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Ontogenetic changes in heterogeneity of parasite communities of fish: disentangling the relative role of compositional versus abundance variability

Published online by Cambridge University Press:  16 October 2012

J. T. TIMI*
Affiliation:
Laboratorio de Parasitología, Instituto de Investigaciones Marinas y Costeras (IIMyC), Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata – Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Funes 3350, (7600) Mar del Plata, Argentina
A. L. LANFRANCHI
Affiliation:
Laboratorio de Parasitología, Instituto de Investigaciones Marinas y Costeras (IIMyC), Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata – Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Funes 3350, (7600) Mar del Plata, Argentina
*
*Corresponding author: Tel: +54 223 4752426. Fax: +54 223 4753150. E-mail: [email protected]

Summary

In order to determine how much of the variability in parasite assemblages is driven by differences in composition or in abundance we used multivariate dispersions (average distance from infracommunities to their size class centroid in the multivariate space) as a measurement of β-diversity in infracommunities of Conger orbignianus, applying a set of dissimilarity measures with different degrees of emphasis on composition versus relative abundance information. To evaluate comparatively the rate of such changes, we also analysed the effect of host size by regressing differences in β-diversity among size classes against differences in mean fish size. Multivariate dispersions varied along an ontogenetic gradient, its significance depending on the measurement used. Larger fish showed higher richness and abundance; however, smaller fish displayed lower variations in abundance but higher in composition. This could be caused by stochastic encounters at low densities due to the overdispersion of parasites in previous hosts. As fish grow, the composition of their parasite assemblages becomes homogenized by repeated exposure, with abundance thus arising as the main source of variability. Both variables act at different rates, with the exponential decay in the compositional variability as differences in fish size increase being about twice as steep as the decay in abundance variability, indicating that compositional homogeneity is reached faster than abundance heterogeneity as fish grow. Discerning between both variables is crucial in order to understand how community structure is formed by size-dependent variability of host populations.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Alarcos, A. J. and Timi, J. T. (2012). Parasite communities in three sympatric flounder species (Pleuronectiformes: Paralichthyidae): similar ecological filters driving toward repeatable assemblages. Parasitology Research 110, 21552166. doi: 10.1007/s00436-011-2741-5.CrossRefGoogle ScholarPubMed
Anderson, M. J. (2006). Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62, 245253. doi: 10.1111/j.1541-0420.2005.00440.x.CrossRefGoogle ScholarPubMed
Anderson, M. J., Ellingsen, K. E. and McArdle, B. H. (2006). Multivariate dispersion as a measure of beta diversity. Ecology Letters 9, 683693. doi: 10.1111/j.1461-0248.2006.00926.x.CrossRefGoogle ScholarPubMed
Anderson, M. J., Gorley, R. N. and Clarke, K. R. (2008). PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. Plymouth: PRIMER-E.Google Scholar
Anderson, M. J., Crist, T. O., Chase, J. M., Vellend, M., Inouye, B. D., Freestone, A. L., Sanders, N. J., Cornell, H. V., Comita, L. S., Davies, K. F., Harrison, S. P., Kraft, N. J. B., Stegen, J. C. and Swenson, N. G. (2011). Navigating the multiple meanings of b diversity: a roadmap for the practicing ecologist. Ecology Letters 14, 1928. doi: 10.1111/j.1461-0248.2010.01552.x.CrossRefGoogle Scholar
Braicovich, P. E. and Timi, J. T. (2008). Parasites as biological tags for stock discrimination of the Brazilian flathead Percophis brasiliensis in the South West Atlantic. Journal of Fish Biology 73, 557571. doi: 10.1111/j.1095-8649.2008.01948.x.CrossRefGoogle Scholar
Bush, A. O., Heard, R. W. and Overstreet, R. M. (1993). Intermediate hosts as source communities. Canadian Journal of Zoology 71, 13581363.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, 575583.CrossRefGoogle Scholar
Cousseau, M. B. and Perrotta, R. G. (2004). Peces marinos de Argentina. Biología, distribución, pesca. Publicaciones especiales INIDEP, Mar del Plata, Argentina.Google Scholar
Dogiel, V. A., Petrushevski, G. K. and Polyanski, Y. I. (1958). Parasitology of Fishes. Oliver & Boyd, London. (Translated from Russian by Z. Kabata, 1961.)Google Scholar
Etchegoin, J. A., Lanfranchi, A. L., Cremonte, F. and Timi, J. T. (2006). A new species of Acaenodera (Digenea: Acanthocolpidae) parasitizing Conger orbignyanus (Pisces: Congridae) from Argentina. Parasitology International 55, 291293. doi:10.1016/j.parint.2006.08.003.CrossRefGoogle ScholarPubMed
Figueroa, D. E., Macchi, G. and Haimovici, M. (2010). News about the reproductive ecology of the southern conger eel Conger orbignianus. Journal of the Marine Biological Association of the United Kingdom 90, 461465. doi: 10.1017/S0025315409991135.CrossRefGoogle Scholar
Guégan, J.-F., Lambert, A., Lévêque, C., Combes, C. and Euzet, L. (1992). Can host body size explain the parasite species richness in tropical freshwater fishes? Oecologia 90, 197204. doi: 10.1007/BF00317176.CrossRefGoogle ScholarPubMed
