Journal of Experimental Marine Biology and Ecology 390 (2010) 160–168

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Journal of Experimental Marine Biology and Ecology

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Habitat partitioning between prey soldier crab Mictyris brevidactylus and predatorfiddler crab Uca perplexa

Satoshi Takeda ⁎Marine Biological Station, Tohoku University, Asamushi, Aomori 039-3501, Japan

⁎ Tel.: +81 17 752 3388; fax: +81 17 752 2765.E-mail address: stakeda@mail.tains.tohoku.ac.jp.

0022-0981/$ – see front matter © 2010 Elsevier B.V. Adoi:10.1016/j.jembe.2010.04.039

a b s t r a c t

a r t i c l e i n f o

Article history:Received 10 March 2010Received in revised form 28 April 2010Accepted 28 April 2010

Keywords:Aggregation mechanismBioturbationBurrowing behaviourFiddler and soldier crabsHabitat segregationSandy tidal flat

Interaction and habitat partition between the soldier crab Mictyris brevidactylus (prey) and the fiddler crabUca perplexa (predator) were examined at a sandy tidal flat on Okinawa Island, Japan, where they co-occur.Both live in dense colonies. When the soldier crabs were released in the densely populated habitat of thefiddler crab, male fiddler crabs, which maintain permanent burrows in hard sediment, preyed on smallsoldier crabs and repelled large ones. Thus, the fiddler crabs prevented the soldier crabs from trespassing. Itwas also observed whether soldier crabs burrowed successfully when they were released 1) where soldiercrab burrows just under the sand were abundant, 2) in a transition area between the two species, 3) an areawithout either species, and 4) where artificial tunnels simulated soldier crabs' feeding tunnels were made bypiling up sand in the area lacking either species. In contrast to the non-habitat area, many soldier crabsburrowed in the sediment near the release point in the tunnel, transition and artificial tunnel areas. Thisindicates that the feeding tunnels on the surface attracted other crabs after emergence. When the large malefiddler crabs were transplanted into the artificial burrows made in soft sediment of the soldier crab habitat,all left their artificial burrows by 2 days. In the fiddler crab habitat, however, about one-third of thetransplanted male fiddler crabs remained in the artificial burrows after 3 days. The soldier crabs regularlydisturb the sediment by the up and down movement of their burrow (small air chamber) between tides. Thisdisturbance probably prevents the fiddler crab from making and occupying permanent burrows. Thus, itappears that these crabs divide the sandy intertidal zone by sediment hardness and exclude each other bydifferent means.

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1. Introduction

Estuarine crabs that dig burrows in the sediment partition theirhabitats along the gradient of salinity (Ono, 1965; Nakasone, 1977), bywater condition in the sediment (Takeda and Kurihara, 1987;Henmi, 1989), by the grain size distribution of the sediment (Macnae,1968; Sasekumar, 1974; Wada, 1982), by the hardness of the sediment(Bertness andMiller, 1984; Kelaher et al., 1998), and by the presence orabsenceof structures in or on the sediment (Ringold, 1979; Bertness andMiller, 1984; Kurihara et al., 1989; Nobbs, 2003).

In the sandy and muddy bare flats (without vegetation) of the westPacific region, Ocypodidae and Mictyridae dominate the crab commu-nity (McNeil, 1926; Macnae, 1968; Sasekumar, 1974; Crane, 1975).Their surface activities usually are centered on their burrows (Crane,1975;Kitaura et al., 1998),whichare used for protection frompredators,as refuges from environmental stresses (Macnae, 1968; Crane, 1975;Warner, 1977; Montague, 1980), and also as sources of water (Crane,1975; Takeda and Murai, 2003).

Except for a few species of carnivorous Ocypode (Hughes, 1966;Wolcott, 1978), these crabs feed onfine organicmatter includingmicro-and meiobenthos in the sediment near the surface (Altevogt, 1957;Miller, 1961; Ono, 1965; Dye and Lasiak, 1986; Wolfrath, 1992). Thefeeding organs of these crabs have different shapes allowing effectivefeedingonmuddy and sandy sediments andon rocks (Crane, 1975; Icelyand Jones, 1978; Rosenberg, 2002; Takeda and Murai, 2003; Takedaet, al., 2004), in addition to the behavioural adaptation (Takeda andMurai, 2003). Moreover, they have developed specialized mouth parts,notably three pairs of maxillipeds, to select fine organic matter in thesediment (Miller, 1961; Robertson and Newell, 1982; Vogel, 1984),being known as “floating feeders” for their manner of feeding (Dye andLasiak, 1986). Therefore, it has been considered that the sedimenttexture affects the distribution and abundance of these deposit-feedingcrabs (Ono, 1965).

Predationby larger ocypodid crabs on smaller oneshas recently beenreported. Koga et al. (1995) andMilner et al. (2010) reported that largemale fiddler crabs (Uca tetragonon or U. annulipes) preyed upon smallconspecific and other ocypodid individuals in the rocky shore on PhuketIsland, Thailand, ormudflats on Inhaca Island,Mozambique. Kitaura andWada (2005) observed that large sentinel crabs (Macrophthalmus bosciiandM. convexus) preyed on small conspecific individuals on tidalflats in

Fig. 1. Soldier crabs (centre and upper) and their burrows in the form of long horizontaltunnels under the sand.

