, Volume 186, Issue 1, pp 73–84 | Cite as

What to eat in a warming world: do increased temperatures necessitate hazardous duty pay?

  • L. Embere HallEmail author
  • Anna D. Chalfoun
Behavioral ecology –original research


Contemporary climate change affects nearly all biomes, causing shifts in animal distributions and resource availability. Changes in resource selection may allow individuals to offset climatic stress, thereby providing a mechanism for persistence amidst warming conditions. Whereas the role of predation risk in food choice has been studied broadly, the extent to which individuals respond to thermoregulatory risk by changing resource preferences is unclear. We addressed whether individuals compensated for temperature-related reductions in foraging time by altering forage preferences, using the American pika (Ochotona princeps) as a model species. We tested two hypotheses: (1) food-quality hypothesis—individuals exposed to temperature extremes should select higher-quality vegetation in return for accepting a physiologically riskier feeding situation; and (2) food-availability hypothesis—individuals exposed to temperature extremes should prioritize foraging quickly, thereby decreasing selection for higher-quality food. We quantified the composition and quality (% moisture, % nitrogen, and fiber content) of available and harvested vegetation, and deployed a network of temperature sensors to measure in situ conditions for 30 individuals, during July–Sept., 2015. Individuals exposed to more extreme daytime temperatures showed increased selection for high-nitrogen and for low-fiber vegetation, demonstrating strong support for the food-quality hypothesis. By contrast, pikas that experienced warmer conditions did not reduce selection for any of the three vegetation-quality metrics, as predicted by the food-availability hypothesis. By shifting resource-selection patterns, temperature-limited animals may be able to proximately buffer some of the negative effects associated with rapidly warming environments, provided that sufficient resources remain on the landscape.


Thermoregulatory risk Climate change Forage choice Resource selection Ochotona princeps 



The Wyoming Game and Fish Department, in cooperation with the Meg & Bert Raynes Wildlife Fund, Natural Resource Conservation Service, University of Wyoming-Office of Research, University of Wyoming-Program in Ecology, University of Wyoming-Zoology and Physiology Department, U.S. Geological Survey, and Louise & Ralph Haberfeld, funded our work. We are grateful to C. Tarwater, T. Robinson, J. Ceradini and J. Carlisle for advice on statistical analyses, along with colleagues in the Quantitative Analysis of Field Data course at the University of Wyoming. G. Barille and L. Sanders provided helpful comments on our preliminary findings. We thank E. Beever, M. Ben-David, J. Merkle, J. Shinker, C. Whelan and two anonymous referees for insightful feedback on an earlier draft of the manuscript. Field and data support were provided by: S. DuBose, S. Gaddis, J. Henningsen, R. Jakopak, A. Ruble, C. Tappe and M. Wallace. Any use of trade, firm or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Author contributions

LEH formulated the idea, LEH and ADC developed hypotheses and designed the study, LEH conducted the fieldwork, completed the analyses and drafted the manuscript, ADC provided critical feedback on manuscript drafts as well as essential intellectual input throughout the entirety of the study.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

All applicable institutional and/or national guidelines for the care and use of animals were followed.


