Abstract
The reproductive system of hermit crabs shows species-specific morphology, which can be used in phylogenetic analysis. Here, we describe the male reproductive system of the hermit crab Dardanus insignis, including morphological and biometric analyses of the spermatophore, the gonopore, and sperm ultrastructure. The morphological analyses were based on 15 selected specimens and carried out by means of light and electron microscopy. Our results indicate a reproductive system composed of lobular testes attached to a simple straight vas deferens connected to the exterior via ventral gonopores. The gonopores are ovoid, surrounded by dense serrulate setae, and covered by a membranous operculum. The spermatophores exhibit a tripartite structure, with an elongate ovoid ampulla, a long narrow stalk, and a proximal foot. The spermatozoal ultrastructure shows three main regions: an ovoid-oblong acrosomal vesicle, a nucleus, and cytoplasm with three armlike extensions. Some of these characteristics can also be found in other species of Diogenidae within the genus Dardanus and in members of Coenobitidae, a closely related family. The available information on spermatophore and spermatozoal structure may indicate a closer similarity between the genus Dardanus and the Coenobitidae, compared with other members of Diogenidae.
Similar content being viewed by others
References
Ahyong ST, Schnabel KE, Maas EW (2009) Anomuran phylogeny: new insights from molecular data. In: Martin JW, Felder DL, Crandall KA (eds) Decapod Crustacean Phylogenetics Crustacean Issues 18. CRC Press, Boca Raton, pp 399–414
Amadio LM, Mantelatto FL (2009) Description of the male reproductive system of the hermit crab Calcinus tibicen (Decapoda: Anomura: Diogenidae). J Crustacean Biol 29:466–475
Bracken-Grissom HD, Cannon ME, Cabezas P, Feldmann RM, Schweitzer CE, Ahyong ST, Felder DL, Lemaitre R, Crandall KA (2013) A comprehensive and integrative reconstruction of evolutionary history for Anomura (Crustacea: Decapoda). BMC Evol Biol 13:1–28
Branco JO, Turra A, Souto FX (2002) Population biology and growth of the hermit crab Dardanus insignis at Armação do Itapocoroy, Southern Brazil. J Mar Biol Assoc UK 82:597–603
Buranelli RC, Mantelatto FL (2012) Reproductive apparatus of the male giant hermit crab Petrochirus diogenes (Anomura, Diogenidae): morphology and phylogenetic implications. Aquat Biol 16:241–251
Felgenhauer BE, Abele LG (1991) Morphological diversity of decapod spermatozoa. In: Bauer RT (ed) Crustacean Sexual Biology. Columbia University Press, New York, pp 322–341
Fernandes-Góes LC, Fransozo A, Góes JM (2005) Population dynamics of Dardanus insignis (Saussure, 1858) (Crustacea, Anomura, Diogenidae) in the Ubatuba region, São Paulo, Brazil. Nauplius 13:191–196
Greenwood JG (1972) The male reproductive system and spermatophore formation in Pagurus novizealandiae (Dana) (Anomura: Paguridea). J Nat Hist 6:561–574
Hamon M (1942) Recherches sur les Spermatophores. Dissertation, L’Université d’Alger
Hebling NJ, Mansur CB (1995) Desenvolvimento larval de Dardanus insignis (Saussure) (Crustacea, Decapoda, Diogenidae) em laboratório. Rev Bras Zool 12:471–491
Hess GS, Bauer RT (2002) Spermatophore transfer in the hermit crab Clibanarius vittatus (Crustacea, Anomura, Diogenidae). J Morphol 253:166–175
Jamieson BGM (1991) Ultrastructure and phylogeny of crustacean spermatozoa. Mem Queensl Mus 31:109–142
Jamieson BGM (1994) Phylogeny of the Brachyura with particular reference to the Podotremata: evidence from a review of spermatozoal ultrastructure (Crustacea, Decapoda). Phil Trans R Soc London [Biol] 345:373–393
Jamieson BGM, Tudge CC (2000) Crustacea-Decapoda. In: Jamieson BGM (ed) Reproductive Biology of Invertebrates. Wiley, Chichester, pp 1–95
Krol RM, Hawkins WE, Overstreet RM (1992) Reproductive components. In: Harrison FW (ed) Microscopic Anatomy of Invertebrates, Decapoda, Crustacea, vol 10. Wiley-Liss, New York, pp 295–343
Manjón-Cabeza ME, García-Raso E (2000) Morphological reproductive aspects of males of Diogenes pugilator (Roux, 1829) (Crustacea, Decapoda, Anomura) from southern Spain. Sarsia 85:195–202
