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Morphological and molecular characterisation of Alella igillimpethu n. sp. (Copepoda: Siphonostomatoida: Lernaeopodidae) parasitising the southern African endemic intertidal klipfish, Clinus superciliosus

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Abstract

Lernaeopodidae Milne Edwards, 1840, is an ecological and economically important fish parasite family of copepods (Crustacea: Copepoda), consisting of 48 genera with 334 valid species. To date, approximately 17 genera have been documented from both teleost and elasmobranch hosts from South African marine waters. As part of parasitological surveys targeting parasites of the endemic intertidal klipfish, Clinus superciliosus (Linnaeus) (Clinidae) along the South African coast, a species of Lernaeopodidae was discovered on the gills of this host. Alella igillimpethu n. sp. is described from Clinus superciliosus from Langebaan marina on the west coast of South Africa, with a prevalence of 42.1% and mean intensity of 2.9 (ranging from 1–13). Morphological identification was done using light and scanning electron microscopy and the species description was generated with the aid of DEscription Language for TAxonomy (DELTA) software. The mitochondrial cytochrome c oxidase subunit 1 (COI) region, as well as partial 18S and 28S ribosomal RNA genes confirmed the classification within the family Lernaeopodidae. This is the first report of Lernaeopodidae from C. superciliosus, or in fact any member of Clinidae, as well as the first molecular characterisation of any marine lernaeopodid infecting teleost fish from South Africa. This study contributes valuable genetic and morphological data for this copepod family, as well as new host and distribution records.

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Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Boxshall, G. A. & Hayes, P. (2019). Biodiversity and Taxonomy of Parasitic Crustacea. In Smit, N. J., Bruce, N. L. & Hadfield, K. A. (Eds.), Parasitic Crustacea: Sate of Knowledge and Future Trends (73–133). Springer, Gewerbestrasse, Switzerland. https://doi.org/10.1007/978-3-030-17385-2

  • Boxshall, G. A. & Halsey, S. H. (2004). An introduction to copepod diversity. The Ray Society, London.

    Google Scholar 

  • Brian, A. (1906). Copepodi parassiti dei Pesci d’Italia. Stab. Tipo-Litografico R. Istituto Sordomuti, Genova.

  • Byrnes, T. (1988) Lernanthropids and lernaeopodids (Copepoda) parasitic on Australian bream (Acanthopagrus spp.). Publications of the Seto Marine Biological Laboratory 33:97–120. http://hdl.handle.net/2433/176147

  • Bucklin, A., Frost, B. W., Bradford-Grieve, J., Allen, L. D. & Copley, N. J. (2003). Molecular systematic and phylogenetic assessment of 34 calanoid copepod species of the Calanidae and Clausocalanidae. Marine Biology, 142, 333–343.

    Article  CAS  Google Scholar 

  • Bucklin, A., Guarnieri, M., Hill, R. S., Bentley, A. M. & Kaartvedt, S. (1999). Taxonomic and systematic assessment of planktonic copepods using mitochondrial COI sequence variation and competitive, species-specific PCR. Hydrobiologia, 401, 239–254.

    Article  CAS  Google Scholar 

  • Dippenaar, S. M. (2004). Reported siphonostomatoid copepods parasitic on marine fishes of southern Africa. Crustaceana, 77, 1281–1328.

    Article  Google Scholar 

  • Dippenaar, S. M. (2016a). Biodiversity and studies of marine symbiotic siphonostomatoids off South Africa, African Journal of Marine Science, 38:1, 1–5. http://doi.org/https://doi.org/10.2989/1814232X.2016.1161664

    Article  Google Scholar 

  • Dippenaar, S. M. (2016b). Does Alella Leigh-Sharpe, 1925 (Siphonostomatoida: Lernaeopodidae) really consist of seven species? Systematic Parasitology, 93(1), 47–56.

    Article  Google Scholar 

  • Dippenaar S. M. (2020). Neoalbionella izawai n. sp. from the smallfin gulper shark Centrophorus moluccensis Bleeker and additional host records for N. etmopteri (Yamaguti, 1939) off South Africa. Systematic Parasitology, 97(6),669–673. http://doi.org/https://doi.org/10.1007/s11230-020-09934-4

  • Dippenaar, S. M., Mathibela, R. B. & Bloomer, P. (2010). Cytochrome oxidase I sequences reveal possible cryptic diversity in the cosmopolitan symbiotic copepod Nessipus orientalis Heller, 1868 (Pandaridae: Siphonostomatoida) on elasmobranch hosts from the KwaZulu-Natal coast of South Africa. Experimental Parasitology, 125, 42–50.

