Oecologia

, Volume 185, Issue 4, pp 537–549 | Cite as

The balancing act of foraging: mammalian herbivores trade-off multiple risks when selecting food patches

  • M. J. Camp
  • L. A. Shipley
  • T. R. Johnson
  • P. J. Olsoy
  • J. S. Forbey
  • J. L. Rachlow
  • D. H. Thornton
Highlighted Student Research

Abstract

Animals face multiple risks while foraging such as the risk of acquiring inadequate energy from food and the risk of predation. We evaluated how two sympatric rabbits (pygmy rabbits, Brachylagus idahoensis, and mountain cottontail rabbits, Sylvilagus nuttallii) that differ in size, use of burrows, and habitat specialization in the sagebrush-steppe of western North America respond to different types and levels of perceived risks (i.e., fitness cost × probability of occurrence), including fiber and toxins in food, exposure to predation, and distance from a refuge. We measured food intake by the rabbits at paired food patches that varied in these risks and used the method of paired comparisons to create a relative ranking of habitat cues, which revealed an animal’s perceived risk on a single scale representing an integrated response to a variety of risks. Pygmy rabbits perceived exposure to predation risk and distance from a burrow as riskier than did cottontails, whereas cottontails perceived dietary toxin as riskier. Pygmy rabbits consumed lower quality food, containing higher fiber or toxins, thereby avoided feeding in exposed patches or traveling far from their burrow to forage. In contrast, cottontails fed in exposed patches and traveled farther from the burrow to obtain higher quality food. We have shown how risks can be integrated into a single model that allows animals to reveal their perceptions of risks on a single scale that can be used to create a spatially explicit landscape of risk.

Keywords

Landscape of fear Marginal rate of substitution Method of paired comparisons Monoterpene Optimal foraging Plant secondary metabolite 

Notes

Acknowledgements

We would like to thank the undergraduate volunteers and researchers at Washington State University who cared for animals and collected data. J. Fluegel provided valuable assistance in creating experimental patches and arenas, and R. Camp (EcoLogical Research) assisted in creating figures. This research was funded by the National Science Foundation (NSF; DEB-1146368, L.A. Shipley; DEB-1146166, J.L. Rachlow; DEB-1146194, J.S. Forbey), and USDA National Institute of Food and Agriculture (NIFA; Hatch Project 1005876, L.A. Shipley).

Author contribution statement

MJC and LAS conceived and designed the experiments, MJC performed the experiments. MJC, LAS, TRJ, PJO analyzed the data. MJC and LAS wrote the manuscript; other authors provided editorial advice.

