Same place, different time, head up: Multiple antipredator responses to a recolonizing apex predator

. 2023 Dec ; 69 (6) : 703-717. [epub] 20221026

Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37876645

Prey adjust their antipredator behavioral tactics to minimize the risk of an encounter with predators. Spatiotemporal responses of prey to predators have been reported, but the nature of antipredator response is not ubiquitous and it is the object of increasing interest, especially considering the recent recovery of large carnivores in Europe, and the potential for behavioral antipredator responses to elicit consequences at the ecosystem level. We have tested multiple antipredator responses by fallow deer Dama dama to wolf Canis lupus in a Mediterranean protected area recently recolonized by this apex predator. Through intensive camera trapping, we tested for temporal and spatial association between predator and prey, and we have also studied deer vigilance in forest habitats where focal observations are usually impossible. Wolf detection rates were spatially associated with those of fallow deer. Accordingly, no evidence was found for fallow deer avoiding sites with higher predator detection rates. Temporal activity patterns were significantly different between the 2 species, with the wolf being mainly nocturnal whereas fallow deer was active especially during daylight. A comparison with a preliminary study strongly suggests an increase in the diurnal activity of fallow deer along with the stabilization of wolf presence in the area. Both the rate and the duration of vigilance of female fallow deer increased with the local frequency of wolf activity. We suggest an antipredator response based on temporal-rather than spatial-avoidance, as well as increased vigilance.

Zobrazit více v PubMed

Apollonio M, Andersen R, Putman R, 2010. European Ungulates and Their Management in the 21st Century. Cambridge: Cambridge University Press.

Arrigoni PV, Gellini R, Innamorati M, Lenzi M, Grillini Cet al. , 1976. Relazione al consorzio per l’istituzione del “parco della maremma”. Inf Bot Ital 8:283–324.

Ausilio G, Sand H, Månsson J, Mathisen KM, Wikenros C, 2021. Ecological effects of wolves in anthropogenic landscapes: The potential for trophic cascades is context-dependent. Front Ecol Evol 8:481.

Barton K, 2012. Mumin: Multi-model Inference. R Package Version 1.7. 2. https://CRAN.R-project.org/package=MuMIn

Bates D, Mächler M, Bolker B, Walker S, 2015. Lme4: Linear Mixed-Effects Models Using Eigen and s4. R Package Version 1.1–7. 2014. http://CRAN.R-project.org/package=lme4.

Beschta RL, Ripple WJ, 2009. Large predators and trophic cascades in terrestrial ecosystems of the Western United States. Biol Conserv 142(11):2401–2414.

Bonsen GT, Wallach AD, Ben-Ami D, Keynan O, Khalilieh Aet al. , 2022. Tolerance of wolves shapes desert canid communities in the Middle East. Glob Ecol Conserv 36:e02139.

Bu H, Wang F, McShea WJ, Lu Z, Wang Det al. , 2016. Spatial co-occurrence and activity patterns of mesocarnivores in the temperate forests of Southwest China. PLoS ONE 11(10):e0164271. PubMed PMC

Bubnicki JW, Churski M, Schmidt K, Diserens TA, Kuijper DP, 2019. Linking spatial patterns of terrestrial herbivore community structure to trophic interactions. ELife 8:e44937. PubMed PMC

Burnham KP, Anderson DR.. 2002. A Practical Information-Theoretic Approach. Model Selection and Multimodel Inference. Vol. 2, 2nd edn. New York: Springer.

Caniglia R, Fabbri E, Greco C, Galaverni M, Manghi Let al. , 2013. Black coats in an admixed wolf × dog pack is melanism an indicator of hybridization in wolves? Eur J Wildlife Res 59(4):543–555.

Chapron G, Kaczensky P, Linnell JD, Von Arx M, Huber Det al. , 2014. Recovery of large carnivores in Europe’s modern human-dominated landscapes. Science 346(6216):1517–1519. PubMed

Chen A, Reperant L, Fischhoff IR, Rubenstein DI, 2021. Increased vigilance of plains zebras

Creel S, Christianson D, 2008. Relationships between direct predation and risk effects. Trends Ecol Evol 23(4):194–201. PubMed

Creel S, Schuette P, Christianson D, 2014. Effects of predation risk on group size, vigilance, and foraging behavior in an African ungulate community. Behav Ecol 25(4):773–784.

