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Interactions between species and the structure of helminth communities

Published online by Cambridge University Press:  24 October 2011

R. POULIN
R. POULIN
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand
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Abstract

The role of interspecific interactions in the structure of gastrointestinal helminth communities has been at the core of most research in parasite community ecology, yet there is no consensus regarding their general importance. There have been two different approaches to the study of species interactions in helminths. The first one consists of measuring the responses of helminth species in concomitant infections, preferably in laboratory experiments. Any change in numbers of parasite individuals or in their use of niche space, compared with what is observed in single infections, provides solid evidence that the species are interacting. The second approach can only provide indirect, circumstantial evidence. It consists in contrasting observed patterns either in the distribution of species richness of infracommunities from wild hosts, in their species composition, or in pairwise associations between helminth species among infracommunities, with the random patterns predicted by appropriate null models. In many cases, observed patterns do not depart from predicted ones; when they do, alternative explanations are usually as plausible as invoking the effect of interactions among helminth species. The present evidence suggests that the role of species interactions in helminth community structure is often negligible, but that it must always be evaluated on a case-by-case basis.

Keywords

Competitionexclusionnestednessniche segregationspecies richnesssaturation
Type
Research Article
Information
Parasitology , Volume 122 , Supplement S1 , March 2001 , pp. S3 - S11
Copyright
© 2002 Cambridge University Press

