Microhabitat Use by the Soldier Crab

MICROHABITAT USE BY THE SOLDIER CRAB MICTYRIS BREVIDACTYLUS (BRACHYURA: MICTYRIDAE): INTERCHANGEABILITY OF SURFACE AND SUBSURFACE FEEDING THROUGH BURROW STRUCTURE ALTERATION Author(s): Satoshi Takeda and Minoru Murai Source: Journal of Crustacean Biology, 24(2):327-339. 2004. Published By: The Crustacean Society DOI: http://dx.doi.org/10.1651/C-2436 URL: http://www.bioone.org/doi/full/10.1651/C-2436

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.

BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. JOURNAL OF CRUSTACEAN BIOLOGY, 24(2): 327–339, 2004

MICROHABITAT USE BY THE SOLDIER CRAB MICTYRIS BREVIDACTYLUS (BRACHYURA: MICTYRIDAE): INTERCHANGEABILITY OF SURFACE AND SUBSURFACE FEEDING THROUGH BURROW STRUCTURE ALTERATION

Satoshi Takeda and Minoru Murai

(ST, correspondence) Marine Biological Station, Tohoku University, Asamushi, Aomori 039-3501, Japan ([email protected]); (MM) Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyus, 3422 Sesoko, Motobu, Okinawa 905-0227, Japan

ABSTRACT The soldier crab Mictyris brevidactylus Stimpson inhabits sandy flats of Southeast Asia. The crabs that we studied fed on deposited matter in the surface sand in two ways. On well-drained sand in the upper part of their habitat, they usually made a single tunnel roofed with sand to conceal themselves while they fed. After feeding, they returned to an ascending shaft from which they had earlier emerged. Then, they descended via the plugged ascending shaft and transformed the shape of the shaft into an ovoid air chamber at a sufficient depth. During the daytime low tide, on the waterlogged, fluid sand near the shoreline, large individuals, mostly males, fed in droves on the surface while moving along the shoreline as it moved with the tide. After feeding for about 2 h, they made a small air chamber slightly above the shoreline by using corkscrew-style digging, and descended into the semi-fluid sand. During the night-time low tide, the crabs fed separately for about 4 h on both the fluid sand near the shoreline and the well- drained firm sand in the upper habitat, and retreated into the sand, although they took longer to retreat into the well-drained sand than into the semi-fluid sand. That is, the crabs feeding on the surface at the daytime low tide returned to the subsurface-feeding area and made a small air chamber during the night-time low tide. Later, at low tide, the small air chamber was elongated to allow subsurface feeding. We consider that the movement to the upper habitat at night-time and the feeding near the shoreline in the daytime help the crabs evade predators that rely on sight, such as birds.

Crabs of the genus Mictyris Latreille (Bra- vault roofed with sand on the sand surface. The chyura: Mictyridae), each with a spherical body, crabs cover themselves entirely with the sand are classified into four species, which inhabit roof. This construction, which is termed a ‘‘tun- tropical and subtropical sandy or muddy shores nel’’ by Yamaguchi (1976), is found in the of the eastern Indian Ocean and the western upper part of their habitat, where the water table Pacific region (McNeill, 1926; Takeda, 1978). falls well below the surface at low tide. When Two of the species are distributed in Australia, they perceive danger, crabs return to the tube- one in Australia and Southeast Asia, and the re- like ascending shaft, which is dug through the maining one in Southeast Asia (McNeill, 1926; sand to the exposed surface to feed. After Takeda, 1978). feeding, they return to their ascending shafts Mictyris brevidactylus Stimpson, 1858, oc- and plug the entrance with sand (Yamaguchi, cupies the lower part of the sandy shore, usually 1976). below the low water level of the neap tide, from Another method is used on the sand surface, the Ryukyu Islands to Hong Kong and the like that of ocypodid crabs (e.g., Ono, 1965; Philippines (Takeda, 1978). When habitat is Fielder, 1970; Zimmer-Faust, 1987). In the submerged, the crab resides in the sand (Cow- daytime low tide, they feed while walking les, 1915; Takahasi, 1935; Yamaguchi, 1976; forwards in droves near the shoreline. Individ- Nakasone and Akamine, 1981). When the tide uals, which have been feeding beneath the exposes its habitat, the crab ascends to near, or surface of the sand, also emerge and then join emerges onto, the sand surface to feed (Yama- the droves. When they perceive danger, they guchi, 1976). It feeds on deposited matter in the bury themselves directly in the waterlogged sand near the surface in two ways (Yamaguchi, sand near the shoreline (Yamaguchi, 1976). 1976; Nakasone and Akamine, 1981). One After feeding, they bury themselves by ‘‘cork- method is used in, usually, a single tunnel-like screw-style’’ digging into the moist, semi-fluid

