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The Role of Scavenging in Disease Dynamics

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Book cover Carrion Ecology and Management

Part of the book series: Wildlife Research Monographs ((WIREMO,volume 2))

Abstract

There is increasing concern over the exposure of scavenger communities to disease, the effects of disease on scavengers, and the epidemiological role that scavenging plays in disease dynamics. With some exceptions, research does not reliably conclude the role of different species of scavengers, carrion and the environment in the maintenance and transmission of diseases and, consequently, proactive and reactive management actions are taken without solid background. Here, we identify important themes that are central in current and future research on the topic. (1) Exploring the exposure of scavenger communities to disease will subsequently guide specific research on the potential role of scavenging in the spread of disease. (2) In order to clarify the relevance of scavenging for pathogens to spread and persist, we need to assess whether scavenging is limiting disease spread or contrary, i.e. knowing if each species or functional group of scavengers act as a vector or reservoir facilitating disease spread. (3) Do human related factors result in increased risk for disease transmission through scavenging? (4) Determining how management of scavenging could impact pathogen transmission and which specific disposal regimes are most beneficial to scavengers. This management should guarantee the food supply to scavengers, while reducing the exposure of susceptible animals to potentially infectious material. This chapter exemplifies that scavenging of potentially infectious material may pose a confounding duality between the removal of infectious materials by consumption and potential dispersion of infectious material in the environment. Assessing this challenge requires changes in human activities and close collaboration among wildlife ecologists, veterinarians and public health professionals.

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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 aggregation: a novel method in epidemiological risk assessment. Epidemiol Infect 135:519–527

    Article  CAS  PubMed  Google Scholar 

  • Alexander KA, Kat PW, Wayne RK, Fuller TK (1994) Serologic survey of selected canine pathogens among free-ranging jackals in Kenya. J Wildl Dis 30:486–491

    Article  CAS  PubMed  Google Scholar 

  • Anderson DP, Ramsey DSL, de Lisle GW, Bosson M, Cross ML, Nugent G (2015) Development of integrated surveillance systems for the management of tuberculosis in New Zealand wildlife. N Z Vet J 63:89–97

    Article  PubMed  PubMed Central  Google Scholar 

  • Apollonio M, Andersen R, Putman R (2010) Introduction. In: Apollonio M, Andersen R, Putman R (eds) European ungulates and their management in the 21st century. Cambridge University Press, Cambridge

    Google Scholar 

  • Artois M, Bengis R, Delahay RJ, Duchêne M, Duff JP, Ferroglio E et al (2009) Wildlife disease surveillance and monitoring. In: Delahay RJ, Smith GC, Hutchings MR (eds) Management of disease in wild mammals. Springer, Tokyo, pp 187–213

    Chapter  Google Scholar 

  • Barron MC, Tompkins DM, Ramsey DSL, Bosson MAJ (2015) The role of multiple wildlife hosts in the persistence and spread of bovine tuberculosis in New Zealand. N Z Vet J 63:68–76

    Article  PubMed  PubMed Central  Google Scholar 

  • Bellan SE, Turnbull PCB, Beyer W, Getz WM (2013) Effects of experimental exclusion of scavengers from carcasses of anthrax-infected herbivores on Bacillus anthracis sporulation, survival, and distribution. Appl Environ Microbiol 79:3756–3761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beschta RL, Ripple WJ (2009) Large predators and trophic cascades in terrestrial ecosystems of the western United States. Biol Conserv 142:2401–2414

    Article  Google Scholar 

  • Briones V, de Juan L, Sánchez C et al (2000) Bovine tuberculosis and the endangered Iberian lynx. Emerg Infect Dis 6(2):189–191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bruning-Fann CS, Schmitt SM, Fitzgerald SD et al (2001) Bovine tuberculosis in free-ranging carnivores from Michigan. J Wildl Dis 37:58–64

