JOURNAL OF BIOLOGY, 23(3): 723–728, 2003

MASS WANDERING IN THE REPRODUCTIVE SEASON BY THE FIDDLER UCA PERPLEXA (: OCYPODIDAE)

Satoshi Takeda

Marine Biological Station, Tohoku University, Asamushi, Aomori 039-3501, Japan ([email protected])

ABSTRACT Downloaded from https://academic.oup.com/jcb/article/23/3/723/2679928 by guest on 28 September 2021 I investigated mass wandering by the fiddler crab Uca perplexa on Okinawa Island, Japan. Many larger males wandered during the daytime low tide for four continuous days in their reproductive season. Just after exposure of their burrows they moved uphill, then returned to the burrow area before dead low tide without feeding. During the wandering phase, the males did not wave to females to initiate mating. Males resumed waving after the wandering phase. I discuss why the large males wander en masse in relation to the ’ mating system and larval release.

It is well known that ocypodid and mictyrid sone and Okadome, 1981). They have two crabs inhabiting tidal fats make burrow struc- spawning periods a year, but each female tures in the substratum and engage in surface spawns only once a year (Nakasone and activities such as feeding and courtship behav- Okadome, 1981). In the earlier period, larger ior. These activities are centered around their females (more than one year after settlement) burrows, which provide the crabs protection in April and May and release the zoea from , extreme temperature, and des- larvae in early June. In the later period, larger iccation during the period of exposure at low and smaller females (about one year after tide (e.g., Altevogt, 1957; Macintosh, 1979). settlement) spawn from June to August and Some researchers, however, have reported that release their larvae from August to September. the crabs leave their burrows, move downhill, In the reproductive season, mature females and feed along the waterline (e.g., Cameron, leave their burrows and begin wandering 1966; Yamaguchi, 1976; Wada, 1981; Murai (Nakasone and Murai, 1998). Males attract et al., 1983; Henmi, 1984, 1989; Koga, 1995). wandering females through lateral-circular claw After feeding, they return to their burrows or waving (Nakasone and Murai, 1998). Females make new burrows. This wandering and sub- choose larger males than themselves and sequent feeding are considered to supply their examine males’ burrows (Nakasone and Murai, energy for growth and reproduction (Koga, 1998). The crabs copulate on the surface near 1995), though only one , Uca vocans the female’s burrow or under the ground in the vocans (Linnaeus, 1758), moves to the shoreline male’s burrow (Nakasone and Murai, 1998). both to mate and to feed (Nakasone, 1982; After a female has spawned in a male’s burrow, Nakasone et al., 1983). the male offers his burrow to her. The male then The fiddler crab Uca perplexa (H. Milne digs or occupies a new burrow. Alternatively, if Edwards, 1837) is distributed in the tropical they copulate on the surface, the female returns western Pacific between the Ryukyu Islands and to her own burrow. The ovigerous female stays Vanuatu (Crane, 1975). The crabs dig individ- about two weeks in the plugged burrow ual burrows along sandy shores (Nakasone and (Nakasone and Murai, 1998). Murai, 1998). Males and females burrow close On Okinawa, U. perplexa displays mass to each other. They stay in their burrows while wandering over several days in their earlier the burrows are submerged (Nakasone and reproductive period. The crabs move uphill just Murai, 1998). During the daytime low tide, after exposure of their burrows during the they engage in feeding and courtship behavior daytime low tide and return later, unlike some on the surface near their burrows (Nakasone and ocypodid and mictyrid crabs which move Murai, 1998). downhill en masse and feed along the shoreline. On Okinawa, one of the Ryukyu Islands, the Here I describe the features of the wandering crabs reproduce in spring and summer (Naka- individuals, the time that wandering occurs, and

