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Endoparasite communities of five fish species (Labridae: Cheilininae) from Lizard Island: how important is the ecology and phylogeny of the hosts?

Published online by Cambridge University Press:  07 December 2005

G. MUÑOZ ,
A. S. GRUTTER  and
T. H. CRIBB
G. MUÑOZ
Affiliation:
School of Molecular and Microbial Sciences, Department of Microbiology and Parasitology, University of Queensland, Brisbane 4072, Qld, Australia
A. S. GRUTTER
Affiliation:
School of Integrative Biology, University of Queensland, Brisbane 4072, Qld, Australia
T. H. CRIBB
Affiliation:
School of Molecular and Microbial Sciences, Department of Microbiology and Parasitology, University of Queensland, Brisbane 4072, Qld, Australia
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Abstract

The parasite community of animals is generally influenced by host physiology, ecology, and phylogeny. Therefore, sympatric and phylogenetically related hosts with similar ecologies should have similar parasite communities. To test this hypothesis we surveyed the endoparasites of 5 closely related cheilinine fishes (Labridae) from the Great Barrier Reef. They were Cheilinus chlorourus, C. trilobatus, C. fasciatus, Epibulus insidiator and Oxycheilinus diagramma. We examined the relationship between parasitological variables (richness, abundance and diversity) and host characteristics (body weight, diet and phylogeny). The 5 fishes had 31 parasite species with 9–18 parasite species per fish species. Cestode larvae (mostly Tetraphyllidea) were the most abundant and prevalent parasites followed by nematodes and digeneans. Parasites, body size and diet of hosts differed between fish species. In general, body weight, diet and host phylogeny each explained some of the variation in richness and composition of parasites among the fishes. The 2 most closely related species, Cheilinus chlorourus and C. trilobatus, had broadly similar parasites but the other fish species differed significantly in all variables. However, there was no all-encompassing pattern. This may be because different lineages of parasites may react differently to ecological variables. We also argue that adult parasites may respond principally to host diet. In contrast, larval parasite composition may respond both to host diet and predator-prey interactions because this is the path by which many parasites complete their life-cycles. Finally, variation in parasite phylogeny and parasite life-cycles among hosts likely increase the complexity of the system making it difficult to find all-encompassing patterns between host characteristics and parasites, particularly when all the species in rich parasite communities are considered.

Keywords

parasite communitieswrassesLabridaehost body weighthost diethost phylogenycoral reefsecology
Type
Research Article
Information
Parasitology , Volume 132 , Issue 3 , March 2006 , pp. 363 - 374
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Abbott, R. T. and Dance, S. P. ( 1998). Compendium of Seashells. Odyssey Publishing, California.
Aldana, M., Pulgar, J. M., Ogalde, F. and Ojeda, F. P. ( 2002). Morphometric and parasitological evidence for ontogenetic and geographical dietary shifts in intertidal fishes. Bulletin of Marine Science 70, 55–74.Google Scholar
Anderson, R. C. ( 1992). Nematode Parasites of Vertebrates, their Development and Transmission. CAB International, Cambridge.
Bartoli, P., Morand, S., Riutort, J. J. and Combes, C. ( 2000). Acquisition of parasites correlated with social rank and behavioral changes in fish species. Journal of Helminthology 74, 289–293.CrossRefGoogle Scholar
Bellwood, D. R. and Wainwright, P. C. ( 2001). Locomotion in labrid fishes: implications for habitats use and cross-shelf biogeography on the Great Barrier Reef. Coral Reefs 20, 139–150.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 species. Journal of Natural History 23, 429–473.CrossRefGoogle Scholar
Bush, A. O., Aho, J. M. and Kennedy, C. R. ( 1990). Ecological versus phylogenetic determinants of helminth parasite community richness. Evolutionary Ecology 4, 1–20.CrossRefGoogle Scholar
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. ( 1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Campbell, R. A. and Beveridge, I. ( 1994). Order Trypanorhyncha Diesing, 1863. In Keys to Cestode Parasites of Vertebrates ( ed. L. F. Khalil, Jones, A. and Bray, R. A.), pp. 51–148. CAB International, Cambridge.
