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AMER. ZOOL., 30:559-594 (1990)
Coral Reef Communities as Prime Resources for Analysis of
Evolution and Physiology of Behavior1
EDWARD S. HODGSON
Department of Biology, Tufts University,
Medford, Massachusetts 02155
AND
C. LAVETT SMITH
Department of Ichthyology, American Museum of Natural History,
Central Park West at 79th Street, New York, New York 10024
SYNOPSIS. The abundance and great diversity of life on coral reef ecosystems provides
many good opportunities for studying the evolution and specializations of neurophysiological systems and behavior. Crucial stages in the evolution of nervous systems appear to
have occurred in the Precambrian, as revealed in Ediacaran fossils and their closest living
relatives. By the Ordovician, when Chazy "reefs" exemplify some of the earliest complex
animal communities fixed in one place, more elaborate neurological mechanisms for
orientation, predation, and escape reactions are indicated. With the evolution offish, the
behavioral richness of reef communities became further enhanced. Elaborate specializations of feeding, defensive, aggressive, signaling, schooling, and reproductive behaviors
are common in fish. Several examples of behavioral studies on reef organisms are used
to illustrate research methodologies and the types of conclusions which may be drawn.
These examples include: (1) analysis of symbiotic behavior of an invertebrate and a vertebrate—sea anemone and clownfish; (2) signaling behavior of a fish—the sailfish blenny;
and (3) a combined electrophysiological and behavioral analysis of orientation and feeding/attack behavior—sharks. An almost endless number of possibilities for similar analysis
makes the organisms of coral reefs especially useful, and challenging, for teaching purposes
as well as further research.
activity patterns, special types of behavThe life within a coral reef ecosystem has ioral interactions between species, or we
a very special significance for perspectives wish to analyze the complex sensory cues
on neurobiology and behavior. In the num- and responses that facilitate maximal space
bers and variety of species living there, and and resource utilization, the reef inhabitalso in the great antiquity of these ecosys- ants provide us with unsurpassed study
tems as stable, integrated complex com- materials and opportunities. And for anymunities, coral reefs surpass all other eco- one with the opportunity to do field obsersystems. They are virtual museums of the vations around a living coral reef (or even
history and adaptive modifications of ner- some of the fossil ones!), there is another
vous systems, and of the behaviors that have payoff, perhaps the most valuable of all.
provided crucial selective advantages The very richness of the fauna, plus the
throughout half a billion years of evolu- myriad activities and functions its members
display, virtually assure that one's insights
tion.
If we seek an example of a particular and perspectives on biology will be
specialization of neurons, and it exists any- expanded and refreshed through a yield of
where, some example can probably be unexpected and novel observations. Perfound among members of the coral reef haps because coral reefs are confined to
fauna. If we seek illustrations of particular shallow seas, an environment that is truly
alien to human experience, there is little
about them that we can take for granted,
1
From the Symposium on Science as a Way of Know- and therefore we avoid the pitfalls of
ing—Neurobiology and Behavior organized by Edward
unwitting assumptions that slip by without
S. Hodgson and presented at the Centennial Meeting adequate challenge or testing. As well as
of the American Society of Zoologists, 27-30 Decem- being some of the most attractive biotopes
ber 1989, at Boston, Massachusetts.
INTRODUCTION
559
560
E. S. HODGSON AND C. L. SMITH
in the world, coral reefs are currently com- itats, and some authors have suggested that
ing into their own as living laboratories these ideal conditions have been a contribwhere phenomena can be studied conve- uting factor in the development of the high
niently and economically. The develop- diversity we observe in coral reef comment of safe, easily mastered self-con- munities. One must not, however, lose sight
tained diving gear in the 1940s made these of the fact that coral reefs arejust as unsuitpreviously inaccessible environments avail- able (harsh) environments for penguins or
able to any person in good health, with a polar bears, not to mention humans. Morefew hours training and careful attention to over, some of the most accessible and
familiar parts of coral reefs (e.g., the reef
safety precautions.
For teaching, the attributes of coral reef flat) are areas of very high physiological
communities provide many helpful advan- stresses (Ross and Hodgson, 1981).
tages. It is hardly surprising that an
Two characteristics of coral reef enviincreasing number of colleges and univer- ronments complicate the lives of all resisities are finding ways to encourage, and dent organisms. First of all the reefs are
provide opportunities for their biology stu- confined to clear waters, which limits their
dents to obtain some direct experience of distribution along continental coasts. This
tropical marine biology, including coral means the most coral reefs are found
reef ecosystems. Marine laboratories and around tropical islands rather than around
field stations, special short semesters mainlands (Fig. 1). It further means that
devoted to field courses and research, all reef biotopes are widely separated from
provide venue and formats for these types each other, and this is reflected in life cycles
of educational experiences. The growing that include pelagic stages that can pasnumber of scientifically oriented films and sively drift from one reef area to another.
videotapes about various aspects of coral A second characteristic of reefs is that their
reef biology are also valuable resources at best growth is in strongly lighted areas,
all levels of instruction. Some of the special near the surface of the water, where their
educational aspects of these studies, rec- symbiotic algae can carry out photosynognized during a consortium course in thesis. In such environments, they are subwhich the present authors participated, ject to continuous wave action and occahave been described by Hodgson (1972). sional devastating storms. Thus, coral reef
organisms have the multiple problems of
reaching their environments, carrying on
COMPARISON WITH MORE FAMILIAR
adequate metabolism, and coping with the
ENVIRONMENTS
Students, like everyone who begins to effects of constant (and at times violent)
think about the phenomena that take place water movement.
on coral reefs, typically have difficulty comSpecial biological features of coral reef
prehending the special features which communities center around the enormous
impose selective pressures upon the reef numbers of species living in such limited
fauna. The physical and chemical aspects space. Comparisons between familiar
of the environment are probably easier to "human environments" and the reef are
understand, although not entirely obvious. sometimes useful in helping students
It is easy to regard the coral reef environ- appreciate this aspect.
ments of warm, clear water as benign habOne analogy that has proven helpful
FIG. 1. Heron Island, a coral cay which is a center for research, teaching, and tourist activities in the Capricorn
group of islands, Great Barrier Reef, Australia. A. Aerial view of the island and nearby reef, showing areas
of patch reefs (p), reef crest (c), and back reef (b). A channel, cleared for boats, is at upper right. Research
and teaching facilities (r), close to tourist accommodations (t) are on the end of the island nearest the channel.
B. Shallow-water patch reef area, with island edge at upper right. See text for discussion of richly diverse
fauna inhabiting such patch reefs.
BEHAVIOR OF CORAL REEF ORGANISMS
561
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E. S. HODGSON AND C. L. SMITH
ysis would have to be used also, to include
minute planktonic forms as well as the benthic species.
As an illustration of this herculean job,
an attempted census of animals on a small
area of reef in Mindoro, Philippines,
yielded the following: 111 species of
Alcyonaria (soft corals), 70 species of chaetopod worms, 200 to 250 species of crustaceans (including 25 to 30 species of hermit crabs), and numerous species of other
invertebrate animal groups. As for the reefbuilding "hard" corals of that area, Ross
and Hodgson (1981) found 90 different
species of corals living along a 27-ft transect of the upper dropoff of the reef. The
total number of Philippine hermatypic corals has been estimated as about 500 species!
Each colony of each species is probably
home for some other animals as well. For
example, Grassle (cited by Sale, 1988)
extracted 103 species and 1,441 individual
polychaete worms from a single "head" of
the coral Pocillopora damicornis at Heron
Island on the Great Barrier Reef of Australia! It can hardly be surprising that complete inventories of coral reef fauna are only
rough estimates.
Each animal species has to obtain food,
defend itself against enemies, reproduce,
etc., in order to survive as a successful component species in the reef ecosystem. Each
species has different neural "equipment,"
and the variety of sensory cues used for
survival on even a small patch reef far outstrips the signals and cues in any human
street intersection. Indeed, the survival of
such large numbers of animals in such a
small space requires intensive exploitation
of strategies like space-sharing, mutualism,
alternation of day-night cycles of activities,
By contrast, on a comparable area of finely-tuned visual and chemical cues for
shallow-water reef in a faunally rich area precise orientation to micro-habitats,
of the Indo-Pacific (Fig. 1), there may be appropriate food materials, breeding parthundreds of species living, moving about, and ners, etc. At the same time, each species
interacting. Inventories of even small areas must have equally finely-tuned mechaof reefs are generally incomplete, for they nisms for detecting predators, and for
require the combined contributions of doz- operating avoidance and escape reactions.
ens of experts on the different groups of Is it any wonder that the designs and operanimals represented, the use of blasting to ations of nervous systems, producing an
obtain the reef samples, and probably some almost incredible array of behavioral pattechniques for immobilizing or exposing terns, attain what may be their greatest
cryptic (hidden) fauna. Microscopic anal- variety among coral reef animals?
emphasizes the almost incredible number
and variety of sensory signals and stereotyped response mechanisms used by reef
animals, and draws attention to the reasons
why this complexity seems an inevitable
requirement for the survival of so many
species in a limited area. The comparison
might be made between a small, but familiar, part of a modern human environment—a street intersection—and a comparable area of a reef, such as a "patch
r e e f in shallow water.
Both the street intersection and the patch
reef may have about the same surface area.
Beyond the similarity in their physical
dimensions, however, there are enormous
differences in the fauna utilizing each place,
and in the requirements for effective use
of the space. A street intersection is created and used by one species, Homo sapiens.
In order to have pedestrians, bicyclists, and
variously "motorized" humans moving
through a street intersection in orderly
ways, without collisions and serious (even
fatal) damage, it is necessary to employ
some sensory cues to which Homo sapiens is
sensitive, and to which humans can be
trained to respond (one hopes!) in reliable
stereotyped and safe ways. Students may
be surprised if they actually count the signals at a moderately busy street intersection. At one suburban street crossing in the
Boston area—a crossing not associated with
any special hazards or intensive use—58
different signals (signs, and lights) were
counted; this impressive assortment of
visual cues is all the more remarkable
because it regulated the local mobility of
a single species, which utilized the area only
during part of the 24-hr day, leaving it
mostly vacant for 25-35% of the time!
BEHAVIOR OF CORAL REEF ORGANISMS
In the introductory courses, toward
which this series is aimed, it will be necessary to select only a few of the more
remarkable and instructive examples, and
the remainder of this short analysis is organized to facilitate such an approach, with
discussion of outstanding cases. Most people think first of the fish in any aquatic
environment, and, to be sure, many of the
most striking examples can be found among
those animals, as explained below. But
nearly every class of invertebrate provides
some particular neural specializations and
behavioral adaptions, as Bullock and Horridge (1965) have pointed out in their major
reference work. It is also important, we
believe, that all students should have some
appreciation of the evolutionary background for such special mechanisms and
behavioral adaptations; here, the paleontological record has much to teach us, and
hence we include some highlights from the
evolutionary history of reef fauna, extending back, in certain cases, to the Precambrian when skeleton-producing coelenterates had not even appeared! Although less
well-known than the rich and often bizarre
fauna of the Cambrian, as revealed particularly well in the Burgess Shales, the fauna
of the Ordovician reef communities evidently continued the "explosion" of new
forms of life, and provides insights concerning some of the earliest complex animal communities that became fixed in place
on our planet. For this reason, some examples from the Chazy reefs of the upper
Champlain Valley of New York and Vermont are also discussed.
INSIGHTS FROM PALEONTOLOGY
Evidence from the oldest known assemblage
of metazoans: The Ediacaran fauna
Long before coral reefs existed, it appears
that certain crucial steps must have been
taken in the evolution of nervous systems
and behavioral capabilities. The earliest
"window" through which we can search
for evidence of those evolutionary steps is
currently to be found in the Ediacaran
fauna, the oldest diverse assemblage of
multi-celled animals—dated approximately 600 to 550 million years ago, near
563
the end of the Precambrian Era. The most
thoroughly documented locality where fossils of Ediacaran animals are found is in the
Flinders Ranges, some 600 km north of
Adelaide, South Australia. About 40 kinds
of animal remains and a dozen different
trace fossils characterize the deposits there.
The name "Ediacara" is an Aboriginal
place name (loosely translated as "vein-like
spring of water") and the name has now
been applied to fossils of similar ages and
structures known from more than 20 localities throughout the world.
The original discovery of casts and
impressions of "jellyfishes" in South Australia was by R. C. Sprigg in 1946, with
extensive subsequent collections made by
Sir Douglas Mawson and his students, and
more recently by Martin Glaessner (1962,
1984) and Richard Jenkins (1984), all of
the University of Adelaide, as well as by
many other paleontologists. Particularly
helpful general reviews of the "Ediacaran
Period" include those of Cloud and Glaessner (1982), Glaessner (1984), Jenkins
(1981) and Scrutton (1979).
The majority of Australian Ediacaran
organisms resembled jellyfish and frondlike octocorals (sea pens, soft corals), and
they lived (or were stranded) in shallow
intertidal flats or strandlines. Silt and clay
settling in "limited pools or lagoons
between sand ridges . . . [buried] . . . the
remains of animals and traces of their activities" (Glaessner, 1984). The biological
forms from the earliest part of Ediacaran
time are limited to microfossils and algae
(Jenkins, 1984), with the Anthozoa and
medusoid animals appearing later. Softbodied worm-like burrowing, or presumed
detritus-feeding animals are also represented among the Ediacaran fossils.