    Article  CAS  Google Scholar 

  • Dippenaar, S. M. & Sebone, M. M. (2021) The first report of Naobranchia cygniformis Hesse, 1863 (Copepoda: Lernaeopodidae) off South Africa, with a redescription of the adult female. African Journal of Marine Science, 43(3), 413-416. https://doi.org/https://doi.org/10.2989/1814232X.2021.1946425

    Article  Google Scholar 

  • Edgar, R.C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughout. Nucleic Acids Research, 32, 1792–1797.

    Article  CAS  Google Scholar 

  • Fricke, R., Eschmeyer, W. N. & van der Laan, R. (Eds.), (2022). Eschmeyer's Catalog of Fishes: Genera, Species, References. (http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp). Electronic version accessed 05 02 2022.

  • Froese, R. & Pauly, D. (Eds.), (2021). FishBase. World Wide Web electronic publication. www.fishbase.org, version (08/2021)

  • Guindon, S. & Gascuel, O. (2003). A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology, 52, 696–704.

    Article  Google Scholar 

  • Hayes, P. M., Christison, K. W., Vaughan, D. B., Smit, N. J. & Boxshall, G. A. (2021). Sea lice (Copepoda: Caligidae) from South Africa, with descriptions of two new species of Caligus. Systematic Parasitology, 98, 369–397.

    Article  Google Scholar 

  • Heller, C. (1865). Crustaceen. Reise der Österreichischen Fregatte Novarra um die Erdre, in den Jahren 1857, 1858, 1859 unter den Befehlen des Commodore B. von Wüllerstorf-Urbair, Zoologischer Theil. Kaiserlich-Königliche Hof- und Staatsdruckerei, Wein, Band 2 (Abtheilung 3): 1–280, Pls. 1–25. , available online at https://www.biodiversitylibrary.org/page/13188320

  • Hewitt, G. C., & Blackwell, R. G. (1987). A new species of Alella (Copepoda, Lernaeopodidae) parasitic in the tarakihi, Cheilodactylus macropterus, in New Zealand. New Zealand Journal of Marine and Freshwater Research, 21, 141–147.

    Article  Google Scholar 

  • Ho, J-S. (1977). Marine Flora and Fauna of the Northeastern United States. Copepoda: Lernaeopodidae and Sphyriidae (Vol. 406). Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service.

  • Ho J-S. (1983). Copepod parasites of Japanese surfperchers: their inference on the phylogeny and biogeography of Embiotocidae in the Far East. Annual report of the Sado Marine Station, Niigata University, 13, 31–62.

    Google Scholar 

  • Huys, R., & Boxshall, G. A. (1991). Copepod Evolution. London: The Ray Society.

    Google Scholar 

  • Kabata, Z. (1964). The morphology and the taxonomy of Clavellodes pagelli (Krøyer, 1863) (Copepoda, Lernaeopodidae). Crustaceana, 7, 103–112.

    Article  Google Scholar 

  • Kabata, Z. (1968). Copepoda parasitic on Australian fishes. Journal of Natural History, 2, 505–523.

    Article  Google Scholar 

  • Kabata, Z. (1979). Parasitic Copepoda of British fishes. The Ray Society, London.

    Google Scholar 

  • Kabata, Z. & Cousens, B. (1972). The Structure of the Attachment Organ of Lernaeopodidae (Crustacea: Copepoda). Journal of the Fisheries Research Board of Canada, 29(7), 1015–1023. http://doi.org/https://doi.org/10.1139/f72-147

    Article  Google Scholar 

  • Kawatow, K., Muroga, K., Izawa, K. & Kasahara, S. (1980) Life cycle of Alella macrotrachelus (Copepoda) parasitic on cultured black seabream (Acanthopagrus schlegeli). Journal of the faculty of applied biological science. Hiroshima University 19, 199–214.

    Google Scholar 

  • Klimpel, S., Kuhn, T., Münster, J., Dörge, D. D., Klapper, R. & Kochmann, J. (2019). Parasites of marine fish and cephalopods. Springer International Publishing.

  • Krøyer, H. (1837). Concerning parasitic Crustacea with special reference to the Danish fauna. Om Snyltekrebsene, isaer med Hensyn til den danske Fauna. III. Formbeskrivelser (Fortsaettelse). Naturhistorisk Tidsskrift Ser. I. 1(3): 252-302, pl. 3.

  • Krøyer, H. (1863) Bidrag til Kundskab om Snyltekrebsene. Naturhistorisk Tidsskrift, (3) 2 (1–2), 75–320, plates 1–9. https://doi.org/10.5479/si.00963801.3-141.251

  • Lebepe, M. C. & Dippenaar, S. M. (2016). Bernard’s Brachiella sp., Parabrachiella supplicans (Barnard, 1955) and Eubrachiella sublobulata (Barnard, 1955) (Copepoda: Siphonostomatoida: Lernaeopodidae) deposited in the Iziko South African Museum. Zootaxa, 4061(1), 1–51.

