Socially mediated effects of climate change decrease survival of hibernating Alpine marmots

Journal of Animal Ecology

Volumn 85, Issue 3, 2016, Pages 761-773

  Rézouki, Célia ^a   Tafani, Marion ^a   Cohas, Aurélie ^a   Loison, Anne ^b   Gaillard, Jean Michel ^a   Allainé, Dominique ^a   Bonenfant, Christophe ^a  

^a UNIVERSITÉ LYON 1   (France)

^b UNIVERSITÉ DE SAVOIE   (France)

Author keywords

French Alps; Lifestyle; Marmota marmota; Path analysis; Sociality; Winter conditions

Indexed keywords

CLIMATE CHANGE; GLOBAL CHANGE; GROWING SEASON; HIBERNATION; JUVENILE; LIFE HISTORY TRAIT; POPULATION DYNAMICS; RODENT; SURVIVAL; TEMPORAL VARIATION; WINTER;

ALPS; FRANCE;

MARMOTA MARMOTA; MARMOTA MARMOTA MARMOTA;

SNOW;

ANIMAL; ANIMAL BEHAVIOR; CLIMATE CHANGE; FRANCE; HIBERNATION; LONGITUDINAL STUDY; MARMOTA; PHYSIOLOGY; SOCIAL BEHAVIOR; SURVIVAL ANALYSIS;

ANIMALS; BEHAVIOR, ANIMAL; CLIMATE CHANGE; FRANCE; HIBERNATION; LONGITUDINAL STUDIES; MARMOTA; SNOW; SOCIAL BEHAVIOR; SURVIVAL ANALYSIS;

EID: 84964403005     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/1365-2656.12507     Document Type: Article

References (96)