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References

ANDERSEN, K. I. & VALTONEN, E. T. (1990). On the infracommunity structure of adult cestodes in freshwater fishes. Parasitology 101, 257–264.CrossRefGoogle Scholar
BARGER, M. A. & NICKOL, B. B. (1999). Effects of coinfection with Pomphorhynchus bulbocolli on development of Leptorhynchoides thecatus (Acanthocephala) in amphipods (Hyalella azteca). Journal of Parasitology 85, 60–63.CrossRefGoogle Scholar
BUSH, A. O., HEARD, R. W. & OVERSTREET, R. M. (1993). Intermediate hosts as source communities. Canadian Journal of Zoology 71, 1358–1363.CrossRefGoogle Scholar
BUSH, A. O. & HOLMES, J. C. (1986a). Intestinal helminths of lesser scaup ducks: patterns of association. Canadian Journal of Zoology 64, 132–141.Google Scholar
BUSH, A. O. & HOLMES, J. C. (1986b). Intestinal helminths of lesser scaup ducks: an interactive community. Canadian Journal of Zoology 64, 142–152.Google Scholar
BUSH, A. O., LAFFERTY, K. D., LOTZ, J. M. & SHOSTAK, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
CONNELL, J. H. (1980). Diversity and the coevolution of competitors, or the ghost of competition past. Oikos 35, 131–138.CrossRefGoogle Scholar
CORNELL, H. V. & 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
CURTIS, L. A. (1997). Ilyanassa obsoleta (Gastropoda) as a host for trematodes in Delaware estuaries. Journal of Parasitology 83, 793–803.CrossRefGoogle Scholar
CURTIS, L. A. & HUBBARD, K. M. K. (1993). Species relationships in a marine gastropod-trematode ecological system. Biological Bulletin 184, 25–35.CrossRefGoogle Scholar
DASH, K. M. (1981). Interaction between Oesophagostomum columbianum and Oesophagostomum venulosum in sheep. International Journal for Parasitology 11, 201–207.CrossRefGoogle Scholar
DOBSON, A. P. (1985). The population dynamics of competition between parasites. Parasitology 92, 675–682.CrossRefGoogle Scholar
DOBSON, A. P. & ROBERTS, M. (1994). The population dynamics of parasitic helminth communities. Parasitology 109, S97–S108.CrossRefGoogle Scholar
DOVE, A. D. M. (1999). A new index of interactivity in parasite communities. International Journal for Parasitology 29, 915–920.CrossRefGoogle Scholar
ELLIS, R. D., PUNG, O. J. & RICHARDSON, D. J. (1999). Site selection by intestinal helminths of the Virginia opossum (Didelphis virginiana). Journal of Parasitology 85, 1–5.CrossRefGoogle Scholar
ESCH, G. W., BUSH, A. O. & AHO, J. M. (1990). Parasite Communities: Patterns and Processes. London, Chapman & Hall.
ESCH, G. W., WETZEL, E. J., ZELMER, D. A. & SCHOTTHOEFER, A. M. (1997). Long-term changes in parasite population and community structure: a case history. American Midland Naturalist 137, 369–387.CrossRefGoogle Scholar
FORBES, M. R., ALISAUSKAS, R. T., MCLAUGHLIN, J. D. & CUDDINGTON, K. M. (1999). Explaining co-occurrence among helminth species of lesser snow geese (Chen caerulescens) during their winter and spring migration. Oecologia 120, 613–620.CrossRefGoogle Scholar
GORDON, D. M. & WHITFIELD, P. J. (1985). Interactions of the cysticercoids of Hymenolepis diminuta and Raillietina cesticillus in their intermediate host, Tribolium confusum. Parasitology 90, 421–431.CrossRefGoogle Scholar
GOTELLI, N. J. & GRAVES, G. R. (1996). Null Models in Ecology. Washington, D.C., Smithsonian Institution Press.
GUÉGAN, J.-F. & 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 Scholar
HAUKISALMI, V. & HENTTONEN, H. (1993a). Coexistence in helminths of the bank vole Clethrionomys glareolus. I. Patterns of co-occurrence. Journal of Animal Ecology 62, 221–229.Google Scholar
HAUKISALMI, V. & HENTTONEN, H. (1993b). Coexistence in helminths of the bank vole Clethrionomys glareolus. II. Intestinal distribution and interspecific interactions. Journal of Animal Ecology 62, 230–238.Google Scholar
HAUKISALMI, V. & HENTTONEN, H. (1998). Analysing interspecific associations in parasites: alternative methods and effects of sampling heterogeneity. Oecologia 116, 565–574.CrossRefGoogle Scholar
HOLLAND, C. (1984). Interactions between Moniliformis (Acanthocephala) and Nippostrongylus (Nematoda) in the small intestine of laboratory rats. Parasitology 88, 303–315.Google Scholar
HOLMES, J. C. (1961). Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). I. General effects and comparison with crowding. Journal of Parasitology 47, 209–216.Google Scholar
HOLMES, J. C. (1973). Site segregation by parasitic helminths: interspecific interactions, site segregation, and their importance to the development of helminth communities. Canadian Journal of Zoology 51, 333–347.CrossRefGoogle Scholar
HOLMES, J. C. & PRICE, P. W. (1986). Communities of parasites. In Community Ecology: Pattern and Process (ed. ANDERSON, D. J. & KIKKAWA, J.), pp. 187–213. Oxford, Blackwell Scientific Publications.
JANOVY, J. JR., CLOPTON, R. E., CLOPTON, D. A., SNYDER, S. D., EFTING, A. & KREBS, L. (1995). Species density distributions as null models for ecologically significant interactions of parasite species in an assemblage. Ecological Modelling 77, 189–196.CrossRefGoogle Scholar
