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Negative covariance between parasite load and body condition in a population of feral horses

Published online by Cambridge University Press:  22 March 2016

LUCIE DEBEFFE*
Affiliation:
Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK S7N 5E2, Canada
PHILIP D. MCLOUGHLIN
Affiliation:
Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK S7N 5E2, Canada
SARAH A. MEDILL
Affiliation:
Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK S7N 5E2, Canada
KATHRINE STEWART
Affiliation:
Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK S7N 5E2, Canada
DANIEL ANDRES
Affiliation:
Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK S7N 5E2, Canada
TODD SHURY
Affiliation:
Parks Canada Agency, 52 Campus Drive, Saskatoon SK S7N 5B4, Canada
BRENT WAGNER
Affiliation:
Department of Veterinary Microbiology, University of Saskatchewan, 52 Campus drive, Saskatoon, SK S7N 5B4, Canada
EMILY JENKINS
Affiliation:
Department of Veterinary Microbiology, University of Saskatchewan, 52 Campus drive, Saskatoon, SK S7N 5B4, Canada
JOHN S. GILLEARD
Affiliation:
Department of Comparative Biology and Experimental Medicine, University of Calgary, 3330 Hospital Drive, Calgary, AB T2N 4N1, Canada
JOCELYN POISSANT*
Affiliation:
Department of Comparative Biology and Experimental Medicine, University of Calgary, 3330 Hospital Drive, Calgary, AB T2N 4N1, Canada College of Life and Environmental Sciences, University of Exeter, Cornwall Campus, Penryn TR10 9FE, UK
*
*Corresponding authors: Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK S7N 5E2, Canada. E-mail: lucie.debeffe@gmail.com and Centre for Ecology and Conservation, University of Exeter, Cornwall Campus, Penryn TR10 9FE, UK. E-mail: j.poissant@exeter.ac.uk
*Corresponding authors: Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK S7N 5E2, Canada. E-mail: lucie.debeffe@gmail.com and Centre for Ecology and Conservation, University of Exeter, Cornwall Campus, Penryn TR10 9FE, UK. E-mail: j.poissant@exeter.ac.uk

Summary

In wild and domestic animals, gastrointestinal parasites can have significant impacts on host development, condition, health, reproduction and longevity. Improving our understanding of the causes and consequences of individual-level variation in parasite load is therefore of prime interest. Here we investigated the relationship between strongyle fecal egg count (FEC) and body condition in a unique, naturalized population of horses that has never been exposed to anthelmintic drugs (Sable Island, Nova Scotia, Canada). We first quantified variation in FEC and condition for 447 individuals according to intrinsic (sex, age, reproductive status, social status) and extrinsic (group size, location, local density) variables. We then quantified the repeatability of measurements obtained over a field season and tested for covariance between FEC and condition. FECs were high relative to other horse populations (mean eggs per gram ± SD = 1543·28 ± 209·94). FECs generally decreased with age, were higher in lactating vs non-lactating females, and unexpectedly lower in males in some part of the island. FECs and condition were both spatially structured, with patterns depending on age, sex and reproductive status. FECs and condition were both repeatable. Most notably, FECs and condition were negatively correlated, especially in adult females.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Altizer, S., Nunn, C. L., Thrall, P. H., Gittleman, J. L., Antonovics, J., Cunningham, A. A., Dobson, A. P., Ezenwa, V., Jones, K. E., Pedersen, A. B., Poss, M. and Pulliam, J. R. C. (2003). Social organization and parasite risk in mammals: integrating theory and empirical studies. Annual Review of Ecology, Evolution and Systematics 34, 517547.Google Scholar
