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Type: Article
Published: 2023-03-10
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Species of Hexabothriidae (Monogenea) may have extensive distribution ranges reflecting multiple host species: evidence from three new South African records

1School of Access Education, Tertiary Education Division, Central Queensland University, Rockhampton, Queensland, Australia.
3Department of Forestry, Fisheries and Environment, Aquaculture Innovation and Technology Development, Cape Town, South Africa.
5Norwegian Veterinary Institute, Fish Health Research Group, Pb 64, N-1431 Ås, Norway.
6Aquatic Parasitology Laboratory and Southeastern Cooperative Fish Parasite & Disease Laboratory, School of Fisheries, Aquaculture, & Aquatic Sciences, College of Agriculture, Auburn University, 559 Devall Drive, Auburn, AL 36832, USA. Department of Zoology, School for Environmental Sciences and Development, North-West University, Private Bag X6001, Potchefstroom, 2520, South Africa.
Monogenea Hexabothriidae Erpocotyle catenulata Heteronchocotyle gymnurae Hypanocotyle bullardi Elasmobranch

Abstract

Many hexabothriid genera require renewed taxonomic attention to provide additional detailed comparative data from new material to resolve existing species quandaries. Our current study describes and provides additional museum material for three hexabothriid species from three genera from South Africa: Erpocotyle catenulata (Guberlet), which is confirmed as a valid species, Heteronchocotyle gymnurae Neifar, Euzet and Ben Hassine, and Hypanocotyle bullardi Chero, Cruces, Sáez, Carolina, Camargo, Portes Santos and Luque. Evidence of these three hexabothriid species from South Africa suggests that hexabothriids have more globally widespread distributions, and that they are less host-specific than previously considered. A detailed summary of hexabothriids reported from the triakid hosts, Galeorhinus galeus and Mustelus mustelus is provided, and the host-specificity of hexabothriids is discussed.

 

References

  1. Agosta, S.J. & Klemens, J.A. (2008) Ecological fitting by phenotypically flexible genotypes: implications for species associations, community assembly and evolution. Ecology Letters, 11, 1123–1134. https://doi.org/10.1111/j.1461-0248.2008.01237.x
    Araujo, S.B.L., Braga, M.P., Brooks, D.R., Agosta, S.J., Hoberg, E.P., von Hartenthal, F.W. & Boeger, W.A. (2015) Understanding host-switching by ecological fitting. PLoS ONE, 10, e0139225. https://doi.org/10.1371/journal.pone.0139225
    Barta, J.R., Martin, D.S., Liberator, P.A., Dashkevicz, M., Anderson, J.W., Feighner, S.D., Elbrecht, A., Perkins-Barrow, A., Jenkins, M.C., Danforth, H.D., Ruff, M.D. & Profous-Juchelka, H. (1997) Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. The Journal of Parasitology, 83, 262–271. https://doi.org/10.2307/3284453
    Benmansour, B., Toussef, F., Ben Ali, M., Albogami, B. & Boufahja, F. (2022) The survey of ectoparasites on two species of Triakids (Mustelus mustelus and M. punctulatus) sharks from Tunisian coasts. Saudi Journal of Biological Sciences, 29, 3610–3616. https://doi.org/10.1016/j.sjbs.2022.02.052
    Boeger, W.A. & Kritsky, D.C. (1989) Phylogeny, coevolution, and revision of the Hexabothriidae Price, 1942 (Monogenea). International Journal for Parasitology, 19, 425–440. https://doi.org/10.1016/0020-7519(89)90099-4
    Boeger, W.A., Kritsky, D.C., Domingues, M.V. & Bueno-Silva, M. (2014) The phylogenetic position of the Loimoidae Price, 1936 (Monogenoidea: Monocotylidea) based on analyses of partial rDNA sequences and morphological data. Parasitology International, 63, 492–499. https://doi.org/10.1016/j.parint.2014.01.005
    Brinkmann, A. (1952) Fish trematodes from Norwegian waters. I. The history of fish trematode investigations in Norway and the Norwegian species of the order Monogenea. Årbok for Universitetet i Bergen, Naturvitenskapelig rekke, 1, 1–134.
