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Temporal and spatial variation in prevalence of the parasite Syngamus trachea in a metapopulation of house sparrows (Passer domesticus)

Published online by Cambridge University Press:  21 June 2013

HÅKON HOLAND ,
HENRIK JENSEN ,
JARLE TUFTO ,
BERNT-ERIK SÆTHER  and
THOR HARALD RINGSBY
HÅKON HOLAND*
Affiliation:
Department of Biology, Norwegian University of Science and Technology, Centre for Biodiversity Dynamics, 7491 Trondheim, Norway
HENRIK JENSEN
Affiliation:
Department of Biology, Norwegian University of Science and Technology, Centre for Biodiversity Dynamics, 7491 Trondheim, Norway
JARLE TUFTO
Affiliation:
Department of Mathematical Sciences, Norwegian University of Science and Technology, Centre for Biodiversity Dynamics, 7491 Trondheim, Norway
BERNT-ERIK SÆTHER
Affiliation:
Department of Biology, Norwegian University of Science and Technology, Centre for Biodiversity Dynamics, 7491 Trondheim, Norway
THOR HARALD RINGSBY
Affiliation:
Department of Biology, Norwegian University of Science and Technology, Centre for Biodiversity Dynamics, 7491 Trondheim, Norway
*
*Corresponding author. Department of Biology, Norwegian University of Science and Technology, Centre for Biodiversity Dynamics, 7491 Trondheim, Norway. E-mail: hakon.holand@bio.ntnu.no
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Summary

When investigating parasite–host dynamics in wild populations, a fundamental parameter to investigate is prevalence. This quantifies the percentage of individuals infected in the population. Investigating how prevalence changes over time and space can reveal interesting aspects in the parasite–host relationship in natural populations. We investigated the dynamic between a common avian parasite (Syngamus trachea) in a host metapopulation of house sparrows (Passer domesticus) on the coast of Helgeland in northern Norway. We found that parasite prevalence varied in both time and space. In addition, the parasite prevalence was found to be different between demographic groups in the local populations. Our results reveal just how complex the dynamic between a host and its parasite may become in a fragmented landscape. Although temperature may be an important factor, the specific mechanisms causing this complexity are not fully understood, but need to be further examined to understand how parasite–host interactions may affect the ecological and evolutionary dynamics and viability of host populations.

Keywords

ParasiteSyngamus tracheahouse sparrowprevalencemetapopulation
Type
Research Article
Information
Parasitology , Volume 140 , Issue 10 , September 2013 , pp. 1275 - 1286
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Agresti, A. (2002). Categorical Data Analysis. Wiley-Interscience, New York, USA.CrossRefGoogle Scholar
Aiken, L. and West, S. (1991). Multiple Regression: Testing and Interpreting Interactions. Sage, Newbury Park, CA, USA.Google Scholar
Anderson, T. R. (2006). Biology of the Ubiquitous House Sparrow: From Genes to Populations. Oxford University Press, New York, USA.CrossRefGoogle Scholar
Arneberg, P. (2001). An ecological law and its macroecological consequences as revealed by studies of relationships between host densities and parasite prevalence. Ecography 24, 352–358. doi: 10.1034/j.1600-0587.2001.240313.x.CrossRefGoogle Scholar
Atkinson, C. T., Dusek, R. J., Woods, K. L. and Iko, W. M. (2000). Pathogenicity of avian malaria in experimentally-infected Hawaii Amakihi. Journal of Wildlife Diseases 36, 197–204.CrossRefGoogle ScholarPubMed
