Volume 22, Number 2, Summer 1979

m -.

• •••-

Oceanus

The International Magazine of Marine Science

Volume 22, Number 2, Summer 1979

William H. MacLeish, Editor
Paul R. Ryan,/\ssoc/afe Editor
Deborah Annan, Editorial Assista

nt

Editorial Advisory Board

'o

•z.

Edward D. Goldberg, Professor of Chemistry, Scripps Institution of Oceanography

Richard L. Haedrich,/4ssoc;afe Scientist, Department of Biology, Woods Hole Oceanographic Institution

John A. Knauss, Dean of the Graduate School of Oceanography, University of Rhode Island

Robert W. Morse, Associate Director and Dean of Graduate Studies, Woods Hole Oceanographiclnstitution

Allan R. Robinson, Gordon McKay Professor of Geophysical Fluid Dynamics, Harvard University

David A. Ross,/\ssoda(e Scientist, Department of Geology and Geophysics, Woods Hole Oceanographic Institution

John G. Sclater,/\ssoc/afe Professor, Department of Earth and Planetary Sciences, Massachusetts Institute of Technology

Allyn C. Vine, Senior Scientist, Department of Geology and Geophysics, Woods Hole Oceanographic Institution

A

Published by Woods Hole Oceanographic Institution

Charles F. Adams, Chairman, Board of Trustees
Paul M. Fye, President of the Corporation
Townsend Hornor, President of the Associates

John H. Steele, Director of the Institution

1930

The views expressed in Oceanus are those of the authors and do not necessarily reflect
those of Woods Hole Oceanographic Institution.

Editorial correspondence: Oceanus, Woods Hole Oceanographic Institution, Woods Hole,
Massachusetts 02543. Telephone (617) 548-1400.

Subscription correspondence: All subscriptions, single copy orders, and change-of-address information
should be addressed to Oceanus Subscription Department, 1172 Commonwealth Avenue, Boston, Mass.
02134. Urgent subscription matters should be referred to our editorial office, listed above. Please make
checks payable to Woods Hole Oceanographic Institution. Subscription rates: one year, $10; two years,
$18. Subscribers outside the U.S. or Canada please add $2peryear handling charge; checks accompanying
foreign orders must be payable in U.S. currency and drawn on a U.S. bank. Current copy price, $2.75; forty
percent discount on current copy orders of five or more. When sending change of address, please include
mailing label. Claims for missing numbers will not be honored later than 3 months after publication;
foreign claims, 5 months. For information on back issues, see page 60.

Postmaster: Please send Form 3579 to Oceanus, Woods Hole, Massachusetts 02543.

ITIAL FINDINGS OF A DEEP-SEA BIOLOGICAL QUEST
<gy Expedition Participants

to the Galapagos Rift area has found surprising forms of life that
ists and other scientists the challenge of understanding a new
re. 2

D ECOLOGY OF FISH SCHOOLING

\ss and Evelyn Shaw
y'oy a better chance of survival under a variety of environmental

IEW OF PLANKTON BIOLOGY
/son and Laurence P. Madin

bservation of plankton behavior in the open ocean is yielding insights

itional net sampling. J D

WATERS OF THE CONTINENTAL SHELVES?

I mixing processes indicates that any waste heat discharged nearshore from power
'ficiently transferred to offshore waters and dissipated. 2Q

MARINE ENVIRONMENT

i

serves as one of man's best disinfecting agents, there is growing evidence of its

he marine environment. Development of an alternative biocide could be a

RUGS FROM THE SEA

ts between university research groups and pharmaceutical companies offer the
loping drugs from the sea. A A

EXICO'S PACIFIC INSHORE FISHERIES
cGoodwin
by exporting less shrimp and increasing supplies to its own seafood

scientific worker Frederic P. (Ted) Fitts looking out bow chamber underwater
board the Research Vessel Atlantis II, owned and operated by the Woods Hole
titution. Photo by Anita Brosius. ©7979. BACK COVER: Eurhamphea
nic ctenophore (see article page 18). Photo by Laurence P. Madin.

Copyright © 1979 by Woods Hole Oceanographic Institution. Oceanus (ISSN 0029-8182) is
published quarterly by Woods Hole Oceanographic Institution, Woods Hole, Massachusetts
02543. Second-class postage paid at Falmouth, Massachusetts, and additional mailing points.

Oceanus

The International Magazine of Marine Science

Volume 22, Number 2, Summer 1979

William H. MacLeish, Editor
Paul R. Ryan,/\ssoc/ate Editor
Deborah Annan, Editorial Assista

0°

I*

Editorial Advisory Board

Edward D. Goldberg, Professor of Chemistry, Scripps Institution of Oceanogi
Richard L. Haedrich,/\ssoc/afe Scientist, Department of Biology, Woods Holt
John A. Knauss, Dean of the Graduate School of Oceanography, University o
Robert W. Morse, Associate Director and Dean of Graduate Studies, Woods /
Allan R. Robinson, Gordon McKay Professor of Geophysical Fluid Dynamics, ,
David A. Ross,/\ssoc/ate Scientist, Department of Geology and Geophysics, \
John G. Sclater,/4ssoc7afe Professor, Department of Earth and Planetary Scien
Allyn C. Vine, Senior Scientist, Department of Geology and Geophysics, Woe

Published by Woods Hole Oceanographic Institutio

Charles F. Adams, Chairman, Board of Trustees
Paul M. Fye, President of the Corporation
Townsend Hornor, President of the Associates

John H. Slee\e,Director of the Institution

1930

The views expressed in Oceanus are those of the authors and do not necess^
those of Woods Hole Oceanographic Institution.

Editorial correspondence: Oceanus, Woods Hole Oceanographic Institutior
Massachusetts 02543. Telephone (617) 548-1400.

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02134. Urgent subscription matters should be referred to our editorial office,
checks payable to Woods Hole Oceanographic Institution. Subscription rates: one year, $10; two years,
$18. Subscribers outside the U.S. or Canada please add $2peryear handling charge; checks accompanying
foreign orders must be payable in U.S. currency and drawn on a U.S. bank. Current copy price, $2.75; forty
percent discount on current copy orders of five or more. When sending change of address, please include
mailing label. Claims for missing numbers will not be honored later than 3 months after publication;
foreign claims, 5 months. For information on back issues, see page 60.

Postmaster: Please send Form 3579 to Oceanus, Woods Hole, Massachusetts 02543.

Contents

GALAPAGOS '79: INITIAL FINDINGS OF A DEEP-SEA BIOLOGICAL QUEST

by Galapagos Biology Expedition Participants

A return expedition to the Galapagos Rift area has found surprising forms of life that

offer marine biologists and other scientists the challenge of understanding a new

community structure. O

DEVELOPMENT AND ECOLOGY OF FISH SCHOOLING

by J. Wesley Burgess and Evelyn Shaw

Schooling fishes enjoy a better chance of survival under a variety of environmental

pressures. 1 1

DIVING -A NEW VIEW OF PLANKTON BIOLOGY

by G. Richard Harbison and Laurence P. Madin

Direct underwater observation of plankton behavior in the open ocean is yielding insights

unattainable by traditional net sampling.

WHAT DRIVES THE WATERS OF THE CONTINENTAL SHELVES?

By G. T. Csanady

Research on coastal mixing processes indicates that any waste heat discharged nearshore from power

plants would be efficiently transferred to offshore waters and dissipated.

CHLORINE IN THE MARINE ENVIRONMENT

by Joel C. Goldman

Although chlorine serves as one of man's best disinfecting agents, there is growing evidence of its

harmful effects in the marine environment. Development of an alternative biocide could be a

solution.

water supply
(chlorinated)

THE SEARCH FOR DRUGS FROM THE SEA

by D. ]ohn Faulkner

Collaborative efforts between university research groups and pharmaceutical companies offer the

best hope for developing drugs from the sea. A A

THE DECLINE OF MEXICO'S PACIFIC INSHORE FISHERIES

by James Russell McGoodwin

Mexico might gain by exporting less shrimp and increasing supplies to its own seafood

markets. C 1

COVER: Volunteer scientific worker Frederic P. (Ted) Fitts looking out bow chamber underwater
observation ports aboard the Research Vessel Atlantis II, owned and operated by the Woods Hole
Oceanographic Institution. Photo by Anita Brosius. ©7979. BACK COVER: Eurhamphea
vexilligera, an oceanic ctenophore (see article page 18). Photo by Laurence P. Madin.

Copyright © 1979 by Woods Hole Oceanographic Institution. Oceanus (ISSN 0029-8182) is
published quarterly by Woods Hole Oceanographic Institution, Woods Hole, Massachusetts
02543. Second-class postage paid at Falmouth, Massachusetts, and additional mailing points.

Galapagos '79:

initial Findings of a

Deep-Sea Biological Quest

by Galapagos Biology Expedition Participants*

Alvin starting the one-and-a-half-hour descent to the
Galapagos Rift. (Photo by Emory Kristof. © 1979 National
Geographic Society)

/\t a time when many are looking to outer space for
new forms of life, a self-contained community of
unusual creatures has been discovered deep within
the ocean. These animals have been found living at
depths of 2,500 to 2,700 meters, in an area just over
380 kilometers from the Galapagos Islands, evoking
the memory of Charles Darwin and The Origin of
Species. The filter-feeding animals — limpets,
serpulid worms, enormous clams and mussels, to
name a few — are living in and around hot water

*J. F. Grassle, Woods Hole Oceanographic Institution
(WHOI); C. |. Berg, Harvard University; J. |. Childress,
University of California at Santa Barbara (UCSB); J. P.
Grassle, Marine Biological Laboratory; R. R. Hessler, Scripps
Institution of Oceanography (SIO); H. |. Jannasch, WHOI;
D. M. Karl, University of Hawaii; R. A. Lutz, Yale University;
T. J. Mickel, UCSB; D. C. Rhoads, Yale University; H. L.
Sanders, WHOI; K. L. Smith, SIO; G. N. Somero, SIO; R. D.
Turner, Harvard University; J. H. Turtle, University of Texas;
P. J. Walsh, SIO; A. J. Williams, WHOI.

vents in what is known as the Galapagos Rift area, an
active zone of sea-floor spreading (see Oceanus,
Winter 1974). Most of the normally sparse life found
at these depths live off particles that settle to the
bottom from surface waters, where they have been
created through the processes of photosynthesis
and decomposition. These recently discovered
animal colonies, however, are using as their
ultimate food source the products of chemical
synthesis — that is, the upwelling of minerals
(mostly sulfur compounds) from the earth's molten
interior that support a population of bacteria
subsisting on hydrogen sulfide and carbon dioxide.

The exploration of sea-floor spreading
centers that gave rise to the present discoveries
began in 1974 with dives by submersibles on the
Mid-Atlantic Ridge. Later, the Cayman Trough near
Cuba was explored. But it was not until early in 1977
that the existence of these unusual colonies of
marine animals became known. At that time, a third
major geological expedition, part of the
International Decade of Ocean Exploration
sponsored by the National Science Foundation,
departed for the Galapagos Rift area, some 380
kilometers northwest of the islands and 1 ,000
kilometers west of Ecuador.

Since the initial discovery of the unusual
forms of life was made by geologists and chemists
(see Oceanus, Vol. 20, Number 3, Summer 1977), a
team of biologists joined the next Galapagos Rift
expedition (January 14 to February 26 of this year).
The objectives of the biology program — there also
was integrated geology and chemistry work going
on — weretostudythedistribution and structureof
the communities; to learn how the newly
discovered animals adapt to their unusual chemical
and thermal regime; and to determine if a

Alvinp//of Dudley Foster talking
to surface controller on the
underwater telephone. The
observer, Fred Grassle, holds the
control box for the pumping
system. (Photo by Al Giddings.
© 7979 National Geographic
Society)

self-sustaining group of microorganisms was
responsible for the concentration of life at the
hydrothermal vents. Included were studies of
microorganisms; the growth, distribution, and life
histories of organisms comprising the unusual hot
springs communities; genetics; biochemistry; and
in situ and laboratory physiological studies of
mussels and crabs.

Our detailed observations of the behavior
and habits of organisms at the Galapagos vents were
made possible through use of a new television
system developed specially for the cruise. A CCD
(charged coupled device) camera was developed
by the Radio Corporation of America in conjunction
with the National Geographic Society (which sent a
photography team to participate in the expedition),
and Robert Ballard, a geologist and engineer at
Woods Hole Oceanographic Institution. The
camera, instead of having a regular Vidicon
television tube, houses a solid state system that
allows it to be miniaturized. It is about 20
centimeters long and can be equipped with a
macrolens that permits zoom capability, recording
images on a 2.5-centimeter tape.

Another advance in underwater technology
connected with the expedition concerned Angus
(Acoustically navigated underwater system). Angus
is an unmanned two-ton sled that is towed across
the bottom terrain. It can take some 3,000 colored
pictures of the bottom in a 15- to 16-hour period.
Previously it had been towed at about 3.6 meters
from the bottom, giving pictures of a relatively small
area. With a new lighting system, Angus can "fly" at
about 18 meters from the bottom, increasing the
picture range by a factor of seven. It can now
provide pictures covering a half acre — or 1 ,765
square meters — in one frame. This system was

used to search for the vents — a patch of bottom 50
meters in diameter, 380 kilometers from land.

The Biology Program

The biology team was assigned 10 dives out of a total
of 30 on the expedition. Participating vessels
included the submersible Alvin, operated by
Woods Hole Oceanographic Institution; the
submarine's mother ship, the R/V Lulu; and thetf/V7
Gilliss, owned by the U.S. Navy and operated by the
University of Miami. J. Frederick Grassle, an
Associate Scientist in the Biology Department at
Woods Hole Oceanographic Institution, was the
chief scientist for the biology portion of the cruise,
heading a group of scientists from Harvard
University, Scripps Institution of Oceanography,
Yale University, the University of California at Santa
Barbara, the University of Texas, the University of
Hawaii, the Marine Biological Laboratory, and
Woods Hole Oceanographic Institution. Ballard led
the geology program and John Edmond of the
Massachusetts Institute of Technology led the
geochemistry study.

Typically, Alvin's front basket was cluttered
with a vast array of gear that included a stereo
camera with thermistor probe, insulated
containers, a slurp gun, sterile microbial samplers,
two kinds of in situ microbiology experiments,
scrapers, corers, exclusion cages, fish traps,
amphipod traps, larvae traps, plankton nets,
collecting plates for studying colonization, two
kinds of current meters, a recording thermistor
string, and in situ respirometers. A new pumping
system was devised for obtaining water samples and
filtered samples of varying particle size. The filter
samples will be used for studies of microorganisms
and particulate organic material.

Gilliss was delayed in Panama and arrived late
at the diving site, which meant that the first two
dives in Alvin had to be made without the results
from the Angus sled and a network of navigational
transponders. The first dive was made in a region of
hydrothermally deposited sediment mounds 20
kilometers south of the ridge axis. These structures
are so common that precise navigation was not
needed to locate them. High water temperatures
were detected at the crest of the mounds where
thick crusts of manganese and iron oxides are
formed (Corliss, and others, 1979). Later
examination of box core samples taken on and
around the mounds indicated a rich infaunal
community on the slopes and areas surround ing the
mounds. The rarely seen flower-like
xenophyophorian protozoan is common in the
sediment of this area.

On the second dive to the general area of
hydrothermal vents, white webs of worms, dubbed
"spaghetti," and occasional large dead clams were
observed. These were similar to the specimens
collected on the 1977 expedition. The specially

Larger Colonies
of Life Found

The Galapagos Rift is part of a global
mid-oceanic ridge system in which the crust of
the earth is separating as a result of what are
thought to be convective processes. Similar
regions include the Mid-Atlantic Ridge and the
East Pacific Rise; the latter is an area south of the
Gulf of California and west of Puerto Vallarta,
Mexico. In late April and early May of this year, a
joint French-American-Mexican expedition to
the Rise reported further interesting
discoveries, including chimney-like volcanic
vents where water temperatures may exceed
300 degrees Celsius (570 degrees Fahrenheit).

The eruptions from the volcanic
structures have carpeted the region with
deposits of copper, iron, zinc, cobalt, lead,
silver, and cadmium - often combined with
sulfur. It is believed to be the first time such
mineral deposits have been found in the open
ocean. In addition, the scientists -diving in the
research submarine Alvin, operated by Woods
Hole Oceanographic Institution - discovered
new colonies of life covering areas more than
twice the size of the Galapagos Rift
communities. The participating American
scientists on this expedition were from Woods
Hole and Scripps Institution of Oceanography.

designed slurp gun vacuumed the spaghetti off the
rocks. Later, on deck, we finally solved the mystery
of their identity: they were enteropneusts,
worm-like relatives of the early ancestors of
vertebrates, normally found living in sediments.
Yellowish bal Is suspended just above the bottom -
previously called "dandelions" by geochemists -
also were collected with the slurp gun, but
fragmented in surface waters. An intact specimen
was collected on a later dive. It is a benthic
siphonophore (a relative of the Portuguese
man-of-war) belonging to the family Rhodaliidae.
Although members of this group were first
collected during the Challenger Expedition
(1872-76), they have seldom been collected whole
and have been assumed to occur in the water
column above the bottom. By the end of the second
dive, two promising vent sites had been located
from Angus film processed on board the Gilliss.
On the third dive, an active vent with live
communities was located near Clambake I (an area
explored on the1977dives) and named Mussel Bed.
The major portion of the dive was spent placing
testing equipment on the bottom, including slides
for studies of microbial colonization. In addition,

Originally called "spaghetti" because of their appearance,
these worms have been identified as enteropneusts.
(Photo byj. J. Childress)

mussels were sampled and vent water filtered. With
so many tasks to accomplish, our studies were
limited to Mussel Bed and the Garden of Eden area
(also explored in 77) 3 kilometers to the east.
Meanwhile, collections and photographs were
made by the geologists in a new area called Rose
Garden, which was named after dense beds of
red-tipped vestimentiferan worms living in white
tubes up to 3 meters long.

The stereo camera, mounted on a
mechanical manipulator outside /A/wn, was used to
study the distribution of organisms with respect to
temperature. A temperature probe gave a distance
reference and provided a continuous recording of
temperature on a data log inside the submersible.
Detailed photogrammetric analysis of these stereo
photos will enable us to accu rately measure size and
distance in three dimensions.

By using the slurp gun and carefully picking

Vestimentiferan worms with
brilliant red plumes extend from
tough flexible tubes. Limpets and
anemones are common, and a
single crab is visible. (Photo by R.
R. Messier)

animals from clumps of mussels and rocks,
numerous smaller animals were obtained, many of
which promise to be as interesting as the larger
specimens collected. One, a small shrimp-like
Leptostracan crustacean, has comb-like structures
at the end of its eyestalks where eyes would
normally be. This sort of eyestalk modification has
never been observed in other crustaceans. The
combs are probably used to scrape microorganisms
(food) from the hard rock and mussel surfaces.

Collecting and observing large numbers of
animals was necessary to answer some of the
questions posed by these new discoveries. For
example: To what extent is each area an island? How
do rates of growth and metabolism there compare
to other areas of the deep sea, where relatively low
rates have been recorded (seeOceanus, Vol. 21,
Numberl, Winter)? How do temperature, pressure,
and food supply relate to metabolic rates?

Live brachyuran crabs were recovered from
the vents, and a number were kept alive for almost
three months after the expedition. Studies of their
metabolic rates at different temperatures and
pressures indicate they need pressures of at least
125 atmospheres to survive and are killed at about
400 atmospheres. Their metabolic rates appear to be
somewhat lower than those of shallow-living crabs
at comparable temperatures. The Galapagos crabs
are able to remove oxygen from water at very low
partial pressures, so they probably rely largely on
aerobic (oxygen-dependent) metabolism in the vent
waters. The upper temperature limit for the crabs is
greater than 22 degrees Celsius at in situ pressures.

More than 100 mussels were collected from
each of two areas for studies of genetic
differentiation between populations at the vents.
Analysis of enzyme variants will determine the
differences between vent populations. In addition
to the studies of mussels on the surface, rates of
oxygen uptake were compared using respirometers

r

• >.'-/

Calatheid crabs perched on the top of pillow lavas. The dense field of mussels, some with their siphons out, are close to
the source of hot water. (Photo by R. R. Messier)

in situ. By comparing respiration in mussels living at
2 degrees Celsius in the central and peripheral areas
of the vents, it may be possible to determine how
food supply relates to metabolic rate.

Many shells of the large white clam were
found around dead vents. Living specimens,
meanwhile, were observed nestled among the large
mussels surrounding live vents, but they were never
abundant. Of the material collected thus far, the
size of the clams ranges from 130 to 264 millimeters
in length. The anatomy of the large clam places it in
the family Vesicomyidae, genus Calyptogena.
Unlike most bivalves, it has red blood and a meaty
odor. These features have not yet been analyzed.
Karl Turekian and colleagues at Yale University have
used thorium-228/radium-228 activity ratios to
estimate the age of a 22-centimeter-long clam to be
less than 10 years.

The very abundant mussels clustered in the
vicinity of active vents were hosts for polynoid
polychaetes. At some vents almost all mussels
contained polychaete symbionts in the mantle
cavity, whereas at other vents they were rarely
found. Like their shallow-water counterparts, the
mussels are capable of forming lustrous pearls (a
few small ones were found).