    Bullard, S.A., Snyder, S.D., Jensen, K. & Overstreet, R.M. (2008) New genus and species of Aporocotylidae (Digenea) from a basal Actinopterygian, the American Paddlefish, Polyodon spathula, (Acipenseriformes: Polyodontidae) from the Mississippi Delta. The Journal of Parasitology, 94, 487–495. https://doi.org/10.1645/GE-1323.1
    Bullard, S.A., Warren, M.B. & Dutton, H.R. (2021) Redescription of Cathariotrema selachii (MacCallum, 1916) Johnston and Tiegs, 1922 (Monogenoidea: Monocotylidae), emendation of monotypic Cathariotrema Johnston and Tiegs, 1922, and proposal of Cathariotrematinae n. subfam. based on morphological and nucleotide evidence. Journal of Parasitology, 107, 481–513. https://doi.org/10.1645/21-12
    Caira, J.N., Jensen, K. & Holsinger, K.E. (2003) On a new index of host specificity. In: Combes, C. & Jourdane, J. (Eds.), Taxonomie, écologie et évolution des métazoaires parasites. Vol. 1. PUP Perpignan, France, pp. 161–201.
    Carvalho-Azevedo, A., Huancachoque, E.G., Ceullar, I., Sáez, G.M., Cruces, C.L., Chero, J.D. & Luque, J.L. (2021) New record of monogeneans (Platyhelminthes: Monogenea) infecting some marine fishes from the Peruvian coastal zone. Revista peruana de biología, 28, e21125. https://doi.org/10.15381/rpb.v28i3.21125
    Cerfontaine, P. (1899) Contribution à l’étude des Octocotylidés. V. Onchocotylinae (Planches XVIII a XXI). Archives de Biologie, Liège, 16, 345–478.
    Chaabane, A., Justine J.-L., Grey, D., Bakenhaster, M.D. & Neifar, L. (2016) Pseudorhabdosynochus sulamericanus (Monogenea, Diplectanidae), a parasite of deep-sea groupers (Serranidae) occurs transatlantically on three congeneric hosts (Hyporthodus spp.), one from the Mediterranean Sea and two from the western Atlantic. PeerJ, 4: e2233. https://doi.org/10.7717/peerj.2233
    Chabot, C.L. (2015) Microsatellite loci confirm a lack of population connectivity among globally distributed populations of the tope shark Galeorhinus galeus (Triakidae). Journal of Fish Biology, 87, 371–385. https://doi.org/10.1111/jfb.12727
    Chero, J.D., Cruces, C.L., Sáez, G., Camargo, A.C.A., Portes Santos, C. & Luque, J.L. (2018) Hypanocotyle bullardi n. gen. n. sp. (Monogenea: Hexabothriidae) from gill of the diamond stingray Hypanus dipterurus (Jordan et Gilbert) (Myliobatiformes: Dasyatidae) in the Southeastern Pacific Ocean off Peru. Parasitology International, 67, 425–430. https://doi.org/10.1016/j.parint.2018.03.010
    Chirichigno, N.F. (1974) Clave para identificar los peces marinos del Peru. Instituto del Mar del Perú, 44, 1–387.
    Chisholm, L.A., Whittington, I.D. & Kearn, G.C. (2001) Dendromonocotyle colorni sp. n. (Monogenea: Monocotylidae) from the skin of Himantura uarnak (Dasyatididae) from Israel and a new host record for D. octodiscus from the Bahamas. Folia Parasitologica, 48, 15–20. https://doi.org/10.14411/fp.2001.004
    Cohen, S.C., Justo, M.C.N. & Kohn, A. (2013) South American Monogenoidea parasites of fishes, amphibians and reptiles. Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq), Brazil, 659 pp.