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Japan. Moreover, Pratt et al. (2002) and McLain et al. (2003) observedthat large male fiddler crabs (Uca minax) moved to their prey habitatandpreyedupon small individuals (Uca pugilator andUcapugnax) in thetidal flat of eastern USA. These observations strongly suggest that thespatial and temporal distributions and abundance of ocypodid crabs areaffected by prey–predator interactions among them, as is the case forrelationships between other prey and predator crabs (U. pugnax andEurytium limosum: Teal, 1958; Lee and Kneib, 1994: Macrophthalmusjaponica and Helice tridens: Kurihara et al., 1989: Uca uruguayensis andChasmagnathus granulatus: Daleo et al., 2003).

In the subtropical estuaries of southern Japan, the soldier crabMictyris brevidactylus and the fiddler crab Uca perplexa both occupysandy to muddy–sandy tidal flats: the soldier crab above the lowwaterlevel of the spring tide (Yamaguchi, 1976), and thefiddler crab betweenthe low and high water levels of the neap tide (Nakasone, 1977).In general, these two crabs segregate on large tidal flats. They both digburrows and feed on fine organic matter deposited on the surface(Yamaguchi, 1976; Murai et al., 1982; Takeda and Murai, 2004).

The soldier crabs and the female fiddler crabs use two slender,small chelipeds when feeding. The male fiddler crabs use only onesmall cheliped, because the other cheliped is hypertrophied and isused in courtship and combat (Crane, 1975; Levinton and Judge, 1993;Levinton et al., 1995). Fiddler crabs, especially males, prey on smallcrabs, including conspecifics (Koga et al., 1995; Pratt et al., 2002).Likewise, it has been seen male U. perplexa preying on trespassingsoldier crabs on Okinawa (personal observation), suggesting that thefiddler crab may affect the distribution and abundance of the soldiercrab where they co-occur.

On Okinawa, male fiddler crabs U. perplexa reach about 19 mm incarapace width with females slightly smaller at 16 mm carapace width(Nakasone and Okadome, 1981). The crabs dig closely-spaced,individual permanent burrows (Nakasone and Murai, 1998). Duringthe daytime low tide they emerge from the burrows and engage insurface activities nearby. At night and during the daytime high tide, theystay in the plugged burrows (Nakasone and Murai, 1998). Theyreproduce between April and September (Nakasone and Murai, 1998),when burrow ownership changes every few days (unpublished data) inconsequence of their breeding system (Nakasone and Okadome, 1981;Nakasone and Murai, 1998). The juveniles recruit mainly between Julyand November (Nakasone and Okadome, 1981).

The soldier crab M. brevidactylus, with a spherical body, grows toabout 16 mm long among males and 14 mm among females(Nakasone and Akamine, 1981). The crabs feed on detritus in twoways (Yamaguchi, 1976; Takeda and Murai, 2004). During both thedaytime and night-time at low tide, on well-drained sand in the upperpart of their habitat, both small and large crabs usually make a tunnelrunning parallel to the surface and roofed with sand to concealthemselves while they feed (Fig. 1). After feeding, they return to anascending shaft from which they had emerged earlier. They thendescend in the sediment with the plugged shaft and transform theshaft into an ovoid air chamber at a sufficient depth (Takeda andMurai, 2004). During the daytime low tide, on the waterlogged, fluidsand near the shoreline, large crabs after emergence feed in droves onthe surface while staying with the shoreline as it moves with the tide(Yamaguchi, 1976; Takeda and Murai, 2004). After feeding arounddead low tide mark, they make a small air chamber slightly above theshoreline by using corkscrew-style digging, and descend into the fluidsand together with the air chamber (Takeda and Murai, 2004). Duringthe night at low tide, large crabs emerge and wander about, feedingindividually on both the fluid sand near the shoreline and the well-drained firm sand in the upper habitat, and then burrow into the sand(Takeda and Murai, 2004). A proportion of the large crabs that haveburrowed into the sediment slightly above the shoreline in daytime atdead low tide return to the upper, subsurface-feeding area to make asmall air chamber for the low tide at night. Later, at low tide, theyreconnect the small air chamber to a long shaft to allow subsurface

feeding (Takeda and Murai, 2004). They reproduce between Decem-ber and February (Nakasone and Akamine, 1981; Takeda, 2005). Thejuveniles are recruited mainly between February and April (Nakasoneand Akamine, 1981).

The aim of this study was to clarify how the distribution of bothfiddler and soldier crabs is determined. The differences in theirbehaviour between the daytime and night-time strongly suggest thatsoldier crabs are affected by the presence of the fiddler crabs on thesediment surface. First, the prey–predator relationship between themwas clarified in relation to their body sizes, and the effects of the fiddlercrab and the feeding tunnel of the soldier crab on the behaviour of thesoldier crab were examined at daytime low tide. The texture of thesurface sediment that affected the feeding andburrowingbehaviour andburrow structure was examined. Moreover, a transplantation experi-ment was carried out in the field to clarify whether the distribution ofthe fiddler crab is affected by the soldier crab and sediment texture.

