Skip to main content

Snow roosting reduces temperature-associated stress in a wintering bird

Abstract

Animals in temperate northern regions employ a variety of strategies to cope with the energetic demands of winter. Behavioral plasticity may be important, as winter weather conditions are increasingly variable as a result of modern climate change. If behavioral strategies for thermoregulation are no longer effective in a changing environment, animals may experience physiological stress, which can have fitness consequences. We monitored winter roosting behavior of radio–tagged ruffed grouse (Bonasa umbellus), recorded snow depth and temperature, and assayed droppings for fecal corticosterone metabolites (FCM). Grouse FCM levels increased with declining temperatures. FCM levels were high when snow was shallow, but decreased rapidly as snow depth increased beyond 20 cm. When grouse used snow burrows, there was no effect of temperature on FCM levels. Snow burrowing is an important strategy that appears to allow grouse to mediate the possibly stressful effects of cold temperatures. This is one of the first studies to explore how variable winter weather conditions influence stress in a free–living cold–adapted vertebrate and its ability to mediate this relationship behaviorally. Animals that depend on the snowpack as a winter refuge will likely experience increased stress and possible fitness costs resulting from the loss of snow cover due to climate change.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Anderson KJ, Jetz W (2005) The broad-scale ecology of energy expenditure of endotherms. Ecol Lett 8:310–318. https://doi.org/10.1111/j.1461-0248.2005.00723.x

    Article  Google Scholar 

  2. Astheimer LB, Buttemer WA, Wingfield JC (1992) Interactions of corticosterone with feeding, activity and metabolism in passerine birds. Ornis Scand 23:355–365. https://doi.org/10.2307/3676661

    Article  Google Scholar 

  3. Baltic M, Jenni-Eiermann S, Arlettaz R, Palme R (2005) A noninvasive technique to evaluate human-generated stress in the Black Grouse. Ann N Y Acad Sci 1046:81–95

    Article  CAS  PubMed  Google Scholar 

  4. Barton K (2018) MuMIn: multi-model inference. R. package version 1.42.1, https://CRAN.R-project.org/package=MuMIn. Accessed 1 July 2018

  5. Bates D, Machler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  6. Beever EA et al (2017) Behavioral flexibility as a mechanism for coping with climate change. Front Ecol Environ 15:299–308. https://doi.org/10.1002/fee.1502

    Article  Google Scholar 

  7. Blanchette P, Bourgeois JC, St-Onge S (2007) Winter selection of roost sites by ruffed grouse durling daytime in mixed nordic-temperate forests, Quebec, Canada. Can J Zool 85:497–504. https://doi.org/10.1139/z07-027

    Article  Google Scholar 

  8. Boonstra R (2013) Reality as the leading cause of stress: rethinking the impact of chronic stress in nature. Funct Ecol 27:11–23. https://doi.org/10.1111/1365-2435.12008

    Article  Google Scholar 

  9. Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441:81–83. https://doi.org/10.1038/nature04539

    Article  CAS  PubMed  Google Scholar 

  10. Both C, van Asch M, Bijlsma RG, van den Burg AB, Visser ME (2009) Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? J Anim Ecol 78:73–83. https://doi.org/10.1111/j.1365-2656.2008.01458.x

    Article  PubMed  Google Scholar 

  11. Breheny P, Burchett W (2017) Visualization of regression models using visreg. R J 9:56–71

    Article  Google Scholar 

  12. Breuner CW, Greenberg AL, Wingfield JC (1998) Noninvasive corticosterone treatment rapidly increases activity in Gambel’s white-crowned sparrows (Zonotrichia leucophrys gambelii). Gen Comp Endocrinol 111:386–394. https://doi.org/10.1006/gcen.1998.7128

    Article  CAS  PubMed  Google Scholar 

  13. Bump GR, Darrow RW, Edminster FC, Crissey WF (1947) The Ruffed grouse: life history, propagation, and management. New York State Conservation Department, Buffalo

