Fear of large carnivores is tied to ungulate habitat use: evidence from a bifactorial experiment
1.Ripple, W. J. et al. Status and ecological effects of the world’s largest carnivores. Science 343, 1241484. https://doi.org/10.1126/science.1241484 (2014).CAS
Article
PubMed
PubMed Central
Google Scholar
2.Estes, J. A. et al. Trophic downgrading of planet Earth. Science 333, 301–306 (2011).ADS
CAS
PubMed
Article
PubMed Central
Google Scholar
3.Ford, A. T. & Goheen, J. R. Trophic cascades by large carnivores: A case for strong Inference and mechanism. Trend Ecol. Evol. 30, 725–735 (2015).Article
Google Scholar
4.Suraci, J. P., Clinchy, M., Dill, L. M., Roberts, D. & Zanette, L. Y. Fear of large carnivores causes a trophic cascade. Nat. Commun. 7, 10698. https://doi.org/10.1038/ncomms10698 (2016).ADS
CAS
Article
PubMed
PubMed Central
Google Scholar
5.Atkins, J. L. et al. Cascading impacts of large-carnivore extirpation in an African ecosystem. Science 364, 173–177 (2019).ADS
CAS
PubMed
PubMed Central
Google Scholar
6.Brown, J. S., Laundre, J. W. & Gurung, M. The ecology of fear: Optimal foraging, game theory and trophic interactions. J. Mammal. 80, 385–399 (1999).Article
Google Scholar
7.Brown, J. S. Ecology of fear. In Encyclopedia of Animal Behaviour (ed. Chun, C.) (Academic Press, 2019).
Google Scholar
8.Trussell, G. C., Ewanchuk, P. J. & Matassa, C. M. The fear of being eaten reduces energy transfer in a simple food chain. Ecology 87, 2979–2984 (2006).PubMed
Article
PubMed Central
Google Scholar
9.Schmitz, O. J., Krivan, V. & Ovadia, O. Trophic cascades: The primacy of trait-mediated indirect interactions. Ecol. Lett. 7, 153–163 (2004).Article
Google Scholar
10.Say-Sallaz, E., Chamaillé-James, S., Fritz, H. & Valeix, M. Non-consumptive effects of predation in large terrestrial mammals: Mapping our knowledge and revealing the tip of the iceberg. Biol. Conserv. 235, 36–52 (2019).Article
Google Scholar
11.Malhi, Y. et al. Megafauna and ecosystem function from the Pleistocene to the Anthropocene. Proc. Natl. Acad. Sci. U.S.A. 113, 838–846 (2016).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
12.Asner, G. P. et al. Large-scale impacts of herbivores on the structural diversity of African savannas. Proc. Natl. Acad. Sci. USA 106, 4947–4952 (2009).ADS
CAS
PubMed
Article
PubMed Central
Google Scholar
13.Ford, A. T. et al. Large carnivores make savanna tree communities less thorny. Science 346, 346–349 (2014).ADS
CAS
PubMed
Article
PubMed Central
Google Scholar
14.Bernes, C. et al. Manipulating ungulate herbivory in temperate and boreal forests: effects on vegetation and invertebrates: A systematic review. Environ. Evid. 7, 13. https://doi.org/10.1186/s13750-018-0125-3 (2018).Article
Google Scholar
15.Creel, S. The control of risk hypothesis: Reactive vs proactive antipredator responses and stress-mediated vs food-mediated costs of response. Ecol. Lett. 21, 947–956 (2018).PubMed
Article
PubMed Central
Google Scholar
16.Riginos, C. Climate and the landscape of fear in an African savanna. J. Anim. Ecol. 84, 124–133 (2015).PubMed
Article
PubMed Central
Google Scholar
17.le Roux, E. G., Kerley, I. H. & Cromsigt, J. P. G. M. Megaherbivores modify trophic cascades triggered by fear of predation in an African savanna ecosystem. Curr. Biol. 28, 2493–2499 (2018).PubMed
Article
CAS
PubMed Central
Google Scholar
18.Eldridge, D. J. et al. Impacts of shrub encroachment on ecosystem structure and functioning: Towards a global synthesis. Ecol. Lett. 14, 709–722 (2011).PubMed
PubMed Central
Article
Google Scholar
19.Stanton, R. A. et al. Shrub encroachment and vertebrate diversity: A global meta-analysis. Glob. Ecol. Biogeogr. 27, 368–379 (2018).Article
Google Scholar
20.Soto-Shoender, J. R., McCleery, R. A., Monadjem, A. & Gwinn, D. C. The importance of grass cover for mammalian diversity and habitat associations in a bush encroached savanna. Biol. Conserv. 221, 127–136 (2018).Article
Google Scholar
