EFFECT OF MALE / FEMALE SIZE RATIO ON MATING BEHAVIOR OF THE HERMIT CRAB PAGURUS FILHOLI (ANOMURA: PAGURIDAE) UNDER EXPERIMENTAL CONDITIONS

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1 EFFECT OF MALE / FEMALE SIZE RATIO ON MATING BEHAVIOR OF THE HERMIT CRAB PAGURUS FILHOLI (ANOMURA: PAGURIDAE) UNDER EXPERIMENTAL CONDITIONS Shingo Minouchi and Seiji Goshima A B S T R A C T We studied the mating behavior and clarified the mating sequences of the hermit crab Pagurus filholi under laboratory conditions. The mating sequences differed, depending on the male to female size ratio. Before copulation, larger males relative to potential female mates tended to perform precopulatory guarding behavior, i.e., grasping the rim of the shell of the female with their chelipeds, more frequently than smaller males. On the other hand, smaller males relative to the females appeared to insert their chelipeds and to attempt copulation by pulling the female out of the shell without performing precopulatory mate-guarding behavior. These different behaviors may be conditional strategies that depend on the male/female size ratio. In order to clarify the mating system of a species, it is important to know its reproductive behavior. There have been many studies of the ways males search and obtain receptive females and of the ways females select their mate in various crab species. Published reports include studies of the effect of body size on mate choice in the grapsid crab Gaetice depressus (de Haan) (see Fukui, 1995), female choice and the breeding behavior of the fiddler crab Uca beebei Crane (see Christy, 1987), the effect of body size and ripeness of the females on male assessment of mates in the fiddler crab Uca tetragonon (Herbst) (see Goshima et al., 1996a), and the mating behavior of hermit crabs (Hazlett, 1966, 1970, 1972, 1996). Males often compete with other males to copulate with females. Males have high potential reproductive ability and there is strong evolutionary selection for traits and tactics involved in competing for and obtaining females (Krebs and Davies, 1993). There are various mating systems, not only between species, but also within populations of the same species. For example, the fiddler crab Uca lactea (de Haan) (see Murai et al., 1987; Goshima and Murai, 1988), and the sand-bubbler crab Scopirrcera globosa (de Haan) mate either on the surface of a tidal flat or below the surface in male-defended burrows, depending on their size (Henmi et al., 1993). In the shore crab Carcinus maenas (L.), males also use two different mating tactics, and the tactic chosen varies both temporally and spa- tially (Meeren, 1994). No studies, however, have examined the mating tactics of hermit crabs (Anomura). Precopulatory mate-guarding behavior occurs in many crustaceans (Ridley, 1983). In many cases, hard-shelled males carry premolt females for up to several days until they spawn, and mating occurs shortly after the female molts. Thus, males can probably ensure their paternity, because of the last-male advantage (Koga et al., 1993; Goshima et al., 1995). Various kinds of hermit crabs occur in the intertidal zone around the world. In many species, males are larger than females (Asakura, 1995). In the precopulatory phase, a male grasps a female by pinching the rim of the shell of the female with his cheliped (e.g., Hazlett, 1966; Imafuku, 1986; Goshima et al., 1996b; Wada et al., 1996). Precopulatory mate-guarding behavior is triggered by the release of a pheromone by a ripe female (Imafuku, 1986). Although a number of studies have examined the reproductive biology of hermit crabs based on shell condition (Bertness, 1981a; Hazlett, 1989; Hazlett and Baron, 1989), none has assessed the effect of the male/female size ratio. In this study, we investigate the mating behavior of the hermit crab Pagurus filholi (de Man) (formerly P. geminus McLaughlin) and describe the mating behavioral sequence under laboratory conditions to determine whether mating behavior differs among different size ratios of male and female pairs in a population.

