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.
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References
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
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
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
Barton K (2018) MuMIn: multi-model inference. R. package version 1.42.1, https://CRAN.R-project.org/package=MuMIn. Accessed 1 July 2018
Bates D, Machler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
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
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
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
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
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
Breheny P, Burchett W (2017) Visualization of regression models using visreg. R J 9:56–71
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
Bump GR, Darrow RW, Edminster FC, Crissey WF (1947) The Ruffed grouse: life history, propagation, and management. New York State Conservation Department, Buffalo
Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach, 2nd edn. Springer, New York
Cade BS (2015) Model averaging and muddled multimodel inferences. Ecology 96:2370–2382
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
Cooper SJ (2002) Seasonal metabolic acclimatization in mountain chickadees and juniper titmice. Physiol Biochem Zool 75:386–395. https://doi.org/10.1086/342256
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
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
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
Dickens MJ, Romero LM (2013) A consensus endocrine profile for chronically stressed wild animals does not exist. Gen Comp Endocrinol 191:177–189
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
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
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
Geiser F (2013) Hibernation. Curr Biol 23:R188–R193. https://doi.org/10.1016/j.cub.2013.01.062
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
Gullion GW (1965) Improvements in methods for trapping and marking ruffed grouse. J Wildl Manag 29:109–116
Gullion GW (1970) Factors affecting ruffed grouse populations in boreal forests of northern Minnesota, USA. Finn Game Res 30:103–117
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
Hale JB, Wendt RF, Halazon GC (1954) Sex and age criteria for Wisconsin ruffed grouse. Wisconsin Conservation Department, Madison, Technical bulletin 9
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
Heinrich B (2017) Winter strategies of ruffed grouse in a mixed northern forest. Northeast Nat 24:B55–B71
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
Jimeno B, Hau M, Verhulst S (2018) Corticosterone levels reflect variation in metabolic rate, independent of ‘stress’. Sci Rep 8:1–8
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Pomara LY, Zuckerberg B (2017) Climate variability drives population cycling and synchrony. Divers Distrib 23:421–434. https://doi.org/10.1111/ddi.12540
Post ES (2013) Ecology of climate change: the importance of biotic interactions. Princeton University Press, Princeton
Randall DJ, Burgren W, French K (2000) Eckert animal physiology: mechanisms and adaptations, 4th edn. W.H. Freeman and Company, New York
Rasmussen G, Brander R (1973) Standard metabolic rate and lower critical temperature for ruffed grouse. Wilson Bulletin 85:223–229
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
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
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
Romero LM, Dickens MJ, Cyr NE (2009) The reactive scope model—a new model integrating homeostasis, allostasis, and stress. Horm Behav 55:375–389
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
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
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
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
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
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
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
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
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
Sheriff MJ, Dantzer B, Delehanty B, Palme R, Boonstra R (2011a) Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166:869–887
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
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
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
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
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
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
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
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
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
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
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
Thompson FR, Fritzell EK (1988a) Ruffed grouse metabolic rate and temperature cycles. J Wildl Manag 52:450–453
Thompson FR, Fritzell EK (1988b) Ruffed grouse winter roost site preference and influence on energy demands. J Wildl Manag 52:454–460
Thompson FR, Fritzell EK (1989) Habitat use, home range, and survival of territorial male ruffed grouse. J Wildl Manag 53:15–21
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
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
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
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
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
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
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
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
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
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
Wingfield JC et al (1998) Ecological bases of hormone-behavior interactions: the “emergency life history stage”. Am Zool 38:191–206
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
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
Zuckerberg B, Pauli JN (2018) Conserving and managing the subnivium. Conserv Biol 32:774–781
Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York
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.
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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.
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Communicated by Pawel Koteja.
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.
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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
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DOI: https://doi.org/10.1007/s00442-019-04389-x