21.Courbin, N. et al. Reactive responses of zebra to lion encounters shape their predator-prey space game at large scale. Oikos 125, 829–838 (2016).Article
Google Scholar
22.van Buskirk, J. Specific induced responses to different predator species in anuran larvae. J. Evol. Biol. 14, 482–489 (2001).Article
Google Scholar
23.Chalcraft, D. R. & Resetarits, W. J. Jr. Predator identity and ecological impacts: Functional redundancy or functional diversity?. Ecology 84, 2407–2418 (2003).Article
Google Scholar
24.Templeton, C. N., Greene, E. & Davis, K. Allometry of alarm calls: Black-capped chickadees encode information about predator size. Science 308, 1934–1937 (2005).ADS
CAS
PubMed
Article
PubMed Central
Google Scholar
25.Cooper, W. E. Jr. & Frederick, W. G. Predator lethality, optimal escape behavior, and autonomy. Behav. Eco. 21, 91–96 (2009).Article
Google Scholar
26.Dröge, E., Creel, S., Becker, M. S. & Msoka, J. Risky times and risky places interact to affect prey behaviour. Nat. Ecol. Evol. 1, 1123–1128 (2017).PubMed
Article
PubMed Central
Google Scholar
27.Davies, A. B., Tambling, C. J., Kerley, G. I. H. & Asner, G. P. Effects of vegetation structure on the location of lion kill sites in African thicket. PLoS ONE https://doi.org/10.1371/journal.pone.0149098 (2016).Article
PubMed
PubMed Central
Google Scholar
28.Bertram, B. C. R. Serengeti Predators and their Social Systems in Serengeti: Dynamics of an Ecosystem, 221–285. (Sinclair, A. R. E. and Norton-Griffiths, M., Eds). (University of Chicago Press, Chicago, 1979).29.Bailey, T. N. The African Leopard: Ecology and Behavior of a Solitary Felid (Columbia University Press, 1993).Book
Google Scholar
30.Hayward, M. W. & Kerley, G. I. H. Prey preferences and dietary overlap amongst Africa’s large predators. S. Afr. J. Wildl. Res. 38, 93–108 (2008).Article
Google Scholar
31.McCleery, R. A. et al. Animal diversity declines with broad-scale homogenization of canopy cover in African savannas. Biol. Conserv. 226, 54–62 (2018).Article
Google Scholar
32.Roques, K. G., O’Connor, T. G. & Watkinson, A. R. Dynamics of shrub encroachment in an African savanna: Relative influences of fire, herbivory, rainfall and density dependence. J. Appl. Ecol. 38, 268–280 (2001).Article
Google Scholar
33.Sirami, C. & Monadjem, A. Changes in bird communities in Swaziland savannas between 1998 and 2008 owing to shrub encroachment. Divers. Distrib. 18, 390–400 (2012).Article
Google Scholar
34.Estes, R. D. The Behavior Guide to African Mammals: Including Hoofed Mammals, Carnivores, Primates (University of California Press, 2012).
Google Scholar
35.Hayward, M. et al. Prey preferences of the leopard (Panthera pardus). J. Zool. 270, 298–313 (2006).Article
Google Scholar
36.Holekamp, K. E. & Dloniak, S. M. Intraspecific Variation in the Behavioral Ecology of a Tropical Carnivore, the Spotted Hyena in Advances in the Study of Behavior. Vol. 42 189–229 (Elsevier, 2010).37.Retief, F. The Ecology of Spotted Hyena, Crocuta crocuta, in Majete Wildlife Reserve, Malawi. Dissertation. (Stellenbosch University, 2016).38.Suraci, J. P. et al. A new automated behavioural response system to integrate playback experiments into camera trap studies. Methods Ecol. Evol. 8, 957–964 (2017).Article
Google Scholar
39.Smith, J. A. et al. Fear of the human ‘super predator’ reduces feeding time in large carnivores. Proc. R. Soc. Lond. Ser. B. https://doi.org/10.1098/rspb.2017.0433 (2017).Article
Google Scholar
40.Stankowich, T. & Blumstein, D. T. Fear in animals: A meta-analysis and review of risk assessment. Proc. R. Soc. Lond. B. 272, 2627–2634 (2005).
Google Scholar
41.Scogings, P. F. Large herbivores and season independently affect woody stem circumference increment in a semi-arid savanna. Plant Ecol. 215, 1433–1443 (2014).Article
Google Scholar
42.Skinner, J. D. & Chimimba, C. T. The Mammals of the Southern African Sub-region (Cambridge University Press, 2005).Book
Google Scholar
43.Canfield, R. H. Application of the line interception method in sampling range vegetation. J. For. 39, 388–394 (1941).