Barger, I. (1993). Influence of sex and reproductive status on susceptibility of ruminants to nematode parasitism. International Journal for Parasitology 23, 463469.Google Scholar
Barnett, C. A., Suzuki, T. N., Sakaluk, S. K. and Thompson, C. F. (2015). Mass-based condition measures and their relationship with fitness: in what condition is condition? Journal of Zoology 296, 15.Google Scholar
Bates, D., Maechler, M., Bolker, B. and Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 148. doi:10.18637/jss.v067.i01.Google Scholar
Body, G., Ferte, H., Gaillard, J. M., Delorme, D., Klein, F. and Gilot-Fromont, E. (2011). Population density and phenotypic attributes influence the level of nematode parasitism in roe deer. Oecologia 167, 635646.Google Scholar
Bonenfant, C., Gaillard, J.-M., Coulson, T., Festa-Bianchet, M., Loison, A., Garel, M., Loe, L. E., Blanchard, P., Pettorelli, N., Owen-Smith, N., Du Toit, J. and Duncan, P. (2009). Empirical evidence of density-dependence in populations of large herbivores. Advances in Ecological Research 41, 313357.Google Scholar
Bowman, D. D. (2003). Georgis’ Parasitology for Veterinarians, 8th Edn. W. B. Saunders, Philadelphia, Pennsylvania.Google Scholar
Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Multimodel Inference – a Practical Information-Theoretic Approach, 2nd Edn. Springer-Verlag, New York.Google Scholar
Carroll, C. and Huntington, P. (1988). Body condition scoring and weight estimation of horses. Equine Veterinary Journal 20, 4145.Google Scholar
Carstensen, H., Larsen, L., Ritz, C. and Nielsen, M. K. (2013). Daily variability of strongyle faecal egg counts in horses. Journal of Equine Veterinary Science 33, 161164.Google Scholar
Cattadori, I., Boag, B., Bjornstad, O., Cornell, S. and Hudson, P. (2005). Peak shift and epidemiology in a seasonal host-nematode system. Proceedings of the Royal Society B: Biological Sciences 272, 11631169.CrossRefGoogle Scholar
Christie, B. J. (1995). The Horses of Sable Island. Pottersfield Press, Lawrencestown, Nova Scotia, Canada.Google Scholar
Clancey, E., Dunn, S. J. and Byers, J. A. (2012). Do single point condition measurements predict fitness in female pronghorn (Antilocapra americana)? Canadian Journal of Zoology-Revue Canadienne De Zoologie 90, 729735.CrossRefGoogle Scholar
Clutton-Brock, T. and Sheldon, B. C. (2010). Individuals and populations: the role of long-term, individual-based studies of animals in ecology and evolutionary biology. Trends in Ecology & Evolution 25, 562573.Google Scholar
Connan, R. (1976). Effect of lactation on the immune response to gastrointestinal nematodes. The Veterinary Record 99, 476477.Google Scholar
Contasti, A. L., Tissier, E. J., Johnstone, J. F. and McLoughlin, P. D. (2012). Explaining spatial heterogeneity in population dynamics and genetics from spatial variation in resources for a large herbivore. PLoS ONE 7, e47858.CrossRefGoogle ScholarPubMed
Cressler, C. E., Nelson, W. A., Day, T. and McCauley, E. (2014). Disentangling the interaction among host resources, the immune system and pathogens. Ecology Letters 17, 284293.Google Scholar
Davidson, R. K., Ličina, T., Gorini, L. and Milner, J. M. (2015). Endoparasites in a Norwegian moose (Alces alces) population – faunal diversity, abundance and body condition. (International Congress on Parasites of Wildlife, pp. 49–158) International Journal for Parasitology: Parasites and wildlife 4, 2936.Google Scholar
Ezenwa, V. O. (2004). Host social behavior and parasitic infection: a multifactorial approach. Behavioral Ecology 15, 446454.Google Scholar
Ezenwa, V. O., Ekernas, L. S. and Creel, S. (2012). Unravelling complex associations between testosterone and parasite infection in the wild. Functional Ecology 26, 123133.CrossRefGoogle Scholar
Fairbanks, B., Hawley, D. M., Demas, G. E. and Nelson, R. J. (2012). Interactions between host social behavior, physiology, and disease susceptibility. In Ecoimmunology (ed. Demas, G. and Nelson, R.), pp. 440467. Oxford University Press, Oxford, UK.Google Scholar
