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Spermatophore and spermatozoal ultrastructure of the Mediterranean hermit crab Pagurus excavatus (Paguridae: Anomura: Decapoda)

Published online by Cambridge University Press:  26 February 2013

Tina Tirelli*
Affiliation:
Life Sciences and Systems Biology Department, University of Torino–Via Accademia Albertina, 13–10123 Torino (Italy)
Marco Gamba
Affiliation:
Life Sciences and Systems Biology Department, University of Torino–Via Accademia Albertina, 13–10123 Torino (Italy)
Daniela Pessani
Affiliation:
Life Sciences and Systems Biology Department, University of Torino–Via Accademia Albertina, 13–10123 Torino (Italy)
Christopher C. Tudge
Affiliation:
Biology Department, American University, Washington, DC, 20016-8007, USA and Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington DC, 20013-7012, USA
*
Correspondence should be addressed to: T. Tirelli, Life Sciences and Systems Biology Department, University of Torino-Via Accademia Albertina, 13–10123 Torino (Italy) email: [email protected]

Abstract

The ultrastructure of the spermatophores and spermatozoa of the Mediterranean hermit crab Pagurus excavatus are described, using transmission electron microscopy. The size of the different parts of the spermatophore and spermatozoa are given and their ultrastructure described and compared to similar data already present in the literature for other hermit crabs. The morphology and ultrastructure of the spermatophore and spermatozoa of P. excavatus are species-specific, clearly distinguishing the species from the others already described. The spermatophore and spermatozoa show some similarities with those produced by other representatives of the genus. In particular, the tripartite spermatophore is divided into two halves by the lateral ridge and, as with the spermatophores produced by other species belonging to the genus Pagurus, it is morphologically very different from any other Paguroidea. The spermatozoa are composed of an ovoidal acrosomal vesicle capped by the operculum; the acrosome has a length:width ratio of approximately 1.75, therefore larger than 1 as reported for all anomurans studied to date. At the base of the acrosomal vesicle, there is the thin cytoplasm, the large nucleus and three arms positioned to form a 120° angle between each other. The present description is an important additional step allowing for better understanding of the relationships among the different hermit crab taxa.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2013 