From studies of the larval shell morphology
on juvenile specimens, it appears that these animals
have a long planktonic larval life. Abyssal currents
may transport the larval stage hundreds of
kilometers. Since the hot water supply is not likely
to be constant, a long-lived dispersal stage would be
needed to locate new sources of water. The mussels
are thought to be a new genus in the family
Mytilidae.

The large red vestimentiferan worms
mentioned earlier were collected on the eighth
dive. Smaller relatives were discovered several
years ago during dives with the submersible
Deepstar400 at 1 ,125 meters off California. These
were assigned to the phylum Pogonophora (Webb,
1969). More recent studies indicate that these

should be classified as a major taxon distinct from
the Pogonophora (Van der Land and Norrevang,
1977). Forty-five to 76-centimeter specimens were
collected in 1977 in the Galapagos Rift area. The
specimens from the 1979 expedition are larger, with
tubes as long as 2.4 to 3 meters. The largest animal
collected had a tube more than 2.4 meters long and
a body length, after preservation, of 1 .5 meters,
with a diameter measuring about 5 centimeters.
Juvenile specimens less than 15 centimeters in
length clustered around the base of the large tube
also were recovered. The creature has a brilliant red
tip, the color deriving from oxygenated hemoglobin
in the blood. The animals have no gut and are
thought to live on dissolved organic material in the
water.

For reasons not clearly understood, each
species occurs at a different distance from the
vents. The pillow lava formations farthest from the
vents are largely barren, with occasional corals,
anemones, or sea cucumbers. As the vent is
approached, crabs, enteropneusts, and dandelions
appear — the enteropneusts found draped on rocks
at the edge of the zone and the dandelions in
protected low spots closer to the vents. The clam
beds, mussels, serpulid worms, and large numbers
of small anemones are located at intermediate
distances. Although thedistribution of musselsand
crabs extends into the supply of warm water, most
of the animals are living at the ambient water
temperature of 2 degrees Celsius. The tops of pillow
lava formations adjacent to the vents are covered
with serpulid worms, their feathery plumes
enabling them to filter particles from the water.
Galatheid crabs — the females carrying large
numbers of eggs — are common on the tops of
pillow lava formations. These relatively active
animals crawled into the frame oiAlvin and many
were "collected" when the submersible surfaced.

The vestimentiferan worms live only in the
supply of warm water — ranging in number from a
dense field spread along a 50-meter fissure at Rose
Garden to only two or three small individuals in the

narrow vent openings at Mussel Bed. The rock walls
of the vents are densely covered by a species of
light-colored, filter-feeding limpet, which also is
found scattered along the tubes of the
vestimentiferan worms. The warm-water flow from
the vents is the preferred place for a pink brotulid
fish, often seen with its head nestled down in the
vent, where it probably feeds.

The Collection of Microorganisms

"Milky-bluish" water flows from the most active
hydrothermal vents, suggesting that bacterial
oxidation of hydrogen sulfide to elementary sulfur
and sulfate could produce the basic food source for
the entire community in the form of bacterial cells.
Chemosynthetic bacteria use the energy from this
chemical oxidation for the fixation of carbon
dioxide into organic matter, similar to the way
photosynthetic organisms use sunlight as their
energy source. Other compounds that can be
chemosynthetically oxidized are elementary sulfur
and thiosulfate, as well as hydrogen, ammonia,
nitrite, iron, and manganese. Iron and manganese
crusts are prevalent in the vent area, indicating that
the oxidation of materials other than sulfur
compounds may contribute to the amount of
carbon dioxide fixed.

The shimmering water approximately one
meter above the vents contained 105 to 106 bacterial
cells per milliliteras measured by direct counts with
an epifluorescence microscope. These counts
indicate a high bacterial output at the vents,
consideringthatthere is strong mixing with ambient
water in this stratum as revealed by temperature
fluctuations. The cells in these water samples
(Figure 1) displayed morphological uniformity, as
well as a relatively low fraction of amorphous
material, both of which were unexpected. Dense
clumps (mostly 12 to 100 microns in diameter) of
bacterial cells were common (Figure 2).

Scanning electron microscope studies of a
number of different surfaces collected near the
vents disclosed some unusual forms of organisms
(Figure 3). Pieces of mussel surface were rusty
brown in appearance. Instead of a deposit of
amorphous material, dense layers of cells or
nodule-like structures were found, some
apparently heavily encrusted with metal oxides
(unidentified at this time). A network of filamentous
structures appears to relate to prosthecate (stalked)
bacteria.

Some 200 isolates of sulfur oxidizers are now
under investigation. Their growth on a large variety
of different enrichment media indicates an unusual
diversity of metabolic types. Depending on their
specific oxidation products, the growth media after
incubation varies in pH from 5.1 to 8.6. Most strains
prefer reduced concentrations of oxygen. Many
grow well in the absence of an added nitrogen
source, but only one strain has been found to

Figure 1. Water samples collected several feet above an
active vent on a Nucleopore filter (pore size 0.22 micron).
Bacterial cells of rather uniform appearance show division
stages, indicating active growth. Magnification 5,000x
(bar = 10 microns).

Figure 2. Representative sample of bacterial clump and
amorphous matter, probably elemental sulfur.
Magnification 20,000x (bar=l micron).

exhibit enzymatic nitrogen fixation. Spirilla strains
that can oxidize thiosulfate but prefer an organic
substrate have been cultured. Anaerobic bacteria,
which grow in the absence of oxygen and reduce
sulfur compounds, also have been found.
Prosthecate bacteria are in the process of being
isolated. A free-living spirochaete (an elongated,
spirally twisted, unicellular bacteria that moved by
the contraction of flagella-like filaments) has been
isolated.

Preliminary measurements of in situ carbon
dioxide fixation indicate much higher bacterial
activities compared with previous measurements at
other marine oxic/anoxic interfaces. The analysis of
ATP (adenosine triphosphate) as an indirect
measure of active bacterial biomass showed values
two to four times higher than in local productive
surface waters, and a hundred to a thousand times

8

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..-'.. ' -. • . '• "
-*<X sN

^^

D

Figure 3. (A): Surface of a piece of a mussel sh ell collected near the Mussel Bed vent. Cracks are due to critical point drying
during preparation of the specimen. Magnification 500x (bar =100 microns). (B) and (C): same preparation; network of
stalks from prosthecate-like bacteria and sessile forms, apparently related to heavy mineral deposits. Magnification 2,500
and5,000x, respectively (bar =10 microns). (D): closeup of attached and some non-attached forms, some of which appear
to have an outer coating. Magnification 70,000* (bar=l micron).

higher than in a control sample taken at some
distance from the vents. This observation — along
with the high bacterial content of the vent water, the
extraordinary metabolic diversity, and the carbon
dioxide fixation by pure cultures — appears to
confirm that bacterial chemosynthesis, largely
through oxidation of hydrogen sulfide, is the basic
food source for the vent community (Rau and
Hedges, 1979). The major bacterial production
probably takes place within subsurface "growth
chambers," with a large percentage becoming
diluted by ambient water before reaching
consumers. Because of the complexity of the vents,
it will be difficult to obtain a realistic quantification
of bacterial production and efficiency.

The Work Is Just Beginning

The hydrothermal vents contain a combination of
unusual factors, such as elevated temperatures
(animals in the vents experience 10- to 15-degree

Celsius temperatures, and occasionally higher
ones), high pressures, and a unique chemical
environment that supports a rich concentration of
active sulfur bacteria. Growth and metabolic rates
are high compared with other deep-sea regions. In
contrast to other deep-sea habitats, the changeable
environment and rich food supply favor species
with rapid growth and a relatively short life span.
The large areas containing dead clams may indicate
the ephemeral nature of the food supply. At least
some species have long-lived planktonic larvae,
which enable them to colonize other areas along
the ridge axis.

Despite the unusual composition of the
communities, initial findings suggest that diversity
- the number of species in a given population — is
low. Although the communities are not directly
comparable, this finding differs from the large
number of species that are found in individual
sediment samples in the deep sea.

Respirometer used to measure oxygen uptake of mussels
in situ. (Photo by R. D. Turner)

The vent food chains appear to be relatively
simple, with the bulk of the organisms dependent
on bacteria for food by taking up released dissolved
organic material, filtering particles out of the water,
or scraping material off hard surfaces. Less
understood are the secondary consumers, such as
scavengers and predators. The most obvious
members of this group are rattail fish, an
undetermined species of crab, and small
amphipods — all attracted to bait.

The vent areas are more extensive than first
believed. The individual concentrations of animals
are part of a larger community that may extend for
hundreds of miles along the axial ridge of the
Galapagos Rift. The discoveries of large colonies of
animals along the East Pacific Rise lend support to
this view.

The greater part of the work from the
Galapagos 79 expedition has only started. The
biological work still to be done includes:
photogrammetry; analyzing proteins for genetic
information; studying the thermodynamic
properties of enzymes; sorting out the numerous
strains of bacteria; sectioning tissues for studies of
reproduction; determining gut contents; and
performing a variety of morphological studies.

Trap to catch larvae released from the bottom. Panels in
background are for studies of larval settlement. (Photo by
H. L. Sanders)

Another biological expedition to the
Galapagos is scheduled for this November. More
organisms will be collected, and a number of
long-term experiments will be picked up that were
placed on the bottom in January. It is expected that
the experimental plates and glass slides will be
colonized by rich growths of organisms, which will
allow a comparison of growth rates with other areas
of the deep sea. Thus these hydrothermal vents at
major oceanic spreading centers will considerably
advance our knowledge of deep-sea processes, but
may also provide us with perplexing questions that
will take some time to answer.

ThisarticleiscontributionNumber3of the Galapagos Rift
Biology Expedition, supported by the National Science
Foundation.

References

Corliss, J. B., J. Dymond, L. I. Cordon, ). M. Edmond, R. P. von

Hezen, R. D. Ballard, K. Green, D. Williams, A. Bainbridge, K.

Crane, and T. H. van Andel. 1979. Submarine thermal springs

on the Galapagos Rift. Science 203:1073-1083.
Rau, G. H., and ). I. Hedges. 1979. Carbon-13 depletion in a

hydrothermal vent mussel : suggestion of a chemosynthetic

food source. Science 203:648-49.
Van der Land, )., and A. Norrevang. 1977. Structure and

relationships of Lamellibrachia (Annelida, Vestimentifera). Det

Kongelige Danske Videnskabernes Selskab, Biologiske Skrifter

21 (3): 1-155.
Webb, M. 1969. Lamellibrachia barhami, gen. nov., sp. nov.

(Pogonophora), from the northeast Pacific. Bull. Mar. Sci.

19:18-47.

10

•'

• •

development and^cology"

of

Schooling

by J. Wesley Burgess and Evelyn Shaw

I he phenomenon of schooling in fishes has
captured the attention of marine scientists and
amateur fish observers for generations — indeed,
Aristotle discussed this behavior about 2,400 years
ago. There are several good reasons why schooling
has provoked this interest. First, schooling fish are
the foundation of major worldwide fishing
industries. Fishes — such as mackerel, herring, cod,
and tuna — live and swim together in large schools.
They also meet their deaths together in the seines of
fishermen. Second, schooling is a very prevalent
behavior. About 80 percent of the approximately
20,000 known fish species exhibita schooling phase
during their life cycle. Finally, to the scientist, the
behavior of schooling fish poses many biological
questions that only can be answered through
experimentation.

As a rule, schools arecomposed of many fish
of the same species, moving in synchrony.
Individuals tend to arrange themselves in certain
configurations, maintaining predictable distances
and orientations to each other (Figure 1). How this
behavior is established in marinefish, whatadaptive
advantages schooling provides, and how schooling
may have evolved are questions this article will
address.

The Development of Schooling

A schooling fish spends the first part of its life
imprisoned in a transparent egg shell called the
chorion. Upon hatching, the young of some species
are very immature, burdened by a large yolk sac and
incapable of locomotion. Other species at hatching
are more advanced, being capable of feeding and
sustained swimming. Most of the studies of early
schooling have examined fish of the latter type.

Although schooling is not found in fish that
have just hatched, it is manifested gradually during
a period of social interaction. Silversides fry,
Menidia menidia, M. beryllina, artdAtherina
mochon, begin their interactions by repeatedly
approaching each other and then veering sharply
away. At this early stage, preschooling fish often
approach each other head-on, or at right angles, but
as they mature, head-to-tail approaches become
predominant. Finally, fish begin to swim together,
at first in pairs and then in larger groups, until
parallel, synchronized schooling is established.

Above, a school of herring, Herklotsichthys punctatus,/n
the Central Pacific. (Photo by Edmund Hobson, NMFS)

11

Overall, the normal development of schooling
seems to be an ordered, gradual process that is
preceded by well-formed, simpler behaviors.

Experiments have revealed more details
about the developmental process. Some following
behavior is exhibited by young fish before they are
old enough to school. One way of measuring this
response is to place fish of different ages into an
optomotor apparatus, which consists of a round
aquarium surrounded by a slowly revolving drum.
The drum can be lined with alternating black and
white stripes or other patterns to test the response
of the fishes to moving stimuli. When tested in this
apparatus, many fishes, including both schooling
and nonschooling species, orient to and move at
the same speed as the rotating pattern. In a 1967
study, one of the authors (E. Shaw) and B. D. Sachs
compared the following responses of the silversides
(M. menidia) prior to schooling age (fry 5 to 7
millimeters in length), or while school ing was being
established (fry 8 to 10 millimeters), and after its
onset (fry 11 to 12 millimeters). A well-developed
following response was found in both the olderand
theyoungerfish. In 1975, Shawtested preschooling
and schooling silversides, M. menidia and A.
mochon, to determine their response to different
types of patterns. Preschooling fry followed fewer
patterns than the older fish, and their following
responses were poorly organized and more erratic.
It is easy to imagine the utility of such a response,
even for young fish that have just hatched. By
orienting toward and following their neighbors,
even tiny larvae can manage to stay together, thus
avoiding dispersion in the vast ocean. These early
grouping mechanisms may provide the proper
environment for the later development of
schooling.

What conditions are necessary for schooling
to develop? To find out if early experience with
other speciesmates is "essential for the formation of
schooling," M. M. Williams and Shaw reared
silversides, M. menidia, in groups of 20 fish or singly
under complete isolation. When isolate-reared fry
were placed together with other speciesmates, they
showed obvious schooling behavior. However,
schooling among the isolates was of shorter
duration and the schools appeared to be less
regular than group-reared fish. The same results
were obtained in a later study by Williams when fish
were reared in isolation, but were given visual
contact with one other speciesmate. These studies
indicate that schooling behavior is resistant to
extreme manipulation, but early experience can
produce qualitative differences in later life.

The first appearance of schools may depend
on the maturation of sensory systems in young
fishes. Different senses become operational at
different stages of earlydevelopment. Fish have the
usual complement of vertebrate sense organs. The
visual system, for example, is functional

immediately after hatching, allowing fish to feed
before schooling. Fish eyes are especially sensitive
to lateral movements, and thus may be useful in
schooling. Fish also have another sensory system
that is peculiar to fishes and some amphibians: the
acoustico-lateralis system, commonly known as the
lateral-line system. The lateral line contains sensory
structures called neuromast cells that are sensitive
to the movement and displacement of water. Since
fish in schools swim close to the flanks of their
schoolmates, it has been suggested that the lateral
line might function in schooling. For example, in
the perch and the ruff, clustering in close groups
occurs only after the canal mast cells are formed. In
young silversides, M. menidia and M. beryllina,
prolonged parallel swimming and stable schooling
first appear at the same time neural connections to
mast cells are formed; approach behavior and
occasional parallel orientation appear before this
time. In these species, establishment of mature
schooling patterns appears to be dependent on the
presence of a functional lateral-line system.

The Senses of Schooling

We have seen the importance of the lateral-line
sensory system for the onset of schooling.
However, in the adult fish neither the lateral line nor
any other single sense appears to be solely
responsible for maintain ing coherent schools. Even
when certain senses are absent, many experienced
fish continue to show some facets of schooling
behavior. For example, without lateral line and
olfactory stimuli, single jacks oriented to schools
behind a solid plexiglas partition, presumably by
using visual cues. Furthermore, when saithe were

Optomotor apparatus. Drum is lined with alternating black
and white stripes to test the response of fishes to moving
stimuli.

12

Figure 7. A small pelagic school, showing a characteristic spatial pattern. Schoolmates maintain parallel orientation and
move in synchrony. Note that the fish are of the same species and are of similar size.

kept \r\ groups of 25 \r\ large tanks that permitted
constant movement, even bilaterally blinded fish
could be made to school. However, schooling
could be prevented by both blinding and severing
the fishes' lateral lines. So to a point, deficits in one
sensory system can be compensated for by using
the other, intact senses. This flexibility in the
sensory control of adult school ing could insure that
injured fish or groups in adverse environments (like
silty water permitting low visibility) still would be
able to school. For schooling to have evolved such
strong resistance to outside interference, we would
expect that this behavior has considerable adaptive
value.

Ecological Advantages of Schooling

While considering the various advantages that have
been proposed for schooling, it is useful to imagine
what optimal school form, organization, and
structure would best satisfy each advantage.
Eventually, the behaviorof a schooling species must
aid individuals' survival under a variety of
environmental pressures, and might not be
explainable by any single constraint.

Fish may gain immediate benefits just by
traveling in a group. For example, when a fish
swims, the oscillating movement of its tail produces
small currents in the water called vortices. By
swimming in staggered checkerboard rows, each
individual theoretically can use the vortices of
surrounding fish to reduce its own swimming
friction, perhaps by as much as a fifth. Some
evidence (Zulev and Belyayev, 1969) supports this
claim, and the three-dimensional structure of some
fish schools does show the checkerboard pattern
that would be optimal for reducingdrag, and hence
reducing energy output. Increased ease of

locomotion might also result from swimming in
water that has flowed over other schoolmates. In
1970 and 1971 studies, Rosen and Cornford found
that the polysaccharide "slime" that is secreted on
the bodies of many fishes could reduce the fluid
friction of moving through the water. By swimming
in the wake of schoolmates, each individual fish
may use the flow of dissolved slime to further save
energy. When menhaden, Brevoortia patronus,
schools were subjected to a synthetic
polysaccharide similar to natural slime, which was
slowly added to the water, C. M. Breder found that
individuals did, in fact, swim faster.

In addition to the immediate benefits of
energy conservation, fish may receive some
selective advantages by traveling in schools. By
examining such advantages, we can try to
understand the process of evolution through which
schooling originated. Schooling is probably an
ancestral behavior, because it is found in so many
divergent species. As mentioned previously, about
80 percent of the approximately 20,000 known
species of fishes school as juveniles, and 20 percent
continue to school as adults. Because so many
species in different orders have adopted this
behavior, it is likely that there are considerable
survival advantages for populations of schooling
fishes, especially during juvenile stages.

The major ecological advantages of
schooling can be divided into two categories:
behaviors that help species avoid predators, and
behaviors that contribute to the competitive
success of a species. I n the first category, V. E. Brock
and R. H. Riffenburgh demonstrated in a geometric
analysis published in 1960 that a predator searching
at random has a more difficult time finding prey that
are spaced close together in a school (Figure 2).

13

(2A)

<2B)

T^=^

Figure 2. Advantages of schooling as a defense against predation. A solitary predator fish searches for prey among
equal-sized populations of evenly-spaced territorial fish (A) or clumped, schooling fish (B). A larger area must be searched
to find the prey in schools. Even when a predator finds the school, improved detection, group maneuverability, the
confusion effect, and nredator satiation can orotect individuals.

Certainly in any population, a close-schooling
species will leave more vacant territory for
predators to search in vain than a species that is
dispersed uniformly. In this way, the distribution
pattern of a school within the ocean may deter
predation.

Within a school, there truly may be safety in
numbers. As several investigators have realized, a
predator cannot consume unlimited quantities of
prey at one meal. When a predator becomes
satiated, the other fish in the school are safe. One
example of predator satiation is seen in the prey fish
Pempheris oualensis, an inhabitant of coral reefs.
These fish rest du ring the day in caves and crevices,
forming schools of hundreds to thousands of
individuals. Although they regularly encounter
territorial predators residing in their hiding places,
the predator fishes can eat only a few individuals at a
time, and the bulk of the schooling fish benefit from
the protection of their surroundings. The use of
schooling for increased protection during resting
periods has been observed in various other reef
fishes.

There are several reasons why schooling may
be especially advantageous for juvenile fishes.
Many adult fishes spawn at the same time, often in
areas where larval food is plentiful. The resulting
concentrations of tiny, newly hatched fry become
especially vulnerable targets for marine predators.
Just like adults in resting schools, juveniles may find
a survival advantage in staying close together in
large numbers in order to swamp potential
predators. For example, D. V. Radakov found in a
1973 study that horse mackerel in a 300-liter
aquarium quickly eat as many as 59 young
silversides if presented one at a time. When the prey
fish were presented in groups, they either were
consumed less rapidly or escaped from the horse
mackerel. If schooling is advantageous for juvenile
fish (as these results suggest), it explains why so

many species have evolved juvenile schooling.

