Oecologia

, Volume 181, Issue 3, pp 709–720 | Cite as

Linking habitat selection to fitness-related traits in herbivores: the role of the energy landscape

  • Ryan A. Long
  • R. T. Bowyer
  • Warren P. Porter
  • Paul Mathewson
  • Kevin L. Monteith
  • Scott L. Findholt
  • Brian L. Dick
  • John G. Kie
Physiological ecology - original research

Abstract

Animals may partially overcome environmental constraints on fitness by behaviorally adjusting their exposure to costs and supplies of energy. Few studies, however, have linked spatiotemporal variation in the energy landscape to behaviorally mediated measures of performance that ostensibly influence individual fitness. We hypothesized that strength of selection by North American elk (Cervus elaphus) for areas that reduced costs of thermoregulation and activity, and increased access to high-quality forage, would influence four energetically mediated traits related to fitness: birth mass of young, nutritional condition of adult females at the onset of winter, change in nutritional condition of females between spring and winter, and neonatal survival. We used a biophysical model to map spatiotemporally explicit costs of thermoregulation and activity experienced by elk in a heterogeneous landscape. We then combined model predictions with data on forage characteristics, animal locations, nutritional condition, and mass and survival of young to evaluate behaviorally mediated effects of the energy landscape on fitness-related traits. During spring, when high-quality forage was abundant, female elk that consistently selected low-cost areas before parturition gave birth to larger young than less-selective individuals, and birth mass had a strong, positive influence on probability of survival. As forage quality declined during autumn, however, lactating females that consistently selected the highest quality forage available accrued more fat and entered winter in better condition than less-selective individuals. Results of our study highlight the importance of understanding the dynamic nature of energy landscapes experienced by free-ranging animals.

Keywords

Behavior Biophysics Energetics Thermoregulation Ingesta-free body fat 

Notes

Acknowledgments

This research was funded by the US Forest Service, the Shikar Safari Club, and Idaho State University. R. Long was supported by a STAR Fellowship from the Environmental Protection Agency, a GK-12 Fellowship from the National Science Foundation, and the American Society of Mammalogists Fellowship in Mammalogy. We are indebted to R. Kennedy, D. Rea, and M. Vavra of the US Forest Service, B. Johnson of the Oregon Department of Fish and Wildlife, and K. Stewart, C. McKee, D. Walsh, and J. Zweifel of the University of Nevada Reno for providing substantial logistical support during the study. We thank K. Aho for assistance with statistical analyses. W. Porter is an author of Niche Mapper, patented software that may be purchased for independent research or commercial use. The authors declare that they have no conflict of interest.

Author contribution statement

R. A. L. conceived of the study; J. G. K., R. A. L., and R. T. B. designed the study; B. L. D., K. L. M., R. A. L., and S. L. F. conducted fieldwork; P. M., R. A. L., and W. P. P. carried out the biophysical modeling; K. L. M. and R. A. L. analyzed the data; and R. A. L. wrote the manuscript; other authors provided editorial advice.

Supplementary material

442_2016_3604_MOESM1_ESM.docx (59 kb)
Supplementary material 1 (DOCX 58 kb)