327 328 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 24, NO. 2, 2004 sand slightly above the shoreline before flood the outer containers. The sand below the water level was tide (Cowles, 1915; Yamaguchi, 1976). always fluid. A crab with a maximum carapace length of about 13 mm (mean 6 SD ¼ 13.55 6 1.20, n ¼ 47) was Yamaguchi (1976) observed the behavior released onto the sand in each inner vessel. We observed its of M. brevidactylus in several habitats in the concealment behavior and burrowing behavior. In addition, Ryukyu Islands, Japan, and reported that only we observed how the crab descended in the sand when it large individuals in crowded habitats fed on the burrowed against the wall of the vessel. We determined the surface of the sand. In contrast, tunnels were presence or absence of air around the crab in the sand and the depth below the surface at which we found the crab by constructed in all habitats regardless of body digging it up 30 min after it had retreated into the sand. The size. Consequently, he presumed that M. brevi- time during which the crab had been entirely concealed in the dactylus usually feeds in the tunnels. sand was also recorded. These observations were replicated, Are the crabs able to move down and up after the previous observed crab was extracted in the vessel. between the surface-feeding area and the sub- Subsurface Feeding and Water-Table Level in surface-feeding area, and to employ two modes the Aquarium of feeding interchangeably? If this were impos- We clarified the relationship between the depth of the water sible, they would densely accumulate near the table and the construction of the ascending shaft for shoreline at low tide. The purpose of this study subsurface feeding in the tunnel and how the crab builds was to clarify the mechanism of interchange- its ascending shaft in the sand. We conducted an experiment ability between surface- and subsurface-feeding under artificial conditions from 18 to 28 May 1998 and 11 to 21 June 2000. Sand and crabs were collected from the tidal to provide some clues to the ecological function flat at the mouth of the Okukubi River. The collected sand of the two modes of feeding. We observed the was packed to a depth of 10 cm in four transparent glass relationship between the two feeding modes and aquaria (35 3 20 3 25 cm deep). Each aquarium contained the construction of two kinds of burrows: a small a pipe with small holes in its wall to drain or add seawater. air chamber made by surface-feeding individu- Thirty individuals, with a maximum carapace length of about 7 mm (mean 6 SD ¼ 6.83 6 0.57, n ¼ 120), that fed in the als and an ascending shaft made by subsurface- tunnels in the field were released on the sand in the aquaria feeding individuals. We also examined the when the water level was 0.5 cm below the sand surface. relationship between the construction of two Immediately, the crabs buried themselves by corkscrew- kinds of burrows and the depth of the water style digging and trapped air in the sand (see Results). Then seawater was poured in to 1 cm above the sand surface. table in the laboratory and field. In addition, we After one day, the water in each aquarium was drained saw how the crabs switch from surface feeding out about 7 cm below the surface of the sand and thereafter to subsurface feeding through the alteration of poured back in twice a day, in synchrony with the natural the burrows. We investigated the activity pat- tidal rhythm. Three days after the beginning of the experi- terns in the daytime and night-time in the field. ment, a few crabs made ascending shafts to the surface of the sand and fed while making tunnels on the sand surface, and Finally, we discuss the movement of the crabs by the following day many tunnels had been constructed in up to the subsurface-feeding area from the day- the aquaria when the water table was well drained. time surface-feeding area during the night-time After five days, we examined the relationship between low tide, based on the difference in the extent of the tunnel construction and the depth of the water table. We measured the numbers of tunnels, depressions, and small the surface-feeding area between the daytime low domes on the sand surface, when the water was drained and night-time. in the daytime. A depression like a crater indicated the emergence of a crab; a dome like a swelling indicated the ascent of a crab beneath the surface. The water in each MATERIALS AND METHODS aquarium was drained to 0.5 cm above or to 1, 3, 6, or 9 cm Corkscrew-Style Digging and Water-Table Depth in below the surface of the sand twice a day, and water was the Laboratory added to approximately 5 cm above the sand surface about 6 h later. To clarify the relationship between the depth of the water When the water level fell more than 3 cm below the sand table and the construction of the small air chamber and to surface in the aquarium, the crabs, which had made a small observe the burying behavior on the surface and subsequent air chamber and descended with it into the sand, enlarged behavior, we made the following observations under it before making an ascending shaft (see Results). The artificial conditions from 25 to 30 September 1996 (non- enlargement of the small air chamber, the construction of the breeding season). Sand and crabs were collected from the ascending shafts, and the construction of the tunnel and tidal flat at the mouth of the Okukubi River, Okinawa Island, feeding were observed when the crab was active against the Japan (268279N, 1278569E). The collected sand (mean ¼ wall of the aquarium. 2.052/, dispersion ¼ 1.145) was packed to a depth of 19 cm into five transparent vessels (11 cm in diameter) with many small holes in their walls up to a height of 5 cm from the Tunnel Construction in the Field bottom, allowing free percolation of water. The vessels were The following observations were made on the tidal flat at the placed in larger containers, and the water level of the inner mouth of the Oura River, Okinawa Island, Japan (268339N, vessels was maintained at 1 cm above the sand surface, level 1288039E) during the daytime of 23 and 25 May 1998 with it, or at 1, 7, or 14 cm below, by pouring seawater into (nonbreeding season), to clarify the relationship between the TAKEDA AND MURAI: BURROWING BEHAVIOR OF MICTYRID CRAB 329

Table 1. Relationship among water-table depth and the percentage of crabs constructing an air chamber; the depth (mean 6 SD) of crabs with or without an air chamber 30 min after retreating into the sand; and the time (mean 6 SD) taken for the crab to conceal its body in the sand.

Water-table depth (cm) Percentage (%) Crab depth (cm) Time (sec) þ10(n ¼ 23) 4.0 6 1.0 (n ¼ 23) nd 00(n ¼ 24) 4.6 6 2.1 (n ¼ 24) 11.9 6 2.3 (n ¼ 24) 1 100 (n ¼ 22) 15.6 6 4.3 (n ¼ 22) 16.3 6 6.1 (n ¼ 24) 7 100 (n ¼ 24) 16.0 6 4.8 (n ¼ 24) 148.2 6 144.9 (n ¼ 23) 14 100 (n ¼ 22) 7.3 6 3.1 (n ¼ 22) 314.5 6 136.7 (n ¼ 22)

Numbers in parentheses indicate numbers of observations; nd, not determined; all crabs that constructed burrows were present in air chambers in the substratum.

