Abstract
Avoiding death affects biological processes, including behavior. Habitat selection, movement, and sociality are highly flexible behaviors that influence the mortality risks and subsequent fitness of individuals. In the Anthropocene, animals are experiencing increased risks from direct human causes and increased spread of infectious diseases. Using integrated step selection analysis, we tested how the habitat selection, movement, and social behaviors of gray wolves vary in the two months prior to death due to humans (being shot or trapped) or canine distemper virus (CDV). We further tested how those behaviors vary as a prelude to death. We studied populations of wolves that occurred under two different management schemes: a national park managed for conservation and a provincially managed multi-use area. Behaviors that changed prior to death were strongly related to how an animal eventually died. Wolves killed by humans moved slower than wolves that survived and selected to be nearer roads closer in time to their death. Wolves that died due to CDV moved progressively slower as they neared death and reduced their avoidance of wet habitats. All animals, regardless of dying or living, maintained selection to be near packmates across time, which seemingly contributed to disease dynamics in the packs infected with CDV. There were no noticeable differences in behavior between the two management areas. Overall, habitat selection, movement, and sociality interact to put individuals and groups at greater risks, influencing their cause-specific mortality.
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Data availability
Data and code are available at https://zenodo.org/record/8187843 and https://github.com/JWTurn/WolfDeathComing.
References
Albery GF, Kirkpatrick L, Firth JA, Bansal S (2020) Unifying spatial and social network analysis in disease ecology. J Anim Ecol 30:17. https://doi.org/10.1111/1365-2656.13356
Almberg ES, Cross PC, Dobson AP, Smith DW, Metz MC, Stahler DR, Hudson PJ (2015) Social living mitigates the costs of a chronic illness in a cooperative carnivore. Ecol Lett 18:660–667. https://doi.org/10.1111/ele.12444
Altizer S, Bartel R, Han BA (2011) Animal migration and infectious disease risk. Science 331:296–302. https://doi.org/10.1126/science.1194694
Avgar T, Potts JR, Lewis MA, Boyce MS (2016) Integrated step selection analysis: bridging the gap between resource selection and animal movement. Methods Ecol Evol 7:619–630. https://doi.org/10.1111/2041-210X.12528
Avgar T, Lele SR, Keim JL, Boyce MS (2017) Relative selection strength: quantifying effect size in habitat- and step-selection inference. Ecol Evol 7:5322–5330. https://doi.org/10.1002/ece3.3122
Avgar T, Betini GS, Fryxell JM (2020) Habitat selection patterns are density dependent under the ideal free distribution. J Anim Ecol. https://doi.org/10.1111/1365-2656.13352
Bartoń KA, Zwijacz-Kozica T, Zięba F, Sergiel A, Selva N (2019) Bears without borders: long-distance movement in human-dominated landscapes. Global Ecol Conserv 17:e00541. https://doi.org/10.1016/j.gecco.2019.e00541
Bastille-Rousseau G, Wittemyer G (2022) Simple metrics to characterize inter-individual and temporal variation in habitat selection behaviour. J Anim Ecol. https://doi.org/10.1111/1365-2656.13738
Becker DJ, Albery GF, Kessler MK, Lunn TJ, Falvo CA, Czirják GÁ, Martin LB, Plowright RK (2020) Macroimmunology: the drivers and consequences of spatial patterns in wildlife immune defence. J Anim Ecol 89:972–995. https://doi.org/10.1111/1365-2656.13166
