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Taxonomic approaches to and interpretation of host specificity of trematodes of fishes: lessons from the Great Barrier Reef

Published online by Cambridge University Press:  26 April 2011

T. L. MILLER ,
R. A. BRAY  and
T. H. CRIBB
T. L. MILLER*
Affiliation:
Biodiversity Program, Queensland Museum, PO Box 3300, South Brisbane, Queensland, Australia
R. A. BRAY
Affiliation:
Department of Zoology, Natural History Museum, Cromwell Road, London SW7 5BD, UK
T. H. CRIBB
Affiliation:
School of Biological Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia
*
*Corresponding author. Tel: +61 0432 158 502. E-mail: [email protected]
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Summary

The taxonomy of trematodes of Great Barrier Reef (GBR) fishes has been studied in some detail for over 20 years. Understanding of the fauna has been informed iteratively by approaches to sampling, understanding of morphology, the advent of molecular methodology and a feed-back loop from the emergent understanding of host specificity. Here we analyse 658 host-parasite combinations for 290 trematode species, 152 genera and 28 families from GBR fishes. These are reported from 8 orders, 38 families, 117 genera and 243 species of fishes. Of the 290 species, only 4 (1·4%) have been reported from more than one order of fishes and just 23 (7·9%) infect more than one family; 77·9% of species are known from only one genus, and 60% from only one species of fish. Molecular studies have revealed several complexes of cryptic species and others are suspected; we conclude that no euryxenous host distribution should be accepted on the basis of morphology only. The occurrence of individual trematode species in potential hosts is patchy and difficult to predict reliably a priori or explain convincingly a posteriori. These observations point to the need for a vigorous iterative interaction between the accretion of host specificity data and its interpretation.

Keywords

DigeneafishesGreat Barrier Reefhost specificitysystematicstaxonomyTrematoda
Type
Research Article
Information
Parasitology , Volume 138 , Special Issue 13: Systematics as a cornerstone of parasitology , November 2011 , pp. 1710 - 1722
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Almany, G. R., Peacock, L. F., Syms, C., McCormick, M. I. and Jones, G. P. (2007). Predators target rare prey in coral reef fish assemblages. Oecologia 152, 751–761.CrossRefGoogle ScholarPubMed
Barker, S. C., Bray, R. A. and Cribb, T. H. (1993). Preptetos cannoni n. sp. (Digenea: Lepocreadiidae) from Siganus lineatus (Teleostei: Siganidae) from the southern Great Barrier Reef, Australia. Systematic Parasitology 26, 151–155.CrossRefGoogle Scholar
Barker, S. C., Cribb, T. H., Bray, R. A. and Adlard, R. D. (1994). Host-parasite associations on a coral reef: pomacentrid fishes and digenean trematodes. International Journal for Parasitology 24, 643–647.CrossRefGoogle ScholarPubMed
Bott, N. J. and Cribb, T. H. (2005). First report of a bucephalid digenean from an apogonid teleost: Prosorhynchoides apogonis n. sp. from Cheilodipterus macrodon on the southern Great Barrier Reef, Australia. Systematic Parasitology 60, 33–37.CrossRefGoogle Scholar
Bott, N. J. and Cribb, T. H. (2009). Prosorhynchine trematodes (Digenea: Bucephalidae) from epinephelines (Perciformes: Serranidae) on the Great Barrier Reef, Australia. Systematic Parasitology 72, 57–69.CrossRefGoogle ScholarPubMed