Guégan, J. F., Morand, S. and Poulin, R. (2005). Are there general laws in parasite community ecology? In The Emergence of Spatial Parasitology and Epidemiology (ed. Thomas, F., Renaud, F. and Guégan, J. F.), pp. 2242. Parasitism and Ecosystems. Oxford University Press, Oxford.Google Scholar
Johnson, M. W., Nelson, P. A. and Dick, T. A. (2004). Structuring mechanisms of yellow perch (Perca flavescens) parasite communities: host age, diet, and local factors. Canadian Journal of Zoology 82, 12911301. doi:10.1139/z04-092.CrossRefGoogle Scholar
Luque, J. L. and Poulin, R. (2007). Metazoan parasite species richness in Neotropical fishes: hotspots and the geography of biodiversity. Parasitology 134, 865878. doi:10.1017/S0031182007002272.CrossRefGoogle ScholarPubMed
Luque, J. L. and Poulin, R. (2008) Linking ecology with parasite diversity in Neotropical fishes. Journal of Fish Biology 72, 189204. doi:10.1111/j.1095-8649.2007.01695.x.CrossRefGoogle Scholar
Marcogliese, D. J. (1995). The role of zooplankton in the transmission of helminth parasites to fish. Reviews in Fish Biology and Fisheries 5, 336371.CrossRefGoogle Scholar
Marcogliese, D. J. (2002). Food webs and the transmission of parasites to marine fish. Parasitology 124, 8399. doi:10.1017/S003118200200149X.CrossRefGoogle ScholarPubMed
Pérez-del-Olmo, A., Fernández, M., Raga, J. A., Kostadinova, A. and Poulin, R. (2008). Halfway up the trophic chain: development of parasite communities in the sparid fish Boops boops. Parasitology 135, 257268. doi:10.1017/S0031182007003691.CrossRefGoogle ScholarPubMed
Poulin, R. (2000). Variation in the intraspecific relationship between fish length and intensity of parasitic infection: biological and statistical causes. Journal of Fish Biology 56, 123137.CrossRefGoogle Scholar
Poulin, R. (2004). Macroecological patterns of species richness in parasite assemblages. Basic and Applied Ecology 5, 423434. doi:10.1016/j.baae.2004.08.003.CrossRefGoogle Scholar
Poulin, R. (2007). Are there general laws in parasite ecology? Parasitology 134, 763776. doi:10.1017/S0031182006002150.CrossRefGoogle ScholarPubMed
Poulin, R. and Leung, T. L. F. (2011). Body size, treophic level, and the use of fish as transmission routes by parasites. Oecologia 166, 731738. doi:10.1007/s00442-011-1906-3.CrossRefGoogle ScholarPubMed
Poulin, R. and Valtonen, E. T. (2001). Nested assemblages resulting from host size variation: the case of endoparasite communities in fish hosts. International Journal for Parasitology 31, 11941204.CrossRefGoogle ScholarPubMed
Sardella, N. H. and Timi, J. T. (2004). Parasites of Argentine hake in the Argentine Sea: population and infracommunity structure as evidences for host stock discrimination. Journal of Fish Biology 65, 14721488. doi:10.1111/j.0022-1112.2004.00572.x.CrossRefGoogle Scholar
Tanzola, R. D. and Guagliardo, S. B. (2000). Helminth fauna of the Argentine conger, Conger orbignyanus (Pisces: Anguilliformes). Helminthologia 37, 229232.Google Scholar
Timi, J. T. and Lanfranchi, A. L. (2006). A new species of Cucullanus (Nematoda: Cucullanidae) parasitizing Conger orbignianus (Pisces: Congridae) from Argentinean waters. Journal of Parasitology 92, 151154.CrossRefGoogle ScholarPubMed
Timi, J. T., Luque, J. L. and Poulin, R. (2010). Host ontogeny and the temporal decay of similarity in parasite communities of marine fish. International Journal for Parasitology 40, 963968. doi:10.1016/j.ijpara.2010.02.005.CrossRefGoogle ScholarPubMed
Timi, J. T., Luque, J. L. and Sardella, N. H. (2005). Parasites of Cynoscion guatucupa along South American Atlantic coasts: evidence for stock discrimination. Journal of Fish Biology 67, 16031618. doi:10.1111/j.1095-8649.2005.00867.x.CrossRefGoogle Scholar
Timi, J. T. and Poulin, R. (2003). Parasite community structure within and across host populations of a marine pelagic fish: how repeatable is it? International Journal for Parasitology 33, 13531362. doi:10.1016/S0020-7519(03)00203-0.CrossRefGoogle Scholar
Timi, J. T., Rossin, M. A., Alarcos, A. J., Braicovich, P. E., Cantatore, D. M. P. and Lanfranchi, A. L. (2011). Fish trophic level and the similarity of larval parasite assemblages. International Journal for Parasitology 41, 309316. doi:10.1016/j.ijpara.2010.02.005.CrossRefGoogle ScholarPubMed
Timi, J. T., Rossin, M. A. and Lanfranchi, A. L. (2006). A new species of Capillaria (Nematoda: Capillariidae) parasitizing Conger orbignianus (Pisces: Congridae) from Argentina. Journal of Parasitology 92, 628630.CrossRefGoogle ScholarPubMed
Valtonen, E. T., Marcogliese, D. J. and Julkunen, M. (2010). Vertebrate diets derived from trophically transmitted fish parasites in the Bothnian Bay. Oecologia 162, 139152. doi:10.1007/s00442-009-1451-5.CrossRefGoogle ScholarPubMed
Vidal-Martinez, V. M., Kennedy, C. R. and Aguirre-Macedo, M. L. (1998). The structuring process of the macroparasite community of an experimental population of Cichlasoma urophthalmus through time. Journal of Helminthology 72, 199207. doi:10.1017/S0022149X00016448.CrossRefGoogle ScholarPubMed
Whittaker, R. H. (1960). Vegetation of the Siskiyou Mountains, Oregon and California. Ecological Monographs 22, 144.CrossRefGoogle Scholar
Zar, J. H. (1999). Biostatistical Analysis. 4th Edn. Prentice-Hall Inc., Englewood Cliffs, NJ, USA.Google Scholar