Mantelatto FL, Scelzo MA, Tudge CC (2009) Morphological and morphometric appraisal of the spermatophore of the southern hermit crab Isocheles sawayai Forest and Saint Laurent, 1968 (Anomura: Diogenidae), with comments on gonopores in both sexes. Zool Anz 248:1–8
Matthews DC (1953) The development of the pedunculate spermatophore of a hermit crab Dardanus asper (De Hann). Pac Sci 7:255–266
Matthews DC (1956) The probable method of fertilization in terrestrial hermit crabs based on a comparative study of spermatophores. Pac Sci 10:303–309
McLaughlin PA (1983) Internal anatomy. In: Mantel LH (ed) The biology of Crustacea, vol 10. Academic, London, pp 1–52
McLaughlin PA, Komai T, Lemaitre R, Rahayu DL (2010) Annotated checklist of anomuran decapod crustaceans of the world (exclusive of the Kiwaoidea and families Chirostylidae and Galatheidae of the Galatheoidea) Part I—Lithoidea, Lomisoidea and Paguroidea. Raffles Bull Zool 23:5–107
Meireles AL, Mantelatto FL (2008) Biological features of a puzzling symbiotic association between the hermit crab Dardanus insignis and the porcellanid crab Porcellana sayana (Crustacea). J Exp Mar Biol Ecol 362:38–42
Meireles A, Biagi R, Mantelatto FL (2003) Hermit crabs in evidence: unusual gastropod shell occupation. Nauplius 11:63–66
Melo GAS (1999) Manual de Identificação dos Crustacea Decapoda do Litoral Brasileiro: Anomura, Thalassinidea, Palinuridea, Astacidea. Editora Plêiade, São Paulo
Miranda I, Meireles AL, Biagi R, Mantelatto FL (2006) Is the abundance of the red brocade hermit crab Dardanus insignis (Decapoda: Anomura: Diogenidae) in the infralittoral region of Southern Brazil determined by reproductive potential? Crustacean Res 6:45–55
Mouchet S (1930) Mode de formation des spermatophores chez quelques Pagures. CR Acad Sci III 190:691–692
Mouchet S (1931) Spermatophores des crustacés decápodes anomures et brachyoures et castration parasitaire chez quelques pagures. Ann Stn Océanogr Salammbô 6:1–210
Richter S, Scholtz G (1994) Morphological evidence for a hermit crab ancestry of lithodids (Crustacea, Decapoda, Anomala, Paguroidea). Zool Anz 233:187–210
Sant’Anna BS, Turra A, Zara FJ (2010) Simultaneous activity of male and female gonads in intersex hermit crabs. Aquat Biol 10:201–209
Santos NM, Mantelatto FL (2011) Reproductive system of the male hermit crab Clibanarius sclopetarius: gonopore, spermatophore, and spermatozoal morphologies. Aquat Biol 12:271–280
Scelzo MA, Mantelatto FL, Tudge CC (2004) Spermatophore morphology of the endemic hermit crab Loxopagurus loxochelis (Anomura, Diogenidae) from the Southwestern Atlantic—Brazil and Argentina. Invertebr Reprod Dev 46:1–9
Schnabel KE, Ahyong ST, Maas EW (2011) Galatheoidea are not monophyletic—molecular and morphological phylogeny of the squat lobsters (Decapoda: Anomura) with recognition of a new superfamily. Mol Phylogenet Evol 58:157–168
Subramonian T (1984) Spermatophore formation in two intertidal crabs Albunea symnista and Emerita asiatica (Decapoda: Anomura). Biol Bull 166:78–95
Subramonian T (1991) Chemical composition of spermatophores in decapod crustaceans. In: Bauer RT, Martin JW (eds) Crustacean Sexual Biology. Columbia University Press, New York, pp 308–321
Subramonian T (1993) Spermatophores and sperm transfer in marine crustaceans. Adv Mar Biol 29:129–214
Tirelli T, Pessani D (2007) Multivariate analysis: a useful tool in separating spermatophores produced by the diogenids, Clibanarius erythropus, Diogenes pugilator, and Calcinus tubularis (Decapoda, Anomura, Diogenidae). Crustaceana 80(8):999–1011
Tirelli T, Campantico E, Pessani D, Tudge C (2006) Description of the male reproductive apparatus of the hermit crab Calcinus tubularis (Decapoda: Anomura: Diogenidae). Crustacean Res 6:13–21
Tirelli T, Campantico E, Pessani D, Tudge C (2007) Reproductive biology of mediterranean hermit crabs: male reproductive apparatus of Clibanarius erythropus (Decapoda, Anomura). J Crustacean Biol 27:404–410