Bray, R. A. (1983). On the fellodistomid genus Proctoeces Odhner, 1911 (Digenea), with brief comments on two other fellodistomid genera. Journal of Natural History 17, 321–339.CrossRefGoogle Scholar
Bray, R. A. and Cribb, T. H. (1989). Digeneans of the family Opecoelidae Ozaki, 1925 from the southern Great Barrier Reef, including a new genus and three new species. Journal of Natural History 23, 429–473.CrossRefGoogle Scholar
Bray, R. A. and Cribb, T. H. (1996). Preptetos and Neopreptetos (Digenea: Lepocreadiidae) from Australian marine fishes. Folia Parasitologica 43, 209–226.Google Scholar
Bray, R. A. and Cribb, T. H. (1998). Lepocreadiidae (Digenea) of Australian coastal fishes: new species of Opechona Looss, 1907, Lepotrema Ozaki, 1932 and Bianium Stunkard, 1930 and comments on other species reported for the first time or poorly known in Australian waters. Systematic Parasitology 41, 123–148.CrossRefGoogle Scholar
Bray, R. A. and Cribb, T. H. (2007). Monostephanostomum nolani sp n. and M. krusei Reimer, 1983 (Digenea: Acanthocolpidae) from carangid fishes from coral reef waters off Australia. Folia Parasitologica 54, 19–26.CrossRefGoogle Scholar
Bray, R. A., Cribb, T. H. and Barker, S. C. (1993 a). Hemiuridae (Digenea) from marine fishes of the Great Barrier Reef, Queensland, Australia. Systematic Parasitology 25, 37–62.CrossRefGoogle Scholar
Bray, R. A., Cribb, T. H. and Barker, S. C. (1993 b). The Hemiuroidea (Digenea) of pomacentrid fishes (Perciformes) from Heron Island, Queensland, Australia. Systematic Parasitology 24, 159–184.CrossRefGoogle Scholar
Bray, R. A., Cribb, T. H. and Barker, S. C. (1993 c). The Lepocreadiidae (Digenea) of pomacentrid fishes (Perciformes) from Heron Island, Queensland, Australia. Systematic Parasitology 26, 189–200.CrossRefGoogle Scholar
Bray, R. A., Cribb, T. H. and Barker, S. C. (1994). Fellodistomidae and Lepocreadiidae (Platyhelminthes: Digenea) from chaetodontid fishes (Perciformes) from Heron Island, Southern Great Barrier Reef, Queensland, Australia. Invertebrate Taxonomy 8, 545–581.CrossRefGoogle Scholar
Bray, R. A., Cribb, T. H. and Barker, S. C. (1996). Four species of Lepidapedoides Yamaguti, 1970 (Digenea: Lepocreadiidae) from fishes of the southern Great Barrier Reef, with a tabulation of host-parasite data on the group. Systematic Parasitology 34, 179–195.CrossRefGoogle Scholar
Bray, R. A., Cribb, T. H. and Justine, J. L. (2010). Multitestis Manter 1931 (Digenea: Lepocreadiidae) in ephippid and chaetodontid fishes (Perciformes) in the south-western Pacific Ocean and the Indian Ocean off Western Australia. Zootaxa 2427, 36–46.CrossRefGoogle Scholar
Bray, R. A., Cribb, T. H., Waeschenbach, A. and Littlewood, D. T. J. (2007). A new species of Stephanostomum Looss, 1899 (Digenea, Acanthocolpidae) with a bizarre oral sucker: S. adlardi sp. nov. from the common coral trout Plectropomus leopardus (Lacepède, 1802) (Perciformes, Serranidae) from Lizard Island, Great Barrier Reef. Acta Parasitologica 52, 206–212.CrossRefGoogle Scholar
Bray, R. A., Waeschenbach, A., Cribb, T. H., Weedall, G. D., Dyal, P. and Littlewood, D. T. J. (2009). The phylogeny of the Lepocreadioidea (Platyhelminthes, Digenea) inferred from nuclear and mitochondrial genes: Implications for their systematics and evolution. Acta Parasitologica 54, 310–329.CrossRefGoogle Scholar
