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Are there general laws in parasite ecology?

Published online by Cambridge University Press:  19 January 2007

R. POULIN
R. POULIN*
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
*
*Corresponding author. Tel: +64 3 479 7983. Fax: +64 3 479 7584. E-mail: [email protected]
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Summary

As a scientific discipline matures, its theoretical underpinnings tend to consolidate around a few general laws that explain a wide range of phenomena, and from which can be derived further testable predictions. It is one of the goals of science to uncover the general principles that produce recurring patterns in nature. Although this has happened in many areas of physics and chemistry, ecology is yet to take this important step. Ecological systems are intrinsically complex, but this does not necessarily mean that everything about them is unpredictable or chaotic. Ecologists, whose grand aim is to understand the interactions that govern the distribution, abundance and diversity of living organisms at different scales, have uncovered several regular patterns, i.e. widely observable statistical tendencies, in the abundance or diversity of organisms in natural ecosystems. Some of these patterns, however, are contingent, i.e. they are only true under particular circumstances; nevertheless, the broad generality of many patterns hints at the existence of universal principles. What about parasite ecology: is it also characterized by recurring patterns and general principles? Evidence for repeatable empirical patterns in parasite ecology is reviewed here, in search of patterns that are consistently detectable across taxa or geographical areas. The coverage ranges from the population level all the way to large-scale patterns of parasite diversity and abundance (or biomass) and patterns in the structure of host-parasite interaction networks. Although general laws seem to apply to these extreme scales of studies, most patterns observed at the intermediate scale, i.e. the parasite community level, appear highly contingent and far from universal. The general laws uncovered to date are proving valuable, as they offer glimpses of the underlying processes shaping parasite ecology and diversity.

Keywords

aggregationbiomasscontingencyinteraction networksmacroecologymetabolismscalespecies richness
Type
Research Article
Information
Parasitology , Volume 134 , Issue 6 , June 2007 , pp. 763 - 776
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Allen, A. P., Brown, J. H. and Gillooly, J. F. (2002). Global biodiversity, biochemical kinetics, and the energy equivalence rule. Science 297, 1545–1548.CrossRefGoogle Scholar
Anderson, R. M. (1993). Epidemiology. In Modern Parasitology, 2nd Edn (ed. Cox, F. E. G.), pp. 75–116. Blackwell, Oxford.CrossRefGoogle Scholar
Anderson, T. J. C., Blouin, M. S. and Beech, R. N. (1998). Population biology of parasitic nematodes: applications of genetic markers. Advances in Parasitology 41, 219–283.CrossRefGoogle ScholarPubMed
Barker, D. E., Marcogliese, D. J. and Cone, D. K. (1996). On the distribution and abundance of eel parasites in Nova Scotia: local versus regional patterns. Journal of Parasitology 82, 697–701.CrossRefGoogle ScholarPubMed
Bascompte, J., Jordano, P., Melián, C. J. and Olesen, J. M. (2003). The nested assembly of plant-animal mutualistic networks. Proceedings of the National Academy of Sciences, USA 100, 9383–9387.CrossRefGoogle ScholarPubMed
Blouin, M. S., Yowell, C. A., Courtney, C. H. and Dame, J. B. (1995). Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141, 1007–1014.CrossRefGoogle ScholarPubMed
Brown, J. H. (1995). Macroecology. University of Chicago Press, Chicago.Google Scholar
Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. and West, G. B. (2004). Toward a metabolic theory of ecology. Ecology 85, 1771–1789.CrossRefGoogle Scholar
Bush, A. O. and Holmes, J. C. (1986). Intestinal helminths of lesser scaup ducks: patterns of association. Canadian Journal of Zoology 64, 132–141.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
Calvete, C., Blanco-Aguiar, J. A., Virgos, E., Cabezas-Diaz, S. and Villafuerte, R. (2004). Spatial variation in helminth community structure in the red-legged partridge (Alectoris rufa L.): effects of definitive host density. Parasitology 129, 101–113.CrossRefGoogle Scholar
Carney, J. P. and Dick, T. A. (2000). Helminth communities of yellow perch (Perca flavescens (Mitchill)): determinants of pattern. Canadian Journal of Zoology 78, 538–555.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
Cone, D. K., Marcogliese, D. J., Barse, A. M. and Burt, M. D. B. (2006). The myxozoan fauna of Fundulus diaphanus (Cyprinodontidae) from freshwater localities in eastern North America: Prevalence, community structure, and geographic distribution. Journal of Parasitology 92, 52–57.CrossRefGoogle ScholarPubMed
Cornell, H. V. and Lawton, J. H. (1992). Species interactions, local and regional processes, and limits to the richness of ecological communities: a theoretical perspective. Journal of Animal Ecology 61, 1–12.CrossRefGoogle Scholar
Criscione, C. D. and Blouin, M. S. (2004). Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evolution 58, 198–202.Google ScholarPubMed
Crofton, H. D. (1971). A quantitative approach to parasitism. Parasitology 62, 179–193.CrossRefGoogle Scholar
Diekmann, O. and Heesterbeek, J. A. P. (2000). Mathematical Epidemiology of Infectious Diseases: Model Building, Analysis and Interpretation. John Wiley and Sons, Chichester, NY.Google Scholar
Dobson, A. P. and Roberts, M. (1994). The population dynamics of parasitic helminth communities. Parasitology 109, S97–S108.CrossRefGoogle ScholarPubMed
Dove, A. D. M. (2006). Defining parasite communities is a challenge for neutral theory. Journal of Parasitology 92, 673–675.CrossRefGoogle ScholarPubMed
Fellis, K. J. and Esch, G. W. (2005). Autogenic-allogenic status affects interpond community similarity and species-area relationship of macroparasites in the bluegill sunfish, Lepomis macrochirus, from a series of freshwater ponds in the Piedmont area of North Carolina. Journal of Parasitology 91, 764–767.CrossRefGoogle ScholarPubMed
Gaston, K. J. and Blackburn, T. M. (2000). Pattern and Process in Macroecology. Blackwell Science, Oxford.CrossRefGoogle Scholar
George-Nascimento, M., Muñoz, G., Marquet, P. A. and Poulin, R. (2004). Testing the energetic equivalence rule with helminth endoparasites of vertebrates. Ecology Letters 7, 527–531.CrossRefGoogle Scholar
Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. and Charnov, E. L. (2001). Effects of size and temperature on metabolic rate. Science 293, 2248–2251.CrossRefGoogle ScholarPubMed
González, M. T. and Poulin, R. (2005). Nested patterns in parasite component communities of a marine fish along its latitudinal range on the Pacific coast of South America. Parasitology 131, 569–577.CrossRefGoogle ScholarPubMed
Gotelli, N. J. and Graves, G. R. (1996). Null Models in Ecology. Smithsonian Institution Press, Washington, DC.Google Scholar
Gotelli, N. J. and Rohde, K. (2002). Co-occurrence of ectoparasites of marine fishes: a null model analysis. Ecology Letters 5, 86–94.CrossRefGoogle Scholar
Guégan, J.-F. and Hugueny, B. (1994). A nested parasite species subset pattern in tropical fish: host as major determinant of parasite infracommunity structure. Oecologia 100, 184–189.CrossRefGoogle ScholarPubMed
