Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-20T03:33:13.527Z Has data issue: false hasContentIssue false

Explaining variability in parasite aggregation levels among host samples

Published online by Cambridge University Press:  24 January 2013

ROBERT POULIN*
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand
*
*Corresponding author: Tel: +64 3 479 7983. Fax: +64 3 479 7584. E-mail: robert.poulin@otago.ac.nz

Summary

Aggregated distributions among individual hosts are a defining feature of metazoan parasite populations. Heterogeneity among host individuals in exposure to parasites or in susceptibility to infection is thought to be the main factor generating aggregation, with properties of parasites themselves explaining some of the variability in aggregation levels observed among species. Here, using data from 410 samples of helminth parasites on fish hosts, I tested the contribution of (i) within-sample variation in host body size, taken as a proxy for variability in host susceptibility, and (ii) parasite taxon and developmental stage, to the aggregated distribution of parasites. Log-transformed variance in numbers of parasites per host was regressed against log mean number across all samples; the strong relationship (r2 = 0·88) indicated that aggregation levels are tightly constrained by mean infection levels, and that only a small proportion of the observed variability in parasite aggregation levels remains to be accounted for by other factors. Using the residuals of this regression as measures of ‘unexplained’ aggregation, a mixed effects model revealed no significant effect of within-sample variation in host body size or of parasite taxon or stage (i.e. juvenile versus adult) on parasite aggregation level within a sample. However, much of the remaining variability in parasite aggregation levels among samples was accounted for by the number of individual hosts examined per sample, and species-specific and study-specific effects reflecting idiosyncrasies of particular systems. This suggests that with most differences in aggregation among samples already explained, there may be little point in seeking universal causes for the remaining variation.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Anderson, R. M. and Gordon, D. M. (1982). Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85, 373398.CrossRefGoogle ScholarPubMed
Bandilla, M., Hakalahti, T., Hudson, P. J. and Valtonen, E. T. (2005). Aggregation of Argulus coregoni (Crustacea: Branchiura) on rainbow trout (Oncorhynchus mykiss): a consequence of host susceptibility or exposure? Parasitology 130, 169176.CrossRefGoogle ScholarPubMed
Crofton, H. D. (1971). A quantitative approach to parasitism. Parasitology 62, 179193.CrossRefGoogle Scholar
Elston, D. A., Moss, R., Boulinier, T., Arrowsmith, C. and Lambin, X. (2001). Analysis of aggregation, a worked example: numbers of ticks on red grouse chicks. Parasitology 122, 563569.CrossRefGoogle ScholarPubMed
Galvani, A. P. (2003). Immunity, antigenic heterogeneity, and aggregation of helminth parasites. Journal of Parasitology 89, 232241.CrossRefGoogle ScholarPubMed
Gregory, R. D. and Woolhouse, M. E. J. (1993). Quantification of parasite aggregation: a simulation study. Acta Tropica 54, 131139.CrossRefGoogle ScholarPubMed
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 fish. Marine Ecology Progress Series 164, 263271.CrossRefGoogle Scholar
Hansen, F., Jeltsch, F., Tackmann, K., Staubach, C. and Thulke, H.-H. (2004). Processes leading to a spatial aggregation of Echinococcus multilocularis in its natural intermediate host Microtus arvalis. International Journal for Parasitology 34, 3744.CrossRefGoogle ScholarPubMed
Janovy, J. Jr. and Kutish, G. W. (1988). A model of encounters between host and parasite populations. Journal of Theoretical Biology 134, 391401.CrossRefGoogle Scholar
Karvonen, A., Hudson, P. J., Seppälä, O. and Valtonen, E. T. (2004). Transmission dynamics of a trematode parasite: exposure, acquired resistance and parasite aggregation. Parasitology Research 92, 183188.CrossRefGoogle ScholarPubMed
Keymer, A. E. and Anderson, R. M. (1979). The dynamics of infection of Tribolium confusum by Hymenolepis diminuta: the influence of infective-stage density and spatial distribution. Parasitology 79, 195207.CrossRefGoogle ScholarPubMed
Knudsen, R., Curtis, M. A. and Kristoffersen, R. (2004). Aggregation of helminths: the role of feeding behavior of fish hosts. Journal of Parasitology 90, 17.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Stanko, M., Miklisova, D. and Morand, S. (2006). Host specificity, parasite community size and the relation between abundance and its variance. Evolutionary Ecology 20, 7591.CrossRefGoogle Scholar
Lester, R. J. G. (2012). Overdispersion in marine fish parasites. Journal of Parasitology 98, 718721.CrossRefGoogle ScholarPubMed
Leung, B. (1998). Aggregated parasite distributions on hosts in a homogeneous environment: examining the Poisson null model. International Journal for Parasitology 28, 17091712.CrossRefGoogle Scholar
Lysne, D. A. and Skorping, A. (2002). The parasite Lernaeocera branchialis on caged cod: infection pattern is caused by differences in host susceptibility. Parasitology 124, 6976.CrossRefGoogle ScholarPubMed
Morand, S. and Krasnov, B. (2008). Why apply ecological laws to epidemiology? Trends in Parasitology 24, 304309.CrossRefGoogle ScholarPubMed
Morrill, A. and Forbes, M. R. (2012). Random parasite encounters coupled with condition-linked immunity of hosts generate parasite aggregation. International Journal for Parasitology 42, 701706.CrossRefGoogle ScholarPubMed
Pérez-del-Olmo, A., Morand, S., Raga, J. A. and Kostadinova, A. (2011). Abundance–variance and abundance–occupancy relationships in a marine host–parasite system: the importance of taxonomy and ecology of transmission. International Journal for Parasitology 41, 13611370.CrossRefGoogle Scholar
Poulin, R. (1993). The disparity between observed and uniform distributions: a new look at parasite aggregation. International Journal for Parasitology 23, 937944.CrossRefGoogle Scholar
Poulin, R. (1996). Measuring parasite aggregation: defending the index of discrepancy. International Journal for Parasitology 26, 227229.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. (2007). Are there general laws in parasite ecology? Parasitology 134, 763776.CrossRefGoogle ScholarPubMed
Poulin, R. and Morand, S. (2000). Parasite body size and interspecific variation in levels of aggregation among nematodes. Journal of Parasitology 86, 642647.CrossRefGoogle ScholarPubMed
Poulin, R., Rau, M. E. and Curtis, M. A. (1991). Infection of brook trout fry, Salvelinus fontinalis, by ectoparasitic copepods: the role of host behaviour and initial parasite load. Animal Behaviour 41, 467476.CrossRefGoogle Scholar
Shaw, D. J. and Dobson, A. P. (1995). Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111, S111S133.CrossRefGoogle ScholarPubMed