Skip to main content
SpringerLink
Log in

Weather and land cover create a predictable “stress-scape” for a winter-adapted bird

  • Research Article
  • Published:
Landscape Ecology Aims and scope Submit manuscript

Abstract

Context

Variability in temperature and snow cover are characteristics of high-latitude environments that impose significant pressures on overwintering species. To cope with increased energetic demands and decreased resources, species occupying seasonal environments often seek out refugia that buffer them from inclement conditions. Ruffed grouse (Bonasa umbellus) roosting in the thermally stable microhabitat beneath deep snow are buffered from negative effects of cold temperatures on physiological stress (glucocorticoid hormone levels).

Objective

Despite physiological advantages of accessing warmer refugia during winter, it is unknown how land cover and winter climate promote the occurrence of such refugia over space and time. Analogous to the landscape of fear, which mediates how prey navigate spatial variation in predation risk, mapping a landscape of stress, or stress-scape, may identify hotspots where metabolic challenges persist.

Methods

We assayed droppings for fecal corticosterone metabolites (FCMs) collected from radio-tagged ruffed grouse over three winters and developed a spatial model of FCM concentrations across the extent of our study area, thus quantifying a stress-scape.

Results

FCMs increased with shallower snow depths, less dense snow, colder ambient temperatures, and more open habitat. However, despite considerable spatiotemporal variation in snow depth, snow density, and temperature, the regions across the landscape where grouse had elevated FCM levels were consistent and predictable across years.

Conclusions

Stress-scapes offer a new tool for understanding and quantifying indirect effects of stressors and can identify areas of the landscape where there may be consistent hotspots of stress that are the result of multiple ecological and environmental challenges.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

Data associated with this manuscript are available via Dryad: https://doi.org/10.5061/dryad.t4b8gtj3h.

References

  • Ames EM, Gade MR, Nieman CL et al (2020) Striving for population-level conservation: integrating physiology across the biological hierarchy. Conservation Physiology 8:1–17

    Google Scholar 

  • Arthur SM, Manly BFJ, McDonald LL, Garner GW (1996) Assessing habitat selection when availability changes. Ecology 77(1):215–227

    Google Scholar 

  • Astheimer LB, Buttemer WA, Wingfield JC (1992) Interactions of corticosterone with feeding, activity and metabolism in passerine birds. Ornis Scand 23(3):355–365

    Google Scholar 

  • Astheimer LB, Buttemer WA, Wingfield JC (2000) Corticosterone treatment has no effect on reproductive hormones or aggressive behavior in free-living male tree sparrows, Spizella arborea. Hormones and Behavior 37(1):31–39

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Bateman BL, Pidgeon AM, Radeloff VC et al (2016) Potential breeding distributions of US birds predicted with both short-term variability and long-term average climate data. Ecol Appl 26(8):2718–2729

    PubMed  Google Scholar 

  • Bateman BL, VanDerWal J, Johnson CN (2012) Nice weather for bettongs: using weather events, not climate means, in species distribution models. Ecography 35(4):306–314

    Google Scholar 

  • Blanchette P, Bourgeois JC, St-Onge S (2007) Winter selection of roost sites by ruffed grouse during daytime in mixed nordic-temperate forests, Quebec, Canada. Can J Zool 85(4):497–504

    Google Scholar 

  • Bump GR, Darrow RW, Edminster FC, Crissey WF (1947) The Ruffed Grouse: Life History, Propagation, and Management. New York State Conservation Department Buffalo NY

  • Busch DS, Sperry TS, Peterson E, Do CT, Wingfield JC, Boyd EH (2008) Impacts of frequent, acute pulses of corticosterone on condition and behavior of Gambel’s white-crowned sparrow (Zonotrichia leucophtys gambelii). Gen Comp Endocrinol 158(3):224–233

    CAS  PubMed  Google Scholar 

  • Campomizzi AJ, Butcher JA, Farrell SL et al (2008) Conspecific attraction is a missing component in wildlife habitat modeling. J Wildl Manag 72(1):331–336

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Cooke SJ, O’Connor CM (2010) Making conservation physiology relevant to policy makers and conservation practitioners. Conserv Lett 3(3):159–166

    Google Scholar 

  • Cooke SJ, Suski CD (2008) Ecological restoration and physiology: an overdue integration. Bioscience 58(10):957–968

    Google Scholar 

  • Da Silveira NS, Niebuhr BBS, Muylaert RD, Ribeiro MC, Pizo MA (2016) Effects of land cover on the movement of frugivorous birds in a heterogeneous landscape. PLoS ONE 11(6):19

    Google Scholar 

  • 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? Conservation Physiol 2(1):23

