Behavioral Adaptations of Intertidal Hermit Grabs

Transcription

1 AM. ZOOLOGIST, 9: (1909). Behavioral Adaptations of Intertidal Hermit Grabs ERNST S. REESE Department of Zoology, and The Hawaii Institute of Marine Biology, University of Hawaii, Honolulu, Hawaii SYNOPSIS. AS an ecotone, the littoral environment is often complex and is generally rich in numbers and species of organisms. The disadvantages of the biotope in terms of exposure to physical factors of both the marine and terrestrial environments are patent, but the advantages are not so evident. The continual replenishment of food brought from the sea, particularly for detritus-feeding animals such as hermit crabs, coupled with the possibility and ability to establish microhabitats with microclimatic conditions may constitute the principal advantage. Escape from specialized predators may also be important. Hermit crabs have successfully exploited most intertidal environments. As members of the "benthic detritus-feeding guild" food is abundant, and by utilizing their shells in conjunction with movements within the littoral zone they have met successfully most of the rigors of the environment. The shell also provides some protection from predation, particularly from non-specialized predators. Indeed, the behavioral patterns associated with living in shells which permit the shell to serve as a microhabitat constitute the major adaptation enabling the hermit crabs to exploit the intertidal environment so successfully. During the past two to three decades the same period in which ethology has developed as a major area of zoological research behavior has been increasingly recognized as a major category of adaptation related to the geographical and ecological distribution of animals. Indeed, many species of terrestrial and semiterrestrial crustaceans simply could not survive in the environments in which they live, if given structural and physiological adaptations alone (Barnwell, 1968; Bliss, 1968; Edney, 1968; Herrnkind, 1968; Hurley, 1968; Warburg, 1968). This now obvious truism became apparent when zoologists began to observe and study animals in nature or nearly natural settings. The importance of behavioral adaptations was not recognized by the zoologist studying preserved material, caged animals under conditions of deprivation, or specimens pinned down under bright lights and the Contribution Xo. 326 of the Hawaii Institute of Marine Biology, University of Hawaii, Honolulu, Hawaii The author's research reported herein was supported by Grants GB-1003 and GB-3651 from the National Science Foundation and by the Eniwetok Marine Biological Laboratory. 343 probing tip of an electrode. The purpose of this paper is to examine the role of behavior as an adaptation enabling hermit crabs to exploit successfully the rigorous intertidal environment. I have drawn on the literature as well as unpublished data on the behavioral ecology of hermit crabs from studies by my students and me during the past eight years. I am particularly indebted to Charles K. Barry and Dominic Papagni. THE INTERTJDAL ENVIRONMENT. The intertidal or littoral zone can be thought of as the most dramatic ecotone of all. Organisms which are able to exploit it successfully as a place to live have the best of two worlds, the marine and the terrestrial, but they must also be able to meet the exigencies characteristic of each. The intertidal organism must be able to avoid or tolerate such physical environmental factors as wave action with concomitant abrasion, desiccation, and exposure to both salt and fresh water, and extreme temperatures and very abrupt changes in these extreme conditions. In the biotic realm the intertidal animal may

2 344 ERNST S. REESE be exposed to both terrestrial and marine predators. It is relatively easy to list many apparent disadvantages and "hardships" imposed by the harsh intertidal environment. It is more difficult to understand the advantages which accrue from the exploitation of this environment. A few are obvious. For example, the sessile barnacle waits for the rising tide and waves to bring food to its outstretched and rhythmically beating captorial cirri. There can be modification of this theme as Barnes and Reese (1959, 1960) showed in the stalked barnacle, Pollicipes. Recently Magnus (1962, 1964) observed the ophiuroid, Ophiocoma, exploiting the incoming tide as a source of suspended food, and MacGinitie (1949) and Efford (1965, 1966) described the behavior of Emerita filtering food from the waves washing a sandy beach. Although direct proof is lacking, I suggest that (1) the continual flux of food into the intertidal environment due to the tides and waves, and (2) the possibility of creating microclimatic conditions when exposed to air and thereby avoiding extremes of temperature and the stress of desiccation imposed by the terrestrial environment, together constitute the major advantage of living in the intertidal environment. The sea supplies the food, and the organisms avoid the extreme adverse conditions of the land by establishing microhabitats. In addition, motile animals can migrate and aggregate or disperse with changing tidal levels. It is also possible that the intertidal habitat offers refuge from predation. In spite of the fact that intertidal animals are subjected to predation by both marine and terrestrial animals (Reeder, 1951; Mitchell, 1953; Recher, 1966; Shoup, 1968), periodicity in the availability of intertidal organisms as food would decrease the probability of predator specialization. For example, a shore bird hunting visually can only exploit intertidal animals as a source of food at certain seasons during low tides and daylight hours. Similarly a predatory fish is restricted to periods of incoming and high tides, because due to the possibility of being trapped in a shallow pool the period of falling tide is a potentially dangerous time to hunt in the littoral zone. In hermit crabs, I suggest that the behavior associated with the use of shells is the major behavioral adaptation enabling them to exploit so successfully the intertidal environment. Being for the most part scavengers and feeders on detritus (Boltt, 1961; Roberts, 1968), the flotsam of organic material being continually washed into the intertidal region provides them with a continually replenished source of food. Adaptations related to movement within the littoral zone, and to reproduction, also have facilitated the successful exploitation of the intertidal environment by hermit crabs. HERMIT CRABS: A SUCCESSFUL GROUP Just how successful are hermit crabs in the intertidal environment? There are perhaps 40 to 50 valid genera and probably more than 700 species of shell-carrying hermit crabs (Gordon, 1956). In addition, new species and genera are being described as collections are made in remote areas and in the abyssal environment {e.g., Forest and Saint-Laurent, 1967; Provenzano, 1968). The great majority of these species are in the families Diogenidae and Paguridae. The Coenobitidae is a small family containing the shell-inhabiting, terrestrial hermit crabs of the genus Coenobita, and the monospecific genus Birgus which carries shells only as glaucothoes and during its first two years as small crabs (Reese, 1968a; Reese and Kinzie, 1968). The Pylochelidae contains those crabs which generally do not live in shells but instead keep their soft abdomens in holes in rocks, pieces of bamboo, sponges, etc. (Alcock, 1905). Russell (1962) has written a most provocative account of the great diversity to be found in this fascinating group of decapod crustaceans. Hermit crabs are one of the most conspicuous groups of organisms in north temperate rocky littoral environments, and the