Since most modern jellyfishes, "sea pens"
and detritus-feeding worms do not actively
pursue, or engage in obvious combat with
any living prey, it is understandable that
Ediacaran animals were once viewed as
rather passive, existing in a non-competitive world without the elements of aggression and predation that later became common—the "garden of Ediacara" notion,
rather like an idyllic and tranquil evolutionary "Garden of Eden." This view was
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E. S. HODGSON AND C. L. SMITH
FIG. 2. Reconstruction of Kimberella quadrata (Glaessner and Wade), redrawn after Jenkins (1984). This
Precambrian cubozoan suggests that highly specialized sensory and locomotor structures must have had
a long evolutionary history even before the time of
the oldest known assemblages of multi-cellular animals, the Ediacaran fauna of Australia and elsewhere.
Pedalia (p), tentacles (t) and gonads (g) resemble those
of some living cubomedusae found around coral reef
areas. See text for details.
shattered following the discovery and evaluation of a most unexpected and remarkable member of the Ediacaran fauna, originally reported in 1966 by Glaessner and
Wade. They described the fossil imprint of
a box-like jellyfish, Kimberella quadrata,
which further study has confirmed as an
early cubomedusa (Fig. 2).
The most remarkable implications of
Kimberella stem from the fact that living
cubomedusae are generally regarded as
among the most highly specialized of all
jellyfish, well endowed with sense organs
(statolith and complex eye structures with
image-forming capabilities), able to move
rapidly and execute aggressive attacks,
capable of causing death (even to such large
animals as humans) within a few minutes—
making them "probably the most dangerous venomous marine animal known"
(Halstead, 1967) and, arguably at least, the
most feared of all marine animals. What is
such a creature doing in the supposedly
struggle-free "garden" of a shallow tropical marine environment at the "dawn of
animal life" (to use Glaessner's phrase)?
Obviously, there must have been a long
period of evolution and adaptive radiation
of some "jellyfish-like" organisms prior to
the Ediacaran Period. From a present-day
perspective, even if Kimberella is viewed as
an early ancestral form of modern cubomedusae, it must have had an extensive
evolutionary history itself, concerning
which we currently do not have substantial
evidence.
But is the four-sided medusa Kimberella
really ancestral to living cubomedusae? Or,
should it be regarded as a bizarre one-time
experiment in evolutionary design that did
not pan out and has no genetic-evolutionary connection to any organisms that came
after the Precambrian? This question is
certainly an important one because evolutionary pathways are opportunistic, frequently dead-ended, and rarely follow any
sort of straight-line "progressions." Moreover, the human tendency to "see" only
what is expected can lead anyone (scientists
included) to mistake superficial resemblances for evolutionary relationships and
to interpret chance irregularities for links
in lines of evolutionary descent, "evolutionary trees," etc.
Since the early 1980s, the paleontologist
Adolf Seilacher has advocated an entirely
new interpretation of the Ediacaran fauna
(Seilacher, 1989). He proposes, as Steven
Gould has summarized, ". . . the similarities of Ediacaran and modern animals are
misleading and superficial, and that the
Ediacaran forms could not work as their
supposed living counterparts" Gould
(1984). If this interesting, but unproven,
hypothesis withstands careful analysis, and
appears applicable to the Ediacaran fauna
as a whole, then Kimberella, along with all
the other species in that shallow water community, would be merely another example
of a dead-end evolutionary experiment. If
not, then Kimberella may be ancestral to
one of the world's fiercest families of predators, with all the neurological and behavioral equipment and capabilities necessary
for success in that way of life.
What is the evidence? In body form, Kimberella resembles the living cubomedusa
Chiropsalmus (Fig. 2), which is greatly feared
around the coral reefs of the Indo-Pacific
region today. The tentacles, in both these
fossil and living species, are attached to
large stalks (pedalia). Zones of "puckered"
imprints around the umbrella appear to
represent an extensive circular muscle system in Kimberella, as would be essential for
BEHAVIOR OF CORAL REEF ORGANISMS
rapid swimming. A longitudinal groove and
fold in the fossil remains ". . . becomes
deeper and more accentuated at about the
position where the rhopalia are located in
living Carybdeidae" (Jenkins, 1984). Consequently, even though no ocelli have been
recognized in the fossil imprints—hardly
surprising, in view of the small size of these
sense organs and the processes of fossilization—there are structural modifications at
those points where thickened expansions
of mesoglea surround the rhopalia (which
bear the ocelli) in living cubomedusae.
These, and other, similarities of the fossil
and living forms have been discussed and
illustrated by Jenkins (1984), and certainly
the weight of present evidence supports his
conclusion that "Ki?nberella appears to be
a direct ancestor of the chirodropid sea
wasps."
Based upon that entirely plausible interpretation, it seems reasonable to examine
the neurological and behavioral capabilities of living cubomedusae, and to bear
them in mind when interpreting related
fossil species. Statoliths (and a gravity sense)
and ocelli (providing visual capabilities,
including image formation) are found in
Chironex and Chiropsalmus, the modern
cubomedusae that are best known because
of their extreme danger to humans. Behavior of cubomedusae in their normal environments, especially around tropical reefs,
is known from a few isolated observations,
rather than any systematic long-term studies—in part, no doubt, because of the hazards of carrying out such observations.
There is some evidence of cycles of activity
in these animals. The inactive Chiropsalmus, with its body inclined at an angle above
the pendant tentacles, is reported by local
Philippine fishermen, who are constantly
alert to these animals, to be exhibiting typical afternoon "resting" behavior; they
report that as the light declines in the evening, the animals become active and, moving horizontally with tentacles forward,
could overtake fish or a human swimmer.
These reports parallel observations upon
Caribbean cubomedusae (Carybdea) which
are most active in surface waters after dark,
are attracted to light, and swim rapidly with
565
tentacles directed forward toward their
prey (Kaplan, 1982; Hodgson, 1983). The
active swimming posture of the predatory
cubomedusae, incidentally, clarifies the
long-standing puzzle of what the "eyes" of
the cubomedusae see, when they are positioned to "look into the subumbreller cavity" (Hyman, 1940); when swimming with
tentacles spread forward, the visual receptors may be directed ahead, toward anything in front of the animal.
The behavior of other jellyfish that are
typically found around modern coral reefs
may help explain another puzzle concerning the Ediacaran fauna. Glaessner (1962)
noted the "peculiar" fact that the Ediacaran jellyfish casts indicated that the animals were generally preserved with their
convex "dorsal" sides downward, i.e.,
"upsidedown" from the way that dead jellyfish are generally found stranded on
present-day beaches. Yet some tropical
Scyphozoa (e.g., Cassiopeia) spend most of
their time "upsidedown," and others (e.g.,
Mastigea) have been observed to adopt this
inverted posture during inactive periods of
midday hours on reefs, even though most
of their time is spent in the normal upright
position, drifting or swimming (Hodgson,
1983). The upsidedown posture undoubtedly facilitates photosynthesis by algal symbionts in the subumbrellar tissues. Recent
arguments supporting the hypothesis that
Ediacaran animals contained algal symbionts (Rowland, 1988) suggest this might
influence the posture of ancient "upsidedown" jellyfish, although direct evidence
of algal symbionts in the Precambrian has
not been obtained.
The fact that "upsidedown" jellyfish can
leave distinctive imprints upon mud or sand
substrates was observed in the 19th century when Henry Guppy, a physician
aboard a British surveying ship in the Western Pacific, described the behavior of Casseiopeia in shallow waters of the Solomon
Islands (Guppy, 1887). It was observed at
that time that not only the outline of the
inverted medusa could be traced on the
substrate, but even the composition of the
substrate underlying the medusa was
changed from that of the general sur-
566
E. S. HODGSON AND C. L. SMITH
roundings—an observation that might well
repay further analysis with living specimens in other areas and also with fossil
imprints still undisturbed at their original
sites.
Regarding the Precambrian frond- or
leaf-like fossils, which in general outline
resemble octocorals of the order Pennatulacea ("sea pens"), any true relationship
to living animals is still unclear. In early
studies, Glaessner simply listed them as
"Problematical Coelenterata" (Glaessner,
1984); Seilacher (1984, 1989) has argued
that their flattened, matted form does not
match any modern anatomical plan, so
these animals represent an entirely separate, and dead-end experiment in multicellular life.
Whether these animals actually were colonies of polyps, and whether their
"extreme and pervasive" deformation
during fossilization and embedding
(Glaessner, 1984) may account for the flattened form which Seilacher has emphasized, remains to be judged. Further studies need to be made on the many fossils of
this type that are not yet fully documented.
One group of them (the Charniidae)
appears more loosely allied to the pennatulaceans, but most investigators have
found no convincing grounds for excluding them from the sessile colonial Cnidaria
(Anderson and Conway Morris, 1982;
Glaessner, 1984; Jenkins, 1984). Consequently, it seems appropriate to ask what
is known about the neurobiology of living
pennatulaceans, while remembering that
proposed links between fossil Ediacaran
forms and living "sea pens" are not settled
matters.
Much of the basic structure of living pennatulids is similar to that of sea anemones
and coral polyps. Early anatomical studies
indicated that multiple neural conduction
systems might exist in colonial pennatulids,
but virtually nothing was known of their
physiology prior to the early studies of Pantin (1935),]. C. C. Nicol in the mid-1950s,
and the electrophysiological studies by
James Case and his co-workers in the 1970s.
Using the luminescence of Renilla as a
convenient measure of effector activity,
Anderson and Case (1975) made electrical
recordings from all parts of the colony,
using suction electrodes. The electrical
pulses recorded appear to be muscle action
potentials or potentials from epithelial cells,
but evidently they closely reflect activity in
a nerve net, such as found in other Cnidaria. There are several different conducting systems in the animal. One conduction system is within the individual
polyps, mediating withdrawal responses.
There are also two conducting systems
which operate to control the colonial, or
supraorganismal, unit. Since luminescence
increases after the second or third of a series
of nerve net pulses, and increases in intensity with subsequent pulses, it is apparent
that there is a capability for facilitation.
Effector function is based upon what might
be considered the simplest integrative
mechanism—peripheral frequency-dependent facilitation (Satterlie and Case,
1979).
The development of these systems and
the behaviors they mediate have been
explored, with fascinating results, by Satterlie and Case (1979). Extending the early
descriptions of the development of Renilla
by E. B. Wilson (1883), these investigators
have described the behavior from the
swimming larval stage (planula) through the
gradual emergence of adult effector systems after the planula attaches. The settling and attachment of the planulae
involves discrimination between various
substrates, with most rapid attachment and
development of completed adult conduction and effector systems if the larva settles
on sand. At least one conduction system is
present in the swimming larva, prior to settlement; this system mediates muscle activity of the entire larva. Neuro-effector
mechanisms mature later, as do facilitation
capabilities of the system.
The evolutionary origin of the brain also
has been placed within a Precambrian time
frame. There is general agreement that
the earliest concentrations of neurons
which might be called "brains" occurred
among worms, probably among some
groups of flatworms (platyhelminthes).
Anatomical studies suggest that these early
brain structures arose as concentrations of
neurons around the statocyst, the balance
567
BEHAVIOR OF CORAL REEF ORGANISMS
organ of many coelenterates and flatworms
(Hodgson, 1977). The Acoela, an order of
small free-living marine flatworms, show
all stages of transition from a diffuse subepidermal neural plexus (as found in radially symmetrical coelenterates) to a concentration of nerve stands which run
longitudinally from an anterior brain (Fig.
3).
Glaessner (1984) noted that about 25%
of the Ediacaran fossils are worm-like animals. Several species can be distinguished.
One of the most extensively studied of
them, Dickensonia, was once considered to
be a true flatworm because of its flattened
body form. However, further study suggests that it more closely resembles the
annelid worms, somewhat similar to (but
certainly not ancestral to) polychaete annelids. Glaessner (1984) has provided a
detailed summary of discussions concerning Dickensonia's evolutionary affinities. It
appears that these animals were already
"beyond" the simpler flatworm stage, and
possibly had a sensory tentacle on the anterior dorsal surface, and crawled or swam
to find sediment or detritus for food.
Another Ediacaran "worm," Spriggina,
shows significant cephalization (an enlarged
and sclerotized head) and parapodia, which
are comparable to the appendages used for
crawling by living polychaete annelids of
the family Aphroditidae. No elaborate
sense organs, or burrows, have been identified with Spriggina, and it is believed to
have fed on detritus in the soft mud in
which it was preserved (Glaessner, 1984).
Although its precise evolutionary affinities
are debatable, it seems reasonable to
assume that the operation of its parapodia,
during crawling or turning, would have
required more than the simplest epidermal
nervous system of the Acoela (e.g., Fig. 3A),
and involved at least a relatively simple
brain structure, perhaps comparable to the
polyclad annelids (e.g., Fig. 3B). As is so
often the case with evolutionary studies,
the lack of evidence about soft parts which
do not survive fossilization is unfortunate.
