Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-22T18:04:36.411Z Has data issue: false hasContentIssue false
  • English
  • Français

A new record of a cryptogenic Dipolydora species (Annelida: Spionidae) in South Africa

Published online by Cambridge University Press:  25 March 2021

Andrew A. David Open the ORCID record for Andrew A. David [Opens in a new window] ,
Jason D. Williams  and
Carol A. Simon
Andrew A. David*
Affiliation:
Department of Biology, Clarkson University, Potsdam, New York13699, USA
Jason D. Williams
Affiliation:
Department of Biology, Hofstra University, Hempstead, New York11549, USA
Carol A. Simon
Affiliation:
Department of Botany and Zoology, Stellenbosch University, Stellenbosch7601, South Africa
*
Author for correspondence: Andrew A. David, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

In this study we report a new record of a cryptogenic polychaete from southern Africa. The species was found inhabiting sand tubes in intertidal sand flats in the Knysna Estuary on the southern coast of South Africa. Morphological comparisons using light and scanning electron microscopy showed extensive taxonomic similarities with Dipolydora socialis described from other localities and from museum vouchers. In addition, 18S rRNA and COI barcodes were generated for the species. Genetic analysis of the assembled polydorid dataset corroborated the morphological data in delineating the species as a taxonomic unit with >99% genetic similarity to available sequences of D. socialis in the GenBank database. Dipolydora socialis has been reported as having a widespread distribution, and since it can reside within tubes associated with fouling communities or as a shell borer, several vectors may have been responsible for its global spread and introduction to southern Africa. Finally, considering the many cryptic complexes that are currently being uncovered within polychaetes, including spionids, future taxonomic studies should incorporate additional genetic data from other regions of the world to determine whether D. socialis may also be part of a larger species complex.

Keywords

Barcodinginvasivemarinepolychaetepolydorid
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 101 , Issue 2 , March 2021 , pp. 271 - 278
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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

Abd Elnaby, FA (2019) New recorded alien polydorid species (Polychaeta: Spionidae) from the Egyptian waters. Egyptian Journal of Aquatic Biology and Fisheries 23, 409–420.CrossRefGoogle Scholar
Abe, H and Sato-Okoshi, W (2021) Molecular identification and larval morphology of spionid polychaetes (Annelida: Spionidae) from northeastern Japan. ZooKeys 1015, 1–86.CrossRefGoogle ScholarPubMed
Berkeley, E (1927) Polychaetous annelids from the Nanaimo district, Part 3: Leodicidae to Spionidae. Contributions to Canadian Biology and Fisheries 3, 405–422.CrossRefGoogle Scholar
Berkeley, E and Berkeley, C (1936) Notes on Polychaeta from the coast of western Canada, I: Spionidae. Journal of Natural History 18, 468–477.CrossRefGoogle Scholar
Berkeley, E and Berkeley, C (1952) Polychaeta Sedentaria. Canadian Pacific Fauna. Annelida 9b(2), 1–139.Google Scholar
Blake, JA (1971) Revision of the genus Polydora from the east coast of North America (Polychaeta: Spionidae). Smithsonian Contributions to Zoology 75, 1–32.CrossRefGoogle Scholar
