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Larval Growth, Development and Duration in Terrestrial Hermit Crabs

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Larval Growth, Development and Duration in Terrestrial Hermit Crabs Vol. 1: 93–107, 2015 SEXUALITY AND EARLY DEVELOPMENT IN AQUATIC ORGANISMS Published online February 25 doi: 10.3354/sedao00010 Sex Early Dev Aquat Org OPENPEN ACCESSCCESS Larval growth, development and duration in terrestrial hermit crabs Katsuyuki Hamasaki1,*, Saori Kato1, Yu Murakami1, Shigeki Dan2, Shuichi Kitada1 1Graduate School of Marine Science and Technology, Tokyo University of Marine Science and Technology, Konan, Minato, Tokyo 108-8477, Japan 2Tamano Laboratory, National Research Institute of Fisheries and Environment of Inland Sea, Fisheries Research Agency, Tamano, Okayama 706-0002, Japan ABSTRACT: We investigated patterns of larval growth and development in terrestrial hermit crabs of the family Coenobitidae (genera Coenobita and Birgus). Larvae of 5 species (C. cavipes, C. purpureus, C. rugosus, C. violascens, and B. latro) were cultured individually at ~28°C, and their moulting, growth and developmental duration were analysed in conjunction with published data for coenobitid species (C. brevimanus, C. cavipes, C. clypeatus, C. compressus, C. purpureus, C. rugosus, C. scaevola, C. variabilis, and B. latro). Coenobitid crabs metamorphosed into mega- lopae after 2 to 7 zoeal stages, and intraspecific variability in developmental pathways (number of zoeal stages) was observed in 6 out of 10 species. Interspecific variability in body lengths was large at hatching but reduced in megalopae. Linear growth equations (y = a + bx) between num- ber of moults (x) and body length (y) in the zoeal stages were determined, parameters a and b rep- resenting body length at hatching and mean growth increment at moulting, respectively. The relationship between parameters a and b for the species examined suggested the existence of 4 larval growth and development patterns in coenobitids: (1) initially smaller larvae and smaller growth increments — longer pathway; (2) initially smaller larvae and larger growth increments — shorter pathway; (3) initially larger larvae and smaller growth increments — shorter pathway; and (4) initially largest larvae and smallest growth increments — shortest pathway (abbreviated devel- opment). Total zoeal duration increased with decreasing water temperatures and increasing num- ber of zoeal stages and was apparently unrelated to the geographical distribution of coenobitid species. KEY WORDS: Coconut crab · Land hermit crab · Intraspecific variation · Interspecific variation · Larval duration INTRODUCTION 2009). Many benthic decapod crustaceans pass through a planktonic zoeal stage, the duration of Many marine benthic invertebrates develop via which is determined by the number of moults, inter- complex life cycles comprising embryonic, mero- moult period, and body size increment at moulting. planktonic larval, and benthic juvenile−adult phases They then metamorphose into a megalopa, during (Anger 2006). In general, pelagic larval duration which the transition from the plankton to the benthos determines the length of time that larvae are subject takes place (Anger 2001, 2006). The number of zoeal to movement by ocean currents, and therefore it is instars/stages varies between and among species correlated with larval dispersal distance in the sea within evolutionary constraints (Knowlton 1974, Rice (Shanks et al. 2003, O’Connor et al. 2007, Shanks 1980, Hines 1986, Anger 2001, 2006). Megalopae © The authors 2015. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 94 Sex Early Dev Aquat Org 1: 93–107, 2015 may actively select a suitable habitat for settlement The number of zoeal stages, zoeal duration, and by detecting abiotic and biotic environmental stimuli body length at zoeal and megalopal stages based on such as changes in temperature and salinity, and laboratory rearing have been reported for 9 coeno- chemical cues derived from conspecific adults and/or bitid species: C. brevimanus Dana, 1852 (Hamasaki nursery areas (Anger 2001, 2006, Forward et al. et al. 2014a), C. cavipes Stimpson, 1858 (Shokita & 2001). Therefore, the duration of zoeal and mega- Yamashiro 1986, Nakasone 1988a), C. clypeatus lopal stages should have an effect on population con- (Fabricius, 1787) (Provenzano 1962), C. compressus nection and geographical distribution of species H. Milne-Edwards, 1836 (Brodie & Harvey 2001), C. through dispersal and recruitment processes. purpureus Stimpson, 1858 (Nakasone 1988a), C. Terrestrial hermit crabs of the family Coenobitidae rugosus H. Milne-Edwards, 1837 (Shokita & Yama - comprise 16 species of land hermit crabs of the genus shiro 1986, Nakasone 1988a), C. scaevola (Forskål, Coenobita