BULLETIN OF MARINE SCIENCE, 63(1): 241–247, 1998 PAPER

SELECTION BY TWO DECAPOD ( GIBBESI AND SETICORNIS) ASSOCIATING WITH AN URCHIN ( ANTILLARUM) AT TOBAGO, WEST INDIES

Floyd E. Hayes, Victor L. Joseph, Horace S. Gurley and Brian Y. Y. Wong

ABSTRACT We studied the relationships among two of decapod crabs, and , associating with an urchin, , in shallow water along the coasts of Tobago, West Indies. The crabs did not associate with other shorter-spined urchin species, suggesting that the crabs gained protection by associating with the relatively long-spined D. antillarum. Most D. antillarum (83.4%; n = 259) lacked an associating ; P. gibbesi associated with D. antillarum more often (11.6% of ur- chins) than did S. seticornis (3.5%) and an unidentified crab (1.5%). We found no evi- dence that P. gibbesi and S. seticornis differed in their selection of D. antillarum hosts. We also found no evidence that the crabs selected D. antillarum hosts providing a poten- tially safer microhabitat by having longer spines, occurring in denser populations, occur- ring nearer to each other, or occurring in deeper water (within the depth range of this study). These results suggest that selection of D. antillarum hosts by P. gibbesi and S. seticornis is random, with minimal interspecific competition.

Decapod form symbiotic relationships with a variety of hosts, including (Ross, 1983). However, the ecological relationships of most symbioses re- main poorly studied. In the Sea, the spines of the long-spined urchin, D. antillarum, have been reported to provide refuge for a variety of commensal organisms, including an anemone, a flatworm, a copepod, a mysid shrimp, the young of many species, and a variety of decapod crustaceans including several palaemonid shrimp (Periclimenes sp., Stegopontonia sp., Tuleariocaris neglecta), a spiny lobster (Panulirus argus), and a grapsid crab (Percnon gibbesi; Randall et al., 1964; Chase, 1969; Clifton et al., 1970; Davis, 1971; Castro, 1974; Gooding, 1974; Serafy, 1979; Criales, 1984). The urchin crab, P. gibbesi, is a well known associate of D. antillarum (Schmalfuss, 1976; Adey et al., 1977; Powers, 1977; Colin, 1978; Kaplan, 1988; Humann, 1992). Colin (1978) stated that the crab gains protection from the relatively long, mildly toxic spines of the urchin, but the urchin apparently derives no benefit from the crab. The arrow crab, Stenorhynchus seticornis, has been observed closely associating with sponges, stony cor- als, soft corals, gorgonians, anemones and crinoids in the Bahamas and Virgin Islands (Barr, 1971, 1975; Herrnkind et al., 1976; Stanton, 1977; Schriever, 1978). However, there are only a few anecdotal reports of S. seticornis associating with urchins. Sefton and Webster (1986) reported that S. seticornis associated with urchins, but did not specify which species. When attempting to capture individual S. seticornis, Barr (1971: 220; 1975: 55) noted that “At times the crab would retreat among the spines of one or more urchins (Diadema). Whether this response was by design or chance is unknown, but the net result was extremely effective.” Adey et al. (1977: 36 and 49) stated that “Percnon gibbesi and Stenorhynchus hispidus are common near Diadema, crevices and sometimes anemones” in the Virgin Islands. However, it remains uncertain whether Adey et al. (1977) were referring to S. seticornis, of which S. hispidus is not a known (Goeke, 1989), or the coral spider crab, Mithrax hispidus.

241 242 BULLETIN OF MARINE SCIENCE, VOL. 63, NO. 1, 1998

During excursions in June and November 1994 to Tobago, we repeatedly observed both P. gibbesi and S. seticornis within 5 cm of and retreating under the spines of D. antillarum in shallow water (<5 m deep) along the coasts. We subsequently returned to Tobago to further study the relationships among these species and a third unidentified crab associat- ing with D. antillarum. This study reports for the first time the association of S. seticornis with D. antillarum. We tested the hypothesis that the three species of crabs differed in their selection of urchin hosts as a consequence of interspecific competition. We also tested the hypothesis that the crabs selected D. antillarum hosts providing a potentially safer microhabitat by (1) having longer spines, (2) occurring in greater densities, (3) occurring nearer to each other and (4) occurring in deeper water.