Blake, JA (1975) Phylum Annelida: Class Polychaeta. In Light, SF, Smith, RI and Carlton, JT (eds), Light's Manual: Intertidal Invertebrates of the Central California Coast. Berkeley, CA: University of California Press, pp. 309–410.Google Scholar
Blake, JA (1979) Revision of some polydorids (Polychaeta: Spionidae) described and recorded from British Columbia by Edith and Cyril Berkeley. Proceedings of the Biological Society of Washington 92, 606–617.Google Scholar
Blake, JA (1981) Polydora and Boccardia species (Polychaeta: Spionidae) from western Mexico, chiefly from calcareous habitats. Proceedings of the Biological Society of Washington 93, 947–962.Google Scholar
Blake, JA (1983) Polychaetes of the family Spionidae from South America, Antarctica, and adjacent seas and islands. Biology of the Antarctic Seas 14. Antarctic Research Series 39, 205–288.CrossRefGoogle Scholar
Blake, JA (1996) Family Spionidae Grube, 1850. Including a revision of the genera and species from California and a revision of the genus Polydora Bosc, 1802. In Blake, JA, Hilbig, B and Scott, PH (eds), Taxonomic Atlas of the Benthic Fauna of the Santa Maria Basin and The Western Santa Barbara Channel. Vol. 6. The Annelida. Part 3. Polychaeta: Orbiniidae to Cossuridae. Santa Barbara, CA: Santa Barbara Museum of Natural History, pp. 81–224.Google Scholar
Blake, JA (2006) Spionida. In Rouse, G and Pleijel, F (eds), Reproductive Biology and Phylogeny of Annelida. Enfield, NH: Science Publishers, pp. 565–638.Google Scholar
Blake, JA and Arnofsky, PL (1999) Reproduction and larval development of the spioniform Polychaeta with application to systematics and phylogeny. Hydrobiologia 402, 57–106.CrossRefGoogle Scholar
Blake, JA and Kudenov, JD (1978) The Spionidae (Polychaeta) from southeastern Australia and adjacent areas with a revision of the genera. Memoirs of the National Museum of Victoria 32, 129–170.Google Scholar
Bowles, CM (2013) Stability, Resilience, and Persistence of Two Alternate Soft-Sediment Communities in Bodega Harbour, California. PhD thesis, University of California Davis, USA.Google Scholar
Boyd, M, Mulligan, TJ and Shaughnessy, FJ (2002) Non-indigenous Marine Species of Humboldt Bay, California. A report to the California Department of Fish and Game, 118 pp.Google Scholar
Carlton, JT (1996) Biological invasions and cryptogenic species. Ecology 77, 1653–1655.CrossRefGoogle Scholar
Carlton, JT and Gellar, JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science (New York, N.Y.) 261, 78–82.CrossRefGoogle Scholar
Carr, CM, Hardy, SM, Brown, TM, Macdonald, TA and Herbert, PD (2011) A tri-oceanic perspective: DNA barcoding reveals geographic structure and cryptic diversity in Canadian polychaetes. PLoS ONE 6, e22232.CrossRefGoogle ScholarPubMed
Carrasco, FD (1974) Spionidae (Polychaeta) proventientes de la Bahia de Concepcion y lugares adyacentes. Boletin de la Sociedad de Biologia de Concepcion 48, 185–201.Google Scholar
Cinar, ME (2013) Alien polychaete species worldwide: current status and their impacts. Journal of the Marine Biological Association of the United Kingdom 93, 1257–1278.CrossRefGoogle Scholar
Claassens, L, Barnes, RSK, Wasserman, J, Lamberth, SJ, Miranda, NAF, van Niekerk, L and Adams, JB (2020) Knysna Estuary health: ecological status, threats and options for the future. African Journal of Aquatic Science 45, 65–82.CrossRefGoogle Scholar
Clements, JC, Bourque, D, McLaughlin, J, Stephenson, M and Comeau, LA (2018) Wanted dead or alive: Polydora websteri recruit to both live oysters and empty shells of the eastern oyster, Crassostrea virginica. Journal of Fish Diseases 41, 855–858.CrossRefGoogle ScholarPubMed
