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Mortality, perception, and scale: Understanding how predation shapes space use in a wild prey population


Autoři: Lindsey N. Messinger aff001;  Erica F. Stuber aff001;  Christopher J. Chizinski aff002;  Joseph J. Fontaine aff001
Působiště autorů: Nebraska Cooperative Fish & Wildlife Research Unit, University of Nebraska–Lincoln, Lincoln, Nebraska, United States of America aff001;  School of Natural Resources, University of Nebraska–Lincoln, Lincoln, Nebraska, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222272

Souhrn

Attempts to assess behavioral responses of prey to predation risk are often confounded by depredation of prey. Moreover, the scale at which the response of prey is assessed has important implications for discovering how predation risk alters prey behavior. Herein, we assessed space use of wild Ring-necked Pheasants (Phasianus colchicus) in response to spatial and temporal variation in recreational hunting. We radio-marked pheasants and monitored space use at two spatial scales: short-term seasonal home range, and nightly resting locations. Additionally, we considered temporal variation in predation risk by monitoring space use prior to and during the pheasant hunting season. Although we found no change in nightly resting location, pheasants subjected to predation risk expanded their home range and shifted home range location even when invulnerable to predation. Home range formation was plastic, with home ranges expanding and contracting as risk fluctuated before and during the hunting season. Depredation reduced the measured response within the population, obscuring the potential importance of perceived predation risk in shaping prey communities, particularly when not measured at the appropriate scale. By assessing space use of a wild prey population at multiple scales, considering spatial and temporal variation in predation risk, we show that not only does predation risk affect space use, but that the effects at the population level may be challenging to assess when not measured at the appropriate ecological scale because of the direct effects of differential mortality on the same behaviors.

Klíčová slova:

Behavior – Birds – Death rates – Hunting behavior – Predation – Seasons – Predator-prey dynamics – Sunrise


Zdroje

1. Fretwell SD, Lucas HLJ. On territorial behavior and other factors influencing habitat distribution in birds. Acta Biotheor. 1969;19(1):16–36.

2. Rosenzweig ML. Habitat selection and population interactions: The search for mechanism. Am Nat [Internet]. 1991;137:S5–28. Available from: http://www.journals.uchicago.edu/doi/10.1086/285137

3. Holmes RT, Marra PP, Sherry TW. Habitat-specific demography of breeding black-throated blue warblers (Dendroica caerulescens): Implications for population dynamics. J Anim Ecol [Internet]. 1996;65(2):183. Available from: http://www.jstor.org/stable/5721?origin=crossref

4. Morris DW. Toward an ecological synthesis: A case for habitat selection. Vol. 136, Oecologia. 2003. p. 1–13. doi: 10.1007/s00442-003-1241-4 12690550

5. Morales JM, Moorcroft PR, Matthiopoulos J, Frair JL, Kie JG, Powell RA, et al. Building the bridge between animal movement and population dynamics. Philos Trans R Soc B Biol Sci [Internet]. 2010;365(1550):2289–301. Available from: http://rstb.royalsocietypublishing.org/cgi/doi/10.1098/rstb.2010.0082

6. MacArthur R, Levins R. Competition, habitat selection, and character displacement in a patchy envrionment. Proc Natl Acad Sci [Internet]. 1964;51(6):1207–10. Available from: http://www.pnas.org/cgi/doi/10.1073/pnas.51.6.1207

7. Whitham TG. Habitat selection by pemphigus aphids in response to response limitation and competition. Ecology [Internet]. 1978;59(6):1164–76. Available from: http://doi.wiley.com/10.2307/1938230

8. Jorde DG, Krapu GL, Crawford RD, Hay MA. Effects of weather on habitat selection and behavior of Mallards wintering in Nebraska. Condor [Internet]. 1984;86:258–65. Available from: http://www.jstor.org/stable/1366993%5Cnhttp://www.jstor.org/stable/1366993?seq=1&cid=pdf-reference#references_tab_contents

