Abstract
Predation is a central organizing process affecting populations and communities. Traditionally, ecologists have focused on the direct effects of predation—the killing of prey. However, predators also have significant sublethal effects on prey populations. We investigated how fluctuating predation risk affected the stress physiology of a cyclic population of snowshoe hares (Lepus americanus) in the Yukon, finding that they are extremely sensitive to the fluctuating risk of predation. In years of high predator numbers, hares had greater plasma cortisol levels at capture, greater fecal cortisol metabolite levels, a greater plasma cortisol response to a hormone challenge, a greater ability to mobilize energy and poorer body condition. These indices of stress had the same pattern within years, during the winter and over the breeding season when the hare:lynx ratio was lowest and the food availability the worst. Previously we have shown that predator-induced maternal stress lowers reproduction and compromises offspring’s stress axis. We propose that predator-induced changes in hare stress physiology affect their demography through negative impacts on reproduction and that the low phase of cyclic populations may be the result of predator-induced maternal stress reducing the fitness of progeny. The hare population cycle has far reaching ramifications on predators, alternate prey, and vegetation. Thus, predation is the predominant organizing process for much of the North American boreal forest community, with its indirect signature—stress in hares—producing a pattern of hormonal changes that provides a sensitive reflection of fluctuating predator pressure that may have long-term demographic consequences.
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References
Armitage KB (2004) Badger predation on yellow-bellied marmots. Am Midl Nat 151:378–387
Baker ML, Gemmell E, Gemmell RT (1998) Physiological changes in brushtail possums, Trichosurus vulpecula, transferred from the wild to captivity. J Exp Zool 280:203–212
Bian J, Wu Y, Liu J (2005) Breeding behaviour under temporal risk of predation in male root voles (Microtus oeconomus). J Mamm 86:953–960
Boonstra R, Singelton GR (1993) Population declines in the snowshoe hare and the role of stress. Gen Comp Endocrinol 91:126–143
Boonstra R, Hik D, Singelton GR, Tinnikov A (1998a) The impact of predator-induced stress on the snowshoe hare cycle. Ecol Monogr 79:317–394
Boonstra R, Krebs CJ, Stenseth NC (1998b) Population cycles in small mammals: the problem of explaining the low phase. Ecology 79:1479–1488
Boutin S (1984) Effects of late winter food addition on numbers and movements of snowshoe hares. Oecologia 62:393–400
Boutin S, Krebs CJ, Sinclair ARE, Smith JNM (1986) Proximate causes of losses in a snowshoe hare population. Can J Zool 64:606–610
Breuner CW, Orchinik M (2002) Plasma binding proteins as mediators of corticosteroid action in vertebrates. J Endocrinol 175:99–112
Campbell TW (1996) Clinical pathology. In: Mader DR (ed) Reptile medicine and surgery. Saunders, Philadelphia, pp 248–257
Cary JR, Keith LB (1979) Reproductive change in the 10-year cycle of snowshoe hares. Can J Zool 57:375–390
Charbonnel N, Chaval Y, Berthier K, Deter J, Morand S, Palme R, Cosson J-F (2008) Stress and demographic decline: a potential effect mediated by impairment of reproduction and immune function in cyclic vole populations. Physiol Biochem Zool 81:63–73
Childress MJ, Lung MA (2003) Predation risk, gender and the group size effect: does elk vigilance depend upon the behaviour of conspecifics. Anim Behav 66:389–398
Clinchy M, Zanette L, Boonstra R, Wingfield JC, Smith JNM (2004) Balancing food and predation pressure induces chronic stress in songbirds. Proc R Soc Lond B 271:2473–2479