References

  1. Apfelbach R, Blanchard CD, Blanchard RJ et al (2005) The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci Biobehav Rev 29:1123–1144. doi: 10.1016/j.neubiorev.2005.05.005 CrossRefPubMedGoogle Scholar
  2. Bakker ES, Reiffers RC, Olff H, Gleichman JM (2005) Experimental manipulation of predation risk and food quality: effect on grazing behaviour in a central-place foraging herbivore. Oecologia 146:157–167. doi: 10.1007/s00442-005-0180-7 CrossRefPubMedGoogle Scholar
  3. Banks PB, Hume ID, Crowe O (1999) Behavioural, morphological and dietary response of rabbits to predation risk from foxes. Oikos 85:247–256CrossRefGoogle Scholar
  4. Bedoya-Pérez MA, Issa DD, Banks PB, McArthur C (2014) Quantifying the response of free-ranging mammalian herbivores to the interplay between plant defense and nutrient concentrations. Oecologia 175:1167–1177. doi: 10.1007/s00442-014-2980-0 CrossRefPubMedGoogle Scholar
  5. Behmer ST, Simpson SJ, Raubenheimer D (2002) Herbivore foraging in chemically heterogeneous environments: nutrients and secondary metabolites. Ecology 83:2489–2501. doi: 10.1890/0012-9658(2002)083[2489:HFICHE]2.0.CO;2 CrossRefGoogle Scholar
  6. Bond BT, Burger W, Leopold BD, Godwin KD (2001) Survival of cottontail rabbits (Sylvilagus floridanus) in Mississippi and an examination of latitudinal variation. Am Midl Nat 145:127–136. doi: 10.1674/0003-0031(2001)145[0127:SOCRSF]2.0.CO;2 CrossRefGoogle Scholar
  7. Brown JS (1988) Patch use as an indicator of habitat preference, predation risk, and competition. Behav Ecol Sociobiol 22:37–47. doi: 10.1007/BF00395696 CrossRefGoogle Scholar
  8. Brown JS, Kotler BP (2004) Hazardous duty pay and the foraging cost of predation. Ecol Lett 7:999–1014. doi: 10.1111/j.1461-0248.2004.00661.x CrossRefGoogle Scholar
  9. Camp MJ, Rachlow JL, Woods BA, Johnson TR, Shipley LA (2012) When to run and when to hide: the influence of concealment, visibility, and proximity to refugia on perceptions of risk. Ethology 118:1010–1017CrossRefGoogle Scholar
  10. Camp MJ, Shipley LA, Johnson TR et al (2015) Modeling trade-offs between plant fiber and toxins: a framework for quantifying risks perceived by foraging herbivores. Ecology 96:3292–3302. doi: 10.1890/14-2412.1 CrossRefPubMedGoogle Scholar
  11. Caraco T (1980) On foraging time allocation in a stochastic environment. Ecology 61:119–128. doi: 10.2307/1937162 CrossRefGoogle Scholar
  12. Caraco T, Martindale S, Whittam TS (1980) An empirical demonstration of risk-sensitive foraging preferences. Anim Behav 28:820–830. doi: 10.1016/S0003-3472(80)80142-4 CrossRefGoogle Scholar
  13. Chapman JA (1975) Sylvilagus nuttallii. Mamm Species 56:1–3CrossRefGoogle Scholar
  14. Coleman BT, Hill RA (2014) Living in a landscape of fear: the impact of predation, resource availability and habitat structure on primate range use. Anim Behav 88:165–173. doi: 10.1016/j.anbehav.2013.11.027 CrossRefGoogle Scholar
  15. Cooper AB, Millspaugh JJ (1999) The application of discrete choice models to wildlife resource selection studies. Ecology 80:566–575. doi: 10.1890/0012-9658(1999)080[0566:TAODCM]2.0.CO;2 CrossRefGoogle Scholar
  16. Crawford JA, Anthony RG, Forbes JT, Lorton GA (2010) Survival and causes of mortality for pygmy rabbits (Brachylagus idahoensis) in Oregon and Nevada. J Mammal 91:838–847CrossRefGoogle Scholar
  17. Crowell MM, Shipley LA, Camp MJ, Rachlow JL, Forbey JS, Johnson TR (2016) Selection of food patches by sympatric herbivores in response to concealment and distance from a refuge. Ecol Evol 6:2865–2876CrossRefPubMedPubMedCentralGoogle Scholar