Atkinson, C. T., Thomas, N. J. and Hunter, D. B. (2008). Parasitic Diseases of Wild Birds. Wiley-Blackwell, Ames, IA, USA.CrossRefGoogle Scholar
Bakke, T. A. (1973). Studies of the helminth fauna of Norway part 27. Syngamiasis in Norway. Norwegian Journal of Zoology 21, 299–303.Google Scholar
Barus, V. (1966 a). The effect of temperature and air humidity on the development and the resistance of eggs of the nematode Syngamus-trachea. Helminthologia (Bratislava) 7, 103–106.Google Scholar
Barus, V. (1966 b). The longevity of the parasitic stages and the dynamics of eggs production of nematode Syngamus-trachea in chicken and turkeys. Folia Parasitologica (Ceske Budejovice) 13, 274–277.Google Scholar
Barus, V. (1966 c). Seasonal dynamics of the invasion extensity of the nematode Syngamus-trachea in breeding turkeys Meleagris-gallopavo-f-domestica. Helminthologia (Bratislava) 7, 29–37.Google Scholar
Barus, V. and Blazek, K. (1965). Revision of exogenous and endogenous phases of the developmental cycle and the pathogenesis of Syngamus (Syngamus) trachea (Montagu, 1811) Chapin, 1925 into the organs of the final host. Cesk Parasitol 12, 47–70.Google Scholar
Bensch, S. and Akesson, A. (2003). Temporal and spatial variation of hematozoans in Scandinavian willow warblers. Journal of Parasitology 89, 388–391. doi: 10.1645/0022-3395(2003)089[0388:tasvoh]2.0.co;2.CrossRefGoogle ScholarPubMed
Billing, A. M., Lee, A. M., Skjelseth, S., Borg, Å. A., Hale, M. C., Slate, J. O. N., Pärn, H., Ringsby, T. H., Sæther, B.-E. and Jensen, H. (2012). Evidence of inbreeding depression but not inbreeding avoidance in a natural house sparrow population. Molecular Ecology 21, 1487–1499. doi: 10.1111/j.1365-294X.2012.05490.x.CrossRefGoogle ScholarPubMed
Borg, A. A., Pedersen, S. A., Jensen, H. and Westerdahl, H. (2011). Variation in MHC genotypes in two populations of house sparrow (Passer domesticus) with different population histories. Ecology and Evolution 1, 145–159.CrossRefGoogle ScholarPubMed
Burnham, K. and Anderson, D. (2002). Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer-Verlag, New York, USA.Google Scholar
Clapham, P. A. (1934). Experimental studies on the transmission of gapeworm (Syngamus trachea) by earthworms. Proceedings of the Royal Society of London Series B – Biological Sciences 115, 18–29.Google Scholar
Earn, D. J. D., Rohani, P. and Grenfell, B. T. (1998). Persistence, chaos and synchrony in ecology and epidemiology. Proceedings of the Royal Society of London Series B – Biological Sciences 265, 7–10.CrossRefGoogle ScholarPubMed
Engen, S., Ringsby, T. H., Sæther, B.-E., Lande, R., Jensen, H., Lillegard, M. and Ellegren, H. (2007). Effective size of fluctuating populations with two sexes and overlapping generations. Evolution 61, 1873–1885. doi: 10.1111/j.1558-5646.2007.00155.x.CrossRefGoogle ScholarPubMed
Gaspar da Silva, D., Barton, E., Bunbury, N., Lunness, P., Bell, D. J. and Tyler, K. M. (2007). Molecular identity and heterogeneity of Trichomonad parasites in a closed avian population. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases 7, 433–440. doi:10.1016/j.meegid.2007.01.002.CrossRefGoogle Scholar
Gjerde, B. (2007). Kompendium i veterinærmedisinsk parasittologi. (ed. Veterinærhøyskole, N.). Norwegian School of Veterinary Science, Oslo.Google Scholar