    Compagno, L.J.V. (1984) FAO Species Catalogue. Vol. 4. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Part 2 - Carcharhiniformes. FAO Fisheries Synopsis 125 (4, part 2), 251–655. [Rome: FAO]
    Compagno, L.J.V., Ebert, D.A. & Smale, M.J. (1989) Guide to the sharks and rays of southern Africa. New Holland Ltd., London, 158 pp.
    Coupland, A.C. (1962) The taxonomy of monogeneans gill parasites from Scyliorhinus canicula and Raia clavata at Plymouth. Journal of the Marine Biological Association of the United Kingdom, 42, 521–526. https://doi.org/10.1017/S0025315400054230
    Derouiche, I. (2022) Les Métazoaires Plathelminthes parasites de quelques Chondrichtyens Chiméridés (Holocéphales) et Batoides (Élasmobranches) de la côte algérienne. Thèse de doctorat, Université des Sciences de la Technologie Houari Boumedienne, Alger, 250 pp.
    Dollfus, R.P. (1937) Parasitologia Mauritanica helmintha (III): Trématodes de sélaciens et de chéloniens. Bulletin du Comité d'Études Historiques et Scientifiques de l'Afrique Occidentale Française, 19, 397–519.
    Domingues, M.V., Pancera, N.C.M. & Marques, F.P.L. (2007) Monogenoidean parasites of freshwater stingrays (Rajiformes: Potamotrygonidae) from the Negro River, Amazon, Brazil: species of Potamotrygonocotyle (Monocotylidae) and Paraheteronchocotyle (Hexabothriidae). Folia Parasitologica, 54, 177–190. https://doi.org/10.14411/fp.2007.025
    Dulvy, N.K., Charvet, P., Carlson, J., Badji, L., Blanco-Parra, M.P., Chartrain, E., De Bruyne, G., Derrick, D., Dia, M., Doherty, P., Dossa, J., Ducrocq, M., Leurs, G.H.L., Notarbartolo di Sciara, G., Pérez Jiménez, J.C., Pires, J.D., Seidu, I., Serena, F., Soares, A., Tamo, A., Vacchi, M., Walls, R.H.L. & Williams, A.B. (2021a) Gymnura altavela. The IUCN Red List of Threatened Species 2021: e.T63153A3123409. Available from: https://dx.doi.org/10.2305/IUCN.UK.2021-1.RLTS.T63153A3123409.en (accessed 08 April 2022) https://doi.org/10.2305/IUCN.UK.2021-1.RLTS.T63153A3123409.en
    Dulvy, N.K., Charvet, P., Badji, L., Chartrain, E., De Bruyne, G., Derrick, D., Dia, M., Doherty, P., Dossa, J., Ducrocq, M., Leurs, G.H.L., Metcalfe, K., Pires, J.D., Seidu, I., Soares, A., Tamo, A., VanderWright, W.J. & Williams, A.B. (2021b) Gymnura sereti. The IUCN Red List of Threatened Species 2021: e.T180502386A180503121. https://doi.org/10.2305/IUCN.UK.2021-1.RLTS.T180502386A180503121.en
    Euzet, L. (1955) Larves gyrodactyloïdes nageantes de quelques Trématodes monogénétiques des poissons marins. Bulletin de la Société Neuchâteloise des Sciences Naturelles, 78, 71–79.
    Euzet, L. & Maillard, C. (1974) Les Monogènes Hexabothriidae Price, 1942. Historique, systématique, phylogenèse. Bulletin du Muséum National d’Histoire Naturelle, 206, 113–141.
