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High diversity of metazoan parasites in carp gudgeons (Eleotridae: Hypseleotris spp.) from Eastern Australia

Published online by Cambridge University Press:  05 May 2020

E.C. Rochat*
Natural History Museum of Geneva, Malagnou Road 1, 1208Geneva, Switzerland
I. Blasco-Costa
Natural History Museum of Geneva, Malagnou Road 1, 1208Geneva, Switzerland Department of Arctic and Marine Biology, UiT The Arctic University of Norway, Langnes, PO Box 6050, 9037Tromsø, Norway
T. Scholz
Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05České Budějovice, Czech Republic
P.J. Unmack
Centre for Applied Water Science, Institute for Applied Ecology, University of Canberra, ACT, Canberra, 2601, Australia
Author for correspondence: E.C. Rochat, E-mail:


Knowledge of the parasite fauna of Australian freshwater fish is fragmentary and incomplete. An understanding of fish hosts and their associated parasites is vital for the successful management of aquatic ecosystems. In this study, we surveyed the parasite fauna of carp gudgeons (Hypseleotris spp.), a complex of species of Australian freshwater fishes, using morphology and molecular data for the 18S and 28S ribosomal RNA genes. We examined 137 individuals of three different taxa in the carp gudgeon species complex and found 16 parasitic taxa of the Digenea, Cestoda, Nematoda and Arthropoda (five adults and 11 larvae). Eleven parasites are reported for the first time from the carp gudgeons (Pseudodactylogyrus sp., Gyrodactylus sp., Clinostomum sp., Paradilepis patriciae, P. cf. kempi, two unidentified species of Paradilepis, Dendrouterina sp., Parvitaenia sp., two lineages of Cyclophyllidea gen. sp., Procamallanus sp., larvae of a spirurine nematode and Lernaea sp.), in addition to Apatemon cf. hypseleotris Negm-Eldin & Davies, 2001 and the invasive tapeworm Schyzocotyle acheilognathi (Yamaguti, 1934), which were previously reported from these fish hosts. Parasite species richness was double in Lake's and Midgley's carp gudgeons relative to western carp gudgeon. These findings highlight the key role of carp gudgeons as intermediate hosts for multiple parasites with complex life cycles using native birds as definitive hosts and the usefulness of DNA data for the identification of parasite larvae.

Research Paper
Copyright © The Author(s), 2020. Published by Cambridge University Press