Another insight is derived from studies of
birds. Instead of laying eggs throughout the
breeding season, many bird species synchronize
their reproduction so that many young hatch at the
same time. This is called the Fraser Darling effect.
The resulting brief oversupply of prey is difficult for
predators to utilize and may serve the same
ecological function as group spawning and juvenile
schooling in fishes— concentrating age classes in
space and time in order to decrease the effects of
predation on juveniles.

Even before a predator reaches satiation, fish
may be able to hide behind other schoolmates and
avoid being caught. The notion that animals band
together to screen themselves from predators (the
"selfish herd," W. D. Hamilton, 1971) has been
applied to many animals that live in groups. G. C.
Williams has suggested that schools serve as a form
of cover and that schooling may be little more than
an attempt by fish to hide behind their schoolmates
for protection. However, the cinematographic
observations of Radakov do not confirm that
schooling fish try to swim behind others in the
group, even when alarmed by the appearance of a
predator. Predators can be confused by the rush of
swimming fish that pass in a school. Without having
to hide behind their schoolmates, the confusion
effected by a mass of alternating colors and shapes
may increase predators' difficulty in isolating and
catching individuals.

Another way fishes can foil predators is to use
the combined watchfulness of their other
schoolmates to detect harmful intruders. It is
known that fish can respond rapidly to changes in
the swimming speed of neighbors in a school. After
detecting a predator, schools can execute quick
turns and synchronized escape maneuvers. For
example, P. F. Major in a 1977 study found that
single jacks could readily approach and catch

14

anchovies swimming alone, but were less
successful at preyingon anchovies in schools. In the
oceans, the increased scanning of the environment
and increased group maneuverability combine to
give schooling prey a survival advantage over
solitary predators.

Thus the increased difficulty of searching for
fishes in schools, coupled with the abi lity to satiate,
confuse, detect, and outmaneuver predators all
contribute to the anti-predator value of schooling.
All or many of these specialized strategies appear to
be employed by diverse fish species whose
schooling patterns are basically similar. It may be
the combination of different survival advantages
that makes schooling flexible enough to serve as a
successful lifestyle for so many fishes.

Schooling also can help fishes to be
successful competitors, facilitatinga widevariety of
feeding strategies, including plankton-feeding,
omnivorous, and predation. For example, tiny
animals fed upon by planktivorous fishes do not
appear to be uniformly distributed throughout the
ocean, but are concentrated in patches. Where
plankton are clumped, fishes that swim close
together in schools have an advantage, since this
"bonanza strategy" allows many individuals to
search for food clusters that will feed the entire
school.

Adult omnivores also can use schooling to
their advantage, especially when competing with
territorial fishes. In the parrot fish Scarus
era/census, for example, individuals either can
defend territories, or swim in schools. When
available territories are depleted by a competing
damselfish species, the remaining parrot fish form
schools where individuals feed more often and
suffer fewer attacks than their territorial
speciesmates.

Predator fishes, on the other hand, can use
schooling to aid in the capture of food fish.
Although solitary predators are less successful with
schooling prey, predators that travel in groups
actually have an advantage in finding and catching
schooling prey fish (Figure 3). For example, Major
found that schools of jack were more efficient at
capturing anchovies from schools than a jack
working alone.

Schools of predatory fish may be able to use
specialized tactics to make food capture more
effective. Predatory schools are commonly
observed encircling all or part of a school of food
fish. Maneuvers such as circling may help counter
the confusion effect and reduce the
maneuverability of prey fish schools.

Structure of Fish Schools

Although schooling has been studied for some
time, the form and structure of schools are only now
beginning to be understood. One reason for this is
that the required studies of schooling individuals'

Figure 3. Schooling predators encircling a school of prey
fish. This is one way predators can utilize the advantages of
schooling. In pursuing clumped resources, school
members benefit from the combined searching abilities of
their schoolmates. Predatory schooling maneuvers like
this help circumvent prey schools' antipredator tactics,
such as confusion, predator satiation, and synchronized
escape swimming.

movement, orientation, and interdistances are
rigorous and time consuming, usually requiring
frame-by-frame analysis of photographs of a school.
Such analyses have been performed by several
behavioral scientists. All found that fish in schools
stayed close together, maintaining positions 0.18 to
1 .0 body lengths apart from their nearest neighbors.
Actual distances depended on the age and species
of the fish in the school and the experimenter's
measurement techniques. Fish in schools
synchronized their swimming speeds and stayed in
predominantly parallel orientation without
touching. When J. C. Van Olst and J. R. Hunter in a
1970 study compared orientation angles within
schools of Pacific mackerel, jack mackerel,
northern anchovy, jack smelt, and topsmelt, all
species were found to follow their schoolmates in
front and behind more than their neighbors to the
sides. Schooling pilchards, Harengula sp., were
arranged in diagonal rows like a checkerboard, with
animals distributed in equal density on all planes.
We know only a few factors that affect the
structure of a school. Disturbances or the
appearance of a predator can cause schools to draw
together. In jack mackerel, food deprivation also
can cause changes in interdistances and less
compact schools. S. A. Moss and W. M. McFarland

15

found in a 1970 study that anchovy schools respond
to short-lived, abrupt changes in dissolved oxygen
and acidity by abruptly altering their swimming
speed. Inside mullet schools there occurred areas
where oxygen concentration and acidity were
significantly less than in the surrounding water. Fish
in these areas moved at a higher rate and
maintained more uniform orientation. What
function these internal chemical variations might
have under natural conditions is not known.
Many behavioral variables have been
measured in fish schools: for example, tendencies
for aggregation, uniform distances, parallel
orientation, group alarm responses, and
synchronized swimming maneuvers.
Unfortunately, we know little about how these
behaviors interact or what causes the variations in
schoolingthatwe observe in nature. Aswecontinue
to study schooling, we will have an opportunity to
learn more about the relationship between the
behaviors we observe and their ecological value.

Evolution of Schooling

It is impossible to be sure how or when schooling
first began. We could infer evolutionary steps by
using our understanding of the development and
ecology of schooling in contemporary species to
reconstruct the most direct ancestral route to this
behavior. We would expect to find the roots of
schooling in the previously existing behavior
patterns of many species. Although serving other
functions, these so-called "preadaptations" could
act as stepping stones for the evolution of new
behaviors like schooling. For example,
synchronized adult spawning would initially result
in clumps of newly hatched juveniles. Young fishes
that had good lateral eyesight, a lateral-line system
fordetecting nearby water movements, and an early
tendency to orient toward and follow moving
patterns would possess many of the behavioral
prerequisites for schooling. In several species, an
immediate facility for swimming results from
following speciesmate's vortices and swimming in
the wake of their drag-reducing slime. This behavior
might have been sufficient for some ancestral
juveniles to have begun swimming close together.

We also would expect the same
environmental pressures — namely, to avoid
predation and to increase competitive ability that
favor modern schooling fishes — to increase the
survival rate of ancestral juveniles swimming in
groups. The more solitary juveniles might have
been selected against by predators or they may have
been out-competed for limited resources, such as
food, shelter, or territory. Thus we would expect
ecological factors to have selected for genetically
programmed schooling patterns.

Once a pattern of schooling becomes
established in juveniles, the general schooling
behavior seen in many mature fishes can be

explained by selection pressures acting on the
timing of development or certain behaviors. For
example, the onset of avoidance or aggressive
behaviors may gradually have been delayed or lost
in maturing schoolers. Juvenile behaviors, such as
interattraction and following, that had adaptive
value in groups might have been retained in
maturing individuals through neoteny (delayed
development). Selection operating on each species
of generalized schoolers then could have favored
specialized mechanisms to control the synchrony
and structure of schools, leading to different
strategies for finding food and avoiding predators.
Of course, this is what we find today: a constellation
of generalized schooling behaviors similar in many
fishes, along with specialized patterns that serve the
divergent lifestyles of each separate species.

In summary, we have seen in juvenilefishthe
gradual, ordered unfolding of schooling that is
highly resistant to changes in early social
environment and the loss of sensory input. The
simple behaviors of juveniles are elaborated in
adults to form specialized schooling adaptations
that aid fishes with diverse lifestyles to feed and
avoid becoming food for others. Thus schooling
provides fishes with not one, but a whole complex
of ecologically adaptive advantages. A better
understanding of the form and biological function
of fish schooling will help us to use, protect, and
appreciate a resource that supports our fishing
industries, supplying the world with high-protein
food and valuable by-products. Beyond these
practical considerations, it is certain that the grace
and beauty of great schools of ocean fish will
continue to stimulate and intrigue the minds of men
and women for generations to come.

). Wesley Burgess is a postdoctoral researcher on fish
schooling in the laboratory of Evelyn Shaw at Stanford
University. Evelyn Shaw is an Adjunct Professor in the
Department of Biological Sciences.

16

References

Baylor, E. R., and E. Shaw. 1962. Refractive error and vision in

fishes. Science 136: 157-158.
Belyayev, V. V., and C. V. Zuyev. 1969. Hydrodynamic hypothesis

of school formation in fishes. Journal of Ichthyology 9: 578-584.
Breder, C. M., Jr. 1954. Equations descriptive of fish schools and

other animal aggregations. fco/ogx35: 361-370.
. 1967. On the survival value of fish schools. Zoologica 52:

25-40.
— . 1976. Fish schools as operational structures. Fishery Bull.

74:471-502.
Brock, V. E., and R. H. Riffenburgh. 1960. Fish schooling: a possible

factor in reducing predation. ]. Conseil Perm. Internal. Explor.

Mer. 25:307-317.
Cahn, P. H., E. H. Atz, and E. Shaw. 1965. Lateral-line nerve

differentiation correlated with schooling in the marine fish

Menidia. Amer. Zoo/. 5: 142.
Cahn, P. H., E. Shaw, and E. H. Atz. 1968. Lateral-line histology as

related to the development of schooling in the atherinid fish

Menidia. Bull, of Marine Sci. 18: 660-670.
Coulson, J. C., and E. White. 1956. A study of the colonies of the

kittiwakeK/ssa tridactyla (L). Ibis 98: 63-79.
Cullen, ). M., E. Shaw, and H. A. Baldwin. 1965. Methods for

measuring the three-dimensional structure of fish schools.

Anim. Behav. 13: 534-543.
Gushing, D. H., and F. R. Harden-Jones. 1968. Why dofish school?

Nafure218: 918-920.
Darling, F. F. 1938. Bird flocks and the breeding cycle: A

contribution to thestudyofavian sociality. Cambridge, Mass. :

Cambridge Univ. Press.
Disler, N. N. 1950. Development of the sense organs of the lateral

line system of the perch and ruff. Trudy Inst. Morfol. Zhirol.

/men. A. N. Severtsova, Vyn. 2: 85-139.
Eggers, D. M. 1976. Theoretical effect of schooling by

planktivorous fish predators on rate of prey consumption. I.

Fisheries Res. Board of Canada 33: 1964-1971.
Eibl-Eibesfeldt, 1.1962. Freiwasserbeobachtungen zur Deutung

des Schwarm verhaltens verschiedener fische. Zeitschrift

Tierpsychologie 19: 165-182.
Fishelson, L., D. Popper, and N. Cunderman. 1971. Diurnal cyclic

behavior of Pempheris oualensis Cuv. & Val. (Pempheridae:

Teleostei)./. ofNatur. Hist. 5: 503-506.
Hamilton, W. D. 1971. Geometry for the selfish herd./. ofTheor.

Biol. 31:295-311.
Healey, M. C., and R. Prieston. 1973. The interrelationships

between individuals in a fish school. Fisheries Res. Board of

Canada Tech. Reports 389: 1-15.
Hobson, E. 1968. Predatory behavior of some shore fishes in the

Gulf of California. U.S. Bureau of Sport Fisheries and Wildlife

Res. Reports 73: 1-92.
Hunter, J. R. 1968. Effects of light on schooling and feeding of jack

mackerel Trachurus symmetricus. J. Fisheries Res. Board of

Canada 25 : 393-407.
— . 1972. Swimming and feeding behavior of larval anchovy

Engraulismordax. Fisheries Bull. 70: 821-838.
Jorne-Safriel,O.,and E. Shaw. 1966. The development of schooling

in the atherinid fish Af/ier/na mochon (Cuvier). Pubbl. Staz.

Zoo/. Napoli 35: 76-88.
McFarland, W. N., and S. A. Moss. 1967. Internal behavior in fish

schools. Science 156: 260-262.
Magnuson, J. )., and ). H. Prescott. 1966. Courtship, locomotion,

feeding and miscellaneous behaviors of Pacific bonito (Sarda

chiliensis). Anim. Behav. 14: 54-67.
Major, P. F. 1977. Predator-prey interactions in schooling fishes

during periods of twilight: A study of the silverside Pranesus

isularum in Hawaii. Fisheries Bull. 75: 415-426.
Manteifel', B. P., and D. V. Radakov. 1960. The adaptive

significance of school behavior in fishes. Russian Rev. of Biol.

50: 338-45.
Moss, S. A., and W. N. McFarland. 1970. The influence of dissolved

oxygen and carbon dioxide on fish schooling behavior. /. Mar.

Biol. 5: 100-107.

O'Connell, C. P., and C. P. Raymond. 1970. The effect of food

density on survival and growth of early post yolk-sac larvae of

the northern anchovy (Engraulis mordax Girard) in the

laboratory. J. Exper. Mar. Biol. and Ecol. 5: 187-197.
Ogden, J. C., and P. R. Ehrlich. 1977. The behavior of heterotypic

resting schools of juvenile grunts (Pomadasyidae).y. Mar. Biol.

10: 273-280.
Olson, F. C. W. 1964. The survival value of fish schooling. ]. Conseil

Perm. Internat. Explor. Mer. 29: 115-116.
Orfeev, Yu-V. 1963. The adaptive role of schooling behavior.

Doklady Akademiya Nauk USSR 152(4).
Pitcher, T. J. 1973. The three-dimensional structure of schools in

the minnow, Phoxinus phoxinus, L. Anim. Behav. 21 : 673-686.
Radakov, D. V. 1973. Schooling in the ecology offish. New York:

John Wiley and Sons, (translated from Russian)
Robertson, D. R., E. A. Fletcher, M. G. Cleland, and H. P. A.

Sweatman. 1976. Schooling as a mechanism for circumventing

territoriality of competitors. Ecology 57: 1208-1220.
Rosen, M. W.,and N. E. Cornford. 1970. Fluid friction of the slime

of aquatic animals. Nav. Undersea Res. Dev. CenterTech. Publ.

N.U.C. T.P. 193: 1-45.
— . 1971. Fluid friction offish slimes. Nature (London) 234:

49-51 .
Shaw, E. 1960. The development of schooling behavior in fishes.

Physiol.Zool. 32: 79-86.
— . 1961 . The development of schooling in fishes II . Physiol.

Zoo/. 34: 263-272.
— . 1969. The duration of schooling among fish separated and

those not separated by barriers. Amer. Mus. Novitates 2373:

1-13.
— . 1970. Schooling in fishes: critiqueand review, pp. 452-480.

In Development and evolution of behavior, ed. by L. R.

Aronson, E. Tobach, D. S. Lehrman and J. S. Rosenblatt. San

Francisco: W. H. Freeman and Co.
— . 1975a. Fish in schools. Natur. Hist. October: 40-46.
— . 1975b. Various visual patterns and the optomotor reactions
of atherinid fish Menidia menidia andAtherina mochon during

their preschooling and schooling phases. Pubbl. Staz. Zoo/.

Napoli 39: 187-200.

— . 1978. Schooling fishes. Amer. So. 66(2): 166-175.
Shaw, E., and B. D. Sachs. 1967. Development of theoptomotor

response in the schooling fish Menidia menidia. ]. Comp. and

Physiol. Psych. 63: 385-388.
Symons, P. E. K.1971. Spacing and density in schooling threespine

stickleback (Casterosteus aculeatus) and mummichog

(Fundulus heteroclitus). J. Fisheries Res. Board of Canada 28:

999-1004.
Van Olst, ).C., and ). R. Hunter. 1970. Some aspects of the

organization of fish schools./. Fisheries Res. Board of Canada

27: 1225-1238.
Verheijen, F. ). 1956. Transmission of a flight reaction amongst a

school of fish and the underlying sensory mechanisms.

Experiential!: 202-204.
Welty, J. C. 1934. Experiments in group behavior of fishes. Physiol.

Zoo/. 7: 85-128.
Williams, G. C. 1964. Measurement of consociation among fishes

and comments on the evolution of schooling. Publ. of the

Museum, Michigan State Univ. 2: 349-384.
. 1966. Adaptation and natural selection. Princeton, N.).:

Princeton Univ. Press.
Williams, M. M. 1976. Rearing environments and their effects on

schooling of fishes. Pubbl. Staz. Zoo/. Napoli 40: 238-254.
Williams, M. M., and E. Shaw. 1971. Modifiability of schooling

behavior in fishes: the role of early experience. Amer. Mus.

Novitates 2448: 1-19.
Wilson, E. 0. 1975. Sociobiology. Cambridge, Mass.: Harvard

Univ. Press.
Zuyev, G. V., and V. V. Belyayev. 1970. An experimental study of

the swimming of fish in groups as exemplified by the horse

mackerel Trachurus mediterraneus ponticus Aleev.y.

Ichthyology 10: 545-549.

17

Diving - A New View

of Plankton Biology

by G. Richard Harbison
and Laurence P. Madin

I he principal research tool in plankton biology -
the study of freely drifting organisms — is the towed
net. It has provided the basic data for most of our
knowledge on the distribution, diversity,
productivity, and behavior of zooplankton. In the
last 10 years, an alternative method for studying
these animals has been developed — direct
underwater observation and collection of animals
by divers. The results obtained using this approach
often differ greatly from those derived from net
samples. In situ studies have shown that a great deal
of essential information about the lives of
planktonic animals cannot be learned by collecting
the animals with a net. Diving studies also have
limitations, however, and further progress in
plankton biology will depend on a careful synthesis
of the two methods.

Research by the authors on the natural
history and behavior of large, gelatinous
zooplankton has stressed the importance of in situ
work. Our results, obtained at Woods Hole
Oceanographic Institution, and those of others
elsewhere, have changed the conception of how

Divers connected by tether lines collecting plankton in
North Atlantic. (Photo by Anita Brosius. © 1979)

Setting out for a dive to
observe plankton in the
open ocean. (Photo by
M Vicki McAlister)

many planktonic animals live. This new perspective
is essential to understanding the place of pelagic
animals in the open ocean — one of the largest and
least known of all environments on earth.

It is a very still place. A planktonic animal that
lives in the open sea is generally free from
mechanical stress, such as tidal rips, currents, and
turbulence associated with nearshore
environments. In contrast to many marine
environments, the water of the open ocean is very
clear. Nutrients are dilute, so the plant life is dilute,
and the silt and detritus found close to shore have
settled out long before reaching the open sea.

Another characteristic of this environment is
stability. The great mass of water i n the ocean basins
acts as a buffer against rapid changes in physical
properties. For an animal living there, such
environmental parameters as temperature, salinity,
and oxygen concentration are stable and
predictable. Animals often can seek preferred
conditions simply by swimming up or down in the
water column.

These general environmental characteristics
provide both possibilities and restrictions for the

plankton. The lack of mechanical stress means that
many oceanic animals are much more delicate than
their nearshore relatives. The transparency of the
water makes vision an important sense to many
pelagic animals. The diluteness of the algae, the
primary food source, forces grazing animals to
develop ingenious and efficient methods of
gathering phytoplankton. Filter-feeding animals in
the open sea must be able to process large volumes
of water, or have sensory means of locating dense
concentrations of food. Since the concentration of
the primary producers is low, the numberof grazing
animals per unitvolume also is low, and the
carnivores that prey on them (or on one another)
must also develop effective mechanisms for
collecting or locating their prey.

Without some simplifying assumptions, the
study of the distribution and abundance of plankton
in the open ocean is nearly impossible. One of the
first of these suppositions was formulated in 1885 by
the German oceanographer Victor Hensen, who
stated that "... in the ocean the plankton must be
regularly distributed; . . . from a few catches very
safe estimates can be made upon the conditions of

Meter net tow used to
sample plankton. The
distance across the face of
the net is 1 meter.

20

very great areas of the sea." Clearly, if this is a false
assumption, any truly quantitative study of plankton
is impossible. This central axiom has guided the
course of plankton research to the present day. A
second important assumption is that plankton
nets, if used correctly, can sample representative
fractions of all the different types of animals that
make up the plankton.

But as the technology of plankton sampling
progressed, new techniques and equipment raised
questions about these assumptions. The Hardy
Plankton Recorder* unequivocally demonstrated
that the distribution of plankton is patchy and not
regular. As larger nets that could be towed faster
through the water were built, it became apparent
that some animals had not been caught before-
those that were too fast or too wary. Other forms
were being caught, but escaped through the
meshes or were destroyed by preservatives. Various
statistical procedures and mathematical models
were developed to try to deal with the problems of
patchiness and avoidance.