For this reason, as well as the multiplicity
of "design experiments" typical of certain
periods of rapid evolutionary speciation and
radiation, it is impossible to pin-point a spe-
B
FIG. 3. Stages in evolution of the brain among flatworms. A. Tetraposthia (Acoela), with epidermal nervous system (ens) and statocyst (st); B. Gnesioceros
(Polycladida), with bilobed brain surrounding statocyst; C. Mesosloma (Rhabdocoela), with increased
cephalization and loss of nerve net. (Diagrams modified after Hyman, 1951, and Hodgson, 1977.)
cific fossil species as being "the" transition
point, marking the first appearance of a
major change in body design. However,
some approximation of the time when the
change occurred can be reasonable. If the
known samples of Precambrian "worms"
all seem "advanced" beyond the postulated beginning stages of neural aggregations into primordial brains, it should be
remembered that even the Ediacaran fauna
are not the earliest metazoans. Or, as
Glaessner (1984) reminds us, "A considerable interval of time was required for
metazoan 'prehistory.'"
Hyman (1951) has summarized an interesting assortment of laboratory experiments on flatworms, showing that even
simple cerebral ganglia are critical for initiation of locomotion, as well as achieving
orientation toward chemical stimuli in
many species. Comparable studies on annelids have been reviewed by Dales (1967),
and by Russell-Hunter (1979), among others. Unfortunately, field observations are
sparse, so that the full range of behavioral
capabilities mediated by the simplest brains
and nervous systems of metazoans are
probably underestimated. For example, the
polyclad worm Pseudoceros is a conspicuous
inhabitant of many coral reefs, and because
of its size and great beauty generally attracts
attention. It has been observed to crawl,
swim freely, climb branches of staghorn
568
E. S. HODGSON AND C. L. SMITH
corals, cling to corals with its posterior end
while swinging the anterior end to-and-fro
in a current (sampling water movement or
chemical stimuli?), and sometimes to burrow in loose sand, effectively concealing
itself (Hodgson, 1983)—an impressive,
although doubtless incomplete, behavioral
repertoire for an animal with relatively
simple neural structures! There are virtually limitless opportunities, both challenging and scientifically useful, for systematic behavioral studies in the field; these
can become important components of
learning and research experiences for students in the burgeoning field courses in
tropical marine biology offered at the college and university level today.
In addition, although it would be beyond
the scope of this paper to review them, the
range of functions carried out by "nerve
nets" of single cnidarian polyps (anemones, corals, etc.) should not be overlooked.
The late Donald Ross, whose abundantly
productive research centered on that topic,
noted that nerve nets of anemones modulated spontaneous behavior patterns, controlled complicated responses to stimuli,
swimming behaviors, and habituation or
inhibitory responses, among others. In
summarizing his observations, he wrote:
" . . . we are being driven toward the idea
that the actinians possess the equivalent of
a central nervous system in a dispersed
form" (Ross, 1973). V. Hodgson (1981)
reached a similar conclusion from behavioral studies on the complex interactions
between anemones and their associated
symbionts. (See Case Study No. 2, below.)
other arthropods, many animals that cannot be grouped with any living forms (and
generally are considered new phyla), and
the first known member of our own phylum (Chordata). Recent general reviews of
Cambrian evolution have been written by
Eldredge (1987) and by Gould (1989), the
latter concentrating especially upon the
Burgess shales, which are a particularly rich
source of tantalizing Cambrian fossils.
Attempts to envision community structures or behavioral interactions among
Cambrian animals are often handicapped
by circumstances of their fossilization. The
animals represented in the best assortment
of Cambrian fossils (in the Burgess shale),
for example, apparently owe their preservation to a mudslide which obliterated
any tracks as it moved the creatures some
distance from their normal habitat. However, exoskeletons of the trilobites provide
direct evidence of the highly-developed
sense organs of those animals, and permit
reasonable inferences about the central
nervous ganglia needed to control and
integrate the muscles which moved
appendages of the thoracic and posterior
segments. There were also antennae at the
front end, as well as cerci which protruded
from the tail ends of some species. The
typical arrangement of trilobite sense
organs and segmental branched appendages will be familiar to those who have
studied some modern crustaceans—a tribute to the durability of a basically successful design, even though its earliest possessors (trilobites) became extinct after a
glowing track record of some 300 million
years!
The Cambrian evolutionary explosion
The compound eyes, which were already
present in the earliest trilobites, are one of
the greatest marvels in the history of sense
organs. A few trilobite species lacked them
entirely, but others had enormous eyes,
taking up most of the surface of the head.
In some species, the lateral eyes merged
into a "panoramic dome" or have a turretlike structure—adaptations presumably
giving a visual field covering the trilobite's
entire surroundings.
In the Ordovician trilobite species, and
persisting until the trilobite extinction at
the end of Permian time, there was a
Soft-bodied animals, preserved as Precambrian fossils, do not look like the imperfect prototypes of Cambrian hard-shelled
fossils. Nor do the earliest "reefs" resemble the hard-coral ecosystems of today; they
were essentially mounds built upon the sea
floor during the Cambrian Period (and
subsequently) by archeocyathids, relatives
of limestone-producing algae or sponges,
now extinct. Trilobites were the dominant
form of life in Cambrian seas, but there
was a virtual "explosion" of multicellular
life forms during that period, including
BEHAVIOR OF CORAL REEF ORGANISMS
"peculiar form of evolutionary optimization of optical function" in their eyes, analyzed by the physicist Levi-Setti (1975) and
illustrated in his beautiful photographic
atlas of trilobites. Clarkson and Levi-Setti
found that the lenses of these later types
of trilobite eyes were doublet structures
constructed so that they corrected the otherwise large spherical aberration of simple
lenses—". . . perhaps the most sophisticated dioptric elements ever produced by
nature" (Levi-Setti, 1975). Thus, the trilobites, several hundred million years ago,
"solved" a problem of overcoming optical
aberration, the same problem that was
solved again during the 17th century, when
the philosopher Descartes and the father
of wave optics, Christian Huygens, were
challenged by it. In the "corrected" trilobite eyes, as structured by evolutionary
selection, the upper lens unit is formed of
oriented calcite, while the lower component is formed of chitin; this arrangement
works perfectly for an eye that must function in water, and is a somewhat more complex solution than the glass lenses Huygens
and Descartes designed for use in air. LeviSetti noted that the corrected lenses would
have increased the efficiency of light transmission to the visual receptor sites of the
eye. This might have conferred significant
selective advantage if the trilobites were
nocturnal or lived in turbid waters. Such
a remarkable sensory apparatus, appearing
when it did, certainly provides a powerful
corrective for any contemporary human
tendencies to think of ancient life forms as
imperfect primordia or evolutionary
experiments that were only marginally successful. Any animal types that lived through
those several hundred million years must
have been intensely honed, through mutations and selection, to function superbly in
the environments of their own times.
Ordovician coral communities
Another great evolutionary burst, and
one of particular importance for any consideration of coral reef ecosystems,
occurred during the Ordovician period,
approximately 435-450 million years ago
(McKerrow et ah, 1985). As Eldredge summarized it, ". . . in the Lower Middle
569
Ordovician the fossil record (certainly in
North America and in Eurasia as well) all
of a sudden gets markedly better"
(Eldredge, 1987). This was the period when
all the main animal groups, not already
represented in the Cambrian, made their
appearance in the evolutionary record. In
particular, the corals became prominent
and contributed to the structure of the oldest known complex animal communities
fixed in one place. These are the oldest
communities for which present-day
researchers have been able to study the
integrated, ecological roles of many species.
Such interactions give important clues to
the behaviors and nervous systems that
must have been involved.
It was long believed that the very earliest
known coral was Lamottia, a tabulate coral
named after Vermont's Isle LaMotte where
it was found {Lamottia has been considered
by some workers to be equivalent to the
genus Lichenaria). Recently, fragments of
two species of horn (rugose) coral were
described from Cambrian deposits in Australia. If this report is correct, Lamottia (or
Lichenaria) would lose one of its claims to
fame, and there are also some specialists
who suggest that tabulate corals should be
classified among the sponges (see Eldredge,
1987, for discussion). However these issues
are eventually resolved, it remains valid to
consider the Ordovician as the first time
the corals really did, in Eldredge's phrase,
"get going in force," and certainly the
advantages of mineralized skeletons were
not extensively exploited until the Ordovician (Jell, 1984).
There is also some controversy about the
long-standing claim that the Chazy limestones, and similar levels of the Ordovician, represent the oldest functionally integrated communities of organisms. Again,
this is a matter of scale and proportion,
rather than the sudden appearance of a
total novelty in evolution. The Burgess
shale fauna undoubtedly included some
predators, and ecological specializations
within some Cambrian species do suggest
some integrated community organization
(Gould, 1989); there are similar suggestions for the still earlier Ediacaran fauna,
considering the presumed predatory role
570
E. S. HODGSON AND C. L. SMITH
of Kimberella. However, it is still true that
in the sequence of increasing community
complexity, from the lowest Chazyan fossils
to the later " r e e f communities, there is
an excellent "window" upon one of the
earliest examples of evolving integrated
fixed communities.
There are almost as many definitions and
usages of the terms reef and reef environment
as there are scientists interested in them
(Boucot and Carney, 1981). Here too, the
main perspectives will be more important
to most students than ongoing debates
about specialized semantics. Whatever terminology eventually sticks, the coral-based
communities of Chazy and other Ordovician deposits provided great new opportunities for evolutionary radiation, and the
beginnings of the complex reef communities which intrigue us today.
All the levels of Chazy limestones can be
seen in a few islands of northern Lake
Champlain, and adjacent shores of New
York State and Vermont. (The name Chazy
is taken from a town in New York where
these limestones were first studied.) The
lowest and earliest levels of Chazy formations (the "Day Point" level) contain ripple
marks indicating a shallow water environment. There are also a variety of worm
tubes and trails. The earliest "mounds" or
"reefs" in the Chazy deposits were built by
bryozoans, chiefly of one species, or at most
two. Lamottia appeared in these older levels,
and the fossil remains of this historical coral
resemble a stack of thin dinner plates; the
circular coral colonies are quite localized
in their occurrence, but conspicuous where
they do occur. These may have been the
oldest-known attached carnivores with a
skeleton, but the small size of the polyps
indicates that they could have fed only upon
very minute organisms in the sea water,
and the sparse assemblages of organisms at
that level (and time) probably cannot be
considered as indicative of a functionally
integrated community.
At higher levels in the Chazy limestones,
all that is changed. In the so-called "Crown
Point" deposits (again named for an early
study locality), it is possible to see where a
great variety of animals once lived on, or
around, limestone mounds built by organ-
isms in shallow warm seas. (Improbable as
it may seem, what is now Vermont was
located near the earth's equator during
Ordovician times—another of the startling insights provided by studies on plate
tectonics!) In fact, there is a distinct resemblance between the scattered fossil reefs
that now rise from some Vermont pasturelands (Fig. 4) and the shallow patch
reefs that are familiar parts of coral ecosystems today (Fig. 1).
By drilling and extracting samples of the
Crown Point reefs, as well as studying the
fossils visible at their surfaces, Max Pitcher
(1971) found that the reef structure was
mainly produced by stromatoporoids,
bryozoans, corals and calcareous algae. At
least 4 species of corals were identified on
these reefs, along with brachiopods,
ostracods, and trilobites. Most conspicuous
among the assorted fossils are the molluscs.
One gastropod, a marine snail (Maclurites),
is so abundant and distinctive that it is virtually an indicator species for Crown Point
deposits. Nautiloid molluscs, early relatives
of squids, also left their shells in abundance. Elsewhere in North America Ordovician fossil deposits, it is possible to recognize the imprints of tentacles from
nautiloids that were feeding or resting, and
there is evidence of their predatory activities and other behaviors (Fig. 5). Even the
"worms" seem to have lived more complicated lives in the upper Chazyan levels, for
their trails arise from holes bored in the
limestone, and appear highly oriented,
rather than meandering. There is evidence
of distinct changes in organic composition
through time, competition for space on the
limestone substrate, associations of different species, and other characteristics that
typify reef ecosystems even today.
Without attempting to review the enormously detailed and abundant findings on
these Ordovician reefs, one conclusion is
inescapable: they were highly integrated
communities when alive. Gastropods
grazed on algae, and were themselves prey
to nautiloids, which may have also attacked
trilobites (as represented in Fig. 5). Filterfeeding sponges and corals fed upon minute
plankton, and their skeletons provided
shelter for other species (Copper, 1988;
BEHAVIOR OF CORAL REEF ORGANISMS
Cowen, 1988; Clarkson, 1986; Laporte,
1983; Oxley and Kay, 1959; Pitcher, 1971).