    FAO (2022) Galeorhinus galeus Linnaeus,1758. Fisheries and Aquaculture Division [online]. Rome. Available from: https://www.fao.org/fishery/en/aqspecies/2828/en (accessed 21 April 2022)
    Fernandez, J.C., Villalba, C.S. & Alvina, A. (1986) Parasitos del pejegallo Callorhynchus callorhynchus (L.) en Chile. Aspectos biologicos y sistemáticos. Biologia Pesquera, 15, 63–73.
    Froese, R. & Pauly, D. (2022) FishBase. World Wide Web electronic publication. Available from: www.fishbase.org (accessed 2 February 2022)
    Giresi, M.M., Grubbs, R.D., Portnoy, D.S., Driggers, W.B., III, Jones, L. & Gold, J.R. (2015) Identification and distribution of morphologically conserved smoothhound sharks in the Northern Gulf of Mexico. Transactions of the American Fisheries Society, 144, 1301–1310. https://doi.org/10.1080/00028487.2015.1069212
    Glennon, V., Chisholm, L.A. & Whittington, I.D. (2007) Experimental infections, using a fluorescent marker, of two elasmobranch species by unciliated larvae of Branchotenthes octohamatus (Monogenea: Hexabothriidae): invasion route, host specificity and post-larval development. Parasitology, 134, 1243–1252. https://doi.org/10.1017/S0031182007002545
    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
    Griffiths, C.L. & Robinson, T.B. (2016) Use and usefulness of measures of marine endemicity in South Africa. South African Journal of Science, 112, e2015–0249. https://doi.org/10.17159/sajs.2016/20150249
    Guberlet, J.E. (1933) Notes on some Onchocotylinae from Naples with a description of a new species. Pubblicazioni della Stazione Zoologica di Napoli, 12, 323–336.
    Harris, P.D., Cable, J., Tinsley, R.C. & Lazarus, C.M. (1999) Combined ribosomal DNA and morphometric analysis of individual gyrodactylid monogeneans. Journal of Parasitology, 85, 188–191. https://doi.org/10.2307/3285617
    Hermans, R., Vanhove, M.P.M., Ditrich, O., Tyml, T., Gelnar, M., Artois, T. & Kmentová, N. (2021) Parasitic flatworms infecting thorny skate, Amblyraja radiata: Infection by the monogeneans Acanthocotyle verrilli and Rajonchocotyle emarginata in Svalbard. Parasitology International, 81, 102261. https://doi.org/10.1016/j.parint.2020.102261
    ICZN (1999) International Code of Zoological Nomenclature, 4th edition, xxix. The International Trust for Zoological Nomenclature, London, 306 pp.
    Justine, J.-L. (2011) Protocotyle euzetmaillardi n. sp. (Monogenea: Hexabothriidae) from the bigeye sixgill shark Hexanchus nakamurai Teng (Elasmobranchii: Hexanchidae) off New Caledonia. Systematic Parasitology, 78, 41–55. https://doi.org/10.1007/s11230-010-9275-6
    Kuznetsova, I.G. (1975) Monogenea from Chondrichthyes of the Patagonian shelf. Ekologiceskaja i Eksperimental'naja Parazitologija 1, 143–153. [In Russian]
    Lambert, A. & Maillard, C. (1979) L’oncomiracidium d’Erpocotyle catenulata (Guberlet, 1933) (Monogène Hexabothriidae) parasite de Mustelus mustelus (L.) (Selachii). Annale de Parasitologie Humaine et Comparée, 54, 113–115. https://doi.org/10.1051/parasite/1979541113
    Lopez-Roman, R. & De Armas, F. (1987) Hexabothrium musteli (MacCallum, 1931) Price, 1942 (Hexabothriidae: Monogenea) en los arcos branquiales de Mustelus mustelus (L. 1758) capturados en aguas del archipielago Canario. Revista Iberica de Parasitologia, 125–129.