    Article  CAS  PubMed  Google Scholar 

  • Butler JRA, du Toit JT (2002) Diet of free-ranging domestic dogs (Canis familiaris) in rural Zimbabwe: implications for wild scavengers on the periphery of wildlife reserves. Anim Conserv 5:29–37

    Article  Google Scholar 

  • Butler JRA, du Toit JT, Bingham J (2004) Free-ranging domestic dogs (Canis familiaris) as predators and prey in rural Zimbabwe: threats of competition and disease to large wild carnivores. Biol Conserv 115:369–378

    Article  Google Scholar 

  • Byrom A (2004) Spread of Tb by ferrets in the northern South Island high country. Landcare Research Contract Report: LC0304/146

    Google Scholar 

  • Byrom AE, Caley P, Paterson BM, Nugent G (2015) Feral ferrets (Mustela furo) as hosts and sentinels of tuberculosis in New Zealand. N Z Vet J 63:42–53

    Article  PubMed  PubMed Central  Google Scholar 

  • Cano-Terriza D, Risalde MA, Jiménez-Ruiz S et al (2018) Management of hunting waste as control measure for tuberculosis in wild ungulates in south-central Spain. Transbound Emerg Dis 65(5):1190–1196

    Article  CAS  PubMed  Google Scholar 

  • Carrasco-Garcia R, Barroso P, Perez-Olivares J, Montoro V, Vicente J (2018) Consumption of big game remains by scavengers: a potential risk as regards disease transmission in central Spain. Front Vet Sci 5:4

    Article  PubMed  PubMed Central  Google Scholar 

  • Clark NJ, Clegg SM (2017) Integrating phylogenetic and ecological distances reveals new insights into parasite host specificity. Mol Ecol 26:3074–3086

    Article  PubMed  Google Scholar 

  • Choo K, Williams PD, Day T (2003) Host mortality, predation, and the evolution of parasite virulence. Ecol Lett 6:310–315

    Article  Google Scholar 

  • Cook WE, Williams ES, Dubay SA (2004) Disappearance of bovine fetuses in northwestern Wyoming. Wildl Soc Bull 32:254–259

    Article  Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife—Threats to biodiversity and human health. Science 287:443–449

    Article  CAS  PubMed  Google Scholar 

  • Delahay RJ, Smith GC, Barlow AM, Walker N, Harris A, Clifton-Hadley RS, Cheeseman CL (2006) Bovine tuberculosis infection in wild mammals in the south-west region of England: a survey of prevalence and a semi-quantitative assessment of the relative risks to cattle. Vet J 164:90–105

    Article  Google Scholar 

  • DeVault TL, Rhodes OE, Shivik JA (2003) Scavenging by vertebrates: behavioural, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos 102:225–234

    Article  Google Scholar 

  • Donázar JA, Cortés-Avizanda A, Carreta M (2009a) The role of trophic resource predictability in the structure of scavenger guild. Vultures, feeding stations and sanitary legislation, a conflict and its consequences from the perspective of conservation biology. Munibe 29:344–352

    Google Scholar 

  • Donázar JA, Margalida A, Carrete M, Sánchez-Zapata JA (2009b) Too sanitary for vultures. Science 326:664

    Article  PubMed  Google Scholar 

  • EFSA (European Food Safety Authority) (2017) Scientific report on the European Union summary report on surveillance for the presence of transmissible spongiform encephalopathies (TSE) in 2016. EFSA J 15(5069):68

    Google Scholar 

  • European Commission – Health & Consumer Protection Directorate-General (2002) Scientific Steering Committee. Opinion on: necrophagous birds as possible transmitters of TSE/BSE. Adopted by the scientific steering committee at its meeting of 7–8 November 2002. https://ec.europa.eu/food/sites/food/files/safety/docs/sci-com_ssc_out295_en.pdf

  • Farner DS (1967) The hydrogen ion concentration in avian digestive tracts. Poultry Sci 21:445