Cannon, L. R. G. ( 1977). Some larval ascaridoids from south-eastern Queensland marine fishes. International Journal for Parasitology 7, 233–243.CrossRefGoogle Scholar
Chabaud, A. G. ( 1975). Keys to the genera of the order Spirurida. Part 2. Spiruroidea, Habronematoidea and Acuaroidea. In CIH Keys the Nematode Parasites of Vertebrates No. 3 ( ed. Anderson, R. C. and Willmott, S.), pp. 29–58. Commonwealth Agricultural Bureaux, Farnham Royal, UK.
Chambers, C. B., Cribb, T. H. and Jones, M. K. ( 2000). Tetraphyllidean metacestodes of teleosts of the Great Barrier Reef, and the use of in vitro cultivation to identify them. Folia Parasitologica 47, 285–292.CrossRefGoogle Scholar
Choudhury, A. and Dick, T. A. ( 2000). Richness and diversity of helminth communities in tropical freshwater fishes: empirical evidence. Journal of Biogeography 27, 935–956.CrossRefGoogle Scholar
Clarke, K. R. and Warwick, R. M. ( 1994). Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. Natural Environment Research Council, Bournemouth, UK.
Cribb, T. H., Bray, R. A. and Barker, S. C. ( 1994). 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., Wright, T. and Pichelin, S. ( 2002). The trematodes of groupers (Serranidae: Epinephelinae): knowledge, nature and evolution. Parasitology 124 (Suppl.) S23–S42.CrossRefGoogle Scholar
De Loach, N. ( 1999). Reef Fish Behavior; Florida, Caribbean, Bahamas. New World Publications, Jacksonville.
Dove, A. D. M. ( 2000). Richness patterns in the parasite communities of exotic poeciliid fishes. Parasitology 120, 609–623.CrossRefGoogle Scholar
Everitt, B. S. ( 1993). Cluster Analysis, 3rd Edn. Halsted Press, New York.
Fiorillo, R. A. and Font, W. F. ( 1999). Seasonal dynamics and community structure of helminths of spotted sunfish, Lepomis miniatus (Osteichthyes: Centrarchidae) from an oligohaline estuary in southeastern Louisiana, U.S.A. Journal of the Helminthological Society of Washington 66, 101–110.Google Scholar
García, L. V. ( 2004). Escaping the Bonferroni iron claw in ecological studies. Oikos 105, 657.CrossRefGoogle Scholar
George-Nascimento, M., Muñoz, G., Marquet, P. and Poulin, R. ( 2004). Testing the energetic equivalence rule with helminth endoparasites of vertebrates. Ecology Letters 7, 527–531.CrossRefGoogle Scholar
Grutter, A. S. ( 1994). Spatial and temporal variations of the ectoparasites of seven reef fish species from Lizard Island and Heron Island, Australia. Marine Ecology Progress Series 115, 21–30.CrossRefGoogle Scholar
Grutter, A. S. ( 1998). Habitat-related differences in the abundance of parasites from a coral reef fish: an indication of the movement patterns of Hemigymnus melapterus. Journal of Fish Biology 53, 49–57.Google Scholar
Grutter, A. S. and Poulin, R. ( 1998). Intraspecific and interspecific relationships between host size and the abundance of parasitic larval gnathiid isopods on coral reef fishes. Marine Ecology Progress Series 164, 263–271.CrossRefGoogle Scholar
Hafeezullah, M. ( 1981). Schistorchiid trematodes of marine fishes of India, with considerations on the status of the genus Megacreadium Nagaty, 1956 and the family Schistorchiidae Yamaguti, 1942. Bulletin of the Zoological Survey of India 3, 167–177.Google Scholar
Hemmingsen, W., Halvorsen, O. and MacKenzie, K. ( 2000). The occurrence of some metazoan parasites of Atlantic cod Gadus morhua L. in relation to age and the sex of the host in Balsfjord (70 degree N), North Norway. Polar Biology 23, 368–372.Google Scholar
Hoberg, E. P. ( 1997). Phylogeny and historical reconstruction: host-parasite systems as keystones in biogeography and ecology. In Biodiversity II. Understanding and Protecting Our Biological Resources ( ed. Reaka-Kudla, M. L., Wilson, D. E. M. L. and Wilson, E. O.), pp. 243–261. Joseph Henry Press, Washington.