3 ADAPTATIONS OF HERMIT CRABS PATTERNS OF DISTRIBUTION The pattern of distribution within the littoral zone is variable in both space and time depending upon the particular species. For example, three sympatric species of intertidal hermit crabs are found in the broken coral rubble of Hawaiian reef-flats. We have studied the behavior of the populations in Kaneohe Bay. In the field, larger individuals of all three species are most often found inhabiting shells of Trochus sandwichiensis or Turbo sandwicensis. The breeding seasons of all three species overlap, and occasionally all three have been found in the same tidal pool (Reese, 1968b); hence, there is no doubt about the sympatry of these three species. Calcinus laevimanus is found throughout the littoral zone but is especially abundant in the supralittoral fringe and midlittoral zone. It does not occur in the sublittoral. C. laevimanus is most active at the water's edge, and there is some movement with the incoming and ebbing tide. One can observe the animals feeding by reciprocally bringing the chelipeds from the detrituscovered rocks to the mouth. Another species, Calcinus latens, inhabits the infralittoral fringe and shallow sublittoral. This species tends to be active at low tide but aggregates under rocks and coral boulders during high tide, perhaps in FIG. 1. Calcinus elegans, an inhabitant of the algal ridge of most tropical Pacific islands, often is found in relatively very large and heavy shells of a variety of species. The shells are frequently encrusted with coralline algae. (Photo courtesy of Charles K. Barry). response to potential predation. The third species, Clibanarius zebra, is distributed higher in the littoral zone, being perhaps most common in the supralittoral fringe. In contrast to Calcinus latens, G. zebra tends to aggregate under rocks and chunks of broken coral during low tide when the supralittoral fringe is subjected to maximum insolation and desiccation. It becomes active as the incoming tide covers its habitat. It would be interesting to determine whether aggregating and subsequent dispersal of the crabs are stimulated by hydrostatic pressure, as Moulton (1962) found in the gastropod, Cerithium moniliferum. Clibanarius zebra also differs from the other two species in that very small individuals of this species occur in a great variety of shells and are extremely abundant (MacKay, 1945), whereas it is difficult to find small individuals of the other species. Generally, the smaller the crabs the greater is the diversity of shells in which they are found. Two other species of intertidal hermit crabs are common along Hawaiian shores. Calcinus elegans is found on the outer edge of the reef-flat, on the algal ridge and along its inner margin. The crabs are found in relatively large and heavy shells (Fig. 1) which are often encrusted with the calcareous alga, Porolithon onkodes. same is true for the reef-flat environment of the tropical Pacific from Australia to Hawaii to the Gulf of California and Panama. They are common in mangrove swamps, which constitute a surprisingly large portion of tropical, continental shorelines. Hazlett (1966a) found them to be extremely abundant on Caribbean shores. In sandy environments, hermit crabs tend to be sublittoral rather than littoral. Hermit crabs tend to be absent along with most other larger plants and animals from wave-exposed environments composed of loose and shifting rocks. It seems fair to conclude that hermit crabs are abundant, widespread, and successful in the intertidal environment. 345