KENNEDY, C. R., BUSH, A. O. & AHO, J. M. (1986). Patterns in helminth communities: why are birds and fish so different? Parasitology 93, 205–215.Google Scholar
KENNEDY, C. R. & 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.Google Scholar
KURIS, A. M. & LAFFERTY, K. D. (1994). Community structure: larval trematodes in snail hosts. Annual Review of Ecology and Systematics 25, 189–217.CrossRefGoogle Scholar
LAFFERTY, K. D. (1999). The evolution of trophic transmission. Parasitology Today 15, 111–115.CrossRefGoogle Scholar
LAFFERTY, K. D., THOMAS, F. & POULIN, R. (2000). Evolution of host phenotype manipulation by parasites and its consequences. In Evolutionary Biology of Host-Parasite Relationships: Theory Meets Reality (ed. Poulin, R., Morand, S. & Skorping, A.), pp. 117–127. Amsterdam, Elsevier Science Publishers.
LOTZ, J. M., BUSH, A. O. & FONT, W. F. (1995). Recruitment-driven, spatially discontinuous communities: a null model for transferred patterns in target communities of intestinal helminths. Journal of Parasitology 81, 12–24.CrossRefGoogle Scholar
LOTZ, J. M. & FONT, W. F. (1991). The role of positive and negative interspecific associations in the organization of communities of intestinal helminths of bats. Parasitology 103, 127–138.CrossRefGoogle Scholar
LOTZ, J. M. & FONT, W. F. (1994). Excess positive associations in communities of intestinal helminths of bats: a refined null hypothesis and a test of the facilitation hypothesis. Journal of Parasitology 80, 398–413.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, 336–371.CrossRefGoogle Scholar
MOORE, J. & SIMBERLOFF, D. (1990). Gastrointestinal helminth communities of bobwhite quail. Ecology 71, 344–359.CrossRefGoogle Scholar
MORAND, S., POULIN, R., ROHDE, K. & HAYWARD, C. (1999). Aggregation and species coexistence of ectoparasites of marine fishes. International Journal for Parasitology 29, 663–672.CrossRefGoogle Scholar
PATRICK, M. J. (1991). Distribution of enteric helminths in Glaucomys volans L. (Sciuridae): a test for competition. Ecology 72, 755–758.Google Scholar
PATTERSON, B. D. & 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
POULIN, R. (1996). Richness, nestedness, and randomness in parasite infracommunity structure. Oecologia 105, 545–551.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. (1998). Evolutionary Ecology of Parasites: From Individuals to Communities. London, Chapman & Hall.
POULIN, R., GUÉGAN, J.-F. (in press). 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.
ROHDE, K. (1991). Intra- and interspecific interactions in low density populations in resource-rich habitats. Oikos 60, 91–104.CrossRefGoogle Scholar
ROHDE, K. (1994). Niche restriction in parasites: proximate and ultimate causes. Parasitology 109, S69–S84.CrossRefGoogle Scholar
ROHDE, K. (1998). Is there a fixed number of niches for endoparasites of fish? International Journal for Parasitology 28, 1861–1865.Google Scholar
ROHDE, K., WORTHEN, W. B., HEAP, M., HUGUENY, B. & GUÉGAN, J.-F. (1998). Nestedness in assemblages of metazoan ecto- and endoparasites of marine fish. International Journal for Parasitology 28, 543–549.CrossRefGoogle Scholar
SHAW, D. J. & DOBSON, A. P. (1995). Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111, S111–S133.CrossRefGoogle Scholar
SILVER, B. B., DICK, T. A. & WELCH, H. E. (1980). Concurrent infections of Hymenolepis diminuta and Trichinella spiralis in the rat intestine. Journal of Parasitology 66, 786–791.CrossRefGoogle Scholar
SIMBERLOFF, D. & MOORE, J. (1997). Community ecology of parasites and free-living animals. In Host-Parasite Evolution: General Principles and Avian Models (ed. CLAYTON, D. H. & MOORE, J.), pp. 174–197. Oxford, Oxford University Press.
SOUSA, W. P. (1992). Interspecific interactions among larval trematode parasites of freshwater and marine snails. American Zoologist 32, 583–592.CrossRefGoogle Scholar
SOUSA, W. P. (1993). Interspecific antagonism and species coexistence in a diverse guild of larval trematode parasites. Ecological Monographs 63, 103–128.CrossRefGoogle Scholar
SOUSA, W. P. (1994). Patterns and processes in communities of helminth parasites. Trends in Ecology & Evolution 9, 52–57.CrossRefGoogle Scholar
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
STOCK, T. M. & HOLMES, J. C. (1988). Functional relationships and microhabitat distributions of enteric helminths of grebes (Podicipedidae): the evidence for interactive communities. Journal of Parasitology 74, 214–227.CrossRefGoogle Scholar
SUKHDEO, M. V. K. (1991). The relationship between intestinal location and fecundity in adult Trichinella spiralis. International Journal for Parasitology 21, 855–858.CrossRefGoogle Scholar
THOMAS, F., RENAUD, F. & POULIN, R. (1998). Exploitation of manipulators: ‘hitch-hiking' as a parasite transmission strategy. Animal Behaviour 56, 199–206.CrossRefGoogle Scholar
THOMSON, J. D. (1980). Implications of different sorts of evidence for competition. American Naturalist 116, 719–726.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. & 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. & ATMAR, W. (1998). A comparative analysis of nested subset patterns of species composition. Oecologia 113, 1–20.Google Scholar