Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-26T17:55:59.589Z Has data issue: false hasContentIssue false
  • English
  • Français

Reproduction, larval development and settlement of the intertidal serpulid polychaete Spirobranchus cariniferus

Published online by Cambridge University Press:  07 December 2012

Louis A. Gosselin  and
Mary A. Sewell
Louis A. Gosselin*
Affiliation:
Department of Biological Sciences, Thompson Rivers University, 900 McGill Road, Kamloops BC, V2C 0C8, Canada Department of Biology, University of Victoria, Victoria BC, V8W 3N3, Canada
Mary A. Sewell
Affiliation:
School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand
*
Correspondence should be addressed to: Louis Gosselin, Department of Biological Sciences, Thompson Rivers University, 900 McGill Road, Kamloops BC, V2C 0C8, Canada email: lgosselin@tru.ca
Get access Rights & Permissions [Opens in a new window]

Abstract

Serpulid polychaetes are often important components of marine communities, yet current knowledge of serpulid reproduction, development and settlement is largely based on the study of only a few species. This study examined whether spawning and sexual development of the mid-intertidal serpulid Spirobranchus cariniferus are typical of patterns observed in other serpulids, and also examined the effect of diet on larval development and identified cues that induce metamorphosis. Populations of S. cariniferus on the east and west coasts of New Zealand's North Island had an extended spawning season with a high proportion (75–100%) of individuals carrying ripe gametes at any given time from the late spring to early autumn, consistent with other serpulid species. However, contrary to proposed patterns of sexual development in serpulids, sex-ratios and average male and female body masses suggest S. cariniferus are not protandric hermaphrodites. A diet experiment revealed that larval growth was fastest when provided with a mixed diet of three algal species. Solutions of 3-isobutyl-1-methylxanthine at a concentration of 10−4 M were potent inducers of metamorphosis in S. cariniferus larvae, revealing that competence is reached by 13–15 days after fertilization. When exposed to surfaces coated with conspecific tube or tissue homogenates, 6% of competent larvae settled and metamorphosed on surfaces coated with tube homogenate whereas none settled on tissue homogenate or in the controls, suggesting specific cues are required for settlement and the likely presence of a settlement cue in the tubes of adult worms, consistent with the highly gregarious distribution of the species.