4 346 ERNST S. REESE TABLE 1. Distribution, of the common sprcies of hermit, crabs across the reef-flat and littoral zone of Oalni, Hawaiian Islands, and Eniwetok Atoll, Marshall Islands. Position in littoral zone Hawaii Eniwetok Algal ridge Middle reef-flat and mid-littoral Inner reef-flat and supralittoral Wave-cut bench The encrusting alga tends to obscure the shape of the shell, and the pinkish to purple color of the algae makes the camouflage of the shell very effective. At low tide the crabs move about picking at the substratum. I have not observed their behavior at high tide, as their habitat is then subjected to heavy wave action. The heavy shells may serve both to keep the crabs and shells from being washed away and to protect them from the impact and abrasion of the waves. Another species, Calcinus seurati, is found on wave-washed limestone benches and exposed areas where basaltic rocks have been eroded to form "pot-holes". Again relatively little is known of the behavior of this species; however, in Hawaii the availability of shells seems to limit the size of individuals in the population. The crabs are usually found in the rather small shells of Nerita picea, which are usually encrusted with Spirorbis tubes, but there are a few locations, e.g., Kapapa Island, where larger shells are available to C. seurati, and there one finds larger specimens. Most of these same sjiecies occur at Eniwetok Atoll in the Marshall Islands. Table 1 compares their distribution across the reef-flat in the two localities. The large spectacular species, Aniculus aniculus, is common on the algal ridge at Eniwetok and usually inhabits the large shell of Turbo argyrostomus. Incidentally, this species of Turbo also is a conspicuous member of the biota of the algal ridge. Whereas Calcinus latens occurs in the littoral, especially the infralittoral fringe and down into the sublittoral in Hawaii, it appears to be Calcinus elegans Calcinus laevimanus Calcinus latens Clibanarius zebra Calcinus seurati Calcinus elegans Calcinus gaimardi Anicitlus anicuhis Calcinus laevimanus Calcinus latens Calcinus seurati Clibanarius corallinvs No equivalent habitat more common in the sublittoral at Eniwetok where it is particularly abundant on dead coral heads in the lagoon and inhabits a variety of shells, often broken. At Eniwetok its niche is occupied in part by Calcinus seurati, which in Hawaii occupies specialized situations of wave-cut limestone and basaltic benches. At Port Sudan in the Red Sea, Calcinus latens was abundant in extremely shallow areas over a sandy, occasionally broken bottom. Since there are no daily tidal fluctuations, this is a shallow sublittoral habitat. At Eniwetok, Clibanarius corallinus is ecologically and behaviorally equivalent to Clibanarius zebra in Hawaii. Calcinus gaimardi is quite common just behind the algal ridge at Eniwetok, while in Hawaii it occurs in the subtidal and is not common. Hazlett (1966a) provided similar data on the distribution of intertidal species of hermit crabs in the Caribbean. Again there are minor changes in the distributional patterns between species. For example, in Curacao, Clibanarius tricolor, Calcinus tibicen, and Pagurus miamensis occur in shallow, open water, rocky habitats. They tend to be nocturnal and may aggregate to varying degrees depending on species membership and local conditions. In contrast, Clibanarius cubensis is active during periods of high tide regardless of whether it is day or night. It migrates from the sublittoral onto the shallow mudflats with the rising tide. Another species, Clibanarius antillensis, also inhabits the mudflats in Curacao, but in Miami, Florida, it is sympatric with Clibanarius tricolor. Two species of hermit crabs were

5 ADAPTATION'S OF HERMIT CRABS 347 TABLE 2. Numbers of hermit crabs occupying various species of shells, collected from the littoral zone along the northern shore of Santa Monica Bay, California. Species of shell Acanthina spirala Olivella biplicata Tegula funebralis Comix calif ornicus Murejc (Jaton) festivus and M. (Pterorytis) nuttallii N assarius perpinquis and N. fossatus Norissia norrisii Ocenebra (Tritonali) poulxoni Thais emarginata Total number of crabs P. xamitelix 117 (61.9%) P. hirxutiuscitlus 300 (50.3%) 266 (44.6%) studied in the rocky intertidal areas of southern California. Paguriis sarnuelis is abundant in extremely rocky areas, while Pa gurus hirsutiusculus is found in tidal pools with sandy bottoms. In many areas, however, the two species are locally sympatric. The rocky intertidal area extending along the northwest side of Palos Verdes, Los Angeles County, California, supports a huge population of P. sarnuelis, but very few P. hirsutiusculus. The larger specimens of P. sarnuelis were found to be in the shells of Tegula funebralis, occasionally in Norissia norrisii, Acanthina spirata, or Thais emarginata, but rai - ely in shells of Olivella biplicata. The smaller crabs were usually found in the shells of either Littorinn planaxis or L. scutulata. Very small animals were found in a variety of small shells, with Mitrella and Lacuna conspicuous. Tegula funebralis and Littorina planaxis appeared to be the most common living gastropods in the area. Thus, there is a correlation between the abundance of living gastropods and the shells most frequently utilized by P. sarnuelis. In contrast to Palos Verdes, the intertidal area extending along the northern shore of Santa Monica Bay, is predominantly sandy with only a few rocky areas. All of the rocky areas are occupied by hermit crabs, of which P. hirsutiusculus is the most common. Table 2 shows the numbers of P. samuelis and P. hirsutiusculus collected in clifferent species of shells from the rocky intertidal areas along the northern shore of Santa Monica Bay. It is apparent that (1) P. hirsutiusculus is the most common hermit crab in the area, (2) P. hirsutiusculus usually was found in shells of Acanthina or Olivella and (3) P. samuelis, though less common, usually was found in shells of Acanthina, or of Tegula and Norissia when they were available, but rarely in shells of Olivella. A similar study was made of the rocky intertidal area on the northeast side of San Nicolas Island (Table 3). The following conclusions are based on these data: (1) Paguriis samuelis usually occupies shells of Acanthina or Tegula, and is the most common hermit crab in the more rocky intertidal areas; (2) Paguriis hirsutiusculus usually occurs in shells of Acanthina or Olivella and is the most common hermit crab in intertidal areas with a sandy bottom between the rocks; (3) In some habitat areas such as at San Nicolas Island, both crabs are common, often in the same tidal pool. However, in very sandy situations only P. hirsutiusculus is found. Where both Olivella and Tegula are available, P. samuelis usually occupies the shells of Tegula, and P. hirsutiusculus usually is in Olivella shells. Bollay (1964) and Orians and King (1964) provided additional data on the distribution and utilization of TABLE 3. Numbers of hermit crabs occupying various species of shells, collected from the littoral zone of San Nicolas Island, California. Species of shell P. samuelis P. hirsutiusculus Acanthina spirata 20 5 Olivella biplicata (95.7%) Tegula fuucbralis 154(72.3%) 5 small crabs Litiorina sp. (both) 13 small crabs 5 small crabs Norissia norrisii 19 0 Other species of shells 6 0 Total number of crabs

