1 1 II II I II || I II M II M ! I I II M I II 1 1 1 II I II I I 1 1 1 II II I I I l| I I I 1 1 ' I 1 1 1 I I I 1 1 I I U 1 1 1 1 1 1 1 I II 1 1 I 1 1 I 1 1 1 1 1 1 1 1 M 1 1 II 1 1 Ml I I M

Oceanus

Volume 24, Number 4, Winter, 1981/82

Oceanus

The International Magazine of Marine Science

Volume 24, Number 4, Winter 1981/82

William H. MacLeish, Editor
Paul R. Ryan, Managing Editor
Ben McKelway,/4ss/'sfanr Editor

Editorial Advisory Board

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

Charles D. Hollister, Dean of Graduate Studies, Woods Hole Oceanographic Institution

Holger W. Jannasch, Senior Scientist, Department of Biology, Woods Hole Oceanographic Institution

Judith T. Kildow, /Associate Professor of Ocean Policy, Department of Ocean Engineering,

Massachusetts Institute of Technology

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

Robert W. Morse, Senior Scientist, Department of Ocean Engineering, Woods Hole Oceanographic Institution

Ned A. Ostenso, Deputy Assistant Administrator for Research and Development; and Director, Office of Sea Grant,

at the National Oceanic and Atmospheric Administration

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

David A. Ross, Senior Scientist, Department of Geology and Geophysics; Sea Grant Coordinator; and Director of the Marine

Policy and Ocean Management Program, Woods Hole Oceanographic Institution

Derek W. Spencer, Associate Director for Research, Woods Hole Oceanographic Institution

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

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. Steele, Director of the Institution

Acknowledgment

The editors would like to acknowledge the
advice and assistance given by Stewart
Springer, Adjunct Curator in Ichthyology,
The Florida State Museum, in the
development of this issue.

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.

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should be addressed to Oceanus Subscription Department, 1172 Commonwealth Avenue, Boston, Mass.
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ION

teert 3

\US REALITY: THE JAWS IMAGE AND SHARK DIVERSITY
'. Compagno
ill into eight majortaxonomic groups, or orders, of grossly unequal size but

5

\ARKS

\en

[em of sharks is not as deficient as previously thought. J 7

1C MECHANISMS
loss
\echanisms of sharks are apt examples of their economy of form and

\ SHARK REPRODUCTION
llbert

' many species of sharks have survived for many millions of years is

leir reproductive success. ^Q

JD BLUE SHARKS

MO

-.PTION IN BLUE SHARKS

i

?an field study, blue sharks appear to respond to electrically simulated

IN SHARKS: IS THE GRA Y REEF SHARK DIFFERENT?

Jelson

larkis the only shark presently known to attack man forviolating a specific

45

\KS: SUPPLY-SIDE ECONOMISTS OF THE SEA
Jruber

iltidisciplinary study is under way to assess the role of the lemon shark in
irine environment.

\EHAVIOR OF THE SCALLOPED HAMMERHEAD

iley

jorts on recent research into the grouping behavior of the scalloped
In the Gulf of California.

Lf NTS: PERSPECTIVES FOR THE FUTURE
\Gruber
)e//enf based on an industrial detergent appears to be a promising

INDEX

79

flMMERS, DIVERS, AND VICTIMS 77

COVER: Drawing of blue shark and graph of its muscle (solid line) and water
temperature (dotted line) over an 18-hour period. Concept by E. Kevin King.

Copyright 1981 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 24, Number 4, Winter 1981/82

William H. MacLeish, Editor
Paul R. Ryan, Managing Editor
Ben McKelway,/4ss/sfanf Editor

Editorial Advisory Board

Edward D. Goldberg, Professor of Chemistry, Scripps Institution of Oceanograpr
Charles D. Hollister, Dean of Graduate Studies, Woods Hole Oceanographic Ins*
Holger W. Jannasch, Senior Scientist, Department of Biology, Woods Hole Ocea
Judith T. Kildow,/\ssoc/afe Professor of Ocean Policy, Department of Ocean Eng
Massachusetts Institute of Technology

John A. Knauss, Dean of the Graduate School of Oceanography, University of Rh
Robert W. Morse, Senior Scientist, Department of Ocean Engineering, Woods H
Ned A. Ostenso, Deputy Assistant Administrator for Research and Development;
at the National Oceanic and Atmospheric Administration

Allan R. Robinson, Gordon McKay Professor of Geophysical Fluid Dynamics, Har
David A. Ross, Senior Scientist, Department of Geology and Geophysics; Sea Gra
Policy and Ocean Management Program, Woods Hole Oceanographic Institutior
Derek W. Spencer, Associate Director for Research, Woods Hole Oceanographic
Allyn C. Vine, Senior Scientist Emeritus, Department of Geology and Geophysics

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. Steele, Director of the Institution

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, W
Massachusetts 02543. Telephone (617) 548-1400.

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Contents

INTRODUCTION
by Perry W. Gilbert 3

LEGEND VERSUS REALITY: THE JAWS IMAGE AND SHARK DIVERSITY

by Leonard J. V. Compagno

Livingsharks fall into eight majortaxonomic groups, ororders, of grossly unequal size but

great antiquity. $

VISION IN SHARKS

by Joel L. Cohen

The visual system of sharks is not as deficient as previously thought. | 7

SHARK FEEDING MECHANISMS

by Sanford A. Moss

The feeding mechanisms of sharks are apt examples of their economy of form and

function. 23

PATTERNS OF SHARK REPRODUCTION

by Perry W. Gilbert

The fact that so many species of sharks have survived for many millions of years is

testimony to their reproductive success. ^Q

TELEMETRY AND BLUE SHARKS
-a photo essay 4Q

ELECTRORECEPTION IN BLUE SHARKS

by Paul R. Ryan

In an open ocean field study, blue sharks appear to respond to electrically simulated

prey. 42

AGGRESSION IN SHARKS: IS THE GRA Y REEF SHARK DIFFERENT?

by Donald R. Nelson

The gray reef shark is the only shark presently known toattackman forviolating a specific

warning display. 45

LEMON SHARKS: SUPPLY-SIDE ECONOMISTS OF THE SEA

by Samuel H. Gruber

A five-year, multidisciplinary study is under way to assess the role of the lemon shark in

the tropical marine environment,

GROUPING BEHAVIOR OF THE SCALLOPED HAMMERHEAD

by A. Peter Klimley

The author reports on recent research into the grouping behavior of the scalloped

hammerhead in the Gulf of California. C

SHARK REPELLENTS: PERSPECTIVES FOR THE FUTURE

by Samuel H. Gruber

A chemical repellent based on an industrial detergent appears to be a promising

agent.

ADVICE TO SWIMMERS, DIVERS, AND VICTIMS 77

INDEX

79

COVER: Drawing of blue shark and graph of its muscle (solid line) and water
temperature (dotted line) over an 18-hour period. Concept by E. Kevin King.

Copyright 1981 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.

k.

Introduction

Photo by Flip Nicklin

From 1957 to 1977, there was a resurgence of
interest in the basic biology and behavior of sharks,
sparked by the United States Navy's commitmentto
the development of more effective shark
deterrents. During these two decades more was
learned about sharks than in the previous 200 years.
It is reassuring to know that, in spite of diminished
funding, a small but dedicated group of
investigators still carries on, using imaginative
approaches implemented by modern technology.
Several of these investigators are represented in this
issue of Oceanus, and their contributions are most
timely and welcome.

The reader will find much new and exciting
information about modern approaches to shark
biology and behavior. Donald R. Nelson, A. Peter
Klimley, and Paul R. Ryan report on field studies
carried out in the open sea on several species of
large sharks. Samuel H. Gruber's ambitious and

Page opposite: a plaster model of the jaws of Carcharodon
megalodon, a prehistoric shark of the Tertiary period that
reached an estimated length of 45 feet. (Photo courtesy of
the American Museum of Natural History)

carefully conceived interdisciplinary approach to
lemon shark energetics and biology, under both
laboratory and field conditions, has already
provided rewarding results. In a second short
paper, Gruber summarizes preliminary
experiments with pardaxin and detergent-like
surfactants which repel sharks under laboratory
conditions. Sanford A. Moss describes in some
detail the various feeding mechanisms in sharks and
correlates these with functional analyses of jaw
movement and diet. Joel L. Cohen reviews the
anatomy of the shark's visual system and remarks on
the distribution of retinal rods and cones as well as
visual projection centers in the brain. I describethe
reproductive patterns of sharks and comment on
theiradaptive significance. Leonard J. V. Compagno
presents a most welcome review of the major orders
and families of living sharks and cites the
ever-increasing number of described genera and
species in each. While all the articles are deserving
of extensive comment, I will call attention to only
two, for historical reasons.

Compagno points out that more than 80
percent of the 300 to 350 species of sharks are less
than 5 feet (average 1.6 meters) in length and that

the 32 species implicated in attacks on humans are
of relatively large size (2.8 meters). These, coupled
with 36 other species considered to be potentially
dangerous, represent about 20 percent of the total
species of living sharks.

Information on the number of attacks on
humans on a worldwide basis in any given year is
unfortunately incomplete. When Leonard P.
Schultz and I started the International Shark Attack
File (SAP) in 1957, we attempted to secure
information on shark attacks from physicians,
divers, scientists, and clipping services throughout
the world, but this effort was only partially
successful. Many areas known to be the scenes of
frequent shark attacks, such as Indonesia, India,
Central America, and South America, were only
spottily represented. Of the 1,652 cases we were
able to compile, H. D. Baldridge reduced 1,165 of
these to a form usable by automatic data retrieval
systems and concluded there was adequate
documentation on 874 cases in which sharks were
considered directly responsible for attacks on
humans. Baldridge's thoughtful analysis was
published in 1974 as "Contributions from the Mote
Marine Laboratory, Volume 1, Number 2." At the
same time, a widely acclaimed popular version of
the report appeared as a Berkley Medallion Book in
paperback entitled Shark Attack.

Based on the limited information in the SAP,
Schultz and I concluded there were 30 to 50
recorded shark attacks per year on humans.
Because we had so few records, or no records at all,
for many of the shark-infested spots in the world,
we estimated that at most there were less than 100
attacks on humans peryear worldwide, and of these
not more than 25 to 30 were fatal. Once the SAP
(now under the direction of John J. McAniff ,
National Underwater Accident Data Center,
University of Rhode Island, P.O. Box 68, Kingston,
R. I., 02881) is reactivated this figure may increase for
in Florida waters alone this year there have been 14
documented shark attacks, two of which were fatal.
Bathers, boaters, and scuba divers, without being
unduly alarmed, may well heed the advice Baldridge
offers in this issue.

Gruber's article entitled "Shark Repellents:
Perspectives for the Future" will probably evoke the
most controversy in this issue and should be of
great interesttothose involved in seeking improved

shark deterrents. The exciting discovery by Dr.
Eugenie Clark and her col leagues that a secretion of
the Moses sole, Pardachirus marmoratus, inhibits
the jaw movement of sharks has sparked the
important line of investigations into the nature of
the toxin, pardaxin. Gruber and Elihau Zlotkin have
carried these studies a step further and, under
laboratory conditions, have found that certain
relatively cheap industrial detergents were ten
times more effective in repelling young lemon
sharks than was the Moses sole extract. We all await
with interest test results of these surfactants on
dangerous sharks in the open sea. Lest we become
too optimistic, it is well to bear in mind Baldridge's
conclusion (in Seaman, 1976) that "incapacitation
would probably be required for terminating
preattack [shark] behavior by chemical means, and
mathematical analyses clearly indicate that this is
not likely to be realized in terms of realistic
quantities of drugs and available exposure times."
Meanwhile, we do have a wide variety of physical
agents that are promising or have proved to be
effective as shark deterrents (Gilbert, P. W., and C.
Gilbert, 1973).

The studies presented in this issue are but a
sampling of the exciting investigations currently
under way. Reference to some of these
investigations will be found in the selected readings
at the end of each article or in other publications
based on presentations at the 1976 New Orleans
Shark Symposium and edited by R. Glenn
Northcutt. As we gain an increased understanding
of the basic biology and behavior of sharks, their
use as biological models in medical research will
certainly increase, and improved measures will be
developed to protect humans and their gear in
shark-infested waters.

^^^1 Perry W. Gilbert

Selected Readings

Gilbert, P. W., and C. Gilbert. 1973. Sharks and shark deterrents.

Underwater journal, 5: 69-79.
Northcutt, R. G., ed. 1977. Recent advances in the biology of

sharks. Amer. Zoo/., 17(2): 287-515.
Seaman, Wm., Jr., ed. 1976. Sharks and man: a perspective. Florida

Sea Grant Report No. 10, pp i-iv, 1-36.

Legend Versus Reality

V

The Jaws Image and Shark Diversity

by Leonard J. V. Compagno

Ihe word "shark" calls up visions of large, toothy,
dangerous marine monsters, rather like the
protagonist of the novel and filmyaws. Many people
may be familiar with sharks that do not fit this
popular image, but the general impression that
sharks can be typified by large and powerful
species, such as the great white shark, persists in
the public media and even in some scientific
literature.

The large, formidable, predatory sharks are
spectacular in appearance and noted for occasional
attacks on human beings, but these are a decided
minority among the approximately 350 species of
sharks that inhabit the world's oceans and tropical
rivers and lakes.

Most sharks are small and innocuous to
humans. I recently compiled data on the total

lengths attained by 296 shark species. Of these,
about 8 percent we re dwarves, reaching between 20
and 40 centimeters long; 42 percent were small,
between 40 centimeters and 1 meter; another 32
percent were of moderate size, between 1 and 2
meters; 6 percent were moderately large, between
2 and 3 meters; about 8 percent were large,
between 3 and 4 meters; and the remaining 4
percent were 4+ meters long. In the sample, 82
percent of the species reached a maximum size in
the range between 20 centimeters and 2 meters. An

Above: although the great white shark, Carcharodon
carcharias, epitomizes sharks to many people, it is unusual
asasuperpredatorof great size, with exceptionally
powerful jaws and teeth that enable it to prey on large
marine vertebrates.

average maximum adult size for these species was
about 1 .5 meters, or 4.9 feet, which is probably
somewhat greater than a grand average of the mean
adult size obtained by the species sampled.

Of about 32 species of sharks definitely
identified in attacks on humans or boats, more than
80 percent are large species between 2 and 8+
meters long. Those sharks implicated in attacks on
humans, and about 36 other species considered
potentially dangerous, comprise about 20 percent
of all species of sharks.

Although sharks are relatively common,
shark attacks on people are not. According to H.
David Baldridge, author of Shark Attack, shark
attacks on a worldwide basis have averaged about 28
a year since 1940 and i n no year up to 1 974 surpassed
56. Data for Baldridge's study was from the
International Shark Attack File (now discontinued)
compiled by the United States Navy and the
Smithsonian Institution. It included more than 1,600
examples of known shark attacks. Although it can
be argued that this data base missed a certain
number of shark attacks in the period covered, the
impression one got from these records and other
information is that the rate of shark attacks on
people is miniscule compared to the massive rate of
human attacks on sharks as reflected in fisheries
statistics.

According to fisheries data gathered by the
Food and Agriculture Organization of the United
Nations and presented m Shark Utilization and
Marketing by R. Kreuzer and R. Ahmed, the world
shark catch for 1976 was about 307,085 metric tons.
If the average shark in this catch weighed
approximately as much astheaverage human being
-say 68 kilos or 150 pounds the catch would be
equivalent to sharks "catching" 4.5 million people!
Clearly, sharks have far more to fear from people
than vice versa.

8 Major Taxonomic Groups

Living sharks fall into eight major taxonomic
groups, or orders, of grossly unequal size but great
antiquity. Most of these date back as fossils to the
Jurassic period of the Mesozoic era, between 130
and 180 million years ago. New finds may push the
living shark orders even further back in time. Sharks
and their relatives, the rays, form one of numerous
major phyletic branches of the class
Chondrichthyes, or cartilaginous fishes. Fossil
shark-like fishes first appeared in the Devonian
period of the Paleozoic era, between 340 and 400
million years ago. They subsequently evolved into
many divergent groups of cartilaginous fishes. Only
two of these groups, the neoselachians (comprising
the eight orders of living sharks and the rays) and
the holocephalians (chimaeras, ratfishes, and
elephant fishes) survive at present. Most of the
other groups of cartilaginous fishes became extinct
at the end of the Permian period and Paleozoic era,
about 230 million years ago.

The diversity of living sharks is indicated in
Table 1 , which lists orders, families, and genera of
living sharks. Numbers of species are presented
parenthetically after each genus and order, and
separately for each family with two or more genera.
The numbers are from a checklist of world sharks I
am preparing for publication by the Food and
Agriculture Organization. It represents a revision
over earlier numbers published in my article on
shark phyletics (Compagno, 1977). The species
numbers given after families and orders represent
minimum numbers of valid species recognized at
this time. Since systematics at the species level is
still in a state of flux for many higher groups of
sharks, it is to be expected that these species
numbers will change as some described species are
synonymized with others and new species are
discovered.

The frilled shark,
Chlamydoselachus
anguineus,/'sa
deep-water, eel-like
hexanchoid with poorly
known habits. Its long,
snake-like mouth,
tri cuspid teeth, and
enlarged, pointed
denticles on its lips may
help it to capture slippery
prey, such as squid.

Table 1 . Orders, families, and genera of living sharks.

ORDER HEXANCHIFORMES (5+). Hexanchoid sharks.

Family Hexanchidae (six-gill and seven-gill sharks): Heptranchias (1 +),Hexanchus (2), Notorynchus (1); (5 + ).
Family Chlamydoselachidae (frilled sharks): Chlamydoselachus (1).

ORDER SQUALIFORMES (70+). Squaloid, or dogfish, sharks.

Family Echinorhinidae (prickly sharks): Echinorhinus (2).

Family Squalidae (dogfish sharks): Aculeola (1), Centrophorus (8+), Centroscyllium (6), Centroscymnus (5-7), Cirrhigaleus (1),
Dalatias (1), Deania (3),Etmopterus (18+),fuprofom/cro/c/es C\),Heteroscymnoides (1),/s/sf/us (2),
Scymnodalatias (\),Scymnodon (3-4),Somn/osus (3 + ?),S</ua//o/os (1),S</ua/us (7+); (64+).

Family Oxynotidae (rough sharks): Oxynotus (4-5?).

ORDER PRISTIOPHORIFORMES (5 + ). Pristiophoroid sharks.
Family Pristiophoridae (sawsharks): Pliotrema C\),Pristiophorus (4-5 + ); (5+).

ORDER SQUATINIFORMES (12+). Squatinoid sharks.
Family Squatinidae (angel sharks): Squatina (12-13?).

ORDER HETERODONTIFORMES (8). Heterodontoid or bullhead sharks.
Family Heterodontidae (bullhead sharks): Heterodontus (8).

ORDER ORECTOLOBIFORMES (27+). Orectoloboid or carpet sharks.
Family Parascyllidae (collared carpet sharks): Cirrhoscyllium (1-3?),Parascx///u/n (4); (5 + ).
Family Brachaeluridae (blind sharks): Brachaelurus (1), Heteroscyllium (1); (2).
Family Orectolobidae (wobbegongs): Eucrossorhinus (1-2?), Orectolobus (5); (6+).
Family Hemiscyllidae (long-tailed carpet sharks): Chiloscyllium (4+i),Hemiscyllium (5); (9+).
Family Ginglymostomatidae (nurse sharks): Ginglymostoma (2), Nebrius (1-2?); (3+).
Family Stegostomatidae (zebra sharks): Stegostoma (1 ?).
Family Rhiniodontidae (whale sharks): Rhincodon (1).*

ORDER LAMNIFORMES (14+). Lamnoid sharks.

Family Odontaspididae (sand tiger sharks): Eugomphodus (1-2?), Odontaspis (1-2?); (2 + ).
Family Pseudocarchariidae (crocodile sharks): Pseudocarcharias (1 ).
Family Mitsukurinidae (goblin sharks): Mitsukurina (1).
Family Alopiidae (thresher sharks): Alopias (3).
Family Cetorhinidae (basking sharks): Cetorhinus (1 ?).

Family Lamnidae (mackerel sharks): Carcharodon (1),lsurus (2),Lamna (2); (5).
Family (unnamed, for "megamouth" shark; 1).

ORDER CARCHARHINIFORMES (199+). Carcharhinoid, or carcharhiniform, sharks.
Family Scyliorhinidae (catsharks): Apristurus (25 + ), Asymbolus (1 ), Atelomycterus (2 + ), Aulohalaelurus (1 ), Cephaloscyllium

(5 + ), Cephalurus (1+),Ga/eus (10),Ha/ae/urus (10),Haploblepharus (3),Holohalaelurus (2),Juncrus (1),

Parmaturus (4),Pentanchus (1) , Poroderma (3),Schroederichthys (4),Scyliorhinus (14); (87+).
Family Proscylliidae (finback catsharks): Ctenacis (1) , Eridacnis (3+?), Collum (\),Proscy Ilium (1 + ?); (6+).
Family Pseudotriakidae (false catsharks): Pseudotriakis (2?).
Family Leptochariidae (slender houndsharks): Leptocharias (1).
Family Triakidae (houndsharks): Furgaleus (1 ?), Galeorhinus (1 ?), Gogolia (1 ), Hemitriakis (2-3?), Hypogaleus (1 ), /ago (3),

Mustelus (24),Scylliogaleus (1), Triakis (5); (39+).

Family Hemigaleidae (weasel sharks): Chaenogaleus (1), Hemigaleus (1), Hemipristis (1),Paragaleus (3 + ?): (6+).
Family Carcharhinidae (requiem sharks): Carcharhinus (32+?),Ca/eocere/o (1?),/sogo/np/iodon (1),/.am/ops/s (1),Loxodon (1),

Negaprion (2),Prionace (]),Rhizoprionodon (7?),Sco//ot/on (1), Triaenodon (2); (49).
Family Sphyrnidae (hammerhead sharks): Eusphyra (1),Sphyrna (8); (9).

*The spell ing of this genus name is in dispute. A ruling on the matter is forthcoming from the International Commission on
Zoological Nomenclature.

Table 2. Numbers of families, genera, and species of living sharks.

Families

Nos. %

Genera
Nos. %

Species (Minimum)

Nos. %

Order Hexanchiformes

2

6.7

4

4.2

5

1.5

Order Squaliformes

3

10.0

19

19.8

70

20.3

Order Pristiophoriformes

1

3.3

2

2.1

5

1.5

Order Squatiniformes

1

3.3

1

1.0

12

3.5

Order Heterodontiformes

1

3.3

1

1.0

8

2.3

Order Orectolobiformes

7

23.3

12

12.5

27

7.8

Order Lamniformes

7

23.3

10

10.4

14

4.1

Order Carcharhiniformes

8

26.7

47

49.0

199

57.8

Totals:

30

100.0

96

100.0

340

100.0

The numbers in Table 1 include a few
undescribed species of /ago (2) and Mustelus (4) in
theTriakidae, and of Paragaleus (1) in the
Hemigaleidae; and the undescribed family, genus,
and species for the bizarre megamouth shark. The
classification follows my paper in Interrelationships
of Fishes (Compagno, 1973).

The eight shark orders, using the criteria of
relative numbers of genera, species, and
morphological diversity, fall into three categories:
the minor groups, the major groups, and the
dominant group (Table 2). The minor groups-
orders Hexanchiformes, Pristiophoriformes,
Squatiniformes, and Heterodontiformes are
relatively undiverse, representing relatively small, if
highly distinctive, adaptive radiations during their
history. The Hexanchiformes were formerly more
varied than at present, but it is doubtful if they ever
approached the present diversity of the
Squaliformes at any period in their history. The
Pristiophoriformes, Squatiniformes, and
Heterodontiformes are essentially monomorphic
groups, with very little past and present diversity.

The major but nondominant orders of
Squaliformes, Orectolobiformes, and Lamniformes
are presently quite diverse in families and genera
(the families of Squaliformes are possibly undersplit
as presently recognized), but are far inferior to the
dominant order Carcharhiniformes in numbers of
genera and species.

The major and dominant groups represent
large adaptive radiations, with dozens of genera and
numerous species. The Lamniformes was formerly
far more diverse in genera and species in the late
Mesozoic and early Cenozoic, but shows an
apparent decline in numbers of genera and
especially in species since the mid-Cenozoic
(possibly due to competition with advanced
Carcharhiniformes).

The Orectolobiformes retains more species,
but its greatest generic and specific diversity is
confined to the Indo-West Pacific especially the

Australian region, where 10 of the 12 orectoloboid
genera and most of the species occur (versus six
genera from the rest of the Indo-West Pacific and
only two genera in the Atlantic and eastern Pacific).
The Squaliformes has a large number of species, but
these mostly complement the Carcharhiniformes
by occurring in habitats with moderate or low
carcharhinoid diversity, such as the upper
continental slopes, higher latitudes, and ocean
basins.

The order Carcharhiniformes predominates
in genera, species, and shark biomass in the
habitats probably optimal for shark diversity. These
include the continental and insular shelves of warm
temperate and tropical marine waters, the upper
continental slope (primarily Scyliorhinidae), and a
few species that enter tropical and temperate rivers
and lakes. Fisheries surveys of tropical and warm
temperate shelf and oceanic environments typically
yield about 96 percent carcharhinoids by number of
individuals compared to other sharks.

With the possible exception of the
hammerhead sharks, the Carcharhiniformes
includes few really specialized sharks with unusual
trophic adaptations or other peculiarities. The
hammerheads are essentially carcharhinid
derivatives with their prebranchial heads modified
as flattened bowplanes (see page 65).

The Squaliformes includes highly specialized
pelagic genera Euprotomicrus, Squaliolus,
Euprotomicroides, Heteroscymnoides, and
especially the semiparasitic "cookie-cutter" sharks,
genus Isistius. It also includes genera with bizarre
body forms (Dean/a, Oxynotus), many genera and
species with luminous organs, and a genus
(Somniosus) with species dwelling in arctic and
subantarctic cold.

The Orectolobiformes includes
bottom-dwelling specialists, such as the flat,
anglerfish-like wobbegongs (Orectolobidae),
slender, crevice-loving hemiscylliids with limb-like
paired fins, theanatomically divergent parascylliids,

8

Several squaloid sharks,
including this pygmy
shark, Euprotomicrus
bispinatus,are oceanic
and have minute,
scattered luminescent
organs on their bodies.
This species is
wide-ranging in warm
oceanic waters, reaches a
maximum length of 27
centimeters, and may
migrate from the surface to
the bottom in a daily cycle.

and the genusStegosfoma with a caudal fin about as
long as the rest of the shark, but also the pelagic,
filter-feeding whale shark.

The small, but highly diverse, order
Lamniformes includes two types of pelagic
filter-feeders, probably separately evolved the
megamouth and the basking sharks the
long-tailed thresher sharks (using their elongated
caudal fins as weapons for feeding), the grotesque
goblin shark, the oceanic crocodile shark, the
high-speed shortfin mako (Isurus oxyrinchus), and
the superpredatory great white shark.

The reasons for the preeminence of the
Carcharhiniformes among modern sharks and the
greater morphological variety within the three
major groups are unclear. The implication is that
carcharhinoids are competitively superior to other
sharks. The advanced carcharhinoid families, such
as the Hemigaleidae, Carcharhinidae, and
Sphyrnidae, may have more efficient feeding
mechanisms (jaws, hyoid arch, and musculature)
and reproduction (placental viviparity) than
noncarcharhinoids and more primitive
carcharhinoids. The wide morphological diversity
among lam noids, orectoloboids, and squaloids may
be due to competitive exclusion of these groups
from more generalized shark niches by
carcharhinoids, optimizing their evolution into
more peripheral specialists. However, all this is
speculatory, and there may be other, more
compelling reasons that explain the relative
numbers and comparative morphological variation
of the Carcharhiniformes and other shark groups.