Costello, MJ, Coll, M, Danovaro, R, Halpin, P, Ojaveer, H and Miloslavich, P (2010) A census of marine biodiversity knowledge resources, and future challenges. PLoS ONE 5, e12110.CrossRefGoogle ScholarPubMed
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
David, AA (2015) An Integrated Larval Development and Population Genetics Approach for Predicting the Establishment and Dispersal Potential of a Recently Introduced Polychaete (Annelida: Spionidae) in Southern Africa. PhD thesis, Stellenbosch University, South Africa.Google Scholar
David, AA and Krick, M (2019) DNA barcoding of polychaetes collected during the 2018 Rapid Assessment Survey of floating dock communities from New England. Marine Biology Research 15, 317–324.CrossRefGoogle Scholar
David, AA and Williams, JD (2012 a) Morphology and natural history of the cryptogenic sponge associate Polydora colonia Moore, 1907 (Polychaeta: Spionidae). Journal of Natural History 46, 1509–1528.CrossRefGoogle Scholar
David, AA and Williams, JD (2012 b) Asexual reproduction and anterior regeneration under high and low temperatures in the sponge associate Polydora colonia (Polychaeta: Spionidae). Invertebrate Reproduction and Development 56, 315–324.CrossRefGoogle Scholar
David, AA, Matthee, CA and Simon, CA (2014) Poecilogony in Polydora hoplura (Polychaeta: Spionidae) from commercially important molluscs in South Africa. Marine Biology 161, 887–898.CrossRefGoogle Scholar
Day, JH (1967) A monograph on the Polychaeta of southern Africa. British Museum of Natural History Publications 656, 459–878.Google Scholar
Foster, NM (1971) Spionidae (Polychaeta) of the Gulf of Mexico and the Caribbean Sea. Studies of the Fauna of Curacao and Other Caribbean Islands 36, 1–183.Google Scholar
Griffiths, CL, Mead, A and Robinson, TB (2009) A brief history of marine bio-invasions in South Africa. African Zoology 44, 241–247.CrossRefGoogle Scholar
Guy-Haim, T, Lyons, DA, Kotta, J, Ojaveer, H, Queirós, AM, Chatzinikolaou, E, Arvanitidis, C, Como, S, Magni, P, Blight, AJ and Orav-Kotta, H (2018) Diverse effects of invasive ecosystem engineers on marine biodiversity and ecosystem functions: a global review and meta-analysis. Global Change Biology 24, 906–924.CrossRefGoogle ScholarPubMed
Hall, TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hartman, O (1941) Some contributions to the biology and life history of Spionidae from California. Allan Hancock Pacific Expeditions 7, 289–324.Google Scholar
Hartman, O (1961) Polychaetous annelids from California. Allan Hancock Pacific Expeditions 25, 1–226.Google Scholar
Hartman, O (1969) Atlas of the Sedentariate Polychaetous Annelids from California. Los Angeles, CA: Allan Hancock Foundation, 812 pp.Google Scholar
Hartman-Schröder, G (1962) Zur Kenntnis des Eulitorals der chilenischen Pazifikkuste und der argentinischen Kuste Sudpatagoniens unter besonderer Berucksichtigung der Polychaeten and Ostracoden. Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 60, 57–270.Google Scholar
Hartman-Schröder, G (1965) Die Polychaeten des Sublitorals. In Hartmann-Schröder, G and Hartmann, G (eds), Zur Kenntnis des Sublitorals der chilenischen Kuste under besonderer Berucksichtigung der Polychaeten und Ostracoden. Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut. Germany, 60, 59–305.Google Scholar
Haupt, TM, Griffiths, CL, Robinson, TB and Tonin, AFG (2010) Oysters as vectors of marine aliens, with notes on four introduced species associated with oyster farming in South Africa. African Zoology 45, 52–62.CrossRefGoogle Scholar