2. Materials and methods

2.1. Study site

The experiments were carried out on a sandy tidal flat on the bankof the Okukubi estuary, Okinawa, Japan (26° 27′ N; 127° 56.5′ E). Amangrove forest backs the tidal flat. U. perplexa inhabits the sandy flatbetween the low and high water levels of the neap tide. M.brevidactylus inhabits the sandy flat above the low water level ofthe spring tide. The habitats of both crabs adjoined in a transition areaabout 1 m wide and 8 m long around the low water level of the neaptide. Another area lower than the mean water level had no crabs.

2.2. Predation experiment

To clarify whether the fiddler crab preys on the soldier crab,experiments were carried out during the daytime low tide between 29September and 10 October 2008. Soldier crabswere collected at a sandyflat in Katabaru estuary (26° 30.5′ N; 128° 00′ E) each day for theseexperiments, and measured the carapace length (nearest 0.05 mm)with calipers. At Okukubi, in the habitat of the fiddler crab, a soldier crabwas placed on a cork plate (10 cmdiameter) and coveredwith a conicalbluevessel (about6 cmdiameter). After a fewminutes,when thefiddlercrabs had resumed their activities, the vessel was opened carefully bypulling on a fine string. Usually, the soldier crab walked off after a few

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seconds. The behaviour of the soldier crabwas recorded for 2 min, afterwhich it walked too far to follow (N6.5 m).

The fate of each soldier crab was recorded as: eaten by a fiddlercrab, attacked but not eaten, not attacked, or hid in the sedimentwithout attack. When the soldier crab was eaten, the time (s) whenthe fiddler crab attacked it, and the minimum distance (cm) betweenthe plate and the point where the fiddler crab attackedwere recorded.Then the diameter (nearest 0.05 mm) of the fiddler crab's burrowwasmeasured with calipers. The plate was set up again on the surfacemore than 2 m away from the previous site for the next observation.

At dead low tide on 15October 2008, a quadrat (50 cm×50 cm)wasplaced randomly 20 times on the surface of the sediment, and thenumber of female and male fiddler crabs that emerged on the surfaceduring 10 minwas counted. Then the diameter of each burrow openingwas measured. The carapace width of the male fiddler crab that preyedupon the soldier crabwasestimatedby linear regression showinga closerelationship between the diameter (X, mm) and the carapace width (Y,mm) (Y=1.133X+1.451, r=0.939, n=58) (Takeda, 2006).

2.3. Burrowing behaviour

To clarify whether the behaviour of the soldier crab is affected bythe presence either of the fiddler crab or the feeding tunnels of soldiercrabs, experiments were carried out at Okukubi during 2 h around thedaytime dead low tide between 2 and 12 October 2008. The behaviourof the soldier crabs was observed where the habitats of both crabsadjoined, and an area between low and high water of the neap tidewhere neither crab frequented (called here non-habitat), but wherethe small ocypodid crab Scopimera globosa inhabited (b1 m−2).

The adjoining area was divided into three parts: (1) tunnel area,where only tunnels were observed (tunnel coverage in the quadrat(50 cm×50 cm), mean±SD: 75.83±8.61%, n=6); (2) fiddler crabarea, where only fiddler crabs were observed; and (3) transition area,with both tunnels (16.67±7.53%, n=6) and fiddler crabs during thedaytime low tide. The transition area was about 1 m wide along theshoreline between the tunnel area (nearer the shoreline) and thefiddlercrab area.

Soldier crabs were collected at Katabaru each day and divided intotwo groups: small crabs (carapace length b10mm), which had beenengaging in subsurface activities, and large crabs (N13mm), which hadbeen wandering on the surface. The cork plate (10 cm diameter) wasput on the centreline in the transition area, the tunnel area (about 1 mfrom the centreline), or the non-habitat area. The soldier crabs werereleased as above. The time when the soldier crabs began burrowinginto the sediment was recorded, because the time it takes them tocompletely bury themselves depends on the firmness of the sediment(Takeda and Murai, 2004). Subsequently, the minimum distance (cm)between the cork plate and the burrowwasmeasured, and thedirectionof the burrow (seaward, landward or intermediate) was recorded.When a soldier crab entered an existing tunnel, the entrance on thetunnel was regarded as the point of burrow. The plate was set up againon the surface more than 1 m away from the previous site for thenext observation.

In an “artificial tunnel” area created in the non-habitat area, thebehaviour of the soldier crabs was observed as above. Surface sedimentwas collected and formed into sand bars (artificial tunnels: 2 cm wide,15 cm long, and 1 cm high) using a trowel. Sixty sand bars (coverage:22.93%) were laid randomly in an area 1 m across. Then, small soldiercrabs were released at the centre of the area (large soldier crabs willwander beyond that range; see Results).