6 348 ERNST S. REESE shells of these two species and another species, Pagurus granosimanus, and Reese (1962a) studied the behavior for shellselection of all three species. It is apparent that the distributional pattern of hermit crabs in the intertidal habitat is dependent on a complex of interacting factors. Of foremost importance is species membership and the geographical location of the populations. Species membership and geographical location determine the macro-environment and distributional pattern, while photoperiod, migration, aggregation, and dispersal interact to determine the micro-distribution within the larger, overall pattern. Of course, physiological tolerances to environmental extremes of temperature, salinity, and desiccation are of great importance, especially in those species and environments where the extreme conditions cannot be avoided or lessened by behavior. This relationship is discussed below. THE SHELL AS A MICROHABITAT If the use and selection of shells is viewed as a form of selection of habitat, then its evolutionary and ecological significance become evident. The degree of importance of this behavior is reflected in the many specific patterns of behavior related to it, e.g., those related to social behavior (Hazlett, 1966a, b, 1967, 1968 a, b, c, d; Hazlett and Bossert, 1965; Reese, 1962b) and to selection of shell (Reese, 1962a, 1963). Based on field observations in Bermuda, Provenzano (1960) suggested that availability of shells may be a limiting factor for some species of hermit crabs, and I believe that this is the case for Calcinus seurati in Hawaii. Availability of shells is affected by both their abundance in the particular habitat and inter- and intraspecific competition for shells. Bollay (1964) found that more eggs were carried by larger female Pagurus samuelis in California. Thus, when large shells are not available to a population of crabs, large individuals are excluded from the population, and the reproductive potential of the population is reduced. Frequently, as was described above (see also Bollay, 1964; Volker, 1967), the species of shells which are most often used by hermit crabs in a given population are also those of the most abundant gastropods in the habitat. This picture is modified, however, by species-specific shell preferences (Reese, 1962a; Grant, 1963; Orians and King, 1964; Volker, 1967) and, of course, by competition for shells within and between species (Hazlett, 1967, 1968a; Reese, 1961, 19626). In addition, many investigators have noted that smaller crabs occur in a greater variety of shells and have a greater variety of shells to choose from than do larger crabs (Jackson, 1913; Rabaud, 1941; MacKay, 1945; and others). As a microhabitat, the shell must serve a number of functions besides simply being a place to live. That it serves an important function in the social structure of hermit crabs is obvious from the studies mentioned above on selection of shell and particularly from the extensive studies of social behavior by Hazlett (pp. cit.). Other functions of the shell have been less well documented. One suspects that it would help to reduce predation and desiccation, the latter in intertidal and terrestrial species. Although its role would seem to be less direct in meeting the problems of tolerating extremes of temperature and salinity, it is important that the shell can be carried about, thereby permitting the crabs to avoid these extreme conditions by moving away from them. I would like to comment on each of these ecological functions of the shell. PREDATION Although there are insufficient data to determine the extent to which the behavior of living in shells protects hermit crabs from predation, the shells do apparently provide some protection. Decapod crustaceans are an important source of food for fishes in California tidal pools, e.g., Gibbonsia elegans and G. metzi (Mitchell,

7 ADAPTATIONS OF HERMIT CRABS FIG. 2. The xanthid crab, Eriphia sebana, a conspicuous inhabitant of the supralittoral fringe at Eniwetok Atoll in the Marshall Islands, was observed breaking away the heavy outer lip of a shell of Turbo argryostomus which contained the hermit crab, Coenobita perlatus. cance of the shell with respect to predation is not settled, the limited data available suggest that the shell does reduce predation by all but the most highly specialized predators such as crabs of the genus Calappa. DESICCATION When exposed to air, intertidal hermit crabs can respond in a number of ways. First, they can simply "take it or die." Thus, species distributed higher in the littoral zone are able to withstand desiccation and insolation better than species distributed lower in the same intertidal environment. This is true for Pagurus samuelis in California (Bollay, 1964), for a number of species in the Caribbean (Pearse, 1929), and on the basis of preliminary work, for Clibanarius zebra, in Hawaii. Second, the crabs can withdraw into their shells to varying degrees and thereby control the rate of evaporation and desiccation. At Eniwetok, when exposed to air at times of low tide, the behavior of Calcinus laevimanus and Clibanarius corallinus depends on whether it is night or day. During the day when the effects of exposure to air are augmented by insolation, the crabs withdraw deeply into their shells, often with the aperture of the shell pointing upward (Fig. 3). At night the crabs also 1953), and Gobiesox maeandricus (G. Arita, pers. comm.), as well as some surf perches such as Rhacochilus vacca (J. Quast, pers. comm.), but hermit crabs which are abundant in these habitats are relatively rare in the stomachs of these fishes. The same relationship seems to hold between predatory fishes and hermit crabs associated with coral reefs. In contrast to the relatively large numbers of hermit crabs in the habitat (Orians and King, 1964), hermit crabs were only occasionally found in the stomachs of reef fishes (Hiatt and Strasburg, 1960; Randall, 1967). Reeder (1951), Meyerriecks (1965), and Recher (1966) have pointed out the importance of intertidal organisms in the diets of shore birds. Again, although hermit crabs are abundant in the habitat, they were not found in any of the bird stomachs sampled. Other decapod crustaceans were, however, especially the sand crab, Emerita analoga. The remains of Pachygrapsus were found in the snowy plover, Charadrius nivosus, and of another grapsid crab, Hemigrapsus, in the western willet, Catoptrophorus semipalmatus. In contrast, shells may offer little protection to hermit crabs from predation by crabs of the genus Calappa. Shoup (1968) described the specialized structures and behavior of these crabs which enable them to break into gastropod shells and eat the inhabitant, whether mollusc or hermit crab. Octopuses, too, may be highly effective predators on hermit crabs (Boycott, 1954), and I have observed the xanthid crab, Eriphia sebana, breaking away the very heavy outer whorl of a shell of Turbo argyrostomus presumably to eat the resident hermit crab, Coenobita perlatus (Fig. 2). Where predation is slight, one might expect that the shell would be less important to a hermit crab, particularly a subtidal species, and indeed, MacGinitie (1955) observed that large individuals of Pagurus splendescens at Point Barrow, Alaska, used very small shells which covered only the tips of their abdomens, even though larger empty shells were available. Although the adaptive signifi-