  • Leigh-Sharpe, W.H. (1925). A revision of the British species of Clavella (Crustacea, Copepoda) with a diagnosis of new species: C. devastatrix and C. invicta. Parasitology, Cambridge 17:194-200, figs. 1-4. (18-v-1925)

  • Leigh-Sharpe, W.H. (1936). New parasitic Copepoda from Naples. Parasitology, Cambridge 28:63-71, figs. 1-9. (27-i-1936)

  • Luque, J.L. & Farfán, C. (1991) Copépodos de la familia Lernaeopodidae (Siphonostomatoida) parásitos de algunos peces de la familia Sciaenidae (Teleostei) en el mar peruano. Parasitologia al Día, 14, 63–66

    Google Scholar 

  • Mangena, T., Jordaan, B. P. & Dippenaar, S. M. (2014). Phylogenetic relationships and genetic diversity of Nemesis Risso, 1926 species found on different elasmobranch host species off the KwaZulu-Natal coast, South Africa. African Journal of Marine Science, 36, 163–173.

    Article  Google Scholar 

  • Miller, M. A., Pfeiffer, W. & Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans, LA. 1–8.

  • Milne Edwards, H. (1840) Ordre des Copépodes. In: Milne Edwards, H. (Ed.), Histoire naturelle des Crustacés, comprenant l’anatomie, la physiologie et la classification de ces animaux, Vol. 3. Librairie Encyclopédique de Roret, Paris, pp. 411–529. http://dx.doi.org/https://doi.org/10.5962/bhl.title.39738

  • Montes, M. M., Castro-Romero, R. & Martorelli, S. R. (2017). Morphological identification and DNA barcoding of a new species of Parabrachiella (Siphonostomatoida: Lernaeopodidae) with aspects of their intraspecific variation. Acta Tropica, 173, 34–44. http://dx.doi.org/https://doi.org/10.1016/j.actatropica.2017.05.025

    Article  CAS  Google Scholar 

  • Montes, M.M., Castro-Romero, R., Öktener, A., Balcazar, D., Cardarella, G.F.R. & Martorelli, S., (2022). Molecular evidence supports the validity of three Parabrachiella species infecting mugilids. Acta Tropica, 225, 106211. https://doi.org/https://doi.org/10.1016/j.actatropica.2021.106211

    Article  CAS  Google Scholar 

  • Neethling, L. A. M. & Avenant-Oldewage, A. (2020). Host selection and notes on the distribution of Chonopeltis australis Boxshall, 1976 in southern Africa. African Journal of Aquatic Science, 45, 500–508.

    Article  Google Scholar 

  • Ohtsuka, S., Piasecki, W., Ismail, N. & Kamarudin, A. S. (2020). A new species of Brachiella (Copepoda, Siphonostomatoida, Lernaeopodidae) from Peninsular Malaysia, with relegation of two genera Charopinopsis and Eobrachiella to junior synonyms of Brachiella. Parasite, 27, 40. https://doi.org/https://doi.org/10.1051/parasite/2020038

    Article  Google Scholar 

  • Øines, Ø. & Heuch, P. A. (2007). Caligus elongatus Nordmann genotypes on wild and farmed fish. Journal of Fish Diseases, 30, 81–91. https://doi.org/https://doi.org/10.1111/j.1365-2761.2007.00783.x

    Article  Google Scholar 

  • Olsson, P. (1869). Prodromus Faunae Copepodorum Parasitantium Scandinaviae. Acta Universitatis Lundensis (Acta Universitets Lunds). 5(III)(8):1-49, pls. 1-2.

  • Piasecki, W., Kempter, J., Saraiva, A. & Baptista, A. (2016). The identity of two morphotypes of Alella macrotrachelus (Brian, 1906) (Copepoda: Siphonostomatoida: Lernaeopodidae) from white seabream, Diplodus sargus (Actinopterygii: Sparidae). Annals of Parasitology, 62, 63.

