 to 20% were
expected. Since pink abalone are more susceptible to picking and replacement
injury (Burge et al. 1975) than other California species, initial mortality
exceeding 20% was not considered unlikely. In the January collection, from the
northeast side of San Clemente Island, it was found that the pink abalone's foot
often blistered where the abalone iron contacted it and that cuts were frequent.
In addition, many of these animals appeared stunted and lethargic. The pink
abalone collected in April from the northwest side of the island appeared to be
healthy but were still easily cut. The higher injury rate (29% vs. 14%) and
mortality {ll^/o vs. 10%) of the January group was probably a result of the
general condition of the animals (Table 1 ).

A low level of natural mortality was expected for the relatively large abalone
used in this study. Doi et al (1977) calculated a natural mortality (M) estimate
of .35 for pink abalone. Although not all shells are recovered, losses due to
natural mortality result in empty shells.

Another possible source of shell loss might be movement of live abalone
away from the site. Migration of pink abalone is not common. After following
the movement of pink abalone at Santa Catalina for several years Tutschulte
(1976) concluded "that adult pink abalone do not migrate once they take up
residence on the open substrate". At Indian Rock there was no evidence of
abalone movement. The expanse of sand surrounding the site may also have
impeded abalone movement away from the site. During post-planting visits to
the site we noticed little movement of the tagged abalones, and we frequently
found animals in the same location from one visit to the next. Also contiguous
rocky areas and a reef 15 m from site were searched, as was the sand
surrounding the site. No live abalone or shells were found. If these abalone had
migrated we should have noticed major movement within the site and should
have found animals or shells in the surrounding areas.

Starvation was probably not the reason for the disappearance of the tagged
abalone, although food supplies were reduced. MacGinitie and MacGinitie
(1966) reported that starvation did not stimulate pink abalone to move in an
area off Laguna Beach denuded of seaweed. Abalone can survive for extended
periods without food. Tegner and Levin (1982) ran food deprivation experi-
ments on red abalone, and found the LD50 was 203 days with a tendency for
the smaller animals to die first. However, the shells of those abalone that did
starve would remain.

36 CALIFORNIA FISH AND CAME

Illegal take is the most likely cause of the disappearance of transplanted
abalone from this site. Emerald Bay is a popular recreational dive site with 101
rented moorings. In one case a recreational diver reported harvesting three of
the transplanted abalone while assuming the site was not within the closure. The
Lion Head to Arrow Point invertebrate closure does not appear to be well
known or regularly enforced. No specific printed matter is available on the
closure and no signs are posted on the beach.

Burge et al. (1975) reported average annual growth for pink abalone at San
Clemente and Santa Cruz Islands of 10 mm for animals in the 136 to 145 mm
size range. The poor growth of the surviving Catalina transplants could reflect
measurement error, but more likely was the result of the poor conditions at
Emerald Bay. The El Nino event that began in late 1982 caused deepened
isotherms at Santa Catalina Island resulting in nutrient limited water. The island's
algal community was devastated by the warmer than usual water (Zimmerman
and Robertson 1985). Giant kelp, an important food item for abalone,
disappeared from the transplant site, as did most of the algal understory. Food
scarcity severely impacts abalone growth (Cox 1962) but the low survival of
these pink abalone is considered an anomaly. This study strongly suggests that
a fishing closure area does not always protect an experimental site. Future
abalone transplant sites should be selected with the added criteria of minimal
diving and boating activity.

ACKNOWLEDGMENTS

Special thanks to Mia Tegner, Scripps Institution of Oceanography, for her
encouragement and editorial assistance. We also thank Mike Lonich and the
crew of the R/V KELP BASS for their tireless efforts in support of our research.

LITERATURE CITED

Burge, R., S. Schultz, and M. O. Odemar. 1975. Draft report on recent abalone research in California with

recommendations for management. Calif. Dept. Fish and Came. 62 p.
Cox, K. W. 1962. California abalones, family Haliotidae. Calif. Dept. Fish and Came, Fish Bull. 188: 133 p.
Doi, T., S. A. Guzman del Proo, V. Marin A., M. Ortiz Q., ). Camacho A., and T. Munoz L. 1977. Analisis de la

poblacion y diagnostico de la pesqueria de abulon amarillo {Haliotis corrugata) en el area de Punta Abreojos

e Isia Cedros, B.C. Direccion General Del Institudo Nacional de Pesca, Mexico. Serie Cientifica No. 18.

17 p.
MacGinitie, N, and G. E. MacGinitie. 1966. Starved abalones. Veliger 8:313.
Tegner, M. |. In Press. The California abalone fishery: production, ecological interactions, and prospects for the

future. In ). F. Caddy (Ed.) Scientific approaches to the management of invertebrate stocks. John Wiley and

Sons, New York.
Tegner, M. J. and R. A. Butler. 1985. The survival and mortality of seeded and native red abalones, Haliotis

rufescens, on the Palos Verdes peninsula. Calif. Fish and Game, 71 (3): 150-163.
Tegner, M. |. and L. L. Levin, 1982. Do sea urchins and abalones compete in California kelp forest communities?

Pages 265-271 In ). W. Lawrence (Ed.), International Echinoderms Conference, Tampa Bay. A. A. Balkema,

Rotterdam.
Tutschulte, T. 1976. The comparative ecology of three sympatric abalones. Dissertation. Univ. California, San

Diego. 335 p.
Zimmerman, R. C. and D. L. Robertson. 1985. Effects of El Nino on local hydrography and growth of the giant

kelp, Macrocystis pyrifera, at Santa Catalina Island, California. Limnol. Oceanogr., 30 (6): 1298-1 302.

RECORDS OF DEEP-SEA SKATES 87

Calif. Fish and Came 74 ( 2 ): 87-1 05 1 988

RECORDS OF THE DEEP-SEA SKATES, RAJA (AMBLYRAJA)

BAD/A CARMAN, 1899 and BATHYRAJA ABYSS/COLA

(CILBERT, 1896) IN THE EASTERN NORTH PACIFIC, WITH

A NEW KEY TO CALIFORNIA SKATES '

GEORGE D. ZORZI

and

M. ERIC ANDERSON

Department of Ichthyology,
California Academy of Sciences

Golden Gate Park,
San Francisco, California, 94118

The broad skate, Ra/a (Amblyraja) badia, previously described in the eastern
Pacific from the holotype is here recorded from off central Panama north to
Vancouver Island, British Columbia and redescribed from two recently collected
California specimens. External morphological characters, counts, and measurements
of these specimens are provided. The deepsea skate, Bathyraja abyssicola, previ-
ously described from two adult males, is here recorded from 22 specimens ranging
from West Cortes Basin, California, to the Pacific coast of central Japan. External
morphological characters, counts, and measurements are given from nine speci-
mens, including juveniles and adults of both sexes, from off southern and central
California. An updated key for field identification of adults and subaduits of the
nine species of skates currently known from California waters is provided.

INTRODUCTION

Due to their relatively large size and the great expense associated with
collecting and preserving specimens, chondrichthyan fishes are often rather
poorly represented in museum collections, especially deep-water species.
Published descriptions and identification keys based on the relative paucity of
such specimens, not to mention our knowledge of their biology and distribution,
are too often fragmentary and incomplete. We found this to be the case with
the skates Raja badia and Bathyraja abyssicola.

Carman (1899) described Raja badia from a single juvenile female, MCZ
1008-S, collected off the Pacific coast of Panama. The only subsequent
published descriptions of R. badia (Carman 1913, Beebe and Tee-Van 1941 ) are
based on this account.

Three additional eastern Pacific records of R. badia have been reported, but
with little further comment. Taylor (1972) briefly recorded the capture of a
second specimen from the Culf of California. Yves et al. (1981 ) first listed the
species from Canadian waters (off Vancouver Island). They also applied the
vernacular "broad skate" to the species. Eschmeyer et al. (1983) briefly
described a hardnosed skate (as Raja sp.) from off British Columbia and
Oregon, noting it was "Most likely the adult of Raja badia . . . ." While Yves et
al. (1981) and Eschmeyer et al. (1983) did not identify individual specimens,
the Canadian record was based on BCPM 979-11101. The Oregon record was
based on a 950 mm total length (tl) adult male collected off Oregon in 1968

' Accepted for publication October 1987.

88 CALIFORNIA FISH AND CAME

(L. J. V. Compagno, J. L. B. Smith Institute of Ichthyology, pers. comm.). We
have been unable to locate this Oregon specimen, and have little additional data
on it. A fifth eastern Pacific specimen, also from off Oregon (OS 5035), is
knov^n, but it is currently being studied by M. Stehmann (Institut fur
Seefischerei, Hamburg, Fed. Rep. of Germany).

Although Ishihara and Ishiyama (1986) gave an "Oregonian" distribution for
Raja badia, this species has not been recorded previously from off California. As
a result of collections made by research vessel DAVID STARR JORDAN for the
National Marine Fisheries Service, two juveniles of R. badia are now known
from California waters, a male (CAS 58604) captured in 1381-1404 m off Pt. Sur
and a female (SIO 87-77) captured in 1280 m off Half Moon Bay.

Gilbert (18%) described Bathyraja abyssicola (as Raja) from an adult male
(USNM 48623) taken off the Queen Charlotte Islands, British Columbia. This
specimen was collected in 2903 m, about which Gilbert commented ". . . the
greatest depth recorded for any species of skate ..." a record which continues
to stand after more than ninety years. Subsequent published descriptions of B.
abyssicola (Jordan and Evermann 1898, Garman 1913, Clemens and Wilby
1949, Hart 1973) are based on this account.

Grinols (1965) recorded B. abyssicola from off northern Oregon in 1463-
1554 m. He noted that this "rare species is known from only 4 recorded
specimens . . ." [USNM 48623 (holotype), UW 19372 (now missing, T. Pietsch,
University of Washington, pers. comm.), UW 19393, and USNM 73913]. Miller
and Lea (1972) reported an additional specimen (SIO 62-692) from off North
Coronado Island. This extended the known range to southern California.

Bathyraja abyssicola has been reported recently from the western North
Pacific. Dolganov (1983) gave a brief description, counts, and measurements of
six specimens collected by Soviet vessels between Japan and the Bering Sea,
however he incorrectly referred to the authorship of the species as "Gilbert and
Thoburn, 1895." Nakaya (1983) and Masuda et al. (1984) published photo-
graphs and short descriptions of an adult male (HUMZ 78181) collected in
1110 m off the Pacific coast of northern Japan. Ishihara and Ishiyama (1985)
redescribed the species from a re-examination of data and drawings of the
holotype made previously (H. Ishihara, Institute of Skatology, Fujisawa, Japan,
pers. comm.), plus the western Pacific specimen. They provided a table of
counts and measurements for both specimens and a description of the
neurocranium and adult male clasper of HUMZ 78181, important structures in
skate systematics. Ishihara and Ishiyama (1986) figured the scapulocoracoid
from a second western Pacific specimen of B. abyssicola (MTUF 25270),
collected off central Honshu Island in 800-1000 m. (H. Ishihara, pers. comm.).
Tanaka (1987) published a photograph of a skate which greatly resembles B.
abyssicola taken by the submersible SHINKAI 2000 in Suruga Bay, Japan at
1350 m.

Thus, B. abyssicola is known in the literature from only five specimens from
the eastern Pacific and eight from the western Pacific. It has been adequately
described, however, from only two large adult males. Descriptions of juveniles
and adult female B. abyssicola are lacking. Additionally, disagreement in recent
literature as to the number of median nuchal thorns as a key character for field
identification (Wilimovsky 1958, Miller and Lea 1972, Ishihara and Ishiyama,

RECORDS OF DEEP-SEA SKATES 89

1985), as well as other discrepancies, especially in the earlier literature, are
attributed to an inadequate sample size.

We provide additional data on the external morphology, counts and
measurements, and report new records and range extensions of both R. badia
and B. abyssicola. In addition, we correct some errors noted in our literature
review. Finally, we present an updated key for field identification of adults and
subadults of the nine species of skates known from California waters.

METHODS AND MATERIALS

Preserved specimens examined for this study were measured to the nearest
millimeter (mm). Internal counts were made from radiographs. Counts and
measurements were generally made according to the methods proposed by
Hubbs and Ishiyama (1968) and Ishiyama and Ishihara (1977), with the
following exceptions: (i) orbit length was externally measured and included the
orbital cavity and overlying tissue, thus differing slightly from that made on
cleaned and dissected preparations; (ii) interbranchial distance to first gill slit
(g. s. #1 ) was measured between the inner margins of the left and right first
gill slits and differs somewhat from the measurement "over 1st gill slits" of
authors; (iii) we record both distal and proximal clasper lengths, but use
proximal clasper lengths, but use proximal clasper length as the standard for
these measurements. Total length (tl) is the basis for all body proportions
unless otherwise indicated. Terminology for thorn patterning follows Stehmann
and Burkel (1984).