8 350 ERNST S. REESE like middle and inner portion of the reef-flat. The coral rubble of the beach marks the supralittoral fringe and zone. Along the right border of the picture is seen the end of the asphalt apron of the air strip. The distance from shore to algal ridge is approximately 200 feet at this point. pull into their shells, frequently with the aperture upward, but the degree to which they withdraw is much less. In the case of the terrestrial hermit crabs, there can be little doubt that the shells serve an important function in reducing desiccation. Seurat (1904) noted that Coenobita perlatus carries a small reservoir of water in the basal whorl of its shell, and if the shell wears away so that there is a hole in this region the shell is no longer suitable and is discarded. The glaucothoes and juveniles of the coconut crab, Birgus latro, live in shells like ordinary hermit crabs. From laboratory studies it was concluded (Reese, 1968a) that the adaptive value of retaining the behavior of living in shells by these early stages primarily was to protect the glaucothoes from desiccation when they emigrate from the sea to begin their life on land. These same laboratory-reared crabs, now almost three years old and no longer living in shells, differ strikingly in two aspects of their behavior from Coenobita perlatus and C. brevirnanus living in the laboratory without shells. The small Birgus are strongly nocturnal, being particularly active in the early evening, and they are extremely fossorial, extensively digging up their terraria and hiding in deep burrows during the day. Coenobita, on the other hand, even without shells under experimental conditions, is active periodically throughout the day and night and, although it crawls under and into things during periods of inactivity, it only digs extensive burrows when it buries itself preparatory to molting. These observations in the laboratory agree with field studies in the Marshall Islands. I suggest that the differences in behavior between Birgus and Coenobita are related to the loss of the shell-inhabiting behavior in adult Birgus. Why young Birgus stop living in shells FIG. 3. A and B. Shells oe Calcinus laevimanus and Clibanarius corallinus are seen in the apertureup position at low tide on the reef-flat oc Eniwetok Atoll, Marshall Islands. C. View of the seaward reef-flat at Eniwetok with the algal ridge at the top of the picture. Many shallow tidal pools can be seen on the pavement-

9 ADAPTATIONS OF HERMIT CRABS 351 when still much smaller than adult Coenobita is not clear; however, by assuming the adult pattern of being nocturnal and fossorial and thereby obviating the need for a shell, they have taken themselves out of competition with Coenobita in at least one important aspect of their ecology. I believe that the same avoidance of competition explains why Pagurus hirsutiusciilns prefers species of shells which are not preferred by species with which it is sympatric (Reese, 1962«), and with which it cannot successfully fight for shells (Reese, 1961). The third and final pattern of response is for the hermit crabs to avoid the adverse condition by moving away from it. For example, crabs can avoid desiccation by following the receding tide, as Calcinus laevimanus does to a limited extent in Hawaii and Clibanarius cubensis does in the Caribbean (Hazlett, 1966a). The crabs may also aggregate beneath rocks as the tide recedes, thereby gaining protection from the sun as well as concentrating in a moist location. This is probably a pattern of behavior found in most species of hermit crabs living in supralittoral zones. Hazlett (1966a) reported it for Caribbean species, and it is pronounced in both Clibanarius corallinus and C. zebra in the Pacific. There may be more than a hundred small C. zebra in an aggregation under a rock or broken chunk of coral (MacKay, 1945). TEMPERATURE AND SALINITY Since the physical factors of exposure to air, sun, temperature, and salinity are continuously interacting in the environment, the avenues of response open to intertidal hermit crabs undergoing desiccation also apply to meeting extreme conditions of temperature and salinity. Although hermit crabs may crawl out of very warm tidal pools, as I have observed for Calcinus laevimanus and Clibanarius corallinus, and thereby avoid the extreme temperature, it seems that species living in the supralittoral zone of tropical shores are well adapted to withstand temperatures for short periods of time at least as high as occur in the natural environment. At Tortugas, Florida, Pearse (1929) observed Calcinus sulcatus in tidal pools in which the temperatures were between C, and recently Glynn (1968) reported mass mortalities of a number of reef-flat invertebrates in Puerto Rico when temperatures in tidal pools went to 40 C. Hermit crabs, however, were not mentioned by Glynn and presumably were not killed by these extremely high water temperatures. Or, perhaps they crawled out of the pools, as the hermit crabs tend to do on the reef-flat at Eniwetok when tidal pools reach temperatures of C. I have seen crabs active in small high pools with a temperature of 38 C, so even this temperature can be tolerated for at least short durations. One may speculate that hermit crabs which have apparently crawled out of the warm tidal pools and are now quiescent in the aperture-up position (Fig. 3) are able to control evaporative water loss and thus exert some control over their temperature and rate of desiccation by moving their bodies within the shells. In most species of hermit crabs the chelipeds and walking legs can be held to form a very effective "operculum" for the aperture of the shell. Magnus (1960) described this in detail for Coenobita scaevola which lives along the arid shores of the Red Sea. The crabs could either block the entrance to the shell to prevent water loss, or they could control evaporative loss of water by exposing their moist cephalothorax and pereiopods. Vernberg (1967) reported that the temperature tolerance of Pagurus longicarpus depends on its thermal history. Preliminary laboratory studies by Charles K. Barry on three species of Hawaiian hermit crabs indicate that the lethal temperature for Calcinus latens is between 38 and 40 C, depending on the rate of increase in temperature, while that for both C. laevimanus and C. seurati, which are distributed higher in the littoral zone (Table 2), is somewhat higher (40 to 43 C), as one might expect. Additional data are needed because samples were small (N = 5