Guégan, J.-F., Morand, S. and Poulin, R. (2005). Are there general laws in parasite community ecology? The emergence of spatial parasitology and epidemiology. In Parasitism and Ecosystems (ed. Thomas, F., Renaud, F. and Guégan, J.-F.), pp. 22–42. Oxford University Press, Oxford.CrossRefGoogle Scholar
Hanski, I. (1982). Dynamics of regional distribution: the core and satellite species hypothesis. Oikos 38, 210–221.CrossRefGoogle Scholar
Hanski, I. and Gilpin, M. E. (1997). Metapopulation Biology: Ecology, Genetics and Evolution. Academic Press, London.Google Scholar
Hillebrand, H. (2005). Regressions of local on regional diversity do not reflect the importance of local interactions or saturation of local diversity. Oikos 110, 195–198.CrossRefGoogle Scholar
Holmes, J. C. and Price, P. W. (1986). Communities of parasites. In Community Ecology: Pattern and Process (ed. Anderson, D. J. and Kikkawa, J.), pp. 187–213. Blackwell Scientific Publications, Oxford.Google Scholar
Karvonen, A. and Valtonen, E. T. (2004). Helminth assemblages of whitefish (Coregonus lavaretus) in interconnected lakes: similarity as a function of species-specific parasites and geographical separation. Journal of Parasitology 90, 471–476.CrossRefGoogle ScholarPubMed
Kauffman, S. A. (1993). The Origins of Order: Self-organization and Selection in Evolution. Oxford University Press, Oxford.CrossRefGoogle Scholar
Kennedy, C. R. and Guégan, J.-F. (1996). The number of niches in intestinal helminth communities of Anguilla anguilla: are there enough spaces for parasites? Parasitology 113, 293–302.CrossRefGoogle Scholar
Krasnov, B. R., Shenbrot, G. I., Mouillot, D., Khokhlova, I. S. and Poulin, R. (2005). Spatial variation in species diversity and composition of flea assemblages in small mammalian hosts: geographical distance or faunal similarity? Journal of Biogeography 32, 633–644.CrossRefGoogle Scholar
Krasnov, B. R., Stanko, M., Khokhlova, I. S., Miklisova, D., Morand, S., Shenbrot, G. I. and Poulin, R. (2006). Relationships between local and regional species richness in flea communities of small mammalian hosts: saturation and spatial scale. Parasitology Research 98, 403–413.CrossRefGoogle ScholarPubMed
Kuris, A. M., Blaustein, A. R. and Alió, J. J. (1980). Hosts as islands. American Naturalist 116, 570–586.CrossRefGoogle Scholar
Lawton, J. H. (1999). Are there general laws in ecology? Oikos 84, 177–192.CrossRefGoogle Scholar
MacArthur, R. H. and Wilson, E. O. (1967). The Theory of Island Biogeography. Princeton University Press, Princeton.Google Scholar
McCoy, K. D., Boulinier, T., Tirard, C. and Michalakis, Y. (2003). Host-dependent genetic structure of parasite populations: differential dispersal of seabird tick host races. Evolution 57, 288–296.Google ScholarPubMed
Morand, S. (2000). Wormy world: comparative tests of theoretical hypotheses on parasite species richness. In Evolutionary Biology of Host-Parasite Relationships: Theory Meets Reality (ed. Poulin, R., Morand, S. and Skorping, A.), pp. 63–79. Elsevier Science, Amsterdam.Google Scholar
Morand, S. and Guégan, J.-F. (2000). Distribution and abundance of parasite nematodes: ecological specialisation, phylogenetic constraint or simply epidemiology? Oikos 88, 563–573.CrossRefGoogle Scholar
Mouillot, D., George-Nascimento, M. and Poulin, R. (2003). How parasites divide resources: a test of the niche apportionment hypothesis. Journal of Animal Ecology 72, 757–764.CrossRefGoogle Scholar
Muñoz, G., Mouillot, D. and Poulin, R. (2006). Testing the niche apportionment hypothesis with parasite communities: is random assortment always the rule? Parasitology 132, 717–724.CrossRefGoogle ScholarPubMed
Nekola, J. C. and White, P. S. (1999). The distance decay of similarity in biogeography and ecology. Journal of Biogeography 26, 867–878.CrossRefGoogle Scholar