Festa-Bianchet, M. (1989). Individual differences, parasites, and the costs of reproduction for bighorn ewes (Ovis canadensis). Journal of Animal Ecology 58, 785795.Google Scholar
Festa-Bianchet, M., Gaillard, J. and Jorgenson, J. (1998). Mass- and density-dependent reproductive success and reproductive costs in a capital breeder. American Naturalist 152, 367379.Google Scholar
Flanagan, K. L., Morton, J. M. and Sandeman, R. M. (2013). Prevalence of infestation with gastrointestinal nematodes in Pony Club horses in Victoria. Australian Veterinary Journal 91, 241245.Google Scholar
Fog, P., Vigre, H. and Nielsen, M. (2011). Strongyle egg counts in Standardbred trotters: are they associated with race performance? Equine Veterinary Journal 43, 8992.Google Scholar
Gilmour, A. R., Gogel, B., Cullis, B., Thompson, R. and Butler, D. (2009). ASReml User Guide Release 3.0. VSN International Ltd, Hemel Hempstead, UK.Google Scholar
Habig, B. and Archie, E. A. (2015). Social status, immune response and parasitism in males: a meta-analysis. Philosophical Transactions of the Royal Society B: Biological Sciences 370, 20140109.Google Scholar
Hayward, A. (2013). Causes and consequences of intra-and inter-host heterogeneity in defence against nematodes. Parasite Immunology 35, 362373.Google Scholar
Hayward, A. D., Wilson, A. J., Pilkington, J. G., Pemberton, J. M. and Kruuk, L. E. B. (2009). Ageing in a variable habitat: environmental stress affects senescence in parasite resistance in St Kilda Soay sheep. Proceedings of the Royal Society B: Biological Sciences 276, 34773485.Google Scholar
Hayward, A. D., Garnier, R., Watt, K. A., Pilkington, J. G., Grenfell, B. T., Matthews, J. B., Pemberton, J. M., Nussey, D. H. and Graham, A. L. (2014). Heritable, heterogeneous, and costly resistance of sheep against nematodes and potential feedbacks to epidemiological dynamics. The American Naturalist 184, S58S76.Google Scholar
Houdijk, J. (2008). Influence of periparturient nutritional demand on resistance to parasites in livestock. Parasite Immunology 30, 113121.CrossRefGoogle ScholarPubMed
Hutchings, M. R., Milner, J. M., Gordon, I. J., Kyriazakis, I. and Jackson, F. (2002). Grazing decisions of Soay sheep, Ovis aries, on St Kilda: a consequence of parasite distribution? Oikos 96, 235244.Google Scholar
Irvine, R. J., Corbishley, H., Pilkington, J. G. and Albon, S. D. (2006). Low-level parasitic worm burdens may reduce body condition in free-ranging red deer (Cervus elaphus). Parasitology 133, 465475.Google Scholar
Jolles, A. E. and Ezenwa, V. O. (2015). Ungulates as model systems for the study of disease processes in natural populations. Journal of Mammalogy 96, 415.Google Scholar
Keymer, A. and Hiorns, R. (1986). Faecal egg counts and nematode fecundity: Heligmosomoides polygyrus and laboratory mice. Parasitology 93, 189203.Google Scholar
Khan, M., Roohi, N. and Rana, M. (2015). Strongylosis in Equines: a review. Journal of Animal and Plant Sciences 25, 19.Google Scholar
Lichtenfels, J. R., Kharchenko, V. A. and Dvojnos, G. M. (2008). Illustrated identification keys to strongylid parasites (strongylidae: Nematoda) of horses, zebras and asses (Equidae). Identification Keys to Strongylid Nematode Parasites of Equids 156, 4161.Google Scholar
Lloyd, S. (1983). Immunosuppression during pregnancy and lactation. Irish Veterinary Journal 37, 6470.Google Scholar
Love, S., Murphy, D. and Mellor, D. (1999). Pathogenicity of cyathostome infection. Veterinary Parasitology 85, 113122.CrossRefGoogle ScholarPubMed
Marjamäki, P. H., Contasti, A. L., Coulson, T. N. and McLoughlin, P. D. (2013). Local density and group size interacts with age and sex to determine direction and rate of social dispersal in a polygynous mammal. Ecology and Evolution 3, 30733082.CrossRefGoogle Scholar
