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Phylogeography of the invasive Mediterranean fan worm, Sabella spallanzanii (Gmelin, 1791), in Australia and New Zealand

Published online by Cambridge University Press:  23 March 2017

Shane T. Ahyong ,
Elena Kupriyanova ,
Ingo Burghardt ,
Yanan Sun ,
Pat A. Hutchings ,
Maria Capa  and
Serena L. Cox
Shane T. Ahyong*
Affiliation:
Australian Museum Research Institute, Australian Museum, 1 William Street, Sydney, NSW 2010, Australia School of Biological, Earth and Environmental Sciences, University of New South Wales, Kensington, NSW 2052, Australia
Elena Kupriyanova
Affiliation:
Australian Museum Research Institute, Australian Museum, 1 William Street, Sydney, NSW 2010, Australia Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia
Ingo Burghardt
Affiliation:
Australian Museum Research Institute, Australian Museum, 1 William Street, Sydney, NSW 2010, Australia
Yanan Sun
Affiliation:
Australian Museum Research Institute, Australian Museum, 1 William Street, Sydney, NSW 2010, Australia Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia
Pat A. Hutchings
Affiliation:
Australian Museum Research Institute, Australian Museum, 1 William Street, Sydney, NSW 2010, Australia
Maria Capa
Affiliation:
NTNU University Museum, Norwegian University of Science and Technology, NO-7491 Trondheim, Norway
Serena L. Cox
Affiliation:
National Institute of Water & Atmospheric Research, Private Bag 14901, Kilbirnie, Wellington, New Zealand
*
Correspondence should be addressed to: S. Ahyong, Australian Museum Research Institute, Australian Museum, 1 William Street, Sydney, NSW 2010, Australia email: shane.ahyong@austmus.gov.au
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Abstract

The Mediterranean fan worm, Sabella spallanzanii (Gmelin, 1791), is a highly invasive pest species introduced to Australia and New Zealand, with the ability to alter marine ecosystems by outcompeting native species for food and space. Sabella spallanzanii has been established in southern Australia for decades, but was discovered in Botany Bay (NSW, eastern Australia) in 2013. In New Zealand, S. spallanzanii was first detected in March 2008. Using cytochrome c oxidase subunit 1 (COI) sequences, we investigate the phylogeography of the Australian and New Zealand populations of S. spallanzanii, including the possible origins of the recent incursions in both countries. Australian and New Zealand S. spallanzanii show minimal genetic diversity (0.2% divergence) and were dominated by two main haplotypes suggesting a commonality. Our molecular data are insufficient by themselves to identify fine-scale invasion pathways in antipodean S. spallanzanii, but the similar, minimal haplotype diversity in combination with well-constrained field survey data suggests that the New Zealand incursion originated from southern Australia, rather than as a new incursion from the Mediterranean Sea. This highlights the importance of ongoing marine biosecurity surveillance and monitoring as well as improvements to biosecurity protocols for international and domestic vessels. The origin of the eastern Australian (Botany Bay) incursion is plausibly derived from either southern Australia or as a ‘return’ from New Zealand, and requires further, more detailed investigation.

Keywords

PolychaetaAnnelidainvasive speciesAustraliaNew ZealandCOI
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 97 , Special Issue 5: Proceedings of the 12th International Polychaete Conference Amgueddfa Cymru - National Museum Wales Cardiff, Wales, UK, 1-5 August 2016 , August 2017 , pp. 985 - 991
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

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References

REFERENCES

Andrew, J. and Ward, R.D. (1997) Allozyme variation in the marine fanworm Sabella spallanzanii: comparison of native European and introduced Australian populations. Marine Ecology Progress Series 152, 131–143.CrossRefGoogle Scholar
Australian Museum Business Services (2002) Port survey for introduced marine species – Sydney Harbour. Final report for Sydney Ports Corporation. Sydney: Australian Museum Business Services, 62 pp.Google Scholar
Capa, M., Bybee, D. and Bybee, S. (2010) Integrative taxonomy reveals cryptic species within Sabellastarte Krøyer, 1856 (Sabellidae: Annelida) and establishes the systematics of the genus. Organisms Diversity and Evolution 10, 351–371.CrossRefGoogle Scholar
Capa, M., Pons, J. and Hutchings, P. (2013) Cryptic diversity, intraspecific phenetic plasticity and recent geographic translocations in Branchiomma (Sabellidae, Annelida). Zoologica Scripta 42, 637–655.Google Scholar
Clapin, G. and Evans, D.R. (1995) The status of the introduced marine fanworm Sabella spallanzanii in Western Australia: a preliminary investigation. Centre for Research on Introduced Marine Pests, CSIRO Division of Fisheries, Hobart, Australia, Technical Report 2, pp. 1–34.Google Scholar
Clement, M., Posada, D. and Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 4, 331–346.Google Scholar
Cohen, B.F., Currie, D.R. and McArthur, M.A. (2000) Epibenthic community structure in Port Phillip Bay, Victoria, Australia. Marine and Freshwater Research 51, 689–702.CrossRefGoogle Scholar
Currie, D.R., McArthur, M.A. and Cohen, B.F. (2000) Reproduction and distribution of the invasive European fanworm Sabella spallanzanii (Polychaeta: Sabellidae) in Port Phillip Bay, Victoria, Australia. Marine Biology 136, 645–656.CrossRefGoogle Scholar
Dias, P.J., Rocha, R., Godwin, S., Tovar-Hernández, M.A., Delahoz, M.V., McKirdy, S., de Lestang, P., McDonald, J.I. and Snow, M. (2016) Investigating the cryptogenic status of the sea squirt Didemnum perlucidum (Tunicata, Ascidiacea) in Australia based on a molecular study of its global distribution. Aquatic Invasions 11, 239–245.Google Scholar
Giangrande, A., Licciano, M., Pagliara, P. and Gambi, M.C. (2000) Gametogenesis and larval development in Sabella spallanzanii (Polychaeta: Sabellidae) from the Mediterranean Sea. Marine Biology 136, 847–861.CrossRefGoogle Scholar
Giangrande, A., Pierri, C., Fanelli, G., Schirosi, R., Licciano, M. and Stabili, L. (2014) Rearing experiences of the polychaete Sabella spallanzanii in the Gulf of Taranto (Mediterranean Sea, Italy). Aquaculture International 22, 1677–1688.Google Scholar
Glasby, T. and Lobb, K. (2008) Assessing likelihoods of marine pest introductions in Sydney estuaries: a transport vector approach. New South Wales Department of Primary Industries Report, 86 pp.Google Scholar
Gmelin, J.F. (1791) Vermes. In Gmelin, J.F. (ed.) Caroli a Linnaei Systema Naturae per Regna Tria Naturae, Editio Decima Tertia, Aucta Reformata 1(6) (Vermes). Lipsiae [Leipzig]: G.E. Beer, pp. 3021–3910.Google Scholar
Hall, T. (1999) BioEdit. A user friendly biological sequence alignment editor and analysis program for windows 95/99/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hayes, K., Silwa, C., Migus, S., McEnnulty, F. and Dunstan, P. (2005) National priority pests: Part II. Ranking of Australian marine pests. An Independent Report Undertaken for the Department of Environment and Heritage by CSIRO Marine Research, 106 pp.Google Scholar
Hewitt, C.L., Gibbs, P., Moore, K.M., Murfet, N.B. and Ross, J. (1998) Introduced species survey of Newcastle, New South Wales. a report for the Newcastle Port Authority. Hobart, Tasmania: CRIMP Port Survey Report Series, CSIRO Marine Research, 53 pp.Google Scholar
Holloway, M.G. and Keough, M.J. (2002) Effects of an introduced polychaete, Sabella spallanzanii, on the development of epifaunal assemblages. Marine Ecology Progress Series 236, 137–154.Google Scholar
Huisman, J.M., Jones, D.S., Wells, F.E. and Burton, T. (2008) Introduced marine biota in Western Australian waters. Records of the Western Australian Museum 25, 1–44.Google Scholar
Knight-Jones, P. and Perkins, T.H. (1998) A revision of Sabella, Bispira and Stylomma (Polychaeta: Sabellidae). Zoological Journal of the Linnean Society 123, 385–467.Google Scholar
Lejeusne, C., Saunier, A., Petit, N., Béguer, M., Otani, M., Carlton, J.T., Rico, C. and Green, A.J. (2014) High genetic diversity and absence of founder effects in a worldwide aquatic invader. Scientific Reports 5, 1–9.Google Scholar
Licciano, M., Murray, J.M., Watson, G.J. and Giangrande, A. (2012) Morphological comparison of the regeneration process in Sabella spallanzanii and Branchiomma luctuosum (Annelida, Sabellida). Invertebrate Biology 131, 40–51.Google Scholar