    Google Scholar 

  14. Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  15. Cade BS (2015) Model averaging and muddled multimodel inferences. Ecology 96:2370–2382

    Article  PubMed  Google Scholar 

  16. Carere C, Groothuis TGG, Mostl E, Daan S, Koolhaas JM (2003) Fecal corticosteroids in a territorial bird selected for different personalities: daily rhythm and the response to social stress. Horm Behav 43:540–548

    Article  CAS  PubMed  Google Scholar 

  17. Cooper SJ (2002) Seasonal metabolic acclimatization in mountain chickadees and juniper titmice. Physiol Biochem Zool 75:386–395. https://doi.org/10.1086/342256

    Article  PubMed  Google Scholar 

  18. Dammhahn M, Landry-Cuerrier M, Reale D, Garant D, Humphries MM (2017) Individual variation in energy-saving heterothermy affects survival and reproductive success. Funct Ecol 31:866–875. https://doi.org/10.1111/1365-2435.12797

    Article  Google Scholar 

  19. Dantzer B, Fletcher QE, Boonstra R, Sheriff MJ (2014) Measures of physiological stress: a transparent or opaque window into the status, management and conservation of species? Conserv Physiol. https://doi.org/10.1093/conphys/cou023

    Article  PubMed  PubMed Central  Google Scholar 

  20. Descovich KA, Lisle AT, Johnston S, Keeley T, Phillips CJC (2012) Intrasample variation and the effect of storage delay on faecal metabolite concentrations in the southern hairy-nosed wombat (Lasiorhinus latifrons). Aust Mammal 34:217–222

    Article  Google Scholar 

  21. Dickens MJ, Romero LM (2013) A consensus endocrine profile for chronically stressed wild animals does not exist. Gen Comp Endocrinol 191:177–189

    Article  CAS  PubMed  Google Scholar 

  22. Dormann CF et al (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46. https://doi.org/10.1111/j.1600-0587.2012.07348.x

    Article  Google Scholar 

  23. Frigerio D, Dittami J, Mostl E, Kotrschal K (2004) Excreted corticosterone metabolites co-vary with ambient temperature and air pressure in male Greylag geese (Anser anser). Gen Comp Endocrinol 137:29–36. https://doi.org/10.1016/j.ygcen.2004.02.013

    Article  CAS  PubMed  Google Scholar 

  24. Gallagher AJ, Creel S, Wilson RP, Cooke SJ (2017) Energy landscapes and the landscape of fear. Trends Ecol Evol 32:88–96. https://doi.org/10.1016/j.tree.2016.10.010

    Article  PubMed  Google Scholar 

  25. Geiser F (2013) Hibernation. Curr Biol 23:R188–R193. https://doi.org/10.1016/j.cub.2013.01.062

    Article  CAS  PubMed  Google Scholar 

  26. Goymann W (2012) On the use of non-invasive hormone research in uncontrolled, natural environments: the problem with sex, diet, metabolic rate, and the individual. Methods Ecol Evol 3:757–765

    Article  Google Scholar 

  27. Gullion GW (1965) Improvements in methods for trapping and marking ruffed grouse. J Wildl Manag 29:109–116

    Article  Google Scholar 

  28. Gullion GW (1970) Factors affecting ruffed grouse populations in boreal forests of northern Minnesota, USA. Finn Game Res 30:103–117

    Google Scholar 

  29. Hahn TP, Sockman KW, Breuner CW, Morton ML (2004) Facultative altitudinal movements by mountain white-crowned sparrows (Zonotrichia leucophrys oriantha) in the Sierra Nevada. Auk 121:1269–1281. https://doi.org/10.1642/0004-8038(2004)121%5b1269:fambmw%5d2.0.co;2

    Article  Google Scholar 

  30. Hale JB, Wendt RF, Halazon GC (1954) Sex and age criteria for Wisconsin ruffed grouse. Wisconsin Conservation Department, Madison, Technical bulletin 9