The evidence of predation suggests welldeveloped sense organs—chemoreceptors,
as well as eyes—(trilobites continued
numerous)—and the body form and jetpropulsion of the nautiloids certainly set
the stage for the evolution of giant motor
axons, if it had not yet occurred. Unfortunately, the fossils do not reveal the nerve
or muscle structures of these animals. All
in all, one gets the impression that these
Ordovician reefs were ecosystems that are
understandable in terms of modern coral
reef ecology and physiology. Museum
reconstructions {e.g., Fig. 5) obviously
involve a number of guesses and some
questionable conclusions (such as using
modern polychaete annelids to represent
the "worms" that made the trails), but they
do help us bridge the 450 million year gap
back to the earliest days of reefs.
Since the Ordovician—More recent
history of reefs
Despite their seemingly tranquil tropical
environment, coral reefs actually have had
a turbulent history since their Ordovician
beginnings. Episodes of mass extinction,
some of them worldwide, have greatly
affected them—sea level changes, climatic
and other environmental changes have
taken their tolls at various times. However,
the reefs have survived, albeit with great
fluctuations (Newell, 1972), justifying their
distinction as our planet's oldest and most
durable ecosystem.
Types of corals and other inhabitants of
the reef ecosystem changed dramatically
throughout this long history. The Devonian period (starting roughly 400 million
years ago) was the last time when stromatoporoids and tabulate corals were major
inhabitants of coral reefs. But it was also
the period in which many sharks and bony
fishes evolved and radiated into new environments in the sea—hence the familiar
designation of that "age of fishes."
Today, fishes of enormous variety are
perhaps the most prominent fauna of reefs,
apart from the reef-building corals themselves. As noted above, it is not unusual to
find several hundred species of teleost fishes
571
living within a particular reef area, and
some elasmobranch fishes (sharks and their
relatives) are often at the top of the food
chain in reef communities. For many people, getting acquainted with coral reefs is
tantamount to "watching fishes"—which,
incidentally, is the title of a recent, helpful
and readable book for general readers
about the behavior of coral reef organisms
(Wilson and Wilson, 1985). The prominence and importance of fishes, and their
behaviors, on coral reefs entitles them to
a special section of this essay, before we go
on to several illustrative examples of
research on neurobiology and behavior of
reef organisms.
CORAL REEF FISHES
Introduction and comparative features
In comparison to those of more familiar
environments, coral reef fishes, at least,
display a great range of morphological
variability. It is instructive to compare the
fishes of freshwater streams with those of
coral reefs. Freshwater streams in the
northern hemisphere are dominated by
Ostariophysan fishes, whereas coral reefs
are dominated by a diversity of perciform
fishes. Most stream fishes have moderately
compressed to slightly depressed bodies
without prolonged fin rays or conspicuous
spines on the head. Their colors, except
for special breeding plumage tend to be
olive or silvery, sometimes with tints of yellow or white, and their mouth and tooth
structures are variations of a few morphological themes. In contrast, the coral reef
fishes have body shapes ranging from slender cylinders to highly compressed disks
and the fins often have extended, trailing
rays. Some groups of coral reef fishes have
conspicuous cranial armature and their
colors range from totally cryptic to downright gaudy. Mouths vary in size and position and teeth range from slender canines
to chisel-shaped incisors to molariform
crushers and complex pharyngeal mills.
These specializations cry out for "explanations" but the specific questions that lead
to understanding have to develop in concert with specific and detailed descriptive
and experimental data gathering. Such data
572
E. S. HODGSON AND C. L. SMITH
BEHAVIOR OF CORAL REEF ORGANISMS
were not readily obtainable before the
development of diving gear and the study
of the behavioral ecology of coral reef fishes
did not come into its own until the development of modern self-contained underwater breathing apparatus (SCUBA).
Before the invention of SCUBA, researchers were limited to observations through a
glass-bottom bucket and experiments in
small aquaria in the laboratory. Surface
observation is always difficult and really
effective observations can only be made in
a few special habitats peripheral to the most
interesting reefs. Laboratory observations
suffer from the artificiality of the environment.
Field study techniques
In the 1930s William Beebe began using
a diving helmet for collecting coral reef
fishes and soon W. H. Longley began a
series of studies in the Dry Tortugas that
marks the beginning of modern coral reef
studies. Today students of reef fish behavior have a wide range of equipment that
makes underwater observation and data
collecting as easy as terrestrial data gathering, and in some respects easier, for the
diver can move in three dimensions with
ease and most coral reef fishes can be
approached quite closely.
The basic working tools for the modern
student of any type of coral reef biology
are the face mask, snorkel and swim fins.
With these simple items one has mobility
and the capacity to see beneath the surface
without raising one's head to breathe. For
deeper environments submersibles and
remotely operated vehicles are available
and, for prolonged studies, saturation div-
573
ing makes it possible to continue observations for days at a time. Effective underwater television and video recorders
provide the means for recording data for
later review and analysis. One thing that
we still do not have is the ability to record
behavioral data in the dark and our understanding of nocturnal activities suffers from
this.
Understanding behavior patterns
In looking at behavior, or its underlying
neurological mechanisms, it is essential to
bear in mind the essential end results of
the behavior. These results, if favorable to
the animal, confer selective advantages, and
account for the retention of the underlying
neurological mechanisms in evolution.
All animals have to do four basic things:
on a continuing day-to-day basis they must
1) find and remain in a suitable physicalchemical environment; 2) obtain oxygen
and food, and get rid of metabolic waste
products; 3) avoid predators, and at least
match their competitors; 4) finally, they
must reproduce sometime in their life cycle,
often as their last act.
In this section of the paper we will examine some examples of the behavioral and
structural correlates of each of these activities, with special attention to the role of
behavior in meeting the special requirements of life on coral reefs. We will also
consider some of the difficulties and pitfalls
of interpreting observed behavior patterns.
The physical and chemical environment
Some of the special features of the coral
reef environment {e.g., their restriction to
FIG. 4. Ordovician coral communities—among the oldest known complex animal communities fixed in one
place. Fossil-rich mounds (Crown Point reefs) rise from pastureland on Isle LaMotte, Vermont. Pointer in
foreground indicates drillhole from which a core sample was removed to study the internal reef structure
and fauna. Camera on tripod has been elevated to height of 5 ft, for scale; also note researcher on distant
reef, near center. Compare these fossil reef formations with modern patch reefs (Fig. IB).
FIG. 5. Museum reconstruction of an Ordovician reef community. In foreground, a large cephalopod (Endoceras) attacks a trilobite (Isotelus). Behind the trilobite is a rounded colony of a tabulate coral (Tetradium), with
a starfish (Promopalaeaster) on its surface. Just to the right of the Telradium is the polyp of an early horn coral
(Streptelasma), with another cephalopod (Streptoceras). Also represented: small clams (pelecypods), crinoids,
and (in right foreground) an annelid reconstructed similar to a living marine polychaete. (Exhibit at Museum
of Comparative Zoology, Harvard University.)
574
E. S. HODGSON AND C. L. SMITH
clear, well-lighted shallow waters) have
already been mentioned. Another conspicuous feature of active coral reefs is the
abundance of shelter. The growth forms
of corals and hermatypic algae produce
many small crevices and overhangs and
their combined growth and eventual death
and collapse form caves and rubble piles
that provide excellent habitat for myriads
of small, mobile organisms. Reef systems
include peripheral habitats such as sand
flats and beaches, grass flats, rubble zones
behind the reef crest, and mangrove shore
lines, all of which provide habitats that are
utilized by reef associated organisms. These
make possible highly diverse communities
of organisms so that there are large numbers of potential predators, prey, and competitors, both vertebrate and invertebrate.
These characteristics are not, of course,
unique to coral reefs but they are common
to all coral reef environments and
undoubtedly have been critical factors in
the evolution of coral reef organisms and
their behaviors.
The problem of dispersal across environments that are unacceptable to the
adults is met by having pelagic life history
stages which are adapted for survival in the
open sea. Longdistance transport is passive
and depends on favorable currents since it
is unlikely that these fragile stages could
swim very far, and even if they could, would
have no way of consciously locating a destination, nor could they know that such a
destination existed. There are, however,
behavioral traits that contribute to the
effectiveness of this transport. One is the
ability to seek particular light levels and
this appears to keep them at depths where
they are apt to encounter favorable currents. Once they arrive near suitable new
environments their behavior changes and
they seek benthic habitats as they transform into their juvenile morphology. The
slippery dick, a member of the family
Labridae (wrasses) burrows into sand bottom for a few days while it transforms from
a transparent planktonic larva to a pigmented juvenile with a full complement of
scales (Victor, 1983, 1986).
Our knowledge of the early life histories
of fishes has been limited by the difficulty
of maintaining larval fishes in the laboratory. Recently it was discovered that the
otoliths, calcareous structures in the ear,
grow by concentric deposition of layers of
calcium carbonate that correspond to daily
growth increments and reflect major life
history events (Brothers, 1981; Brothers
and McFarland, 1981). The otoliths of most
reef fishes display clear growth increments
during the pelagic phase, then a blurred
zone that represents the transitional period,
after which the daily rings become regular
again. Once this pattern has been verified,
it is possible to determine the length of the
larval period from examination of the otoliths. And also to determine the precise
time of spawning of species for which the
spawning has not been observed.
For sessile organisms, which are denied
the option of seeking a suitable environment, the only control over their location
comes at the time of settlement. Once they
become attached they either survive, or, if
conditions are not favorable to them, perish. Mobile organisms, on the other hand
can and must constantly sample their environment and avoid unacceptable conditions. This is so much a constant activity
that it is difficult for human observers to
be alert to this aspect of their behavior,
and failure to consider the environmental
comfort of the subject undoubtedly hampers laboratory studies of behavior. The
selection of a suitable habitat by early life
history stages is currently receiving a great
deal of attention because of its importance
to maintaining populations of commercially useful species. If the settlement process is strictly passive then managers must
concentrate their efforts on assuring that
there are enough reproducing adults to
provide the numbers of eggs required for
maintenance of the population. If, however, the larval stages actively seek acceptable conditions, there is the possibility that
steps can be taken to selectively attract larvae of the target species.
Microhabitat selection begins as soon as
the fish have assumed their definitive form,
i.e., after metamorphosis is completed.
Some fishes have been shown to do this in
a series of stages and this may be a general
pattern with the fish changing their micro-
BEHAVIOR OF CORAL REEF ORGANISMS
habitats as they increase in size (McFarland,
1985). Hole dwellers, in particular, change
their residences as they grow, and grunts
(Haemulon sp.) move from grass beds to
hard bottom and from mixed to monospecific schools as they get older. In general,
the larger fish are found in deeper water.
Many coral reef fishes have very specific
microhabitats; others may be equally specialized but in less obvious ways. For the
beginning student it is perhaps easier to
observe the most specialized habitat selection first. Inquiline and commensal species
are among the most specialized and are
easily seen even in waters of snorkeling
depth. Outstanding examples are the
pearlfish, Carpus bermudensis, which lives in
sea cucumbers (holothurians), the conchfish, Astrapogon stellatus, which lives in the
mantle cavity of the queen conch, and
numerous gobies and blennies that dwell
in sponges and branching coral. Less specialized, but still recognizable as selecting
specific microhabitats, are fishes that live
in particular kinds of holes (blennies, cardinalfishes) or at specific depths (several
small sea basses).
575
of three groups: nocturnal prey, diurnal
prey, and crepuscular predators? How
much of the activity cycle is determined
environmentally and how much is innate?
How dependent is the cycle on the prey
rather than on the active species themselves?
Behavior and community structure
The factors that have led to the development and maintenance of high diversity
in coral reef fish communities continue to
be the subjects of intense thought and considered debate. True understanding of this
subject will come only from creative analysis of facts which are still being gathered.
It seems clear that high diversity is the result
of a large number of species that are able
to utilize common resources in slightly different ways coming together and integrating their life styles.
Adaptations consist of morphological
components that enable an organism to do
certain things in a particular way, accompanied by behavioral patterns that take
advantage of the special abilities conferred
by morphology. Morphology is stable;
changes occur slowly in response to long
Activity cycles
term selective pressure through many genOne of the most exciting behavioral phe- erations. Heredity behavioral norms also
nomena on the reef is the day-night undergo slow changes at rates similar to
changeover. Many reef species have well- rates of morphological change but many
defined diurnal activity periods and the aspects of behavior are volatile and, within
hours when the diurnal and nocturnal limits, can change from minute to minute
species change places is dramatic (Collette in response to immediate environmental
and Talbot, 1972; Domm and Domm, conditions. The plasticity of behavior pat1973; Smith and Tyler, 1972). In itself the terns governs niche breadth. As a hypoexistence of these separate patterns sug- thetical example, consider a fish that is
gests that shelter space is a resource that morphologically a generalized carnivore
is in short supply, at least at times. Change- with the ability to feed on a large variety
over is regarded as a mechanism for species of prey. In spite of this ability, the species
packing, i.e., it permits more species to use will probably feed on the most easily availthe existing resources without directly able prey and may develop a strong prefinterfering with each other. This simplistic erence for a particular prey species that is
concept, however, requires more research readily available to it. If that prey then
and analysis before it can be accepted as becomes scarce the fish's continued well
proven. For example, what resources, other being will be contingent on its ability to
than shelter sites, are being shared in this utilize less preferred prey. Thus, flexibility
way? How would the interference work if in its behavior pattern will determine the
the resources are adequate for all of the breadth of its feeding niche, and similar
species? Would timing of use of food sources arguments can be made for other aspects
really make a difference? Is it possible that of its ecology (niche dimensions).
changeover is an example of coevolution
If any of the species had a narrow niche
576
E. S. HODGSON AND C. L. SMITH
(which implies adaptations to a narrow
range of conditions) the arrival of a second
species with similar requirements would
result in a conflict which could end with
the elimination of the species least able to
compete (the Competitive Exclusion principle). Presumably this would occur whenever both species had a narrow niche on
any one niche dimension. In contrast,
species with broad niches can compete simply by utilizing alternate segments of their
niche in the presence of a superior competitor.