9. Gilliam JF, Fraser DF. Habitat selection under predation hazard: test of a model with foraging minnows. Ecology. 1987;68(6):1856–62. doi: 10.2307/1939877 29357169

10. Binckley CA, Resetarits WJ. Habitat selection determines abundance, richness and species composition of beetles in aquatic communities. Biol Lett [Internet]. 2005;1(3):370–4. Available from: http://rsbl.royalsocietypublishing.org/cgi/doi/10.1098/rsbl.2005.0310

11. Orians GH, Wittenberger JF. Spatial and temporal scales in habitat selection. Am Nat [Internet]. 1991;137:S29–49. Available from: http://www.journals.uchicago.edu/doi/10.1086/285138

12. Johnson CJ, Parker KL, Heard DC. Foraging across a variable landscape: Behavioral decisions made by woodland caribou at multiple spatial scales. Oecologia. 2001;127(4):590–602. doi: 10.1007/s004420000573 28547497

13. Turner AM, Montgomery SL. Spatial and temporal scales of predator avoidance: Experiments with fish and snails. Ecology. 2003;84(3):616–22.

14. Lima SL, Dill LM. Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool [Internet]. 1990;68(4):619–40. Available from: http://www.nrcresearchpress.com/doi/abs/10.1139/z90-092

15. Creel S, Winnie J, Maxwell B, Hamlin K, Creel M. Elk alter habitat selection as an antipredator response to wolves. Ecology. 2005;86(12):3387–97.

16. Fontaine JJ, Martin TE. Habitat selection responses of parents to offspring predation risk: An experimental test. Am Nat [Internet]. 2006;168(6):811–8. Available from: doi: 10.1086/508297 17109323

17. Valeix M, Loveridge AJ, Chamaillé-Jammes S, Davidson Z, Murindagomo F, Fritz H, et al. Behavioral adjustments of African herbivores to predation risk by lions: Spatiotemporal variations influence habitat use. Ecology. 2009;90(1):23–30. doi: 10.1890/08-0606.1 19294909

18. Lima SL. Stress and decision making under the risk of predation: Recent developments from Bbhavioral, reproductive, and ecological perspectives. Adv Study Behav. 1998;27(C):215–90.

19. Hebblewhite M, Pletscher DH, Paquet PC. Elk population dynamics in areas with and without predation by recolonizing wolves in Banff National Park, Alberta. Can J Zool [Internet]. 2002;80(5):789–99. Available from: http://www.nrcresearchpress.com/doi/abs/10.1139/z02-058

20. Frid A, Baker GG, Dill LM. Do shark declines create fear-released systems? Oikos. 2008;117(2):191–201.

21. Lima SL, Bednekoff PA. Temporal variation in danger drives antipredator behavior: The predation risk allocation hypothesis. Am Nat [Internet]. 1999;153(6):649–59. Available from: doi: 10.1086/303202 29585647

22. Sih A, McCarthy TM. Prey responses to pulses of risk and safety: Testing the risk allocation hypothesis. Anim Behav. 2002;63(3):437–43.

23. Creel S, Winnie JA. Responses of elk herd size to fine-scale spatial and temporal variation in the risk of predation by wolves. Anim Behav. 2005;69(5):1181–9.

24. Creel S, Winnie JA, Christianson D, Liley S. Time and space in general models of antipredator response: tests with wolves and elk. Anim Behav. 2008;76(4):1139–46.

25. Tolon V, Dray S, Loison A, Zeileis A, Fischer C, Baubet E. Responding to spatial and temporal variations in predation risk: space use of a game species in a changing landscape of fear. Can J Zool [Internet]. 2009;87(12):1129–37. Available from: http://www.nrcresearchpress.com/doi/abs/10.1139/Z09-101

26. Sih A. Predators and prey lifestyles: An evolutionary and ecological overview. In: Kerfoot WC, Sih A, editors. Predation: direct and indirect impacts on aquatic communities. University Press of New England; 1987. p. 203–24.