tunnel construction and the depth of the water table in the to the depth of 30 cm by using a sieve with a 2.5-mm mesh field. The tidal flat had been leveed, so it was possible to size. We recorded their sex and carapace length. observe the crabs’ behavior from the levee through binoculars, without disturbing their behavior. If the observer RESULTS was present on the sand, the crabs nearby rarely appeared on or beneath the surface, as reported for Mictyris platycheles Corkscrew-Style Digging and H. Milne-Edwards, 1852 (Kraus and Tautz, 1981). During Air Trap Formation exposure of the sand on 22 May, three quadrats (30 3 30 cm) were put on the surface at the same tidal level, where Immediately after being released, all crabs numerous tunnels were present. A stake was erected on the began to retreat directly into in the sand (Table tidal flat at the same tidal level, about 5 m distant from the 1). When the water level was 1 cm above or quadrats, to measure the height of the water surface relative level with the sand surface, all crabs buried to the sand surface. The number and coverage of tunnels on the sand surface in the quadrats and the height of the water themselves in the sand using corkscrew-style surface in a 40-cm-deep pit dug adjacent to the stake just digging, and then remained beneath the sand after exposure were recorded every 10 minutes. The amount surface without an air chamber for 30 min. In of the sand surface covered by tunnels was used as a measure contrast, when the water level was 1 cm below of feeding activity. At the same time, the behavior of crabs, especially how they constructed the tunnels, was observed. the sand surface, all crabs buried themselves In addition, the proportion of each ascending shaft that directly and made air chambers in the sand, and was open or plugged by sand was investigated in relation to then descended to deeper sand. On the firm sand the change in tunnel coverage: about 10%, 40%, and 60% of near the surface, when the water level fell 7 or the coverage on the sand surface in the quadrats on 25 May. 14 cm below the surface, the crab scooped up Water-Table Depth in the Surface- and sand using its three anterior thoracic legs on one Subsurface-Feeding Area side and made a shallow depression. It con- To clarify the behavior patterns of the crabs at low tide in the tinued to scoop and push out the sand from daytime and night-time, we measured the depth of the water the depression intermittently, resting frequently, table in the sand where the crabs were feeding and where and then made an air chamber. they buried themselves. The depth of the water table was We did not measure the time it took for the measured in pits that were dug at the highest and lowest crabs to bury themselves completely in the sand limit in each area. The subsurface-feeding area was indicated by the when the water level was 1 cm above the sand presence of tunnels, and the depth of the water table was surface, because the crabs’ activity made the measured at dead low tide in the daytime or night-time. The water so turbid that we could not see the crabs surface-feeding and burial areas were indicated by the (Table 1). The period was short in fluid or semi- presence of crabs in the daytime, and the depth was measured while the crabs fed on the sand or just after they had fluid sand with a high water level, and much buried themselves. In the night-time, both areas were longer in well-drained, firm sand with a low indicated by the presence of the feeding sand-pellets or water level. The depth of crabs 30 min after mounds of excavated sand clods, in addition to direct ob- burial was shallower when the water level was servation, and the depth was measured at dead low tide. In deeper (Table 1). this study area, no small ocypodid crabs were engaged in surface activities at night. On semi-fluid sand, when the water level was These measurements were carried out every day from 1 cm below the sand surface, a crab trapped 22 to 25 October 2001 (nonbreeding season) in the tidal flat air by the following process (Fig. 1). The crab at the mouth of the Okukubi River. At the same time, we first inserted its chelipeds and first, second, and collected crabs that were feeding on the sand surface. In addition, during the daytime low tide on 24 October, we third ambulatory legs on both sides into the placed a 50 350 cm quadrat five times randomly on the sand semi-fluid sand (Fig. 1a, b) and held the sand surface where the crabs made tunnels and collected the crabs between its thoracic legs on both sides. It then 330 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 24, NO. 2, 2004