At daytime low tide on 14 and 15 October 2008, a quadrat(25 cm×25 cm) was placed randomly 5 times on the surface of thesedimentof the tunnel and transition areas and the crabs to15 cmdepthwere collected ina sievewitha2.5-mmmesh. The carapace lengthof thesoldier crabs and the carapacewidthof thefiddler crabsweremeasured,and the sex of the fiddler crabs was recorded.

2.4. Fiddler crab transplantation experiment

To clarify whether the fiddler crab can invade in the habitat of thesoldier crab, 26 (day 1) and 32 (day 2) large male fiddler crabs werecollected in traps set at the openings of the burrows during thedaytime low tide on 26 and 27 September 2008. The carapace widthdid not differ between days (mean±SD; day 1: 15.00±1.18 mm;day 2: 16.56±1.30 mm; ANOVA: F (1, 56)=3.920, p=0.0526). Thecarapace of each fiddler crab was marked with spots of coloured paint(Paint-marker PX-30, Mitsubishi, Japan) for discrimination. Eachindividual was put into an artificial burrow 13 mm wide and 15 cmdeep in the habitat of the soldier crabs (day 1, 50 m distant from thecollection area) or the fiddler crabs (day 2, 30 m distant), which wasmade by using a pipe. (Gravel at 15 cm below the surface preventedthe crabs from burrowing deeper.) The burrows were spaced 50 cmapart and distinguished by small numbered flags. Through binoculars,during 1 h around dead low tide every day to 7 October, it wasobserved whether each artificial burrow was opened or a markedfiddler crab occupied it.

On 14 October 2008, during low tide, a quadrat (25 cm×25 cm)was placed randomly 5 times on the surface of the soldier crab habitatand the crabs to 15 cm depth were collected in a sieve. In addition, aquadrat (50 cm×50 cm)was placed randomly 20 times on the surfaceof the fiddler crab habitat and the number of fiddler crabs engaged insurface activities was recorded.

2.5. Sediment disturbance

To examine how the crabs disturb the sediment by burrowing, 8-mm glass beads were used as an indicator, because it was expectedthat at this size, their heavy specific gravity would bury them deeperas the intensity of mixing increased. On 27 September 2008, 20 glassbeads were buried just under the sand. The beads were placed at50 cm intervals (4×5 grids) in the sediment of the fiddler crab habitatand the soldier crab habitat, and stakes were planted at the fourcorners of each site (2 m×2.5 m).

On 15 October, the sediment was removed carefully, and theminimumdistance (nearest 1 mm) between the sediment surface andthe top of each bead was measured.

2.6. Sediment texture

The sediment hardness, water content and silt-clay content in thehabitats of the soldier crabs and fiddler crabs were measured, becausethese physical factors of the sediment influence the distribution ofestuarine crabs.

The hardness wasmeasured with a soil hardness tester (Yamanaka;Fujiwara Seisakusho Ltd., Japan) at dead low tide on 10 October 2008.The measurements were carried out 15 times at each of five sites: thesoldier crab and fiddler crab habitats used for the transplantationexperiment, and the non-habitat, tunnel and transition areas usedobservations of the burrowing behaviour.

At dead low tide on 17 October 2008, sediment samples werecollected to a depth of 5 mm at each site. The water content of about100 g of sediment was measured as the difference between the wetweight and the weight after drying at 110 °C for 3 days. Part of eachsediment sample was passed through a sieve (mesh size 0.063 mm)and then dried at 110 °C for 2 days to give the silt-clay content. Eachwas measured three times in each sample.

3. Results

3.1. Predation experiment

After the vessel was opened, the soldier crabs did not move forseveral seconds (b1 min) on the cork plate, and then moved onto the

163S. Takeda / Journal of Experimental Marine Biology and Ecology 390 (2010) 160–168

surface of the sediment and walked about. While the soldier crabswere resting, the fiddler crabs did not approach them. But when theywalked about, the nearby male fiddler crabs smaller than them beaton the sediment surface with the tip of the flexed major cheliped,which faced the soldier crabs. When approached by soldier crabs, thesmall male fiddler crabs entered their burrows. In contrast, largermales approached and repelled the soldier crabs. Sometimes theyswiftly flipped the soldier crabs with the major cheliped, especiallywhen the soldier crabs began digging. When the large male fiddlercrabs attacked, the soldier crabs rose on their ambulatory legs in adefensive posture.

Only the large male fiddler crabs attacked the soldier crabs. Afterthey tried to repel the soldier crabs, they sometimes preyed on them.They captured the soldier crabs with their chelipeds and anteriorambulatory legs, snipped them with the major cheliped, and thencarried them into their burrows. On theway to the burrow, somemaleand female fiddler crabs tried to steal the soldier crabs.

All soldier crabs smaller than 8 mm were eaten by larger malefiddler crabs (Fig. 2). In contrast, no soldier crabs larger than 11 mmwere eaten, although they were attacked. On the soldier crabsbetween 8 and 11 mm, the smaller ones were eaten more frequently.However, a few that hid in the sediment immediately after movingonto it were not attacked (Fig. 2).

