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Observations on the ecology and reproductive biology of the sipunculan worm Aspidosiphon muelleri in temperate waters

Published online by Cambridge University Press:  23 June 2014

L.M. Ferrero-Vicente ,
C. Marco-Méndez ,
A. Loya-Fernández  and
J.L. Sánchez-Lizaso
L.M. Ferrero-Vicente*
Affiliation:
Department of Marine Sciences and Applied Biology, University of Alicante, PO Box 99, E-03080 Alicante, Spain Research Marine Centre of Santa Pola (CIMAR), Santa Pola City Council—University of Alicante, Torre d'Enmig s/n, E-03130, Cabo de Santa Pola, Alicante, Spain
C. Marco-Méndez
Affiliation:
Department of Marine Sciences and Applied Biology, University of Alicante, PO Box 99, E-03080 Alicante, Spain
A. Loya-Fernández
Affiliation:
Department of Marine Sciences and Applied Biology, University of Alicante, PO Box 99, E-03080 Alicante, Spain
J.L. Sánchez-Lizaso
Affiliation:
Department of Marine Sciences and Applied Biology, University of Alicante, PO Box 99, E-03080 Alicante, Spain
*
Correspondence should be addressed to: L.M. Ferrero-Vicente, Department of Marine Sciences and Applied Biology, University of Alicante, PO Box 99, E-03080 Alicante, Spain. email: lmferrero@ua.es
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Abstract

A population of the sipunculan worm Aspidosiphon muelleri, located in temperate waters of the western Mediterranean Sea, was monitored monthly for a year. Some aspects related to its ecology and reproductive biology are shown in the present work. The sex-ratio for this population was close to 1:1 (54% females vs 46% males), thus indicating a dioecious reproduction, although showing a lack of sexual dimorphism. Oocytes were detected in females from 4–5 mm; this size might be reached by A. muelleri in a few months. The population density increased notably during the summer (June–August). The spawning event date was indirectly estimated from the average size of the oocytes and the percentage of females with free oocytes in the coelom. Both variables were significantly correlated to shallow water temperature (Pearson correlation; P = 0.003 and P = 0.001, respectively). Oocyte size was also significantly correlated to average irradiance level (Pearson correlation; P = 0.044). Spawning took place between August and September (when the water temperature is getting close to its annual maximum) and may last only a few weeks in these temperate waters. The abundance of A. muelleri decreased drastically in September, likely as a consequence of the spawning event effort. Bivalves of the species Epilepton clarkiae were collected together with specimens of A. muelleri living inside the polychaete tubes used as shelters by the sipunculans, with a prevalence of 11.64%. To a lesser extent some Foraminifera were also reported attached to the body of the sipunculans.

Keywords

sipunculareproductionMediterranean SeagametocytesAspidosiphon muelleriEpilepton clarkiae
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 94 , Issue 8 , December 2014 , pp. 1629 - 1638
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