A Review of Living Sharks

Unfortunately, very little is known of the basic
biology of most sharks, and much of the research on
sharks has been concentrated on species, such as
the spiny dogfish (Squalus acanthias), that occur in
northern temperate waters and are objects of
important fisheries.

The Hexanchiformes, or hexanchoid sharks,
are easily identified by their single, spineless dorsal
fin, anal fin, and six or seven pairs of gill openings
(all other sharks have five, except the six-gill
sawshark, Pliotrema). Hexanchoids are primarily

deep-water, bottom-dwelling, temperate-
to-tropical, continental or insular sharks
with a worldwide distribution and a depth range
from close inshore to at least 1 ,875 meters. The rare
frilled shark, Chlamydoselachus, is elongated and
eel-shaped, with small tricuspid teeth in both jaws
and a terminal mouth. The six-gill and seven-gill
sharks, Hexanchidae, have stouter bodies, large,
comb-like slicing teeth in the lower jaw, and a
subterminal mouth. Frilled sharks reach 196
centimeters in length, while six-gill and seven-gill
sharks range from 137 to 482 centimeters long.
Virtually nothing is known of the frilled shark's
habits, except that it may feed on squid, but the
six-gill and seven-gill sharks are known to take a
wide variety of bony fishes, other sharks, rays,
crustaceans, and carrion for food. All hexanchoids
are aplacentally viviparous, bearing live young.
Some of the larger species, including the
broadnosed six-gill (Hexanchus griseus) and
seven-gill (Notorynchus cepedianus) sharks, are
excellent for food.

The large-tooth cookie-cutter shark, Isistius plutodus,/7as
suctorial lips for clinging to its prey. This shark has the
largest teeth relative to its size of any living shark, about
twice the tooth height to total length ratio of the great
white shark (the species with the physically largest teeth of
any living shark), but reaches a total length of only 42
centimeters.

Head of a Philippine sawshark, Pristiophorus sp. , from the
underside, showing its saw-like snout and rostral barbels.

The Squaliformes, or dogfish sharks, are
cylindrical, compressed, orslightlyflattened sharks
with two spined or spineless dorsal fins and no anal
fin. Like the hexanchoids, squaloid sharks are
mainly inhabitants of deep water near the bottom,
from the continental shelves down to at least 2,700
meters on the slopes and possibly also occurring on
the ocean floor. Several squaloids are pelagic over
the ocean basins, and the common spiny dogfish,
Squalus acanthias, and large sleeper sharks,
Somniosus microcephalus and S. pacificus, can
occur close inshore and even intertidally. Small
unicuspid or tricuspid teeth occur in both jaws of a
few squaloids (Aculeola, Centroscyllium), but most
squaloids have enlarged, compressed, blade-like
teeth in the lower jaw or both jaws. The extreme in
blade-like cutting teeth is seen in the lower jaws of
the cookie-cutter sharks (Isistius), one species of
which (/. plutodus) has the largest teeth in
proportion to body size of any living shark.

Many of the deep-water squaloids are
blackish or dark brown in color, and commonly
have small luminous organs scattered on the body
or in well-marked areas. The majority of squaloids
reach lengths of between 30 and 170 centimeters,
but there are several dwarf species below 30
centimeters and one, Squaliolus laticaudus, that
may be the smallest shark, maturing at 15 to 26
centimeters. In contrast, the large prickly and
bramble sharks, Echinorhinus, reach 3 to 4 meters,
and the large sleeper sharks may exceed 7 meters.
Deep-water squaloids often have very long bodies,
with immense livers serving as hydrostatic organs.

Squaloids usually have cylindrical or
moderately compressed bodies, but the rough
sharks, Oxynotus, have high bodies with a
triangular cross section and high, sail-like dorsal
fins. Squaloids eat a wide variety of fish, other
sharks, rays, crustaceans, and cephalopods. The
cookie-cutter sharks are semiparasitic, with
suctorial lips that enable them to attach to large
bony fishes and cetaceans and core out a plug of
flesh with their huge teeth; they also feed on small
fishes and squid. All squaloids are aplacentally
viviparous. A number of dogfish sharks are
commercially important, especially the spiny
dogfish and the sleeper sharks, supporting large
fisheries. Deep-sea dogfish are prized for the
squalene in their livers, which, among other things,
is used as a base for cosmetics. Squaloid sharks are
generally not considered dangerous to people, but
the sharp teeth and weakly toxic fin spines of some
species can inflict injuries.

The Pristiophoriformes, or sawsharks, have
two dorsal fins and no anal fin like squaloids, but
differ in their greatly attenuated, blade-like snouts
with lateral teeth and long barbels on the
undersides. One sawshark, Pliotrema warreni, has
six pairs of gill openings, but the others, genus
Pristiophorus, have only five. Sawsharks favor

10

The California angel shark,
Squatina californica, a
depressed, ray-like
bottom shark of the
eastern Pacific.

warm-temperate-to-tropical waters and occur in the
western Indian Ocean, western Pacific, and western
North Atlantic in the vicinity of Cuba and the
Bahamas. These sharks are little-known
bottom-dwellers of the continental shelves and
upper slopes at depths from 18 to 951 meters.
Presumably these small (80-140 centimeters)
sawsharks use their saw-like snouts to disable small
fishes and crustaceans, as do the larger sawfishes,
Pristidae, but this has never been observed.
Sawsharks are live-bearing (aplacentally
viviparous). A considerable fishery for sawsharks
exists off southern Australia.

The Squatiniformes, or angel sharks, are
greatly flattened, bottom-dwelling, ray-like sharks
with an expanded oval head, large pectoral fins with
short, triangular lobes covering the gill openings,
no anal fin, and a unique caudal fin with the lower
lobe longer than the upper. These cold-
temperate-to-tropical sharks are found in the
Atlantic, southwestern Indian Ocean, and Pacific
Ocean, on the continental shelves and upper
slopes, from close inshore down to possibly 1 ,289
meters.

Angel sharks often bury themselves in sandy
or muddy bottoms, lurking like anglerfish to suck
and grab small fish and Crustacea with their
protrusable jaws and small, needle-sharp impaling
teeth. Angel sharks are live-bearing and reach a
length of 108 to 200 or more centimeters. Several
angel shark species are fished for human
consumption and also are used for fishmeal and
other fish products. They can inflict serious
lacerations when provoked.

The Heterodontiformes, or bullhead sharks,
are the only living sharks that have two spined
dorsal fins and an anal fin. They have prominent
crests above the eyes, small, piglikesnouts with the
nostrils and mouth connected by deep grooves, and
eyes that are well behind the mouth. Theirteeth are
peculiar small and cuspidate at the front of the
mouth, but large and molariform in back. Bullhead
sharks are found in shallow, warm-temperate-
to-tropical seas, often close inshore
on the continental shelf, but ranging down
to 275 meters. These sharks presently have a
restricted geographic range in the western Indian
Ocean, western Pacific, and eastern Pacific, but

Bullhead sharks are the
only living sharks with
spined dorsal fins and an
anal fin. This zebra
bullhead shark,
Heterodontus zebra,
occurs in the western
Pacific.

11

This nurse shark,
Cinglymostoma cirratum,
shows the pig-like snout,
small anterior mouth in
front of the eyes, and nasal
barbels characteristic of
orectoloboid sharks.

formerly inhabited the Atlantic. Many species favor
rocky areas with reefs and crevices, where they
slowly swim just above the bottom or clamber
across it on their muscular paired fins.

Bullhead sharks eat much hard-shelled
invertebrate prey, including crustaceans, molluscs,
and echinoderms (especially sea urchins), but they
also eat small fishes; their large rear teeth enable
them to crush prey without difficulty. These sharks
lay eggs (oviparous) in conical egg cases with
unique spiral flanges. Although of little interest to
commercial fisheries, bullhead sharks are
occasionally taken by sportfishermen and often by
divers. They may bite when provoked but are
considered harmless.

The Orectolobiformes, or carpet sharks,
resemble bullhead sharks in their piglike snouts,
grooves between nostrils and mouth, eyes behind
the mouth, and two dorsal fins and an anal fin, but
they lack dorsal spines and usually have nasal
barbels. Most have small, cuspidate impaling and
crushing teeth, but the wobbegongs
(Orectolobidae) have enlarged, fang-like teeth and
the tawny shark, Nebrius, has blade-like teeth. All
arewarm-temperate-to-tropical sharks of shallowto
moderate depths on the continental shelves or in
the upper layer of the oceans, ranging down to 183
meters. Almost all of the carpet sharks are bottom
dwellers, except for the pelagic whale shark,
Rhincodon typus.

Some carpet sharks are specialized for
bottom dwelling. The long-tailed carpet sharks
(Hemiscylliidae) have muscular paired fins that help
them move on coral and rocky reefs, and the
wobbegongs (Orectolobidae) have a camouflage of
dermal flaps along the head and a variegated color
pattern. Like the angel sharks (Squatinidae), the
wobbegongs are bottom lurkers often half buried
in sand or blending in rock or coral that ambush
bottom prey.

Most carpet sharks eat small fishes and
invertebrates and are helped by the bellows-like
arrangement of their small mouths and large oral
cavities, which enablethem to suck in prey. Someof
these sharks can expel water from their mouths in a
strong stream, sometimes in the faces of fishermen
who catch them.

The huge whale shark has grid-like gill filters
that enable it to strain plankton and small fish while
swimming horizontally, but it also feeds vertically,
with its head at the surface in a school of small fish,
by raising its head and draining its oral cavity
through the gills, then lowering its head with open
mouth to let water and fish pour in.

The smaller carpet sharks (Parascylliidae,
Brachaeluridae, Hemiscylliidae) grow 1 meter long
at most, but others (Stegostomatidae,
Ginglymostomatidae, Orectolobidae) attain 3 or
more meters in length. The whale shark, the largest
living fish, may reach 18 to 21 meters (based on sight
records of huge individuals).

Orectoloboid sharks either lay eggs in oval or
conical egg cases without spiral flanges or are
live-bearing. The carpet sharks are fished
commercially as well as by sportfishermen and
divers. Nurse sharks (Ginglymostomatidae), some
long-tailed carpet sharks, Chiloscyllium, and zebra
sharks, Stegostoma, are commonly consumed for
food. One nurse shark, Cinglymostoma cirratum, is
prized forthe leather madefrom its tough hide. The
whale shark is harpooned for food in India and may
be fished in China. The larger orectoloboids,
especially nurse sharks and wobbegongs, can be
dangerous when provoked and sometimes attack
people unprovoked; the whale shark is usually
harmless, but has infrequently rammed boats
(usually boats and ships ram it instead).

The Lamniformes, or lamnoid sharks, are
"typical sharks," with long mouths, conical or
flattened snouts, two dorsal fins without spines, an

12

The Australian ornate
wobbegong, Orectolobus
ornatus,a
bottom-dwelling
orectoloboid shark
camouflaged with flaps of
skin on the sides of its
head and a variegated
color pattern.

anal fin, eyes over the mouth, and nostrils separate
from the mouth. Most have enlarged teeth in the
front of the mouth, separated from more rearward
teeth by small intermediate teeth in the upper jaw
that divide the dentition into impaling and slicing
areas. Lamnoid sharks are found in tropical-
to-cold-temperate and boreal waters. Some
species are oceanic and epipelagic, some
coastal-pelagic on the continental shelves, and
others are found nearthe bottom on the continental
slopes, down to below 1 ,000 meters. Almost all of
the lamnoids are large or very large sharks, reaching
a maximum size of 4 meters or more.

The small, oceanic crocodile shark,
Pseudocarcharias, is exceptional in attaining only
1.2 meters in length, but the great white shark may
reach between 6 to 9 meters and the basking shark
10 to 14 meters. Most lamnoids eat fishes, other
sharks, crustaceans, and cephalopods, butthe great
white shark also eats marine mammals, especially
pinnipeds, and the basking and megamouth sharks
eat plankton. Most lamnoids are firm-bodied and
probably strong swimmers, but the deep-water
goblin shark may be an exception. The long,
blade-like snout, very slender teeth, soft, flabby
body, low, rounded fins, and unforked caudal fin of
the goblin shark suggest that it is a slow,
weak-swimming bottom-lurker, ambushing small
fishes, crustaceans, and cephalopods with its highly
protrusible jaws.

The sand tiger sharks (Odontaspididae) are
generalized large coastal and insular sharks that
feed largely on bony fishes. The crocodile shark and
longfin mako shark, Isurus paucus, are oceanic
species, probably feeding mainly on fish and squid.

The megamouth shark is a tropical, oceanic
plankton feeder, with gill rakers formed from
finger-like dermal papillae and a huge,
small-toothed mouth apparently rimmed by
luminous gum tissue; only a single specimen is
known, captured in the vicinity of the Hawaiian
Islands.

The basking shark is another lamnoid
filter-feeder (its relation to megamouth is unclear),
with gill rakers formed of bristle-like placoid scales
and a bipolar distribution in temperate coastal
waters.

The shortfin mako, Isurus oxyrinchus,
porbeagle, and salmon sharks, Lamna, are
coastal-oceanic, primarily fish and squid eaters. The
great white shark is a coastal superpredator with a
wide food range, possibly biased in larger
individuals toward marine mammals, but toward
bony fish, other sharks, and even invertebrates in
smaller ones. The mackerel sharks, Lamnidae, are
partially homoiothermic, or warm-blooded, with
countercurrent networks of blood vessels in their
body muscles that increase muscle power; their
spindle-shaped bodies, strongly horizontal tail
keels, and crescentic caudal fins make them
powerful swimmers.

The crocodile shark, Pseudocarcharias kamoharai, a small
(to 110 centimeters) oceanic lamnoid with highly
protrusible jaws and slender, hook-like teeth.

13

Three plankton-feeders.
Left a 7-meter basking
shark, Cetorhinus
maximus. (Photo by
Chuck Davis) Below left -
the taxonomically
unclassified
"megamouth " shark,
caught at a depth of 750
meters near Hawaii. (U.S.
Navy photo) Below a
whale shark, Rhincodon
typus, the largest fish.
(Photo by Jeremiah S.
Sullivan)

14

Thresher shark, Alopias
vulpinus. The long dorsal
lobe of the caudal fin of
this large, wide-ranging
lamnoid shark is used to
stun small fish and other
prey. (Drawing by L.J. V.
Compagno)

The shortfin mako is outstanding in its speed
and in its ability to leap marl in-like from the water; it
may be the fastest-swimming shark. The thresher
sharks, Alopias , are coastal and oceanic sharks that
use their extremely elongated upper caudal fins as
whips to strike and stun small fish.

Some lamnoids are noted for uterine
cannibalism, in which a developing fetus in the
uterus devours its potential siblings in the form of
eggs from the ovary. Many lamnoids are important
food fishes and support significant fisheries,
especially the mackerel, thresher, and sand tiger
sharks; the basking shark has been sporadically
fished for its liver, meat, and other products. The
great white shark and shortfin mako are implicated
in many attacks on swimmers, divers, and boats.

Last but hardly least are the
Carcharhiniformes, "typical sharks" with long
mouths, two dorsal fins without spines, an anal fin,
and theeyes overthe mouth, butdifferingfrom the
lamnoids in having movable lower eyelids. These
sharks swarm in the tropics, are very common in
temperate coastal waters, are found on the
continental and insularslopesdowntoatleast2,000
meters, and, in the form of a few species of large
carcharhinid sharks, such as the blue shark,
Phonace glauca, and silky and oceanic whitetip
sharks, Carcharhinus falciformis and C.
longimanus, in the upper levels of the ocean basins.
Most carcharhinoids are small, below 2 meters in
length, but the requiem and hammerhead sharks
have many large species more than 2 meters long
(two of which, the tiger shark, Caleocerdo cuvier,
and the great hammerhead, Sphyrna mokarran,
exceed 5.5 meters). On the other hand, the
catsharks (Scyliorhinidae and Proscylliidae) have
several species not exceeding 30 centimeters, with
one, Eridacnis radcliffei, being among the smallest
known sharks at 19 to 24 centimeters.

Carcharhinoid sharks eat a wide variety of
bony fishes, sharks, rays, invertebrates, and
carrion. Some of the houndsharks (Triakidae) feed

heavily on crustaceans, and the tiger shark is
remarkably indiscriminate in its feeding, often
swallowing garbage as well as oddities such as sea
snakes, marine turtles, and conch shells. The
carcharhinoids are a varied but relatively
homogeneous group, and carcharhinoid families
are for the most part not easy to distinguish (unlike
lamnoid families). There is a morphological
gradient in this group, ranging from the small,
weak-swimming, small-toothed scyliorhinid
catsharks through intermediate families
(Proscylliidae, Pseudotriakidae, Leptochariidae,
Triakidae, and Hemigaleidae) to the large,
strong-swimming, large-toothed requiem and
hammerhead sharks.

The catsharks (Scyliorhinidae and
Proscylliidae) are small, mainly upper-slope and
outer-shelf species that are also found in shallow
water. The false catsharks, Pseudotriakis, are large
(to about 3 meters), deep-water species rivalled by
the whale, megamouth, and basking sharks in
number of teeth but differing in diet from these
filter-feeders (one was photographed underwater
while swallowinga large bonyfish).

The houndsharks (Leptochariidae and
Triakidae) and weasel sharks (Hemigaleidae) are
small to moderately large (usually less than 2
meters) fish- and invertebrate-feeding sharks that
are common close inshore, primarily in the tropics.

The large requiem shark family
(Carcharhinidae) includes many large and
dangerous species as well as common well-known
smaller forms. These include the bull, dusky,
blacktipped, gray reef, bronze whaler, oceanic
whitetip, Galapagos, and silvertip sharks
(Carcharhinus), blue sharks (Prionace), tiger sharks
(Caleocerdo), lemon sharks (Negaprion),
sharpnosed sharks (Rhizoprionodon), and the reef
whitetip shark (Triaenodon).

The hammerhead sharks are very similar to
the requiem sharks, but have a unique bowplane,
formed from the sides of the head, apparently

15

Some carcharhinoids are among the smallest living sharks.
This Philippine ribbontail catshark, Eridacnis radcliffei, ;'s
mature at a length of 79 to 24 centimeters. The upper left
shark is a 23-centimeter pregnant female, from which the
center 11-centimeter full-term fetus was removed; the
lower right adult male is 22 centimeters long.

Hammerhead sharks have the prebranchial head
expanded laterally as a flat hydrofoil that presumably
increases their ability to maneuver. The extreme among
hammerheads is this winghead shark, Eusphyra blochii,
from the Indian Ocean and western Pacific, which has a
head width 40 to 50 percent of its total length.

equipping these sharks for fast maneuvering; the
wings of the bowplane are supported by special
expansions of the orbital and nasal regions of the
cranium.

Many carcharhinoids are live-bearing. Some
areaplacentally viviparous, buta large number have
placental viviparity, with yolk-sac placentas formed
from the fetal yolk sacand the maternal uterine wall.
Most scyliorhinid catsharks and one finbacked
catshark, Proscyllium , are oviparous, and lay eggs in
rectangular egg cases with corner tendrils.

Many carcharhinoid sharks support
important fisheries for food and fish products such
as fishmeal, liver oil, and leather. The most
significant fisheries are for some catsharks

(especial \y Scyliorhinus in the eastern Atlantic),
houndsharks (Triakidae, especially Caleorhinus,
Hemitriakis, Mustelus, and Triakis), weasel sharks,
and especially requiem sharks and hammerheads.

The large hammerheads and requiem sharks
are dangerous to swimmers and divers, and the
requiem shark family may contribute the bulk of
shark attack cases through its abundance in warm
waters where most shark attacks occur. A few
requiem sharks, primarily the bull shark,
Carcharhinus leucas , enter freshwater rivers and
lakes far from the sea.

Leonard J. V. Compagno is an Adjunct Professor at the
Tiburon Center for Environmental Studies, San Francisco
State University. He also is a Research Associate of the
American Museum of Natural History, New York, and of
the California Academy of Sciences, San Francisco.

All photos by the author unless otherwise indicated.

References and Further Reading

Baldridge, H. D. 1974. Shark attack, 263 pp. New York, N.Y. :

Berkeley Publishing Corp.
Bigelow, H. B.,andW. C. Schroeder. 1948. Sharks, Chapter 3 in

Fishes of the Western North Atlantic, No. 1, Part 1, pp. 59-576:

Memoir, Sears Foundation for Marine Research.
Budker, P., and P. J. Whitehead. 1971. The life of sharks, 222 pp.

New York, N.Y. : Columbia University Press.
Compagno, L. J. V. 1973. Interrelationships of living

elasmobranchs. In Interrelationships of Fishes, ed. P. H.

Greenwood, R. S. Miles, and C. Patterson. Supplement 1,

Zoological Journal of the Linnean Society of London, vol. 53,

pp. 15-61.

. 1977. Phyletic relationships of living sharks and rays. In

recent advances in the biology of sharks, ed. R. C. Northcutt.

American Zoologist, Vol. 17, no. 2, pp. 303-322.
Gilbert, P. W., ed.1%3. Sharks and survival, 578pp. Boston, Mass.:

D. C. Heath and Co.
Gilbert, P. W., R. F. Mathewson, and D. P. Rail, eds. 1967. Sharks,

skates and rays , 624 pp. Baltimore, Md.: Johns Hopkins Press.
Hodgson, E. S.,and R. F. Mathewson, eds. 1978. Sensory biology of

sharks, skates and rays, 666 pp. Arlington, Va: Office of Naval

Research , Department of the Navy.
Kreuzer, R., and R. Ahmed. 1978. Shark utilization and marketing,

180 pp. Rome, Italy: Food and Agriculture Organization of the

United Nations.
Lineaweaver, T. H., Ill, and R. H. Backus. 1969. The natural history

of sharks, 256pp. Philadelphia, Penn. and New York, N.Y.: J. B.

Lippincott Co.
Northcutt, R. G., ed. 1977. Recent advances in the biology of

sharks, pp. 287-515. American Zoologist, vol. 17, no. 2.

16

Vision in Sharks

by Joel L. Cohen

Photo by
Chuck Davis

The eyes were sightless in the black,
and the other senses transmitted
nothing extraordinary to the small,
primitive brain.

Jaws, Peter Benchley

is the impression in popular literature
regarding the vision of sharks. Thought to see
poorly and only at night, sharks have even been
called "swimming noses." Stories abound
concerning sharks that home in on minute
quantities of blood in the water from miles away, yet
the animals' visual abilities are, for the most part,
ignored. Where did these impressions aboutthe
poor visual system of sharks come from? How well
do sharks see?

Most of the early research on sharks was
done in the late 1800s and early 1900s by European
anatomists. The specimens studied were those
obtained from local fishermen. Knowledge of the
shark visual system thus came from only two or

three species and was applied to all species. Hence,
a "typical shark eye" was described, and was
thought to be valid for all sharks. However, there
are more than 300 species of sharks. They live in
many different habitats, ranging from near shore to
the deep sea. As we shall see, their visual systems
adapt quite well to their specific environments.

Differences in Design of Eyes

The design of the shark eye closely follows that of
the typical terrestrial vertebrate eye. But there are
some notable exceptions. If one compares a cross
section of a shark eye with that of the eye from a
terrestrial vertebrate, there is a strikingdifference in
the size and shape of the lens (Figure 1a, 1b, 1c).

17

CORNEA

CILIARY
PROCESS

SCLERA

CHOROID

CILIARY MUSCLE

NERVE /

SHEATH

Cornea

Figure 1. The vertebrate eye. a) Drawing of a typical
terrestrial eye. The lens is thin and flattened. In relation to
the rest of the eye, the lens takes up a proportionally small
amount of space, b) Frozen section from the eye of a
juvenile lemon shark, Negaprion brevirostris. The lens is
large and almost spherical in shape. (Photo by R. E. Hueter)
c) Photograph through the front of the eye of a six-gill
shark, Hexanchus griseus. Note the large spherical lens.

Why is the lens of the shark so large and almost
spherical in shape, whilethat of theterrestrial eye is
small and flattened?

The cornea is the transparent front of the eye.
In the terrestrial environment, there is a large
difference between thedensity of theairand that of
the cornea, the cornea being denser. This
difference in density causes light rays entering the
eye to be bent, or refracted. Because this refraction
aids the lens in focusing the light on the
photoreceptor cells of the retina, the lens does not
have to be very powerful. As a result, eyes in land
vertebrates have thin lenses that can change their
point of focus by changing shape. This is
accomplished by two small ciliary muscles.

In aquatic animals, however, the water and
the cornea are of the same density, so the cornea
cannot contribute to the focusing of an image. That
job falls to the lens, which must be powerful.
Hence, it is large and lenticular in shape. Because it
is large, it can not accommodate or focus the image
by changing its shape as the lenses in terrestrial
vertebrates do. In teleosts( bony fishes), focusing is
accomplished by means of the retractor lentis
muscle, which, instead of changing the shape of the
lens, moves the entire lens toward the retina. In
sharks, the story is not yet clear. When electrodes
are placed on the muscles attached to the lens,
there is no noticeable lens movement. However, a
difference in the focal point has been found
between anesthetized and unanesthetized sharks,
implying lens movement of some sort.

If the lens of a shark does not move, what is
the quality of an image falling on the retina? This
may determine the resolving power of the visual
system. If a poor, unfocused image is projected
onto the retina, then this would set a lower limit on
how well the shark sees. In essence, it would be the
weak link in the chain of the visual system.

Robert Hueter, now at the University of
Florida, has examined the eyes of live juvenile
lemon sharks much the same way an eye doctor
examines human eyes. By constructing a
mathematical model from frozen sections of eyes,
Hueter has shown that the eyes of these young
sharks are hypermetropic, or farsighted, by 2.76
diopters.* It is as if the lens were not powerful
enough to focus an image onto the retina. In human
terms, this is a moderate farsightedness; the person
would need glasses for reading, but the condition
would not be debilitating. Further research is
needed in this area to determine if a mechanism
exists to bring the eye into a condition of perfect
focus.

In a number of species of skates and rays, an
unusual focusing mechanism termed a "ramp
retina" - has been described by Dr. Jake Sivak of

*A diopter is a unit of measurement for lens power equal
to the reciprocal of the lens focal length in meters.

18

the University of Waterloo, Ontario, Canada. This is
a static mechanism consisting of a variation in the
distance between the lens and retina. To focus on
an image, the animal would only have to move the
eyes or bend the head.

No matter what the quality of the shark's
optical system, the aquatic environment in which
the animal lives plays a vital role in what it sees and
how well it sees. We are used to seeing through a
medium that is for the most part clear. The
underwaterworld iscompletelydifferent. It isfilled
with particulate matter and tiny organisms that act
to scatter light and degrade the quality of an optical
image. And as one goes deeper, the spectral quality
of light changes.

Rods and Cones

The actual process of vision takes place in the retina,
a semi-transparent tissue located at the back of the
eye. Embryologically, the retina is an extension of
the brain. Five types of cells are found within the
retina, and they are organized into three cellular
layers and two plexiform or synaptic layers
(Figure 2).

The first event of vision occurs when a
photon of light strikes visual pigment in the
photoreceptor cells. Photoreceptors occur as two
types: rods and cones (Figures 3 and 4). Anatomists
in the 1800s observed that animals which were
active during daylight hours had retinas that
contained a majority of cone photoreceptors, while
rods predominated in the retinas of nocturnal
animals. This led to the duplexity theory of vision,
which correlated the activity patterns of an animal
with the complement of photoreceptors in its
retina. Thetheory also ascribed certain functions to
each photoreceptor type. Rods were said to be used
for nighttime or low-light-level vision as well as for
achromatic vision. On the other hand, cones were
functional during daytime and were responsible for
chromatic, or color, vision.

.

in

'P
9

Figure 2. Light micrograph of the retina of the lemon
shark, p = photoreceptors, on = outer nuclear layer, op =
outer plexiform layer, in = inner nuclear layer, ip = inner
plexiform layer, g = ganglion cell layer.

i

Figure 3. Light micrograph of the photoreceptor layer of
the retina of the lemon shark. The arrows point to the cone
photoreceptors. They have short, conically tapering outer
segments. The remaining receptors are termed rod
photoreceptors and have elongated cylindrical outer
segments.