  18. David HA (1988) The method of paired comparisons, 2nd edn. Hodder Arnold, London, New YorkGoogle Scholar
  19. DeGabriel JL, Moore BD, Foley WJ, Johnson CN (2009) The effects of plant defensive chemistry on nutrient availability predict reproductive success in a mammal. Ecology 90:711–719. doi: 10.1890/08-0940.1 CrossRefPubMedGoogle Scholar
  20. Demment MW, Van Soest PJ (1985) A nutritional explanation for body-size patterns of ruminant and nonruminant herbivores. Am Nat 641–672Google Scholar
  21. Fedriani JM, Boulay R (2006) Foraging by fearful frugivores: combined effect of fruit ripening and predation risk. Funct Ecol 20:1070–1079. doi: 10.1111/j.1365-2435.2006.01199.x CrossRefGoogle Scholar
  22. Fishburn PC (1968) Utility theory. Manag Sci 14:335–378CrossRefGoogle Scholar
  23. Foley WJ, McArthur C (1994) The effects and costs of allelochemicals for mammalian herbivores: an ecological perspective. Dig Syst Mamm Food Form Funct 1:370–391CrossRefGoogle Scholar
  24. Fowler ME (1983) Plant poisoning in free-living wild animals: a review. J Wildl Dis 19:34–43CrossRefPubMedGoogle Scholar
  25. Freeland WJ, Janzen DH (1974) Strategies in herbivory by mammals: the role of plant secondary compounds. Am Nat 108:269–289. doi: 10.2307/2459891 CrossRefGoogle Scholar
  26. Frye GG, Connelly JW, Musil DD, Forbey JS (2013) Phytochemistry predicts habitat selection by an avian herbivore at multiple spatial scales. Ecology 94:308–314CrossRefPubMedGoogle Scholar
  27. Goering HK, Van Soest PJ (1970) Forage fiber analysis (apparatus, reagents, procedures and some applications). U.S. Department of Agriculture Research Station. Agriculture Handbook 379. U.S. Government Printing Office, Washington, D.C., USAGoogle Scholar
  28. Götmark F, Blomqvist D, Johansson OC (1995) Nest site selection: a trade-off between concealment and view of the surroundings? J Avian Biol 26:305–312CrossRefGoogle Scholar
  29. Grand TC (2002) Alternative forms of competition and predation dramatically affect habitat selection under foraging—predation-risk trade-offs. Behav Ecol 13:280CrossRefGoogle Scholar
  30. Green JS, Flinders JT (1980) Brachylagus idahoensis. Mamm Species 125:1–4CrossRefGoogle Scholar
  31. Grubb TC (1975) Weather-dependent foraging behavior of some birds wintering in a deciduous woodland. The Condor 77:175–182. doi: 10.2307/1365788 CrossRefGoogle Scholar
  32. Hebblewhite M, Merrill EH (2009) Trade-offs between predation risk and forage differ between migrant strategies in a migratory ungulate. Ecology 90:3445–3454. doi: 10.1890/08-2090.1 CrossRefPubMedGoogle Scholar
  33. Heithaus MR, Dill LM (2002) Food availability and tiger shark predation risk influence bottlenose dolphin habitat use. Ecology 83:480–491CrossRefGoogle Scholar
  34. Hernández L, Laundré JW (2005) Foraging in the “landscape of fear” and its implications for habitat use and diet quality of elk Cervus elaphus and bison Bison bison. Wildl Biol 11:215–220. doi: 10.2981/0909-6396(2005)11[215:FITLOF]2.0.CO;2 CrossRefGoogle Scholar
  35. Hochman V, Kotler PB (2006) Effects of food quality, diet preference and water on patch use by Nubian ibex. Oikos 112:547–554. doi: 10.1111/j.0030-1299.2006.14214.x CrossRefGoogle Scholar
  36. Holmes WG (1991) Predator risk affects foraging behaviour of pikas: observational and experimental evidence. Anim Behav 42:111–119. doi: 10.1016/S0003-3472(05)80611-6 CrossRefGoogle Scholar