The time (Y, s) before soldier crabs were attacked increased withcarapace length (X, mm) (Y=14.02X−77.44, r=0.553, p=0.0002,n=41). The distance (Y, cm) between the cork plate and the point ofattack increased also with carapace length (Y=13.41X−66.01,r=0.535, p=0.0003, n=41). The burrow diameter of the male fiddlercrabs that preyed on the soldier crabs ranged from 7.85 to 14.60 mm,corresponding to a carapace width of 10.35 to 17.99 mm. The burrowdiameter (Y,mm)offiddler crabs that preyed on soldier crabswas largerthan the carapace length (X, mm) of the soldier crabswhichwere eaten,except in one case, suggesting a tendency of a positive relationship(Y=0.40X+7.81, r=0.305, p=0.0524, n=41; Fig. 3). Fiddler crabsthat did not attack large soldier crabs attacked small ones, suggestingthat they assess the size of the soldier crabs visually.

Fig. 2. Changes in theproportion of soldier crabs not attacked, hiding in sediment, attackedor eaten by fiddler crabs within 2 min after release in a fiddler crab habitat in relation tocarapace length. Numerals in parentheses above bars represent the numbers of soldiercrabs observed. : eaten, : attacked, : hid in sediment, : not attacked.

The density of the fiddler crabs was 33.2±8.5 m−2 (mean±SD;females, 9.0±6.4 m−2; males, 24.2±8.0 m−2). The burrow diametersranged from 3.15 to 9.65 mm (females) and from 3.85 to 13.35 mm(males). The burrow diameters showed a modal frequency distribution(Fig. 4), with modes of 8 mm (females) and 8–9 mm (males).

3.2. Burrowing behaviour

Carapace lengths of the soldier crabs did not differ among the areas(ANOVA; small crabs: F (3, 121)=0.651, p=0.5838; large crabs: F (2,92)=0.006, p=0.9937; Table 1).

The proportions of small crabs that burrowed seaward, landward orintermediately did not differ among the tunnel, transition, non-habitatandartificial tunnel areas (χ2 test:df=6,χ2=9.823,p=0.1323;Table2).Neither did the proportions of large crabs among the tunnel, transitionandnon-habitat areas (df=4,χ2=6.821,p=0.1457; Table 2). Thepointswhere the soldier crabs burrowed in the sediment were not biasedseaward or landward (χ2 test: pN0.05), except among the large crabsreleased in the tunnel area (χ2=11.819, p=0.0006; Table 2).

Small crabs burrowedsooner after release than the large ones ineacharea (ANOVA; tunnel area: F (1, 62)=10.608, p=0.0018; transitionarea: F (1, 58)=4.343, p=0.0416; non-habitat area: F (1, 63)=48.775,pb0.0001; Fig. 5). The time to burrow increased in the order oftransition=tunnelbartificial tunnel (small crabs only)=non-habitatarea (ANOVA; small crabs: F (3, 121)=4.383, p=0.0058; large crabs: F(2, 92)=36.132, pb0.0001; Fig. 5). The distance between the cork plateand burrow increased in the order of transition, tunnel and artificialtunnel (small crabs only)bnon-habitat area (ANOVA; small crabs: F (3,121)=3.900, p=0.0106; large crabs: F (2, 90)=71.526, pb0.0001;Fig. 6). More small crabs burrowed in the sediment within 50 cm of thecork plate than large ones in each area (Fisher's exact probability test:tunnel area: p=0.0002; transition area: p=0.0011; non-habitat:pb0.0001; Table 3). The proportion decreased in the order of tunnel,transition and artificial tunnel (small crabs only)Nnon-habitat area (χ2

test; small crabs: df=3, χ2=36.840, pb0.0001; large crabs: df=2,χ2=25.182, pb0.0001; Table 3). Few small crabs, however, burrowedfar from the release point at each site (maximum distance: transitionarea 101 cm, tunnel area 460 cm, artificial tunnel area 319 cm, non-habitat area 202 cm). In the artificial tunnel area, 2 of 8 small crabs leftthe area, then returned and burrowed. The time it took them to beginburrowing within 50 cm of the release point did not differ between thenon-habitat (mean±SD: 15.84±13.84 s, n=12) and artificial tunnel(19.24±22.46 s, n=25) areas (ANOVA: F (1, 35)=0.230, p=0.6342).

Fig. 3. Relationship between carapace length of soldier crabs eaten bymale fiddler crabsand burrow diameter of those fiddler crabs. Broken line indicates equal size.

Fig. 4. Frequency distributions of burrow diameter of female and male fiddler crabs inthe dense habitat where the soldier crabs were released.

Table 2Numbers of soldier crabs which retreated seaward, landward or intermediately afterrelease.