723 724 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 23, NO. 3, 2003 how this mass wandering relates to other surface RESULTS activities and the release of larvae. Wandering Phase Many U. perplexa wandered on 10, 11, 12, MATERIALS AND METHODS and 13 June 2001 (wandering phase). Just after Study Site exposure, they moved uphill. After reaching the mangrove tree zone, they walked along the bank The study site was an area of sandy shore about 100 3 100 m, bounded by a stone wall to the east and by small of the creek and then moved downhill. During creeks to the north and south, on Hanejiuchimi Bay, this phase, the males scarcely waved. Okinawa Island, Japan (128829110E; 268379440N). The site In the wandering phase, the crabs were is covered by water at high tide. Mangrove trees grow in trapped from just after exposure only to dead Downloaded from https://academic.oup.com/jcb/article/23/3/723/2679928 by guest on 28 September 2021 a strip of about 2 m wide along the eastern one-fourth of the low tide (n ¼ 81), except for two males. In the bank of the northern creek. Sedges (Carex scabrifolia Stend.) grow in a strip about 5 m wide along the strip of resident phase, however, the crabs were trapped mangrove trees. from just after exposure to just before sub- The fiddler crab Uca perplexa inhabits the upper three- mergence, at a uniformly low frequency (Krus- fourths of this shore between the high and low water levels kal Wallis test; uphill-moving male: H ¼ of the neap tide. A few Uca vocans vocans inhabit the water- logged area and the bank of the southern creek. A very few 14.980, P ¼ 0.2426; uphill-moving female: H ¼ Uca dussumieri dussumieri (H. Milne Edwards, 1852) 19.043, P ¼ 0.0875; downhill-moving male: inhabit the area around the mangrove trees. Mictyris H¼7.992, P¼0.7857; downhill-moving female: brevidactylus Stimpson, 1858, inhabits the area below the H ¼ 7.803, P ¼ 0.8003) (Fig. 1). low water level of the neap tide. In the uphill-facing traps, more crabs were collected in the wandering phase than in the Collection of Wandering Crabs resident phase between 3.0 and 2.5 h and I buried an empty PVC cup (8 cm diameter, 12 cm deep) between 2.0 and 1.5 h before dead low tide vertically, ensuring that its opening was flush with the sand surface. Two transparent PVC plates (6039 cm) were placed (Mann Whitney U-test) (Fig. 1). In the downhill- on their long edges on the sand surface, ensuring that one end facing traps, more crabs were collected between of each plate was touching the buried cup. The other ends of 2.5 and 1.0 h before dead low tide. These mean the plates were 50 cm apart, so the angle of the vertex was that the crabs moved more frequently just after 498. Six such traps were set at random in the middle of the U. exposure, especially uphill, and did not pause perplexa habitat at low tide on 16 May 2001. The two plates of three traps were fanned out downhill and those of the other upon the destination, corresponding with the three traps were fanned out uphill. field observation. I collected crabs from the traps every 30 min from just The number of individuals collected from after exposure during every daytime low tide from 17 May to traps was greatest on 10 June, then decreased to 15 June 2001. I recorded the sex, carapace width (nearest 0.05 mm), and presence or absence of eggs on the pleopods zero on 14 June (Fig. 2). The numbers of males of each crab. I recorded the air temperature at the dead low and females trapped and their total were greater tide. in the wandering phase than in the resident phase (excluding five rainy days in the resident Observation of Crabs on the Surface phase, when they did not emerge on the I randomly set two quadrats with transparent sides (60 cm surface), even though they were trapped only long, 9 cm high) in the U. perplexa habitat. I then observed before extreme low tide in the wandering phase the crabs in each quadrat for 30 min and recorded their sex (Fig. 1) (Mann Whitney U-test; male: jzj¼ and size class: large (greater than about 9 mm carapace width) or small (less than about 9 mm). I investigated these 2.574, P ¼ 0.0101; female: jzj¼3.222, P ¼ items in 31 quadrats between 20 May and 6 June when most 0.0013; total: jzj¼2.666, P ¼ 0.0077). There crabs were engaged in surface activities near their burrows was no clear relationship between the mass (resident phase), and in 46 quadrats after the crabs had wandering and air temperature (Fig. 2). stopped wandering on 10 and 13 June when many crabs Most of the trapped crabs were large males in wandered (wandering phase). both the wandering phase (male : female ¼ 75:8) Proportion of Ovigerous Females and the resident phase (80:8) (Fig. 3). The carapace width of the trapped males was larger I collected the crabs present in a quadrat (50 3 50 3 20 cm deep) placed randomly in the U. perplexa habitat by than 9.85 mm in the resident phase, except for using a sieve with a 2.5-mm mesh-size, and recorded the one at 5.7 mm (mean 6 SD ¼ 13.71 6 1.94 sex, carapace width (nearest 0.05 mm), and presence or mm), and larger than 12.55 mm in the wandering absence of eggs on the pleopods of each crab. The survey phase (14.60 6 1.00 mm). No ovigerous females was carried out five times on 2 and 3 June in the resident were trapped in either phase. The carapace width phase, and five times after the crabs had stopped wandering on 11, 12, and 13 June in the wandering phase. of the females was larger than 10.3 mm in the TAKEDA: MASS WANDERING BY UCA PERPLEXA 725 Downloaded from https://academic.oup.com/jcb/article/23/3/723/2679928 by guest on 28 September 2021