Gulland, F. M. D., Albon, S. D., Pemberton, J. M., Moorcroft, P. R. and Cluttonbrock, T. H. (1993). Parasite-associated polymorphism in a cyclic ungulate population. Proceedings of the Royal Society of London Series B – Biological Sciences 254, 7–13.Google Scholar
Gurski, K. C. and Ebbert, M. A. (2003). Host age, but not host location within a stream, is correlated with the prevalence of gut parasites in water striders. Journal of Parasitology 89, 529–534. doi: 10.1645/0022-3395(2003)089[0529:habnhl]2.0.co;2.CrossRefGoogle Scholar
Henriques-Gil, N., Haro, M., Izquierdo, F., Fenoy, S. and del Aguila, C. (2010). Phylogenetic aApproach to the variability of the microsporidian enterocytozoon bieneusi and its implications for inter- and intrahost transmission. Applied and Environmental Microbiology 76, 3333–3342. doi: 10.1128/aem.03026-09.CrossRefGoogle Scholar
Hess, G. (1996). Disease in metapopulation models: implications for conservation. Ecology 77, 1617–1632. doi: 10.2307/2265556.CrossRefGoogle Scholar
Hudson, P. J., Dobson, A. P. and Newborn, D. (1998). Prevention of population cycles by parasite removal. Science 282, 2256–2258.CrossRefGoogle ScholarPubMed
Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P. (2002). The Ecology of Wildlife Diseases. Oxford: Oxford University Press.CrossRefGoogle Scholar
Ilmonen, P., Penn, D. J., Damjanovich, K., Clarke, J., Lamborn, D., Morrison, L., Ghotbi, L. and Potts, W. K. (2008). Experimental infection magnifies inbreeding depression in house mice. Journal of Evolutionary Biology 21, 834–841. doi: 10.1111/j.1420-9101.2008.01510.x.CrossRefGoogle ScholarPubMed
Jensen, H., Bremset, E. M., Ringsby, T. H. and Sæther, B. E. (2007). Multilocus heterozygosity and inbreeding depression in an insular house sparrow metapopulation. Molecular Ecology 16, 4066–4078. doi: 10.1111/j.1365-294X.2007.03452.x.CrossRefGoogle Scholar
Jensen, H., Steinsland, I., Ringsby, T. H. and Sæther, B. E. (2008). Evolutionary dynamics of a sexual ornament in the house sparrow (Passer domesticus): the role of indirect selection within and between sexes. Evolution 62, 1275–1293. doi: 10.1111/j.1558-5646.2008.00395.x.CrossRefGoogle ScholarPubMed
Jesse, M. and Heesterbeek, H. (2011). Divide and conquer? Persistence of infectious agents in spatial metapopulations of hosts. Journal of Theoretical Biology 275, 12–20. doi: 10.1016/j.jtbi.2011.01.032.CrossRefGoogle ScholarPubMed
Kutz, S. J., Hoberg, E. P., Polley, L. and Jenkins, E. J. (2005). Global warming is changing the dynamics of Arctic host–parasite systems. Proceedings of the Royal Society B– Biological Sciences 272, 2571–2576. doi: 10.1098/rspb.2005.3285.CrossRefGoogle ScholarPubMed
Lachish, S., Knowles, S. C. L., Alves, R., Wood, M. J. and Sheldon, B. C. (2011). Infection dynamics of endemic malaria in a wild bird population: parasite species-dependent drivers of spatial and temporal variation in transmission rates. Journal of Animal Ecology 80, 1207–1216. doi: 10.1111/j.1365-2656.2011.01893.x.CrossRefGoogle Scholar
Macdonald, D. W., Anwar, M., Newman, C., Woodroffe, R. and Johnson, P. J. (1999). Inter-annual differences in the age-related prevalences of Babesia and Trypanosoma parasites of European badgers (Meles meles). Journal of Zoology 247, 65–70. doi: 10.1111/j.1469-7998.1999.tb00193.x.CrossRefGoogle Scholar
McCurdy, D. G., Shutler, D., Mullie, A. and Forbes, M. R. (1998). Sex-biased parasitism of avian hosts: relations to blood parasite taxon and mating system. Oikos 82, 303–312. doi:10.2307/3546970.CrossRefGoogle Scholar
