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An apex carnivore’s life history mediates a predator cascade

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Abstract

Apex predators can shape communities via cascading top–down effects, but the degree to which such effects depend on predator life history traits is largely unknown. Within carnivore guilds, complex hierarchies of dominance facilitate coexistence, whereby subordinate species avoid dominant counterparts by partitioning space, time, or both. We investigated whether a major life history trait (hibernation) in an apex carnivore (black bears Ursus americanus) mediated its top–down effects on the spatio-temporal dynamics of three sympatric mesocarnivore species (coyotes Canis latrans, bobcats Lynx rufus, and gray foxes Urocyon cinereoargenteus) across a 15,000 km2 landscape in the western USA. We compared top–down, bottom–up, and environmental effects on these mesocarnivores using an integrated modeling approach. Black bears exerted top–down effects that varied as a function of hibernation and were stronger than bottom–up or environmental impacts. High black bear activity in summer and fall appeared to buffer the most subordinate mesocarnivore (gray foxes) from competition with dominant mesocarnivores (coyotes and bobcats), which were in turn released by black bear hibernation in winter and early spring. The mesocarnivore responses occurred in space (i.e., altered occupancy and site visitation intensity) rather than time (i.e., diel activity patterns unaffected). These results suggest that the spatio-temporal dynamics of mesocarnivores in this system were principally shaped by a spatial predator cascade of interference competition mediated by black bear hibernation. Thus, certain life history traits of apex predators might facilitate coexistence among competing species over broad time scales, with complex implications for lower trophic levels.

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References

  • Atwood TC, Fry TL, Leland BR (2011) Partitioning of anthropogenic watering sites by desert carnivores. J Wildl Manag 75:1609–1615

    Google Scholar 

  • Beckmann JP (2002) Changing dynamics of a population of black bears (Ursus americanus): causes and consequences. University of Nevada, Reno

    Google Scholar 

  • Beckmann JP, Berger J (2003) Rapid ecological and behavioural changes in carnivores: the responses of black bears (Ursus americanus) to altered food. J Zool 261:207–212

    Google Scholar 

  • Beckmann JP, Lackey CW (2018) Lessons learned from a 20-year collaborative study on American black bears. Human-Wildlife Interact 12:396–404

    Google Scholar 

  • Birch LC (1957) The meanings of competition. Am Nat 91:5–18

    Google Scholar 

  • Bjørnstad ON (2008) The ncf package: spatial nonparametric covariance functions

  • Blanchet FG, Cazelles K, Gravel D (2020) Co-occurrence is not evidence of ecological interactions. Ecol Lett 23:1050–1063

    PubMed  Google Scholar 

  • Caro T (2005) Antipredator defenses in birds and mammals. University of Chicago Press

    Google Scholar 

  • Carothers JH, Jaksić FM (1984) Time as niche difference: the role of interference competition. Oikos 42:403–406

    Google Scholar 

  • Elbroch LM, Kusler A (2018) Are pumas subordinate carnivores, and does it matter? PeerJ 6:e4293

    PubMed  PubMed Central  Google Scholar 

  • Elmhagen B, Rushton SP (2007) Trophic control of mesopredators in terrestrial ecosystems: top-down or bottom-up? Ecol Lett 10:197–206

    PubMed  Google Scholar 

  • Elmhagen B, Ludwig G, Rushton SP et al (2010) Top predators, mesopredators and their prey: Interference ecosystems along bioclimatic productivity gradients. J Anim Ecol 79:785–794

    CAS  PubMed  Google Scholar 

  • Enders MS, Vander Wall SB (2012) Black bears Ursus americanus are effective seed dispersers, with a little help from their friends. Oikos 121:589–596

    Google Scholar 

  • Estes JA (1995) Top-level carnivores and ecosystem effects: question and approaches. In: Jones C, Lawton JH (eds) Linking species and ecosystems. Chapman & Hall, New York, pp 151–158

    Google Scholar 

  • Fedriani JM, Fuller TK, Sauvajot RM, York EC (2000) Competition and intraguild predation among three sympatric carnivores. Oecologia 125:258–270

