Sex- and concentration-dependent effects of predator feces on seasonal regulation of body mass in the bank vole Clethrionomys glareolus

Hormones and Behavior

Volumn 52, Issue 4, 2007, Pages 436-444

  Tidhar, Wendy L ^a   Bonier, Frances ^b   Speakman, John R ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b UNIVERSITY OF IDAHO   (United States)

Author keywords

Bank vole; Clethrionomys glareolus; Daily energy expenditure; Fecal corticosterone; Least weasel; Mustela nivalis; Photoperiod; Predation risk

Indexed keywords

CORTICOSTERONE; STRESS HORMONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BODY MASS; CALORIC INTAKE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; ENERGY EXPENDITURE; FECES; FEMALE; FOOD INTAKE; MALE; NONHUMAN; PREDATION RISK; PREDATOR; PRIORITY JOURNAL; RADIOIMMUNOASSAY; SEASONAL VARIATION; SEX DIFFERENCE; VOLE;

ANALYSIS OF VARIANCE; ANIMALS; ARVICOLINAE; AVOIDANCE LEARNING; BODY COMPOSITION; BODY WEIGHT; CORTICOSTERONE; ENERGY METABOLISM; FEAR; FECES; FEEDING BEHAVIOR; FEMALE; LINEAR MODELS; MALE; ODORS; PHOTOPERIOD; RISK ASSESSMENT; SEASONS; SEX FACTORS; STRESS, PSYCHOLOGICAL;

EID: 34848918152     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2007.06.009     Document Type: Article

References (101)