    MacCallum, G.A. (1931) Four new species of trematode worms of the subfamily Onchocotylinae. Proceedings of the U. S. National Museum, 79, 1–8. https://doi.org/10.5479/si.00963801.79-2892.1
    Mackenzie, K. & Hemmingsen, W. (2015) Parasites as biological tags in marine fisheries research: European Atlantic waters. Parasitology, 142, 54–67. https://doi.org/10.1017/S0031182014000341
    Maduna, S.N., da Silva, C., Winter, S.P., Roodt-Wilding, R. & Bester-van der Merwe, A.E. (2016) When two oceans meet: regional population genetics of an exploited coastal shark, Mustelus mustelus. Marine Ecology Progress Series, 544, 183–196. https://doi.org/10.3354/meps11596
    Maillard, C. (1972) Redescription d’Hexabothrium musteli (MacCallum. 1931) Price, 1942 (Hexabothriidae, Monogenea). Bulletin de la Société Zoologique de France, 97 (1), 79–87.
    Neifar, L., Euzet, L. & Ben Hassine, O.K. (2001) Heteronchocotyle gymnurae sp. n. (Monogenea: Hexabothriidae), a gill parasite of Gymnura altavela (Elasmobranchii: Gymnuridae) from the Mediterranean Sea. Comparative Parasitology, 68, 91–96.
    Nowlin, W.D. & Klinck, J.M. (1986) The physics of the Antarctic Circumpolar Current. Reviews of Geophysics, 24, 469–491. https://doi.org/10.1029/RG024i003p00469
    Ogawa, K. (1991) Ectoparasites of sawfish, Pristis microdon, caught in freshwaters of Australia and Papua New Guinea. In: Shimizu, M. & Taniuchi, T. (Eds.), Studies on Elasmobranchs Collected from Seven River Systems in Northern Australia and Papua New Guinea. University Museum, University of Tokyo. Nature Culture, 3, 91–102.
    Olsson, P. (1876) Bidrag till skandinaviens Helminthfauna. I. Kongl. Svenska vetenskaps–akademiens handlingar, 14, 1–35.
    Palombi, A. (1849) L Trematodi d'Italia. Parte I. Trematodi monogenetici. Archivio zoologico italiano, 34, 203–408.
    Patella, R. & Bullard, S.A. (2013) Hexabothriids of devil rays (Mobulidae): new genus and species from gill of Mobula hypostoma in the northern Gulf of Mexico and redescription of a congener from Mobula rochebrunei in the eastern Atlantic Ocean. Journal of Parasitology 99, 856–867. https://doi.org/10.1645/12-153.1
    Price, E.W. (1942) North American monogenetic trematodes. V. The family Hexabothriidae, n. n. (Polystomatoidea). Proceedings of the Helminthological Society of Washington, 9, 39–56.
    Sproston, N.G. (1946) A synopsis of the monogenetic trematodes. Transcripts of the Zoological Society of London, 25, 185–600. https://doi.org/10.1111/j.1096-3642.1946.tb00218.x
    Suriano, D.M. & Incorvaia, I.S. (1982) Sistematica y biologia de Callorhynchocotyle marplatensis gen. et sp. nov. (Monogenea: Polyopisthocotylea) parasita de las branquias de Callorhynchus callorhinchus (Linne, 1758) Garman, 1904 (Pisces: Holocephali) de la región costera de Mar del Plata. Parasitologia, 2, 19–32.
    Tendeiro, J. & Valdez, V. (1955) Helmintologia Ictiológica. Sobre os helmintes de alguns peixes da costa Portuguesa. Boletim Cultural da Guiné Portuguesa, 10, 81–128.