Chambers, C. B. and Cribb, T. H. (2006). Phylogeny, evolution and biogeography of the Quadrifoliovariinae Yamaguti, 1965 (Digenea: Lecithasteridae). Systematic Parasitology 63, 61–82.CrossRefGoogle ScholarPubMed
Cole, A. J. (2010). Cleaning to corallivory: ontogenetic shifts in feeding ecology of tubelip wrasse. Coral Reefs 29, 125–129.CrossRefGoogle Scholar
Craig, M. T. and Hastings, P. A. (2007). A molecular phylogeny of the groupers of the subfamily Epinephelinae (Serranidae) with a revised classification of the Epinephelini. Ichthyological Research 54, 1–17.CrossRefGoogle Scholar
Craig, M. T., Pondella, D. J., Franck, J. P. C. and Hafner, J. C. (2001). On the status of the serranid fish genus Epinephelus: evidence for paraphyly based upon 16S rDNA sequence. Molecular Phylogenetics and Evolution 19, 121–130.CrossRefGoogle ScholarPubMed
Cribb, T. H., Bray, R. A. and Barker, S. C. (1992). A review of the family Transversotrematidae (Trematoda: Digenea) with the description of a new genus, Crusziella. Invertebrate Taxonomy 6, 909–935.CrossRefGoogle Scholar
Cribb, T. H., Bray, R. A. and Barker, S. C. (1994 a). Bivesiculidae and Haplosplanchnidae (Digenea) from fishes of the southern Great Barrier Reef, Australia. Systematic Parasitology 28, 81–97.CrossRefGoogle Scholar
Cribb, T. H., Bray, R. A., Barker, S. C. and Adlard, R. D. (1996). Taxonomy and biology of Mitotrema anthostomatum Manter, 1963 (Digenea: Cryptogonimidae) from fishes of the southern Great Barrier Reef, Australia. Journal of the Helminthological Society of Washington 63, 110–115.Google Scholar
Cribb, T. H., Bray, R. A., Barker, S. C., Adlard, R. D. and Anderson, G. R. (1994 b). Ecology and diversity of digenean trematodes of reef and inshore fishes of Queensland. International Journal for Parasitology 24, 851–860.CrossRefGoogle ScholarPubMed
Cribb, T. H., Bray, R. A., Littlewood, D. T. J., Pichelin, S. and Herniou, E. A. (2001). The Digenea. Interrelationships of the Platyhelminthes. (ed. Littlewood, D. T. J. and Bray, R. A.), pp. 168–185. Taylor & Francis, London.Google Scholar
Cribb, T. H., Bray, R. A., Olson, P. D. and Littlewood, D. T. J. (2003). Life cycle evolution in the Digenea: a new perspective from phylogeny. Advances in Parasitology 54, 197–254.CrossRefGoogle ScholarPubMed
Downie, A. J., Bray, R. A., Jones, B. E. and Cribb, T. H. (2011). Taxonomy, host-specificity and biogeography of Symmetrovesicula Yamaguti, 1938 (Digenea: Fellodistomidae) from Chaetodontidae (Teleostei: Perciformes) from the tropical Indo-west Pacific region. Systematic Parasitology 78, 1–18.CrossRefGoogle Scholar
Durio, W. O. and Manter, H. W. (1968 a). Some digenetic trematodes of marine fishes of New Caledonia. Part I. Bucephalidae, Monorchiidae, and some smaller families. Proceedings of the Helminthological Society of Washington 35, 143–153.Google Scholar
Durio, W. O. and Manter, H. W. (1968 b). Some digenetic trematodes of marine fishes of New Caledonia. Part II. Opecoelidae and Lepocreadiidae. Journal of Parasitology 54, 747–756.CrossRefGoogle Scholar
Euzet, L. and Combes, C. (1980). Les problemes de l'espece chez les animaux parasites. Memoires Societe Zoologique de France 40, 239–285.Google Scholar
Froese, R. and Pauly, D. (2010). FishBase. World Wide Web electronic publication. www.fishbase.org, version (03/2010).Google Scholar