References

  1. Albon SD, Clutton-Brock TH, Guinness FE (1987) Early development and population dynamics in red deer. II. Density-dependent effects and cohort variation. J Anim Ecol 56:69–81CrossRefGoogle Scholar
  2. Arnold TW (2010) Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Manage 74:1175–1178CrossRefGoogle Scholar
  3. Barber-Meyer SM, Mech LD, White PJ (2008) Elk calf survival and mortality following wolf restoration to Yellowstone National Park. Wildl Monogr 169(1):1–30CrossRefGoogle Scholar
  4. Barbknecht AE, Fairbanks WS, Rogerson JD, Maichak EJ, Meadows LL (2009) Effectiveness of vaginal-implant transmitters for locating elk parturition sites. J Wildl Manage 73:144–148CrossRefGoogle Scholar
  5. Barnett CA, Suzuki TN, Sakaluk SK, Thompson CF (2015) Mass-based condition measures and their relationship with fitness: in what condition is condition? J Zool. doi: 10.1111/jzo.12213 Google Scholar
  6. Belovsky GE (1984) Herbivore optimal foraging: a comparative test of three models. Am Nat 124:97–115CrossRefGoogle Scholar
  7. Bender LC, Thomas LA, Kamienski T (2007) Habitat effects on condition of doe mule deer in arid mixed woodland-grassland. Rangel Ecol Manage 60:277–284CrossRefGoogle Scholar
  8. Bolker BM, Brooks MW, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135CrossRefPubMedGoogle Scholar
  9. Bowyer RT, Kie JG, van Ballengerghe V (1998) Habitat selection by neonatal black-tailed deer: climate, forage, or risk of predation? J Mamm 79:415–425CrossRefGoogle Scholar
  10. Bubenik AB (1982) Physiology. In: Thomas JW, Toweill DE (eds) Elk of North America: ecology and management. Stackpole, Harrisburg, pp 125–179Google Scholar
  11. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information theoretic approach, 2nd edn. Springer-Verlag, New York, USAGoogle Scholar
  12. Cook JG (2002) Nutrition and food. In: Toweill DE, Thomas JW (eds) North American elk: ecology and management. Smithsonian, Washington, DC, pp 259–349Google Scholar
  13. Cook JG, Johnson BK, Cook RC, Riggs RA, DelCurto T, Bryant LD, Irwin LL (2004) Effects of summer–autumn nutrition and parturition date on reproduction and survival of elk. Wildl Monogr 155(1):1–61Google Scholar
  14. Cook RC, Cook JG, Stephenson TR, Myers WL, McCorquodale SM, Vales DJ, Irwin LL, Hall PB, Spencer RD, Murphie SL, Schoenecker KA, Miller PJ (2010) Revisions of rump fat and body scoring indices for deer, elk, and moose. J Wildl Manage 74:880–896CrossRefGoogle Scholar
  15. Côté SD, Festa-Bianchet M (2001) Birthdate, mass and survival in mountain goat kids: effects of maternal characteristics and forage quality. Oecologia 127:230–238CrossRefPubMedGoogle Scholar
  16. Fauchald P, Torkild T, Henaug C, Yoccoz N (2004) Adaptive regulation of body reserves in reindeer, Rangifer tarandus: a feeding experiment. Oikos 107:583–591CrossRefGoogle Scholar
  17. Festa-Bianchet M, Jorgenson JT, Bérubé CH, Portier C, Wishart WD (1997) Body mass and survival of bighorn sheep. Can J Zool 75:1372–1379CrossRefGoogle Scholar
  18. Forester JD, Ives AR, Turner MG, Anderson DP, Fortin D, Beyer HL, Smith DW, Boyce MS (2007) State-space models link elk movement patterns to landscape characteristics in Yellowstone National Park. Ecol Monogr 77:285–299CrossRefGoogle Scholar
  19. Gaillard JM, Festa-Bianchet M, Yoccoz NG, Loison A, Togo C (2000) Temporal variation in fitness components and population dynamics of large herbivores. Annu Rev Ecol Syst 31:367–393CrossRefGoogle Scholar
  20. Gaillard JM, Hebblewhite M, Loison A, Fuller M, Powell R, Basille M, Van Moorter B (2010) Habitat-performance relationships: finding the right metric at a given spatial scale. Philos Trans R Soc B 365:2255–2265CrossRefGoogle Scholar
  21. Gillies CS, Hebblewhite M, Nielsen SE, Krawchuk MA, Aldridge CL, Frair JL, Saher DJ, Stevens CE, Jerde CL (2006) Application of random effects to the study of resource selection by animals. J Anim Ecol 75:887–898CrossRefPubMedGoogle Scholar
  22. Haskell SP, Ballard WB, Wallace MC, Humphrey MH, Butler DA (2010) Postpartum group cohesion of sympatric deer in Texas. J Wildl Manage 74:1686–1692CrossRefGoogle Scholar
  23. Houston AI, McNamara JM (2013) Foraging currencies, metabolism and behavioural routines. J Anim Ecol 83:30–40CrossRefPubMedGoogle Scholar
  24. Huey RB, Hertz PE, Sinervo B (2003) Behavioral drive versus behavioral inertia in evolution: a null model approach. Am Nat 161:357–366CrossRefPubMedGoogle Scholar