Creel S, Winnie J Jr, Maxwell B, Hamlin K, Creel M, 2005. Elk alter habitat selection as an antipredator response to wolves. Ecology 86(12):3387–3397.

Cusack JJ, Kohl MT, Metz MC, Coulson T, Stahler DRet al. , 2020. Weak spatiotemporal response of prey to predation risk in a freely interacting system. J Anim Ecol 89(1):120–131. PubMed PMC

Davidson Z, Valeix M, Loveridge AJ, Hunt JE, Johnson PJet al. , 2012. Environmental determinants of habitat and kill site selection in a large carnivore: Scale matters. J Mammal 93(3):677–685.

Davies AB, Tambling CJ, Kerley GI, Asner GP, 2016. Effects of vegetation structure on the location of lion kill sites in African thicket. PLoS ONE 11(2):e0149098. PubMed PMC

Delm MM, 1990. Vigilance for predators: Detection and dilution effects. Behav Ecol Sociobiol 26(5):337–342.

Endler J, 1986. Defence against predators. In: Feder M, Lauder G, editors. Predator-Prey Relationships: Perspectives and Approaches from the Study of Lower Vertebrates. Chicago (IL): University of Chicago Press, 109–134.

Escobedo R, Muro C, Spector L, Coppinger R, 2014. Group size, individual role differentiation and effectiveness of cooperation in a homogeneous group of hunters. J R Soc Interface 11(95):20140204. PubMed PMC

Fattorini L, Ferretti F, Pisani C, Sforzi A, 2011. Two-stage estimation of ungulate abundance in Mediterranean areas using pellet group count. Environ Ecol Stat 18(2):291–314.

Ferretti F, Fattorini N, 2021. Competitor densities, habitat, and weather: Effects on interspecific interactions between wild deer species. Integr Zool 16(5):670–684. PubMed PMC

Ferretti F, Lovari S, Mancino V, Burrini L, Rossa M, 2019. Food habits of wolves and selection of wild ungulates in a prey-rich Mediterranean coastal area. Mamm Biol 99:119–127.

Ferretti F, Pacini G, Belardi I, ten Cate B, Sensi Met al. , 2021. Recolonizing wolves and opportunistic foxes: Interference or facilitation? Biol J Linn Soc 132(1):196–210.

Ferretti F, Sforzi A, Lovari S, 2008. Intolerance amongst deer species at feeding: Roe deer are uneasy banqueters. Behav Proc 78(3):487–491. PubMed

Ford AT, Goheen JR, Augustine DJ, Kinnaird MF, O’Brien TGet al. , 2015. Recovery of African wild dogs suppresses prey but does not trigger a trophic cascade. Ecology 96(10):2705–2714. PubMed

Fortin D, Beyer HL, Boyce MS, Smith DW, Duchesne Tet al. , 2005 Wolves influence elk movements: Behavior shapes a trophic cascade in Yellowstone National Park. Ecology 86(5):1320–1330.

Foster VC, Sarmento P, Sollmann R, Tôrres N, Jácomo ATet al. , 2013. Jaguar and puma activity patterns and predator-prey interactions in four Brazilian biomes. Biotropica 45(3):373–379.

Frid A, 1997. Vigilance by female dall’s sheep: Interactions between predation risk factors. Anim Behav 53(4):799–808.

Fryxell JM, 1991. Forage quality and aggregation by large herbivores. Am Naturalist 138(2):478–498.

Gable TD, Homkes AT, Johnson-Bice SM, Windels SK, Bump JK, 2021. Wolves choose ambushing locations to counter and capitalize on the sensory abilities of their prey. Behav Ecol 32(2):339–348.

Gable TD, Stanger T, Windels SK, Bump JK, 2018. Do wolves ambush beavers? Video evidence for higher-order hunting strategies. Ecosphere 9(3):e02159.

