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Type: Article
Published: 2023-03-28
Page range: 197-210
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Epibiotic association of encrusting cheilostome bryozoans on shells of an invasive mussel from rocky shores of South Africa, with the description of a new aviculiferous species of Chaperia

1Research and Exhibitions Department, Iziko Museums of South Africa, Cape Town, 8000, South Africa.
2Department of Zoology and Entomology, Rhodes University, Grahamstown, 6139, South Africa. Department of Ocean Sciences, Memorial University of Newfoundland, St. John’s, A1C 5S7, Canada.
2Department of Zoology and Entomology, Rhodes University, Grahamstown, 6139, South Africa.
Bryozoa Celleporella epibiosis Hippomonavella intertidal mussels Mytilus galloprovincialis new species

Abstract

Rocky shores typically exhibit a variety of sedentary and free-moving forms of epibionts associated with the shells of mussel basibionts. This paper provides a first report on epibiotic bryozoans found on shells of the invasive Mediterranean mussel, Mytilus galloprovincialis Lamarck. More than 2500 mussels were collected between December 2019 and October 2020 from rocky shores during low spring tides across the south–southeast coast of South Africa. Ten percent of these mussels hosted epibiotic bryozoans. We examined a subset of these epibiotised mussels to assess the diversity of bryozoans. Three encrusting cheilostome species were identified: Chaperia atypica n. sp., Celleporella hyalina (Linnaeus), and Hippomonavella sp. This new species is the first Chaperia with avicularia and the first South African species with ooecia. This study highlights the biological diversity of epibiotic bryozoans on mussel shells and, given their differences in microtopography, the possibility that invasive species can provide a new substratum for rare, overlooked or undescribed species of epibionts.

 

References

  1. Barea-Arco, J., Pérez-Martinez, C. & Morales-Baquro, R. (2001) Evidence of a mutualistic relationship between an algal epibiont and its host, Daphnia pulicaria. Limnology and Oceanography, 46, 871–881. https://doi.org/10.4319/lo.2001.46.4.0871
    Barkai, A. & McQuaid, C. (1988) Predator-prey role reversal in a marine benthic ecosystem. Science, 242, 62–64. https://doi.org/10.1126/science.242.4875.62
    Bell, C., McQuaid, C.D. & Porri, F. (2015) Barnacle settlement on rocky shores: substratum preference and epibiosis on mussels. Journal of Experimental Marine Biology and Ecology, 473, 195–201. https://doi.org/10.1016/j.jembe.2015.09.006
    Bers, A.V., D’Souza, F., Klijnstra, J.W., Willemsen, P.R. & Wahl, M. (2006) Chemical defence in mussels: antifouling effect of crude extracts of the periostracum of the blue mussel Mytilus edulis. Biofouling, 22 (4), 251–259.https://doi.org/10.1080/08927010600901112
    Bers, A.V., Díaz, E.R., da Gama, B.A.P., Vieira-Silva, F., Dobretsov, S., Valdivia, N., Thiel, M., Scardino, A.J., McQuaid, C.D., Sudgen, H.E., Thomason, J.C. & Wahl, M. (2010) Relevance of mytilid shell microtopographies for fouling defence - a global comparison. Biofouling, 26, 367–377.https://doi.org/10.1080/08927011003605888
    Bers, A.V. & Wahl, M. (2004) The influence of natural surface microtopographies on fouling. Biofouling, 20, 43–51.https://doi.org/10.1080/08927010410001655533
    Bock, P.E. (1982) Bryozoans (Phylum Bryozoa or Ectoprocta). In: Shepherd, S.A. & Thomas, I.M. (Eds.), Marine invertebrates of southern Australia: Part I. Adelaide, South Australia. D.J. Woolman, Government Printer, Adelaide, pp. 319–394.
    Boonzaaier, M.K. (2017) Diversity and Zoogeography of South African Bryozoa Unpublished doctoral dissertation, University of the Western Cape, Cape Town, 339 pp.
