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The dynamics of macroparasite host-self-infection: a study of the patterns and processes of pinworm (Oxyuridae) aggregation

Published online by Cambridge University Press:  24 February 2011

DANIEL A. GREAR  and
PETER HUDSON
DANIEL A. GREAR*
Affiliation:
Center for Infectious Disease Dynamics, Pennsylvania State University, 208 Mueller Laboratory, University Park, PA 16802, USA
PETER HUDSON
Affiliation:
Huck Institute of the Life Sciences, Pennsylvania State University, 201 Life Sciences, University Park, PA 16802, USA
*
*Corresponding author: Center for Infectious Disease Dynamics, 208 Mueller Laboratory, Pennsylvania State University, University Park, PA 16802, USA. Tel: +1 814 863 5895. Fax: +1 814 865 9131. E-mail: [email protected]
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Summary

Objectives. Among parasites, Taylor's power law identifies a tight relationship in aggregation of macroparasite infection intensity with few exceptions; notably, the nematode family Oxyuridae tends to have higher than expected aggregation. Oxyuridae infect a wide range of mammalian hosts and have a unique reproductive strategy that involves conventional horizontal transmission, as well as re-infection of an already infected host. We asked the question, do the unique aspects of pinworm life-history explain an exception to the widely observed patterns of aggregation of parasite populations? Methods. We empirically examined the differences among Oxyuridae (genus: Syphacia) compared with other helminth (genus: Heligmosomoides) parasite aggregations in 2 rodent hosts with similar ecology: the yellow-necked mouse (Apodemus flavicollis) from Trento, Italy and the white-footed mouse (Peromyscus leucopus) from Pennsylvania, USA. To investigate the effects of pinworm life-history characteristics on generating aggregation, we present a stochastic model that explores aggregation under a range of host-self-infection, parasite death, and transmission scenarios. Results. Oxyuridae parasites had consistently greater aggregation compared to other nematodes regardless of host or parasite species identity, and pinworm aggregation exceeded the range of macroparasite aggregation described previously. Conclusions. Our simulations demonstrate that host-self-infection, on its own, is sufficient to generate aggregation values greater than the predicted values.

