Hostname: page-component-7479d7b7d-pfhbr Total loading time: 0 Render date: 2024-07-13T18:39:24.706Z Has data issue: false hasContentIssue false

Relationship between the excretion of eggs of parasitic helminths in roe deer and local livestock density

Published online by Cambridge University Press:  01 June 2020

H. Verheyden*
Affiliation:
Université de Toulouse, INRAE, Comportement & Ecologie de la Faune Sauvage, Chemin de Borde-Rouge, Castanet-TolosanF-31326, France
C. Richomme
Affiliation:
ANSES, Nancy Laboratory for Rabies & Wildlife, MalzévilleF-54220, France
J. Sevila
Affiliation:
Université de Toulouse, INRAE, Comportement & Ecologie de la Faune Sauvage, Chemin de Borde-Rouge, Castanet-TolosanF-31326, France ANSES, Nancy Laboratory for Rabies & Wildlife, MalzévilleF-54220, France Université de Toulouse, UMR 1225 IHAP INRAE/ENVT, 23 Chemin des Capelles, ToulouseF-31076, France
J. Merlet
Affiliation:
Université de Toulouse, INRAE, Comportement & Ecologie de la Faune Sauvage, Chemin de Borde-Rouge, Castanet-TolosanF-31326, France
B. Lourtet
Affiliation:
Université de Toulouse, INRAE, Comportement & Ecologie de la Faune Sauvage, Chemin de Borde-Rouge, Castanet-TolosanF-31326, France
Y. Chaval
Affiliation:
Université de Toulouse, INRAE, Comportement & Ecologie de la Faune Sauvage, Chemin de Borde-Rouge, Castanet-TolosanF-31326, France
H. Hoste
Affiliation:
Université de Toulouse, UMR 1225 IHAP INRAE/ENVT, 23 Chemin des Capelles, ToulouseF-31076, France
*
Author for correspondence: H. Verheyden, E-mail: helene.verheyden@inrae.fr

Abstract

Because of their continuing expansion, wildlife ruminant species that prosper in rural landscapes may be increasingly affected by and/or contribute to the circulation of certain generalist pathogens also infecting domestic ruminants, when they share common spaces or resources. In this study, we aimed to test the hypothesis that parasitism with gastrointestinal nematodes (GINs) of wild roe deer inhabiting different rural landscapes is correlated with livestock density. We used faecal egg counts of GINs and spatial data of 74 GPS-collared roe deer, inhabiting various landscapes from closed forests to open fields, together with weekly records of livestock abundances on pasture. We tested whether the excretion of GIN eggs in roe deer was influenced by the density of livestock in their home range over the grazing season. Our results showed that all of the roe deer home ranges, except four, contained pastures occupied by livestock. Excretion of GIN eggs occurred in 77% of the roe deer. The excretion of GIN eggs in roe deer tended to increase with livestock density in their home range. This result suggests, but does not prove, a higher risk of ingesting GIN larvae originating from livestock dung. In the context of increasing overlap between roe deer and livestock ranges, the exchange of pathogens between both hosts is plausible, although species identity of the parasites present was not determined. Assessing which GIN species are shared between wild and domestic ruminants, and how this may affect the health of both hosts, is a central question for future research in the context of interspecific pathogen circulation.

Type
Research Paper
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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