Coral reefs and associated environments
are ideal laboratories for the study of such
important and intriguing problems.
and one gets the impression that each
author views the problem in his own way
and provides a summary that reflects his
unique viewpoint. We find that the following classification of structural adaptations
is a workable beginning as long as the categories are not regarded as absolutely rigid:
Herbivores.—Fishes that feed primarily
on plant materials have triturating organs
to crush the cell walls of the plants they
ingest. Some have pharyngeal mills consisting of clattered teeth on a modified gill
arch and others have muscular gizzard-like
modifications of the esophagus or stomach.
Fishes that feed on filamentous algae often
have brush-like jaw teeth. Those that feed
on larger algae sometimes have saw-edged
Feeding
cutting teeth.
Parrotfishes feed on macrophytes and
Fishes show a wide variety of structures
that can be regarded as feeding adapta- also on algae that penetrate the skeletons
tions. Although relatively few fishes are of dead coral and other limestone surfaces,
herbivorous, reef faunas have dispropor- as well as the symbiotic algae in the tissues
tionately high numbers of herbivores, of live coral. They have heavy beaks with
especially of the families Blenniidae, Poma- which they scrape the calcareous surfaces
of the reef itself.
centridae, Acanthuridae, and Scaridae.
Carnivores.—Carnivores exhibit a wide
The act of feeding can be viewed as consisting of several phases. First the food must range of specializations correlated with
be located and identified as such. Then it particular kinds of prey. At the same time
must be captured and swallowed before the nearly all carnivores feed opportunistically
digestive process can begin. Clearly, this on whatever prey is most easily taken, even
requires a high degree of behavioral coor- if it is not the type for which they are mordination between the senses, the analysis phologically most specialized.
of the observations, and the motor skills
Plnnktivores.—While numerous reef
necessary to harvest the food, be it a sessile fishes feed on plankton over the reef, they
plant or a fast-moving fish.
tend to crop individual food items and there
The study of feeding in fishes is complex are no good examples of filter feeders
and difficult. Apart from the complicated among reef fishes. Like the grazing herphysiology of nutrition (one has only to bivores, they feed throughout most of the
consider the diet of humans to appreciate daylight hours. Most plankton croppers
how difficult it is to reach meaningful con- have villiform jaw teeth and bodies that are
clusions about food), there are questions adapted for maneuverability.
about the availability of food items, seaPickers.—In this category we include
sonal and diurnal cycles, and the effects of species that simply grab food as they
competitors for the same food items.
encounter it. Wrasses are typical examples.
Food studies are generally of two types— Pickers seem to be generalists, without easexamination of food habits considering the ily identifiable specializations for feeding,
actual quality and quantity of food con- although many species have special strucsumed as determined from examination of tures for processing particular types of prey.
stomach contents (a classic example is Ran- For example, those that eat molluscs often
dall, 1967), and feeding studies which deal have crushing, molariform jaw or pharynwith the behavioral aspects of food utili- geal teeth; piscivores tend to have long caniniform teeth with which to hold their
zation.
prey.
There seems not to be any generally
agreed upon classification of feeding habits
Capturing and swallowing prey is a com-
BEHAVIOR OF CORAL REEF ORGANISMS
plicated matter and involved several bones
and a complex array of muscles, all of which
have to function at the proper time. We
can recognize two general types of food
capture—graspers and suction feeders.
Those that grasp their prey usually have
teeth that are specialized either to hold
their free-swimming prey or to harvest sessile organisms.
Suction feeders feed on free swimming
organisms and inhale their prey by suddenly expanding their orobranchial cavity
and sucking in a volume of water with the
prey in it. Suction feeders often have large
mouths and wide heads, but some have
elongated facial regions and feed by a precise pipetting action. They usually have
rather unspecialized villiform jaw teeth in
bands.
Each of these structural adaptations must
be accompanied by precise behavioral patterns that enable the animals to use them
effectively. In addition, there are general
strategies that characterize particular feeding adaptations.
Herd feeding.—Herbivores that feed on
macroscopic algae frequently feed as
groups that move over the feeding areas.
Possibly this provides an advantage in that
many sets of sense organs are combined.
Since the algae are often abundant, the
advantage of more efficient searches overrides the disadvantage of competition.
577
highly specialized for grazing on sand
dwelling invertebrates. It has unique mandibular barbels with which it stirs and sifts
through sand areas. Its long face and posterior eyes enable it to push deep into the
sand. It never chases prey that escapes by
swimming upward, although such prey are
abundant and fed upon by other species,
such as wrasses, following the goatfish.
A second specialized feeder is the garden
eel. Garden eels live in colonies in sand
areas where there is a steady current. They
extend from their burrows and feed by
cropping particles that drift by. Unlike most
eels they have large eyes and feed by sight.
Garden eels are fishes that have assumed
what is essentially a sessile way of life.
It is a working hypothesis that feeding
habits are mechanisms for avoiding competition, hence one of the major factors in
maintaining high diversity in the fauna, if
not in an individual community. The goatfish and the garden eel are easily recognized as specialists, but it is very likely that
other species are equally restricted by their
behavior even though they are morphologically generalized.
Defensive behavior
Predation is a constant threat in any system and is probably the chief source of
mortality of coral reef fishes, although
recent epidemics of bacterial infections in
Feeding territoriality. —Many damselfishes sea urchins (and possibly some corals)
vigorously guard their feeding territories. throughout the Caribbean raise the posIn so doing they provide conditions that sibility that diseases play a more important
role than heretofore realized. Defense
favor the growth of particular foods.
Ambushfeeding.—Camouflaged or crypti- mechanisms include flight, weaponry
cally colored species often feed by waiting (armor, spines, venoms, and toxins),
for their prey to come within range where schooling, mimicry, camouflage, shelter
they can be consumed by suction. Anten- seeking, and activity cycles. All of these are
nariids actually attract their prey within contingent upon appropriate behavior patrange with their specialized dorsal fin lure. terns of both the prey and the predator.
Stalkers.—Midwater and near surface
First, there is simple flight. Fast swimmers
feeders frequently stalk their prey by hov- are constantly alert and flee at the first
ering and moving slowly until they are close threat of danger. Two extreme examples
enough to grab the prey with a quick rush. are the razorfishes (Hemipteronotus) which
Most species using this type of behavior dive into loose sand when threatened, and
have grasping or slashing teeth.
some clingfishes (Gobiesocidae) which
Within these general categories of struc- attach to rocks above the mean water level
ture and behavior there are numerous so they are actually out of the water
examples of highly specialized feeding between waves and, hence, invisible to
modes. Two examples will serve to dem- predators in the water.
onstrate the possibilities. The goat fish is
Fishes of the tetraodontiformes (plecto-
578
E. S. HODGSON AND C. L. SMITH
gnathi) provide some of the best examples
of weapon bearers. The trunkfishes and boxfishes are encased in a bony armor of modified scales. It is interesting that the slime
of some of these contains a virulent toxin
that will kill other fishes under some conditions. Pufferfishes, also plectognaths, are
able to inflate their bodies with air or water,
and this is generally supposed to discourage predators.
Venomous spines are part of the defensive
arsenal of numerous reef fishes, notably
the spinefoots and the scorpaenoid fishes,
including the most venomous fish in the
world, Synanceia, the infamous stonefish.
Many puffers also have poisonousfleshand
this is an area where speculation has outstripped observation and speculations are
all too often accepted as facts. Poisonous
fishes are found on reefs the world over
and are a serious impediment to human
use of tropical fishes as food. The difficulty
in assessing the benefits of poisonous flesh
is that the individual gains nothing since
the effects of the poison are not manifested
until after the death of its possessor. Thus,
the interpretation of poisonous flesh as a
benefit is based on the ability of the predator to learn to avoid toxic prey species.
Clearly, many assumptions about this phenomenon remain to be tested.
Mimicry is another aspect of defense that
depends on behavioral, as well as structural
specialization. Cases of mimicry have been
well documented by Randall and Randall
(1960), as well as by Tyler (1966).
Schooling is a conspicuous behavior of such
diverse fish groups as herrings and tunas.
(Herrings are rather primitive fishes while
scombroids are highly evolved.) Although
monospecific aggregations are common on
reefs, true schooling, as defined by highly
polarized movements, is actually limited to
a few groups that are more common in
habitats other than coral reefs and, hence,
probably did not evolve in association with
coral reefs. In general, schooling is not a
coral reef phenomenon.
Camouflage, as exemplified by the scorpion fishes and flatfishes, is common on the
reefs but it is difficult to interpret because
we have only the window of human vision
through which to study it. It is entirely
possible that species we perceive as camouflaged are actually quite conspicuous to
their predators or mates.
Acoustic signaling is common among reef
fishes (Winn et al., 1964) and visual analogs
are not unexpected. The sailfin blenny is
a superb experimental animal that lends
itself ideally to in situ field experiments (see
below).
Reproduction
Traditionally coral reef fish communities
were regarded as being limited resources,
with competition for food and space the
major restraints on population size. Recent
studies have provided evidence that many
reef fish species are more likely to be limited by the number of larval recruits that
are available to maintain the population.
Successful spawning, successful transport,
and avoidance of predation before settlement all determine the numbers of recruits
that survive to confront the demands of
day-to-day competition.
Reproduction represents an apparent
conflict with the requirements of defense
in that the organisms must attract mates,
but in so doing they risk attracting predators. Reproduction can be considered as
consisting of several stages; 1) gamete production, 2) locating of spawning sites, 3)
attracting mates and courtship leading to
release of gametes and fertilization, and 4)
parental care of early life stages.
In tropical environments seasonal phenomena are less obvious than in temperate
environments, and some fishes have multiple or protracted spawning periods. Others show definite reproductive periodicity
correlated with annual cycles that are present, albeit subtle.
Spawning activities are easy to observe
in reef environments. An outstanding
example is the blue-head wrasse which
spawns throughout the year and during the
middle of the day when the sun is highest.
Other species spawn in the crepuscular
hours, most often shortly after sunset
(Colin, 1982).
Most coral reef fishes have pelagic eggs
but there are some outstanding exceptions.
Damselfishes lay demersal eggs and the
male guards the clutch. Certain blennies
BEHAVIOR OF CORAL REEF ORGANISMS
179
FIG. 6. Signaling behavior of the sailfish blenny, Emblemaria pandionis. A. The dark-colored male has emerged
from his nest cavity and is rapidly raising and lowering his dorsal and anal fins. B. Lateral aggressive display.
This male has emerged from his nest cavity and has assumed a pattern of dark markings on a pale background.
He has also erected his dorsal fins and turned his flank to the threat, in this case his own reflection in the
lens of the camera. Photographs by Chip Clark, Smithsonian Institution.
lay eggs in cavities that are then guarded
by the male. Jawfishes and cardinalfishes
are oral incubators and certain ophidioids
are live bearers.
Most reef fishes show some movement
associated with spawning. Often this is to
particular edges of the reef or offshore near
deep water. The effect of this is to facilitate
finding mates and also to release the eggs
in areas where they are subject to passing
currents, thus enhancing the chances for
transport to distant areas. It also enhances
the chances for the eggs and larvae to be
lost at sea so the arguments about the benefits of spawning in particular locations are
not especially productive.
Courtship takes many forms, but usually
is ritualized and, for species that lay pelagic
eggs, often ends with an upward rush that
concludes with the release of the gametes
one to several meters above the bottom.
This disperses the gametes in the water in
column and thus avoids their settling prematurely and also keeps them away from
some predators that do not venture far
from shelter. It has also been suggested
that the change in water pressure during
the rush aids in the release of the eggs.
EXAMPLES OF CONTEMPORARY
RESEARCH ANALYSIS
In order that students may appreciate
some of the actual procedures, underlying
rationales, and types of conclusions that
may be drawn from observations of the
behavior or neurophysiology of coral reef
organisms, three case studies are presented
below. The first concerns a behavioral
study, conducted in the field—a study
which is presently ongoing. The second is
a laboratory study of modifiability of
behavior in a large sea anemone, compared
with field observations at each stage of the
work, in the effort to understand better
the mechanisms involved in a conspicuous
case of commensalism. The final case
involves a combination of neurophysiological techniques and field tests of behavior,
aimed at better understanding the sensory
and behavioral mechanisms involved in
feeding/attack behavior by sharks.