    Boonzaaier-Davids, M.K., Florence W.K. & Gibbons, M.J. (2020) Novel taxa of Cheilostomata Bryozoa discovered in the historical backlogs of the Iziko South African Museum. Zootaxa, 4820 (1), 105–133. https://doi.org/10.11646/zootaxa.4820.1.5
    Borthagaray, A.I. & Carranza, A. (2007) Mussels as ecosystem engineers: their contribution to species richness in a rocky littoral community. Acta Oecologica, 31, 243–250.https://doi.org/10.1016/j.actao.2006.10.008
    Calvo-Ugarteburu, G. & McQuaid, C.D. (1998) Parasitism and introduced species: epidemiology of trematodes in the intertidal mussels Perna perna and Mytilus galloprovincialis. Journal of Experimental Marine Biology and Ecology, 220, 47–65.https://doi.org/10.1016/S0022-0981(97)00083-X
    Cook, P.L., Bock, P.E., Hayward, P.J. & Gordon, D.P. (2018) Class Gymnolaemata, order Cheilostomata. In: Cook, P.J., Bock, P.E., Gordon, D.P. & Weaver, H.J. (Eds.), Australian Bryozoa. Vol. 2. Taxonomy of Australian Families. CSIRO Publishing, Melbourne, pp. 61‒279.https://doi.org/10.1071/9781486306831
    de Sá, F.S., Nalesso, R.C. & Paresque, K. (2007) Fouling organisms on Perna perna mussels: Is it worth removing them? Brazilian Journal of Oceanography, 55 (2), 155–161.https://doi.org/10.1590/S1679-87592007000200008
    Dick, M.H., Grischenko, A.V. & Mawatari, S.F. (2005) Intertidal Bryozoa (Cheilostomata) of Ketchikan, Alaska. Journal of Natural History, 39 (43), 3687–3784.https://doi.org/10.1080/00222930500415195
    Florence, W.K., Hayward, P.J. & Gibbons, M.J. (2007) Taxonomy of shallow-water Bryozoa from the west coast of South Africa. African Natural History, 3, 1–58.
    Gordon, D.P. (1982) The genera of the Chaperiidae (Bryozoa). New Zealand Journal of Zoology, 9, 1–23.https://doi.org/10.1080/03014223.1982.10423832
    Gordon, D.P. (1984) The marine fauna of New Zealand: Bryozoa: Gymnolaemata from the Kermadec Ridge. New Zealand Oceanographic Institute Memoir, 91, 1–198.
    Gray, J.E. (1848) s.n. In: List of the specimens of British animals in the collections of the British Museum. Part 1. Centrionae or radiated animals. Trustees of the British Museum, London, pp. 91–151.
    Gray, C.A., McQuaid, C.D. & Davies-Coleman, M.T. (2005) A symbiotic shell-encrusting bryozoan provides subtidal whelks with chemical defence against rock lobsters. African Journal of Marine Science, 27, 549–556.https://doi.org/10.2989/18142320509504115
    Griffiths, C.L., Robinson, T.B., Lange, L. & Mead, A. (2010) Marine Biodiversity in South Africa: an evaluation of current states of knowledge. PLoS ONE, 5, e12008.https://doi.org/10.1371/journal.pone.0012008
    Grischenko, A.V., Dick, M.H. & Mawatari, S.F. (2007) Diversity and taxonomy of intertidal Bryozoa (Cheilostomata) at Akkeshi Bay, Hokkaido, Japan. Journal of Natural History, 41, 1047–1161. https://doi.org/10.1080/00222930701391773
    Gutiérrez, J.L., Bagur, M. & Palomo, M.G. (2019) Algal epibionts as co-engineers in mussel beds: effects on abiotic conditions and mobile interstitial invertebrates. Diversity, 11, 17. https://doi.org/10.3390/d11020017
    Gutiérrez, J.L., Jones, C.G., Strayer, D.L. & Iribarne, O.O. (2003) Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos, 101, 79–90.https://doi.org/10.1034/j.1600-0706.2003.12322.x
    Hayward, P.J. (1980) Cheilostomata (Bryozoa) from the South Atlantic. Journal of Natural History, 14, 701–722.https://doi.org/10.1080/00222938000770591
    Hayward, P.J. & Cook, P.L. (1983) The South African Museum’s Meiring Naude Cruises. Part 13, Bryozoa II. Annals of the South African Museum, 91, 1–161. [http://biodiversitylibrary.org/page/40684336#page/17/mode/1up]
    Hayward, P.J. & Fordy, M.R. (1982) A new species of Bryozoan epizooite from South Africa. Journal of Natural History, 16, 769–773.https://doi.org/10.1080/00222938200770601
    Hayward, P.J. & Ryland, J.S. (1999) Cheilostomatous Bryozoa. Part 2. Hippothooidea—Celleporoidea. Issue 14. 2nd Edition. Field Studies Council for The Linnean Society of London and The Estuarine and Coastal Science Association, Shrewsbury, 416 pp.