  25. Humphries MM, Umbanhowar J, McCann KS (2004) Bioenergetic prediction of climate change impacts on northern mammals. Integr Comp Bio 44:152–162CrossRefGoogle Scholar
  26. Johnson DE (1951) Biology of the elk calf, Cervus canadensis nelsoni. J Wildl Manage 15:396–410CrossRefGoogle Scholar
  27. Johnson BK, Kern JW, Wisdom MJ, Findholt SL, Kie JG (2000) Resource selection and spatial separation of mule deer and elk during spring. J Wildl Manage 64:685–697CrossRefGoogle Scholar
  28. Johnson BK, McCoy T, Kochanny CO, Cook RC (2006) Evaluation of vaginal implant transmitters in elk. J Zoo Wildl Med 37:301–305CrossRefPubMedGoogle Scholar
  29. Kearney MR, Matzelle A, Helmuth B (2012) Biomechanics meets the ecological niche: the importance of temporal data resolution. J Exp Biol 215:922–933CrossRefPubMedGoogle Scholar
  30. Keech MA, Bowyer RT, Ver Hoef JM, Boertje RD, Dale BW, Stephenson TR (2000) Life-history consequences of maternal condition in Alaskan moose. J Wildl Manage 64:450–462CrossRefGoogle Scholar
  31. Kie JG (1999) Optimal foraging and risk of predation: effects on behavior and social structure in ungulates. J Mamm 80:1114–1129CrossRefGoogle Scholar
  32. Leckenby DA (1984) Elk use and availability of cover and forage in the Blue Mountains, northeast Oregon, 1976–1982. Research report number 14. Oregon Department of Fish and Wildlife, Portland, ORGoogle Scholar
  33. Loison A, Langvatn R, Solberg EJ (1999) Body mass and winter mortality in red deer calves: disentangling sex and climate effects. Ecography 22:20–30CrossRefGoogle Scholar
  34. Long RA, Rachlow JL, Kie JG, Vavra M (2008) Fuels reduction in a western coniferous forest: effects on quantity and quality of forage for elk. Rangel Ecol Manage 61:302–313CrossRefGoogle Scholar
  35. Long RA, Kie JG, Bowyer RT, Hurley MA (2009) Resource selection and movements by female mule deer Odocoileus hemionus: effects of reproductive stage. Wildl Biol 15:288–298CrossRefGoogle Scholar
  36. Long RA, Bowyer RT, Porter WP, Mathewson P, Monteith KL, Kie JG (2014) Behavior and nutritional condition buffer a large-bodied endotherm against direct and indirect effects of climate. Ecol Monogr 84:513–532CrossRefGoogle Scholar
  37. Loudon ASI, Racey PA (eds) (1987) Reproductive energetics in mammals. Symposium of the Zoological Society of London 57. Oxford University Press, OxfordGoogle Scholar
  38. McLoughlin PD, Gaillard JM, Boyce MS, Bonenfant C, Messier F, Duncan P, Delorme D, Van Moorter B, Saïd S, Klein F (2007) Lifetime reproductive success and composition of the home range in a large herbivore. Ecology 88:3192–3201CrossRefPubMedGoogle Scholar
  39. McNamara JM, Houston AI (1996) State-dependent life histories. Nature 380:215–221CrossRefPubMedGoogle Scholar
  40. Millspaugh JJ, Brundige GC, Jenks JA, Tyner CL, Hustead DR (1995) Immobilization of Rocky Mountain elk with Telazol® and xylazine hydrochloride, and antagonism by yohimbine hydrochloride. J Wildl Dis 31:259–262CrossRefPubMedGoogle Scholar
  41. Moen AN (1978) Seasonal changes in heart rates, activity, metabolism, and forage intake of white-tailed deer. J Wildl Manage 42:715–738CrossRefGoogle Scholar
  42. Monteith KL, Stephenson TR, Bleich VC, Conner MM, Pierce BM, Bowyer RT (2013) Risk-sensitive allocation in seasonal dynamics of fat and protein reserves in a long-lived mammal. J Anim Ecol 82:377–388CrossRefPubMedGoogle Scholar
  43. Monteith KM, Bleich VC, Stephenson TR, Pierce BM, Conner MM, Kie JG, Bowyer RT (2014) Life-history characteristics of mule deer: effects of nutrition in a variable environment. Wildl Monogr 186(1):1–62CrossRefGoogle Scholar
  44. Morales JM, Fortin D, Frair JL, Merril EH (2005) Adaptive models for large herbivore movements in heterogeneous landscapes. Landsc Ecol 20:301–316CrossRefGoogle Scholar
  45. Mysterud A, Langvatn R, Yoccoz NG, Stenseth NC (2001a) Plant phenology, migration and geographical variation in body weight of a large herbivore: the effect of a variable topography. J Anim Ecol 70:915–923CrossRefGoogle Scholar
  46. Mysterud A, Stenseth NC, Yoccoz NG, Langvatn R, Steinheim G (2001b) Nonlinear effects of large-scale climatic variability on wild and domestic herbivores. Nature 410:1096–1099CrossRefPubMedGoogle Scholar
  47. Natori Y, Porter WP (2007) Model of Japanese serow (Capricornis crispus) energetics predicts distribution on Honshu, Japan. Ecol Appl 17:1441–1459CrossRefPubMedGoogle Scholar