Norton, J., Lewis, J. W. and Rollinson, D. (2004 a). Temporal and spatial patterns of nestedness in eel macroparasite communities. Parasitology 129, 203–211.CrossRefGoogle ScholarPubMed
Norton, J., Rollinson, D. and Lewis, J. W. (2004 b). Patterns of infracommunity species richness in eels, Anguilla anguilla. Journal of Helminthology 78, 141–146.CrossRefGoogle ScholarPubMed
Oliva, M. E. and González, M. T. (2005). The decay of similarity over geographical distance in parasite communities of marine fishes. Journal of Biogeography 32, 1327–1332.CrossRefGoogle Scholar
Paterson, A. M. and Gray, R. D. (1997). Host-parasite cospeciation, host switching and missing the boat. In Host-Parasite Evolution: General Principles and Avian Models (ed. Clayton, D. H. and Moore, J.), pp. 236–250. Oxford University Press, Oxford.CrossRefGoogle Scholar
Patterson, B. D. and Atmar, W. (1986). Nested subsets and the structure of insular mammalian faunas and archipelagos. Biological Journal of the Linnean Society 28, 65–82.CrossRefGoogle Scholar
Peters, R. H. (1991). A Critique for Ecology. Cambridge University Press, Cambridge.Google Scholar
Pickett, S. T. A., Kolasa, J. and Jones, C. G. (1994). Ecological Understanding. Academic Press, San Diego.CrossRefGoogle Scholar
Poulin, R. (1996). Richness, nestedness, and randomness in parasite infracommunity structure. Oecologia 105, 545–551.CrossRefGoogle ScholarPubMed
Poulin, R. (1997). Species richness of parasite assemblages: evolution and patterns. Annual Review of Ecology and Systematics 28, 341–358.CrossRefGoogle Scholar
Poulin, R. (2001). Another look at the richness of helminth communities in tropipcal freshwater fish. Journal of Biogeography 28, 737–743.CrossRefGoogle Scholar
Poulin, R. (2003). The decay of similarity with geographical distance in parasite communities of vertebrate hosts. Journal of Biogeography 30, 1609–1615.CrossRefGoogle Scholar
Poulin, R. (2004). Macroecological patterns of species richness in parasite assemblages. Basic and Applied Ecology 5, 423–434.CrossRefGoogle Scholar
Poulin, R. (2005). Structure of parasite communities. In Marine Parasitology (ed. Rohde, K.), pp. 309–315. CABI Publishing, Wallingford, UK.Google Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn. Princeton University Press, Princeton.CrossRefGoogle Scholar
Poulin, R. and George-Nascimento, M. (2007). The scaling of total parasite biomass with host body mass. International Journal for Parasitology (in the Press).CrossRefGoogle ScholarPubMed
Poulin, R. and Guégan, J.-F. (2000). Nestedness, anti-nestedness, and the relationship between prevalence and intensity in ectoparasite assemblages of marine fish: a spatial model of species coexistence. International Journal for Parasitology 30, 1147–1152.CrossRefGoogle Scholar
Poulin, R. and Luque, J. L. (2003). A general test of the interactive-isolationist continuum in gastrointestinal parasite communities of fish. International Journal for Parasitology 33, 1623–1630.CrossRefGoogle ScholarPubMed
Poulin, R. and Morand, S. (1999). Geographical distances and the similarity among parasite communities of conspecific host populations. Parasitology 119, 369–374.CrossRefGoogle ScholarPubMed
Poulin, R. and Morand, S. (2004). Parasite Biodiversity. Smithsonian Institution Press, Washington, DC.Google Scholar
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, 1194–1204.CrossRefGoogle ScholarPubMed
Poulin, R. and Valtonen, E. T. (2002). The predictability of helminth community structure in space: a comparison of fish populations from adjacent lakes. International Journal for Parasitology 32, 1235–1243.CrossRefGoogle ScholarPubMed
Roberts, M. G., Dobson, A. P., Arneberg, P., de Leo, G. A., Krecek, R. C., Manfredi, M. T., Lanfranchi, P. and Zaffaroni, E. (2002). Parasite community ecology and biodiversity. In The Ecology of Wildlife Diseases (ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), pp. 63–82. Oxford University Press, Oxford.CrossRefGoogle Scholar
