Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-23T23:51:23.809Z Has data issue: false hasContentIssue false

And then there was one: Polydora uncinata and Polydora hoplura (Annelida: Spionidae), the problematic polydorid pest species represent a single species

Published online by Cambridge University Press:  13 July 2016

Waka Sato-Okoshi*
Affiliation:
Laboratory of Biological Oceanography, Graduate School of Agricultural Science, Tohoku University, Sendai 981-8555, Japan
Hirokazu Abe
Affiliation:
Tohoku National Fisheries Research Institute, Fisheries Research Agency, Miyagi 985-0001, Japan
Goh Nishitani
Affiliation:
Laboratory of Biological Oceanography, Graduate School of Agricultural Science, Tohoku University, Sendai 981-8555, Japan
Carol A. Simon
Affiliation:
Department of Botany and Zoology, Stellenbosch University, Matieland Private Bag X1, Stellenbosch, South Africa
*
Correspondence should be addressed to: W. Sato-Okoshi, Laboratory of Biological Oceanography, Graduate School of Agricultural Science, Tohoku University, Sendai 981-8555, Japan email: [email protected]

Abstract

It is necessary to monitor shell-associated polydorid worms owing to the risk that they pose to commercially important molluscs. This requires accurate identification, but is often hampered by morphological similarities among species, insufficient type specimens, and abridged species descriptions. Thus morphological characteristics and molecular sequences of the most harmful polydorid species, Polydora uncinata from Japan and Australia and Polydora hoplura from South Africa were compared to determine whether they represent two morphologically similar, but genetically distinct species, or a single species. A wide range of morphological variation (with respect to size, length of caruncle and pigmentation patterns) was observed in each species and population, and their variations largely overlapped and revealed them to be at the intraspecific level of a single species. This was confirmed by gene sequences of nuclear 18S and 28S rRNA that were completely identical for P. uncinata and P. hoplura. The mitochondrial 16S rRNA and cyt b gene analyses also showed no genetic differences between these two species. The tree topology of the mitochondrial cyt b gene did not reflect geographic differences but instead suggests artificial transportation of the species. We recommend the synonymization of P. uncinata with P. hoplura.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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

Bailey-Brock, J.H. (2000) A new record of the polychaete Boccardia proboscidea (family Spionidae), imported to Hawaii with oysters. Pacific Science 54, 2730.Google Scholar
Bilbao, A., Núñez, J., Viera, M.D.P., Sosa, B., Fernández-Palacios, H. and Hernández-Cruz, C.M. (2011) Control of shell-boring polychaetes in Haliotis tuberculata Coccinea (Reeve 1846) aquaculture: species identification and effectiveness of mebendazole. Journal of Shellfish Research 30, 331336.CrossRefGoogle Scholar
Blake, J.A. (1996) Family Spionidae Grube, 1850. In Blake, J.A., Hilbig, B. and Scott, P.H. (eds.) Taxonomic atlas of the benthic fauna of the Santa Maria Basin and Western Santa Barbara Channel, Volume 6. The Annelida, Part 3, California: Santa Barbara Museum of Natural History, pp. 81224.Google Scholar
Blake, J.A. and Evans, J.D. (1973) Polydora and related genera (Polychaeta: Spionidae) as borers in mollusk shells and other calcareous substrates. Veliger 15, 235249.Google 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 of Victoria 39, 171280.Google Scholar
Carazzi, D. (1893) Revisione del genere Polydora Bosc, e cenni su due specie che vivono sulle ostriche. Mitteilungen aus der Zoologischen Station zu Neapel 11, 445.Google Scholar