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Allen, G, Midgley, S and Allen, M (2002) A field guide to the freshwater fishes of Australia. Perth, Western Australian Museum.Google Scholar
Beveridge, I and Gasser, RB (2014) Diversity in parasitic helminths of Australasian marsupials and monotremes: a molecular perspective. International Journal for Parasitology 44, 859864.CrossRefGoogle ScholarPubMed
Blasco-Costa, I and Poulin, R (2017) Parasite life‒cycle studies: a plea to resurrect an old parasitological tradition. Journal of Helminthology 91, 647656.CrossRefGoogle Scholar
Blasco-Costa, I, Balbuena, JA, Kostadinova, A and Olson, PD (2009) Interrelationships of the Haploporinae (Digenea: Haploporidae): a molecular test of the taxonomic framework based on morphology. Parasitology International 58, 263269.CrossRefGoogle ScholarPubMed
Blasco-Costa, I, Cutmore, SC, Miller, TL and Nolan, MJ (2016) Molecular approaches to trematode systematics: ‘best practice’ and implications for future study. Systematic Parasitology 93, 295306.CrossRefGoogle ScholarPubMed
Bona, FV (1975) Étude critique et taxonomique des Dilepididae Fuhrm., 1907 (Cestoda) parasites des ciconiiformes: considérations sur la spécificité et la spéciation. 750 pp. Florence, Italy, Monitore Zoologico Italiano.Google Scholar
Bradley, CA and Altizer, S (2007) Urbanization and the ecology of wildlife diseases. Trends in Ecology & Evolution 22, 95102.CrossRefGoogle ScholarPubMed
Briosio-Aguilar, R, García-Varela, M, Hernández-Mena, DI, Rubio-Godoy, M and Pérez-Ponce de León, G (2019) Morphological and molecular characterization of an enigmatic clinostomid trematode (Digenea: Clinostomidae) parasitic as metacercariae in the body cavity of freshwater fishes (Cichlidae) across Middle America. Journal of Helminthology 93, 461474.CrossRefGoogle Scholar
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575583.CrossRefGoogle Scholar
Černotíková, E, Horák, A and Moravec, F (2011) Phylogenetic relationships of some spirurine nematodes (Nematoda: Chromadorea: Rhabditida: Spirurina) parasitic in fishes inferred from SSU rRNA gene sequences. Folia Parasitologica 58, 135148.CrossRefGoogle ScholarPubMed
Choudhury, A, Aguirre-Macedo, ML, Curran, SS, de Nunez, MO, Overstreet, RM, de Leon, GP and Santos, CP (2016) Trematode diversity in freshwater fishes of the Globe II: ‘New World’. Systematic Parasitology 93, 271282.CrossRefGoogle ScholarPubMed
Cribb, TH (1998) The diversity of the Digenea of Australian animals. International Journal for Parasitology 28, 899911.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
Dove, ADM and Fletcher, AS (2000) The distribution of the introduced tapeworm Bothriocephalus acheilognathi in Australian freshwater fishes. Journal of Helminthology 74, 121127.CrossRefGoogle ScholarPubMed
Dove, ADM, Cribb, TH, Mockler, SP and Lintermans, M (1997) The Asian fish tapeworm, Bothriocephalus acheilognathi, in Australian freshwater fishes. Marine and Freshwater Research 48, 181183.CrossRefGoogle Scholar
Drummond, AJ, Ashton, B, Buxton, S, et al. (2010) Geneious V5.3. Secondary Geneious V5.3. Available at (accessed 13 January 2020).Google Scholar
Dušek, L, Gelnar, M and Šebelová, S (1998) Biodiversity of parasites in a freshwater environment with respect to pollution: metazoan parasites of chub (Leuciscus cephalus L.) as a model for statistical evaluation. International Journal for Parasitology 28, 15551571.CrossRefGoogle Scholar
Hernández-Mena, DI, García-Varela, M and Pérez-Ponce de León, G (2017) Filling the gaps in the classification of the Digenea Carus, 1863: systematic position of the Proterodiplostomidae Dubois, 1936 within the superfamily Diplostomoidea Poirier, 1886, inferred from nuclear and mitochondrial DNA sequences. Systematic Parasitology 94, 833848.CrossRefGoogle ScholarPubMed
Hoese, D, Larson, H and Llewellyn, L (1980). Family Eleotridae: gudgeons. pp. 169185 in McDowall, RM (Ed) Freshwater fishes of Southeastern Australia, vol. 1. Sydney, Reed Pty Ltd.Google Scholar
Jorge, F and Poulin, R (2018) Poor geographical match between the distributions of host diversity and parasite discovery effort. Proceedings of the Royal Society B-Biological Sciences, 285(1879). ScholarPubMed
Justine, JL, Briand, MJ and Bray, RA (2012) A quick and simple method, usable in the field, for collecting parasites in suitable condition for both morphological and molecular studies. Parasitology Research 111, 341351.CrossRefGoogle ScholarPubMed
Katoh, K, Kuma, K, Toh, H and Miyata, T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research 33, 511518.CrossRefGoogle ScholarPubMed
Kearse, M, Moir, R, Wilson, A, et al. (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 16471649.CrossRefGoogle ScholarPubMed
Kuchta, R, Choudhury, A and Scholz, T (2018) Asian fish Tapeworm: the most successful invasive parasite in Freshwaters. Trends in Parasitology 34, 511523.CrossRefGoogle ScholarPubMed
Kwak, ML, Heath, ACG and Palma, RL (2019) Saving the Manx shearwater flea Ceratophyllus (Emmareus) fionnus (Insecta: Siphonaptera): the road to developing a recovery plan for a threatened Ectoparasite. Acta Parasitologica 64, 903910.Google ScholarPubMed
