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How does supplementary feeding affect endoparasite infection in wild boar?

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Abstract

Supplementary feeding is widely used in game management but may aid the transmission of parasites. Firstly, feeding sites attract animals and may be regarded as high-risk areas for parasite transmission. Secondly, high host population densities resulting from and supported by supplementary feeding, as well as accumulation of parasites in the environment, may increase parasite prevalence. Our aim was to investigate whether host density or the number of feeding sites drives endoparasite infection in an Estonian wild boar (Sus scrofa) population. For this, we collected wild boar faeces from forests, and soil samples from supplementary feeding sites in central and south-eastern Estonia. The role of host density and number of feeding sites on both the risk and mean abundance of endoparasite infection was modelled using generalized linear models (GLM). The presence of biohelminths in faecal samples was associated with both wild boar and feeding site density, whereas the presence of Eimeria sp. oocysts in faecal samples was only associated with wild boar density. Helminth eggs were found more often from the soil of active and abandoned feeding sites than from control areas. This could reflect parasitic contamination or indicate that supplementary feeding sites are suitable habitat for soil-dwelling nematodes. These results suggest that the effects of supplementary feeding on parasite prevalence in wild boar are mediated by the characteristics of parasite life cycles.

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References

  • Acevedo P, Vicente J, Höfle U, Cassinello J, Ruiz-Fons F, Gortazar C (2007) Estimation of European wild boar relative abundance and aggrecation: a novel method in epidemiological risk assessment. Epidemiol Infect 135:519–527

    Article  CAS  PubMed  Google 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

    Article  Google Scholar 

  • Arneberg P (2002) Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals. Ecography 25:88–94

    Article  Google Scholar 

  • Bieber C, Ruf T (2005) Population dynamics in wild boar Sus scrofa: ecology, elasticity of growth rate and implications for the management of pulsed resource consumers. J Appl Ecol 42:1203–1213

    Article  Google Scholar 

  • Brmež M, Ivezić M, Raspudić E (2006) Effect of mechanical disturbances on nematode communities in arable land. Helminthologia 43:117–121. doi:10.2478/s11687-006-0022-0

    Google Scholar 

  • Burnham KP, Anderson DR (2004) Multimodel inference understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304. doi:10.1177/0049124104268644

    Article  Google Scholar 

  • Cellina S (2008) Effects of supplemental feeding on the body condition and reproductive state of wild boar (Sus scrofa) in Luxembourg. PhD thesis, University of Sussex, UK

  • Collender PA, Kirby AE, Addiss DG, Freeman MC, Remais JV (2015) Methods for quantification of soil-transmitted helminths in environmental media: current techniques and recent advances. Trends in Parasitol 31:625–639. doi:10.1016/j.pt.2015.08.007

    Article  Google Scholar 

  • Demeler J, Ramünke S, Wolken S, Ianiello D, Rinaldi L, Gahutu JB, Cringoli G, von Samson-Himmelstjerna G, Krücken J (2013) Discrimination of gastrointestinal nematode eggs from crude fecal egg preparations by inhibitor-resistant conventional and real-time PCR. PLoS One 8:e61285. doi:10.1371/journal.pone.0061285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandez-de-Mera IG, Vicente J, Gortazar C, Höfle U, Fierro Y (2004) Efficacy of an in-feed preparation of ivermectin against helminths in the European wild boar. Parasitol Res 92:133–136

    Article  PubMed  Google Scholar 

  • Foata J, Mouillot D, Culioli J-L, Marchand B (2006) Influence of season and host age on wild boar parasites in Corsica using indicator species analysis. J Helminthol 80:41–45

    Article  CAS  PubMed  Google Scholar 

  • Gassó D, Feliu C, Ferrer D, Mentaberre G, Casas-Díaz E, Velarde R, Fernández-Aguilar X, Colom-Cadena A, Navarro-Gonzalez N, López-Olvera JR, Lavín S, Fenández-Llario P, Segalés J, Serrano E (2015) Uses and limitations of faecal egg count for assessing worm burden in wild boars. Vet Parasitol 209:133–137. doi:10.1016/j.vetpar.2015.02.006

    Article  PubMed  Google Scholar 

  • Gompper ME, Wright AN (2005) Altered prevalence of raccoon roundworm (Baylisascaris procyonis) owing to manipulated contact rates of hosts. J Zool 266:215–219

    Article  Google Scholar 

  • Hines AM, Ezenwa VO, Cross P, Rogerson JD (2007) Effects of supplemental feeding on gastrointestinal parasite infection in elk (Cervus elaphus): preliminary observations. Vet Parasitol 148:350–355

    Article  PubMed  Google Scholar 

  • Humbert J-F, Henry C (1989) Studies on the prevalence and the transmission of lung and stomach nematodes of the wild boar (Sus scrofa) in France. J Wildl Dis 25:335–341

