From process to pattern: How fluctuating predation risk impacts the stress axis of snowshoe hares during the 10-year cycle

Oecologia

Volumn 166, Issue 3, 2011, Pages 593-605

  Sheriff, Michael J ^a,b   Krebs, Charles J ^b   Boonstra, Rudy ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Cortisol; Low phase; Maternal effects; Population cycles; Sublethal effects

Indexed keywords

HYDROCORTISONE;

BODY CONDITION; BOREAL FOREST; BREEDING SEASON; DEMOGRAPHY; HORMONE; LAGOMORPH; MATERNAL EFFECT; METABOLITE; PREDATION RISK; PREDATOR-PREY INTERACTION; PREY AVAILABILITY; SUBLETHAL EFFECT;

ANIMAL; ARTICLE; BLOOD; BLOOD ANALYSIS; BODY COMPOSITION; CANADA; CHEMISTRY; ENERGY METABOLISM; FECES; FEMALE; FOOD CHAIN; HARE; IMMUNOLOGY; LYNX; MALE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; POPULATION DYNAMICS; REPRODUCTION; SEASON;

ANIMALS; BLOOD CHEMICAL ANALYSIS; BODY COMPOSITION; ENERGY METABOLISM; FECES; FEMALE; FOOD CHAIN; HARES; HYDROCORTISONE; LYNX; MALE; POPULATION DYNAMICS; REPRODUCTION; SEASONS; STRESS, PHYSIOLOGICAL; YUKON TERRITORY;

CANADA; YUKON TERRITORY;

LEPUS; LEPUS AMERICANUS; LYNX;

EID: 79958757841     PISSN: 00298549     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00442-011-1907-2     Document Type: Article

References (83)

1. Armitage KB (2004) Badger predation on yellow-bellied marmots. Am Midl Nat 151: 378-387.
2. 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.
3. 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.
4. Boonstra R, Singelton GR (1993) Population declines in the snowshoe hare and the role of stress. Gen Comp Endocrinol 91: 126-143.
5. 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.
6. Boonstra R, Krebs CJ, Stenseth NC (1998b) Population cycles in small mammals: the problem of explaining the low phase. Ecology 79: 1479-1488.
7. Boutin S (1984) Effects of late winter food addition on numbers and movements of snowshoe hares. Oecologia 62: 393-400.
8. Boutin S, Krebs CJ, Sinclair ARE, Smith JNM (1986) Proximate causes of losses in a snowshoe hare population. Can J Zool 64: 606-610.
9. Breuner CW, Orchinik M (2002) Plasma binding proteins as mediators of corticosteroid action in vertebrates. J Endocrinol 175: 99-112.
10. Campbell TW (1996) Clinical pathology. In: Mader DR (ed) Reptile medicine and surgery. Saunders, Philadelphia, pp 248-257.
11. Cary JR, Keith LB (1979) Reproductive change in the 10-year cycle of snowshoe hares. Can J Zool 57: 375-390.
12. 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.
13. 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.
14. 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.
15. 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.
16. Davis AK (2005) Effects of handling time and repeated sampling on avian white blood cell counts. J Field Ornithol 76: 334-338.
17. 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.
18. 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.
19. 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.
20. 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.
21. 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.
22. 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.
23. Hik DS (1995) Does risk of predation influence population dynamics? Evidence from the cyclic decline of snowshoe hares. Wildl Res 22: 115-129.
24. 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.
25. 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.
26. 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.
27. 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.
28. Hone J, Krebs CJ, O'Donoghue M, Boutin S (2007) Evaluation of predator numerical responses. Wildl Res 34: 335-341.
29. Jain NC (1986) Schalm's veterinary hematology. Lea & Febiger, Philadelphia.
30. 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.
31. Keith LB (1963) Wildlife's ten-year cycle. University of Wisconsin Press, Madison.
32. Keith LB (1990) Dynamics of snowshoe hare populations. Curr Mamm 2: 119-195.
33. 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.
34. 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.
35. 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.
36. Krebs CJ, Boonstra R, Boutin S, Sinclair ARE (2001a) What drives the 10-year cycle of snowshoe hares? Bioscience 51: 25-35.
37. Krebs CJ, Boutin S, Boonstra R (2001b) Ecosystem dynamics of the boreal forest. The Kluane project. Oxford University Press, New York.
38. 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.
39. 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.
40. Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behaviour: the predation risk allocation hypothesis. Am Nat 153: 649-659.
41. 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.
42. 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.
43. 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.
44. 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.
45. Munck A, Guyre P, Holbrook N (1984) Physiological functions of glucocorticoids during stress and their relation to pharmacological actions. Endocr Rev 5: 25-44.
46. Murray DL (2002) Differential body condition and vulnerability to predation in snowshoe hares. J Anim Ecol 71: 614-625.
47. Nelson EH, Matthews CE, Rosenheim JA (2004) Predators reduce prey population growth by inducing changes in prey behaviour. Ecology 85: 1853-1858.
48. 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.
49. 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.
50. 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.
51. Olaf F, Halle S (2004) Breeding suppression in free-ranging grey-sided voles under the influence of predator odour. Oecologia 138: 151-159.
52. 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.
53. Otis D, Burnham KP, White GC, Andrews DR (1978) Statistical inference from capture data on closed animal populations. Wildl Monogr 62: 1-135.
54. Paine RT (1966) Food web complexity and species diversity. Am Nat 100: 65-75.
55. 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.
56. Pangle KL, Peacor SD, Johannsson OE (2007) Large nonlethal effects of an invasive invertebrate predator on zooplankton population growth rate. Ecology 88: 402-412.
57. Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator-prey interactions. Ecology 86: 501-509.
58. 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.
59. Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19: 249-255.
60. Sapolsky RM (1992) Neuroendocrinology of the stress-response. In: Becker JB, Breedlove SM, Crews D (eds) Behavioural endocrinology. MIT Press, Cambridge, pp 287-324.
61. 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.
62. 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.
63. Schmitz OJ (2008) Effects of predator hunting mode on grassland ecosystem function. Science 319: 952-954.
64. Schmitz OJ, Beckerman AP, O'Brien KM (1997) Behaviourally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78: 1388-1399.
65. 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.
66. 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.
67. 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.
68. 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.
69. 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.
70. Silverin B (1997) The stress response and autumn dispersal behavior in willow tits. Anim Behav 53: 451-459.
71. 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.
72. 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.
73. 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.
74. Stefan CI, Krebs CJ (2001) Reproductive changes in a cyclic population of snowshoe hares. Can J Zool 79: 2101-2108.
75. Taylor RJ (1984) Predation. Chapman-Hill, London.
76. 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.
77. Vamosi SM, Schluter D (2004) Character shifts in the defensive armor of sympatric sticklebacks. Evolution 58: 376-385.
78. 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.
79. Whittaker ME, Thomas VG (1983) Seasonal levels of fat and protein reserves of snowshoe hares in Ontario. Can J Zool 61: 1339-1345.
80. 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.
81. 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.
82. 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.
83. Yoccoz NG (1991) Overuse and misuse of significance tests in evolutionary biology and ecology. Bull Ecol Soc Am 72: 106-111.