J. South Asian Nat. Hist., ISSN 1022-0828. May, 1999. Vol.4, No. 1, pp. 65-70; 3 figs. © Wildlife Heritage Trust of Sri Lanka, 95 Cotta Road, Colombo 8, Sri Lanka.

A note on the sea cucumber , Hapalonotus reticulatus (Crustacea: Brachyura: Eumedonidae)

Diana G. B. Chia* and Peter K. L. Ng* * Department of Biological Sciences, National University of Singapore, Kent Ridge, Singapore 119260, Republic of Singapore.

Abstract The rare sea cucumber crab, Hapalonotus reticulatus (De Man, 1879) is redescribed and figured in detail. Its familial affinities with the Eumedonidae and Pilumnidae are discussed.

Introduction The rare and unusual sea cucumber crab, Hapalonotus Etymology. The name Hapalonotus is derived from reticulatus (De Man, 1879) is redescribed. Its the Latin 'hapalus' and 'notus' for soft back, in relationship with the Eumedonidae and Pilumnidae reference to the original description of the type are discussed, and problems with its classification which stated its carapace was soft. Gender in the Eumedonidae highlighted. The is masculine. The original genus name, Malacomsoma, nevertheless retained in the Eumedonidae until the was derived from the Greek 'malacus' (soft) and family Pilumnidae can be revised and its affinities 'soma' (back), and its gender was neuter. with the closely related Eumedonidae established. Specimens examined are deposited in the IRSNB Diagnosis. Carapace oval, distinctly broader than (Institut Royale des Sciences Naturelles de Belgique, long, dorsal surface very convex, carapace appears Brussels), MZB (Balitbang Zoologi, Museum very high; rostrum very short, deflexed downwards; Zoologicum Bogoriense, Bogor), RMNH (Nationaal inner supraorbital teeth absent; regions poorly Natuurhistorisches Museum (former Rijksmuseum defined; surfaces of carapace, chelipeds and van Natuurlijke Histoire), Leiden), and ZRC ambulatory legs smooth, without granules, covered (Zoological Reference Collection, Department of with dense layer of very short, stiff, transparent setae. Biological Sciences, National University of Antero- and posterolateral margins demarcated; Singapore). The abbreviations G1 and G2 are used anterolateral margin entire, without teeth, lobes or for the male first and second pleopods respectively crest. Antennules folding slightly obliquely, ca. 15o Measurements provided are of the carapace length from horizontal. Second antennal segment short, and width respectively. length to width ratio of second antennal segment ca. 1.0. Epistome very narrow. Median part of sternites Family Eumedonidae 3 and 4 depressed. Chelipeds smooth, covered with dense layer of very short, stiff, transparent setae; Genus Hapalonotus Rathbun, 1897 carpus with low, rounded tubercle on inner distal angle; merus unarmed except for small rounded Malacosoma De Man, 1879: 67; Alcock, 1900: 294. tubercle on subdistal dorsal margin; chela short, Hapalonotus Rathbun, 1897:164; Tesch, 1918: 275 [in stout, length 2 times length of fingers, height ca. 2-3 key], 277; Balss, 1933:90; Balss, 1957:1650; SerSne, times height of fingers; fingers not carinate, pollex 1968: 74; Schmitt et al., 1973:131; Vandenspiegel not bent downwards. Ambulatory leg segments et al., 1992a: 172. smooth, covered with dense layer of very short, stiff, transparent setae, cylindrical, not cristate; dactylus Type species. Malacosoma reticulatum De Man, 1879, of first pair not distinctly longer or more slender than by monotypy. Gender of genus masculine. those on other legs. G1 long, slender, sinuous. C hi a & N g