Owing to their relative scarcity in museum collections, specimens were not
dissected to make cranial or skeletal preparations, determine gut contents,
condition of gonads or clasper structures, or to count spiral valve turns. We did,
however, partially dissect the dorsal portion of the left scapulocoracoid of a
somewhat mutilated B. abyssicola (SIO 71-201 ) for comparison with that of a
western Pacific specimen (MTUF 25270). We also radiographed and dissected
the left clasper of SIO 85-68 for comparison with drawings of that of the western
Pacific specimen (HUMZ 78181) published by Ishihara and Ishiyama (1985).
Institutional abbreviations are as listed in Leviton et al. (1985).

Material Examined

Raja badia

CAS 58604 (568 mm cf); SIO 87-77 (601 mm $).

Bathyraja abyssicola

CAS 38013 (2; 1191 mm cf, 1316 mm $); CAS 38289 (672 mm $); CAS
58481 (3; 622 mm J, 676 mm of, 684 mm CT); MTUf 125270 (1294 mm $;
left scapulocoracoid only); SIO 71-201 (ca. 1010 mm $); SIO 85-45 (1233 mm
J); SIO 85-68 (1315 mm cf); USNM 73913 (735 mm $; radiograph).

Raja (Amblyraja) badia Carman, 1899
(Figure 1)

Diagnosis

A medium sized Raja (to 985 mm tl); disc rhomboid, width 1.3 times in disc
length; dorsal surface of disc and tail covered with prickles; rostrum with greatly

CALIFORNIA FISH AND GAME

enlarged thornlets in random pattern; one pair each of preorbital, postorbital
and interspiracular thorns; two or three pairs of scapular thorns; continuous row
of 24-29 thorns along midline of body and tail; tail short, with row of enlarged
thornlets on either side of median thorns (more pronounced anteriorly); ventral
surface completely smooth.

FIGURE 1 . Raja (Amblyraja) badia Garman. Left, dorsal view of CAS 58604, photo by B. S. Eddy,
Right, snout region of same specimen, photo by G. D. Zorzi.

Description

A full redescription of this species will be given by Stehmann, Ishihara and
Nakaya (in prep.). We include the following description of the California
specimens (CAS 58604; SIO 87-77) to distinguish the species for the aid of
fisheries workers who may encounter this skate in the future. Proportional
measurements, expressed as percent TL, are given in Table 1 .

TABLE 1. Proportional Measurements (mm) And Counts Of Raja (Amblyraja) badia.

Total length

Disc width

Head length

Disc length

Disc depth between orbits

Greatest disc depth

Trunk length

Tail length

Tail width, end P2

Tail depth, end P2

Preorbital length

Prespiracular length

Snout tip to maximum disc width

Predorsal 1 length

Predorsal 2 length

Snout tip to caudal fin origin

D1 origin to tail tip

Prenarial length

CAS 58604

SIO 87-77

% TL

568

601

431

75.9

443

71.7

138

24.3

141

23.5

322

567

337

561

5.0

4.8

7.4

7.1

202

35.6

202

33.6

228

40.1

258

42.9

4.0

3.0

3.3

14.6

112

19.7

118

19.6

225

39.6

235

39.1

497

87.5

522

86.9

519

91.4

550

91.5

540

95.1

580

96.5

12.5

13.3

13.0

12.3

RECORDS OF DEEP-SEA SKATES 91

TABLE 1. Proportional Measurements (mm) And Counts Of Raja (Amblyraja) Aac^ri?.— Continued

Preoral length

Prebranchial length

Snout tip to gill slit #5

Snout tip to vent center

Precaudal body length

Corneal length

Orbit length

Interorbital distance

Spiracle length

Interspiracular distance

D1 base length

D1 vertical height

D2 base length

D2 vertical height

Interdorsal distance

D2 to caudal fin origin

Caudal base length

Caudal upper lobe vertical height

Lateral fold length (avg)

Nasal curtain length

Nasal curtain width

Internarial distance

Mouth width

Interbranchial distance, g. s. #1

Interbranchial distance, g. s. #5

Pelvic fin anterior lobe length

Pelvic fin posterior lobe length

Clasper length, distal

Clasper length, proximal

Counts

Tooth rows in upper jaw

Pseudobranchial folds(r/l)

Vertebrae, trunk

Vertebrae, predorsal-caudal

Pectoral fin radials

Pelvic fin radials

Preorbital thorns

Postorbital thorns

Interspiracular thorns

Scapular thorns

Total median thorns

Disc rhomboid, 1.3 times as broad as long. Tip of snout moderately produced,
broadly rounded. Anterior margins of disc form almost a right angle; margins
gently convex from behind tip of snout to approximately the level of orbits,
becoming weakly concave, then broadly rounded distally. Apex of disc sharply
rounded at posterior margin. Posterior margin forming angle of about 105° with
anterior margin; posterior margin moderately concave near apex, becoming

CAS 58604

SIO 87-77

% TL

17.3

100

16.6

146

25.7

138

23.0

195

34.3

180

30.0

325

57.2

324

53.9

340

59.9

343

57.1

2.1

2.3

4.9

4.5

6.5

6.0

2.6

3.2

9.7

9.3

4.2

4.3

1.6

2.0

3.9

4.8

1.9

1.8

0.5

0.0

4.2

0.5

198

34.9

224

37.3

5.8

5.0

2.1

2.7

13.6

10.8

13.2

13.0

121

21.3

125

20.8

13.7

14.8

12.5

11.1

14.1

13.1

3.7

6.0

—

10/11

11/11

1 pr

2 pr

92 CALIFORNIA FISH AND GAME

very gently convex at posterior tip, then broadly rounded to axil. Disc relatively
thin. Depth between orbits less than 7% disc width; less than 10% at greatest
disc depth (across scapula).

Head large, length nearly 25% tl. Eyes snnall, corneal length less than 50%
interorbital distance. Spiracles slightly longer than cornea, with 10-1 1 pronninent
pseudobranchial folds. Nasal curtain lobular, with weakly developed finnbriae.
Mouth moderately wide, nearly 20% disc width. Teeth homodont, retrorse, in
37-42 rows in upper jaw, mushroomlike, appearing as thin, ovoid crowns
supported on short, sturdy, somewhat conical bases. Single, stout, sharp cusp
arising from rear-center of each crown and projecting obliquely backward; cusp
reinforced anteriorly by thin, median ridge running nearly all crown length, and
posteriorly by heavy retrorse keel. Posterior teeth inclined backwards into oral
cavity.

Five pairs of gill slits, nearly uniform in length except fifth pair of SIO 87-77,
which is considerably shorter than anteriormost pairs.

Pelvic fins lobate, narrow, moderately long. Anterior margin of anterior lobe
moderately to sharply rounded at tip. Posterior lobe broadly rounded, becom-
ing sharply rounded at posterior tip; inner margin weakly concave to axil.
Claspers of CAS 58604 (immature) stubby, uncalcified, with broadly rounded
tips.

Tail relatively short, less than 43% tl, narrow, tapering gradually to tip. Tail
with paired, continuous lateral folds, about equal in length, originating as ridges
near base of tail, widen distally to folds along ventrolateral surface and terminate
near tail tip. Two small dorsal fins, nearly equal, closely set. Female with no
discernible interdorsal space, male with space of 3 mm. Dorsal fin base
approximately twice as long as vertical height. Anterodorsal margins of both
dorsal fins hyperboloid, terminating as sharply pointed tips; posterior margins
sharply recurved, except second dorsal of female, which has a broadly rounded
posterior margin. Caudal fin smalt, low, its height about 1% of tail length,
formed as narrow, dorsal ridge immediately posterior to second dorsal fin, rising
gradually from about 33% its base length to broadly rounded posterior margin.
Ventral tip of tail with short, low, longitudinal keel.

Dorsal surface of disc and tail completely covered with prickles, skin
especially rough in middorsal area posterior to spiracles. Enlarged thornlets in
malar and alar areas in both specimens (representing both sexes). Rostral area
covered with enlarged thornlets, many of which are greatly enlarged and appear
as small thorns (Figure 1 ) in random pattern about rostral midline, not in distinct
series; five to six principal thornlets with three to four smaller thornlets. One
pair each of preorbital, postorbital and interspiracular thorns, two or three pairs
of scapular thorns. Twenty-four to 29 thorns in continuous row along body and
tail midline. No interdorsal thorns. Tail with row of enlarged thornlets on either
side of median thorns, more prominent anteriorly. Pelvic fins smooth, except for
prickles near posterior tip of posterior lobe. Ventral surface of disc and tail
completely smooth.

Color of dorsal surface of male medium gray-brown, with numerous darker
spots and blotches, especially toward apices of disc and along tail. Whitish
beneath eyes. A conspicuous brown bar across scapular region. Snout, margins
of disc and tip of pelvic fin anterior lobe dark. Dorsal surface of female dark

RECORDS OF DEEP-SEA SKATES 93

chocolate brown; dark spots and blotches present, but less discernible than
those of nnale. Ventral surface of disc same color as dorsal surface, but nnargins
of disc, pelvic fin anterior lobe and ventral surface of tail darker than other
areas. Whitish blotches on snout and upper abdomen, nares, nasal curtain,
mouth, gill slits, and cloacal opening. Female with three moderately large white
interbranchial blotches. Lateral folds of both specimens whitish.

Remarks

Our description of the California specimens of Raja badia agrees in nearly all
respects with Carman's (1899) description of the holotype, with the following
exceptions: (i) the enlarged rostral thornlets do not form "... a couple of
series," but appear in a random pattern about the rostrum. Radiographs reveal
the locations of the largest of these thornlets coincide closely with the
underlying rostral cartilage; (ii) the holotype is considerably smaller than the
California specimens; from Carman's plate it appears to have more prominent
rostral thornlets; (iii) Carman did not report a dorsal pigment pattern, but
merely noted the color to be "chocolate brown," this possibly due to fading
after nine years in alcohol. Both California specimens have distinctly rounded
dark spots and irregular blotches on the tail and a wide brown bar across the
scapular region; (iv) Carman described the teeth as ". . . resembling a pair of
small parallel discs united by a short narrow column . . ." that is the teeth
appeared to him somewhat spool-shaped. We found, on close examination,
however, that the teeth appear mushroom-shaped; they have only one crown
("disc") supported by a conical base which flares out where it attaches to the
dermis.

Owing to its rarity, virtually nothing is known of the life history of this species.
The large head, v/ide mouth, and retrorse teeth suggest this species is capable
of feeding on relatively large, active prey. We did not examine gut contents of
the California specimens, but vertebrae and other calcified material seen in
radiographs of CAS 58604 suggest fish and possibly crustaceans as prey. Sexual
maturity of males occurs at about 900 mm tl, possibly less.

Raja badia is known from six, possibly seven, specimens from the eastern
Pacific (M. Stehmann, pers. comm.; Table 2). Nakaya (1983) published
photographs and brief descriptions of two morphologically similar specimens
(listed as Raja sp.) from off Japan. Ishihara and Ishyiyama (1986) noted these
specimens fit the description of R. hyperborea from the North Atlantic and
Arctic (Stehmann and Blirkel, 1984), but the taxonomic status of these
specimens remains unresolved (M. Stehmann, pers. comm.).

Bathyraja abyssicola (Cilbert, 1896)
(Figure 2)

Diagnosis

A large Bathyraja (to 1350 mm tl); disc bell-shaped; moderately triangular
anteriorly, broadly rounded posteriorly. Disc slightly broader than long; orbit
length equal to interorbital distance; both surfaces of disc and tail covered with
denticles; median nuchal thorns 1-5, separated from continuous row of 21-33
medial thorns on trunk and tail; orbital and scapular thorns absent.

CALIFORNIA FISH AND GAME

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RECORDS OF DEEP-SEA SKATES

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FIGURE 2. Bathyraja abyssicola (Gilbert) . Upper, dorsal view of CAS 58481 . Lower, ventral view
of same specimen. Photos by M. E. Anderson.