NOMA (2001). Antiparasittærbehandling av produksjonsdyr, The Norwegian Medicines Agency, Oslo, Norway.Google Scholar
Pärn, H., Jensen, H., Ringsby, T. H. and Sæther, B. E. (2009). Sex-specific fitness correlates of dispersal in a house sparrow metapopulation. Journal of Animal Ecology 78, 1216–1225. doi: 10.1111/j.1365-2656.2009.01597.x.CrossRefGoogle Scholar
Pärn, H., Ringsby, T. H., Jensen, H. and Sæther, B. E. (2012). Spatial heterogeneity in the effects of climate and density-dependence on dispersal in a house sparrow metapopulation. Proceedings of the Royal Society B – Biological Sciences 279, 144–152. doi: 10.1098/rspb.2011.0673.CrossRefGoogle Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites. Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
R Development Core Team (2012). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/.Google Scholar
Ringsby, T. H., Sæther, B. E., Tufto, J., Jensen, H. and Solberg, E. J. (2002). Asynchronous spatiotemporal demography of a house sparrow metapopulation in a correlated environment. Ecology 83, 561–569.CrossRefGoogle Scholar
Ringsby, T. H., Berge, T., Sæther, B. E. and Jensen, H. (2009). Reproductive success and individual variation in feeding frequency of House Sparrows (Passer domesticus). Journal of Ornithology 150, 469–481. doi: 10.1007/s10336-008-0365-z.CrossRefGoogle Scholar
Rothman, K. J. (2012). Epidemiology: An Introduction. Oxford University Press, New York, USA.Google Scholar
Sæther, B. E., Ringsby, T. H., Bakke, O. and Solberg, E. J. (1999). Spatial and temporal variation in demography of a house sparrow metapopulation. Journal of Animal Ecology 68, 628–637.CrossRefGoogle Scholar
Saunders, D. A., Hobbs, R. J. and Margules, C. R. (1991). Biological consequences of ecosystem fragmentation – a review. Conservation Biology 5, 18–32. doi:10.1111/j.1523-1739.1991.tb00384.x.CrossRefGoogle Scholar
Summers-Smith, J. D. (1988). The Sparrows. T. & A.D. Poyser, Calton, UK.Google Scholar
Thompson, P. M., Corpe, H. M. and Reid, R. J. (1998). Prevalence and intensity of the ectoparasite Echinophthirius horridus on harbour seals (Phoca vitulina): effects of host age and inter-annual variability in host food availability. Parasitology 117, 393–403. doi: 10.1017/s0031182098003072.CrossRefGoogle ScholarPubMed
Vogeli, M., Lemus, J. A., Serrano, D., Blanco, G. and Tella, J. L. (2011). An island paradigm on the mainland: host population fragmentation impairs the community of avian pathogens. Proceedings of the Royal Society B – Biological Sciences 278, 2668–2676. doi: 10.1098/rspb.2010.1227.CrossRefGoogle ScholarPubMed
Weatherhead, P. J. and Bennett, G. F. (1991). Ecology of red-winged blackbird parasitism by hematozoa. Canadian Journal of Zoology–Revue Canadienne De Zoologie 69, 2352–2359. doi: 10.1139/z91-331.CrossRefGoogle Scholar
Wissler, K. and Halvorsen, O. (1975). The occurrence of gapeworm syngamus-trachea in willow grouse. Journal of Wildlife Diseases 11, 245–247.CrossRefGoogle ScholarPubMed
Wood, M. J., Cosgrove, C. L., Wilkin, T. A., Knowles, S. C. L., Day, K. P. and Sheldon, B. C. (2007). Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Molecular Ecology 16, 3263–3273. doi: 10.1111/j.1365-294X.2007.03362.x.CrossRefGoogle ScholarPubMed
Yamaguti, S. (1961). Systema Helminthum. Vol. Ill, pts. I-II. The Nematodes of Vertebrates. Interscience Publishers, New York, USA.Google Scholar
Zuk, M. and McKean, K. A. (1996). Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 1009–1023. doi: 10.1016/s0020-7519(96)00086-0.CrossRefGoogle ScholarPubMed