Remarks. De Man (1897) described the taxon as (Castro, 1971; Fishelson, 1973; Suzuki & Takeda, 1974; Malacosoma reticulatum. Rathbun (1897) commented Ng & Lim, 1990). that Malacosoma was a preoccupied name (Insecta: Many of the above characters make Hapalonotus Lepidoptera) and substituted it with Hapalonotus rather peculiar among eumedonids and it may not instead. The genus Hapalonotus is monotypic, belong to the family after all. However, in the form containing only the type species, M alacosoma of the legs, shape of the antennules, antennae, reticulatum De Man, 1879 (present H. reticulatus). chelipeds, third maxilliped, abdomen and general The familial placement of this genus is difficult. habits, it does not differ greatly from the other Tesch (1918) and Schmitt et al. (1973) referred members of the family. These characters, however, Hapalonotus to the Pinnotheridae, probably because are also in common with most species of Pilumnidae. of its appearance and habits. Balss (1933) thought it For purely ecological reasons, the recognition of the was a Xanthidae. Vandenspiegel et al. (1992a) Eumedonidae has merit, all genera are after all reported males of H. reticulatus for the first time, and obligate symbionts on . For this reason they showed that it had features more in common alone, Hapalonotus is retained in the Eumedonidae with the Eumedonidae, i.e. a sinuous G1 and having for the time being. When the limits of the Pilumnidae all seven male abdominal segments free, following are fully revised, the Eumedonidae will probably be the revision of Stevcic et al. (1988). Its possible part of the Pilumnidae, during which time, it might affinities with the Pilumnidae were also discussed. be proper to consider placing Hapalonotus in its own Its placement there, however, is rather difficult as subfamily as well. the of the Eumedonidae is still not completely resolved (see Ng & Rodriguez, 1986; Lim Hapalonotus reticulatus (De Man, 1879) & Ng, 1988; Mori et al., 1991). (Figures 1-3) With regards to its habits and general features, Hapalonotus does seem to be a eumedonid. In terms Malacosoma reticulatum De Man, 1879: 67 [type of its carapace shape, eyes, epistome, antennules, locality Ambon, Moluccas = Maluku Islands, ambulatory dactyli, the tip of Gl, large size and host, Indonesia] however, H. reticulatus is very different from the other Hapalonotus reticulatus - Tesch, 1918: 278, pi. 18: Fig. eumedonids. The carapace of H. reticulatus is high, 3 ,3a [Ambon, holotype re-examined]; Balss 1933: bulbous, broad and oval in shape. The eye stalk is 90, Fig. 3, pi. 2: Fig. 1 [Banda Islands, Moluccas = very broad and large, slightly lamelliform and Maluku, Indonesia]; SerSne, 1968: 74 [list only]; expanded at the anterior and posterior margins. The Schmitt et al., 1973:131 [list only]; Vandenspiegel epistome and antennules are highly compressed and et al., 1992a: 172, Figs. 5,6 [Hansa Bay, Papua New narrow. The ambulatory leg also only has a weakly Guinea]; Vandenspiegel et al., 1992b: 242 [Hansa developed dactylo-propodal articulation which is Bay, Papua New Guinea]. very distinct in other eumedonids. The distal tip of Gl is short and stunted in Hapalonotus but sharp and Material examined. Holotype - female (20.0 by 24.0 tapering in other eumedonids. The very short, dense mm) (RMNH 319), Amboina (= Ambon), Indonesia, and almost transparent setae covering the dorsal coll. D. S. Hoedt, 1864. Others: Indonesia: 1 female surfaces is very interesting, and quite unlike anything (19.0 by 24.5 mm) (MZB Cru 070), Banda Islands, known in the Eumedonidae thus far. While many Lesser Sunda Islands, Indonesia, coll. Baidilla. Papua eumedonids, e.g. Harrovia and Ceratocarcinus species, New Guinea: 1 male, 1 female (IRSNB IG27522), can be covered with short, dense setae, these setae Laing Island, in Holothuria sp. - 2 females (IRSNB are coarse, gather dirt and pigmented (Chia et al., IG27754/179-180), Hansa Bay, 6 m, coll. D. 1993; Castro et al., 1995). In Hapalonotus, the hair is Vandenspiegel. -1 male (16.1 by 19.3 mm), 1 female velvet-like and does not gather dirt easily. (20.5 by 24.7 mm) (ZRC 1997.170-171, ex IRSNB Hapalonotus is by far the largest eumedonid IG27598/135, 133), Hansa Bay, seagrass beds off known. It is the only species known to be symbiotic Awar Plantation, 4°08'27"S, 144°51,22"E, 10 m, in the with sea cucumbers. It is also the only species which respiratory of a holothurian, coll. C. Massin, 13 X is an endosymbiont. In most aspects, the ecology of 1989. Hapalonotus is similar to what has been reported for many species of holothurian-associated pea Description. Carapace oval, distinctly broader than (Pinnotheridae) (see Chopra, 1931; Schmitt et al., long, dorsal surface very convex, appears very high; 1973; Vandenspiegel & Jangoux, 1989). All other rostrum very short, deflexed downwards; inner eumedonids are obligate external symbionts on sea supraorbital teeth absent; regions poorly defined; urchins (Echinoidea) or featherstars (Crinoidea) surfaces of carapace, chelipeds and ambulatory legs

66 J. South Asian Nat. Hist. The sea cucumber crab, H apalonotus reticulatus

Figure 1. Hapalonotus reticulatus (De Man, 1879). Male, 16.1 by 19.3 mm (ZRC 1997.170-171): A, dorsal view; B, ventral view.