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References

REFERENCES

Amadio, L.M. and Mantelatto, F.L. (2009) Description of the male reproductive system of the hermit crab Calcinus tibicen (Decapoda: Anomura: Diogenidae). Journal of Crustacean Biology 29, 466475.CrossRefGoogle Scholar
Bastock, M. (1967) Courtship: an ethological study. Chicago, IL: Aldine Press.Google Scholar
Bauer, R.T. (1986) Phylogenetic trends in sperm transfer and storage complexity in decapod crustaceans. Journal of Crustacean Biology 6, 313325.CrossRefGoogle Scholar
Bauer, R.T. (1991) Sperm transfer and storage structures in penaeoid shrimps. A functional and phylogenetic perspective. In Bauer, R.T. and Martin, J.W. (eds) Crustacean sexual biology. New York: Columbia University Press, pp. 183207.CrossRefGoogle Scholar
Chintiroglou, C., Doumenc, D. and Koutsoubas, D. (1992) Allométrie d'une nouvelle association entre le décapode anomure Pagurus excavatus (Herbst, 1991) et l'actinie acontiaire Sagartiogeton undatus (Müller, 1788). Crustaceana 62, 111.CrossRefGoogle Scholar
De Grave, S., Pentcheff, N.D., Ahyong, S.T., Chan, T.-Y., Crandall, K.A., Dworschak, P.C., Felder, D.L., Feldmann, R.M., Fransen, C.H.J.M., Goulding, L.Y.D., Lemaitre, R., Low, M.E.Y., Martin, J.W., Ng, P.K.L., Schweitzer, C.E., Tan, S.H., Tshudy, D. and Wetzer, R. (2009) A classification of living and fossil genera of decapods crustaceans. Raffles Bulletin of Zoology Supplement 21, 1109.Google Scholar
Doumenc, D., Chintiroglou, C. and Koukouras, A. (1985) Actinies de la Mer Egée: methods d'identification zoogéographie. Bulletin du Muséum d'Histoire Naturelle, Paris 7, 497529.CrossRefGoogle Scholar
Fantucci, M.Z. and Mantelatto, F.L. (2011) Male reproductive apparatus and spermatophore morphology of the hermit crabs Pagurus brevidactylus and P. criniticornis (Anomura, Paguridae). Journal of Morphology 272, 12711280.CrossRefGoogle ScholarPubMed
Felgenhauer, B.E. and Abele, L.G. (1991) Morphological diversity of decapod spermatozoa. In Bauer, R.T. and Martin, J.W. (eds) Crustacean sexual biology. New York: Columbia University Press, pp. 322341.CrossRefGoogle Scholar
Greenwood, J.G. (1972) The male reproductive system and spermatophore formation in Pagurus novae-zealandiae (Dana) (Anomura: Paguridea). Journal of Natural History 6, 561574.CrossRefGoogle Scholar
Hazlett, B.A. (1968) The sexual behaviour of some European hermit crabs. Pubblicazioni della Stazione Zoologica di Napoli 36, 238252.Google Scholar
Hess, G.S. and Bauer, R.T. (2002) Spermatophore transfer in the hermit crab Clibanarius vittatus (Crustacea, Anomura, Diogenidae). Journal of Morphology 253, 166175.CrossRefGoogle ScholarPubMed
Hinsch, G.W. (1991) Ultrastructure of the sperm and spermatophores of the Anomuran crab Pleuroncodes planipes. Journal of Crustacean Biology 11, 1722.CrossRefGoogle Scholar
Ingle, R. (1993) Hermit crabs of the northeastern Atlantic Ocean and Mediterranean Sea. An illustrated key. London: Chapman & Hall.Google Scholar
Jamieson, B.G.M. (1991) Ultrastructure and phylogeny of crustacean spermatozoa. Memoirs of the Queensland Museum 31, 109142.Google Scholar
Jamieson, B.G.M. and Tudge, C.C. (2000) Crustacea–Decapoda. In Jamieson, B.G.M. (ed.) Reproductive biology of invertebrates. Progress in male gamete ultrastructure and phylogeny, Volume IX, part c. Chichester: John Wiley & Sons, pp. 195.Google Scholar
Krol, R.M., Hawkins, W.E. and Overstreet, R.M. (1992) Reproductive components. In Harrison, F.W. (ed.) Microscopic anatomy of invertebrates, Decapoda, Crustacea, Volume 10. New York NY: Wiley-Liss, pp. 295343.Google Scholar
Kronenberger, K., Brandis, D., Turkay, M. and Storch, V. (2004) Functional morphology of the reproductive system of Galathea intermedia (Decapoda, Anomura). Journal of Morphology 262, 500516.CrossRefGoogle ScholarPubMed
Lemaitre, R. and Cruz Castaño, N. (2004) A new species of Pagurus Fabricius, 1775 from the Pacific coast of Colombia, with a checklist of eastern Pacific species of the genus. Nauplius 12, 7182.Google Scholar
Mainardi, D. and Rossi, A.C. (1969) Adamsia palliata and Calliactis parasitica on the same Pagurus excavatus (first record), and the problem of A. palliate as obligatory partner of P. prideaux. Atti della Società Italiana di Scienze Naturali 109, 220222.Google Scholar
Manjón-Cabeza, M.E. and García Raso, J.E. (2000) Morphological reproductive aspects of males of Diogenes pugilator (Roux, 1829) (Crustacea, Decapoda, Anomura) from southern Spain. Sarsia 85, 195202.CrossRefGoogle Scholar
Mantelatto, F.L., Scelzo, M.A. and Tudge, C.C. (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. Zoologischer Anzeiger 248, 18.CrossRefGoogle Scholar