Gable TD, Windels SK, Bruggink JG, Homkes AT, 2016. Where and how wolves PubMed PMC

Geffroy B, Samia DS, Bessa E, Blumstein DT, 2015. How nature-based tourism might increase prey vulnerability to predators. Trends Ecol Evol 30(12):755–765. PubMed

Ghigi A, 1911. Ricerche faunistiche e sistematiche sui mammiferi d’italia che formano oggetto di caccia. Natura 2(10–11):289–337.

Hartig F, 2019. Dharma: Residual Diagnostics for Hierarchical (Multi-level/mixed) Regression Models. R Package Version 0.1. 0. http://florianhartig.github.io/DHARMa

Hebblewhite M, Merrill E, McDonald T, 2005. Spatial decomposition of predation risk using resource selection functions: An example in a wolf - elk predator - prey system. Oikos 111(1):101–111.

Henrich M, Niederlechner S, Kröschel M, Thoma S, Dormann CFet al. , 2020. The influence of camera trap flash type on the behavioural reactions and trapping rates of red deer and roe deer. Remote Sens Ecol Conserv 6(3):399–410.

Jedrzejewski W, Schmidt K, Theuerkauf J, Jedrzejewska B, Okarma H, 2001. Daily movements and territory use by radio-collared wolves

Kohl MT, Stahler DR, Metz MC, Forester JD, Kauffman MJet al. , 2018. Diel predator activity drives a dynamic landscape of fear. Ecol Monogr 88(4):638–652.

Kuijper D, De Kleine C, Churski M, Van Hooft P, Bubnicki Jet al. , 2013. Landscape of fear in Europe: Wolves affect spatial patterns of ungulate browsing in Białowieża Primeval Forest, Poland. Ecography 36(12):1263–1275.

Kuijper D, Sahlén E, Elmhagen B, Chamaillé-Jammes S, Sand Het al. , 2016. Paws without claws? Ecological effects of large ­carnivores in anthropogenic landscapes. Proc R Soc B 283(1841):20161625. PubMed PMC

Kuijper DP, Bubnicki JW, Churski M, Mols B, Van Hooft P, 2015. Context dependence of risk effects: Wolves and tree logs create patches of fear in an old-growth forest. Behav Ecol 26(6):1558–1568.

Kuijper DP, Verwijmeren M, Churski M, Zbyryt A, Schmidt Ket al. , 2014. What cues do ungulates use to assess predation risk in dense temperate forests? PLoS ONE 9(1):e84607. PubMed PMC

Lashley MA, Chitwood MC, Biggerstaff MT, Morina DL, Moorman CEet al. , 2014. White-tailed deer vigilance: The influence of social and environmental factors. PLoS ONE 9(3):e90652. PubMed PMC

Li S, McShea WJ, Wang D, Lu Z, Gu X, 2012. Gauging the impact of management expertise on the distribution of large mammals across protected areas. Divers Distrib 18(12):1166–1176.

Li S, McShea WJ, Wang D, Shao L, Shi X, 2010. The use of infrared‐triggered cameras for surveying phasianids in Sichuan Province, China. Ibis 152(2):299–309.

Lima SL, 1998. Stress and decision-making under the risk of predation: Recent developments from behavioral, reproductive, and ecological perspectives. Adv Study Behav 27(8):215–290.

Lima SL, Bednekoff PA, 1999. Temporal variation in danger drives antipredator behavior: The predation risk allocation hypothesis. Am Naturalist 153(6):649–659. PubMed

Lima SL, Dill LM, 1990. Behavioral decisions made under the risk of predation: A review and prospectus. Can J Zool 68(4):619–640.

Lingle S, 2001. Anti-predator strategies and grouping patterns in white-tailed deer and mule deer. Ethology 107(4):295–314.

Lingle S, Pellis S, 2002. Fight or flight? Antipredator behavior and the escalation of coyote encounters with deer. Oecologia 131(1):154–164. PubMed

Lingle S, Pellis SM, Wilson WF, 2005. Interspecific variation in antipredator behaviour leads to differential vulnerability of mule deer and white-tailed deer fawns early in life. J Anim Ecol 74(6):1140–1149.

Lipetz VE, Bekoff M, 1982. Group size and vigilance in pronghorns. Z Tierpsychol 58(3):203–216.