backwards, thus rotating the crab’s body around the inserted thoracic legs, which acted as a fulcrum. The crab then pushed away the sand with its inserted legs and thereby constructed a shallow depression into which it rapidly moved (Fig. 1e). Immediately, the crab scooped the pushed-away sand using the thoracic legs on its lower side (Fig. 1f ), and lay on its back in the depression while holding the sand pellet in the thoracic legs on both sides (Fig. 1g), thus concealing its body in the sand. After a few minutes, the crab lay on its side and pushed up the surface sand slightly using the thoracic legs on its upper side (Fig. 1h). The surface of the sand was broken, and the water around the body of the crab was immediately drained away (Fig. 1i). Immediately after this, the crab replaced the sand to cover it and completed a small air chamber in the sand that was isolated from the outside environment (Fig. 1j). In the small air chamber, the crab repeatedly scooped up the sand from the bottom of the chamber using the thoracic legs on its lower side, and attached it to the ceiling of the chamber, thus moving down together with the air chamber, similar to Mictyris longicarpus Latreille, 1806 (Maitland and Maitland, 1992). On the well-drained, firm sand, when the water level was 7 and 14 cm below the sand surface, the crab scooped up a clod of the sand and pushed it aside on the sand surface using the thoracic legs on one side, creating a depression. The crab repeatedly scooped up the sand from the bottom of the depression and pushed it away. When the crab reached a level below the surface of the sand, it continued to scoop Fig. 1. Construction of a small air chamber in the semi- the sand while supporting it with the thoracic fluid sand with water table slightly below the sand surface. legs on its upper side, ensuring a small space in (a) Standing form on the surface of the sand. (b) Insertion of which to work. Consequently, the sand clods thoracic legs on both sides into the sand. (c) Deeper insertion of thoracic legs on one side. (d) Gap constructed by pushed away on the surface were heaped up on pushing away the sand using thoracic legs. (e) Insertion of the opening of the depression. the crab into the gap. (f ) Holding sand mass in thoracic legs When the water level was at the sand surface on both sides. (g) Form of the crab in the sand immediately or 1 cm above, the crabs made no air chamber, after burying itself. (h) Positioning its body in the sand. (i) Splitting the sand covering its body and subsequent drainage because they cannot push up saturated sand with of the water surrounding its body. (j) Trapping air in the their slender thoracic legs. sand by repositioning the sand covering its body. Construction of Ascending Shaft inserted its cheliped and ambulatory legs on one in the Aquarium side deeper into the sand, and pushed away the When the water level fell, the crabs ascended held sand with its thoracic legs on the inserted through the sand. When the water level was side toward the opposite thoracic legs (Fig. 1c). 0.5 cm above, or 1 cm below the surface of the Consequently, a space was formed outside the sand, some small low domes appeared on the pushing legs, and the crab inserted its thoracic surface (Table 2). The crabs did not appear on legs on this side deeper into the gap (Fig. 1d). the sand surface, and later descended again. The opposite ambulatory legs were moved When the water level was 3, 6 or 9 cm below TAKEDA AND MURAI: BURROWING BEHAVIOR OF MICTYRID CRAB 331 the surface, no domes could be distinguished, Table 2. Relationship among water-table depth and the because the surface was disturbed by tunnel numbers (mean 6 SD) of small low domes on the surface of the sand, tunnels constructed on the surface of the sand, and construction. When the water level was more shallow depressions from which crabs had emerged onto than 3 cm below the surface, the number of the sand surface, in four aquaria into each of which 30 tunnels increased, but it did not differ between 6 individuals were released. and 9 cm (Table 2). Depressions were found on Water-table the surface when the water level was 3, 6, or depth (cm) No. domes No. tunnels No. depressions 9 cm below the surface, and a peak was found when the level was 3 cm below the surface. þ0.5 11.25 6 6.13 0 0 1 8.75 6 6.40 0 0 Crabs constructed oblique shafts when they 3 nd 5.25 6 2.50 9.25 6 6.50 ascended in the sand substratum. When the 6 nd 19.00 6 2.94 1.50 6 1.73 water level was 3, 6 or 9 cm below the sand sur- 9 nd 17.25 6 2.50 2.25 6 2.63 face, the crab constructed an ascending shaft by nd, not determined. the following process. It rested in a large ovoid air chamber in the sand (Fig. 2a). First, it ambulatory legs on its upper side onto the sand ascended sideways along the wall of the surface and made a small opening, smaller than chamber (Fig. 2b). The crab began to scrape the diameter of the shaft (Fig. 3b). In almost all the sand off the wall using the cheliped and the cases, the surface sand removed to open the first, second, and third ambulatory legs on its shaft was carried to the bottom of the shaft. upper side while leaning against the wall (Fig. After opening the shaft, the crab pushed up the 2c). Next, it scooped it up and carried it to the sand mass that still covered the rim of the shaft, opposite side of the chamber (Fig. 2d). Conse- using the thoracic legs on its upper side (Fig. quently, a small hollow was made above the 3c). Then it scooped out the sand mass at the scraped wall, and the floor of the hollow and the margin of the floor of the shaft and also deeply wall of the air chamber formed an inclined plane excavated the surface sand adjacent to the floor, (Fig. 2e). The crab climbed sideways up the and carried the sand mass into the shaft using plane and again scraped, scooped, and carried the cheliped and first and second ambulatory away the sand from the top of the hollow. The legs on its upper side (Fig. 3d). The sand mass hollow was thus elongated obliquely upwards that was scooped out was formed into pellets, and formed a long shaft. The original air cham- pushed up, and attached to the outer edge of ber became filled with scraped sand and disap- the sand mass that had previously covered the peared. The crab continued scraping off the sand opening of the shaft (Fig. 3e). Consequently, the from the top of the shaft and ascended, together opening of the shaft was roofed entirely by sand with the shaft, through the sand substratum masses, except for a space adjacent to the floor (Fig. 2f), and then reached the surface. The crab of the shaft. opened the shaft and began to feed on the sur- After the crab had roofed the opening of the face while constructing a tunnel over itself. shaft, it scooped deeply and quickly pulled in After feeding, the crab returned to the a large amount of fresh sand from just beyond ascending shaft and plugged it with sand masses the opening, using the chelipeds and the first scooped from the bottom of the shaft, enclos- and second ambulatory legs on both sides, ing a large quantity of air in the shaft. Next, it which were extended widely, while facing the scooped up a sand mass from the bottom of the forward end of the tunnel (Fig. 3f). Therefore, shaft, carried it up and attached it to the top of only the tips of the anterior three thoracic legs the shaft, and descended together with the shaft. emerged momentarily from beneath the sand When the crab had descended to a sufficient roof. In contrast, its body was concealed under depth, it transformed the shape of the shaft into the sand roof. The manner of scooping and the an ovoid chamber. quantity of scooped sand in the tunnel were different from those on the sand surface, where the crab pinched up a small amount of sand Tunnel Construction and Subsurface using both chelipeds and inserted it into its Feeding in the Aquarium buccal cavity. A crab constructed a tunnel and fed in it in the A small amount of the scooped sand was following ways. It ascended obliquely to the placed in the buccal cavity, sorted, and stored surface of the sand within a long, hollow shaft beneath the mouthparts. The stored sand was (Fig. 3a). Then it extended its first and second combined with unsorted sand and carried to the 332 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 24, NO. 2, 2004 TAKEDA AND MURAI: BURROWING BEHAVIOR OF MICTYRID CRAB 333 forward end of the tunnel in the anterior three Tunnel Construction and Water-Table thoracic legs on one side while the crab walked Depth in the Field sideways (Fig. 3g). The sand pellet was then During the field observations, the investigated transferred to the outer edge of the opposite region was exposed for 6 h on 23 May and 6 h thoracic legs and pushed out. Alternatively, the 20 min on 25 May (Fig. 5). Immediately after crab rotated its body through about 908 while exposure, the water table fell gently, then steeply holding the sand pellet in the thoracic legs on between about 1 and 2 h after exposure, and then its lower side, and subsequently transferred the again gently. The water table rose slightly about sand pellet to the outer margin of the opposite, 20 or 30 min before submergence and then upper thoracic legs, pushed it up, and attached it steeply about 10 min before submergence. to the outer edge of the sand mass roof (Fig. 3h). About 30 min after exposure, some low The crab repeated these movements and thus dome-like swellings appeared on the sand elongated the tunnel on the sand surface while surface, suggesting that the crabs had ascended concealing itself under the sand roof. beneath the surface of the sand. The tunnels There were two types of tunnel, one in which appeared about 1 h after exposure, when the one end was open and one in which both ends water table was about 6 cm below the surface of were closed. We think that the crab built the the sand (Fig. 5), which corresponds to the closed tunnel using similar movements, because observation in the aquarium. Then the tunnels the sand masses covering the tunnel appeared elongated separately, rapidly covering the sand to result from the same behavior on the sand surface and reaching a maximum after 1 h. surface as when the open end of the tunnel was When the tunnels covered about 10% and 40% elongated by the crab. of the sand surface, i.e., when one end of Enlargement of Small Air Chamber a tunnel was elongated, almost all tunnels were connected to a hollow shaft constructed in the The small air chamber as above was enlarged to sand substratum (Table 3). On the other hand, trap some more air to construct an ascending after the coverage had reached the maximum of shaft when the water level fell more than 3 cm about 60%, i.e., after the tunnel elongation was below the sand surface. The crab ascended finished, almost all tunnels were connected to with its small air chamber in the sand (Fig. 4a). a shaft plugged with sand, and the crabs had When it arrived at the surface, it opened the air retreated into the sand. Thus, the crabs engaged chamber by pushing away the sand covering the in their surface activities for only 1 h, between opening, consequently constructing a spherical about 1 and 2 h after exposure, and the tunnel depression in the surface of the sand. The crab and shaft formed a unit. scooped the sand from the bottom of the depression (Fig. 4b). It pulled it up using the anterior three thoracic legs on its lower side Sex Ratio and Size of Crabs while walking sideways, and pushed it out The sex ratio of the crabs collected from the irregularly around the opening of the depression area where many tunnels were made was almost using the opposite cheliped and first and second equal (male/female ¼ 60/71). The carapace ambulatory legs (Figs. 4c, d). length of the subterranean females ranged from When the depression was elongated suffi- 3.85 mm to 11.7 mm, and a bimodal frequency ciently, the crab scooped up the surface sand distribution with the first mode at 6 mm and the around the opening and sealed the gaps among second at 10 mm was found (Fig. 6). The the sand pellets on the surface of the sand, thus carapace length of the males ranged from 4.75 completing a long shaft (Fig. 4e). The crab has mm to 14.4 mm, and two modes were found at transformed the initial small air chamber into 6 mm and 9–10 mm. a long shaft, and subsequently into a larger Mainly, larger males appeared on the sand ovoid air chamber in deeper sand (Fig. 4f). surface at low tide (daytime: male/female ¼