  37. Houston AI, McNamara JM, Hutchinson J (1993) General results concerning the trade-off between gaining energy and avoiding predation. Philos Trans R Soc Lond B Biol Sci 341:375CrossRefGoogle Scholar
  38. Iason G, Van Wieren SE (1999) Digestive and ingestive adaptations of mammalian herbivores to low-quality forage. In: Olff H, Brown VK, Drent RH (eds) Herbivores: between plants and predators. Blackwell Science, Oxford, pp 337–370Google Scholar
  39. Iribarren C, Kotler BP (2012) Foraging patterns of habitat use reveal landscape of fear of Nubian ibex Capra nubiana. Wildl Biol 18:194–201. doi: 10.2981/11-041 CrossRefGoogle Scholar
  40. Jakubas WJ, Mason JR (1991) Role of avian trigeminal sensory system in detecting coniferyl benzoate, a plant allelochemical. J Chem Ecol 17:2213–2221. doi: 10.1007/BF00988002 CrossRefPubMedGoogle Scholar
  41. Katzner TE, Parker KL, Harlow HH (1997) Metabolism and thermal response in winter-acclimatized pygmy rabbits (Brachylagus idahoensis). J Mammal 78:1053–1062. doi: 10.2307/1383048 CrossRefGoogle Scholar
  42. Kelsey RG, Stephens JR, Shafizadeh F (2006) The chemical constituents of sagebrush foliage and their isolation. J Range Manag Arch 35:617–622CrossRefGoogle Scholar
  43. Kirmani SN, Banks PB, McArthur C (2010) Integrating the costs of plant toxins and predation risk in foraging decisions of a mammalian herbivore. Oecologia 164:349–356. doi: 10.1007/s00442-010-1717-y CrossRefPubMedGoogle Scholar
  44. Kleiber M (1975) The fire of life: an introduction to animal energetics. Krieger, HuntingtonGoogle Scholar
  45. Kohl KD, Pitman E, Robb BC et al (2015) Monoterpenes as inhibitors of digestive enzymes and counter-adaptations in a specialist avian herbivore. J Comp Physiol [B] 185:425–434. doi: 10.1007/s00360-015-0890-z CrossRefGoogle Scholar
  46. Kotler BP, Blaustein L (1995) Titrating food and safety in a heterogeneous environment: when are the risky and safe patches of equal value? Oikos 74:251–258. doi: 10.2307/3545654 CrossRefGoogle Scholar
  47. Kotler BP, Brown JS, Bouskila A (2004) Apprehension and time allocation in gerbils: the effects of predatory risk and energetic state. Ecology 85:917–922. doi: 10.1890/03-3002 CrossRefGoogle Scholar
  48. Kotler BP, Brown J, Mukherjee S et al (2010) Moonlight avoidance in gerbils reveals a sophisticated interplay among time allocation, vigilance and state-dependent foraging. Proc R Soc B Biol Sci 277:1469–1474. doi: 10.1098/rspb.2009.2036 CrossRefGoogle Scholar
  49. Lima SL (1985) Maximizing feeding efficiency and minimizing time exposed to predators: a trade-off in the black-capped chickadee. Oecologia 66:60–67CrossRefPubMedGoogle Scholar
  50. Longland WS, Price MV (1991) Direct observations of owls and heteromyid rodents: can predation risk explain microhabitat use? Ecology 72:2261–2273CrossRefGoogle Scholar
  51. Lucas JR (1983) The Role of foraging time constraints and variable prey encounter in optimal diet choice. Am Nat 122:191–209CrossRefGoogle Scholar
  52. MacCracken JG, Hansen RM (1984) Seasonal foods of blacktail jackrabbits and Nuttall cottontails in southeastern Idaho. J Range Manag 256–259Google Scholar
  53. McArthur C, Hagerman AE, Robbins CT (1991) Physiological strategies of mammalian herbiores against plant defenses. In: Palo RT, Robbins CT (eds) Plant defenses against mammalian herbivores. CRC Press, Boca Raton, pp 103–114Google Scholar