1. Adriaensen F., Dhondt A.A., Van Dogen S., Lens L., and Matthysen E. Stabilizing selection on blue tit fledgling mass in the presence of sparrow hawks. Proc. R. Soc. Lond. B 265 (1998) 1011-1016
2. Apfelbach R., Blanchard C.D., Blanchard R.J., Hayes R.A., and McGregor I.S. The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci. Biobehav. Rev. 29 (2005) 1123-1144
3. Bairlein F. How to get fat: nutritional mechanisms of seasonal fat accumulation in migratory songbirds. Naturwissenschaften 89 (2002) 1-10
4. Banks P.B., and Dickman C.R. Effects of winter food supplementation on reproduction, body mass, and numbers of small mammals in montane Australia. Can. J. Zool. 78 (2000) 1775-1783
5. Banks P.B., Hume I.D., and Crowe O. Behavioural, morphological and dietary response of rabbits to predation risk from foxes. Oikos 85 (1999) 247-256
6. Banks P.B., Norrdahl K., and Korpimäki E. Nonlinearity in the predation risk of prey mobility. Proc. R. Soc. Lond. B 267 (2000) 1621-1625
7. Bartmann S., and Gerlach G. Multiple paternity and similar variance in reproductive success in male and female wood mice (Apodemus sylvaticus) housed in an enclosure. Ethology 107 (2001) 889-899
8. Bartness T.J., Demas G.E., and Song C.K. Seasonal changes in adiposity: the roles of the photoperiod, melatonin and other hormone and sympathetic nervous system. Exp. Biol. Med. 227 (2002) 363-376
9. Berteaux D., Thomas D.W., Bergeron J.-M., and Lapierre H. Repeatability of daily field metabolic rate in female meadow voles (Microtus pennsylvanicus). Funct. Ecol. 10 (1996) 751-759
10. Blanchard R.J., Nikulina J.N., Sakai R.R., McKittrick C., McEwen B., and Blanchard D.C. Behavioral and endocrine change following chronic predatory stress. Physiol. Behav. 63 4 (1998) 561-569
11. Boonstra R., Hik D., Singleton G.R., and Tinnikov A. The impact of predator-induced stress on the snowshoe hare cycle. Ecol. Monogr. 68 (1998) 371-394
12. Borowski Z. Influence of predator odour on the feeding behaviour of the root vole (Microtus oeconomus Pallas, 1776). Can. J. Zool. 76 (1998) 1791-1794
13. Borowski Z. Influence of weasel (Mustela nivalis Linnaeus, 1766) odour on spatial behaviour of root voles (Microtus oeconomus Pallas, 1776). Can. J. Zool. 76 (1998) 1799-1804
14. Bouskila A., and Blumstein D.T. Rules of thumb for predation hazard assessment: predictions from a dynamic model. Am. Nat. 139 (1992) 161-176
15. Brodin A. Mass-dependent predation and metabolic expenditure in wintering birds: is there a trade-off between different forms of predation?. Anim. Behav. 62 (2001) 993-999
16. Brown J.H., and Lasiewski R.C. Metabolism of weasels: the cost of being long and thin. Ecology 53 (1972) 939-943
17. Burns J.G., and Ydenberg R.C. The effects of wing loading and gender on the escape flights of least sandpipers (Calidris minutilla) and western sandpipers (Calidris mauri). Behav. Ecol. Sociobiol. 52 (2002) 128-136
18. Calder C.J., and Gorman M.L. The effects of red fox Vulpes vulpes faecal odours on the feeding behaviour of Orkney voles Microtus arvalis. J. Zool. 224 (1991) 599-606
19. Carlsen M., Lodal J., Leirs H., and Secher Jensen T. The effect of predation risk on body weight in the field vole, Microtus agrestis. Oikos 87 (1999) 277-285
20. Clinchy M., Zanette L., Boonstra R., Wingfield J.C., and Smith J.N.M. Balancing food and predator pressure induces chronic stress in songbirds. Proc. R. Soc. Lond. B 271 (2004) 2473-2479
21. Dark J., and Zucker I. Short photoperiods reduce winter energy requirements of the meadow vole, Microtus pennsylvanicus. Physiol. Behav. 31 (1983) 699-702
22. Dobson F.S., Risch T.S., and Murie J.O. Increasing returns in the life history of Columbian ground squirrels. J. Anim. Ecol. 68 (1999) 73-86
23. Eilam D., Dayan T., Ben-Eliyahu S., Schulman I., Shefer G., and Hendrie C.A. Differential behavioural and hormonal responses of voles and spiny mice to owl calls. Anim. Behav. 58 (1999) 1085-1093
24. Eisenberg J.F., and Kleiman D.G. Olfactory communication in mammals. Ann. Rev. Ecolog. Syst. 3 (1972) 1-32
25. Ekman J., and Hake M. Monitoring starvation risk: adjustment of body reserves in greenfinches (Carduelis chloris L.) during periods of unpredictable foraging success. Behav. Ecol. 1 (1990) 62-67