Thanks to quantitative sampling
methodology, oceanographers know much more
about planktonic animals than they did 100 years
ago. Plankton nets have taught us about the
diversity of planktonic organisms, their abundance
on local scales, and their global distribution. From
net samples, we have been able to deduce or
calculate primary and secondary productivity, life
cycles, migration patterns, and effects of grazing or
predation. Sampling systems are increasingly
sophisticated, and the samples obtained are ever
more precise and well defined. Within the limits of
its underlying assumptions, sampling technology is
an advanced art.

However, the problem with this precision
and sophistication is that it tells us almost nothing
about what individual animals are doing. In fact, it
can indirectly paint a convincing but erroneous
picture of plankton behavior. From assemblages of
dead organisms, samplers seek to reconstruct
patterns of life. The biology of a population is
inferred from statistics and analogy, with the
behavior of individual animals drawn from these
results. As field ecologists we work in a different
way, using in situ observation and specific
experi ments to discover how organ isms function -
what they eat, how they grow, when they
reproduce, how they respond to the stimuli of the

*A collection device developed in the 1930s by Sir Alister
Hardy. It can be towed for long distances and traps a
sample of plankton on a continually moving strip of gauze,
providing a sort of "tape-recording" of changes in
plankton abundance over the length of the tow. The
sampler thus indicates horizontal distribution or
"patchiness" in plankton populations.

surroundings. From this information, we are
constructing a mosaic of the pelagic ecosystem.

Because it had to await suitable technology,
in situ research in marine environments is a
relatively recent pursuit. Nevertheless, it already
has contributed many significant advances to
marine biology. The study of coral reef ecology has
been revolutionized by scuba diving; it is now
unusual to study reefs in any other way. And
manned submersibles have revealed enough about
life on the ocean floor to render dredges and grabs
nearly obsolete. In situ study of zooplankton is the
most recent innovation.

The need for this new approach is apparent
when one considers gelatinous zooplankton — a
mixed group of organisms from many different
phyla that have diffuse, watery bodies. In situ
research, however, can be applied to other
planktonic organisms and phenomena as well. To
illustrate the applications and advantages of such
field work, we will consider two examples from our
own research.

Ctenophores and Amphipods

Ctenophores constitute an entire phylum of
gelatinous animals, most of them planktonic. They
propel themselves through the water by bands of
tiny paddles. All are carnivores. The phylum
contains 25 genera of pelagic forms. About six of
these commonly are found close to shore; and a
great deal of what is known about Ctenophores
comes from the study of three or four of these
genera. Anyone who has spent time on the coast is
likely to have seen Pleurobrachia, the
sea-gooseberry. Marine biologists have known for
some time that these can occur in great numbers,
often with significant effects on the rest of the
plankton. But there have been only scattered
reports of the other 19 genera, and almost never a
mention of Ctenophores in the open ocean.

When we began looking at the upper waters
of the open ocean on dives, we noticed a great
diversity and abundance of Ctenophores. We have
found that 12 genera commonly occur in the
oceanic environment. It is clear why Ctenophores
were hitherto unreported from the open sea-
almost every species is so delicate that it is torn to
unrecognizable shreds by a plankton net.

The most fragile of these, and the
ctenophore that differs most from the typical
sea-gooseberry, is the "Venus Girdle," Cestum
veneris. This animal has a flat, belt-like body that is
upto2meters long, butonlyafewmillimeters thick.
The stomach sits crosswise in the middle of the
band; rows of paddles run down one long edge,
and rows of fine sticky tentacles down the other.
Seen underwater, Cestum is like a wing, moving
slowly forward under the power of its paddles. The
sticky tentacles lie back along the flat sides of the
body, forming a sort of flypaper for small

21

Gelatinous Planktonic

•

Pleurobrachia, the common nearshore sea-gooseberry. (Photo by Laurence Madin)

Eurhamphea vexilligera, an oceanic
ctenophore of the lobate group. (Photo by
Laurence Madin)

Mnemiopsis mccradyi, a ctenophore restricted
to the central and southern Atlantic coast.
(Photo by Neil Swanberg)

Creatures of the Ocean

. '

• I

I

\

Ocyropsis crystallinasvw'ms and catches prey with strong
muscular lobes. (Photo by Laurence Madin)

The widely spread lobes of Leucothea multicornis trap
small crustaceans. (Photo by Laurence Madin)

Feeding only on salps, Lampea panceri na attaches to and slowly digests prey that are too large to engulf. (Photo by
Laurence Madin)

crustaceans to adhere to when they swim into the
ctenophore. The essence of the feed ing mechanism
of Cestum is silent running, but if disturbed it
switches to a rapid wriggling motion and swims
away. We have found Cestum to be the most
common species in the North Atlantic. It was
present on 178 of 445 dives made from 1974 through
1978. In comparison with ctenophores found close
to shore, Cestum veneris is indeed a bizarre
creature, but from the perspective of large-scale
distribution, it is the typical ctenophore.

Other ctenophores catch their food in
different ways. Leucothea, a large member of the
lobate group, extends its filmy lobes to form a sticky
trap up to 20 centimeters in diameter. Copepods
and even larger crustaceans swim into parts of the
lobe, which folds over them and prevents their
escape while fine tentacles draw the prey to the
mouth. In Ocyropsis, the lobes are muscular,
grasping the prey and moving it to the mouth in
seconds. This feeding mechanism enables
Ocyropsis to catch larger and more active prey such
as euphausiids, salps, and small fish.

The large sticky surfaces of Leucothea and
Cestum make food capture and ingestion a
continuous, conveyor-belt process. In contrast,
many smaller ctenophores hang their tentacles out
in the water and catch one prey at a time. Often their
food consists of small crustaceans, but the genus
Lampea has specialized in feeding on salps -
gelatinous tunicates that often are larger than the
ctenophore itself. The body of Lampea is capable of
great extension and can engulf a salp in a matter of
minutes. If the prey is much too large, the
ctenophore fastens to the salp's body and rides
along as a parasite.

Oceanic ctenophores constitute an
important component of the zooplankton,
interacting with other organisms in many different
ways. Indeed, the diversity of form and function in
oceanic ctenophores is so much greater than that
found in any other part of the ocean that we believe
most of the evolution of the phylum occurred in the
open sea.

Scuba diving as a tool for plankton research
can be criticized for its lack of quantitative
precision, compared to plankton nets. Yet in the
case of ctenophores, the precision of a plankton net
is totally misleading. Our crude methods have
already uncovered four times as many genera of
ctenophores in the open ocean as all the net
samples combined. More importantly, observation
and collection by diving have made it possible to
learn how these animals feed, escape predators,
and interact with other organisms.

This elucidation of behavior is best illustrated
by another aspect of our research — the biology of
hyperiid amphipods. These animals are usually the
third or fourth most abundant crustaceans found
during plankton tows in the open ocean. One of our
earliest underwater observations confirmed earlier
speculation that amphipods live on different
gelatinous organisms — medusae, siponophores,
ctenophores, and salps. The number and variety of
amphipods we saw doing this was striking. During
eightyearsof observations, wefound that nearly all
the surface living species, and 31 of a total 72 genera
in the sub-order, are associated with gelatinous
animals. As with ctenophores, the diversity of
feeding behavior nearly matches the diversity of
species.

Checking plankton
samples aboard ship after
diving expedition. (Photo
by Anita Bros/us. © 1979)

24

s

Attaining a meter or more in length, the belt-like Cesium
venerismay be the commonest ctenophore in the Atlantic.
(Photo by Laurence Madin)

Some genera are rather generalized
predators. Oxycephalus, for example, is a large, fast
swimming amphipod that tears ctenophores to
pieces when feeding. But when a female
Oxycephalus is ready to release her juveniles from
the brood pouch, she does so on a large ctenophore
that she herself leaves untouched, using it only to
support heryoung.

Amphipods in the genus Vibilia are
associated exclusively with salps, and live by
stealing food. Sitting near the salp's esophagus,
Vibilia uses its first pair of legs to divert part of the
food collected by its filter-feeding host, juvenile
and female amphipods spend all their lives doing
this inside salps; only the adult males are
free-swimming, visiting females. Another genus
restricted to salps is Lycaea. At least two species in
this group have highly specific associations with
particular species of salps. UnlikeWb/7/a, individual
Lycaea commonly feed on the tissues of their hosts.

Several other hyperiid families specialize on
siphonophores. Eupronoe juveniles are enclosed
totally in the swimming bells (pulsating chambers)
ofForskalia; their legs are so small in relation to their
bodies that they cannot move. The closely related
amphipod Sympronoe walks around on a very
different siphonophore, Rosacea. Some of the
species associated with medusae are immune to the
stinging cells of their hosts, and even eat them; but
others, on siphonophores, can be stung and killed if
they are careless. Among the smallest hyperiid
amphipods are the species of Hyperietta, which
occuronly in radiolarian colonies (gelatinous
masses of microscopic protozoans with symbiotic
algae).

Juvenile amphipods, like these Oxycephalusclausi, often grow up on the body of a gelatinous host, here a Cestum veneris.
(Photo by Douglas Biggs)

25

Beroe cucumispreys on other ctenophores. The holes
were made by the amphipod Hyperoche (upper right).
(Photo by Laurence Madin)

The relationship of hyperiid amphipods to
their hosts is an aquatic parallel to the interactions
among plants and plant-eating insects on land,
exhibiting specificity, diversity, and, probably, a
history of coevolution. The amphipods certainly
are not typical free-swimming plankton, though
they still are treated as such by some plankton
ecologists. Although net samples can be analyzed in
such away as to provide information about
amphipod associations, it is tedious and uncertain.
Direct in situ observation and collection make the
biology of these animals immediately clear.

Other researchers studying plankton in the
field have learned a number of things that could
never be discovered from net collections or
shipboard experiments alone. For example, Ronald
Cilmer, while a student at the University of
California, observed that certain species of
planktonic molluscs called pteropods feed with an
external web of mucus that resembles a spider's
web. The web may be as large as 2 meters across,
and cannot be re-created in a laboratory tank. Other
researchers have described in detail how
amorphous organic aggregates (marine snow) are
formed, and how they function as microcosms for a
great variety of supposedly planktonic plants and
animals. William Hamner, who developed the use
of in situ methods for the study of plankton while at
the University of California, has recently shown that

planktonic shrimp can follow scent trails in the
water to locate food, and has investigated the
swarming behavior of copepods.

A Look Ahead

Field studies of plankton are beginning to
fundamentally alter our conception of animal life in
the open ocean. Direct observation has disclosed a
vast variety of interactions among planktonic
animals. We have learned that there are many ways
to survive in the pelagic environment, with
organisms sometimes behaving differently than we
had thought. Just as importantly, in situ plankton
studies are another step in man's exploration of the
earth, reminding us that remote sensing and robot
devices cannot take the place of the scientist in the
field until we know what it is we want to sense. For
many purposes, it is still cheaper and more effective
for a scientist to don a diving tank and take to the
water.

Although plankton nets and remote devices
will continue to be important in studying plankton,
theirdesign and use can be increasinglydirected by
the kind of data that divers gather. For example,
even though we have found that most ctenophores
are not retrieved by nets, we know that their

Immune to the stings and digestive enzymes of their host,
these Brachyscelus roam at will over the medusa
Aequorea. (Photo by Laurence Madin)

26

Casting a mucus web into
the water around it, the
pteropod Cleba cordata
catches and eats small
particles, living and dead.
(Photo by Laurence Madin)

amphipod parasites can be collected, serving as an
index to the presence of the hosts. Similarly, if we
know predatory relationships, collecting the
predator in a net can suggest the presence of its
prey in the water. Specific elements of an
organism's behavior, once known, can be the basis
of design for sampling methods directed at that
animal. As more is learned aboutthe natural history
of individual plankton, blind sampling can be
replaced by specific and efficient sampling.

For the study of deep-living plankton, we
believe that manned submersibles — equipped for
lock-out diving and on-board experimental work-
will provide the best opportunities to find out what
is really happening in deep waters. The potential for
exciting new research is enormous. Vertical
migrators — squid, mid-water fishes, and
bioluminescent organisms — are only a few of the
animals that could be studied from such a vessel.

Experimental work on behavior, feeding biology,
and sensory physiology could be guided and tested
by field observations.

A great deal of what plankton biologists
presently believe about the animals that inhabit the
open sea is based on catch statistics, laboratory
observations, computer simulation, or analogies
with better known environments. New field studies
are showing that many of the conclusions derived
from these sources are in error. As more and more
plankton biologists begin working underwater,
rather than from the decks of ships, new areas of
research will open up. The next decade of work in
the open sea promises new and exciting
discoveries.

G. Richard Harbison is an Associate Scientist in the Biology
Department of the Woods Hole Oceanographic
Institution. Laurence P. Madin is an Assistant Scientist in
the same department.

Selected Readings

Alldredge, A. L. 1976. Discarded appendicularian houses as
sources of food, surface habitats, and particulate organic
matter in planktonic environments. Limnol. and Oceanog. 21 :
14-23.

Gilmer, R. W. 1972. Free-floating mucus webs: a novel feeding
adaptation in the open ocean. Science 176: 1239-40.

Hamner, P. P., and W. M. Hamner. 1977. Chemosensory tracking
of scent trails by the planktonic shrimp Acefes sibogae
australis. Science 195: 886-88.

Hamner, W. M., L. P. Madin, A. L. Alldredge, R. W. Cilmer, and P.
P. Hamner. 1975. Underwater observations of gelatinous
zooplankton: sampling problems, feeding biology, and
behavior. Limnol. and Oceanog. 20: 907-17.

Hamner, W. M. 1977. Observations at sea of live, tropical

zooplankton. Proceedings of the Symposium on Warm Water
Zooplankton. Coa, India, Oct. 14-19, 1976. Published by
National Institute of Oceanography, Goa, India.

Harbison, G. R., D. C. Biggs, and L. P. Madin. 1977. The

associations of amphipoda hyperiidea with gelatinous

zooplankton — II. Associations with cnidaria, ctenophora and

radiolaria. Deep-Sea Res. 24: 465-88.
Harbison, G. R., L. P. Madin, and N. R. Swanberg. 1978. On the

natural history and distribution of oceanic ctenophores.

Deep-Sea Res. 25: 233-56.
Hardy, A. C. 1965. The open sea: its natural history. Boston, MA:

Houghton Mifflin.
Madin, L. P., and G. R. Harbison. 1977. The associations of

amphipoda hyperiidea with gelatinous zooplankton — I.

Associations with salpidae. Deep-Sea Res. 24: 449-63.
Trent, ). D., A. L. Shanks, and M. W. Silver. 1978. In situ and

laboratory measurements on macroscopic aggregates in

Monterey Bay, California. Limnol. and Oceanog. 23: 626-35.

27

What Drives the Waters of

by G. T. Csanady

/\n issue of considerable public interest at present
is the construction of nuclear power plants. One of
the many concerns voiced by opponents of nuclear
power is the environmental impact of such plants.
U nder f ire from the antinuclear lobby, the two main
regulatory agencies involved — the Nuclear
Regulatory Commission (NRC) and the
Environmental Protection Agency (EPA) — have
been forced to take positions sometimes leading to
a distortion of priorities. One of the most serious
has been the tendency to prohibit waste heat
rejection into the Great Lakes or the coastal ocean
and instead force utility companies to build cooling
towers, where the waste heat resulting from power

generation escapes to the atmosphere rather than
into large bodies of water. Because cooling towers
are costly to build and operate, this has a general
dampen ing effect on new power plant construction
(nuclear or conventional). However, apart from the
extra cost of electricity, cooling tower operation
results in reduced sunlight due to clouds and fog in
the vicinity of large installations, and severe icing of
roads on a fargreater number of days than normal in
any given area.

Significant harmful effects attributable to
waste heat rejected into open coastal waters have
not been found anywhere. In fact, many
conventional (non-nuclear) power stations in

the Continental Shelves?

coastal locations around the world operate
apparently without problems. However, there have
been no detailed studies of the structure and
climatology of coastal currents and mixing
processes. Thereforein recent debates on thesiting
of nuclear power stations, extravagant claims
regarding the long-term buildup of water
temperature in the neighborhood of a projected
coolingwaterdischargecould not be easily refuted.
Meanwhile, the regulatory agencies began
requiring open-ended oceanographic studies of
any such projected discharge, without a clear
guideline as to how the results would be judged.
How much research is enough research? What are
betteror worse sites foroceanic heat disposal? How
is the environmental impact of an oceanic heat
discharge to be estimated and compared with the
rather serious consequences of cooling tower
construction? For regulatory agencies to make
informed licensing decisions, the properties of the
coastal ocean should be thoroughly understood
from a quantitative perspective.

The Woods Hole Oceanographic Institution
has been involved in coastal waters research since
its inception in 1930. In 1974, with financial support
from the Department of Energy, it undertook a
project to build the necessary conceptual
framework for the understanding and prediction of
water movements and mixing processes in the
coastal ocean. Joint experimental work with
Brookhaven National Laboratory (BNL) was carried
out off Tiana Beach, Long Island, New York, to
document the flow properties of the coastal
boundary layer. This layer consists of a band of
water adjacent to an open coast, some 10 kilometers
wide, where motions are strongly influenced by the
presence of the coast and differ in many significant
respects from motions further offshore. This also is
the region of the coastal ocean directly involved in
arguments relating to environmental impact.

In addition to the Long Island experiment,
Woods Hole carried out basic research on the
large-scale oceanic setting of the coastal boundary
layer, the hydrodynamics of the continental

Cooling tower, right, dwarfs the Davis-Besse Nuclear
Power Station in Ohio. The tower was designed to
dissipate 98 percent of the waste heat from the plant to the
atmosphere by means of evaporative cooling. The
remaining 2 percent was to be discharged to Lake Erie.
(Photo courtesy Department of Energy)

Left, the Atlantic off the Long Island coast. (Photo by Peter
Gavin, PR)

shelves. This has led to some important general
insights that help place the environmental impact
question in perspective.

Trapped Pressure Fields

One of the early ideas in coastal oceanography was
that a "mound" of water generated off a straight
open coast could not persist for very long because
surface level disturbances propagate very rapidly
upcoast and downcoast, if not out to sea. High
tides, for example, are mounds of water that come
and go, propagating with speeds approaching 100
kilometers an hour. A few years ago, it was
universally thought that when winds — for example,

during a hurricane — pile up the water against a
local coast, the disturbance propagated away
rapidly. We now know that this is not so. A coastal
mound or hollow of water, if accompanied by an
appropriate distribution of currents, can be quite
persistent. Key factors contributing to the
persistence of mounds or hollows on the surface of
the coastal ocean are, in addition to the wind, the
rotation of the earth, and the changing depth of
shelf and slope regions with distance from shore.

From the physical oceanographer's point of
view, mounds and hollows on the surface represent
a field of pressure in the water below, much the
same as highs and lows on a weather map. In the
region between a high and a low, the water is being
pushed more on the high side than on the low side,
and tends to flow "downhill" from the mound
toward the hollow. However, on a rotating earth,
the relatively small pressure differences in
atmospheric or oceanic highs and lows produce
flow nearly parallel to the high and low contours in a
condition known technically as geostrophic
balance. The rotation of the earth results in a
deflecting force on any moving object, including
moving particles of air or water, known as the
Coriolis force. This force causes moving particles to
be deflected to the right in the Northern
Hemisphere and to the left in the Southern
Hemisphere; the deflection is proportional to the
speed of the moving particle, and to the sine of
geographic latitude. Geostrophic balance is a state
of equilibrium between the Coriolis force and the
push of the water from a region of high to low
pressure.

In a coastal region of variable depth, the
establishment of geostrophic equilibrium is

constrained by continuity. When water flows from a
deeper to a shallower region, the same rate of flow
must be accommodated in a reduced cross section,
so that the speed increases correspondingly.
However, increased speed also means increased
Coriolis force, which requires increased pressure
differences for geostrophic balance, such as
steeper mounds and hollows near the coast. Thus
mounds and hollows, if they are to persist, must
have rather special shapes to satisfy the various
constraints placed upon them.

Using simple coastal zone models, it is
possible to calculate the distribution of highs and
lows that may persist indefinitely with a given
distribution of surface wind. Consider, for example,
the coastline of the Mid-Atlantic Bight (Figure 1).
Average winds in this region are west-north
westerlies, which point more or less directly
offshore in New Jersey, but are more parallel to the
coast off Long Island. The most effective part of the
wind force exerted on the surface of coastal waters
is its projection parallel to the coast, which can
cause relatively unhindered flow. This component
of the wind force is seen to vary from place to place
according to the orientation of the coastline: the
mean wind indicated in Figure 1 has a large
longshore projection off Long Island, a small one off
New Jersey.

The curvature of the coastline — or of the
constant depth contours that are more or less
parallel to the coast — has little influence on the
motions induced by wind or other factors, so that
mathematical models of open coastal regions can
be straight, for the sake of simplicity. The details of
how the depth varies with distance from shore are
more important, but the main physical effect is

Figure 1. Portions of the
coastline of the
Mid-Atlantic Bight near
New York, showing forces
driving the circulation over
a typical ocean continental
shelf. These include the
wind force, freshwater
inflow, and an alongshore
sea-level slope. Inflow and
outflow across open
boundaries of a chosen
shelf region complicate
the mathematical
modelling of these
phenomena.