    Article  Google Scholar 

  • Ferroglio E, Gortazar C, Vicente J (2011) Wild ungulate diseases and the risk for livestock and public health. In: Putman R, Apollonio M, Andersen R (eds) Ungulate management in Europe: problems and practices. Cambridge University Press, Cambridge

    Google Scholar 

  • Glass CM, Mclean RG, Katz JB et al (1994) Isolation of pseudorabies (Aujeszky’s disease) virus from a Florida panther. J Wildl Dis 30:180–184

    Article  CAS  PubMed  Google Scholar 

  • Gortazar C, Acevedo P, Ruiz-Fons F, Vicente J (2006) Disease risks and overabundance of game species. Eur J Wildl Res 52:81–87

    Article  Google Scholar 

  • Gortazar C, Torres MJ, Vicente J et al (2008) Bovine tuberculosis in Doñana Biosphere Reserve: the role of wild ungulates as disease reservoirs in the last Iberian lynx strongholds. PLoS One 3:1–8

    Article  CAS  Google Scholar 

  • Gortazar C, Vicente J, Fierro Y, Leon L, Cubero MJ, González M (2002) Natural Aujeszky’s disease in a Spanish wild boar population. Ann N Y Acad Sci 969:210–212

    Article  CAS  PubMed  Google Scholar 

  • Gross JE, Miller MW (2001) Chronic wasting disease in mule deer: disease dynamics and control. J Wildl Manag 65:205–215

    Article  Google Scholar 

  • Harrison TM, Mazet JK, Holekamp KE, Dubovi E, Engh AL, Nelson K, Van Horn RC, Munson L (2004) Antibodies to canine and feline viruses in spotted hyena (Crocuta crocuta) in the Masai Mara National Reserve. J Wildl Dis 40:1–10

    Article  CAS  PubMed  Google Scholar 

  • Heesterbeek JAP, Roberts MG (1995) Mathematical models for microparasites of wildlife. In: Grenfell BT, Dobson AP (eds) Ecology of infectious diseases in natural populations. Cambridge University Press, Cambridge, pp 90–122

    Chapter  Google Scholar 

  • Holt RD, Roy M (2007) Predation can increase the prevalence of infectious disease. Am Nat 169:690–699

    Article  PubMed  Google Scholar 

  • Houston DC, Cooper JE (1975) The digestive tract of the whitebacked griffon vulture and its role in disease transmission among wild ungulates. J Wild Dis 11:306–313

    Article  CAS  Google Scholar 

  • Hugh-Jones ME, De Vos V (2002) Anthrax and wildlife. Rev Sci Tech 21:359–383

    Article  CAS  PubMed  Google Scholar 

  • Hutson JM, Burke C, Haynes G (2013) Osteophagia and bone modifications by Giraffe and other large ungulates. J Archaeol Sci 40:4139–4149

    Article  Google Scholar 

  • Inger R, Cox DTC, Per E, Norton BA, Gaston KJ (2016) Ecological role of vertebrate scavengers in urban ecosystems in the UK. Ecol Evol 6:7015–7023. https://doi.org/10.1002/ece3.2414

    Article  PubMed  PubMed Central  Google Scholar 

  • Jennelle CS, Samuel MD, Nolden CA, Berkley EA (2009) Deer carcass decomposition and potential scavenger exposure to chronic wasting disease. J Wildl Manag 73:655–662

    Article  Google Scholar 

  • Karesh WB, Cook RA, Bennett EL, Newcomb J (2005) Wildlife trade and global disease emergence. Emerg Infect Dis 11:1000–1002

    Article  PubMed  PubMed Central  Google Scholar 

  • Leighton FA, Artois M, Capucci L, Gavierwiden D, Morisse JP (1995) Antibody-response to rabbit viral hemorrhagic disease virus in red foxes (Vulpes vulpes) consuming livers of infected rabbits (Oryctolagus cuniculus). J Wildl Dis 31:541–544