Fig. 2. Construction of an ascending shaft from a large ovoid air chamber in the sand. Filled part indicates sand scraped off, scooped, and carried by the crab. (a) An ovoid air chamber and a resting crab in the sand during the emergence period. (b) Initial stage of construction of an ascending shaft. (c) Scraping of the sand from part of the wall in the chamber. (d) Transport of the scraped sand to the opposite wall of the chamber. (e) Early stage of the ascending shaft. (f ) Ascending shaft and ovoid air chamber ﬁlled with the transferred sand. 334 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 24, NO. 2, 2004 TAKEDA AND MURAI: BURROWING BEHAVIOR OF MICTYRID CRAB 335

192/9; night-time: 169/60) (Fig. 6). The carapace length of the males ranged from 10.1 mm to 15.05 mm in the daytime (one mode at 13 mm) and from 9.6 mm to 15.45 mm in the night-time (one mode at 12 mm; Fig. 6). The carapace length of the females appearing at the night-time low tide ranged from 8.65 mm to 11.75 mm (except for one female at 5.9 mm), corresponding to the second mode of carapace length in the subterranean females (Fig. 6). These results indicate that the smaller individuals fed in the tunnels, and larger females and males fed on the sand surface. Water-Table Depth in the Surface- and Subsurface-Feeding Area The tunnels were found on the well-drained sand at both the daytime and night-time low tides (Table 4). The subsurface-feeding area in the daytime closely overlapped the night-time area, although the water-table depth was slightly different between the daytime and night-time. In the daytime, the crabs fed while walking around the shoreline in droves; the water-table depth was close to 0 cm (Table 4). In the night- time, the crabs did not aggregate in droves. They fed separately on the sand surface in a wide range beyond the subsurface-feeding area; the range of Fig. 4. Enlargement of a small air chamber to allow the water-table depth was between 0.30 cm and feeding while making a tunnel on the sand surface. (a) Crab 34.4 cm. They engaged in surface activities and a small air chamber ascending to the surface of the sand. from just after exposure to before the dead low (b) Pushing away the sand masses scooped from the bottom tide in the daytime (about 2 h), but to before of the air chamber onto the surface of the sand. (c) Shaft constructed by enlargement of the small air chamber. (d) submergence in the night-time (more than 4 h). Transport of a sand pellet scooped from the bottom to After feeding on the sand surface, the crabs the ceiling in the enlarged shaft. (e) Early stage of the buried themselves only in the semi-fluid sand transformation of the shaft into an ovoid air chamber. (f ) slightly above the shoreline in the daytime, but Large air chamber transformed from the enlarged shaft. in both the semi-fluid and well-drained sand in the night-time; the range of the water-table engaged in the surface activities differed between depth was between –0.25 cm and –1.88 cm in the daytime and night-time low tides. During the the daytime, and between –0.38 cm and –33.9 daytime low tide, the large individuals fed in cm in the night-time. The highest limit of the droves in the narrow area near the shoreline burial area in the night-time was greatly higher (Table 4, Fig. 6). When they perceived danger, than that in the daytime. they quickly buried themselves directly in the DISCUSSION fluid sand (Table 1), like ocypodid crabs inhabiting sandy and muddy shores Surface Feeding (e.g., Takeda et al. 1996). After ceasing surface