10 352 ERNST S. REESE for each species and each condition). Motor activity increased with increasing temperature, as the crabs, confined to the experimental chambers, tried to escape the intolerable condition. An unusual behavioral pattern which we have seen many times in a number of species is that a dying hermit crab abandons its shell. The significance of this behavior is immediately evident if one recalls that the availability of the preferred species and size of shells probably is an important limiting factor on the size of many populations of hermit crabs. Although I do not know of any data on salinity-tolerances of hermit crabs other than the studies by Gross (1963, 1964) on salt and water balance in terrestrial hermit crabs, I would expect that the general pattern of adaptations would be similar to those described above for desiccation and temperature. MOVEMENT AND RHYTHMIC BEHAVIOR In nature, animals are active periodically, often rhythmically, based on the photoperiod or tidal cycle. I have cited examples of directed movements of hermit crabs to feed, to aggregate or disperse, and to escape from adverse conditions. Movements related to reproductive behavior [e.g., terrestrial hermit crabs must release their eggs into the sea (Reese and Kinzie, 1968) ] also occur. Fiddler crabs show similar behavior, and Barnwell (1963, 1968) and Herrnkind (1968) emphasized the importance of rhythmic and directionally oriented behavior as basic to their existence. Thompson (1903, p. 151) noted that Pagurus longicarpus "is crepuscular and during the day a majority of individuals remain buried in the sand or congregated in the shade." Besides the examples given above, Hazlett (1966a) observed rhythmic activity in a number of other Caribbean species of hermit crabs. Grant (1963) concluded that Pagurus acadianus was an extremely errant species because the population in his study area fluctuated so greatly. Rebach (1968) found that P. longicarpus tends to orient towards its home direction and that the movements are influenced by a simple sun-compass, the slope of the bottom, and chemical cues in the water. Orians and King (1964) were impressed with the rates of invasion into tidal pools from which Pagurus samuelis and P. hirsutiusculus had been removed. This rapid dispersal into vacant habitats suggests that the populations were at or near the carrying capacity of the environment, since high density or crowding leads to an increase in agonistic encounters in hermit crabs (Hazlett, 1968&) and other animals (Bovbjerg, 1964), and aggression is generally believed to stimulate dispersal into all available habitat space. Clearly, all of these movements and activities are adapted to the survival of the species. NEW APPROACHES TO OLD PROBLEMS Throughout this paper I have given many examples of different genera and species of hermit crabs living in different biotopes of the intertidal environment. There seems to be a direct relationship between environmental complexity and diversity of species although this was not measured or considered at the time the data were collected. Kohn (1967), however, was able to demonstrate this relationship in the gastropod genus, Conus, based on numbers of species found in each of three different types of Pacific reef-flat environments. He concluded that complexity of habitat is an important determinant of diversity of species. Intuitively, it seems that in more complex environments, such as the reef-flat, there would be more niches available for exploitation, but the problem lies in the difficulty of measuring an ecological niche. I feel that Root's (1967) hypothetical exploitation curve (Fig. 4) and the guildconcept have important applications to the problems faced by the ecologist and ethologist interested in adaptations of marine animals to their environments. Root defined a guild as "a group of species that exploit the same class of environmental