Creel S, Winnie J Jr, Maxwell B, Hamlin K, Creel M (2005) Elk alter habitat selection as an antipredator response to wolves. Ecology 86:3387–3397
Davis AK (2005) Effects of handling time and repeated sampling on avian white blood cell counts. J Field Ornithol 76:334–338
Davis AK, Maney DL, Maerz JC (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22:760–772
Dhabhar FS, Miller AH, McEwen BS, Spencer RL (1996) Stress induced changes in blood leukocyte distribution—role of adrenal steroid hormones. J Immunol 157:1638–1644
Doyle FI, Smith JNM (2001) Raptors and scavengers. In: Krebs CJ, Boutin S, Boonstra R (eds) Ecosystem dynamics of the boreal forest. the Kluane project. Oxford University Press, New York, pp 378–404
Fujiwara T, Cherrington AD, Neal DN, McGuinness OP (1996) Role of cortisol in the metabolic response to stress hormone infusion in the conscious dog. Metabolism 45:571–578
Harris SB, Gunion MW, Rosenthal MJ, Walford RW (1994) Serum glucose, glucose tolerance, corticosterone and free fatty acids during aging in energy restricted mice. Mech Ageing Dev 73:209–221
Hellgren EC, Rogers LL, Seal US (1993) Serum chemistry and hematology of black bears: physiological indices of habitat quality or seasonal patterns. J Mamm 74:304–315
Hik DS (1995) Does risk of predation influence population dynamics? Evidence from the cyclic decline of snowshoe hares. Wildl Res 22:115–129
Hik DS, McColl CJ, Boonstra R (2001) Why are arctic ground squirrels more stressed in the boreal forest than in alpine meadows? Ecoscience 8:275–288
Hodges KE, Stefan CI, Gillis EA (1999) Does body condition affect fecundity in a cyclic population of snowshoe hares? Can J Zool 77:1–6
Hodges KE, Krebs CJ, Hik DS, Gillis EA, Doyle CE (2001) Snowshoe hare dynamics. In: Krebs CJ, Boutin S, Boonstra R (eds) Ecosystem dynamics of the boreal forest. The Kluane project. Oxford University Press, New York, pp 141–178
Hodges KE, Krebs CJ, Boonstra R (2006) Overwinter mass loss of snowshoe hares in the Yukon: starvation, stress, adaptation or artefact? J Anim Ecol 75:1–13
Hone J, Krebs CJ, O’Donoghue M, Boutin S (2007) Evaluation of predator numerical responses. Wildl Res 34:335–341
Jain NC (1986) Schalm’s veterinary hematology. Lea & Febiger, Philadelphia
Kalin NH, Cohen RM, Kraemer GW, Risch SC, Shelton S, Cohen M, McKinney WT, Murphy DL (1981) The dexamethasone suppression test as a measure of hypothalamic-pituitary sensitivity and its relationship to behavioural arousal. Neuroendocrinology 32:92–95
Keith LB (1963) Wildlife’s ten-year cycle. University of Wisconsin Press, Madison
Keith LB (1990) Dynamics of snowshoe hare populations. Curr Mamm 2:119–195
Kitaysky AS, Piatt JF, Wingfield JC, Romano M (1999) The adrenocortical stress-response of black-legged kittiwake chicks in relation to dietary restrictions. J Comp Physiol B 169:303–310
Krebs CJ, Gilbert BS, Boutin S, Sinclair ARE, Smith JNM (1986) Population biology of snowshoe hares. I. Demography of food-supplemented populations in southern Yukon, 1976–1984. J Anim Ecol 55:963–982
Krebs CJ, Boutin S, Boonstra R, Sinclair ARE, Smith JNM, Dale MRT, Martin K, Turkington R (1995) Impact of food and predation on the snowshoe hare cycle. Science 269:1112–1115
Krebs CJ, Boonstra R, Boutin S, Sinclair ARE (2001a) What drives the 10-year cycle of snowshoe hares? Bioscience 51:25–35
Krebs CJ, Boutin S, Boonstra R (2001b) Ecosystem dynamics of the boreal forest. The Kluane project. Oxford University Press, New York
Krebs CJ, Dale MRT, Nams VO, Sinclair ARE, O’Donoghue M (2001c) Shrubs. In: Krebs CJ, Boutin S, Boonstra R (eds) Ecosystem dynamics of the boreal forest. The Kluane project. Oxford University Press, New York, pp 92–116