26. Fey K., Banks P.B., and Korpimäki E. Different microhabitat preferences of field and bank voles under manipulated predation risk from an alien predator. Ann. Zool. Fenn. 43 (2006) 9-16
27. Frid A., and Dill L.M. Human-caused disturbance stimuli as a form of predation risk. Conserv. Ecol. 6 (2002) 11-26
28. Gosler A.G., Greenwood J.J.D., and Perrins C. Predation risk and the cost of being fat. Nature 377 (1995) 621-623
29. Graham I.M., and Lambin X. The impact of weasel predation on cyclic field-vole survival: the specialist predator hypothesis contradicted. J. Anim. Ecol. 71 (2002) 946-956
30. Harper J.M., and Austad S.N. Fecal glucocorticoids: a noninvasive method of measuring adrenal activity in wild and captive rodents. Physiol. Biochem. Zool. 73 (2000) 12-22
31. Hedenstrom A. Flight performance in relation to fuel load in birds. J. Theor. Biol. 158 (1992) 535-537
32. Heldmaier G., Steinlechner S., and Rafael J. Nonshivering thermogenesis and cold resistance during seasonal acclimatization in the Djungarian hamster. J. Comp. Physiol. 149 (1982) 1-9
33. Hickling G.J., Millar J.S., and Moses R.A. Reproduction and nutrient reserves of bushy-tailed wood rats (Neotoma cinerea). Can. J. Zool. 69 (1991) 3088-3092
34. Je{ogonek}drzejewska B., and Je{ogonek}drzejewski W. Diets and hunting habits of predators. Predation in Vertebrate Communities: the Bialowieza Primeval Forest as a Case Study (1998), Springer-Verlag, Berlin 180-323
35. Je{ogonek}drzejewski W., and Je{ogonek}drzejewska B. Effect of a predator's visit on the spatial distribution of bank voles: experiments with weasels. Can. J. Zool. 68 (1990) 660-666
36. Je{ogonek}drzejewski W., Rychlik L., and Je{ogonek}drzejewska B. Responses of bank voles to odours of seven species of predators: experimental data and their relevance to natural predator-vole relationships. Oikos 68 (1993) 251-257
37. Jessop T., Sumner J., Lance V., and Limpus C. Reproduction in shark-attacked sea turtles is supported by stress-reduction mechanisms. Proc. R. Soc. Lond. B 271 (2004) S91-S94 (Suppl)
38. Kats L.B., and Dill L.M. The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5 (1998) 569
39. Kerstel E.R.T., Piersma T.A.J., Gessaman G.J., Dekinga A., Meijer H.A.J., and Visser G.H. Assessment of the amount of body water in the red knot (Calidris canutus): an evaluation of the principle of isotope dilution with H-2, O-17, and O-18 as measured with laser spectrometry and isotope ratio mass spectrometry. Isot. Environ. Health Stud. 42 (2006) 1-7
40. King J. Adaptive periodic fat storage in birds. In: Voous K.H. (Ed). Proceedings of the Fifteenth International Ornithological Congress, London (1972)
41. Klemme I., Eccard J.A., Gerlach G., Horne T.J., and Ylönen H. Does it pay to be a dominant male in a promiscuous species?. Ann. Zool. Fenn. 43 (2006) 248-257
42. Koivula M., and Korpimäki E. Do scent marks increase predation risk of microtine rodents?. Oikos 95 (2001) 275-281
43. Korpimäki E., Koivunen V., and Hakkarainen H. Microhabitat use and behavior of voles under weasel and raptor predation risk: predator facilitation?. Behav. Ecol. 7 (1996) 30-34
44. Koskela E., Horne T.J., Mappes T., and Ylönen H. Does risk of small mustelid predation affect the oestrous cycle in the bank vole, Clethrionomys glareolus?. Anim. Behav. 51 (1996) 1159-1163
45. Kriegsfeld L.J., and Nelson R.J. Gonadal and photoperiodic influences on body mass regulation in adult male and female prairie voles. Am. J. Physiol. 270 (1996) R1013-R1018
46. Krol E., and Speakman J.R. Isotope dilution spaces of mice injected simultaneously with deuterium, tritium and oxygen-18. J. Exp. Biol. 202 (1999) 2839-2849
47. Kullberg C., Fransson T., and Jakobsson S. Impaired predator evasion in fat blackcaps (Sylvia atricapilla). Proc. R. Soc. Lond. B 263 (1996) 1671-1675
48. Lima S.L. Predation risk and unpredictable feeding conditions - determinants of body mass in birds. Ecology 67 (1986) 377-385
49. Lima S.L., and Bednekoff P.A. Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am. Nat. 153 (1999) 649-659
50. Lima S.L., and Dill L.M. Behavioral decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68 (1989) 619-640