    Google Scholar 

  • de Bruijn R, Romero LM (2018) The role of glucocorticoids in the vertebrate response to weather. Gen Comp Endocrinol 269:11–32

    PubMed  Google Scholar 

  • Dormann CF, Elith J, Bacher S et al (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36(1):27–46

    Google Scholar 

  • Fletcher RJ (2006) Emergent properties of conspecific attraction in fragmented landscapes. Am Nat 168(2):207–219

    PubMed  Google Scholar 

  • Gaynor KM, Brown JS, Middleton AD, Power ME, Brashares JS (2019) Landscapes of fear: spatial patterns of risk perception and response. Trends Ecol Evol 34(4):355–368

    PubMed  Google Scholar 

  • George AD, Connette GM, Thompson FR, Faaborg J (2017) Resource selection by an ectothermic predator in a dynamic thermal landscape. Ecol Evol 7(22):9557–9566

    PubMed  PubMed Central  Google Scholar 

  • Gigliotti LC, Diefenbach DR, Sheriff MJ (2017) Geographic variation in winter adaptations of snowshoe hares (Lepus americanus). Can J Zool 95(8):539–545

    Google Scholar 

  • Gullion GW (1965) Improvements in methods for trapping and marking Ruffed Grouse. J Wildl Manag 29:109–116

    Google Scholar 

  • Gullion GW (1970) Factors affecting Ruffed Grouse populations in boreal forests of northern Minnesota, USA. Finnish Game Research 30:103–117

    Google Scholar 

  • Hale JB, Wendt RF, Halazon GC (1954) Sex and age criteria for Wisconsin Ruffed Grouse. Wisconsin Conservation Department Technical Bulletin 9:24

    Google Scholar 

  • Hebblewhite M, Merrill EH, McDonald TL (2005) Spatial decomposition of predation risk using resource selection functions: an example in a wolf-elk predator-prey system. Oikos 111(1):101–111

    Google Scholar 

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

    Google Scholar 

  • Hengl T, Heuvelink GBM, Rossiter DG (2007) About regression-kriging: From equations to case studies. Comput Geosci 33(10):1301–1315

    Google Scholar 

  • Hohn EO (1977) Snowshoe effect of feathering on ptarmigan feet. Condor 79(3):380–382

    Google Scholar 

  • Hunninck L, May R, Jackson CR, Palme R, Roskaft E, Sheriff MJ (2020) Consequences of climate-induced vegetation changes exceed those of human disturbance for wild impala in the Serengeti ecosystem. Conservation Physiol 8:14

    Google Scholar 

  • Jachowski DS, Kauffman MJ, Jesmer BR, Sawyer H, Millspaugh JJ (2018) Integrating physiological stress into the movement ecology of migratory ungulates: a spatial analysis with mule deer. Conservation Physiol 6:12

    Google Scholar 

  • Jimeno B, Hau M, Verhulst S (2018) Corticosterone levels reflect variation in metabolic rate, independent of “stress.” Sci Rep 8(13020):1–8

    CAS  Google Scholar 

  • Johnson CJ, Seip DR, Boyce MS (2004) A quantitative approach to conservation planning: using resource selection functions to map the distribution of mountain caribou at multiple spatial scales. J Appl Ecol 41(2):238–251

    Google Scholar 

  • Kalinski A, Banbura M, Gladalski M et al (2014) Landscape patterns of variation in blood glucose concentration of nestling blue tits (Cyanistes caeruleus). Landscape Ecol 29(9):1521–1530

    Google Scholar 

  • Kittle AM, Fryxell JM, Desy GE, Hamr J (2008) The scale-dependent impact of wolf predation risk on resource selection by three sympatric ungulates. Oecologia 157(1):163–175

    PubMed  Google Scholar 

  • Kohl MT, Stahler DR, Metz MC et al (2018) Diel predator activity drives a dynamic landscape of fear. Ecol Monogr 88(4):638–652

    Google Scholar 

  • Kordosky JR, Gese EM, Thompson CM et al (2021) Landscape of stress: tree mortality influences physiological stress and survival in a native mesocarnivore. PLoS ONE 16(7):e0253604

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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(2):132–149

    CAS  PubMed  Google Scholar 

  • Latimer CE, Zuckerberg B (2019) How extreme is extreme? Demographic approaches inform the occurrence and ecological relevance of extreme events. Ecol Monogr 89(4):15

    Google Scholar 

  • Laundre JW, Hernandez L, Altendorf KB (2001) Wolves, elk, and bison: reestablishing the “landscape of fear” in Yellowstone National Park, USA. Can J Zool 79(8):1401–1409

    Google Scholar 

  • Leblond M, Dussault C, Ouellet JP (2013) Impacts of human disturbance on large prey species: do behavioral reactions translate to fitness consequences? PLoS ONE 8(9):9

    Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68(4):619–640

    Google Scholar 

  • MacDougall-Shackleton SA, Bonier F, Romero LM, Moore IT (2019) Glucocorticoids and “Stress” Are Not Synonymous COMMENT. Integrative Organismal Biol 1(1):8

    Google Scholar 

  • MacLeod KJ, Krebs CJ, Boonstra R, Sheriff MJ (2018) Fear and lethality in snowshoe hares: the deadly effects of non-consumptive predation risk. Oikos 127(3):375–380

    Google Scholar 

  • Madliger CL, Cooke SJ, Crespi EJ et al (2016) Success stories and emerging themes in conservation physiology. Conservation Physiology 4:17

    Google Scholar 

  • Madliger CL, Love OP (2015) The power of physiology in changing landscapes: considerations for the continued integration of conservation and physiology. Integr Comp Biol 55(4):545–553

    PubMed  Google Scholar 

  • 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(1–2):284–292

    PubMed  Google Scholar 

  • McCann NP, Zollner PA, Gilbert JH (2017) Temporal scaling in analysis of animal activity. Ecography 40(12):1436–1444

    Google Scholar 

  • Millspaugh JJ, Washburn BE (2004) Use of fecal glucocorticold metabolite measures in conservation biology research: considerations for application and interpretation. Gen Comp Endocrinol 138(3):189–199

    CAS  PubMed  Google Scholar 

  • Mohlman JL, Navara KJ, Sheriff MJ, Terhune TM II, Martin JA (2020) Validation of a noninvasive technique to quantify stress in northern bobwhite (Colinus virginianus). Conservation Physiology 8(1):coaa026

    PubMed  PubMed Central  Google Scholar 

  • Morelli TL, Daly C, Dobrowski SZ et al (2016) Managing climate change refugia for climate adaptation. PLoS ONE 11(8):17

    Google Scholar 

  • Mosser AA, Avgar T, Brown GS, Walker CS, Fryxell JM (2014) Towards an energetic landscape: broad-scale accelerometry in woodland caribou. J Anim Ecol 83(4):916–922

    PubMed  Google Scholar 

  • Mysterud A, Ostbye E (1999) Cover as a habitat element for temperate ungulates: effects on habitat selection and demography. Wildl Soc Bull 27(2):385–394

    Google Scholar 

  • Nagra CL, Meyer RK, Breitenbach RP (1963) Influence of hormones on food intake and lipid deposition in castrated pheasants. Poult Sci 42(3):770–775

    Google Scholar 

  • Pauli JN, Zuckerberg B, Whiteman JP, Porter W (2013) The subnivium: a deteriorating seasonal refugium. Front Ecol Environ 11(5):260–267

    Google Scholar 

  • 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(2):470–475

    Google Scholar 

  • Preisler HK, Ager AA, Wisdom MJ (2006) Statistical methods for analysing responses of wildlife to human disturbance. J Appl Ecol 43(1):164–172

    Google Scholar 

  • Romero LM, Wikelski M (2001) Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Nino events. Proc Natl Acad Sci USA 98(13):7366–7370

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rosalino LM, Macdonald DW, Santos-Reis M (2004) Spatial structure and land-cover use in a low-density Mediterranean population of Eurasian badgers. Can J Zool 82(9):1493–1502

    Google Scholar 

  • Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21(1):55–89

    CAS  PubMed  Google Scholar 

  • 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(8):1–17

    Google Scholar 

  • Shepard ELC, Wilson RP, Rees WG, Grundy E, Lambertucci SA, Vosper SB (2013) Energy landscapes shape animal movement ecology. Am Nat 182(3):298–312

    PubMed  Google Scholar 

  • 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. Conservation Physiology. https://doi.org/10.1093/conphys/cox065

    Article  PubMed  PubMed Central  Google Scholar 

  • 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(3):305–313

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Sheriff MJ, Krebs CJ, Boonstra R (2009b) The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares. J Anim Ecol 78(6):1249–1258

    PubMed  Google Scholar 

  • 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(3):614–619

    CAS  PubMed  Google Scholar 

  • Sheriff MJ, Thaler JS (2014) Ecophysiological effects of predation risk; an integration across disciplines. Oecologia 176(3):607–611

    PubMed  Google Scholar 

  • Shipley AA (2021) Changing Winters: The Effects of Snow and Land Cover on the Behavior, Physiology, and Survival of Ruffed Grouse. The University of Wisconsin - Madison, Ph.D.