Figure 4. Electron micrograph of a cone photoreceptor
from the retina of the lemon shark.

19

Because retinas from only a limited number
of species were examined, sharks were categorized
as possessing either rod or rod-dominated retinas.
With the advent of better fixation techniques and
better optics, the situation has changed.

The electron microscope has enabled
scientists to divide photoreceptors into rods and
cones based notonlyontheirexternal morphology,
but on ultrastructural criteria, such as whether the
plasma membrane is continuous (cones) or
discontinuous (rods) and whether the synaptic
terminal is small and rounded (termed a spherule-
rods) or larger and elongated (termed a pedicle -
cones).

For example, the retina of the common
dogfish, Squalus acanthias, was first studied by
Retzius in 1896. Based on his observations and those
of Verrierand Franz in theearly 1930s, the retina was
said to contain only rods. But in 1972, working with
an electron microscope, Dr. William Stell showed
that there also are cone photoreceptors present.
Dr. Stell is now at the University of Calgary, Alberta,
Canada.

In fact, most sharks possess duplex retinas,
containing both rods and cones. Of all the
elasmobranchs studied, the only exceptions to this
are the skates Raja erinacea and R. oscillata, and
possibly some of the deep-sea sharks.

What this means is that sharks are capable of
both nocturnal and daylight activity. Possession of
two types of photoreceptors also means that sharks
might possess color vision. For this to occur, the
spectral sensitivity of the two receptors must be
different. Work done by myself and Dr. Samuel H.
Gruber of the University of Miami have shown by
electrophysiological methods that in the juvenile
lemon shark at least two different spectral
mechanisms are present and working together.
Ultimate determination of color vision, however,
rests with behavioral testing.

Green Light, Blue Light

In cross section, the outer segment of each
photoreceptor consists of a series of stacked discs
called lamellae (Figure 5). It is thought that the
photopigment is located on or within the
membrane of the lamellae. The rod visual pigment
of sharks is based on vitamin A and is termed
rhodopsin. It absorbs light maximally in the green
part of the spectrum at approximately 500
nanometers.

Oceanic waters transmit the most light at
approximately 500 nanometers. Thus the visual
pigment of sharks is well matched to the
environment. But there are species of sharks and
skates that spend their entire lives in the deep
ocean. As one goes deeper, the spectral quality of
light changes, until only blue light is left.

Elasmobranchs having visual pigment with a
maximum absorbancy in the green part of the

Figure 5. Electron micrograph of the outer segment of a
photoreceptor showing the lamellae. The visual pigment is
located on or within the lamellae membrane.

spectrum would be poorly adapted for life in the
deep sea, where blue light predominates. However,
deep-water sharks have been found to possess a
golden visual pigment termed chrysopsin, which
has its maximal absorbancy shifted 20 to 30
nanometers into the blue end of the spectrum, at
470 to 480 nanometers. So it appears that the
elasmobranchs inhabitingthe deep sea also have
well-adapted visual pigments.

To make use of all the available light in the
sea, elasmobranchs, like many vertebrates, possess
a specialized ocular structure termed the tapetum
lucidum. The tapetum is responsible for the
eyeshine commonly seen in animals at night. The
tapetum consists of a series of reflecting plates in
the choroidal layer behind the retina (Figure 6).
These plates are aligned differently in different parts
of the eye so as to reflect entering light straight back
along the same optical path. Thus, when a photon of
light enters the eye and strikes a photoreceptor, it is
reflected by the tapetum and strikes the
photoreceptor a second time. This serves to
increase the sensitivity of the eye.

20

CH-

IP

p

Figured. Light micrograph
of the retina of the lemon
shark. The tapetal plates
can be seen oriented at an
angle so as to reflect light
back onto the
photoreceptor cells. CH =
choroid layer, TP =
tapetum lucidum, P =
photoreceptors.

To protect the retina from too much light
during the day, pigment granules migrate over the
tapetum, thus blocking it from light. This occlusive
tapetum is found in those sharks inhabiting pelagic
waters. Deep-sea sharks, however, do not possess
these screening pigment granules; their tapetums
are always exposed to light.

Brain Studies

The orderly arrangement of cells in the retina serves
to transfer and process the visual signals from the
photoreceptors vertically via bipolar cells and
laterally via horizontal cells and amacrine cells. The
ganglion cells serve as the final relay station in the
retina. Their axons form the optic nerve, through
which visual signals are sent to the brain.

Unlike higher vertebrates, sharks do not
possess a visual cortex. It has been thought that all

higher-center visual processing was done in the
optic tectum of the brain (Figure 7), but new
evidence suggests that the optic tectum is not as
important in visual processing as once believed. In
addition, other areas of the brain may play an
important part in the processing of visual
information.

This new information comes in part from
anatomical and behavioral research done by Dr.
Curt Graeber at Lerner Marine Laboratory, Bimini,
the Bahamas. Graeber has shown that there is little
difference in visually guided behavior between a
nurse shark that has had its optic tectum surgically
removed and one that has not. This is contrary to the
findings of early scientists, who believed such an
operation left the shark blind.

The belief that sharks were "swimming
noses" came in part from the fact that the large area

21

Nasal Capsule

Olfactory Bulb
Olfactory Tract

Telencephalon

Thalamus
Optic Tectum
Cerebellum

Figure 7. Drawing of the brain of a dogfish shark, Squalus
acanthias. The large frontal lobes, termed the
telencephalon, were originally thought to be involved only
with ol faction.

of the brain termed the telencephalon, or forebrain,
was thought to receive only olfactory input. Dr.
Sven Ebbesson of Catholic University in Ponce,
Puerto Rico, and others, using the newer
anatomical techniques that allow one to trace
neural pathways, has shown that in the lemon,
nurse, and tiger sharks, the telencephalon receives
a large visual input from the optic tectum via the
thalamus, a mid-brain structure. Furthersupportfor
this comes from the recording of evoked electrical
responses from the telencephalon when the optic
nerve is electrically stimulated. Upon removal of all
or part of the telencephalon, defects were found in
visually guided behavior.

In conclusion, we have determined that the
visual system of sharks is not as deficient as
previously thought. In contrast to that depicted in
the early literature, the visual system of sharks is
highly developed. Sharks are morethan "swimming
noses," but they do not need a fine-detail visual
system such as ours because their world is far
different from ours. They require mechanisms that
enable them to hunt prey, and, for this function,
they are well adapted.

Joel L. Cohen is a post-doctoral research fellow at the
Biological Laboratories, Harvard University, Cambridge,
Massachusetts. He received his Ph.D. from the Rosenstiel
School of Marine and Atmospheric Science at the
University of Miami, Florida.

Acknowledgments

I would like to thank Robert E. Hueter for permission to
use material from his research as well as for many hours of
useful discussion. I would also like to thank Dr. S. H.
Gruber for giving me the opportunity to learn about vision
in sharks.

Selected Readings

Cohen, ). L., S. H. Gruber, and D. I. Hamasaki. 1977. Spectral
sensitivity and Purkinje shift in the retina of the lemon shark,
Negaprion brevirostris (Poey). Vision Research 17: 787-92.

Graeber, C. 1978. Behavioral studies correlated with central
nervous system integration of vision in sharks. In Sensory
Biology of Sharks, Skates and Rays, ed. by E. S. Hodgson and R.
F. Mathewson. Washington, D. C.: U. S. Government Printing
Office.

Gruber, S. H. 1975. Duplex vision in the elasmobranchs:
histological, electrophysiological, and psychophysical
evidence. In Vision in fishes: new approaches to research, ed.
by M. A. AM. New York: Plenum Press.

Gruber, S. H., and J. L. Cohen. 1978. Visual system of the

elasmobranchs: State of the art 1960-1975. In Sensory Biology
of Sharks, Skates and Rays, ed. by E. S. Hodgson and R. F.
Mathewson. Washington, D. C.: U. S. Government Printing
Office.

Gruber, S. H., R. L. Gulley, and ). Brandon. 1975. Duplex retina in
seven elasmobranch species. Bull. Mar. Sci. 25: 353-58.

Hueter, R. E.,andS. H. Gruber. 1980. Retinoscopy of aquatic eyes.
Vision Res. 20,197-200.

Sivak, ). G. 1978. Refraction and accommodation of the

elasmobranch eye. In Sensory Biology of Sharks, Skates and
Rays, ed. by E. S. Hodgson and R. F. Mathewson. Washington,
D. C. : U.S. Government Printing Office.

22

^^H

P

Figure 7. The "looseness" of the upper jaw of a mako shark, Isurus oxyrinchus, is demonstrated. By protruding the upper
jaw during the bite, many sharks are able to gouge chunks out of large prey. (Photo by Marty Snyderman)

Shark Feeding Mechanisms

by Sanford A. Moss

/\ key to individual survival and evolutionary
success is adequate nutrition. A reasonably full
belly is necessary in order to grow, move, mature,
and mate. Feeding mechanisms, along with their
concomitant locomotor and sensory gear, are
critical features in any animal's existence. The
evolutionary persistence of sharks can in some
measure be explained by their success in feeding.
This comes as no surprise to a public that is
educated to the view that sharks eat spectacularly,
successfully, and often gruesomely. Moreover, the
public and many scientists think of sharks as
primitive beasts that have persisted in the modern
world only as prehistoric anachronisms. Such
thinking is fallacious: sharks are elegantly adapted
animals, and their feeding mechanisms are apt
examples of their economy of form and function.
Sharks are particularly well equipped in the
sensory aspects of feeding, as consideration of their

olfactory, electrosensory, visual, and
acousticolateralis systems suggests. They also seem
particularly able to avoid detection by potential
prey. Scientists have been surprised at finding fast
swimming tuna and billfish in the stomachs of
apparently lethargic sharks, such as the oceanic
whitetip, Carcharhinus longimanus. Sharks make
very little hydrodynamic noise when swimming,
and may thereby escape acoustic detection by prey
(see Oceanus, Vol. 23, No. 3). Also, the color
patterns of many sharks are probably very cryptic in
their feeding environments, making them
functionally invisible to the prey they seek. Our
understanding of these matters is sketchy,
however, and more work needs to be done on this
aspect of their feeding success.

The actual ingestion of prey by sharks is
accomplished with an anatomical system that is
elegant in its simplicity and effectiveness. With

23

relatively small modifications of the basic feeding
mechanism, elasmobranchs have evolved into a
surprising number of functional types, feeding on
differentfoods.

The feeding mechanism of typical
carcharhiniform sharks has a characteristic external
appearance (Figures 1 and 2). The mouth is tucked
well behind the snout on the underside of the head,
giving the animal its peculiar "chinless"
appearance. The mouth is broad, but not long. It
has numerous sharp teeth which, in most species,
are not evident until the animal opens its mouth
wide (Figure 2). The shortness and ventral position
of the mouth may seem awkward for a top predator.
Predaceous bony fishes, such as barracudas and
pikes, have long jaws at the fronts of their snouts.
Moreover, these fishes can see their own mouths
and thus "look" food into them; sharks cannot.
These seeming disadvantages, however, are not
consequential. Sharks can eat anything a barracuda
can and more.

Three Important Features

The internal anatomy of the shark feeding
mechanism has three important features: the
skeletal elements, including the braincase
(chondrocranium) and the jaws; the cranial
musculature which moves the skeletal elements;
and the teeth.

Sharks lack true bone in the skeletal system.
The basic skeletal material in these animals is
cartilage, which is flexible, but does not resist

mechanical deformation well. Where hardness
becomes necessary in cartilage, sharks have
strengthened it by the deposition of calcium salts in
the surface layers of the skeletal element. The jaws
and chondrocrania of sharks are thus often
hardened by these calcium salts. Indeed, it is
sometimes possible to make inferences about the
diets of various shark species by examining the
degree to which their jaws are calcified. For
example, nurse sharks, Cinglymostoma cirratum,
which feed predominantly on hard-shelled
molluscs and crustaceans, have significantly heavier
jaws than fish-eating sharks.

The jaws of carcharhinoid sharks (Figure 3)
typically consist of tooth-bearing upper
(palatoquadrate cartilage) and lower elements
(mandible of Meckel's cartilage). They are formed
from paired cartilages that meet in symphyses
(joints) at the midline in the front of each jaw. These
connections are loose, allowing each side of the jaw
a fair amount of latitude in its movement. Sharks
that eat tough prey, such as tiger sharks, may have
tight, well-fused symphyses. The jaw cartilages are
expanded toward the rear, allowing large
attachment surfaces for the considerable muscle
masses that close the jaws. The upper and lower
jaws meet in a special joint, which allows vertical
flexibility but resists lateral movement. This
articulation really consists of two ball-and-socket
joints, arranged next to each other with one ball
from the upper jaw fitting into a mandibular socket
and the other ball from the mandible fitting into a
palatoquadrate socket.

I

Fig ure 2. A great wh i te
shark, Carcharodon
carcharias,affac/c/ngba/f
suspended next to a shark
cage in Australian waters.
The ventrally placed
mouth is broad, but
relatively short. Sharks
evolved a more powerful
biting apparatus by
reducing the length of the
jaws. (Photo by David
Doubilet)

24

Figure 3. Lateral view of a carcharhinid shark

chondrocranium (stippled) and jaw complex. The upper

and lower jaw are loosely connected to the

chondrocranium by the hyomandibular cartilage and by

the ethmopalatine ligament (not visible here), which runs

from the orbital process of the upper jaw to the underside

of the chondrocranium. cth ceratohyal cartilage;

hy hyomandibula; me Meckel's cartilage; nc nasal

capsule; obp orbital process; oc occiput;

pq palatoquadrate cartilage; re rostral cartilage. (From

Moss, 1972).

The jaws are loosely connected to the rest of
the skull at two points. First, a ligamentous
connection runs from knobs (orbital processes)
near the front of each side of the upper jaw to the
underside of the chondrocranium (Figure4). With
the jaws closed, these ligaments (ethmopalatine
ligaments) are slack and have no suspensory
function. When the jaws are engaged in biting,
however, these ligaments passively restrain the
upper jaw from making excessive downward
movements. They are in a sense "safety lines."

The second and principal connection of the
jawcomplextothechondrocranium is by cartilages,
the hyomandibulae. These cartilages serve as struts
or braces that run on each side from the lateral
posterior (otic) surface of the chondrocranium back
to the inner surface of the rear-most portion of the
lower jaw, near its articulation with the upper jaw.
The connections made here are also loose, allowing
the ends of the hyomandibulae to swing out and
forward, pushing the rear ends of the jaws outward
and, in some sharks, pushing the entire jaw
complex forward as well (Figure 4).

When the jawapparatus of a shark is carefully
dissected, it is easy to appreciate a similarity in the
form and position of the jaws and hyomandibulae
with the rows of cartilages behind them, supporting
the gill apparatus. In fact, it has long been a tenet of
comparative vertebrate anatomy that the jaws
represent a modification of the first in a series of
ancestral gill or branchial arches. According to this
idea, the hyomandibula is a modification of part of
the second in this series of primitive gill arches. In
some living sharks, such as the six-gill shark,
Hexanchus griseus, this second, or hyoid, arch
actually supports functional gills.

Many living sharks, as well as skates and rays,
also have openings behind the eyes known as

Figure 4. Lateral view of a carcharhinid shark
chondrocranium (stippled) and jaw complex with the jaws
maximally opened and the upper jaw protruded. The outer
end of the hyomandibula has been pulled forward and
laterally, bracing the jaws. The palatoquadrate cartilage has
been pulled down to the limit imposed by the
ethmopalatine ligament. The upper jaw teeth can thus cut
deeply into the prey, el ethmopalatine ligament;
hy hyomandibula; me Meckel's cartilage; obp orbital
process (From Moss, 1972).

spiracles. These openings into the pharynx are
remnants of the gill si it between t he mandibular and
hyoid arches. In addition to the hyomandibula,
additional cartilages exist in the hyoid arch. The
ceratohyal cartilages pass down and forward from
articulation points at the ends of the
hyomandibulae to meet the lower jaw. These
ceratohyal cartilages curve just inside the mandibles
toarticulatewithasingle, median basihyal cartilage.
Together with other gill-arch cartilages projecting
forward in the bottom of the mouth, these elements
form a "tongue," which is pulled down and back to
enlarge the oral cavity during feeding and
ventilation.

The Muscles of the Jaw

The muscles that operate the jaw complex are large
and conspicuous. The most obvious group, the first
met in a lateral dissection, is the quadrato-
mandibularis complex (Figure 5). It runs from the
posterior expanded portion of the palatoquadrate
down to the lower jaw. This large muscle mass is
divided into smaller muscle groups in different
species, but its major function is to close the jaws by
pulling them together.

Three other large muscles also participate in
the generalized shark feeding apparatus. These
include levators of the hyomandibulae and upper
jaws (levator hyoideus and levator palatoquadratii,
respectively). These two muscles run from
attachments high on the chondrocranium to the
rear ends of the hyomandibula and upper jaw

25

lev pq

lev hy

ri

preorb

Figure 5. Musculature of the carcharhinid feeding mechanism. The jaws are closed
principally by the quadratomandibularis complex (qd and qv) with help from the
preorbitalis muscle (pre orb). The levatorpalatoquadratii (lev pq) and preorbitalis pull the
jaw complex forward, helping to protrude the upper jaw. The levatorhyoideus (lev hy)
raises the hyomandibula and pulls it forward, bracing it between the chondrocranium and
the jaw complex, thus supporting the apparatus against the lateral forces generated during
feeding, hy hyomandibula; me Meckel's cartilage; pq palatoquadrate. (From Moss,
1972).

(Figure 5). The third muscle, the preorbitalis, also
orginates well forward and high on the
chondrocranium and runs down and back to join
the quadratomandibularis, where it attaches to the
lower jaw. The effect of these three muscles is
similar in carcharhiniform sharks. Together they
pull the back of the jaw complex forward, rotatingit
so that the front of the upper jaw is forced forward
and down. The outer ends of the hyomandibulae
are also pulled laterally, pushing the articulation
point of the jaws outward and effectively bracing
the sides of the jaws against the tough skin of the
head. The hitherto loose jaw complex is now
stiffened, able to withstand the side-to-side forces
generated during feeding.

The quadratomandibularis and the jaws act as
a third-class lever system with the force (muscle)
acting between the fulcrum (jaw articulation) and
the resistance (food). For maximum power to be
exerted, the moment arm (length of jaw) should be
as short as possible. Sharks have very powerful
biting capabilities.

The effects of the levator and preorbitalis
muscles are considerable in shark feeding. They
produce an effective upper-jaw protrusion
mechanism that allows the upper jaw to take an
active role in feeding (Figure 2). The upper jaw
during protraction can thus bite deeply into the kerf
made by its sharp teeth. Most predators that live on
fishes are limited to prey which they can engulf at a
single bite hence the long jaws of the barracuda
and pike. Carchariniform sharks, however, are able
to gouge chunks out of prey that are too large to be

taken intothemouthinonebite.Thisopensup new
gastronomic worlds to the shark, placing large
teleosts, whales, and even other sharks on their
menu.

A Rapid Turnover of Teeth

One of the many unique characteristics of living
elasmobranchs is a dentition that appears to be
continually replaced throughout their lifetimes
(Figure 6). As early as 1846, Sir Richard Owen an
anti-evolutionist who was to be a thorn in Charles
Darwin's side called attention to the
elasmobranch dental array, calling ita"phalanx . . .
ever marching slowly forward in rotatory progress
over the alveolar border of the jaw. "Subsequent to
Owen's description, controversy arose as to
whether sharks really do replacetheirteeth. In 1948,
James Ifft and Donald Zinn, working in Woods
Hole, demonstrated that the smooth dogfish,
Mustelus canis, replaced its teeth at a rate of one
functional rowof teeth every 10 to 12 days. In 1967, 1
marked the teeth of young, captive lemon sharks,
and recorded replacement rates of about one
functional row of teeth a week. Similar tooth
replacement times have since been measured in
other species of sharks. What is the reason for such
a rapid turnover of teeth?

Shark teeth are relatively fragile. In the face
of the biting force sharks routinely produce, it is not
surprising to find that these teeth are often broken
(Figure 6). Rapid replacement of teeth thus allows
sharks to compensate for the premature
disintegration of theirdentition an adaptation that

26

Figure6. The lower jaw of the smooth dogfish, Musteluscanis, as seen from above. Inthis
species the teeth are low and rounded, producing a modified crushing dentition. Several
generations of teeth are functional at any one time. The replacement of teeth occurs by an
outward movement (toward the top of the picture). The younger, replacement teeth at the
bottom can be seen to be slightly larger than the older, outer teeth, thus compensating for
growth of the shark. It is not unusual to find shark dentitions, like this one, with damaged
teeth. (From S. A. Moss, 1972, Tooth replacement and body growth rates in the smooth
dogfish, Mustelus canis [Mitchell]. Cope/a, 7972 (4): 808-811).

befits the predatory lives they lead. Tooth
replacement also allows for growth. As the shark
grows, so does its jaws. The number of teeth,
however, remains constant. Each tooth family (the
replacement teeth in a single sequence) must grow
in order to maintain a set of teeth large enough to
carry outthe requisite predatory tasks. Each tooth is
thus a little larger than the one it replaces.

Most sharks have a heterodont dentition.
This means that all the teeth are not
morphologically the same. Carcharhiniform sharks,
for instance, often have broader teeth in the upper
jaw than in the lower. In some sharks (a good
example being Heterodontus francisci, the horned
shark), the dentition in a single jaw may vary
considerably from sharp, cutting teeth in the front
of the jaw to crushing, molar-like teeth in the back.
Some of these differences in tooth structure
become meaningful when the diet and feeding
behavior of each species of shark is considered
(Figure/).

Feeding Behavior

Contrary to what is often written about sharks, there
is not a lot of unpredictable behavior associated
with their feeding. Once a decision is made to

attack, that decision is communicated to the
observer clearly. Carcharhiniform sharks may
slowly circle a prospective prey, and even bump it
tentatively with the snout or pectoral fins. When the
decision is madetoattack, however, this behavior is
altered dramatically. The shark is transformed from
a sinuously swimming, graceful creature to a
stiffened, herky-jerky animal. The back may seem
arched, the body is stiff, and the tail beats more
quickly. The shark will now swim directly at its
intended victim with its snout somewhat elevated.
The jaws may be opened and closed rapidly as
often as three times per second during this
closing rush. As the shark approaches its prey, the
pectoral fins are depressed, raising the forepart of
the body and braking the animal's speed. The
opened mouth makes contact with the prey and, as
soon as the teeth obtain a purchase, the shark
begins to shake its head and forebody from side to
side. The frequency of head shaking varies from
species to species. Tiger sharks rather slowly throw
their massive heads from side to side, while gray
reef sharks, Carcharhinus amblyrhynchos, quickly
shake their heads in what almost seems likea
vibration. Whatever the species, the effect is the
same. These side-to-side movements bring the

27

D

Figure 7. Three examples of some forms of shark teeth. A
and B are the upper and lower jaw teeth, respectively, of
the lemon shark (Negaprion brevirostris). In this species,
which usually feeds on fish, the upper jaw teeth are not
very much broader than those in the lower jaw. C and D
represent teeth from the tiger shark (Galeocerdo cuvieri).
These heavy, serrated teeth make effective saws forcutting
through the sea turtles they frequently eat. E and F are
teeth from the nurse shark CCinglymostomacirratum). The
teeth in this species are relatively small and serve to hold
prey, such as crustaceans that have been sucked into the
mouth, while the heavy, broad jaws crush them.

sharp lateral cutting edges of the teeth into play,
slicing ever deeper into the prey. The major role
played by the upper jaw is reflected in the dentition
of carcharhiniform sharks. Many species have
broad, blade-like teeth confined to the upper jaw.
The awl-like lower jaw teeth are designed for
puncturing and holding the prey while the upper
jaws do their work.

This feeding mechanism is capable of more
versatility than merely taking bites out of large prey.
Carcharhiniform sharks, to some extent, are dietary
generalists. While the bulk of their diet may be fish
and squid, most are not above eating benthic
invertebrates, such as crabs, lobsters, and
octopuses.

Certain species do seem to have
preferences hammerheads (Sphyrna spp) prefer
sting rays; bull sharks (Carcharhinus leucas) often
eat other sharks; smooth dogfish are crab and
lobster specialists; and tiger sharks attack sea
turtles with regularity. But all possess a feeding
mechanism of great versatility that helps to make
them perhaps the ultimate predatory type.

The carcharhiniform gouging mechanism is
but one of a surprising number of feeding
mechanisms evolved by sharks. The basic type is the
crushing-feeding mechanism. This features heavy,
short almost transverse jaws; short, heavy
hyomandibulae incapable of much lateral or
forward movement, and a heavy molariform
dentition. This feeding mechanism is seen in
rays and is admirably suited to ingesting and
crushing hard-shelled benthic invertebrates, which
are sucked into the small ventral mouth by
considerable orobranchial expansion. Orbital
processes are reduced or lacking on the upper jaws,
for lateral head-shaking is not important. The
Orectolobiformes, which include nurse and carpet
sharks, have secondarily adopted this sucking and
crushing feeding-mechanism.

Another distinctive feeding type is that
shown by many squaliform dogfishes. These
animals also tend to have short, transverse jaws with
short hyomandibulae (Figure 8). The dentition,
however, is composed of low, blade-like teeth
which are often tightly overlapped into rows of very
sharp cutting edges. The orbital processes are very
long and project nearly to the top of the
chondrocranium when the mouth is closed. In the
absence of a long hyomandibula to brace the
rotating jaws against the braincase, the orbital
processes maintain contact with the braincase even
during periods of extreme upper jaw protrusion.
The resultant feeding mechanism is an effective
cutting one, able to slice up herring-sized fish into
smaller pieces. Some of these sharks such as the
deep-water, luminous shark, Isistius
brasiliensis are known to gouge chunks out of
large prey.

Figure 8. Dorsal view of
the chondrocranium and
jaw complex of the spiny
dogfish, Squalus
acanthias. The short,
laterally directed
hyomandibulae cannot be
pulled further outward to
brace the jaw complex.
The orbital processes (not
shown here) are very long
and do not lose contact
with the sides of the
chondrocranium when the
upper jaw is protruded.
(From Moss, 1977).

28

CUTTING

FILTER- FEEDING

(MOBULIDAE)

(CETORHINIDAE)

(RHINIODONTIDAE)

\

SUCTION-CRUSHING

(ORECTOLOBIFORM)

SUCTION-CRUSHING

CRUSHING

(TRIAKID)

GOUGING

(SQUALIMORPH)

(MYLIOBATIFORM)

\

(CARCHARHINIFORM)
(LAMNIFORM)

SUCTION-GRASPING

(RAJID-LIKE)

t

GRASPING ANCESTOR

(TERMINAL MOUTH)

Figure 9. Possible evolution of feeding mechanisms in elasmobranchs. The ancestral type was probably not unlike that of
modern teleosts, such as pikes. A small ventral mouth, similar to living skates, evolved to deal with small ventral
invertebrates. This basic suction-grasping mechanism evolved into V a cutting-feeding mechanism seen in living
dogfishes; 2) a crushing mechanism found in many living rays; and 3) with the advent of elongate hyomandibulae and sharp
cutting teeth, into thegouging-feeding mechanism of living carcharhiniform and lamniform sharks. Further modifications
produced a secondary crushing-feeding mechanism and, at least three times, the filter-feeding mechanism seen in living
manta rays, whale sharks, and basking sharks. (From Moss, 1977).