  1. Barash DP (1973) Territorial and foraging behavior of pika (Ochotona princeps) in Montana. Am Midl Nat 89:202–207CrossRefGoogle Scholar
  2. Barboza PS, Parker KL, Hume ID (2009) Integrative wildlife nutrition. Springer, BerlinCrossRefGoogle Scholar
  3. Barrio IC, Hik DS, Bueno CG, Cahill JF (2013) Extending the stress-gradient hypothesis—is competition among animals less common in harsh environments? Oikos 122:516–523. CrossRefGoogle Scholar
  4. Bednekoff PA (2007) Foraging in the face of danger. In: Stephenson DW, Brown JS, Ydenberg RC (eds) Foraging behavior and ecology. University of Chicago Press, Chicago, pp 305–332Google Scholar
  5. Beever E, Ray C, Mote PW, Wilkening JL (2010) Testing alternative models of climate-mediated extirpations. Ecol Appl 20:164–178CrossRefPubMedGoogle Scholar
  6. Beever EA, Hall LE, Varner J et al. (2017) Behavioral flexibility as a mechanism for coping with climate change. Front Ecol Environ 15:299–308. CrossRefGoogle Scholar
  7. Bennett AF, Huey RB, John-Alder H, Nagy KA (1984) The parasol tail and thermoregulatory behavior of the cape ground squirrel Xerus inauius’. Physiol Zool 57:57–62CrossRefGoogle Scholar
  8. Bhattacharyya S, Adhikari BS, Rawat GS (2013) Forage selection by Royle’s pika (Ochotona roylei) in the western Himalaya, India. Zoology 116:300–306. CrossRefPubMedGoogle Scholar
  9. Blumstein DT, Daniel JC (2007a) Quantifying behavior the JWatcher way. SinauerAssociates, SunderlandGoogle Scholar
  10. Blumstein DT, Daniel JC (2007b) Checking your reliability. Quantifying behavior the JWatcher way. SinauerAssociates, Sunderland, pp 39–42Google Scholar
  11. Blumstein DT, Daniel JC, Evans CS (2006) JWatcherGoogle Scholar
  12. Bobbink R, Hicks K, Galloway J et al (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20:30–59CrossRefPubMedGoogle Scholar
  13. Boersma M, Mathew KA, Niehoff B et al (2016) Temperature driven changes in the diet preference of omnivorous copepods: no more meat when it’s hot? Ecol Lett 19:45–53. CrossRefPubMedGoogle Scholar
  14. Bowman WD, Murgel J, Blett T, Porter E (2012) Nitrogen critical loads for alpine vegetation and soils in Rocky Mountain National Park. J Environ Manage 103:165–171. CrossRefPubMedGoogle Scholar
  15. Brown JS (1999) Vigilance, patch use and habitat selection: foraging under predation risk. Evol Ecol Res 1:49–71Google Scholar
  16. Brown JS, Kotler BP (2004) Hazardous duty pay and the foraging cost of predation. Ecol Lett 7:999–1014. CrossRefGoogle Scholar
  17. Brown JS, Kotler BP (2007) Foraging and the ecology of fear. In: Stephenson DB, Brown JS, Ydenberg RC (eds) Foraging behavior and ecology. University of Chicago Press, Chicago, pp 437–482Google Scholar
  18. Brown JS, Laundré JW, Gurung M (1999) The ecology of fear: optimal foraging, game theory, and trophic interactions. J Mammal 80:385–399CrossRefGoogle Scholar
  19. Conner DA (1983) Seasonal changes in activity patterns and the adaptive value of haying in pikas (Ochotona princeps). Can J Zool 61:411–416CrossRefGoogle Scholar
  20. Crawley MJ (2013a) Proportion data. The R book, 2nd edn. Wiley, Chichester, pp 628–649Google Scholar
  21. Crawley MJ (2013b) Mathematics. The R book, 2nd edn. Wiley, Chichester, pp 258–343Google Scholar
  22. Daubenmire R (1959) A canopy-coverage method of vegetational analysis. Northwest Sci 33:43–64Google Scholar
  23. Dearing MD (1996) Disparate determinants of summer and winter diet selection of a generalist herbivore, Ochotona princeps. Oecologia 108:467–478. CrossRefPubMedGoogle Scholar
  24. Dearing D (1997a) The function of haypiles of pikas (Ochotona princeps). J Mammal 78:1156–1163CrossRefGoogle Scholar
  25. Dearing D (1997b) The manipulation of plant toxins by a food-hoarding herbivore, Ochotona princeps. Ecology 78:774–781CrossRefGoogle Scholar
  26. Dearing MD (2013) Temperature-dependent toxicity in mammals with implications for herbivores: a review. J Comp Physiol B Biochem Syst Environ Physiol 183:43–50. CrossRefGoogle Scholar
  27. DeGabriel JL, Wallis IR, Moore BD, Foley WJ (2008) A simple, integrative assay to quantify nutritional quality of browses for herbivores. Oecologia 156:107–116. CrossRefPubMedGoogle Scholar