1. Adamik, P. & Kral, M. (2008) Climate- and resource-driven long-term changes in dormice populations negatively affect hole-nesting songbirds. Journal of Zoology, 275, 209-215.
2. Adams, R.A. (2010) Bat reproduction declines when conditions mimic climate change projections for western North America. Ecology, 91, 2437-2445.
3. Alexander, R.D. (1974) The evolution of social behavior. Annual Review of Ecology and Systematics, 5, 323-383.
4. Allainé, D. (2000) Sociality, mating system and reproductive skew in marmots: evidence and hypotheses. Behavioural Processes, 51, 21-34.
5. Allainé, D. & Theuriau, F. (2004) Is there an optimal number of helpers in Alpine marmot family groups? Behavioral Ecology, 15, 916-924.
6. Allainé, D., Brondex, F., Graziani, L., Coulon, J. & Till-Bottraud, I. (2000) Male-biased sex ratio in litters of Alpine marmots supports the helper repayment hypothesis. Behavioral Ecology, 11, 507-514.
7. Armitage, K.B. (1999) Evolution of sociality in marmots. Journal of Mammalogy, 80, 1-10.
8. Armitage, K.B., Blumstein, D.T. & Woods, B.C. (2003) Energetics of hibernating yellow-bellied marmots (Marmota flaviventris). Comparative Biochemistry and Physiology Part A, 134, 101-114.
9. Arnold, W. (1988) Social thermoregulation during hibernation in Alpine marmots (Marmota marmota). Journal of Comparative Physiology B, 158, 151-156.
10. Arnold, W. (1990a) The evolution of marmot sociality: I. Why disperse late? Behavioral Ecology and Sociobiology, 27, 229-237.
11. Arnold, W. (1990b) The evolution of marmot sociality: II. Costs and benefits of joint hibernation. Behavioral Ecology and Sociobiology, 27, 239-246.
12. Arnold, W. (1993a) Social evolution in marmots and the adaptive value of joint hibernation. Verhandlungen der Deutschen Zoologischen Gesellschaft, 86, 79-93.
13. Arnold, W. (1993b) Energetics of social hibernation. Life in the Cold: Ecological, Physiological, and Molecular Mechanism (eds C. Carey, G.L. Florant, B.A. Wunder & B. Horwitz ), pp. 65-80. Westview Press, Boulder, CO, USA.
14. Arnold, W. & Dittami, J. (1997) Reproductive suppression in male Alpine marmots. Animal Behaviour, 53, 53-66.
15. Arnold, W., Heldmaier, G., Ortmann, S., Pohl, H., Ruf, T. & Steinlechner, S. (1991) Ambient temperatures in hibernacula and their energetic consequences for Alpine marmots (Marmota marmota). Journal of Thermal Biology, 16, 223-226.
16. Barash, D.P. (1974) The evolution of marmot societies: a general theory. Science, 185, 415-420.
17. Bateman, A.W., Ozgul, A., Nielsen, J.F., Coulson, T. & Clutton-Brock, T.H. (2013) Social structure mediates environmental effects on group size in an obligate cooperative breeder, Suricata suricatta. Ecology, 94, 587-597.
18. Blumstein, D.T. & Armitage, K.B. (1999) Cooperative breeding in marmots. Oikos, 84, 369-382.
19. Boyles, J.G., Storm, J.J. & Brack Jr, V. (2008) Thermal benefits of clustering during hibernation: a field test of competing hypotheses on Myotis sodalis. Functional Ecology, 22, 632-636.
20. Burnham, K.P. & Anderson, D.R. (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, 2nd edn. Springer-Verlag, New York, NY, USA.
21. Burnham, K.P., Anderson, D.R., White, G.C., Brownie, C. & Pollock, K.H. (1987) Design and Analysis Methods for Fish Survival Experiments Based on Release-Recapture. American Fisheries Society Monograph, Bethesda, MD, USA.
22. Choquet, R., Reboulet, A.M., Lebreton, J.D., Gimenez, O. & Pradel, R. (2005) U-CARE 2.2 User's Manual. CEFE, Montpellier, France.
23. Clutton-Brock, T.H., Russell, A.F., Sharpe, L.L., Brotherton, P.N.M., Mcllrath, G.M., White, S. et al. (2001) Effects of helpers on juvenile development and survival in meerkats. Science, 293, 2446-2449.
24. Cody, M.L. (1966) A general theory of clutch size. Evolution, 20, 174-184.
25. Cohas, A., Bonenfant, C., Gaillard, J.-M. & Allainé, D. (2007) Are extra-pair young better than within-pair young? A comparison of survival and dominance in Alpine marmot. Journal of Animal Ecology, 76, 771-781.
26. Coulson, T., Catchpole, E.A., Albon, S.D., Morgan, B.J., Pemberton, J.M., Clutton-Brock, T.H. et al. (2001) Age, sex, density, winter weather, and population crashes in Soay sheep. Science, 292, 1528-1531.
27. Emlen, S.T. & Wrege, P.H. (1991) Breeding biology of white-fronted bee-eaters at Nakuru: the influence of helpers on breeder fitness. Journal of Animal Ecology, 60, 309-326.
28. Farand, É., Allainé, D. & Coulon, J. (2002) Variation in survival rates for the Alpine marmot (Marmota marmota): effects of sex, age, year, and climatic factors. Canadian Journal of Zoology, 80, 342-349.
29. French, A.R. (1990) Age-class differences in the pattern of hibernation in yellow-bellied marmots, Marmota flaviventris. Oecologia, 82, 93-96.
30. Frick, W.F., Reynolds, D.S. & Kunz, T.H. (2010) Influence of climate and reproductive timing on demography of little brown myotis Myotis lucifugus. Journal of Animal Ecology, 79, 128-136.