Gibson, D. I. and Bray, R. A. (1977). The Azygiidae, Hirudinellidae, Ptychogonimidae, Sclerodistomidae and Syncoeliidae of fishes from the north-east Atlantic. Bulletin of the British Museum (Natural History) Zoology 32, 167–245.Google Scholar
Gibson, D. I. and Bray, R. A. (1986). The Hemiuridae (Digenea) of fishes from the north-east Atlantic. Bulletin of the British Museum (Natural History) Zoology 51, 1–125.Google Scholar
Gibson, D. I., Bray, R. A. and Harris, E. A. (2005). “Host-Parasite Database of the Natural History Museum, London.” from http://www.nhm.ac.uk/research-curation/research/projects/host-parasites/database/.Google Scholar
Hall, K. A., Cribb, T. H. and Barker, S. C. (1999). V4 region of small subunit rDNA indicates polyphyly of the Fellodistomidae (Digenea) which is supported by morphology and life-cycle data. Systematic Parasitology 43, 81–92.CrossRefGoogle ScholarPubMed
Hassanine, R. M. E. S. (2006). The life cycle of Diploproctodaeum arothroni Bray and Nahhas, 1998 (Digenea: Lepocreadiidae) with a comment on the parasitic castration of its molluscan intermediate host. Journal of Natural History 40, 1211–1222.CrossRefGoogle Scholar
Hunter, J. A. and Cribb, T. H. (2010). Transversotrematidae (Platyhelminthes: Trematoda) are rich and abundant on Indo-Pacific fishes. Zootaxa 2442, 25–38.CrossRefGoogle Scholar
Hunter, J. A., Ingram, E., Adlard, R. D., Bray, R. A. and Cribb, T. H. (2010). A cryptic complex of Transversotrema species (Digenea: Transversotrematidae) on labroid, haemulid and lethrinid fishes in the Indo–West Pacific Region, including the description of three new species. Zootaxa 2652, 17–32.CrossRefGoogle Scholar
Jones, C. M., Grutter, A. S. and Cribb, T. H. (2003). Rhipidocotyle labroidei n. sp. (Digenea: Bucephalidae) from Labroides dimidiatus (Valenciennes) (Labridae). Zootaxa 327, 1–5.CrossRefGoogle Scholar
Kolasinski, J., Frouin, P., Sallon, A., Rogers, K., Bruggemann, H. J. and Potier, M. (2009). Feeding ecology and ontogenetic dietary shift of yellowstripe goatfish Mulloidichthys flavolineatus (Mullidae) at Reunion Island, SW Indian Ocean. Marine Ecology-Progress Series 386, 181–195.CrossRefGoogle Scholar
Lester, R. J. G. and Sewell, K. B. (1990). Checklist of parasites from Heron Island, Great Barrier Reef. Australian Journal of Zoology 37, 101–128.CrossRefGoogle Scholar
Letourneur, Y., Galzin, R. and HarmelinVivien, M. (1997). Temporal variations in the diet of the damselfish Stegastes nigricans (Lacepede) on a Reunion fringing reef. Journal of Experimental Marine Biology and Ecology 217, 1–18.CrossRefGoogle Scholar
Le Zotte, L. A. (1954). Studies on marine digenetic trematode of Puerto Rico: the family Bivesiculidae, its biology and affinities. Journal of Parasitology 40, 148–162.CrossRefGoogle Scholar
Lo, C. M., Morgan, J. A. T., Galzin, R. and Cribb, T. H. (2001). Identical digeneans in coral reef fishes from French Polynesia and the Great Barrier Reef (Australia) demonstrated by morphology and molecules. International Journal for Parasitology 31, 1573–1578.CrossRefGoogle ScholarPubMed
Manter, H. W. (1969 a). The occurrence of an accessory excretory vesicle in Prosogonotrema Pérez Vigueras, 1940 (Trematoda: Hemiuroidea). Parazitologicheskii Sbornik 24, 173–177.Google Scholar