Tirelli T, Pessani D, Silvestro D, Tudge C (2008) Reproductive biology of Mediterranean hermit crabs: fine structure of spermatophores and spermatozoa of Diogenes pugilator (Decapoda: Anomura) and its bearing on a sperm phylogeny of Diogenidae. J Crustacean Biol 28:534–542
Tudge CC (1991) Spermatophore diversity within and among the hermit crab families, Coenobitidae, Diogenidae, and Paguridae (Paguroidea, Anomura, Decapoda). Biol Bull 181:238–247
Tudge CC (1992) Comparative ultrastructure of hermit crab spermatozoa (Decapoda: Anomura: Paguroidea). J Crustacean Biol 12:397–409
Tudge CC (1995) Ultrastructure and phylogeny of the spermatozoa of the infraorders Thalassinidea and Anomura (Decapoda, Crustacea). In: Jamieson BG, Ausio J, Justine JL, (eds) Advances in spermatozoal phylogeny and taxonomy. Mém Mus Natl Hist Nat, Paris 166:251–263
Tudge CC (1996) Spermatophore morphology and spermatozoal ultrastructure of the recently described hermit crab, Strigopagurus boreonotus forest, 1995 (Decapoda, Anomura, Diogenidae). Bull Mus Natl Hist Nat, Paris 18:547–555
Tudge CC (1997) Phylogeny of the Anomura (Decapoda, Crustacea): spermatozoa and spermatophore morphological evidence. Contrib Zool 67:125–141
Tudge CC (1999) Spermatophore morphology in the hermit crab families Paguridae and Parapaguridae (Paguroidea, Anomura, Decapoda). Invertebr Reprod Dev 35:203–214
Tudge CC (2009) Spermatozoal morphology and its bearing on decapod phylogeny. In: Martin JM, Crandall KA, Felder DL (eds) Decapod Crustacean Phylogenetics. CRC Press, New York, pp 101–119
Tudge CC, Lemaitre R (2004) Studies of male sexual tubes in hermit crabs (Crustacea, Decapoda, Anomura, Paguroidea). I. Morphology of the sexual tube in Micropagurus acantholepis (Stimpson, 1858), with comments on function and evolution. J Morphol 259:106–118
Tudge CC, Lemaitre R (2006) Studies of male sexual tubes in hermit crabs (Crustacea, Decapoda, Anomura, Paguroidea). II. Morphology of the sexual tube in the land hermit crabs, Coenobita perlatus and C. clypeatus (Coenobitidae). Crustacean Res 6:121–131
Acknowledgments
The present study was supported by a Scientific Initiation Fellowship from the São Paulo Research Foundation (FAPESP) (Proc. 2010/11988-9) to RCB. FLM is grateful to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Proc. 301359/2007-5; PQ 302748/2010-5) and FAPESP (Temático Biota 2010/50188-8; Coleções Científicas 2009/54931-0) for research fellowships and support for this project. FJZ also thanks CNPq for Research Scholarship (PQ 308215/2010-9). A Ph.D fellowship was awarded to RCB by FAPESP (Proc. 2012/06299-5). Special thanks are due to all members of the Laboratory of Bioecology and Crustacean Systematics of FFCLRP/USP for their help with field and laboratory work. Samples were prepared for electron microscopy, analysis, and image capture by Maria Dolores Seabra Ferreira, and José Maulin at the Laboratory of Electron Microscopy of the Faculty of Medicine of Ribeirão Preto, University of São Paulo (USP), and Cláudia A. Rodrigues at the Electron Microscopy Laboratory of the Faculdade de Ciências Agrárias e Veterinárias (FCAV), Universidade Estadual Paulista “Júlio de Mesquita Filho” (UNESP), Jaboticabal. Álvaro da Silva Costa and Djalma Rosa helped with field sampling, and the Instituto Oceanográfico of USP (IO, Ubatuba, SP, Brazil) provided space and infrastructure. We thank Janet W Reid (JWR Associates) for revising the English text and to anonymous reviewer for suggestions and contributions toward improving this article. All experiments conducted in the present study complied with the currently applicable state and federal laws of Brazil.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Schmidt-Rhaesa.
Rights and permissions
About this article
Cite this article
Buranelli, R.C., Zara, F.J. & Mantelatto, F.L. Male reproductive system of the red brocade hermit crab Dardanus insignis (Diogenidae) and its relationship to other family members. Zoomorphology 133, 127–137 (2014). https://doi.org/10.1007/s00435-013-0208-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00435-013-0208-1