Houston, K. A. and Haedrich, R. L. ( 1986). Food habits and intestinal parasites of deep demersal fishes from upper continental slope east of Newfoundland northwest Atlantic Ocean. Marine Biology 92, 563–574.CrossRefGoogle Scholar
Hua, C. ( 1989). Life cycle of Proctoeces orientalis sp. nov. in marine bivalves. Acta Zoologica Sinica 35, 58–65.Google Scholar
Janovy, J. J., Clopton, R. E. and Percival, T. J. ( 1992). The roles of ecological and evolutionary influences in providing structure to parasite species assemblages. Journal of Parasitology 78, 630–640.CrossRefGoogle Scholar
Jones, D. and Morgan, G. ( 2002). A Field Guide to Crustaceans of Australian Waters, 2nd Edn. Reed New Holland, Western Australian Museum, Chatswood, NSW.
Kennedy, C. R. and Bush, A. O. ( 1994). The relationship between pattern and scale in parasite communities: a stranger in a strange land. Parasitology 109, 187–196.CrossRefGoogle Scholar
Khalil, L. F., Jones, A. and Bray, R. A. ( 1994). Keys to the Cestode Parasites of Vertebrates. CAB International, UK.
Lamprell, K. and Healy, J. M. ( 1998). Bivalves of Australia. Backhuys Publishers, Leiden, The Netherlands.
Lamprell, K. and Whitehead, T. ( 1992). Bivalves of Australia. Crawford House Press, Bathurst, NSW.
Magurran, A. E. ( 1988). Ecological Diversity and its Measurements. Croom Helm, London.CrossRef
Meenakshi, M., Madhavi, R. and Swarnakumari, V. G. M. ( 1993). The life-cycle of Helicometra gibsoni n. sp. (Digenea: Opecoelidae). Systematic Parasitology 25, 63–72.Google Scholar
Morand, S., Cribb, T. H., Kulbicki, M., Rigby, M. C., Chauvet, C., Dufour, V., Faliex, E., Galzin, R., Lo, C. M., Lo Yat, A., et al. ( 2000). Endoparasite species richness of New Caledonian butterfly fishes: host density and diet matter. Parasitology 121, 65–73.CrossRefGoogle Scholar
Morand, S., Simkova, A., Matejusova, I., Plaisance, L., Verneau, O. and Desdevises, Y. ( 2002). Investigating patterns may reveal processes: evolutionary ecology of ectoparasitic monogeneans. International Journal for Parasitology 32, 111–119.CrossRefGoogle Scholar
Muñoz, G. and Cribb, T. H. ( 2005). Infracommunity structure of parasites of Hemigymnus melapterus (Pisces: Labridae) from Lizard Island, Australia; the importance of habitat and parasite body size. Journal of Parasitology 91, 38–44.CrossRefGoogle Scholar
Muñoz, G., Valdebenito, V. and George-Nascimento, M. ( 2002). La dieta y la fauna de parásitos metazoos del torito Bovichthys chilensis Regan 1914 (Pisces: Bovichthydae) en la costa de Chile centro-sur: variaciones geográficas y ontogenéticas. Revista Chilena de Historia Natural 75, 661–671.CrossRefGoogle Scholar
Olsen, L. S. ( 1952). Some nematodes parasitic in marine fishes. Publication of the Institute of Marine Science, University of Texas 2, 172–215.Google Scholar
Pichelin, S. and Cribb, T. H. ( 2001). The status of the Diplosentidae (Acanthocephala: Palaeacanthocephala) and a new family of acanthocephalans from Australian wrasses (Pisces: Labridae). Folia Parasitologica 48, 289–303.CrossRefGoogle Scholar