  54. McArthur C, Orlando P, Banks PB, Brown JS (2012) The foraging tightrope between predation risk and plant toxins: a matter of concentration. Funct Ecol 26:74–83. doi: 10.1111/j.1365-2435.2011.01930.x CrossRefGoogle Scholar
  55. McArthur C, Banks PB, Boonstra R, Forbey JS (2014) The dilemma of foraging herbivores: dealing with food and fear. Oecologia 176:677–689CrossRefPubMedGoogle Scholar
  56. McDonald TL, Manly BFJ, Nielson RM, Diller LV (2006) Discrete-choice modeling in wildlife studies exemplified by northern spotted owl nighttime habitat selection. J Wildl Manag 70:375–383. doi: 10.2193/0022-541X(2006)70[375:DMIWSE]2.0.CO;2 CrossRefGoogle Scholar
  57. Mella VSA, Ward AJW, Banks PB, McArthur C (2014) Personality affects the foraging response of a mammalian herbivore to the dual costs of food and fear. Oecologia. doi: 10.1007/s00442-014-3110-8 PubMedGoogle Scholar
  58. Nersesian CL, Banks PB, McArthur C (2011) Titrating the cost of plant toxins against predators: determining the tipping point for foraging herbivores. J Anim Ecol 80:753–760. doi: 10.1111/j.1365-2656.2011.01822.x CrossRefPubMedGoogle Scholar
  59. Nobler JD (2016) Risky business: tradeoffs between nutrition, toxicity, and predation by a specialist mammalian herbivore. Master’s Thesis, Boise State University, Boise, IDGoogle Scholar
  60. Orr RT (1940) The rabbits of California. California academy of sciences, CaliforniaGoogle Scholar
  61. Parsons MA, Barkley TC, Rachlow JL et al (2016) Cumulative effects of an herbivorous ecosystem engineer in a heterogeneous landscape. Ecosphere. doi: 10.1002/ecs2.1334 Google Scholar
  62. Price AJ, Estes-Zumpf W, Rachlow J (2010) Survival of juvenile pygmy rabbits. J Wildl Manag 74:43–47. doi: 10.2193/2008-578 CrossRefGoogle Scholar
  63. Provenza FD, Burritt EA, Clausen TP et al (1990) Conditioned flavor aversion: a mechanism for goats to avoid condensed tannins in blackbrush. Am Nat 136:810–828CrossRefGoogle Scholar
  64. R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/
  65. Rachlow JL, Sanchez DM, Estes-Zumpf WA (2005) Natal burrows and nests of free-ranging pygmy rabbits (Brachylagus idahoensis). West North Am Nat 65:136–139Google Scholar
  66. Rapport DJ (1971) An optimization model of food selection. Am Nat 105:575–587CrossRefGoogle Scholar
  67. Rapport DJ (1980) Optimal foraging for complementary resources. Am Nat 116:324–346CrossRefGoogle Scholar
  68. Robbins CT, Hagerman AE, Austin PJ et al (1991) Variation in mammalian physiological responses to a condensed tannin and its ecological implications. J Mammal 72:480. doi: 10.2307/1382130 CrossRefGoogle Scholar
  69. Schmidt KA (2000) Interactions between food chemistry and predation risk in fox squirrels. Ecology 81:2077–2085. doi: 10.1890/0012-9658(2000)081[2077:IBFCAP]2.0.CO;2
  70. Schooley RL, Sharpe PB, Van Horne B (1996) Can shrub cover increase predation risk for a desert rodent? Can J Zool 74:157–163CrossRefGoogle Scholar
  71. Searle KR, Stokes CJ, Gordon IJ (2008) When foraging and fear meet: using foraging hierarchies to inform assessments of landscapes of fear. Behav Ecol 19:475CrossRefGoogle Scholar
  72. Shipley LA, Spalinger DE (1995) Influence of size and density of browse patches on intake rates and foraging decisions of young moose and white-tailed deer. Oecologia 104:112–121. doi: 10.1007/BF00365569 CrossRefPubMedGoogle Scholar
  73. Shipley LA, Davila TB, Thines NJ, Elias BA (2006) Nutritional requirements and diet choices of the pygmy rabbit (Brachylagus idahoensis): a sagebrush specialist. J Chem Ecol 32:2455–2474. doi: 10.1007/s10886-006-9156-2 CrossRefPubMedGoogle Scholar