Site Small crabs Large crabs

Seaward Intermediate Landward Seaward Intermediate Landward

Tunnel 21 3 8 28 2 2Transition 13 10 7 22 1 7Non-habitat

12 7 13 24 0 9

Artificialtunnel

12 8 11

164 S. Takeda / Journal of Experimental Marine Biology and Ecology 390 (2010) 160–168

Proportionally more small crabs entered the tunnels (18/32) thanlarge ones (4/32) (Fisher's exact probability test: p=0.0005).Moreover, 27 of 31 small crabs tried to enter the artificial tunnels.Consequently, the time it took them to begin burrowing within 50 cmof the release point was longer in the artificial tunnel (mean±SD:19.24±22.46 s, n=25) than in the tunnel (8.63±6.48 s, n=30)areas (ANOVA: F (1, 53)=6.111, p=0.0167).

The densities of soldier crabswere 294.4±97.1 m−2 (mean±SD) inthe tunnel area and 166.4±56.1 m−2 in the transition area (ANOVA: F(1, 8)=6.517, p=0.0340). The carapace lengths ranged from 3.95 to7.85 mm and 5.05 to 9.85 mm, respectively (Fig. 7). These showed amodal frequency distribution (Fig. 7), with modes of 5–6 and 6–7 mm,respectively. The carapace lengths differed between the tunnel area(5.68±0.68 mm, n=92) and the transition area (6.72±0.93 mm,n=52; ANOVA: F (1, 142)=59.572, pb0.0001). On the other hand, thedensity of fiddler crabs was 9.6±8.8 m−2 in the transition area.

3.3. Fiddler crab transplantation experiment

After transplantation into the soldier crab habitat, the male fiddlercrabs fed on the surface of the sediment, threw out sand pellets fromthe artificial burrows, or retreated into them and plugged the opening.However, half of them left their artificial burrowswithin 1 day, and alldid so by 2 days (Fig. 8). Carapace widths did not differ between thosethat remained (mean±SD: 15.80±1.11 mm, n=11) and those thatleft the artificial burrows (15.53±1.45 mm, n=15) after 1 day(ANOVA: F (1, 24)=0.275, p=0.6045).

In the fiddler crab habitat, some transplanted male fiddler crabsfought with large male fiddler crabs near the artificial burrows. Morethan half of them left the artificial burrows within 1 day, and a fewmore did so by 2 days, but the rest remained (Fig. 8). Carapace widthsdid not differ between those that remained (14.77±0. 81 mm, n=9)and those that left within 3 days (15.09±1.30 mm, n=23; ANOVA: F(1, 30)=0.479, p=0.4944).

All fiddler crabs left the artificial burrows in the soldier crab habitatafter only 2 days. The proportion of crabs that remained in the artificial

Table 1Carapace length (mm) of soldier crabs released onto four sites for observations ofretreat into the sediment.

Site Small crabs Large crabs

n Mean±SD (Range) n Mean±SD (Range)

Tunnel 32 8.15±0.99 (6.60–9.75) 32 14.65±0.60 (13.05–15.85)Transition 30 8.35±0.92 (7.05–9.95) 30 14.64±0.61 (13.10–15.80)Non-habitat 32 8.24±0.88 (7.00–9.95) 33 14.64±0.67 (13.00–15.70)Artificial tunnel 31 8.05±0.89 (7.00–9.65)

burrows did not differ between thefiddler crab and soldier crab habitatsafter 1 day (Fisher's exact probability test: p=0.7903), but differedfrom 2 days (2 days: p=0.0013; ≥3 days: p=0.0029; Fig. 8).

In the soldier crab habitat, the density of soldier crabs was 329.6±61.6 m−2 (mean±SD). The carapace length ranged from 3.30 to9.15 mm, and showed a modal frequency distribution (Fig. 9), with amode of 5–6 mm. On the other hand, in the fiddler crab habitat, thedensity of fiddler crabs was 30.4±5.1 m−2 (females: 14.2±4.4 m−2;males: 16.2±5.3 m−2).

3.4. Sediment disturbance

The recovery rate of the glass beads was higher in the fiddler crabhabitat (19/20) than in the soldier crab habitat (11/20) (Fisher's exactprobability test: p=0.0044). The depth of the glass beads was greater inthe soldier crab habitat (mean±SD: 7.37±4.63 mm, n=11) than in thefiddler crab habitat (0.95±1.62 mm, n=19; ANOVA: F (1, 28)=19.447,p=0.0001), indicating that the sedimentwas disturbed frequently in thesoldier crab habitat, but little in the fiddler crab habitat.

3.5. Sediment texture

The sediment hardness varied among sites: non-habitatb tunnelarea=transition area=soldier crab habitatbfiddler crab habitat(ANOVA: F (4, 70)=102.242, pb0.001; Fig. 10). That is, the sedimentin the fiddler crab habitat was more compact than that in the areasinhabited bymany or few soldier crabs. Thewater content did not differamong thefive sites (ANOVA: F (4, 10)=2.071, p=0.1598; Fig. 10). Thesilt-clay content differed (ANOVA: F (4, 10)=81.321, pb0.0001;Fig. 10), increasing in the order of non-habitatb tunnel area=soldiercrab habitat=fiddler crab habitatb transition area (but, tunnel area b

fiddler crabs habitat). The fraction of silt-clay in the non-habitatwas lessthan half those of the other sites.