STUDY AREA AND METHODS

The island of Tobago is perched along the edge of the South American continental shelf in the southeastern Caribbean Sea. The marine environment of Tobago is dominated by the northward flowing Guyana current, and is seasonally influenced by discharges of freshwater and sediments from South American rivers (Kenny and Bacon, 1981). The coasts of Tobago are characterized by steeply sloping volcanic rock formations alternating with sandy embayments, with the rock forma- tions forming a foundation for patches of fringing coral reefs (Laydoo, 1985, 1991). More exten- sive fringing reefs occur on an elevated limestone platform along the southwestern coast of Tobago (Kenny, 1976; Kenny and Bacon, 1981; Laydoo, 1985, 1991). The coral reef ecosystems of Tobago have been described by Kenny (1976), Ramsaroop (1981) and Laydoo (1985, 1991). The maximum tidal range is about 1.3 m (Kenny and Bacon, 1981). During 22–24 March 1995 and 5 September 1996, we carefully examined 259 D. antillarum urchins during daylight on rock or coral substrates in shallow water (<5 m deep) at Mount Irvine Bay, Arnos Vale Bay, Bloody Bay and Man-of-War Bay; each locality is situated along the northern coast of Tobago. We recorded the species of crab and the number of individuals present within 5 cm of each D. antillarum. Four specimens of S. seticornis were later collected from the urchins and three from nearby gorgonians at Mount Irvine Bay; each was examined under a dissecting micro- scope and distinguished from the sympatric but deeper water (>30 m, thus unlikely to occur) S. yangi by the presence of dense felt and setae on the rostrum (Goeke, 1989). For each D. antillarum examined, we measured the following variables: (1) length (cm) of the longest spines, at the top of the urchin (using a transparent plastic ruler inserted between spines); (2) number of conspecific individuals within a 0.57 m radius (=1.0 m2); (3) number of individuals of other urchin species (an estimated 98% rock-boring urchins, Echinometra lucunter, and 2% slate-pencil urchins, Eucidaris tribuloides) within a 0.57 m radius (=1.0 m2); (4) distance (m) to the nearest conspecific individual; and (5) depth (estimated to nearest 0.5m) below the surface. Because of the low frequency of crabs associating with D. antillarum, the data from all four localities were pooled for subsequent analyses. A one-sample chi-square test (Χ2 statistic; Zar, 1984) was used to compare the proportions of crab species associating with D. antillarum. A one- way anova (F statistic; Zar, 1984) was used to test for differences in spine length and depth below the surface among D. antillarum with or without crabs; a posteriori multiple comparison tests were computed using student’s t test (t statistic; Zar 1984) with Bonferroni adjustments of the alpha level (Lentner and Bishop, 1986). Kruskal-Wallis tests (H statistic; Zar, 1984) were used to test for differences in density and nearest conspecific distance among D. antillarum with or without crabs. A student’s t test was used to compare spine length between D. antillarum with either one or two P. gibbesi. All tests were computed using Statistix 3.1 software (Anonymous, 1990). HAYES ET AL.: CRAB-URCHIN ASSOCIATIONS 243

ybnoitcelestsohgnitceffayllaitnetopselbairaV.1elbaT isebbignoncreP , suhcnyhronetS sinrocites nihcruehthtiwgnitaicossabarcdeifitnedinunadna .murallitnaamedaiD

INelbairavtnednepedn MDEASNMXIMNA Snipeelnhtgc(m)foD.aurallitnma noarcbeserptn 10.24208.560.9.1621 P.gibbesip8resent 171.720.965.7.103 S.seticornisp6resent 110.520.080.5.19 u5nidentifiedcrabpresent 80.220.550.1.14 Density(within0.57mradius)ofD.antillarumb n5ocrabpresent 15.71162.7 20 .Pbigisebp0tneser 29.01168.3 2 sinrocites.S p7tneser 13.61136.0 u5deifitnedin barc tneserp 10.20124.5 Dytisne(wnihti5.07m)suidarfollanihcru seicepsc n6obarc tneserp 23.4216.2 1220 P.gibbesip5resent 31.7416.3 182 S.seticornisp7resent 32.1311.9 16 u5nidentifiedcrabpresent 10.20124.5 Decnatsi(mot)tseraen.Daurallitnmd n4obarc tneserp 19.322.300.0.02220 P.gibbesip8resent 28.141.500.0.282 S.seticornisp0resent 25.731.800.0.16 u8nidentifiedcrabpresent 19.721.100..54 Depth(m)ofD.antillarumfromsurfacee n8ocrabpresent 29.005.805..4621 P.gibbesip0resent 23.005.805..303 S.seticornisp1resent 27.615.115..49 u0nidentifiedcrabpresent 12.505.805..24 aF=3.06,P=0.028;bH=1.83,P=0.61;cH=3.30,P=0.35;dH=0.82,P=0.84;eF=1.72,P=0.16