  74. Shipley LA, Davis EM, Felicetti LA et al (2012) Mechanisms for eliminating monoterpenes of sagebrush by specialist and generalist Rabbits. J Chem Ecol 38:1178–1189. doi: 10.1007/s10886-012-0192-9 CrossRefPubMedGoogle Scholar
  75. Shrader MA, Kotler BP, Brown JS, Kerley GH (2008) Providing water for goats in arid landscapes: effects on feeding effort with regard to time period, herd size and secondary compounds. Oikos 117:466–472. doi: 10.1111/j.2007.0030-1299.16410.x CrossRefGoogle Scholar
  76. Sih A (1980) Optimal behavior: can foragers balance two conflicting demands? Science 210:1041–1043CrossRefPubMedGoogle Scholar
  77. Siitari H, Viitala J, Hovi M (2002) Behavioural evidence for ultraviolet vision in a tetraonid species—foraging experiment with black grouse Tetrao tetrix. J Avian Biol 33:199–202. doi: 10.1034/j.1600-048X.2002.330212.x CrossRefGoogle Scholar
  78. Sorensen JS, McLister JD, Dearing MD (2005) Plant secondary metabolites compromise the energy budgets of specialist and generalist mammalian herbivores. Ecology 86:125–139. doi: 10.1890/03-0627 CrossRefGoogle Scholar
  79. Stamps JA (2007) Growth-mortality tradeoffs and “personality traits” in animals. Ecol Lett 10:355–363. doi: 10.1111/j.1461-0248.2007.01034.x CrossRefPubMedGoogle Scholar
  80. Thines NJ, Shipley LA, Sayler RD (2004) Effects of cattle grazing on ecology and habitat of Columbia Basin pygmy rabbits (Brachylagus idahoensis). Biol Conserv 119:525–534CrossRefGoogle Scholar
  81. Turner AK (1982) Optimal foraging by the swallow (Hirundo rustica, L): prey size selection. Anim Behav 30:862–872. doi: 10.1016/S0003-3472(82)80160-7 CrossRefGoogle Scholar
  82. Ulappa AC, Kelsey RG, Frye GG et al (2014) Plant protein and secondary metabolites influence diet selection in a mammalian specialist herbivore. J Mammal 95:834–842. doi: 10.1644/14-MAMM-A-025 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Utz JL, Shipley LA, Rachlow JL, Johnston-Yellin T, Camp MJ, Forbey JS (2016) Understanding tradeoffs between food and predation risks in a specialist mammalian herbivore. Wildl Biol 22:167–173CrossRefGoogle Scholar
  84. Wagoner SJ, Shipley LA, Cook RC, Hardesty L (2013) Spring cattle grazing and mule deer nutrition in a bluebunch wheatgrass community. J Wildl Manag 77:897–907CrossRefGoogle Scholar
  85. Willems EP, Hill RA (2009) Predator-specific landscapes of fear and resource distribution: effects on spatial range use. Ecology 90:546–555. doi: 10.1890/08-0765.1 CrossRefPubMedGoogle Scholar
  86. Wirsing AJ, Heithaus MR, Dill LM (2007) Fear factor: do dugongs (Dugong dugon) trade food for safety from tiger sharks (Galeocerdo cuvier)? Oecologia 153:1031–1040. doi: 10.1007/s00442-007-0802-3 CrossRefPubMedGoogle Scholar
  87. Wolf M, van Doorn GS, Leimar O, Weissing FJ (2007) Life-history trade-offs favour the evolution of animal personalities. Nature 447:581–584. doi: 10.1038/nature05835 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • M. J. Camp
    • 1
  • L. A. Shipley
    • 1
  • T. R. Johnson
    • 2
  • P. J. Olsoy
    • 1
  • J. S. Forbey
    • 3
  • J. L. Rachlow
    • 4
  • D. H. Thornton
    • 1
  1. 1.School of the EnvironmentWashington State UniversityPullmanUSA
  2. 2.Department of Statistical ScienceUniversity of IdahoMoscowUSA
  3. 3.Department of Biological SciencesBoise State UniversityBoiseUSA
  4. 4.Department of Fish and Wildlife SciencesUniversity of IdahoMoscowUSA

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