Behringer DC, Butler MJ, Shields JD (2006) Avoidance of disease by social lobsters. Nature 441:421–421. https://doi.org/10.1038/441421a
Beineke A, Baumgärtner W, Wohlsein P (2015) Cross-species transmission of canine distemper virus—an update. One Health 1:49–59. https://doi.org/10.1016/j.onehlt.2015.09.002
Blecha KA, Boone RB, Alldredge MW (2018) Hunger mediates apex predator’s risk avoidance response in wildland-urban interface. J Anim Ecol 87:609–622. https://doi.org/10.1111/1365-2656.12801
Blixenkrone-Møller M, Svansson V, Have P, Orvell C, Appel M, Pedersen IR, Dietz HH, Henriksen P (1993) Studies on manifestations of canine distemper virus infection in an urban dog population. Vet Microbiol 37:163–173
Boydston EE, Kapheim KM, Van Horn RC, Smale L, Holekamp KE (2005) Sexually dimorphic patterns of space use throughout ontogeny in the spotted hyena (Crocuta crocuta). J Zool Lond 267:271–281. https://doi.org/10.1017/S0952836905007478
Broekhuis F, Madsen EK, Klaassen B (2019) Predators and pastoralists: how anthropogenic pressures inside wildlife areas influence carnivore space use and movement behaviour. Anim Conserv 22:404–416. https://doi.org/10.1111/acv.12483
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Maechler M, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9:378–400
Buderman FE, Hooten MB, Alldredge MW, Hanks EM, Ivan JS (2018) Time-varying predatory behavior is primary predictor of fine-scale movement of wildland-urban cougars. Move Ecol 6:1–16. https://doi.org/10.1186/s40462-018-0140-6
Byrne AW, O’Keeffe J, Buesching CD, Newman C (2018) Push and pull factors driving movement in a social mammal: context dependent behavioral plasticity at the landscape scale. Curr Zool 65:517–525. https://doi.org/10.1093/cz/zoy081
Calenge C (2006) The package “adehabitat” for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model 197:516–519. https://doi.org/10.1016/j.ecolmodel.2006.03.017
Campana JLM, Raffard A, Chaine AS, Huet M, Legrand D, Jacob S (2022) Dispersal plasticity driven by variation in fitness across species and environmental gradients. Ecology Lett ele. https://doi.org/10.1111/ele.14101
Cantor M, Maldonado-Chaparro AA, Beck KB, Brandl HB, Carter GG, He P, Hillemann F, Klarevas-Irby JA, Ogino M, Papageorgiou D, Prox L, Farine DR (2020) The importance of individual-to-society feedbacks in animal ecology and evolution. J Anim Ecol. https://doi.org/10.1111/1365-2656.13336
Caravaggi A, Banks PB, Burton AC, Finlay CMV, Haswell PM, Hayward MW, Rowcliffe MJ, Wood MD (2017) A review of camera trapping for conservation behaviour research. Remote Sens Ecol Conserv 3:109–122. https://doi.org/10.1002/rse2.48
Cleaveland S, Mlengeya T, Kaare M, Haydon D, Lembo T, Laurenson MK, Packer C (2007) The conservation relevance of epidemiological research into carnivore viral diseases in the Serengeti. Conserv Biol 21:612–622. https://doi.org/10.1111/j.1523-1739.2007.00701.x
Commission for Environmental Cooperation, 2020. 2015 Land Cover of North America at 30 meters
Dickie M, McNay SR, Sutherland GD, Cody M, Avgar T (2019) Corridors or risk? Movement along, and use of, linear features varies predictably among large mammal predator and prey species. J Anim Ecol 8:1–12. https://doi.org/10.1111/1365-2656.13130
Duque-Valencia J, Sarute N, Olarte-Castillo XA, Ruíz-Sáenz J (2019) Evolution and interspecies transmission of canine distemper virus—an outlook of the diverse evolutionary landscapes of a multi-host virus. Viruses 11:582. https://doi.org/10.3390/v11070582