11 ADAPTATIONS OF HERMIT CRABS 353 HYPOTHETICAL EXPLOITATION CURVE (after Root, 1967) ENVIRONMENTAL VARIABLE SPECIALIZATION (Interspecific competition) FIG. 4. The curve (Root, 1967) shows the frequency of exploitation of an environmental variable, e.g., the frequency that different species or size-classes of shells are used by a species of hermit crab. resources in a similar way... without regard to taxomonic position." Ecological needs rather than membership in a taxon are relevant to the problem. Thus it is important, I think, to view intertidal hermit crabs as "guild-members" rather than in terms of this or that genus. Probably most intertidal hermit crabs could be grouped in the "benthic detritus-feeding guild", and ecologically, guild-membership means that the various species can be compared at least along one aspect of their niche-requirements. Based on known preferences for shells, species could be grouped into "shell-preference guilds", e.g., the "turban-like shell guild" as opposed to the "olive-like shell guild." In this way, each species would belong to a number of guilds each relating to an important environmental variable. The hypothetical exploitation curve (Fig- 4) shows the way in which the exploitation of each environmental variable may be viewed. Thus, if there were interspecific competition for turban-like shells, then one would expect that preferences for species of shells and exploitation of these species would be very well defined between guild-members. As more and more data of this type accumulated, one would hope that an increasingly clearer picture of the requirements of the various species for a niche would emerge. CONCLUSION Two points seem pre-eminent. First, the shell is a movable object, and therefore, unlike burrow-inhabiting animals such as the fiddler crabs, hermit crabs can exploit environments such as rocky intertidal habitats and reef-flats in which burrowing is relatively difficult, as well as habitats characterized by soft substrata. Within these environments hermit crabs have augmented or even replaced physiological tolerances, avoiding extreme conditions by either moving away from them, creating micro-climatic conditions within their shells, aggregating, or probably in many cases doing all of these. Shells also seem effective in reducing predation. In short, the shell provides all the advantages of a burrow without any of its restrictions. Thus, the hermit crabs are an extremely successful group of intertidal animals, so successful that they have been able to invade the terrestrial environment, where on many tropical islands they are one of the most conspicuous members of the biota. The second point is that the hermit crabs are an extremely diverse and often specialized group affording an almost infinite variety of opportunities for research. REFERENCES Alcock, A Catalogue of the Indian decapod Crustacea in the collection of the Indian Museum. Part II. Anomura. Fasc. I. Pagurides. Calcutta. 197p. Barnes, H., and E. S. Reese Feeding in the pedunculate cirripede Pollicipes polymerus Sowerby. Proc. Zool. Soc. London 132: Barnes, H., and E. S. Reese The behavior of the stalked intertidal barnacle Pollicipes polymerus Sowerby, with special reference to its ecology and distribution. J. Animal Ecol. 29: Barnwell, F. H Observations on daily and tidal rhythms in some fiddler crabs from equatorial Brazil. Biol. Bull. 125: Barnwell, F. H The role of rhythmic systems in the adaptation of fiddler crabs to the intertidal zone. Am. Zoologist 8: Bliss, D. E Transition from water to land in decapod crustaceans. Am. Zoologist 8: Bollay, M Distribution and utilization oe gastropod shells by the hermit crabs Pagurus samuelis, Pagurus granosimanus, and Pagurus

12 354 ERNST S. REESE hirsutiusculits at Pacific Grove, California. Veliger (Suppl.) 6: Boltt, R. E Antennary feeding of the hermit crab, Diogenes brevirostris Stimpson. Nature 192: Bovbjerg, R. V Dispersal of aquatic animals relative to density. Verh. Int. Ver. Limnol. 15: Boycott, B. B Learning in Octopus vulgaris and other cephalopods. Pubbl. Staz. Zool. Napoli 25: Edney, E. B Transition from water to land in isopod crustaceans. Am. Zoologist 8: Efford, I. E Aggregation in the sand crab, Emerita analoga (Stimpson). J. Animal Ecol. 34: Efford, I. E Feeding in the sand crab, Emerita analoga (Stimpson) (Decapoda, Anomura). Crustaceana 10: Forest, J., and M. de Saint Laurent Campagne de la Calypso au large des Cotes Atlantiques de L'Amerique du Sud ( ). I. 6. Crustaces Decapodes: Pagurides. Res. Sci. Camp. "Calypso", 8. Ann. Inst. Ocean. 45: Glynn, P. W Mass mortalities of echinoids and other reef-flat organisms coincident with midday, low water exposures in Puerto Rico. Marine Biol. 1: Gordon, J A bibliography of pagurid crabs, exclusive of Alcock, Bull. Am. Mus. Nat. Hist. 108: Grant, W. C, Jr Notes on the ecology and behavior of the hermit crab, Pagurus acadianus. Ecology 44: Gross, W. J Cation and water balance in crabs showing the terrestrial habit. Physiol. Zool. 36: Gross, W. J Water balance in anomuran land crabs on a dry atoll. Biol. Bull. 126: Hazlett, B. A. 1966a. Social behavior of the Paguridae and Diogenidae of Curacao. Studies Fauna Curacao and other Carib. Islands 23: Hazlett, B. A. 1966b. Factors affecting the aggressive behavior of the hermit crab Calcinus tibicen. Z. Tierpsychol. 6: Hazlett, B. A Interspecific shell fighting between Pagurus bernhardus and Pagurus cuanetisis (Decapoda, Paguridea). Sarsia 29: Hazlelt, B. A. 1968a. Dislodging behavior in European pagurids. Pubbl. Staz. Zool. Napoli 36: Hazlett, B. A Effects of crowding on the agonistic behavior of the hermit crab, Pagurus bernhardus. Ecology 49: Hazlett, B. A. 1968c. The sexual behavior of some European hermit crabs (Anomura: Paguridae). Pubbl. Staz. Zool. Napoli 36: Hazlett, B. A. 1968d. Size relationship and aggressive behavior in the hermit crab Clibanarius viltalus. Z. Tierpsychol. 25: Hazlett, B. A., and W. H. Bossert A statistical analysis of the aggressive communications systems of some hermit crabs. Animal Behaviour 13: Herrnkind, W. F Adaptive visually-directed orientation in Uca pugilator. Am. Zoologist 8: Hiatt, R. W., and D. W. Strasburg Ecological relationships of the fish fauna on coral reefs o the Marshall Islands. Ecol. Monogr. 30: Hurley, D. E Transition from water to land in amphipod crustaceans. Am. Zoologist 8: Jackson, H. G Eupagurus. Proc. Trans. Liverpool Biol. Soc. 27: Kohn, A. J Environmental complexity and species diversity in the gastropod genus Conus on Indo-west Pacific reef platforms. Am. Naturalist 101: MacGinitie, G. E., and N. MacGinitie Natural history of marine animals. McGraw-Hill Book Co. New York. 473 p. MacGinitie, G. E Distribution and ecology of marine invertebrates of Point Barrow, Alaska. Smithsonian Misc. Collections 128: MacKay, D. C. G Notes on the aggregating marine invertebrates of Hawaii. Ecology 26: Magnus, D. B. E Zur Okologie des Landeinsiedlers Coenobita jousseaumei Bouvier und der Krabbe Ocypode aegyptiaca Gerstaecker am Roten Meer. Verh. Deut. Zool. Ges. Bonn/Rhein, 1960, Magnus, D. B. E t)ber das "Abweiden" der Flutwasseroberflache durch den Schlangenstern Ophiocoma scolopendrina (Lamarck). Verh. Deut. Zool. Ges. Wien, 1962, Magnus, D. B. E Gezeitenstromung und Nahrungsfiltration bei Ophiuren und Crinoiden. Helgol. Wiss. Meeresunters. 10: Mitchell, D. F An analysis of stomach contents of California tide pool fishes. Am. Midland Naturalist 49: Moulton, J. M Intertidal clustering of an Australian gastropod. Biol. Bull. 123: Meyerriecks, A. J Ring-billed gulls gorge on fiddler crabs. Wilson Bull. 77: Orians, G. H., and C. E. King Shell selection and invasion rates of some Pacific hermit crabs. Pacific Sci. 18: Pearse, A. S Observations on certain littoral and terrestrial animals at Tortugas, Florida, with special reference to migrations from marine to terrestrial habitats. Carnegie Inst. Wash., Dept. Mar. Biol., Papers Tortugas Lab. 26: Provenzano, A. J., Jr Notes on Bermuda hermit crabs (Crustacea; Anomura). Bull. Mar. Sci. Gulf Carib. 10: Provenzano, A. J., Jr Biological investigations of the deep sea. 37. Lithopagurus yucatanicus, a new genus and species of hermit crab with a distinctive larva. Bull. Mar. Sci. 18: Rabaud, E Recherches sur l'adaption et le