Matthews, D.C. (1957) Further evidences of anomuran nonpedunculate spermatophores. Pacific Science 11, 380385.Google Scholar
McLaughlin, P.A. (1980) Comparative morphology of the recent crustacea. San Francisco, CA: W.H. Freeman.Google Scholar
McLaughlin, P.A. (1983) Internal anatomy. In Mantel, L.H. (ed.) The biology of crustacea, Volume 5. London: Academic Press, pp. 152.Google Scholar
McLaughlin, P.A., Komai, T., Lemaitre, R. and Rahayu, D.L. (2010) Annotated checklist of anomuran decapod crustaceans of the world (exclusive of the Kiwaoidea and families Chirostylidae and Gatatheidae of the Galatheoidea) Part I—Lithodoidea, Lomisoidea and Paguroidea. Raffles Bulletin of Zoology Supplement 23, 5107.Google Scholar
Mouchet, S. (1930) Mode de formation des spermatophores chez quelques Pagures. Comptes rendus de l'Académie des Sciences, Paris 190, 691693.Google Scholar
Mouchet, S. (1931) Spermatophores des Crustacés Décapodes Anomoures et Brachyoures et castration parasitaire chez quelques Pagures. Annales Station Océanographique de Salammbô 6, 1203.Google Scholar
Mura, M. and Cau, A. (2002) Biologia riproduttiva di Pagurus excavatus (Fabricius, 1775) (Crustacea; Paguridae) nel Canale di Sardegna. Biologia Marina Mediterranea 9, 770773.Google Scholar
Mura, M., Orrù, F. and Cau, A. (2006) Reproduction strategy of the deep-sea hermit crabs Pagurus alatus and Pagurus excavatus of the Central-Western Mediterranean Sea. Hydrobiologia 557, 5157.CrossRefGoogle Scholar
Pax, F. and Müller, I. (1962). Die anthozoenfauna der Adria. Fauna et flora Adriatica, III. Institut za Oceanografiju i Ribarstvo, Split, pp. 1343.Google Scholar
Ross, D.M. (1979) ‘Stealing’ of the symbiotic anemone, Calliactis parasitica, in intraspecific and interspecific encounters of three species of Mediterranean pagurids. Canadian Journal of Zoology 6, 11811189.CrossRefGoogle Scholar
Santos, N.M. and Mantelatto, F.L. (2011) Reproductive system of the male hermit crab Clibanarius sclopetarius: gonopore, spermatophore, and spermatozoal morphologies. Aquatic Biology 12, 271280.CrossRefGoogle Scholar
Scelzo, M.A., Mantelatto, F.L. and Tudge, C.C. (2004) Spermatophore morphology of the endemic hermit crab Loxopagurus loxochelis (Anomura, Diogenidae) from the southwestern Atlantic—Brazil and Argentina. Invertebrate Reproduction and Development 46, 19.CrossRefGoogle Scholar
Scelzo, M.A., Medina, A. and Tudge, C.C. (2006) Spermatozoal ultrastructure of the hermit crab Loxopagurus loxochelis (Moreira, 1901) (Anomura, Diogenidae) from the southwestern Atlantic. In Asakura, A. (ed.) Biology of Anomura II, Crustacean Research, Special Number 6. Tokyo: Kokusai-Bunken Printing Inc., pp. 111.Google Scholar
Scelzo, M.A., Fantucci, M.Z. and Mantelatto, F.L. (2010) Spermatophore and gonopore morphology of the Southwestern-Atlantic hermit crab Pagurus exilis (Benedict, 1892) (Anomura, Paguridae). Zoological Studies 49, 421433.Google Scholar
Subramoniam, T. (1982) A morphological investigation on the spermatophores of selected crustaceans. In Subramoniam, T. (ed.) Manual of research methods for marine invertebrate reproduction, Volume 9. Kochi: Central Marine Fisheries Research Institute, pp. 9398.Google Scholar
Subramoniam, T. (1993) Spermatophores and sperm transfer in marine crustaceans. In Blaxter, J.H.S. and Southward, A.J. (eds) Advances in marine biology. New York: Academic Press, pp. 129214.Google Scholar
Subramoniam, T. (1995) Light and electron microscopic studies on the seminal secretions and the vas deferens of the penaeiodean shrimp, Sicyonia ingentis. Journal of Biosciences 20, 691706.CrossRefGoogle Scholar
Tirelli, T., Campantico, E., Pessani, D. and Tudge, C.C. (2006) Description of the male reproductive apparatus of the hermit crab Calcinus tubularis (Anomura, Diogenidae). In Asakura, A. (ed.) Biology of Anomura II, Crustacean Research, Special Number 6. Tokyo: Kokusai-Bunken Printing Inc., pp. 1321.Google Scholar
Tirelli, T., Campantico, E., Pessani, D. and Tudge, C.C. (2007) Reproductive biology of the Mediterranean hermit crabs: male reproductive apparatus of Clibanarius erythropus (Decapoda Anomura). Journal of Crustacean Biology 27, 404410.CrossRefGoogle Scholar
Tirelli, T., Pessani, D., Silvestro, D. and Tudge, C.C. (2008) Reproductive biology of the Mediterranean hermit crabs: fine structure of spermatophores and spermatozoa of Diogenes pugilator (Decapoda, Anomura) and its bearing on a sperm phylogeny of the Diogenidae. Journal of Crustacean Biology 28, 534542.CrossRefGoogle Scholar