4. Discussion

4.1. Fiddler crab habitat

Male fiddler crabs attacked and killed soldier crabs with theirmajor cheliped. They carried the soldier crab back to their burrows toeat, and the burrow diameters were larger than the carapace length ofthe soldier crabs in all cases but one. All soldier crabs smaller than8 mm that were released in the fiddler crab habitat were eaten by themale fiddler crabs, but none larger than 11 mm were eaten, althoughthey were attacked. Both the time and distance to attack by the malefiddler crabs increased with the carapace length of the soldier crabs,indicating that small soldier crabs encountered male fiddler crabscapable of predation sooner than large ones. These results may beattributable to the frequency distribution of the burrow diameter ofthe male fiddler crabs, with a mode at 8–9 mm.

Male fiddler crabs that did not attack the large soldier crabssometimes attacked the small ones. This observation indicates that thebehaviourof thefiddler crabswas affectedby thebody size of the soldier

Fig. 5. Time (+SD) until soldier crabs began to burrow after release. Values with different letters in each column are significantly different (ANOVA: pb0.05).

165S. Takeda / Journal of Experimental Marine Biology and Ecology 390 (2010) 160–168

crab, strongly suggesting that the fiddler crabs can visually measure thebody size of the soldier crabs before attacking them, as well as that ofconspecific females (Takeda, 2006). This could explain why the soldiercrabs raised themselves in defence, pretending to appear larger.

Large soldier crabs that were not attacked by fiddler crabs whilewalking about the fiddler crab habitat were attacked by all fiddler crabswhen they began digging: the fiddler crabs harassed the soldier crabsuntil they left. Thus, in addition to predation, the fiddler crabs drove thesoldier crabs away.

During the daytime and night-time low tides, the small soldier crabsrise up through the sediment with an air chamber and engage insubsurface feedingwhilemaking a tunnel on the surface, and then retreatback into the sediment with the air chamber (Takeda and Murai, 2004).Large soldier crabs longer than 8 mm sometimes emerge onto the surfaceand walk about while feeding (Yamaguchi, 1976; Nakasone andAkamine, 1981; Takeda and Murai, 2004; Takeda, 2005). During thedaytime low tide, theymove about and feed in droves near the shoreline.After feeding, they burrow in the soft, wet sediment slightly above theshoreline. During the night-time low tide, however, they walk aboutindividually all over the tidalflat andburrow in the sediment (Takeda andMurai, 2004; Takeda, 2005). Such behaviour of the large soldier crabs

Fig. 6. Distance (+SD) between point of release and point where soldier crabs burrowed. LaValues with different letters in each column are significantly different (ANOVA: pb0.05).

during the night-time low tide might be related to their large body sizeand the absence of disturbance from diurnal fiddler crabs.

It was never seem that soldier crabs emerged onto the sedimentsurface athighdensity in thefiddler crabhabitat (personal observation).This suggests that the soldier crabs are site-selective. Thewater and silt-clay contents in the sediment did not differ widely between the soldiercrab andfiddler crabhabitats. On the other hand, the sediment hardnessvariedwidely, and the hardness in thefiddler crab habitat was 5.2 timesthat in the soldier crab habitat. When soldier crabs burrow into thesediment, they work harder in firm, well-drained sediment than in soft,wet sediment (Takeda and Murai, 2004), and so may use sedimenthardness as a selection criterion. In contrast, fiddler crabs might preferharder sediment to prevent the burrows from collapsing, because theyuse their burrows for a long period (Nakasone and Murai, 1998).

4.2. Soldier crab habitat

Most small soldier crabs that were released in the tunnel, transitionand artificial tunnel areas burrowed in the sediment within 50 cm ofwhere theywere released. In the artificial tunnel area, two crabs that leftthe area returned and then burrowed, although they were unable to

rge crabs that left and returned to the transition and non-habitat areas were excluded.

Table 3Numbers of soldier crabs that retreated into the sediment b or N50 cm distant from thepoint of release.

Site Small crabs Large crabs

b50 cm N50 cm b50 cm N50 cm

Tunnel 30 2 13 19Transition 28 2 17 13Non-habitat 12 20 0 33Artificial-tunnel 25 6

Fig. 8. Changes in the proportions of male fiddler crabs that remained where they weretransplanted into a soldier crab habitat (solid circles) or a fiddler crab habitat(open circles). * indicates a significant difference at p=0.05 between a soldier crabhabitat and a fiddler crab habitat (Fisher's exact probability test: pb0.05).

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enter the tunnels. In contrast, fewer than one-third released in the non-habitat area burrowed into the sediment within 50 cm of where theywere released. Large soldier crabs showed a similar tendency. Thesefacts indicate that structures such as surface tunnels hasten burrowingby soldier crabs and consequently lead to their accumulation, especiallysmall crabs after emergence.