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References

REFERENCES

Adrianov, A.V. and Maiorova, A.S. (2010) Reproduction and development of common species of peanut worms (Sipuncula) from the sea of Japan. Russian Journal of Marine Biology 36, 1–15.Google Scholar
Adrianov, A.V., Maiorova, A.S. and Malakhov, V.V. (2011) Embryonic and larval development of the peanut worm Phascolosoma agassizii (Keferstein 1867) from the Sea of Japan (Sipuncula: Phascolosomatidea). Invertebrate Reproduction & Development 55, 22–29.CrossRefGoogle Scholar
Açik, S. (2008) Sipunculans along the Aegean coast of Turkey. Zootaxa 1852, 21–36.CrossRefGoogle Scholar
Açik, S. (2011) Sipuncula from the southern coast of Turkey (eastern Mediterranean), with a new report for the Mediterranean Sea. Cahiers de Biologie Marine 52, 313–329.Google Scholar
Açik, S., Murina, G.V., Çinar, M.E. and Ergen, Z. (2005) Sipunculans from the coast of northern Cyprus (eastern Mediterranean Sea). Zootaxa 1077, 1–23.Google Scholar
Åkesson, B. (1958) A study of the nervous system of the Sipunculideae: with some remarks on the development of the two species Phascolion strombi Montagu and Golfingia minuta Keferstein. Undersökningar över Öresund 38, 1–249.Google Scholar
Amor, A. (1993) Reproductive cycle of Golfingia margaritacea, a bipolar sipunculan, in subantarctic water. Marine Biology 117, 409–414.CrossRefGoogle Scholar
Bolam, S.G. and Fernandes, T.F. (2002) Dense aggregations of tube-building polychaetes: response to small-scale disturbances. Journal of Experimental Marine Biology and Ecology 269, 197–222.CrossRefGoogle Scholar
Buchanan, J.B. (1984) Sediment analysis. In Holme, N.A. and McIntyre, A.D. (eds) Methods for the study of marine benthos. 2nd edition. Oxford: Blackwell Scientific Publications, pp. 41–46.Google Scholar
Cutler, E.B. (1994) The sipuncula: their systematics, biology, and evolution. Ithaca, NY: Cornell University Press, 453 pp.Google Scholar
Cutler, E.B. and Cutler, N.J. (1986) A revision of the genus Nephasoma (Sipuncula: Golfingiidae). Proceedings of the Biological Society of Washington 99, 547–573.Google Scholar
Cutler, E.B. and Cutler, N.J. (1989) A revision of the genus Aspidosiphon (Sipuncula: Aspidosiphonidae). Proceedings of the Biological Society of Washington 102, 826–865.Google Scholar
Ferrero-Vicente, L.M., Del-Pilar-Ruso, Y., De-La-Ossa-Carretero, J.A. and Sánchez-Lizaso, J.L. (2013a) Distribution of Sipuncula in the Gulf of Valencia and Cape Nao (western Mediterranean). Zootaxa 3646, 235–250.Google Scholar
Ferrero-Vicente, L.M., Loya-Fernández, A., Marco-Méndez, C., Martínez–García, E. and Sánchez-Lizaso, J.L. (2011) Soft–bottom sipunculans from San Pedro del Pinatar (Western Mediterranean): influence of anthropogenic impacts and sediment characteristics on their distribution. Animal Biodiversity and Conservation 34, 101–111.Google Scholar
Ferrero-Vicente, L.M., Loya-Fernández, A., Marco-Méndez, C., Martínez–García, E., Saiz-Salinas, J.I. and Sánchez-Lizaso, J.L. (2012) First record of the sipunculan worm Phascolion (Phascolion) caupo Hendrix, 1975 in the Mediterranean Sea. Mediterranean Marine Science 13, 89–92.Google Scholar
Ferrero-Vicente, L.M., Marco-Méndez, C., Loya-Fernández, A. and Sánchez-Lizaso, J.L. (2013b) Limiting factors on the distribution of shell/tube-dwelling sipunculans. Journal of Experimental Marine Biology and Ecology 446, 345–354.Google Scholar
Gage, J. (1968) The mode of life of Mysella cuneata, a bivalve ‘commensal’ with Phascolion strombi (Sipunculoidea). Canadian Journal of Zoology 46, 919–934.Google Scholar
Gage, J. (1979) Mode of life and behaviour of Montacuta phascolionis, a bivalve commensal with the sipunculan Phascolion strombi. Journal of the Marine Biological Association of the United Kingdom 59, 635–657.Google Scholar
Gibbs, P.E. (1975) Gametogenesis and spawning in a hermaphroditic population of Golfingia minuta (Sipuncula). Journal of the Marine Biological Association of the United Kingdom 55, 69–82.Google Scholar
Gibbs, P.E. (1977) British sipunculans. Synopses of the British Fauna No. 12. London:The Linnean Society of London, pp. 1–35.Google Scholar
Grémare, A., Amouroux, J.M. and Vétion, G. (1998a) Long-term comparison of macrobenthos within the soft bottoms of the Bay of Banyuls-sur-mer (northwestern Mediterranean Sea). Journal of Sea Research 40, 281–302.Google Scholar