    Hincks, T. (1880) Contributions towards a general history of the marine Polyzoa. Part I. Madeiran Polyzoa. Annals and Magazine of Natural History, 6, 69–80.https://doi.org/10.1080/00222938009458955
    Jullien, J. (1881) Remarques sur quelques espèces des Bryozoaires cheilostomiens. Bulletin de la Société zoologique de France, 6, 163–168.
    Kang, J.Y., Bangoura, I., Cho, J.Y., Joo, J., Choi, Y.S., Hwang, D.S. & Hong, Y.K. (2016) Antifouling effects of the periostracum on algal spore settlement in the mussel Mytilus edulis. Fisheries and Aquatic Sciences, 19, 7. https://doi.org/10.1186/s41240-016-0007-y
    Key, Marcus M., Jr., Jeffries, W.B., Voris, H.K. & Yang, C.M. (1996) Epizoic bryozoans and mobile ephemeral host substrata. In: Gordon, D.P., Smith, A.M. & Grant-Mackie, J.A. (Eds.), Bryozoans in Space and Time. National Institute of Water and Atmospheric Research, Wellington, pp. 157–165.
    Key, M.M., Jr & Hendrickx, M.E. (2022) Biflustra irregulata (Cheilostomata: Membraniporidae): a tsunami debris rafted Indo-Pacific bryozoan found in the eastern Pacific Ocean. Zootaxa, 5128 (3), 340–354. https://doi.org/10.11646/zootaxa.5128.3.2
    Kumar, R., Kumari, S., Malika, A., Sharma, A.P. & Dahms, H.-U. (2022) Protistan epibionts affect prey selectivity patterns and vulnerability to predation in a cyclopoid copepod. Scientific Reports, 12, 22631. https://doi.org/10.1038/s41598-022-26004-5
    Kumari, S., Kumar, R., Sarkar, U.K. & Das, B.K. (2021) Record of Epibiont ciliates (Ciliophora: Peritrichia) living on freshwater invertebrates in a floodplain wetland. Journal of the Inland Fisheries Society of India, 53 (3 & 4), 210–214.