Vol. 4, No. 1. 67 Chia & Ng

Figure 2. Hapalonotus reticulatus (De Man, 1879). Male, 16.1 leg; F, left third maxilliped; G, ventral view of left Gl; H, by 19.3 mm (ZRC 1997.170-171): A, dorsal view of distal tip of left Gl; I, left G2 (dotted line indicates carapace; B, postero-dorsal view of left cheliped; C, breakage); J, abdomen. Scales for A- G, I-J = 1.0 mm; for H sternum; D, face of carapace; E, fourth right ambulatory = 0.1 mm.

68 J. South Asian Nat. Hist. The sea cucumber crab, H apalon otus reticulatus

Figure 3. Hapalonotus reticulatus (De Man, 1879), specimen from Papua New Guinea (photograph courtesy of D. in situ in dissected sea cucumber, showing live colours, Vandenspiegel). smooth, without granules, covered with dense layer Sutures between anterior thoracic sternites 1 and of very short, stiff, transparent setae. Antero- and 2 indistinct, between 2 and 3 shallow; between 3 and posterolateral margins demarcated; anterolateral 4 interrupted medially; lateral clefts shallow. Median margin entire, without teeth lobes, or crest, margin part of sternites 3 and 4 depressed, male abdominal rounded, not cristate. Antennules folding slightly cavity reaching to just before anterior edge of sternite obliquely, ca. 15° from horizontal. Antenna free, does 4. not fill orbital hiatus, reaching into orbit; antennal Male abdomen triangular, 7-segmented, all basal segment rectangular; length to width ratio of segments mobile; telson triangular, lateral margins second antennal segment ca. 1.0. Eyes well gently convex; lateral margins of trapezoidal developed, filling orbit; cornea distinct, pigmented; segments 4-6 distinctly concave; segment 3 widest. infraorbital teeth developed. Epistome very narrow; Ambulatory leg segments smooth, covered with eye stalk long and broad; posterior margin appears dense layer of very short, stiff, transparent setae, entire because of 2 fused truncate median lobes. cylindrical in cross-section, unarmed, not cristate; Pterygostomial, subhepatic, suborbital regions dactylus of first pair not distinctly longer or more smooth. slender than those on other legs; ventral margin of Third maxilliped quadrate; ischium rectangular, dactylus with dense row of short setae. Gl long, median oblique sulcus absent; merus squarish; slender, distal tip short, tip bends at approximately exopod just reaches half-way of antero-external edge 90o. G2 relatively short, distal segment short. No of merus. obvious sexual dimorphism. Chelipeds smooth, covered with dense layer of very short, stiff, transparent setae; carpus with low, Remarks. De Man (1897) had described the species rounded tubercle on inner distal angle; merus from a single female specimen from Ambon. Balss unarmed except for small rounded tubercle on (1933) subsequently reported two female specimens subdistal dorsal margin; chela short, stout, length 2 from Banda in the Lesser Sunda Islands. Tesch (1918) times length of fingers, height ca. 2-3 times height of had commented that the holotype female was rather fingers; fingers not carinate, pollex not bent soft and Balss (1933) noted that the carapaces of his downwards. specimens were also somewhat thin. We have