Eberhard MJW (1975) The evolution of social behavior by kin selection. Q Rev Biol 50:33. https://doi.org/10.1086/408298
Fairbanks BM, Hawley DM, Alexander KA (2014a) The Impact of health status on dispersal behavior in banded mongooses (Mungos mungo). EcoHealth 11:258–262. https://doi.org/10.1007/s10393-014-0912-4
Fairbanks BM, Hawley DM, Alexander KA (2014b) No evidence for avoidance of visibly diseased conspecifics in the highly social banded mongoose (Mungos mungo). Behav Ecol Sociobiol 69:371–381. https://doi.org/10.1007/s00265-014-1849-x
Farias V, Fuller TK, Wayne RK, Sauvajot RM (2005) Survival and cause-specific mortality of gray foxes (Urocyon cinereoargenteus) in southern California. J Zool (Lond) 266:249–254. https://doi.org/10.1017/S0952836905006850
Ferry NS (1911) Etiology of canine distemper. J Infect Dis 8:399–420. https://doi.org/10.2307/30074785?refreqid=search-gateway:bc87f7fcbd5c27e8efcaea6bdc071cce
Fieberg J, Signer J, Smith B, Avgar T (2021) A ‘How to’ guide for interpreting parameters in habitat-selection analyses. J Anim Ecol. https://doi.org/10.1111/1365-2656.13441
Forester JD, Ives AR, Turner MG, Anderson DP, Fortin D, Beyer HL, Smith DW, Boyce MS (2007) State–space models link elk movement patterns to landscape characteristics in yellowstone national park. Ecol Monogr 77:285–299. https://doi.org/10.1890/06-0534
Fortin D, Beyer HL, Boyce MS, Smith DW, Duchesne T, Mao JS (2005) Wolves influence elk movements: behavior shapes a trophic cascade in Yellowstone national park. Ecology 86:1320–1330. https://doi.org/10.1890/04-0953
Fuller TK, Mech LD, Cochrane JF (2003) Wolf Population Dynamics. Wolves: behavior, ecology, and conservation. University of Chicago Press, Chicago, pp 161–191
Gaynor KM, Brown JS, Middleton AD, Power ME, Brashares JS (2019) Landscapes of fear: spatial patterns of risk perception and response. Trends Ecol Evol. https://doi.org/10.1016/j.tree.2019.01.004
Geffre AC, Gernat T, Harwood GP, Jones BM, Morselli Gysi D, Hamilton AR, Bonning BC, Toth AL, Robinson GE, Dolezal AG (2020) Honey bee virus causes context-dependent changes in host social behavior. Proc Natl Acad Sci USA 117:10406–10413. https://doi.org/10.1073/pnas.2002268117
Gigliotti LC, Slotow R, Hunter LTB, Fattebert J, Sholto-Douglas C, Jachowski DS (2020) Habitat complexity and lifetime predation risk influence mesopredator survival in a multi-predator system. Sci Rep 10:17841. https://doi.org/10.1038/s41598-020-73318-3
Greenberg JR, Holekamp KE (2017) Human disturbance affects personality development in a wild carnivore. YANBE 132:303–312. https://doi.org/10.1016/j.anbehav.2017.08.023
Guindre-Parker S, Rubenstein DR (2020) Survival benefits of group living in a fluctuating environment. Am Nat 195:1027–1036. https://doi.org/10.1086/708496
Hart BL (2011) Behavioural defences in animals against pathogens and parasites: parallels with the pillars of medicine in humans. Phil Trans R Soc B 366:3406–3417. https://doi.org/10.1098/rstb.2011.0092
Hart EE, Fennessy J, Chari S, Ciuti S (2019) Habitat heterogeneity and social factors drive behavioral plasticity in giraffe herd-size dynamics. J Mammal 101:248–258. https://doi.org/10.1093/jmammal/gyz191
Haswell PM, Kusak J, Hayward MW (2017) Large carnivore impacts are context-dependent. Food Webs 12:3–13. https://doi.org/10.1016/j.fooweb.2016.02.005