31. Gaillard, J.-M. & Yoccoz, N.G. (2003) Temporal variation in survival of mammals: a case of environmental canalization? Ecology, 84, 3294-3306.
32. Gaillard, J.-M., Boutin, J.-M., Delorme, D., Van Laere, G., Duncan, P. & Lebreton, J.-D. (1997) Early survival in roe deer: causes and consequences of cohort variation in two contrasted populations. Oecologia, 112, 502-513.
33. Gaillard, J.-M., Festa-bianchet, M., Yoccoz, N.G., Loison, A. & Toïgo, C. (2000) Temporal variation in fitness components and population dynamics of large herbivores. Annual Review of Ecology and Systematics, 31, 367-393.
34. Garel, M., Loison, A., Gaillard, J.-M., Cugnasse, J.-M. & Maillard, D. (2004) The effects of a severe drought on mouflon lamb survival. Proceedings of the Royal Society of London. Series B, Biological Sciences, 71, S471-S473.
35. Geiser, F. & Körtner, G. (2010) Hibernation and daily torpor in Australian mammals. Australian Zoologist, 35, 204-215.
36. Grosbois, V., Gimenez, O., Gaillard, J.-M., Pradel, R., Barbraud, C., Clobert, J. et al. (2008) Assessing the impact of climate variation on survival in vertebrate populations. Biological Reviews, 83, 357-399.
37. Hackländer, K., Möstl, E. & Arnold, W. (2003) Reproductive suppression in female Alpine marmots, Marmota marmota. Animal Behaviour, 65, 1133-1140.
38. Hallett, T.B., Coulson, T., Pilkington, J.G., Clutton-Brock, T.H., Pemberton, J.M. & Grenfell, B.T. (2004) Why large-scale climate indices seem to predict ecological processes better than local weather. Nature, 430, 71-75.
39. Harvey, P.H. & Purvis, A. (1991) Comparative methods for explaining adaptations. Nature, 351, 619-624.
40. Healy, K., Guillerme, T., Finlay, S., Kane, A., Kelly, S.B.A., McClean, D. et al. (2014) Ecology and mode-of-life explain lifespan variation in birds and mammals. Proceedings of the Royal Society of London. Series B, Biological Sciences, 281, 20140298.
41. Hodge, S.J., Manica, A., Flower, T.P. & Clutton-Brock, T.H. (2008) Determinants of reproductive success in dominant female meerkats. Journal of Animal Ecology, 77, 92-102.
42. Hufnagl, S., Franceschini-Zink, C. & Millesi, E. (2011) Seasonal constraints and reproductive performance in female Common hamsters (Cricetus cricetus). Mammalian Biology, 76, 124-128.
43. Humphries, M.M., Thomas, D.W. & Speakman, J.R. (2002) Climate-mediated energetic constraints on the distribution of hibernating mammals. Nature, 418, 313-316.
44. Humphries, M.M., Umbanhowar, J. & McCann, K.S. (2004) Bioenergetic prediction of climate change impacts on northern mammals. Integrative and Comparative Biology, 44, 152-162.
45. Hurrell, J.W. (1995) Decadal trends in the North-Atlantic Oscillation: regional temperatures and precipitations. Science, 269, 676-679.
46. IPCC (2013) Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds T.F. Stocker, D. Qin, G.-K. Plattner, M. Tignor, S.K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex & P.M. Midgley ), pp. 1535. Cambridge University Press, Cambridge, UK and New York, NY, USA.
47. Jenouvrier, S., Barbraud, C. & Weimerskirch, H. (2005) Long-term contrasted responses to climate of two Antarctic seabird species. Ecology, 86, 2889-2903.
48. Jorgenson, J.T., Festa-Bianchet, M., Gaillard, J.-M. & Wishart, W.D. (1997) Effects of age, sex, disease and density of survival of bighorn sheep. Ecology, 78, 1019-1032.
49. Kager, T. & Fietz, J. (2009) Food availability in spring influences reproductive output in the seed-preying edible dormouse (Glis glis). Canadian Journal of Zoology, 87, 555-565.
50. Keller, L. & Genoud, M. (1997) Extraordinary lifespans in ants: a test of evolutionary theories of ageing. Nature, 389, 958-960.
51. Kneip, E., Van Vuren, D.H., Hostetler, J.A. & Oli, M.K. (2011) Influence of population density and climate on the demography of subalpine golden-mantled ground squirrels. Journal of Mammalogy, 92, 367-377.
52. Laake, J. & Rexstad, E. (2007) RMark - an alternative approach to building linear models in MARK. Program MARK: A Gentle Introduction. (eds E. Cooch & G. C. White), Appendix C, C1-C113. http://www.phidot.org/software/mark/docs/book/.
53. Lane, J.E., Kruuk, L.E.B., Charmantier, A., Murie, J.O. & Dobson, F.S. (2012) Delayed phenology and reduced fitness associated with climate change in a wild hibernator. Nature, 489, 554-557.
54. Lardy, S., Allainé, D., Bonenfant, C. & Cohas, A. (2015) Sex-specific determinants of fitness in a social mammal. Ecology, 96, 2947-2959.
55. Lebreton, J.-D., Nichols, J.D., Barker, R.J., Pradel, R. & Spendelow, J.A. (2009) Modeling individual animal histories with multistate capture-recapture models. Advances in Ecological Research (eds H. Caswell ), Vol. 41, pp. 87-173. Academic Press, Burlington, MA, USA.
56. Lyman, C.P., Willis, J.S., Malan, A. & Wang, L.C.H. (1982) Hibernation and Torpor in Mammals and Birds. Academic Press, New York, NY, USA.