Keywords

aggregationTaylor's power lawOxyuridaemacroparasite dynamicsApodemusPeromyscus
Type
Research Article
Information
Parasitology , Volume 138 , Issue 5 , April 2011 , pp. 619 - 627
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Abu-Madi, M. A., Behnke, J. M., Lewis, J. W. and Gilbert, F. S. (2000). Seasonal and site specific variation in the component community structure of intestinal helminthes in Apodemus sylvaticus from three contrasting habitats in south-east England. Journal of Helminthology 74, 7–15.CrossRefGoogle ScholarPubMed
Adamson, M. (1989). Evolutionary biology of the Oxyurida (Nematoda): biofacies of a haplodiploid taxon. Advances in Parasitology 28, 175–228.CrossRefGoogle ScholarPubMed
Adamson, M. (1994). Evolutionary patterns in the life histories of Oxyruida. International Journal for Parasitology 24, 1167–1177.CrossRefGoogle Scholar
Anderson, R. C. (2000). Nematode Parasites of Vertebrates: their Development and Transmission. 2nd Edn. CABI Publishing, New York, USA.CrossRefGoogle Scholar
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, 373–398.CrossRefGoogle ScholarPubMed
Anderson, R. M., Gordon, D. M., Crawley, M. J. and Hassell, M. P. (1982).Variability in the abundance of animal and plant species. Nature, London 296, 245–248.CrossRefGoogle Scholar
Behnke, J. M., Lewis, J. W., Mohd Zain, S. N. and Gilbert, F. S. (1999). Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host age, sex and year on the prevalence and abundance of infections. Journal of Helminthology 73, 31–44.CrossRefGoogle ScholarPubMed
Chan, K. F. (1952). Life-cycle studies on the nematode Syphacia obveleta. American Journal of Hygiene 56, 14–21.Google Scholar
Fuentes, M. V., Saez, A., Trelis, M., Galan-Puchades, M. T. and Esteban, J. G. (2004). The helminth community if the wood mouse, Apodemus sylvaticus, in the Sierra Espuna, Murcia, Spain. Journal of Helminthology 78, 219–223.CrossRefGoogle ScholarPubMed
Gandon, S., van Baalen, M. and Jansen, V. A. A. (2002). The evolution of parasite virulence, superinfection, and host resistence. American Naturalist 159, 658–669.CrossRefGoogle Scholar
Grundman, A. W., Warnock, R. G. and Wasson, D. L. (1976). Some mechanisms of natural regulation of parasitic helminth populations. American Midland Naturalist 95, 347–360.CrossRefGoogle Scholar
Hanski, I. (1980). Spatial patterns and movements in coprophagous beetles. Oikos 34, 293–310.CrossRefGoogle Scholar
Hussey, K. L. (1957). Syphacia muris vs. S. obvelata in laboratory rats and mice. Journal of Parasitology 43, 555–559.CrossRefGoogle Scholar
Kilpatrick, A. M. and Ives, A. R. (2003). Species interactions can explain Taylor's power law for ecological time series. Nature, London 422, 65–68.CrossRefGoogle ScholarPubMed
Luong, L. T., Perkins, S. E., Grear, D. A., Rizzoli, A. and Hudson, P. J. (2010). The relative importance of host characteristics and co-infection in generating variation in Heligmosomoides polygyrus fecundity. Parasitology 137, 1003–1012. doi:10.1017/S0031182009991892.CrossRefGoogle ScholarPubMed
Morand, S. and Guegan, J. F. (2000). Distribution and abundance of parasitic nematodes: ecological specialization, phylogenetic constraint or simply epidemiology? Oikos 88, 563–573.CrossRefGoogle Scholar
Muller-Graf, C. D. M., Durand, P., Feliu, C., Hugot, J. P., O'Callaghan, C. J. O., Renaud, F., Santalla, F. and Morand, S. (1999). Epidemiology and genetic variability of two species of nematodes (Heligmosomoides polygyrus and Syphacia stroma) of Apodemus spp. Parasitology 118, 425–432.CrossRefGoogle ScholarPubMed
Parker, G. A., Ball, M. A. and Chubb, J. C. (2009). Why do larval helminthes avoid the gut of intermediate hosts? Journal of Theoretical Biology 260, 460–473.CrossRefGoogle ScholarPubMed
Prince, M. J. (1950). Studies on the life cycle of Syphacia obveleta, a common nematode parasite of rats. Science 111, 66–67.CrossRefGoogle ScholarPubMed
Read, A. F. (1994). The evolution of virulence. Trends in Microbiology 2, 73–76.CrossRefGoogle ScholarPubMed
Read, A. F. and Skorping, A. (1995). The evolution of tissue migration by parasitic nematode larvae. Parasitology 111, 359–371.CrossRefGoogle ScholarPubMed
Schad, G. A. (1957). Preliminary observations of the life history of the sheep pinworm, Skrjabinema ovis. Journal of Parasitology 43, 13.Google Scholar
Shaw, D. J. and Dobson, A. P. (1995). Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111 (Suppl.) S111–S133.CrossRefGoogle ScholarPubMed
Shaw, D. J., Grenfell, B. J. and Dobson, A. P. (1998). Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117, 597–610.CrossRefGoogle ScholarPubMed
Taylor, L. R. (1961). Aggregation, variance and the mean. Nature, London 189, 732–735.CrossRefGoogle Scholar
Taylor, L. R. and Taylor, R. A. J. (1977). Aggregation, migration, and population mechanics. Nature, London 265, 415–420.CrossRefGoogle ScholarPubMed
Taylor, L. R., Woiwod, I. P. and Perry, J. N. (1978). The density-dependence of spatial behaviour and the rarity of randomness. Journal of Animal Ecology 47, 383–406.CrossRefGoogle Scholar
Taylor, L. R. and Woiwod, I. P. (1980). Temporal stability as a density-dependent species characteristic. Journal of Animal Ecology 49, 209–224.CrossRefGoogle Scholar
Vandegrift, K. J. and Hudson, P. J. (2009). Could parasites destabilize mouse populations? The potential role of Pterygodermitites peromysci in the population dynamics of free-living mice, Peromyscus leucopus. International Journal for Parasitology 39, 1253–1262.CrossRefGoogle ScholarPubMed
Wilson, K., Bjornstad, 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, UK.CrossRefGoogle Scholar