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Helminth parasites are associated with reduced survival probability in young red deer

Published online by Cambridge University Press:  02 September 2022

Claudia I. Acerini Open the ORCID record for Claudia I. Acerini [Opens in a new window] ,
Sean Morris ,
Alison Morris ,
Fiona Kenyon ,
David McBean ,
Josephine M. Pemberton  and
Gregory F. Albery
Claudia I. Acerini*
Affiliation:
School of Biological Sciences, Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3FL, UK
Sean Morris
Affiliation:
School of Biological Sciences, Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3FL, UK
Alison Morris
Affiliation:
School of Biological Sciences, Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3FL, UK
Fiona Kenyon
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Midlothian EH26 0PZ, UK
David McBean
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Midlothian EH26 0PZ, UK
Josephine M. Pemberton
Affiliation:
School of Biological Sciences, Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3FL, UK
Gregory F. Albery
Affiliation:
Wissenschaftskolleg zu Berlin, Berlin 14193, Germany Department of Biology, Georgetown University, Washington, DC 20007, USA
*
Author for correspondence: Claudia I. Acerini, Email: [email protected]
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Abstract

Helminths are common parasites of wild ungulates that can have substantial costs for growth, mortality and reproduction. Whilst these costs are relatively well documented for mature animals, knowledge of helminths' impacts on juveniles is more limited. Identifying these effects is important because young individuals are often heavily infected, and juvenile mortality is a key process regulating wild populations. Here, we investigated associations between helminth infection and overwinter survival in juvenile wild red deer (Cervus elaphus) on the Isle of Rum, Scotland. We collected fecal samples non-invasively from known individuals and used them to count propagules of 3 helminth taxa (strongyle nematodes, Fasciola hepatica and Elaphostrongylus cervi). Using generalized linear models, we investigated associations between parasite counts and overwinter survival for calves and yearlings. Strongyles were associated with reduced survival in both age classes, and F. hepatica was associated with reduced survival in yearlings, whilst E. cervi infection showed no association with survival in either age class. This study provides observational evidence for fitness costs of helminth infection in juveniles of a wild mammal, and suggests that these parasites could play a role in regulating population dynamics.