RESULTS

In the shallow waters of Tobago, P. gibbesi was ubiquitous on rocks both above and below the surface of the ocean within or just below the intertidal zone, and often did not associate with D. antillarum. In contrast, S. seticornis was considerably less common than P. gibbesi, associating almost exclusively with D. antillarum and an unidentified gorgonian at a minimum depth of 1 m. An unidentified red crab (probably Mithrax sp.) that eluded capture was found associating only with D. antillarum in shallow water. When found on the substrate within 5 cm of D. antillarum, each crab species quickly retreated under the urchin’s spines. The crabs followed the urchin when it moved as we measured and examined the urchin for associating crabs. Of 259 D. antillarum examined, 43 (16.6%) had an associated crab; P. gibbesi was present with 30 urchins (11.6%), S. seticornis was present with nine urchins (3.5%), and an unidentified crab was present with four urchins (1.5%). Of the 30 D. antillarum host- ing P. gibbesi, a single crab was present with 22 (73.3%) and two crabs were present with eight (26.7%). None of the D. antillarum hosted two or more S. seticornis or the uniden- tified crab. On no occasion during this study were two crab species present with the same 244 BULLETIN OF MARINE SCIENCE, VOL. 63, NO. 1, 1998

urchin. Based on the proportions of urchins with crabs, P. gibbesi was present signifi- cantly more often than either S. seticornis or the unidentified crab (Χ2 = 26.6, df = 1, P < 0.001). The mean spine length of D. antillarum was 11.90 cm (SD = 2.87, range = 5–19 cm, n = 259). There were significant differences in spine length among D. antillarum with or without crabs (Table 1). The D. antillarum with the unidentified crab averaged shorter spines than did the D. antillarum without crabs (t = 2.64, P = 0.009); no other paired comparison was significant. Among urchins with P. gibbesi, there was no difference in spine length when either one crab (mean = 11.89 cm, SD = 3.13, n = 22) or two (mean = 11.50 cm, SD = 2.66, n = 8) were present (t = 0.31, P = 0.76). The mean density of D. antillarum within a radius of 0.57 m of each D. antillarum individual was 1.77 individuals m−2 (including the urchin; SD = 0.92, range = 1–6, n = 240). The mean density of all urchin species combined within a radius of 0.57 m of each D. antillarum individual was 2.60 individuals m−2 (SD = 2.61, range = 1–16, n =240). The mean distance from each D. antillarum to the nearest conspecific individual was 1.48 m (SD = 2.77, range = 0.02–20 m, n = 240). There were no significant differences in density or distance to nearest conspecific among D. antillarum with or without crabs (Table 1). Our study was confined to shallow waters (≤5 m deep) where D. antillarum could be examined easily by snorkeling. The urchins were found at an average depth of 2.08 m (SD = 0.89, range = 0.5–4.5 m, n = 259). There were no significant differences in depth among D. antillarum with or without crabs (Table 1).