Case study #1—Signaling behavior of the
sailfin blenny, Emblemaria pandionis
The sailfin blenny Emblemaria pandionis
is a small fish that lives in colonies in coral
580
E. S. HODGSON AND C. L. SMITH
rubble areas where there is slow to mod- produce a continuous record of the sigerate current. It is widely distributed in the naling activities during a period of several
Caribbean at depths ranging from less than days.
one meter to more than 10 meters. The
Examination of the videotapes conspecies is currently being studied by James firmed our observations that a signal by
C. Tyler of the Smithsonian and C. L. Smith one male will not necessarily result in an
at the field laboratory of the Smithsonian answering signal by another male, although
Institution on Carrie Bow Cay, Belize. The during periods when one male signals
following preliminary observations will repeatedly other males may also signal.
serve as an example of how a field study Further examination of the tapes revealed
can proceed as a series of simple questions. that the usual pattern consists of intense
The male sailfin blennies guard nests nagging in the early morning, beginning
consisting of small cavities in fist-sized at first light. The flagging rate decreases
pieces of coral rubble. Females are mobile as the sun gets higher, and during midday
and have no special residence holes. The it occurs only sporadically. Late in the
species is strongly sexually dimorphic; the afternoon the signaling again increases in
males have the dorsal fin expanded with intensity, then decreases but continues until
an anterior lobe that is much larger than it becomes too dark for our camera to
that of the female. Spawning seems to occur record. The amount of energy devoted to
throughout the year; our observations have this behavior is impressive; most of the subbeen made in March, June and November. jects had from 300 to more than 1,000
Males guarding eggs spend most of the flagging episodes each day. Such a tremendaylight hours resting in their burrows with dous expenditure of time and energy is
their heads protruding. Normally, the head strong evidence that the signaling behavior
and anterior part of the body are dark is of benefit to the species.
brown to jet black. Periodically, they
The observation that flagging decreased
emerge part way or completely out of their during the midday caused us to look at the
burrows and raise and lower their dorsal correlation between flagging and the presand anal fins in a spectacular display, which ence of ripple marks on the bottom. Freappears to be some kind of signal (Fig. 6). quently, when a cloud passed in front of
During this signaling episode, the fins are the sun, the ripple marks disappeared and
raised from one to 30 times, and often the there was a brief flurry of signaling. To
males rise 20 to 30 cm above the bottom check this further, we floated a semias they signal.
opaque plastic tarpaulin over the colony
Such a conspicuous behavior immedi- and this did indeed stimulate flagging durately raises the question of why they do ing the period when normally there would
this, but "why" by itself is a question that have been little if any such activity. A clear
is too general to be meaningful. It must be plastic did not have the same result. More
broken down into some form that is more recently, we have conducted the reverse
direct and testable. To whom are they sig- experiment placing a floodlight over the
naling? If to other sailfin blennines, is the site to produce ripple shadows during times
signal a warning to other males or is it an when the sun was too low to produce them
attempt to attract females? Is it a warning naturally. The results have not been anato other species? Is it possible that the lyzed, but the object is to see if the observed
behavior is not a signal at all but merely a rhythm is determined directly by environfeeding excursion? Finally, what is the ben- mental factors or if there is an innate
rhythm that will be immune to such perefit to the sailfin?
Our first efforts to record this behavior turbations.
Videotapes often reveal phenomena that
using a stopwatch and notebook were
unsuccessful, so we enlisted that aid of Mr. might otherwise be missed. Our tapes have
Chip Clark, photographer at the National shown that the nests of the sailfin blennies
Museum of Natural History, to build an are frequently disturbed by other fishes that
underwater video system so that we can crop algae growing on the nest rock and
BEHAVIOR OF CORAL REEF ORGANISMS
by rays that dig in the sand in search of
their prey and scatter the nests in the process. This made us aware that the nest holes
are usually in parts of the rocks that will
still be accessible even if rock itself is
inverted. Presentation of artificial nests
with holes in various positions confirmed
that the fish select sites on the sides of the
structure rather than at highest part of the
rock.
If a mirror is presented to the males they
will emerge from their burrows and go into
an aggressive display that is quite different
from the signaling, and includes a general
blanching so that a pattern of stripes
becomes visible on the dorsal fin (Fig. 6).
If another male is moved close, there will
be an actual attack that can result in one
male being forced to abandon its nest. It
therefore appears that the aggressive
behavior is quite different from the signaling behavior (compare Fig. 6A and 6B).
From this we postulate that the two behavior patterns are antagonists: the signaling
behavior attracts conspecifics and the
aggressive behavior prevents them from
approaching too closely. During our next
field season we propose to test this hypothesis by setting up artificial habitats with
suitable nesting sites and seeding some with
males while others are left without males.
We expect the sites with males to be colonized more rapidly than the ones without
males.
On one of our tapes there is an indication
that the approach of the sand tilefish Malacanthus plumieri will trigger a signaling
response. Since sand tilefishes gather coral
fragments for their own nests, they may
represent a particular type of threat to the
rubble-dwelling blennies. Crude model
experiments have not been successful, but
we are examining our tapes to see if there
are other cases of a response to the sand
tilefish. If this response to the sand tilefish
is confirmed, one might well ask why the
response is signaling rather than an aggressive display?
What might some of the benefits of signaling be? It seems reasonable to assume
that signaling and aggressive behavior act
in concert to establish a desirable spacing
of individual males—close but not too close.
581
Sailfin blennies have rather precise habitat
requirements. They must have proper size
holes for nest sites and they must be where
there is enough water movement to bring
in a continuous food supply since they, like
the garden eels, are sessile feeders. Signaling could benefit the species by attracting other males to suitable habitat once
such habitat has been located and colonized by one or more males. Since the
females move to the males for spawning,
it is advantageous to have the males concentrated in a relatively small area. Spacing
of the males regulated by aggressive behavior would benefit the males by lessening
competition for the food particles that drift
by, would reduce competition for mates
and would also benefit the larvae as they
leave the nest by lessening the possibility
that any given larva would be immediately
preyed upon by an adjacent male.
Acoustic signaling is common among reef
fishes (Winn et al., 1964) and visual analogs
are not unexpected. The sailfin blenny is
a superb experimental animal that lends
itself ideally to in situ field experiments.
Case study #2—Mechanisms and benefits
of symbiotic behavior: Sea anemones
and anemonefish
Close associations of different species of
organisms are commonplace in coral reef
ecosystems. In fact, it has been said that if
one observes a particular species living on
a reef and does not observe at least one
other species associated closely with it, the
observations have been too brief or superficial! (Students jn field courses may be
challenged to check out this assertion.)
Sponges commonly "house" large numbers of other invertebrate species and small
fish. Corals, sea anemones and some molluscs and worms contain millions of algal
cells (zooxanthellae) within their tissues.
Other examples of interspecific associations have been mentioned above and it
would be beyond the scope of this paper
to attempt an inventory of even the major
known examples.
One of the most conspicuous of all animal associations to be observed in tropical
seas is the interactive behavior that occurs
between sea anemones and their symbiotic
588
E. S. HODGSON AND C. L. SMITH
FIG. 7. Interspecific behavior between Amphiprion akindynos and Entacmaea quadricolor involving food storage
responses. A. A. akindynos swimming toward food (white bread) in an attempt to carry it to anemone in
background. Food was seized by faster pomacentrid fish at left although it was further away. B. A. akindynos
carrying food (dark square) successfully to anemone in background. C. E. quadricolor showing mouth opening
in response to swimming activities of nearby anemonefish which is attempting (unsuccessfully) to catch and
store food. D. Tail of A. akindynos retrieving food stored in gastrovascular cavity of E. quadricolor. Photographs
by Valorie Hodgson.
fishes. This association is not confined to
one single species of fish or anemone but
is most notable among the more than two
dozen species of anemonefish or clownfish
included in the genus Amphiprion, which
associate with sea anemones of several genera including Entacmaea (formerly Physobrachia), Heteractis (formerly Radianthus)
and Stichodactyla (formerly Stoichactis).
These are found specifically in the shallow
waters of Indo-Pacific coral reefs but can
often be seen on display in the exhibition
tanks of public marine aquariums.
An observer's attention is quickly drawn
to these small, orange or black fish decorated with one or more white patches or
stripes and usually seen darting in and out
between the tentacles of a sea anemone. If
disturbed or frightened, the little fish may
dive directly into the large mouth opening
of the anemone (Fig. 7). Since anemone
tentacles bear stinging cells which are capable of ejecting nematocysts containing toxins lethal to small fish, an immediate question is how the anemonefish escapes being
stung while presumably benefiting from the
fact that pursuing fish of other species
would be stung by the host anemone.
Other questions also come to mind as
this obviously close relationship is observed
further. Are the benefits reciprocal as in
true symbiosis, or is only one animal bene-
BEHAVIOR OF CORAL REEF ORGANISMS
583
fiting as in commensalism? As the fish's "pro- ones, compared to fish in tanks without
tection-seeking" behavior is repeatedly anemones. However, a suggestion that
observed in the field and the specificity of anemones kill or remove ectoparasites from
this adaptive association continues to fas- the fish was not supported by the obsercinate, another question arises: What was vations of Mariscal (1970). Although it is
its evolutionary origin? How does such a more difficult to study and describe prespecialized adaptive-linkage in the behav- cisely, there are indications that the fish
ior of two species become established? Are seek some sort of tactile stimulation from
there any less-than-perfect intermediate their anemones and occasionally Amphistages of associations between fish and prion will nibble and ingest anemone tenanemones that might suggest how it all got tacles or mucus strands from its host. The
started?
exact significance of the latter behavior of
These are not types of questions that the fish remains unknown.
apply only to the anemone and clownfish
Is there any benefit to the anemone from
association. Similar questions arise in almost this association, and if so, what? Amphiprion
any instance of animal cooperation, com- is highly territorial and has been observed
mensalism or symbiosis—making this an to chase away various other species of fish
attractive illustration to enhance under- which are known to feed upon anemones,
standing of an important type of animal so some protective benefit to a host anembehavior (McFarland, 1985). It is useful to one is obvious. Less easily interpreted is
consider these, and other questions in the carrying of food to the anemone by its
sequence even if some important obser- anemonefish as observed by a number of
vations were made by chance rather than investigators (reviewed by Mariscal, 1970).
derived from a single line of research Is the food carrying simply to feed the host
inquiry.
anemone, or is it the fish's attempt to transFirst of all, although the "protective port or store food in its own territory, which
benefits" of this association for the anemo- just happens to be the area near the anemnefish may seem obvious, without confirm- one? In any case such behavior can be easily
ing observations or experiments such ben- demonstrated in the field by allowing pieces
efits remain only assumptions. Mariscal of food to drift past the fish and anemone,
(1970) removed specimens of Amphiprion whereupon the fish will swim out, grasp the
percula from their host anemone Radian- food in its mouth and immediately return
thus ritteri during field experiments off to the anemone. Needless to say, the anemThailand. When the anemonefish were one frequently ingests dropped bits of the
released up to 10 meters away from their fish's meal and this undoubtedly furnishes
home anemones, they were ". . .often eaten nutrients to the anemone.
by larger predatory fishes in the vicinity,"
Figure 7 illustrates a field experiment
a fate they never suffered when they stayed conducted at Heron Island on the Great
closed to their anemones. These observa- Barrier Reef, in which Amphiprion akindytions are consistent with 19th century nos competed with fast-swimming dansel
reports concerning experiments on the fish for food chunks placed near the anemsame species of Amphiprion confined in one Entacmaea quadricolor. The slower
aquaria—as long as anemones were pres- anemonefish succeeded in capturing food
ent in the tank, A. percula used them as in half the trials by seizing food and usually
shelter and protection from other species spitting it out near, or in the direction of,
of fish, but when the anemones were the anemone tentacles which would conremoved the anemonefish were promptly tact the food and carry it to the mouth.
eaten by the predatory fish.
Occasionally, the fish would carry food
Are there other benefits to the fish from directly to the mouth and push it into the
this association? There are some data gastrovascular cavity of the anemone. The
showing that Amphiprion is less susceptible anemone's own behavior of mouth opento various fungus and protozoan diseases ing to receive food also changed over time
when they are placed in aquaria with anem- as the daily trials were repeated. The initial
584
E. S. HODGSON AND C. L. SMITH
vigorous swimming movements of the
anemonefish as it left the safety of the tentacles to swim out to catch the food were
apparently associated with food by the
anemone, so that in later trials mouth
opening would occur before the food
reached the tentacles, indicating a more
than passive partner in the procedure (V.
Hodgson, 1981).
Another important point is species variability. Not all species of Amphiprion engage
in this food storage and retrieval behavior
and some species will grasp and store nonfood items that happen to drift past (Mariscal, 1970). Such species differences, in
either the fish or the anemones, may well
be important in explaining inconsistencies
between observations of various investigators working in different localities.
The behavioral observations and experiments, noted thus far, have led to a consensus that the fish-anemone association is
an example of true mutualism, with both
partners deriving some benefits. This evidence does not make clear what sensory
cues are used by either the fish or the
anemone in the behavior patterns that
establish the association and maintain its
benefits. Nor did these observations clarify
the mystery of the mechanisms by which
the fish is protected from its host's nematocysts.