30

COAST

SEAFLOOR

Figure2. Idealized straight coast and inclined plane beach,
subject to variable longshore wind.

captured by a sloping plane beach model (Figure 2).
The variability of the longshore wind-stress
projection is simply modelled by a sine wave — the
wind blowing upcoast in some regions, downcoast
in others, with smooth variation in between.
Upcoast is taken to be the direction with the coast to
the left, the ocean to the right — for example,
northeastward along the east coast.

The calculated sea level distribution fora
straight, sloping beach under variable longshore
wind is shown in Figure 3, which illustrates a series
of mounds and hollows elongated in a direction at a
small angle to the coast. The elevation or
depression of the surface becomes negligible at
some distance from the coast; or, in common
theoretical terminology, the pressure field is
coastally "trapped." This peculiar distribution of
surface levels results from the combined effect of
earth rotation, bottom slope, and friction: delete
any one of these, and the trapped field disappears.
On the other hand, changing the magnitude of the
bottom slope, or of friction, merely changes the
width of the trapped field. Therefore, one can be
fairly sure that in the more complex natural
geometry of the coastal waters similar trapped fields
also occur.

Model calculations yield a streamline picture
of the flow field that accompanies the pressure field
(Figure 4). Very close to shore the flow is downwind
everywhere: it is upcoast where the wind blows
upcoast, downcoast where the wind blows
downcoast. Far from shore, on the other hand, the
flow is perpendicular to the wind — offshore where
the wind blows upcoast, onshore where the wind
blows downcoast, but always to the right of the
wind. This type of flow is known as Ekman drift in
honor of Waif rid Ekman, the Norwegian theoretical
oceanographer who first explained it. The function
of the coastally trapped pressure field is to bring
about a transition between the downwind flow at
the coast and the Ekman drift far offshore.

Given the physical characteristics of the
continental shelf in the Mid-Atlantic Bight, the
width of the coastally trapped pressure field
(beyond which the elevation disturbance becomes
small) is typically 30 kilometers. Wind effects, with
their localized mounds and hollows tied to the
orientation of the coastline, are therefore strongly
felt within the first 10 kilometers from the coast, in
the coastal boundary layer. Studies of coastal sea
levels, and of level differences between tide gauges
separated by a few hundred kilometers, sometimes
demonstrate such effects with particular clarity.
Bradford Butman, in his Ph.D. thesis (prepared in
the Massachusetts Institute of Technology -
Woods Hole Oceanographic Institution Joint
Program in Oceanography), has contributed the
illustrations reproduced as Figures 5 and 6.

Coastally trapped pressure fields also occur
in response to other factors. The offshore wind
component is somewhat less effective in this regard
(surprisingly, perhaps), but nevertheless important.
Figures 7and 8 show three illustrations of mounds
and hollows caused by a variable offshore wind. The
influx of freshwater, especially from such massive
sources as the St. Lawrence estuary, also generates
a local mound, somewhat downcoast of the
discharge. The St. Lawrence mound apparently
extends over the entire shelf off Nova Scotia and
even portions of the Gulf of Maine. All of these
effects are confined essentially to the vicinity of an

•94 .126 -157 -188 -220 -251 -283 -314

Figure 3. Contours of constant sea level elevation calculated from model, with
idealizations as illustrated in Figure 2. A full "wave" of the wind is shown from ky= -TT to
+ TT. At y = 0, the wind blows with maximum strength to the left. The y axis is the coastline.
Significant elevations are confined to a narrow nearshore band.

31

314 283 251 220 188 157 128

-126 -157 -188 -220 -251 -283 -314

Figure 4. Streamline
picture of steady flow
associated with elevation
pattern of Figure 3.

open coastline, or to pronounced embayments
such as Long Island Sound and the Gulf of Maine.

Shelf Circulation

As one turns one's attention from local influences,
such as coastline orientation or river inflow, to the
larger picture of circulation over major portions of
the continental shelf, one discovers a nearly
uniform mean flow pattern. Along the east coast of
North America, for example, the shelf waters move
generally northeastward from Miami to Cape
Hatteras, and southwestward from the Grand Banks
of Newfoundland to Cape Hatteras. Using various
types of drifting objects, Dean Bumpus of the
Woods Hole Oceanographic Institution and others
have shown that the southwestward drift north of
Cape Hatteras encompasses the entire continental
shelf with the exception of embayments and
nearshore waters, and indeed extends beyond the
shelf-break — the line where the depth begins to
increase more abruptly at the edge of the North
American continental plate. In recent years, Robert

Beardsley of the Woods Hole Oceanographic
Institution and other investigators, utilizing the
newly developed moored current meter, confirmed
that such relatively uniform mean flow patterns
extended over large areas.

The proximate cause of the southwestward
drift north of Cape Hatteras is a sloping down of the
sea surface southwestward. Geodetic levelling
carried out in North America in the 1930s, which at
that time was thought to be quite precise, showed
such a sea level slope. Later work led scientists to
question the accuracy of geodetic levelling and to
reject the result relating to coastal sea level slope.
However, more recent studies on shelf circulation,
including those already mentioned, helped
reestablish the reality of the sea level slope. One
argument is that the water moving toward the
southwest must be running downhill against the
opposing eastward forces of bottom friction and
wind because there is no other plausible force that
could drive it.

NE-SW Component of wind stress at Logan Airport
Sea Level at Boston,
Corrected for Atm Pressure

SEA LEVEL -
WIND STRESS -

'

50

-50

-100

15 20

February 1972

25

^

I

fc

NW-SE Component of wind stress at Logan Airport
Sea Level (Sandwich -Boston)

SEA LEVEL -
WIND STRESS-

February 1972

20

25

d Hi

8

Figure 5. Smoothed history of sea level at Boston for
February 7972, compared with cross-shore component of
wind force as measured at Logan Airport. (From Ph.D.
thesis of Bradford Butman)

Figure 6. Sea-level difference between Sandwich (on Cape
Cod) and Boston, compared with component of wind
force that points alongshore on this region of coast. (From
Ph.D. thesis of Bradford Butman)

32

Figure 7. Hills and valleys on sea surface (greatly
exaggerated vertically) generated by off shore wind varying
sinusoidally alongshore.

Figure 8. Contours of hills and valleys in Figure 7 in an
illustration similar to Figure 3. The skewness of the
contours does not show up well on the three-dimensional
drawing.

Thereare, however, moresubtlecluestothe
presence of a longshore sea level slope. If such a
slope is indeed present, and if it \snot trapped
within a narrow coastal band as in the models
discussed earlier, but is more or less the same at
increasing distances from shore, then its influence
should be stronger as the water gets deeper,
because the force of gravity there acts on a larger
water mass. The larger total gravity force should
drive the deep water faster. Current meter studies
have shown precisely such behavior. Furthermore,
in deeper water — 100 meters or so — the middle of
the water column is outside the direct influence of
wind force or bottom friction and the flow should
be in the geostrophic balance condition described
earlier. This means that where the sea surface
slopes southwestward, an onshore component of
the flow should be superimposed on the
southwestward drift. This again is found to be
present not only over the shelf, but also well
beyond the shelf-break. The result shows not only
that a southwestward slope is present, but also that
it extends, more or less undiminished, a long
distance from shore, quite unlike the trapped fields
discussed previously.

A final, rather intriguing clue to the mean
longshore sea level slope isthe lineof divergenceof
bottom drift discovered by Bumpus. The wind force
over the continental shelf from Cape Hatteras to the
Grand Banks of Newfoundland is generally
eastward, tending to cause strong offshore flow at
the surface, with a return flow in the interior of the
watercolumn, includingthe layer directly above the
sea floor. Freshwater influx adds to the offshore
surface drift, with some compensating onshore
flow near the bottom. A southwestward sea level
slope, on the other hand, induces onshore flow
both near the surf ace and in the middle of the water
column, with a compensating offshore flow near
the sea floor. The flow that results above the sea
floor depends on the relative strength of these

factors. The wi nd force and freshwater i nf luence act
in much the same way everywhere. The gravity force
associated with the sloping level, on theother hand,
depends on depth, being weak in shallow waterand
strong where the wateris relatively deep. Therefore
the wind and freshwater influx "win" in shallow
water nearshore and cause onshore bottom drift. At
about the 60-meter depth line, the relationship
changes and the sea level slope begins to win, so
that the bottom drift is seaward further offshore. A
line of divergence thus occurs in bottom drift near
the 60-meter isobath, as was inferred by Bumpus
from the motion of mushroom-like bottom drifters
that hop over the seabed when dragged along by
bottom currents.

A sea level slope over large regions of the
continental shelf and slope is a much larger-scale
phenomenon than the trapped fields discussed
previously. It is plausible that pressure fields of such
scale relate to deepwater oceanic gyres (basin-wide
circulation of large bodies of water). If a mathematical
model of shelf circulation is constructed, based on
principles similar to the trapped field, but having
the longshore slope impressed at the seaward edge
of the shelf, the observed features of shelf
circulation are reproduced with remarkable
accuracy. In a manner of speaking, the deepwater
gyre drives the larger-scale shelf circulation; or,
more accurately, shelf circulation is a component
(what hydrodynamicists describe as a
boundary-layer component) of a deepwater gyre.

Different regions of the continental shelves
of the world ocean are affected by different
deepwater gyres. Off the east coast, the Gulf Stream
affects the flow from Miami to Cape Hatteras, and
generates a northwestward slope. A narrow,
counterclockwise gyre between the Gulf Stream
and the continental margin generates the
southwestward sea level slope north of Cape
Hatteras. The physical factors responsible for this
latter gyre are not well known (surprisingly perhaps,

33

Figure 9.

Counterclockwise gyre
between the Gulf Stream
and the North American
continent.

in view of its proximity to large North American
population centers) but some reasonable
speculations can be made.

One major factor is the variation of wind
force with distance from shore. Over the warm
waters of the Gulf Stream, the air rises and stirs up
the atmosphere, bringing the faster-moving air
layers above (the jet stream and its surroundings)
into closer contact with the water surface. The result
is a particularly strong eastward wi nd force over the
Gulf Stream, which has been dramatically illustrated
in charts of the wind force by Andrew Bunker and L.
Valentine Worthington of the Woods Hole
Oceanographic Institution. The Ekman drift, which
the wind sets up in the oceanic surface layer, is
much stronger over the Gulf Stream than closer to
shore. The direction of the Ekman drift is generally
offshore in this region, and the sudden increase in
its intensity over the Gulf Stream has the effect of
depleting the surface waters just to its north. A
trough or surface low tends to be generated
between the Stream and the mainland. Low-
pressure regions in the ocean generally migrate
spontaneously westward, leading to a "westward
intensification" of currents, a principle elucidated
by Henry Stommel of Woods Hole some 30 years
ago. If the same effect operates in the narrow region
between the Gulf Stream and the mainland, it
should produce a low with its center shifted close to
Cape Hatteras (Figure 9). Northwest of the low
center, the sea surface slopes down in a generally
southward direction and presumably produces the
effects on the shelf previously discussed.

This conceptual model lacks many details. It
is necessary to investigate what other contributing
factors might be involved in the generation of the
counterclockwise gyre north of the Gulf Stream.
Whatever the outcome of future investigations, we

know today that the leg of this gyre over the shelf
and continental slope transports a large quantity of
water southwestward, about 10 million cubic
meters per second. A small fraction of it — 2 to 3
percent — passes over the continental shelf proper,
depending on precisely where one places the shelf
boundary. This large-scale, counterclockwise gyre
is not a local effect, but is produced by the action of
the atmosphere on the ocean, exerted over many
thousands of square kilometers. Thus this is a
massive natural phenomenon, presumably
changeable over time spans of climatic variations.

A Summing Up

What can one learn from these newly gained
insights into the mechanics of shelf circulation in
terms of such practical matters as power plant
siting? One general result is the awesome scale of
the counterclockwise deepwater gyre north of the
Gulf Stream, which is actually small by oceanic
standards. Its total longshore transport (107m3sec. 1)
is equal to the discharge of 500 Mississippi rivers, all
flowing within some 200 kilometers of the shore.
The waste heat of a thousand large power plants
(1 ,000 megawatts each) would only heat up this
stream by 0.3 degrees Fahrenheit — if, that is, the
radiation of this heat into space could be prevented
somehow.

The only legitimate remaining question is
whether waste heat discharged nearshore can be
efficiently transferred to the vast and dynamically
active offshore mass of water. Local circulations of
the kind we have discussed in connection with
trapped pressure fields are particularly effective in
promoting such exchange. So are differences in
onshore-offshore motions between various parts of
the water column. Direct evidence of the efficiency
of onshore-offshore mixing processes is the rapid

34

disappearance of the freshwater runoff: in an open
coastal region, even very close to land, it is hard to
find freshwaterdiluted less than thirty-fold. Coastal
lagoons discharge heated water on the ebb-cycle of
a summer day into the coastal ocean. As it happens,
the heat emptied on an ebb cycle into the ocean
during a summer day by a medium-sized lagoon is
comparabletothedaily waste heat output of a large
power station. The warm plumes flowing out from
such lagoons are quickly dissipated, their heat
being distributed over a large coastal water mass.
This, in turn, is effectively mixed with the massive
shelf-slope current, and ultimately with the mass of
the world ocean.

Evaluation of the observations recently
carried out in the coastal boundary layer off Long
Island will provide the quantitative background
necessary for making more specific estimates of the
exchange rates between nearshore and offshore
waters. These are expected to be important in
predicting such matters as the concentration in
nearshore waters of heavy metals and of other
undesirable constituents of municipal waste. It also
will be possible to know precisely what degree of
temperature buildup is likely to occur in the vicinity
of any waste heat discharge, even if such a buildup,
in light of the facts presented, is unimportant.
Although legitimate environmental issues exist in
connection with power plant siting (see page 36), it
would appear that waste heat disposal in an open
coastal environment may not be one of them.

C. T. Csanady is a Senior Scientist in the Physical
Oceanography Department of the Woods Hole
Oceanographic Institution.

References

Beardsley, R. C., W. C. Boicourt, and D. V. Hansen. 1976. Physical

oceanography of the mid-Atlantic bight. Special symposia, Vol.

2, pp. 20-34. Amer. Soc. Limnology and Oceanography.
Bumpus, D. F. 1973. A description of the circulation on the

continental shelf of the east coast of the United States. Progr.

Oceanogr. 6: 111-57.
Csanady, G. T. 1978. The arrested topographic wave./. Phys.

Oceanogr. 8: 47-62.
— . In press. The pressure field on the western margin of the

north Atlantic. A Ceophys. Res.

35

Chlorine in the

Marine Environment

by Joel C. Goldman

\-Ji the many hazardous chemicals being
introduced into the marine environment, chlorine
has one of the most paradoxical histories. This
chemical is a powerful oxidizing agent, and its uses
have ranged from the most hideous — it was one of
the many poison gases of World War I — to the
common household cleanser, bleach. Attainment
of the very high standards of public health enjoyed
in the United States, to a large degree, has been
possible through the continuous application of
small doses of chlorine to drinking water supplies.
For example, until the turn of the century,
waterborne outbreaks of two of the deadly killers of
mankind, typhoid fever and cholera, were common
throughout the United States. With the
introduction of chlorine as a disinfecting agent in
municipal water supplies in 1908, the death rate in
the United States from waterborne diseases
dropped dramatically. This result is demonstrated
by the sharp decrease in the incidence of typhoid
fever soon after chlorination was started in one
major American city, Detroit, which receives its
drinking water from a nearby lake (Figure 1).
Today chlorination of municipal water
supplies is a common practice throughout the
United States and in many other parts of the world.
The taste that we sometimes notice in tap water is
the chlorine residual, which is the small excess of
chlorine added to maintain high-level disinfection
of the water supply all the way to the end of the
pipeline at our home or business. In addition,
industrial and other public service uses of chlorine
are extensive. As of 1975, more than 10 million tons
of this chemical were manufactured in the United
States, of which more than 95 percent was used
exclusively for various industrial applications. The
rest, about 400,000 tons, was used for biocidal
functions, such as disinfection of swimming pools,
public water supplies, and wastewaters, and forthe
control of fouling in cooling water systems.

Environmental Impact on Man

In recent years, there has been a growing awareness
among environmentalists and members of the
health professions that the tremendously positive
role chlorine plays in preventing the outbreak of

The San Francisco Bay-delta waterway, one of the
largest estuarine systems in the United States. One of the
most serious threats to marine life in this area is the
residual chlorine present in domestic wastewaters being
discharged directly into the bay. (Photo courtesy U.S.
Army Corps of Engineers)

waterborne diseases may be offset by an insidious,
but as yet poorly understood, threat it poses to man
and his environment.

Because of its great oxidizing power,
chlorine is highly reactive and thus combines in a
variety of ways with both inorganic and organic
compounds. Based on recent evidence, it is now
confirmed that chlorination of waters, such as rivers
and lakes containing relatively large quantities of
organics, can result in the formation of numerous
chlorinated organic compounds, including the
trihalomethanes (most notably chloroform) . These
latter compounds, along with a growing list of other
chlorinated organics (Table 1), are known or
suspected carcinogens and mutagens. Through an
elaborate nationwide surveillance program to
identify and quantify these compounds, the United
States Environmental Protection Agency has found
significant levels of these chlorinated organics in
numerous water supply systems throughout the
country.

Public concern over the widespread
presence of carcinogens in drinking water stems
from the results of two recent epidemiologic
studies in the United States that were popularized
by the news media. It was found that the incidence
rate of gastrointestinal cancers in test populations in
Louisiana and Ohio was significantly higher for
those who drank water originating from surface
water supplies than for those serviced by

X.

Untreated

Chlorinated

Filtered and Chlorinated

Figure 1. The effect of chlorination and filtration on the
death rate from typhoid fever in a typical American city -
Detroit, Michigan — that started chlorination of the public
water supply soon after 7900.

37

Table 1 . Major halogenated compounds found in water
supplies suspected of posing serious health hazards to
man.

C/i/oro-esfers

Bis (2-chloroethyl) ether
Bis (2-chloroisopropyl) ether

Halobenzenes
Chlorobenzenes
Bromobenzenes
Chloro-bromo- benzenes

Ha lot 'or ms
Chloroform

Bromodichloromethane
Dibromochloromethane
Bromoform

groundwater systems. Although chlorinated
organics were not pinpointed as the causative
agents, surface waters tend to contain much greater
organics and require more extensive treatment,
including chlorination, than groundwaters. For
example, the Mississippi River is both the source of
drinking water and the wastewater repository for
numerous communities along its banks, including
New Orleans, where one of the studies was
performed. By the time the flow reaches New
Orleans, very large inputs of organics have
occurred, and the water has been recycled and
chlorinated repeatedly. These facts, together with
the available epidemiologic evidence, make for a
strong cause-effect relationship between
chlorination and increased risks of gastrointestinal
cancer.

Chlorine in the Marine Environment

Our main concern with chlorine in the marine
environment is the potential damage it may do to
the biota, particularly its possible disruption of the
food chain, leading to both aesthetic deterioration
of the coastal environment, and economic hardship
to those who depend on the sea fortheir income.

Chlorine finds its way into the marine
environment by numerous paths (Figure 2) .
Because of its reactivity, uncombined or "free
chlorine" does not exist for long in natural fresh and
marine waters. But, when it combines to form
chlorinated organic compounds, it may persist for
extremely long periods, because many of these
compounds are highly resistant to biological or
chemical oxidation. In a recent study, Robert Jolley,
at the Oak Ridge National Laboratory, identified
more than 50 chlorinated organic compounds
formed upon chlorination of wastewater.
According to his estimates, potentially more than
5,000 tons of these compounds are released
annually into the aquatic environment. And,
because more than a third of our population lives in

coastal areas, mostly in urban centers, a great deal
of this chlorinated organic waste load eventually
finds its way into the coastal marine environment.

Little is known about the effects of these
compounds on various marine species, mainly
because the seriousness of the problem has been
only recently identified. However, it is reasonable
to assume that the potential effects of these
compounds are similar to those of the commercially
prepared chlorinated organics, such as DDT and
PCBs. The main threat is that these compounds are
resistant to degradation so that they are taken up by
organisms and accumulated in biomass
(biomagnified) as smaller marine species are fed
upon by larger organisms. Off the coast of Southern
California, for example, there are numerous ocean
outfalls discharging chlorinated wastewater into the
coastal environment. Recent studies have
uncovered that bottom-dwelling and other fish
species in these areas — such as queenfish,
flounder, kelp bass, and black perch — tend to
accumulate at very high levels such majoridentified
chlorinated organics in discharged wastewaters as
DDT, PCBs, and chlorinated benzenes. During the
spring of 1976, a large number of captive birds in the
Los Angeles City Zoo that suddenly died were found
toexhibit pesticide poisoning. Subsequently, it was
determined that the source of this poison was

Section of outfall pipe near discharge outlet in Santa
Monica Bay, California. Area is nearly five miles from
shore. The white (colonial) animals on top of pipe are
Metridium senile. Fish are various Sebastes. (Photo
courtesy William Bascom, Southern California Coastal
Water Research Project)

38

Figure 2. Sources of
uncombined chlorine and
chlorinated organics in the
coastal marine
environment. The buildup
of chlorinated organics in
rivers occurs as
communities downriver
recycle water with
successively more
chlorine added. The
coastal environment is the
final repository for the
chlorinated organics
formed during transport
down the river.

water supply
(chlorinated)

waste water<^'
(chlorinated)

uncombined

chlorine affecting

organisims

chlorine
added to
condenser

entrained

marine

organisims

accumulated DDT in the bird's food — queenfish
caught in the vicinity of the ocean wastewater
outfalls. In another recent study, it was shown that
two chlorinated compounds associated with
wastewaters, 4-chlororesorcinol and
5-chlororesorcinol, in concentrations as low as 1
microgram per liter, could cause reductions in the
hatching of carp eggs. Clearly, a major research
effort is needed to identify and quantify these
compounds, determine their modes of transport in
the marine environment, and assess their effects on
marine biota.