Filter-Feeding Sharks

Perhaps one of the most spectacular evolutionary
modifications of shark feeding mechanisms was the
development of filter-feeding for planktonic
organisms. This mechanism was developed by: 1)
elongation and broadening of the jaws; 2) often
moving the mouth forward to its ancestral location
at the front of the snout; 3) reducing the dentition;
and 4) increasing spectacularly the size and number
of gill rakers in the pharynx to act as a filter. The
evolution of filter-feeding has occurred at least
three different times among elasmobranchs. It first
happened in mobu'id rays, such as Manta birostris,
by modification of the primary crushing-feeding
mechanism (Figure 9). Secondly, the whale shark,
Rhincodon typus, resulted from modification of a
secondary crushing-feeding mechanism seen today
in its orectolobid (nurse shark) relatives. Finally, the
gouging lamniform sharks represented by such as
the spectacular mako, Isurus oxyrinchus, and great
white shark, Carcharodon carcharias produced
the filter-feeding basking shark, Cetorhinus
maximus.

The evolution of sharks has been a rich and
varied process. The diversity of feeding

mechanisms in living sharks is extraordinary in view
of the relatively small number of extant species.

Sharks comprise a group of finely tuned
predators, which in their diversity are well
equipped to survive whatever environmental
exigencies may lie ahead.

SanfordA. Moss is a Professor in the Biology Department at
Southeastern Massachusetts University, North Dartmouth,
Massachusetts.

Selected Readings

Gilbert, P. W. 1962. The behavior of sharks. Scientific American

207(1): 60-68.
Johnson, R. H., and D. R. Nelson. 1973. Agonistic display in the

gray reef shark, Carcharhinus menisorrah, and its relationship

to attacks on man. Cope/a 1973: 76-84.
Moss, S. A. 1967. Tooth replacement in the lemon shark,

Negaprion brevirostris. In Sharks, Skates and Rays, ed. P. W.

Gilbert, R. F. Mathewson, and D. P. Rail, pp. 319-329.

Baltimore, Md.: The Johns Hopkins Press.

. 1972. The feeding mechanism of sharks of the family

Carcharhinidae.7. Zoo/. (London) 167: 423-436.
-. 1977. Feeding mechanisms in sharks. Amer. Zoo/. 17:

355-364.

29

Patterns of

Shark

Reproduction

by Perry W. Gilbert

ne reason sharks have survived many millions of
years is because of their reproductive capabilities.
In all species, some 300 to 350 in number, semen is
introduced into the female, fertilizing eggs at the
upperendof hergenital tract. Although most sharks
produce relatively few young at one time, the
embryos receive substantial protection, either
inside resistant egg cases or within the body of the
mother until birth. Once the young sharklet or
"pup" is released from the egg or from the mother,
it is on its own, for there is no parental care. At this
critical time, it may be devoured by predators,
including other sharks, but sufficient numbers
survive to handily perpetuate the species.

Male Reproductive Structures

Claspers. The sex of any shark may be readily
recognized, for the males possess prominent
cylindrical extensions of their pelvic fins known as
claspers. First reported by Aristotle, it was thought
that these structures served to embrace and hold
the female during the mating act. Actually, one of
these claspers is introduced into the distal end of
the oviduct of the female during copulation, and
sperm pass from the male along a groove in the
clasper into the reproductive tract of the female.

Claspers may be recognized even in small
embryos but do not become conspicuously
developed until the testes of the male begin to
produce sperm. We have found in several species of
sharks that the growth of the claspers is very rapid at
about the time the testes begin to produce sperm
(Figure 1), and in a matter of a few months the shark
passes through a period analogous to puberty in
man.

In all sharks, the claspers are supported by
cartilaginous rods, frequently calcified, and in
some, such as the spiny dogfish, Squa/us acanthias,
the distal end of each clasper possesses a prominent
spine that is erected once the clasper is inserted,
thus anchoring the male securely to the female. In
the sandbar shark, Carcharhinus milberti, the tip of
the clasper expands after insertion into the oviduct
of the female; the cartilages of the tip open like the

ribs of a fan at right angles to the clasper axis. The
expanded tip not only holds the oviduct open for
the passage of sperm but also prevents withdrawal
of the clasper.

Siphon sacs. Associated with each clasper is a
curious muscular bladder that lies just beneath the
belly skin of all sharks. These paired structures,
known as clasper siphons (Figure 2), open distally
into each clasper groove. According to W.
Leigh-Sharpe (1920.7. Morph. 34: 245-65), the
siphon sacs become filled with seawater prior to
mating and, after the clasper is inserted, seawater is
discharged from one of the sacs and washes sperm
along the clasper groove into the body of the
female.

The problem of how these empty clasper
siphons became filled with seawater long puzzled
us. It is just not possible to place an empty bladder,
devoid of all air, in seawater and, by squeezing, fill
it. The shark must in some way force or pump water
into these sacs.

30

This 2.5-meter female blue shark, Prionace glauca, was carrying 52 sharklets when she was caught in a shark-fishing
tournament off Long Island, New York. Tenth from left on the bottom row is a decomposing embryo that was already dead
when its mother was disemboweled. (Photo by Harold Wes Pratt, National Marine Fisheries Service)

In 1958, while working at the Mt. Desert
Island Biological Laboratory in Maine, I noticed on
two occasions that adult male spiny dogfish
periodically flexed thei r right or left clasper so that it
formed a 90-degree angle with the long axis of their
body (Figure 3). When I examined the siphons of
these sharks, I found them partly filled with
seawater. By manually flexing each clasper inward,
when the shark was submerged, it was possible to
pump additional seawater into the siphons. Each
time the clasper was flexed, a fleshy funnel
extended outward from the base of the clasper and
served to direct water into the open distal end of the
siphon. If the shark was moved forward through the
water with the clasper tied in the flexed position,
the funnel again served to divert water into the
siphon associated with the flexed clasper. The spiny
dogfish voluntarily flexed only one clasper at a time,

and in no case did it rotate its clasper inward more
than 90 degrees.

It would appear, then, that the siphon maybe
filled as the shark moves through the water with
clasper flexed. Some species may rest in one
position and pump water into their siphons by
alternately flexing and extending each clasper. In
this regard, Stewart Springer injected an isotonic
solution into the caudal vein of an adult male
blacktip shark, Carcharhinus limbatus. He was able
to induce the claspers to revolve inward and
forward the presumed mating position of the
claspers for this species. In 1960, Springer stated:
"As the claspers moved into a forward pointing
position, a funnel, formed by a membrane
supported by rods of cartilage, opened at the base
of each clasper. The mouth of the funnel was also
directed forward and the constricted end led into

31

lOOr

2
2

ID

10

20

30 40 50 60 70
STANDARD LENGTH IN CM.

400
380
360
340
320
300
280
2 260
* 240
x 220
| 200
j 180
160
140
120
100
80
60
40
20

B

10 20 3O 40 50 60 70 80 90 OO IK) 120 130 140 150
STANDARD LENGTH IN CM.

Figure 1. Growth curve of clasper (broken line) and siphon sac (solid line) in (A) the spiny dogfish, Squalus acanthias,anc/
(B) the smooth dogfish, Mustelus canis. (From Gilbert and Heath, 1972)

Figure 2. Siphon sacs of (A) the spiny dogfish and (B) the
smooth dogfish, ventral aspect. The siphon sacs are
situated between the belly skin and body musculature,
end blindly at their forward end, and open into the clasper
groove distally. (From Gilbert and Heath, 1972)

the siphon. The caudal vein was plugged
experimentally to hold the claspers and funnel in
position and the shark was moved forward as
rapidly as possible through the water. This caused
the clasper siphons to fill with water. Application of
additional pressure to the caudal vein resulted in
complete expansion of the fan-like tip of each
clasper."

In addition to drawing in seawater prior to
copulation, the clasper siphons are lined with
epithelial cells that secrete a clear, sticky, slightly
acid, mucus-like polysaccharide-protein substance.
This substance serves to lubricatetheclasperduring
copulation and mayalsocontributetothetransport
of seminal fluid and sperm (Gilbert and Heath,
1972).

Sperm formation and storage. The testes of
sharks, in which the sperm are formed, are paired
structures and are located at the forward end of the
body cavity. They connect via several efferent
ductules with the anterior portion of the elongate
kidney on each side. Transformed kidney tubules
convey the sperm from the efferent ductules to the
ductus deferens. A modified portion of the anterior
kidney, known as Leydig's gland, secretes seminal
fluid into the ductus deferens. In some species, for
example Cetorhinus maximus and Prionace glauca,
sperm traveling along the ductus deferens are
enclosed in packets known as spermatophores.

32

Figure 3. Claspers of the spiny dogfish in (A) resting
position and (B) right clasper flexed medially when
electrically stimulated, simulating the position after
insertion into the female; ventral aspect. (From Gilbert and
Heath, 1972)

The distal end of each ductus deferens is
usually expanded into a sperm storage reservoir, or
seminal vesicle, one on each side of the body. In
some of the larger sharks, such as the basking shark,
Cetorhinus maximus, one seminal vesicle may
contain 5 to 6 gallons of seminal fluid. I have taken
as much as a pint of seminal fluid from the seminal
vesicle of a tiger shark, Caleocerdo cuvieri, 12 feet in
length. During copulation, seminal fluid passes

from the two seminal vesicles into a common
chamber and thence through a urogenital papilla
into the clasper groove.

Mating Activities

During courtship, the male of many shark species
repeatedly bites the female on her pectoral fins as
well as on her back between the two dorsal fins.
These areas frequently appear torn or scarred on
sharks captured during the mating season. Just
prior to clasper insertion, the male usually grasps
the trailing edge of the female's pectoral fin in his
mouth, and, in some species, such as the catshark,
Apristurus riveri, the teeth of the male are modified
for this purpose. Thus it is possible to sex some
species of sharks by their teeth alone.

Relatively few people have actually witnessed
the mating activities of any shark. R. P. Dempster
and E. S. Herald (1961) described copulation in the
hornshark, Heterodontus francisci, Eugenie Clark
(1963) reported on courtship behavior in the lemon
shark, Negaprion brevirostris, and R. H. Johnson
and D. R. Nelson (1978) described copulation in two
common species of tropical Indo-Pacific
carcharhinids, the blackfin reef shark, Carcharhinus
melanopterus, and the reef whitetip, Triaenodon
obesus. In the classic photograph (Figure 4), taken
by F. Schensky in 1914, the male catshark,
Scyliorhinus canicula, is observed to coil about the
female at the time of copulation. In this position, it
would be possible to introduce but one clasper at a
time. This is the probable mating position in the
smaller species of sharks.

Hormone-induced mating behavior. In many
vertebrates, a hormone produced by the pituitary
gland regulates mating behavior as well as the
production of sperm and eggs. It is possible to inject
pituitary extract into certain teleosts and cause them
to shed their sperm and eggs into the water, where
the eggs are normally fertilized. We have frequently

Figure 4. A catshark known
as the European spotted
dogfish, Scyliorhinus
canicula, copulating. The
male has curled itself
about the female and
inserted one clasper. This
is the probable copulatory
position in smaller species
of sharks. (Photo by F.
Schensky at the Helgoland
Aquarium)

33

tried this method to induce mating behavior in
various species of sharks, but these experiments
have, for the most part, been unsuccessful.

In 1960, I collected pituitary glands from
some large sting rays frequenting the shallow banks
of the Bahamas. I carefully removed these
pituitaries from the underside of the brain and dried
and powdered them. More than 200 milligrams of
pituitary powder, suspended in seawater, was then
injected into the body cavities of two adult nurse
sharks male and female at the Miami
Seaquarium. After injection, the sharks were tagged
and placed in the large oceanarium for subsequent
observation. Six other adult male and female nurse
sharks in the the same tank were used as controls
for our experiment. One day later the male and
female nurse sharks that had been injected with
pituitary extract showed a remarkable interest in
each other and swam side by side for the next three
days. None of the other sharks showed this
behavior pattern, nor had it ever been observed in
any of them. While mating was not noted, this
behavior was interpreted as part of a mating pattern,
forthe male would frequently nudgethefemaleand
bite the trailing edge of her pectoral fin.

Female Reproductive Structures

Ovary and eggs. The female reproductive tract in all
sharks receives semen from the male and consists of
a pair of oviducts that join at their forward end to
open into the body cavity by a common funnel, or
ostium, below the liver (Figure 5). Eggs are
produced in the ovaries, or in only the right ovary of
many species. When fully formed, the eggs rupture
from their ovarian follicles into the body cavity in
the vicinity of the ostium. Small, hair-like cells,
known as cilia, located on the peritoneal covering of
the liver and body cavity in the vicinity of the ovary,
create a current of coelomic fluid that moves the
eggs forward into the ostium.

Once in the ostium, eggs are forwarded
down either oviduct by both peristaltic and ciliary
action. Shortly after entering the ostium, the eggs
are fertilized by sperm stored in a swollen portion of
the upper oviduct known as the nidamental gland.
This gland secretes a protective covering about the
fertilized egg. In oviparous (egg-laying) sharks this
covering is very heavy and is usually dark brown or
reddish brown in color. A few deep-water species
produce eggs with transparent cases. J. P. Wourms
(1977) has found that the egg cases of oviparous
sharks are composed of a "unique collagenous
protein," organized as a cholesteric liquid crystal.

Oviparous types. The egg cases of oviparous
sharks vary greatly i n shape and size. The egg case of
the Port Jackson shark, Heterodontus
portusjacksoni, is a cone-shaped structure about 6
inches longwith two spiral, screw-likeflanges about
the outside (Figure 6). It contains a single embryo.
R. H. Mclaughlin and A. K. O'Gower (1971) believe

ostium

nidamental gland
right ovary

uterus

urinary papilla

Figure 5. Diagram of female reproductive tract in the spiny
dogfish, ventral aspect. The left ovary has been removed.
Both ovaries are functional in this species, but in many
species of sharks the left ovary is rudimentary and only the
one on the right side is functional.

that the female, after extruding an egg, carries the
soft egg case in her mouth and places it in a rocky
crevice near shore. Because of its screw-like shape,
it becomes anchored once it has hardened and thus
resists buffeting waves and ocean currents.

Recently (through the courtesy of Lewis H.
Bullock at the Florida Department of Natural
Resources Marine Laboratory), I obtained the egg
cases and developing young of the chain dogfish,
Scyliorhinus retifer, that were taken in a box dredge
at a depth of 750 feet in the Gulf of Mexico. Eggs of
this shark are rectangular: 2 1 /2 inches long, 1 inch
wide, and % of an inch thick. From each corner of
the thin, horny egg case, a prominent tendril
extends 2 to 3 inches. The case of this deep-water
shark is transparent, and one can easily see the large
yolk and developing embryo within (Figure 7).

On July 2, 1953, Captain Odell Freeze of the
shrimp trawler Don's, fishing in the western Gulf of
Mexico, obtained a real prize the egg case of a
whale shark, Rhincodon typus, containing a live
embryo 141/2 inches long (Figure 8). The case
measured 12 inches long, 5 1 /2 inches wide, and 3V2
inches thick.

34

Figure 6. Egg cases of two
hornshark species (A)
Heterodontus francisci
and (B) Heterodontus
galeatus. (From Daniel:
1934. The elasmobranch
fishes, p. 304) The egg case
of the Australian
hornshark or Port Jackson
shark, Heterodontus
portusjacksoni, described
by McLaughlin and
O 'Cower (1971), is similar
to that of Heterodontus
francisci found in
California waters.

B

Figure 7. Translucent egg case and newly hatched young of
the chain dogfish, Scyliorhinus retifer. (Photo by Robert
Pelham)

Viviparous aplacental types. In contrast to
oviparous species, the majority of sharks are
viviparous and retain the fertilized eggs in the lower
portion of the oviduct known as the uterus. The egg
envelopes, secreted by the nidamental gland, are
much thinner than the egg cases of oviparous
species. In some sharks, such as the spiny dogfish,
several fertilized eggs are contained in a single,

thin, amber-colored, horny envelope, known as a
"candle" (Figure 9).

In pregnant females, the uterus becomes
heavily vascularized to supply the developing pups
with oxygen. In some sharks, oxygen is all the pups
receive from the mother during development.
These shark pups must rely on their enormous yolks
for their entire nutriment during their life in utero.

Again, the spiny dogfish is a good example. I
have studied the relationship of mother to
developing young in this species at the Mt. Desert
Island Biological Laboratory in Maine. There, spiny
dogfish are found in large numbers during the
summer months in the cold waters of Frenchman
Bay. The sexes are usually segregated during the
summer months; when one fishes in the upper part
of the bay one catches pregnant females, while the
males are to be found principally in the lower bay,
three miles away.

By means of radioisotopes injected into the
bloodstream of thepregnantfemale,C. Bevelander
and I were able to follow phosphates and sulphates
(substances necessary for the development of the
young) from the bloodstream of the mother out into
the uterine fluid surrounding the developing pup.
Within 12 hours, the radioactive materials passed
through the blood vessels of the mother into the
cavity of the uterus and literally bathed the young
pups in "hot" phosphate or sulphate. After
sampling the uterine fluid and determining the
amount of radioactive material it contained, we
carefully removed the pups one at a time, passed

35

Figure 8. Young whale
shark and egg case from
which it was removed.
(From I. L Baugham, 1955)

them through several rinses of distilled water, and
then assayed various organs in their body with a
Geiger counter. To our surprise, we found that the
pups, although they had been bathed for many
hours by radioactive phosphate and sulphate, had
not picked up these materials and incorporated
them into their own tissues. This has led us to
conclude that the large yolk sac suspended from the
belly and connected to the gut of the spiny dogfish
pup contains sufficient nourishment to last it during
its prolonged (up to 22 months) gestation period,
the longest known for any vertebrate.

Toward the close of the spiny dogfish's
gestation period, the yolk sac is gradually resorbed
(Figure 10), and at birth the young pup, 8 to 9 inches
in length, emerges with a tiny scar on its belly to
mark the former position of the yolk sac. After a few
weeks, the scar disappears, and no trace remains of
thefood reservethat nourished the developing pup
for a period of nearly two years within the body of its
mother.

One of the most unusual patterns of
reproduction to be found in sharks is that of the
sand tiger, Odontaspis taurus a common shark
found off the eastern coastline of the United States

from Cape Cod to Delaware Bay. This species has
been successfully maintained for years in large
tanks at the New York Aquarium and also at
Marineland in St. Augustine, Florida. The sand tiger
matures at about 8 feet. Little was known of its
reproductive eccentricities until Springer caught
one off Chandeleur Island, Louisiana. While
conducting an autopsy on a pregnant female,
Springer reached into the oviduct, and, to his
complete surprise, was bitten by the single sharklet
within. An examination of the other oviduct
disclosed that it too contained a single pup about 9
inches long and light pink in color. Both pups
possessed thread-like, blood-red external gills,
which extended outward from each gill slit. The
external yolk sac had been completely resorbed.
Springer's curiosity was aroused. Over a period of
years, he pieced together the following story.
The sand tiger has one enormous ovary
which serves both oviducts. The eggs are relatively
small, about the size of large peas, and there may be
as many as 25, 000 in a single ovary. Fifteen or 20 eggs
are shed at a time, passing down the oviduct. A thin
egg case is secreted about each group of eggs
(Figure 11). Presumably the eggs are fertilized in the

Ol

Figure 9. Candle young,
two months old, of the
spiny dogfish. One
candle, enclosing 2 to 6
developing embryos, is
found in each uterus of a
gravid female. As the
embryo grows, the thin
candle wall ruptures and
the young spend the
balance of the 20- to
22-month gestation period
within the maternal uteri.
(Photo by the author)

36

Figure 10. Stages in the resorption of the yolk sac, during
the final weeks of the 20- to 22-month gestation period in
the spiny dogfish. (Photo by the author)

Figure 77. Egg clusters from the uterus of the sand tiger
shark, Odontaspis taurus. Each cluster contains 75 to 20
pea-sized eggs and a continuous supply serves to nourish
the single pup in each uterus during the greater part of its
gestation period. (Photo by Robert Pelham)

upper reaches of the oviduct before they become
enclosed in a common case.

As development proceeds, apparently one
embryo grows more rapidly than the rest. Its
carnivorous appetite spells disaster for its siblings
enclosed in the envelope. Afterthat feast, the pup's
growth might be seriously impaired were it not for
the fact that the ovary sheds forth additional egg
cases. These in turn find their way into the oviduct
and thence into the mouth of the young predator.

This process of producing eggs in groups of
15 to 20, only to have them consumed by the single
shark pup in each oviduct, continues for months
until the ovary is completely exhausted of its crop.
By this time, possibly after a full year, the growing
pup in each uterus has attained a length of 40
inches. This indeed is a respectable length for a
shark pup whose mother may measure no more
than 100 inches. All this time, the developing pup is
oriented in the uterus with its head forward. At
birth, however, it somehow turns around in its
confined quarters and emerges from its mother
headfirst. I ntrauterine cannibalism is also known to
occur in mackerel sharks (family Lamnidae) and
thresher sharks (family Alopiidae).

Viviparous placental types. In two families of
sharks, the requiem (Carcharhinidae) and
hammerheads (Sphyrnidae), the developing
embryos, after exhausting theiryolk supply,
depend for the balance of their life in utero on
nourishment and oxygen from the maternal
bloodstream via a yolk sac placenta. We have
studied the placental structure in the silky shark,
Carcharhinus falciformis, and the Pacific blackfin
reef shark, Carcharhinus melanopterus. In the silky
shark, the vascularized yolk sac wall is but loosely
attached to the uterine wall and may be readily
peeled away from it (Figure 12). In the blackfin reef
shark, however, a portion of the yolk sac wall

37

becomes so intimately interdigitated with the
uterine wall that it is impossible to separate the fetal
portion of the placenta from the maternal portion
(Figure 13).

The hammerhead shark placentae we have
examined Sphyrna tiburo, S. lewini, S. mokarran
-all havesimilarintimateconnections between the
fetal and maternal portions. Numerous finger-like
processes, known as appendiculae and believed to
be respiratory in function, extend outward from the
umbilical stalk of Sphyrna tiburo andSphyrna lewini
but are absent in the great hammerhead, Sphyrna
mokarran (Figure 14).

This advanced form of nourishing the
developing young is analogous to that found in
most mammals, for the mother's bloodstream
provides nourishment to, and waste removal from,
the fetal young. The precise physiological
relationship of mother to developing young in
placental and aplacental sharks offers a fertile field
of investigation. Scant attention has been given this
subject since the classic work of S. Ranzi (1932,
1934).

Conclusion

In his excellent 1977 paper, Wourms lists eight
factors that appear to be important in the evolution
ofviviparityand retention of ovi parity, one of which
is the phylogenetic position of the species.
"Oviparity is the least specialized and primitive
pattern" in sharks and "from it viviparity has
independently evolved in several different groups."
Of the 16 families of sharks discussed by Wourms,
12 are viviparous or presumed to be, two are
oviparous, and in two families both types of
reproduction occur. Placental viviparity is confined
to two families. Wourms notes that oviparous
species are generally benthic, littoral, and not of
large size. Viviparous species have more diverse
habitats, have larger embryos, grow to larger adult
size, and are active predators.

The advantages of viviparity are that the
developing young receive protection within the
body of the mother and are assured of a constant
and stable environment. This form of reproduction
culminates in placental viviparity, in which the
developing embryo, via its yolk sac, establishes
intimate contact with the uterine wall and relies on
the maternal bloodstream for nourishment,
oxygen, and the removal of wastes.

Figure 12. Placenta of the silky shark, Carcharhinus
falciformis, (A) intact, and(B) with maternal and fetal parts
separated; p proximal region of the yolk sac; d distal
region of yolk sac; m maternal component of placenta; u
umbilical stalk. (From Gilbert and Schlernitzauer, 1966)

Figure 13. Pups, each with attached umbilical cord and
placenta, of the blackfin reef shark, Carcharhinus
melanopterus. In this species, the fetal and maternal
components of the placenta are intimately interdigitated
and cannot be manually separated. (Photo by the author at
Tikehau, French Polynesia)

38

Figure 14. Developing
young of the scalloped
hammerhead, Sphyrna
lewini (left) and the great
hammerhead, Sphyrna
mokarran (right). Note the
appendiculae, believed to
be respiratory in function,
associated with the
umbilical cord of S. lewini.
(Photo by Robert Pelham)

A

B

The practice of internal fertilization, coupled
with the protection afforded the developing
embryo inside a resistant egg case or within the
body of the mother, assures a high survival rate
during development. Once the young shark
emerges from the egg case or the uterus, it must rely
on its own sensory and motor systems to locate food
and avoid predators. The fact that so many species
of sharks have survived for many millions of years is
testimony to their reproductive success and to the
efficiency of their anatomical equipment.

Perry W. Gilbert is Director Emeritus of the Mote Marine
Laboratory, Sarasota, Florida, and Professor Emeritus of
Neurobiology and Behavior at Cornell University, Ithaca,
New York.

Selected Readings

Baugham, J. L. 1955. The oviparity of the whale shark, Rhincodon

typus, with records of this and other fishes in Texas waters.

Cope/a 1955(11,54-55.
Breder, C. M., and D. E. Rosen. 1966. Modes of reproduction in

fishes. Garden City, N.Y.: The Natural History Press.
Budker, P. 1958. La viviparite chez les selaciens. \r\Traitede

Zoologie, P. P. Grasse, ed., Vol. 13, Part 2, 1,755-90. Paris:

Masson.
Clark, E. 1963. The maintenance of sharks in captivity with a report

on their instrumental conditioning. \nSharksandSurvival, P.

W. Gilbert, ed., 145-46. Boston: D. C. Heath & Co.
Dempster, R. P., and E. S. Herald. 1961. Notes on the hornshark,

Heterodontus francisd, with observations on mating activities.

Occ. Papers Cal. Acad. Sci. no. 33, 1-7.

D'Aubry, J. 1963. Elasmobranch reproduction. South African

Association for Marine Research, Bull. No. 4, 25-30.
Gilbert, P. W., and D. A. Schlernitzauer. 1966. The placenta and

gravid uterus of Carcharhinus falciformis. Cope/a, 1966 (3),

451-57.
Gilbert, P. W., and G. W. Heath. 1972. The clasper-siphon sac

mechanism in Squalus acanthias andMustelus canis. Comp.

Biochem. Physiol. 42A: 97-119.
Johnson, R. H., and D. R. Nelson. 1978. Copulation and possible

olfaction-mediated pair formation into two species of

carcharhinid sharks. Cope/a, 1978 (3), 539-42.
Mclaughlin, R. H.,and A. K. O'Gower. 1971. Life history and

underwater studies of heterodont sharks. Ecol. Monographs

41: 271-89.
Ranzi, S. 1932. Le basi fisio-morphologische dello sviluppo

embrionale dei Selaci Parte I. Pubb. Staz. Zool. Napoli. 13:

209-90.
1934. Le basi fisio-morphologische dello sviluppo

embrionale dei Selaci Parte II e III. Pubb. Staz. Zool. Napoli

13: 331-437.
Schlernitzauer, D. A., and P. W. Gilbert. 1966. Placentation and

associated aspects of gestation in the bonnethead shark,

Sphyrna tiburo. J. Morph., 120: 219-31.
Springer, S. 1960. Natural history of the sandbar shark, Eulamia

milberti. U.S. Fish Wildl. Serv. Fish. Bull. 61: 1-38.
Wourms, J. P. 1977. Reproduction and development in

Chondrichthyan fishes. Amer. Zool. 17: 379-410.