    Article  CAS  PubMed  Google Scholar 

  • Maichak EJ, Scurlock BM, Rogerson JD, Meadows LL, Barbknecht AE, Edwards WH, Cross PC (2009) Effects of management, behavior, and scavenging on risk of brucellosis transmission in elk of western Wyoming. J Wildl Dis 45:398–410

    Article  PubMed  Google Scholar 

  • Margalida A, Colomer MA (2012) Modelling the effects of sanitary policies on European vulture conservation. Sci Rep 2:753

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Margalida A, Carrete M, Sánchez-Zapata JA, Donázar JA (2012) Good news for European vultures. Science 335:284–284

    Article  CAS  PubMed  Google Scholar 

  • Margalida A, Moleón M (2016) Toward a carrion-free ecosystem. Front Ecol Environ 14:182–183

    Article  Google Scholar 

  • Markandya A, Taylor T, Longo A, Murty MN, Murty S, Dhavala K (2008) Counting the cost of vulture decline: an appraisal of the human health and other benefits of vultures in India. Ecol Econ 67:194–204

    Article  Google Scholar 

  • Martín-Hernando MP, Höfle U, Vicente J et al (2007) Lesions associated with Mycobacterium tuberculosis complex infection in the European wild boar. Tuberculosis 87:360–367

    Article  PubMed  Google Scholar 

  • Masot AJ, Gil M, Risco D, Jiménez OM, Núñez JI, Redondo E (2016) Pseudorabies virus infection (Aujeszky’s disease) in an Iberian lynx (Lynx pardinus) in Spain: a case report. BMC Vet Res 13:6

    Article  Google Scholar 

  • Mateo-Tomás P, Olea PP (2010) When hunting benefits raptors: a case study of game species and vultures. Eur J Wildl Res 56:519–528

    Article  Google Scholar 

  • Mateo-Tomás P, Olea PP, Moleón M, Vicente J, Botella F, Selva N, Viñuela J, Sánchez-Zapata JA (2015) From regional to global patterns in vertebrate scavenger communities subsidized by big game hunting. Divers Distrib 21:913–924

    Article  Google Scholar 

  • Mateo-Tomás P, Olea PP, Moleón M, Selva N, Sánchez-Zapata JA (2017) Both rare and common species support ecosystem services in scavenger communities. Glob Ecol Biogeogr 26:1459–1470

    Article  Google Scholar 

  • Millan J, Jimenez MA, Viota M, Candel MG, Peña L, León-Vizcaino L (2008) Disseminated bovine tuberculosis in a wild red fox (Vulpes vulpes) in southern Spain. J Wildl Dis 44:701–706

    Article  PubMed  Google Scholar 

  • Miller MW, Williams ES, Hobbs NT, Wolfe LL (2004) Environmental sources of prion transmission in mule deer. Emerg Infect Dis 10:1003–1006

    Article  PubMed  PubMed Central  Google Scholar 

  • Mills MGL (1993) Social systems and behaviour of the African wild dog Lycaon pictus and the spotted hyaena Crocuta crocuta with special reference to rabies. Onderstepoort J Vet Res 60:405–409

    CAS  PubMed  Google Scholar 

  • Moreno-Opo R, Trujillano A, Margalida A (2015) Optimization of supplementary feeding programs for European vultures depends on environmental and management factors. Ecosphere 6(7):127

    Article  Google Scholar 

  • Moreno-Opo R, Margalida A, García F, Arredondo A, Rodríguez C, González LM (2012) Linking sanitary and ecological requirements in the management of avian scavengers: effectiveness of fencing against mammals in supplementary feeding sites. Biodivers Conserv 21:673–1685

    Article  Google Scholar 

  • Naranjo V, Gortazar C, Vicente J, de la Fuente J (2008) Evidence of the role of European wild boar as a reservoir of Mycobacterium tuberculosis complex. Vet Res 127:1–9