Lobo, J., Costa, P.M., Teixeira, M.A.L., Ferreira, M.S.G., Costa, M.H. and Costa, F.O. (2013) Enhanced primers for amplification of DNA barcodes from a broad range of marine Metazoans. BMC Ecology 13, 34.Google Scholar
Murray, A. and Keable, S.J. (2013) First report of Sabella spallanzanii (Gemlin, 1791) (Annelida: Polychaeta) from Botany Bay, New South Wales, a northern range extension for the invasive species within Australia. Zootaxa 3670, 394–395.CrossRefGoogle Scholar
Nguyen, L.-T., Schmidt, H.A., von Haeseler, A. and Minh, B.Q. (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution 32, 268–274.CrossRefGoogle ScholarPubMed
NSW DPI (Department of Primary Industries) (2016) European fan worm. Available at http://www.dpi.nsw.gov.au/fishing/pests-diseases/marine-pests/found-in-nsw/european-fan-worm (accessed 21 September 2016).Google Scholar
Nygren, A. (2014) Cryptic polychaete diversity: a review. Zoologica Scripta 43, 172–183.Google Scholar
O'Brien, A.L., Ross, D.J. and Keough, M.J. (2006) Effects of Sabella spallanzanii physical structure on soft sediment macrofaunal assemblages. Marine and Freshwater Research 57, 363–471.CrossRefGoogle Scholar
Pallas, P.S. (1766) Miscellanea zoologica. Quibus novae imprimis atque obscurae animalium species describuntur et observationibus iconibusque illustrantur. Petrum van Cleef. Hagí Comitum., xii + 224 pp., 14 pls.CrossRefGoogle Scholar
Parry, G.D., Lockett, M., Crookes, D.P., Coleman, N. and Sinclair, M. (1996) Mapping and distribution of Sabella spallanzanii in Port Phillip Bay. Final Report to Fisheries Research and Development Corporation, Project 94/164. Queenscliff, Victoria: Marine and Freshwater Resources Institute.Google Scholar
Patti, F.P. and Gambi, M.C. (2001) Phylogeography of the invasive polychaete Sabella spallanzanii (Sabellidae) based on the nucleotide sequence of internal transcribed spacer 2 (ITS2) of nuclear rDNA. Marine Ecology Progress Series 215, 169–177.Google Scholar
Pollard, D.A. and Pethebridge, R.L. (2002) Report on port of Botany Bay introduced marine pest species survey. New South Wales Fisheries Final Report Series 40, 1–69.Google Scholar
Rambaut, A. (2014) FigTree: Tree Figure Drawing Tool Version 1.4.2. Edinburgh: Institute of Evolutionary Biology, University of Edinburgh. Available at http://tree.bio.ed.ac.uk/.Google Scholar
Read, G.B., Inglis, G., Stratford, P. and Ahyong, S.T. (2011) Arrival of the alien fanworm Sabella spallanzanii (Gemlin, 1791) (Polychaeta: Sabellidae) in two New Zealand harbours. Aquatic Invasions 6, 273–279.CrossRefGoogle Scholar
Roman, J. and Palumbi, S.R. (2004) A global invader at home: population structure of the green crab, Carcinus maenas, in Europe. Molecular Ecology 13, 2891–2898.Google Scholar
Ross, D.J., Keough, M.J., Longmore, A.R. and Knott, N.A. (2007) Impacts of two introduced suspension feeders in Port Phillip Bay, Australia. Marine Ecology Progress Series 340, 41–53.CrossRefGoogle Scholar
Savigny, J.-C. (1822) Système des annélides, principalement de celles des côtes de l’Égypte et de la Syrie, offrant les caractères tant distinctifs que naturels des Ordres, Familles et Genres, avec la Description des Espèces. Description de l’Égypte ou Recueil des Observations et des Recherches qui ont été faites en Égypte pendant l'Expédition de l'Armée Française, publié par les Ordres de sa Majesté l'Empereur Napoléon le Grand. Histoire Naturelle, Paris 1, 1–128.Google Scholar
Styan, C.A., McCluskey, C.F., Sun, Y. and Kupriyanova, E.K. (2017) Cryptic sympatric species across the Australian range of the global estuarine invader Ficopomatus enigmaticus (Fauvel, 1923) (Serpulidae, Annelida). Aquatic Invasions 12, 53–65.CrossRefGoogle Scholar
Summerson, R., Darbyshire, R. and Lawrence, E. (2007) Invasive marine species range mapping. Canberra: Australian Government Bureau of Rural Sciences, 77 pp.Google Scholar
Sun, Y., Wong, E., Tovar-Hernández, M.A., Williamson, J.E. and Kupriyanova, E.K. (2016) Is Hydroides brachyacantha (Serpulidae: Annelida) a widespread species? Invertebrate Systematics 30, 41–59.CrossRefGoogle Scholar
Sydney, Ports (2012) Sydney Ports Corporation Trade & Logistics Report 2011/2012. Sydney: Sydney Ports Corporation, 54 pp.Google Scholar
Templeton, A.R., Crandall, K.A. and Sing, C.F. (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. Cladogram estimation. Genetics 132, 619–663.CrossRefGoogle ScholarPubMed
Turón, X., Tarjuelo, I., Durán, S. and Pascual, M. (2003) Characterising invasion processes with genetic data: an Atlantic clade of Clavelina lepadiformis (Ascidiacea) introduced into Mediterranean harbours. Hydrobiologia 503, 29–35.Google Scholar