39

sharing fishing information

harpoon dart with transmitter

chum

~~ '

blue shark taking chum

locating more blue sharks

6 '-_
ready to harpoon

I

ready to come aboard

starting to haul aboard

shark with two transmitters

opening belly to remove stomach

Telemetry

and Blue Sharks

Photos by E. Kevin King

These photographs were taken during research conducted by Dr. Francis C. Carey of the Woods Hole
Oceanographic Institution and by Fisheries biologist Nancy Kohler of the National Marine Fisheries Service,
Narragansett, Rhode Island, aboard the 50-foot motor sailer Bird of Passage in July 1980, in waters south of
Martha's Vineyard, Mass. Chum was used to attract blue sharks, Prionace glauca, and after one particular
shark was chosen it was fed whole mackerel and tagged with two transmitters, one for depth and the other for
temperature. The shark's movements were recorded every 5 minutes, and after a specified period the shark
was located, harpooned, and landed (photo sequence). The stomach was removed and measured forweight,
volume, content, and rate of digestion of the mackerel.

harpooning

harpoon placed

checking deck space

blue shark aboard

*"

76

six 10-hour mackerel and a normal one

two 26-hour mackerel

Clectrore
in Blue Sharks

Photo by Marty Snyderman

by Paul R. Ryan

Figure 1. The Boston Whaler from which research was
conducted on the blue sharks, Prionace glauca. (Photo by
Gail W. Heyer)

LA> sharks seeking food in the open sea home in on
the weak electric fields of their prey? Does the
sharks' electric detection system one of the most
remarkable in all nature also aid the animals in
the process of daily movement as well as long-range
migration, allowing them to orient in the open sea
electromagnetically?

To answer the first of these questions, Dr.
Adrianus J. Kalmijn, a specialist in sensory
biophysics at the Woods Hole Oceanographic
Institution, arranged a series of expeditions to the
shark-inhabited waters off Cape Cod. During last
summer, Gail W. Heyer, Melanie C. Fields, and R.
Douglas Fields joined the research effort.

Working at night from a 21-foot Boston
Whaler (Figure 1) in 40 meters of water,
approximately 25 kilometers south of Martha's
Vineyard, they endeavored to test the oceanic blue
shark, Prionace glauca, on its behavioral responses
to electrically simulated prey.

In previous work, under contract with the
U.S. Office of Naval Research, Kalmijn had
demonstrated that the bottom-dwelling,
shallow-water shark Mustelus canis, the common
smooth dogfish, can detect minute electrical
voltage gradients as small as five-thousandths of a
microvolt (= 5 nanovolts) per centimeter. This
degree of electrical sensitivity is by far the highest
known in the animal kingdom. It enables dogfish
sharks and the kindred skates and rays to
locate prey, such as small flounder buried beneath

42

the sand, by the weak DC and low-frequency
bioelectric fields that all aquatic animals produce.

The Blue-Shark Studies

The team first made a few trips to locate a desirable
research site for the blue shark studies and to adapt
the shallow-water gear to the open-ocean work.
During spells of relatively calm seas, four long
nights were spent drifting on the water, one of
which yielded most of the observed feeding
responses. For safety reasons, the crew maintained
radio contact with a nearby fishing boat.

A current source and two pairs of salt-bridge
electrodes, each located 30 centimeters from a
central odor source (Figure 2), produced the
electric fields to simulate the prey. The electrodes
and odor source were suspended 5 meters beneath
a glass viewing well in the bottom of the fiberglass
research vessel,* which was designed to provide a
working platform free of galvanic fields. A single
underwater light, positioned near the water
surface, dimly illuminated the observation area -
just enough to see the sharks, without noticeably
disturbing them.

The blue sharks observed ranged in sizefrom
about 2 to 3 meters. Slender, of a shiny "metallic"
blue color, they commonly roam and feed in the top
layer of the water column and are noted for their
keen sense of sight and smell .

A direct current of 8 microamperes was
applied to one or the other of the electrode pairs to
represent the prey. With the electrodes 5
centimeters apart, the current gave rise to a dipole
field decreasing to 5 nanovolts per centimeter
within a radius of 24 to 30 centimeters from its
source. The electrode pairs were embedded in two
yellow sponges to provide the sharks with distinct
targets.

To attract the sharks to the observation area,
small amounts of menhaden chum were pumped
through the odor port between the two electrode
pairs. According to a random sequence, one dipole
was activated while the other served as the control
for equal trial periods.

During the most active night, five sharks
attacked the test apparatus a total of 40 times, with 2
bites at the odor source, 7 on the unactivated
dipole, and 31 on the activated dipole. On the other
less calm test nights, nine bites were recorded at the
electrically simulated prey and only one bite at the
control electrodes. As faras statistical methods may
be applied to the data, the researchers conclude
that the blue sharks show a highly significant
preference for the current-carrying electrodes.
Thus, despite concurrent olfactory and visual cues,
the oceanic blue sharks will execute typical feeding

*The boat was built through a grant from the Eppley
Foundation for Research.

Figure 2. Dipole apparatus. Electrode pairs are embedded
in two yellow sponges and separated by odor port at
center. (Photo by Call W. Heyer)

attacks in response to electric fields simulating
prey.

The results of Kalmijn's research indicate that
attacks on humans and underwater equipment may
also be elicited and guided by electric fields
resembling those of prey. The human body,
especially when the skin is damaged, creates DC
bioelectric fields that sharks in the ocean can detect
from distances up to at least one meter. The galvanic
fields of metallic objects are usually even stronger
and may either attract or, for that matter, confuse
the animals. This could explain much of the
aberrant behavior of sharks in the presence of man
and underwater gear.

A Compass Mechanism?

Sharks, skates, and rays detect the low-level electric
fields with the ampullae of Lorenzini delicate
sensory structures (Figure 3) in the protruding
snouts of these elasmobranch fishes.

Figure 3. Ampullae of Lorenzini and mechanical
lateral-line system in head region of the shark Scyliorhinus
canicula. Solid dots: skin pores ofelectroreceptors. Small
circles: openings of lateral-line canals. (After Dijkgraaf and
Kalmijn, 1963)

43

Horizontal Component of
Earth's Magnetic Field

Induced Electric Current

Figure 4. A shark swimming through the earth's magnetic field induces electric fields giving the animal's compass heading.
(From Kalmijn, 1974)

Wind-driven and tidal ocean currents flowing
through the earth's magnetic field induce electric
fields that are perpendicular to and, in the Northern
Hemisphere, directed to the left with respect to the
flow of water. When measured with towed
electrodes, the voltage gradients range from 0.05 to
0.5 microvolts per centimeter. In these fields,
marine elasmobranchs may orient electrically,
either to compensate for passive drift or to follow
the ocean currents during migration. In fresh water,
the prevailing electric fields are much stronger and
of electrochemical rather than electromagnetic
origin, offering more local, territorial cues. Over
the years, Kalmijn has demonstrated the animals'
ability to orient with respect to these inanimate,
environmental fields. Thus, in well-controlled
laboratory experiments, the stingray Urolophus
halleri learned to procure food from a plastic corral
to the right with respect to a uniform electric field
and to avoid a similar enclosure to the left with
respect to the field. The stingrays were able to
locate the "correct" corral down to the same
threshold gradient as was found in the studies on
the sharks' feeding responses.

When actively swimming through the earth's
magneticfield, sharks, skates, and rays induce local
electric fields of which the voltage gradients
depend on the fishes' compass headings (Figure 4).
As these fields are strong enough to be detected at
swimming speeds of only a few centimeters per
second, the elasmobranchs could, in addition, be
endowed with an electromagnetic compass sense.
They not only receive the electrical information, but
also are readily trained to orient with respect to the
earth's magnetic field. Natural scientists have often
wondered whether animals, in particular migrating

birds and fish, might not direct themselves to the
earth's magnetic field. Sharks certainly could, and
we may even know their detection mechanism. By
thesametoken, biological organismscouldalsouse
the principle of the magnetic compass needle, as
has been recently demonstrated for bacteria (see
Oceanus, Vol. 23, No. 3, p. 55).

Paul R. Ryan is Managing Editor of Oceanus magazine,
published by the Woods Hole Oceanographic Institution.

Acknowledgment

The author would like to acknowledge the help and advice
given in the preparation of this article by Dr. Adrianus J.
Kalmijn, presently at the Scripps Institution of
Oceanography, University of California, San Diego.

Further Reading

Clark, E. 1981. Sharks: magnificent and misunderstood. National

Geographic magazine, 160: 138-87.
Heyer, C. W., M. C. Fields, R. D. Fields, and A. ). Kalmijn. 1981.

Field experiments on electrically evoked feeding responses in

the pelagic blue shark, Prionace glauca. Short communication

in Biol. Bull., October issue.
Kalmijn, A. J. 1974. The detection of electric fields from inanimate

and animate sources other than electric organs. In Handbook

of Sensory Physiology, vol. Ml/3, A. Fessard, ed., pp. 147-200.

Berlin-Heidelberg-New York: Springer- Verlag.
. 1977. The electric and magnetic sense of sharks, skates,

and rays. Oceanus, vol. 20, no. 3.
. 1978. Electric and magnetic sensory world of sharks, skates,

and rays. In Sensory Biology of Sharks, Skates, and Rays, E. S.

Hodgson and R. F. Mathewson, eds., pp. 507-528. Washington,

DC: Government Printing Office.
-. 1981. Biophysics of geomagnetic field detection. I.E.E.E.

Trans. Magnetics, 17: 1113-24.
Ryan, P. R. 1980. Geomagnetic guidance systems in bacteria, and
sharks, skates and rays. Oceanus, vol. 23, no. 3.

44

Aggression in Sharks:
Is the

Gray Reef Shark
Different?

Figure 1. The gray reef shark, Carcharhinus amblyrhynchos,an aggressive shark of the tropical Indo-Pacific region. It is
known to threaten and attack skin divers. (Photo by j. McKibben)

by Donald R. Nelson

/Vlost shark species do not appear to be very
aggressive. This may seem surprising in view of the
popular image of sharks as voracious predators.
Many sharks are indeed voracious feeders, but
predation and aggression are not the same.

In the strict behavioral sense of the word,
"aggression" refers to fighting in defense of self or
of resources considered valuable. Scientists
distinguish between social aggression fighting
against competitors (usual ly of the samespecies) for
resources such as space, food, or mates and
antipredatory aggression, fighting off predators
(usually of other species) to save oneself or one's
offspring. Predation, killing to obtain food, is
considered separate from aggression by most
ethologists.

If one observes most kinds of sharks in
nature or in large enclosures, one rarely sees overt
aggression between individuals, such as threats,
attacks, or chases. Even during active feeding, each
shark seems interested only in getting directly tothe
food, without threatening or attacking competing
sharks. Such scramble competition can be likened
to football players chasing a fumbled ball, and is
distinctly different from contest competition,
where accesstoadesired item isearned by winning
an aggressive interaction, like boxers competingfor
a trophy. Exceptions to this have been noted, and
will be discussed later, but thus far they have been
relatively few.

In 1970, University of Miami scientists Arthur
Myrberg and Samuel Cruber studied a group of 10

45

bonnethead sharks, Sphyrna tiburo, in a
semi-natural pool at the Miami Seaquarium. They
made a point of mentioning the "relative lack of
belligerency" among members of the group, and
that aggression between individuals was "not seen
during competition for limited food." In more than
200 hours of observation duringa six-month period,
no active fighting was seen. However, they did see
several cases of "hits" by one shark on another, and
a behavior they called the "hunch" -both of which
occurred most often when a newcomer was added
to the pool. Myrberg and Gruber were also able to
show that a subtle, size-dependent dominance
hierarchy existed in the group. Si nee few aggressive
behaviors occurred, they established the hierarchy
by watching "give-ways," where one shark altered
its course to avoid a head-on collision with another.
From observations such as these, we are left
with the impression that, intraspecifically (within a
species), sharks lead relatively peaceful lives in
comparison to many other vertebrates. Numerous
species of mammals, birds, and reptiles are overtly
much more aggressive than sharks; and so are many
fishes, such as the little damselfishes of tropical
coral reefs. Aggressive behaviors in these other
animals, however, are most obvious at times when
they are defending territories, mates, or offspring.
None of these behaviors has yet been observed in
sharks. Is this because they do not exist, or because
sharks in the wild are very difficult to observe? For
instance, copulation is one behavior that we know
exists, yet has never been observed in the great
majority of active, dangerous sharks.

Attacks on Humans: Feeding or Fighting?

What about interspecific aggression? How do
sharks interact with other species, including man?
There is very little data, but certain observations
indicate that some species show dominance over
others. From a vessel at sea, fishery biologist
Stewart Springer observed feeding in a mixed
aggregation of similarly sized silky sharks,
Carcharhinus falciformis, and oceanic whitetip
sharks, C. longimanus. "When competition for a
tidbit was between a whitetip and a silky shark at
close quarters, the silky shark gave way to the
whitetip shark, but, when the competition was
between two whitetips or two silky sharks, both
appeared to close in on the food without
reluctance," Springer wrote. Does the existence of
a subtle "dominance" in a species indicate that it
might be capable of more aggressive actions such
as attacking other sharks or humans? Perhaps, but
more evidence is needed before we can say this for
sure.

What can be learned from statistics on shark
attacks on humans? The International Shark Attack
File (SAF) is a collection of more than 1,600 case
histories obtained from eyewitness accounts,
newspaper articles, medical records, and other

reports. Working at the Mote Marine Laboratory in
Sarasota, Florida, U.S. Navy Captain H. David
Baldridge undertook a thorough analysis of SAF
data, using 1 ,165 cases which were judged complete
enough for computer coding. An important point
that emerged from this analysis is that not all attacks
appeared to be motivated by hunger, as was once
more or less assumed. Baldridge and J. Williams, in
their 1969 paper "Shark attack: feeding or
fighting?", pointed out that many victims bore
wounds of the "slash" type that did not seem
consistent with an attempt to remove flesh. They
concluded that as many as 50 to 75 percent of the
SAF cases could have been non-hunger motivated,
perhaps the "results of aggressive behavior
directed at victims in an attitude of fighting rather
than feeding."

Is it possible that sharks in general are really
more aggressive than previously suspected, and
that we simply have not been able to observe them
at the appropriate times and places? The answer is
probably yes, but there is one notable species, the
gray reef shark, for which we do have direct
experimental evidence of attacks based on true
aggression rather than feeding.

The Gray Reef Shark

In the tropical Indo-Pacific region, around the coral
atolls of Polynesia and Micronesia, there is one
shark that skin divers have learned to be wary of-
the gray reef shark, Carcharhinus amblyrhynchos
(=menisorrah: Figure 1). Although reaching only
about 2 meters in length, it is the boldest, most
aggressive shark of the area, appears dominant over
other reef species, and has attacked divers on a
number of occasions. It also is one of the most
social sharks, in terms of grouping behavior. Study
of this species has been one of the major efforts of
our shark research program at California State
University, Long Beach.

Significantly, nearly all attacks by gray reef
sharks have been prefaced by a distinct
exaggerated-swimming display. This strange body
language was first studied in detail in 1971 by
Richard H. Johnson and myself while workingoutof
the marine laboratory (presently called the
Mid-Pacific Research Lab) at Enewetak, Marshall
Islands. A type of agonistic display (threat display), it
consists of a tense, laterally exaggerated swimming
with the back arched, snout raised, and pectoral fins
lowered (Figure 2). Among other things, it was
determined that an "aggressive" approach by the
diver could trigger the display, especially if the
shark was in any way cornered.

The gray reef sharks of Enewetak are
particularly bold and have a habit of making close
investigatory passes at scuba divers. It can be
disconcerting to a diver to see a shark approach out
of the distant blue, swim directly at him, and circle

46

DISPLAY

NON-DISPLAY

Figure 2. Comparison of
threat display postures
(left) and ordinary
swimming (right) in the
gray reef shark. Note the
arching of the back, lifting
of the snout, and lowering
of the pectoral fins. (From
R. H. Johnson and D. R.
Nelson, 7973; with
permission of Copeiaj

him excitedly at arm's reach. If many sharks are
present, as occurs at some places along the
ocean-reef dropoff, the diver may find himself the
center of attention for a dozen or more sharks.
Aggressive as these sharks may seem, however, full
threat displays are usually not seen in this situation.
If the diver remains calm and "defensive," the
sharks will eventually disperse without incident. We
noticed, however, that if one of us swam rapidly
toward an approaching shark, especially one just
arriving, the shark would almost invariably go into
exaggerated-swimming behavior. We made 10
experimental approaches to sharks in this way and
obtained some degree of display in each case. If we
managed to partially corner the shark, the display
became more intense (Figure 3). Si nee the behavior
was clearly related to provocation by the diver, and
since we knew of one case where it did precede an
attack, we concluded that it probably represented
defensive threat.

Attacks on Divers and Submersibles

Although Johnson and I did not fully realize it at the
time, we came very close to being attacked during
our 1971 experiment. Shortly after our Enewetak
study, we learned of several more attacks by gray
reef sharks on divers and on a small submarine. All
involved the exaggerated-swimming display. As a
result of these incidents and further experiments, it
is now clear that if a diver approaches a displaying

shark too closely, it will quite likely launch a
sudden, high-speed strike. These attacks are so fast
that defense is nearly impossible, and the resulting
bites or slashes can produce severe wounds
requiring emergency treatment, hospitalization,
and reconstructive surgery.

The first agonistic attack by a gray reef shark
that we know of occurred at Wake Island in 1961 ,
and was well documented by Ron Church in an
article in Skin Diver magazine. Church and Jim
Stewart, the diving officer at Scripps Institution of
Oceanography, were free-diving on the ocean reef,
checking out a wave-height recording instrument.
The shark was swimming along a coral ravine and
passed between the two divers, whereupon they
both made moves at it triggering the
exaggerated-swimming behavior. After the display,
the shark abruptly turned and made a
lightning-fast attack on Stewart, delivering two
severe bites just above the elbow. Although the
article described the shark as a "black tip,'' a photo
Church took seconds before the attack clearly
identifies it as a gray reef shark, in agonistic display.

Another attack occurred at Enewetak in 1976
and was witnessed by John Randall, an ichthyologist
from the Bishop Museum, Honolulu. Randall and
Shot Miller were scuba diving in about 20 meters of
water near the deep entrance channel to the
lagoon. Miller had a powerhead weapon and was
"riding shotgun" above Randall in order to protect

47

Figure 3. The effect of
cornering on the intensity
of threat display in the gray
reef shark. In situation D
(strong cornering), an
approaching diver is more
likely to trigger an intense
display and be attacked
than in situation A (no
cornering). (From R. H.
Johnson and D. R. Nelson,
1973; with permission of
Copeiaj

him from sharks. As described by Randall (quoted in
The Book of Sharks by Richard Ellis), "A gray reef
shark came up behind me and started its threat
posturing. Shot whacked his scuba tank with his
powerhead shaft to warn me. The shark (which was
only about 4.5 feet) then veered to him and
threatened him even more strongly, the head
moving thru an arc of nearly 180 degrees. He
didn't have time to look at the shells as the shark
closed on him too rapidly he picked the old
(wrong) shell and it misfired as he struck the shark's
head with it. It came right on and bit him on the
head on one side cut off his face mask and he
headed right for the surface. Shot had seven gashes
that required 25 stitches to close. It was only the
result of a slash with the upper jaw."

Perhaps the worst gray reef shark incident
occurred in 1978at Enewetak on a pinnacle reef near
the center of the lagoon. One five-foot shark
attacked two scuba divers, laboratory manager
Michael deGruy and his partner Phil Light. The
actual strike was apparently triggered when deGruy
took a flash photo of the threat-displaying shark
from about 6 meters away. As described by deGruy,
"Immediately the shark broke its awkward posture,
turned, and began swimming directly toward
deGruy at a high rate of speed. Before deGruy even
lowered his camera from his eye, the shark was half-
way to him. Not having time to get to his bang stick
(powerhead), he reacted by shoving his camera into
the face of the oncoming shark." The charging

shark knocked the camera aside, "opened its
mouth and closed it around deGruy's upper right
arm, elbow, and forearm. Exerting clamping
pressure on the arm, the shark began shaking its
body and head, tearing muscle, tissue, and skin
from deGruy's arm." After releasing his arm, the
shark quickly circled back and bit deGruy's swim
fin, removing a chunk of rubber. Phil Light moved in
with his multi-pronged "shark billy," but the shark
attacked him also, raking his left hand with its lower
teeth, then grasping the billy in its mouth and
shaking it violently before releasing it and
swimming away. Both divers were evacuated to the
U.S. Navy Hospital in Guam, and later transferred to
Honolulu for surgery.

Not only have gray reef sharks attacked
divers, but they have also struck small diver
submarines. In the late summer of 1971, about six
months after the Johnson/Nelson study, marine
biologist Walter A. Starck 1 1 arrived at Enewetak on
his own vessel. He had with him a two-person
submersible called the Perry Sharkhunter. Starck
had previously seen movie footage that Johnson
and I had taken of the displaying gray reef sharks.
He soon recognized that the Enewetak grays would
respond aggressively to the submarine if pursued,
even at relatively slow speed. Not only did the
sharks threat-posture at the sub; some eventually
attacked it. Rhett McNair, then laboratory manager
at Enewetak, was with Starck in the sub one day and
described what happened when they followed one

48

shark in intense display: "The shark moved slowly
ahead of us in this attitude for perhaps 30 seconds
before exploding into an incredibly fast back loop
which brought it crashing straight down onto the
half-inch-thick plexiglass hood a few inches over
our heads. The deep scratches on the hood clearly
showed that both upper and lower teeth bit the
plexiglass. ..." From this attack and others like it,
it became evident that gray reef sharks would not
hesitate to attack adversaries many times larger than
themselves.

Experimentally Induced Attacks

It was clear that the threat and attack behaviors of
the gray reef shark were very relevant to an overall
understanding of the problem of shark attack on
humans. It also was obvious that it was too risky for
unprotected divers to attempt to study this
behavior, so our California State University group
set out to build a bite-proof diver vehicle specifically
forexperiments on shark aggression. Designed and
built by Robert R. Johnson and myself, the
one-man, fiberglass Shark Observation
Submersible (SOS) was smaller, faster, and more
maneuverable than the two-person sub previously
used at Enewetak (Figure 4). The streamlined SOS
has an acrylic-dome entry port at the forward end
which also provides excel lent visibility for the diver
lying prone within. The scuba air supply, battery
pack, and foam flotation are mounted inside. The
three electric motors, two forward "pectoral fins,"
and aft tail fin are all independently controllable by
the operator. The craft can be launched from a small
boat, usinga special aluminum-rail launching ramp.
Initial experiments on gray reef sharks were
conducted at Enewetak in 1977 and 1978 by Robert
Johnson, James McKibben, Gregory Pittenger, and
myself. A total of 10 attacks on the SOS were
elicited, several being double strikes, and several
causing minor damage to the sub. Typically,
exaggerated-swimming display was triggered by an

Figure 4. The author with the Shark Observation
Submersible as used at Enewetak, Marshall Islands, in
1978. The streamlined, fiberglass craft is 8 feet long and 2
feet in diameter. It is entered underwater by removing the
forward acrylic-dome port. (Photo by I . McKibben)

Figure 5. A gray reef shark performing exaggerated-
swimming display in response to the submarine. In this
case, the shark is "carouse/ling" (circling with) the sub,
and is making no apparent effort to escape. (Photo by J.
McKibben, from 16mm movie footage)

"oriented pursuit" - the sub following the shark's
every move (Figure 5), especially if this resulted in
some degree of cornering. The shark would then
slow down, intensifying its display as the sub
neared. The attack itself usually came when the sub
had closed to about 2 meters, by which time the
shark had often begun to roll somewhat on its side
in a very tense, contorted posture. The strikes were
incredibly fast. In one attack filmed by Wild
Kingdom photographer Ralph Nelson, the shark
took only .33 of a second to hit the sub, biting the
forward motor and breaking the plastic propeller
(Figure6).

Experimental trials were run to test the
effects of 1) presence of bait, 2) grouping type, 3)
location on reef, and 4) species of shark. Gray reef
sharks would attack either with or without bait
present, but seemed more attack-prone if they were
already at the test site and did not have to be baited
in. Lone individuals seemed more prone to display
and attack than those in aggregations or schools.
Attacks occurred over flat reef bottoms and along
steep dropoffs (Figure 7). Significantly, all of the
attacks were by gray reef sharks (both sexes).
Neitherattacknorfull display could be elicited from
silvertip sharks, Carcharhinus albimarginatus;
blackfin reef sharks, C. melanopterus; or reef
whitetips, Triaenodon obesus.

49

Figure6. Agonistic attack by a gray reef shark on the approaching submarine. Note the extreme rolling and intense posture
just prior to attack. Shark bit motor and broke plastic propeller, disabling sub. (Photos by R. Nelson, from 16mm frames,
courtesy of Don Meier Productions)

50

Figure 7. Attack from the rear by a gray reef shark at Enewetak in 1978. The shark avoided a direct frontal attack, instead
circling around and striking from behind. (Photos by A. Ciddings, from 16mm footage, courtesy of Hessischer Rundfunk,
Frankfurt, West Germany)

Attack Motivation

Why do gray reef sharks attack divers and
submarines? The sharks are certainly not trying to
eat the subs. Furthermore, the exaggerated-
swimming behavior is very conspicuous exactly
the opposite of what would be expected prior to a
feeding-motivated attack. No predator forewarns its
prey of its intent to attack. The real question is
whether the shark regards the sub or diver as a
competitor for food or other resources, as a danger
to itself, or as both.

If the reason is competitive, is the shark
defending a territory? Although this idea is
frequently mentioned, it must be emphasized that
territoriality in sharks is still only a theory, and has
not been scientifically established. If gray reef
sharks were territorial in the usual sense, one would
expect that a resident would exclude other gray reef
sharks with as much or more vigor than it would
exclude other species. Behaviors such as threats
and chases have never been observed between
individual sharks, even though they are frequently
close enough together for this to happen.

51

Individuals, in fact, intermix freely in both baited
and unbaited situations with no obvious aggression
toward one another. Is it possible that all the sharks
at a particular spot recognize each other as familiar
individuals? Would a shark from afar be recognized
as a stranger and attacked? This would seem
unlikely for the loosely-grouped sharks found on
the outer reefs, considering the extent of their
movements and the numbers of other sharks they
must encounter. Trackings of these sharks tagged
with ultrasonic transmitters show they can make
location changes of up to 15 kilometers per day, and
are less site-oriented than the sharks of the lagoon
reefs. Territoriality in these sharks, therefore, is
improbable.

Yet there are other observations which do
suggest a type of territoriality, or at least a
site-dependent dominance. Sometimes a lone
shark on a lagoon pinnacle reef will swim directly up
to a newly arrived diver and exhibit a mild or
moderate threat display, without any apparent
provocation by the person. If the diver (or sub) then
advances on the shark, its threat intensifies and an
attack can be easily induced (FigureS). These lone
sharks inhabiting the lagoon pinnacles or patch
reefs are the most aggressive ones we have
encountered at Enewetak. Is it possible that these
individuals are in a "territorial phase," while others,
such as those from the ocean-reef dropoff, are not?
This question could probably be answered by a
detailed telemetry study tracking a number of
neighboring sharks over periods of several months
or more. One could then intercept and observe
these sonically-tagged individuals at various times
and places to look for signs of territorial behavior.

McNair believes that he has seen territorial
behavior in certain gray reef sharks at Enewetak that
he identified by scars or other markings. According
to McNair, there is a "predictable difference in
temperament when the same individual is
encountered in different areas. On one piece of
reef, the shark may always be aggressive, for
example, while a half mile away it may be docile or
shy, indicating that the first place was 'home.' After
seeing this pattern repeat itself with the same
individual several times, territoriality seems the
only logical conclusion." Whether this indicates
territoriality is a semantic question. Some would call
an area of elevated aggressiveness or dominance a
"dominion," unless actual forceful expulsion of
intruders were demonstrated. Whatever it is called,
site-dependent aggression in sharks would be a
significant finding, and McNair's observations
should be confirmed by more quantitative studies.