In contrast to the poorly defined impact of
naturally formed chlorinated organics in the marine
environment, considerably more is known about
the destructive capacity of reactive chlorine.
Reactive chlorine is chemically unstable. It may
combine with ammonium ions to form
chloramines, which are somewhat more stable but
have less biocidal power than free chlorine; but
none of the reactive chlorine compounds persist for
long in the marine environment.

The chemistry of chlorine in seawater is
exceedingly complex. It is now well established that

chlorine reacts with bromide, a conservative
constituent of seawater, to form bromine
compounds. It is these latter halogens that act as
biocides in the marine environment. The relative
biocidal action of chlorine versus bromine is not
well understood, but both sets of compounds have
great destructive power. When chlorine is added to
seawater, two events occur. First, there is a rapid
loss that is associated with the oxidation of organics
present. Second, there is a slower, but persistent
loss that cannot be attributed to any oxidative
reactions. This loss, as measured by any of several
standard analytical techniques, does not appear to
have a saturation limit. Because nothing is known
about the chemistry of this loss and because it is
unique to seawater, the unrecoverable chlorine (in
whatever form) must remain suspect as a potential
biocide. This result presents a serious dilemma to
biologists and environmental scientists because
there is 1) no way of knowing what the fate of the
"lost chlorine" is, and 2) no way of assessing the
environmental impact of a particular chlorine
application.

Reactive chlorine enters the coastal

39

environment primarily in two ways: through
chlorination of wastewaters being discharged
directly into marine or estuarine waters, and
through chlorination of entrained waters used for
cooling in coastal power plants (Figure 2). To gauge
the potential impact of these two sources on marine
biota, it is instructive to examine the results of two
recent environmental studies on the subject.

Wastewater Chlorination

The San Francisco bay-delta waterway is one of the
largest estuarine systems in the United States. More
than five million people live in bordering
communities, and by 2020, the population is
expected to reach 16 million. The bay-delta system
plays a vital role in the affairs of the community and
it is imperative that high standards of water quality
be maintained. To this end, several major
investigations have been undertaken duringthe last
20 years by state and university organizations.
Recently, scientists at the University of California at
Berkeley carried out an extensive study to
determine the sources of toxic material entering the
bay-delta, and the impact of the material on marine
life in that area. In this study, all sources of toxic
material were considered, including industrial,
domestic, and agricultural wastewaters. Through
fish bioassay experiments with elaborate
continuous-flow systems, it was found that one of
the most serious threats to marine life in the
bay-delta was the residue of chlorine present in
domestic wastewaters being discharged directly
into the bay. By simply dechlorinating the

wastewaters through additions of strong reducing
chemicals, such as sodium bisulfide, the toxicity
was completely eliminated. Corroborative evidence
for this finding came from a related study in which a
strong correlation between increased chlorination
of wastewaters discharged into the bay and
reductions in landings of the dungeness crab, once
a commercially important indigenous species, was
found.

By the year 2020, more than two billion
gallons per day of domestic and industrial
wastewaters are expected to be discharged into the
bay-delta. Certain areas, particularly the south bay
where the city of Oakland is located, have minimal
circulation, but nevertheless contribute a sizeable
fraction of the waste load to the waterway. For
obvious public health reasons, disinfection of the
discharged wastewater is required. To control the
releases of pathogenic bacteria into the bay, while
at the same time protecting marine biota from
chlorine toxicity, it has become a standard practice
among municipal wastewater dischargers to the bay
to remove chlorine residuals before final discharge.
Today, most of the chlorinated wastewaters in
California are dechlorinated prior to discharge.

Power Plant Chlorination

Power plants require tremendous quantities of
cooling water to dissipate unused heat energy. It is
estimated that by 1985 almost 700 million gallons per
day of cooling water will be required in the United
States for nuclear-fueled plants located in marine
settings. Water entrained for cooling purposes
contains a variety of marine organisms — from the

POWER

PLANT

MECHANICAL.
PRESSURE, AND
THERMAL SHOCK
DAMAGES

COOLING POND
OR CANAL /

Figure 3. A condenser cooling system and sources of potential biological damage. (Courtesy John Clark, American Littoral
Society)

40

POWER PLANT

ORGANISMS NOT ENTRAINED BUT
DEPENDENT ON SUSCEPTIBLE ORGANISMS

STRIPED BASS

IMMATURE AND MATURE ADULTS

YOUNG-OF.THE.YEAR
(20 DAYS-I YEAR)

•x-

AND

ZOOPLANKTON

STRIPED BASS

EGGS AND LARVAE

STRIPED BASS PREY

ANCHOVIES

AND

YOUNG OF
ALEWIFES
MENHADEN
WHITE PERCH
CROAKER
SPOT

PREY SPECIES
(NO CROAKER OR
MENHADEN EGGS)

MACROPLANKTON
(WATER FLEAS. COPEPODS
MYSIDS. ETC.)

I

SHRIMP AND MUD CRAB
LARVAE AND YOUNG

' 4
PHYTOPLANKTON

ORGANISMS SUSCEPTIBLE
TO ENTRAINMENT

Figure 4. Damage done in an estuarine ecosystem to organisms susceptible to entrainment can affect young-of-the-year
and adult striped bass. (Courtesy John Clark, American Littoral Society)

smallest bacteria to large zooplankton, and even
small fish. Screening devices are usually installed to
prevent entrainment of larger organisms.

To control fouling caused by bacterial slimes
and nuisance larvae, such as barnacles and mussels,
within the condenser system and connecting
pipelines, chlorine is added as a biocide. In
American power plants, chlorine is applied
intermittently, usually for 20- to 30-minute periods,
two to three times daily, whereas in Great Britain
continuous low-level chlorination is practiced.

In the United States chlorination is practiced
in more than 90 percent of the power plants,
representing an annual usage rate of more than
100,000 tons. Hence, the environmental impact of
power plant chlorination is a two-fold problem.
First, entrained organisms are exposed to a shock
doseof chlorinewhenthebiocide isapplied (Figure
3); and second, any chlorine remaining when the
cooling water is returned to the receiving water can
affect organisms in the area. Generally, the
entrainment problem is the more serious of the two
(Figure 4). This is because the easily entrained
plankton and small fish are fragile and, hence,
experience the most severe stresses during power
plant operation. Not only are these organisms
exposed to chlorine, but they suffer severely from
mechanical damage and from heat shock during
entrainment. Edward J. Carpenter, formerly of the
Woods Hole Oceanographic Institution and now at
the State University of New York at Stony Brook, has

outlined in detail the problems associated with
power plant entrainments (see Oceanus, Vol. 18,
No. 1, page 35, 1974).

In a recent three-year study at the Woods
Hole Oceanographic Institution, the effect of
chlorine on marine plankton was examined. The
study involved bioassay experiments with
phytoplankton, zooplankton, larval invertebrates,
and juvenile fish. Because entrained organisms are
exposed to the combined effects of chlorine and
heat shock, any meaningful bioassay must simulate
to some degree these stresses. To meet these
criteria, bioassay systems were developed with the
common features of continuous-flow, short-term
toxicant exposure, and/or heat rise, rapid
elimination of these stresses, and subsequent
long-term observation of the test organisms. Thus
the history of a test species was simulated as it might
pass through an entrainment and enter a receiving
water.

During the three-year study period, a wide
variety of marine species were examined (Table 2).
The results, summarized in Figure 5, revealed
several important trends. There appeared to be a
general pattern of differences in the modes of
chlorine toxicity affecting marine invertebrates and
vertebrates. Juvenile fish responded in a step or
threshold fashion: that is, there were no deaths up
to a certain toxicant level and then all died beyond
that level. On the other hand, the various
invertebrate species responded in a classical

41

Table 2. Marine planktonic species tested for response
to chlorine toxicity in bioassay experiments at the
Woods HoleOceanographic Institution.

Phytoplankton

Test dtatom(Phaeodactylum tricornutum)
Natural assemblages from power plant
entrainments.

Zooplankton

Copepods (Acartia tonsa)
Rotifers (Brachionus plicatilus)
Natural assemblages from power plant
entrainments.

Larval invertebrates

Lobster-stage I and \\(Homarusamericanus)
Oysters — 7 days old (Crassostrea virginica)

Juvenile fish

Winter flounder (Pseudopleuronectes americanus)
Common scup (Stenotomus versicolor)
Killifish (Fundulus heteroclitus)

fashion: a more gradual increase in mortality with
increases in added chlorine. The mode of action of
chlorine on the test organisms appeared to be some
form of metabolic inhibition, but the mechanisms
are still unknown.

1

k.

I

100

50

0

Juvenile Fish

I 1 , I

0.1

0.5

1.0

5.0

100

50

Zooplankton 8
Larvae

0
0.1 0.5 1.0 5.0

ADDED UNCOMBINED CHLORINE - mg/liter

Figure 5. Survival of test species of juvenile fish,
zooplankton, and larvae 48 hours after exposure to varying
concentrations of uncombined chlorine. Experiments
were performed by Dr. Judith Capuzzo at the Woods Hole
Oceanographic Institution.

In addition, it was found that phytoplankton
and zooplankton, organisms low on the food chain
and with relatively short generation periods,
probably are not threatened seriously by power
plant chlorination. This is because only a small
fraction of the natural population of these
organisms are entrained and exposed to chlorine.
In addition, the surviving organisms, once returned
to their natural environment where chlorine is
absent, are capable of renewed growth.

In contrast, the effects of short-term
chlorination on larval species and small fish are
potentially catastrophic. The larval species show
considerable sensitivity to chlorine, measured as
reductions in metabolic rates, at very low
concentrations — for example, less than 0.01
milligram per liter. Even if these organisms survive
entrainment, their subsequent chances for survival
in the receiving water are diminished because they
become more susceptible to predation. Many of the
larval species that display this sensitivity to chlorine
are important marine food resources, such as
lobsters, oysters, clams, and flounder. All of these
organisms spawn intermittently in coastal waters.
Thus, if a significant portion of the larvae of these
species were destroyed by entrainment, there
would be potential for a correspond! ng reduction in
the adult populations over time. Eventually, various
stocks of commercially important species could
become depleted in coastal spawning grounds near
power plants.

Future Prospects

The hazardous effects of chlorine are slowly but
surely being understood; we know that it poses
serious threats to our health, both through direct
exposure and indirectly by altering aquatic food
chains. In recent years, two major conferences on
the environmental impact and health effects of
water chlorination have been held at the Oak Ridge
National Laboratory, bringing together scientists,
engineers, and health specialists to study these
problems. A third conference is planned for this fall.
Thus research activity in this area is intense.
Hopefully, solutions to the problems
mentioned in this article will be at hand in the near
future. Requirements for dechlori nation, such as
already practiced at wastewater treatment plants in
California, would help immensely. But to simply
ban the use of chlorine, before an effective but less
harmful alternative biocide is found, clearly would
be a poor solution. For we would then have to ask,
what would the consequences be? Would we be
willing to turn back to the 19th century, when
waterborne diseases such as typhoid fever and
cholera decimated entire communities? Would we
be willing to accept major reductions in the supply
of electric power because power plant operating
efficiencies were reduced due to fouling problems?

42

Fisherman trying his luck for trout near chlorinated discharge outlet (circle) from Waterville Valley, New Hampshire, waste
treatment plant. (Photo courtesy EPA, Boston)

Clearly, the answer is no. Ideally, a simple solution
would be to find an alternativedisinfectantwith the
same biocidal power as chlorine, but without the
potential for forming carcinogenic compounds.
Unfortunately, virtually all effective biocides have
side properties similar to chlorine. Hence, it is a sad
reality of our modern life that the chemicals that
serve us so well today, hold many hidden dangers
for future generations.

Joel C. Goldman is an Associate Scientist in the Biology
Department of the Woods Hole Oceanographic
Institution.

Selected Readings

Brungs, W. A. 1976. Effects of wastewater and cooling water

chlorination on aquatic life. Environmental Protection Agency

Ecological Research Series Report EPA-600/3-76-098.

Springfield, VA.: National Technical Information Service.
Capuzzo, J. M., J. C. Goldman, ). A. Davidson, and S. A. Lawrence.

1977. Chlorinated cooling waters in the marine environment:

development of effluent guidelines. Mar. Pollut. 8: 161-63.
Esvelt, L. A., W. ). Kaufmann, and R. E. Selleck. 1973. Toxicity

assessment of treated municipal wastewaters. Jour. Water

Pollut. Contr. Fed. 45: 1558-72.
Goldman, ). C., H. L. Quinby, and J. M. Capuzzo. 1979. Chlorine

disappearance in sea-water. Wafer Res. 13: 315-23.
Jolley, R. L., ed. 1977. Water chlorination: environmental impact

and health effects. Vol. 1. Ann-Arbor, Mich.: Ann Arbor

Science,
lolley, R. L., H. Gorchev, and D. H. Hamilton, eds. 1978. Water

chlorination: environmental impact and health effects. Vol. 2.

Ann-Arbor, Mich.: Ann Arbor Science.
White, G.C. 1972. Handbook of chlorination. New York, N.Y.: Van

Nostrand Reinhold.

43

The sponge Callyspongia plicifera, surrounded by
gorgonian corals. (Photo by M. D. Higgs)

The

Search for
Drugs

i^-F

from the
Sea

by D. John Faulkner

/\t the 1967 conference on "Drugs from the Sea"
there were confident predictions that new miracle
drugs could be obtained from marine organisms
within a relatively short period of time. It was
suggested that because of their greater numbers
and variety, marine organisms could yield even
more drugs than terrestrial plants and
microorganisms, which are the source of
approximately half the pharmaceuticals in use.*
However, no new drugs have resulted from
systematic studies of marine organisms. Today even
the most enthusiastic supporters of this research
seem disillusioned, for the proceedings of the 1978
conference were published under the title
"Food-Drugs from the Sea — Myth or Reality?" The
author does not share this disenchantment.

In retrospect, it appears that those who
expected early success in finding new drugs from
marine organisms did not understand the process
of creating a new drug. Most people regard a drug
as a compound prescribed by a physician to cure or
alleviate distress accompanying an illness. They
expect the finished product, which only the
pharmaceutical industry can supply. Yet there is
only one pharmaceutical company that has the full
facilities required to develop a new drug from
marine sources — the Roche Research Institute for
Marine Pharmacology, established in 1974 at Dee
Why, Australia. If studies there prove successful,
other companies will no doubt commit themselves
to marine research. Meanwhile, collaborative
efforts between university research groups and
pharmaceutical companies offer the best hope for
developing drugs from the sea.

The other half are synthetic drugs.

44

Table 1 . Steps in the development of a new drug from a marine organism.

UNIVERSITY
Collection of biological material.

Bioassays on crude extracts (optional).
Chemical studies to isolate and identify pure compounds.
Pharmacological screening of pure compounds.
DISCOVERY OF PURE COMPOUNDS WITH DESIRABLE PHARMACOLOGICAL PROPERTIES

PHARMACY

Chemical synthesis of the compound and close relatives.
Large-scale synthesis and synthesis of radioactive material.
Determination of physical properties and in vivo stability.
Pharmacological screening of all derivatives.
Extended pharmacology in more sophisticated test systems.
Determination of the mode of action.

Metabolic studies.
INDUSTRY
Toxicology.
Formulation.
Clinical studies.

Legal studies, market research, etc.
PRODUCTION OF A NEW DRUG

Analysis of the stages involved in developing
a drug from a marine organism (Table 1) led
researchers at the University of California to define
their goal as "the discovery of pure compounds
with desirable pharmacological properties." The
university researchers can provide sufficient
screeningdataon pure marine products to allowthe
pharmaceutical company to decide whether the
compound should be studied in-house. The
company then can embark on the long and
expensive process of transforming a physiologically
active compound into a useful pharmaceutical
agent. It has been estimated that the development
of a new drug takes at least 10 years and costs more
than $50 million, provided all goes well.

In a typical drug development program, both
the natural compound and a large number of
slightly modified compounds called analogues are
synthesized. Through pharmacological testing, the
analogues are compared with the natural material,
in the hope that they will prove to be more effective
than the natural product, since they are easier to
patent. Even if the natural material is selected,
developing a synthetic product would probably be
cheaper and certainly more reliable than extracting
the same compound from most marine organisms.
The pharmacological screening program, which is
based on a few general screens, must become more

and more sophisticated until the mode of action of
the drug can be determined. The compound must
be synthesized into a radioactive form to be used in
metabolic studies. The toxicity of the compound
and all its metabolites must be determined
according to government regulations. Finally, after
determining the best method of administering the
drug, it must be subjected to stringent clinical trials.
Many compounds have interesting
pharmacological activity but few will be used in
medicine.

A Collaborative Effort

The discovery of marine natural products with
interesting pharmacological properties requires a
close collaboration between chemists and
pharmacologists. Unfortunately, such activity is
discouraged in academia because it runs counterto
the requirement of independent creative research.
Our program at the University of California cannot
be modelled after an industrial one since we must
be independent researchers working toward a
common goal. Our collaborating pharmacologist,
Dr. Robert Jacobs of the University of California at
Santa Barbara, must perform routine assays as part
of the undergraduate and graduate teaching
program, while allowing graduate students to
pursue in-depth pharmacological studies for their

45

thesis research. Fortunately, he found that some
marine natural products can be used as probes to
study the basic principles of pharmacology. By
allowing undergraduates to screen marine natural
products, the service aspect of this research has
become a valuable and exciting educational
experience. Although the screening performed by
Jacobs and his co-workers might be considered
modest by pharmaceutical company standards, the
results have been substantial.

The chemists participating in the program -
Dr. Phillip Crews of the University of California at
Santa Cruz, and Dr. William Fenical and this author
at Scripps Institution of Oceanography — have the
task of supplying the interesting compounds for
pharmacological screening. To preserve
independent areas of research, Dr. Fenical and the
author have undertaken to study marine plants and
marine invertebrates, respectively. This simple
division of interests gives us ample opportunity to
make original contributions to basic research in
marine natural products chemistry, while
participating in an applied research project.

There are many thousands of marine
invertebrates from which we must choose a very
small number to study. Due to the high cost of
collecting marine organisms, we must devise
strategies to obtain a greater percentage of animals
that produce physiologically active compounds
than would be found in a random collection. During
our research, we have used two such strategies that
we refer to as the screening and ecological
approaches.

The screening approach requires that the
investigator select in advance the pharmacological
activity that he wishes to study. He establishes an
assay, and then screens solvent extracts from
hundreds or even thousands of marine organisms
to find those having that particular pharmacological
activity. The extract then must be separated into its
chemical constituents, following the
pharmacological activity by performing the assay
after each step of the separation process, until pure
active compounds have been isolated. Success
depends upon the sophistication of the bioassay
and the length of time required to obtain it. The
bioassay for antimicrobial activity, which requires
no sophisticated equipment and can be performed
overnight, has proven to be an ideal basis for the
screening approach. Unfortunately, the usual
bioassays for potential anti-cancer and
cardiovascular drugs require sophisticated
equipment or animal-care facilities and often take
days or even weeks to obtain results. Using the
screening approach for discovering new
Pharmaceuticals has the advantage of being
methodical, which makes it unlikely to overlook
potential drugs. The disadvantages of this method
are evident in the program to find new anti-cancer

drugs from marine organisms, which has identified
hundreds of active extracts but few, if any, pure
compounds that might be used for the treatment of
cancer.

One of the major problems encountered by
those who use the screening approach requiring a
complicated laboratory-based bioassay is that of
recollecting the active organisms in the quantities
needed fora "bioassay-directed" chemical
purification. Let us suppose that an investigator
makes a random collection of 100 algae and 100
sponges. If he finds that four seaweeds and 10
sponges give extracts that show activity in the
chosen bioassay, he must then re-collect enough
material (up to 10 kilograms) to ensure that he is
able to isolate and identify the active chemicals. He
may be fortunate and find that the seaweed is large,
easily located, and can be collected by hand in the
intertidal zone at low tide. On the other hand, most
of the sponges can only be collected by scuba
diving. The reduced underwater visibility and time
constraints might make re-collection slow or even
impractical, especially when the collection site is
not adjacent to diving facilities. In this situation a
research vessel becomes invaluable.