Tirelli, T., Pessani, D., Silvestro, D. and Tudge, C.C. (2010) Description of the male reproductive system of Paguristes eremita (Anomura, Diogenidae) and its placement in a phylogeny of diogenid species based on spermatozoal and spermatophore ultrastructure. Zoologischer Anzeiger 248, 299312.CrossRefGoogle Scholar
Tudge, C.C. (1991) Spermatophore diversity within and among the hermit crab families, Coenobitidae, Diogenidae and Paguridae (Paguroidea, Anomura, Decapoda). Biological Bulletin. Marine Biological Laboratory, Woods Hale 181, 238247.CrossRefGoogle ScholarPubMed
Tudge, C.C. (1992) Comparative ultrastructure of hermit crab spermatozoa (Decapoda: Anomura: Paguroidea). Journal of Crustacean Biology 12, 397409.CrossRefGoogle Scholar
Tudge, C.C. (1995a) Ultrastructure and phylogeny of anomuran crab spermatozoa. PhD thesis. University of Queensland, Australia.Google Scholar
Tudge, C.C. (1995b) Ultrastrucure and phylogeny of the spermatozoa of the infraorders Thalassinidea and Anomura (Decapoda, Crustacea). In Jamieson, B.G.M, Ausio, J. and Justine, J.L. (eds) Advances in spermatozoal phylogeny and taxonomy. Mémoires du Muséum d'Histoire Naturelle, Paris 166, 251263.Google Scholar
Tudge, C.C. (1996) Spermatophore morphology and spermatozoa ultrastructure of the recently described hermit crab, Strigopagurus boreonotus Forest, 1995 (Decapoda, Anomura, Diogenidae). Bulletin du Muséum National d'Histoire Naturelle, Paris 18, 547555.CrossRefGoogle Scholar
Tudge, C.C. (1997) Phylogeny of the Anomura (Decapoda, Crustacea): spermatozoa and spermatophore morphological evidence. Contributions to Zoology 67, 125141.CrossRefGoogle Scholar
Tudge, C.C. (1999a) Ultrastructure of the spermatophore lateral ridge in hermit crabs (Decapoda, Anomura, Paguroidea). Crustaceana 72, 7784.CrossRefGoogle Scholar
Tudge, C.C. (1999b) Spermatophore morphology in the hermit crab families Paguridae and Parapaguridae (Paguroidea, Anomura, Decapoda). Invertebrate Reproduction and Development 35, 203214.CrossRefGoogle Scholar
Tudge, C.C. (2009) Spermatozoal morphology and its bearing on decapods phylogeny. In Martin, J.W., Crandall, K.A. and Felder, D.L. (eds) Decapod crustacean phylogenetics. Crustacean Issues 18. Boca Raton, FL: CRC Press, pp. 101119.CrossRefGoogle Scholar
Tudge, C.C. and Justine, J.L. (1994) The cytoskeletal proteins actin and tubulin in the spermatozoa of four decapod crabs (Crustacea, Decapoda). Acta Zoologica 75, 277285.CrossRefGoogle Scholar
Tudge, C.C. and Jamieson, B.G.M. (1996) Spermatophore and spermatozoal morphology in the Porcellanidae. I. Aliaporcellana suluensis and Pisidia longicornis (Decapoda: Anomura: Porcellanidae). Crustacean Research 25, 7385.CrossRefGoogle Scholar
Tudge, C. and 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. Journal of Morphology 259, 106118.CrossRefGoogle ScholarPubMed
Tudge, C.C. and Lemaitre, R. (2006) Studies of male sexual tubes in hermit crabs (Crustacea, Decapoda, Anomura, Coenobitidae). II. Morphology of the sexual tube in the land hermit crabs, Coenobita perlatus and C. clypeatus. Crustacean Research, Special Number 6 121131.CrossRefGoogle Scholar
Tudge, C.C. and Scheltinga, D.M. (2002) Spermatozoal morphology of the freshwater anomuran Aegla longirostri Bond-Buckup, 1994 (Crustacea: Decapoda: Aeglidae) from South America. Proceedings of the Biological Society of Washington 115, 118128.Google Scholar
Tudge, C.C., Grellier, P. and Justine, J.L. (1994) Actin in the acrosome of the spermatozoa of the crab, Cancer pagurus L. (Decapoda, Crustacea). Molecular Reproduction and Development 38, 178186.CrossRefGoogle ScholarPubMed
Tudge, C.C., Scheltinga, D.M. and Jamieson, B.G.M. (1999) Spermatozoal ultrastructure in the Hippoidea (Anomura, Decapoda). Journal of Submicroscopic Cytology and Pathology 31, 113.Google Scholar
Tudge, C.C., Scheltinga, D.M. and Jamieson, B.G.M. (2001) Spermatozoal morphology in the symmetrical hermit crab, Pylocheles (Bathycheles) sp. (Crustacea, Decapoda, Anomura, Paguroidea, Pylochelidae). Zoosystema 23, 117130.Google Scholar
Tudge, C.C., Jamieson, B.G.M., Sandberg, L. and Ersèus, C. (1998a) Ultrastructure of the mature spermatozoon of the king crab Lithodes maja (Lithodidae, Anomura, Decapoda): further confirmation of a lithodid–pagurid relationship. Invertebrate Biology 117, 5766.CrossRefGoogle Scholar
Tudge, C.C., Jamieson, B.G.M., Segonzac, M. and Guinot, D. (1998b) Spermatozoal ultrastructure in the three species of hydrothermal vent crab, in the genera Bythograea, Austinograea and Segonzacia (Decapoda, Brachyura, Bythograeidae). Invertebrate Reproduction and Development 34, 1323.CrossRefGoogle Scholar