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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 561 562 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 564 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. 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