We began our research on antibiotics from
marine organisms in 1970 aboard R/V Dolphin, a
privately owned motor yacht. Although its
laboratory was compact in comparison with
laboratories ashore, it was ideal for performing
antimicrobial assays in the field. At each collecting
site, we obtained small samples of the most
abundant organisms, homogenized each one in
ethanol , and screened each extract against a variety
of test microorganisms. Since the screening was an
overnight operation, we were able to re-collect
larger quantities of the active organisms the next
day before moving to a new collection site. This
procedure not only made the most efficient use of
the limited storage space aboard, but it also caused
the least ecological impact since only active
organisms were collected.

Our most recent collections were made
during a research cruise on R/V Alpha Helix to
Glover and Lighthouse Reefs in the Caribbean off
the coast of Belize. These coral reefs were selected
because the steep reef slopes are an ideal habitat for
sponges. The vessel had almost everything that was
required for our research, with laboratories well
equipped for both chemical and microbiological
studies. The ship was used as a floating laboratory
and remained in a sheltered anchorage while
collections of marine organisms were made by
teams of scuba divers operating from small boats.
After each collecting trip, the organisms were
sorted, photographed, and stored either in ethanol
or in the ship's large freezer. A portion of each
sample was homogenized forantimicrobial
screening against six representative

46

Inhibition of cell division
in fertilized sea urchin
eggs. C=control (normal
division), T=treatedwith
active material (no
division). (Photo by
R. Jacobs)

microorganisms and for a simple chemical screen
using thin-layer chromatography. We collected
more than 100 sponge samples and found that
higher than 50 percent contained chemicals that
inhibited the growth of one or more of the test
microorganisms (Table 2). It was fortunate that we
were able to freeze sponge samples, for we found
that many antimicrobial compounds decomposed
when stored in ethanol for a month or more.

Since screening is most successful when it is
performed at the collecting site, we must now
develop new bioassays that do not require the use

of rats, mice, and other small mammals. (Imagine
the reaction of the ship's cook when he sees mice
being brought aboard!) Toxicity assays can be
performed on small fish instead of mammals, but
may be of limited value since we do not yet know
enough about fish physiology to determine the
cause of death or mode of action. Dr. Jacobs is
developing a promising bioassay that may enable us
to screen for cytotoxic compounds aboard a
research vessel. The assay consists of adding
extracts of marine organisms to seawater containing
fertilized sea urchin eggs. If the extract is inactive,

Table 2. Antibacterial screening data summary: Lighthouse Reef and Glover Reef, Belize.

Test

Microorganisms

Total

number

(D

(2)

(3)

(4)

(5)

(6)

(7)

(8)

Samples

screened

S. aur.

E. coli

C.alb.

B-392

V. ang.

E. aero.

P. aeru.

B. sub.

Sponge

107

58

19

35

23

26

14

12

46

Algae

7

3

0

1

0

0

0

0

2

Mollusc

1

0

0

0

0

0

0

0

0

Gorgonian

15

0

0

0

0

0

0

0

4

Tunicate

3

1

0

0

0

0

0

0

2

Zooanthids

2

0

0

0

0

0

0

0

0

Tube Worms

1

0

0

0

0

0

0

0

0

Phylum ?

1

0

0

0

0

0

0

0

0

Total

137

62

19

36

23

26

14

12

54

Key to Test Microorganisms: ( 1 ) Staphylococcus aureus, (2) Escherichia coli, (3) Candida albicans, (4) B-392
(marine bacterium), (5) Vibrio anguillarum, (6) Enterobacter aerogenes, (7) Pseudomonas aeruginosa, (8)
Bacillus subtilis.

47

the eggs will undergo synchronous cell division
within 2 to 4 hours; if active, it will inhibit cell
division in the eggs. The potential pharmaceutical
significance of this assay is unknown, since it is
difficult to correlate activity in an invertebrate
system with corresponding activity in a mammalian
system. However, many of the compounds used in
cancerchemotherapyalsoinhibitcell division inthe
sea urchin assay. This rapid assay might be used to
locate cytotoxic compounds that then could be sent
for the more rigorous and time-consuming
screening in mammalian systems.

The results of the large screening programs
have provided a statistical basis as evidence that
there may be many undiscovered pharmaceutical
agents in marine organisms. For example, Dr. A. J.
Weinheimer of the University of Houston and
co-workers at the University of Oklahoma have
shown that more than 10 percent of marine
organisms contain cytotoxic compounds,
compared to 2 to 3 percent of terrestrial species. His
data indicated that cytotoxic compounds are more
likely to be found in marine invertebrates than
marine algae, in sessile rather than mobile
invertebrates, and in tropical rather than temperate
or cold-water environments. These data support
arguments that form the basis of the ecological
approach.

The ecological approach to the discovery of
potential drugs from marine organisms is based on
observing the behavior and interactions of marine
invertebrates in a natural environment. The
organisms that contain interesting chemical
structures are purified and identified prior to
pharmacological screening. We have searched the
literature for clues to the presence of
physiologically active molecules in marine animals.
The most helpful were the reports of toxicity, many
of which had been thoroughly studied previously.
Marine toxins generally are not very good drugs
because theirphysiological activities usually are too
powerful and dangerous, but they are used
frequently in the study of biochemical mechanisms.
Tetrodotoxin is a toxin that is occasionally
responsible for the deaths of those who eat
improperly prepared puffer fish. Despite the fact
that it is used effectively in neurophysiological
studies, tetrodotoxin is too toxic for use as a
pharmaceutical agent.

We have focused our attention on reports of
behavior modification occurring in one organism
caused by chemicals released from a second
organism; of apparently defenseless animals that
lack predators; of organisms that overgrow or
prevent the growth of their neighbors; and of
organisms that live in symbiotic relationships. We
now are able to recognize some of these situations
in the field.

Some of the most striking examples of
behavior modification are the effects of starfish

exudate on various animals. When exposed to the
exudate, limpets and abalone attempt to escape
from the area instead of exhibiting their normal
reaction to disturbance, which is to attach
themselves even more firmly to the substrate. We
and others found that the escape response was
caused by complex mixtures of surfactant
compounds (similar to detergents) called saponins,
which were very difficult to study chemically. With
modern advances in separation science, it is now
possible to obtain pure compounds from the
complex mixtures and to screen them for
pharmacological activity.

There are several groups of marine
organisms that appear defenseless, but have few
predators: soft-bodied sessile invertebrates, such as
tunicates, soft corals and sponges that lack spicules,
and the shell-less molluscs (opistobranchs), which,
though mobile, are too slow to escape from
potential predators. Sea hares are opistobranch
molluscs that always have had an unsavory
reputation. They owe this reputation and their
survival to eating habits. These organisms have
a chemical defense mechanism that uses the
noxious or even toxic halogenated chemicals
produced by certain red algae. They eat the algae,
digesting normal chemicals, but storing the noxious
halogenated chemicals in a special organ known as
the digestive gland. The noxious chemicals then are
transported to the skin of the sea hare, where they
are released in a mucus. The mucus, which contains
the noxious algal metabolites, gives the sea hares an
unpleasant taste and thus discourages predators.
The chemicals stored in the digestive gland of the
sea hare comprise the most interesting ones
that can be obtained from the red algae. In effect,
the sea hares concentrate the compounds that are
of most interest to the chemist and pharmacologist.
The colorful nudibranchs use the same mechanism
to derive a defensive secretion, using chemicals
from their diet of sponges.

The sessile invertebrates, such as sponges,
tunicates, and soft corals, have a special problem of
survival for they are literally sitting targets. Some
sponges manage to hide in crevices or under rocks
while others have sharp spicules of silica built into a
tough dermal layer, but many sponges appear to
have no physical defense mechanism. These
sponges, along with similarly unprotected tunicates
and soft corals, have provided many of the
antibiotics and other pharmacologically active
compounds that have been evaluated by Dr. Jacobs
and nis colleagues. Large sponges without spicules
appear to be the most prolific sources of
interesting, pharmacologically active compounds.

Unusual growth patterns of sessile organisms
also can indicate the production of physiologically
active compounds. Where two organisms compete
for the same substrate, one organism may defeat
the other by exuding a mucus containing a toxic

48

chemical. We have studied a sponge that burrows
into coral heads. To prevent overgrowth by the
coral or by epiphytes, the sponge maintains a clean
area around its oscular opening by exuding a
mucus. The sponge contains a highly active
antimicrobial compound, which is probably in the
mucus and is responsible for its chemical defense.

The study of symbiosis is still in its infancy. It
is recognized that gorgonian corals containing algal
symbionts produce many physiologically active
compounds, including prostaglandins, whereas
gorgonians without symbionts rarely contain large
quantities of secondary metabolites. This suggests
that the production of physiologically active
compounds may be closely linked to the
maintenance of the symbiotic relationships.

Perhaps the most interesting and bizarre
source of antimicrobial compounds was a marine
bacterium that seemed intent on suicide. The
bacterium was difficult to culture in the laboratory
because it died after 2 to 4 days. The marine
bacterium, accustomed to the infinite dilution of
the ocean, produced antimicrobial compounds for
its protection. However, when grown in an
enriched culture medium, the bacterium produced
enough antimicrobial compoundsto inhibit its own
growth, providing an example of autotoxicity. We
isolated the antimicrobial agent and found that it
was as active as the most effective antibiotics
available, but the compound is quite useless as a
drug since it is too toxic to be administered to an
animal.

In case the author has persuaded any reader
that his research is always carefully planned and
methodically executed, he must now confess that
the most unusual chemicals encountered by his
team were isolated from a dried sponge sent in by a
biologist who was working on an unrelated project
at Arno Atoll in the mid-Pacific. This was a reward ing
example of a truly random collection!

Looking Ahead

It is far too early to predict whether the University of
California project will provide the inspiration for
new medicinal agents. We believe it is wrong to
make premature claims based on pharmacological
assays in animals, for we consider a drug to be an
agent that is effective in the treatment of human
illness. Our stance is one of cautious optimism.

We have isolated and identified many marine
natural products with very unusual chemical
structures, including more than 50 compounds
having antimicrobial activity in vitro. When we
began our research, we predicted that we would
have greater success screening pure compounds
than crude extracts. Screening results obtained
duringthefirstyearsupportthis prediction: 22 of 41
pure compounds have shown interesting
pharmacological activity, whereas 6 of 24 extracts

The sea hare Aplysia parvula. (Photo by author)

So deadly is the force of this poison that it
poisons not only those who took it in by
mouth, but also those who touched or
looked at it, as 'Pliny reports, and if a
pregnant woman sees it or even comes
near it, especially if this happens to be
a young woman, she immediately feels
pain in the belly and nausea and then
she has an abortion

The unsavory reputation of the sea hare is captured in this
cartoon by Jeanne Carleton. The quotation above is taken
from Poisonous and Venomous Marine Animals of the
World, Vol. 1, 7965, by Bruce W. Halstead.

49

The sponge Haliclona cinerea. (Photo byj. Thompson)

An antimicrobial assay. An extract from the sponge
Verongia inhibits the growth of two marine bacteria
isolated from the surface of the same sponge. (Photo by
author)

showed sufficient activity to warrant isolation of the
active constituents using bioassay-directed
purification methods. These results are far better
than those to be expected from the random
screening approach. We now know that marine
plants and animals produce many unusual
pharmacologically active compounds, but we also
are aware that only the pharmaceutical industry can
convert these research results into drugs from the
sea.

D. John Faulkner is an Associate Professor of Marine
Chemistry at Scripps Institution of Oceanography,
University of California at San Diego.

Further Reading

Baslow, M. H. 1977. Marine pharmacology. Huntington, N.Y.:

Krieger.
Faulkner, D. }., and W. F. Fenical, eds. 1977. Marine natural

products chemistry. N.Y.: Plenum Press.
Freudenthal, H. D., ed. 1968. Drugs from thesea. Washington,

D.C.: Marine Technology Society.
Kaul, P. N., ed. 1979. Food-drugs from the sea — myth or reality?

Norman, Okla.: University of Oklahoma Press.
Ruggieri, C. D., ed. 1976. Food-drugs from the sea. Washington,

D.C.: Marine Technology Society.
Worthen, L. R., ed. 1973. Food- drugs from the sea. Washington,

D.C.: Marine Technology Society.
Youngken, H. W., Jr., ed. 1970. Food-drugs from thesea.

Washington, D.C.: Marine Technology Society.

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50

i

The
Decline of
Mexico's
Pacific Inshore
Fisheries

by James Russell McGoodwin

IN ow that most of the less-developed countries
have extended their jurisdictional claims overocean
resources out to 200 nautical miles, there is great
enthusiasm among them for promoting new
maritime developments. Many of these nations -
struggling with domestic food shortages and scarce
capital for development — look to their fisheries as
a source of protein-rich foods, and substantial
export income. But before these countries surge
ahead with development of their fisheries, they
should consider the possible consequences of the
strategies available to them, benefiting from the
past experiences of other nations.

Mexico's shrimp industry on the Pacific coast
provides an instructive case. The growth of its
exporttrade has been extraordinary, especially with
regard to the income it has generated (Figure 1).
Today the state-instituted, urban-based industry
boasts seven trawler fleets with more than 450
vessels; 10 freezing, packing, and canning plants;
two fisheries-research institutions; one shipyard;
and two Mexican-owned importing corporations
(chartered in the United States and located in San
Diego, California) . More than 94 percent of the
industry's shrimp catch is sent abroad — some
30,000 metric tons last year, which brought nearly
$80 million in the international marketplace.
Crustaceans are Mexico's leading primary
commodity export: 47 percent of the total value of
all such exports, according to the 1972 Food and
Agriculture Organization Trade Yearbook.

South Sinaloa: A Case in Point

Map 1 shows a number of coastal lagoons, salt
marshes, and estuaries along Mexico's Pacific coast.
These regions are the major inshore fisheries and
the main rearing grounds for commercially
important species of shrimp. In former times, they
also produced great quantities of other seafoods,
particularly oysters and fish.

Although the focus of this article is on the
rural fisheries in the municipio (like a county in the
United States) of Escuinapa, south Sinaloa state, the
situation described is applicable to all of Mexico's
Pacific rural-coastal fisheries. South Sinaloa is
where today's shrimp-export industry had its
beginnings, and where the social, economic, and
political problems accompanying the growth of the
industry have reached their point of greatest strain.
Northward along the lagoons and estuaries of
Sonora, for example, the rural population is
relatively less dense, whereas southward — in the

OVERLEAF

Subsistence fishermen (pescadores libres) shrimp fishing
in the Laguna Los Cahales, south Sinaloa. Such activity is
discouraged by regulations, which reserve production of
exportable marine species for the inshore fishing
cooperatives. (Photo by author)

PRODUCT/ON (THOUSANDS METRIC TONS)

— — rsj no L
3 en o en o en C

281

26, /\
/— 26, \

.288 290
/268\ /

2,4

/ ^

r

'20 1

'241 24, V /
2*2.8

^

168

120 /'34

A/

/ V94

>0 '52 '54 '56 '58 '60 '62 '64 '66 '68 19"
YEAR

Figure 7. Annual offshore shrimp production for Mexico's
Pacific coast, 7950-7970. Source: Institute de Pesca,
Mexico, D. F.

rural regions of the Gulf of Tehuantepec — the
impact of the shrimp-export industry has been less
severe. Nevertheless, living conditions are
distressing in all of Mexico's Pacific rural-coastal
regions.

A Brief History of South Sinaloa

South Sinaloa's inshore fisheries were not always
underdeveloped, nor were their inhabitants as cut
off from marine resources as they are today.
Indeed, people have relied upon this region's rich
coastal resources for at least 8,000 years — perhaps
longer. Evidence of this extensive maritime history
is apparent to even a casual observer.

The coastal region contains numerous shell
mounds, some more than three kilometers long and
180 meters wide, with peaks reaching nearly 11
meters. Not far from Escuinapa, cabecera (head
town) of the municipio by that same name,
archeologists recently discovered a particularly
large shell mound — a protopyramid, perhaps — 21
meters high, quadrilateral in shape, and flat on top.
Radiocarbon dating indicates that this structure was
built about 2,000 years ago, suggesting the
existence of coastal chiefdoms, and perhaps even
nascent states, which subsisted on the region's
seafoods 16 centuries before the arrival of the
Spanish conquerors.

Estimates of the pre-Columbian population
vary and are highly speculative, but some historians
suggest that a relatively dense population inhabited
the coastal plain at the time of the Spanish conquest
(early 16th century). From all indications, these
people were part of the Mesoamerican culture
tradition, the same as the Aztec and Maya. They
built platform mounds and ball courts on the higher
ground behind the coastal zone; decorated their
pottery in the Mesoamerican style; grew corn,
beans, and squash along the river courses; and

52

Sonora-Sinaloa

Canachi

--.*-' SWAMP, FLOOD-AREA

*2000m. ABOVE SEA LEVEL

100

200

KILOMETERS.

Gulf of Tehuantepec

Map 7. Major shrimp fishery regions along Mexico's Pacific coast.

harvested and traded great quantities of seafoods
from the estuaries and lagoons.

The conquest of south Sinaloa brought the
destruction of the aboriginal population. The
I ndians were victims of various diseases introduced
by the Spaniards, and their ranks were further
reduced by a number of factors that were either
non-existent, or at least not as severe, in other parts
of conquest-era Mexico. They had the misfortune of
beingconquered initiallyby NunodeGuzman,one
of the era's most genocidal conquistadores . Later
many were taken as slaves forthe mines in the Sierra

Madre Occidental and for Cuba's sugar plantations.
The scattered few who remained were pushed out
of the region, displaced by the lords of cattle-raising
haciendas. Indeed, the region was effectively
depopulated of indigenous peoples by the 1750s,
and today none inhabit the coastal zone.

For about three centuries the region was
nearly empty of inhabitants, so its abundant marine
resources went unexploited. Then, in the early to
middle 19th century, a trickle of new settlers arrived
— mestizo immigrants from other parts of Mexico.
They settled the coastal lands that became available

53

ar>

Aboriginal shell mound near Venadillo, south Sinaloa.
Shell accumulations — some more than 3 kilometers long
and 180 meters wide, with peaks reaching 77 meters -
indicate the reliance of ancient populations on the marine
resources in this area. (Photo by author)

after Mexico's independence from Spain in 1821 .
Still more immigrants came after the French
occupation in 1867. These new arrivals were quick
to recognize the potential of the region's marine
resources for subsistence and commerce, and soon
south Sinaloa's smoked oysters and salted shrimp
were carried by muleteers across the Sierra to
Durango, and southward toward Guadalajara and
Mexico City.

The landmark event forthese fisheries
occurred in the early 1870s when Chinese
immigrants from Mazatlan visited the region around
Escuinapa, bought large quantities of shrimp and
oysters, and began to sell them to buyers from the
United States, China, and Japan. In this manner,
south Sinaloa's inshore fisheries made their debut
in the international marketplace.

By the outbreak of the Revolution in 1910,
serious conflicts had arisen regarding the region's
marine resources. The Diaz administration granted

exclusive fishing rights to a number of small
companies, and limited subsistence fishing by
regional fishermen not employed by the
companies. During the Revolution, the brief
Madero administration declared that subsistence
fishing activities would be "free, "and not subject to
regulation. Today subsistence fishermen are still
identified as Pescadores libres, but now the term
has a negative connotation because fishing industry
officials use it when referring to fishermen who are
not members of the state-sanctioned rural fishing
cooperatives. Theoretically, subsistence fishing is
still "free," but in actual practice it is greatly
encumbered by various regulations that forbid
shrimp harvesting for most of the year, or that
prohibit such fishing in territories exclusively
reserved for the cooperatives.

By the end of the Revolution, vessels from
Japan and the United States were actively shrimp
trawling along Mexico's Pacific coast. Mexico was
powerless to prevent such incursions at that time,
nor did it have sufficient capital with which to
finance the construction of its own vessels. I nstead,
it attempted to regulate and tax the foreigners
fishing offshore, while developing its own shrimp
export industry in its inshore fisheries.

Offshore, the Japanese eventually gained
preeminence in the international shrimp market,
driving competitors from Mexico's Pacific coast by
the middle 1930s. However, on the eve of World
War II in 1939, Japan abruptly withdrew its fleets
from the area. Mexico finally had decisive control
over all of its Pacific shrimp fisheries; at this
juncture, it began to develop its own offshore
fleets.

Mexico already had developed a system of
State-instituted, inshore fishing cooperatives and
central packing plants. Shortly afterthe Revolution,
the Pacific inshore fisheries were declared federal
territories. Then, with passage of the Ley General de
Cooperativas in 1933, the nation undertook
development of the various "enterprises of State
participation." Cooperatives were established in
the rural areas, along with a number of central
packing plants for export operations. The rural
fishing cooperatives of south Sinaloa and the
packing plant at Escuinapa were the first of their
kind on the Pacific coast.

Nearly all the capital available for these
enterprises went toward the construction of the
regional packing plants. Development of the rural
inshore fishing cooperatives involved little more
than granting exclusive fishing territories and the
recruitment of rural fishermen. The rural
cooperatives required only rudimentary and fairly
inexpensive weirs, which were made of mangrove
posts and erected across tidal channels.

The rural cooperatives were inextricably
bound to the regional packing plants by the terms of
theircharters. They were required toturn overall of

54

Shrimp trawlers with freezing and packing plant in background, Guaymas, Sonora. (Photo by author)

their exportable harvest at prices established
annually by the federal government. Only in the
conduct of their own internal affairs were they
allowed to act as autonomous entities. Initially, this
was not a handicap to the rural cooperativistas :
marine resources were plentiful, the new
organizations accepted nearly all rural fishermen
wishing to join, and prices were such that most
fishermen increased their incomes.