  31. Hansen BB, Aanes R, Herfindal I, Kohler J, Saether BE (2011) Climate, icing, and wild arctic reindeer: past relationships and future prospects. Ecology 92:1917–1923. https://doi.org/10.1890/11-0095.1

    Article  PubMed  Google Scholar 

  32. Heinrich B (2017) Winter strategies of ruffed grouse in a mixed northern forest. Northeast Nat 24:B55–B71

    Article  Google Scholar 

  33. Humphries MM et al (2005) Expenditure freeze: the metabolic response of small mammals to cold environments. Ecol Lett 8:1326–1333. https://doi.org/10.1111/j.1461-0248.2005.00839.x

    Article  Google Scholar 

  34. Jimeno B, Hau M, Verhulst S (2018) Corticosterone levels reflect variation in metabolic rate, independent of ‘stress’. Sci Rep 8:1–8

    Article  CAS  Google Scholar 

  35. Kearney M, Shine R, Porter WP (2009) The potential for behavioral thermoregulation to buffer “cold-blooded” animals against climate warming. Proc Natl Acad Sci USA 106:3835–3840. https://doi.org/10.1073/pnas.0808913106

    Article  PubMed  Google Scholar 

  36. Khan MZ, Altmann J, Isani SS, Yu J (2002) A matter of time: evaluating the storage of fecal samples for steroid analysis. Gen Comp Endocrinol 128:57–64

    Article  CAS  PubMed  Google Scholar 

  37. Krasting JP, Broccoli AJ, Dixon KW, Lanzante JR (2013) Future changes in northern hemisphere snowfall. J Clim 26:7813–7828. https://doi.org/10.1175/jcli-d-12-00832.1

    Article  Google Scholar 

  38. Landys MM, Ramenofsky M, Wingfield JC (2006) Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. Gen Comp Endocrinol 148:132–149. https://doi.org/10.1016/j.ygcen.2006.02.013

    Article  CAS  PubMed  Google Scholar 

  39. Lorenz DJ et al (2009) Wisconsin’s changing climate: temperature. Understanding climate change: climate variability, predictability, and change in the midwestern United States. Indiana University Press, Bloomington, p 11

    Google Scholar 

  40. MacLeod KJ, Krebs CJ, Boonstra R, Sheriff MJ (2018a) Fear and lethality in snowshoe hares: the deadly effects of non-consumptive predation risk. Oikos 127:375–380. https://doi.org/10.1111/oik.04890

    Article  Google Scholar 

  41. MacLeod KJ, Sheriff MJ, Ensminger DC, Owen DAS, Langkilde T (2018b) Survival and reproductive costs of repeated acute glucocorticoid elevations in a captive, wild animal. Gen Comp Endocrinol 268:1–6

    Article  CAS  PubMed  Google Scholar 

  42. Marjakangas A (1986) On the winter ecology of the black grouse, Tetrao tetrix, in central Finland. Acta Universitatis Ouluensis, Series A Scientiae Rerum Naturalium No 183, Biologica No 29. ISBN: 951-42-2269-5

  43. Marjakangas A, Rintamaki H, Hissa R (1984) Thermal responses in the capercaillie Tetrao urogallus and the black grouse Lyrurus tetrix roosting in the snow. Physiol Zool 57:99–104. https://doi.org/10.1086/physzool.57.1.30155972

    Article  Google Scholar 

  44. Marra PP, Holberton RL (1998) Corticosterone levels as indicators of habitat quality: effects of habitat segregation in a migratory bird during the non-breeding season. Oecologia 116:284–292. https://doi.org/10.1007/s004420050590

    Article  PubMed  Google Scholar 

  45. Mellander PE, Lofvenius MO, Laudon H (2007) Climate change impact on snow and soil temperature in boreal Scots pine stands. Clim Chang 85:179–193. https://doi.org/10.1007/s10584-007-9254-3