Abbas, F, Morellet, N, Hewison, AJM, et al. (2011) Landscape fragmentation generates spatial variation of diet composition and quality in a generalist herbivore. Oecologia 167, 401411.CrossRefGoogle Scholar
Albery, GF, Becker, DJ, Kenyon, F, Nussey, DH and Pemberton, JM (2019) The Fine-scale landscape of immunity and parasitism in a Wild Ungulate Population. Integrative and Comparative Biology, 111. doi: 10.1093/icb/icz016.Google Scholar
Avramenko, RW, Redman, EM, Lewis, R, Bichuette, MA, Palmeira, BM, Yazwinski, TA and Gilleard, JS (2017) The use of nemabiome metabarcoding to explore gastro-intestinal nematode species diversity and anthelmintic treatment effectiveness in beef calves. International Journal for Parasitology 13, 893902.CrossRefGoogle Scholar
Becker, DJ, Streicker, DG and Altizer, S (2015) Linking anthropogenic resources to wildlife-pathogen dynamics: a review and meta-analysis. Ecology Letters 18, 483495.CrossRefGoogle ScholarPubMed
Body, G, Ferté, 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.CrossRefGoogle ScholarPubMed
Börger, L, Franconi, N, De Michele, G, Gantz, A, Meschi, F, Manica, A, Lovari, S and Coulson, T (2006) Effects of sampling regime on the mean and variance of home range size estimates. Journal of Animal Ecology 75, 13931405.CrossRefGoogle ScholarPubMed
Cargnelutti, B, Coulon, A, Hewison, AJM, Goulard, M, Angibault, JM and Morellet, N (2007) Testing Global Positioning System performance for wildlife monitoring using mobile collars and known reference points. The Journal of Wildlife Management 71, 13801387.CrossRefGoogle Scholar
Cerutti, MC, Citterio, CV, Bazzocchi, C, Epis, S, D'Amelio, S, Ferrari, N and Lanfranchi, P (2010) Genetic variability of Haemonchus contortus (Nematoda: Trichostrongyloidea) in alpine ruminant host species. Journal of Helminthology 84, 276283.CrossRefGoogle ScholarPubMed
Chintoan-Uta, C, Morgan, ER, Skuce, PJ and Coles, GC (2014) Wild deer as potential vectors of anthelmintic-resistant abomasal nematodes between cattle and sheep farms. Proceedings of the Biological Society 281, 20132985.CrossRefGoogle ScholarPubMed
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 373, 20170197.CrossRefGoogle ScholarPubMed
De Mendonca, RMA, Leite, RC, Lana, AMQ and Costa, JO (2014) Parasitic helminth infection in young cattle raised on silvopasture and open-pasture in Southeastern Brazil. Agroforestry Systems 88, 5362.CrossRefGoogle Scholar
Forristal, VE, Creel, S, Taper, ML, Scurlock, BM and Cross, PC (2012) Aggregation on fecal glucocorticoid metabolite concentrations in elk. The Journal of Wildlife Management 76, 694702.CrossRefGoogle Scholar
Gilot-Fromont, E, Jégo, M, Bonenfant, C, Gibert, P, Rannou, B, Klein, F and Gaillard, J-M (2012) Immune phenotype and body condition in roe deer: individuals with high body condition have different, not stronger immunity. PLoS One 7, e45576.CrossRefGoogle Scholar
Goater, CP and Colwell, DD (2007) Epidemiological characteristics of an invading parasite: Dicrocoelium dendriticum in sympatric wapiti and beef cattle in southern Alberta, Canada. The Journal of Parasitology 93, 491494.CrossRefGoogle ScholarPubMed
Gunn, A and Irvine, RJ (2003) Subclinical parasitism and ruminant foraging strategies – a review. Wildlife Society Bulletin 31, 117126.Google Scholar
Han, B, Kramer, AM and Drake, JM (2016) Global patterns of zoonotic disease in mammals. Trends in Parasitology 32, 565577.CrossRefGoogle ScholarPubMed
Hewison, AJM, Vincent, J-P and Reby, D (1998) Social organisation of European roe deer. pp. 189219in Andersen, R, Duncan, P and Linnell, JDC (Eds) The European roe deer: the biology of success. Oslo, Scandinavian University Press.Google Scholar
Hewison, AJM, Vincent, J-P, Joachim, J, Angibault, J-M, Cargnelutti, B and Cibien, C (2001) The effects of woodland fragmentation and human activity on roe deer distribution in agricultural landscapes. Canadian Journal of Zoology – Revue Canadienne de Zoologie 79, 679689.CrossRefGoogle Scholar
Hewison, AJM, Morellet, N, Verheyden, H, et al. (2009) Landscape fragmentation influences winter body mass of roe deer. Ecography 32, 10621070.CrossRefGoogle Scholar
Horcajada-Sánchez, F, Navarro-Castilla, A, Boadella, M and Barja, I (2018) Influence of livestock, habitat type, and density of roe deer (Capreolus capreolus) on parasitic larvae abundance and infection seroprevalence in wild populations of roe deer from central Iberian Peninsula. Mammal Research 63, 213222.CrossRefGoogle Scholar
Hoste, H, Jackson, F, Athanasiadou, S, Thamsborg, SM and Hoskin, SO (2006) The effects of tannin-rich plants on parasitic nematodes in ruminants. Trends in Parasitology 22, 253261.CrossRefGoogle ScholarPubMed
Hutchings, MR, Judge, J, Gordon, IJ, Athanasiadou, S and Kyriazakis, I (2006) Use of trade-off theory to advance understanding of herbivore-parasite interactions. Mammal Review 36, 116.CrossRefGoogle Scholar
Jones, KE, Patel, NG, Levy, MA, Storeygard, A, Balk, D, Gittleman, JL and Daszak, P (2008) Global trends in emerging infectious diseases. Nature 451, 990994.CrossRefGoogle ScholarPubMed
Lamberti, P, Mauri, L, Merli, E, Dusi, S and Apollonio, M (2006) Use of space and habitat selection by roe deer Capreolus capreolus in a Mediterranean coastal area: how does woods landscape affect home range? Journal of Ethology 24, 181188.CrossRefGoogle Scholar
Lembo, T, Hampson, K, Haydon, DT, et al. (2008) Exploring reservoir dynamics: a case study of rabies in the Serengeti ecosystem. Journal of Applied Ecology 45, 12461257.CrossRefGoogle ScholarPubMed
Linnel, JDC and Sachos, FE (2011) Status and distribution patterns of European ungulates: genetics, population history and conservation. pp. 1253in Putman, R, Apollonio, M, and Anderson, R (Eds) Ungulate management in Europe. Cambridge, Cambridge University Press.CrossRefGoogle Scholar
Martin, C, Pastoret, PP, Brochier, B, Humblet, MF and Saegerman, C (2011) A survey of the transmission of infectious diseases/infections between wild and domestic ungulates in Europe. Veterinary Research 42, 7085.CrossRefGoogle ScholarPubMed
McGhee, MB, Nettles, VF, Rollor, EA, Prestwood, AK and Davidson, WR (1981) Studies on cross-transmission and pathogenicity of Haemonchus contortus in white-tailed deer, domestic cattle and sheep. Journal of Wildlife Diseases 17, 353364.CrossRefGoogle ScholarPubMed
Megyesi, SL, Königová, A, Babják, M, et al. (2020) Wild ruminants as a potential risk factor for transmission of drug resistance in the abomasal nematode Haemonchus contortus. European Journal of Wildlife Research 66, 9.CrossRefGoogle Scholar
Morellet, N, Verheyden, H, Angibault, JM, Cargnelutti, B, Lourtet, B and Hewison, MAJ (2009) The effect of capture on ranging behaviour and activity of the European roe deer Capreolus capreolus. Wildlife Biology 15, 278287.CrossRefGoogle Scholar
Morgan, ER, Shaikenov, B, Torgerson, PR, Medley, GF and Milner-Gulland, EJ (2005) Helminths of Saiga antelope in Kazakhstan: implications for conservation and livestock production. Journal of Wildlife Diseases 41, 149162.CrossRefGoogle ScholarPubMed
Morgan, ER, Lundervold, M, Medley, GF, Shaikenov, BS, Torgerson, PR and Milner-Gulland, EJ (2006a) Assessing risks of disease transmission between wildlife and livestock: the Saiga antelope as a case study. Biological Conservation 131, 244254.CrossRefGoogle Scholar
Morgan, ER, Torgerson, PR, Shaikenov, BS, Usenbayev, AE, Moore, ABM, Medley, GF and Milner-Gulland, EJ (2006b) Agricultural restructuring and gastrointestinal parasitism in domestic ruminants on the rangelands of Kazakhstan. Veterinary Parasitology 139, 180191.CrossRefGoogle Scholar
Moskwa, B, Bien, J, Cybulska, A, Kornacka, A, Krzysiak, M, Cencek, T and Cabaj, W (2015) The first identification of a blood-sucking abomasal nematode Ashworthius sidemi in cattle (Bos taurus) using simple polymerase chain reaction (PCR). Veterinary Parasitology 211, 106109.CrossRefGoogle Scholar
Murray, MH, Becker, DJ, Hall, RJ and Hernandez, SM (2016) Wildlife health and supplemental feeding: A review and management recommendations. Biological Conservation 204, 163174.CrossRefGoogle Scholar
Nagy, G, Csivincsik, A, Sugár, L and Zsolnai, A (2017) Benzimidazole resistance within red deer, roe deer and sheep populations within a joint habitat in Hungary. Small Ruminant Research 149, 172175.CrossRefGoogle Scholar