Mechanisms
Davenport and Norris (1958) explored
the behavior of Amphiprion percula as it
became "acclimated" to a specimen of Stoichactis in an exhibition aquarium. They
found that "unacclimated" fish (previously
isolated from anemones for at least 6 weeks)
went through a fairly stereotyped series of
reactions when introduced into the anemone tank: approaching and lightly touching the anemone's stinging tentacles with
increasing frequency, gradually swimming
deeper among the tentacles, and finally
swimming rapidly enough to flail the tentacles aside with strong lateral body flexures, as if "bathing" its entire skin surface
among the now non-reactive tentacles.
Complete acclimation occurred during
periods of several minutes to several hours,
with an average time of one hour.
It was found that the acclimated fish oriented visually to the anemone, and there
was some evidence that the presence of the
fish affected the neuromotor apparatus of
the host. Apparently, some active principle
on the skin surface of the fish raises the
threshold of nematocyst discharge, because
a piece of skinless Amphiprion meat was
quickly eaten by the anemone, while a piece
with skin attached was neither seized nor
eaten.
Starting with the presumption that
chemical alteration takes place on the
integument of the fish during acclimation,
Dietrich Schlichter (1976) questioned
whether the crucial chemical differences
are produced by synthesis in the fish or,
alternatively, were derived from the anemone. He found that the mucus covering the
bodies of anemones that formed symbiotic
associations with fish differed chemically
from the mucus of non-symbiotic anemones. (The symbiotic anemones, for example, had distinctive free acid mucopolysaccharides and a higher content of serine and
glycine in their mucus.) Examination of the
protein and amino acid contents of mucus
covering Amphiprion clarkii, before and after
acclimation to anemones, showed additions to the skin mucus of acclimated fish,
corresponding to the special chemical features of anemone mucus. But was this
merely a chance result of body contact, or
the real explanation of the fish's protection? Schlichter postulated that the anemones produced special chemicals in their
own mucus to inhibit the discharge of
stinging cells, thus protecting their tentacles from self-stinging. The acclimation
behavior of the fish merely transferred
these inhibitory chemicals to the fish's
mucus, making the fish surface chemically
disguised as another part of the anemone
("macromolecular mimicry").
Shortly thereafter, experiments by Roger
Lubbock led to a different interpretation,
which also could explain the behavioral
observations (Lubbock, 1979). He carried
out detailed tests to determine what categories of organic substances present on the
skin actually were more effective in eliciting nematocyst discharge in two species of
anemones. It was found that the receptors
BEHAVIOR OF CORAL REEF ORGANISMS
associated with nematocyst discharge were
sensitive to very subtle chemical differences; the evidence suggested that those
chemical groups triggering responses are
absent from external surfaces of the anemone, and a similar interpretation (absence
of crucial chemicals from fish mucus) might
explain the failure of clownfish to trigger
nematocyst firing. Contrary to Schlichter's
observations, Lubbock (1980) found only
slight amounts of labelled anemone mucus
on acclimated clownfish, but he found that
acclimated fish have a mucus layer that is
three or four times thicker than in nonsymbiotic fish. This thicker mucus layer,
he concluded, acts as an inert physical barrier and lacks the chemicals that trigger
nematocyst discharge. Brooks and Mariscal (1984) further tested the hypothesis that
the fish is responsible for manufacturing
its own protection. They found that A. clarkii greatly decreased its acclimation time to
an anemone, following exposure to a simulated model of an anemone, constructed
of rubber bands. Obviously, such a model
could not be transferring "inhibitory
mucus" to the fish, so the results would
have to be accounted for by processes
within the fish itself.
Stimulus specificity and modifiability of
anemone behavior.—Lubbock also noted that
the discharge of stinging cells depended
upon the level of mechanical stimulation
which accompanied precise chemical stimuli, and concluded that the "recognition
process associated with nematocyst discharge may be of a rather sophisticated
nature." Consequently, the mere presence, or absence, of particular chemicals
(however specific) in mucus or food will not
provide fully adequate predictions of
whether an anemone will sting or ingest
potential prey. Actually, many such recent
observations are re-discoveries of much
earlier findings on anemone behavior, such
as (1) the necessity for summation of
mechanical and chemical stimuli to trigger
feeding responses of anemones under certain conditions, (2) progressively decreasing responsiveness of continuously stimulated sea anemones, and (3) fluctuation of
sensitivity (thresholds) of the anemone's
receptor mechanisms and transmission of
585
excitation from tentacles first stimulated to
others via the nerve net (summarized by
Maier and Schneirla, 1964). Model experiments undoubtedly reveal some important
mechanisms of behaviors in the anemonefish associations, but the reported variability of anemone responses suggest that
other mechanisms need investigation as
well. These considerations prompt questions such as the following: (1) How do the
stinging and eating behaviors of anemones
relate to their previous experience? (2) Do
anemones habituate to non-food mechanical stimuli or symbioticfish?(3) Are anemones capable of long-term modifications of
their behavior, analogous to "conditioned
responses" that are familiar in other animals?
Progress in answering some of these
questions has come from studies by V. S.
Hodgson (1981), using 7 anemone species,
6 species of anemonefish symbionts, and a
combination of field and laboratory experiments in the Pacific and Caribbean areas.
Habituation (decreased responses with
repeated applications of stimulus) was
observed in both Caribbean (Condylactis)
and Australian {Entacmaea) anemones, after
several applications of mild tactile stimuli
at two hour intervals. Such habituated
responses indicated lack of nematocyst discharge and can persist for several days, even
in the absence of further testing. The
anemones discriminate between mechanical and chemical stimuli, since at any time
when responses are habituated to mechanical stimuli, the addition of food chemicals
to the stimuli immediately triggers a full
nematocyst discharge and feeding reaction. The latter finding rules out sensory
adaptation, fatigue, injury, synchronization
to tidal rhythms, etc., as explanations of
the habituation to mechanical stimuli, a
type of simple learning.
The presence or absence of habituation
to mechanical stimuli was found to correlate with the environments where the
anemones were found. Animals located
where grasses or water currents buffeted
their tentacles were invariably habituated
to mechanical stimuli—an obvious advantage in preventing consumption of energy
and time in carrying out complex feeding
586
E. S. HODGSON AND C. L. SMITH
FIG. 8. Sequence of mouth opening responses of Condylactis gigantea undergoing food association training.
A. Medium-sized anemone from Bimini, Bahamas, measuring 5 cm in column height with 10 cm tentacles
and an oral disc of 4 cm diameter. B. Normal, pre-trial appearance of C. gigantea mouth when closed, showing
white, X-shaped closure lines and two siphonoglyphs. C. Food association training response. Anemone mouth
opening as a modified behavioral response (MR) following presentation of conditioned stimulus (CS), warm
sea water, after several reinforcement trials. Width of mouth opening is 7 mm. Tentacles are moved aside
for photographic purposes. D. Food association training response. Anemone mouth opening response to
unconditioned stimulus (US), food. As mouth widens, the pharyngeal lining is everted forming bulbous lobes.
Two such lobes are shown here. Mouth opening measures 25 mm. Photographs by Valorie Hodgson.
behaviors in reaction to non-food stimuli.
Differing abilities to habituate to tactile
stimulation in various anemones may help
to explain why some species seem to require
acclimation, while others do not. This ability of some anemones to demonstrate
habituation or simple learning raises the
question of the possibility for more complex responses requiring sophisticated uses
of the nervous system.
To explore this hypothesis, two types of
quantitative conditioning experiments
were conducted (V. Hodgson, 1981). Using
Condylactis anemones as the study species,
she set up two conditioning paradigms, one
in food avoidance and the other using food
association, with both test procedures
adapted from standard experimental procedures used on vertebrate animals. In the
avoidance training, it was found that anemone tentacles rapidly reduced their holding
time to food which could not be pulled
down into the mouth, when the food presentation was paired with mild electric
shock. In another experiment, to avoid the
use of aversive stimuli, slightly warmed sea
water was applied to the anemone's oral
disc followed immediately by a solution of
fish homogenate. After several pairings of
these two stimuli, the anemones exhibited
mouth openings and eversions of their
pharyngeal linings in response to the
BEHAVIOR OF CORAL REEF ORGANISMS
warmed sea water alone (Fig. 8). The
behavioral modifications in these experiments were statistically significant and none
of the modified behavior as a result of
training could be interpreted as the result
of adaptation, fatigue or sensitization.
Although the modified behavioral
responses do resemble conditioned
responses in vertebrate animals, the neurological mechanisms must be quite different between sea anemones and organisms
with central nervous systems. As techniques (especially electrophysiological procedures) become refined to record from
ever-smaller nerve fibers, the physiological
mechanisms underlying these behavioral
patterns will provide a fascinating challenge for study. Meanwhile, ever more subtle discriminations and long-term behavioral modifications by anemones (as well as
anemonefish) must be remembered as possible components underlying the intricate
behavioral adjustments of sea anemones
and their symbiotic fish.
Evolutionary origins.—The inevitable
curiosity about the origin of this close and
intricate symbiotic relationship must
depend upon indirect evidence. Gendron
and Mayzel (1976) observed that young
blue-headed wrasses, Thalassoma bifasciatum, sometimes swam within the tentacular
sphere of the anemone Condylactis gigantea,
although the fish are not confined to this
habitat. The association is therefore facultative, rather then obligatory. The young
wrasses may spend considerable time picking paniculate matter from the tentacles
of Condylactis, or resting delicately against
the anemone, apparently without being
stung; in aquaria, other anemone species
were avoided by this wrasse, as reported
by Hanlon and Kaufman (1976), who
observed 7 more species of fish in facultative associations with Condylactis in the
West Indies. Some fish exhibited specialized acclimation behavior, which appeared
to keep nematocysts from firing, when they
first approached Condylactis. In laboratory
experiments, fish which were observed as
facultative associates in the field, were
readily stung if they moved quickly or violently against the anemones. By 1983, no
less than 30 species of West Indian reef
587
fishes were known to occasionally dwell
within the tentacle of sea anemones, mainly
Condylactis.
These facultative associates appear to
utilize their anemones as temporary shelters from predators. Most of the fish are
juvenile or small species, but 7 adult members of the Family Clinidae can live in full
contact with the anemone's tentacles, without apparent harm (Hanlon et al., 1983).
Through successive stages of adaptation,
staring with facultative associations, it is
not difficult to imagine the selective advantages of better protection or mutual nourishment, could lead to the much closer
obligatory associations of the Indo-Pacific
clownfishes and their anemones.
There are still many aspects of the formation and operation of these associations
which are not understood. For example, it
is still unknown by what sensory cues a larval clownfish locates its own anemone after
two or three weeks of swimming in the
plankton. Nor do we understand what
sometimes prompts an adult clownfish to
venture ten or twenty times its usual distance from the host anemone, and behave
with unusual aggression toward other fish
(or human divers) that it cannot possibly
damage; these may be manifestations of
hormonal changes in particular parts of a
breeding cycle, but much more evidence
is needed on such matters (Hodgson, 1983).
In animals like clownfish, which are so
restricted to small territories around single
anemones, there are probably many physiological and behavioral adaptations that
are only beginning to be understood—such
as their capacity to change sex if one of a
mating pair dies (Fautin, 1989).
There are many examples of such symbiotic relationships among coral reef animals, still awaiting investigation. In undertaking such studies, it appears likely that
the subtleties of the behaviors involved,
and the underlying physiological mechanisms, will be more complex than heretofore imagined. Even in the relatively simple nerve nets of sea anemones and their
relatives, the once-accepted idea of single
excitable system seems no longer applicable. Quick and slow components analogous
to the giant and ordinary fiber systems of
588
E. S. HODGSON AND C. L. SMITH
many other invertebrates, and some equivalent of a central nervous system in a dispersed form have been noted by Ross
(1973). The findings concerning simple
learning mechanisms in these animals
extend the challenge for attempts at physiological explanations.
Case study #3—Sensory physiology of
orientation and feeding / attack
behavior of sharks
As the largest predators in coral reef
ecosystems, with some species capable of
attacking humans, sharks engender respect
and fear. An upsurge of interest in them
came during World War II, as troops were
deployed throughout the South Pacific.
When ships were sunk or planes shot down,
military personnel found themselves in
unfamiliar tropical waters. The occasional
shark attacks on servicemen had continuing profound effects upon the morale of
survivors, and the Department of Defense
initiated a search for a shark repellent.
However, the inadequacies of basic knowledge about the senses and behavior of
sharks quickly became apparent. Efforts to
obtain basic information led to research
endeavors such as the Shark Research Panel
of the American Institute of Biological Sciences, and a wide range of research projects supported by the U.S. Office of Naval
Research and other government agencies.
Since this case study does not attempt to
provide an overall review, interested students may obtain general background from
the excellent books available, including
Baldridge (1974), Ellis (1975), Moss (1984),
and Stevens (1987). Much of the research
discussed below is considered in greater
detail in the various articles in Hodgson
and Mathewson (1978).