DISCUSSION

Because we often observed both P. gibbesi and S. seticornis not associating with D. antillarum, neither species of crab represents a specialized symbiont of D. antillarum. The surplus of potential D. antillarum hosts lacking crabs (83.4%) indicates that P. gibbesi and S. seticornis populations are not limited by the availability of D. antillarum hosts. In the Bahamas, Schriever (1978) reported that 68% of S. seticornis were associated with anemones and crinoids. In contrast, P. gibbesi has not been reported closely associating with other species, yet it can live independently of D. antillarum (Colin, 1978; pers. observ.). Although we have observed both species of crab near (5–10 cm) the considerably more common rock-boring urchin, E. lucunter, we have not observed either crab species re- treating under its much shorter spines (up to 3 cm long), or under the thicker spines (up to 5 cm long) of the less common slate-pencil urchin, E. tribuloides. This supports the hy- pothesis that the crabs gained protection by crawling under the relatively long and mildly toxic spines of D. antillarum, which offer more protection from potential predators than do the spines of other available urchin hosts. Furthermore, both E. lucunter and E. tribuloides typically occupied holes bored into the rock surface, leaving little space for the crabs to crawl under the urchins. We concur with Colin (1978) that D. antillarum likely derives no benefit from the associating crabs, suggesting that the crab-urchin rela- tionship is commensal rather than mutual. Our data indicate that P. gibbesi associates with D. antillarum more frequently in the shallow waters of Tobago than does S. seticornis. This may reflect a greater abundance of P. gibbesi rather than a greater tendency to associate with urchins. On rare occasions (but HAYES ET AL.: CRAB-URCHIN ASSOCIATIONS 245

not during this study) we have seen up to three P. gibbesi with a single urchin and two S. seticornis with a single urchin. Our failure to locate P. gibbesi and S. seticornis cohabit- ing an urchin host suggests competitive exclusion. However, this may be explained by the low frequency with which crabs occupy D. antillarum and the low probability that two crab species will meet each other at the same urchin host. On 5 November 1994, Hayes observed a P. gibbesi and S. seticornis cohabiting a D. antillarum at Mount Irvine Bay, Tobago, indicating that cohabitation does occur, but apparently in less than 0.4% of D. antillarum (based on our sample size of 259). In the Bahamas, S. seticornis has been recorded cohabiting individual branching anemones, Lebrunia danae, with at least four species of decapod crustaceans, including the cleaner shrimp Periclimenes americanus, P. rathbunae, and P. yucatanicus, and the anemone shrimp Thor amboinensis (Stanton, 1977). We are puzzled by the scarcity of reports of S. seticornis associating with D. antillarum, which suggests that this association is either absent in other parts of the Caribbean or simply overlooked. In the Bahamas, S. seticornis frequently associates with anemones, where Herrnkind et al. (1976) recorded it associating with 26.7% of branching anemo- nes, Lebrunia danae (n = 75), and 36.8% of corkscrew anemones, Bartholomea annulata (n = 19). These frequencies are considerably higher than the frequency with which S. seticornis associates with D. antillarum at Tobago (3.5%). Anemones are apparently rare in the shallow coastal waters of Tobago, where the densities are apparently much smaller than those reported for the Bahamas (Herrnkind et al., 1976; Stanton, 1977). Thus far we have found only one anenome species, B. annulata, in shallow tidal pools at Tobago; the only decapod observed associating with it was an unidentified snapping shrimp, Alpheus sp. We hypothesize that the frequency with which S. seticornis associates with D. antillarum in Tobago is related to the rarity of anemones, which may be preferred by S. seticornis when both anemones and D. antillarum are present. Further studies of the asso- ciation between S. seticornis and D. antillarum are needed from other areas of the Carib- bean to confirm this hypothesis. We found no differences between P. gibbesi and S. seticornis in the selection of D. antillarum hosts. We also found no evidence that the crabs select D. antillarum hosts providing a potentially safer microhabitat by having longer spines, occurring in greater densities, occurring nearer each other or occurring in deeper water. In contrast, the uni- dentified crab appeared to prefer D. antillarum with shorter spines, but the sample size (n = 4) was insufficient for conclusions. The degree of exposure may be another factor influencing the selection of D. antillarum hosts, with crabs preferentially selecting urchins in more sheltered microhabitats (e.g., in deep crevices or under overhangs). Although we initially attempted to rank exposure of D. antillarum hosts, our criteria (e.g., top of substrate, side of substrate, under overhang or in crack) were too variable and subjective to be ranked accurately, and would be diffi- cult for other researchers to repeat. Our general impression was that the crabs did not preferentially select urchins in more sheltered microhabitats. Had we extended this study into deeper water, we may have found differences between P. gibbesi and S. seticornis in the frequency of association with D. antillarum. Colin (1978) reported that P. gibbesi is most common at a depth of 2–7 m, but ranges from the surface to 23 m deep. Goeke (1989) reported that S. seticornis ranges from 1–366 m deep. Previous studies of S. seticornis took place at depths of 8–65 m deep, where consid- erably higher densities were recorded (up to 2.0 m−2 at 8–22 m in the Virgin Islands and 246 BULLETIN OF MARINE SCIENCE, VOL. 63, NO. 1, 1998

