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Evidence of simultaneous hermaphroditism in the brooding Diopatra marocensis (Annelida: Onuphidae) from northern Spain

Published online by Cambridge University Press:  19 March 2013

Andrés Arias ,
Alexandra Richter ,
Nuria Anadón  and
Hannelore Paxton
Andrés Arias*
Affiliation:
Department of Biology of Organisms and Systems (Zoology), University of Oviedo, Oviedo 33071, Spain
Alexandra Richter
Affiliation:
Department of Biology of Organisms and Systems (Zoology), University of Oviedo, Oviedo 33071, Spain
Nuria Anadón
Affiliation:
Department of Biology of Organisms and Systems (Zoology), University of Oviedo, Oviedo 33071, Spain
Hannelore Paxton
Affiliation:
Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia Australian Museum, 6 College Street, Sydney, NSW 2010, Australia
*
Correspondence should be addressed to: A. Arias, Department of Biology of Organisms and Systems (Zoology), University of Oviedo, Oviedo 33071, Spain email: ariasandres.uo@uniovi.es
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Abstract

A one-year study of the reproductive biology of a population of Diopatra marocensis at the Villaviciosa estuary, northern Spain, was undertaken with emphasis on brooding behaviour, larval development and gametogenesis. Field observations together with a histological study of monthly collected individuals revealed that the population was iteroparous, reproducing annually during a short breeding season extending from March to June. The study demonstrated that all individuals of the population at Villaviciosa estuary were producing at the same time eggs and sperm providing for the first time evidence for the occurrence of simultaneous hermaphroditism in D. marocensis. Mature sperm was of the ent-aquasperm type and was stored in modified nephridial chambers in brooding individuals. In the latter, eggs in advanced cleavage phases were also observed inside the coelom suggesting that fertilization was internal. Eggs in late vitellogenesis presented micronucleoli in the periphery of the nucleus, a phenomenon reported previously for few polychaete species. Pure males and females were never found. It is here suggested that in D. marocensis population size may influence sex allocation and that under conditions of low population densities simultaneous hermaphrodites may be favoured. The study of the larval development confirmed the direct development reported previously for populations of Morocco and Portugal. Further results suggest consumption of nurse eggs and adelphophagy by developing larvae.

Keywords

polychaetesreproductive cyclegametogenesisent-aquaspermmicronucleolidirect developmentinternal fertilizationnurse eggsadelphophagiaBay of Biscay
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 93 , Issue 6 , September 2013 , pp. 1533 - 1542
Copyright
Copyright © Marine Biological Association of the United Kingdom 2013 

