STUDIES ON THE FAUNA OF CURAÇAO AND OTHER CARIBBEAN ISLANDS: No. 88. Social behavior of the Paguridae and Diogenidae of Curaçao by Brian A. Hazlett (Biological Laboratories, Harvard University) INTRODUCTION 1 Collecting areas on Curafao 6 Relationships of the hermit crabs studied 7 SOCIAL BEHAVIOR OF HERMIT CRABS IN GENERAL 9 DESCRIPTIONS OF BEHAVIOR PATTERNS 18 Clibanarius tricolor 18 Clibanarius antillensis 38 Clibanarius cubensis 41 Clibanarius vittatus 45 Calcinus tibicen 47 Paguristes cadenati 57 Paguristes grayi 60 Pagurus miamensis 63 Pagurus pygmaeus 72 Pagurus bonairensis 76 Pagurus marshi 82 Pylopagurus operculatus 86 EXPERIMENTAL ANALYSES OF HERMIT CRAB BEHAVIOR 90 Aggression 90 Diel variation 90 Dominance orders 90 Shell-fighting 102 Analyses of stimuli 104 Visual stimuli 104 Chemical stimuli Ill Tactile stimuli 115 DISCUSSION 120 SUMMARY 138 LITERATURE 140 INTRODUCTION The number of unanswered questions and untouched problems This is in the study of animal behavior is very large. particularily true in the sub-discipline of animal communications. The fact that the behavior of one animal can change the behavior of a second animal is too often only tacitly implied or stated without amplifi- cation. Before the of be studied "language" any organism can as behavioral the of a phenomenon or communications systems a phylogenetic series studied as an evolutionary phenomenon, it is that the basic behavioral of the essential biology species or group examined work be and described. The present is an attempt to fulfillthis latter requirement. The social behavior of the marine hermit crabs (Paguridae and Diogenidae) of Curasao, N.A., is described and in part analyzed. In addition to providing this basis, data have been gathered, which upon analysis have elucidated certain features of the aggressive communications systems of eight species of hermit crabs. From the data gathered, the following aspects of hermit crab behavior are described: the behavior patterns of these crustaceans, as observed under laboratory and field conditions, the results of a number of experimental analyses of behavioral stimuli, and the of of results some preliminary investigations dominance hierarchies. behavior of hermit crabs has little The social taken very space in zoological literature. However, much has been written about the behavior and physiology of individual crabs from the viewpoint 3 of shell habitation (see REESE 1962a, 1963), neurophysiology STIEVE (ALEXANDROWICZ 1952, 1963), sensory physiology (BOHN 1902, GOLDSMITH 1918, BROCK 1927, ROLLER 1927, TEN CATE 1930, and others), symbiotic relationships (BROCK 1927, BRIGHTWELL 1951, 1953, BERNER 1953) and feeding behavior (ORTON 1927, of BROCK 1930). JACKSON (1913) produced a rather good study general anatomy and biology as did MAKAROV (1938) in his intro- ductionto a systematic treatmentof the Russian Paguridae. BOUVIER (1892) and BOHN (1903) briefly mentioned that hermit crabs do themselves for shells. ALLEE & DOUGLIS fight among (1945) observed that specimens of Pagurus longicarpus fight one another for shells and that there was a dominance order in this fighting, crabs extracted smaller crabs. Their obser- insofar as larger always vations were confined mostly to interactions in which one individual was without a shell. They observed that the aggressive (shell-less) crab "grasps the chelae and the legs of the occupant with one of its large pinchers jerks quickly, and so removes the smaller crab, and often throws it some distance away." REESE (1962b) carried out more extensive observations of shell fights between individuals but of crabs of Calcinus laevimanus, again, one the interacting was artificially shell-less. Reports of sexual behavior also have been few. MATTHEWS (1959) suggested that copulation in Pagurus prideauxi is not necessarily confined to the short period following female ecdysis. He found the spermatophores on immature females, outer cuticular membrane of living, embryonated ova attached to the pleopods and on imma- ture males. MATTHEWS attributed this diversity of recepients of spermatophores to "indiscrimination of the part of the male [which] proposes he may copulate with any hermit crab of his species that he can physically overpower." MACGINITIE & MAC- GINITIE (1949) and MATTHEWS (1956) mention that male hermit crabs are sometimes seen dragging females about prior to copulation. BOTT (1940) reported that in Pagurus prideauxi, a male remains with the female during the period of moulting and until egg laying. BRANDES (1897) mentioned that the male P. prideauxi holds the tarsal segment of the second right ambulatory leg of the female with his left cheliped prior to copulation. BRANDES observed that 4 the is held the during copulation, major cheliped over female (in a protective fashion) as they both ease partially out of their shells. COFFIN (1960) noted that the male Pagurus samuelis held the shell of the with his minor for number of female cheliped a hours prior to the one-second long copulation. The male waved the shell of the female back and forth, bumping it against his shell his and shell while or body and/or twisting body pressing against the shell of the female. During copulation, both eased out until only 2/3 of their abdomens remained in their shells. KAMALVENI (1949) reported on the copulation of Clibanarius olivaceous. How- ever, the observed pairs were without shells artificially and their minute with ambulatories have been 90 pairing, intertwining may aberrant. He also stated that recently moulted females generally attracted the attention of but details. males, gave no Although the literature pertaining directly to the social behavior of hermit crabs is limited, many of the phenomena mentioned in this paper have been observed in other crustaceans. DOUGLIS (1946) reported straight-line dominance orders in the lobster, Homarus americanus. BOVBJERG (1953, 1956) and LOWE (1956) have investigated the development of aggression and straight-line dominance orders in several species of crayfish. Both size and sex, predominantly the former, were found to be factors in determining the order in a hierarchy. Although many authors have mentioned that members of a given crustacean species may fight with conspecific individuals, the is described the manner of fighting usually not nor signal-display level of aggression recognized. One notable exception has been the work of CRANE (1941a, 1943, 1957, 1958) and others on the conspicu- ous movements of the major cheliped of male fiddler crabs, Uca species. CRANE has observed that these courtship movements signal territory holding to other males and thus tend to keep them from intruding. In additon, CRANE (1958) has described a number of displays in Uca maracoaniwhich she believes act as communicatory signals to conspecific individuals concerning the psycho-physiological stateof the displaying crab. Another groupin which a signal-display level of aggressive communication has been recognized is the snapping shrimp, Alpheus and Synalpheus (HAZLETT & WINN 1962). 5 Both the of the claw and the of sight open snapping jet water produced by a "snap", act as retreat-causing stimuli, thereby avoiding actual physical contact between interacting individuals. without individuals Physical combats damage are frequent among of the common shore crab, Pachygrapsus crassipes (HIATT 1948, BOVBJERG 1960) and the grapsoid crab, Dotilla mictyroides (TWEEDIE 1950). ALCOCK (1892) and CRANE (1941b) reported that burrow- occupying Ocypode crabs produce a twittering sound when an intruding conspecific individual enters its burrow. Presumably, substrate detection of this sound tends to induce retreat in the intruder. The of males presence of chemical attraction and/or excitation by ripe females has been supposed for a number of lower crustaceans - Pandalus danae (NEEDLER 1931), P. borealis (CARLISLE 1959), Palaemonetesvulgaris (BURKENROAD 1947), Leanderserratus (FORSTER 1951), Crangon crangon (NOUVEL 1939), Orchestia gammarella - for (WILLIAMSON 1954) but proven none. A wide-spread charac- is restriction of time teristic among crustaceans the when mating takes place. In the great majority of species investigated, copulation is restricted to a short period following a female moult - Cancer pagurus and Carcinus maenas (WILLIAMSON 1902) and Neptunus pelagicus (CHHAPGAN 1956). Often the male crab carries the female about for hours or days prior to her moulting, probably to assure that he is present when she is ready to mate - Carcinus maenas (BROEKHUYSEN 1937), Callinectes hastatus (CHIDESTER 1911) and Gammarus pungens (HOMES 1903). The author wishes his Dr. E. O. WILSON for his to express gratitude to guidance, aid and advice in connection with all phases of this work, and to Dr. W. H. BOSSERT for his with mathematical in of Harvard University assistance problems and pro- gramming the computer-analyzed portions of this study. In addition, thanks are given to Dr. A. J. PROVENZANO, Jr., of the University of Miami, for confirmation of species identification, to Dr. INGVAR KRISTENSEN and the staff of the Carai'bisch Marien-Biologisch Instituut (Caribbean Marine Biological Institute) in Cura9ao, N.A., for their aid and hospitality, and to Miss JOANNE HELSBERG for aid in the preparation of the text. I also wish to thank the National Science Foundation, whose training grant in evolutionary biology, administered by the Department of Biology of Harvard University, was the source of travel and facility funds that made this work possible. Part of this research was carried