More than two-thirds of the male fiddler crabs that weretransplanted into artificial burrows in the fiddler crab habitat left theburrows within 3 days. Their evacuation was perhaps caused byintraspecific interactions. The remainder stayed in their burrows duringthe observation period. However, all male fiddler crabs that weretransplanted into the soldier crab habitat left there within 2 days,although there was little or no intraspecific interaction. The water andsilt-clay contents,which influence feeding and burrowing (Wada, 1982;Takeda and Kurihara, 1987), did not differ widely between the twohabitats. In the transition area, where the sediment hardness did notdiffer fromthat in the soldier crabhabitat, allfiddler crabs stayed in theirburrows during the observation period (personal observation),although their density was low. The density of the soldier crabs waslower in the transition area than in the tunnel area. These results suggestthat the evacuation of the fiddler crabs from the artificial burrows in thetunnel area is related to the density of soldier crabs.

Soldier crabs rise obliquely in the sediment with an air chamber thatthey made during the previous subsurface activity (Takeda andMurai, 2004). After feeding while making a tunnel, they descend againtogether with the air chamber. The angle of descent is 64° (SD=12°,n=14) (unpublished data). Therefore, when they rise in the sediment by15 cm from the starting position to the surface at 64°, they move about16.7 cmobliquely. Thus, they shift the sediment by the diameter of the airchamber through this distance. Unpublished data shows a closerelationship between carapace length (X, mm) and the diameter of theair chamber (Y,mm):Y=1.86X+2.36 (r=0.9136,n=46).Using ameancarapace length of 5.74 mm, this equation gives a mean diameter of13.04 mm. Their densitywas 329.6 m−2 in the soldier crab habitat wherethe fiddler crabs were transplanted. These values indicate that the soldier

Fig. 7. Frequency distributions of carapace length of soldier crabs in the areas withmany tunnels on the sediment surface (tunnel area) and with several tunnels and fewfiddler crabs (transition area), where the soldier crabs were released.

crabs disturb about 6.7% of the sediment through their burrowingactivities during one low tide. That is, the soldier crabs would disturb thesediment once 7.5 days, resulting that they prevent the sediment frombeing compact and hard. The differences in the recovery rate and depth ofthe glass beads between the soldier crab and fiddler crab habitats supportthis idea. In addition, they would encounter and collapse the artificialburrows in the sediment. The evacuation of the fiddler crabs from theburrowsmade in the soldier crab habitat appears to be explainable by thefrequent disturbance of the sediment by the soldier crabs.

In the transition area, however, the fiddler crabs, although at lowdensity, stayed in their burrows during the observation period. Thedensity of the soldier crabs therewas low too, and the coverage of tunnels,which indicate the frequency of subsurface activity, wasmuch lower thanthe value estimated from the density (density: transition area/tunnelarea=166.4/294.4=0.565; coverage: 16.67/75.83=0.220), althoughthe carapace length was slightly larger in the transition area. The lowfrequency of sediment disturbance by the soldier crabs may be related tothe long stay of the fiddler crabs.

By preying on the small soldier crabs and repelling the large ones fromtheir habitat, the fiddler crabs prevented the soldier crabs fromtrespassing. Moreover, the fiddler crabs' continued use of the same

Fig. 9. Frequency distribution of carapace length of soldier crabs in the dense habitatwhere the male fiddler crabs were transplanted in artificial burrows.

Fig. 10. Sediment texture (mean+SD) at the five sites where experiments were carriedout. Values with different letters in each column are significantly different (ANOVA:pb0.05).

167S. Takeda / Journal of Experimental Marine Biology and Ecology 390 (2010) 160–168

burrows (but frequent turnover of ownership in the reproductive season;Nakasone andMurai, 1998) restricted the reworking of the sediment andthe consequent decrease in sediment hardness that would have allowedthe soldier crabs to trespass. On the other hand, the soldier crabs excludedthe fiddler crabs from their habitat by their constant sedimentdisturbance. This reciprocal exclusion would be more effectual whenthe crabs aggregate densely, especially the soldier crabs, which excludethe predator fiddler crabs indirectly. The soldier crabs' subsurface-feedingtunnels attracted more soldier crabs, partially explaining their aggrega-tion. O'Connor and Van (2006) found that conspecific megalopaeinhabiting tidal flats accelerated their molting in response to sediment-associated cues. A similar behaviourwould help the aggregation of soldiercrabs,which reproduce inwinter,whenpredatorfiddler crabs are inactive(Nakasone andAkamine, 1981; Nakasone andOkadome, 1981; Nakasoneand Murai, 1998; Takeda, 2005). Thus, differences in characteristicsbetween the two species might enable them to segregate on sandytidal flats.

Acknowledgements

I thank Dr.M.Murai, Mrs. Y. Nakano and S. Nakamura and other staffof Sesoko Station, Tropical Biosphere Research Center, University of theRyukyus, for their help and facilitating my work there. I am grateful toDr. M. Murai and two anonymous reviewers for their invaluablesuggestions for this study. [SS]

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