Keywords

larval growthSerpulidaetubewormlife historyrecruitmentsettlement behavioursettlement cuespawningcompetencegregarious distribution
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 93 , Issue 5 , August 2013 , pp. 1249 - 1256
Copyright
Copyright © Marine Biological Association of the United Kingdom 2012 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Allen, M.J. (1957) The breeding of polychaetous annelids near Parguera, Puerto Rico. Biological Bulletin. Marine Biological Laboratory, Woods Hole 113, 49–57.CrossRefGoogle Scholar
Baxter, G.T. and Morse, D.E. (1987) G protein and diacylglycerol regulate metamorphosis of planktonic molluscan larvae. Proceedings of the National Academy of Sciences of the United States of America 84, 1867–1870.CrossRefGoogle ScholarPubMed
Bryan, P.J., Qian, P.Y., Kreider, J.L. and Chia, F.S. (1997) Induction of larval settlement and metamorphosis by pharmacological and conspecific associated compounds in the serpulid polychaete Hydroides elegans. Marine Ecology Progress Series 146, 81–90.CrossRefGoogle Scholar
Castric-Fey, A. (1984) Contribution à l'étude de la sexualité chez Pomatoceros lamarckii et P. triqueter en Baie de Concarneau (Sud Finistère). Annales de l'Institut d'Océanographie, Paris 60, 163–187.Google Scholar
Chapman, N.D., Moore, C.G., Harries, D.B. and Lyndon, A.R. (2007) Recruitment patterns of Serpula vermicularis L. (Polychaeta, Serpulidae) in Loch Creran, Scotland. Estuarine, Coastal and Shelf Science 73, 598–606.CrossRefGoogle Scholar
Clare, A.S., Thomas, R.F. and Rittschof, D. (1995) Evidence for the involvement of cyclic AMP in the pheromonal modulation of barnacle settlement. Journal of Experimental Biology 198, 655–664.CrossRefGoogle ScholarPubMed
Cotter, E., O'Riordan, R.M. and Myers, A.A. (2003) A histological study of reproduction in the serpulids Pomatoceros triqueter and Pomatoceros larmarkii (Annelida: Polychaeta). Marine Biology 142, 905–914.CrossRefGoogle Scholar
Dixon, D.R. (1981) Reproductive biology of the serpulid Ficopomatus (Mercierella) enigmaticus in the Thames Estuary, S.E. England. Journal of the Marine Biological Association of the United Kingdom 61, 80–81.CrossRefGoogle Scholar
Dixon, D.R. and Wilson, J.T. (2000) Genetics and marine pollution. Hydrobiologia 420, 29–43.CrossRefGoogle Scholar
Dobretsov, S. and Qian, P.Y. (2003) Pharmacological induction of larval settlement and metamorphosis in the blue mussel Mytilus edulis L. Biofouling 19, 57–63.CrossRefGoogle ScholarPubMed
D'Souza, F.M.L. and Loneragan, N.R. (1999) Effects of monospecific and mixed-algae diets on survival, development and fatty acid composition of penaeid prawn (Penaeus spp.) larvae. Marine Biology 133, 621–633.CrossRefGoogle Scholar
Fragoso, B. and Icely, J.D. (2009) Upwelling events and recruitment patterns of the major fouling species on coastal aquaculture (Sagres, Portugal). Journal of Coastal Research Special Isssue 56, 419–423.Google Scholar
Glasby, C.J. and Read, G.B. (1998) A chronological review of polychaete taxonomy in New Zealand. Journal of the Royal Society of New Zealand 28, 347–374.CrossRefGoogle Scholar
Hadfield, M.G. (2011) Biofilms and marine invertebrate larvae: what bacteria produce that larvae use to choose settlement sites. Annual Review of Marine Science 3, 453–470.CrossRefGoogle ScholarPubMed
Hadfield, M.C., Unabia, C.C., Smith, C.M. and Michael, T.M. (1994) Settlement preferences of the ubiquitous fouler Hydroides elegans. In Thompson, M.F., Nagabhushanam, R., Sarolini, R. and Fingerman, M. (eds) Recent developments in biofouling control. Rotterdam, The Netherlands: A.A. Balkema, pp. 65–74.Google Scholar
Hamer, J.P., Walker, G. and Latchford, J.W. (2001) Settlement of Pomatoceros lamarkii (Serpulidae) larvae on biofilmed surfaces and the effect of aerial drying. Journal of Experimental Marine Biology and Ecology 260, 113–131.CrossRefGoogle ScholarPubMed
Hayward, B.W. and Morley, M.S. (2004) Intertidal life around the coast of the Waitakere Ranges, Auckland. Auckland Regional Council Technical Report 298, 79 pp.Google Scholar
Hayward, B.W. and Morley, M.S. (2008) Intertidal life of the Tamaki Estuary and its entrance, Auckland. Auckland Regional Council Technical Report, No. 373, 72 pp.Google Scholar
Holm, E.R., McClary, M. Jr and Rittschof, D. (2000) Variation in attachment of the barnacle Balanus amphitrite: sensation or something else? Marine Ecology Progress Series 202, 153–162.CrossRefGoogle Scholar