Lima SL (1998) Nonlethal effects in the ecology of predator–prey interactions. What are the ecological effects of anti-predator decision-making? Bioscience 48:25–34
Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behaviour: the predation risk allocation hypothesis. Am Nat 153:649–659
López-Olvera JR, Mereno I, Merino S, Sanz JJ, Arriero E (2005) Haematological variables are good predictors of recruitment in nestling pied flycatchers (Ficedula hypoleuca). Ecoscience 12:27–34
Miller WL, Tyrrell JB (1995) The adrenal cortex. In: Felig P, Baxter JD, Frohman LA (eds) Endocrinology and metabolism, 3rd edn. McGraw-Hill, New York, pp 555–711
Monclús R, Palomares F, Tablado Z, Martínez-Fontúrbel A, Palme R (2009) Testing the threat-sensitive predator avoidance hypothesis: physiological responses and predator pressure in wild rabbits. Oecologia 158:615–623
Moreno J, de León A, Fargallo JA, Moreno E (1998) Breeding time, health and immune response in the chinstrap penguin Pygoscelis antarctica. Oecologia 11:312–319
Munck A, Guyre P, Holbrook N (1984) Physiological functions of glucocorticoids during stress and their relation to pharmacological actions. Endocr Rev 5:25–44
Murray DL (2002) Differential body condition and vulnerability to predation in snowshoe hares. J Anim Ecol 71:614–625
Nelson EH, Matthews CE, Rosenheim JA (2004) Predators reduce prey population growth by inducing changes in prey behaviour. Ecology 85:1853–1858
O’Donoghue M, Krebs CJ (1992) Effects of supplemental food on snowshoe hare reproduction and juvenile growth at a cyclic population peak. J Anim Ecol 61:631–641
O’Donoghue M, Boutin S, Krebs CJ, Hofer EJ (1997) Numerical responses of coyotes and lynx to the snowshoe hare cycle. Oikos 80:150–162
O’Donoghue M, Boutin S, Murray DL, Krebs CJ, Hofer EJ, Breitenmoser U, Breitenmoser-Wüersten C, Zuleta G, Doyle C, Nams VO (2001) Coyotes and lynx. In: Krebs CJ, Boutin S, Boonstra R (eds) Ecosystem dynamics of the boreal forest. The Kluane project. Oxford University Press, New York, pp 276–323
Olaf F, Halle S (2004) Breeding suppression in free-ranging grey-sided voles under the influence of predator odour. Oecologia 138:151–159
Ortiz RM, Wade CE, Ortiz CL (2001) Effects of prolonged fasting on plasma cortisol and TH in postweaned northern elephant seal pups. Am J Physiol Regul Integr Comp Physiol 280:R790–R795
Otis D, Burnham KP, White GC, Andrews DR (1978) Statistical inference from capture data on closed animal populations. Wildl Monogr 62:1–135
Paine RT (1966) Food web complexity and species diversity. Am Nat 100:65–75
Palme R, Möstl E (1997) Measurement of cortisol metabolites in faeces of sheep as a parameter of cortisol concentration in blood. Int J Mamm Biol 62(Suppl II):192–197
Pangle KL, Peacor SD, Johannsson OE (2007) Large nonlethal effects of an invasive invertebrate predator on zooplankton population growth rate. Ecology 88:402–412
Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86:501–509
Rohner C, Doyle FI, Smith JNM (2001) Great horned owls. In: Krebs CJ, Boutin S, Boonstra R (eds) Ecosystem dynamics of the boreal forest. The Kluane project. Oxford University Press, New York, pp 340–376
Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19:249–255
Sapolsky RM (1992) Neuroendocrinology of the stress–response. In: Becker JB, Breedlove SM, Crews D (eds) Behavioural endocrinology. MIT Press, Cambridge, pp 287–324
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
Scheuerlein A, Van’t Hof TJ, Gwinner E (2001) Predators as stressors? Physiological and reproductive consequences of predation risk in tropical stonechats (Saxicola torquata axillaris). Proc R Soc Lond B 268:1575–1582
Schmitz OJ (2008) Effects of predator hunting mode on grassland ecosystem function. Science 319:952–954