    PubMed  Google Scholar 

  • Ferretti F, Worm B, Britten GL et al (2010) Patterns and ecosystem consequences of shark declines in the ocean. Ecol Lett 13:1055–1071

    PubMed  Google Scholar 

  • Frey S, Fisher JT, Burton AC, Volpe JP (2017) Investigating animal activity patterns and temporal niche partitioning using camera-trap data: challenges and opportunities. Remote Sens Ecol Conserv 5:272–285

    Google Scholar 

  • Gelman A, Hill J (2007) Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, New York

    Google Scholar 

  • Gelman A, Carlin JB, Stern HS, Rubin DB (2004) Bayesian data analysis. Chapman & Hall/CRC, London

    Google Scholar 

  • Gompper ME, Lesmeister DB, Ray JC et al (2016) Differential habitat use or intraguild interactions: what structures a carnivore community? PLoS ONE 11:e0146055

    PubMed  PubMed Central  Google Scholar 

  • Greene W (2008) Functional forms for the negative binomial model for count data. Econ Lett 99:585–590

    Google Scholar 

  • Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 94:421–425

    Google Scholar 

  • Halpin MA, Bissonette JA (1988) Influence of snow depth on prey availability and habitat use by red fox. Can J Zool 66:587–592

    Google Scholar 

  • Hartigan JA, Wong MA (1979) A k-means clustering algorithm. J R Stat Soc C 28:100–108

    Google Scholar 

  • Hayward MW, Slotow R (2009) Temporal partitioning of activity in large African carnivores: tests of multiple hypotheses. South Afr J Wildl Res 39:109–125

    Google Scholar 

  • Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23:202–210

    PubMed  Google Scholar 

  • Henke SE, Bryant FC (1999) Effects of coyote removal on the faunal community in western Texas. J Wildl Manag 63:1066–1081

    Google Scholar 

  • Hody JW, Kays R (2018) Mapping the expansion of coyotes (Canis latrans) across North and central America. Zookeys 2018:81–97

    Google Scholar 

  • Holt RD, Polis GA (1997) A theoretical framework for intraguild predation. Am Nat 149:745–764

    Google Scholar 

  • Jachowski DS, Butler A, Eng RYY et al (2020) Identifying mesopredator release in multi-predator systems: a review of evidence from North America. Mamm Rev 50:367–381

    Google Scholar 

  • Johnson HE, Breck SW, Baruch-Mordo S et al (2015) Shifting perceptions of risk and reward: dynamic selection for human development by black bears in the western United States. Biol Conserv 187:164–172

    Google Scholar 

  • Kernohan BJ, Gitzen RA, Millspaugh JJ (2001) Analysis of animal space use and movements. In: Millspaugh JJ, Marzluff JM (eds) Radio tracking and animal populations. Academic Press, San Diego, pp 125–166

    Google Scholar 

  • Kéry M, Royle JA (2015) Applied hierarchical modeling in ecology: analysis of distribution, abundance and species richness in R and BUGS, vol 1. Prelude and static models. Elsevier, San Diego

    Google Scholar 

  • Kuo L, Mallick B (1998) Variable selection for regression models. Sankhya Ser B 60:65–81

    Google Scholar 

  • Lackey CW (2004) Nevada’s black bear: ecology and conservation of a charismatic carnivore. Biol Bull Number 15

  • Lackey CW, Beckmann JP, Sedinger J (2013) Bear historical ranges revisited: documenting the increase of a once-extirpated population in Nevada. J Wildl Manag 77:812–820

    Google Scholar 

  • Lepard CC, Moll RJ, Cepek JD et al (2019) The influence of the delay-period setting on camera-trap data storage, wildlife detections and occupancy models. Wildl Res 46:37–53

    Google Scholar 

  • Levi T, Wilmers C (2012) Wolves–coyotes–foxes: a cascade among carnivores. Ecology 93:921–929. https://doi.org/10.1890/11-0165.1

    Article  PubMed  Google Scholar 

  • Levi T, Kilpatrick AM, Mangel M, Wilmers CC (2012) Deer, predators, and the emergence of Lyme disease. Proc Natl Acad Sci 109:10942–10947