Fig. 1. Mean number of individuals collected from three traps that opened uphill or downhill at 30-min intervals based on the dead low tide. * and ** mean significant difference at 0.05 and 0.01 levels between the wandering and resident phases. resident phase (11.85 6 1.21 mm) and larger (resident: male : female ¼ 308:75; wandering: than 11.45 mm in the wandering phase (13.08 6 385:204; v2 ¼ 24.9662, df ¼ 1, P , 0.001). 0.83 mm). The carapace width of the trapped Among the large crabs, the density of males crabs was larger in the wandering phase than in (resident: 9.16 6 2.45; wandering: 8.24 6 the resident phase (Mann Whitney U-test; male: 3.06) decreased by 0.92 individuals (Mann jzj¼3.105, P ¼ 0.0019; female: jzj¼2.312, P ¼ Whitney U-test; jzj¼1.170, P ¼ 0.2418), and 0.0208) (Fig. 3). the density of females (resident: 1.68 6 1.22; wandering: 4.20 6 2.28) increased by 2.52 Crabs on the Surface individuals (jzj¼5.143, P , 0.0001). These The density of males that emerged on the values correspond to the decrease in the whole surface of the quadrat was slightly less in the male density and the increase in the whole wandering phase (mean 6 SD ¼ 8.37 6 3.05) female density between the resident and wan- than in the resident phase (9.94 6 2.35) (Mann dering phases. Thus, the changes in density Whitney U-test; jzj¼2.027, P ¼ 0.0426). In were caused mainly by the large individuals. contrast, the density of females was much greater in the wandering phase (4.43 6 2.50) than in the Proportion of Ovigerous Females resident phase (2.42 6 1.71) (jzj¼3.773, P ¼ The densities of the males and females 0.0002). Therefore, the sex ratio differed be- collected from the quadrats and their sex pro- tween the resident and wandering phases portion did not differ between the resident and 726 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 23, NO. 3, 2003

from just after exposure to the dead low tide, and the number of wandering individuals was greater, especially just after exposure (Fig. 1). The mass wandering of U. perplexa differed from those of other ocypodid and mictyrid crabs in the direction of movement and the behavior on the destination. In general, ocypodid and mictyrid crabs move downhill from the burrow area to the waterline and feed there (e.g., Murai et al., 1982), although U. vocans mates in