The extent of the area where the mictyrid crabs activities, they retreated into the semi-ﬂuid, soft !

Fig. 3. Tunnel construction and feeding behavior. (a) The crab has ascended beneath the surface of the sand using a long, hollow shaft. (b) Opening the shaft. (c) Pushing up the sand mass that covered the rim of the shaft. (d) Scooping out the sand mass at the margin of the ﬂoor of the shaft. (e) Attaching the scooped-out sand mass to the outer margin of the sand covering the opening of the shaft. (f ) Scooping out the sand mass just beyond the opening of the sand roof. (g) Sideways walking in the tunnel while carrying the sand mass. (h) Attaching the sand mass to the outer margin of the sand roof. 336 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 24, NO. 2, 2004

Fig. 5. Sequential changes in the height of the water level (triangles) and tunnel coverage (circles; mean 6 SD, n ¼ 3) on the surface of the sand, during the daytime low tides of 23 and 25 May 1998. sand slightly above the shoreline (Fig. 1, Table refuge from predators that depend on sight, such 4). During the night-time low tide, however, they as birds. In this case, the formation of groups fed separately in a wide area from the shoreline to increases the number of guards (Kenward, slightly above the subsurface-feeding area (Table 1978) and reduces each individual’s chance of 4). When we approached them, they began predation (Calvert et al., 1979). In addition, the corkscrew-style digging in both the waterlogged, return to the subsurface-feeding area at night fluid sand and the well-drained, firm sand. After may help crabs evade predation. ceasing surface activities, they retreated into the Only large Mictyris longicarpus males walk well-drained, firm sand where they could engage to the shoreline and feed there, then return to in subsurface feeding after enlargement of the their subsurface-feeding area during the daytime small air chamber (Fig. 4), or into the semi-fluid low tide (Cameron, 1966; Dittmann, 1998). The sand slightly above the shoreline. These results juveniles and females never go to the shore- indicate that the large individuals, which fed line, although they emerge and feed on the around the shoreline at the daytime low tide, surface. Mictyris longicarpus grow larger than moved to the subsurface-feeding area at the M. brevidactylus (McNeill, 1926; Takeda, night-time low tide, because we found many 1978). The large body of the males may allow small depressions made by the emergence of the them to evade predation and to return to the crabs on the surface in the area above the subsurface-feeding area from the shoreline. shoreline. Zimmer-Faust (1987) has reported that the Subsurface Feeding small ocypodid crab Scopimera inflata H. Like M. longicarpus (see Quinn, 1986), M. Milne-Edwards, 1873, restricts its feeding area brevidactylus made the tunnel separate from the to near its burrow in the daytime owing to the hollow ascending shaft only when the sand was risk of predation and to physical stresses. At our drained (Figs. 2, 3, 5, Table 1). Our observa- study site, the mictyrid crabs were sometime tions (Fig. 3) reveal that the mictyrid crabs preyed upon by plovers and fiddler crabs (Uca evolutionarily acquired the habit of making the perplexa (H. Milne-Edwards, 1837)), which tunnel and feeding in it after or simultaneous inhabit the upper area of their habitat. These with the advance to the tidal flat; a tunnel predators, however, never fed at this study site without lining could not maintain its shape in at night. The fact that the crabs fed on and the sea (Takeda and Kurihara, 1987). buried themselves in the well-drained, firm sand When the crabs perceived danger in the at night, where they required a longer period tunnel, they returned to their ascending shaft, and heavier labor to bury themselves, strongly and then buried themselves in the fluid or suggests that the surface feeding in the daytime semi-fluid sand at the bottom of the shaft. is restricted to near the shoreline to secure easy We consider that the sand roof of the tunnel TAKEDA AND MURAI: BURROWING BEHAVIOR OF MICTYRID CRAB 337

Table 3. Proportion of tunnels connected with a hollow shaft or a plugged shaft at three stages of tunnel coverage (see Fig. 5).