Google Scholar
44.Favreau, F. R., Pays, O., Goldizen, A. W. & Fritz, H. Short-term behavioural responses of impalas in simulated antipredator and social contexts. PLoS ONE https://doi.org/10.1371/journal.pone.0084970 (2013).Article
PubMed
PubMed Central
Google Scholar
45.Suraci, J. P., Clinchy, M. & Zanette, L. Y. Do large carnivores and mesocarnivores have redundant impacts on intertidal prey?. PLoS ONE https://doi.org/10.1371/journal.pone.0170255 (2017).Article
PubMed
PubMed Central
Google Scholar
46.Chandler, R. B., Engebretsen, K., Cherry, M. J., Garrison, E. P. & Miller, K. V. Estimating recruitment from capture–recapture data by modelling spatio-temporal variation in birth and age-specific survival rates. Methods Ecol. Evol. 9, 2115–2130 (2018).Article
Google Scholar
47.Ydenberg, R. C. & Dill, L. M. The economics of fleeing from predators. Stud. Behav. 16, 229–249 (1986).Article
Google Scholar
48.Lind, J. & Cresswell, W. Determining the fitness consequences of anti-predation behavior. Behav. Ecol. 16, 945–956 (2005).Article
Google Scholar
49.Berger, J. Carnivore repatriation and holarctic prey: Narrowing the deficit in ecological effectiveness. Conserv. Biol. 21, 1105–1116 (2007).PubMed
Article
PubMed Central
Google Scholar
50.Dalerum, F. & Belton, L. African ungulates recognize a locally extinct native predator. Behav. Ecol. 26, 215–222 (2015).Article
Google Scholar
51.Palmer, M. S. & Gross, A. Eavesdropping in an African large mammal community: Antipredator responses vary according to signaler reliability. Anim. Behav. 137, 1–9 (2018).Article
Google Scholar
52.Crawley, M. J. Statistical Computing: An Introduction to Data Analysis Using S-PLUS (Wiley, 2002).MATH
Google Scholar
53.Hodges, J. S. Richly Parameterized Linear Models: Additive, Time Series, and Spatial Models Using Random Effects (CRC Press, 2016).MATH
Book
Google Scholar
54.Agresti, A. An Introduction to Categorical Data Analysis 2nd edn. (Wiley, 2002).MATH
Book
Google Scholar
55.Hopcraft, J. G. C., Sinclair, A. R. E. & Packer, C. Planning for success: Serengeti lions seek prey accessibility rather than abundance. J. Anim. Ecol. 74, 559–566 (2005).Article
Google Scholar
56.Gorini, L. et al. Habitat heterogeneity and mammalian predator-prey interactions. Mammal Rev. 42, 55–77 (2011).Article
Google Scholar
57.Creel, S. et al. What explains variation in the strength of behavioral responses to predation risk? A standardized test with large carnivore and ungulate guilds in three ecosystems. Biol. Conserv. 232, 164–172 (2019).Article
Google Scholar
58.Palmer, M. S., Fieberg, J., Swanson, A., Kosmala, M. & Packer, C. A ‘dynamic’ landscape of fear: prey responses to spatiotemporal variations in predation risk across the lunar cycle. Ecol. Lett. 20, 1364–1373 (2017).CAS
PubMed
Article
PubMed Central
Google Scholar
59.Kohl, M. T. et al. Diel predator activity drives a dynamic landscape of fear. Ecol. Monogr. 88, 1–10. https://doi.org/10.1002/ecm.1313 (2018).Article
Google Scholar
60.Breitenmoser, U., Breitenmoser-Wursten, C., Carbyn, L. N. & Funk, S. M. Assessment of Carnivore Reintroduction in Carnivore Conservation (eds. J. L. Gittleman, S. M. Funk, D. W. Macdonald and R. K. Wayne) 241–280 (Cambridge University Press and Zoological Society of London, 2001).61.Hayward, M. W. et al. The reintroduction of large carnivores to the Eastern Cape, South Africa: an assement. Oryx 41, 205–214 (2007).Article
Google Scholar
62.Thaker, M. et al. Minimizing predation risk in a landscape of multiple predators: Effects on the spatial distribution of African ungulates. Ecology 92, 398–407 (2011).PubMed
Article
Google Scholar
63.Augustine, D. J. & Mcnaughton, S. J. Regulation of shrub dynamics by native browsing ungulates on East African rangeland. J. Appl. Ecol. 41, 45–58 (2004).Article
Google Scholar
64.Daskin, J. H., Stalmans, M. & Pringle, R. M. Ecological legacies of civil war: 35-year increase in savanna tree cover following wholesale large-mammal declines. J. Ecol. 104, 79–89 (2016).Article
Google Scholar
65.Loggins, A. A., Shrader, A. M., Monadjem, A. & McCleery, R. A. Shrub cover homogenizes small mammals’ activity and perceived predation risk. Sci. Rep. https://doi.org/10.1038/s41598-019-53071-y (2019).Article
PubMed
PubMed Central
Google Scholar
66.Keesing, F. & Young, T. P. Cascading consequences of the loss of large mammals in an African savanna. Bioscience 64, 487–495 (2014).Article
Google Scholar More