Lucherini M, Reppucci JI, Walker RS, Villalba ML, Wurstten Aet al. , 2009. Activity pattern segregation of carnivores in the High Andes. J Mamm 90(6):1404–1409.

Lund U, Agostinelli C, Arai H, Gagliardi A, Portugues Eet al. , 2017. Circular statistics. R package version, 4–93.

MacNulty DR, Mech LD, Smith DW, 2007. A proposed ethogram of large-carnivore predatory behavior, exemplified by the wolf. J Mamm 88(3):595–605.

Magnusson A, Skaug H, Nielsen A, Berg C, Kristensen Ket al. , 2017. Package ‘glmmtmb’. https://github.com/glmmTMB.

Makin DF, Chamaillé-Jammes S, Shrader AM, 2017. Herbivores employ a suite of antipredator behaviours to minimize risk from ambush and cursorial predators. Anim Behav 127:225–231.

Mao JS, Boyce MS, Smith DW, Singer FJ, Vales DJet al. , 2005. Habitat selection by elk before and after wolf reintroduction in Yellowstone National Park. J Wildlife Manag 69(4):1691–1707.

Martin JL, Chamaillé-Jammes S, Waller DM, 2020. Deer, wolves, and people: Costs, benefits and challenges of living together. Biol Rev 95(3):782–801. PubMed

Mech L, Boitani L, 2003. Wolf Social Ecology: Wolves Behavior, Ecology and Conservation. Chicago (IL): University of Chicago Press. 1–34.

Mech LD, 2012. Is science in danger of sanctifying the wolf? Biol Conserv 150(1):143–149.

Mech LD, Smith DW, MacNulty DR, 2021. Introduction: The wolf as a killing machine. In: Mech LD, Smith DW, MacNulty DR, editors. Wolves on the Hunt: The Behavior of Wolves Hunting Wild Prey. Chicago (IL): University of Chicago Press, 1–9.

Melini D, Agrillo E, Ferretti F, Tonelli L, 2019. Piano di gestione della zsc/zps it51a0016 monti dell’uccellina. Alberese: Ente Parco Regionale della Maremma.

Mencagli M, Stefanini P, 2008. Carta della vegetazione per il piano del parco. Alberese: Ente Parco Regionale della Maremma,

Meredith M, Ridout M, 2017. Overlap: Estimates of Coefficient of Overlapping for Animal Activity Patterns. R Package Version 0.30. https://cran.R-project.Org/package= overlap. Accessed May 2017.

Meredith M, Ridout M, Meredith M, 2017. Estimates of coefficient of overlapping for animal activity patterns. R CRAN Repository.

Monterroso P, Alves PC, Ferreras P, 2014. Plasticity in circadian activity patterns of mesocarnivores in Southwestern Europe: Implications for species coexistence. Behav Ecol Sociobiol 68(9):1403–1417.

Mooring MS, Fitzpatrick TA, Nishihira TT, Reisig DD, 2004. Vigilance, predation risk, and the allee effect in desert bighorn sheep. J Wildlife Manag 68(3):519–532.

Mori E, Bagnato S, Serroni P, Sangiuliano A, Rotondaro Fet al. , 2020. Spatiotemporal mechanisms of coexistence in an European mammal community in a protected area of Southern Italy. J Zool 310(3):232–245.

Muro C, Escobedo R, Spector L, Coppinger R, 2011. Wolf-pack PubMed

Murray DL, Boutin S, O’Donoghue M, Nams VO, 1995. Hunting behaviour of a sympatric felid and canid in relation to vegetative cover. Anim Behav 50(5):1203–1210.

Nichols TC, 2015. Cooperative hunting of Canada geese

Niglio M, 1995. Home ranges, ritmi di attività e scelta dell, habitat di femmine di daino nel parco regionale della maremma [M. Sc. Thesis]. Bologna: University of Bologna.

Oberosler V, Groff C, Iemma A, Pedrini P, Rovero F, 2017. The influence of human disturbance on occupancy and activity patterns of mammals in the Italian Alps from systematic camera trapping. Mamm Biol 87(1):50–61.

Paine RT, 1969. A note on trophic complexity and community stability. Am Naturalist 103(929):91–93.