27. Frid A, Dill L. Human-caused disturbance as a form of predation risk. J Wildl Manage [Internet]. 2002;6(1):11. Available from: http://www.consecol.org/vol6/iss1/art11

28. Cresswell W. Non-lethal effects of predation in birds. Ibis (Lond 1859). 2008;150(1):3–17.

29. Laundre JW, Hernandez L, Ripple WJ. The landscape of fear: Ecological implications of being afraid. Open Ecol J [Internet]. 2010;3(3):1–7. Available from: http://benthamopen.com/ABSTRACT/TOECOLJ-3-3-1

30. Schmitz OJ. Direct and indirect effects of predation and predation risk in old‐field interaction webs. Am Nat [Internet]. 1998;151(4):327–42. Available from: doi: 10.1086/286122 18811324

31. Zanette LY, White AF, Allen MC, Clinchy M. Perceived predation risk reduces the number of offspring songbirds produce per year. Science (80-). 2011;334(6061):1398–401.

32. Abbey-Lee RN, Mathot KJ, Dingemanse NJ. Behavioral and morphological responses to perceived predation risk: A field experiment in passerines. Behav Ecol. 2016;27(3):857–64.

33. Brown J. Patch use as an indicator of habitat preference, predation risk, and competition. Behav Ecol Sociobiol. 1988;22(1):37–47.

34. Brown JS, Kotler BP. Hazardous duty pay and the foraging cost of predation. Ecol Lett. 2004;7(10):999–1014.

35. Thomson RL, Forsman JT, Sardà-Palomera F, Mönkkönen M. Fear factor: Prey habitat selection and its consequences in a predation risk landscape. 2016;29(4):507–14.

36. Kotler BP, Holt RD. Predation and competition: The interaction of two types of species interactions. Oikos. 1989;54(2):256–60.

37. Kauffman MJ, Brodie JF, Jules ES. Are wolves saving Yellowstone’s aspen? A landscape-level test of a behaviorally mediated trophic cascade. Ecology. 2010;91(9):2742–55. doi: 10.1890/09-1949.1 20957967

38. Nelson EH, Matthews CE, Rosenheim JA. Predators reduce prey population growth by inducing changes in prey behavior. Ecology. 2004;85(7):1853–8.

39. Stuber EF, Grobis MM, Abbey-Lee R, Kempenaers B, Mueller JC, Dingemanse NJ. Perceived predation risk affects sleep behaviour in free-living great tits, Parus major. Anim Behav. 2014;98:157–65.

40. Kelley JL, Evans JP, Ramnarine IW, Magurran AE. Back to school: Can antipredator behaviour in guppies be enhanced through social learning? Anim Behav. 2003;65(4):655–62.

41. Smith ME, Belk MC. Risk assessment in western mosquitofish (Gambusia affinis): Do multiple cues have additive effects? Behav Ecol Sociobiol. 2001;51(1):101–7.

42. Bleicher SS, Ylönen H, Käpylä T, Haapakoski M. Olfactory cues and the value of information: voles interpret cues based on recent predator encounters. Behav Ecol Sociobiol. 2018;72(12). doi: 10.1007/s00265-018-2600-9 30573941

43. Proffitt KM, Grigg JL, Hamlin KL, Garrott RA. Contrasting effects of wolves and human hunters on elk behavioral responses to predation risk. J Wildl Manage [Internet]. 2009;73(3):345–56. Available from: http://www.bioone.org/doi/abs/10.2193/2008-210

44. Nebraska G and PC (NGPC). Hunting Guide [Internet]. 2016. Available from: http://digital.outdoornebraska.gov/i/707958-hunting-guide-2016

45. Stokes AW. An eight-year study of a northern Utah pheasant population. J Wildl Manage. 1968;32(4):867–74.

46. Leif A. Survival, spatial ecology and habitat use of male Ring-necked Pheasants in South Dakota: Completion report. South Dakota Department of Game, Fish and Parks, Wildlife Division; 2003.