Schmitz OJ, Beckerman AP, O’Brien KM (1997) Behaviourally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78:1388–1399
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
Sheriff MJ, Kuchel L, Boutin S, Humphries MM (2009c) Seasonal metabolic acclimatization in a northern population of free-ranging snowshoe hares, Lepus americanus. J Mamm 90:761–767
Sheriff MJ, Krebs CJ, Boonstra R (2010a) The ghosts of predators past: population cycles and the role of maternal programming under fluctuating predation risk. Ecology 91:2983–2994
Sheriff MJ, Krebs CJ, Boonstra R (2010b) Assessing stress in animal populations: do feces and plasma glucocorticoids tell the same story? Gen Comp Endocrinol 166:614–619
Silverin B (1997) The stress response and autumn dispersal behavior in willow tits. Anim Behav 53:451–459
Sinclair ARE, Krebs CJ, Smith JNM (1982) Diet quality and food limitation in herbivores: the case of the snowshoe hare. Can J Zool 60:889–897
Sinclair ARE, Krebs CJ, Smith JNM, Boutin S (1988) Population biology of snowshoe hares III. Nutrition, plant secondary compounds and food limitation. J Anim Ecol 57:787–806
Sitteri PK, Murai JT, Hammond GL, Nisker JA, Raymoure WJ, Kuhn RW (1982) The serum transport of steroid hormones. Recent Prog Horm Res 38:457–510
Stefan CI, Krebs CJ (2001) Reproductive changes in a cyclic population of snowshoe hares. Can J Zool 79:2101–2108
Taylor RJ (1984) Predation. Chapman-Hill, London
Tollrian R, Harvell CD (1999) The evolution of inducible defenses: current ideas. In: Tollrian R, Harvell CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, pp 306–321
Vamosi SM, Schluter D (2004) Character shifts in the defensive armor of sympatric sticklebacks. Evolution 58:376–385
Wasser SK, Thomas R, Nair PP, Guidry C, Southers J, Lucas J, Wildt DE, Monfort SL (1993) Effects of dietary fiber on fecal steroid measurements in baboons (Papio cynocephalus cynocephalus). J Reprod Fertil 97:569–574
Whittaker ME, Thomas VG (1983) Seasonal levels of fat and protein reserves of snowshoe hares in Ontario. Can J Zool 61:1339–1345
Wingfield JC, Romero LM (2001) Adrenocortical responses to stress and their modulation in free-living vertebrates. In: McEwen BS (ed) Handbook of physiology, Section 7. Coping with the environment: neural and endocrine mechanisms. Oxford University Press, Oxford, pp 211–236
Wingfield JC, Maney DL, Breuner CW, Jacobs JD, Lynn S, Ramenofsky M, Richardson RD (1998) Ecological bases of hormone–behavior interactions: the “emergency life history stage”. Am Zool 38:191–206
Winnie J Jr, Creel S (2007) Sex-specific behavioural responses of elk to spatial and temporal variation in the threat of wolf predation. Anim Behav 73:215–225
Yoccoz NG (1991) Overuse and misuse of significance tests in evolutionary biology and ecology. Bull Ecol Soc Am 72:106–111
Acknowledgments
We thank A.T. Sheriff, K. Pieczora, S. Mitford and E. Hofer for their contributions to this project. The Natural Sciences and Engineering Research Council of Canada, the Department of Indian Affairs and Northern Development, the EJLB Foundation, and the Arctic Institute of North America all supported this research. We thank Andrew Williams and the Arctic Institute of North America, University of Calgary, for providing facilities at Kluane Lake. The University of British Columbia Animal Care Committee approved all procedures in accordance with the guidelines of the Canadian Council for Animal Care.
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Sheriff, M.J., Krebs, C.J. & Boonstra, R. From process to pattern: how fluctuating predation risk impacts the stress axis of snowshoe hares during the 10-year cycle. Oecologia 166, 593–605 (2011). https://doi.org/10.1007/s00442-011-1907-2
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DOI: https://doi.org/10.1007/s00442-011-1907-2