Mazerolle, M. J. (2015). AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 2.0–3. http://CRAN.R-project.org/package=AICcmodavg.Google Scholar
Miller, J. M., Kijas, J. W., Heaton, M. P., McEwan, J. C. and Coltman, D. W. (2012). Consistent divergence times and allele sharing measured from cross-species application of SNP chips developed for three domestic species. Molecular Ecology Resources 12, 11451150.CrossRefGoogle ScholarPubMed
Moore, S. L. and Wilson, K. (2002). Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297, 20152018.Google Scholar
Moretti, E. H., Madelaire, C. B., Silva, R. J., Mendonca, M. T. and Gomes, F. R. (2014). The relationships between parasite intensity, locomotor performance, and body condition in adult toads (Rhinella icterica) from the Wild. Journal of Herpetology 48, 277283.Google Scholar
Nielsen, M. K., Vidyashankar, A. N., Andersen, U. V., DeLisi, K., Pilegaard, K. and Kaplan, R. M. (2010 a). Effects of faecal collection and storage factors on strongylid egg counts in horses. Veterinary Parasitology 167, 5561.Google Scholar
Nielsen, M. K., Baptiste, K. E., Tolliver, S. C., Collins, S. S. and Lyons, E. T. (2010 b). Analysis of multiyear studies in horses in Kentucky to ascertain whether counts of eggs and larvae per gram of faeces are reliable indicators of numbers of strongyles and ascarids present. EVPC 2009: Veterinary Parasitosis in the Mediterranean Area 174, 7784.Google Scholar
Osterman, L. E. (2005). Prevalence and control of strongyle nematode infections of horses in Sweden. Doctoral thesis. Swedish University of Agricultural Sciences, Uppsala, Sweden.Google Scholar
Patterson, J. E. H. and Ruckstuhl, K. E. (2013). Parasite infection and host group size: a meta-analytical review. Parasitology 140, 803813.CrossRefGoogle Scholar
Pilar Valdez-Cruz, M., Hernandez-Gil, M., Galindo-Rodriguez, L. and Angel Alonso-Diaz, M. (2013). Gastrointestinal nematode burden in working equids from humid tropical areas of central Veracruz, Mexico, and its relationship with body condition and haematological values. Tropical Animal Health and Production 45, 603607.Google Scholar
Poulin, R. (1996). Helminth growth in vertebrate hosts: does host sex matter? International Journal for Parasitology 26, 13111315.CrossRefGoogle ScholarPubMed
Poulin, R. (2007). Evolutionary Ecology of Parasites. Princeton University Press, Princeton.Google Scholar
Poulin, R. and Forbes, M. R. (2012). Meta-analysis and research on host-parasite interactions: past and future. Evolutionary Ecology 26, 11691185.Google Scholar
R Development Core Team. (2010). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.Google Scholar
Raynaud, J. (1970). Etude de l'efficacité d'une technique de coproscopie quantitative pour le diagnostic de routine et le contrôle des infestations parasitaires des bovins, ovins, équins et porcins. Annales de Parasitologie Humaine et Comparée 45, 321342.Google Scholar
Reading, C. and Clarke, R. (1995). The effects of density, rainfall and environmental temperature on body condition and fecundity in the common toad, Bufo bufo. Oecologia 102, 453459.Google Scholar
Relf, V. E., Morgan, R., Hodgkinson, J. E. and Matthews, J. B. (2013). Helminth egg excretion with regard to age, gender and management practices on UK Thoroughbred studs. Parasitology 140, 641652.Google Scholar
Rifkin, J. L., Nunn, C. L. and Garamszegi, L. Z. (2012). Do animals living in larger groups experience greater parasitism? A meta-analysis. American Naturalist 180, 7082.Google Scholar
Rozen-Rechels, D., van Beest, F. M., Richard, E., Uzal, A., Medill, S. A. and McLoughlin, P. D. (2015). Density-dependent, central-place foraging in a grazing herbivore: competition and tradeoffs in time allocation near water. Oikos 124, 11421150.CrossRefGoogle Scholar
Rubenstein, D. and Hohmann, M. (1989). Parasites and social-behavior of Island feral horses. Oikos 55, 312320.Google Scholar