Lagrue, C, Kaldonski, N, Motreuil, S, Lefevre, T, Blatter, O, Giraud, P and Bollache, L (2011) Interspecific differences in drift behaviour between the native Gammarus pulex and the exotic Gammarus roeseli and possible implications for the invader's success. Biological Invasions 13, 14091421.CrossRefGoogle Scholar
Lester, RJG and Hayward, CJ (2006) Phylum Arthropoda. pp. 466565 in Woo, PTK (Ed) Fish diseases and disorders. Volume 1: protozoan and metazoan infections, vol. 1. Wallingford, CAB International.CrossRefGoogle Scholar
Lintermans, M (2009) Fishes of the Murray – Darling basin. An introductory guide. 157 pp. Canberra, Murray–Darling Basin Authority.Google Scholar
Littlewood, DTJ, Curini-Galletti, M and Herniou, EA (2000) The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics and Evolution 16, 449466.CrossRefGoogle ScholarPubMed
Lockyer, AE, Olson, PD and Littlewood, DTJ (2003) Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biological Journal of the Linnean Society 78, 155171.CrossRefGoogle Scholar
Lymbery, AJ, Hassan, M, Morgan, DL, Beatty, SJ and Doupe, RG (2010) Parasites of native and exotic freshwater fishes in south–western Australia. Journal of Fish Biology 76, 17701785.CrossRefGoogle ScholarPubMed
Matthews, D and Cribb, TH (1998) Digenetic trematodes of the genus Clinostomum Leidy, 1856 (Digenea: Clinostomidae) from birds of Queensland, Australia, including C. wilsoni n. sp. from Egretta intermedia. Systematic Parasitology 39, 199208.CrossRefGoogle Scholar
Miller, MA, Pfeiffer, W and Schwartz, T (2010) The CIPRES science gateway: a community resource for phylogenetic analyses. in Gateway Computing Environments Workshop, 4 November 2010, New Orleans, Louisiana, USA, pp. 18.Google Scholar
Mouritsen, KN, Sørensen, MM, Poulin, R and Fredensborg, BL (2018) Coastal ecosystems on a tipping point: global warming and parasitism combine to alter community structure and function. Global Change Biology 24, 43404356.CrossRefGoogle ScholarPubMed
Negm-Eldin, M and Davies, RW (2001) Morphology and life cycle of Apatemon hypseleotris species novum from Australia including metacercariae viability and excystment. Deutsche Tierarztliche Wochenschrift 109, 306314.Google Scholar
Olson, PD, Cribb, TH, Tkach, VV, Bray, RA and Littlewood, DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733755.CrossRefGoogle Scholar
Ortega-Olivares, MP and García-Varela, M (2018) Phylogenetic relationships of the family Gryporhynchidae (Cestoda: Cyclophyllidea) inferred through SSU and LSU rDNA sequences. Journal of Helminthology 93, 763771.CrossRefGoogle ScholarPubMed
Poulin, R and Presswell, B (2016) Taxonomic quality of species descriptions varies over time and with the number of authors, but unevenly among parasitic taxa. Systematic Biology 65, 11071116.CrossRefGoogle ScholarPubMed
Pusey, B, Kennard, M and Arthington, A (2004) Freshwater fishes of North-Eastern Australia. Collingwood, Victoria, Csiro Publishing.CrossRefGoogle Scholar
Ronquist, F, Teslenko, M, van der Mark, P, et al. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539542.CrossRefGoogle ScholarPubMed
Scholz, T, Besprozvannykh, VV, Boutorina, TE, et al. (2016) Trematode diversity in freshwater fishes of the Globe I: ‘Old World’. Systematic Parasitology 93, 257269.CrossRefGoogle ScholarPubMed
Stamatakis, A (2006) RAxML–VI–HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 26882690.CrossRefGoogle ScholarPubMed
Thacker, CE and Unmack, PJ (2005) Phylogeny and biogeography of the eleotrid genus Hypseleotris (Teleostei: Gobioidei: Eleotridae), with redescription of H. cyprinoides. Records of the Australian Museum 57, 113.CrossRefGoogle Scholar
Thacker, CE, Unmack, PJ, Matsui, L and Rifenbark, N (2007) Comparative phylogeography of five sympatric Hypseleotris species (Teleostei: Eleotridae) in south-eastern Australia reveals a complex pattern of drainage basin exchanges with little congruence across species. Journal of Biogeography 34, 15181533.CrossRefGoogle Scholar
Thomas, F, Guegan, JF, Michalakis, Y and Renaud, F (2000) Parasites and host life–history traits: implications for community ecology and species co–existence. International Journal for Parasitology 30, 669674.CrossRefGoogle ScholarPubMed
Unmack, PJ (2000) The genus Hypseleotris in southeastern Australia: its identification and breeding biology. Fish Sahul 14, 645657.Google Scholar
Unmack, PJ, Adams, M, Bylemans, J, Hardy, C, Hammer, M and Georges, A (2019) Perspectives on the clonal persistence of presumed ‘ghost’ genomes in unisexual or allopolyploid taxa arising via hybridization. Scientific Reports, 9(4730). ScholarPubMed
Walker, K and Humphries, P (2013) Ecology of Australian freshwater fishes. Collingwood, Australia, CSIRO Publishing.Google Scholar
Werle, E, Schneider, C, Renner, M, Volker, M and Fiehn, W (1994) Convenient single–step, one tube purification of PCR products for direct sequencing. Nucleic Acids Research 22, 43544355.CrossRefGoogle ScholarPubMed
Williams, J, Read, C, Norton, T, Dovers, S, Burgman, M and Anderson, H (2001) Biodiversity, Australia State of the Environment Report 2001. Canberra, CSIRO Publishing on behalf of the Department of the Environment and Heritage.Google Scholar
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