    Google Scholar 

  • Newsome TM, Dellinger JA, Pavey CR et al (2014) The ecological effects of providing resource subsidies to predators. Glob Ecol Biogeogr 24:1–11

    Article  Google Scholar 

  • Nichols TA, Fischer JW, Spraker TR, Kong Q, VerCauteren KC (2015) CWD prions remain infectious after passage through the digestive system of coyotes (Canis latrans). Prion 9:367–375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oaks JL, Gilbert M, Virani MZ et al (2004) Diclofenac residues as the cause of vulture population decline in Pakistan. Nature 427:630–633

    Article  CAS  PubMed  Google Scholar 

  • Ogada DL, Torchin ME, Kinnaird MF, Ezenwa VO (2012) Effects of vulture declines on facultative scavengers and potential implications for mammalian disease transmission. Conserv Biol 26:453–460

    Article  CAS  PubMed  Google Scholar 

  • Packer C, Holt RD, Hudson PJ, Lafferty KD, Dobson AP (2003) Keeping the herds healthy and alert: implications of predator control for infectious disease. Ecol Lett 6:797–802

    Article  Google Scholar 

  • Pain DJ et al (2003) Causes and effects of temporospatial declines of Gyps vultures in Asia. Conserv Biol 17:661–671

    Article  Google Scholar 

  • Pedersen AB, Jones KE, Nunn CL, Altizer S (2007) Infectious diseases and extinction risk in wild mammals. Conserv Biol 21:1269–1279

    Article  PubMed  PubMed Central  Google Scholar 

  • Pérez J, Calzada J, León-Vizcaino L, Cubero MJ, Velarde J, Mozos E (2001) Tuberculosis in an Iberian lynx (Lynx pardina). Vet Rec 148:414–415

    Article  PubMed  Google Scholar 

  • Probst C, Globig A, Knoll B, Conraths FK, Depner K (2016) Behaviour of free ranging wild boar towards their dead fellows: potential implications for the transmission of African swine fever. R Soc Open Sci 4(5):170054

    Article  PubMed  PubMed Central  Google Scholar 

  • Roelke-Parker ME et al (1996) A canine distemper outbreak in Serengeti lions (Panthera leo). Nature 379:441–445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roen KT, Yahner RH (2005) Behavioral responses of avian scavengers in different habitats. Northeast Nat 12:103–112

    Article  Google Scholar 

  • Seidel B, Thomzig A, Buschmann A, Groschup MH, Peters R, Beekes M, Terytze K (2007) Scrapie agent (strain 263k) can transmit disease via the oral route after persistence in soil over years. PLoS One 2:E435.10.1371

    Article  CAS  Google Scholar 

  • Selva N, Jedrzejewska B, Jedrzejewski W, Wajrak A (2005) Factors affecting carcass use by a guild of scavengers in European temperate woodland. Can J Zool 83:1590–1601

    Article  Google Scholar 

  • Sharp D (2006) Meloxicam to prevent rabies? Lancet 367:887–888

    Article  PubMed  Google Scholar 

  • Smith CR (1994) Wild carnivores as plague indicators in California: a cooperative interagency disease surveillance program. In: Halverson WS, Crabb AC (eds) Proceedings of 16th vertebrates pest conference. University of California, Davies, pp 192–199

    Google Scholar 

  • Towne EG (2000) Prairie vegetation and soil nutrient responses to ungulate carcasses. Oecologia 122:232–239

    Article  CAS  PubMed  Google Scholar 

  • Turner KL, Abernethy EF, Conner LM, Rhodes OE Jr, Beasley JC (2017) Abiotic and biotic factors modulate carrion fate and vertebrate scavenging communities. Ecology 98:2413–2424