    Article  CAS  Google Scholar 

  46. Mills LS, Zimova M, Oyler J, Running S, Abatzoglou JT, Lukacs PM (2013) Camouflage mismatch in seasonal coat color due to decreased snow duration (vol 110, pg 7360, 2013). Proc Natl Acad Sci USA 110:11660. https://doi.org/10.1073/pnas.1310823110

    CAS  Article  Google Scholar 

  47. Millspaugh JJ, Washburn BE (2004) Use of fecal glucocorticold metabolite measures in conservation biology research: considerations for application and interpretation. Gen Comp Endocrinol 138:189–199. https://doi.org/10.1016/j.ygcen.2004.07.002

    Article  CAS  PubMed  Google Scholar 

  48. Millspaugh JJ, Washburn BE, Milanick MA, Slotow R, van Dyk G (2003) Effects of heat and chemical treatments on fecal glucocorticoid measurements: implications for sample transport. Wildl Soc Bull 31:399–406

    Google Scholar 

  49. Montgomerie R, Lyon B, Holder K (2001) Dirty ptarmigan: behavioral modification of conspicuous male plumage. Behav Ecol 12:429–438. https://doi.org/10.1093/beheco/12.4.429

    Article  Google Scholar 

  50. Nagra CL, Meyer RK, Breitenbach RP (1963) Influence of hormones on food intake and lipid deposition in castrated pheasants. Poult Sci 42:770. https://doi.org/10.3382/ps.0420770

    Article  Google Scholar 

  51. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  52. Notaro M, Lorenz DJ, Vimont D, Vavrus S, Kucharik C, Franz K (2011) 21st century Wisconsin snow projections based on an operational snow model driven by statistically downscaled climate data. Int J Climatol 31:1615–1633. https://doi.org/10.1002/joc.2179

    Article  Google Scholar 

  53. Notaro M, Lorenz D, Hoving C, Schummer M (2014) Twenty-first-century projections of snowfall and winter severity across central–eastern north America. J Clim 27:6526–6550. https://doi.org/10.1175/jcli-d-13-00520.1

    Article  Google Scholar 

  54. Pauli JN, Zuckerberg B, Whiteman JP, Porter W (2013) The subnivium: a deteriorating seasonal refugium. Front Ecol Environ 11:260–267. https://doi.org/10.1890/120222

    Article  Google Scholar 

  55. Pokallus JW, Pauli JN (2016) Predation shapes the movement of a well-defended species, the North American porcupine, even when nutritionally stressed. Behav Ecol 27:470–475. https://doi.org/10.1093/beheco/arv176

    Article  Google Scholar 

  56. Pomara LY, Zuckerberg B (2017) Climate variability drives population cycling and synchrony. Divers Distrib 23:421–434. https://doi.org/10.1111/ddi.12540

    Article  Google Scholar 

  57. Post ES (2013) Ecology of climate change: the importance of biotic interactions. Princeton University Press, Princeton

    Book  Google Scholar 

  58. Randall DJ, Burgren W, French K (2000) Eckert animal physiology: mechanisms and adaptations, 4th edn. W.H. Freeman and Company, New York

    Google Scholar 

  59. Rasmussen G, Brander R (1973) Standard metabolic rate and lower critical temperature for ruffed grouse. Wilson Bulletin 85:223–229

    Google Scholar 

  60. Roche DG, Careau V, Binning SA (2016) Demystifiying animal ‘personality’ (or not): why individual variation matters to experimental biologists. J Exp Biol 219:3832–3843

    Article  PubMed  Google Scholar 

  61. Rohr JR, Civitello DJ, Cohen JM, Roznik EA, Sinervo B, Dell AI (2018) The complex drivers of thermal acclimation and breadth in ectotherms. Ecol Lett 21:1425–1439

    Article  Google Scholar 

  62. Romero LM, Wikelski M (2001) Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Nino events. Proc Natl Acad Sci USA 98:7366–7370. https://doi.org/10.1073/pnas.131091498