  28. Elzinga CL, Salzer DW, Willoughby JW (2001) Measuring and monitoring plant populations, 1st edn. Bureau of Land Management, DenverGoogle Scholar
  29. Erb LP, Ray C, Guralnick R (2011) On the generality of a climate-mediated shift in the distribution of the American pika (Ochotona princeps). Ecology 92:1730–1735CrossRefPubMedGoogle Scholar
  30. Espinheira PL, Ferrari SLP, Cribari-Neto F (2008) Influence diagnostics in beta regression. Comput Stat Data Anal 52:4417–4431. CrossRefGoogle Scholar
  31. Ferrari SLP, Cribari-Neto F (2004) Beta regression for modelling rates and proportions. J Appl Stat 31:799–815. CrossRefGoogle Scholar
  32. Fick LG, Kucio TA, Fuller A et al (2009) The relative roles of the parasol-like tail and burrow shuttling in thermoregulation of free-ranging Cape ground squirrels, Xerus inauris. Comp Biochem Physiol Part A 152:334–340. CrossRefGoogle Scholar
  33. Fortin D, Beyer HL, Boyce MS et al (2005) Wolves influence elk movements: behavior shapes a trophic cascade in Yellowstone National Park. Ecology 86:1320–1330CrossRefGoogle Scholar
  34. Fournier D, Skaug H, Ancheta J et al. (2012) AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Methods Softw 27:233–249CrossRefGoogle Scholar
  35. Galbreath KE, Hafner DJ, Zamudio KR (2009) When cold is better: climate-driven elevation shifts yield complex patterns of diversification and demography in an alpine specialist (American pika, Ochotona princeps). Evolution 63:2848–2863. CrossRefPubMedGoogle Scholar
  36. Garshelis D (2000) Delusions in habitat evaluation: measuring use, selection and importance. In: Boitani L, Fuller T (eds) Research techniques in animal ecology. Controversies and consequences. Columbia University Press, New York, pp 111–161Google Scholar
  37. Hall LE (2017) Behavioral plasticity and resilience of a montane mammal in a changing climate. PhD dissertation, Department of Zoology and Physiology, University of Wyoming, Laramie, Wyoming, USAGoogle Scholar
  38. Hall LE, Chalfoun AD, Beever EA, Loosen AE (2016) Microrefuges and the occurrence of thermal specialists: implications for wildlife persistence amidst changing temperatures. Clim Change Responses 3:1–12. CrossRefGoogle Scholar
  39. Holmes WG (1991) Predator risk affects foraging behaviour of pikas: observational and experimental evidence. Anim Behav 42:111–119. CrossRefGoogle Scholar
  40. Hovick TJ, Elmore RD, Allred BW et al (2014) Landscapes as a moderator of thermal extremes: a case study from an imperiled grouse. Ecosphere 5:1–12. CrossRefGoogle Scholar
  41. Hudson JMG, Morrison SF, Hik DS (2008) Effects of leaf size on forage selection by Collared Pikas, Ochotona collaris. Arctic Antarct Alp Res 40:481–486.[HUDSON]2.0.CO;2 CrossRefGoogle Scholar
  42. Huntly NJ (1987) Influence of refuging consumers (Pikas: Ochotona princeps) on subalpine meadow vegetation. Ecology 68:274–283CrossRefGoogle Scholar
  43. Huntly NJ, Smith AT, Ivins BL (1986) Foraging behavior of the Pika (Ochotona princeps), with comparisons of grazing versus haying. J Mammal 67:139–148CrossRefGoogle Scholar
  44. IPCC (2013) Annex I: Atlas of global and regional climate projections. In: Stocker TF, Qin D, Plattner G-K et al (eds) Climate Change 2013: the physical science basis. Contribution of Working Group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge and New York, pp 1313–1390Google Scholar
  45. Jakopak R, Hall LE, Chalfoun AD (2017) Organizing the pantry: cache management improves quality of overwinter food stores in a montane mammal. J Mammal. Google Scholar
  46. Jezkova T, Wiens JJ (2016) Rates of change in climatic niches in plant and animal populations are much slower than projected climate change. Proc R Soc B Biol Sci 283:20162104. CrossRefGoogle Scholar
  47. Knight DH, Jones GP, Reiners WA, Romme WH (2014) Mountains and plains, 2nd edn. Yale University Press, New HavenGoogle Scholar
  48. Kotler B, Blaustein L (1995) Titrating food and safety in a heterogeneous environment: when are the risky and safe patches of equal value? Oikos 74:251–258CrossRefGoogle Scholar