47. Morris DW. Scales and costs of habitat selection in heterogeneous landscapes. Evol Ecol. 1992;7653(1):412–32.

48. Lima SL, Zollner PA. Towards a behavioral ecology of ecological landscapes. Trends Ecol Evol. 1996;11(3):131–5. doi: 10.1016/0169-5347(96)81094-9 21237783

49. Hebblewhite M, Merrill EH. Trade-offs between predation risk and forage differ between migrant strategies in a migratory ungulate. Ecology. 2009;90(12):3445–54. doi: 10.1890/08-2090.1 20120812

50. Giudice JH, Ratti JT. Ring-necked Pheasant (Phasianus colchicus), version 2.0. In: Poole AF, Gill F., editors. The Birds of North America [Internet]. Ithaca, NY, USA: Cornell Lab of Ornithology; 2001. Available from: https://doi.org/10.2173/bna.572

51. Simonsen VL, Fontaine JJ. Landscape context influences nest survival in a Midwest grassland. J Wildl Manage. 2016;80(5):877–83.

52. Bates D, Maechler M, Bolker BM, Walker S. lme4: Linear mixed-effects models using Eigen and S4 [Internet]. Vol. xx, Journal of Statistical Software. 2015. p. xx. Available from: http://cran.r-project.org/package=lme4%5Cnhttp://arxiv.org/abs/1406.5823

53. Gelman A, Su Y, Yajima M, Hill J, Pittau M, Kerman J, et al. Arm: data analysis using regression and multilevel/hierarchical models. 2015.

54. Gelman A, Hill J. Data analysis using regression and multilevel/hierarchical models. Cambridge. 2007. 651 p.

55. Labisky R. Nightlighting: its use in capturing pheasants, prairie chickens, bobwhites, and cottontails. Biol notes. 1968;062.

56. Kenward R. A manual for wildlife radio tagging. Academic Press; 2000.

57. Gilsdorf JM, Vercauteren KC, Hygnstrom SE, Walter WD, Boner JR, Clements GM. An integrated vehicle-mounted telemetry system for VHF telemetry applications. J Wildl Manage [Internet]. 2008;72(5):1241–6. Available from: http://www.bioone.org/doi/abs/10.2193/2007-348

58. Lenth R V. On finding the source of a signal. Technometrics. 1981;23(2):149–54.

59. DeNardo DF, Sinervo B. Effects of steroid hormone interaction on activity and home-range size of male lizards. Horm Behav. 1994;28(3):273–87. doi: 10.1006/hbeh.1994.1023 7814007

60. Anderson DP, Forester JD, Turner MG, Frair JL, Merrill EH, Fortin D, et al. Factors influencing female home range sizes in elk (Cervus elaphus) in North American landscapes. Landsc Ecol. 2005;20:257–71.

61. Winkle W Van. Comparison of several probabilistic home-range models. J Wildl Manage [Internet]. 1975;39(1):118. Available from: http://www.jstor.org/stable/3800474?origin=crossref

62. Worton BJ. Kernel methods for estimating the utlization distribution in home-range studies. Vol. 70, Ecology. 1989. p. 164–8.

63. Calenge C. The package “adehabitat” for the R software: A tool for the analysis of space and habitat use by animals. Ecol Modell. 2006;197(3–4):516–9.

64. Kernohan BJ, Gitzen RA, Millspaugh JJ. Analysis of animal space use and movements. In: Radio Tracking and Animal Populations [Internet]. 2001. p. 125–66. Available from: http://linkinghub.elsevier.com/retrieve/pii/B9780124977815500062

65. Wszola LS, Simonsen VL, Corral L, Chizinski CJ, Fontaine JJ. Simulating detection-censored movement records for home range analysis planning. Ecol Modell [Internet]. 2019;392(December 2018):268–78. Available from: https://doi.org/10.1016/j.ecolmodel.2018.10.017

66. Swihart RK, Slade NA. Influence of sampling interval on estimates of home-range size. J Wildl Manage. 1985;49(4):1019–25.