He P, Maldonado-Chaparro AA, Farine DR (2019) The role of habitat configuration in shaping social structure: a gap in studies of animal social complexity. Behav Ecol Sociobiol 73:1–14. https://doi.org/10.1007/s00265-018-2602-7
Hebblewhite M, Whittington J (2020) Wolves without borders: transboundary survival of wolves in Banff national park over three decades. Global Ecol Conserv 24:e01293. https://doi.org/10.1016/j.gecco.2020.e01293
Heinze J, Walter B (2010) Moribund ants leave their nests to die in social isolation. Curr Biol 20:249–252. https://doi.org/10.1016/j.cub.2009.12.031
Herrero A, Heikkinen J, Holmala K (2020) Movement patterns and habitat selection during dispersal in Eurasian lynx. Mamm Res 31:1–11. https://doi.org/10.1007/s13364-020-00499-7
Houle M, Fortin D, Dussault C, Courtois R, Ouellet J-P (2010) Cumulative effects of forestry on habitat use by gray wolf (Canis lupus) in the boreal forest. Landscape Ecol 25:419–433. https://doi.org/10.1007/s10980-009-9420-2
Jęodrzejewska B, Jęodrzejewski W, Bunevich AN, Milkowski L, Okarma H (1996) Population dynamics of wolves Canis lupus in Bialowieża Primeval forest (Poland and Belarus) in relation to hunting by humans, 1847–1993. Mam Rev 26:103–126
Joly K, Gurarie E, Sorum MS, Kaczensky P, Cameron MD, Jakes AF, Borg BL, Nandintsetseg D, Hopcraft JGC, Buuveibaatar B, Jones PF, Mueller T, Walzer C, Olson KA, Payne JC, Yadamsuren A, Hebblewhite M (2019) Longest terrestrial migrations and movements around the world. Sci Rep 9:1–10. https://doi.org/10.1038/s41598-019-51884-5
Kikusui T, Winslow JT, Mori Y (2006) Social buffering: relief from stress and anxiety. Phil Trans R Soc B 361:2215–2228. https://doi.org/10.1098/rstb.2006.1941
Knowlton JL, Graham CH (2010) Using behavioral landscape ecology to predict species’ responses to land-use and climate change. Biol Cons 143:1342–1354. https://doi.org/10.1016/j.biocon.2010.03.011
Lamb CT, Ford AT, McLellan BN, Proctor MF, Mowat G, Ciarniello L, Nielsen SE, Boutin S (2020) The ecology of human-carnivore coexistence. Proc Natl Acad Sci USA 117:17876–17883. https://doi.org/10.1073/pnas.1922097117
Lesmerises F, dà Ric M, Dussault C, St-Laurent M-H (2012) Wolf habitat selection is shaped by human activities in a highly managed boreal forest. Forest Ecol Manag 276:125–131. https://doi.org/10.1016/j.foreco.2012.03.025
Loots AK, Mitchell E, Dalton DL, Kotzé A, Venter EH (2017) Advances in canine distemper virus pathogenesis research: a wildlife perspective. J Gen Virol 98:311–321. https://doi.org/10.1099/jgv.0.000666
Lopes PC, Block P, König B (2016) Infection-induced behavioural changes reduce connectivity and the potential for disease spread in wild mice contact networks. Sci Rep 6:31790. https://doi.org/10.1038/srep31790
Lüdecke D, Ben-Shachar M, Patil I, Waggoner P, Makowski D (2021) Performance: an R package for assessment, comparison and testing of statistical models. JOSS 6:3139. https://doi.org/10.21105/joss.03139
Mancinelli S, Falco M, Boitani L, Ciucci P (2019) Social, behavioural and temporal components of wolf (Canis lupus) responses to anthropogenic landscape features in the central Apennines. Italy J Zool Lond 19:247–311. https://doi.org/10.1111/jzo.12708
Martin J, Basille M, Van Moorter B, Kindberg J, Allainé D, Swenson JE (2010) Coping with human disturbance: spatial and temporal tactics of the brown bear (Ursus arctos ). Can J Zool 88:875–883. https://doi.org/10.1139/Z10-053