Formulating
the basic
questions.—There
are about 350 living species of sharks,
belonging to 30 different families. Relatively few of these—perhaps a few dozen
species—are of immediate practical concern to humans, either because of risks
from their attacks, or their beneficial contributions to fisheries, as sources of natural
products for medical uses, etc. It is clearly
necessary to narrow down the basic questions bearing upon the life of sharks—
questions with attainable answers that
might enable humans to locate the animals,
predict their behaviors, and possibly modify particular behavioral patterns of those
species significant to us.
As is commonly the case in analyzing
behavior, one of the most useful starting
points is an analysis of the sensory cues that
trigger the animal's activities. What are the
stimuli that initiate and guide the orientation of sharks, and influence their feeding and attack behaviors? How are the
inputs from various sensory systems integrated during these behaviors? Is it possible to block, or interfere with, crucial sensory processes so that the overall behavior
will also be blocked or modified? These are
the sorts of questions that guided the
research in this case study.
Early attempts to answer these questions
concentrated upon the shark's olfactory
(smell) sense, after nineteenth century biologists plugged the nasal openings in the
snouts of sharks and found that the animals
were unable to detect food. Sharks came
to be regarded as "swimming noses." Anatomical studies of shark brains revealed one
or two olfactory bulbs associated with each
nasal sac and connected to the forebrain
by nerve fibers that collectively formed the
olfactory tract (Fig. 9). The most direct
physiological method of studying mechanisms of olfaction would be to attach electrodes to the nerve fibers of the olfactory
tract and record whatever patterns of action
potentials pass to the forebrain, while
chemical stimuli flow through the nasal sac.
Unfortunately, despite many attempts to
achieve such electro-physiological recordings from afferent fibers in the olfactory
tract, thus far this method has failed to
produce records of action potentials that
are stable or reproducible enough to make
a useful experimental method. (The reasons for this failure are not clear, but some
possible explanations are discussed by
Hodgson and Mathewson, 1978.) However, it is possible to record electrical
changes in large numbers of nerve cells
which are simultaneously active in various
parts of the shark's brain (Fig. 9). This
method gives records that resemble electroencephalogram (EEG) patterns recorded
BEHAVIOR OF CORAL REEF ORGANISMS
589
v•'-•'*^^«*••«^^^*^>r^^
FIG. 9. Brain and electroencephalograms of lemon shark, Negaprion brevirostris. Left—diagram of brain with
numbers indicating EEG recording points. OS—olfactory sac; OB—olfactory bulb; OT—olfactory tract; T—
telencephalon; CER—cerebellum; MES—mesencephalon; MED—medulla. Right—EEG responses from electrodes in positions 1-2 and 7 during stimulation by chemicals. A. and C. during stimulation with 1-glutamic
acid alone in seawater; B. with holothurin added to the stimulus. Note changes in forebrain and medulla
potentials during normal stimulation, and disruption of normal EEG responses when holothurin (a naturallyoccurring repellent/toxin) is added to the stimulus. See text for details.
from mammals. The EEG method does
demonstrate electrical patterns in the
shark's brain which correlate with olfactory stimulation by chemicals dissolved in
sea water, as they pass through the nasal
sac.
Typically, things that stimulate feeding,
like meat extracts, cause increase in some
basal level of electrical fluctuations in the
shark's forebrain (Fig. 9B). When recordings are made from electrodes implanted
into the medulla of some shark species,
another regular electrical pattern is
observed; this correlates with rhythmic
movement of the gills, and the brain activity is believed to come from nerve centers
that trigger contractions in gill muscles.
The EEG from the medulla, along with gill
movements, is modified when the shark is
stimulated by food. It appears that the
sharks, as they sense an "attractive" smell,
give an extra gill beat, thus taking in an
extra portion of oxygen that probably
assists as they lunge forward toward a stimulus.
The ideal possibility for experimentation would be to permanently implant electrodes within the forebrain and medulla of
a shark, then make simultaneous records
of its EEG patterns and its swimming
behavior in some situation where defined
chemical stimuli would contact the animal
at precisely-known times. In this way,
behavioral changes might be correlated
with neurological events, as different kinds
or amounts of chemical stimuli were
administered. This possibility was realized
through use of a "hydrodynamic tunnel"
designed for studying the flow of water
around various models of ship hulls. Essentially, the apparatus was a circularflowsystem for 1,150 gallons of sea water, driven
by propellers in such a way that the water
movement was uniform and without turbulence in all parts of the circular tunnel.
Chemicals introduced near the propellers
circulated in known dilutions and time
intervals; at one point, they passed through
a glass observation chamber where a shark,
wired for EEG recordings, swam freely (see
Hodgson and Mathewson, 1978, for additional details).
Getting the experimental analysis to this
stage, where tests of various chemical stimuli could be routine, required several years
of work and many unproductive trials of
590
E. S. HODGSON AND C. L. SMITH
alternative methods. For example, progress was frustrated for a long time by the
tendency of sharks, especially when
extremely active in response to chemical
stimuli, to tangle the wires attached to their
implanted electrodes. Only after development of a special swivel for the EEG wires,
designed to allow complete freedom of
movement by the sharks while maintaining
electrical contacts without twisting of the
wires, could the simultaneous electrophysiological and behavioral records be
achieved. Only a few species of sharks were
available in quantity, in useful sizes, and a
decision was taken to concentrate on the
lemon shark, Negaprion brevirostris, and the
nurse shark, Ginglymostoma cirratum, both
of which seemed highly responsive to
chemicals. More than 100 pure chemicals
and extracts, dissolved in sea water, were
tested for possible neurological effects
within the shark's brain and any effects
upon the behavior of the animals.
Tests of electrolytes, carbohydrates,
amino acids, amines, lipids, polyhydric
alcohols, purified blood fractions, and miscellaneous other extracts were carried out;
details of the results have been reviewed
by Hodgson and Mathewson (1978). In
brief, it was found that certain amino acids
(glycine and glutamic acid) and amines
(betaine, trimethylamine—TMA—and
TMA-oxide, amines which are breakdown
products in tissues and excretions of fish)
elicited particularly strong electrophysiological and behavioral responses from the
sharks, under the standardized test conditions. No claim could be made that all
the chemical stimuli to which sharks are
sensitive had been identified. However, it
was possible to make some informed guesses
about the specializations of the receptors
that triggered the initial behaviors of sharks
reacting to chemical cues.
Do the sharks "follow through" after
their initial reactions of lunging upstream
in the water currents which carry chemical
cues? What further stimuli do they use in
orienting to potential food or prey? To
investigate these questions, it was necessary to study the sharks in larger spaces
than the observation chamber of" the
hydrodynamic tunnel. Also, in order to
keep the study conditions as close to the
normal environment as possible, a way was
sought to monitor shark behavior in dim
light or darkness, when these species are
most active.
High intensity electronic blinkers
attached to the dorsal fins of sharks, traced
the movements of sharks at night in a large
outdoor pen (Fig. 10). An underwater
videotaping system, similar to the one
employed in the signaling behavior studies
of case #1 above, provided additional valuable information. To everyone's surprise,
it was found that lemon sharks and nurse
sharks oriented in quite different ways, following initial reactions to underwater
odors. Nurse sharks followed a zig-zag
route, of progressively narrower width,
toward a source of chemicals in the water;
evidently, they were sampling concentrations of chemical stimuli, from side to side,
and "homing in" on the source. This is
true gradient-searching, or klinotaxis.
Lemon sharks, however, exhibited a pattern of behavior that puzzled everyone for
a long time. They swam in relatively
straight lines, and sometimes appeared to
become locked into a circling behavior in
one corner of the shark pen—even if the
source of chemical stimulation was in a different corner! Eventually, it was realized
that the lemon sharks, once stimulated, oriented against the strongest current in the
pen, and continued trying to swim upstream
even if the source of chemical stimulant
was elsewhere, in a weaker current.
Negaprion displays rheotaxis rather than
klinotaxis. A chemical stimulus serves as a
rheotaxis-release mechanism, and subsequent orientation behavior of the lemon
shark is dominated by input from mechanoreceptors situated along the head and
lateral line. In most natural situations, this
integration of responses to chemical and
mechanical stimuli would bring the lemon
shark close to the potential source of food,
but in our experimental situation (where
tidal currents moved in different speeds on
two sides of the large shark pen), the dominance of the mechanical stimuli was
revealed. Figure 10 illustrates the blinker
light trail of a lemon shark which swam
directly against the strongest current in its
BEHAVIOR OF CORAL REEF ORGANISMS
591
FIG. 10. Behavioral responses of sharks to pure chemical stimuli. A. Tracking the behavior of a shark at
night by use of an attached blinker light and time-exposure. The lemon shark, after encountering an odor
trail of glutamic acid, orients against the flow of the water current (rheotaxis) and swims to the source of
stimulation, then circles the source at the far end of the large enclosure. B. Lemon shark biting source bottle
of TMAO-glycine mixture in a reef channel, during tests of responses by wild sharks exposed to defined
chemical stimuli. See text for details.
pen (right side), encountered the source of
chemical stimulation (glutamic acid) in one
corner and circled it.
Do "wild" sharks, never confined to pens
or previously tested with pure chemicals,
behave in the same ways as the experimental animals? Open sea tests are appropriate to answer this question, and
underwater videotapes provide helpful
documentation. Figure 10B shows the
result of allowing a mixture of TMAO and
glycine to seep from a perforated source
bottle that was tethered in a narrow gully
in a small fringing reef in the Bahamas.
The gully carried currents up to 0.7 knot
during tidal flow between the shallow
lagoon and an area seaward of the reef.
Two lemon sharks and a large ray (Dasyatis)
were attracted to the gully which carried
the chemical stimuli. The lemon shark pictured had proceeded against the current,
approached the bottle, and was vigorously
biting it. It was quite possible that visual
cues assisted this "attack" behavior, for the
tethered bottle moved slightly in the current. The integration of chemical,
mechanical, visual, and even electrical or
magnetic sensory cues in guiding such
behavior remains an interesting topic for
continuing investigations.
Returning to the initial practical question which stimulated much of the wartime
interest in shark neurophysiology and
behavior, is it possible to block any of these
sensory processes with some sort of "shark
repellent?" Baldridge (1974) has shown that
a chemical that is toxic enough to incapacitate a shark will probably also harm the
human who uses it in the water. Recent
attention has focused upon the natural
repellents and toxins produced by various
invertebrates and fish in coral reef ecosystems. One such is "holothurin," produced
by some species of sea cucumbers (Echinodermata, class Holothuroidea). Holothurin elicited avoidance behavior from
several species of sharks under simulated
natural conditions, and when mixed with
known chemical stimulants like glutamic
acid, produced marked changes in the EEG
patterns, both forebrain and medullar
recording, of sharks. This effect, and
recovery from it, is illustrated in tracings
B and C of Figure 9B.
592
E. S. HODGSON AND C. L. SMITH
ture tell us about daily and subdaily events in the
early life history offish? Rapp. P.-V. Reun. Cons.
Int. Explor. Mer. 178:369-374.
Brothers, E. B. and W. N. McFarland. 1981. Correlations between otolith microstructure, growth,
and life history transitions in newly recruited
French grunts [Haemulonflavolineatvm(Desmarest), Haemulidae]. In R. Lasker and K. Sherman
(eds.), The early life history offish. Rapp. P.-V. Reun.
Cons. Int. Explor. Mer. 178.
Bullock, T. H. and G. A. Horridge. 1965. Structure
and function in nervous systems of invertebrates. 2
vols. W. H. Freeman, San Francisco.
Clarkson, E. N. K. 1986. Invertebrate palaeontology and
evolution. 2nd ed. Allen and Unwin, London.
Cloud, P. E. and M. F. Glaessner. 1982. The Ediacaran Period and system: Metazoa inherit the
earth. Science 217:783-792.
Colin, P. L. 1982. Aspects of the spawning of Western Atlantic reef fishes. In G. R. Huntsman et al.
(eds.), The biological bases for reeffishmanagement.
NOAA Tech. Mem. NMFS-SEFC-80. NOAA
National Marine Fisheries Series, Beaufort, North
Carolina.
ACKNOWLEDGMENTS
Collette, B. B. and F. H. Talbot. 1972. Activity patterns of coral reef fishes with emphasis on nocWe are indebted to many colleagues for
turnal-diurnal changeover. Bull. Los Angeles
valuable discussions of various portions of
County Mus. 14:98-124.
this material; these include Niles Eldredge, Copper, P. 1988. Ecological succession in phaneroGregor Hodgson, Richard Jenkins, and
zoic reef ecosystems: Is it real? Palaios 3:136-152.
James Tyler. The manuscript benefited Cowen, R. 1988. The role of algal symbiosis in reefs
through time. Palaios 3:221-227.
from the reading and suggestions of ValoDales, R. P. 1967. Annelids. Hutchinson Univ. Library,
rie Hodgson, who also provided the phoLondon.
tographs of her experiments on sea anem- Davenport, D. and K. S. Norris. 1958. Observations
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on the symbiosis of the sea anemone Stoichactis
and the pomacentridfish,/lw/)/M/)non/)?rcu/a. Biol.
of signaling sailfish blennies. None of these
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Domm, S. B. and A.J. Domm. 1973. The sequence
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