2 MATERIALS AND METHODS We studied Pagurus filholi collected from the intertidal rocky shore at Kattoshi (41 44'N, 'E), located in the western part of Hakodate Bay, Hokkaido, Japan. The reproductive biology of P. filhnli can be summarized as follows (based on Goshima et al., in press). The main breeding season is from February to August, when precopulatory mate-guarding pairs are commonly seen at the intertidal rocky shore. Males are larger than females, and the size variance of males is greater than for females; mean male size (±SD) of the Kattoshi population = 2.09 t 0.77 mm SL (shield length; hard portion of carapace) (N = 597, range = mm), mean female size (±SD) = 1.96 ± 0.35 mm SL (N = 722, range = mm) (unpublished data). Females lay eggs several times within a breeding season. Females do not always molt before copulating. Eggs are attached to the pleopods of the female. At a water temperature of 20 C females incubate their eggs for approximately 2 weeks. Clutch size increases with body size, and large females can carry up to 200 eggs. Males show no preference for female size when choosing mates, nor do they select females depending on the time remaining before the female can mate in the precopulatory guarding period. Mating Behavioral Sequence.-Both pairs and solitary individuals were collected at Kattoshi. Pairs were separated and each individual was kept in a small plastic cup for 24 h. Solitary animals were reared en masse in a tank at 16-18'C, 12L:12D. Observations were carried out in a laboratory at Hokkaido University from 23 April to 20 August A male and a female were placed in an experimental tank (10 x 16 x 10 cm), and the behavior of individuals was recorded for 6 h with a video camera. All females used in the experiment had been guarded by males in the field, but both paired and solitary males were used. We categorized each mating behavior using the following criteria: "assessment," the male touches the aperture of the shell of the female with his chelipeds; "attempt," the male holds his chelipeds over the aperture of the shell of the female, with the apertures of their shells facing one another, or the male attempts to pull the female from the shell of the female with his chelipeds; "embrace," the male embraces the female shell with his ambulatory legs; "precopulatory guard," the male grasps the rim of the shell of the female with his left minor cheliped; "rejection," the male separates from the female; "copulation," the female draws further out from the aperture of her shell as the male holds her with his cheliped (in this position, the coxae of the fifth pereiopods of the male are approximately opposite the coxae of the third pereiopods of the female); and "postcopulatory guard," the male holds the shell of the female with his chelipeds from behind. Experiment with Different-Sized Male.s.-Experiments were carried out at the Usujiri Fisheries Laboratory, Faculty of Fisheries, Hokkaido University, Minamikayabe, Japan, from 6 April to 6 June 1996 to explore the differences in the behavior of 2 different-sized males with a receptive female. Solitary animals were collected from the intertidal rocky shore at Kattoshi, and the sexes were maintained in separate plastic tanks supplied with running sea water under natural light conditions. We distinguished mature, immature, and ovigerous females by holding the shells with tweezers under a stereoscopic microscope and observed them emerging from shells fully, showing their ovaries through the thin skin of the abdomen. We selected mature females whose ovaries con- tained ripe eggs. A male was released into an experimental tank (17 x 13 x 8 cm in height) filled with sea water (at 12 C). After several minutes, a mature female (male/female size ratio 1.5) was presented to the male and the behavior of the animals was observed for 30 min. We described the mating activity of the male in terms of the previously described behavioral categories. After the 30-min observation period, the mature female was taken out of the experimental tank. A larger male (male/female size ratio > 1.5) was placed in another experimental tank filled with sea water, and the same mature female was placed in the second experimental tank. We then repeated the 30-min observation period. In order to eliminate any effect that the order in which the 2 size groups were introduced might have had, the above experiment was repeated, but large males were first introduced followed by small males. After each experiment, all individuals were preserved in 10% Formalin and their shield lengths were measured with a stereoscopic microscope. The size range of males was considerably greater than that of females. The female size range was very narrow in the Kattoshi population, as previously shown. Therefore, if male size increased, then the male/female size ratio also increased inevitably, which made it difficult to distinguish the effects of male size and male/female size ratio on mat- ing behavior. It is important to make clear the relative importance of each size effect on mating behavior. Therefore, we first examined each size effect both within a size class of males ( 3.0 mm, N = 31; guard = 20, attempt = 11) and within a male/female size-ratio class ( 1.5, N = 29; guard = 18, attempt = 11), in which both mating behaviors of guard and attempt were observed (see Results for detail). As a result, there was a significant difference between both mating behaviors (Mann-Whitney U test, U = 61, P = 0.043) across male/female size ratio, while there was no such difference across male size (U = 67, P = 0.149). Thus, we concluded that male/female size ratio was more important than male size on male mating behavior. We analyzed our data and consistently indicated our results in terms of male/female size ratio. RESULTS Mating Behavioral Sequences The mating behavioral sequence is shown in Fig. 1. To investigate the relationship between mating behavior and male-female body size, all pairs were divided into three groups de- pending on the male-female size ratio (Fig. 2). Forty-eight observations (34 with paired males, 14 with solitary males) were recorded by video camera. All males showed assess- ment behavior when they.encountered fe- males in the experimental tank. After dis- playing assessment behavior, 25 males per- formed precopulatory guard behavior, 14 males performed attempt behavior, and 9 males separated from the female. Copulation by 16 pairs was recorded, and no precopula molts were found throughout the experiment.