    CAS  PubMed  Google Scholar 

  • Linnell JDC, Strand O (2000) Interference interactions, co-existence and conservation of mammalian carnivores. Divers Distrib 6:169–176

    Google Scholar 

  • Litvaitis JA (1992) Niche relations between coyotes and sympatric carnivora. In: Boer AH (ed) Ecology and management of the eastern Coyote. Wildlife Research Unit, University of New Brunswick, Fredericton

    Google Scholar 

  • Long RA, Donovan TM, MacKay P et al (2011) Predicting carnivore occurrence with noninvasive surveys and occupancy modeling. Landsc Ecol 26:327–340

    Google Scholar 

  • Macarthur R, Levins R (1967) THe limiting similarity, convergence, and divergence of coexisting species. Am Nat 101:377–385

    Google Scholar 

  • MacKenzie DI, Nichols JD, Lachman GB et al (2002) Estimating site occupancy rates when detection probabilities are less than one. Ecology 83:2248–2255

    Google Scholar 

  • Malaney JL, Lackey CW, Beckmann JP, Matocq MD (2018) Natural rewilding of the Great Basin: genetic consequences of recolonization by black bears (Ursus americanus). Divers Distrib 24:168–178

    Google Scholar 

  • Martin TE (1995) Avian life history evolution in relation to nest sites, nest predation, and food. Ecol Monogr 65:101–127

    Google Scholar 

  • Moll RJ, Cepek JD, Lorch PD et al (2018) Humans and urban development mediate the sympatry of competing carnivores. Urban Ecosyst 21:765–778

    Google Scholar 

  • Neale JCC, Sacks BN (2001) Resource utilization and interspecific relations of sympatric bobcats and coyotes. Oikos 94:236–249

    Google Scholar 

  • NOHRSC (2004) Snow data assimilation system (SNODAS) data products at NSIDC, Version 1

  • Nouvellet P, Rasmussen GSA, MacDonald DW, Courchamp F (2012) Noisy clocks and silent sunrises: measurement methods of daily activity pattern. J Zool 286:179–184

    Google Scholar 

  • Plummer M (2003) JAGS: a program for analysis of Bayesian graphical models using Gibbs sampling. In: Proceedings of the 3rd international workshop on distributed statistical computing, pp 124:1–8

  • Polis GA, Holt RD, Menge BA, Winemiller KO (1996) Time, space, and life history: Influences on food webs. In: Polis GA, Winemiller KO (eds) Food webs: integration of patterns and dynamics. Springer, Boston, pp 435–460

    Google Scholar 

  • Promislow DEL, Harvey PH (1990) Living fast and dying young: a comparative analysis of life-history variation among mammals. J Zool 220:417–437

    Google Scholar 

  • Prugh LR, Sivy KJ (2020) Enemies with benefits: integrating positive and negative interactions among terrestrial carnivores. Ecol Lett 23:902–918

    PubMed  Google Scholar 

  • Prugh LR, Stoner CJ, Epps CW et al (2009) The rise of the mesopredator. Bioscience 59:779–791

    Google Scholar 

  • Reznick D, Endler JA (1982) The impact of predation on life history evolution in Trinidadian Guppies (Poeciliareticulata). Evolution (N Y) 36:160–177

    Google Scholar 

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

    Google Scholar 

  • Ripple WJ, Estes JA, Beschta RL et al (2014) Status and ecological effects of the world’s largest carnivores. Science 343:1241484

    PubMed  Google Scholar 

  • Ritchie EG, Johnson CN (2009) Predator interactions, mesopredator release and biodiversity conservation. Ecol Lett 12:982–998

    PubMed  Google Scholar 

  • Ritchie EG, Elmhagen B, Glen AS et al (2012) Ecosystem restoration with teeth: what role for predators? Trends Ecol Evol 27:265–271

    PubMed  Google Scholar 

  • Rowcliffe JM (2019) Package “activity”

  • Royle JA, Dorazio RM (2008) Hierarchical modeling and inference in ecology: the analysis of data from populations, metapopulations and communities. Elsevier Academic Press, Oxford