Matthiopoulos J, Fieberg JR, Aarts G (2020) Species-habitat associations: spatial data, predictive models, and ecological insights. University of Minnesota Libraries Publishing, Minneapolis. https://doi.org/10.24926/2020.081320
McLoughlin PD, Morris DW, Fortin D, Vander Wal E, Contasti AL (2010) Considering ecological dynamics in resource selection functions. J Anim Ecol 79:4–12. https://doi.org/10.1111/j.1365-2656.2009.01613.x
Morris DW (2003) Toward an ecological synthesis: a case for habitat selection. Oecologia 136:1–13. https://doi.org/10.1007/s00442-003-1241-4
Muff S, Signer J, Fieberg J (2019) Accounting for individual-specific variation in habitat-selection studies: efficient estimation of mixed-effects models using Bayesian or frequentist computation. J Anim Ecol 82:1135–1213. https://doi.org/10.1111/1365-2656.13087
Murray MH, St Clair CC (2015) Individual flexibility in nocturnal activity reduces risk of road mortality for an urban carnivore. Behav Ecol 26:1520–1527. https://doi.org/10.1093/beheco/arv102
Murray MH, St Clair CC (2017) Predictable features attract urban coyotes to residential yards. Jour Wild Mgmt 81:593–600. https://doi.org/10.1002/jwmg.21223
Murray DL, Smith DW, Bangs EE, Mack C, Oakleaf JK, Fontaine J, Boyd D, Jiminez M, Niemeyer C, Meier TJ, Stahler D, Holyan J, Asher VJ (2010) Death from anthropogenic causes is partially compensatory in recovering wolf populations. Biol Cons 143:2514–2524. https://doi.org/10.1016/j.biocon.2010.06.018
Nathan R, Getz WM, Revilla E, Holyoak M, Kadmon R, Saltz D, Smouse PE (2008) A movement ecology paradigm for unifying organismal movement research. Proc Natl Acad Sci USA 105:19052–19059. https://doi.org/10.1073/pnas.0800375105
Nickel BA, Suraci JP, Allen ML, Wilmers CC (2019) Human presence and human footprint have non-equivalent effects on wildlife spatiotemporal habitat use. Biol Conserv 241:108383. https://doi.org/10.1016/j.biocon.2019.108383
Palmer MS, Gaynor KM, Becker JA, Abraham JO, Mumma MA, Pringle RM (2022) Dynamic landscapes of fear: understanding spatiotemporal risk. Trends Ecol Evolut. https://doi.org/10.1016/j.tree.2022.06.007
Pigeon KE, MacNearney D, Hebblewhite M, Musiani M, Neufeld L, Cranston J, Stenhouse G, Schmiegelow F, Finnegan L (2020) The density of anthropogenic features explains seasonal and behaviour-based functional responses in selection of linear features by a social predator. Sci Rep 10:1–13. https://doi.org/10.1038/s41598-020-68151-7
Prager KC, Mazet JAK, Munson L, Cleaveland S, Donnelly CA, Dubovi EJ, Gunther MS, Lines R, Mills G, Davies-Mostert HT, McNutt JW, Rasmussen G, Terio K, Woodroffe R (2012) The effect of protected areas on pathogen exposure in endangered African wild dog (Lycaon pictus) populations. Biol Cons 150:15–22. https://doi.org/10.1016/j.biocon.2012.03.005
Prokopenko CM, Boyce MS, Avgar T (2016) Characterizing wildlife behavioural responses to roads using integrated step selection analysis. J Appl Ecol 54:470–479. https://doi.org/10.1111/1365-2664.12768
R Core Team, 2021. R: A language and environment for statistical computing
Recio MR, Zimmermann B, Wikenros C, Zetterberg A, Wabakken P, Sand H (2019) Integrated spatially-explicit models predict pervasive risks to recolonizing wolves in Scandinavia from human-driven mortality. Biol Cons 226:111–119. https://doi.org/10.1016/j.biocon.2018.07.025
Robitaille AL, Webber QMR, Vander Wal E (2019) Conducting social network analysis with animal telemetry data: applications and methods using spatsoc. Methods Ecol Evolut. https://doi.org/10.1111/2041-210X.13215