0.5 m−2 at 18–21 m in the Bahamas (Barr, 1971, 1975; Shriever, 1978) than what we have observed in the shallow waters of Tobago. Randall et al. (1964) reported that D. antillarum occurs in depths up to 400 m. Thus it is probable that S. seticornis associates with D. antillarum more frequently than does P. gibbesi in deeper water. In conclusion, P. gibbesi associated with D. antillarum hosts more frequently than did S. seticornis and an unidentified crab in the shallow coastal waters of Tobago. Most po- tential D. antillarum hosts lacked an associating crab. We found no evidence that P. gibbesi and S. seticornis differed in their selection of D. antillarum hosts, or that the crabs se- lected urchin hosts providing a potentially safer microhabitat. These results suggest that selection of D. antillarum hosts by P. gibbesi and S. seticornis is random, with minimal interspecific competition.

ACKNOWLEDGMENTS

We thank D. Cowles, R. Mooi and an anonymous referee for reviewing the manuscript; D. Cowles further assisted in providing pertinent literature. This study was indirectly financed by grants (for ornithological research) from the American Bird Conservancy, Bird Life International, British Pe- troleum, the Center for the Study of Tropical Birds, and Fauna and Flora International. We thank these institutions for their support of our environmental education and research program at Tobago.

LITERATURE CITED

Adey, W. H., W. Gladfelter, J. Ogden and R. Dill. 1977. Field guide book to the reefs and reef communities of St. Croix, Virgin Islands. The Atlantic Reef Committee, Univ. Miami, Fisher Island, Miami Beach, Florida. 52 p. Anonymous. 1990. Statistix manual. Analytical Software, St. Paul, Minnesota. 280 p. Barr, L. 1971. Observations on the biology and behavior of the arrow crab, Stenorhynchus seticornix [sic] (Herbst), in Lameshur Bay, St. John, Virgin Islands. Pages 213–220 in J. W. Miller, J. G. Van Derwalker, and R. A. Waller, eds. Scientists-in-the-sea. U. S. Department of the Interior, Washington, D.C. ______. 1975. Biology and behavior of the arrow crab, Stenorhynchus seticornis (Herbst), in Lameshur Bay, St. John, Virgin Islands. Sci. Bull. Nat. Hist. Mus. Los Angeles Co. 20: 47–56. Castro, P. 1974. A new host and notes on the behavior of Tuleariocaris neglecta Chace, 1969 (, Palaemonidae, Pontoniinae), a symbiont of diadematid sea urchins. Crustaceana 26:318–320. Chase, F. A. 1969. A new and five new species of shrimps (Decapoda, Palaemonidae, Pontoniinae) from the western Atlantic. Crustaceana 16: 251–272. Clifton, H. E., C. V. W. Mahnken, J. C. Van Derwalker, and R. A. Waller. 1970. Tektite 1, Man-in- the-sea project: Marine Science Program. Science 168: 659–663. Colin, P. L. 1978. Caribbean reef and plants. A field guide to the invertebrates and plants occurring on coral reefs of the Caribbean, the Bahamas and Florida. TFH Publications, Hong Kong. 512 p. Criales, M. M. 1984. Shrimps associated with coelenterates, echinoderms, and molluscs in the Santa Marta region, Colombia. J. Crust. Biol. 4: 307–317. Davis, G. E. 1971. Aggregations of spiny sea urchins, Diadema antillarum, as shelter for young spiny lobsters, Panulirus argus.Trans. Amer. Fish. Soc. 100: 586–587. Goeke, G. D. 1989. Stenorhynchus yangi, a new western Atlantic species of arrow crab (Crustacea, Brachyura, Majidae) and a redescription of S. seticornis (Herbst, 1788). Proc. Biol. Soc.Wash. 102: 620–636. HAYES ET AL.: CRAB-URCHIN ASSOCIATIONS 247