96 CALIFORNIA FISH AND CAME

Description

Adult males of B. abyssicola have been described in detail by Gilbert (1896)
and Ishihara and Ishiyama ( 1 985 ) . We provide the follov^ing description of nine
specimens of juveniles and adults of both sexes from off California. Proportional
measurements, as percent tl, are given in Table 3.

Disc somewhat bell-shaped; moderately triangular anteriorly, broadly
rounded posteriorly, slightly broader than long. Greatest disc width in posterior
half of disc, 55.9-65. 5%disc length. No differences in disc shape between sexes
or sizes. Tip of snout moderately produced, acutely rounded. Anterior margins
of disc form less than right angle; gently convex from behind snout tip to about
the level of orbits, becoming weakly to moderately concave, than broadly
rounded to apex. Apices of disc broadly rounded. Posterior margins of disc
form less than right angle; nearly straight to gently rounded, becoming sharply
rounded at posterior tips, then weakly concave to axil. Disc moderately thin,
more dorsoventrally depressed in juveniles than adults.

Head large, length nearly 25% tl. Eyes small, orbit length equal to interorbital
distance, corneal length less than 50% interorbital distance. Spiracle slightly
longer than cornea. Pseudobranchial folds 15-18, more prominent in larger
individuals. Nasal curtain broadly rounded, with weakly developed fimbriae.
Mouth weakly arched, somewhat narrow, 13.6-16.0% disc width. Teeth
homodont, retrorse, in 31-36 rows in upper jaw.

Five pairs of gill slits; four anteriormost nearly equal, posteriormost markedly
shorter.

Pelvic fins moderately elongate, broadly rounded. Anterior lobe with whitish
tip. Posterior lobe broadly rounded to posteriormost tip; inner margin straight to
axil. Claspers of both juvenile and adult males relatively long and thin. Claspers
of SIO 85-68 mature, tips ovoid and bulbous. Left clasper 44.1% tail length;
pseudosiphon 1 10% of proximal clasper length. No dermal denticles on dorsal
surface.

Tail moderately long, narrow, stout anteriorly, tapering gradually to tip.
Paired, narrow lateral folds present; asymmetric and discontinuous. Two
relatively large dorsal fins, nearly equal, closely set, except in CAS 38013
(female), which has interdorsal distance nearly twice the mean. Interdorsal
thorn present in most specimens. Anterodorsal margins of both dorsal fins
hyperboloid, terminating in broadly rounded tips. Posterior margins straight to
weakly rounded. Caudal fin small, low, completely separated from second
dorsal fin (not formed anteriorly as narrow, distinct ridge, as noted for R.
badia). Anterodorsal margin of caudal fin gently rounded, rising gradually to
broadly rounded tip. Posterior margin broadly rounded, extending beyond tail
tip. Ventrally developed caudal fold formed anteriorly as low, fleshy ridge,
widening slightly posteriorly to broadly rounded tip connected to and extending
slightly beyond tail tip.

Dorsal surface of disc and tail completely and evenly covered with denticles,
except on distal margins of disc and around eyes. Adult males with alar hooks
in 3-5 Irregular rows; no malar hooks. Nuchal thorns 3-5, separated from 21-28
median thorns in continuous row along trunk and tail. Scapular thorns absent.
Interdorsal thorn present in eight of nine specimens with intact tails. Single

RECORDS OF DEEP-SEA SKATES 97

specimen without interdorsal thorn, CAS 38013 (male), with extremely short
interdorsal distance (0.3% tl). Tail with two bands of enlarged denticles on
either side of median thorns.

Ventral surface of disc covered with minute denticles except for midsnout
and abdominal region of juveniles. Ventral surface of tail smooth anteriorly,
minute denticles in mid- or posterior regions.

Dorsal surface of pelvic fin anterior lobe smooth in all. Ventral surface
smooth in juveniles, but with prickles proximally in adults. Posterior pelvic fin
lobe covered with prickles in all except at posterior tip.

Dorsal pigmentation generally monotone, uniform; colors of preserved
specimens ranging from light gray to dark gray-brown, with slightly darker distal
margins. Color in life uniform dark chocolate brown. Occasional, small, round
spots of darker pigment occurring randomly on disc. Tip of pelvic fin anterior
lobe whitish.

Ventral surface of disc same color as dorsal or slightly darker; distal margins
of disc and tail darker. Whitish around mouth, posterior edges of labial folds,
tips of pelvic fin anterior lobes, and tips of claspers. Gill slit distal margins
whitish; much darker posterior to gill openings. Whitish around cloacal opening,
surrounded by darker ring. Lateral folds whitish. Males with large, irregular
whitish blotches, often with numerous dark spots, on abdomen; whitish
blotches greatly reduced or, more usually, absent in females.

Remarks

Our description of the California specimens of B. abyssicola agrees in nearly
all respects with that of the holotype (Gilbert, 1896), with the following
exceptions: (i) Gilbert stated, ". . . the greater part of the upper surface of
ventrals . . . naked." We found only the dorsal surfaces of the anterior pelvic
lobes and the posterior tips of the posterior lobes naked; (ii) Gilbert noted, "A
wide lateral fold along either side of tail." We found the lateral fold width to
range 1.0-2.8% its length, and, while qualitative modifiers are certainly
subjective, we characterize the lateral folds as relatively narrow; (iii) Gilbert
also noted the ". . . caudal fold but little higher than the lateral ones, with
which it becomes confluent at tip of tail." We found the lateral folds terminate
posteriorly in advance of the tail tip, whereas the caudal fin (fold) extends
beyond the tail tip; (iv) neither Gilbert nor Ishihara and Ishiyama (1985)
commented on the ventrally developed caudal fold, which was present in all
specimens with intact tails we examined.

Gilbert (1896) did not state the total length of the holotype, which we
calculated from his table of measurements to be 1,350 mm, or approximately
4.5 ft. Jordan and Evermann (1898) noted the length to be ". . . 45 inches
long . . ." This mistake went unnoticed by Garman (1913), Grey (1956; as
1,143 mm), as well as Ishihara and Ishiyama (1985), who also listed it as 1,143
mm. Thus, proportions as percent tl given for the holotype by Ishihara and
Ishiyama (1985; table 1) should be recalculated on the basis of 1,350 mm tl.

Counts for trunk vertebrae and predorsal-caudal vertebrae for USNM 73913
vary considerably from those made for the nine California specimens (Table 3).
Some variation also exists between these specimens and western Pacific B.
abyssicola. HUMZ 78181 differs by having only one nuchal thorn, 31 median

CALIFORNIA FISH AND CAME

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thorns, 42 trunk vertebrae, interorbital distance greater than orbit length,
spiracles as large as orbits, 13-14 pseudobranchial folds, preoral snout length
12.9% TL, dermal denticles on the posterior third of the dorsal surface of the
claspers, the caudal fin developed only dorsally, and a few other measurements
that vary slightly from those we obtained (Ishihara and Ishiyama 1985, H.
Ishihara, pers. comm.). Photographs of this specimen published by Nakaya
(1983) show it to have a greater number of dark spots on the dorsal surface of
the disc and no large irregular whitish blotch on the ventral surface, a feature
found on all males we examined.

Nevertheless, on the basis of comparison of clasper structures between
HUMZ 78181 and the holotype, Ishihara and Ishiyama (1985) concluded the
western Pacific form was conspecific with the holotype from the eastern
Pacific. Our comparison of the left clasper of SIO 85-68 with drawings of the
same of HUMZ 78181 (Ishihara and Ishiyama 1985, fig. 4)supports this
conclusion.

A second western Pacific specimen of B. abyssicola, MTUF 25270, differs
from California specimens in having a higher median thorn count (33) and
lower preoral length (12.4% tl) (H. Ishihara, pers. comm.). Our comparison
of the scapulocoracoid of this specimen with a dorsally dissected scapuloco-
racoid of SIO 71-201, ca. 1,010 mm TL, revealed a similarity in their shapes,
location of the condyles, and size, position, and location of the anteriormost
dorsal openings. The posteriormost dorsal fenestrae differed both in size and
number, however, a condition recognized for Bathyraja species by Ishihara
(pers. comm.).

Little more is known of the life history of B. abyssicola than of R. badia. It also
has been collected in great depths and appears eurybathic (362-2,903 m). Its
large head and retrorse teeth suggest this species is also capable of feeding on
relatively large, active prey, but we cannot corroborate this.

Juveniles are more dorsoventrally depressed than adults. The bases of both
dorsal and caudal fins are comparatively longer in juveniles and the distance
"D1 origin to tip of tail" is longer, indicating ontogenetic decrease in fin size.
Juveniles lack denticles on the abdominal region of the disc and ventral surface
of the pelvic fin anterior lobe.

Sexual maturity of males occurs at about 1,100 mm tl, however, we know of
no specimens in the 750-1,000 mm range which would have enabled us to
make a closer estimate. CAS 38013 (1,191 mm tl) did not have fully calcified
claspers and lacked the alar hooks of mature males.

Bathyraja abyssicola is known from 16 specimens (Table 4), not including an
additional six from the western Pacific reported by Dolganov (1983) from
unspecified localities ranging between Japan and the Bering Sea. It ranges from
west of Bishop Rock, West Cortes Basin, California (LACM 38378-1 ) to off the
Queen Charlotte Islands, British Columbia, in the eastern North Pacific and from
the Bering Sea to off Chosi, Pacific coast of Honshu Island, Japan (MTUF
25270), and possibly Suruga Bay (Tanaka, 1987). As a eurybathic, slope-
dwelling species, its range appears to be continuous from at least California to
Japan.

RECORDS OF DEEP-SEA SKATES

101

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102 CALIFORNIA FISH AND GAME

DISCUSSION

Nearly all known specimens of R. badia and B. abyssicola have been
collected by fisheries research vessels using bottonn trawls (Tables 2 & 4). At
least one specimen of each, however, was collected in a commercial sablefish
trap. Thus, fisheries biologists and commercial fishermen remain the most
important sources for obtaining new specimens to learn more about the
systematics and biology of these fishes, but most investigators are relatively
unfamiliar with California's deep-sea fish fauna. After examining many speci-
mens of each of California's skates, we have devised an updated key to the
adults and subadults of the nine species presently known from California waters,
the first since Miller and Lea's (1972) somewhat dated key.

Only two genera of skates occur in California waters, indeed, in the entire
eastern North Pacific. The so-called "hardnosed" skates of the genus Raja
Linnaeus are characterized by robust, stiff, rostral cartilages and, consequently,
stiff snouts. The so-called "soft-nosed" skates of the genus Bathyraja Ishiyama
are characterized by very slender, usually curved rostral cartilages and,
consequently, pliable snouts. These characters can be reliably observed using
radiography or by dissection of the snout. Another method, which works better
with small specimens, is to hold the snout up to bright light. For several obvious
reasons, these methods are generally impractical for field identification. A more
common method is to simply bend the snout backward. The snout of Bathyraja
species bends readily, that of Raja species only with sufficient effort and is
usually very resistant to much bending. Even this method is not absolutely
reliable, as snouts can be damaged by heavy gear.

Our key uses the presence or absence of orbital thorns as a convenient
additional character for distinguishing the two genera. All Raja presently known
from California waters have orbital thorns and all California Bathyraja do not.
This key is not reliable for skates from outside California, as presence or absence
of orbital thorns is not diagnostic for either genus. It will also be unreliable with
very young individuals, as thorn characteristics are not well expressed in these.
The following references should be consulted for additional information,
illustrations, and terminology: Miller and Lea (1972), Hart (1973), Eschmeyer
et al. (1983), and Stehmann and BiJrkel (1984). Thorn terminology used in the
key is illustrated in Fig. 3.

RECORDS OF DEEP-SEA SKATES

103

FIGURE 3. Composite sketch of dorsal surface of hypothetical skate showing thorn pattern for
identification of California species. Abbreviations: AL, alar thorns (hooks); LTT, lateral
tail thornlets; MA, malar thorns and thornlets; MTR, median thorn row; NU, nuchal
thorns; ORB, orbital thorns; RT, rostral thornlets; SCA, scapular thorns.