    Article  CAS  PubMed  Google Scholar 

  63. Romero LM, Dickens MJ, Cyr NE (2009) The reactive scope model—a new model integrating homeostasis, allostasis, and stress. Horm Behav 55:375–389

    Article  PubMed  Google Scholar 

  64. Rusch DH, Destefano L, Reynolds MC, Lauten D (2000) Ruffed grouse (Bonasa umbellus). In: Poole A (ed) The birds of North America online, vol 515. Cornell lab of Ornithology, Ithaca

    Google Scholar 

  65. Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89. https://doi.org/10.1210/er.21.1.55

    CAS  Article  Google Scholar 

  66. Scheiber IBR, de Jong ME, Komdeur J, Pschernig E, Loonen MJJE (2017) Diel pattern of corticosterone metabolites in Arctic barnacle goslings (Branta leucopsis) under continuous natural light. PLoS One 12:1–17

    Article  CAS  Google Scholar 

  67. Sheriff MJ, Thaler JS (2014) Ecophysiological effects of predation risk; an integration across disciplines. Oecologia 176:607–611. https://doi.org/10.1007/s00442-014-3105-5

    Article  PubMed  Google Scholar 

  68. Sheriff MJ, Bosson CO, Krebs CJ, Boonstra R (2009a) A non-invasive technique for analyzing fecal cortisol metabolites in snowshoe hares (Lepus americanus). J Comp Physiol B 179:305–313

    Article  CAS  PubMed  Google Scholar 

  69. Sheriff MJ, Krebs CJ, Boonstra R (2009b) The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares. J Anim Ecol 78:1249–1258. https://doi.org/10.1111/j.1365-2656.2009.01552.x

    Article  PubMed  Google Scholar 

  70. Sheriff MJ, Kuchel L, Boutin S, Humphries MM (2009c) Seasonal metabolic acclimatization in a northern population of free-ranging snowshoe hares, Lepus americanus. J Mammal 90:761–767. https://doi.org/10.1644/08-mamm-a-247r.1

    Article  Google Scholar 

  71. Sheriff MJ, Speakman JR, Kuchel L, Boutin S, Humphries MM (2009d) The cold shoulder: free-ranging snowshoe hares maintain a low cost of living in cold climates. Can J Zool 87:956–964. https://doi.org/10.1139/z09-087

    Article  Google Scholar 

  72. Sheriff MJ, Krebs CJ, Boonstra R (2010) Assessing stress in animal populations: do fecal and plasma glucocorticoids tell the same story? Gen Comp Endocrinol 166:614–619. https://doi.org/10.1016/j.ygcen.2009.12.017

    Article  CAS  PubMed  Google Scholar 

  73. Sheriff MJ, Dantzer B, Delehanty B, Palme R, Boonstra R (2011a) Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166:869–887

    Article  PubMed  Google Scholar 

  74. Sheriff MJ et al (2011b) Phenological variation in annual timing of hibernation and breeding in nearby populations of Arctic ground squirrels. Proc R Soc B Biol Sci 278:2369–2375. https://doi.org/10.1098/rspb.2010.2482

    Article  Google Scholar 

  75. Sheriff MJ, Boonstra R, Palme R, Buck CL, Barnes BM (2017) Coping with differences in snow cover: the impact on the condition, physiology and fitness of an arctic hibernator. Conserv Physiol. https://doi.org/10.1093/conphys/cox065

    Article  PubMed  PubMed Central  Google Scholar 

  76. Sinclair BJ, Stinziano JR, Williams CM, MacMillan HA, Marshall KE, Storey KB (2013) Real-time measurement of metabolic rate during freezing and thawing of the wood frog, Rana sylvatica: implications for overwinter energy use. J Exp Biol 216:292–302. https://doi.org/10.1242/jeb.076331