Another possibility is that the sharks are
attacking because of a defensive, antipredatory
motivation, regarding the sub as an object
dangerous to themselves. If so, the exaggerated-
swimmingdisplay has the samewarningfunction as
the rattling of a rattlesnake. And yet if this is the

Figure 8. Acrylic dome of the Shark Observation
Submersible showing several bite scars (tooth scratches)
from attacks by gray reef sharks. (Photos by]. McKibben)

case, it is a real mystery why the sharks do not just
swim away when pursued by the relatively slow-
movingsubmarine. Is itpossibletheydo not realize
they can easily outswim the sub? The other common
reef sharks (blackfin, whitetip, silvertip) always
move away when chased, often in a high-speed
bu rst, but the gray reef sharks more often choose to
stand and fight. Behaviorists often refer to "flight
distances" and "fight distances" in predator-prey
situations, the latter delimiting what is sometimes
called a "personal space" surrounding the animal.
When a predator is seen approaching, the prey
animal will flee when the predator reaches the flight
distance. If, perhaps by surprise, the predator gets
to within the fight distance, the prey may suddenly
turn and attack. This attack presumably gives it a
better chance for an eventual escape. In the case of
the gray reef shark, there does not seem to be any
flight distance; only the fight distance. The shark
permits the submarine to approach without any real
effort to get away. After attacking, however, the
shark often flees the area at high speed.

If the antipredatory hypothesis is correct,
then one must ask why the sharks need such a

52

behavior. What predators might represent a danger
to the gray reef shark, itself a relatively large
predator? Larger species do occur in the same areas,
for example the tiger shark, Caleocerdo cuvieri, and
the Galapagos shark, Carcharhinus galapagensis,
but the extent of their predation on gray reef sharks
is unknown.

What other possibilities are there for the
unusual aggressiveness of the gray reef shark?
Marine biologist Richard Johnson, in his book
Sharks of Polynesia, argues that this species may be
expressing a general dominance, such as for the
purpose of intimidating potential competitors for
food. He relates an incident from the Cook Islands
in which a speared but escaped fish was about to be
eaten by a moray eel. "A gray reef shark appeared
and was observed to direct a display posture toward
the eel, which persisted in its efforts to feed on the
fish. The shark abruptly terminated the display and
attacked the eel, leaving a noticeable white slash."
In a potentiallyantipredatory context, he reportsan
observation in which a gray reef shark apparently
displayed to an approaching hammerhead shark,
Sphyrnamokarran, much largerthan itself. Johnson
suggests that exaggerated-swimming display occurs
"under such a variety of circumstances, it seems no
single motivation can adequately account for all
situations."

Aggressive Behavior in Other Sharks

Besides gray reef sharks, do other species exhibit
aggressive patterns such as threat, chase, or attack?
Definitely yes, but for most sharks the information
available is mainly anecdotal bits and pieces.
Careful observational studies are needed, both in
the natural environment and in captivity situations
such as Myrberg and Cruber used to study
bonnethead sharks. They noticed the similarity
between the hunch posture of the bonnethead and
the more conspicuous threat display of the gray reef
shark. Both have similar postural elements -
arched back, snout up, and pectoral fins down -
but the exaggerated-swimming component was not
seen in the bonnetheads. It was significant that the
hunch, although only rarely seen, occurred mainly
by resident sharks toward newcomers, or when a
diver-observer entered the pool. A hunch posture
also was noted in captive blacknose sharks,
Carcharhinus acronotus, and in free-ranging silky
sharks under related circumstances.

The bonnetheads also made "hits" on other
individuals, especially newcomers. Similar hits
were observed in scalloped hammerhead sharks,
Sphyrna lewini, in the Gulf of California during
studies of their schooling behavior by A. Peter
Klimley and myself (see page 65). Are such hits
aggressive, or for another reason, such as courtship?
It is well known that mating in sharks can be rather
rough on the females, as the frequently seen
"mating scars" attest.(Figure9). Some such scars are

definitely tooth marks from bites, as on gray reef
sharks, while others appear more like scrapes
caused by hits with the snout, as on female
hammerheads. These scars are believed the result
of ardent courtship activities by males and/or efforts
by males to gain purchase on females during
copulation. Eugenie Clark, of the University of
Maryland, observed courtship biting in the
short-nosed gray reef shark, Carcharhinus wheeleri,
in the Red Sea. Writing in \\r\eNational Geographic
magazine, she described how a female "swimming
among a group of sharks would break away, almost
as if inviting trouble. A male in the group would
quickly oblige, rushing at her and biting her, often
severely. Each would eventually return to the
group." In one case, observed at a distance, a male
appeared to make an attempt at copulation after
biting the female. These "courtship attacks"
produced quite deep gashes on the female's fins
and pelvic flanks, which appeared to heal rather
quickly. Damaging as they may be, however, such
courtship bites are not considered aggression in the
usual sense of the word. Bites on male sharks,
however, may be a different matter.

Figure 9. Mating bites on a female gray reef shark from
Enewetak. Note the severity of the tooth gashes, some of
which were produced by bites using both jaws. (Photos by
J. McKibben)

53

Recent evidence suggests that the mako
shark, Isurus oxyrinchus, is a rather aggressive
species (Figure 10). Robert Johnson and Jeffrey
Landesman, of California State University, Long
Beach, have observed interactions in baited
aggregations of pelagic sharks off southern
California and have noted howaggressive the mako
appears in comparison to the more commonly seen
blue shark, Prionaceglauca (see page 42). In several
instances, one mako was observed to chase another
away from the bait basket, as if protecting a personal
space or the food source itself. Open-mouthed
"jaw-gapes" were frequently seen (perhaps a type
of threat), and the sharks sometimes charged
divers. Some males bore clear bite scars, possibly a
sign of intraspecific fighting. Underwater
photographers Howard Hall, Marty Synderman,
and others have seen similar behaviors in baited
makes and are unanimous in assessing their
disposition toward divers as aggressive. Thus far, no
mako shark has actually bitten a diver, but there
have been some close calls, and the concensus is
that if a mako is not treated with caution, a serious
attack might occur.

Do any other sharks attack man for
antipredatory or other non-feeding reasons? Both
the Atlantic and Pacific species of lemon shark,
Negaprion brevirostris and N. acutidens, have been
reported to make violent retaliatory attacks on boats
or divers if sufficiently provoked, such as by being
speared or harpooned. Some attacks, however,
occurred even with non-contact provocation. John
Randall, in a chapter in Sharks and Sur\'ival, relates
incidents in Florida in which lemon sharks charged
and bit boats after being chased over shallow flats.
According to Richard Johnson, the lemon shark in
French Polynesia, while generally shy of divers, is
"widely noted for its malevolence if disturbed.
Attempting to touch, let alone prodding, shooting
at, or spearing, is reported to result in an attack
released in anger against the person or boat
involved."

In none of the above lemon-shark incidents
was a specific threat posture noticed, but an
experiment by A. Peter Klimley, while a graduate
student at the University of Miami, is significant. At
the Sharkquarium, on Grassy Key, Florida, he
dressed in a wet suit painted to resemble a killer
whale (complete with dorsal fin) and entered an
enclosure containing several lemon sharks. He
swam in a "porpoising" manner at an eight-foot
shark, and it immediately became agitated -
swimming in front of him in rapid, tight circles and
figure-eights and displaying repeated rapid
openings and closings of the mouth. These
behaviors appeared to be directed at Klimley, and
were probably threats. They were not seen when
Klimley swam at the sharks wearing a normal
bathing suit.

The Great White Shark

What about aggression in the great white shark,
Carcharodon carcharias, the world's largest
predatory fish and close relative of the mako? Might
some of the attacks by white sharks on humans be
due to aggression, perhaps territorial, rather than to
feeding? This intriguing idea has been repeatedly
advanced, but on close examination has little
support. For one thing, territorial residents usually
confront and threaten intruders before resorting to
attack. Most white-shark attacks have occurred
without warning, from behind the victim, as if the
shark were stalking prey. Furthermore, aggressive
attacks like those of the gray reef shark are
usuallyforceful, all-out efforts. Accordingto Daniel
Miller and Ralph Collier, who have recently
published a well-documented analysis of shark
attacks in California, most white shark attacks were
"apparently slow, deliberate movements." They
reached the general conclusion that "most of the
attacks resemble the feeding behavior of an
isolated, large shark that appears to be investigating
an object." John McCosker, Director of San
Francisco's Steinhart Aquarium, emphasizes that

Figure 10. The shortfin
mako shark, Isurus
oxyrinchus, aggressively
approaches the
photographer during a
baiting session off Santa
Catalina Island, California.
(Photo by C. Matheson)

54

the great white shark is a "man-attacker but not a
man-eater" and usually releases its human victim
shortly after the first bite. He points out the
similarity of a black neoprene-suited skin diver to
the shark's normal pinniped prey(seals). Millerand
Collier likewise mention how a person paddling on
a surfboard could also resemble a pinniped from
below. It seems most reasonable, therefore, that
the white-shark bites are cases of mistaken-identity
predation. Why do the sharks release their victims?
Probably because they quickly sense that
something is wrong that the person (often
wearing a neoprene suit, lead weights, and a steel
tank) is not the food object they expected.

Does this imply that white sharks do not have
aggressive behaviors? Not necessarily, for large bite
scars have been seen on male whites, possibly the
result of aggressive action by other whites. Fights
between white sharks, of course, are presently
conjecture, but some intraspecific interactions have
been noted by Australian underwater
photographers Ron and Valerie Taylor, who have
filmed baited white sharks many times off southern
Australia. Valerie writes that whites avoid being
close together, and if two are on a collision course,
"each, on sighting the other, will flick away at great
speed." One large white they observed seemed to
have an "unchallenged right of way," and smaller
ones always gave way to it as soon as it was within
sight. Although theTaylors never observed outright
aggression between white sharks, they did witness a
case in which a white was the recipient of
aggression by a much smaller sea lion. In 10or15
minutes of active harassment, the sea lion
succeeded in chasingthe white shark from the area.
In California, sea lions have been observed on
several occasions to chase and nip at mako sharks,
causing them to flee the area (J. Landesman, M.
Synderman).

In conclusion, it is becoming clear that quite
a few species of sharks participate in some
aggressive interactions. Does this support
Baldridge's suggestion that most shark attacks on
man are non-feeding motivated? Perhaps, but more
information is needed before this can be said with
certainty. The gray reef shark remains the only shark
presently known to attack man for violating a
specific warning display. Is it unique in this regard?
Probably not, but only future behavioral studies will
tell. Unfortunately, most other species of
dangerous sharks are more difficult to observe in
the natural environment than is the gray reef shark.

Donald R. Nelson is a Professor of Biology at California
State University, Long Beach. He has been studying sharks
since 7962, when he was a graduate student at the
University of Miami.

Acknowledgment

Dr. Nelson's program of research is supported by the
Office of Naval Research under contract
N00014-77-C-0013, NR-104-062, with additional support
from the National Geographic Society and the Mid-Pacific
Research Lab (Enewetak) of the University of Hawaii.

Selected Readings

Baldridge, H. D., Jr. 1974. Shark Attack, 236pp. New York, NY:

Berkley Medallion Books.
Baldridge, H. D., Jr., and). Williams. 1969. Shark attack: Feedingor

fighting? Military Medicine 134: 130-133.
Clark, E. 1981. Sharks Magnificentand misunderstood. National

Geographic 160(2): 138-187.
Ellis, R. 1975. The Book of Sharks, 320 pp. New York, NY: Grosset

and Dunlap.
Gilbert, P. W., ed. 1963. Sharksand Survival, 578pp. Boston: D.C.

Heath and Co.
Johnson, R. H. 1978. Sharks of Polynesia, 170 pp. Papeete, Tahiti:

Editions du Pacifique.
Johnson, R. H., and D. R. Nelson. 1973. Agonistic display in the

gray reef shark, Carcharhinus menisorrah, and its relationship

to attacks on man. Cope/a 1973: 76-84.
Klimley, A. P. 1974. An inquiry into the causes of shark attacks. Sea

Frontiers 20(2): 66-75.
Klimley, A. P., and D. R. Nelson. 1981. Schooling of the scalloped

hammerhead shark, Sphyrna lewini, in the Gulf of California.

Fishery Bulletin 79(2): 356-360.

McCosker, J. E. 1981. Great white shark. Science 81, 2(6): 42-51.
McNair, R. 1975. Sharks I have known. Skin Diver 24(1): 52-57.
Miller, D. J., and R. S. Collier. 1980. Shark attacks in California and

Oregon, 1926-1979. Calif. Fish and Game 67(2): 76-104.
Myrberg, A. A., Jr., and S. H. Gruber. 1974. The behavior of the

bonnethead shark, Sphyrna tiburo. Cope/a 1974: 358-374.
Nelson, D. R. 1977. On the field study of shark behavior. American

Zoologist 17: 501-507.
Nelson, D. R., and R. H. Johnson. 1980. Behavior of the reef sharks

of Rangiroa, French Polynesia. National Geographic Society

Research Reports 12: 479-499.
Springer, S. 1967. Social organization of shark populations, pp.

149-174. In Sharks, Skates, and Rays, P. W. Gilbert, R. F.

Mathewson, and D. P. Rail, eds., 624 pp. Baltimore: Johns

Hopkins Press.
Taylor, V., and R. Taylor, eds. 1978. Creaf Shark Stories, 403 pp.

New York, NY: Bantam Books.

Attacks on Animals

Sharks have been known to attack and at
times devour a wide variety of land animals,
including dogs, cats, cattle, and horses.
Race-horses have been attacked a number of
times in Australia, where they are routinely
exercised in the surf. And there is one story of a
thirst-crazed elephant which, in 1959,
stampeded into the sea off Kenya, evidently in
search of water on a nearby island. It never
made it; huge sharks attacked and tore the
pachyderm to shreds.

Adapted from Shark Attack
by H.David Baldridge

Lemon Sharks:

Supply-Side

Economists

of the

Sea

by Samuel H. Gruber

higher predators make a living or where they
acquire their resources.

Information on the dynamics of shark
populations including data on age, growth, food
intake, and mortality is required to develop a
rational approach for managing this under-utilized
living resource. Yet such statistics are simply not
available because historically sharks have not been
an important fishery resource in the United States.
However, with the implementation of the 200-mile
United States fishery conservation zone a few years
ago, fishery management councils were mandated
by federal law to provide management plans for the
utilization of living resources, including the top
predators. Results of the present research on the
lemon shark can directly aid fishery scientists by
providing baseline data for estimating rates of

Sharks comprise one of the most important and
successful groups of top predators in the marine
environment. In the pelagic realm, for example,
ubiquitous sharks, such as the blue, dusky, silky,
and oceanic whitetip, may represent the most
numerous/arge predators in the sea. Yet the
influence of these creatures on such factors as
exchange of energy between trophic levels remains
largely unknown. This is because very little is known
of the basic biology of most sharks. Much of what is
known arises from fishery statistics or experimental
research. Few comprehensive field studies have
been undertaken in which the ecology of a single
species has been broadly investigated.

To bridge the gap in our understanding
of the basic biology of sharks, a five-year,
multidisciplinary study, supported by the National
Science Foundation, has been undertaken toassess
the role of the lemon shark, Negaprion brevirostris,
in the tropical marine environment. The overall
objective of this program is to provide a conceptual
model for this species with which we will be able to
predict its "cost of living" in units of energy, its rate
of production, and, eventually, its impact on the
animal communities on which it feeds. To make
these predictions, we are studying a number of
major biological variables, such as behavior,
population dynamics, and bioenergetics.

Little is known about the actual effects of
"apex predators," such as sharks, on the marine
ecosystem. Indeed, little is known about the
ecology of sharks in general. By way of contrast, the
flow of solar energy to primary producers via
photosynthesis is fairly well understood. How that
energy in the form of living tissue gets transferred
from trophic level to trophic level, however, is less
understood. For example, at the apex of the food
web, we have little idea how fast sharks grow, how
long they live, how much food they require, how
efficiently they convert food into tissue, and so on.
In short, we do not know much about how these

Photo by Ed Fisher

production in shark populations the biological
basis for any resource management.

The choice of the lemon shark as a subject for
study came about after serious consideration. First,
it is a highly successful species as judged by
abundance within its range. It is a member of the
most successful family of sharks and grows to large
size. Possibly the most important aspect is this
species' ability to adapt to captivity. Oceanaria are
able to keep adults in large tanks for years; smaller
lemon sharks have been kept under rigidly
controlled conditions for periods of up to six years.

Field Studies

The actual research in our program can be broken
down into a number of subtasks under the major
headings of field and laboratory investigations. The
first field study is an orthodox mark-and-recapture
program. Nearly 1,300 young lemon sharks have
already been tagged and released back into the
environment. The eventual goal is to mark 2,500 of

56

these sharks over a period of five years. The
recapture of about 10 percent of our marked
population will permit us to estimate such variables
as population size, growth rates, mortality of the
various age groups, local movements, and
long-term migration.

Each of the captured sharks has been
weighed, measured, and cataloged as to sex. It was
then fitted with a plastic tag in its dorsal fin and a
darttagwas placed in its back behind the fin. Then it
was given a freeze brand and a small plastic
identification tag was surgically implanted in its
body cavity. Finally, it was given a shot of
tetracycli ne to mark it for age and growth
determination. Tetracycline is taken up in the hard
parts of the shark's body, such as the vertebral
centra which make up its flexible spine. These

A 62-centimeter (total length) lemon shark. This size is
typical of the young specimens used in laboratory
research. The lemon shark grows to a maximum size of
more than 3 meters.

centra have rings in them in the same way that a
cross section of a tree shows annual growth rings.
The problem with sharks, especially tropical ones, is
that we don't know how many rings are laid down
per year. By injecting the animal with tetracycli ne, a
fluorescent marker is made on the ring at the time of
injection. If the animal is recaptured say five years
later, there will be a ring that shows up under
ultraviolet light and it will be a relatively simple
matter of counting rings to determine the number
of rings elaborated in unit time. Then it will be
possible to fix the age of any lemon shark simply by
counting the number of rings in a centrum.

Preliminary findings from this tagging study
indicate that young lemon sharks remain localized
in their first years of life. Also, they grow more
slowly than had been previously thought. A control

study on the effects of tagging on growth was done
using 35 lemon sharks held under semi-natural
conditions. The unmarked (control) sharks grew
slightly faster (8 percent by weight) than the marked
subjects. Thus the tagging method does seem to
affect the shark.

Another subtask is our ongoing investigation
of lemon shark eating habits. We have identified a
number of prey items from these sharks by
pumping out their stomachs. Food items consist
mostly of teleost and crustacean remains, including
fish, crawfish, crabs, and, curiously, lots of turtle
grass. Some larger lemon sharks specialize in
stingrays as evidenced by the great number of
spines embedded in their jaws and gums. However,
more quantitative food studies presently underway
must be completed before we can hope to
understand the impact of lemon shark populations
on the communities on which they feed.

In sum, an essentially pristine population of
lemon sharks has been sampled, measured, and
systematically marked. Resulting data are being
integrated into the model of input/output energy
relationships of this species. One final point is that
we have begun an aerial census of lemon sharks.
This method will give us an independent estimate of
lemon shark abundance.

A second field study involves acoustic
telemetry of the lemon shark. Little is known about
shark behavior because sharks in general are
wide-ranging animals. However, for the overall
project to have meaning we must know what the
animals do from day to day. This is especially true if
we are to assess the relative importance of activity to
their budgeting of energy in the natural
environment. Thus we have placed transmitters on
eight lemon sharks and have followed their
movements for periods of up to 112 hours. We were
able to pinpoint one shark's location every 15
minutes for five days.

Because lemon sharks frequently inhabit the
shallow flats around mangrove islands, we were not
able to track them with an ordinary boat and so we
developed a very stable airboat. In addition to the
airboat, we have employed a motorized glider to
make aerial observations of shark behavior.

Several majorpointsaboutthelemon shark's
behavior can be inferred from the trackings. First,
the larger sharks (1.8 to 2. 2 meters in length) are
somewhat site-oriented, although not as much so as
the very young ones. We observed recurring
patterns of activity in which certain of the lemon
sharks returned to a spot just to the east of North
Bimini, Bahamas, each day. We considered this area
a refuge, and by aerial observation we confirmed
the presence of several other lemon sharks milling
about there. Unlike some other species, lemon
sharks do not passively drift with the current.
Measurements taken during tidal changes verified
that the animals are able to orient with respect to a

57

Crass section of the vertebral centrum from a 2.34-meter
lemon shark. The concentric rings are the key to
determining a shark's age. Injected tetracycline
accumulates on the outer ring and will show up under
ultraviolet light when the shark is recaptured years later.
(Photo by author)

particular locale and maintain a heading across or
into the current.

Our lemon sharks were almost equally active
day and night, with a rate of movement just over 1 .5
kilometers per hour. However, this rate rose at
dawn and dusk to nearly 2.5 kilometers per hour;
this was because the lemon sharks were strongly
affected by the sun. Each morning and even ing they
made a long, concerted move toward the sun. Thus
weconcluded thatthe lemon shark is crepuscular, a

finding which agrees with that of other marine
biologists who have observed that reef sharks are
also more active at twilight.

Still the belief persists that sharks are
nocturnal and there is good scientific evidence
that, for some species, this is true. For the lemon
shark, however, the evidence is conflicting:
although ourfield studiesdid not reveal an increase
in activity at night, our laboratory experiments
clearly did. In a respirometer, both the rate of
activity and the metabolic rate significantly
increased at night. Perhaps size differences or
effects of captivity can explain this disparity, but we
will need more data before we can identify this
shark's period of peak activity.

The underwater acoustic beacon attached to
the shark is directional, so we were able to observe
our tagged animals several times underwater. On
five occasions, during three different trackings, the
sharks were associated with several jack fish
species. Because of the unusual interaction
between the jacks and sharks we tentatively
concluded that lemon sharks may utilize the
expanded sensory capabilities of a school of jacks as
an aid in finding prey.

While lemon sharks spend much time in the
shallow flats, they are not restricted to that habitat.
One large shark, which had been captured in waters
only 1 .5 meters deep, swam over a drop-off into 400
meters of water on the first day of tracking. The next
morning we located it on a reef in about 20 meters of
water. This was repeated a year later when a
2.5-meter male shark swam from a reef out into
deep Gulf Stream waters and then moved 100
kilometers north before returning to the shallow
reefs off Miami Beach.

The concept that emerges from this tracking
and from other fishery data is that of an
ever-expanding horizon for the lemon shark.

Underwater photograph of
a transmitter being
attached between the
dorsal fins of a lemon
shark. The cigar-sized
transmitter is tied to a thin
plastic plate, which is
secured to the shark by
two barbs imbedded in its
flesh. This procedure takes
less than five minutes if
the shark is calm. (Photo
by Dee Scan)

58

Three standard ultrasonic transmitters used to track sharks.
Designed by Don Nelson, they emit a 40-kilohertz acoustic
signal. (Photo by Don Nelson)

The ultralight powered glider used to track sharks from the
air. Assembled and launched from the deck of a research
vessel, it weighs 50 kilograms and folds into a package 5.5
meters by 7.75 meters. (Photo by Irene Brown)

Bimini Island, showing the
movements, over a
24-hour period, of the
third shark tracked by the
research team. The small
circles are fixes which were
taken at regular intervals.
The larger circle and
arrowhead represent the
beginning and end of this
tracking, respectively. The
solid line and filled circles
represent nocturnal
activity, while the dashes
and open circles show this
shark's path during the
daylight hours. The map
demonstrates that this
shark made a long run east
at sunrise and west at
sunset. This pattern was
repeated on five
successive days. The area
where the shark lingered
and doubled back is a
daytime place of refuge for
lemon sharks.

Shark 3.
9 July 1980
24 hour track
0015 h - 2345 h

N

1km

59

Duringthefirstfewyears of life, the species remains
restricted to a relatively small area, perhaps 6 to 8
square kilometers. As the shark nears maturity, it
has gradually increased its activity space to about
300 square kilometers, but still it remains in the
shallow flats and bays near land. After maturity, the
shark expands its territory to include reefs and some
deeper offshore waters. At this point, long
migrations may be undertaken. Yet the shark
remains attracted to the coastal zone; females bear
their young in grass flats, lagoons, and other very
shallow tropical habitats.

Laboratory Studies

As for the laboratory part of our project, the primary
objective involves balancing the "energy budget"
for the lemon shark. In other words, we would like
to be able to account for the fate of all calories the
shark takes in. Although a shark receives its calories
from the living tissue of its prey just as we do from
our food, it partitions these calories in a somewhat
different manner. For us, much of our caloric intake
goes toward providing the heat necessary to keep
our bodies warm. Lemon sharks, being
cold-blooded, do not have this caloric "expense."
However, they are at the mercy of the
environmental temperature to keep up their bodily
activities. This means that if the water temperature
falls too low the shark could die of starvation
because its activity rate is directly proportional to
temperature. The major utilization of a shark's
calories goes toward activity, while some energy is
required to break down food into its useful
components and run the biochemical and excretory
machinery. The remainder is used in respiration and
growth. By balancing the "energy budget" of the
lemon shark, we will be able to specify the rate,
amount, and sources of energy that this predator
must remove from its environment to maintain itself
at observed levels of activity and growth.

The laboratory investigations are organized
into three areas: metabolic studies, blood gas
parameters during exercise, and intake and
production studies. The lynchpin of the laboratory
work is metabolic rate. How much energy does the
shark consume in its daily activities? What are the
diel variations in caloric expenditures and what are
the causes of such variation? What is the maximum
sustained rate of caloric expenditure? Howdoesthe
performance of the shark compare with its caloric
utilization? To answer these questions, we have
built a metabolic chamber in the form of a sealed
circular raceway. A small shark placed in the
chamber is free to move about unhindered. The
difference between the (saturated) oxygen content
of water entering and that of water leaving the tank
is a measure of the instantaneous oxygen
consumption of the shark. Sinceoxygen uptakecan
be converted into calories burned, this method is
called indirect calometry, and is a well-known

technique for measuring metabolism of aquatic
organisms. By manipulating the subject sharks prior
to or during testing, it is possible to answer basic
questions about metabolism. For example, if we
wish to determine the energetic cost of digesting a
meal rich in fats, we simply compare the
metabolism of a shark under standard conditions to
that of a shark just fed an oily mackerel.

To date, we have establ ished that the average
metabolic rate of the young lemon shark is about
200 milligrams of oxygen consumed per kilogram of
shark per hour. This works outto about 1.2
kilocalories burned every hour. However, that rate
increases at night and decreases during the day. The
tropical lemon shark is thus about two times more
metabolically active than its temperate cousin, the
spiny dogfish. Lemon sharks have the ability to
"rest" on the bottom, but, curiously, they burn
about 9 percent more energy resting than when
swimming. This is probably because the resting
shark must actively pump water over its gills an
energy-consuming process and because oxygen
extraction may be inefficient at low water velocity.

To determine extraction efficiency and to
understand the kinetics of the oxygen flow from
environment to shark, we have developed a surgical
technique for implanting a fine tube in the dorsal
aorta, a major blood vessel serving the shark's body.
The surgery is rapid and recovery is complete, often
within three hours. Sharks that have been operated
on usually eat the same day, and the tubes have
remained in place for more than 80 days. With this
tube we can withdraw a sample of shark blood at will
and rapidly analyze its pH, electrolyte, and gas
composition. This study has produced some
striking and unexpected findings.

A respiration chamber used to measure the oxygen
consumption and thus the metabolic rate of young lemon
sharks. Containing 70 liters of circulating seawater, the
donut-shaped chamber provides enough space fora
60-centimeter shark to swim nearly four body lengths in
circumnavigation. (Photo by Peter Bushnell)

60

collar >

LATERAL VIEW

ventricle
afrium

VENTRAL VIEW

Through a surgically-implanted tube, researchers can
withdraw a sample of blood from a shark at will, directly
from the animal's aorta. This sketch shows the position of
the plastic tubing, which is inserted under the skin of the
buccal cavity and worked back until blood signals that it
has entered the aorta. The tube is then passed through the
head and fixed in place with two plastic buttons (collar).
Sharks have survived up to 80 days with this tube in place.