Hayes, K, Sliwa, C, Migus, S, McEnnulty, F and Dunstan, P (2005) National priority pests. Part II. Ranking of Australian marine pests. Canberra: Australian Government Department of the Environment and Heritage. 94 pp.Google Scholar
Hutchings, P and Kupriyanova, E (2018) Cosmopolitan polychaetes – fact or fiction? Personal and historical perspectives. Invertebrate Systematics 32, 1–9.CrossRefGoogle Scholar
Jaubet, ML, de los Angeles Sanchez, M, Rivero, MS, Garaffo, GV, Vallarino, EA and Elias, R (2011) Intertidal biogenic reefs built by the polychaete Boccardia proboscidea in sewage-impacted areas of Argentina, SW Atlantic. Marine Ecology 32, 188–197.CrossRefGoogle Scholar
Johnson, PG (1984) Family Spionidae Grube, 1850. In Uebelacker, JM and Johnson, PG (eds), Taxonomic Guide to the Polychaetes of Northern Gulf of Mexico. Mobile, AL: Barry A. Vittor and Associates, pp. 6.1–6.99.Google Scholar
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGAX: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.CrossRefGoogle Scholar
Light, WJ (1977) Spionidae (Annelida: Polychaeta) from San Francisco Bay, California: a revised list of nomenclatural changes, new records, and comments on related species from the northeastern Pacific. Proceedings of the Biological Society of Washington 90, 66–88.Google Scholar
Light, WJ (1978) Invertebrates of the San Francisco Bay Estuary System. Family Spionidae (Annelida, Polychaeta). Pacific Grove, CA: The Boxwood Press.Google Scholar
Lissner, A, Phillips, C, Cadien, D, Smith, R, Bernstein, B, Cimberg, R, Kauwling, T andAnikouchine, W (1986) Assessment of long-term changes in biological communities in the Santa Maria Basin and western Santa Barbara Channel. Phase I. Final report submitted for the Minerals Management Service: U.S. Department of the Interior, Pacific OCS Office. Contract No. 14-12-0001-30032. NMS OCS Study, MMS 86-0012.Google Scholar
Malan, A, Williams, JD, Abe, H, Sato-Okoshi, W, Matthee, CA and Simon, CA (2020) Clarifying the cryptogenic species Polydora neocaeca Williams & Radashevsky, 1999 (Annelida: Spionidae): a shell-boring invasive pest of molluscs from locations worldwide. Marine Biodiversity 50, 1–19.CrossRefGoogle Scholar
Manchenko, GP and Radashevsky, VI (2002) Genetic differences between two sibling sympatric Dipolydora species (Polychaeta: Spionidae) from the Sea of Japan, and a new species description. Journal of the Marine Biological Association of the United Kingdom 82, 193–199.CrossRefGoogle Scholar
Miza, SA, Robinson, TB, Peters, K, Majiedt, PA, Jackson, L, Hampton, SL and Sink, KJ (2019) Alien and invasive species. In Sink, KJ, van der Bank, MG, Majiedt, PA, Harris, LR, Atkinson, LJ, Kirkman, SP and Karenyi, N (eds), South African National Biodiversity Assessment 2018 Technical Report Volume 4: Marine Realm. Pretoria: South African National Biodiversity Institute. Available at http://hdl.handle.net/20.500.12143/6372.Google Scholar
Nel, R, Coetzee, PS and Van Niekerk, G (1996) The evaluation of two treatments to reduce mud worm (Polydora hoplura Claparede) infestation in commercially reared oysters (Crassostrea gigas Thunberg). Aquaculture 141, 31–39.CrossRefGoogle Scholar
Nygren, A (2014) Cryptic polychaete diversity: a review. Zoologica Scripta 43, 172–183.CrossRefGoogle Scholar