Carlton, J.T. and Geller, J.B. (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261, 7882.CrossRefGoogle Scholar
Çinar, M.E. (2013) Alien polychaete species worldwide: current status and their impacts. Journal of the Marine Biological Association of the United Kingdom 93, 12571278.CrossRefGoogle Scholar
Claparède, E. (1868) Les annélids chétopodes du Golfe de Naples. Geneva: Ramboz et Schuchardt, 500 pp.Google Scholar
Claparède, E. (1870) Les annélids chétopodes du Golfe de Naples. Mémoires de la Société de Physique et d'Histoire Naturelle de Genéve 20, 365542.Google Scholar
Cohen, A.N. and Carlton, J.T. (1998) Accelerating invasion rate in a highly invaded estuary. Science 279, 555558.CrossRefGoogle Scholar
Day, J.H. (1967) A monograph on the Polychaeta of Southern Africa. Part 2. Sedentaria. London: Trustees of the British Museum (Natural History).Google Scholar
David, A.A., Matthee, C.A. and Simon, C.A. (2014) Poecilogony in Polydora hoplura (Polychaeta: Spionidae) from commercially important molluscs in South Africa. Marine Biology 161, 887898.Google Scholar
Fauvel, P. (1927) Polychètes sedentaires. Faune de France 16, 1494.Google Scholar
Gibson, G., Hart, C., Coulter, C. and Xu, H. (2012) Nurse eggs form through an active process of apoptosis in the spionid Polydora cornuta (Annelida). Integrative and Comparative Biology 52, 151160. doi: 10.1093/icb/ics054.Google Scholar
Haupt, T.M., Griffiths, C.L., Robinson, T.B. and Tonin, A.F.G. (2010) Oysters as vectors of marine aliens, with notes on four introduced species associated with oyster farming in South Africa. African Zoology 45, 5262.Google Scholar
Hutchings, P.A. and Turvey, S.P. (1984) The Spionidae of South Australia (Annelida: Polychaeta). Transactions of the Royal Society of South Australia 108, 120.Google Scholar
Lleonart, M. (2001) Development of an integrated management program for the control of spionid mudworms in cultured abalone. Report to the Fisheries Research & Development Corporation (FRDC). Abalone subprogram Project No. 98/301.Google Scholar
Lleonart, M., Handlinger, J. and Powell, M. (2003) Spionid mud worm infestation of farmed abalone (Haliotis spp.). Aquaculture 221, 8596.Google Scholar
Mack, R.N., Simberloff, D., Lonsdale, W.M., Evans, H., Clout, M. and Bazzaz, F.A. (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications 10, 689710.Google Scholar
Martin, D. and Britayev, T.A. (1998) Symbiotic polychaetes: review of known species. In Ansell, A.D. et al. (eds) Oceanography and marine biology: an annual review, Volume 36. London: University College London Press, pp. 217340.Google Scholar
Mead, A., Carlton, J.T., Griffiths, C.L. and Rius, M. (2011) Introduced and cryptogenic marine and estuarine species of South Africa. Journal of Natural History 45, 24632524.CrossRefGoogle Scholar
Miura, O. (2007) Molecular genetic approaches to elucidate the ecological and evolutionary issues associated with biological invasions. Ecological Research 22, 876883.Google Scholar
Moreno, R.A., Neill, P.E. and Rozbaczylo, N. (2006) Native and nonindigenous boring polychaetes in Chile: a threat to native and commercial mollusk species. Revista chilena de historia natural 79, 263278.Google Scholar
Mori, K., Sato, W., Nomura, T. and Imajima, M. (1985) Infestation of the Japanese Scallop Patinopecten yessoensis by the boring polychaetes, Polydora, on the Okhotsk Sea Coast of Hokkaido, especially in Abashiri Waters. Bulletin of the Japanese Society of Scientific Fisheries 51, 371380. [In Japanese with English abstract]CrossRefGoogle Scholar
Mustaquim, J. (1988) Electrophoretic variation of isozymes in Polydora ciliata complex (Polychaeta: Spionidae). Comparative Biochemistry and Physiology. Part B: Biochemistry and Molecular Biology 91, 197205.Google Scholar
Okoshi, K. and Sato-Okoshi, W. (1996) Biomineralization in mollusc aquaculture – growth and disease. Bulletin de l'Institut Océanographique de Monaco 14, 151169.Google Scholar