51. McDevitt R.M., and Speakman J.R. Long photophase is not a sufficient stimulus to reduce thermogenic capacity in winter-acclimatized short-tailed field voles (Microtus agrestis) during long-term cold-acclimation. J. Comp. Physiol. B. 164 (1994) 159-164
52. McDevitt R.M., and Speakman J.R. Central limits to sustainable metabolic-rate have no role in cold-acclimation of the short-tailed field vole (Microtus agrestis). Physiol. Zool. 67 (1994) 1117-1139
53. McDevitt R.M., and Speakman J.R. Summer acclimatization in the short-tailed field vole, Microtus agrestis. J. Comp. Physiol. B. 166 (1996) 286-293
54. McNamara J.M., and Houston A.I. The common currency for behavioral decisions. Am. Nat. 127 (1986) 358-378
55. McNamara J.M., Barta Z., Houston A.I., and Race P. A theoretical investigation of the effect of predators on foraging behaviour and energy reserves. Proc. R. Soc. Lond. B 272 (2005) 929-934
56. Mercer J.G., and Speakman J.R. Hypothalamic neuropeptide mechanisms for regulating energy balance: from rodent models to human obesity. Neurosci. Biobehav. Rev. 25 (2001) 101-116
57. Merkens M., Harestad A.S., and Sullivan T.P. Cover and efficacy of predator-based repellent for Townsend vole, Microtus townsendii. J. Chem. Ecol. 17 (1991) 401-412
58. Monclús R., Rödel H.G., Von Holst D., and De Miguel J. Behavioural and physiological responses of naïve European rabbits to predator odour. Anim. Behav. 70 (2005) 753-761
59. Morgan P.J., and Mercer J.G. The regulation of body weight: lessons from the seasonal animal. Proc. Nutr. Soc. 60 (2001) 127-134
60. Myers P., and Master L.L. Reproduction by Peromyscus maniculatus: size and compromise. J. Mammal. 64 (1983) 1-18
61. 18O) Method: A Guide to Its Use. UCLA Publication vol. 12-1417 (1983), University of California, Los Angeles
62. Nagy T.R., and Negus N.C. Energy acquisition and allocation in male collared lemmings (Dicrostonyx groenlandicus): effects of photoperiod, temperature and diet quality. Physiol. Zool. 66 (1993) 537-560
63. Norrdahl K., and Korpimäki E. Does mobility or sex of voles affect risk of predation by mammalian predators?. Ecology 79 (1998) 226-232
64. Norrdahl K., and Korpimäki E. The impact of predation risk from small mustelids on prey populations. Mamm. Rev. 30 (2000) 147-156
65. Oksanen L., and Lundberg P. Optimization of reproductive effort and foraging time in mammals: the influence of resource level and predation risk. Evol. Ecol. 9 (1995) 45-56
66. Pastro L.A., and Banks P.B. Foraging responses of wild house mice to accumulations of conspecific odor as a predation risk. Behav. Ecol. Sociobiol. 60 (2006) 101-107
67. Peacock W.L., Król E., Moar K.M., McLaren J.S., Mercer J.G., and Speakman J.R. Photoperiodic effects on body mass, energy balance and hypothalamic gene expression in the bank vole. J. Exp. Biol. 207 (2004) 165-177
68. Perrot-Sinal T.S., Heale V.R., Ossenkopp K.-P., and Kavaliers M. Sexually dimorphic aspects of spontaneous activity in meadow voles (Microtus pennsylvanicus): effects of exposure to fox odor. Behav. Neurosci. 110 (1996) 1126-1132
69. Petterborg L.J. Effect of photoperiod on body weight in the vole, Microtus montanus. Can. J. Zool. 56 (1978) 431-435
70. Pistole D.H., and Cranford J.A. Photoperiodic effects on growth in Microtus pennsylvanicus. J. Mammal. 63 (1982) 547-553
71. Ryan B.F., Joiner B.L., and Ryan T.A. Minitab Handbook (1985), PWS-Kent, Boston, MA
72. Schultz E.T. The effect of energy reserves on breeding schedule: is there a saturation point?. Funct. Ecol. 5 (1991) 819-824
73. Sih A., Ziemba R., and Harding K.C. New insights on how temporal variation in predation risk shapes prey behavior. Trends Ecol. Evol. 15 (2000) 3-4
74. Singleton G.R., Krebs C.J., Davis S., Chambers L., and Brown P. Reproductive changes in fluctuating house mouse populations in southeastern Australia. Proc. R. Soc. Lond. B 268 (2001) 1741-1748
75. 2 production in doubly labeled water studies of animals?. Funct. Ecol. 7 (1993) 746-750
76. Speakman J.R. Doubly Labeled Water: Theory and Practice (1997), Chapman and Hall, London
77. Speakman J.R. The history and theory of the doubly labeled water technique. Am. J. Clin. Nutr. 68 (1998) 932S-938S
78. Speakman J.R., and Król E. Validation of the doubly-labelled water method in a small mammal. Phys. Biochem. Zool. 78 (2005) 650-667