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References

REFERENCES

Arias, A., Anadón, N. and Paxton, H. (2010) New records of Diopatra marocensis (Annelida: Onuphidae) from northern Spain. Zootaxa 2691, 67–68.CrossRefGoogle Scholar
Blake, J.A. (1969) Reproduction and larval development of Polydora from northern New England (Polychaeta: Spionidae). Ophelia 7, 1–63.CrossRefGoogle Scholar
Blake, J.A. and Kudenov, J.D. (1978) The Spionidae (Polychaeta) from southeastern Australia and adjacent areas, with a revision of the genera. Memoirs of the National Museum Victoria 39, 171–280.CrossRefGoogle Scholar
Dhainaut, A. (1972) Evolution nucleolaire au cours de l'ovogenèse de Nereis pelagica: étude morphologique. Journal of Microscopy 13, 67–84.Google Scholar
Eckelbarger, K.J. (2006) Oogenesis. In Rouse, G. and Pleijel, F. (eds) Reproductive biology and phylogeny of Annelida. Cambridge: Enfield Science Publishers, pp. 23–43.Google Scholar
Eulenstein, F. (1914) Über Onuphiden der Nordsee, Wissenschaftliche Meeresuntersuchungen. Abteilung Kiel neue Folge 16, 129–172.Google Scholar
Fadlaoui, S. and Retière, C.H. (1995) Reproduction d'une population de Diopatra marocensis (Paxton, Fadlaoui & Lechapt, 1995) (Polychaeta-Onuphidae) de la côte atlantique marocaine. Bulletin de l'Institut Scientifique Sommaire 19, 111–118.Google Scholar
Fadlaoui, S., Lechapt, J.P. and Retière, C. (1995) Larval development of the onuphid Diopatra marocensis (Annelida: Polychaeta) from the Atlantic coast of Morocco. Journal of the Marine Biological Association of the United Kingdom 75, 957–966.CrossRefGoogle Scholar
Giangrande, A. (1997) Polychaete reproductive patterns, life histories: an overview. Oceanography and Marine Biology: an Annual Review 35, 323–386.Google Scholar
Gibson, G.D. (1997) Variable development in the spionid Boccardia proboscidea (Polychaeta) is linked to nurse egg production and larval trophic mode. Invertebrate Biology 116, 213–226.CrossRefGoogle Scholar
Ghiselin, M.T. (1987) Evolutionary aspects of marine invertebrate reproduction. In Giese, A.C., Pearse, J.S. and Pearse, V.B. (eds) Reproduction of marine invertebrates, Volume 9. General aspects: seeking unity in diversity. Oxford/Palo Alto, CA: Blackwell Scientific/Boxwood Press, pp. 609–665.Google Scholar
Hartman, O. (1967) Polychaetous annelids collected by the USNS Eltanin and Staten Island cruises, chiefly from Antarctic seas. Allan Hancock Monographs in Marine Biology 2, 1–387.Google Scholar
Heath, D.J. (1977) Simultaneous hermaphroditism: cost and benefit. Journal of Theoretical Biology 64, 363–373.CrossRefGoogle ScholarPubMed
Heath, D.J. (1979) Brooding and the evolution of hermaphroditism. Journal of Theoretical Biology 81, 151–155.CrossRefGoogle ScholarPubMed
Hsieh, H.L. and Simon, J.L. (1990) The sperm transfer system in Kinbergonuphis simoni (Polychaeta: Onuphidae). Biological Bulletin: Marine Biological Laboratory, Woods Hole 178, 85–93.CrossRefGoogle ScholarPubMed
Jamieson, B.G. and Rouse, G.W. (1989) The spermatozoa of the Polychaeta (Annelida): an ultrastructural review. Biological Review (Cambridge) 64, 93–157.CrossRefGoogle ScholarPubMed
Mackay, J. and Gibson, G. (1999) The influence of nurse eggs on variable larval development in Polydora cornuta (Polychaeta: Spionidae). Invertebrate Reproduction and Development 35, 167–176.CrossRefGoogle Scholar
Lieber, A. (1931) Zur Oogenese einiger Diopatraarten. Zeitschrift für wissenschaftliche Zoologie 138, 580–649.Google Scholar
Lorenzi, M.C. and Sella, G. (2008) A measure of sexual selection in hermaphroditic animals: parentage skew and the opportunity for selection. Journal of Evolutionary Biology 21, 827–833.CrossRefGoogle ScholarPubMed
Paxton, H. (1986) Generic revision and relationships of the family Onuphidae (Annelida: Polychaeta). Records of the Australian Museum 38, 1–74.CrossRefGoogle Scholar
Paxton, H. (1993) Diopatra Audouin and Milne Edwards (Polychaeta: Onuphidae) from Australia, with a discussion of developmental patterns in the genus. Records of the Northern Territory Museum of Arts and Sciences 10, 115–154.Google Scholar
Pires, A., Quintino, V., Gentil, F., Freitas, R. and Rodrigues, A.M. (2012) Reproductive biology of a brooding Diopatra species: Diopatra marocensis Paxton et al., 1995. Estuarine, Coastal and Shelf Science 110, 85–92.CrossRefGoogle Scholar
Rivest, B. (1983) Development and the influence of nurse egg allotment on hatching size in Searlesia dira (Reeve, 1846) (Prosobranchia: Buccinidae). Journal of Experimental Marine Biology and Ecology 69, 217–241.CrossRefGoogle Scholar
Rodrigues, A.M, Pires, A., Mendo, S. and Quintino, V. (2009) Diopatra neapolitana and Diopatra marocensis from the Portuguese coast: morphological and genetic comparison. Estuarine, Coastal and Shelf Science 85, 609–617.CrossRefGoogle Scholar
Schleicherová, D., Lorenzi, M.C. and Sella, G. (2006) How outcrossing hermaphrodites sense the presence of conspecifics and suppress female allocation. Behavioral Ecology 17, 1–5.CrossRefGoogle Scholar
Schroeder, P.C. and Hermans, C.O. (1975) Annelida: Polychaeta. In Giese, A.G. and Pearse, J.S. (eds) Reproduction of marine invertebrates III. London: Academic Press, pp. 1–169.Google Scholar
Spight, T.M. (1976) Ecology of hatching size for marine snails. Oecologia 24, 283–294.CrossRefGoogle ScholarPubMed
Westheide, W. (1990) A new genus and species of the Syllidae (Annelida, Polychaeta) from south India. Zoologica Scripta 19, 165–167.CrossRefGoogle Scholar
Woodwick, K.H. (1977) Lecithotrophic larval development in Boccardia proboscidea Hartman. In Reish, D.J. and Fauchald, K. (eds) Essays on polychaetous annelids in memory of Dr Olga Hartman. Los Angeles, CA: Allan Hancock Foundation/University of Southern California, pp. 347–371.Google Scholar