Manter, H. W. (1969 b). Three new genera hemiurid trematodes from Australian fishes. Journal of the Fisheries Research Board of Canada 26, 787–792.CrossRefGoogle Scholar
McNamara, M. K. A. and Cribb, T. H. (2009). Hurleytrematoides justinei n. sp (Digenea: Monorchiidae) from Valentinni's sharpnose puffer, Canthigaster valentini (Bleeker) (Tetraodontiformes: Tetraodontidae) from Heron Island, Queensland, Australia. Zootaxa, 63–68.Google Scholar
Miller, T. L. and Cribb, T. H. (2007 a). Coevolution of Retrovarium n. gen. (Digenea: Cryptogonimidae) in Lutjanidae and Haemulidae (Perciformes) in the Indo-West Pacific. International Journal for Parasitology 37, 1023–1045.CrossRefGoogle ScholarPubMed
Miller, T. L. and Cribb, T. H. (2007 b). Phylogenetic relationships of some common Indo-Pacific snappers (Perciformes: Lutjanidae) based on mitochondrial DNA sequences, with comments on the taxonomic position of the Caesioninae. Molecular Phylogenetics and Evolution 44, 450–460.CrossRefGoogle ScholarPubMed
Miura, O., Kuris, A. M., Torchin, M. E., Hechinger, R. F., Dunham, E. J. and Chiba, S. (2005). Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse). International Journal for Parasitology 35, 793–801.CrossRefGoogle ScholarPubMed
Nolan, M. J. and Cribb, T. H. (2004). Two new blood flukes (Digenea: Sanguinicolidae) from Epinephelinae (Perciformes: Serranidae) of the Pacific Ocean. Parasitology International 53, 327–335.CrossRefGoogle ScholarPubMed
Nolan, M. J. and Cribb, T. H. (2005). The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Advances in Parasitology 60, 101–163.CrossRefGoogle ScholarPubMed
Nolan, M. J. and Cribb, T. H. (2006 a). Cardicola Short, 1953 and Braya n. gen. (Digenea: Sanguinicolidae) from five families of tropical Indo-Pacific fishes. Zootaxa 1265, 1–80.CrossRefGoogle Scholar
Nolan, M. J. and Cribb, T. H. (2006 b). An exceptionally rich complex of Sanguinicolidae von Graff, 1907 (Platyhelminthes: Trematoda) from Siganidae, Labridae and Mullidae (Teleostei: Perciformes) from the Indo-west Pacific Region. Zootaxa 1218, 1–80.CrossRefGoogle Scholar
Oliva, M. E., Valdivia, I. M., Cardenas, L., George-Nascimento, M., Gonzalez, K., Guinez, R. E. and Cuello, D. (2010). Molecular and experimental evidence refuse the life cycle of Proctoeces lintoni (Fellodistomidae) in Chile. Parasitology Research 106, 737–740.CrossRefGoogle ScholarPubMed
Olson, P. D., Cribb, T. H., Tkach, V. V., Bray, R. A. and Littlewood, D. T. J. (2003). Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733–755.CrossRefGoogle ScholarPubMed
Paniagua, E., Vilas, R., Sanmartin, M., Santamarina, M. T., Leiro, J. M. and Ubeira, F. M. (1999). Characterization by enzyme electrophoresis of specimens of the genus Helicometra (Trematoda, Opecoelidae) from fish caught off the coast of northwest Spain. Parasite 6, 89–91.CrossRefGoogle ScholarPubMed
Paterson, A. M. and Banks, J. (2001). Analytical approaches to measuring cospeciation of host and parasites: through a glass, darkly. International Journal for Parasitology 31, 1012–1022.CrossRefGoogle ScholarPubMed
Pearson, J. C. (1968). Observations on the morphology and life-cycle of Paucivitellosus fragilis Coil, Reid & Kuntz, 1965 (Trematoda: Bivesiculidae). Parasitology 58, 769–788.CrossRefGoogle Scholar
Poulin, R. (2005). Relative infection levels and taxonomic distances among the host species used by a parasite: insights into parasite specialization. Parasitology 130, 109–115.CrossRefGoogle ScholarPubMed
