Skip to main content Accessibility help
×
Home

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

  • Waka Sato-Okoshi (a1), Hirokazu Abe (a2), Goh Nishitani (a1) and Carol A. Simon (a3)

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.

Copyright

Corresponding author

Correspondence should be addressed to: W. Sato-Okoshi, Laboratory of Biological Oceanography, Graduate School of Agricultural Science, Tohoku University, Sendai 981-8555, Japan email: wsokoshi@tohoku.ac.jp

References

Hide All
Bailey-Brock, J.H. (2000) A new record of the polychaete Boccardia proboscidea (family Spionidae), imported to Hawaii with oysters. Pacific Science 54, 2730.
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.
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.
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.
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.
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.
Carlton, J.T. and Geller, J.B. (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261, 7882.
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.
Claparède, E. (1868) Les annélids chétopodes du Golfe de Naples. Geneva: Ramboz et Schuchardt, 500 pp.
Claparède, E. (1870) Les annélids chétopodes du Golfe de Naples. Mémoires de la Société de Physique et d'Histoire Naturelle de Genéve 20, 365542.
Cohen, A.N. and Carlton, J.T. (1998) Accelerating invasion rate in a highly invaded estuary. Science 279, 555558.
Day, J.H. (1967) A monograph on the Polychaeta of Southern Africa. Part 2. Sedentaria. London: Trustees of the British Museum (Natural History).
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.
Fauvel, P. (1927) Polychètes sedentaires. Faune de France 16, 1494.
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.
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.
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.
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.
Lleonart, M., Handlinger, J. and Powell, M. (2003) Spionid mud worm infestation of farmed abalone (Haliotis spp.). Aquaculture 221, 8596.
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.
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.
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.
Miura, O. (2007) Molecular genetic approaches to elucidate the ecological and evolutionary issues associated with biological invasions. Ecological Research 22, 876883.
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.
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]
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.
Okoshi, K. and Sato-Okoshi, W. (1996) Biomineralization in mollusc aquaculture – growth and disease. Bulletin de l'Institut Océanographique de Monaco 14, 151169.
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.
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.
Radashevsky, V.I. and Olivares, C. (2005) Polydora uncinata (Polychaeta: Spionidae) in Chile: an accidental transportation across the Pacific. Biological Invasions 7, 489496.
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.
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.
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.
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.
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.
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.
Sato-Okoshi, W. (1998) Three new species of polydorids (Polychaeta, Spionidae) from Japan. Species Diversity 3, 277288.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Walker, L.M. (2014) A revision of the Polydora-complex (Annelida: Spionidae) fauna of Australia . PhD thesis. University of Queensland, Brisbane.
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.
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.

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed