Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-26T08:36:41.114Z Has data issue: false hasContentIssue false
  • English
  • Français

Reproductive females and young mouflon (Ovis gmelini musimon × Ovis sp.) in poor body condition are the main spreaders of gastrointestinal parasites

Published online by Cambridge University Press:  17 February 2021

Gilles Bourgoin Open the ORCID record for Gilles Bourgoin [Opens in a new window] ,
Elodie Portanier ,
Marie-Thérèse Poirel ,
Christian Itty ,
Jeanne Duhayer ,
Slimania Benabed ,
Anne Cockenpot ,
Marie-Pierre Callait-Cardinal  and
Mathieu Garel
Gilles Bourgoin*
Affiliation:
Laboratoire de parasitologie vétérinaire, Université de Lyon, VetAgro Sup – Campus Vétérinaire de Lyon, 1 avenue Bourgelat, BP 83, F-69280 Marcy l'Etoile, France Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon 1, CNRS, UMR 5558, F-69622Villeurbanne, France
Elodie Portanier
Affiliation:
Laboratoire de parasitologie vétérinaire, Université de Lyon, VetAgro Sup – Campus Vétérinaire de Lyon, 1 avenue Bourgelat, BP 83, F-69280 Marcy l'Etoile, France Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon 1, CNRS, UMR 5558, F-69622Villeurbanne, France
Marie-Thérèse Poirel
Affiliation:
Laboratoire de parasitologie vétérinaire, Université de Lyon, VetAgro Sup – Campus Vétérinaire de Lyon, 1 avenue Bourgelat, BP 83, F-69280 Marcy l'Etoile, France Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon 1, CNRS, UMR 5558, F-69622Villeurbanne, France
Christian Itty
Affiliation:
Office Français de la Biodiversité, Unité Ongulés Sauvages, 5 allée de Bethléem, Z.I. Mayencin, F-38610Gières, France
Jeanne Duhayer
Affiliation:
Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon 1, CNRS, UMR 5558, F-69622Villeurbanne, France
Slimania Benabed
Affiliation:
Laboratoire de parasitologie vétérinaire, Université de Lyon, VetAgro Sup – Campus Vétérinaire de Lyon, 1 avenue Bourgelat, BP 83, F-69280 Marcy l'Etoile, France Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon 1, CNRS, UMR 5558, F-69622Villeurbanne, France
Anne Cockenpot
Affiliation:
Laboratoire de parasitologie vétérinaire, Université de Lyon, VetAgro Sup – Campus Vétérinaire de Lyon, 1 avenue Bourgelat, BP 83, F-69280 Marcy l'Etoile, France
Marie-Pierre Callait-Cardinal
Affiliation:
Laboratoire de parasitologie vétérinaire, Université de Lyon, VetAgro Sup – Campus Vétérinaire de Lyon, 1 avenue Bourgelat, BP 83, F-69280 Marcy l'Etoile, France Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon 1, CNRS, UMR 5558, F-69622Villeurbanne, France
Mathieu Garel
Affiliation:
Office Français de la Biodiversité, Unité Ongulés Sauvages, 5 allée de Bethléem, Z.I. Mayencin, F-38610Gières, France
*
Author for correspondence: Gilles Bourgoin, E-mail: gilles.bourgoin@vetagro-sup.fr
Get access Rights & Permissions [Opens in a new window]

Abstract

Several individual, environmental and parasitic factors can influence the impacts of parasites on host's fitness and on host's ability to transmit these parasites to new hosts. Identifying these factors and the individuals who play a greater role in parasite transmission is of main concern for the development of parasite control strategies. In the present study, we aimed to describe the diversity of gastrointestinal parasites and to identify the individual factors influencing the faecal spreading of parasites in a free-ranging population of Mediterranean mouflon. From the analysis of 433 faecal samples, we found Eimeria spp. and gastrointestinal strongyles (GIS) were the most common parasites (>94%). The faecal oocyst counts of Eimeria spp. were the highest during the first years of life. It was 1.6 times higher in females than in males and 2.5 times higher in individuals in poor than in good body condition. Similarly, the faecal egg count of GIS was higher in females and decreased with age, but only in males. Finally, reproductive females had GIS faecal egg count values 2.6 times higher than non-reproductive females. Management strategies of parasites should thus primarily focus on reproductive females and young individuals in poor body condition as they represent the main contamination source of the environment.

Keywords

Eimeria spp.nematodestrongyleungulatewild population
Type
Research Article
Information
Parasitology , Volume 148 , Issue 7 , June 2021 , pp. 809 - 818
Check for updates
Copyright
Copyright © The Author(s) 2021. 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

Albon, S, Stien, A, Irvine, R, Langvatn, R, Ropstad, E and Halvorsen, O (2002) The role of parasites in the dynamics of a reindeer population. Proceedings of the Royal Society of London B: Biological Sciences 269, 1625–1632.CrossRefGoogle ScholarPubMed
Aleuy, OA, Ruckstuhl, K, Hoberg, EP, Veitch, A, Simmons, N and Kutz, SJ (2018) Diversity of gastrointestinal helminths in Dall's sheep and the negative association of the abomasal nematode, Marshallagia marshalli, with fitness indicators. PLoS One 13, e0192825.CrossRefGoogle ScholarPubMed
Anderson, RM and Gordon, DM (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
Balicka-Ramisz, A, Laurans, Ł, Jurczyk, P, Kwita, E and Ramisz, A (2017) Gastrointestinal nematodes and the deworming of mouflon (Ovis Aries Musimon) from Goleniowska Forest in West Pomerania province, Poland. Annals of Parasitology 63, 27–32. doi: 10.17420/ap6301.81.Google ScholarPubMed
Barton, K and Barton, MK (2019). Package ‘MuMIn’: Multi-Model Inference. R package version 1.Google Scholar
Bates, D, Mächler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.CrossRefGoogle Scholar
Baudière, A (2020) Recherches phytogéographiques sur la bordure méridionale du Massif Central français (Les Monts de l’Espinouse). Thèse de doctorat, Université de Montpellier, France.Google Scholar
Beldomenico, PM and Begon, M (2010) Disease spread, susceptibility and infection intensity: vicious circles? Trends in Ecology & Evolution 25, 21–27.CrossRefGoogle ScholarPubMed
Beldomenico, PM, Telfer, S, Gebert, S, Lukomski, L, Bennett, M and Begon, M (2008) Poor condition and infection: a vicious circle in natural populations. Proceedings of the Royal Society of London B: Biological Sciences 275, 1753–1759.Google ScholarPubMed
Benavides, JA, Huchard, E, Pettorelli, N, King, AJ, Brown, ME, Archer, CE, Appleton, CC, Raymond, M and Cowlishaw, G (2012) From parasite encounter to infection: multiple-scale drivers of parasite richness in a wild social primate population. American Journal of Physical Anthropology 147, 52–63.CrossRefGoogle Scholar
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, 635–646.CrossRefGoogle ScholarPubMed
Bon, R, Cugnasse, J-M, Dubray, D, Gibert, P, Houard, P and Rigaud, P (1991) Le mouflon de Corse. Revue d’Écologie (La Terre et La Vie) 6, 67–110.Google Scholar
Bon, R, Dardaillon, M and Estevez, I (1993) Mating and lambing periods as related to age of female mouflon. Journal of Mammalogy 74, 752–757.CrossRefGoogle Scholar
Bourgoin, G, Marchand, P, Hewison, AM, Ruckstuhl, KE and Garel, M (2018) Social behaviour as a predominant driver of sexual, age-dependent and reproductive segregation in Mediterranean mouflon. Animal Behaviour 136, 87–100.CrossRefGoogle Scholar
Brearley, G, Rhodes, J, Bradley, A, Baxter, G, Seabrook, L, Lunney, D, Liu, Y and McAlpine, C (2013) Wildlife disease prevalence in human-modified landscapes: wildlife disease in human-modified landscapes. Biological Reviews 88, 427–442.CrossRefGoogle ScholarPubMed
Breheny, P and Burchett, W (2017) Visualization of regression models using visreg. The R Journal 9, 56.CrossRefGoogle Scholar
Burdick, RK, Quiroz, J and Iyer, HK (2006) The present status of confidence interval estimation for one-factor random models. Journal of Statistical Planning and Inference 136, 4307–4325.CrossRefGoogle Scholar
Burnham, KP and Anderson, DR (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. 2nd Edn. New York, USA: Springer.Google Scholar
Cabaret, J, Gasnier, N and Jacquiet, P (1998) Faecal egg counts are representative of digestive-tract strongyle worm burdens in sheep and goats. Parasite 5, 137–142.CrossRefGoogle ScholarPubMed
Cable, J, Barber, I, Boag, B, Ellison, AR, Morgan, ER, Murray, K, Pascoe, EL, Sait, SM, Wilson, AJ and Booth, M (2017) Global change, parasite transmission and disease control: lessons from ecology. Philosophical Transactions of the Royal Society B: Biological Sciences 372, 20160088.CrossRefGoogle ScholarPubMed
Carrau, T, Perez, D, Silva, LM, Macías, J, Martínez-Carrasco, C, Taubert, A, Hermosilla, C and de Ybáñez, RR (2016) Postparturient rise in the excretion of Eimeria Spp. in Manchega dairy sheep. Journal of Veterinary Medicine and Research 3, 1047.Google Scholar
Cassinello, J (2018) Detailed coverage of invasive species threatening livelihoods and the environment worldwide. Retrieved from CABI – Invasive Species Compendium website: https://www.cabi.org/isc/datasheet/71353# (Accessed 14 June 2020).Google Scholar
Chandra, RK (1996) Nutrition, immunity and infection: from basic knowledge of dietary manipulation of immune responses to practical application of ameliorating suffering and improving survival. Proceedings of the National Academy of Sciences 93, 14304–14307.CrossRefGoogle ScholarPubMed
Chartier, C and Paraud, C (2012) Coccidiosis due to Eimeria In sheep and goats, a review. Small Ruminant Research 103, 84–92.CrossRefGoogle Scholar
Chessa, B, Pereira, F, Arnaud, F, Amorim, A, Goyache, F, Mainland, I, Kao, RR, Pemberton, JM, Beraldi, D, Stear, MJ, Alberti, A, Pittau, M, Iannuzzi, L, Banabazi, MH, Kazwala, RR, Zhang, Y, Arranz, JJ, Ali, BA, Wang, Z, Uzun, M, Dione, MM, Olsaker, I, Holm, L-E, Saarma, U, Ahmad, S, Marzanov, N, Eythorsdottir, E, Holland, MJ, Ajmone-Marsan, P, Bruford, MW, Kantanen, J, Spencer, TE and Palmarini, M (2009) Revealing the history of sheep domestication using retrovirus integrations. Science (New York, N.Y.) 324, 532–536.CrossRefGoogle ScholarPubMed
Cheynel, L, Lemaître, J-F, Gaillard, J-M, Rey, B, Bourgoin, G, Ferté, H, Jégo, M, Débias, F, Pellerin, M, Jacob, L and Gilot-Fromont, E (2017) Immunosenescence patterns differ between populations but not between sexes in a long-lived mammal. Scientific Reports 7, 13700.CrossRefGoogle ScholarPubMed
Citterio, CV, Caslini, C, Milani, F, Sala, M, Ferrari, N and Lanfranchi, P (2006) Abomasal nematode community in an alpine chamois (Rupicapra r. rupicapra) population before and after a die-off. Journal of Parasitology 92, 918–927.CrossRefGoogle Scholar
Clutton-Brock, TH, Albon, SD and Guinness, FE (1989) Fitness costs of gestation and lactation in wild mammals. Nature 337, 260–262.CrossRefGoogle ScholarPubMed
Connan, RM (1976) Effect of lactation on the immune response to gastrointestinal nematodes. The Veterinary Record 99, 476–477.CrossRefGoogle ScholarPubMed
Craig, BH, Pilkington, JG and Pemberton, JM (2006) Gastrointestinal nematode species burdens and host mortality in a feral sheep population. Parasitology 133, 485–496.CrossRefGoogle Scholar
Cressler, CE, Nelson, WA, Day, T and McCauley, E (2014) Disentangling the interaction among host resources, the immune system and pathogens. Ecology Letters 17, 284–293.CrossRefGoogle ScholarPubMed
Cugnasse, J-M (1995) L'animal sauvage peut-il être un atout économique? Bulletin Mensuel de l'Office National de la Chasse 156, 22–25.Google Scholar
Davidson, RK, Ličina, T, Gorini, L and Milner, JM (2015) Endoparasites in a Norwegian moose (Alces alces) population – Faunal diversity, abundance and body condition. International Journal for Parasitology: Parasites and Wildlife 4, 29–36.Google Scholar
Debeffe, L, Mcloughlin, PD, Medill, SA, Stewart, K, Andres, D, Shury, T, Wagner, B, Jenkins, E, Gilleard, JS and Poissant, J (2016) Negative covariance between parasite load and body condition in a population of feral horses. Parasitology 143, 983–997.CrossRefGoogle Scholar
Deméautis, G (1981) Rapport d’étude sur le mouflon de Corse. Ajaccio, France: Parc Naturel Régional de Corse, 75pp.Google Scholar
Deméautis, G (1985) Eco-épidémiologie parasitaire: éléments d'enquête autour d'un ongulé sauvage Corse, le mouflon (Ovis ammon musimon Schreber, 1782). Bulletin d'informations sur la pathologie des animaux sauvages en France 3, 65–82.Google Scholar
Descamps, S, Aars, J, Fuglei, E, Kovacs, KM, Lydersen, C, Pavlova, O, Pedersen, ÅØ, Ravolainen, V and Strøm, H (2017) Climate change impacts on wildlife in a High Arctic archipelago – Svalbard, Norway. Global Change Biology 23, 490–502.CrossRefGoogle Scholar
Drimtzia, A and Papadopoulos, E (2016) Reduction rate of nematode egg counts and third-stage larvae development from sheep and goat faeces preserved at 4°C. Journal of the Hellenic Veterinary Medical Society 67, 177–182.CrossRefGoogle Scholar
Dunsmore, JD (1965) Ostertagia spp. in lambs and pregnant ewes. Journal of Helminthology 39, 159–184.CrossRefGoogle ScholarPubMed
Dyk, V and Chroust, K (1973) Helminths and coccidia in mouflons of the School Forest District Krtiny near Blansko. Acta Veterinaria. Brno 42, 159–173.Google Scholar
Festa-Bianchet, M (1989) Individual differences, parasites, and the costs of reproduction for bighorn ewes (Ovis canadensis). The Journal of Animal Ecology 58, 785–795.CrossRefGoogle Scholar
Folstad, I and Karter, AJ (1992) Parasites, bright males, and the immunocompetence handicap. The American Naturalist 139, 603–622.CrossRefGoogle Scholar
Froy, H, Sparks, AM, Watt, K, Sinclair, R, Bach, F, Pilkington, JG, Pemberton, JM, McNeilly, TN and Nussey, DH (2019) Senescence in immunity against helminth parasites predicts adult mortality in a wild mammal. Science (New York, N.Y.) 365, 1296–1298.CrossRefGoogle Scholar
Garel, M, Cugnasse, J-M, Gaillard, J-M, Loison, A, Gibert, P, Douvre, P and Dubray, D (2005) Reproductive output of female mouflon (Ovis gmelini Musimon × Ovis sp.): a comparative analysis. Journal of Zoology 266, 65–71.CrossRefGoogle Scholar
Garel, M, Cugnasse, J-M, Maillard, D, Gaillard, J-M, Hewison, AJ and Dubray, D (2007) Selective harvesting and habitat loss produce long-term life history changes in a mouflon population. Ecological Applications 17, 1607–1618.CrossRefGoogle Scholar
Geist, V (1966) Validity of horn segment counts in aging bighorn sheep. The Journal of Wildlife Management 30, 634–635.CrossRefGoogle Scholar
Gervasi, SS, Civitello, DJ, Kilvitis, HJ and Martin, LB (2015) The context of host competence: a role for plasticity in host–parasite dynamics. Trends in Parasitology 31, 419–425.CrossRefGoogle ScholarPubMed
Gorsich, EE, Ezenwa, VO and Jolles, AE (2014) Nematode-coccidia parasite co-infections in African buffalo: epidemiology and associations with host condition and pregnancy. International Journal for Parasitology: Parasites and Wildlife 3, 124–134.Google ScholarPubMed
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
Gulland, FMD and Fox, M (1992) Epidemiology of nematode infections of Soay sheep (Ovis Aries L.) on St Kilda. Parasitology 105, 481–492.CrossRefGoogle ScholarPubMed
Habig, B and Archie, EA (2015) Social status, immune response and parasitism in males: a meta-analysis. Philosophical Transactions of the Royal Society B 370, 20140109.CrossRefGoogle ScholarPubMed
Hayward, AD (2013) Causes and consequences of intra- and inter-host heterogeneity in defence against nematodes. Parasite Immunology 35, 362–373.Google ScholarPubMed
Hayward, AD, Wilson, AJ, Pilkington, JG, Pemberton, JM and Kruuk, LEB (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, 3477–3485.CrossRefGoogle Scholar
Hille, G (2003) Untersuchungen zum Endoparasitenbefall des Muffelwildes in Thüringen (Veterinary thesis). Universität Leipzig, Leipzig, Germany. 196 pp.Google Scholar
Hoberg, EP, Polley, L, Jenkins, EJ and Kutz, SJ (2008) Pathogens of domestic and free-ranging ungulates: global climate change in temperate to boreal latitudes across North America. Revue scientifique et technique-Office international des épizooties 27, 511–528.CrossRefGoogle ScholarPubMed
Houdijk, JGM (2008) Influence of periparturient nutritional demand on resistance to parasites in livestock. Parasite Immunology 30, 113–121.CrossRefGoogle ScholarPubMed
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
Karrow, NA, Goliboski, K, Stonos, N, Schenkel, F and Peregrine, A (2014) Genetics of helminth resistance in sheep. Canadian Journal of Animal Science 94, 1–9.CrossRefGoogle Scholar
Klein, SL (2000) The effects of hormones on sex differences in infection: from genes to behavior. Neuroscience & Biobehavioral Reviews 24, 627–638.CrossRefGoogle Scholar
Klein, SL (2004) Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunology 26, 247–264.CrossRefGoogle ScholarPubMed
Knutie, SA, Wilkinson, CL, Wu, QC, Ortega, CN and Rohr, JR (2017) Host resistance and tolerance of parasitic gut worms depend on resource availability. Oecologia 183, 1031–1040.CrossRefGoogle ScholarPubMed
Kuznetsova, A, Brockhoff, PB and Christensen, RHB (2017) Lmertest package: tests in linear mixed effects models. Journal of Statistical Software 82, 1–26.CrossRefGoogle Scholar
Leivesley, JA, Bussière, LF, Pemberton, JM, Pilkington, JG, Wilson, K and Hayward, AD (2019) Survival costs of reproduction are mediated by parasite infection in wild Soay sheep. Ecology Letters 22, 1203–1213.Google ScholarPubMed
Lloyd, S (1983) Effect of pregnancy and lactation upon infection. Veterinary Immunology and Immunopathology 4, 153–176.CrossRefGoogle ScholarPubMed
Magi, M, Bertani, M, Dell'Omodarme, M, Prati, MC and Poglayen, G (2005) Seasonal egg output of gastro-intestinal parasites in wild ungulates in a Mediterranean area (central Italy). Hystrix, the Italian Journal of Mammalogy 16, 169–177.Google Scholar
Marchand, P, Garel, M, Bourgoin, G, Dubray, D, Maillard, D and Loison, A (2015) Coupling scale-specific habitat selection and activity reveals sex-specific food/cover trade-offs in a large herbivore. Animal Behaviour 102, 169–187.CrossRefGoogle Scholar
Markle, JG and Fish, EN (2014) SeXX matters in immunity. Trends in Immunology 35, 97–104.CrossRefGoogle ScholarPubMed
Martínez-Guijosa, J, Martínez-Carrasco, C, López-Olvera, JR, Fernández-Aguilar, X, Colom-Cadena, A, Cabezón, O, Mentaberre, G, Ferrer, D, Velarde, R, Gassó, D, Garel, M, Rossi, L, Lavín, S and Serrano, E (2015) Male-biased gastrointestinal parasitism in a nearly monomorphic mountain ungulate. Parasites & Vectors 8, 165.CrossRefGoogle Scholar
Mbora, DNM and McPeek, MA (2009) Host density and human activities mediate increased parasite prevalence and richness in primates threatened by habitat loss and fragmentation. Journal of Animal Ecology 78, 210–218.CrossRefGoogle ScholarPubMed
McRae, KM, Stear, MJ, Good, B and Keane, OM (2015) The host immune response to gastrointestinal nematode infection in sheep. Parasite Immunology 37, 605–613.CrossRefGoogle ScholarPubMed
Meana, A, Luzón-Peña, M, Santiago-Moreno, J, De Bulnes, A and Gómez-Bautista, M (1996) Natural infection by gastrointestinal and bronchopulmonary nematodes in mouflons (Ovis musimon) and their response to netobimin treatment. Journal of Wildlife Diseases 32, 39–43.CrossRefGoogle ScholarPubMed
Monaghan, P, Charmantier, A, Nussey, DH and Ricklefs, RE (2008) The evolutionary ecology of senescence. Functional Ecology 22, 371–378.CrossRefGoogle Scholar
Morgan, E and van Dijk, J (2012) Climate and the epidemiology of gastrointestinal nematode infections of sheep in Europe. Veterinary Parasitology 189, 8–14.CrossRefGoogle ScholarPubMed
Mysterud, A, Yoccoz, NG, Stenseth, NC and Langvatn, R (2001) Effects of age, sex and density on body weight of Norwegian red deer: evidence of density-dependent senescence. Proceedings of the Royal Society of London B: Biological Sciences 268, 911–919.CrossRefGoogle Scholar
Nussey, DH, Coulson, T, Delorme, D, Clutton-Brock, TH, Pemberton, JM, Festa-Bianchet, M and Gaillard, J-M (2011) Patterns of body mass senescence and selective disappearance differ among three species of free-living ungulates. Ecology 92, 1936–1947.CrossRefGoogle ScholarPubMed
Nussey, DH, Watt, K, Pilkington, JG, Zamoyska, R and McNeilly, TN (2012) Age-related variation in immunity in a wild mammal population. Aging Cell 11, 178–180.CrossRefGoogle Scholar
Ozdal, N, Tanritanir, P, Goz, A, Deger, S and Kozat, S (2009) Parasitic protozoans (Eimeria, Giardia, and Cryptosporidium) in lambs with diarrhea in the Van province (Turkey). Bulletin Veterinary Institute in Pulawy 53, 47–51.Google Scholar
Paull, SH, Song, S, McClure, KM, Sackett, LC, Kilpatrick, AM and Johnson, PTJ (2012) From superspreaders to disease hotspots: linking transmission across hosts and space. Frontiers in Ecology and the Environment 10, 75–82.CrossRefGoogle Scholar
Peig, J and Green, AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118, 1883–1891.CrossRefGoogle Scholar
Peig, J and Green, AJ (2010) The paradigm of body condition: a critical reappraisal of current methods based on mass and length. Functional Ecology 24, 1323–1332.CrossRefGoogle Scholar
Poglayen, G, Urbani, L, Modugno, F, Scala, A, Giannetto, S and Rossi, L (2018) The Italian mouflon (Ovis musimon): a brief history of its parasites in the last 45 years. Research Journal of Zoology 1, 1–4.Google Scholar
Portanier, E, Garel, M, Devillard, S, Maillard, D, Poissant, J, Galan, M, Benabed, S, Poirel, M-T, Duhayer, J, Itty, C and Bourgoin, G (2019) Both candidate gene and neutral genetic diversity correlate with parasite resistance in female Mediterranean mouflon. BMC Ecology 19, 12.CrossRefGoogle ScholarPubMed
Poulin, R (1996) Sexual inequalities in helminth infections: a cost of being a male? The American Naturalist 147, 287–295.CrossRefGoogle Scholar
Poulin, R (2013) Explaining variability in parasite aggregation levels among host samples. Parasitology 140, 541.CrossRefGoogle ScholarPubMed
Raynaud, J-P, William, G and Brunault, G (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, 321–342.CrossRefGoogle Scholar
R Core Team (2020) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Rieck, W (1975) Muffelwildalter, Brochure de l'association des chasseurs d'Allemagne Fédérale. Bonn, Germany (in German).Google Scholar
Roeber, F, Jex, AR and Gasser, RB (2013) Impact of gastrointestinal parasitic nematodes of sheep, and the role of advanced molecular tools for exploring epidemiology and drug resistance – an Australian perspective. Parasites & Vectors 6, 1–13.CrossRefGoogle ScholarPubMed
Rose, H, Hoar, B, Kutz, SJ and Morgan, ER (2014) Exploiting parallels between livestock and wildlife: predicting the impact of climate change on gastrointestinal nematodes in ruminants. International Journal for Parasitology: Parasites and Wildlife 3, 209–219.Google ScholarPubMed
Rose, H, Wang, T, van Dijk, J and Morgan, ER (2015) GLOWORM-FL: a simulation model of the effects of climate and climate change on the free-living stages of gastro-intestinal nematode parasites of ruminants. Ecological Modelling 297, 232–245.CrossRefGoogle Scholar
Samuel, WM, Pybus, MJ and Kocan, AA (eds) (2001) Parasitic Diseases of Wild Mammals, 2nd Edn. Iowa, USA: Iowa State University Press.CrossRefGoogle Scholar