67. Blundell GM, Maier JA, Debevec EM. Linear home ranges: Effects of smoothing, sample size, and autocorrelation on kernel estimates. Ecol Monogr. 2001;71(3):469–89.

68. De Solla SR, Bonduriansky R, Brooks RJ. Eliminating autocorrelation reduces biological relevance of home range estimates. J Anim Ecol. 1999;68(2):221–34.

69. Fieberg J, Börger L. Could you please phrase “home range” as a question? J Mammal [Internet]. 2012;93(4):890–902. Available from: https://academic.oup.com/jmammal/article-lookup/doi/10.1644/11-MAMM-S-172.1

70. Börger L, Franconi N, De Michele G, Gantz A, Meschi F, Manica A, et al. Effects of sampling regime on the mean and variance of home range size estimates. J Anim Ecol. 2006;75(6):1393–405. doi: 10.1111/j.1365-2656.2006.01164.x 17032372

71. Seaman DE, Millspaugh JJ, Kernohan BJ, Brundige GC, Raedeke KJ, Gitzen RA. Effects of sample size on kernel home range estimates. J Wildl Manage [Internet]. 1999;63(2):739. Available from: http://www.jstor.org/stable/3802664?origin=crossref

72. Walsberg GE, King JR. The thermoregulatory significance of the winter roost-sites selected by robins in eastern Washington. Wilson Bull. 1980;92(l):33–9.

73. Warner RE, David LM. Woody habitat and severe winter mortality Ring-necked Pheasants in central Illinois. J Wildl Manage. 1982;46(4):923–32.

74. Klimstra WC, Ziccardi VC. Night-roosting habitat of bobwhites. J Wildl Manage. 1963;27(2):202–14.

75. Oksanen J, Blanchet F, Kindt R, Legendre P, Minchin P, O’hara R, et al. Package ‘vegan’. Community ecology package. 2013.

76. Anholt BR, Werner EE. Interaction between food availability and predation mortality mediated by adaptive behavior. Ecology. 1995;76(7):2230–4.

77. Dill LM, Rochette R. Mortality, behavior and the effects of predators on the intertidal distribution of littorinid gastropods. J Exp Mar Bio Ecol. 2000;253:165–91. 11033363

78. Lapiedra O, Schoener TW, Leal M, Losos JB, Kolbe JJ. Predator-driven natural selection on risk-taking behavior in anole lizards. Science (80-). 2018;360(6392):1017–20.

79. Mahr K, Riegler G, Hoi H. Parental risk management in relation to offspring defence: Bad news for kids. Proc R Soc B Biol Sci. 2014;282(1798):27–30.

80. Dorset EE, Sakaluk SK, Thompson CF. Behavioral plasticity in response to perceived predation risk in breeding house wrens. Evol Biol. 2017;44(2):227–39. doi: 10.1007/s11692-016-9402-7 28736461

81. Tufto J, Andersen R, Linnell J. Habitat use and ecological correlates of home range size in a small cervid: The Roe Deer. J Anim Ecol [Internet]. 1996;65(6):715–24. Available from: http://www.jstor.org/stable/5670

82. Lafontaine A, Drapeau P, Fortin D, St-Laurent MH. Many places called home: the adaptive value of seasonal adjustments in range fidelity. J Anim Ecol. 2017;86(3):624–33. doi: 10.1111/1365-2656.12645 28146328

83. Relyea RA, Lawrence RK, Demarais S. Home Range of desert mule deer: Testing the body-size and habitat-productivity hypotheses. J Wildl Manage. 2000;64(1):146–53.

84. Ofstad E., Herfindal I, Solberg EJ, Heim M, Rolandsen CM, Saether B-E. Use, selection, and home range properties: complex patterns of individual habitat utilization. Ecosphere. 2019;10(4):e02695.

85. Wszola LS, Stuber EF, Chizinski CJ, Lusk JJ, Fontaine JJ. Prey availability and accessibility drive hunter movement. Wildlife Biol. 2019;wlb.00526.

