Reproductive Behavior of the Hermit Crab <I>Clibanarius Vittatus</I
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BULLETIN OF MARINE SCIENCE. 58(3): 668-674, 1996 REPRODUCTIVE BEHAVIOR OF THE HERMIT CRAB CLIBANARIUS VI1TATUS (BOSC, 1802) Brian A. Hazlett ABSTRACT The precopulatory behavior patterns of the common intertidal hermit crab Clibanarius vittatus are described. Males precopulatory movements involve rotation of the female with the ambulatory legs and tapping lightly with one or both chelipeds in the aperture of the female's shell. Bouts of these courtship patterns alternate with period of guarding in which the female is held by the male's ambulatory legs with her shell aperture against the substrate. Females that copulated were not soft from a recent moult and brought out a new batch of eggs in less than an hour following copulation. Male-male competition for access to females was intense. The results of experiments demonstrated that courted females give off a pher- omone that stimulates male reproductive activity. Males occupying the sinistrally-spiralled shells of Busycon contratrium (Conrad, 1840) were at a distinct disadvantage in obtaining matings. Descriptions of the reproductive behaviors of animals have often been used for comparative purposes (Ridley, 1983) and the precopulatory behavior of a number of species of hermit crabs have been described (Hazlett, 1966, 1972, 1975). The reproductive behavior patterns of some members of the genus Clibanarius have been analysed both descriptively and to· some extent experimentally, e.g., C. tri- color and C. antillensis from the Caribbean (Hazlett, 1966) and C. zebra from Hawaii (Hazlett, 1989). However, none of the larger species of Clibanarius have been well described with regards to their precopulatory behavior. Existence of pheromones given off by one sex and detected by members of the other sex have been known for some decapods for a number of years (Ryan, 1966). However, clear evidence for a sex pheromone in hermit crabs has been lacking. Absence of a category of information in a major group of decapods, especially one that is reasonably well studied, might suggest something unusal about the courtship behavior of this group. In earlier studies of the mating behavior of hermit crabs it was suggested that the shape of the gastropod shell a male crab occupies could have strong effects on male mating success in some species. Crabs which are shell generalists, i.e., occupy a variety of shell species, had greatly reduced mating success in some shell types but this was not the case for crabs which were shell specialists (Hazlett, 1989; Hazlett and Baron, 1989). This suggestion of differences in resource use on reproductive behavior was based upon a limited number of crab species. The striped-legged hermit crab, Clibanarius vittatus is both common and geo- graphically wide-spread, occurring intertidally from Virginia, U.S.A., to Brazil (Young and Hazlett, 1978). It is an important member of the intertidal community in many areas and many aspects of its behavioral biology have been studied including: aggressive interactions (Hazlett, 1966, 1968a, 1974; Hazlett and Bos- sert, 1965), movements patterns (Fotheringham, 1975; Hazlett, 1981), responses to odors (Hazlett, 1968b, 1982; Katz and Rittschof, 1993), and shell utilization (Brooks and Mariscal, 1985; Fotheringham, 1976; Hazlett and Hermkind, 1980). Despite the number of papers on its behavior and behavioral ecology, the mating behavior of C. vittatus was observed on only one occasion (Hazlett, 1966) and has not been adequately described or characterized. The following observations and experiments were carried out in order to more 668 HAZLEIT: HERMIT CRAB BEHAVIOR 669 carefully characterize the mating behavior and reproductive activity of this com- mon, large, intertidal crab. In addition, because definitive proof of reproductive pheromones in hermit crabs has been lacking, the possibility of a female phero·· mane was examined in this species. The effect of the species of gastropod shell a male hermit crab occupied on its reproductive behavior was also examined. METHODS Mating Behavior.-Observations were made of precopulatory behavior of C. vittatus in both the field and the laboratory during June 1994 at the Duke University Marine Laboratory, Beaufort, N.C. While precopulatory behaviors were seen frequently in the field, the descriptions of reproductive activity are based primarily on the behavior of animals observed in the laboratory. Animals were maintained in water tables (67 cm by 123 cm, water 10 cm deep) supplied with running sea water and the bottoms of the water tables were covered with about three centimeters of sand. Precopulatory behavior was first noted on 6 June but had become infrequent, even with freshly collected animals, by 26 June. Very few instances of precopulatory behavior and no copulations were observed during July despite many hours of observations. In most cases, following observation of copulation, pairs were removed from the water table, isolated, and size and reproductive features recorded. The latter included the molt state of the female (whether her exoskeleton was soft or not), the presence or absence of a spermatophore, and the presence or absence of new eggs on the female's pleopods. Female Pheromone.