Santín-Durán, M, Alunda, JM, Hoberg, EP and de la Fuente, C (2008) Age distribution and seasonal dynamics of abomasal helminths in wild red deer from central Spain. The Journal of Parasitology 94, 1031–1037.CrossRefGoogle Scholar
Smith, KF, Acevedo-Whitehouse, K and Pedersen, AB (2009) The role of infectious diseases in biological conservation. Animal Conservation 12, 1–12.CrossRefGoogle Scholar
Stien, A, Irvine, R, Ropstad, E, Halvorsen, O, Langvatn, R and Albon, S (2002) The impact of gastrointestinal nematodes on wild reindeer: experimental and cross-sectional studies. Journal of Animal Ecology 71, 937–945.CrossRefGoogle Scholar
Sutherst, RW (2001) The vulnerability of animal and human health to parasites under global change. International Journal for Parasitology 31, 933–948.CrossRefGoogle ScholarPubMed
Taylor, M, Coop, RL and Wall, R (2015) Veterinary Parasitology, 4th Edn. UK: Wiley-Blackwell.CrossRefGoogle Scholar
Telfer, S, Birtles, R, Bennett, M, Lambin, X, Paterson, S and Begon, M (2008) Parasite interactions in natural populations: insights from longitudinal data. Parasitology 135, 767–781.CrossRefGoogle ScholarPubMed
Tompkins, DM, Dobson, AP, Arneberg, P, Begon, ME, Cattadori, IM, Greenman, JV, Heesterbeek, JAP, Hudson, PJ, Newborn, D and Pugliese, A (2002) Parasites and host population dynamics. In Hudson, PJ, Rizzoli, A, Grenfell, BT, Heesterbeek, H and Dobson, AP (eds), The Ecology of Wildlife Diseases. New York, USA: Oxford University Press, pp. 45–62.Google Scholar
Turner, WC and Getz, WM (2010) Seasonal and demographic factors influencing gastrointestinal parasitism in ungulates of Etosha National Park. Journal of Wildlife Diseases 46, 1108–1119.CrossRefGoogle ScholarPubMed
VanderWaal, KL and Ezenwa, VO (2016) Heterogeneity in pathogen transmission: mechanisms and methodology. Functional Ecology 30, 1606–1622.CrossRefGoogle Scholar
Vors, LS and Boyce, MS (2009) Global declines of caribou and reindeer. Global Change Biology 15, 2626–2633.CrossRefGoogle Scholar
Weladji, RB, Holand, Ø, Gaillard, J-M, Yoccoz, NG, Mysterud, A, Nieminen, M and Stenseth, NC (2010) Age-specific changes in different components of reproductive output in female reindeer: terminal allocation or senescence? Oecologia 162, 261–271.CrossRefGoogle ScholarPubMed
Weller, KE (2001) The status of mouflon (Ovis musimon) in Europe. In Nahlik, A and Uloth, W (eds), Proceedings of the Third International Symposium on Mouflon. Sopron, Hungary: University of Sopron, pp. 114–140.Google Scholar
Wilson, K, Bjørnstad, ON, Dobson, AP, Merler, S, Poglayen, G, Randolph, SE, Read, AF and Skorping, A (2002) Heterogeneities in macroparasite infections: patterns and processes. In Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H and Dobson AP (eds), The Ecology of Wildlife Diseases. New York, USA: Oxford University Press, pp. 6–44.Google Scholar
Wilson, K, Grenfell, BT, Pilkington, JG, Boyd, HEG and Gulland, FMD (2004) Parasites and their impact. In Clutton-Brock, TH and Pemberton, JM (eds), Soay Sheep: Dynamics and Selection in an Island Population. Cambridge, UK: Cambridge University Press, pp. 113–165.Google Scholar
Woolhouse, ME, Dye, C, Etard, J-F, Smith, T, Charlwood, JD, Garnett, GP, Hagan, P, Hii, JLK, Ndhlovu, PD and Quinnell, RJ (1997) Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proceedings of the National Academy of Sciences 94, 338–342.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Bourgoin et al. supplementary material

Bourgoin et al. supplementary material 1

Download Bourgoin et al. supplementary material(PDF)
PDF 690.4 KB
Supplementary material: File

Bourgoin et al. supplementary material

Bourgoin et al. supplementary material 2

Download Bourgoin et al. supplementary material(File)
File 191.3 KB