    Lathlean, J.A. & McQuaid, C.D. (2017) Biogeographic variability in the value of mussel beds as ecosystem engineers on South African rocky shores. Ecosystems, 20, 568–582.https://doi.org/10.1007/s10021-016-0041-8
    Lathlean, J.A., Seuront, L., McQuaid, C.D., Ng, T.P.T., Zardi, G.I. & Nicastro, K.R. (2016) Cheating the locals: invasive mussels steal and benefit from the cooling effect of indigenous mussels. PLoS ONE, 11, e0152556.https://doi.org/10.1371/journal.pone.0152556
    Linnaeus, C. (1767) s.n. In: Systema naturae per regna tria naturae: secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Regnum Animale. Laurentii Salvii, Holmiae [Stockholm], pp. 533–1327.https://doi.org/10.5962/bhl.title.157601
    Lins, D.M. & Rocha, R.M. (2022) Invasive species fouling Perna perna (Bivalvia: Mytilidae) mussel farms. Marine Pollution Bulletin, 181, 113829.https://doi.org/10.1016/j.marpolbul.2022.113829
    Ma, K.C.K., Gusha, M.N.C., Zardi, G.I., Nicastro, K.R., Monsinjon, J.R. & McQuaid, C.D. (2021) Biogeographic drivers of distribution and abundance in an alien ecosystem engineer: Transboundary range expansion, barriers to spread, and spatial structure. Journal of Biogeography, 48, 1941–1959. https://doi.org/10.1111/jbi.14124
    Ma, K.C.K., McQuaid, C.D., Pulfrich, A. & Robinson, T.B. (2020) Status of a decennial marine invasion by the bisexual mussel Semimytilus algosus (Gould, 1850) in South Africa. African Journal of Marine Science, 42, 507–515.https://doi.org/10.2989/1814232X.2020.1820376
    Malherbe, H. & Samways, M. (2014) Rocky shores of a major southern African protected area are almost free from intertidal invertebrate alien species. Koedoe, 56, 1206.https://doi.org/10.4102/koedoe.v56i1.1206
    Mead, A., Carlton, J.T., Griffiths, C.L. & Rius, M. (2011) Introduced and cryptogenic marine and estuarine species of South Africa. Journal of Natural History, 45, 2463–2524.https://doi.org/10.1080/00222933.2011.595836
    Morris, P.A. (1980) The bryozoan family Hippothoidae (Cheilostomata-Ascophora) with emphasis on the genus Hippothoa. Allan Hancock Monographs in Marine Biology, 10, 1–115.
    Moyano, G.H.I. (1986) Bryozoa marinos chilenos VI. Cheilostomata Hippothoidae: South eastern Pacific species. Boletín de la Sociedad de Biología de Concepción, 57, 89–135.
    Navarrete, Z., Cancino, A., Moyano, G.H.I. & Hughes, R.N. (2005) Morphological differentiation in the Cellepora hyalina (Linnaeus, 1767) complex (Bryozoa: Cheilostomata) along the Chilean coast. In: Moyano, H.I., Cancino, J.M. & Wyse Jackson, P.N. (Eds.), Bryozoan Studies 2004. Taylor & Francis Group, London, pp. 207–213.https://doi.org/10.1201/9780203970799.ch20
    Ndhlovu, A., McQuaid, C.D., Nicastro, K, Marquet, N., Gektidis, M, Monaco, C.J. & Zardi G. (2019). Biogeographical patterns of endolithic infestation in an invasive and an indigenous intertidal marine ecosystem engineer. Diversity, 11, 75.https://doi.org/10.3390/d11050075
    Nicastro, N.R., McQuaid, C.D., Dievart, A. & Zardi, G.I. (2020). Intraspecific diversity in an ecological engineer functionally trumps interspecific diversity in shaping community structure. Science of the Total Environment, 743, 140723.https://doi.org/10.1016/j.scitotenv.2020.140723
    O’Donoghue, C.H. (1924) The Bryozoa (Polyzoa) collected by the S.S. ‘Pickle’. Report on the Fisheries Marine Biological Survey of South Africa, 3 (10), 1–63.
    O’Donoghue, C.H. & de Watteville, D. (1937) Notes on South African Bryozoa. Zoologischer Anzeiger, 117, 12–22.
    O’Donoghue, C.H. & de Watteville, D. (1944) Additional notes on Bryozoa from South Africa. Annals of the Natal Museum, 10, 407–432.