addition to feeding (Nakasone, 1982; Nakasone Downloaded from https://academic.oup.com/jcb/article/23/3/723/2679928 by guest on 28 September 2021 et al., 1983). In contrast, U. perplexa moved uphill and did not pause to feed or engage in mating or other activities (Fig. 1). During and after wandering, most males did not wave or engage in behavior related to mating, as reported in U. vocans (Nakasone, 1982; Nakasone et al., 1983; Christy and Salmon, 1984; Salmon, 1984). After the wan- dering phase, the number of males engaging in waving increased gradually (personal observa- tion). This suggests that males suspended courtship and mating in their burrows during the wandering phase. Fig. 2. Total number of individuals collected from six In the burrow area, the densities, size traps (bottom), water level of the daytime low tide (Japan structures, and sex proportions did not differ Meteorological Agency, 2000) (middle), and air temperature between the resident and wandering phases at the dead low tide (top). * under a date means a rainy day. (Fig. 3). On the other hand, the densities of The breaks in the lines for water level and air temperature mean a change in the investigation time from evening to individuals engaging in surface activities, espe- morning. Closed circle: new moon; open circle: full moon. cially large females, increased in the wandering phase, but the proportion of ovigerous females decreased. These facts indicate that the ovig- wandering phases (male, resident: mean 6 SD ¼ erous females released their larvae in a short 8.0 6 4.69; wandering: 8.6 6 3.05; female, period just before or during the wandering phase resident: 6.8 6 2.68; wandering: 7.8 6 2.17; and resumed their surface activities, because Mann Whitney U-test; male: jzj¼0.316, P ¼ ovigerous females stay in a plugged burrow and 0.7518; female: jzj¼0.865, P¼0.3871; resident: do not emerge for about two weeks until they 2 male : female ¼ 40:34; wandering: 43:39; v ¼ release their larvae (Nakasone and Murai, 0.0017, df¼1, P . 0.90). Females and males had 1998). a bimodal size-frequency distribution in both the Goshima and Murai (1987) reported that the resident and wandering phases (Fig. 3). The burrow of the closed fiddler crab, Uca lactea distribution of their carapace widths did not (De Haan, 1835), is larger among the males than differ significantly between phases (Mann among the females in the reproductive season, Whiney U-test; male: jzj¼1.094, P ¼ 0.2740; that the females prefer a larger burrow when female: jzj¼0.575, P ¼ 0.5652) (Fig. 3). they mate in the burrow, and that the females The carapace width of the ovigerous females then spawn, incubate their eggs in the burrow, was larger than 9.0 mm (Fig. 3). The proportion and release their larvae. Females of U. perplexa of ovigerous females among females larger than enter several males’ burrows before making 9.0 mm carapace width was less in the wandering a choice (Nakasone and Murai, 1998) and phase (6/32 ¼ 18.8%) than in the resident phase probably also prefer larger burrows, because 2 (10/23¼43.5%) (v ¼6.8556, df¼1, P , 0.01). they also incubate their eggs in the burrow. This preference means that the females occupy larger DISCUSSION burrows than the males during the spawning Two factors distinguish the wandering phase term, especially in the early period in when they from the resident phase: the crabs wandered spawn all at once (Nakasone and Okadome, TAKEDA: MASS WANDERING BY UCA PERPLEXA 727 Downloaded from https://academic.oup.com/jcb/article/23/3/723/2679928 by guest on 28 September 2021

Fig. 3. Frequency distribution of the carapace widths of the individuals collected from quadrats (top), or traps in the resident (middle) and wandering (bottom) phases. Solid bars mean ovigerous females.

1981). Thus, larger males come to occupy The mating system (Nakasone and Murai, smaller burrows after mating than before. 1998) and the simultaneous hatch of the eggs I observed that after releasing their larvae, spawned in the early spawning period (Naka- females resumed their surface activities. They sone and Okadome, 1981; this study), which is then have to find or dig a new burrow, because probably related with the spring tide as in other crabs evade predation by occupying a burrow fiddler crabs (e.g., Christy, 1978, 1982; Bergin, suited to their body size (e.g., Willason, 1981; 1981; Kellemeyer and Salmon, 2001), may be Takeda and Kurihara, 1987). In contrast, the related to the occurrence of mass wandering by large males that had been occupying smaller the large males, because many large vacant burrows after offering their larger burrows to the burrows will be made by the females after spawning females had to find a larger burrow releasing their larvae. In addition, the spring tide for the next mating. The mass wandering by the with a longer emergence period (Fig. 2), which large U. perplexa males probably makes small offers more potential opportunity to find burrows vacant. The wandering may increase a burrow suited to body size, may promote the the opportunity for the resident females after mass wandering. This possibility needs to be they have released the larvae to find a burrow examined by further behavioral studies. suited to their body size. Simultaneously, the large wandering males may be able to increase ACKNOWLEDGEMENTS their chance of occupying larger burrows that I thank Dr. M. Murai, Mrs. Y. Nakano, and S. Nakamura had been occupied by ovigerous females in and other staff of Sesoko Station, Tropical Biosphere preparation for the next mating. Research Center, University of the Ryukyus, for their help 728 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 23, NO. 3, 2003 and for facilitating my work there. 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