-The rapid increase in activity of known males when some females were added to a water table suggested the possibility of a female pheromone. To test for a water-born substance given off by females, the following procedure was used. At the end of a day's observations, females that had been courted by males (see below) but had not been observed copulating were placed in a bucket in a different water table and supplied with running sea water and kept overnight (source of female water). Five large males werc kept overnight in another water table. The next morning, the water supply to the 2-gallon bucket containing the females (N = 4-5 depending upon mating activity) was shut off for 1 h as was the water supply to the water table containing the test males. Five smaller males were added to the male water table at the beginning of the hour to serve as possible objects to be grasped by the test males. A 2-gallon bucket containing five males was set aside (source of malt: water). During the control period of 5 min, water was siphoned from the male-containing bucket into one end of the water table at the rate of 200 ml per min. Each water table was divided into six sections by lines on the side and the locomotory rate of the test males was recorded as the number of lines crossed. The other behaviors recorded for the test males were the number of seconds spent by jndi,· viduals within two centimeters of the end of the siphon and the number of times the test males grasped the smaller males with their walking legs. The size differences between the test and smaller males greatly reduced the possibility that grasps were related to shell-exchange behavior. Following the introduction of "male water", the same behavioral parameters were recorded as water from the bucket containing females was introduced. Five replicates of this experiment were carried out and the results analyzed with paired t-tests comparing mean values of behaviors during the introduction of male and female water. Shell Species Occupation.-Observations suggested that the occupation of the sinistrally-spiralled shell Busycon contrarium adversely affected reproductive behavior in males (see below). The shell species occupied by large, reproductively active males in the water tables were recorded every several days during the weeks of observation. As a pilot study, five individual males which were observed to copulate when occupying other species of shell were removed from their original shells and placed in B. contrarium shells of the appropriate size. They were replaced in the water tables being observed and their behavior was followed for 2-3 days. RESULTS Mating Behavior.-Mating activity was observed in the laboratory and in the field throughout June 1994. A number of matings (N = 10) and courtships (N =: 51) were seen during this month but during July only a very few courtship at·- tempts were observed. Thus this phase of reproductive activity seems to be quite constrained at least in the area around the Duke Marine Laboratory. Mating ac.. tivity was observed during both day and night although the majority of obser·- vations were made during the day. In most cases, the first indication of mating activity was the grasping of a 670 BULLETIN OF MARINE SCIENCE, VOL. 58, NO.3, 1996 female's shell by a male, The male initially got into an opposed position (Hazlett, 1966) with the female, the apertures of their shells facing one another. The male executed two types of behavior while holding the female in the opposed position: rotations and cheliped tapping. Rotations involved moving the female's shell from side-to-side in a figure eight fashion through an axis running dorso-ventrally through the aperture of the female's shell. The more common and persistent be- havior was cheliped tapping. The manus of the cheliped was held at a 90° angle to the carpus and the whole appendage moved up and down stiffly. Depending upon the relative size of the male to the female this involved either one or both chelipeds. If the male was not much bigger than the female both chelipeds of the male were raised and then quickly brought down simultaneously making light contact with the female's shell. The most common site "tapped" was the rim of the aperture of the female's shell, either just above or just below the aperture, partially in the aperture itself. If the male was somewhat larger than the female, such that both chelipeds could not easily fit in the aperture of the female shell, the male sometimes alternated single cheliped taps of the two chelipeds. In some cases, very large males persistently used just one cheliped or tapped primarily with just one or the other cheliped for a number of hours.