    O’Donoghue, C.H. (1957) Some South African Bryozoa. Transactions of the Royal Society of South Africa, 35, 71–95.https://doi.org/10.1080/00359195709519012
    Palomo, M.G., People, J., Chapman, M.G. & Underwood, A.J. (2007) Separating the effects of physical and biological aspects of mussel beds on their associated assemblages. Marine Ecology Progress Series, 344, 131–142. https://doi.org/10.3354/meps07002
    Pan, Y.J., Wang, W.L., Hwang, J.S. & Souissi, S. (2021) Effects of epibiotic diatoms on the productivity of the calanoid copepod Acartia tonsa (Dana) in intensive aquaculture systems. Frontiers in Marine Science, 8, 2296–7745.https://doi.org/10.3389/fmars.2021.728779
    Puccinelli, E. & McQuaid, C.D. (2021) Commensalism, antagonism or mutualism? Effects of epibiosis on the trophic relationships of mussels and epibiotic barnacles. Journal of Experimental Marine Biology and Ecology, 540, 151549.https://doi.org/10.1016/j.jembe.2021.151549
    Ramos-Rivera, B.S., Castro-Mondragon, H., Kuk-Dzul, J.G., Flores-Rodríguez, P. & Flores-Garza, R. (2021) Diversity of Epibionts Associated with Lepidochelys olivacea (Eschscholtz, 1829) sea turtles nesting in the Mexican South Pacific. Animals, 11, 1734. https://doi.org/10.3390/ani11061734
    Robinson, T.B., Branch, G.M., Griffiths, C.L., Govender, A. & Hockey, P.A.R. (2007) Changes in South African rocky intertidal invertebrate community structure associated with the invasion of the mussel Mytilus galloprovincialis. Marine Ecology Progress Series, 340, 163–171. https://doi.org/10.3354/meps340163
    Robinson, T.B., Peters, K. & Brooker, B. (2020) Coastal invasions: the South African context. In: van Wilgen, B., Measey, J., Richardson, D., Wilson, J. & Zengeya, T. (Eds.), Biological Invasions in South Africa. Invading Nature—Springer Series in Invasion Ecology. Vol. 14. Springer, Cham, pp 229–247.https://doi.org/10.1007/978-3-030-32394-3_9
    Ryland, J.S. (2001) Convergent colonial organization and reproductive function in two bryozoan species epizoic on gastropod shells. Journal of Natural History, 35, 1085–1101. https://doi.org/10.1080/002229301300323929
    Ryland, J.S. & Gordon, D.P. (1977) Some New Zealand and British species of Hippothoa (Bryozoa: Cheilostomata). Journal of the Royal Society of New Zealand, 7, 17–49.https://doi.org/10.1080/03036758.1977.10419334
    Sadchatheeswaran, S., Branch, G.M., Moloney, C.L. & Robinson, T.B. (2018) Impacts of alien ‘ecosystem engineers’ overwhelm interannual and seasonal shifts in rocky-shore community composition on Marcus Island, South Africa. African Journal of Marine Science, 40, 137–147. https://doi.org/10.2989/1814232X.2018.1462729
    Sousa, R., Gutiérrez, J.L. & Aldridge D.C. (2009) Non-indigenous invasive bivalves as ecosystem engineers. Biological Invasions, 11, 2367–2385. https://doi.org/10.1007/s10530-009-9422-7
    Stephenson, T.A. & Stephenson, A. (1949) The universal features of zonation between tide-marks on rocky coasts. Journal of Ecology, 37, 289–305.https://doi.org/10.2307/2256610
    Thieltges, D.W. (2005) Impact of an invader: epizootic American slipper limpet Crepidula fornicata reduces survival and growth in European mussels. Marine Ecology Progress Series, 286, 13–19. https://doi.org/10.3354/meps286013
    Thomsen, M.S., Wernberg, T., Altieri, A.H., Tuya, F., Gulbransen, D., McGlathery, K.J., Holmer, M. & Silliman, B.R. (2010) Habitat cascades: The conceptual context and global relevance of facilitation cascades via habitat formation and modification. Integrated Comparative Biology, 50, 158–175.https://doi.org/10.1093/icb/icq042
    Thornber, C., Jones, E. & Thomsen, M. (2016) Epibiont-marine macrophyte assemblages. In: Olafsson, E. (Ed.), Marine Macrophytes as Foundation Species (Issue June 2019). CRC Press, Boca Raton, pp. 43–65. https://doi.org/10.4324/9781315370781-4
    Wahl, M. (2009) Epibiosis: ecology, effects and defences. In: Wahl, M. (Ed.), Marine Hard Bottom Communities. Springer, Berlin, Heidelberg, pp. 61–72. https://doi.org/10.1007/b76710_4
    WoRMS Editorial Board (2022) World Register of Marine Species. Available from: https://www.marinespecies.org (accessed 30 November 2022)