Santín-Durán, M., Alunda, J. M., Hoberg, E. P. and de la Fuente, C. (2008). Age distribution and seasonal dynamics of abomasal Helminths in wild red deer from central Spain. Journal of Parasitology 94, 10311037.Google Scholar
Scantlebury, M., McWilliams, M. M., Marks, N. J., Dick, J. T. A., Edgar, H. and Lutermann, H. (2010). Effects of life-history traits on parasite load in grey squirrels. Journal of Zoology 282, 246255.Google Scholar
Schulte-Hostedde, A. I. and Elsasser, S. C. (2011). Spleen mass, body condition, and parasite load in male American mink (Neovison vison). Journal of Mammalogy 92, 221226.Google Scholar
Self, S. G. and Liang, K. Y. (1987). Asymptotic properties of maximum likelihood estimators and likelihood ratio tests under nonstandard conditions. Journal of the American Statistical Association 82, 605610.Google Scholar
Sellon, D. C. and Long, M. (2013). Equine Infectious Diseases, 2dn Edn. Elsevier Health Sciences, New York, pp. 454455.Google Scholar
Sheldon, B. and Verhulst, S. (1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology & Evolution 11, 317321.Google Scholar
Stien, A., Irvine, R. J., Ropstad, E., Halvorsen, O., Langvatn, R. and Albon, S. D. (2002). The impact of gastrointestinal nematodes on wild reindeer: experimental and cross-sectional studies. Journal of Animal Ecology 71, 937945.Google Scholar
Symonds, M. R. E. and Moussalli, A. (2011). A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike's information criterion. Behavioral Ecology and Sociobiology 65, 1321.Google Scholar
Tompkins, D. and Begon, M. (1999). Parasites can regulate wildlife populations. Parasitology Today 15, 311313.CrossRefGoogle ScholarPubMed
Turner, W. C. and Getz, W. M. (2010). Seasonal and demographic factors influencing gastrointestinal parasitism. Journal of Wildlife Diseases 46, 11081119.Google Scholar
Vatta, A., Krecek, R., Letty, B., van der Linde, M., Motswatswe, P. and Hansen, J. (2002). Effect of nematode burden as assessed by means of faecal egg counts on body condition in goats farmed under resource-poor conditions in South Africa. Veterinary Parasitology 108, 247254.Google Scholar
Watson, M. J. (2013). What drives population-level effects of parasites? Meta-analysis meets life-history. International Journal for Parasitology: Parasites and Wildlife 2, 190196.Google Scholar
Welsh, D. A. (1975). Population, behavioural and grazing ecology of the horses of Sable Island. PhD. Thesis, Dalhousie University, Canada.Google Scholar
Williams, G. C. (1966). Natural selection, the costs of reproduction, and a refinement of Lack's principle. American Naturalist 100, 687690.Google Scholar
Wilson, A. (2008). Why h2 does not always equal VA/VP? Journal of Evolutionary Biology 21, 647650.Google Scholar
Wilson, A. J., Reale, D., Clements, M. N., Morrissey, M. M., Postma, E., Walling, C. A., Kruuk, L. E. and Nussey, D. H. (2010). An ecologist's guide to the animal model. Journal of Animal Ecology 79, 1326.CrossRefGoogle ScholarPubMed
Wood, E. L. D., Matthews, J. B., Stephenson, S., Slote, M. and Nussey, D. H. (2013). Variation in faecal egg counts in horses managed for conservation purposes: individual egg shedding consistency, age effects and seasonal variation. Parasitology 140, 115128.Google Scholar
Wood, S. N. (2011). Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. Journal of the Royal Statistical Society Series B: Statistical Methodology 73, 336.CrossRefGoogle Scholar
Yoseph, S., Smith, D. G., Mengistu, A., Teklu, F., Firew, T. and Betere, Y. (2005). Seasonal variation in the parasite burden and body condition of working donkeys in East Shewa and West Shewa regions of Ethiopia. Tropical Animal Health and Production 37, 3545.CrossRefGoogle ScholarPubMed
Zuk, M. and McKean, K. A. (1996). Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 10091024.Google Scholar
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