13 ADAPTATIONS OF HERMIT CRABS 355 comportement des pagures. Arch. Zool. Exptl. Gen. 82: Randall, J. E Food habits of reef fishes of the West Indies. Studies Tropical Oceanogr., No. 5: Rebach, S Orientation and movements of the hermit crab, Pagurus longicarpus. Bull. Ecol. Soc. Am. 49: Recher, H. F Some aspects of the ecology of migrant shorebirds. Ecology 47: Reeder, W. G Stomach analysis of a group of shorebirds. Condor 53: Reese, E. S Inter- and intraspecific dominance relationships of sympatric species of intertidal hermit crabs. Am. Zoologist 1:382. Reese, E. S. 1962a. Shell selection behaviour of hermit crabs. Animal Behaviour 10: Reese, E. S >. Submissive posture as an adaptation to aggressive behavior in hermit crabs. Z. Tierpsychol. 19: Reese, E. S The behavioral mechanisms underlying shell selection by hermit crabs. Behaviour 2k Reese, E. S. 1968a. Shell use: an adaptation for emigration from the sea by the coconut crab. Science 161: Reese, E. S. 1968b. Annual breeding seasons of three sympatric species of tropical intertidal hermit crabs, with a discussion of factors controlling breeding. J. Exptl. Mar. Biol. Ecol. 2: Reese, E. S., and R. A. Kinzie, III The larval development of the coconut or robber crab liirgus latro (L.) in the laboratory (Anomura, Paguridea). Crustaceana, Suppl. 2: Roberts, M. H., Jr Functional morphology of mouth parts of the hermit crabs, Pagurus longicarpus and Pagurus pollicaris. Chesapeake Sci. 9:9-20. Root, R. B The niche exjjloitation pattern of the blue-gray gnatcatcher. Ecol. Monographs 37: Russell, E. S The diversity of animals, an evolutionary study. Bibliotheca Uiotheoretica 9:151p. Seurat, L. G Observations biologiques sur les Cenobiies (Cenobila perlata, Edwards). Bull. Mus. Hist. Nat. Paris 10: Shoup, J. B Shell opening by crabs of the genus Calappa. Science 160: Thompson, M. T The metamorphoses of the hermit crab. Proc. Boston Soc. Xat. Hist. 31: Vernberg, ]. F Some future problems in the physiological ecology of estuarine animals, p In G. H. LaufE, fed.], Estuaries. AAAS Publ. 83, Washington, D. C. 757p. Volker, L Zur Gehausevvahl des Land- Einsiedlerkrebses Coenobita scaevola Forskal vom Roten Meer. J. Exptl. Mar. Biol. Ecol. 1: Warburg, M. R Behavioral adaptations of terrestrial isopods. Am. Zoologist 8:

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