    Article  CAS  PubMed  Google Scholar 

  77. Sinha T, Cherkauer KA (2010) Impacts of future climate change on soil frost in the midwestern United States. J Geophys Res Atmos. https://doi.org/10.1029/2009jd012188

    Article  Google Scholar 

  78. Small RJ, Holzwart JC, Rusch DH (1991) Predation and hunting mortality of ruffed grouse in central Wisconsin. J Wildl Manag 55:512–520. https://doi.org/10.2307/3808983

    Article  Google Scholar 

  79. Smith CC, Reichman OJ (1984) The evolution of food caching by birds and mammals. Annu Rev Ecol Syst 15:329–351. https://doi.org/10.1146/annurev.es.15.110184.001553

    Article  Google Scholar 

  80. Snell-Rood EC (2013) An overview of the evolutionary causes and consequences of behavioural plasticity. Anim Behav 85:1004–1011. https://doi.org/10.1016/j.anbehav.2012.12.031

    Article  Google Scholar 

  81. Somveille M, Rodrigues ASL, Manica A (2015) Why do birds migrate? A macroecological perspective. Glob Ecol Biogeogr 24:664–674. https://doi.org/10.1111/geb.12298

    Article  Google Scholar 

  82. Sultaire SM, Pauli JN, Martin KJ, Meyer MW, Notaro M, Zuckerberg B (2016) Climate change surpasses land-use change in the contracting range boundary of a winter-adapted mammal. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2015.3104

    Article  Google Scholar 

  83. Thierry AM, Massemin S, Handrich Y, Raclot T (2013) Elevated corticosterone levels and severe weather conditions decrease parental investment of incubating Adelie penguins. Horm Behav 63:475–483. https://doi.org/10.1016/j.yhbeh.2012.12.011

    Article  CAS  Google Scholar 

  84. Thomas VG (1987) Similar winter energy strategies of grouse, hares and rabbits in northern biomes. Oikos 50:206–212. https://doi.org/10.2307/3566002

    Article  Google Scholar 

  85. Thompson FR, Fritzell EK (1988a) Ruffed grouse metabolic rate and temperature cycles. J Wildl Manag 52:450–453

    Article  Google Scholar 

  86. Thompson FR, Fritzell EK (1988b) Ruffed grouse winter roost site preference and influence on energy demands. J Wildl Manag 52:454–460

    Article  Google Scholar 

  87. Thompson FR, Fritzell EK (1989) Habitat use, home range, and survival of territorial male ruffed grouse. J Wildl Manag 53:15–21

    Article  Google Scholar 

  88. Touma C, Sachser N, Möstl E, Palme R (2003) Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. Gen Comp Endocrinol 130:267–278

    Article  CAS  PubMed  Google Scholar 

  89. Vaughan DG et al (2013) Observations: cryosphere. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (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

    Google Scholar 

  90. Washburn BE, Millspaugh JJ (2002) Effects of simulated environmental conditions on glucocorticoid metabolite measurements in white-tailed deer feces. Gen Comp Endocrinol 127:217–222

    Article  CAS  PubMed  Google Scholar 

  91. Wasser SK, Monfort SL, Southers J, Wildt DE (1994) Excretion rates and metabolites of oestradiol and progesterone in baboon (Papio cynocephalus cynocephalus) faeces. J Reprod Fertil 101:213–220

    Article  CAS  PubMed  Google Scholar 

  92. Wasser SK et al (2000) A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Gen Comp Endocrinol 120:260–275. https://doi.org/10.1006/gcen.2000.7557

    Article  CAS  PubMed  Google Scholar 

  93. Williams CT, Gorrell JC, Lane JE, McAdam AG, Humphries MM, Boutin S (2013) Communal nesting in an ‘asocial’ mammal: social thermoregulation among spatially dispersed kin. Behav Ecol Sociobiol 67:757–763. https://doi.org/10.1007/s00265-013-1499-4