Nygren, A, Parapar, J, Pons, J, Meißner, K, Bakken, T, Kongsrud, JA, Oug, E, Gaeva, D, Sikorski, A, Johansen, RA and Hutchings, PA (2018) A mega-cryptic species complex hidden among one of the most common annelids in the North East Atlantic. PLoS ONE 13, e0198356.CrossRefGoogle ScholarPubMed
Orensanz, JML, Schwindt, E, Pastorino, G, Bortolus, A, Casas, G, Darrigran, G, Elias, R, Gappa, JJL, Obenat, S, Pascual, M, Penchaszadeh, P, Piriz, ML, Scarabino, F, Spivak, ED and Vallarino, EA (2002) No longer the pristine confines of the world ocean: a survey of exotic marine species in the Southwestern Atlantic. Biological Invasions 4, 115–143.CrossRefGoogle Scholar
Papacostas, KJ, Rielly-Carroll, EW, Georgian, SE, Long, DJ, Princiotta, SD, Quattrini, AM, Reuter, KE and Freestone, AL (2017) Biological mechanisms of marine invasions. Marine Ecology Progress Series 565, 251–268.CrossRefGoogle Scholar
Pederson, J, Carlton, JT, Bastidas, C, David, A, Grady, S, Green-Gavrielidis, L, Hobbs, N-V, Kennedy, C, Knack, J, McCuller, M, O'Brien, B, Osborne, K, Pankey, S and Trott, T (in press) 2019 Rapid Assessment Survey of marine bioinvasions of southern New England and New York, USA, with an overview of new records and range expansions. BioInvasions Records. https://www.reabic.net/journals/bir/2021/Accepted/BIR_2021_Pederson_etal_correctedproof.pdfGoogle Scholar
Pettibone, MH (1967) Type-specimens of polychaetes described by Edith and Cyril Berkeley (1923–1964). Proceedings of the United States National Museum 119, 1–23.CrossRefGoogle Scholar
Radashevsky, VI (1993) Revision of the genus Polydora and related genera from the North West Pacific (Polychaeta: Spionidae). Publications of the Seto Marine Biological Laboratory 36, 1–60.CrossRefGoogle Scholar
Rambaut, A (2007) FigTree: tree figure drawing tool version 1.4.3. Available at http://tree.bio.ed.ac.uk/software/figtree/.Google Scholar
Rice, SA, Karl, S and Rice, KA (2008) The Polydora cornuta complex (Annelida: Polychaeta) contains populations that are reproductively isolated and genetically distinct. Invertebrate Biology 127, 45–64.CrossRefGoogle Scholar
Sato-Okoshi, W and Okoshi, K (1997) Survey of the genera Polydora, Boccardiella and Boccardia (Polychaeta, Spionidae). Bulletin of Marine Science 60, 482–493.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, 485–503.Google Scholar
Sato-Okoshi, W, Abe, H, Nishitani, G and Simon, CA (2017) And then there was one: Polydora uncinata and Polydora hoplura (Annelida: Spionidae), the problematic polydorid pest species represent a single species. Journal of the Marine Biological Association of the United Kingdom 97, 1675–1684.CrossRefGoogle Scholar
Schmarda, LK (1861) Neue wirbellose thiere beobachtet und gesammelt auf einer Reise um die Erde 1853 bis 1857. Vol. 1. Turbellarian, Rotatorien und Anneliden. Leipzig: Wilhelmann.Google Scholar
Schwindt, E, Carlton, JT, Orensanz, JM, Scarabino, F and Bortolus, A (2020) Past and future of the marine bioinvasions along the Southwestern Atlantic. Aquatic Invasions 15, 11–29.CrossRefGoogle Scholar
Simon, CA (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, 39–50.CrossRefGoogle Scholar
Simon, CA, Sato-Okoshi, W and Abe, H (2019 a) Hidden diversity within the cosmopolitan species Pseudopolydora antennata (Claparede, 1869) (Spionidae: Annelida). Marine Biodiversity 49, 25–42.CrossRefGoogle Scholar
Simon, CA, van Niekerk, HH, Burghardt, I, ten Hove, HA and Kupriyanova, EK (2019 b) Not out of Africa: Spirobranchus kraussii (Baird, 1865) is not a global fouling and invasive serpulid of Indo-Pacific origin. Aquatic Invasions 14, 221–249.CrossRefGoogle Scholar