Hollow Plugged Timing shaft shaft Tunnels covered ca. 10% of the surface 92.5% 7.5% (time coverage just beginning) (n ¼ 53) Tunnels covered ca. 40% of the surface 90.9% 9.1% (time of rapid coverage) (n ¼ 55) Tunnels covered ca. 60% of the surface 5.7% 94.3% (coverage not changing) (n ¼ 53)

functions as a shelter to allow this forward- walking mictyrid crab, which moves more slowly than sideways-walking crabs, to reach the refuge of the ascending shaft. The sand roof of the tunnel, and the manner of scooping the fresh sediment from just beyond the forward end of the tunnel, prevents the direct discovery of the crab and the opening of the ascending shaft by predators that depend on sight to find prey. In addition, the tunnel may protect the crab, especially small individuals that have a wider body surface area relative to larger crabs, from water loss due to evaporation, desiccation, and heat during feeding, and consequently enhance their feeding efficiency. In the daytime, the subsurface-feeding period was only 1 h (Fig. 6), although the crabs fed while making a tunnel as a shelter (Fig. 3). The Fig. 6. Size frequencies of the crabs collected in the start of the subsurface feeding after the water sediment where many tunnels were made (bottom), on table has been drained away is probably related the sand surface in the night-time low tide (middle), and in to the retention of sufficient depth or length of the daytime low tide (upper). the ascending shaft as a refuge for the crab, because a hollow shaft connected with the outside environment is unstable in the fluid sand sand to evade imminent danger, because the sand below the water table (Takeda and Kurihara, in the shaft bottom becomes gradually drained 1987). In addition, the end of the subsurface and firm as the water table falls. The short feeding before dead low tide may be dictated by feeding time may be compensated by feeding in the crab’s need to descend to a safer depth in the air chamber (personal observation) and an a large air chamber made from the plugged increase in the sorting efficiency of organic ascending shaft or to bury itself in the bottom matter in the sediment (Quinn, 1986).

Table 4. Water-table depths (cm) of the lower and upper limits of the areas where the crabs fed on the sand surface or in the tunnel (subsurface), or where they buried themselves after ceasing their surface activities.

Subsurface feeding Surface feeding Burial

Lower Upper Lower Upper Lower Upper Daytime 15.6 6 1.49 28.9 6 1.31 0.63 6 0.15 0.20 6 0.24 0.25 6 0.29 1.88 6 0.25 Night-time 18.5 6 1.29 24.6 6 3.73 0.30 6 0.36 34.4 6 1.49 0.38 6 0.48 33.9 6 0.85 jzj* 2.191 1.888 1.348 2.323 0.316 2.366 P 0.0284 0.0591 0.1176 0.0202 0.7518 0.0180

* Mann-Whitney test. 338 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 24, NO. 2, 2004

Communal Feeding Cooperative Research Projects of the Tropical Biosphere Research Center, University of the Ryukyus, and Grant-in- Small individuals of M. brevidactylus fed Aid for Scientific Research (C) from Japan Society for the beneath the surface of the sand, but large in- Promotion of Science (No. 12640605). dividuals fed on the surface of the sand while walking in droves near the shoreline in the daytime low tide (Yamaguchi, 1976; Nakasone and Akamine, 1981). The feeding of crabs in LITERATURE CITED droves near the shoreline is seen with ocypodid Altevogt, R. 1957. Beitrage zur Biologie und Ethologie von crabs, such as Macrophthalmus japonicus (de Dotilla blanfordi Alcock und Dotilla myctiroides (Milne- Haan, 1835) (Henmi, 1984, 1989); Scopimera Edwards) (Crustacea Decapoda).—Zeitshrift fu¨r Morpho- logie und Oekologie der Tiere 46: 369–388. globosa (de Haan, 1835) (Ono, 1965; Yama- Calvert, W. H., L. E. Hedrick, and L. P. Brower. 1979. guchi and Tanaka, 1974; Koga, 1995); Dotilla Mortality of the monarch butterfly, Danaus plexippus: fenestrata (Hilgendorf, 1869) (MacNae and avian predation at five overwintering sites in Mexico.— Kalk, 1962; Hartnoll, 1973); Dotilla myctiroides Science 204: 847–851. Cameron, A. M. 1966. Some aspects of the behaviour of the (H. Milne-Edwards, 1852) (Tweedie, 1950; soldier crab, Mictyris longicarpus.—Pacific Science 20: Altevogt, 1957); Uca pugilator (Bosc, 1802) 224–234. (Salmon and Hyatt, 1983; Christy and Salmon, Christy, J. H., and M. Salmon. 1984. Ecology and evolution 1984); and Uca vocans (Linnaeus, 1758) (Murai of mating systems of fiddler crabs (genus Uca).— et al., 1983; Nakasone et al., 1983). Koga Biological Review 59: 483–509. Cowles, R. P. 1915. The habits of some tropical Crustacea: (1995) concluded, as a result of field investiga- II.—Philippine Journal of Science 10: 11–18. tions, that this behavior was related to energy Dittmann, S. 1998. Behaviour and population structure of requirement in dense habitats, and the crabs soldier crabs Mictyris longicarpus (Latreille): obser- used a wide area of the tidal flats to permit an vations from a tidal flat in tropical North Queensland, Australia.—Senckenbergiana Maritima 28: 177–184. increase in their population size. Feeding in Fielder, D. R. 1970. The feeding behaviour of the sand crab droves by M. brevidactylus occurs only in Scopimera inflata (Decapoda, Ocypodidae).—Journal of habitats where they live in dense populations Zoology 160: 35–49. (Yamaguchi, 1976). These observations strongly Hartnoll, R. G. 1973. Factors affecting the distribution and suggest that it is also related to energy re- behaviour of the crab Dotilla fenestrata on East African shores.—Estuarine and Coastal Marine Science 1: 137– quirement, as pointed out by Koga (1995) for 152. S. globosa. The feeding individuals of M. brevi- Henmi, Y. 1984. The description of wandering behavior and dactylus moved together along the shoreline, its occurrence varying in different tidal areas in Macro- which was itself moved according to the tide, phthalmus japonicus (De Haan) (Crustacea: Ocypodi- dae).—Journal of Experimental Marine Biology and and they fed widely over the tidal flat, in Ecology 84: 211–224. contrast with their feeding behavior while ———. 1989. Factors influencing drove formation and making the tunnel. Feeding in droves near the foraging efficiency in Macrophthalmus japonicus (De shoreline is thought not only to enable use of the Haan) (Crustacea: Ocypodidae).—Journal of Experimen- food sources of the lower part of the sandy tidal tal Marine Biology and Ecology 131: 255–265. Kenward, R. E. 1978. Hawks and doves: factors affecting flat (e.g., Ono, 1965; Murai et al., 1983), but success and selection in goshawk attacks on wood- also to allow evasion of immediate dangers by pigeons.—Journal of Animal Ecology 47: 449–460. rapid direct burial in the fluid sand. The ac- Koga, T. 1995. Movements between microhabitats depend- quisition of the habit of making an air chamber ing on reproduction and life history in the sand-bubbler crab Scopimera globosa.—Marine Ecology: Progress and subsequently descending into the sand Series 117: 65–74. together with it, and modifying the small air Kraus, H. J., and J. Tautz. 1981. Visual distance-keeping in chamber to a large one in order to feed beneath the soldier crab, Mictyris platycheles Latreille (Grapsoi- the surface of sand while making a tunnel, may dea: Mictyridae). A field study.—Marine Behaviour and allow the crabs to inhabit more safely the lower Physiology 6: 123–133. MacNae, W., and M. Kalk. 1962. The fauna and flora of parts of the sandy tidal flats where they cannot sand flats of Inhaca Island, Mocambique.—Journal of construct tube type burrows. Animal Ecology 31: 93–128. Maitland, D. P., and A. Maitland. 1992. Penetration of water into blind-ended capillary tubes and its bearing on the functional design of the lungs of soldier crabs Mictyris ACKNOWLEDGEMENTS longicarpus.—Journal of Experimental Biology 163: We thank Mrs. Y. Nakano and S. Nakamura and other staff 333–344. of Sesoko Station, Tropical Biosphere Research McNeill, F. A. 1926. Studies in Australian carcinology, Center, University of the Ryukyus, for facilitating our No. 2. A revision of the family Mictyridae.—Records of work there. This study was partially supported by Australian Museum 15: 100–128. TAKEDA AND MURAI: BURROWING BEHAVIOR OF MICTYRID CRAB 339

