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Spermatophore Morphology of the Endemic Hermit Crab Loxopagurus Loxochelis (Anomura, Diogenidae) from the Southwestern Atlantic - Brazil and Argentina

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Spermatophore Morphology of the Endemic Hermit Crab Loxopagurus Loxochelis (Anomura, Diogenidae) from the Southwestern Atlantic - Brazil and Argentina Invertebrate Reproduction and Development, 46:1 (2004) 1- 9 Balaban, Philadelphia/Rehovot 0168-8170/04/$05 .00 © 2004 Balaban Spermatophore morphology of the endemic hermit crab Loxopagurus loxochelis (Anomura, Diogenidae) from the southwestern Atlantic - Brazil and Argentina MARCELO A. SCELZ01*, FERNANDO L. MANTELATT02 and CHRISTOPHER C. TUDGE3 1Departamento de Ciencias Marinas, FCEyN, Universidad Nacional de Mar del Plata/CONICET, Funes 3350, (B7600AYL), Mar del Plata, Argentina Tel. +54 (223) 475-1107; Fax: +54 (223) 475-3150; email: [email protected] 2Departamento de Biologia, Faculdade de Filosojia, Ciencias e Letras de Ribeirao Preto (FFCLRP), Universidade de Sao Paulo (USP), Av. Bandeirantes 3900, Ribeirao Preto, Sao Paulo, Brasil 3Department of Systematic Biology, National Museum ofNatural History, Smithsonian Institution, Washington, DC 20013-7012, USA Received 10 June 2003; Accepted 29 August 2003 Summary The spermatophore morphology of the endemic and monotypic hermit crab Loxopagurus loxochelis from the southwestern Atlantic is described. The spermatophores show similarities with those described for other members of the family Diogenidae (especially the genus Cliba­ narius), and are composed of three major regions: a sperm-filled, circular flat ampulla; a columnar stalk; and a pedestal. The morphology and size of the spermatophore of L. loxochelis, along with a distinguishable constriction or neck that penetrates almost halfway into the base of the ampulla, are characteristic of this species. The size of the spermatophore is related to hermit crab size. Direct relationships were found between the spermatophore ampulla width, total length, and peduncle length with carapace length of the hermit crab. These morphological characteristics and size of the spermatophore ofL. loxochelis are species-specific, distinguishing them from other members of the family Diogenidae, and can be used to infer phylogenetic relationships among them. Key words: Spermatophore, hermit crab, Diogenidae, reproduction Introduction there is a unique family, the Aeglidae, restricted to Anomuran dec a pods are a group of crustaceans that freshwater and endemic to South America (Bond­ include a wide variety of forms, such as the attractive Buckup, 2003). hermit and porcellanid crabs, and some commercial According to McLaughlin (1983) and McLaughlin species such as the king crabs, among others. Some of and Holthuis (1985), the Anomura was redefined and them are semi-terrestrial, while the majority inhabits currently constitutes the following superfamilies: Gala­ marine waters, from the intertidal to the deep sea. Also, theoidea, Hippoidea, Paguroidea and Lomisoidea (see 'Corresponding author. 2 M.A. Scelzo eta!. I IRD 46 (2004) 1-9 also Martin and Davis, 2001 ). The superfamily Pagu­ Spermatophores play a major role in sperm transfer roidea, which includes the common hermit crabs and and storage in decapod crustaceans, especially in king crabs, currently consists of the Coenobitidae, hermit crabs that use a gastropod shell as a protective Diogenidae, Paguridae, Parapaguridae, Pylochelidae, cover for their non-calcified abdomen. Spermatophores Lithodidae and Pylojacquesidae families (McLaughlin not only serve as protection for the non-motile sperma­ and Lemaitre, 2001; McLaughlin, 2003). The family tozoa during transmission to females but also may Diogenidae is considered to be an ancient mono­ provide energy rich substrates for prolonged sperm phyletic group (Forest, 1995), but its monophyly has storage in the females (Subramoniam, 1991 ). All the been questioned (Tudge, 1995, 1997). It is a morpho­ representatives in the Diogenidae and Paguridae are logically diverse taxon currently encompassing 19 aquatic, with mating and fertilization occurring in genera: Allodardanus, Aniculus, Bathynarius, Calci­ water. Meanwhile, members of the Coenobitidae are nus, Cancellus, Ciliopagurus, Clibanarius, Dardanus, terrestrial (Birgus /atro) or semi-terrestrial ( Coenobita Diogenes, Isocheles, Loxopagurus, Paguristes, Pagu­ spp.) with mating and fertilization obviously occurring ropsis, Petrochirus, Pseudopaguristes, Pseudopagu­ in the terrestrial environment (Greenaway, 2003). rus, Strigopagurus, Tisea, Trizopagurus (McLaughlin, During copulation the male hermit crab transfers the 2003). pedunculate spermatophores and attaches them to the Loxopagurus loxochelis (Moreira, 1901) is a exoskeleton of the female hermit crab or onto the species endemic to the southwestern Atlantic Ocean, surface of the temporarily inhabited gastropod shell by being one of the most common hermit