Poulin, R. and Keeney, D. B. (2010). Host specificity under molecular and experimental scrutiny. Trends in Parasitology 24, 24–28.CrossRefGoogle Scholar
Poulin, R. and Leung, T. L. F. (2010). Taxonomic resolution in parasite community studies: are things getting worse? Parasitology 137, 1967–1973.CrossRefGoogle ScholarPubMed
Poulin, R. and Mouillot, D. (2003). Parasite specialization from a phylogenetic perspective: a new index of host specificity. Parasitology 126, 473–480.CrossRefGoogle ScholarPubMed
Poulin, R. and Mouillot, D. (2005 a). Combining phylogenetic and ecological information into a new index of host specificity. Journal of Parasitology 91, 511–514.CrossRefGoogle ScholarPubMed
Poulin, R. and Mouillot, D. (2005 b). Host specificity and the probability of discovering species of helminth parasites. Parasitology 130, 709–715.CrossRefGoogle ScholarPubMed
Randhawa, H. S. and Burt, M. D. B. (2008). Determinants of host specificity and comments on attachment site specificity of tetraphyllidean cestodes infecting rajid skates from the northwest Atlantic. Journal of Parasitology 94, 436–461.CrossRefGoogle ScholarPubMed
Reversat, J., Maillard, C. and Silan, P. (1991). Polymorphismes phénotypique et enzymatique: intérêt et limites dans la description d'espèces d’Helicometra (Trematoda: Opecoelidae), mésoparasites de téléostéens marins. Systematic Parasitology 19, 147–158.CrossRefGoogle Scholar
Reversat, J., Renaud, F. and Maillard, C. (1989). Biology of parasite populations: the differential specificity of the genus Helicometra Odhner, 1902 (Trematoda: Opecoelidae) in the Mediterranean Sea demonstrated by enzyme electrophoresis. International Journal for Parasitology 19, 885–890.CrossRefGoogle Scholar
Roberts-Thomson, A. and Bott, N. J. (2007). Exploiting mimicry: Prosorhynchoides thomasi n. sp. (Digenea: Bucephalidae) from the fang blenny genus Plagiotremus (Bleeker) Blenniidae from off Lizard Island on the Great Barrier Reef, Australia. Zootaxa 1514, 61–64.CrossRefGoogle Scholar
Rudolphi, C. A. (1819). Entozoorum synopsis, cui accedunt mantissa duplex et indices locupletissimi, Berolini: Sumtibus Augusti Rucker, 811 pp.CrossRefGoogle Scholar
Saeki, T., Sakai, Y., Hashimoto, H. and Gushima, K. (2005). Foraging behavior and diet composition of Trimma caudomaculata and Trimma caesiura (Gobiidae) on coral reefs in Okinawa, Japan. Ichthyological Research 52, 302–305.CrossRefGoogle Scholar
Stothard, J. R., Webster, B. L., Weber, T., Nyakaana, S., Webster, J. P., Kazibwe, F., Kabatereine, N. B. and Rollinson, D. (2009). Molecular epidemiology of Schistosoma mansoni in Uganda: DNA barcoding reveals substantial genetic diversity within Lake Albert and Lake Victoria populations. Parasitology 136, 1813–1824.CrossRefGoogle Scholar
Valdivia, I. M., Cardenas, L., Gonzalez, K., Jofré, D., George-Nascimento, M., Guiñez, R. and Oliva, M. E. (2010). Molecular evidence confirms that Proctoeces humboldti and Proctoeces chilensis (Digenea: Fellodistomidae) are the same species. Journal of Helminthology 84, 341–347.CrossRefGoogle ScholarPubMed
Westneat, M. W. and Wainwright, P. C. (1989). Feeding mechanism of Epibulus insidiator (Labridae, Teleostei) – evolution of a novel functional system. Journal of Morphology 202, 129–150.CrossRefGoogle ScholarPubMed
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