Poulin, R. ( 1995). Phylogeny, ecology, and the richness of parasite communities in vertebrates. Ecological Monographs 65, 283–302.CrossRefGoogle Scholar
Poulin, R. ( 1997). Species richness of parasite assemblages: evolution and patterns. Annual Review of Ecology and Systematics 28, 341–358.CrossRefGoogle Scholar
Poulin, R. ( 1999). Body size vs abundance among parasite species: positive relationship? Ecography 22, 246–250.Google Scholar
Poulin, R. and Rohde, K. ( 1997). Comparing the richness of metazoan ectoparasite communities of marine fishes: controlling for host phylogeny. Oecologia 110, 278–283.CrossRefGoogle Scholar
Price, P. W. and Clancy, K. M. ( 1983). Patterns in number of helminth parasite species in freshwater fishes. Journal of Parasitology 69, 449–454.CrossRefGoogle Scholar
Pulkkinen, K., Valtonen, E. T., Niemi, A. and Poikola, K. ( 1999). The influence of food competition and host specificity on the transmission of Triaenophorus crassus (Cestoda) and Cystidicola faraonis (Nematoda) to Coregonus lavaretus and Coregonus albula (Pisces: Coregonidae). International Journal for Parasitology 29, 1753–1763.CrossRefGoogle Scholar
Randall, J. E., Allen, G. R. and Steene, R. C. ( 1997). Fishes of the Great Barrier Reef and Coral Sea. Crawford House Publishing, Bathurst, Australia.
Rodríguez, L. and George-Nascimento, M. ( 1996). La fauna de parásitos metazoos del bacalao de profundidad Dissostichus eleginoides Smitt, 1898 (Pisces: Nototheniidae) en Chile central: aspectos taxonómicos, ecológicos y zoogeográficos. Revista Chilena de Historia Natural 69, 21–33.Google Scholar
Sakanari, J. A. and Moser, M. ( 1989). Complete life cycle of the elasmobranch cestode Lacistorhynchus dollfusi Beveridge and Sakanari, 1987 (Trypanorhyncha). Journal of Parasitology 75, 806–808.CrossRefGoogle Scholar
Sasal, P., Niquil, N. and Bartoli, P. ( 1999). Community structure of digenean parasites of sparid and labrid fishes of the Mediterranean sea: a new approach. Parasitology 119, 635–648.CrossRefGoogle Scholar
Vickery, W. L. and Poulin, R. ( 1998). Parasite extinction and colonisation and the evolution of parasite communities: a simulation study. International Journal for Parasitology 28, 727–737.CrossRefGoogle Scholar
Westneat, M. W. ( 1991). Linkage beomechanics and evolution of the unique feeding mecanism of Epibulus insidiator (Labridae, Teleostei). Journal of Experimental Biology 159, 165–184.Google Scholar
Westneat, M. W. ( 1993). Phylogenetic relationship of the tribe Cheilinini (Labridae: Perciformes). Bulletin of Marine Science 52, 351–394.Google Scholar
Westneat, M. W. ( 1995). Feeding, function, and phylogeny: analysis of historical biomechanics in labrid fishes using comparative methods. Systematic Biology 44, 361–383.CrossRefGoogle Scholar
Wilson, B. ( 1993). Australian Marine Shells, Prosobranch and Gastropods, Vols 1–2. Odyssey Publishing, Western Australia.
Zar, J. H. ( 1996). Biostatistical Analysis, 3rd Edn. Prentice Hall International, New Jersey.