    Article  CAS  PubMed  Google Scholar 

  • Järvis T (1993) Uluksõraliste helmindid Eestis ja helmintooside tõrje [Helminths of wild artiodactyls in Estonia and helminthoses control]. D.Sc. Dissertation, Eesti Põllumajandusülikool, Tartu, Estonia (in Estonian, English summary)

  • Järvis T, Kapel C, Moks E, Talvik H, Mägi E (2007) Helminths of wild boar in the isolated population close to the northern border of its habitat area. Vet Parasitol 150:366–369

    Article  PubMed  Google Scholar 

  • Jędrzejewski W, Jędrzejewska B, Okarma H, Ruprecht AL (1992) Wolf predation and snow cover as mortality factors in the ungulate community of the Bialowieża National Park, Poland. Oecologia 90:27–36

    Article  PubMed  Google Scholar 

  • Jokelainen P, Velström K, Lassen B (2015) Seroprevalence of Toxoplasma gondii in free-ranging wild boars hunted for human consumption in Estonia. Acta Vet Scand 57:42

    Article  PubMed  PubMed Central  Google Scholar 

  • Kärssin A, Velström K, Gómez-Morales MA, Saar T, Jokelainen P, Lassen B (2016) Cross-sectional study of anti-Trichinella antibody prevalence in domestic pigs and hunted wild boars in Estonia. Vector Borne Zoonotic Dis 16:604–610. doi:10.1089/vbz.2016.1943

    Article  PubMed  Google Scholar 

  • Larsen MN, Roepstorff A (1999) Seasonal variation in development and survival of Ascaris suum and Trichuris suis eggs on pastures. Parasitology 119:209–220

    Article  PubMed  Google Scholar 

  • Lassen B, Lepik T (2014) Isolation of Eimeria oocysts from soil samples: a simple method described in detail. Agraarteadus 25:77–81

    Google Scholar 

  • Levine ND (1985) Veterinary protozoology. The Iowa University State Press, Iowa, p 414

    Google Scholar 

  • Martin C, Pastoret P-P, Brochier B, Humblet M-F, Saegerman C (2011) A survey of the transmission of infectious diseases/infections between wild and domestic ungulates in Europe. Vet Res 42:70. doi:10.1186/1297-9716-42-70

    Article  PubMed  PubMed Central  Google Scholar 

  • Massei G, Kindberg J, Licoppe A, Gačić D, Šprem N, Kamler J, Baubet E, Hohmann U, Monaco A, Ozoliņš J, Cellina S, Podgórski T, Fonseca C, Markov N, Pokorny B, Rosell C, Náhlik A (2015) Wild boar populations up, numbers of hunters down? A review of trends and implications for Europe. Pest Manag Sci 71:492–500. doi:10.1002/ps.3965

    Article  CAS  PubMed  Google Scholar 

  • Milner JS, Wedul SJ, Laaksonen S, Oksanen A (2013) Gastrointestinal nematodes of moose (Alces alces) in relation to supplementary feeding. J Wildl Dis 49:69–79

    Article  PubMed  Google Scholar 

  • Milner JS, van Beest FM, Schmidt KT, Brook RK, Storaas T (2014) To feed or not to feed? Evidence of the intended and unintended effects of feeding wild ungulates. J Wildl Manag 78:1322–1334

    Article  Google Scholar 

  • Nagy G, Csivincsik Á, Sugár L (2015) Wild boar density drives Metastrongylus infection in earthworm. Acta Parasitol 60:35–39

    Google Scholar 

  • Navarro-Gonzalez N, Fernández-Llario P, Pérez-Martín JE, Mentaberre G, López-Martín JM, Lavín S, Serrano E (2013) Supplemental feeding drives endoparasite infection in wild boar in Western Spain. Vet Parasitol 196:114–123

    Article  PubMed  Google Scholar 

  • Newcombe RG (1998) Two-sided confidence intervals for the single proportion: comparison of seven methods. Stat Med 17:857–872

    Article  CAS  PubMed  Google Scholar 

  • Oja R, Kaasik A, Valdmann H (2014) Winter severity or supplementary feeding—which matters more for wild boar? Acta Theriol 59:553–559. doi:10.1007/s13364-014-0190-0

    Article  Google Scholar 

  • Oja R, Zilmer K, Valdmann H (2015) Spatiotemporal effects of supplementary feeding on wild boar (Sus scrofa) on artificial ground nest depredation. PLoS One 10:e0135254. doi:10.1371/journal.pone.0135254

    Article  PubMed  PubMed Central  Google Scholar 

  • Pilotte N, Papaiakovou M, Grant JR, Bierwert LA, Llewellyn S, McCarthy JS, Williams SA (2016) Improved PCR-based detection of soil transmitted helminth infections using a next-generation sequencing approach to assay design. PLoS Negl Trop Dis 10:e0004578. doi:10.1371/journal.pntd.0004578

