Targeted strategies for the management of wildlife diseases: the case of brucellosis in Alpine ibex

Rhyan JC, Spraker TR (2010) Emergence of diseases from wildlife reservoirs. Vet Pathol 47:34–39. https://doi.org/10.1177/0300985809354466 Corner LAL (2006) The role of wild animal populations in the epidemiology of tuberculosis in domestic animals: how to assess the risk. Vet Microbiol 112:303–312. https://doi.org/10.1016/j.vetmic.2005.11.015 Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451:990–993. https://doi.org/10.1038/nature06536 Gortázar C, Diez-Delgado I, Barasona JA, Vicente J, De La Fuente J, Boadella M (2015) The wild side of disease control at the wildlife-livestock-human interface: a review. Front Vet Sci 1:1–12. https://doi.org/10.3389/fvets.2014.00027 Artois M, Delahay RJ, Guberti V, Cheeseman CL (2001) Control of infectious diseases of wildlife in Europe. Vet J 162:141–152. https://doi.org/10.1053/tvjl.2001.0601 Artois M, Blancou J, Dupeyroux O, Gilot-Fromont E (2011) Sustainable control of zoonotic pathogens in wildlife: how to be fair to wild animals? Rev Sci Tech Off Int Epizoot 30:733–743 Wobeser G (2002) Disease management strategies for wildlife. Rev Sci Tech Off Int Epizoot 21:159–178 Wobeser G (2007) Disease in wild animals: investigation and management. Springer, Berlin McDonald RA, Delahay RJ, Carter SP, Smith GC, Cheeseman CL (2008) Perturbing implications of wildlife ecology for disease control. Trends Ecol Evol 23:53–56. https://doi.org/10.1016/j.tree.2007.10.011 Choisy M, Rohani P (2006) Harvesting can increase severity of wildlife disease epidemics. Proc Biol Sci 273:2025–2034. https://doi.org/10.1098/rspb.2006.3554 Prentice JC, Marion G, White PCL, Davidson RS, Hutchings MR (2014) Demographic processes drive increases in wildlife disease following population reduction. PLoS One 9:e86563. https://doi.org/10.1371/journal.pone.0086563 Miguel E, Grosbois V, Caron A, Pople D, Roche B, Donnelly CA (2020) A systemic approach to assess the potential and risks of wildlife culling for infectious disease control. Commun Biol 3:353. https://doi.org/10.1038/s42003-020-1032-z Cowled BD, Garner MG, Negus K, Ward MP (2012) Controlling disease outbreaks in wildlife using limited culling: modelling classical swine fever incursions in wild pigs in Australia. Vet Res 43:3. https://doi.org/10.1186/1297-9716-43-3 Zanella G, Bar-Hen A, Boschiroli M-L, Hars J, Moutou F, Garin-Bastuji B, Durand B (2012) Modelling transmission of bovine tuberculosis in red deer and wild boar in Normandy, France. Zoonoses Public Health 59:170–178. https://doi.org/10.1111/j.1863-2378.2011.01453.x Anderson LG, Gortázar C, Vicente J, Hutchings MR, White PCL (2013) Modelling the effectiveness of vaccination in controlling bovine tuberculosis in wild boar. Wildl Res 40:367–376. https://doi.org/10.1071/WR12139 Smith GC, Marion G, Rushton S, Pfeiffer D, Thulke HH, Eisinger D, Hutchings MR (2009) Modelling disease dynamics and management scenarios. In: Delahay RJ, Smith GC, Hutchings MR (eds) Management of disease in wild mammals. Springer, New York, pp 53–77 Paull SH, Song S, McClure KM, Sackett LC, Kilpatrick AM, Johnson PTJ (2012) From superspreaders to disease hotspots: linking transmission across hosts and space. Front Ecol Environ 10:75–82. https://doi.org/10.1890/110111 VanderWaal KL, Ezenwa VO (2016) Heterogeneity in pathogen transmission: mechanisms and methodology. Funct Ecol 30:1606–1622. https://doi.org/10.1111/1365-2435.12645 Fenichel EP, Horan RD (2007) Gender-based harvesting in wildlife disease management. Am J Agric Econ 89:904–920. https://doi.org/10.1111/j.1467-8276.2007.01025.x Ebinger M, Cross P, Wallen R, White PJ, Treanor J (2011) Simulating sterilization, vaccination, and test-and-remove as brucellosis control measures in bison. Ecol Appl 21:2944–2959. https://doi.org/10.1890/10-2239.1 Hess G (1996) Disease in metapopulation models: implications for conservation. Ecology 77:1617–1632. https://doi.org/10.2307/2265556 Fulford GR, Roberts MG, Heesterbeek JAP (2002) The metapopulation dynamics of an infectious disease: tuberculosis in possums. Theor Popul Biol 61:15–29. https://doi.org/10.1006/tpbi.2001.1553 Haydon DT, Randall DA, Matthews L, Knobel DL, Tallents LA, Gravenor MB, Williams SD, Pollinger JP, Cleaveland S, Woolhouse MEJ, Sillero-Zubiri C, Marino J, Macdonald DW, Laurenson MK (2006) Low-coverage vaccination strategies for the conservation of endangered species. Nature 443:692–695. https://doi.org/10.1038/nature05177 Bolzoni L, Real L, De Leo G (2007) Transmission heterogeneity and control strategies for infectious disease emergence. PLoS One 2:e747. https://doi.org/10.1371/journal.pone.0000747 Drewe JA, Eames KTD, Madden JR, Pearce GP (2011) Integrating contact network structure into tuberculosis epidemiology in meerkats in South Africa: implications for control. Prev Vet Med 101:113–120. https://doi.org/10.1016/j.prevetmed.2011.05.006 Rushmore J, Caillaud D, Hall RJ, Stumpf RM, Meyers LA, Altizer S (2014) Network-based vaccination improves prospects for disease control in wild chimpanzees. J R Soc Interface 11:20140349. https://doi.org/10.1098/rsif.2014.0349 Lloyd-Smith JO, Schreiber SJ, Kopp PE, Getz WM (2005) Superspreading and the effect of individual variation on disease emergence. Nature 438:355–359. https://doi.org/10.1038/nature04153 Mailles A, Rautureau S, Le Horgne JM, Poignet-Leroux B, d’Arnoux C, Dennetière G, Faure M, Lavigne JP, Bru JP, Garin-Bastuji B (2012) Re-emergence of brucellosis in cattle in France and risk for human health. Euro Surveill 17:20227 Garin-Bastuji B, Hars J, Drapeau A, Cherfa MA, Game Y, Le Horgne JM, Rautureau S, Maucci E, Pasquier JJ, Jaÿ M, Mick V (2014) Reemergence of Brucella melitensis in wildlife, France. Emerg Infect Dis 20:1570–1571. https://doi.org/10.3201/eid2009.131517 ANSES (2019) Pertinence de la vaccination des bouquetins du Bargy contre la brucellose. Rapport ANSES (in French) Marchand P, Freycon P, Herbaux JP, Game Y, Toïgo C, Gilot-Fromont E, Rossi S, Hars J (2017) Sociospatial structure explains marked variation in brucellosis seroprevalence in an Alpine ibex population. Sci Rep 7:15592. https://doi.org/10.1038/s41598-017-15803-w Lambert S, Gilot-Fromont E, Freycon P, Thébault A, Game Y, Toïgo C, Petit E, Barthe MN, Reynaud G, Jaÿ M, Garin-Bastuji B, Ponsart C, Hars J, Rossi S (2018) High shedding potential and significant individual heterogeneity in naturally-infected Alpine ibex (Capra ibex) with Brucella melitensis. Front Microbiol 9:1065. https://doi.org/10.3389/fmicb.2018.01065 Lambert S, Gilot-Fromont E, Toïgo C, Marchand P, Petit E, Garin-Bastuji B, Gauthier D, Gaillard JM, Rossi S, Thébault