Rohde, K. (1992). Latitudinal gradients in species diversity: the search for the primary cause. Oikos 65, 514–527.CrossRefGoogle Scholar
Rohde, K. (2005). Nonequilibrium Ecology. Cambridge University Press, Cambridge.Google Scholar
Rohde, K. and Heap, M. (1998). Latitudinal differences in species and community richness and in community structure of metazoan endo- and ectoparasites of marine teleost fish. International Journal for Parasitology 28, 461–474.CrossRefGoogle ScholarPubMed
Rohde, K., Worthen, W. B., Heap, M., Hugueny, B. and Guégan, J.-F. (1998). Nestedness in assemblages of metazoan ecto- and endoparasites of marine fish. International Journal for Parasitology 28, 543–549.CrossRefGoogle ScholarPubMed
Rosenzweig, M. L. (1995). Species Diversity in Space and Time. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Savage, V. M., Gillooly, J. F., Woodruff, W. H., West, G. B., Allen, A. P., Enquist, B. J. and Brown, J. H. (2004). The predominance of quarter-power scaling in biology. Functional Ecology 18, 257–282.CrossRefGoogle Scholar
Shaw, D. J. and Dobson, A. P. (1995). Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111, S111–S133.CrossRefGoogle ScholarPubMed
Simberloff, D. (2004). Community ecology: is it time to move on? American Naturalist 163, 787–799.CrossRefGoogle ScholarPubMed
Srivastava, D. S. (1999). Using local–regional richness plots to test for species saturation: pitfalls and potentials. Journal of Animal Ecology 68, 1–16.CrossRefGoogle Scholar
Storch, D. and Gaston, K. J. (2004). Untangling ecological complexity on different scales of space and time. Basic and Applied Ecology 5, 389–400.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, 1353–1362.CrossRefGoogle Scholar
Vázquez, D. P. and Aizen, M. A. (2003). Null model analyses of specialization in plant-pollinator interactions. Ecology 84, 2493–2501.CrossRefGoogle Scholar
Vázquez, D. P., Poulin, R., Krasnov, B. R. and Shenbrot, G. I. (2005). Species abundance and the distribution of specialization in host-parasite interaction networks. Journal of Animal Ecology 74, 946–955.CrossRefGoogle Scholar
Vickery, W. L. and Poulin, R. (1998). Parasite extinction and colonization and the evolution of parasite communities: a simulation study. International Journal for Parasitology 28, 727–737.CrossRefGoogle ScholarPubMed
Vidal-Martinez, V. M. and Poulin, R. (2003). Spatial and temporal repeatability in parasite community structure of tropical fish hosts. Parasitology 127, 387–398.CrossRefGoogle ScholarPubMed
Wilson, K., Bjørnstad, O. N., Dobson, A. P., Merler, S., Poglayen, G., Randolph, S. E., Read, A. F. and Skorping, A. (2002). Heterogeneities in macroparasite infections: patterns and processes. In The Ecology of Wildlife Diseases (ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), pp. 6–44. Oxford University Press, Oxford.CrossRefGoogle Scholar
Worthen, W. B. (1996). Community composition and nested-subset analyses: basic descriptors for community ecology. Oikos 76, 417–426.CrossRefGoogle Scholar
Worthen, W. B. and Rohde, K. (1996). Nested subset analyses of colonization-dominated communities: metazoan ectoparasites of marine fishes. Oikos 75, 471–478.CrossRefGoogle Scholar
Wright, D. H., Patterson, B. D., Mikkelson, G. M., Cutler, A. and Atmar, W. (1998). A comparative analysis of nested subset patterns of species composition. Oecologia 113, 1–20.CrossRefGoogle Scholar
Zelmer, D. A. and Arai, H. P. (2004). Development of nestedness: host biology as a community process in parasite infracommunities of yellow perch (Perca flavescens (Mitchill)) from Garner Lake, Alberta. Journal of Parasitology 90, 435–436.CrossRefGoogle ScholarPubMed