3 Fig. 1. Both males and females eased partially out of their shells and entwined their ambulatory legs. The mean duration of copulation was 30 s (SD = 27 s). All males that copulated (N = 16) displayed postcopulatory guard behavior (Fig. 1). A male positioned himself behind the female and held her shell with his chelipeds. During this phase, the female laid eggs while in her shell. The mean duration of the postcopulatory guard phase was 25 min 5 s (SD = 9 min 4 s, N = 16). We compared the behavioral sequence of male mating activity to the male/female size ratio of the mating pairs. When males were smaller than females (male/female size ratio 1.0), the male guarded the female after assessment only one occasion. The other six males displayed attempt behavior. When males were slightly larger than females (1.0 male/female size ratio 2.0), half of the males displayed precopulatory guard behav- Mating behavioral sequence of Pagurus filholi. ior. Very large males (male/female size ratio > 2.0) guarded females, whether or not they copulated (Fig. 2). The mating behavioral pattern after assessment behavior differed depending on the male/female size ratio (P = 0.010, Fisher's exact probability test, Table 1). When males were smaller than females, males tended to display attempt behavior more often than guarding behavior. In contrast, when males were larger than females Table 1. Relationship of the male/female size ratio to precopulatory behavioral patterns after assessment behavior in Pagurus filholi (P = 0.010, Fisher's exact probability test).

4 Fig. 2. Mating behavioral sequences of Pagurus filholi depending on relative body size. (male/female size ratio > 1.0), males guarded the females. Experiment with Different-Sized Males In 39 replicates, 31 large males (male/female size ratio > 1.5) guarded females, but only 16 small males (male/female size ratio 1.5) did so. Only four of the large males displayed attempt behavior in this experiment, in contrast to only 16 of the small males (Tables 2, 3). The behavioral patterns before mating were different between large and small males (P 0.01, McNemar test). DISCUSSION We clarified the mating behavioral sequence of Pagurus filholi under experimental conditions. Males may discriminate the sex of a possible mate during assessment behavior by detecting a sexual-linked pheromone (Imafuku, 1986). Males appear to use vision first to recognize other individuals, after which they may determine sex and maturity. Thus, males often approach and display assessment behavior before other solitary males before determining they are not female and rejecting them (Imafuku, 1986; personal observation). The copulation behavior of P. filholi is similar to that of other hermit crab species (see Elwood and Neil, 1992). In ventral to ventral contact by male and female for mating, the male transfers spermatophores to the female from his genital openings. Males always display postcopulatory guard behavior after copulation. Males appear to wait for the female to lay her eggs, possibly to ensure their paternity. Males of Pagurus bernhardus (L.) grasped the rim of a shell of a female with their mi- nor cheliped, with the female facing away from the male. Mating by P. bernhardus occurs between individuals of similar size (Elwood and Neil, 1992). In this study, males of P. filholi that were much larger than their female mates tended to guard the females, while, in the case of males not much larger than female mates, the males appeared to perform attempt behavior. Larger males relative to females appear to have a lower cost of guarding due to a lower loading constraint (Adams and Greenwood, 1983). Therefore, it should be not disadvantageous for larger males to guard females more frequently than smaller ones. When males were smaller than their female mates, the male grasped the rim of the shell of the female with his minor che- liped, but seldom dragged her because of his smaller body size (personal observation). Since the male was unable to control the fe- male, he was unable to execute precopulatory guarding behavior. Thus, the smaller males relative to females rarely displayed precopulatory guarding behavior. Males often held their chelipeds over the aperture of the shell of the female, the apertures of the two shells in opposite position.