  48. Neter J, Kutner MH, Nachtsheim CJ, Wasserman W (1996) Applied linear statistical models, 4th edn. McGraw-Hill, BostonGoogle Scholar
  49. Noyes JH, Sasser RG, Johnson BK, Bryant LD, Alexander B (1997) Accuracy of pregnancy detection by serum protein (PSPB) in elk. Wildl Soc B 25:695–698Google Scholar
  50. Parker KL, Barboza PS, Gillingham MP (2009) Nutrition integrates environmental responses of ungulates. Funct Ecol 23:57–69CrossRefGoogle Scholar
  51. Porter WP, Gates DM (1969) Thermodynamic equilibria of animals with environment. Ecol Monogr 39:227–244CrossRefGoogle Scholar
  52. Porter WP, Mitchell JW (2006) Method and system for calculating the spatial-temporal effects of climate and other environmental conditions on animals. US patent 7,155,377, December 2006. http://www.warf.org/technologies.jsp?ipnumber=P01251US
  53. Porter WP, Munger JC, Stewart WE, Budaraju S, Jaeger J (1994) Endotherm energetics: from a scalable individual-based model to ecological applications. Aust J Zool 42:125–162CrossRefGoogle Scholar
  54. Porter WP, Sabo JL, Tracy CR, Reichman OJ, Ramankutty N (2002) Physiology on a landscape scale: plant–animal interactions. Integr Comp Biol 42:431–453CrossRefPubMedGoogle Scholar
  55. Porter WP, Ostrowski S, Williams JG (2010) Modeling animal landscapes. Physiol Biochem Zool 83:705–712CrossRefPubMedGoogle Scholar
  56. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. http://www.R-project.org/
  57. Rearden SN, Anthony RG, Johnson BK (2011) Birth-site selection and predation risk of Rocky Mountain elk. J Mamm 92:1118–1126CrossRefGoogle Scholar
  58. Rowland MM, Bryant LD, Johnson BK, Noyes JH, Wisdom MJ, Thomas JW (1997) The Starkey Project: history, facilities, and data collection methods for ungulate research. General technical report PNW-GTR-296. US Forest Service, Portland, ORGoogle Scholar
  59. Scholander PF, Hock R, Walter V, Johnson F, Irving L (1950) Heat regulation in some arctic and tropical mammals and birds. Biol Bull 99:237–258CrossRefPubMedGoogle Scholar
  60. Sikes RS, Gannon WL, The Animal Care and Use Committee of the American Society of Mammalogists (2011) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mamm 92:235–253CrossRefGoogle Scholar
  61. Speakman JR, Król E (2010) Maximal heat dissipation capacity and hyperthermia risk: neglected key factors in the ecology of endotherms. J Anim Ecol 79:726–746PubMedGoogle Scholar
  62. Stewart KM, Bowyer RT, Dick BL, Johnson BK, Kie JG (2005) Density-dependent effects on physical condition and reproduction in North American elk: an experimental test. Oecologia 143:85–93CrossRefPubMedGoogle Scholar
  63. Stewart KM, Bowyer RT, Ruess RW, Dick BL, Kie JG (2006) Herbivore optimization by North American elk: consequences for theory and management. Wildl Monogr 167(1):1–24CrossRefGoogle Scholar
  64. van Beest FM, Milner JM (2013) Behavioural responses to thermal conditions affect seasonal mass change in a heat-sensitive northern ungulate. PLoS One 8:e65972CrossRefPubMedPubMedCentralGoogle Scholar
  65. Wagner T, Diefenbach DR, Norton DS, Christensen SA (2011) Using multilevel models to quantify heterogeneity in resource selection. J Wildl Manage 75:1788–1796CrossRefGoogle Scholar
  66. White RG (1983) Foraging patterns and their multiplier effects on productivity of northern ungulates. Oikos 40:377–384CrossRefGoogle Scholar
  67. White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46 Suppl:120–138CrossRefGoogle Scholar
  68. Wilson RP, Quintana F, Hobson VJ (2012) Construction of energy landscapes can clarify the movement and distribution of foraging animals. Proc R Soc B 279:975–980CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Ryan A. Long
    • 1
    • 6
  • R. T. Bowyer
    • 1
  • Warren P. Porter
    • 2
  • Paul Mathewson
    • 2
  • Kevin L. Monteith
    • 3
  • Scott L. Findholt
    • 4
  • Brian L. Dick
    • 5
  • John G. Kie
    • 1
  1. 1.Department of Biological SciencesIdaho State UniversityPocatelloUSA
  2. 2.Department of ZoologyUniversity of Wisconsin MadisonMadisonUSA
  3. 3.Wyoming Cooperative Fish and Wildlife Research Unit, Department of Zoology and PhysiologyUniversity of WyomingLaramieUSA
  4. 4.Oregon Department of Fish and WildlifeLa GrandeUSA
  5. 5.US Forest ServicePacific Northwest Research StationLa GrandeUSA
  6. 6.Department of Fish and Wildlife SciencesUniversity of IdahoMoscowUSA

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