  49. Kurnath P, Merz ND, Dearing MD (2016) Ambient temperature influences tolerance to plant secondary compounds in a mammalian herbivore. Proc R Soc London B Biol Sci 283:1–5. CrossRefGoogle Scholar
  50. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640. CrossRefGoogle Scholar
  51. Lima SL, Valone TJ (1986) Influence of predation risk on diet selection: a simple example in the gray squirrel. Anim Behav 34:536–544. CrossRefGoogle Scholar
  52. Lima SL, Valone TJ, Caraco T (1985) Foraging-efficiency predation-risk trade-off in the grey squirrel. Anim Behav 33:155–165. CrossRefGoogle Scholar
  53. Livensperger C, Steltzer H, Darrouzet-Nardi A et al. (2016) Earlier snowmelt and warming lead to earlier but not necessarily more plant growth. AoB Plants 8:plw021. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Lucas JR (1985) Time constraints and diet choice: different predictions from different constraints. Am Nat 126:680–705CrossRefGoogle Scholar
  55. Lucas JR (1987) Foraging time constraints and diet choice. In: Kamil AC, Krebs JR, Pulliam HR (eds) Foraging behavior. Plenum Press, New York, pp 239–270CrossRefGoogle Scholar
  56. MacArthur RA, Wang LCH (1973) Physiology of thermoregulation in the pika, Ochotona princeps. Can J Zool 51:11–16CrossRefPubMedGoogle Scholar
  57. Mathewson PD, Moyer-Horner L, Beever EA et al (2017) Mechanistic variables can enhance predictive models of endotherm distributions: the American pika under current, past, and future climates. Glob Chang Biol. Google Scholar
  58. Mathius IW (1987) Utilization of non protein nitrogen by rabbits. Master thesis, Department of Animal Science, Oregon State University, Corvallis, Oregon, USAGoogle Scholar
  59. Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161. CrossRefGoogle Scholar
  60. McIntire EJB, Hik DS (2005) Influences of chronic and current season grazing by collared pikas on above-ground biomass and species richness in subarctic alpine meadows. Oecologia 145:288–297. CrossRefPubMedGoogle Scholar
  61. Merkle JA, Monteith KL, Aikens EO et al (2016) Large herbivores surf waves of green-up in spring. Proc R Soc B 283:1–8. CrossRefGoogle Scholar
  62. Merrill AL, Watt BK (1955) Energy value of foods—basis and derivation. US Department of Agriculture, Washington, DCGoogle Scholar
  63. Millar CI, Westfall RD (2010) Distribution and climatic relationships of the American Pika (Ochotona princeps) in the Sierra Nevada and Western Great Basin, U.S.A.; periglacial landforms as refugia in warming climates. Arctic Antarct Alp Res 42:76–88. CrossRefGoogle Scholar
  64. Millar JS, Zwickel FC (1972) Characteristics and ecological significance of hay piles in pikas. Mammalia 36:657–667CrossRefGoogle Scholar
  65. Morrison SF, Hik DS (2008) Descrimination of intra- and inter-specific forage quality by collared pikas (Ochotona collaris). Can J Zool 86:456–461CrossRefGoogle Scholar
  66. Morrison S, Barton L, Caputa P, Hik DS (2004) Forage selection by collared pikas, Ochotona collaris, under varying degrees of predation risk. Can J Zool 82:533–540CrossRefGoogle Scholar
  67. Morrison SF, Pelchat G, Donahue A, Hik DS (2009) Influence of food hoarding behavior on the over-winter survival of pikas in strongly seasonal environments. Oecologia 159:107–116. CrossRefPubMedGoogle Scholar
  68. Nicotra AB, Beever EA, Robertson AL et al (2015) Assessing the components of adaptive capacity to improve conservation and management efforts under global change. Conserv Biol 29:1268–1278. CrossRefPubMedGoogle Scholar
  69. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669. CrossRefGoogle Scholar
  70. Parsons JL, Hellgren EC, Jorgensen EE, Leslie DM (2005) Neonatal growth and survival of rodents in response to variation in maternal dietary nitrogen: life history strategy vs dietary niche. Oikos 110:297–308CrossRefGoogle Scholar
  71. Quintero I, Wiens JJ (2013) Rates of projected climate change dramatically exceed past rates of climatic niche evolution among vertebrate species. Ecol Lett 16:1095–1103. CrossRefPubMedGoogle Scholar
  72. R Core Team (2015) R: a language and environment for statistical computingGoogle Scholar
  73. Robbins CT, Hanley T, Hagerman A et al (1987) Role of tannins in defending plants against ruminants: reduction in protein availability. Ecology 68:98–107CrossRefGoogle Scholar