5 Table 2. Results of experiments with different-sized males of Pagurus filholi. Precopulatory guarding behavior of two different-sized males to a receptive female. Frequency of precopulatory guarding behavior by large (male/female size ratio 1.5) and small (male/female size ratio 1.5) males (x2 = , d.f. = 1, P 0.01, Mc- Nemar test). Table 3. Results of experiments with different-sized males of Paguru.s filholi. Attempt behavior of two different-sized males to a receptive female. Frequency of attempt behavior by large (male/female size ratio 1.5) and small (male/female size ratio 1.5) males (xz = , d.f. = 1, P 0.01, McNemar test). This characteristic posture was observed only in male-female pairs of similar size. This male attempt behavior was used to encourage the female to emerge from the shell. The male then inserted his chelipeds into the aperture of the shell of the female to draw her out for copulation. Smaller males may copulate without performing precopulatory mate-guarding behavior. This mating tactic may have relatively low time and energy cost, compared with the tactics of guarding behavior. Both guard and attempt mating tactics were adopted by male hermit crabs. Individual males choose their mating tactics based on the relative size of the female encountered. Males smaller than their potential mates have difficulty guarding females because of loading constraint. They then adopt the attempt mating behavior. Since body sizes of hermit crabs are often limited by the supply of vacant shells (Spight, 1977; Scully, 1979; Bertness, 1981b; Ohmori et al., 1995), male and female sizes vary at different sites. In the intertidal zone around Kattoshi, there were few vacant large shells (Ohmori et al., 1995), size variance was larger in males than in females, size distribution differed between males and females, and various-sized males lived in the same place in the field (unpublished data). In such circumstances, an individual was sometimes unable to compete successfully by fighting or guarding, perhaps because of its smaller size. Even if a male grasped a female that was as large as himself, incurring a higher loading cost, the female was often carried off by another larger male, a result of intrasexual competition. Instead, smaller males must make the best of their poor circumstances by employing an alternative mating strategy, the attempt mating tactic (e.g., Krebs and Davies, 1993). Such alternative mating behaviors are also known in several decapod species, such as the sand-bubbler crab Scopimera globosa (see Henmi et al., 1993), the fiddler crab Uca lactea (see Murai et al., 1987; Goshima and Murai, 1988), and Uca tetragonon (see Goshima et al., 1996a). When males encounter unguarded ripe females ready to spawn, the males secure the females for copulation from other competitive males, irrespective of their body sizes. The choice of behavior may be a conditional strategy, depending on the male/female size ratio. If the female encountered is smaller then the male, he then guards her, and, if larger, executes the attempt behavior immediately. The advantage of smaller size may depend on the operational sex ratio. For example, at the beginning of the breeding season, most females lay eggs within the first month (Goshima et al., in press). Since many receptive females are present, small males may have a better chance of copulating than later in the breeding season, when the sex ratio becomes more male-biased. Moreover, when the variance of the size distribution of the population is low and the mean individual size of both sexes is similar, the tactics of a nonguard male may be more advantageous than the tactics of a guard male, because of relatively low male mating cost. There may be two reasons why not all males adopt the attempt tactics in spite of relatively low cost. The first is that the reproductive success of the large-guard and smallattempt tactics will likely differ. Not all males adopt the attempt behavior, in spite of the lower cost. This suggests that reproductive success may not be high for the attempt tactic. Locating a receptive female in the field may be difficult, since we found few solitary receptive females. Most were already guarded by large males. In the field there were probably too few ripe females ready to spawn to

6 allow frequent attempt tactics. Even if males could find such receptive females, they might attract other single males while executing attempt mating behavior (personal observation). The female may then be often carried off by another larger male. The precopulatory guarding tactics may result in increasing reproductive success of the males, by securing their mates from other males until the female can copulate and spawn through pre- and postcopulatory guarding behaviors (Goshima et al., 1995, 1996b), even though it would need greater time and energy cost for the males. The second is that larger males relative to females may not be able to execute attempt behavior with the smaller females. Larger males cannot put their large chelipeds into the aperture of the shell of the female since the chelipeds of the males are larger than the females, and the shell sizes of the females are usually smaller than males. Only smaller males relative to females could perform the attempt mating tactics. In conclusion, the present study provides evidence that hermit crab males use two mat- ing tactics. The tactics that a male decides to adopt may depend on the relative size of his mate. More data are needed to evaluate the relative success of the two mating tactics in the field. ACKNOWLEDGEMENTS We thank S. Nakao, T. Noda, S. Wada, K. Ito, T. Sonoda, and other members of the Laboratory of Benthology, Faculty of Fisheries, Hokkaido University, for their valuable comments and criticisms. We also thank Y. Arashida and other staff of the Usujiri Fisheries Laboratory, Faculty of Fisheries, Hokkaido University, for their help during the experiments. Cordial thanks are also given to S. Hughes of Aberdeen University and J. Bower of Hokkaido University for improving the English of this manuscript. LITERATURE CITED Adams, J., and P. J. 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7 Ridley, M The explanation of organic diversity. Clarendon Press, Oxford, England. Pp Scully, E. P The effects of gastropod shell availability and habitat characteristics on shell utilization by the intertidal hermit crab Pagurus longicarpus Say.â Journal of Experimental Marine Biology and Ecology 37: Spight, T. M Availability and use of shells by intertidal hermit crabs.-biological Bulletin 152: Wada, S., T. Sonoda, and S. Goshima Temporal size covariation of mating pairs of the hermit crab Pagurus middendorffii (Decapoda: Anomura: Paguridae) during a single breeding season.â Crustacean Research 25: RECEIVED: 25 March ACCEPTED: 14 January Address: Department of Marine Biological Science, Faculty of Fisheries, Hokkaido University, Minato, Hakodate 041â 8611, Japan. ( goshima@pop.fish.hokudai. ac.jp)