Grémare, A., Sardá, R., Medernach, L., Jordana, E., Pinedo, S., Amouroux, J.M., Martin, D., Nozais, C. and Charles, F. (1998b) On the dramatic increase of Ditrupa arientina O.F. Müller (Annelida: Polychaeta) along both the French and the Spanish Catalan coasts. Estuarine, Coastal and Shelf Science 47, 447–457.Google Scholar
Hall, J.R. and Scheltema, R.S. (1975) Comparative morphology of open-ocean Pelagospaera. In Rice, M.E. and Todorović, M. (eds) Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Naucno Delo Press, pp. 183–197.Google Scholar
Johnson, R.C., Carreiro, M.M., Jin, H.S. and JacK, J.D. (2012) Within-year temporal variation and life-cycle seasonality affect stream macroinvertebrate community structure and biotic metrics. Ecological Indicators 13, 206–214.CrossRefGoogle Scholar
Klaoudatos, S.D., Klaoudatos, D.S., Smith, J., Bogdanos, K. and Papageorgiou, E. (2006) Assessment of site specific benthic impact of floating cage farming in the eastern Hios island, Eastern Aegean Sea, Greece. Journal of Experimental Marine Biology and Ecology 338, 96–111.Google Scholar
Koukouras, A., voultsiadou-koukoura, E., Chintiroglou, H. and Dounas, C. (1985) Benthic bionomy of the North Aegean Sea. III. A comparison of the macrobenthic animal assemblages associated with seven sponge species. Cahiers de Biologie Marine 26, 301–319.Google Scholar
Labrune, C., Grémare, A., Guizien, K. and Amouroux, J.M. (2007) Long-term comparison of soft bottom macrobenthos in the Bay of Banyuls-sur-Mer (north-western Mediterranean Sea): a reappraisal. Journal of Sea Research 58, 125–143.Google Scholar
Maiorova, A.S. and Adrianov, A.V. (2005) The first finding of spermatozeugmata in sipunculids (Sipuncula), animals with external fertilization. Doklady Biological Sciences 402, 214–216.Google Scholar
Maiorova, A.S. and Adrianov, A.V. (2007) Ultrastructural observations on spermiogenesis in the peanut worm, Themiste pyroides (Chamberlin, 1920) (Sipuncula; Sipunculidea). Invertebrate Reproduction & Development 50, 173–180.Google Scholar
McMillan (1968) British shells. London: Frederick Warne & Co. Ltd., 196 pp.Google Scholar
Morton, B. and Harper, E.M. (2009) Drilling predation upon Ditrupa arietina (Polychaeta: Serpulidae) from the Mid-Atlantic Açores, Portugal. Açoreana Suplemento 6, 157–165.Google Scholar
Morton, B. and Salvador, A. (2009) The biology of the zoning subtidal polychaetes Ditrupa arietina (Serpulidae) in the Açores, Portugal, with a description of the life history of its tube. Açoreana Suplemento 6, 145–156.Google Scholar
Murina, V.V. (1975) Ways of evolution and phylogeny of the phylum Sipuncula. Zoologicheskii Zhurnal 54, 1747–1758.Google Scholar
Murina, G.V.V., Pancucci-Papadopoulou, M.A. and Zenetos, A. (1999) The phylum Sipuncula in the eastern Mediterranean: composition, ecology, zoogeography. Journal of the Marine Biological Association of the United Kingdom 79, 821–830.Google Scholar
O'Connor, M.I., Bruno, J.F., Gaines, S.D., Halpern, B.S., Lester, S.E., Kinlan, B.P. and Weiss, J.M. (2007) Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation. Proceedings of the National Academy of Sciences of the United States of America 104, 1266–1271.CrossRefGoogle ScholarPubMed
Pancucci-Papadopoulou, M.A., Murina, V.V. and Zenetos, A. (1999) The phylum Sipuncula in the Mediterranean Sea. Athens: National Center for Marine Research, 109 pp.Google Scholar
Papazacharias, A., Koukouras, A., Kevrekidis, T. and Voultsiadou, E. (1998) Infra – and circalittoral soft substratum macrofaunal assemblages of Kavala Gulf (Aegean Sea). International Review of Hydrobiology 83, 461–477.Google Scholar
Picard, J. (1965) Recherches qualitatives sur les biocoenoses marines des substrats meubles dragables de la région marseillaise. Bulletin des Recherches et Travaux de la Station Marine d'Endoume 52, 1–160.Google Scholar
Pilger, J.F. (1987) Reproductive biology and development of Themiste lageniformis, a parthenogenic sipunculan. Bulletin of Marine Science 41, 59–67.Google Scholar
Por, F.D. (1975) Boring species of Aspidosiphon (Sipuncula) on the coasts of Israel. In Rice, M.E. and Todorović, M. (eds) Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Naucno Delo Press, pp. 301–304.Google Scholar
Rice, M.E. (1967) A comparative study of the development of Phascolosoma agassizii, Golfingia pugettensis, and Themiste pyroides with a discussion of developmental patterns in the Sipuncula. Ophelia 4, 143–171.Google Scholar