  74. Rodhouse T, Beever E, Garrett L et al. (2010) Distribution of American pikas in a low-elevation lava landscape: conservation implications from the range periphery. J Mammal 91:1287–1299. CrossRefGoogle Scholar
  75. Rowland EL, Davison JE, Graumlich LJ (2011) Approaches to evaluating climate change impacts on species: a guide to initiating the adaptation planning process. Environ Manage 47:322–337. CrossRefPubMedGoogle Scholar
  76. Sih A (1993) Effects of ecological interactions on forager diets: competition, predation risk, parasitism and prey behaviour. In: Huges R (ed) Diet selection: an interdisciplinary approach to foraging behavior. Blackwell Scientific Publications, Oxford, pp 182–212Google Scholar
  77. Sih A, Ferrari MCO, Harris DJ (2011) Evolution and behavioural responses to human-induced rapid environmental change. Evol Appl 4:367–387. CrossRefPubMedPubMedCentralGoogle Scholar
  78. Skaug H, Fournier D, Bolker B et al (2016) Generalized linear mixed models using “AD Model Builder.”Google Scholar
  79. Smith AT (1974) The distribution and dispersal of pikas: influences of behavior and climate. Ecology 55:1368–1376CrossRefGoogle Scholar
  80. Smith JA, Erb LP (2013) Patterns of selective caching behavior of a generalist herbivore, the American Pika (Ochotona princeps). Arctic Antarct Alp Res 45:396–403. CrossRefGoogle Scholar
  81. Strauss RE (1979) Reliability estimates for Ivlev’s electivity index, the forage ratio, and a proposed linear index of food selection. Trans Am Fish Soc 108:344–352CrossRefGoogle Scholar
  82. Tinbergen JM (1981) Foraging decisions in starlings Sturnus vulgaris. Ardea 69:1–67Google Scholar
  83. Torres-Dowdal J, Handelsman CA, Reznick DN, Ghalambor CK (2012) Local adaptation and the evolution of phenotypic plasticity in Trinidadian guppies (Poecilia reticulata). Evolution 66:3432–3443. CrossRefGoogle Scholar
  84. Tuomainen U, Candolin U (2011) Behavioural responses to human-induced environmental change. Biol Rev 86:640–657. CrossRefPubMedGoogle Scholar
  85. Van Buskirk J (2012) Behavioural plasticity and environmental change. In: Candolin U, Wong B (eds) Behavioural responses to a changing world, 1st edn. Oxford University Press, Oxford, pp 145–158CrossRefGoogle Scholar
  86. van der Graff S, Stahl J, Klimkowska A et al (2006) Surfing on a green wave—how plant growth drives spring migration in the Barnacle Goose Branta leucopsis. Ardea 94:567–577Google Scholar
  87. Vander Wall S (1990) How do animals use stored food? Food hoarding in animals. University of Chicago Press, Chicago, pp 8–42Google Scholar
  88. Varner J, Dearing MD (2014) Dietary plasticity in pikas as a strategy for atypical resource landscapes. J Mammal 95:72–81. CrossRefGoogle Scholar
  89. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, OxfordGoogle Scholar
  90. Wilkening JL, Ray C, Beever EA, Brussard PF (2011) Modeling contemporary range retraction in Great Basin pikas (Ochotona princeps) using data on microclimate and microhabitat. Quat Int 235:77–88. CrossRefGoogle Scholar
  91. Williams SE, Shoo LP, Isaac JL et al (2008) Towards an integrated framework for assessing the vulnerability of species to climate change. PLoS Biol 6:2621–2626. CrossRefPubMedGoogle Scholar
  92. Wong BBM, Candolin U (2015) Behavioral responses to changing environments. Behav Ecol 26:665–673. CrossRefGoogle Scholar
  93. Zuur AF, Ieno EN (2016) A protocol for conducting and presenting results of regression-type analyses. Methods Ecol Evol 7:636–645. CrossRefGoogle Scholar
  94. Zuur AF, Ieno EN, Walker NJ et al (2009) Mixed effects modelling for nested data. Mixed effects models and extensions in ecology with R, 1st edn. Springer Science+Business Media, New York, pp 101–139CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Wyoming Cooperative Fish and Wildlife Research Unit, Department of Zoology and Physiology, Program in EcologyUniversity of WyomingLaramieUSA
  2. 2.U.S. Geological Survey, Wyoming Cooperative Fish and Wildlife Research Unit, Department of Zoology and Physiology, Program in EcologyUniversity of WyomingLaramieUSA

Personalised recommendations