A (2020) An individual-based model to assess the spatial and individual heterogeneity of Brucella melitensis transmission in Alpine ibex. Ecol Modell 425:109009. https://doi.org/10.1016/j.ecolmodel.2020.109009 Hars J, Rautureau S, Jaÿ M, Game Y, Gauthier D, Herbaux JP, Le Horgne JM, Maucci E, Pasquier JJ, Vaniscotte A, Mick V, Garin-Bastuji B (2013) Un foyer de brucellose chez les ongulés sauvages du massif du Bargy en Haute-Savoie. Bull Epidémiol Santé Anim Alim 60:2–7 (in French) Calenge C, Lambert S, Petit E, Thébault A, Gilot-Fromont E, Toïgo C, Rossi S (2021) Estimating disease prevalence and temporal dynamics using biased capture serological data in a wildlife reservoir: the example of brucellosis in Alpine ibex (Capra ibex). Prev Vet Med 187:105239. https://doi.org/10.1016/j.prevetmed.2020.105239 ANSES (2015) Mesures de maîtrise de la brucellose chez les bouquetins du Bargy. Rapport ANSES (in French) Diaz-Aparicio E (2013) Epidemiology of brucellosis in domestic animals caused by Brucella melitensis, Brucella suis and Brucella abortus. Rev Sci Tech 32:43–51 Lamboni M, Makowski D, Lehuger S, Gabrielle B, Monod H (2009) Multivariate global sensitivity analysis for dynamic crop models. Field Crops Res 113:312–320. https://doi.org/10.1016/j.fcr.2009.06.007 Bidot C, Lamboni M, Monod H (2017) multisensi: multivariate sensitivity analysis. R package version 2.1 Ponsart C, Riou M, Locatelli Y, Jacques I, Fadeau A, Jaÿ M, Simon R, Perrot L, Freddi L, Breton S, Chaumeil T, Blanc B, Ortiz K, Vion C, Rioult D, Quéméré E, Sarradin P, Chollet JY, Garin-Bastuji B, Rossi S (2019) Brucella melitensis Rev.1 vaccination generates a higher shedding risk of the vaccine strain in Alpine ibex (Capra ibex) compared to the domestic goat (Capra hircus). Vet Res 50:100. https://doi.org/10.1186/s13567-019-0717-0 Lloyd-Smith JO, Cross PC, Briggs CJ, Daugherty M, Getz WM, Latto J, Sanchez MS, Smith AB, Swei A (2005) Should we expect population thresholds for wildlife disease? Trends Ecol Evol 20:511–519. https://doi.org/10.1016/j.tree.2005.07.004 Douhard M, Plard F, Gaillard JM, Capron G, Delorme D, Klein F, Duncan P, Loe LE, Bonenfant C (2014) Fitness consequences of environmental conditions at different life stages in a long-lived vertebrate. Proc Biol Sci 281:20140276. https://doi.org/10.1098/rspb.2014.0276 Pigeon G, Festa-Bianchet M, Pelletier F (2017) Long-term fitness consequences of early environment in a long-lived ungulate. Proc Biol Sci 284:20170222. https://doi.org/10.1098/rspb.2017.0222 Blasco JM, Marin CM, Jiménez-de-Bagués M, Barberàn M, Hernández A, Molina L, Velasco J, Díaz R, Moriyón I (1994) Evaluation of allergic and serological tests for diagnosing Brucella melitensis infection in sheep. J Clin Microbiol 32:1835–1840 Ferreira AC, Cardoso R, Travassos Dias I, Mariano I, Belo A, Rolão Preto I, Manteigas A, Pina Fonseca A, Corrêa De Sá MI (2003) Evaluation of a modified Rose Bengal test and an indirect Enzyme-Linked Immunosorbent Assay for the diagnosis of Brucella melitensis infection in sheep. Vet Res 34:297–305. https://doi.org/10.1051/vetres:2003005 Nielsen K, Gall D, Smith P, Balsevicius S, Garrido F, Durán Ferrer M, Biancifiori F, Dajer A, Luna E, Samartino L, Bermudez R, Moreno F, Renteria T, Corral A (2004) Comparison of serological tests for the detection of ovine and caprine antibody