Oxygen-Rich Blood

The circulatory system of the lemon shark is unlike
that of any otherfish thus far studied. During
exercise, most fish and mammals draw on the
oxygen reserves of their venous blood. For
example, during a chase, the partial pressure of
oxygen bound in the blood flowing through a fish's
veins may fall to a half of the resting value. Lemon
sharks, however, do not have a venous reserve.
Under normal conditions, they draw off most of the
blood-bound oxygen on the arterial side of the
circulatory system leaving almost no oxygen in
venous blood.

However, like other predators, lemon sharks
must chase down prey and flee predators. To do so,
they have evolved a different strategy. During
exercise, they produce an abundance of red blood
cells which quickly enter their bloodstream.
Simultaneously they open an extra 20 percent of
their gill surface to permit enhanced oxygen
exchange. Finally, the blood itself has a great affinity
for oxygen, completely saturating at a partial
pressure some 200 percent lower than most fishes.

Similar high-affinity blood has been found in
burrowing animals and fetuses, which inhabit

environments with a low oxygen content. Thus we
suggest that this respiratory mechanism is an
adaptation for survival in an oxygen-poor habitat.
This makes sense, since lemon sharks are often
found in areas with low oxygen concentrations,
such as very shallow backwater bays within
mangrove islands, where organic matter
accumulates and water temperature can exceed 30
degrees Celsius.

The remaining laboratory studies are
centered on rates of production in the lemon shark
and include experiments on food intake, digestion,
assimilation, and growth. One often hears the
statement that the shark is the perfect "eating
machine. "This conjures up the image of a mindless
automaton always on the prowl, mechanically
attacking and devouring anything that gets in its
way. This impression has even been supported in
some scientific literature: one worker stated that
hunger and satiation play no role in the behavior of
a shark. Common sense would dictate that a
vertebrate animal as highly evolved as a shark would
have mechanisms to control and synchronize food
intake, which, of course, they do. Curators in
oceanaria and scientists using sharks as subjects
have long known that, within limits, sharks will not
overeat; and they can be quite fussy about what
they ingest.

So, to establish the roles of hunger and
satiation, the rate and rhythms of food intake, the
efficiency of food conversion into growth, and the
rate of growth itself, we placed a number of sharks
into several large aquaria (up to 6,000 liters) and
carefully controlled water quality factors, such as
temperature, salinity, oxygen content, and
illumination. These sharks were given unlimited
amounts of preweighed fish fillet and allowed to
feed to satiation twice per day for 100 days. Results
clearly demonstrated that hunger waxes and wanes
on a four-day cycle. The average shark (70
centimeters long) consumed an equivalent of 3
percent of its body weight daily. By the end of the
100-day trial, it had grown in weight by 50 percent.
This means the shark converted 19 percent of its
ration to growth. The remainder, some 43.3
kilocalories, was "burned" daily as fuel to run the
shark's physiological machinery. Thus the picture
emerges of an animal that feeds in bouts and
controls its intake within narrow limits, growing at a
rate similar to other young predators, such as the
freshwater pike.

The second stage in the processing of food
occurs in the stomach. We have therefore
measured rates of digestion and gastric evacuation
as estimators of meal size, feeding rates, and
feedingfrequency. Rate of digestion could limitthe
number of meals per week, while stomach volume
might set a limit on prey size. Of course, digestion
provides the only source of energy available to the
animal and, as such, must be specified to estimate

61

A lemon shark breaks the surface to grab a preweighed
piece offish fillet. Each shark in this 100-day experiment
was allowed to eat as much as it wanted, twice a day.
(Photo by author)

the animal's daily energy requirements. By
withholding food for three days, then feeding sharks
a ration of fish fillet equal to 3 percent of their
bodyweights, then pumping stomachs at 3-hour
intervals, we determined that digestion was nearly
complete after only 24 hours. Using dyed fish, we
found that food can pass completely through the
shark's digestive tract in only 12 to 14 hours.
However, dyed feces continues to show up for two
to three days. Feeding sharks live fish equivalent to
20 percent of their body weights gave a very
different result. We have recovered undigested
food from the stomach even after48 hours. Thus
meal size is an important factor in rate of digestion
and, ultimately, in feeding frequency.

Growth Rate Studies

The final and one of the most important parameters
of an "energy budget" is growth rate, which is a
direct measure of production. The rate at which an
organism removes energy from a lower trophic level
defines its impact on the ecosystem and establishes,
at least in part, the dynamics of trophic webs. Since
growth in a top predator represents the "end of the
line" for the transfer of energy up the food web, it
would be possible to deduce the overall efficiency
of that transfer if production rate, population
numbers, and type of food were all known. Thus we
have studied growth in some detail.

The growth of sharks is poorly understood.
Some species, like the Japanese smooth dogfish,

A fish inside a fish. This X-ray of a lemon shark shows the whole pin fish, Lagodon rhomboides, that it ate one hour earlier.
Digestion appeared complete after approximately two days.

62

reach maturity in only two years. Others, like the
great white shark, may require a decade or more to
attain a length at maturity of 4 meters. The growth
rate of the lemon shark is probably between these
extremes. Originally, it was thought that this
species reached maturity (2.4 meters) in only 12
months. Later that figure was revised upward to 24
months. Based on these tentative conclusions, the
lemon shark has become known as a
rapidly-growing subtropical shark. However, my
studies indicate a much slower rate of growth.

In Florida Bay, lemon sharks give birth in the
spring to between four and nine young, each about
60 centimeters long. At first, these newborn lemon
sharks rapidly increase in size, but growth
decelerates over time until it reaches an asymptote.
We have measured the rapid growth of these
newborns in two experiments. In both studies, the
sharks were free to consume as much food as they
wanted.

The growth rate of these 40 experimental
animals averaged about 0.6 millimeters per day.
Such a rate implies that 7.5 years are required to
reach maturity, provided that growth is constant. If
this figure is correct, the lemon shark grows

considerably slower than first suggested. Support
for this contention was gained when we ran a simple
computer simulation of growth, assuming length at
birth of 60 centimeters, maturity at 245 centimeters,
and a maximum size of 300 centimeters. Again,
assuming a gestation period of one year, maturity
would be reached in just over seven years.

Besides revising our growth rate estimate for
the lemon shark, these studies clearly show that
food is a limiting factor. Captive lemon sharks grow
four times faster than tagged ones. It is here that an
analogy with supply-side economics applies.
Crudely stated, supply-side economists suggest
that by increasing the supply of economic products,
demand for these products will automatically
follow. Thus the economy can be manipulated and
perhaps controlled.

In "biological economics," the same
thinking applies. Clearly, without adequate
supplies (that is, prey), predators cannot survive.
Many examples of "boom and bust" situations are
known in animal populations where the fate of a
predatory species is directly tied to its prey. In our
shark studies, we also find that productivity is
dependent upon resources. In other words, if you

A computer simulation
growth curve for the
lemon shark, based on a
gestation period of 12
months, a 60-centimeter
birth length, and a
300-centimeter maximum
length. Assuming the
lemon shark reaches
maturity (the beginning of
sexual activity) at 245
centimeters, it would take
some seven years to reach
this length. This is close to
the estimate of 6.5 years,
which is based on
laboratory studies and
tagging returns.

LJ

^-00 40.00 80.00 120.00 160.00 200-00

TIME [MO)

240-00 280-00 320-00

63

increase the supply side of the system by providing
more food, the demand will automatically rise and
sharks will increase their intake, to a point.

Unfortunately, it is the opposite which
usually occurs in nature these days. In the realm of
the lemon shark, man has reduced environmental
quality through pollution, construction dredging,
commercial fishing, and other human activities.
Thus the supply side of the shark's economy has
been unfavorably affected. While I can only
speculate that the numbers of lemon sharks have
been declining in recent years, they could quickly
get in trouble if their birth and growth rates were to
fall. Lemon sharks have a reproductive strategy and
growth similar to whales: low fecundity, slow
growth, and delayed maturity. Thus, unlike most
fish, shark populations can quickly become
seriously depleted at the hands of man if care is not
taken in their management.

Our research project is just over two years
old; results seem to me like pieces of a jigsaw
puzzle. Some of the pieces are partly formed while
others are missing. Certainly, we will not find all the
pieces (our program will run at least through 1983),
but there will be enough so that an attempt can be
made to come up with a representation of the
life-style of the lemon shark to use as a basis for
comparisons with other species.

Samuel H. Gruber is an Associate Professor in the Division
of Biology and Living Resources at the Rosenstiel School of
Marine and Atmospheric Science, University of Miami,
Miami, Florida.

Acknowledgment

The author wants to thank the following groups: AMS Oil
for donating synthetic lubricants; Donald Merten of CAI,
Inc., for the loan of an ultrasonic receiver and
hydrophone; OMC (Evinrude) for the loan of a 55 hp
motor; Tycoon-Finn Nor and Southern Tackle for the

donation of fishing equipment; Lederle and Phiser, Inc.,
for the donation of tetracycline; Miami Welding for the
donation of several hundred liters of liquid nitrogen and
oxygen, and Bruce Grey of U.S. Soaring for loan of the
Wizard aircraft. The tag study was carried out at Seaworld's
Shark Institute, Layton, Florida. This study was funded by
the Biological Oceanography Section, National Science
Foundation under grant number OCE 78-26819 and OCE
81-10400. I thank Dr. Robert Carney for his advice and
support. Drs. Donald Nelson and Peter Lutz are senior
investigators in this project.

Suggested Reading

von Bertalanffy, L. 1960. Principles of a theory of growth. In

Fundamental Aspects of Normal and Malignant Growth, ed. W.

W. Nowinsky, pp. 137-259. Amsterdam: Elsevier.
Brett, J. R., and J. M. Blackburn. 1978. Metabolic rate and energy

expenditure in the spiny dogfish, Squalus acanthias. ]. Fish

Res. Bd. Canada 35: 816-821.
Cruber, S. H. 1980. Keeping sharks in captivity./. Aquariculture

1(1): 6-14.
Gruber, S. H., and A. A. Myrberg, Jr. 1977. Approaches to the study

of the behavior of sharks. American Zoo/. 17: 471-486.
Hobson, E. S. 1968. Predatory behavior of some shore fishes in the

Gulf of California. Bureau of Spt. Fish. Wildl. Res. Rpt. 73: 1-92.
Holden, M. ). 1977. Elasmobranchs. In Fish Population Dynamics,

ed. J. A. Gulland, pp. 187-215. London: John Wiley and Sons.
Kleiber, M. 1975. The Fire of Life: An Introduction to Animal

Energetics. Huntington, N.Y.: R. E. Krieger.
Myrberg, A. A., Jr., andS. H. Gruber. 1974. The behavior of the

bonnethead shark, Sphyrna tiburo. Cope/a 1974: 358-374.
Nelson, D. 1974. Ultrasonic telemetry of shark behavior. Nav. Res.

Rev. 27(12): 1-21.
Olson, A. M. 1954. Biology, migration, and growth rate of the

school shark (Caleorhinus australis Macleary) in southeastern

Australian waters. Aust. ]. Mar. Freshwater Res. 5: 353-410.
Ricker, W. W. 1975. Computation and interpretation of biological

statistics from fish populations. Bull. Fish Res. Bd. Canada 191 :

1-382.

Soucie, G. 1976. Consider the shark. Audubon 78(5): 36-54.
Springer, S. 1950. Natural history notes of the lemon shark,

Negaprion brevirostris. Texas j. Science 2(3): 349-359.
Winberg, G. 1956. Rate of metabolism and food requirements of

fishes. Fish Res. Bd. Canada Transl. Series 194: 1-202.
Zahuranec, B. J. 1975. Shark research. Present status and future

direction. ONR report ACR-208. Arlington, Va.

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64

Photo by Marty Snyderman

Grouping Behavior
in the Scalloped Hammerhead

by A. Peter Klimley

/Although swimmers and sport divers usually
encounter no more than a few sharks at a time,
occasionally they sight a massive group of sharks
concentrated in a small area. A number of such
startling encounters in June of 1977 along the coast
of the Gulf of Mexico near Corpus Christi, Texas,
involved as many as 2,000 sharks concentrated in
the surf zone along a 24-kilometer stretch of
shoreline popular with bathers. This leads one to
wonder how common grouping is amongthe more
than 300 species of sharks. What types of sharks
form such groups, and what behaviors go on within
them? Are the groups com posed of adult males and
females engaging in courtship, adult females giving
birthtotheir young, or juveniles seeking protection
from predation? The common function of defense is
less likely because of the paucity of predators large
enough to feed upon sharks.

Fishery scientists and commercial fishermen
have been aware for years of grouping, from
variations in their catches. Sometimes numerous

sharks are caught on hooks on only one section of a
longline, or are tangled in only one part of a gill net.
Also, one longline and net haul may contain an
enormous number of sharks; another may contain
none. Some behavioral scientists have been
fortunate enough to directly observe grouping on
some occasions, more commonly from the deck of a
ship or through the window of an airplane,
however, than underwater in the shark's habitat.

Diversity of Grouping Species

Grouping (a gathering of three or more sharks)
occurs in a wide variety of shark species with
different evolutionary histories, habitats, and
feeding habits. It occurs in the bullhead shark,
Heterodontus portus/acksoni, considered primitive
because of its possession of characteristics present
in early fossil sharks. This shark spends its life
inshore on a rocky bottom and feeds on
invertebrates. The less primitive requiem
(Carcharhinidae) sharks also group.

65

The blacktip Carcharhinus limbatus, the
dusky shark C. obscurus, the sandbar shark C.
plumbeus, and the gray reef shark C.
amblyrhynchos also live inshore but are found more
often in midwater and are primarily fish eaters. The
basking shark, Cetorhinus maximus, and the whale
shark, Rhincodon typus, both reported to group at
times, generally live offshore and feed upon
macroplankton. The scalloped hammerhead,
Sphyrna lewini, spends most of the day along the
dropoff region and moves offshore at night. Itfeeds
on both offshore and inshore fishes and squid. In
all, grouping has been reported in the scientific
literature for five of the eight orders of sharks and
has been observed in another, leaving only the
hexanchiformes and pristiophoriformes orders
without schooling members. Such diversity argues
that grouping probably occurs in some part of the
life cycle in most species of sharks.

Despite the large number of shark species
observed to group, there has been little study of
these groups or of the motivation behind sharks
gathering in such groups. Observers have failed to
determine whether such groups were aggregations
with sharks responding to ecological factors, such
as the presence of clumped prey or upwardly
flowing currents, or were schools with members
drawn together by social bonds. In addition,
observers have failed to note whether sharks were
swimming in a polarized or non-polarized school.
Members of a polarized school all move together in
a common direction, maintaining a constant
distance from each other and changing their
directions synchronously. Authors have referred to
such groups as "large concentrations," "groups,"
"schools," and "packs"; only recently did Donald
Nelson and Richard Johnson, both of California
State University, refer to groups of gray reef sharks
as "social groups."

So far, few attempts have been made at
describing the size and sex of sharks actually within
groups, as well as their behavior patterns. During
the last four years, I have been studying by direct
observation groups of three species of sharks, the
leopard shark, Triakis semifasciata, the blue shark,
Prionace glauca, and the scalloped hammerhead,
Sphyrna lewini. Since my observations of groups of
scalloped hammerheads are at this time the most
complete, I will confine myself to this species in the
rest of the article.

Bajo (a seamount), and Las Arenitas, on the
northwestern coast of Isla Cerralvo (Figure 1).

Scalloped hammerheads are ideal for
underwater study because group members remain
together, swimming near the surface in a relatively
small area for prolonged periods during the day.
They also are not aggressive at this time, and are not
frightened by the repeated approach of
investigators. A single hardship demanded of
observers is that they must free-dive without the use
of scuba tanks because the sharks rapidly move
away from scuba divers, presumably responding to
the sonically and visually conspicuous air bubbles
emitted from their gear.

The members of scalloped hammerhead
schools swim in a polarized fashion (Figure 2). The
degree to which the sharks are oriented in a
common direction is comparable to several other
schooling bony fishes. Tanya Tarshis, an
undergraduate student, found the mean angular
deviation in the direction of individual sharks from a
common direction of the group was 23.4 degrees.
She calculated this by summing the deviations by
vector addition. Although this measure of schooling
has been determined for only a few species, the
deviation is similar to that of a common schooler in
southern California waters, a topsmelt,/\f/7er/nops.
The mean three-dimensional distance between
nearest hammerhead neighbors of 0.92 body
lengths is less than that of the topsmelt and other
marine schoolers, a silverside, Menidia, and the
bonito Sarda, and a freshwater schooler, Tilapia.
Although not yet measured, there appears to be an
obvious tendency of members with! n the schools to
follow directional changes of sharks along the front
of the school.

In addition to swimming in a polarized
fashion, the scalloped hammerheads form schools,
not aggregations. They remain together at the
locations because of an attraction to each other, not
solely to an environmental factor, such as the
presence of upward-lifting currents near the
sloping ridge of the El Bajo seamount. When the
current velocity at the seamount diminishes during
slack tide, school members remain together,
although their parallel orientation is generally less
pronounced. While some prey species are
occasionally observed in the vicinity of the
seamount, the majority are in deeper waters
offshore, yet the sharks remain near the seamount
during the day.

The Scalloped Hammerhead

Scalloped hammerheads spend most of the day
along coastal and insular dropoffs and leave these
sitesat night, probably to forage in the surrounding
pelagic environment. Three locations in the Gulf of
California where the scalloped hammerhead
schools regularly gather are at Isla Las Animas, El

Description of Groups

The average size of groups encountered during our
free dives is about 20 sharks. However, groups with
more than 100 sharks are not uncommon. The
members of the schools are predominately female.
During the summer of 1979, females outnumbered
males by the ratios of 1 .6 to 1 at Isla Cerralvo, 3.8 to 1

66

115'

110

25

Figure 1. Three locations
in the Gulf of California
where schools of
scalloped hammerheads
have been repeatedly
encountered: V Las
Arenitas, a cluster of rocks
WO meters off of Isla
Cerralvo; 2) El Bajo, a
broad-surfaced seamount
with its approximate
extent marked by a dotted
line; and 3) Isla Las
Animas. (From Klimleyand
Nelson, Fishery Bulletin)

Isla Las
Animas

El
Bajo

USA

Isla Del
Espintu Santo

30

25

Figure 2. Hammerhead
school as viewed from the
side. Note polarized
aspect of school with
members oriented in the
same direction and
similarly spaced. (From
Klimley and Nelson,
Fishery Bulletin)

67

attheEl Bajoseamount,and3.1 to1 farther north at
Isla Las Animas. The sizes of sharks within the
groups vary at different locations. Sharks from El
Bajo Gorda, another seamount off the sou them end
of the Baja peninsula, were considerably larger,
with median length of 196 centimeters, than those at
El Bajo and Las Animas with median lengths of 176
and 161 centimeters, respectively. However,
considerably smaller sharks moved into the El Bajo
Gordaarea during the spring of 1981.

The predominance of females appears to
match previous fishery studies in which the catches
of sphyrnid and related carcharhinid species were
strongly female-dominated. Similar disparities in
sex ratios led fishery biologist Stewart Springer to
examine numerous pregnant sandbar sharks to
determine the sex ratio of their full-term pups. He
also examined catches of newly born sharks. The
parity in such ratios led him to hypothesize sexual
segregation for the sandbar shark. He felt that adult
males lived over a larger geographical and depth
range, perhaps in deep, cool oceanic waters
inaccessible to fishermen's gear, while the females
were in warmer inshore waters accessible to
fishermen. Because the temperature gradient
between inshore and offshore waters lessens in late
spring and early summer, he believed the males
moved inshore then to mate with the females.

Measurements of the lengths of sharks
swimming in the schools as well as their individual
distances from each other were determined in the
sharks' habitat using a photogrammetric technique
known as stereophotography. I swam down to the
edge of the school and positioned a beam with two
separated cameras of parallel optical alignment
facing toward a single or several sharks. I then
depressed a trigger, simultaneously firing both
cameras. Later, I measured under a microscope the
minute distance between the snout and tail on the
shark's photographic image (Figure 3b: I) and the
separation between a point, either the snout or tail
tip, on the shark's images from the right-hand and
left-hand cameras (Figure 3b: Xj-xJ. This
displacement is equivalent to the 50-centimeter
separation of the cameras and provides a scale with
which to measure the shark's length from its image
length (I) with a correction for imperfect camera
alignment. The seal loped hammerhead in Figure 3 is
the largest measured to date, reaching 371
centimeters. The shark's huge size should be
evident to the viewer from the number of
displacement lengths that will fit into the length of
the shark image.

The promising stereophotographic
technique will be used again in an attempt to verify
our impression that larger sharks remain along the
edges of the groups. From photographs taken from
outside the group, one can measure approximate
distances from the group's nearest edge to any
shark within, and then compare the lengths of

Figure 3. Stereophotographic pairs of a free-swimming
hammerhead shark. Upper photograph (a) was taken by
right-hand camera; lower photograph (b) by left-hand
camera. Measurements ofx, and x 2 were made with respect
to the left-hand edge of the frame and resulted in the
displacement (x z -x,). Measurement I was made from the tip
of the snout to the tip of the caudal fin. (From Klimley and
Brown, CIBCASIO Transactions, in press)

peripherally located sharks to those centrally
located.

Acrobatic Behavior

Hammerheads within the schools do not always
maintain their parallel schooling orientation.
Frequently single or several adjacent sharks
accelerate from their parallel positions into
acrobatic behavioral patterns. Commonly sharks tilt
their bodies laterally, revealing their highly
reflective undersides for prolonged periods of time.
They then often accelerate upward or downward
and shake their anterior torso or head
spasmodically. The upper right-hand shark in Figure
4 is shown with its head thrust to the side during a
headshaking behavior. This photograph was taken
from a single 16-millimeterframeof movie film.
There appear to be many variations to the behavior.

68

A shark may shake its head continuously,
discontinuously, to one side, or to both sides.
Sometimes the behavior involves just the head;
sometimes the whole forward torso is thrust to the
side. Earl Herald, the late director of San Francisco's
Steinhart Aquarium, observed this behavior in
hammerheads during one of his visits to Isla Las
Animas and called it the "shimmy dance."

Most acrobatic of all behaviors is what I term
"corkscrewing," which involves an explosive
acceleration of the shark into a small circular path
less than a body length in diameter while the shark
rapidly twists its torso around 360 degrees. This all
takes only a second. Almost as spectacular is a
behavior pattern in which the shark quickly rolls
onto its back and propels itself forward in a jerky
manner with exaggerated beats of the tail, while at
times thrusting its midsection to the side.

The three behaviors so fardiscussed all result
in a reflection of light off the ventral surface of the
shark, visible to the observer and to other sharks at a
great distance. It is quite possible that these pulsed
flashes of light are visual signals aimed at other
members of the group. I am now measuring
components of these frequently repeated
behaviors and applying a statistical analysis to their
spatial and temporal features to assess the extent of
their stereotypy or constancy of form, which is an
indicator that they are used in communication.

Other less-frequent behaviors occur within
the groups. One is a sudden movement of a shark
downward, hitting its snout against the back of the
shark below. On two occasions sharks have ended
"corkscrewing" behavior by contacting a nearby
shark on its back. Another prominent behavior is a
wide opening of the jaws. Within the group, this
behavior is presumably directed at school

Figure 4. Shark in upper right-hand corner performing
head-shaking behavior. Note scarring and color-coded
streamer tag on shark beneath head-shaking shark. (From
Klimley and Nelson, Fishery Bulletin)

members, but at other times it is performed by
solitary sharks in the sole presence of a diver. In this
context it is probably a mild aggressive threat
directed at the diver.

Although I have compiled a relatively
complete catalog of behavior patterns in the last
three years by direct observation and repeated
viewing of extensive videotape samples, I am just
beginning to see sequential relationships between
the behaviors. The demonstration of a progression
of behaviors characteristically occurring within the
groups leading to responses, such as copulation,
prey capture, or the attack of another shark, could
lead to an understanding of the reason or reasons
for grouping. Although behaviors such as
"corkscrewing" have been observed to precede a
"hit," which in turn released "headshaking" and
momentary departure of the two sharks from the
school in possible pairing behavior, the sequences
have not been observed to lead to very revealing
acts, such as copulation. Future research will center
on further identifying serial relationships and on
identifying behaviors outside the group by
following one shark at a time, since the
sequence-ending behaviors may be occurring in
slightly deeper water away from the groups.

It is possible that some of the behaviors we
have described may lead to mating. Many of the
school members bearabrasions (see tagged shark in
lower right-hand corner of Figure 4). These are
small, recently inflicted, white contusions, where
most of the dermal denticles are removed, or older,
partially healed, black contusions (FigureS). As one
can see in the histograms, scars occur almost
exclusively on females. Furthermore, these scars do
not occur all over the females but primarily in the
first three 10-percent-length-divisions on
the right and left lateral and dorsal aspects. The
predominance of scars on larger females and their
restricted placement coupled with observations of
the "hit" behavior suggest that these scars may be
similar to other bite scars inflicted by other species
of sharks during mating.

Function of Grouping

What then is the function of these massive groups of
hammerheads? Four broad functional possibilities
are likely: 1) reproduction grouping to carry out
courtship activities, 2) defense grouping to avoid
predation, 3) swimming efficiency grouping for
hydrodynamic advantage, and 4) feeding -
grouping to increase predatory success through
cooperation in locating or capturing prey, or the
clumping of individuals centrally in relation to prey
distribution.

Evidence points toward a rejection of the first
hypothesis. A large number of the sharks are quite
small, less than 140 centimeters long. Current
examination of the reproductive systems of
similarly sized sharks that were captured by local

69

GO

o

CO

O

>-

o

LU

rr

20

10

20

10

20

10

20

10

lateral (right)

lateral (left

dorsal

ventral

FEMALES (white, recently inflicted scars)

FEMALES (black, past inflicted scars)

L

MALES white, recently inflicted scors)

MALES black, past inflicted scars)

i i i i i i i i i i i i i

ooooo ooooo
ro 10 r o~>

ro
I I I

cr>

ooooo o o

rO in I s - CD r ro

ID CO

CD

00

TEN PERCENT TOTAL LENGTH CLASSES

Figure 5. Frequency of
recent and past-inflicted
scars occurring within 10
percent divisions of the
total length for different
aspects of free-swimming
male and female scalloped
hammerheads. The scars
were recorded from films
taken at El Bajo during July
and August, 7979. (From
Klimley and Brown,
CIBCASIO Transactions,
in press)

fishermen indicates these sharks are immature.
Evidence for the rejection of the second hypothesis
is the absence of any predators, such as the tiger
shark, Caleocerdo cuvieri, or the white shark,
Carcharodon carcharias, in the hammerheads'
offshore habitats during the daytime when the
hammerheads are swimming in schools. The third
reason seems unlikely since the sharks remain near
the upward-sloping seamount pinnacles even
during slack tide, when currents are absent.

This leads us to the feeding hypothesis.
Daytime feeding does not occur, or is an extremely
rare event. Co-workers and myself have never
witnessed what we have all agreed to be an
unequivocal predatory act. Furthermore, several
attempts at attracting members from the schools to
macerated prey or to sounds resembling those
generated by prey have only attracted five
hammerheads.

Feeding must then occur during the night.
Do the sharks move off the seamount at night in
groups and stalk their prey cooperatively at that
time? We have some evidence that the sharks leave
the seamount at different times and in different
directions, moving independently of each other.
Nelson (see page 45) attached a telemetry
transmitter to a school member (shaded circles,
Figure 6). We then located the group, using this
tagged shark, and attached another transmitter to a
second shark (clearcircles, Figure6). In Figure6our
first paired tracking is diagramed. After tagging the
second shark we anchored the small tracking boat
over the seamount pinnacle and took directional
bearings on the two sharks at 5-minute intervals.
More recent trackings, involving two tracking
boats, have more precisely located the sharks.