Palmer MS, Portales-Reyes C, Potter C, Mech LD, Isbell F, 2021. Behaviorally-mediated trophic cascade attenuated by prey use of risky places at safe times. Oecologia 195(1):235–248. PubMed

Pecorella I, Fattorini N, Macchi E, Ferretti F, 2019. Sex/age differences in foraging, vigilance and alertness in a social herbivore. Acta Ethol 22(1):1–8.

Périquet S, Valeix M, Loveridge AJ, Madzikanda H, Macdonald DWet al. , 2010. Individual vigilance of African herbivores while drinking: The role of immediate predation risk and context. Anim Behav 79(3):665–671.

Peterson R, Ciucci P, 2003. The wolf as a carnivore. In: Mech LD, Boitani L, editors. Wolves: Behavior, Ecology, and Conservation. Chicago (IL): Chicago Press, 104–130

Prugh LR, Stoner CJ, Epps CW, Bean WT, Ripple WJet al. , 2009. The rise of the mesopredator. BioScience 59(9):779–791.

Pulliam HR, 1973. On the advantages of flocking. J Theor Biol (38):419–422. PubMed

Ridout MS, Linkie M, 2009. Estimating overlap of daily activity patterns from camera trap data. J Agric Biol Environ Stat 14(3):322–337.

Ripari L, Premier J, Belotti E, Bluhm H, Breitenmoser-Würsten Cet al. , 2022. Human disturbance is the most limiting factor driving habitat selection of a large carnivore throughout Continental Europe. Biol Conserv 266:109446–109446.

Ripple WJ, Beschta RL, 2012. Large predators limit herbivore densities in northern forest ecosystems. Eur J Wildlife Res 58(4):733–742.

Ripple WJ, Estes JA, Beschta RL, Wilmers CC, Ritchie EGet al. , 2014. Status and ecological effects of the world’s largest carnivores. Science 343(6167):1241484. PubMed

Roberts G, 1996. Why individual vigilance declines as group size increases. Anim Behav 51(5):1077–1086.

Rossa M, Lovari S, Ferretti F, 2021. Spatiotemporal patterns of wolf, mesocarnivores and prey in a Mediterranean area. Behav Ecol Sociobiol 75(2):1–13.

Rowcliffe JM, Field J, Turvey ST, Carbone C, 2008. Estimating animal density using camera traps without the need for individual recognition. J Appl Ecol 45(4):1228–1236.

Salvatori M, Oberosler V, Augugliaro C, Krofel M, Rovero F, 2022. Effects of free-ranging livestock on occurrence and inter-specific interactions of a mammalian community. Ecol Appl 32:e2644. PubMed PMC

Samelius G, Andrén H, Kjellander P, Liberg O, 2013. Habitat selection and risk of predation: Re-colonization by lynx had limited impact on habitat selection by roe deer. PLoS ONE 8(9):e75469. PubMed PMC

San José C, Lovari S, Ferrari N, 1996. Temporal evolution of vigilance in roe deer. Behav Proc 38(2):155–159. PubMed

Sand H, Jamieson M, Andrén H, Wikenros C, Cromsigt Jet al. , 2021. Behavioral effects of wolf presence on moose habitat selection: Testing the landscape of fear hypothesis in an anthropogenic landscape. Oecologia 197(1):101–116. PubMed PMC

Schmitz OJ, Beckerman AP, O’Brien KM, 1997. Behaviorally mediated trophic cascades: Effects of predation risk on food web interactions. Ecology 78(5):1388–1399.

Schradin C, Vonk J, Shackelford T, 2019. Confusion effect. In: Vonk J, Shackelford TK, editors. Encyclopedia of Animal Cognition and Behaviour. Cham, Switzerland: Springer, 375–376.

Sforzi A, Tonelli L, Cortés-Selva F, Mastacchi R, Lanzi Let al. , 2013. Piano di gestione dei sic/sir it51a0039 [sie 113 e a113 (zps)] palude della trappola e bocca d’ombrone, it51a0014 [sir 114] pineta granducale dell’uccellina e it51a0015 [sir 115] dune costiere del parco dell’uccellina. Ente Parco Regionale della Maremma.