Oyarzun, F.X., Mahon, A.R., Swalla, B.J. and Halanych, K.M. (2011) Phylogeography and reproductive variation of the poecilogonous polychaete Boccardia proboscidea (Annelida: Spionidae) along the West Coast of North America. Evolution and Development 13, 489503.CrossRefGoogle ScholarPubMed
Palumbi, S., Martin, A., Romano, S., McMillan, W.O., Stice, L. and Grabowski, G. (1991) The simple fool's guide to PCR. Version 2.0. Honolulu: Department of Zoology and Kewalo Marine Laboratory, University of Hawaii, 47 pp.Google Scholar
Radashevsky, V.I. and Olivares, C. (2005) Polydora uncinata (Polychaeta: Spionidae) in Chile: an accidental transportation across the Pacific. Biological Invasions 7, 489496.CrossRefGoogle Scholar
Radashevsky, V.I. and Pankova, V.V. (2006) The morphology of two sibling sympatric Polydora species (Polychaeta: Spionidae) from the Sea of Japan. Journal of the Marine Biological Association of the United Kingdom 86, 245252.Google Scholar
Read, G.B. (1975) Systematics and biology of polydorid species (Polychaeta: Spionidae) from Wellington Harbour. Journal of the Royal Society of New Zealand 5, 395419.Google Scholar
Read, G.B. (2010) Comparison and history of Polydora websteri and P. haswelli (Polychaeta: Spionidae) as mud-blister worms in New Zealand shellfish. New Zealand Journal of Marine and Freshwater Research 44, 118.Google Scholar
Rice, S.A., Karl, S. and Rice, K.A. (2008) The Polydora cornuta complex (Annelida: Polychaeta) contains populations that are reproductively isolated and genetically distinct. Invertebrate Biology 127, 4564.Google Scholar
Rice, S.A. and Rice, K.A. (2009) Variable modes of larval development in the Polydora cornuta complex (Polychaeta: Spionidae) are directly related to stored sperm availability. Zoosymposia 2, 397414.Google Scholar
Sato-Okoshi, W. (1994) Life history of the polychaete, Polydora variegata, that bores into the shells of scallops in northern Japan. Memoires du Museum National d'Histoire Naturelle 162, 549558.Google Scholar
Sato-Okoshi, W. (1998) Three new species of polydorids (Polychaeta, Spionidae) from Japan. Species Diversity 3, 277288.Google Scholar
Sato-Okoshi, W. (1999) Polydorid species (Polychaeta, Spionidae) in Japan, with descriptions of morphology, ecology and burrow structure. 1. Boring species. Journal of the Marine Biological Association of the United Kingdom 79, 831848.Google Scholar
Sato-Okoshi, W. (2000) Polydorid species (Polychaeta, Spionidae) in Japan, with descriptions of morphology, ecology and burrow structure. 2. Non-boring species. Journal of the Marine Biological Association of the United Kingdom 80, 443456.Google Scholar
Sato-Okoshi, W. and Abe, H. (2012) Morphological and molecular sequence analysis of the harmful shell boring species of Polydora (Polychaeta: Spionidae) from Japan and Australia. Aquaculture 368–369, 4047.Google Scholar
Sato-Okoshi, W. and Abe, H. (2013) Morphology and molecular analysis of the 18S rRNA gene of oyster shell borers, Polydora species (Polychaeta: Spionidae), from Japan and Australia. Journal of the Marine Biological Association of the United Kingdom 93, 12791286.CrossRefGoogle Scholar
Sato-Okoshi, W., Abe, H., Okoshi, K., Teramoto, W., Shaw, J., Koh, B.-S., Kim, Y.-H., Hong, J.-S. and Li, J.-Y. (2015) Harmful shell borers, Polydora species (Polychaeta: Spionidae), from commercially important mollusc shells in East Asia and Australia. In Ceccaldi, H.-J. et al. (ed.) Marine productivity: perturbations and resilience of socio-ecosystems. Geneva: Springer International Publishing, pp. 3141.Google Scholar
Sato-Okoshi, W., Okoshi, K., Abe, H. and Li, J.-Y. (2013) Polydorid species (Polychaeta, Spionidae) associated with commercially important mollusk shells from eastern China. Aquaculture 406–407, 153159.Google Scholar