86. Dröge E, Creel S, Becker MS, M’soka J. Spatial and temporal avoidance of risk within a large carnivore guild. 2017;7:189–99. doi: 10.1002/ece3.2616 28070283

87. Leedy D, Hicks L. The pheasants in Ohio. In: McAtee W, editor. The Ring-necked pheasant and its management in North America. Washington DC: The American Wildlife Institute; 1945. p. 57–130.

88. Burres E, Fischer D, Wegner D. Analysis of a publicly operated pheasant hunt in southern California. Cross Bord Waters. 1999;244.

89. Altendorf KB, Laundré JW, López González CA, Brown JS. Assessing effects of predation on foraging behavior of mule deer. J Mammal. 2001;82(2):430–9.

90. Sönnichsen L, Bokje M, Marchal J, Hofer H, Jedrzejewska B, Kramer-Schadt S, et al. Behavioural responses of European Roe Deer to temporal variation in predation risk. Ethology. 2013;119(3):233–43.

91. Johnson DH. The comparison of usage and availability measurements for evaluating resource preference. Ecology. 1980;61:65–71.

92. Hutto R. Habitat selection by nonbreeding migrants. In: Cody M, editor. Habitat selection in birds. New York: Academic Press; 1985. p. 455–76.

93. Mayor SJ, Schneider DC, Schaefer JA, Mahoney SP. Habitat selection at multiple scales. Ecoscience. 2009;16(2):238–47.

94. Rettie WJ, Messier F. Hierarchical habitat selection by woodland caribou: its relationship to limiting factors. Ecography (Cop). 2008;23(4):466–78.

95. Lack D. Habitat selection in birds. With special reference to the effects of afforestation on the Breckland avifauna. J Anim Ecol. 1933;2(2):239–62.

96. Heithaus MR, Dill, Lawrence M. Does tiger shark predation risk influence foraging habitat use by bottlenose dolphins at multiple spatial scales? Oikos. 2006;114(2):257–64.

97. Hebblewhite M, Merrill EH. Multiscale wolf predation risk for elk: Does migration reduce risk? Oecologia. 2007;152(2):377–87. doi: 10.1007/s00442-007-0661-y 17287955

98. Eklöv P, Svanbäck R. Predation risk influences adaptive morphological variation in fish populations. Am Nat. 2006;167(3):440–52. doi: 10.1086/499544 16673351

99. Winnie JA. Predation risk, elk, and aspen: Tests of a behaviorally mediated trophic cascade in the Greater Yellowstone Ecosystem. Ecology. 2012;93(12):2600–14. doi: 10.1890/11-1990.1 23431591

100. Beschta R, Ripple W. Are wolves saving Yellowstone’s aspen? A landscape-level test of a behaviorally mediated trophic cascade: comment. Ecology. 2013;94(6):1420–5. doi: 10.1890/11-0063.1 23923505

101. Beschta R, Eisenberg C, Laundre J, Ripple W, Rooney T. Predation risk, elk, and aspen: comment. Ecology. 2014;95(9):2669–71.

102. Ford AT, Goheen JR. Trophic cascades by large carnivores: A case for strong inference and mechanism. Vol. 30, Trends in Ecology and Evolution. 2015. p. 725–35. doi: 10.1016/j.tree.2015.09.012 26498385

103. Jorgensen CF, Powell LA, Lusk JJ, Bishop AA, Fontaine JJ. Assessing landscape constraints on species abundance: Does the neighborhood limit species response to local habitat conservation programs? PLoS One. 2014;9(6).

104. Kittle AM, Fryxell JM, Desy GE, Hamr J. The scale-dependent impact of wolf predation risk on resource selection by three sympatric ungulates. Oecologia. 2008;157(1):163–75. doi: 10.1007/s00442-008-1051-9 18481095

105. Lone K, Loe LE, Gobakken T, Linnell JDC, Odden J, Remmen J, et al. Living and dying in a multi-predator landscape of fear: Roe deer are squeezed by contrasting pattern of predation risk imposed by lynx and humans. Oikos. 2014;123(6):641–51.


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