crabs inhabiting the sticky base of the spermatophore pedestal (Hazlett, the shallow littoral waters of Brazil, Uruguay and 1996; Hess and Bauer, 2002). The spermatophore wall Argentina, down to a depth of 30 m (Boschi et al., is molded into a variety of complex shapes by changes 1992; Melo, 1999). The biology of this species is in the contour of the vas deferens lumen, contraction of reasonably well known (Martinelli et al., 2002). The the vas deferens musculature, and deposition of mater­ data available deal only with the species description ial from adjacent glandular cells (Matthews, 1953; and adult distribution (Moreira, 1901; Forest and Fingerman, 1992; Krol et al., 1992; Tudge, 1999a). De Saint Laurent, 1967; Scelzo and Boschi, 1973; The typical, pedundulate anomuranlhermit crab Scelzo, 1976) and larval distribution along the coast of spermatophore can be divided into three major regions: Rio Grande do Sui, Brazil (Rieger and D'Incao, 1991 ). a sperm-filled ampulla, a columnar stalk of variable The life cycle of L. loxochelis has recently been length, and a foot or pedestal. The ampulla has a par­ studied in the Ubatuba region (Sao Paulo State, Brazil) tition or line of division that runs around the lateral where the occurrence of exobionts on occupied shells, edge and separates the ampulla into two halves. This shell utilization pattern, relative growth, and spatial suture line is the point of weakness where the ampulla distribution were investigated (Martinelli and Mante­ breaks to release the spermatozoa prior to fertilization latto, 1998, 1999; Mantelatto and Martinelli, 2001; (Tudge, 1991, 1999a, 1999b). According to Tudge Mantelatto et al., in press). ( 1991 , 1997), spermatophore form at both the light and Comparisons of the functional morphology of electron microscope levels can be used to separate genitalia and subsequent sperm transfer and storage species of hermit crabs within the Paguroidea and thus mechanisms among taxa provide useful information on have some phylogenetic utility. Spermatophores from phylogenetic relationships and evolutionary diver­ members of the family Coenobitidae, for example, are gence, especially in the Decapoda (Bauer, 1986, 1991 ). robust in nature with large, ovoid-spherical ampullae However, particular modes of sperm transfer used by mounted on short, thick stalks. Members of the Dio­ organisms can be more directly influenced by the genidae have more fragile spermatophores with small habitat of those organisms than by the phylogenetic spherical ampullae mounted on long, slender stalks; relationships, as argued by Mann (1984). Considerable and in the Paguridae, spermatophores are distinctive in morphological variation exists among representatives possessing large, elongate, ampullae, and smaller of the reptant decapods, and members of the various accessory ampullae at the base of the main ampullae groups have evolved different strategies of transferring and a pseudo-stalk analogous with the true stalk of the sperm from the male to the female (Hinsch, 1991; Coenobitidae and Diogenidae (Tudge, 1991 ). The Subramoniam, 1991 ). Also, the mechanism by which unusual accessory ampullae have also been recorded in spermatophores are transmitted from the male gono­ some members of the Lithodidae and Parapaguridae pore to the body of a receptive female has only been (Tudge et al., 1998; Tudge, 1999a). hypothesized (see Hess and Bauer, 2002, and refer­ Since very little information is available on the ences therein). reproductive system of the endemic southwestern M.A. Scelzo et al. I IRD 46 (2004) 1-9 3 Atlantic hermit crab L. loxochelis, we describe and illustrate the spermatophore morphology and biometric relationships of this species and compare it with other members of the family Diogenidae. Any divergence in morphology and variability among the Diogenidae is noted and phylogenetic inferences furnished. ... ,I~ :a 10 PL .- Material and Methods Approximately 400 hermit crab samples were obtained in Mar del Plata/Mar Chiquita (Buenos Aires Province, Argentina) and Ubatuba (Sao Paulo, Brazil) from 1999 through 2002. The capture of the animals was carried out at depths between 5 and 25 m by trawl nets. Each individual was measured in shield length (SL) from the tip of rostrum to the V -shaped groove at the posterior edge of the dorsal shield with a caliper rule (0.1 mm) or stereomicroscope mounted with a graduated eyepiece. Each fresh crab was also weighed (W) using an electronic micro scale (0.001 g sensitivity). From the total number of specimens collected, almost 300 were checked for spermatophore analysis. The male reproductive system was dissected from either freshly killed or fixed specimens. An incision was made between the fourth and fifth pair of pereo­ Fig. 1. Loxopagurus loxochelis. Drawings ofspermatophores pods (P4 and P5, respectively) pulling the abdomen showing the measurements taken: TLSp, spermatophore from the rest of the cephalothorax.
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