    Thaer, A. (1850) Ueber Polystomum appendiculatum (Onchocotyle appendiculata Diesing). Archiv für Anatomie, Physiologie und Wissenschaftliche Medicin, 602–632.
    van Beneden, P.J. (1853) Espèce nouvelle du genre Onchocotyle, vivant sur les branchies du Scimnus glacialis. Bulletins de l’Académie Royale des sciences, des lettres et des beaux-arts de Belgique, 20, part 3, 59–72.
    van Beneden, P.J. (1858) Suppleìment aux Comptes rendus des seìances de l'Acadeìmie des sciences, t. II. Meìmoire sur les vers intestinaux. J.B. BaillieÌre et fils, Paris, pp. 376.
    van Beneden, P.J. (1861) Recherches sur la faune littorale de Belgique, Crustacés. In: Mémoires de l'Académie royale des sciences, des lettres et des beaux-arts de Belgique, 33, 1–174. https://doi.org/10.5962/bhl.title.119687
    van Beneden, P.J. & Hesse, C.E. (1863) Recherches sur les Bdellodes (Hirudinées) et les Trématodes marins. In: Mémoires de l'Académie Royale des Sciences, des Lettres et des Beaux-Arts de Belgique, 34, 1–150 + Plates. https://doi.org/10.5962/bhl.title.11767
    van Beneden, P.J. (1871) Les poissons des côtes de Belgique, leurs parasites et leurs commensaux. In: Mémoires de l'Académie royale des sciences, des lettres et des beaux-arts de Belgique, 38, 1–94. https://doi.org/10.5962/bhl.title.13455
    Vaughan, D. & Christison, K. (2012) Towards addressing the current state of confusion within the Hexabothriidae Price, 1942 (1908): Callorhynchocotyle Suriano & Incorvaia, 1982 (Monogenea: Hexabothriidae) re-visited, with the preliminary evaluation of novel parameters for measuring haptoral armature of hexabothriids. Zootaxa, 3229 (1), 1–34. https://doi.org/10.11646/zootaxa.3229.1.1
    Vaughan, D.B. & Christison, K.W. (2017) Anoplodiscus Sonsino, 1890 (Monogenea: Anoplodiscidae): a new Australian species, and the first African record from South African hosts. Systematic Parasitology, 94, 891–906. https://doi.org/10.1007/s11230-017-9750-4
    Vaughan, D., Chisholm, L. & Christison, K. (2008) Overview of South African Dendromonocotyle (Monogenea: Monocotylidae), with descriptions of 2 new species from stingrays (Dasyatidae) kept in public aquaria. Zootaxa, 1826 (1), 26–44. https://doi.org/10.11646/zootaxa.1826.1.2
    Vaughan, D.B., Christison, K.W. & Hansen, H. (2021) New monogeneans from the bathydemersal southern African endemic catshark, Holohalaelurus regani (Gilchrist, 1922). Systematic Parasitology, 98, 343–355. https://doi.org/10.1007/s11230-021-09982-4
    Võ, T.H., Dmitrieva, E.V., Lê, T.K.O. & Nguyen, T.H.T. (2019) Monogeneans (Platyhelminthes: Monogenea) parasitizing the gills of the stingray (Myliobatiformes: Dasyatidae) from Nha Trang Gulf, off Vietnam. VII All-Russian Conference with International Participation. School of Theoretical and Marine Parasitology, 32, UDC 591.69 (597).
    Watson, D.E. & Thorson, T.B. (1976) Helminths from elasmobranchs in Central American fresh waters. In: Thorson, T.B. (Ed.), Investigations of the Ichthyofauna of Nicaraguan lakes, 52. School of Life Sciences. University of Nebraska, Lincoln, pp. 629–640.
    Wiskin, M. (1970) The oncomiracidium and post-oncomiracidial development of the hexabothriid monogenean Rajonchocotyle emarginata. Parasitology, 60, 457–479. https://doi.org/10.1017/S0031182000078264
    Yokota, L. & de Carvalho, M.R. (2017) Taxonomic and morphological revision of butterfly rays of Gymnura micrura (Bloch & Schneider, 1801) species complex, with the description of two new species (Myliobatiformes: Gymnuridae). Zootaxa, 4332 (1), 1–74. https://doi.org/10.11646/zootaxa.4332.1.1