Vol. 4, No. 1. 69 Chia & Ng

examined the type specimen in RMNH and one of associated with them. J. Mar. Biol. Assoc. India, 15(2): Balss' specimens in the MZB, and while their 461-473, pis. 1-2. carapaces do appear somewhat thinner than free- Lim, G. S. Y. & P. K. L. Ng. 1988. The first zoeal stage of Harrovia albolineata Adams and White, 1848 (Crustacea: living crabs, they are not especially soft. They are Brachyura: Pilumnidae), with a note on eumedonine certainly not "membranaceous" as had been systematics. I. Nat. Hist., 22: 217-223. described by Tesch (1918: 278). Such softness may Man, J.G., De. 1879. On some new or imperfectly known be due to prolonged preservation in acidic formalin podophthalmous Crustacea of the Leyden Museum, or because they had been collected shortly after they Note XIX. Notes Leyden Mus., 1: 53-73. had moulted. Mori, A., Y. Yanagisawa, Y. Fukuda & P. K. L. Ng. 1991. Complete larval development of Zebrida adamsii White, Ecology. The species is an obligate symbiont with 1847 (: Brachyura), reared in the laboratory. sea cucumbers (Holothuria scabra: Holothuroidea), J. Crust. Biol., 11(2): 292-304. living in the respiratory trees (Fig. 3) (see Ng, P. K. L. & G. S. Y. Lim. 1990. On the ecology of Harrovia albolineata Adams & White, 1848 (Crustacea: Vandenspiegel et al., 1992a, for review). Decapoda: Brachyura: Eumedonidae), a crab symbiotic with crinoids. Raffles Bull. Zool., 38(2): 257- Acknowledgements 262. The authors are grateful to Charles Fransen (RMNH), Ng, P. K. L. & G. Rodriguez. 1986. New records of Mimilambrus wileyi Williams, 1979 (Crustacea: A. Ovaere (IRSNB), and Daisy Wowor (MZB) for Decapoda: Brachyura), with notes on the systematics permission to examine the specimens in their of the Mimilambridae Williams, 1979 and collections. Lipke Holthuis kindly commented on the Parthenopoidea MacLeay, 1838 sensu Guinot, 1978. manuscript. The present study has been partially Proc. Biol. Soc. Wash., 99(1): 88-99. supported by a research grant to the second author Rathbun, M. J. 1897. A revision of the nomenclature of from the National University of Singapore. the Brachyura. Proc. Biol. Soc. Wash., 11: 153-167. Schmitt, W. L., J. C. McCain & E. S. Davidson. 1973. Literature cited Decapoda I, Brachyura I, Fam. Pinnotheridae. In: H.E. Gruner & L.B. Holthuis, editors, Crust. Cat., 3: 1-160. Alcock, A. 1900. The Brachyura Catometopa or SerSne, R. 1968. The Brachyura of the Indo-West Pacific Grapsoidea. Materials for a carcinological fauna of region. In: Prodromus for a check list of the non- India, No. 6. J. Asiat. Soc. Bengal, 69(2)(3): 279-456. planctonic marine fauna of South East Asia. Singapore Balss, H. 1933. Ueber einige systematisch interessante Natn. Acad. Sci., Sp. Publn. no. 1: 33-112. indopacifische Dekapoden. Mitt. Zool. Mus. Berlin, 19: Stevcic, Z., P. Castro & R. H. Gore. 1988. Re-establishment 84-97, pi 2. of the Family Eumedonidae Dana, 1853 (Crustacea: Balss, H. 1957. Decapoda, VIII: Systematik. In: H.G. Brachyura). J. Nat. Hist., 22: 1301- 1324. Bronns, Klassen und Ordnungen des Tierreichs. Suzuki, K. & M. Takeda. 1974. On a parthenopid crab, Akademische Verlagsgesellschaft, Leipzig, (5)(1)7(12): Zebrida adamsii on the sea urchins from Suruga Bay, 1131-1199. with a special reference to their parasitic relations. Bull. Castro, P. 1971. Nutritional aspects of the symbiosis Nat. Sci. Mus., Tokyo, 17(4): 287-296, pi. 1. between pentagonus and its host in Hawaii, Tesch, J. J., 1918. Goneplacidae and Pinnotheridae. The calamaris. In: Aspects of the Biology of Decapoda Brachyura of the Siboga Expedition, II. Symbiosis. Ed. T. C. Cheng. Pp. 229-247, Tables 1-5. Siboga-Exped., 39C1: 149-295, pis. 7-18. Univ. Park Press, Baltimore. Vandenspiegel, D. & M. Jangoux. 1989. Sur la symbiose Castro, P., D. G. B. Chia & P. K. L. Ng. 1995. On the entre le Pinnotheride Pinnotheres villosissimus taxonomic status of Ceratocarcinus longimanus White, (Crustacea, Decapoda) et l'Holothurie Actinopyga 1847 (Crustacea: Decapoda: Brachyura: mauritiana (Echinodermata). Vie Mar., Marseille, 10: Eumedonidae), a crab symbiotic with comatulid 205- 213. crinoids. Raff Bull. Zool., 43(1): 239-250. Vandenspiegel, D., A. Ovaere & C. Massin. 1992a. On the Chia, D. G. B., P. K. L. Ng & D. Vandenspiegel. 1993. The association between the crab Hapalonotus reticulatus identities of two crinoid symbionts, Harrovia albolineata (Crustacea, Brachyura, Eumedonidae) and the sea Adams & White, 1849, and H. longipes Lanchester, 1900 cucumber Holothuria (Metriatyla) scabra (­ (Decapoda, Brachyura, Eumedonidae). Crustaceana, ata, Holothuridae). Bull. Inst. Royal Sciences Nat. 64(3): 259-280. Belgique, Biologie, 62: 167-177. Chopra, B. 1931. Further notes on Crustacea Decapoda in Vandenspiegel, D., A. Ovaere & C. Massin. 1992b. On the the Indian Museum. II. On some decapod crustacea association between the crab Hapalonotus reticulatus found in the cloaca of holothurians. Records of the and the sea cucumber Holothuria (Metriatyla) scabra. Indian Museum, 33(3): 303-324, pi. 7. Echinoderm Res., eds. L. Scalera-Liaci & C. Canicatti, Fishelson, L. 1973. Ecology of the crinoids of the northern Balkema: Rotterdam, p. 242. Red Sea with emphasis on epi- and endozoic fauna

70 J. South Asian Nat. Hist.