79. Speakman J.R., and Racey P.A. The equilibrium concentration of O-18 in body-water - implications for the accuracy of the doubly-labeled water technique and a potential new method of measuring RQ in free-living animals. J. Theor. Biol. 127 (1987) 79-95
80. 2 production for accuracy of the doubly labeled water technique - the importance of recapture interval. Comp. Biochem. Physiol. A. 90 (1988) 337-340
81. Speakman J.R., Nagy K.A., Masman D., Mook W.G., Poppitt S.D., Strathearn G.E., and Racey P.A. Interlaboratory comparison of different analytical techniques for determination of oxygen-18 abundance. Anal. Chem. 62 (1990) 703-708
82. Speakman J.R., Racey P.A., Haim A., Webb P.I., Ellison G.T.H., and Skinner J.D. Interindividual and intraindividual variation in daily energy-expenditure of the pouched mouse (Saccostomus campestris). Funct. Ecol. 8 (1994) 336-342
83. Speakman J.R., Rydell J., Webb P.I., Hayes J.P., Hays G.C., Hulbert I.A.R., and McDevitt R.M. Activity patterns of insectivorous bats and birds in northern Scandinavia (69°N), during continuous midsummer daylight. Oikos 88 (2000) 75-86
84. Stoddart D.M. Effect of the odour of weasels (Mustela nivalis L.) on trapped samples of their prey. Oecologia 22 (1975) 439-441
85. Sundell J., and Norrdahl K. Body size-dependent refuges in voles: an alternative explanation of the Chitty effect. Ann. Zool. Fenn. 39 (2002) 325-333
86. Sundell J., and Ylönen H. Behaviour and choice of refuge by voles under predation risk. Behav. Ecol. Sociobiol. 56 (2004) 263-269
87. Van Trigt R., Kerstel E.R.T., Neubert R.E.M., Meijer H.A.J., McLean M., and Visser G.H. Validation of the DLW method in Japanese quail at different water fluxes using laser and IRMS. J. Appl. Physiol. 93 (2002) 2147-2154
88. Visser G.H., and Schekkerman H. Validation of the doubly labeled water method in growing precocial birds: the importance of assumptions concerning evaporative water loss. Physiol. Biochem. Zool. 72 (1999) 740-749
89. Visser G.H., Dekinga A., Achterkamp B., and Piersma T. Ingested water equilibrates isotopically with the body water pool of a shorebird with unrivaled water fluxes. Am. J. Physiol. 279 (2000) R1795-R1804
90. 2 by radio mass spectrometry. Rapid Commun. Mass Spectrom. 14 (2000) 450-453
91. Ward S., Rayner J.M.V., Moller U., Jackson D.M., Nachtigall W., and Speakman J.R. Efficiency of flight in the starling (Sturnus vulgaris). J. Exp. Biol. 204 (2001) 3311-3322
92. Ward S., Moller U., Rayner J.M.V., Jackson D.M., Nachtigall W., and Speakman J.R. Metabolic power of European starlings (Sturnus vulgaris) during flight in a wind tunnel measured by heat transfer modeling, doubly-labelled water, mask respirometry and aerodynamic modeling. J. Exp. Biol. 207 (2004) 4291-4298
93. Wingfield J.C. Control of behavioural strategies for capricious environments. Anim. Behav. 66 (2003) 807-816
94. Wingfield J.C., Maney D.L., Breuner C.W., Jacobs J.D., Lynn S., Ramenofsky M., and Richardson R.D. Ecological bases of hormone-behavior interactions: the "emergency life history stage". Am. Zool. 38 (1998) 191-206
95. Witter M.S., and Cuthill I.C. The ecological costs of avian fat storage. Philos. Trans. R. Soc. Lond., B 340 (1993) 73-92
96. Ylönen H., and Ronkainen H. Breeding suppression in the bank vole as antipredatory adaptation in a predictable environment. Evol. Ecol. 8 (1994) 658-666
97. Ylönen H., Je{ogonek}drzejewska B., Je{ogonek}drzejewski W., and Heikkila J. Antipredatory behavior of Clethrionomys voles - "David and Goliath" arms race. Ann. Zool. Fenn. 29 (1992) 207-216
98. Ylönen H., Eccard J.A., Jokinen I., and Sundell J. Is the antipredatory response in behavior reflected in stress measured in faecal corticosteroids in a small rodent?. Behav. Ecol. Sociobiol. 60 (2006) 350-358
99. Zhao Z.J., and Wang D.H. Short photoperiod enhances thermogenic capacity in male and female Brandt's voles. Physiol. Behav. 85 (2005) 143-149
100. Zhang X.Y., and Wang D.H. Energy metabolism, thermogenesis and body mass regulation in Brandt's voles (Lasiopodomys brandtii) during cold acclimation and rewarming. Horm. Behav. 50 (2006) 61-69
101. Zhang J.-X., Cao C., Gao H., Yang Z.-S., Sun L., Zhang Z.-B., and Wang Z.-W. Effects of weasel odor on behavior and physiology of two hamster species. Physiol. Behav. 79 (2003) 549-552