Hung, O.S., Thiyagarajan, V., Wu, R.S.S. and Qian, P.Y. (2005) Effect of ultraviolet radiation on biofilms and subsequent larval settlement of Hydroides elegans. Marine Ecology Progress Series 304, 155–166.CrossRefGoogle Scholar
Kupriyanova, E.K., Nishi, E., Ten Hove, H.A. and Rzhavsky, A.V. (2001) Life-history patterns in serpulimorph polychaetes: ecological and evolutionary perspectives. Oceanography and Marine Biology: an Annual Review 39, 1–101.Google Scholar
Kurmaly, K., Jones, D.A., Yule, A.B. and East, J. (1989) Comparative analysis of the growth and survival of Penaeus monodon (Fabricius) larvae, from protozoea 1 to postlarva 1, on live feeds, artificial diets and on combinations of both. Aquaculture 81, 27–45.CrossRefGoogle Scholar
Lau, S.C.K., Harder, T. and Qian, P.Y. (2003) Induction of larval settlement in the serpulid polychaete Hydroides elegans (Haswell): role of bacterial extracellular polymers. Biofouling 19, 197–204.CrossRefGoogle ScholarPubMed
Lewis, C. and Watson, G.J. (2012) Expanding the ecotoxicological toolbox: The inclusion of polychaete reproductive endpoints. Marine Environmental Research 75, 10–22.CrossRefGoogle ScholarPubMed
Marsden, J.R. (1991) Responses of planktonic larvae of the serpulid polychaete Spirobranchus polycerus var. augeneri to an alga, adult tubes and conspecific larvae. Marine Ecology Progress Series 71, 245–251.CrossRefGoogle Scholar
Mesías-Gansbiller, C., Bendimerad, M.E.A., Román, G., Pazos, A.J., Sánchez, J.L. and Pérez- Parallé, M.L. (2008) Settlement behavior of black scallop larvae (Chlamys varia, L.) in response to GABA, epinephrine and IBMX. Journal of Shellfish Research 27, 261–264.CrossRefGoogle Scholar
Miura, T. and Kajihara, T. (1981) The development of a serpulid worm, Hydroides ezoensis (Annelida, Polychaeta). Proceedings of the Japanese Society of Systematic Zoology 20, 7–12.Google Scholar
Morton, J. (2004) Seashore ecology of New Zealand and the Pacific. Auckland: Bateman.Google Scholar
Morton, J. and Miller, M. (1973) The New Zealand sea shore. Auckland: Collins.Google Scholar
Olive, P.J.W. and Clark, R.B. (1978) Physiology of reproduction. In Mill, P.J. (ed.) Physiology of annelids. New York: Academic Press, pp. 271–368.Google Scholar
Pawlik, J.R. (1990) Natural and artificial induction of metamorphosis of Phragmatopoma lapidosa californica (Polychaeta: Sabellariidae), with a critical look at the effects of bioactive compounds on marine invertebrate larvae. Bulletin of Marine Science 46, 512–536.Google Scholar
Pechenik, J.A. and Qian, P.Y. (1998) Onset and maintenance of metabolic competence in the marine polychaete Hydroides elegans Haswell in response to three chemical cues. Journal of Experimental Marine Biology and Ecology 226, 51–74.CrossRefGoogle Scholar
Peoples, R.C., Randhawa, H.S. and Poulin, R. (2011) Parasites of polychaetes and their impacts on host survival in Otago Harbour, New Zealand. Journal of the Marine Biological Association of the United Kingdom 92, 449–455.CrossRefGoogle Scholar
Sánchez-Lazo, C. and Martínez-Pita, I. (2012) Induction of settlement in larvae of the mussel Mytilus galloprovincialis using neuroactive compounds. Aquaculture 344, 210–215.CrossRefGoogle Scholar
Schiel, D.R. (2006) Guide to common intertidal species of the South Island, New Zealand. Christchurch: Marine Ecology Research Group, University of Canterbury.Google Scholar
Selim, S.A., Naby, F.A., Gab-Alla, A.A.F.A. and Ghobashy, A. (2005) Gametogenesis and spawning of Spirobranchus tetraceros (Polychaeta, Serpulidae) in Abu Kir Bay, Egypt. Mediterranean Marine Science 6, 89–98.CrossRefGoogle Scholar
Smith, R.S. (1984) Development and settling of Spirobranchus giganteus (Polychaeta; Serpulidae). In Hutchings, P.A. (ed.) Proceedings of the First International Polychaete Conference. Sydney: Linnean Society of New South Wales, pp. 461–483.Google Scholar
Sriyutha Murthy, P., Venugopalan, V.P., Nair, K.V.K. and Subramoniam, T. (1999) Chemical cues inducing settlement and metamorphosis in the fouling oyster Crassostrea madrasensis. Journal of the Indian Institute of Science 79, 513–526.Google Scholar
Ten Hove, H.A. and Kupriyanova, E.K. (2009) Taxonomy of Serpulidae (Annelida, Polychaeta): the state of affairs. Zootaxa 2036, 1–126.CrossRefGoogle Scholar
Toonen, R.J. and Pawlik, J.R. (1996) Settlement of the tube worm Hydroides dianthus (Polychaeta: Serpulidae): cues for gregarious settlement. Marine Biology 126, 725–733.CrossRefGoogle Scholar