Keywords

Disease ecologyfitness costshelminthssurvivalungulatewild mammal
Type
Research Article
Information
Parasitology , Volume 149 , Issue 13 , November 2022 , pp. 1702 - 1708
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Albery, GF, Kenyon, F, Morris, A, Morris, S, Nussey, DH and Pemberton, JM (2018) Seasonality of helminth infection in wild red deer varies between individuals and between parasite taxa. Parasitology 145, 1410–1420.CrossRefGoogle Scholar
Albery, GF, Morris, A, Morris, S, Kenyon, F, Nussey, DH and Pemberton, JM (2021) Fitness costs of parasites explain multiple life-history trade-offs in a wild mammal. The American Naturalist 197, 324–335.CrossRefGoogle Scholar
Albon, SD, Stien, A, Irvine, RJ, Langvatn, R, Ropstad, E and Halvorsen, O (2002) The role of parasites in the dynamics of a reindeer population. Proceedings of the Royal Society B: Biological Sciences 269, 1625–1632.CrossRefGoogle ScholarPubMed
Ashby, B and Bruns, E (2018) The evolution of juvenile susceptibility to infectious disease. Proceedings of the Royal Society B: Biological Sciences 285, 20180844.CrossRefGoogle ScholarPubMed
Böhm, M, White, PCL, Daniels, MJ, Allcroft, DJ, Munro, R and Hutchings, MR (2006) The health of wild red and sika deer in Scotland: an analysis of key endoparasites and recommendations for monitoring disease. The Veterinary Journal 171, 287–294.CrossRefGoogle ScholarPubMed
Böhm, M, White, PCL, Chambers, J, Smith, L and Hutchings, MR (2007) Wild deer as a source of infection for livestock and humans in the UK. The Veterinary Journal 174, 260–276.CrossRefGoogle ScholarPubMed
Budischak, SA, Hoberg, EP, Abrams, A, Jolles, AE and Ezenwa, VO (2015) A combined parasitological molecular approach for noninvasive characterization of parasitic nematode communities in wild hosts. Molecular Ecology Resources 15, 1112–1119.CrossRefGoogle ScholarPubMed
Clutton-Brock, TH, Albon, SD and Guinness, FE (1982) Red Deer: Behaviour and Ecology of Two Sexes. Chicago, IL: University of Chicago Press.Google Scholar
Clutton-Brock, TH, Major, M, Albon, SD and Guinness, FE (1987) Early development and population dynamics in red deer. 1. Density-dependent effects on juvenile survival. Journal of Animal Ecology 56, 53–67.CrossRefGoogle Scholar
Coltman, DW, Pilkington, JG, Smith, JA and Pemberton, JM (1999) Parasite-mediated selection against inbred Soay sheep in a free-living island population. Evolution 53, 1259–1267.Google Scholar
Coulson, T, Albon, S, Guinness, F, Pemberton, J and Clutton-Brock, T (1997) Population substructure, local density, and calf winter survival in red deer (Cervus elaphus). Ecology 78, 852–863.CrossRefGoogle Scholar
Coulson, G, Cripps, JK, Garnick, S, Bristow, V and Beveridge, I (2018) Parasite insight: assessing fitness costs, infection risks and foraging benefits relating to gastrointestinal nematodes in wild mammalian herbivores. Philosophical Transactions of the Royal Society B: Biological Sciences 373, 20170197.CrossRefGoogle ScholarPubMed
Craig, BH, Tempest, LJ, Pilkington, JG and Pemberton, JM (2008) Metazoan-protozoan parasite co-infections and host body weight in St Kilda Soay sheep. Parasitology 135, 433–441.CrossRefGoogle ScholarPubMed
French, AS, Zadoks, RN, Skuce, PJ, Mitchell, G, Gordon-Gibbs, DK, Craine, A, Shaw, D, Gibb, SW and Taggart, MA (2016) Prevalence of liver fluke (Fasciola hepatica) in wild red deer (Cervus elaphus): coproantigen ELISA is a practicable alternative to faecal egg counting for surveillance in remote populations. PLoS ONE 11, e0162420.CrossRefGoogle Scholar
Fuller, RJ and Gill, RMA (2001) Ecological impacts of increasing numbers of deer in British woodland. Forestry 74, 193–199.CrossRefGoogle Scholar
Gaillard, JM, Festa-Bianchet, M, Yoccoz, NG, Loison, A and Toïgo, C (2000) Temporal variation in fitness components and population dynamics of large herbivores. Annual Review of Ecology and Systematics 31, 367–393.CrossRefGoogle Scholar
Gajadhar, AA, Tessaro, SV and Yates, WD (1994) Diagnosis of Elaphostrongylus cervi infection in New Zealand red deer (Cervus elaphus) quarantined in Canada, and experimental determination of a new extended prepatent period. The Canadian Veterinary Journal 35, 433–437.Google Scholar