    Google Scholar 

  • Piasecki, W., Mlynarczyk, M. & Hayward, C. J. (2010). Parabrachiella jarai sp. nov. (Crustacea: Copepoda: Siphonostomatoida) parasitic on Sillago sihama (Actinopterygii: Perciformes: Sillaginidae). Experimental Parasitology, 125, 55–62. http://doi.org/https://doi.org/10.1016/j.exppara.2009.10.001

    Article  Google Scholar 

  • Rambaut, A. (2012). FigTree v1. 4. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh. http://tree.bio.ed.ac.uk/software/figtree/

  • Santacruz, A., Morales-Serna, F. N., Leal-Cardín, M., Barluenga, M. & Pérez-Ponce de León, G. (2020). Acusicola margulisae n. sp. (Copepoda: Ergasilidae) from freshwater fishes in a Nicaraguan crater lake based on morphological and molecular evidence. Systematic Parasitology, 97, 165–177. https://doi.org/https://doi.org/10.1007/s11230-020-09906-8

    Article  Google Scholar 

  • Schaeffner, B. C. & Smit, N. J. (2019). Parasites of cartilaginous fishes (Chondrichthyes) in South Africa – neglected field of marine science. Folia Parasitology, 66, 002. http://doi.org/https://doi.org/10.14411/fp.2019.002. PMID: 30919826.

  • Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Scmid, B., Tinevez, J., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P. & Cardona, A. (2012). Fiji: an open-source platform for biological-image analysis. Nature Methods, 9, 676–682. https://doi.org/https://doi.org/10.1038/nmeth.2019

    Article  CAS  Google Scholar 

  • Smith, M. M. & Heemstra, P. C. (Eds.) (2012) Smiths’ Sea fishes. Springer Science and Business Media.

  • Tamura, K., Stecher, G. & Kumar, S. (2021). MEGA 11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution https://doi.org/https://doi.org/10.1093/molbev/msab120.

    Article  Google Scholar 

  • Van Niekerk, J. P. & Olivier, P. A. S. (1995). Alella gibbosa, a new species of Lernaeopodidae (Copepoda), from Lake St. Lucia, South Africa. South African Journal of Science, 91(1), 41–44.

  • Walter, C. & Boxshall, G. (2021). World Register of Marine Species. Available from https://www.marinespecies.org at VLIZ. Accessed 2022-02-12.

  • Wilson, C.B. (1915). North American parasitic copepods belonging to the Lernaeopodidae, with a revision of the entire family. Proceedings of the United States National Museum 47(2063): 565-729, pls. 25-56, figs. 1-15. (6-iii-1915).

  • Yamaguti, S. (1939). Parasitic copepods from fishes of Japan. Part 6: Lernaeopodoida I. Volumen Jubilare pro Prof. Sadao Yoshida, 2, 529–578.

    Google Scholar 

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Acknowledgements

The authors would like to thank the National Research Foundation (NRF) for funding (UID: 115413; 130494; 120403). Opinions, findings, conclusions and recommendations expressed in this publication are that of the authors, and the NRF accept no liability whatsoever in this regard. We thank members of the North-West University Water Research Group (NWU-WRG) for their assistance with fish collection and fieldwork, as well as Coret van Wyk (neé Hoogendoorn) and Anja Vermaak (NWU-WRG) for assistance with molecular analyses. Willie Landman is thanked for his assistance with SEM. The authors would also like to thank the anonymous reviewers for their valuable comments to improve the quality of the manuscript. This is contribution number 702 from the NWU-Water Research Group.

Funding

This study was funded by the National Research Foundation (UID: 115413; 130494; 120403)

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  1. Water Research Group, Unit for Environmental Sciences and Management, North-West University, Private Bag X6001, Potchefstroom, 2520, South Africa

    Anja Erasmus, Kerry A. Hadfield, Victor Wepener & Nico J. Smit

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Contributions

AE – Sampling collection, formal analysis, investigation, data curation, writing – original draft, writing – editing and revision, visualization, description in DELTA, illustrations, photomicrographs; KAH – Resources, methodology, validation, project administration, supervision, funding; writing – review & editing; VW – Resources, project administration, supervision, funding, writing – review; NJS – Resources, validation, validation, project administration, supervision, funding, writing – review & editing.

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Correspondence to Anja Erasmus.

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All procedures performed in studies involving animals were in accordance with the ethical standards of AnimCare at the North-West University. All applicable international, national and/or institutional guidelines for the use and care of animals were followed. Research permits were obtained prior to sampling from the Department of Agriculture, Forestry and Fisheries (DAFF) (RES2018/35, RES2019/103 and RES2020/29) and South African National Parks (SANParks) (MALH-K/2016-005a). Ethical approval for collections were given to AE through the North-West University’s AnimCare (NWU-00440-16-A5 and NWU-0051-19-A5).

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Erasmus, A., Hadfield, K.A., Wepener, V. et al. Morphological and molecular characterisation of Alella igillimpethu n. sp. (Copepoda: Siphonostomatoida: Lernaeopodidae) parasitising the southern African endemic intertidal klipfish, Clinus superciliosus. Syst Parasitol 100, 69–83 (2023). https://doi.org/10.1007/s11230-022-10071-3

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