Key to Adult and Subadult California Skates

1A. Snout stiff, not easily bent due to stout, broad, tapering rostral cartilage;
orbital thorns present; anteriormost pectoral fin rays falling well short of
rostral tip (genus Raja Linnaeus, 1758) 2

IB. Snout soft and pliable, rostral cartilage slender, orbital thorns absent;
anteriormost pectoral fin rays extending almost to tip of snout (genus
Bathyraja Ishiyama, 1958) 6

2A. Enlarged rostral thornlets present; two or three pairs of scapular spines

present; ventral surface smooth Raja badia Carman, 1899

2B. Enlarged rostral thornlets and scapular spines absent 3

104 CALIFORNIA FISH AND CAME

3A. Pelvic fins very shallowly notched; seismosensory pores on ventral surface
of disc forming distinct right angle distal to gill slits; no lateral tail thornlets
Raja binoculata Cirard, 1854

3B. Pelvic fins deeply notched; ventral seismosensory pores in random pattern
or variously curved lines; lateral tail thornlets present or absent 4

4A. Lateral tail thornlets absent Raja rhina Jordan and Gilbert, 1880

4B. Lateral tail thornlets present 5

5A. Anterior margin of disc nearly straight to slightly convex; median thorn xo\n

not extending anteriorly to vertical through pelvic fin origins

Raja inornata Jordan and Gilbert, 1881
5B. Anterior margin of disc nearly straight to deeply concave; median thorn

row extending anterior to vertical through pelvic origins

Raja stellulata Jordan and Gilbert, 1880

6A. Scapular thorns present Bathyraja interrupta

(Gill and Townsend, 1897)

68. Scapular thorns absent 7

7A. Nuchal thorns 1-5 Bathyraja abyssicola (Gilbert, 1896)

7B. Nuchal thorns absent 8

8A. Ventral surface of disc smooth, except small patches of prickles on snout

and near disc margin; dorsal surface of disc black

Bathyraja trachura (Gilbert, 1892)

8B. Ventral surface of disc covered with prickles; dorsal and ventral surfaces
gray Bathyraja spinosissima (Beebe and Tee-Van, 1941)

CONCLUSIONS

Raja (Amblyraja) badia Carman is added to the California ichthyofauna and
new specimens of Bathyraja abyssicola (Gilbert) are reported and the species
redescribed. This paper is a contribution to the knowledge of their morphology
and distribution. Great individual variation is noted in these skates. The limits of
this variability and, most importantly, determining if it is an expression of
discrete populations, can only be learned by examining many more specimens.
Our key to the California skates includes recently updated zoological nomen-
clature.

ACKNOWLEDGMENTS

We wish to thank the following individuals for their assistance with specimen
loans, advice on skate systematics, and encouragement during the preparation
of this paper: L.J.V. Compagno, H. Ishihara, S. Kato, R.N. Lea, J. McEachran, A.E.
Peden, R.H. Rosenblatt, M. Stehmann, and H.J. Walker, Jr. The following people
also provided assistance in numerous ways: K.A. Bruwelheide, B.S. Eddy, K.E.
Hartel, T.W. Pietsch, J.A. Seigel, S. Smith, D.L. Stein, and D. Woodbury.

The senior author wishes to especially acknowledge the able assistance of his
younger daughter, T.E. Zorzi, who helped clean, preserve and photograph
specimens, and assist in recording measurements.

RECORDS OF DEEP-SEA SKATES 105

LITERATURE CITED

Beebe, W., and J. Tee-Van. 1941. Eastern Pacific expeditions of the New York Zoological Society, 28. Fishes from
the tropical eastern Pacific. Pt. 3. Rays, mantas and chimaeras. Zoologica, 26(26): 245-280.

Clemens, W. A., and C. V. Wilby. 1949. Fishes of the Pacific coast of Canada. Fish. Res. Board Canada, Bull. 68.
368 p.

Dolganov, V. N. 1983 Skates of the family Rajidae from the Pacific coast of North America. Izvest. Tikh.
Nauchno-lssled. Inst. Ryb. Khoz. Okeanogr., 107: 56-72. (In Russian).

Eschmeyer, W. N., E. S. Herald, and H. Hammann. 1983. A field guide to Pacific coast fishes of North America.
Houghton Mifflin Co., Boston. 336 p.

Carman, S. 1899. Reports on an exploration off the west coast of Mexico, Central and South America, and off the
Galapagos Islands, in charge of Alexander Agassiz, by the U. S. Fish Commission steamer "Albatross" during
1891, Lieut. Commander Z. I. Tanner, U. S. N., commanding. 24. The fishes. Mem. Mus. Comp. Zool., 24:
1-431, pis. 1-97.

1913. The Plagiostomia (sharks, skates, and rays). Mem. Mus. Comp. Zool., 36: 1-515, pis. 1-77.

Gilbert, C. H. 1896. The ichthyological collections of the U. S. Fish Commission steamer Albatross during the years
1890 and 1891. Rept. U.S. Comm. Fish & Fish., (19): 393^76.

Grey, M. 1956. The distribution of fishes found below a depth of 2(XX) meters. Fieldiana: Zool., 36(2): 73-337.

Grinols, R. B. 1965. Check-list of the offshore marine fishes occurring in the northeastern Pacific Ocean,
principally off the coasts of British Columbia, Washington, and Oregon. M.S. Thesis, Univ. Washington,
Seattle, 217 p.

Hart, J. L. 1973. Pacific fishes of Canada. Fish. Res. Board Canada, Bull., 180. 740 p.

Hubbs, C.L., and R. Ishiyama. 1968. Methods for the taxonomic study and description of skates (Rajidae). Copeia,
1968(3): 483-491.

Ishihara, H., and R. Ishiyama. 1985. Two new North Pacific skates (Rajidae) and a revised key to Bathyraja in the
area. Jap. J. Ichthyol., 32(2): 143-179.

1 986. Systematics and distribution of the skates of the North Pacific ( Chondrichthyes, Rajoidei ) . Pages

269-280 in; T. Uyeno et al., eds., Indo-Pacific fish biology. Ichthyol. Soc. Japan, Tokyo.

Ishiyama, R., and H. Ishihara. 1977. Five new species of skates of the genus Bathyraja from the western North
Pacific, with reference to their interspecific relationships. Jap. J. Ichthyol., 24(2): 71-90.

Jordan, D. S., and B. W. Evermann. 1896. The fishes of North and Middle America. U. S. Nat. Mus., Bull., 47(1 ):
1-1240.

Leviton, A. E., R. H. Gibbs, Jr., E. Heal, and C. E. Dawson. 1985.

Standards in Herpetology and Ichthyology: Part 1 . Standard symbolic codes for institutional resource collections
in Herpetology and Ichthyology. Copeia, 1985(3): 802-832.

Masuda, H., K. Amaoka, C. Araga, T. Uyeno, and T. Yoshino. 1984. The fishes of the Japanese Archipelago. Tokai
Univ. Press, Tokyo. 450 p.

Miller, D. J., and R. N. Lea. 1972. Guide to the coastal marine fishes of California. Calif. Dept. Fish Game, Fish
Bull. 157. 235 p.

Nakaya, K. 1983. Rajidae, Pages 52-60, 167-171, 220-227, and 310-313 in: K. Amaoka et al., eds.. Fishes from the
north-eastern Sea of Japan and the Okhotsk Sea off Hokkaido. Jap. Fish. Resource Conserv. Assn., Tokyo. 371
P-

Stehmann, M., and D. L. BiJrkel. 1984. Rajidae. Pages 163-196 in: P. J. P. Whitehead et al., eds.. Fishes of the
north-eastern Atlantic and the Mediterranean. UNESCO, Paris 1. 510 p.

Tanaka, S. 1987. A diving in the Suruga Bay by dep-sea submarine "Shinkai 2,000." Jap. Group Elasmobranch
Stud., Rept. 23: 29-31.

Taylor, L. R., Jr. 1972. Apristurus kampae, a new species of scyliorhinid shark from the eastern Pacific Ocean.
Copeia, 1972(1): 71-78.

Wilimovsky, N. J. 1958. Provisional keys to the fishes of Alaska. Fish. Res. Lab., U. S. Fish Wildlife Serv., Juneau.
113 p.

Yves, J., A. E. Peden, and D. E. McAllister. 1981. English, French and scientific names of Pacific fish of Canada.
Brit. Columbia Prov. Mus., Heritage Rec. 13: 51 p.

106 CALIFORNIA FISH AND GAME

Calif. Fish and Came 7 A {2): 1 06- 11 8 1 988

DIFFERENCES IN YIELD, EMIGRATION-TIMING, SIZE, AND

AGE STRUCTURE OF JUVENILE STEELHEAD FROM TWO

SMALL WESTERN WASHINGTON STREAMS'

JOHN J. LOCH, STEVEN A. LEIDER, MARK W. CHILCOTE, RANDY COOPER, and THOM H.

lOHNSON

Fisheries Management Division

Washington Department of Wildlife

600 North Capitol Way

Olympia, Washington 98504

From 1978 through 1984, we examined the yield, emigration-timing, size, and age
structure of juvenile steelhead trout from two small, geographically distinct,
Washington streams. Of the two study streams, one had an allopatric winter-run
steelhead population (Snow Creek), and the other had a sympatric winter- and
summer-run steelhead population (Gobar Creek). Annual smolt yields were greater
in Snow Creek than in Gobar Creek. Mean seven year yields were 1,227 and 331,
respectively. In contrast to Snow Creek, where the proportion of emigrant parr (age
< 1) averaged 20.1%, parr were a dominate proportion (86.1%) of the total
number of emigrants from Gobar Creek. The mean date of outmigration was
significantly different for smolts and parr between streams. Most steelhead smolts
and parr emigrated from Gobar Creek in early May compared to mid-May in Snow
Creek. Steelhead smolt and parr migrating from Snow Creek were larger than Gobar
Creek juvenile steelhead migrants. The age structure of emigrating smolts from
Gobar Creek averaged 15.8% age 1, 76.7% age 2, and 7.5% age 3. in Snow Creek,
migrant smolts were comprised of 5.3% age 1, 86.3% age 2, and 8.4% age 3. The
survival of emigrant parr to the smolt stage is likely related to the availability of
suitable rearing areas in tributary and mainstem reaches. A river system approach
to fishery management and habitat protection is discussed.

INTRODUCTION

In coastal streams and rivers of Washington State, juvenile anadromous
steelhead trout, Salmo gairdneri, undergo a critical life history phase, migration
to the ocean. Information about their downstream migration and age structure
is important in understanding wild steelhead populations. Several researchers
have reported the age structure of emigrating juvenile steelhead from rivers and
streams in British Columbia, Canada (Maher and Larkin 1955, Narver 1969);
Washington (Gudjonsson 1946, Larson and Ward 1954, Loch, Chilcote, and
Leider 1985); Oregon (Wagner, Wallace, and Campbell 1968, Everest 1973);
and California (Shapovalov and Taft 1954). Variations in size and age structure
as they relate to emigration of juvenile rainbow trout have been reported by
Stauffer (1972) and Kwain (1981) for some Great Lakes streams. In the
Columbia River, juvenile salmonid downstream migration timing and age
structure have been reported by Dawley et al.(1980), Dawley et al. (1981 ), and
Loch (1982).

As part of a more comprehensive series of studies by the Washington
Department of Wildlife, we monitored the downstream migration of juvenile
salmonids from two geographically separated streams. One stream had an

Accepted ic Publication November 1987.

MIGRATION CHARACTERISTICS OF JUVENILE STEELHEAD "107

allopatric population of winter-run steelhead, and flowed directly into the
ocean. The second stream had a sympatric population of winter-run and
summer-run steelhead, and flowed into a major tributary of the Columbia River.
Steelhead races are distinguished primarily by their relative sexual maturity at
return and time of freshwater return from the ocean on their spawning migration
(Withler 1966; Leider, Chilcote, and Loch 1986a). The purpose of this study was
to compare downstream migration characteristics of juvenile steelhead from the
two different locations and stream types. Specifically, we examined: (i) yield;
(ii) emigration-timing; and (iii) size and age structure.

Because of the increasing environmental degradation of many stream habitat
areas and the possible reduction of steelhead production, information on
variation in juvenile freshwater life history characteristics associated with
different types of rearing streams is important for the proper management of
wild steelhead populations. Incorporation of this information into present
habitat and harvest management plans may improve the survival rate of juvenile
steelhead rearing in tributary and mainstem complexes, thereby improving
production, and adult return rates.