Rodeheffer C, von Messling V, Milot S, Lepine F, Manges AR, Ward BJ (2007) Disease manifestations of canine distemper virus infection in ferrets are modulated by vitamin A status. J Nutr 137:1916–1922. https://doi.org/10.1093/jn/137.8.1916
Sawyer H, LeBeau CW, McDonald TL, Xu W, Middleton AD (2019) All routes are not created equal: an ungulate’s choice of migration route can influence its survival. J Appl Ecol 56:1860–1869. https://doi.org/10.1111/1365-2664.13445
Sidorovich V, Schnitzler A, Schnitzler C, Rotenko I (2017) Wolf denning behaviour in response to external disturbances and implications for pup survival. Mamm Biol 87:89–92. https://doi.org/10.1016/j.mambio.2016.11.011
Signer J, Fieberg J, Avgar T (2019) Animal movement tools (amt): R package for managing tracking data and conducting habitat selection analyses. Ecol Evol 9:880–890. https://doi.org/10.1002/ece3.4823
Sih A, Stamps JA, Yang LH, McElreath R, Ramenofsky M (2010) Behavior as a key component of integrative biology in a human-altered world. Integr Comp Biol 50:934–944. https://doi.org/10.1093/icb/icq148
Silk JB (2007) The adaptive value of sociality in mammalian groups. Phil Trans R Soc B 362:539–559. https://doi.org/10.1098/rstb.2006.1994
Silk MJ, Croft DP, Delahay RJ, Hodgson DJ, Boots M, Weber N, McDonald RA (2017) Using social network measures in wildlife disease ecology, epidemiology, and management. Bioscience 67:245–257. https://doi.org/10.1093/biosci/biw175
Stillman RA, Goss-Custard JD, West AD, Dit Durell SEALV, Caldow RWG, McGrorty S, Clarke RT (2000) Predicting mortality in novel environments: tests and sensitivity of a behaviour-based model. J Appl Ecol 37:564–588. https://doi.org/10.1046/j.1365-2664.2000.00506.x
Stockmaier S, Bolnick DI, Page RA, Carter GG (2020) Sickness effects on social interactions depend on the type of behaviour and relationship. J Anim Ecol. https://doi.org/10.1111/1365-2656.13193
Stockmaier S, Stroeymeyt N, Shattuck EC, Hawley DM, Meyers LA, Bolnick DI (2021) Infectious diseases and social distancing in nature. Science. https://doi.org/10.1126/science.abc8881
Street GM, Potts JR, Börger L, Beasley JC, Demarais S, Fryxell JM, McLoughlin PD, Monteith KL, Prokopenko CM, Ribeiro MC, Rodgers AR, Strickland BK, Beest FM, Bernasconi DA, Beumer LT, Dharmarajan G, Dwinnell SP, Keiter DA, Keuroghlian A, Newediuk LJ, Oshima JEF, Rhodes O, Schlichting PE, Schmidt NM, Vander Wal E (2021) Solving the sample size problem for resource selection functions. Methods Ecol Evol. https://doi.org/10.1111/2041-210X.13701
Stronen AV, Sallows T, Forbes GJ, Wagner B, Paquet PC (2011) Diseases and parasites in wolves of the riding mountain national park region, Manitoba, Canada. J Wild Dis 47:222–227. https://doi.org/10.7589/0090-3558-47.1.222
Stronen AV, Forbes GJ, Paquet PC, Goulet G, Sallows T, Musiani M (2012) Dispersal in a plain landscape: short-distance genetic differentiation in southwestern Manitoba wolves, Canada. Conserv Genet 13:359–371. https://doi.org/10.1007/s10592-011-0290-1
Suraci JP, Clinchy M, Zanette LY, Wilmers CC (2019) Fear of humans as apex predators has landscape-scale impacts from mountain lions to mice. Ecol Letters 27:472–479. https://doi.org/10.1111/ele.13344
Theuerkauf J (2009) What drives wolves: fear or hunger? humans, diet, climate and wolf activity patterns. Ethology 115:649–657. https://doi.org/10.1111/j.1439-0310.2009.01653.x
Thompson NA (2019) Understanding the links between social ties and fitness over the life cycle in primates. Behaviour. https://doi.org/10.1163/1568539X-00003552