Spencer, LH, Martinelli, JC, King, TL, Crim, R, Blake, B, Lopes, HM and Wood, CL (2020) The risks of shell-boring polychaetes to shellfish aquaculture in Washington, USA: a mini-review to inform mitigation actions. Aquaculture Research 52, 438–455.CrossRefGoogle Scholar
Steinhauer, M and Imamura, E (1990) California OCS Phase II Monitoring Program Three Year Annual Report. Vol. I. Submitted to the US Department of the Interior, Minerals Management Service, Pacific OCS Region, under Contract No. 14-12-0001-30262.Google Scholar
Stock, MW (1964) Anterior Regeneration in Spionidae. MSc thesis, University of Connecticut, USA.Google Scholar
Struck, TH and Cerca De Oliveira, J (2019) Cryptic species and their evolutionary significance. In Encyclopedia of Life Sciences. Chichester: Wiley. https://onlinelibrary.wiley.com/doi/abs/10.1002/9780470015902.a0028292Google Scholar
Struck, TH, Feder, JL, Bendiksby, M, Birkeland, S, Cerca, J, Gusarov, VI, Kistenich, S, Larsson, KH, Liow, LH, Nowak, MD and Stedje, B (2018) Finding evolutionary processes hidden in cryptic species. Trends in Ecology & Evolution 33, 153–163.CrossRefGoogle ScholarPubMed
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, 31–45.CrossRefGoogle Scholar
Van Rensburg, H, Matthee, CA and Simon, CA (2020) Moonshine worms (Diopatra aciculata: Onuphidae, Annelida) in the Knysna Estuary, South Africa; taxonomy and distribution. Journal of the Marine Biological Association of the United Kingdom 100, 897–997.CrossRefGoogle Scholar
Walker, LM (2009) Polydora and Dipolydora (Polychaeta: Spionidae) of Estuaries and Bays of Subtropical Eastern Australia: A Review and Morphometric Investigation of Their Taxonomy and Distribution. M.Sc. thesis, Southern Cross University, Australia.Google Scholar
Walker, LM (2011) A review of the current status of the Polydora-complex (Polychaeta: Spionidae) in Australia and a checklist of recorded species. Zootaxa 2751, 40–62.CrossRefGoogle Scholar
Whitford, TA and Williams, JD (2016) Anterior regeneration in the polychaete Marenzelleria viridis (Annelida: Spionidae). Invertebrate Biology 135, 357–369.CrossRefGoogle Scholar
Williams, JD (2001) Polydora and related genera associated with hermit crabs from the Indo-West Pacific (Polychaeta: Spionidae), with descriptions of two new species and a second polydorid egg predator of hermit crabs. Pacific Science 55, 429–465.CrossRefGoogle Scholar
Williams, L, Matthee, CA and Simon, CA (2016) Dispersal and genetic structure of Boccardia polybranchia and Polydora hoplura (Annelida: Spionidae) in South Africa and their implications for aquaculture. Aquaculture 465, 235–244.CrossRefGoogle Scholar
Williams, L-G, Karl, SA, Rice, S and Simon, C (2017) Molecular identification of polydorid polychaetes (Annelida: Spionidae): is there a quick way to identify pest and alien species? African Zoology 52, 105–117.CrossRefGoogle Scholar
Worsaae, K (2001) The systematic significance of palp morphology in the Polydora complex (Polychaeta: Spionidae). Zoologischer Anzeiger 240, 47–59.CrossRefGoogle Scholar
Yee, A, Mackie, J and Pernet, B (2019) The distribution and unexpected genetic diversity of the non-indigenous annelid Ficopomatus enigmaticus in California. Aquatic Invasions 14, 250–266.CrossRefGoogle Scholar
Zakas, C and Rockman, MV (2014) Dimorphic development in Streblospio benedicti: genetic analysis of morphological differences between larval types. International Journal of Developmental Biology 58, 593–599.CrossRefGoogle ScholarPubMed