STUDY AREA
Gobar Creek

Gobar Creek, a tributary of the Kalama River hence the Columbia River, is
located in southwestern Washington (Figure 1). It is 9.6 kilometres (km) in
length and has a natural barrier that prevents steelhead passage to the upper 1.6
km. The creek has a watershed area of approximately 55 km ^. Gobar Creek
averages 8.0 metres (m) in width, has a moderate gradient (10 m/km), well
developed riffle and pool sequences, and few pools deeper than 1.5 m.
September flows average 0.50 m ^/s. Water temperature ranges from 5.4 to
9.7°C with a mean of 7.2°C (April-June). Habitat composition and substrate
range from boulder-rubble-bedrock to cobble in the lower reaches (mouth to
1.6 km); gravel-cobble-rubble in the middle reaches (1.6 km to 5.3 km); and
gravel-cobble to bedrock in the upper reaches (5.3 km to 9.6 km). Correspond-
ing gradients for each longitudinal zone (lower, middle, and upper) are 12.5
m/km, 8.9 m/km, and 8.5 m/km, respectively. Dense deciduous vegetative
cover is found along the banks. Over the course of our study, extensive logging
has occurred throughout the watershed.

Fish species present include resident and anadromous cutthroat trout, Salmo
clarki; winter- and summer-run steelhead trout (Leider et al. 1986a); coho
salmon, Oncorhynchus kisutch; mountain whitefish, Prosopium williamsoni;
Pacific lamprey, Entosphenus tridentatus; torrent sculpin, Cottus rhotheus, and
coastrange sculpin, C. aleuticus.

Snow Creek

Snow Creek enters the head of Discovery Bay on the northeast side of the
Olympic Peninsula (Figure 1 ). The creek has a watershed area of 52 km ^, and
is 16.0 km in length with 10.4 km accessible to steelhead. Snow Creek has a
mean stream width of 5.0 m with few pools deeper than 1.5 m. Stream gradient
is 25 m/km overall and averages 12, 19, and 45 m/km in the lower, middle, and

108

CALIFORNIA FISH AND CAME

FICURE 1. Map showing the location of Cobar Creek and Snow Creek sampling sites,
Washington, 1978-1984.

upper reaches, respectively. Land directly adjacent to the lower area is largely
agricultural with some residential development, whereas the upper watershed
has had limited development except for periodic logging. Typical mean monthly
flows during January and February range from 0.27 to 5.40 m ^/s and is 0.58
m ^/s during April and June. In August flows average 0.12 m ^/s. Mean monthly
water temperatures range from 3.2°C in January to 15.6°C in August and average
lO.B'C during April-June. Habitat composition and substrate is predominantly
riffle-run-pool over gravel in the lower reaches (mouth to 1.6 km); riffle-pool-

MIGRATION CHARACTERISTICS OF JUVENILE STEELHEAD 109

run over gravel-rubble in the mid-reaches (1.6 km to 3.7 km); and cascade-pool
over boulder-rubble-gravel in the upper reaches (5.3 km to 16.0 km). Riparian
vegetation consists mainly of deciduous vegetative cover.

Fish species present are winter-run steelhead; coho salmon; chum salmon, O.
keta; anadromous and resident cutthroat trout; Pacific lamprey; Western brook
lamprey, Lampetra richardsoni; and sculpins, Cottus spp.

METHODS AND MATERIALS
Gobar Creek

From 1978 to 1981, dov^nstream migrants were sampled in Gobar Creek using
a stationary fyke net trap located 500 m above the confluence of Gobar Creek
and the Kalama River (Figure 1 ). The trap was relocated in the spring of 1982
1 km farther upstream following a severe flood that destroyed the previous site
as a trapping location. Sampling was terminated after 1984. Sampling was
conducted two to five nights each week from mid-March to mid-June. From
preliminary diel sampling in 1977, it was determined that few juvenile steelhead
emigrated from Gobar Creek during daylight hours. In some areas, day time
migrations of steelhead smolts have been observed (Chapman 1958). Howev-
er, we believe this was not the case for Gobar Creek to any great extent.
Accordingly, the trap was fished from sunset to sunrise of each sampling night.
Since the trap blocked off the entire stream, we assumed the trap captured
100% of the migrants during the nights of operation. The net measured 1.2
m X 1.2 m at the opening and had 6.0 m X 1.2 m wings with 6.4 mm mesh.

We divided each sampling season into six, two-week intervals. The total
number of Gobar Creek emigrants of each species and age group for each
season was estimated using the following model:

6 aj

N=2va. (2n,)

j=l i=l

where,

N= total estimated number of emigrating juvenile migrants,

Aj= total number of days in the j**^ sampling interval,

aj= number of days actually sampled within the j'^ interval and,

njj= number of individuals captured on the i'*^ night of the j'*^ interval.

Each season, we calculated the weighted average date of outmigration
following methods in Leider, Chilcote, and Loch (1984).

For each sampling night, water temperatures were measured using a pocket
thermometer and recorded.

Summer-run steelhead (hatchery and wild) account for about 83 percent of
all steelhead spawners in Gobar Creek (Leider et al. 1984). Assuming equal
juvenile survival between juvenile emigrant races was equal, Gobar Creek
emigrants might be predominantly summer-run.

All steelhead captured were classified as either smolts or migrant parr based
primarily on coloration and length. Smolts have external body silvering and fin
margin blackening and parr retain their typical freshwater coloration patterns

no CALIFORNIA FISH AND CAME

(visible bar markings; non-silvery) (Loch, Chilcote, and Leider 1985). In
addition, fork lengths (fl of parr were generally less than 110 mm, whereas
smolts were longer. A weekly subsample of scales was collected from
emigrating smolts for later age determination.

Snow Creek

A permanent fish trapping facility was constructed about one kilometre
upstream from the mouth of Snow Creek in 1977 (Figure 1 ). The trap design
enabled capture of fish greater than 300 mm fl year-round. Fish greater than 50
mm FL were captured when screens were installed during the start of the smolt
emigration, in early March. Although this trap has been in operation continu-
ously since its construction, only data from 1978 to 1984 were used for
comparison to Cobar Creek trapping data.

Trapping efficiencies were measured by releasing large (90-150 mm fl)
marked wild coho smolts upstream of the trap and recording the proportion of
marked smolts recaptured. Trapping efficiencies ranged from 90-100%. Total
number of emigrants was calculated as the total number of emigrants captured
corrected by trapping efficiency.

Stream water level was monitored at the Snow Creek site by a Stevens Type
F continuous float gauge. Rating curves were developed by measuring instan-
taneous stream discharge at various gauge levels with a Pygmy gurley meter and
calculating a relationship to predict discharge for various gauge level readings.
Water temperatures were recorded on a continuous reading Weathermeasure
Model T 601 A thermograph.

Captured steelhead were identified to be smolts or parr as described for
Gobar Creek. A subsample of scales was collected from smolts as described for
Gobar Creek.

RESULTS AND DISCUSSION
Yield

Although smolt yield in Gobar Creek was consistently less than in Snow
Creek (Table 1), the opposite relationship was found for steelhead parr
between streams. The mean number of steelhead parr migrants in Gobar Creek
was 2,049 versus 334 in Snow Creek (Table 1 ). Of the total number of juvenile
steelhead smolt and parr emigrating from Gobar Creek, an average of 86.1%
were emigrant parr. In contrast, an average of 20.1% of the juvenile steelhead
leaving Snow Creek were parr (Table 1 ).

TABLE 1. Estimated Number of Wild Downstream Migrant Steelhead from Cobar Creek and Snow
Creek, 1978-1984.

)t'jr

Migrant Croup 1978 1979 1980 1981 1982 1983 1984 Mean
Gobar Creek

Smolt 349 571 301 316 222 465 90 331

Parr 933 3,034 2,201 1,966 1,908 3,323 975 2,049

Snow Creek

Smolt 1,403 892 1,357 1,541 1,734 1,270 1,114 1,330

Parr 207 45 296 895 81 275 538 334

Differences in yield may partially be due to differences in stream gradient.
Stream gradients were substantially lower in Gobar Creek compared to Snow

MIGRATION CHARACTERISTICS OF JUVENILE STEELHEAD ■\ 1 1

Creek. Johnson (1985) found higher steelhead parr densities in mainstem rivers
in western Washington as gradient increased from 2.5 m/km to 30 m/knn. He
suggested that steeper gradients provided a greater abundance of preferred parr
habitat. Similarly, Card and Flittner (1974) suggested that gradients indirectly
affect current pattern, pool to riffle ratios, bottom type, and water temperature,
and influenced the distribution and abundance of fish in a California stream.
However, Hartman and Gill (1968) suggest that gradients alone do not explain
the abundance and distribution of juvenile steelhead within a gradient zone and
that other factors related to environmental and biological processes are
responsible. For example, low summer flows can reduce the potential for
juvenile production within steep gradient zones. As water levels decrease, so
does the living area available to juveniles, thereby increasing competition for
reduced rearing territory and food. In Gobar Creek, a large percentage of
migrants were parr, suggesting rearing territory for fish of that age was limited.
Such juveniles unable to secure a territory may have been forced to relocate
downstream to areas of less competition. In Snow Creek, a similar movement
of juveniles out of rearing areas would necessitate them entering the marine
environment. Chances of survival would be expected to be minimal because
they would be physiologically ill-adapted for ocean life.

Timing

The emigration of Gobar Creek smolts generally began in late March, peaked
by the first week of May, and ended in mid-June. In Snow Creek, downstream
movement of smolts past the trap began in early April, peaked during the
second week of May, and ceased by the end of June (Figure 2). Gobar Creek
smolts emigrated an average of 7 days earlier than Snow Creek smolts (P<0.01;
paired t-Test). Although timing differences for each Gobar Creek age group
were not statistically significant (P>0.05; ANOVA), age 3 smolts usually
moved downstream first, followed by age 2 smolts and then by age 1 smolts. In
Snow Creek all three age groups tended to move downstream within the same
time interval (Figure 2).

Size and age are important factors governing the outmigration timing of
juvenile salmonids. Shapovalov and Taft (1954) observed that larger steelhead
emigrated earlier than smaller smolts in a California stream. Stauffer (1972) and
Kwain ( 1 981 ) documented that older and larger juvenile rainbow trout of some
Great Lakes tributary streams tended to migrate downstream earlier than smaller
and younger juveniles. Likewise for Gobar Creek, the outmigration timing of
steelhead smolts appeared to be related to size and age although for Snow
Creek this was inconsistent.

The downstream migration of Gobar Creek parr began in early March,
peaked within the second week of May, and ended by early June. In Snow
Creek, the outmigration of parr usually began early March, peaked mid-May,
and essentially was complete by the end of June (Figure 3). Gobar Creek parr
emigrated significantly earlier by an average of 9 days than Snow Creek migrant
parr (P < 0.01; paired t-Test).

It is possible that the normal outmigration patterns of juvenile salmonids may
have been altered to some extent by the blocking of all or part of a stream by
sampling devices. Such sampling biases are very difficult to detect and assess.
In the present study, the effect of our sampling gear on juvenile downstream

112

CALIFORNIA FISH AND CAME

<1>
O

50
0
50H

50-

Gobar Creek

Snow Creek

Age 3
(25)

Age 2
(305)

Age I
(60)

Age 3
(800)

March
16-31

Interval

FIGURE 2.

Mean temporal distribution, by age group, of emigrant steelhead smolts from Gobar
Creek and Snow Creek, 1978 through 1984. Sample sizes are in parentheses.

migrant behavior was assumed to be negligible, and results between streams
were comparable without adjustments.

Steelhead from our study streams may have evolved migratory strategies
whereby expression of temporal differences is dependent on the outcome of
tradeoffs between the energetic costs of protracted stream life (increased
freshwater mortality) versus the potential benefits associated with larger size at
outmigration (increased marine survival). If a population has either exceeded
the carrying capacity of its habitat (e.g. over seeding) or had its habitat altered

MIGRATION CHARACTERISTICS OF JUVENILE STEELHEAD

113

10-

O Gobor Creek

A Snow Creek

^ — ^^^^^^

(1978-1984)

^^"^

""■"^-A

^"^^^■-v.,^^^

^^^^ A A

16-

^J\

12-

— -^^[^

c •*-

— ■

S 2'

S Q.

L 8-

^^rrrm^^S^

Parr

80-

0 14,343

60-

^^2084

40-

(^ ^^ n

Q-

20-

r\ /-.--■'

""^'i^^^ ^

8 ^-—

— ! 1 1

1 '

March
16-31

April
1-15

April
16-30

Interval

May
1-15

May
16-31

June
I- 15

FIGURE 3.

Mean temporal distribution of emigrant steelhead parr, water flow (Snow Creek), and
water temperature by two week intervals for Gobar Creek and Snow Creek, 1978
through 1984.