Obanda, V, Maingi, N, Muchemi, G, Ng'ang’a, CJ, Angelone, S and Archie, EA (2019) Infection dynamics of gastrointestinal helminths in sympatric non-human primates, livestock and wild ruminants in Kenya. Plos One 14(6), e0217929.CrossRefGoogle ScholarPubMed
Ofstad, EG, Herfindal, I, Solberg, EJ and Saether, BE (2016) Home ranges, habitat and body mass: simple correlates of home range size in ungulates. Proceedings of the Royal Society B 283, 20161234.CrossRefGoogle ScholarPubMed
Oja, R, Velström, K, Moks, E, Jokelainen, P and Lassen, B (2017) How does supplementary feeding affect endoparasite infection in wild boar? Parasitology Research 116, 21312137.CrossRefGoogle ScholarPubMed
Preston, SJM, Sandeman, M, Gonzalez, J and Piedrafita, D (2014) Current status for gastrointestinal nematode diagnosis in small ruminants: where are we and where are we going? Journal of Immunology Research 2014. Article ID. 210350, pp. 12 pages. http://dx.doi.org/10.1155/2014/210350.CrossRefGoogle ScholarPubMed
Raynaud, JP (1970) Etude de l'efficacité d'une technique de coproscopie quantitative pour le diagnostic de routine et le contrôle desinfestations parasitaires des bovins, ovins, équins et porcins. Annales de Parasitologie (Paris) 45, 321342.Google Scholar
R Development Core Team (2013) R: a language and environment for statistical computing. 552 Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org.Google Scholar
Roeber, F, Jex, AR and Gasser, RB (2013) Advances in the diagnosis of key gastrointestinal nematode infections of livestock, with an emphasis on small ruminants. Biotechnology Advances 31, 11351152.CrossRefGoogle Scholar
Santos, LL, Salgado, JA, Drummond, MG, Bastianetto, E, Santos, CP, Brasil, BSAF, Taconeli, CA and Oliveira, DAA (2020) Molecular method for the semiquantitative identification of gastrointestinal nematodes in domestic ruminants. Parasitology Research 119, 529543.CrossRefGoogle ScholarPubMed
Segonds-Pichon, A, Ferté, H, Gaillard, J-M, Lamarque, F and Duncan, P (2000) Nematode infestation and body condition in roe deer (Capreolus capreolus). Game and Wildlife Science 17, 241258.Google Scholar
Sevila, J, Richomme, C, Hoste, H, et al. (2014) Does land use within the home range drive the exposure of Roe deer (Capreolus capreolus) to two abortive pathogens in a rural agro-ecosystem? Acta Theriologica 59, 571581.CrossRefGoogle Scholar
Sorensen, A, van Beest, FM and Brook, RK (2014) Impacts of wildlife baiting and supplemental feeding on infectious disease transmission risk: a synthesis of knowledge. Preventive Veterinary Medicine 113, 356363.CrossRefGoogle ScholarPubMed
Tapia-Escarate, D, Pomroy, WE, Scott, I, Wilson, PR and Lopez-Villalobos, N (2015) Establishment rate of sheep gastrointestinal nematodes in farmed red deer (Cervus elaphus). Veterinary Parasitology 209, 138141.CrossRefGoogle Scholar
Tomczuk, K, Szczepaniak, K, Grzybek, M, Studzinska, M, Demkowska-Kutrzepa, M, Roczen-Karczmarz, M, Kostro, K and Krakowski, L (2014) Gastro-intestinal parasite prevention in wild roe deer in selected hunting areas in south-eastern Poland. Medycyna Weterynaryjna 70, 630635.Google Scholar
Verheyden-Tixier, H and Duncan, P (2000) Selection for small amounts of hydrolysable tannins by a concentrate-selecting mammalian herbivore. Journal of Chemical Ecology 26, 351358.CrossRefGoogle Scholar
Walker, JG, Plein, M, Morgan, ER and Vesk, PA (2017) Uncertain links in host–parasite networks: lessons for parasite transmission in a multi-host system. Philosophical Transactions of the Royal Society B 372, 20160095.CrossRefGoogle Scholar
Winter, J, Rehbein, S and Joachim, A (2018) Transmission of helminths between species of ruminants in Austria appears more likely to occur than generally assumed. Frontiers in Veterinary Science 5, 30.CrossRefGoogle ScholarPubMed
Woolhouse, ME and Gowtage-Sequeria, S (2005) Host range and emerging and reemerging pathogens. Emerging Infectious Diseases 11, 18421847.CrossRefGoogle ScholarPubMed
Worton, BJ (1989) Kernel methods for estimating the utilization distribution in home range studies. Ecology 70, 164168.CrossRefGoogle Scholar
Zaffaroni, E, Manfredi, MT, Citterio, C, Sala, M, Piccolo, G and Lanfranchi, P (2000) Host specificity of abomasal nematodes in free ranging alpine ruminants. Veterinary Parasitology 90, 221230.CrossRefGoogle ScholarPubMed