    Article  PubMed  Google Scholar 

  • VerCauteren KC, Atwood TC, DeLiberto TJ, Smith HJ, Stevenson JS, Thomsen BV, Gidlewski T, Payeur J (2008) Sentinel-based surveillance of coyotes to detect bovine tuberculosis, Michigan. Emerg Infect Dis 14:1862–1869

    Article  PubMed  PubMed Central  Google Scholar 

  • VerCauteren KC, Pilon JL, Nash PB, Phillips GE, Fischer JW (2012) Prion remains infectious after passage through digestive system of American crows (Corvus brachyrhynchos). PLoS One 7(10):e45774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vicente J, Carrasco R, Acevedo P, Montoro V, Gortazar C (2011) Big game waste production: sanitary and ecological implications. In: Kumar S (ed) Integrated waste management, vol 2. Intech, Rijeka

    Google Scholar 

  • Wild MA, Hobbs NT, Graham MS, Miller MW (2011) The role of predation in disease control: a comparison of selective and nonselective removal on prion disease dynamics in deer. J Wild Dis 47:78–93

    Article  PubMed  Google Scholar 

  • Wilmers CC, Crabtree RL, Smith DW, Murphy KM, Getz WM (2003a) Trophic facilitation by introduced top predators: grey wolf subsidies to scavengers in Yellowstone National Park. J Anim Ecol 72:909–916

    Article  Google Scholar 

  • Wilmers CC, Stahler DR, Crabtree RL, Smith DW, Getz WM (2003b) Resource dispersion and consumer dominance: scavenging at wolf- and hunter-killed carcasses in Greater Yellowstone, USA. Ecol Lett 6:996–1003

    Article  Google Scholar 

  • Wilson EE, Wolkovich EM (2011) Scavenging: how carnivores and scavenging structure communities. Trends Ecol Evol 26:129–135

    Article  PubMed  Google Scholar 

  • Wobeser GA (2007) Disease in wild animals: investigation and management. Springer, Berlin

    Book  Google Scholar 

  • Wobeser GA (2002) Disease management strategies for wildlife. Rev Sci Tech 21:159–178

    Article  CAS  PubMed  Google Scholar 

  • Yarnell RY, Phipps WL, Dell S, MacTavish LM, Scott DM (2015) Evidence that vulture restaurants increase the local abundance of mammalian carnivores in South Africa. Afr J Ecol 53:287–294

    Article  Google Scholar 

  • Zanin E, Capua I, Casaccia C, Zuin A, Moresco A (1997) Isolation and characterization of Aujeszky’s disease virus in captive brown bears from Italy. J Wildl Dis 33:632–634

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Pedro P. Olea and Patricia Mateo-Tomás their valuable guidance and comments on the chapter.

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Authors and Affiliations

  1. SaBio - Instituto de Investigación en Recursos Cinegéticos, IREC (UCLM-CSIC), Ciudad Real, Spain

    Joaquín Vicente

  2. National Wildlife Research Center, USDA/APHIS/Wildlife Services, Fort Collins, CO, USA

    Kurt VerCauteren

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  1. Joaquín Vicente
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Correspondence to Joaquín Vicente .

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Editors and Affiliations

  1. Centro de Investigación en Biodiversidad y Cambio Global (CIBC-UAM), Universidad Autónoma de Madrid, Madrid, Spain

    Pedro P. Olea

  2. Centre for Functional Ecology (CFE), Department of Life Sciences, University of Coimbra, Coimbra, Portugal

    Patricia Mateo-Tomás

  3. Departamento de Biología Aplicada, Universidad Miguel Hernández, Elche, Spain

    José Antonio Sánchez-Zapata

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Vicente, J., VerCauteren, K. (2019). The Role of Scavenging in Disease Dynamics. In: Olea, P., Mateo-Tomás, P., Sánchez-Zapata, J. (eds) Carrion Ecology and Management. Wildlife Research Monographs, vol 2. Springer, Cham. https://doi.org/10.1007/978-3-030-16501-7_7

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