Murai, M., S. Goshima, and Y. Nakasone. 1983. Adaptive Takeda, S., and Y. Kurihara. 1987. The distribution and droving behavior observed in the fiddler crab Uca abundance of Helice tridens (De Haan) burrows and vocans.—Marine Biology 76: 159–164. substratum conditions in a northeastern Japan salt marsh Nakasone, Y., and T. Akamine. 1981. The reproduction (Crustacea: Brachyura).—Journal of Experimental Marine cycle and young crab’s growth of the soldier crab Mictyris Biology and Ecology 107: 9–19. brevidactylus Stimpson, 1858.—Biological Magazine ———, M. Matsumasa, H.-S. Yong, and M. Murai. 1996. Okinawa 19: 17–23. [In Japanese.] ‘‘Igloo’’ construction by the ocypodid crabs, Dotilla ———, H. Okamine, and K. Asato. 1983. Ecology of the myctiroides (Milne-Edwards) (Crustacea: Brachyura): the fiddler crab Uca vocans vocans (Linnaeus) (Decapoda: role of an air chamber when burrowing in a saturated Ocypodidae). II. Relation between the mating system and sandy substratum.—Journal of Experimental Marine drove.—Galaxea 2: 119–133. Biology and Ecology 198: 237–247. Ono, Y. 1965. On the ecological distribution of ocypodid Tweedie, M. W. F. 1950. Notes on grapsoid crabs from crabs in the estuary.—Memoirs Faculty of Science, the Raffles Museum.—Bulletin of Raffles Museum 23: Kyushu University, Series E (Biology) 4: 1–60. 310–324. Quinn, R. H. 1986. Experimental studies of food ingestion Yamaguchi, T. 1976. A preliminary report on the ecology of and assimilation of the soldier crab, Mictyris longicarpus the sand bubbler crab, Mictyris longicarpus Latreille.— Latreille (Decapoda, Mictyridae).—Journal of Experi- Benthos Research, Japan 11/12: 1–13. [In Japanese.] mental Marine Biology and Ecology 102: 167–181. ———, and M. Tanaka. 1974. Studies on the ecology of Salmon, M., and G. W. Hyatt. 1983. Spatial and temporal a sand bubbler crab, Scopimera globosa De Haan aspects of reproduction in North Carolina fiddler crabs (Decapoda: Ocypodidae). I. Seasonal variation of popula- (Uca pugilator Bosc).—Journal of Experimental Marine tion structure.—Japan Journal of Ecology 24: 165–174. Biology and Ecology 70: 21–43. [In Japanese with English summary.] Takahasi, S. 1935. Ecological notes on the ocypodian crabs Zimmer-Faust, R. K. 1987. Substrate selection and use by (Ocypodidae) in Formosa, Japan.—Annotationes Zoolog- a deposit-feeding crab.—Ecology 68: 955–970. icae Japonenses 15: 78–87. Takeda, M. 1978. Soldier crabs from Australia and Japan.— Bulletin of National Science Museum, Tokyo, Series A RECEIVED: 9 June 2003. (Zoology) 4: 31–38. ACCEPTED: 9 January 2004.