Each polar plotin thefigurecan bethought of
as a compass rose superimposed upon the boat's
position, and the small circles represent the
bearings of each shark with the exact times of these
bearings within the circles. The first four polar plots
refer to the four hours that the sharks were
directionally positioned prior to their departure
from the seamount area. It is evident that bearings
of the two sharks (represented by the shaded and
clearcircles) duringthefirsttwo hours were similar;
lookat the circles for 16:27, 16:47, 17:45, and 17: 55.
After 18:05 the sharks separated, one remaining
northwest of the boat, the other remaining
southeast of the seamount for a while before
departing at 19:00. The second shark left the vicinity
of the boat at 19:55. These departures and
subsequent ones have occurred almost always at
sunset. A comparison of the first four polar plots
with the fifth control plot enables one to see that
during the afternoon the compass bearings of the
two sharks were not random but generally together.
These and subsequent results are still inconclusive,
since there is always the possibility that the sharks
are separating in small groups and we have not yet
been lucky enough, in the several paired trackings,
to pick two sharks who moved off together.

Even if the sharks were not to forage socially,
there could be an energetic advantage for the
sharks to remain based centrally among nearby prey
clumps. Such an advantage would occur if the
clumps of prey were to exist in the surrounding
epipelagic and mesopelagic waters. If these clumps
were to be spread out over a large area, and the
sharks were to move over greater distances, this
energetic benefit would be lost. This reasoning has
been used to explain colonial nesting in avian species.

70

430

300'

270 C

240

JQ

P 300'

90 270

120 240

210

I6 27 - I6 55 hrs

120

210

I7 00 -I7 05 ,l7 45 -I7 55 hrs

10

3 )

300

270

240

ieo ift^- 18^

330

300,

270

240

1) Sunset -I8 55 , Civil Twilight- I8 55
-I9 20 , Nautical Twilight I8 55 -I9 48

2) Numbers 1-12 5min. time intervals,
bearings by random numbers table.

210

1800 Control

As the reader can ascertain, our knowledge
of the ethology and behavioral ecology of the
scalloped hammerhead is still too rudimentary to
determine unequivocally the function of its massive
schools. However, most certainly this species
provides us with an ideal behavioral system to ask
this type of question, and should lead to further
insight into shark grouping as well as to a better
understanding of the social behavior and means of
communication of sharks. Perhaps we will find that
sharks are not only supremely adapted to locate and
capture their prey but also possess a varied social
repertoire of behaviors that contributes to their
evolutionary success.

A. Peter Klimley is in the graduate program at the Scripps
Institution of Oceanography, La folia, California, where he
is conducting research on the scalloped hammerhead,
leopard, and blue sharks.

Figure 6. Directional
bearings at 5-minute
intervals of two scalloped
hammerheads tagged on 4
August 1980 at El Bajo at
13:35 (shaded circles) and
15: 10 (clear circles). Time
intervals noted within
circles.

Recommended Reading

Clark, E. 1963. Massive aggregations of large rays and sharks in and

near Sarasota, Florida. Zoologica, 48: 61-64.
Clarke, T. A. 1971 . The ecology of the scalloped hammerhead

shark, Sphyrna lewini, in Hawaii. Pacific Science, 25(2):

133-144.
Gruber, S. H.,and A. A. Myrberg, )r. 1977. Approaches to the study

of the behavior of sharks. American Zoologist, 17: 471-486.
Klimley, A. P., and D. R. Nelson. 1981. Schooling of hammerhead

sharks Sphyrna lewini, in the Gulf of California. Fisheries

Bulletin, 79(2): 356-360.
Klimley, A. P., and S. T. Brown. 1981. Stereo-photographic

technique for the determination of lengths of free-swimming

scalloped hammerheads, Sphyrna lewini, in the Gulf of

California. CIBCASIO Transactions, in press.
Myrberg, A. A., Jr., and S. H. Gruber. 1974. The behavior of the

bonnethead shark, Sphyrna tiburo. Cope/a, 1974(2): 358-374.
Nelson, D. R., and R. H. Johnson. 1980. Behavior of the reef sharks

of Rangiroa, French Polynesia. National Geographic Society

Reports, 12: 479-499.
Parker, F. R., Jr., and C. M. Bailey. 1979. Massive aggregations of

elasmobranchs near Mustang and Padre Islands, Texas. 7"exas

Journal of Science, 31(3): 255-266.
Springer, S. 1967. Social organization of shark populations, pp.

149-174. In Sharks, Skates, and Rays, eds. P. W. Gilbert, R. F.

Mathewson, and D. P. Rail, 624 pp. Baltimore: Johns Hopkins

Press.

71

Perspectives for the Future

by Samuel H. Gruber

J harks attack men and, less frequently, women
- about 100 times each year. Probably many more
incidents go unreported, but even so, shark attack
must be considered a very rare phenomenon. Why,
then, does the search for a truly effective shark
repellent continue? First, there is a special helpless
horror created by the thought of being attacked and
bitten by a huge shark. The fear created by an attack
is often blown out of proportion, and this in turn
can affect the wider population by bringing such
activities as recreational swimming or underwater
salvage to a halt. Second, under certain conditions
like marine or aviation disasters, the probability of
shark attack can increase from vanishingly small to
almost certain. The wartime accounts of attacks on
shipwrecked sailors on the high seas attest to this,
and such accounts can dramatically affect the
morale of an entire fleet. Finally, sharks attack and
destroy very expensive oceanographic instruments
with some regularity. Not only is the equipment
lost, but cruises are cancelled and programs can be
delayed for months or even years. Thus the search
for a repellent continues.

Haphazard Effort

Early investigations were done on a somewhat
haphazard basis. A "shotgun" approach was used in
hopes of stumbling upon some potent chemical
substance which repelled sharks. In parallel work,
various devices were developed to behaviorally
disrupt or physically damage sharks. Attempts to
fence popular bathing areas in Australia and South
Africa were temporarily successful, but were
eventually foiled by corrosion, tides, and shifting
sands. Those two countries still make use of
staggered gill nets, which catch and kill many sharks
just beyond the surf at some bathing beaches. There
have been some successful experiments with
electrified barriers, but these are expensive to
maintain and, like some electrical gadgets on the
market, can be dangerous to divers. The "shark
screen, "a plastic sack that fills with water and hangs
from the surface by a flotation ring, can prevent a
shark below from seeing or smelling the person
inside. For divers, the powerhead, or "bang-stick,"
can kill an attacking shark with an exploding charge
to the head. However, as with the CCh dart, which is
only disabling when fired into the shark's abdomen,

if you miss you may have one angry shark on your
hands. An Australian has patented an underwater
transmitter that mimics the call of the killer whale, a
predator of sharks. Finally, there is a promising,
light-weight chain-mail diving suit that shark teeth
apparently cannot penetrate.

Yet none of these efforts has produced an
entirely satisfactory repellent. The failure of the
U.S. Navy's "Shark Chaser" underscores this fact.
Shark Chaser is the best known, most widely used
shark repellent ever produced. It was developed in
a crash program during World War II in an effort to
protect our servicemen. The work consisted of
exposing captive smooth dogfish, Mustelus canis,
to a number of systemic poisons and other toxic
agents. Scientists scored the effect of each
substance on feeding responses of the dogfish and
found that rotten shark flesh inhibited feeding
better than any of the toxic agents. Chemical
analysis suggested that copper acetate might mimic
the rotten flesh and that a dense, black-water
soluble material nigrosine dye might hide the
swimmer from sharks. Thus thousands of cakes of
those compounds were fabricated and eventually
distributed to GIs. Actually, some of the field tests
were very encouraging. But in the end, Shark

Valerie Taylor being bitten by blue shark while testing
light-weight chain-mail diving suit. (Photo by Jeremiah S.
Sullivan)

72

Chaser dispersed rapidly in the open sea and did
not always chase sharks. In the middle 1970s, the
military dropped it.

Today, the outlook for developing an
effective chemical shark repellent is better. The
Office of Naval Research supported studies on
shark biologyfor15years in hopes of understanding
shark behavior and sensory physiology. These
studies are about to pay off. Development of a
repellent will require the testing of many
substances on live sharks. Techniques previously
developed in Navy-supported basic research are
now available to scientists so that more valid
bioassays can be undertaken.

What, then, characterizes a chemical shark
repellent? First, the substance or stimulus must
interrupt a special, coordinated behavior the
attack. Contrary to popular belief, many or perhaps
most attacks are motivated by factors other than
hunger. The implication is that a stimulus which
merely inhibits feeding may not be adequate in all
cases. Therefore, any definition of repellency must
go beyond interruption of the feeding drive alone.
Since its effect must be instantaneous, a repellent
should work at the level of the sensory receptors.
Systemic poisons or neurotoxins, for example, are
too slow to be useful. So, an adequate repellent
must provide an aversive stimulus field sufficient to
induce a highly motivated shark to turn and leave
the area regardless of the source of motivation.
Finally, for practicality, the repellent should be
quite stable for a long shelf-life, relatively
inexpensive, effective in minute amounts, and
harmless to man.

Modern Repellent Research

In the 1970s, research on shark repellents shifted
from basic shark biology to the search for
biologically effective natural marine products. In
theory, a marine organism may have "invented"
an effective shark repellent during the process of
evolving a protective mechanism against predation.
Many thousands of toxic and noxious fishes and
invertebrates are known, and more remain to be
discovered. However, the most thoroughly studied
and promising of these protected forms is a small
Red Sea fish, the Moses sole, Pardachirus
marmoratus. Research by Dr. Eugenie Clark of the
University of Maryland established that the Moses
sole produces a proteinaceous, slowly-dispersing,
toxic secretion that protects it from shark attack.
The status of this and other research on shark
repellents was summarized in January, 1981 , at a
symposium sponsored by the American Association
for the Advancement of Science (AAAS). Topics
ranged from the structureand function of pardaxin,
the purified active toxin of the Moses sole; to the
behavior of sharks when exposed to pardaxin; to
the types of toxic organisms found in the world's
oceans.

Powerhead for shark defense. (Photo by Jeremiah S.
Sullivan)

Three possible lines of future research
emerged from this meeting. First, a group led by
Israeli Dr. Naftali Primor suggested continued
study of pardaxin so that its physiological mode and
site of action on sharks could be unambiguously
specified. Primor favors the theory that the gill
membranes are the target organs for pardaxin,
which shuts down the "sodium pump" by
interfering with production of the enzyme
adenosine triphosphatase. This in effect
short-circuits the shark's electrochemical gradient
and makes the gill "leaky" to water and ions. Urea
and sodium flow from the shark's plasma through
the gills and into the sea. Other ions enter the gills
from the surrounding seawater. Thus, the shark's
osmoregulatory and salt-balance systems are
disrupted. According to Primor, these ionic fluxes
could be responsible for the observed repellent
effect of pardaxin.

Anothergroupof Israeli scientists, led by Dr.
Elihau Zlotkin, has taken a somewhat different
approach. Zlotkin recognized the surfactant and
detergent-like qualities of pardaxin and, in a series
of experiments, demonstrated that: 1) pardaxin
reduces the surface tension of water by 60 percent
and foams in aqueous solution; 2) the amino acid
sequence of pardaxin's N-terminal is extremely
hydrophobic and positively charged, which would
amplify its interaction with phospholipid (cell)
membranes; and 3) depending on dosage, pardaxin
can completely disrupt synthetic phospholipid
membranes or, in lower concentration, interfere
with membrane physiology such as specific ion
channels or membrane cable properties. Zlotkin
realized that the complicated sequence of 162
amino acids of which pardaxin is composed could
not be synthesized except perhaps by genetic
engineering techniques. Additionally, pardaxin is
an unstablecompound, which can onlybe stored in
a freeze-dried form that is 70 percent less effective
than the fresh secretion. He thus suggested that it
might be worthwhile to investigate industrial

73

surfactants, theorizing that these strong detergents
might act much like pardaxin in repelling sharks.

The third group, represented by Drs. Gerald
Backus and Doug McClure of the University of
Southern California, called for continued testing of
a wide variety of naturally occurring toxic
compounds so that their potentials as shark
repellents could be scored and cataloged.

There is one common element in all three
lines of research: study of the behavior of live
sharks under controlled conditions. This is where I
could perhaps contribute, since I had been studying
shark behavior in the laboratory for many years. At
the January AAAS meeting Zlotkin and I decided to
test his theory (that simple, inexpensive detergents
might repel sharks). Under a small grant from the
Office of Naval Research, Zlotkin traveled to Miami
with eight substances, including perhaps 90 percent
of the world's supply of freeze-dried Moses sole
extract some 27 grams.

Testing Surfactants

The first task was to develop test methods for
screening these eight substances. We settled on
three bioassays. The first was a simple lethality test.
We seined about 200 pupfish, Fundulus
heterocleitus, from a muddy shore near the
Rosenstiel School of Marine and Atmospheric
Science in Miami. The fish were placed individually
in small containers and exposed to various
concentrations of the eight test substances. We
found that one of the surfactants was more lethal by
an order of magnitude than the Moses sole extract.
A second detergent-like surfactant was equally as
lethal as the extract; at 10 parts per million, it killed
pupfish in six hours or less. The other test
substances were mildly toxic or completely benign.
These findings encouraged us to move on to the
shark tests. We used 41 lemon sharks, Negaprion
brevirostris, in the studies. These were all young
sharks up to 4 kilograms in weight and under three
years old. Some of the sharks had been in captivity
for up to two years, but most had been held for no
more than 10 weeks.

The first test was a simple feeding trial in
which food was withheld from 15 sharks for two
days. Then a bait was prepared by attaching a

25-cubic-centi meter syringe to a whole blue runner,
Caranx crysos (Figure 1). The syringe was fitted with
a plastictube which protruded outthe bait's mouth.
It was possible for the experimenter to manipulate
the bait in such a way that the shark grabbed the
blue runner's head in its mouth. At that instant the
contents of the syringe were released into the
mouth of the attacking shark (Figure 2). The
outcome of these trials took one of three forms: 1)
the shark, unaffected by the substance, continued
its attack, tearing off and consuming the bait's
head; 2) the shark was mildly affected but
continued to feed or, more frequently, did not
press the attack; and 3) the shark was obviously and
strongly repelled, and dashed away disoriented.
Sometime later, a shark in this third category would
show signs of distress, including labored breathing
and color changes.

Results of these tests showed that the same
detergentthat killed pupfish in low concentration, a
common compound found in industrial cleaning
agents, was 10 times more effective at repelling
sharks than was the Moses sole extract. A second
surfactant was as effective as the extract, and two
others were mildly repellent. Four of the test
substances did not deter hungry sharks from
feeding. From these tests, we concluded that
Zlotkin was correct: certain industrial surfactants
mimic the action of pardaxin. Additionally, the
repellent effect of the Red Sea sole is probably
universal and not dependent upon the shark having
prior experience with the toxic fish. We reach this
conclusion because the Moses sole is restricted to
the Red Sea yet our lemon and nurse
(Ginglymostoma cirratum) sharks are repelled by
pardaxin. Two other Atlantic species, the spiny
dogfish, Squalus acanthias, and the Atlantic
sharpnose shark, Rhizoprionodon sp., were shown
in other laboratories to be affected by pardaxin.

Because feeding trials depend on the
motivational state of the shark we were limited in
the number of tests that could run on a single day.
For example, after feeding, and especially after
exposure to a toxin, our sharks typically lost interest
in the bait for a couple of days. We therefore
decided to develop a second bioassay which was
more-or-less independent of the shark's
motivation.

Figure 7. Feeding bioassay:
a 20-centimeter-long blue
runner, Caranx crysos, is
prepared as a bait by
attaching a 25-centimeter
syringe to the fish. The
plastic tube extends out
the bait's mouth. (Photo
by author)

74

Figure 2. Feeding bioassay: an 80-centimeter-long lemon
shark, Negaprion brevirostris,attac/cs the bait and grasps
the head in its mouth. Simultaneously the experimenter
releases the test substance into the shark's mouth. (Photo
by E. Zlotkin)

Tonic Immobility Tests

The response we selected is based on a behavior
known as catalepsy or tonic immobility. If a shark
(or other species, from primate to insect) is
disoriented by being held in an inverted position, it
will fall into a relaxed, trance-like state (Figure 3).
This state can last for 30 minutes or more, during
which the shark is quite insensitive to stimulation.
Forexample, it is possibleto perform minorsurgery
undertonic immobility.

We felt that tonic immobility might offer a
rapid and repeatable way to screen large numbers
of activating compounds. A test would consist of
tonically immobilizing a shark, then instilling a
known concentration of a substance intothe shark's
mouth (Figure 4). The test would be scored as
positive if the shark "awoke" by flipping over and
righting itself (FigureS). Because of the control over
dosage, the ability to give repeated trials, and the
unambiguous behavioral end-point, we expected to
produce some precise threshold values for the eight
test substances. Our expectations were verified.
The tonic immobility trials proved to be a rapid and
reliable way to compare surfactants. Again, the
same potent surfactant effective in the first two
assays was found to be four times more effective
than the Moses sole extract at terminating tonic
immobility and 30 to 100 times more effective than
its nearest surfactant competitor. Thus the three
bioassays lethality, feeding, and tonic immobility
- gave essentially the same result.

This work has shown that it is possible to use
live sharks as subjects in behavioral bioassay trials.
This means that it will be possible to screen a large
number of compounds in a relatively short time.
The work also confirmed Zlotkin's hypothesis that
cheap, readily available industrial surfactants will
repel sharks. This opens up a number of

Figure 3. An 85-centimeter lemon shark inverted and under
tonic immobility. A shark will remain essentially immobile
for at least 10 minutes except for breathing movements of
the mouth and gills. (Photo by author)

Figure 4. Tonic immobility bioassay: experimenter releases
a test substance into the immobilized shark's mouth.
(Photo by author)

75

Figure 5. Tonic immobility
bioassay: a shark
"awakens" from tonic
immobility after a test
substance has been
released into its mouth.
(Photo by author)

possibilities for repellent research, since we now
have a theoretical framework to guide our
experiments and some reliable tests to answer our
research questions. Zlotkin and I plan to continue
thiswork withthedual goalsof producing (isolating
or synthesizing) a highly effective chemical
repellent based on industrial surfactants and
elucidating the repellent's physiological mode of
action.

After the laboratory studies are complete,
field testing must be undertaken. This requires a
completely different technology, including
ultrasonic telemetry and activity monitoring
devices. If the field tests are positive, the ultimate
tests involving wild sharks and human subjects must
be performed. Along with these, the problem of
packaging the repellent for rapid deployment
must be solved. Although our research may
someday be applied to the manufacture of a
mass-marketed repellent for bathers, our first
priority is to protect Navy divers and underwater
military hardware.

Thus much work remains before a final
product will become widely available. Still, there is
renewed enthusiasm in the research community
and renewed interest at the funding agencies.
Interaction of these two factors has a way of
producing results. Prospects for the long-term
solution to the shark repellent problem seem more
favorable today than ever before.

Samuel H. Gruber is an Associate Professor in the Division
of Biology and Living Resources at the Rosenstiel School of
Marine and Atmospheric Science, University of Miami,
Miami, Florida.

Selected Reading

Baldridge, D., and ). Williams. 1969. Shark attack: feeding or

fighting. Military Med. 34: 130-133.
Clark, E., and S. Chao. 1973. A toxic secretion from the Red Sea

flatfish Pardachirus marmoratus (Lacepede). Bull. Sea. Fish.

Res. Sta. (Haifa) 60: 53-56.

Gruber, S. 1980. Keeping sharks in captivity. /. Aquaricult. 1 : 6-14.
Gruber, S., and A. Myrberg. 1977. Approaches to the study of the

behavior of sharks. Amer. Zoo/. 17: 471-486.
Primor, N., and E. Zlotkin. 1975. On the ichthyotoxic and

haemolytic action of the skin secretion of the flatfish

Pardachirus marmoratus (Soleidae). Toxicon 13: 183-187.
Tuve, R. L. 1947. Technology of the U.S. Navy "Shark Chaser."

Naval Instil. Proc. 73: 522-527.

76

Photo by Elgin Ciampi,
National Audubon Society

Advice to Swimmers, Divers, and Victims

Always swim with a companion, and do not wander away from a coherent group of other bathers and
thereby isolate yourself as a prime target for attack.

Do not swim in water known to be frequented by dangerous sharks. Leave the water if sharks have been
recently sighted or thought to be in the area.

Although not conclusively proven, human blood is highly suspect as an attractant and excitant for sharks.
Keep out of the water if possessed of open wounds or sores. Women should avoid swimming in the sea
during menstrual periods.

It is not always convenient, but very murky or turbid water of limited underwater visibility should be
avoided if possible. In any event, a particularly watchful eye should be maintained for shadows and
movements in the water. If there is any doubt, get out at once.

Refrain from swimming far from shore where encountering a shark becomes more probable.

Avoid swimming alongside channels or drop-offs to deeper water which provide ready access for a shark.

Leave the water if fish are noticed in unusual numbers or behaving in an erratic manner.

Take no comfort in the sighting of porpoises, for this does not at all mean sharks are not about.

Avoid uneven tanning of the skin prior to bathing in the sea, for sharks apparently respond to such
discontinuities of shading.

Use discretion in terms of putting human waste into the water.

Avoid swimming with an animal such as a dog or a horse, etc.

Take time to look around carefully before jumping or diving into the sea from a boat.

Particularly at low tide, take notice of a nearby offshore sandbar or reef that might have entrapped a shark.

Avoid swimming at dusk or at night when many species of sharks are known to be searching for food.

It just might be a good idea to select other than extremely bright colors for swimwear.

Never, in any form or fashion, molest a shark no matter how small it is or how harmless it might appear.

Keep a wary eye out towards the open sea for anything suggestive of an approaching shark.

77

Advice to Divers

Never dive alone. Not only might the very presence of your diving buddy deter the shark, but together
you have a far better chance of becoming aware of a nearby shark in time to take effective
countermeasures. Furthermore, if something did happen to you, at least there would be assistance close at
hand.

Do not in any way provoke even a small shark not by spearing, riding, hanging on to its tail, or anything
else that might seem like a good idea at the time. Even a very small shark can inflict serious, possibly fatal,
injury to a man.

Do not keep captured fish, dead or alive, about your person or tethered to you on a stringer or similar
device. Remove all speared or otherwise wounded fish from the water immediately.

Do not spearfish in the same waters for such extended periods of time that curious sharks may be drawn
to the area by either your prolonged quick movements or an accumulation of body juices from numbers of
wounded fish.

Leave the water as soon as possible after sighting a shark of reasonable size, even if it appears to be
minding its own business. Submerged divers, as opposed to surface swimmers, have a better chance of
seeing a shark making investigatory passes prior to being committed to attack. Use smooth swimming
strokes, making no undue com motion, in reach ing the safety of a boat or the shore. To the greatest extent
possible, remain submerged where chances are greater for watching the shark and countering its charge if
attack occurs. Do not count on the shark either circling or passing close at hand without contact before it
makes a direct run.

Use discretion in the choice of wetsuit colors in terms of conditions and sea life prevalent in the waters of
intended operations. Do not take a chance on being mistaken for the area's natural prey of choice.

Carry a shark billy or plan to use the butt of a speargun for this purpose if necessary. Such devices have
been shown to be very effective in holding an aggressive shark at bay until its ardor cools.

Take full advantage of your submerged position and limits of visibility to be aware always of nearby
movements and presences. Shark attack case histories indicate that such vigilance has played a major role
in lowering injuries and mortality rates among diver-victims.

Do not maneuver a shark into a trapped position between yourself and any obstacle such as the beach,
reef, sandbar, or possibly even a boat.

As with swimmers, do not wander away from an established group of other divers and possibly give
thereby an appearance of fair game. Avoid diving at dusk and at night.

Advice to Victims

Try to remain calm and take full advantage of weapons available to you.

Use any object at hand to fend off the shark while at the same time not intentionally provoking it further.

Keep fully in mind the limitations of such devices as powerheads, gas-guns, spearguns, etc., and do not
expect them to accomplish the impossible. Such weapons, if used improperly, may serve only to further
agitate the shark.

Use available spears and knives first to fend off the shark and attempt to wound the fish only as a last
resort. Sharks often seem to react with increased vigor to efforts at sticking it with pointed objects.

Discretion should be used in making aggressive movements towards a shark. One that had not yet
committed itself to attack might be "turned on" by such movements if interpreted by it as a threat. On the
other hand, quick movements towards a shark close at hand might produce a desirable startle response.

Once contact has been made or is imminent, fight the shark as best you can. Hit it with your bare hands
only as a last resort. Probing the shark's eyes especially and perhaps also its gills has often turned the tide.
Startle responses which at least buy valuable time have been produced occasionally by such actions as
shouting underwater or blowing bubbles. Do anything that comes to mind, for the seconds or minutes of
time during which the shark might withdraw as a result could be sufficient to effect your rescue.

Most shark attacks produce wounds that are readily survivable. Bleeding should be controlled as quickly
as possible even before the victim has been brought ashore. Treatment by a physician is indicated even
where wounds are relatively minor.

From Shark Attack
by H. David Baldridge

78

A mako, Isurus oxyrinchus,o^San Diego, California. (Photo by Jeremiah S. Sullivan)

INDEX

Volume 24 (1981)

Number 1, Spring, The Oceans as Waste Space?: Edward D. Goldberg The Oceans As Waste Space: The
Argument Kenneths. Kamlet7he Oceans As Waste Space: The Rebuttal James P. Walsh U.S. Policy
on Marine Pollution: Changes Ahead Judith M. Capuzzo Predicting Pollution Effects in the Marine
Environment Charles B. Officer and John H. Ryther Swordfish and Mercury: a Case History --frank
Cordle The FDA Responds: Mercury Levels in Fish Alan J. Mearns Ecological Effects of Ocean Sewage
Outfalls: Observations and Lessons Ralph F. Vaccaro, Judith M. Capuzzo, and Nancy H. Marcus The
Oceans and U.S. Sewage Sludge Disposal Strategy G. T. Needier and W. L. Templeton Radioactive
Waste: The Need to Calculate an Oceanic Capacity.

Number 2, Summer, general issue: John D. Milliman The U.S. Oceanographic Experience in China -
David R. Watters Linking Oceanography to Prehistoric Archaeology - -Thomas M. Leschine The
Panamanian Sea-level Canal Richard G. B. Brown Seabirds at Sea a picture essay Some Midwater
Fishes John W. H. Dacey How Aquatic Plants Ventilate John M. HuntThe Origin of Petroleum -
Judith Spillerand Alison R\eser Regulating Oil and Gas Activities in the Flower Garden Banks.

Number 3, Fall, Oceanography from Space: Richard Goody Satellites for Oceanography the Promises
and the Realities Clifford C. Ewing From Antiquity On ward W. Stanley Wilson Oceanography from
Satellites? Carl Wunsch The Promise of Satellite Altimetry James J. O'Brien The Future for
Satellite-derived Surface Winds Wayne E. Esaias Remote Sensing in Biological Oceanography W. F.
Weeks Sea Ice: The Potential of Remote Sensing Francis P. Bretherton Climate, the Oceans, and
Remote Sensing D. R. Montgomery Commercial Applications of Satellite Oceanography Robert H .
Stewart Satellite Oceanography: the Instruments Glossary.

Number 4, Winter, Sharks: Perry W. Gilbert Introduction Leonard J. V. Compagno/.egend Versus
Reality: The Jaws Image and Shark Diversity Joel L. Cohen Vision in Sharks Sanford A. Moss Shark
Feeding Mechanisms Perry W. Gilbert Patterns of Shark Reproduction a photo essay Telemetry
and Blue Sharks Paul R. Ryan Electroreception in Blue Sharks Donald R. Nelson Aggression in
Sharks: Is the Gray Reef Shark Different? Samuel H. Gruber Lemon Sharks: Supply-Side Economists
oftheSea A. Peter Klimley Grouping Behavior of the Scalloped Hammerhead Samuel H. Gruber
Shark Repellents: Perspectives for the Future Advice to Swimmers, Divers, and Victims INDEX

79

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Oceanography from Space, Vol. 24:3, Fall 1981 Satellites already provide useful
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