    Article  Google Scholar 

  94. Williams CM, Henry HAL, Sinclair BJ (2015) Cold truths: how winter drives responses of terrestrial organisms to climate change. Biol Rev 90:214–235. https://doi.org/10.1111/brv.12105

    Article  PubMed  Google Scholar 

  95. Wilson EC, Shipley AA, Zuckerberg B, Peery MZ, Pauli JN (2018) An experimental translocation identifies habitat features that buffer camouflage mismatch in snowshoe hares. Conserv Lett. https://doi.org/10.1111/conl.12614

    Article  Google Scholar 

  96. Wingfield JC, Ramenofsky M (1999) Hormones and the behavioral ecology of stress. In: Balm PHM (ed) Stress physiology in animals. CRC Press, Boca Raton, pp 1–51

    Google Scholar 

  97. Wingfield JC, Moore MC, Farner DS (1983) Endocrine responses to inclement weather in naturally breeding populations of white-crowned sparrows (Zonotrichia leucophrys pugetensis). Auk 100:56–62

    Google Scholar 

  98. Wingfield JC et al (1998) Ecological bases of hormone-behavior interactions: the “emergency life history stage”. Am Zool 38:191–206

    Article  CAS  Google Scholar 

  99. Zimmerman GS, Millspaugh JJ, Link WA, Woods RJ, Gutierrez RJ (2013) A flexible Bayesian hierarchical approach for analyzing spatial and temporal variation in the fecal corticosterone levels in birds when there is imperfect knowledge of individual identity. Gen Comp Endocrinol 194:64–70. https://doi.org/10.1016/j.ygcen.2013.08.010

    Article  CAS  PubMed  Google Scholar 

  100. Zimova M, Mills LS, Nowak JJ (2016) High fitness costs of climate change-induced camouflage mismatch. Ecol Lett 19:299–307. https://doi.org/10.1111/ele.12568

    Article  PubMed  Google Scholar 

  101. Zuckerberg B, Pauli JN (2018) Conserving and managing the subnivium. Conserv Biol 32:774–781

    Article  PubMed  Google Scholar 

  102. Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgements

We are grateful to the Ruffed Grouse Society for funding, and the Wisconsin Department of Natural Resources for funding and logistical assistance. The Merrill and Emita Hastings Foundation and the University of Wisconsin-Madison Department of Forest and Wildlife Ecology provided additional support. This material is based upon work supported by the National Institute of Food and Agriculture, United States Department of Agriculture, Hatch Projects 1006604 and 1003605. We would like to thank the staff at Sandhill Wildlife Area for their support and logistical assistance. We thank B. Heindl, A. Walker, K. Kovach, T. Gettelman, A. Elzinga, J. Ostroski, A. Bradley, A. Wilkie, and E. Leicht for many hours collecting data.

Author information

Affiliations

Authors

Contributions

BZ and AAS conceived and designed the study, conducted statistical analyses, and drafted initial versions of the manuscript. AAS collected field data, carried out hormone assays, and led manuscript development. MJS coordinated hormone analysis. JNP provided input on conceptual development. All authors contributed to writing the manuscript and gave final approval for publication.

Corresponding author

Correspondence to Amy A. Shipley.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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

Additional information

We demonstrate how the behavioral adaptations of overwintering species can reduce physiological stress, but that the loss of snow cover in the face of a changing climate may stretch the limits of behavioral flexibility. This is one of the first studies to explore how variable winter weather conditions influence the stress hormones of a free-living, cold-adapted vertebrate and its ability to mediate this relationship through behavioral flexibility.

Communicated by Pawel Koteja.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 18157 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Shipley, A.A., Sheriff, M.J., Pauli, J.N. et al. Snow roosting reduces temperature-associated stress in a wintering bird. Oecologia 190, 309–321 (2019). https://doi.org/10.1007/s00442-019-04389-x

Download citation

Keywords

  • Behavioral plasticity
  • Climate change
  • Ruffed grouse
  • Fecal corticosterone metabolites
  • Winter