Sato-Okoshi, W., Okoshi, K., Koh, B.-S., Kim, Y.-H. and Hong, J.-S. (2012) Polydorid species (Polychaeta, Spionidae) associated with commercially important mollusk shells in Korean waters. Aquaculture 350–353, 8290.Google Scholar
Sato-Okoshi, W., Okoshi, K. and Shaw, J. (2008) Polydorid species (Polychaeta, Spionidae) in southwestern Australian waters with special reference to Polydora uncinata and Boccardia knoxi . Journal of the Marine Biological Association of the United Kingdom 88, 491501.Google Scholar
Sato-Okoshi, W., Sugawara, Y. and Nomura, T. (1990) Reproduction on the boring polychaete Polydora variegata inhabiting scallops in Abashiri Bay, North Japan. Marine Biology 104, 6166.Google Scholar
Sato-Okoshi, W. and Takatsuka, M. (2001) Polydora and related genera (Polychaeta, Spionidae) around Puerto Montt and Chiloe Island (Chile), with description of a new species of Dipolydora . Bulletin of Marine Science 68, 485503.Google Scholar
Scholin, C.A., Herzog, M., Sogin, M. and Anderson, D.M. (1994) Identification of group- and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae). 2. Sequence analysis of a fragment of the LSU rRNA gene. Journal of Phycology 30, 9991011.Google Scholar
Simon, C.A. (2011) Polydora and Dipolydora (Polychaeta: Spionidae) associated with molluscs on the south coast of South Africa, with descriptions of two new species. African Invertebrates 52, 3950.Google Scholar
Simon, C.A. (2015) Observations on the composition and larval developmental modes of polydorid pests of farmed oysters (Crassostrea gigas) and abalone (Haliotis midae) in South Africa. Invertebrate Reproduction and Development 59, 124130.Google Scholar
Simon, C.A. and Booth, A. (2007) Population structure and growth of polydorid polychaetes that infest the cultured abalone, Haliotis midae . African Journal of Marine Science 29, 499509.Google Scholar
Simon, C.A., Ludford, A. and Wynne, S. (2006) Spionid polychaetes infesting cultured abalone Haliotis midae in South Africa. African Journal of Marine Science 28, 167171.Google Scholar
Simon, C.A. and Sato-Okoshi, W. (2015) Polydorid polychaetes on farmed molluscs: distribution, spread and factors contributing to their success. Aquaculture Environment Interactions 7, 147166.Google Scholar
Simon, C.A., Thornhill, D.J., Oyarzun, F. and Halanych, K.M. (2009) Western North American origin of Boccardia proboscidea pests on the cultured abalone, Haliotis midae, in South Africa. Aquaculture 294, 1824.CrossRefGoogle Scholar
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 15961599.Google Scholar
Teramoto, W., Sato-Okoshi, W., Abe, H., Nishitani, G. and Endo, Y. (2013) Morphology, 18S rRNA gene sequence, and life history of a new Polydora species (Polychaeta, Spionidae) from northeastern Japan. Aquatic Biology 18, 3145.Google Scholar
Van Niekerk, S.E. (2014) A systematic review of the so-called cosmopolitan polydorid Polydora hoplura Claparède, 1869 (Polychaeta: Spionidae) on the South African coast . MSc thesis. Stellenbosch University, Stellenbosch.Google Scholar
Walker, L.M. (2011) A review of the current status of the Polydora-complex (Polychaeta: Spionidae) in Australia and a checklist of recorded species. Zootaxa 2751, 4062.Google Scholar
Walker, L.M. (2014) A revision of the Polydora-complex (Annelida: Spionidae) fauna of Australia . PhD thesis. University of Queensland, Brisbane.Google Scholar
Williams, L.G. (2015) Genetic structure of pest polydorids (Annelida: Spionidae) infesting Crassostrea gigas in southern Africa: are pests being moved with oysters? MSc thesis. Stellenbosch University, Stellenbosch.Google Scholar
Wilson, D.P. (1928) The larvae of Polydora ciliata Johnston and Polydora hoplura Claparède. Journal of the Marine Biological Association of the United Kingdom 15, 567603.Google Scholar