Shannon G, Cordes LS, Hardy AR, Angeloni LM, Crooks KR, 2014. Behavioral responses associated with a human-mediated predator shelter. PLoS ONE 9(4):e94630. PubMed PMC

Shrader AM, Brown JS, Kerley GI, Kotler BP, 2008. Do free-ranging domestic goats show ‘landscapes of fear’? Patch use in response to habitat features and predator cues. J Arid Environ 72(10):1811–1819.

Sirot E, Blanchard P, Loison A, Pays O, 2021. How vigilance shapes the functional response of herbivores. Funct Ecol 35:1491–1500.

Sirot E, Touzalin F, 2009. Coordination and synchronization of vigilance in groups of prey: The role of collective detection and predators’ preference for stragglers. Am Naturalist 173(1):47–59. PubMed

Smith JA, Donadio E, Bidder OR, Pauli JN, Sheriff MJet al. , 2020. Where and when to hunt? Decomposing predation success of an ambush carnivore. Ecology 101(12):e03172. PubMed

Sönnichsen L, Bokje M, Marchal J, Hofer H, Jędrzejewska Bet al. , 2013. Behavioural responses of European roe deer to temporal variation in predation risk. Ethology 119(3):233–243.

Tambling CJ, Minnie L, Meyer J, Freeman EW, Santymire RMet al. , 2015. Temporal shifts in activity of prey following large predator reintroductions. Behav Ecol Sociobiol 69(7):1153–1161.

Thaker M, Vanak AT, Owen CR, Ogden MB, Niemann SMet al. , 2011. Minimizing predation risk in a landscape of multiple predators: Effects on the spatial distribution of African ungulates. Ecology 92(2):398–407. PubMed

Theuerkauf J, Rouys S, 2008. Habitat selection by ungulates in relation to predation risk by wolves and humans in the Białowieża Forest, Poland. Forest Ecol Manag 256(6):1325–1332.

Tobler MW, Carrillo-Percastegui SE, Leite Pitman R, Mares R, Powell G, 2008. An evaluation of camera traps for inventorying large-and medium-sized terrestrial rainforest mammals. Anim Conserv 11(3):169–178.

Toïgo C, 1999. Vigilance behavior in lactating female alpine ibex. Can J Zool 77(7):1060–1063.

Torretta E, Caviglia L, Serafini M, Meriggi A, 2018. Wolf predation on wild ungulates: How slope and habitat cover influence the localization of kill sites. Curr Zool 64(3):271–275. PubMed PMC

Torretta E, Mosini A, Piana M, Tirozzi P, Serafini Met al. , 2017. Time partitioning in mesocarnivore communities from different habitats of NW Italy: Insights into Martens’ competitive abilities. Behaviour 154(2):241–266.

Torretta E, Serafini M, Puopolo F, Schenone L, 2016. Spatial and temporal adjustments allowing the coexistence among carnivores in Liguria (NW Italy). Acta Ethol 19(2):123–132.

Valeix M, Fritz H, Loveridge AJ, Davidson Z, Hunt JEet al. , 2009. Does the risk of encountering lions influence African herbivore behaviour at waterholes? Behav Ecol Sociobiol 63(10):1483–1494.

Wallach AD, Izhaki I, Toms JD, Ripple WJ, Shanas U, 2015. What is an apex predator? Oikos 124(11):1453–1461.

Weitzman MS, 1970. Measures of Overlap of Income Distributions of White And Negro Families in the United States. Washington (DC): US Bureau of the Census.

Weterings MJ, Meister N, Fey K, Jansen PA, van Langevelde Fet al. , 2022. Context-dependent responses of naïve ungulates to wolf-sound playback in a human-dominated landscape. Anim Behav 185:9–20.

Wilson RP, Griffiths IW, Mills MG, Carbone C, Wilson JWet al. , 2015. Mass enhances speed but diminishes turn capacity in terrestrial pursuit predators. Elife 4:e06487. PubMed PMC

Zanni M, Brivio F, Grignolio S, Apollonio M, 2021. Estimation of spatial and temporal overlap in three ungulate species in a Mediterranean environment. Mamm Res 66(1):149–162.

Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM, 2009. Mixed Effects Models and Extensions in Ecology with R. Springer Science & Business Media.

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...