    Article  PubMed  PubMed Central  Google Scholar 

  • Popiołek M, Knecht D, Szczęsna-Staśkiewicz J, Czerwińska-Rożałow A (2010) Helminths of the wild boar (Sus scrofa L.) in natural and breeding conditions. Bull Vet Inst Pulawy 53:161–166

    Google Scholar 

  • Pyziel AM, Kowalczyk R, Demiaszkiewicz AW (2011) The annual cycle of shedding Eimeria oocysts by European bison (Bison bonasus) in the Bialowieza Primeval Forest, Poland. J Parasitol 97:737–739

    Article  PubMed  Google Scholar 

  • R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available: http://www.R-project.org. (version 3.2.2)

    Google Scholar 

  • Risco D, Serrano E, Fernández-Llario P, Cuesta JM, Gonçalves P, García-Jiménez WL, Martínez R, Cerrato R, Velarde R, Gómez L, Segalés J, de Mendoza JH (2014) Severity of bovine tuberculosis is associated with co-infection with common pathogens in wild boar. PLoS One 9:e110123. doi:10.1371/journal.pone.0110123

    Article  PubMed  PubMed Central  Google Scholar 

  • Roberts MG, Dobson AP, Arneberg P, de Leo GA, Krecek RC, Manfredi MT, Lanfranchi P, Zaffaroni E (2003) Parasite community ecology and biodiversity. In: Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (eds) The ecology of wildlife diseases. Oxford University Press, Oxford, pp 63–82

    Google Scholar 

  • Roepstorff A, Nansen P (1998) Epidemiology, diagnosis and control of helminth parasites of swine. FAO Animal Health Manual, Rome

    Google Scholar 

  • Rosvold J, Andersen R (2008) Wild boar in Norway—is climate a limiting factor? Norges teknisk-naturvitenskapelige universitet Vitenskapsmuseet. Rapp Zool Ser 1:1–23

    Google Scholar 

  • Servanty S, Gaillard J-M, Toïgo C, Brandt S, Baubet E (2009) Pulsed resources and climate-induced variation in the reproductive traits of wild boar under high hunting pressure. J Anim Ecol 78:1278–1290

    Article  Google Scholar 

  • Sorensen A, van Beest FM, Brook RK (2014) Impacts of wildlife baiting and supplemental feeding on infectious disease transmission risk—a synthesis of knowledge. Prev Vet Med 113:356–363

    Article  PubMed  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern applied statistics with S, Fourth edn. Springer, New York

    Book  Google Scholar 

  • Vicente J, Höfle U, Fernández-De-Mera IG, Gortazar C (2007) The importance of parasite life history and host density in predicting the impact of infections in red deer. Oecologia 152:655–664

    Article  PubMed  Google Scholar 

  • WHO (2004) Integrated guide to sanitary parasitology. Regional Office for the Eastern Mediterranean. P.O. Box 7608, Nasr City, Cairo 1 1371. Egypt/Regional Centre for Environmental Health Activities, Amman

    Google Scholar 

  • Zeithaml J, Pižl V, Sklenička P (2009) Earthworm assemblages in an ecotone between forest and arable field and their relations with soil properties. Pesq Agrop Brasileira 44:922–926. doi:10.1590/S0100-204X2009000800018

    Article  Google Scholar 

  • Zhao J, Neher DA (2013) Soil nematode genera that predict specific types of disturbance. Appl Soil Ecol 64:135–141. doi:10.1016/j.apsoil.2012.11.008

    Article  Google Scholar 

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Acknowledgements

This work was supported by the State Forest Management Centre and the Estonian Research Council (grant IUT-2032). We are grateful to John Davison for proof-reading the manuscript and providing useful comments.

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Authors and Affiliations

  1. University of Tartu, Tartu, Estonia

    Ragne Oja & Epp Moks

  2. Department of Basic Veterinary Sciences and Population Medicine, Institute of Veterinary Medicine and Animal Science, Estonian University of Life Sciences, Tartu, Estonia

    Kaisa Velström, Pikka Jokelainen & Brian Lassen

  3. University of Helsinki, Helsinki, Finland

    Pikka Jokelainen

  4. Statens Serum Institut, Copenhagen, Denmark

    Pikka Jokelainen

  5. Department of Veterinary Disease Biology, University of Copenhagen, Frederiksberg C, Denmark

    Brian Lassen

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  1. Ragne Oja
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Correspondence to Epp Moks.

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Oja, R., Velström, K., Moks, E. et al. How does supplementary feeding affect endoparasite infection in wild boar?. Parasitol Res 116, 2131–2137 (2017). https://doi.org/10.1007/s00436-017-5512-0

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