    Google Scholar 

  • Shipley AA, Cruz J, Zuckerberg B (2020) Personality differences in the selection of dynamic refugia have demographic consequences for a winter-adapted bird. Proceed Royal Soc B-Biol Sci 287(1934):10

    Google Scholar 

  • Shipley AA, Sheriff MJ, Pauli JN, Zuckerberg B (2019) Snow roosting reduces temperature-associated stress in a wintering bird. Oecologia 190(2):309–321

    PubMed  Google Scholar 

  • Squires JR, DeCesare NJ, Olson LE, Kolbe JA, Hebblewhite M, Parks SA (2013) Combining resource selection and movement behavior to predict corridors for Canada lynx at their southern range periphery. Biol Cons 157:187–195

    Google Scholar 

  • Stabach JA, Wittemyer G, Boone RB, Reid RS, Worden JS (2016) Variation in habitat selection by white-bearded wildebeest across different degrees of human disturbance. Ecosphere 7(8):17

    Google Scholar 

  • Thomas VG (1987) Similar winter energy strategies of grouse, hares and rabbits in northern biomes. Oikos 50(2):206–212

    Google Scholar 

  • Thompson FR, Fritzell EK (1988) Ruffed Grouse winter roost site preference and influence on energy demands. J Wildl Manag 52(3):454–460

    Google Scholar 

  • Thompson KL, Zuckerberg B, Porter WP, Pauli JN (2018) The phenology of the subnivium. Environ Res Lett 13(6):12

    Google Scholar 

  • Thompson KL, Zuckerberg B, Porter WP, Pauli JN (2021) The decline of a hidden and expansive microhabitat: the subnivium. Front Ecol Environ 19:268–273

    Google Scholar 

  • Wasser SK, Hunt KE, Brown JL et al (2000) A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Gen Comp Endocrinol 120(3):260–275

    CAS  PubMed  Google Scholar 

  • Westerskov K (1965) Winter ecology of the partridge (Perdix perdix) in the Canadian prairie. Proc NZ Ecol Soc 12:23–30

    Google Scholar 

  • Wikelski M, Cooke SJ (2006) Conservation physiology. Trends Ecol Evol 21(1):38–46

    PubMed  Google Scholar 

  • 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 

  • Wingfield JC, Maney DL, Breuner CW et al (1998) Ecological bases of hormone-behavior interactions: The “emergency life history stage.” Am Zool 38(1):191–206

    CAS  Google Scholar 

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

    Google Scholar 

  • Wolff JO (1980) The role of habitat patchiness in the population-dynamics of snowshoe hares. Ecol Monogr 50(1):111–130

    Google Scholar 

  • Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J Royal Statist Soc Series B-Statist Methodol 73:3–36

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

Download references

Acknowledgements

We are grateful to the Ruffed Grouse Society for funding, and the Wisconsin Department of Natural Resources for logistical assistance and additional funding. The Merrill and Emita Hastings Foundation and the University of Wisconsin-Madison Department of Forest and Wildlife Ecology provided additional support. This study is based on work funded 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 field data. We also thank D. Ensminger, C. Pritchard, L.S. McKay, A. Giordano, and B. Hayden for assistance preparing fecal samples for analysis.

Funding

This study was funded by the National Institute of Food and Agriculture, United States Department of Agriculture, Hatch Projects 1006604 and 1003605. This study was also partially funded by the Wisconsin Department of Natural Resources, the Ruffed Grouse Society, and the University of Wisconsin-Madison Departmetn of Forest and Widlife Ecology. Additional support was received from the Merrill and Emita Hastings Foundation.

Author information

Authors and Affiliations

  1. Department of Forest and Wildlife Ecology, University of Wisconsin-Madison, 1630 Linden Dr, Madison, WI, 53706, USA

    Amy A. Shipley, Jonathan N. Pauli & Benjamin Zuckerberg

  2. School of Natural Resources, University of Missouri, 103 Anheuser-Busch Natural Resources Building, Columbia, MO, 65211, USA

    Amy A. Shipley

  3. Biology Department, University of Massachusetts Dartmouth, 285 Old Westport Rd, Dartmouth, MA, 02747, USA

    Michael J. Sheriff

Authors
  1. Amy A. Shipley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael J. Sheriff
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jonathan N. Pauli
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Benjamin Zuckerberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

BZ, AAS, MJS and JNP conceived and designed the study. AAS and BZ conducted statistical analyses and drafted initial version 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

We declare we have no conflicts of interest or competing interests.

Ethical approval

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

Consent to participate

N/A.

Consent for publication

N/A.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 808 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shipley, A.A., Sheriff, M.J., Pauli, J.N. et al. Weather and land cover create a predictable “stress-scape” for a winter-adapted bird. Landsc Ecol 37, 779–793 (2022). https://doi.org/10.1007/s10980-021-01354-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10980-021-01354-z

Keywords

Search

Navigation