Rice, M.E. (1970) Asexual reproduction in a Sipunculan worm. Science 167, 1618–1620.Google Scholar
Rice, M.E. (1975a) Sipuncula. In Giese, A.C. and Pearse, J.S. (eds) Reproduction of marine invertebrates. Volume II: entoprocts and lesser coelomates. New York: Academic Press, pp. 67–125.Google Scholar
Rice, M.E. (1975b) Observation of the development of six species of Caribbean Sipuncula with a review of development in the phylum. In Rice, M.E. and Todorović, M. (eds) Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Naucno Delo Press, pp. 141–160.Google Scholar
Rice, M.E. (1976) Larval development and metamorphosis in Sipuncula. American Zoologist 16, 563–571.Google Scholar
Rice, M.E. (1981) Larvae adrift: patterns and problems in life histories of sipunculans. American Zoologist 21, 605–619.Google Scholar
Rice, M.E. (1988). Observations on development and metamorphosis of Siphonosoma cumanense with comparative remarks on Sipunculus nudus (Sipuncula, Sipunculidae). Bulletin of Marine Science 42, 1–15.Google Scholar
Rice, M.E. (1989) Comparative observations of gametes, fertilization, and maturation in sipunculans. In Ryl, J.S. and Tyler, P.A. (eds) Reproduction, genetics and distributions of marine invertebrates. 23rd European marine biology symposium. Fredensborg: Olsen & Olsen, pp. 167–182.Google Scholar
Rice, M.E., Reichardt, H.F., Piraino, J. and Young, C.M. (2012) Reproduction, development, growth, and the length of larval life of Phascolosoma turnerae, a wood-dwelling deep-sea sipunculan. Invertebrate Biology 131, 204–215.Google Scholar
Saiz-Salinas, J.I. (1986) Los gusanos sipuncúlidos (Sipuncula) de los fondos litorales y circalitorales de las costas de la Península Ibérica, Islas Baleares, Canarias y mares adyacentes. Monografías del Instituto Español de Oceanografía 1, 84.Google Scholar
Saiz-Salinas, J.I. (1993) Sipuncula. In Ramos, M.A. et al. (eds) Fauna Ibérica. Volume 4. Museo Nacional de Ciencias Naturales. Madrid: CSIC, 200 pp.Google Scholar
Saiz-Salinas, J.I. and Villafranca-Urchegui, L. (1990) Sipuncula from the Alboran Sea and Ibero-Moroccan Bay. Journal of Natural History 24, 1143–1177.Google Scholar
Sardá, R., Pinedo, S. and Martin, D. (1999) Seasonal dynamics of macroinfaunal key species inhabiting shallow soft-bottoms in the Bay of Blanes (NW Mediterranean). Acta Oecologica 20, 315–326.Google Scholar
Scheltema, R.S. and Hall, J.R. (1975) The dispersal of pelagosphaera larvae by ocean currents and the geographical distribution of sipunculans. In Rice, M.E. and Todorović, M. (eds) Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Volume 1. Belgrade: Naucno Delo Press, pp. 103–116.Google Scholar
Schembri, P.J. and Jaccarini, V. (1978) Some aspects of the ecology of the echiuran worm Bonellia viridis and associated infauna. Marine Biology 47, 55–61.Google Scholar
Schulze, A. and Rice, M.E. (2009) Nephasoma pellucidum: a model species for sipunculan development? Smithsonian Contributions to the Marine Sciences 38, 209–217.Google Scholar
Somaschini, A., Martini, N., Gravina, M.F., Belluscio, A., Corsi, F. and Ardizzone, G. D. (1998) Characterization and cartography of some Mediterranean soft-bottom benthic communities (Ligurian Sea, Italy). Scientia Marina 62, 27–36.Google Scholar
Troncoso, J.S. and Urgorri, V. (1992) Asociación de Tellimya phascolionis (Dautzenberg et Fischer, 1925) (Bivalvia, Montacutidae) con el sipuncúlido Phascolion strombi (Montagu, 1804) en la Ría de Ares y Betanzos (Galicia, NO de España). Boletín de la Real Sociedad Española de Historia Natural (Sección Biológica) 88, 189–194.Google Scholar
Vera-García, F., García-Cascales, J.R. and Hernández-Guillén, Z. (2008) Atlas de irradiación solar y temperatura ambiente de la Comunidad Autónoma de la Región de Murcia. Universidad Politécnica de Cartagena y Agencia de Gestión de la Energía de la Región de Murcia (ARGEM). Cartagena. 136.Google Scholar
Wanninger, A., Koop, D., Bromham, L., Noonan, E. and Degnan, B.M. (2005) Nervous and muscle system development in Phascolion strombus (Sipuncula). Development, Genes and Evolution 215, 509–518.Google Scholar
Ying, X.P., Dahms, H.U., Liu, X.M., Wu, H.X., Zhang, Y.P., Chen, C. and Yang, W.X. (2009) Development of germ cells and reproductive biology in the sipunculid Phascolosoma esculenta. Aquaculture Research 40, 305–314.Google Scholar