A morphological and molecular study of Polydora CF. Websteri (Annelida: Spionidae): accurate identification towards improved management of a globally distributed pest of cultured molluscs

Abstract

Polydora websteri Hartman, 1943, a member of the Polydora-complex, commonly known as polydorids (Annelida: Spionidae), is one of the most wide-spread polydorid pests of mollusc culture in the world. Specimens resembling P. websteri were first recorded in South Africa, in 2009, boring into shells of oysters in a culture facility in Port Elizabeth and since then, has been recorded on cultured oysters from Namibia, Kleinzee and Paternoster on the west coast of South Africa. A preliminary investigation showed that specimens collected in South Africa, Australia and Japan were genetically different from P. websteri specimens collected in Rhode Island in the United States of America (USA), near the type locality of P. websteri. The possible wide-spread distribution of this shell-boring polydorid species emphasises the importance of timeous and accurate identification, for improved management and even eradication. The specimens in South Africa, Australia and Japan have therefore been referred to as P. cf. websteri until its taxonomy could be clarified using morphological and molecular information, which was the main aim of this study. Additionally, for improved management of pest polydorids locally and internationally, this study aimed to contribute to the sequence library for polydorid species and develop a taxonomic key of shell-boring polydorid pest species in South Africa for mariculture practitioners. Sequencing of cytochrome c oxidase subunit I (COI), cytochrome b (Cyt b) and 18S rRNA markers conducted in this study, yielded thirty-three sequences of specimens from South Africa, seven from Australia and seven from wild molluscs collected in Rhode Island on the east coast of the USA. Forty-three additional COI, four Cyt b and 24 18S rRNA sequences from South Africa, Namibia, Australia, China, Japan, Hawaii, west and east coasts of the USA were obtained from GenBank. Bayesian and maximum likelihood analysis of COI, Cyt b and 18S rRNA markers indicated that P. cf. websteri from South Africa and sequences of specimens from all other locations form a monophyletic group (share a common ancestor); but do not group with specimens collected from wild molluscs in Rhode Island near the type locality in the USA. Instead, the specimens from Rhode Island clustered with Polydora onagawaensis Teramoto, Sato-Okoshi, Abe, Nishitani & Endo, 2013. The interspecific distances between specimens from Rhode Island and sequences of P. websteri from all other regions were one or two orders of magnitude (10 or 100 times) higher than the intraspecific distances of either P. websteri or P. onagawaensis. However, the interspecific distance between specimens from Rhode Island and P. onagawaensis was 0 %. These results were also confirmed by species delimitation analysis and haplotype networks. Additionally, South African specimens were similar to the P. websteri lectotype and matched morphological descriptions of those from Australia, China, Japan, New Zealand, the east, west and gulf coast of the USA, but not the specimens collected from Rhode Island which were morphologically similar to P. onagawaensis from Japan. It is therefore concluded that specimens from South Africa are P. websteri, a new non-indigenous record, and that the specimens collected from Rhode Island had been misidentified. The confusion between P. websteri and P. onagawaensis in the USA reinforces the difficulty in identifying pest polydorids using only morphology and highlights that such misidentifications may impede accurate identifications of non-indigenous polydorid pests, which is problematic for implementing effective management strategies. Additionally, haplotype sharing and lack of genetic differentiation among populations of P. websteri from geographically distant locations confirm anthropogenic transportation of the species into South Africa. This haplotype sharing has undoubtedly resulted from the repeated movement of molluscs making it difficult to identify the source of the population in South Africa. The results strongly suggest that P. websteri arrived in South Africa via the transport of infested oysters for mariculture and has been spread between farms through the intraregional movement of infested oyster stock. Confirming the identity of P. websteri in Australia, China, Japan, South Africa and the east, west and gulf coasts of the USA shows that it is the second most widespread polydorid pest of mariculture known. The distribution may be even wider if the identity of P. websteri from South America and Europe is confirmed; this may help to better understand the global route of invasion and subsequently assist with preventing, or at least minimising further spread. It is recommended that the mariculture industry in South Africa implement a monitoring plan to facilitate the rapid identification of shell-boring polydorid pests, by using a combination of the taxonomic key provided in this study and genetic methods to identify new non-indigenous pests timeously.