(e.g. poor logging practices), freshwater mortality would be expected to
increase. The relocation of parr to downstream areas may provide an adaptive
mechanism to reduce freshwater mortality and provide the greatest possible
survival of juveniles from each generation. This might be the case for Gobar
Creek, where habitat and gradients may be more conducive to fry rearing than
for parr rearing. In contrast, delayed emigration may provide more time for
growth resulting in greater smolt-to-adult survival rates.

The timing of marine entrance by smolts migrating from Gobar Creek and
Snow Creek may be similar. Trapped Snow Creek smolts must travel down-
stream a distance of only one kilometre before entering the saltwater at
Discovery Bay, therefore peak marine entrance probably occurs near the time
of peak trapping (mid-May). Gobar Creek smolts, however, must migrate 31
km to the confluence of the Kalama River and the Columbia River, and then
another 135 km to the ocean. The seaward migration of steelhead smolts into

114 CALIFORNIA FISH AND CAME

the lower Columbia River estuary peaks about the second week of May
(Dawley et al. 1980, Dawley et al. 1981, Loch 1982). Dawley et al. (1981)
estimated the average downstream movement rate of juvenile steelhead in the
Columbia River to be 27 km/day. Smolts from Gobar Creek would have had to
travel downstream approximately 21 km/day to have a similar marine entry
time to that of Snow Creek smolts. This migration rate would compare favorably
with that estimated by Dawley et al. (1981).

Environmental factors may also have influenced the downstream migration of
juvenile steelhead in our study streams. Temperature affects many aspects of
the smolting process, including the time at which smolts emigrate to the ocean
(Wedemeyer et al. 1980, Schreck 1982). The downstream movement of Snow
Creek steelhead migrants appears to be related to decreasing monthly water
flow and increasing water temperature (Figure 3). However, substantial
numbers of parr and smolts commonly emigrated during freshets. No flow
information was available for Gobar Creek. Downstream movement, however,
appeared to be associated with increasing water temperature (Figure 3).
Solomon (1982) concluded that the emigration of juvenile Atlantic salmon, 5.
salar, was an active process dependent on the physiological state of juveniles as
stimulated by environmental factors such as water temperature. Although
Bjornn (1971), while working with photoperiod, found no direct relationship
between timing of emigrating subyearling steelhead and increasing water
temperature in an Idaho stream, he suggested that temperature may indirectly
influence their movement. Wedemeyer et al. (1980) reported photoperiod
does coordinate the physiological process of smoltification. However, water
temperature acts as the controlling factor determining the rate of smoltification.

Size and Age

Mean lengths of smolts and parr were not the same between streams studied.
Mean lengths of steelhead smolts in each age group were longer in Snow Creek
than in Gobar Creek (Table 2). These differences were significant for age 3
smolts (P < 0.05; t-Test), and for the mean length of all smolts combined
between Gobar Creek (156 mm fl; range 90 — 236 mm fl) and Snow Creek
(165 mm FL; range 110 — 295 mm fl) (P < 0.01; t-Test). The mean length of
Gobar Creek emigrant parr was significantly less (P < 0.05; t-Test) than Snow
Creek emigrant parr. Mean length of emigrant parr in Gobar Creek was 86 mm
fl (range 50 — 150 mm fl), whereas Snow Creek parr averaged 105 mm fl
(range 76 — 140 mm fl) (Figure 4). Differences in sub-sampling procedures,
growth rates, stream-specific age structures or brood survival rates may have
produced these inequities.

Most steelhead smolts emigrated at age 2 in both Gobar Creek and Snow
Creek. However, the mean percentages of age 1 and age 3 smolts differed
between locations (Table 2). In other studies of winter-run steelhead, Gud-
jonsson (1946), Chapman (1958) and Wagner, Wallace, and Campbell (1963)
also reported a predominance of age 2 steelhead smolts and a percentage of age
3 smolts at least twice that of the age 1 smolts (Table 2).

Since age at smoltification can be size (growth) related (Hoar 1976), the age
composition differences we observed between Gobar Creek and Snow Creek
may reflect differential rearing conditions and growth rates. Differences in age
structure may also be associated with the presence of summer-run fish.

MIGRATION CHARACTERISTICS OF JUVENILE STEELHEAD

115

Summer-run steelhead typically spawn at least one month before winter-run
steelhead in Gobar Creek (Leider et al. 1984). Their young will probably
emerge from the gravel earlier than winter-run steelhead. Therefore, summer-
run steelhead may produce offspring with a relative size difference that persist
to the smolt stage.

It is unlikely that many parr leaving Gobar Creek in the spring immigrated
back into the creek during the fall-winter period. Although immigration of
steelhead juveniles can contribute substantially to the number of parr and
smolts emigrating from tributaries the following spring (Bustard and Narver
1975, Cederholm and Scarlett 1982), this occurrence has been shown to be
minimal in Gobar Creek (Leider et al. 1986b).

TABLE 2. Comparison of Mean Smolt

Age
Stream (yr.)

Babiner, B.C 1

4
Chilliwack R., B.C 1

3
Minter Ck., Washington 1

3
Hoh R., Washington 1

3
Snow Ck., Washington 1

3
Gobar Ck., Washington 1

3
Kalama R., Washington 1

3
Alsea R., Oregon 1

3
Rogue R., Oregon 1

3
Waddell Ck., California 1

* W = Winter-run; S = Summer-run
''Backcalculated from scales sampled from

Age Data for Steelhead

in Several West Coast Streams.

Mean

Length

(mm)

Percent

Race''

Data Source

—

0.0

Narver (1969)"

—

2.0

—

82.0

—

15.0

Ill

2.0

Maher and Larkin (1^

165

62.1

200

35.4

—

3.0

Gudjonsson (1946)

—

85.0

—

12.0

—

3.5

Larson & Ward (195-1

—

89.9

—

7.4

132

5.3

This study

162

86.3

195

8.4

128

15.8

W/S

This study

159

76.7

178

7.5

142

6.1

W/S

Lochetal. (1985)

161

80.6

172

13.3

—

5.0

Chapman (1958)

—

82.0
13.0

—

1.0

Wagner etal. (1968)

—

87.0

—

12.0

—

6.0

Everest (1973) "

—

70.0

—

23.0

—

10.1

Withler (1966)''

—

72.3

—

16.7

—

0.9

mature adults

116

CALIFORNIA FISH AND GAME

280-

210
175
I40H
105

70H

x = 86

Gobar Creek

N = l6IOParr E
N = 493 Smolts □

Snow Creek

x=l05

N = 833 Parr
N=I320 Smolts

150 175 200 225 250 275 300

Length (mm)

FIGURE 4. Length frequency histogrann of migrant steelhead smolts and parr from Gobar Creek
and Snow Creek, 1978 througfi 1984. Black area represents overlap in length
frequency between smolts and parr.

Management Implication

In practical terms, simply enumerating tributary smolt run sizes may not give
an accurate indication of that stream's relative ability to produce anadromous
fish. Migrant parr may be a major part of the total emigration from a tributary
and a substantial proportion may survive to become smolts. If these fish are

MIGRATION CHARACTERISTICS OF JUVENILE STEELHEAD 1 1 7

overlooked, then the total smolt contribution from a specific tributary may be
underestimated. In Gobar Creek, most of the emigrant parr which survived to
become smolts are believed to have reared either within the mainstem Kalama
River or in some other lower Kalama River tributary (Leider, Chilcote, and Loch
1986b). Tredger (1980) suggested that 69% of the steel head smolt yield from
a tributary in a British Columbia river system may have been pre-smolt
emigrants to mainstem areas. In contrast, substantial survival of emigrant parr
from Snow Creek is doubtful because of the limited downstream habitat and
direct encounter with the marine environment prior to physiological readiness.
This is supported by the observation that few adults returning to Snow Creek
had lived only one year in freshwater as juveniles (Washington Department of
Wildlife, unpublished report).

Further attention should be given to the interactions of salmonids in
tributary-mainstem complexes. There is a need for a river system approach to
fishery management and habitat protection since the same steelhead juvenile
may use both mainstem and tributary areas during freshwater life cycle.

ACKNOWLEDGMENTS

We are indebted to many individuals for their time spent collecting and
recording Gobar Creek field data. Special thanks to J. Tipping, S. Irvin, R. Jones,
j. Little, B. Leiand, and T. Enyeart. The contributions of B. Crawford in the early
years of our study are gratefully acknowledged. At Snow Creek, J. Tagart, H.
Michael, and S. Elle contributed to the experimental design and data collection.

Financial support for work conducted in Gobar Creek was provided by the
National Marine Fisheries Service, United States National Oceanic and Atmo-
spheric Administration. Financial support for work conducted on Snow Creek
was provided by the U.S. Fish and Wildlife Service (Anadromous Fish Act
funds) and Washington Department of Wildlife.

LITERATURE CITED

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flow, cover, and population density. Am. Fish. Soc, Trans., 100: 423—437

Bustard, D.R., and D.W. Narver. 1975. Aspects of the winter ecology of juvenile echo salmon (Oncorhynchus

kisutch) and steelhead trout (Salmo gairdneri). ). Can. Fish. Res. Board, 32:667-680
Cederholm, C.|., and W.J. Scarlett. 1981. Seasonal immigrations of juvenile salmonids into four small tributaries

of the Clearwater River, Washington, 1977-1981. In E.L. Brannon and E.O. Salo [ed] Salmon and trout

migratory behavior symposium. School of Fisheries, University of Washington, Seattle, Washington. June

1981. p. 98-110.
Chapman, D.W. 1958. Studies on the life history of the Alsea River steelhead. |. Wildl. Manage. 22 (2) :1 23-1 34.
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118 CALIFORNIA FISH AND GAME

Cudjonsson, T.V. 1946. Age and body length at the time of seaward migration of immature steelhead trout in
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Hart, J.L. 1973. Pacific fishes of Canada. Can. Fish. Res. Board Bull. 180.

Hartman, C.F. and C.A. Gill. 1968. Distribution of juvenile steelhead and cutthroat trout (Salmo gairdneri and
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Kwain, Wen-Hwa. 1981. Population dynamics and exploration of rainbow trout in Stokey Creek, eastern Lake
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Larson, R. W. and J. W. Ward. 1954. Management of steelhead trout in the state of Washington. Am. Fish. Soc,
Trans., 84: 261-274.

Leider, S. A., M. W. Chilcote, and J.|. Loch. 1984. Spawning characteristics of sympatric populations of steelhead
trout (Salmo gairdneri): evidence for partial reproductive isolation. J. Can. Fish. Aquat. Sci., 41: 1454-1462.

Leider, S. A., M. W. Chilcote, and J.). Loch. 1986a. Comparative life history characteristics of hatchery and wild
steelhead trout (Salmo gairdneri) of summer and winter races in the Kalama River, Washington. ). Can. Fish.
Aquatic Sci., 43(7): 1398-1409.

Leider, S. A., M. W. Chilcote, and ).). Loch. 1986b. Movement and survival of pre-smolt steelhead trout in a
tributary and mainstem of a Washington river system. North Am. Fish. Manage., 6: 526-531.

Loch, ). j. 1982. Juvenile and adult steelhead and sea-run cutthroat trout within the Columbia River estuary, 1980.
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migrant studies. Fish. Mgmt. Div. Rept. 85-12. Washington Dept. Game, Olympia, Wa., USA.

Maher, F. P. and P. A. Larkin. 1955. Life history of the steelhead trout of the Chilliwack River, British Columbia.
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Narver, D. W. 1969. Age and size of steelhead trout in the Babine River, British Columbia. J. Can. Fish. Res. Board,
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Shapovalov, L. and A. C. Taft. 1954. The life histories of the steelhead rainbow trout, Salmo gairdneri, and silver
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Fisheries, University of Washington, Seattle, Wa, USA. 196-202 pp.
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Tredger, C. D. 1980. Carrying capacity and theoretical steelhead smolt yield from Nuaitch Creek, Nicola River
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ALLOZYME VARIATION IN CALIFORNIA HALIBUT 119

Calif. Fish and Game 74 ( 2 ): 1 1 9-1 27 1 988

ALLOZYME VARIATION IN THE CALIFORNIA HALIBUT,
PARAUCHTHYS CAUFORNICUS '

DENNIS HEDCECOCK
Bodega Marine Laboratory

P.O. Box 247
Bodega Bay, CA 94923

and

DEVIN M. BARTLEY

Department of Aninnal Science

University of California, Davis

Davis, CA 95616

Adult California halibut, Paralichthys californicus, collected from the vicinity of
Marina del Rey, Los Angeles, and juveniles collected from Mission Bay, San Diego,
were surveyed electrophoretically for genetically encoded protein variation. One-
fourth of the 38 protein-coding loci proved to be polymorphic and on average an
individual was heterozygous at 5.2% of the loci; these levels of genetic variation are
typical of flatfishes. Discovery of marked divergences between the two samples in
allelic frequencies at two loci is surprising, given the presumed dispersal potential
of the pelagic larvae of this species. Alternative hypotheses to explain this result are
testable. That the collection of juveniles appears not to be a sample of genotypes
from a randomly mating population calls attention to the importance of under-
standing the process of recruitment in interpreting both these particular results and
the impact of hatchery enhancement efforts.

INTRODUCTION

Legislation (AB1414) in 1984 created the Ocean Resources Enhancement
and Hatchery Program within the California Department of Fish and Game for
the purpose of examing the feasibility of enhancing populations of white
seabass, Atractoscion nobilis, and California halibut, Paralichthys californicus.
Under this program, a project was undertaken to examine whether genetically
coded enzyme polymorphisms might be useful in describing the structures of
natural populations of these species and whether such electrophoretically
detectable enzyme variants might serve as genetic tags of hatchery-reared
stocks. The amount of enzyme variation uncovered in the preliminary study of
California halibut suggests that gel electrophoresis could be useful on both
counts for this species. Moreover, our discovery of substantial variation
between two populations within the southern California Bight suggests that the
natural population of California halibut in this region is subdivided. The cause of
this subdivision is problematical given what is known of the life history of this
species.

The California halibut is distributed in the near shore from northern
Washington to southern Baja California, being particularly concentrated in the
southern California Bight region (Frey 1971, Methot 1983). Spawning, following
an onshore migration of adults (Clark 1931 ), takes place from January through
October with slight peaks in spring and possibly fall. Pelagic eggs and larvae
occur primarily inshore (Ahlstrom and Moser 1975, Gruber, Ahlstrom and

' Accepted for publication November 1987.

120 CALIFORNIA FISH AND GAME

Mullin 1982). Barnett et al. (1984) suggest that larvae may exert some control
over their movements inasmuch as older larvae appear to be more concen-
trated in the nearshore zone than younger larvae. Nevertheless, as pelagic larval
development requires 20 to 30 days, there appears ample opportunity for
considerable dispersal before the 9-10 mm juvenile recruits to the benthos of
bays or estuaries v^hich are the primary nursery habitats (Haaker 1975,
Plummer, DeMartini and Roberts 1983). Except for offshore emigration from
these embayments upon reaching sexual maturity, juveniles and small adults are
remarkably sedentary as demonstrated by mark and recapture studies (Frey
1971, Haaker 1975). Despite these sedentary habits, however, the protracted
spawning season, the dispersal potential of pelagic eggs and larvae, and the long
distance dispersal exhibited by some large adults (Frey 1971) suggest that
natural populations of California halibut ought to be well mixed at least
throughout the southern California Bight.

MATERIALS AND METHODS

Samples of California halibut were obtained from two sources: (i) Mission
Bay (MIS), San Diego, CA., in October, 1985 (N = 30) and (ii) a halibut derby
held at Marina del Rey (MAR), Los Angeles, CA., in April, 1986 (N = 90). The
first sample comprised juvenile fish ranging in size from approximately 10 to 22
cm total length which were taken in trawls, frozen immediately in an ultracold
freezer and later transported to the Bodega Marine Laboratory where they were
stored at —70" C The second sample consisted of tissue samples dissected from
derby catches that ranged in size from 41 to 92.5 cm standard length. These
tissue samples were kept on ice during the derby, then frozen at —20° C for
transport to the Bodega Marine Laboratory where they were stored at —70° C
until processing for electrophoretic analysis.

Tissues dissected for electrophoretic analyses were eye, heart, kidney, liver
and muscle. The day before electrophoresis, whole frozen juvenile fish and
derby specimens were slowly thawed. Tissues were dissected from the juvenile
fish, and both these and the derby specimens were then homegenized in 0.5M
Tris-HCl, pH 7.1 and re-frozen overnight in covered plastic well-trays at —70°
C On the day of electrophoresis, samples were allowed to thaw slowly on ice.

Methods for horizontal starch-gel electrophoresis, protein assays and genetic
interpretation of zymograms were substantially the same as those described by
Ayala et al. (1973) and Tracey et al. (1975). The protocol used to separate and
resolve 21 enzymes and proteins is summarized in Table 1. Proteins are referred
to by the capitalized abbreviations given in Table 1, loci by these same
abbreviations italicized in upper and lower case with numerical suffixes
denoting isozymes in order of increasing anodal migration, and alleles by
italicized numerals that express absolute differences in millimeters of electro-
phoretic separation between variants and the most common electromorphs
observed for each protein. Alleles encoding common electromorphs are
arbitrarily designated 100. Specimens from both population samples were
included in every electrophoretic run so that repeated comparisons of the
relative mobilities of their allozymes could be made.

ALLOZYME VARIATION IN CALIFORNIA HALIBUT

121

Number

Buffer'

Tissue ^

of Loci

H,M

A,E

L,K + M

A,E

M,L

E,K

L,H

E + H + M

A,E

H + M

38 Loci

TABLE 1. Enzymes and Proteins Resolved in an Electrophoretic Survey of Gene-Protein Variation in the
California Halibut.

Enzyme or protein E.C. No.

aconitate hydratase (ACON) 4.2.1.3

aspartate aminotransferase ( AAT) 2.6.1 .1

creatine kinase (CK) 2.7.3.2

esterase (EST) 3.1.1.1

fructose biphosphatase (FBP) 3.1.3.11

fumarate hydratase (FUM) 4.2.1.2

glucose-6-phosphate isomerase (GPI) 5.3.1.9

glyceraldehyde-phosphate dehydrogenase (GAPDH) .. 1.2.1.12

isocitrate dehydrogenase (IDH) 1.1.1.42

lactate dehydrogenase (LDH) 1.1.1.27

malate dehydrogenase (MDH) 1.1.1.37

peptidase (PEP)

L-glycyl-L-leucine (GL) 3.4.13.11

L-leucyl-L-glycyl-L-glycine (LGG) 3.4.13.11

L-phenylalanyl-L-proiine (PP) 3.4.13.9

phosphoglucomutase (PGM) 2.7.5.1

phosphogluconate dehydrogenase (PGDN) 1.1.1.44

protein (PROT)

purine nucleoside phosphorylase (PNP) 2.4.2.1

superoxide dismutase (SOD) 1.15.1.1

xanthine dehydrogenase (XDH) 1.1.1.204

xylulose reductase (XRD) 1.1.1.10

TOTALS: 21 Enzymes or Proteins

' Buffers A, B, C and D are given by Tracey et al. (1975); buffer E is the amino-propylmorpholine citrate system

of Clayton and Tretiak (1972).
^ Tissues: E = eye, H = heart, L = liver, K = kidney, M = skeletal muscle.

Single-individual genotypes were re-coded as alphabetical characters and
submitted to the BIOSYS-1 program of Swofford and Selander (1981) for
calculations of allelic frequencies, average proportions of heterozygous individ-
uals per locus (observed, Hg , and expected [unbiased estimate of Nei (1978)]
/-/g.), proportions of loci polymorphic {P, where a locus is considered
polymorphic if the frequency of the most common allele does not exceed
0.99), goodness-of-fit tests to Hardy- Weinberg-Castle equilibrium genotypic
proportions using Levene's (1949) correction for small sample size, f-statistics
and Nei's (1978) unbiased measure of genetic similarity. Log-likelihood ratio
(C") tests of differences in allelic frequencies between the two population
samples were calculated from absolute frequencies after appropriate pooling of
rare alleles.

RESULTS

A total of 38 discrete zones of activity or staining are resolved on starch-gel
zymograms assayed for the 21 proteins listed in Table 1. Of these zones, 23 are
each represented by a single band in all of the fish examined (CK-1, CK-3,
EST-1, FBP, FUM, GAPDH, IDH, LDH-1, LDH-3, PEP-GL, PGDH, PGM-3, nine
PROTs, SOD and XRD); each of these proteins is inferred to be encoded by a
single, monomorphic locus.

The remaining 15 proteins (ACON, AAT, CK-2, EST-5, GPI-1 and -2, LDH-2,
MDH-1 and -2, PEP-LGG, PEP-PP, PGM-1 and -2, PNP and XDH) exhibit
electrophoretic variation in at least one individual. Phenotypes of presumptive
heterozygotes at the loci inferred to encode these proteins generally conform to

122 CALIFORNIA FISH AND CAME

those expected on the basis of known enzyme subunit structures (Harris and
Hopkinson 1976, Ruth and Wold 1976, Koehn and Eanes 1978). In particular,
phenotypes for AAT, GPI, MDH, PEP, and PGM and their genetic interpreta-
tions are substantially as described by Grant et al. (1983) for yellowfin sole,
Limanda aspera, and by Grant, Teel and Kobayashi (1984) for Pacific halibut,
Hippoglossus stenolepis. Relative allelic frequencies, heterozygosities and
sample sizes for the loci encoding these polymorphic enzymes are presented
for each of the two populations sampled (Table 2).

Three measures of genetic variation are computed from the allelic frequency
data for each of the two populations: average number of alleles per locus,
proportion of loci polymorphic, and average proportion of loci heretorozygous
per individual (Table 3). The two populations appear to be significantly
different for the first measure. Mission Bay having only 1.3 ± 0.1 alleles per
locus vs. 1.7 ± 0.2 for the Marina del Rey sample. A Mest for paired
comparisons of the numbers of alleles at the 15 polymorphic loci yields t =
2.236, 14 d.f., p < 0.05. Except, however, for the Xdh locus, which is
represented by nine alleles in MAR vs. only three alleles in MIS, the difference
in numbers of alleles between the two population samples is attributable to rare
alleles in the larger MAR sample. Eliminating alleles that have a frequency of
0.01 or less in the MAR sample, the paired comparisons test yields a
nonsignificant t = 1.169.

The two populations are each polymorphic for about one-fourth of the loci
surveyed in this study [P — 0.24 and 0.26 for MIS and MAR, respectively), but
they share polymorphisms at only six loci {Est-5, Ldh-2, Mdh-2, Pgm-1, Pgm-2
and Xdh). The MIS sample is polymorphic at three loci that are monomorphic
in MAR {Aat, Mdh-1, and Pnp), while the MAR sample is polymorphic for four
loci that are monomorphic in MIS {Aeon, Gpi-1, Gpi-2 and Pep-pp). {Ck-2 and
Pep-/gg each have one rare allele in the MAR sample and are thus not counted
as polymorphic under the definition adopted.)

Sampling error for average heterozygosity is less sensitive to the numbers of
individuals studies than to the number of loci surveyed (Nei, 1978). The two
populations are not significantly different for H^ or H^ (0.046 vs. 0.058 for MIS
and MAR, respectively; Table 3). As further confirmation that the MIS sample
does not have less heterozygosity than the MAR sample, a paired Mest of
single-locus expected heterozygosity values (transformed by s\n^\/H) for the
15 polymorphic loci yields a nonsignificant t = -0.94 (14 d.f., 0.3 < p <0.4).
Averaged over all individuals from both populations, heterozygosity in the
California halibut is 5.2%.

Sample sizes and levels of variation at six of the eight polymorphic loci in the
MIS sample are too low to permit goodness-of-fit tests between observed
phenotypic proportions and those expected under random mating. For the
remaining two loci, Pgm-2 and Xdh, alleles were pooled into common ( fOO)
and rare allelic classes; x^ tests (1 d.f.) show agreement between observed and
expected phenotypic proportions for PGM-2 (x^ = 0.001, p = 0.97), but a
significant departure for XDH (x^ = 12.81, p < 0.001 ). Wright's fixation index
{F,s) is negative for eight of nine polymorphic loci ( heterozygote excess) but
is significantly positive for the Xdh locus (heterozygote deficiency). For the

ALLOZYME VARIATION IN CALIFORNIA HALIBUT

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Marina del Rey sample, goodness-of-fit tests are possible for Est-5 (x^ = 1-52,
1 d.f., p = 0.22), Pgm-2 (following pooling into common and rare allelic
classes, x^ = 001, 1 d.f., p = 0.92) and Xdh (with pooling, x^ = 0.05, 1 d.f.,
p = 0.83). Inspection of observed and expected phenotypic frequencies at the
remaining nine polymorphic loci in this sample reveals close agreement, with
fixation indices ranging from —0.053 to 0.066. To summarize, with the single
exception oi the Xdh locus in the MIS sample, observed phenotypic porportions
conform to those expected under random mating within California halibut
populations.

Table 3. Genetic Variability at 38 Loci in Two Samples of California Halibut. See Text for Definitions of
Genetic Statistics. Sample Sizes per Locus Are Average Numbers of Individuals. Values in
Parentheses Are Standard Errors.

Population
Mission Bay

Marina del Rey .

Mean Sample

Mean No.

Percentage

Size per

of Alleles

of Loci

Mean Heterozygosity

Locus

per Locus

Polymorphic

Obs. Exp

28.0

1.29

23.7

0.046 0.046

(0.7)

(0.1)

(0.019) (0.019)

82.8

1.68

26.3

0.058 0.058

(3.0)

(0.2)

(0.026) (0.027)

The genetic similarity of the Mission Bay and Marina del Rey population
samples averaged over all 38 allozyme- and protein-coding loci is high, with
Nei's (1978) unbiased /=0.985. This overall similarity, however, belies sub-
stantial divergences of allelic frequencies at two loci, Est-5 and Xdh (Table 2).
Wright's measure of standardized allelic frequency variance, the ratio of
observed variance between localities to maximum variance for the mean allelic
frequencies at a locus, is 0.134 and 0.197 for the £5N5 and Xdh loci, respectively.
For the remaining 13 polymorphic loci, F^r ranges from 0.0 to 0.014, with an
average of only 0.002 (mean calculated using angular transformed values). Log
likelihood ratio tests of the independence of allelic frequency and locality are
possible at the six loci polymorphic in both populations. Not surprisingly, the G
values for Est-5 (24.87, 1 d.f.) and Xdh (126.80, 2 d.f.) are highly significant, p
< 0.001 for both tests. Allelic frequencies at the Mdh-2 locus are also
significantly dependent upon locality (C"=5.03, 1 d.f., p <0.05), even though
FsT^or this locus is only 0.014. Allelic frequencies at the Ldh-2, Pgm-1 and Pgm-2
loci are independent of locality.

DISCUSSION

Electrophoretic separation and assay of soluble enzymes and proteins from
tissues of the California halibut reveals substantial genetic variation. One-fourth
of the 38 proteins studied are polymorphic, and the average individual is
heterozygous at 5.2% of these loci. These results may be compared with data
compiled by Smith and Fujio (1982) from published and unpublished electro-
phoretic studies of 29 species of flatfishes. Because general proteins are highly
conservative in fishes, particularly in the Pleuronectiformes, these authors
recommend using an average heterozygosity based only on enzyme-coding loci
in making comparisons among species that have been assayed for varying
numbers of protein-coding loci. For the California halibut, average observed
heterozygosity is 6.8% over 29 enzyme-coding loci. From Smith and Fujio's
(1982) Table 1 we calculate, using angular transformation, that average

ALLOZYME VARIATION IN CALIFORNIA HALIBUT 125

observed enzyme heterozygosity for 29 flatfishes is 8.1% with a 95%
confidence range from 5.1% to 9.8%. Thus, the California halibut has a level of
genetic diversity that is typical of flatfishes. This abundant genetic variation
should prove useful in the management of California halibut hatcheries and in
the unambiguous, genetic tagging of hatchery releases (Hedgecock 1977).

The surprising result of this study is the marked divergence of allelic
frequencies at the Est-5 and Xdh loci between localities separated by a distance
of only about 200 km. This geographic differentiation contrasts sharply with the
homogeneity observed over distances of thousands of kilometers in other
flatfish species (Grant et al. 1983, 1984) and marine fishes in general
(Gyllensten 1985). Although formal genetic studies have not been made, we
are confident of our genetic interpretations of these enzyme polymorphisms for
two reasons: (1 ) The phenotypes or zymogram patterns themselves are similar
to those shown to be under genetic control in other species; and (2) there is
good agreement of observed and expected phenotypic frequencies in the large
sample of adult fish from Marina del Rey.

Assuming, then, that these two enzyme polymorphisms are indeed geneti-
cally determined, what factors might account for the divergence of allelic
frequencies between the two localities sampled? Four alternative, but not
mutually exclusive, hypotheses require further testing:

(i) Genetic differences between these conspecific populations have accu-
mulated by random sampling processes (genetic drift) in the absence of strong
selection and gene flow (Wright 1931 ). This seems unlikely given the dispersal
potential of the pelagic larvae, but Burton (1983) and Hedgecock (1986) have
argued that actual gene flow cannot be inferred from presumed dispersal
potential of pelagic larvae.

(ii) The genetic differences are historical in origin, and the California halibut
population of the southern California Bight has not yet returned to the
homogeneous, equilibrium expected with large population sizes and high gene
flow.

(iii) The genetic differences are the result of diversifying selection acting on
the loci in question or upon closely linked loci. Transplantation or hatchery
release experiments might provide critical data on the survival of alternative
genotypes in different localities. If the genetic differences are adaptive, hatchery
enhancement efforts should match released genotypes to environments in order
to increase the chances of success and possibly to avoid compromising the
genetic adaptations of natural stocks.

(iv) The genetic differences are the result of sampling different stages in the
life cycle of the organism. We have compared juveniles from Mission Bay with
adults from Marina del Rey. Were those juveniles representative of the adult
halibut population in the San Diego area? If the juveniles were representative of
the adult population, then we are left with the three hypotheses above to
explain the differentiation of adult halibut populations. There is indication in our
data, however, that the juvenile population on the Mission Bay nursery ground
may have represented only a small sample of the reproductive output of the
adult population. The only significant departure from randomly mating pheno-
typic proportions detected in this study was the distribution of Xdh genotypes
in the MIS sample. Moreover, there is a highly significant, non-random
association of genotypes between the Est-5 and Xdh loci in the Mission Bay

126

CALIFORNIA FISH AND CAME

sample (6" = 21.7, 1 d.f., p < 0.001; Table 4A), but not in the Marina del Rey
sample {G = 8.22, 4d.f., 0.1 > p > 0.05; Table 4B). A parsimonious explana-
tion for these results is that the juveniles collected from Mission Bay may have
represented a limited number of sibling groups.

TABLE 4. Associations of Genotypes at the Est-S and Xdh Loci in Samples of California Halibut from (A)
Mission Bay, California, and (B) Marina del Rey, California.

A. Mission Bay Est-5 genotypes

^oT? genotypes 100/103 103/103 totals

100/100 1 19 20

95/95,97/97,95/97,95/100 8 1 9

totals 9 20 29

G = 21.7, 1 d.f.

B. Marina del Rey f5^5 genotypes

A-c/y? genotypes 100/100 100/103 103/103 totals

95/95 112 4

95lr\on-95 6 15 8 29

mn-95lnon-95 12 27 3 42

totals 19 43 13 75

G = 8.22, 4 d.f.

Further electrophoretic study of California halibut populations in the southern
California Bight region are clearly needed to distinguish among the four
explanations of our preliminary results. The intriguing suggestion that familial
structure may be detectable among the juveniles on nursery grounds holds
considerable promise for detailed studies of recruitment processes in this
economically important species.

ACKNOWLEDGMENTS

This work was supported by a grant from the California Department of Fish
and Game to G. A. E. Gall and D. Hedgecock, UC Davis, Department of Animal
Science. We thank S. Caddell, Los Angeles County Museum of Natural History,
for assistance in collecting the Marina del Rey specimens and for sharing an
unpublished annotated bibliography for the California halibut. We are also
grateful to D. Kent and staff, Hubbs Sea World Research Institute, San Diego, for
procuring the Mission Bay specimens. E Hutchinson, F. Sly and R. Xu assisted
in electrophoretic analyses; we thank E. Hutchinson also for performing the
BIOSYS-1 analysis. Finally, we thank four anonymous reviewers for providing
excellent, detailed criticisms of the manuscript originally submitted.

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Ayala, F.)., D. Hedgecock, C.S. Zumwalt and J.W. Valentine. 1973. Genetic variation in Tridacna maxima, an
ecological analog of some unsuccessful evolutionary lineages. Evolution, 27(2):177-191.

Barnett, A. M., A. E. Jahn, P. D. Sertic and W. Watson. 1984. Distribution of ichthyoplankton off San Onofre,
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Burton, R. S. 1983. Protein polymorphisms and genetic differentiation of marine invertebrate populations. Mar.
Biol. Lett., 4:193-206.

Clark, G. H. 1931. The California halibut (Paralichthys californicus) and an analysis of the boat catches. Calif. Div.
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Clayton, |. W. and D. N. Tretiak. 1972. Amine-citrate buffers for pH control in starch gel electrophoresis. ). Fish.

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128 CALIFORNIA FISH AND GAME

BOOK REVIEWS

STRESS AND PERFORMANCE IN DIVING

By Arthur J. Bachrach and Glen H. Egstrom, Best Publishing Co., San Pedro, CA, 1987, 183
p., illustrated. $26.50

It has long been acknowledged that most diving fatalities occur as a direct result of problems
created by the divers themselves, rather than external factors such as equipment failure or marine
life. Analysis of individual accidents, on a case by case basis, almost invariably lead the perceptive
researcher to conclude that stress is at the central core of each of these incidents. With this thesis
in mind, Egstrom and Bachrach proceed through an exhaustive examination of the various elements
which contribute to diver stress and ultimately, diving accidents.

The authors' vast experience, Egstrom at UCLA and Bachrach at the Naval Medical Research
Institute, is evident throughout this text. Indeed, they have been at the forefront of the research on
diver performance for more than twenty years. This work is, essentially, a brief synopsis of the span
of their studies.

The book is well organized, proceeding from defining stress, through stress indicators, and
detailing panic and panic reactions. Serious attention has also been given to identifying the role of
diver training and intelligent equipment evaluation as they relate to diver performance. There are
28 figures, 10 tables, and 5 diagrams.

Although the introduction of this book purports this work to be directed at the sport diving
community, this reader found it extremely technical and probably beyond the scope of the average
sport diving enthusiast. It is an excellent book for the diving instructor, the diving physiologist, or
members of the scientific diving community.

— Kristine Henderson

Photoelectronic composition by
CAUFORNIA OFFICE OF STATE PRINTING

88 77300

INSTRUCTIONS TO AUTHORS

EDITORIAL POLICY

California Fish and Game is a technical, professional, and educational journal
devoted to the conservation and understanding of fish and wildlife. Original manu-
scripts submitted for consideration should deal with the California flora and fauna or
provide information of direct interest and benefit to California researchers and
managers. Authors should submit the original manuscript plus two copies, including
tables and figures.

MANUSCRIPTS: Authors should refer to the CBE Style Manual (Fifth Edition) and a
recent issue of California Fish and Came for general guidance in preparing their
manuscripts. Some major points are given below.

1. Typing — All text submitted, including headings, footnotes, and literature cited
must be typewritten doublespaced, on white paper. Papers shorter than 10
typewritten pages, including tables, should follow the format for notes. Letter
quality computer print-out is acceptable.

2. Citations — All citations should follow the name-and-year system. The "library style"
is used in listing literature cited.

3. Abstracts — Every article must be introduced by a concise abstract. Indent the
abstract at each margin to identify it.

4. Abbreviations and numerals — Use approved abbreviations as listed in the CBE
> Style Manual. In all other cases spell out the entire word.

TABLES: Each table should be typewritten with the heading margin left justified.
Tables should be numbered consecutively beginning with "1" and placed together in
the manuscript following the Literature Cited section. Do not double space tables. See
a recent issue of California Fish and Game for format.

FIGURES: Consider proportions of figures in relation to the page size of California
Fish and Game. The usable printed page is 1 1 7 by 1 91 mm (4.6 by 7.5 in.). This must
be considered in planning a full page figure, for the figure with its caption cannot
exceed these limits. Photographs should be submitted on glossy paper with strong
contrasts. All figures should be identified with the author's name in the upper left

* corner and the figure numbers in the upper right corner. Markings on figures should
be made with a blue china marking pencil. Figure captions must be typed on a
separate sheet headed by the title of the paper and the author's name.

PROOF: Galley proof will be sent to authors approximately 60 days before publi-
cation. The author has the ultimate responsibility for the content of the paper and is

* expected to check the galley proof carefully.

PAGE CHARGES AND REPRINTS: All authors will be charged $35 per printed page
and will be billed before publication of manuscripts. Reprints may be ordered through
the editor at the time the proof is submitted. Authors will receive a reprint charge
schedule along with the galley proof.

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