Latreille, 1829 (McLaughlin et al. 2010), 1775) (Al-Aidaroos & Williamson 1989), C. variabilis and the coconut crab Birgus latro (Linnaeus, 1767). McCulloch, 1909 (Harvey 1992), and B. latro (Reese They mainly occur in subtropical and tropical coastal & Kinzie 1968, Wang et al. 2007, Hamasaki et al. regions (Hartnoll 1988). The coconut crab is the only 2009, Sugizaki et al. 2010). These studies demon- species in the genus Birgus, and is free from gastro- strated intra- and interspecific variations in the num- pod shells except for a juvenile stage that has the ber of zoeal stages, i.e. the developmental pathway shell-carrying habit of its hermit crab ancestors to reach the megalopa stage. However, use of an (Reese 1968, Hamasaki et al. 2011, 2014b). It is the individual culture method whereby the moulting his- largest terrestrial arthropod and has been an impor- tory of individual larvae reared in separate compart- tant local resource for human consumption (Brown & ments is followed (Brodie & Harvey 2001) has been Fielder 1991). However, coconut crab populations applied for 5 species only: C. brevimanus (Hamasaki have been severely depleted on most inhabited et al. 2014a), C. clypeatus (Provenzano 1962), C. islands because of overharvesting and habitat loss compressus (Brodie & Harvey 2001), C. scaevola (Al- (Amesbury 1980, Brown & Fielder 1991, Drew et al. Aidaroos & Williamson 1989) and C. variabilis (Har- 2010). The coconut crab is globally protected, and vey 1992). Reese & Kinzie (1968) also employed the was first listed as ‘Vulnerable’ under the IUCN Red individual culture method for larval rearing of B. List, but was recently categorised as ‘Data deficient’ latro, but their data were based mainly on group cul- in that list — not because the species had recovered ture, which cannot follow the moulting history of but because of the lack of available data (Eldredge individual larvae. 1996, Drew et al. 2010). Land hermit crabs are also Wang et al. (2007) compared the larval develop- the subject of conservation concerns due to their ment of 8 coenobitid species in terms of ecological exploitation as ornamental animals (Nakasone 2001, adaptation, taking adult habitats, body length of the Pavia 2006). glaucothoe (=megalopae), and zoeal life span (num- Although coenobitid species are fully terrestrial, ber of zoeal stages) into consideration. They cate- females return to the sea to hatch their eggs (Hart- gorised 4 development types: mangrove adaptation, noll 1988, Brown & Fielder 1991, Nakasone 2001), larger glaucothoe adaptation, smaller glaucothoe and their larvae develop through planktonic zoeal adaptation, and hypersaline adaptation. However, stages to a megalopa (Nakasone 1988a, Harvey the interspecific variation in the body length at 1992, Brodie & Harvey 2001, Wang et al. 2007, hatching was not taken into account, and the rela- Hamasaki et al. 2009, 2013), similar to marine her- tionship between larval body length and number of mit crab species. After settlement, like marine her- zoeal stages was not analysed thoroughly. mit crabs (Reese 1962, Hazlett & Provenzano 1965), Our objective with this study was to investigate pat- megalopae of terrestrial coenobitid crabs recognise terns of larval growth and development in coenobitid and co-opt gastropod shells before migrating onto species. Larvae of 5 species (C. cavipes, C. purpureus, land (Reese 1968, Harvey 1992, Brodie 1999, 2002, C. rugosus, C. violascens Heller, 1862, and Birgus la- Hamasaki et al. 2011). Therefore, information on tro), whose ovigerous females can be found and col- larval growth, development and duration before lected in subtropical Japan, were cultured individu- metamorphosis into the megalopae is essential for ally, and their moulting, growth and developmental a better understanding of the geographical distri- duration were analysed in conjunction with published bution and population connection of coenobitid data for coenobitid species (C. brevimanus, C. cavipes, species, which in turn have implications for conser- C. clypeatus, C. compressus, C. purpureus, C. rugo- vation of populations. sus, C. scaevola, C. variabilis, and B. latro). Hamasaki et al.: Larvae of terrestrial hermit crabs 95 MATERIALS AND METHODS plex. Artemia (Utah strain) aged 2 d were enriched with a commercial material containing n-3 highly Larval source unsaturated fatty acids (SCP, Chlorella Industry) for 4 h and then fed to the larvae at 2 individuals ml−1. All species belonging to the genus Coenobita in The rotifer B. plicatilis species complex, cultured Japan are recognised collectively as a Natural Mon- with the phytoplankton Chlorella vulgaris containing ument, to promote their conservation. Therefore, n-3 highly unsaturated fatty acids in its cells
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