to Brucella melitensis. Rev Sci Tech 23:979–987 FAO, WHO (1986) Joint FAO/WHO expert committee on brucellosis. World Health Organ Tech Rep Ser 740:1–132 Grimm V, Berger U, DeAngelis DL, Polhill JG, Giske J, Railsback SF (2010) The ODD protocol: a review and first update. Ecol Model 221:2760–2768. https://doi.org/10.1016/j.ecolmodel.2010.08.019 Grimm V, Berger U, Bastiansen F, Eliassen S, Ginot V, Giske J, Goss-Custard J, Grand T, Heinz SK, Huse G, Huth A, Jepsen JU, Jørgensen C, Mooij WM, Müller B, Pe’er G, Piou C, Railsback SF, Robbins AM, Robbins MM, Rossmanith E, Rüger N, Strand E, Souissi S, Stillman RA, Vabø R, Visser U, DeAngelis DL (2006) A standard protocol for describing individual-based and agent-based models. Ecol Model 198:115–126. https://doi.org/10.1016/j.ecolmodel.2006.04.023 Keeling MJ, Rohani P (2008) Modeling infectious diseases in humans and animals. Princeton University Press, Princeton Gauthier D, Martinot JP, Choisy JP, Michallet J, Villaret JC, Faure E (1991) Le bouquetin des Alpes. Rev Ecol 46:233–275 (in French) Willisch CS, Neuhaus P (2009) Alternative mating tactics and their impact on survival in adult male Alpine ibex (Capra ibex ibex). J Mammal 90:1421–1430. https://doi.org/10.1644/08-MAMM-A-316R1.1 Bon R, Rideau C, Villaret J-C, Joachim J (2001) Segregation is not only a matter of sex in Alpine ibex, Capra ibex ibex. Anim Behav 62:495–504. https://doi.org/10.1006/anbe.2001.1776 Stüwe M, Grodinsky C (1987) Reproductive biology of captive Alpine ibex (Capra i. ibex). Zoo Biol 6:331–339. https://doi.org/10.1002/zoo.1430060407 European Commission (2001) Brucellosis in sheep and goats (Brucella melitensis). Health & Consumer Protection Directorate-General, Brussels McCallum H, Barlow N, Hone J (2001) How should pathogen transmission be modelled? Trends Ecol Evol 16:295–300. https://doi.org/10.1016/S0169-5347(01)02144-9 Jesse M, Ezanno P, Davis S, Heesterbeek JAP (2008) A fully coupled, mechanistic model for infectious disease dynamics in a metapopulation: movement and epidemic duration. J Theor Biol 254:331–338. https://doi.org/10.1016/j.jtbi.2008.05.038 Sæther BE, Engen S, Filli F, Aanes R, Schröder W, Andersen R (2002) Stochastic population dynamics of an introduced Swiss population of the ibex. Ecology 83:3457–3465. https://doi.org/10.1890/0012-9658(2002)083[3457:SPDOAI]2.0.CO;2 Willisch CS, Biebach I, Koller U, Bucher T, Marreros N, Ryser-Degiorgis MP, Keller LF, Neuhaus P (2012) Male reproductive pattern in a polygynous ungulate with a slow life-history: the role of age, social status and alternative mating tactics. Evol Ecol 26:187–206. https://doi.org/10.1007/s10682-011-9486-6 Augustine DJ (1998) Modelling Chlamydia–koala interactions: coexistence, population dynamics and conservation implications. J Appl Ecol 35:261–272. https://doi.org/10.1046/j.1365-2664.1998.00307.x Godfroid J, Bishop GC, Bosman PP, Herr S (2004) Bovine brucellosis. In: Coetzer JAW, Tustin RC (eds) Infectious diseases of livestock, 2nd edn. Oxford University Press, Cape Town, pp 1510–1527 Bonenfant C, Gaillard JM, Coulson T, Festa-Bianchet M, Loison A, Garel M, Loe LE, Blanchard P, Pettorelli N, Owen-Smith N, Du Toit J, Duncan P, Caswell H (2009) Empirical evidence of density-dependence in populations of large herbivores. In: Caswell H (ed) Advances in ecological research. Elsevier