    Google Scholar 

  • RStudio Team (2015) RStudio: integrated development for R

  • Schoener TW (1983) Field experiments on interspecific competition. Am Nat 122:240–285

    Google Scholar 

  • Seaman DE, Millspaugh JJ, Kernohan BJ et al (1999) Effects of sample size on kernal home range estimates. J Wildl Manag 63:739–747

    Google Scholar 

  • Sikes RS (2016) 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J Mammal 97:663–688

    PubMed  PubMed Central  Google Scholar 

  • Sivy KJ, Pozzanghera CB, Grace JB, Prugh LR (2017) Fatal attraction? Intraguild facilitation and suppression among predators. Am Nat 190:663–679

    PubMed  Google Scholar 

  • Soulé ME, Bolger DT, Alberts AC et al (1988) Reconstructed dynamics of rapid extinctions of chaparral-requiring birds in urban habitat islands. Conserv Biol 2:75–92

    Google Scholar 

  • Stoessel M, Elmhagen B, Vinka M et al (2019) The fluctuating world of a tundra predator guild: bottom-up constraints overrule top-down species interactions in winter. Ecography (Cop) 42:488–499

    Google Scholar 

  • Su YS, Yajima M (2012) R2jags: a package for running jags from R

  • Tobler MW, Powell GVN (2013) Estimating jaguar densities with camera traps: problems with current designs and recommendations for future studies. Biol Conserv 159:109–118

    Google Scholar 

  • Vanak AT, Fortin D, Thaker M et al (2013) Moving to stay in place: behavioral mechanisms for coexistence of African large carnivores. Ecology 94:2619–2631

    PubMed  Google Scholar 

  • Vander Wal E, Rodgers AR (2012) An individual-based quantitative approach for delineating core areas of animal space use. Ecol Model 224:48–53

    Google Scholar 

  • Worton BJ (1989) Kernel methods for estimating the utilization distribution in home-range studies. Ecology 70:164–168

    Google Scholar 

  • Young DD, McCabe TR (1997) Grizzly bear predation rates on caribou calves in Northeastern Alaska. J Wildl Manag 61:1056–1066

    Google Scholar 

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Acknowledgements

This research was supported by the Nevada Department of Wildlife $3 Predator Fee Program and the statewide game management support (F17AF00482). Field work support was provided by W. Ortiz-Calo, A. Kimmel, D. Heit, and M. Verch. Thanks also to H. Reich of NDOW for logistic support and undergraduate researchers at MSU for assistance in image analysis. We thank two anonymous reviewers and A. Angerbjörn for comments that improved the manuscript.

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Authors and Affiliations

  1. Department of Natural Resources and the Environment, University of New Hampshire, 56 College Road, Durham, NH, 03824, USA

    Remington J. Moll

  2. Department of Fisheries and Wildlife, Michigan State University, 480 Wilson Road, Room 13 Natural Resources Building, East Lansing, MI, 48824, USA

    Remington J. Moll & Robert A. Montgomery

  3. Nevada Department of Wildlife, 6980 Sierra Center Parkway, Suite 120, Reno, NV, 89511, USA

    Patrick J. Jackson & Carl W. Lackey

  4. Montana Fish, Wildlife, and Parks, Wildlife Division, PO Box 200701, Helena, MT, 59620-0701, USA

    Brian F. Wakeling

  5. Wildlife Conservation Society, Rockies Program, 1050 E Main, Suite 2, Bozeman, MT, 59715, USA

    Jon P. Beckmann

  6. Wildlife Biology Program, W.A. Franke College of Forestry and Conservation, University of Montana, Missoula, MT, 59812, USA

    Joshua J. Millspaugh

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  1. Remington J. Moll
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Contributions

RAM and RJM conceived the ideas and designed methodology. RJM analyzed the data and led the writing of the manuscript. All authors contributed to drafts and gave approval for publication.

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Correspondence to Remington J. Moll.

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Communicated by Anders Angerbjörn.

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Moll, R.J., Jackson, P.J., Wakeling, B.F. et al. An apex carnivore’s life history mediates a predator cascade. Oecologia 196, 223–234 (2021). https://doi.org/10.1007/s00442-021-04927-6

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