Gulland, FMD (1992) The role of nematode parasites in Soay sheep (Ovis aries L.) mortality during a population crash. Parasitology 105, 493–503.CrossRefGoogle ScholarPubMed
Hayward, AD, Wilson, AJ, Pilkington, JG, Clutton-Brock, TH, Pemberton, JM and Kruuk, LE (2011) Natural selection on a measure of parasite resistance varies across ages and environmental conditions in a wild mammal. Journal of Evolutionary Biology 24, 1664–1676.CrossRefGoogle Scholar
Hayward, AD, Garnier, R, Watt, KA, Pilkington, JG, Grenfell, BT, Matthews, JB, Pemberton, JM, Nussey, HH and Graham, AL (2014) Heritable, heterogeneous, and costly resistance of sheep against nematodes and potential feedbacks to epidemiological dynamics. American Naturalist 184, S58–S76.CrossRefGoogle ScholarPubMed
Hayward, AD, Skuce, PJ and Mcneilly, TN (2021) The influence of liver fluke infection on production in sheep and cattle: a meta-analysis. International Journal for Parasitology 51, 913–924.CrossRefGoogle ScholarPubMed
Hoberg, EP, Kocan, AA and Rickard, LG (2001) Gastrointestinal strongyles in wild ruminants. In Samuel, W, Pybus, M and Kocan, AA (eds), Diseases of Wild Mammals. Ames, IA, USA: Iowa State University Press, pp. 193–227.CrossRefGoogle Scholar
Hudson, P, Rizzoli, A, Grenfell, BT, Heesterbeek, H and Dobson, AP (2002) The Ecology of Wildlife Diseases. Oxford, UK: Oxford University Press.Google Scholar
Irvine, RJ, Corbishley, H, Pilkington, JG and Albon, SD (2006) Low-level parasitic worm burdens may reduce body condition in free-ranging red deer (Cervus elaphus). Parasitology 133, 465–475.CrossRefGoogle Scholar
Kenyon, F, McBean, D, Greer, AW, Burgess, CGS, Morrison, AA, Bartley, DJ, Bartley, Y, Devin, L, Nath, M and Jackson, F (2013) A comparative study of the effects of four treatment regimes on ivermectin efficacy, body weight and pasture contamination in lambs naturally infected with gastrointestinal nematodes in Scotland. International Journal for Parasitology: Drugs and Drug Resistance 3, 77–84.Google ScholarPubMed
Loison, A, Langvatn, R and Solberg, EJ (1999) Body mass and winter mortality in red deer calves: disentangling sex and climate effects. Ecography 22, 20–30.CrossRefGoogle Scholar
Mason, PC (1989) Elaphostrongylus cervi – a review. Surveillance 16, 3–10.Google Scholar
McSorley, HJ and Maizels, RM (2012) Helminth infections and host immune regulation. Clinical Microbiology Reviews 25, 585–608.CrossRefGoogle ScholarPubMed
Moore, SL and Wilson, K (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297, 2015–2018.CrossRefGoogle ScholarPubMed
Murray, DL, Cary, JR and Keith, LB (1997) Interactive effects of sublethal nematodes and nutritional status on snowshoe hare vulnerability to predation. Journal of Animal Ecology 66, 250–264.CrossRefGoogle Scholar
RStudio Team (2021) RStudio: Integrated Development Environment for R. Boston, MA, USA: RStudio, PBC.Google Scholar
Sparks, AM, Hayward, AD, Watt, K, Pilkington, JG, Pemberton, JM, Johnston, SE, Mcneilly, TN and Nussey, DH (2020) Maternally derived anti-helminth antibodies predict offspring survival in a wild mammal. Proceedings of the Royal Society B 287, 20201931.CrossRefGoogle Scholar
Taylor, MA, Coop, RL and Wall, RL (2015 a) Laboratory Diagnosis of Parasitism. Veterinary Parasitology. Chichester, UK: John Wiley & Sons, Inc., pp. 259–312.CrossRefGoogle Scholar
Taylor, MA, Coop, RL and Wall, RL (2015 b) Veterinary Helminthology. Veterinary Parasitology. Chichester, UK: John Wiley & Sons, Inc., pp. 1–109.CrossRefGoogle Scholar
Tompkins, DM, Dobson, AP, Arneberg, P, Begon, ME, Cattadori, IM, Greenman, JV, Heesterbeek, JAP, Hudson, PJ, Newborn, D, Rizzoli, AP, Rosà, R, Rosso, F and Wilson, K (2001) Parasites and host population dynamics. In Hudson, PJ, Rizzoli, A, Grenfell, BT, Heesterbeek, H and Dobson, AP (eds), The Ecology of Wildlife Diseases. Oxford, UK: Oxford University Press, pp. 45–62.Google Scholar
Wickham, H (2016) ggplot2: Elegant Graphics for Data Analysis. New York: Springer-Verlag. Available at https://ggplot2.tidyverse.org.CrossRefGoogle Scholar
Wilson, K, Grenfell, BT, Pilkington, JG, Boyd, HEG and Gulland, FMD (2003) Parasites and their impact. In Pemberton, JM and Clutton-Brock, TH (eds), Soay Sheep: Dynamics and Selection in an Island Population. Cambridge, UK: Cambridge University Press, pp. 113–165.CrossRefGoogle Scholar