Academic Press Inc, San Diego, pp 313–357 Toïgo C, Gaillard JM, Festa-Bianchet M, Largo E, Michallet J, Maillard D (2007) Sex- and age-specific survival of the highly dimorphic Alpine ibex: evidence for a conservative life-history tactic. J Anim Ecol 76:679–686. https://doi.org/10.1111/j.1365-2656.2007.01254.x Conner MM, Miller MW (2004) Movement patterns and spatial epidemiology of a prion disease in mule deer population units. Ecol Appl 14:1870–1881. https://doi.org/10.1890/03-5309 Islam A, Khatun M, Baek BK (2013) Male rats transmit Brucella abortus biotype 1 through sexual intercourse. Vet Microbiol 165:475–477. https://doi.org/10.1016/j.vetmic.2013.04.016 Plommet M, Fensterbank R, Renoux G, Gestin J, Philippon A (1973) Brucellose bovine expérimentale. XII. - Persistance à l’âge adulte de l’infection congénitale de la génisse. Ann Rech Vét 4:419–435 (in French) Philippon A, Renouy G, Plommet M, Bosseray N (1971) Brucellose bovine expérimentale. V. - Excrétion de “Brucella abortus” par le colostrum et le lait. Ann Rech Vét 2:59–67 (in French) Grilló MJ, Barberán M, Blasco JM (1997) Transmission of Brucella melitensis from sheep to lambs. Vet Rec 140:602–605. https://doi.org/10.1136/vr.140.23.602 Grignolio S, Rossi I, Bertolotto E, Bassano B, Apollonio M (2007) Influence of the kid on space use and habitat selection of female Alpine ibex. J Wildl Manag 71:713–719. https://doi.org/10.2193/2005-675 Grignolio S, Rossi I, Bassano B, Apollonio M (2007) Predation risk as a factor affecting sexual segregation in Alpine ibex. J Mammal 88:1488–1497. https://doi.org/10.1644/06-MAMM-A-351R.1 Kobilinsky A, Bouvier A, Monod H (2015) PLANOR: an R package for the automatic generation of regular fractional factorial designs. R package version 0.2–4. INRA, MIA, Jouy-en-Josas Bailey R (2008) Design of comparative experiments. Cambridge University Press, Cambridge Kobilinsky A (1997) Les plans factoriels. In: Droesbeke J-J, Fine J, Saporta G (eds) Plans d’expériences: applications à l’entreprise. Technip, Paris, pp 69–209 (in French) Blasco JM (1997) A review of the use of B. melitensis Rev 1 vaccine in adult sheep and goats. Prev Vet Med 31:275–283. https://doi.org/10.1016/S0167-5877(96)01110-5 Elberg SS, Faunce K (1957) Immunization against Brucella infection VI. Immunity conferred on goats by a nondependent mutant from a streptomycin-dependent mutant strain of Brucella melitensis. J Bacteriol 73:211–217 Blasco JM (2010) Control and eradication strategies for Brucella melitensis infection in sheep and goats. Prilozi 31:145–165 Elberg SS (1959) Immunization against Brucella infection. Bull World Health Organ 20:1033–1052 Alton GG (1968) Further studies on the duration of the immunity produced in goats by the Rev. 1 Brucella melitensis vaccine. J Comp Pathol 78:173–178. https://doi.org/10.1016/0021-9975(68)90093-5 Thébault A, Toïgo C, Gaillard JM, Gauthier D, Vaniscotte A, Garin-Bastuji B, Ganière JP, Dufour B, Gilot-Fromont E (2015) First results of modelling brucellosis in a wild population of Alpine ibex (Capra ibex) under management strategies. Epidemics5. Clearwater Beach Treanor JJ, Johnson JS, Wallen RL, Cilles S, Crowley PH, Cox JJ, Maehr DS, White PJ, Plumb GE (2010) Vaccination strategies for managing brucellosis in Yellowstone bison. Vaccine 28:F64–F72. https://doi.org/10.1016/j.vaccine.2010.03.055