It was the era of the establishment of the
nation's agrarian ejidos (communal, community
farms). The fishing cooperatives similarly were
hailed as important socio-economic reforms.
Proponents claimed that they would raise the
standard of living of rural-coastal inhabitants and
encourage wide participation in the fishing industry
- that the entire nation would benefit from the
production of vitally needed foodstuffs and the
generation of export income. In retrospect,
however, it appears that the generation of export
income was the main reason why fishing
cooperatives were founded, as the reform-oriented
goals soon eroded.

As economic entities, the rural cooperatives
were fairly successful from the time of their
inception through the middle 1960s when Mexico's

offshore shrimp-trawling industry finally
overshadowed them. But long before that they had
begun to suffer from serious problems.

Probably the most severe of these was
corruption, orcaciqui'smo (corrupt,
political-economic bossism). During the Aleman
administration, 1946-1952, caciquismo became
widespread in the cooperatives. In many cases,
corrupt men undertook to run them for their own
personal gain, relegating the cooperativistas to the
status of mere shift laborers. During that period,
analogous situations arose on the nation's ejidos,
particularly those producing export items.

Other serious problems surfaced. While the
federal government appropriated lands and
redistributed them to impoverished campesinos
(peasants) — many of whom were resettling in
Sinaloa from other parts of the nation — south
Sinaloa's rural-coastal population boomed (from
about 8,000 persons in 1935 to nearly 35,000 by
1975). This resulted in increased competition for
local marine resources. Eventually, the rural fishing
cooperatives became entrenched economic
entities, serving only a minority of the rural-coastal
population. They also suffered the effects of
population growth from within; today most of

55

Rural houses around Teacapan, south Sinaloa. Homes in this region lack running water and modern sanitary facilities. The
inhabitants suffer a high incidence of nutritional, infectious, and parasitic diseases. (Photo by author)

south Sinaloa's cooperatives have more members
than they need, with the result that many must share
theirdwindling incomes with marginally productive
members.

Thus by the early 1950s south Sinaloa's
rural-coastal population began to surfer serious
strains. This situation was greatly aggravated by the
introduction of outboard motors and nylon nets.
The use of these motors with large dugout canoes
eased the transport of large nylon nets, which,
because they are nearly invisible underwater,
proved tremendously effective in catching fish.

By then, most of the region's shrimp and
oyster harvest was being sent abroad, so fish that
were abundant in the estuaries and lagoons -
snappers, snook, drumfish, mullet, and others-
became the new mainstays of domestic
consumption. However, the technological
introductions quickly decimated the inshore fish
stocks, reducingthem to very low levels within only
a few years. Rural fishermen speak of former times,
before the introduction of motors and nets, when
the surface waters of the lagoons sometimes
appeared red from the large numbers of snappers
congregated there. This is no longer seen, however.

Continued fishing pressure has prevented the
recovery of these resources, and net fishermen now
rely on secondary species — so called trash fish -
which are converted into fish meal, a high-protein
dietary supplement for poultry and livestock.

Other factors also contributed to the rapid
decline of south Sinaloa's inshore fisheries. Natural
catastrophes, for example, played a part. In 1967,
during the fall rainy season, a particularly severe
flood buried the region's oyster beds under tons of
silt, causing an almost total loss of that resource.
Floods have occurred previously in the region,
sometimes with devastating consequences — in
about 1300 A.D., one similarly destroyed the
region's oyster beds, forcing the fishery to be
partially abandoned for a number of years
thereafter. Following the flood in 1967, the federal
government imposed a moratorium on oyster
harvesting and attempted to reestablish the beds,
but these efforts were only partly successful. The
reduced oyster stocks have been under heavy
pressure by rural campesinos, who illegally harvest
them in orderto provide food fortheirfamilies. The
stocks also have been damaged by contaminants -
mainly chemical pesticides — used in the region's

56

A weir (called a tapo) on theEstero ElMezcal, south Sinaloa. This weir, which belongs to an inshore fishing cooperative, is
not in production. Its fencing has been rolled up and placed on the shore (foreground) so it will not rot. (Photo by author)

agricultural sector and reaching the beds mostly by
runoff processes.

Overshadowing all these disasters, however,
was the development of offshore trawling, which
brought about a corresponding decline in inshore
fisheries. To understand why, the life cycle of
Mexico's commercially important Pacific species of
shrimp, all members of the Penaeid family, must be
examined.

In simplest terms, the shrimp are hatched
from fertilized eggs in the open sea, and then, in the
form of microscopically small larvae, they migrate
up coastal estuaries and into briny lagoons. In those
delicate environments, they spend several months,
growing to what would be recognizable as subadult
shrimp. Finally, they migrate back to sea, reach their
maximal size, and eventually spawn, thus
completing their life cycle. Their seaward migration
is particularly intense during the fall rainy season
when the influx of freshwater greatly reduces the
salinity of the lagoons. It is this movement that
inshore fishermen have relied upon for millennia.

From the perspective of Mexico's offshore
shrimp industry and the marine biologists and
fisheries managers who advise it, harvesting shrimp
while they inhabit the inshore waters is regarded as
poor practice. Inshore harvesting takes the shrimp
out of the ecosystem before they have a chance to
spawn, which potentially threatens the ability of the
resource to recover rapidly. Also, by removing
shrimp before they reach adult size, the
ecosystem's maximum potential shrimp biomass is
not produced. Furthermore, the large shrimp

caught offshore command higher prices per unit of
weight in the international marketplace. Finally,
harvesting shrimp with trawlers is less costly and far
more productive than the low-yield, labor-i ntensive
methods employed by inshore fishermen.

Thus, as Mexico pursued the development
of its shrimp export trade in this century, it
progressively curtailed the inshore shrimp harvest,
dissociating the rural population from a resource
that had been central to subsistence and commerce
(Figure 2). Today the government discourages
fishing by subsistence-oriented pescadores libres,
and permits south Sinaloa's rural cooperatives to

2,500

1950 '52 '54 '56

* MEXICO IMPOSED A MORATORIUM ON
PRODUCTION IN THESE YEARS

58

'60 '62 * '64 * '66
YEAR

'68 1970

Figure 2. Annual shrimp production of south Sinaloa's
major inshore fishing cooperative, 1950-1970. Source:
Mendoza von Borstel, Xavier, Mem. IV Congr. Nac.
Oceanografia (Mexico); 407-418, 1972.

57

Trawlers being constructed at Astilleros del Pacifico (Shipyards of the Pacific), Mazatlan, Sinaloa. Mexico continues to
develop its shrimp-export industry despite evidence that the industry has reached the limits of its growth. (Photo by
author)

harvest shrimp for only 10 to 12 weeks per year,
whereas the offshore trawlers are permitted 35 to 40
weeks of production annually.

South Sinaloa's rural fishermen are aware of
the political events that have marginalized their
traditional way of life. Often, in discussions with
this writer concerning the development of the
offshore trawling industry, they have exclaimed:
"Camaron que duerme se la lleva la marea" (a
shrimp that sleeps is taken by the tide). It is a
statement pregnant with irony, through which they
self-consciously acknowledge their powerlessness
to stem the tide of events that has impoverished
them.

Policy Reconsideration Needed

It would be glib to conclude that the development
of Mexico's Pacific fisheries could have been
otherwise. Hindsight is always clearer than
foresight. When the shrimp export industry was first
organized, the nation badly needed capital to
finance its reconstruction, and, at least initially, the
rural fishing cooperatives did elevate the standard of
living in their areas. In 1933, the post-revolutionary
leaders could not have foreseen the great population
growth to come, and, given the nation's

preoccupation with its agricultural sector at that
time, its reformers should not be blamed for
overemphasizing the development of shrimp
exports.

However, Mexico is now experiencing acute
and widespread food shortages, rising infant
mortality rates, and an exodus of rural poor to the
crowded cities and to the United States. On the
problem of malnutrition in rural Mexico, Dr. Adolfo
Chavez, director of the National Nutrition Institute
in Mexico City, was recently quoted as having said,
"... we see infant mortality rising again. In some
really depressed rural communities, few children
born since 1974 have survived. We have what we call
'generational holes'." Nevertheless, the federal
government continues to announce further
development of the shrimp export industry, despite
evidence that the industry already has reached the
limits of its growth (shrimp stocks have been
declining for a number of years). A few industry
officials question the evidence, pointing out steady
production increases overthe last decade, buttheir
own fisheries biologists state that such increases
only reflect the annual addition of new trawlers to
the fleets. Various methods for increasing shrimp

58

stocks are still being tried; the most important are
dredging projects that would facilitate shrimp
migrations between offshore and inshore waters,
but these do not promise to make much difference
overall.

Furthermore, the industry's dependency on
the international market often places it in a
precarious economic position. In 1971 , for example,
the United States unilaterally imposed a 10-percent
surcharge on import tariffs, which precipitated an
economic crisis throughout Mexico's shrimp
industry. President Echeverria responded by
courting other foreign buyers for Mexican shrimp,
particularly the Japanese, promising to "weaken the
embraceof the North," but such actions were futile.
The United States still purchases most of Mexico's
shrimp exports, and the industry is still highly
vulnerable to the vagaries of the international
marketplace.

Mexico needs to reconsider its policy for the
management and development of its Pacific-coastal
fisheries. It should stress revitalization of the
inshore fisheries, encourage the resurgence of fish
stocks, and relax its restrictions on the activities of
individual subsistence fishermen, or pescadores
libres. Everything possible should be done to
increase supplies to the nation's domestic seafood
markets.

Such a change of policy would not be as
radical as it might first seem, especially considering
the nation's anticipation of great increases in export
income from development of petroleum resources
on the Campeche Banks. With so much potential
income from petroleum, Mexico should not have to
rely as heavily as it has in the past on the export of
foodstuffs.

Of course, few of the less-developed
countries are fortunate enough to have large
underdeveloped reserves of energy resources, but
a great deal still can be learned from studying the
development of Mexico's shrimp export industry.
The Philippines, for example, has both rich shrimp
resources and a large artisanal rural fishing
population, and is now developing its offshore
shrimp fisheries.

Fishing is a small part of the Gross National
Product of most nations. Even in Japan, a nation well
known for its fisheries and maritime traditions, the
value of agricultural output exceeds that of fishing
by 50 times. Thus fishing often is not well
understood as a socio-economic phenomenon.
This sometimes leads national economic planners
to group various forms of fishing under one rubric,
thereby failing to distinguish between crucial
differences, such as subsistence versus commercial
fishing, or inshore versus offshore fishing.
Moreover, many nations may not be aware -
because they lack the appropriate information -
that increased income from fisheries' exports may,
in some cases, be more than offset by the
consequent social and economic costs among
artisanal fishermen in rural-coastal zones.

James Russell McCoodwin is a Fellow in the Marine Policy
and Ocean Management Program, Woods Hole
Oceanographic Institution, and Assistant Professor of
Anthropology (on leave) at the University of Colorado. He
has conducted research in Mexico since 7977.

Selected References

Beals, Ralph L. 1932. The comparative ethnology of northern

Mexico before 1750. Ibero Americana (monograph) 2.

Berkeley, Ca. : University of California Press.
Chevalier, Francois. '\97Q.Landandsociety in colonial Mexico: The

great hacienda. Berkeley, Ca.: The University of California

Press.
Cordell, John C. 1973. Modernization and marginality. Oceanus

5(17):28-33.
Firth, Raymond. 1965. Malay fishermen: Their peasant economy.

London: Routledge and Kegan Paul.
Fraser, Thomas M. 1966. Fishermen of South Thailand. New York,

N.Y.: Holt, Rinehart, and Winston.
Hubbs, Carl I., and Cunnar I. Roden. 1964. Oceanography and

marine life along the Pacific coast of Middle America. In

Handbook of Middle American Indians, Vol. 1, ed. by Robert C.

West. Austin, Tx. : The University of Texas Press.

Kelly, Charles, and Howard D. Winters. 1960. A revision of the
archaeological sequence in Sinaloa, Mexico. American
Antiquity 25 (December).

Nishimura, Asahitaro. 1973. A preliminary report on current trends
in marine anthropology. Occasional Papers of the Center of
Marine Ethnology 1. Tokyo: Waseda University.

Sauer, Carl, and Donald Brand. 1932. Aztatlan. Ibero Americana
(monograph) 1 . Berkeley, Ca. : The University of California
Press.

Scott, Stuart D. etal. ^72. Archeological reconnaissances and
excavations in the marismas nacionales, Sinaloa and Nayarit,
Mexico, 7967-7972. Buffalo, N.Y.: Department of
Anthropology, State University of New York at Buffalo.

Spicer, Edward H. 1969. Northwest Mexico. In Handbook of
Middle American Indians, Volume 8, ed. by Evon Z. Vogt.
Austin, Tx.: The University of Texas Press.

59

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Checks should be made payable to Woods Hole Oceanographic Institution; checks accompanying foreign
orders must be payable in U.S. currency and drawn on a U.S. bank. Address orders to: Oceanus Back
Issues, 1172 Commonwealth Ave., Boston, MA 02134.

ENERGY AND THE SEA, Vol. 17:5, Summer 1974 — One of our most popular issues. There is extractable
energy in the tides, currents, and temperature differences; in the winds that blow over them; in the very
waters themselves. Eight articles discuss these topics as well as the likelihood of finding oil under the deep
ocean floor and of locating nuclear plants offshore. $4.00

MARINE POLLUTION, Vol. 18: 1 , Fall 1974 — Popular controversies, such as the one over whether or not the
seas are "dying," tend to obscure responsible scientific effort to determine what substances we flush into
the ocean, in what amounts, and with what effects. Some progress is being made in the investigation of
radioactive wastes, DDT and PCB, heavy metals, plastics and petroleum. Eleven authors discuss this work as
well as economic and regulatory aspects of marine pollution. $4.00

FOOD FROM THE SEA, Vol. 18:2, Winter 1975 — Fisheries biologists and managers are dealing with the hard
realities of dwindling stocks and increasing international competition for what is left. Seven articles deal
with these problems and point to ways in which harvests can be increased through mariculture, utilization
of unconventional species, and other approaches. $4.00

DEEP-SEA PHOTOGRAPHY, Vol. 18:3, Spring 1975 — A good deal has been written about the use of
hand-held cameras along reefs and in shallow seas. Here eight professionals look at what the camera has
done and can do in the abyssal depths. Topics include the early history of underwater photography,
present equipment and techniques, biological applications, TV in deep-ocean surveys, the role of
photography aboard the submersible/\/wn along the Mid-Atlantic Ridge, and future developments in
deep-sea imaging. $4.00

MARINE BIOMEDICINE, Vol. 19: 2, Winter 1976 — Marine organisms offer exciting advantages as models for
the study of how eel Is and tissues work under both normal and pathological conditions — study lead ing to
better understanding of disease processes. Vision research is being aided by the skate; neural
investigation, bythe squid; workon gout, bythe dogfish. Eight articles discuss these developments, as well
as experimentation involving egg-sperm interactions, bioluminescence, microtubules, and diving
mammals. $3.00

ESTUARIES, Vol. 19:5, Fall 1976 — Of great societal importance, estuaries are complex environments
increasingly subject to stress. The issue deals with their hydrodynamics, nutrient flows, and pollution
patterns, as well as plant and animal life — and the constitutional issues posed by estuarine management.
$4.00

OIL IN COASTAL WATERS, Vol. 20:4, Fall 1977 — Very limited supply. $3.00

60

WH IfllU 3

GENERAL ISSUE, Vol. 21: 3, Summer 1978 — The lead article looks at the future of deep-ocean drilling, which
is at a critical juncture in its development. Another piece — heavily illustrated with sharp, clear micrographs
— describes the role of the scanning electron microscope in marine science. Rounding out the issue are
articles on helium isotopes, seagrasses, red tide and paralytic shellfish poisoning, and the green sea turtle
of the Cayman Islands. $3.00

Oceanus

The Illustrated Magazine
of Marine Science
Published by Woods Hole
Oceanographic Institution

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Oceanus

The Illustrated Magazine
of Marine Science
Published by Woods Hole
Oceanographic Institution

SUBSCRIPTION ORDER FORM

Please make checks payable to Woods Hole Oceanographic Institution.

Checks accompanying foreign orders must be payable in U.S. currency and drawn on a U.S. bank.

(Outside U.S., Possessions, and Canada add $2 per year to domestic rates.)

Please enter my subscription to OCEANUS for

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MARINE MAMMALS, Vol. 21 :2, Spring 1978 — Attitudes toward marine mammals are changing worldwide. I nis
phenomenon is appraised in the issue along with articles on the bowhead whale, the sea otter's interaction with man,
behavioral aspects of the tuna/porpoise problem, strandings, a radio tag for big whales, and strategies for protecting
habitats. $2.00

The 25% discount granted on orders of five or more back copies does not apply to these special sale issues.

Oceanus

Woods Hole Oceanographic Institution
Woods Hole, Mass. 02543

Oceanus

Woods Hole Oceanographic Institution
Woods Hole, Mass. 02543

increasingly subject to stress. The issue deals with their hydrodynamics, nutrient tlows, and pollution
patterns, as well as plant and animal life — and the constitutional issues posed by estuarine management.
$4.00

OIL IN COASTAL WATERS, Vol. 20:4, Fall 1977 — Very limited supply. $3.00

60

IJH IfilU 3

GENERAL ISSUE, Vol. 21 : 3, Summer 1978 — The lead article looks at the future of deep-ocean drilling, which
is at a critical juncture in its development. Another piece — heavily illustrated with sharp, clear micrographs
— describes the role of the scanning electron microscope in marine science. Rounding out the issue are
articles on helium isotopes, seagrasses, red tide and paralytic shellfish poisoning, and the green sea turtle
of the Cayman Islands. $3.00

OCEANS AND CLIMATE, Vol. 21:4, Fall 1978 — This issue examines how the oceans interact with the
atmosphere to affect our climate. Articles deal with the numerous problems involved in climate research,
the El Nino phenomenon, past ice ages, how the ocean heat balance is determined, and the roles of carbon
dioxide, ocean temperatures, and sea ice. $4.00 (Reissue price).

HARVESTING THE SEA, Vol. 22:1, Spring 1979— Although there will be two billion more mouths to feed in
the year 2000, it is doubtful that the global fish harvest will increase much beyond present yields.
Nevertheless, third world countries are looking to more accessible vessel and fishery technology to meet
their protein needs. These topics and others — the effects of the new law of the sea regime, postharvest fish
losses, long-range fisheries, and krill harvesting — are discussed in this issue. Also included are articles on
aquaculture in China, the dangers of introducing exotic species into aquatic ecosystems, and cultural
deterrents to eating fish. $3.00

SEA-FLOOR SPREADING, Vol. 17:3, Winter 1974
AIR-SEA INTERACTION, Vol. 17:4, Spring 1974

OUT OF PRINT THE SOUTHERN OCEAN, Vol. 18:4, Summer 1975

SEAWARD EXPANSION, Vol. 19:1, Fall 1975
OCEAN EDDIES, Vol. 19:3, Spring 1976
GENERAL ISSUE, Vol. 19:4, Summer 1976
HIGH-LEVEL NUCLEAR WASTES IN THE SEABED? Vol. 20:1 , Winter 1977

Special Back Issue Sale!

Fora limited time only, we are offering the following issues at a reduced rate:

SOUND IN THE SEA, Vol. 20:2, Spring 1977 — Beginning with a chronicle of man's use of ocean acoustics, this issue
covers the use of acoustics in navigation, probing the ocean, penetrating the bottom, studying the behavior of whales,
and in marine fisheries. In addition, there is an article on the military uses of acoustics in the era of nuclear submarines.
$2.00

GENERAL ISSUE, Vol. 20:3, Summer 1977 — The controversial 200-mile limit constitutes a mini-theme in this issue,
including its effect on U.S. fisheries, management plans within regional councils, and the complex boundary disputes
between the U.S. and Canada. Other articles deal with the electric and magnetic sense of sharks, the effects of tritium on
ocean dynamics, nitrogen fixation in salt marshes, and the discovery during a recent Galapagos Rift expedition of marine
animal colonies existing on what was thought to be a barren ocean floor. $2.00

THE DEEP SEA, Vol. 21 :1 , Winter 1978— Over the last decade, scientists have become increasingly interested in the deep
waters and sediments of the abyss. Articles in this issue discuss manganese nodules, the rain of particles from surface
waters, sediment transport, population dynamics, mixing of sediments by organ isms, deep-sea microbiology — and the
possible threat to freedom of this kind of research posed by international negotiations. $2.00

MARINE MAMMALS, Vol. 21 :2, Spring 1978 — Attitudes toward marine mammals are changing worldwide. This
phenomenon is appraised in the issue along with articles on the bowhead whale, the sea otter's interaction with man,
behavioral aspects of the tuna/porpoise problem, strandings, a radio tag for big whales, and strategies for protecting
habitats. $2.00

The 25% discount granted on orders of five or more back copies does not apply to these special sale issues.

Oceanus

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