Gooding, R. U. 1974. associated with the , Diadema antillarum. Pages 333–336 in T. J. Bright and L. H.Pequegnat, eds. Biota of the West Flower Garden Bank. Gulf Publishing Co., Houston, Texas. 435 p. Herrnkind, W., G. Stanton and E. Conklin. 1976. Initial characterization of the commensal complex associated with the anemone, Lebrunia danae, at Grand Bahama. Bull. Mar. Sci. 26: 65–71. Humann, P. 1992. Reef creature identification. Florida–Caribbean–Bahamas. New World Publica- tions, Inc., Jacksonville, Florida. 320 p. Kaplan, E. H. 1988. A field guide to southeastern and Caribbean seashores. Cape Hatteras to the Gulf Coast, Florida, and the Caribbean. Houghton Mifflin Company, Boston, Massachusetts. 425 p. Kenny, J. S. 1976. A preliminary study of the Buccoo Reef/Bon Accord Complex. Dept. Biol. Sci., Univ. West Indies, St. Augustine, Trinidad. 123 p. ______and P. R. Bacon. 1981. Aquatic resources. Pages 112–144 in St. G. C. Cooper and P. R. Bacon, eds. The natural resources of Trinidad and Tobago. Edward Arnold (Publishers) Ltd., London. 123 p. Laydoo, R. S. 1985. Executive summary. Ecological survey of reefs around Tobago. Inst. Mar. Affairs, Carenage, Trinidad. 47 p. ______. 1991. A guide to the coral reefs of Tobago. Inst. Mar. Affairs and Asa Wright Nature Centre, Port of Spain, Trinidad. 43 p. Lentner, M., and T. Bishop. 1986. Experimental design and analysis. Valley Book Co., Blacksburg, Virginia. 465 p. Powers, L. W. 1977. A catalogue and bibliography to the crabs (Brachyura) of the Gulf of Mexico. Port Aransas Mar. Lab., Univ.Texas Mar. Sci. Inst., Port Aransas, Texas. 190 p. Ramsaroop, D. 1981. A preliminary survey of the coral reefs in Man-of-War Bay, Tobago. Living World (J. Trin. Tob. Field Nat.Club) 1981–1982: 26–33. Randall, J. E., R. E. Schroeder and W. A. Starck, II. 1964. Notes on the biology of the echinoid Diadema antillarum. Carib. J. Sci. 4:421–433. Ross, D. M. 1983. Symbiotic relations. Pages 163–212 in F. J. Vernberg and W. B. Vernberg, eds. The biology of crustacea. vol. 7. Behavior and ecology. Academic Press, New York. 338 p. Schmalfuss, H. 1976. Ökologish-funktionsmorphologische Untersuchungen an karibischen Krabben (Decapoda, Brachyura) I. Percnon gibbesi (H. Milne-Edwards, 1837) (, Plagusiinae). Stud. Neotrop. Fauna Environ. 11: 211–222. Schriever, G. 1978. In situ observations on the behaviour and biology of the tropical spider crab Stenorhynchus seticornis Herbst (Crustacea, Decapoda, Brachyura). Pages 297–302 in D. S. Mclusky and A. J. Berry, eds. Physiology and behaviour of marine organisms. Proc. 12th Euro- pean Symp. Mar. Biol. Pergamon Press, Oxford, England. 388 p. Sefton, N. and S. K. Webster. 1986. A field guide to Caribbean reef invertebrates. Sea Challengers, Monterey, . 112 p. Serafy, D. K. 1979. Echinoids (Echinodermata: Echinoidea). Mem. Hourglass Cruises (Florida Dept. Nat. Res. Mar. Res. Lab.) 5: 1–120. Stanton, G. 1977. Habitat partitioning among associated decapods with Lebrunia danae at Grand Bahama. Pages 169–175 in D. L.Taylor, ed. Proc. 3rd Int’l. Coral Reef Symp. Vol. 1. Biology. Univ. Miami, Miami, Florida. 656 p. Zar, J. H. 1984. Biostatistical analysis. 2nd ed. Prentice-Hall, Inc., Englewood Cliffs, New Jersey. 718 p.

DATE SUBMITTED: September 30, 1996. DATE ACCEPTED: January 27, 1997.

ADDRESS: Department of Biology, Caribbean Union College, P. O.Box 175, Port of Spain, Trinidad and Tobago.