Vonholdt BM, Stahler DR, Smith DW, Earl DA, Pollinger JP, Wayne RK (2008) The genealogy and genetic viability of reintroduced Yellowstone grey wolves. Mol Ecol 17:252–274. https://doi.org/10.1111/j.1365-294X.2007.03468.x
Weary DM, Huzzey JM, von Keyserlingk MAG (2009) BOARD-INVITED REVIEW: using behavior to predict and identify ill health in animals1. J Anim Sci 87:770–777. https://doi.org/10.2527/jas.2008-1297
Webber QMR, Vander Wal E (2018) An evolutionary framework outlining the integration of individual social and spatial ecology. J Anim Ecol 87:113–127. https://doi.org/10.1111/1365-2656.12773
Webber QMR, Albery GF, Farine DR, Pinter-Wollman N, Sharma N, Spiegel O, Vander Wal E, Manlove K (2023) Behavioural ecology at the spatial–social interface. Biol Rev brv. https://doi.org/10.1111/brv.12934
Wynn-Grant R, Ginsberg JR, Lackey CW, Sterling EJ, Beckmann JP (2018) Risky business: modeling mortality risk near the urban-wildland interface for a large carnivore. Global Ecol Conserv 16:e00443. https://doi.org/10.1016/j.gecco.2018.e00443
Yirga G, Leirs H, De Iongh HH, Asmelash T, Gebrehiwot K, Deckers J, Bauer H (2015) Spotted hyena (Crocuta crocuta) concentrate around urban waste dumps across Tigray, northern Ethiopia. Wildl Res 42:563–568. https://doi.org/10.1071/WR14228
Zhao J, Shi N, Sun Y, Martella V, Nikolin V, Zhu C, Zhang H, Hu B, Bai X, Yan X (2015) Pathogenesis of canine distemper virus in experimentally infected raccoon dogs, foxes, and minks. Antiviral Res 122:1–11. https://doi.org/10.1016/j.antiviral.2015.07.007
Zylberberg M, Klasing KC, Hahn TP (2012) House finches (Carpodacus mexicanus) balance investment in behavioural and immunological defences against pathogens. Biol Let 9:20120856–20120856. https://doi.org/10.1098/rsbl.2012.0856
Acknowledgements
We would like to acknowledge that our research takes place within the traditional homeland of the Anishinaabe people and the Métis Nation, within Treaties 2, 3 and 5 Territory and at the crossroads of Treaties 1 and 4. This work would not be possible without the support of Parks Canada, Manitoba Wildlife and Fisheries Branch, and Manitoba Hydro. In particular, we thank K. Leavesley, V. Harriman, T. Sallows, D. Bergeson, K. Kingdon, R. Robinson, and R. Baird for their continuing support. We thank all members of the Wildlife Evolutionary Ecology Lab, including J. Balluffi-Fry, I. Richmond, J. Hogg, J. Kennah, A. Robitaille, J. Aubin, J. Hendrix, Q. Webber, S. Boyle, and L. Newediuk for their reviews. Thanks also to T. Avgar for input on the methods. Thanks to C. Berkvens, who conducted necropsies of wolf specimens. We also thank two anonymous reviewers. Funding for this study was provided by a NSERC Discovery Grant to EVW.
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JWT, CMP, and EVW conceptualized the idea and study design. CMP, KAK, DLJD, and SZS collected the field data. JWT ran the analyses and drafted the manuscript. All authors critically revised the manuscript and gave final approval for publication.
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Turner, J.W., Prokopenko, C.M., Kingdon, K.A. et al. Death comes for us all: relating movement-integrated habitat selection and social behavior to human-associated and disease-related mortality among gray wolves. Oecologia 202, 685–697 (2023). https://doi.org/10.1007/s00442-023-05426-6
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DOI: https://doi.org/10.1007/s00442-023-05426-6