57. MacDonald, D.W. & Newman, C. (2002) Population dynamics of badgers (Meles meles) in Oxfordshire, U.K.: numbers, density and cohort life histories, and a possible role of climate change in population growth. Journal of Zoology, 256, 121-138.
58. Magnolon, S. (1999) The natal dispersal of Alpine marmot (Marmota marmota). Pattern and the influence of some proximal factors. PhD thesis, Université de Tours, Tours.
59. Maldonado-Chaparro, A.A., Martin, J.G.A., Armitage, K.B., Oli, M.K. & Blumstein, D.T. (2015) Environmentally induced phenotypic variation in wild yellow-bellied marmots. Journal of Mammalogy, 96, 269-278.
60. Melis, C., Herfindal, I., Kauhala, K., Andersen, R. & Høgda, K.-A. (2010) Predicting animal performance through climatic and plant phenology variables: the case of an omnivore hibernating species in Finland. Mammalian Biology, 75, 151-159.
61. Merilä, J. (2012) Evolution in response to climate change: in pursuit of the missing evidence. BioEssays, 34, 811-818.
62. Mysterud, A., Yoccoz, N.G., Langvatn, R., Pettorelli, N. & Stenseth, N.C. (2008) Hierarchical path analysis of deer responses to direct and indirect effects of climate in northern forest. Philosophical Transactions of the Royal Society of London B, 363, 2359-2368.
63. Oro, D., Torres, R., Rodriguez, C. & Drummond, H. (2010) Climatic influence on demographic parameters of a tropical seabird varies with age and sex. Ecology, 91, 1205-1214.
64. Ozgul, A., Childs, D.Z., Oli, M.K., Armitage, K.B., Blumstein, D.T., Olson, L.E. et al. (2010) Coupled dynamics of body mass and population growth in response to environmental change. Nature, 466, 482-485.
65. Paquet, M., Doutrelant, C., Hatchwell, B.J., Spottiswoode, C.N. & Covas, R. (2015) Antagonistic effect of helpers on breeding male and female survival in a cooperatively breeding bird. Journal of Animal Ecology, 84, 1354-1362.
66. Patil, V.P., Karels, T.J. & Hik, D.S. (2015) Ecological, evolutionary and social constraints on reproductive effort: are hoary marmots really biennial breeders? PLoS ONE, 10, e0119081.
67. Patil, V.P., Morrison, S.F., Karels, T.J. & Hik, D.S. (2013) Winter weather versus group thermoregulation: what determines survival in hibernating mammals? Oecologia, 173, 139-149.
68. Perrin, C., Allainé, D. & Le Berre, M. (1993) Socio-spatial organization and activity distribution of the Alpine marmot Marmota marmota: preliminary results. Ethology, 93, 21-30.
69. Pettorelli, N., Vik, J.O., Mysterud, A., Gaillard, J.-M., Tucker, C.J. & Stenseth, N.C. (2005a) Using the satellite-derived NDVI to assess ecological responses to environmental change. Trends in Ecology and Evolution, 20, 503-510.
70. Pettorelli, N., Weladji, R.B., Holand, Ø., Mysterud, A., Breie, H. & Stenseth, N.C. (2005b) The relative role of winter and spring conditions: linking climate and landscape-scale plant phenology to alpine reindeer body mass. Biology letters, 1, 24-26.
71. Pettorelli, N., Pelletier, F., Von Hardenberg, A., Festa-Bianchet, M. & Côté, S.D. (2007) Early onset of vegetation growth vs. rapid green-up: impacts on juvenile mountain ungulates. Ecology, 88, 381-390.
72. Pradel, R., Wintrebert, C. & Gimenez, O. (2003) A proposal for a goodness-of-fit test to the Arnason-Schwarz multisite capture-recapture model. Biometrics, 59, 43-53.
73. Pretzlaff, I. & Dausmann, K.H. (2012) Impact of climatic variation on the hibernation physiology of Muscardinus avellanarius. Living in a Seasonal World: Thermoregulatory and Metabolic Adaptations (eds T. Ruf, C. Bieber, W. Arnold & E. Millesi ), pp. 175-187. Springer-Verlag, Berlin, Germany.
74. R Development Core Team. (2011) R: A Language and Environment for Statistical Computing. R foundation for Statistical Computing, Vienna, Austria.
75. Rebelo, H., Tarroso, P. & Jones, G. (2009) Predicted impact of climate change on European bats in relation to their biogeographic patterns. Global Change Biology, 16, 561-576.
76. Rézouki, C., Tafani, M., Cohas, A., Loison, A., Gaillard, J.-M., Allainé, D. et al. (2016) Data from: socially-mediated effects of climate change decrease survival of hibernating Alpine marmots. Dryad Digital Repository, http://dx.doi.org/10.5061/dryad.cp1cc.
77. Rödel, H.G. & Dekker, J.J.A. (2012) Influence of weather factors on population dynamics of two lagomorph species based on hunting bag records. European Journal of Wildlife Research, 58, 923-932.
78. Rödel, H.G., Bora, A., Kaetzke, P., Khaschei, M., Hutzelmeyer, H.D., Zapka, M. et al. (2005) Timing of breeding and reproductive performance of female European rabbits in response to winter temperature and body mass. Canadian Journal of Zoology, 83, 935-942.
79. Russell, A.F., Clutton-Brock, T.H., Brotherton, P.N.M., Sharpe, L.L., McIlrath, G.M., Dalerum, F.D. et al. (2002) Factors affecting pup growth and survival in co-operatively breeding meerkats (Suricata suricatta). Journal of Animal Ecology, 71, 700-709.
80. Schwartz, O.A. & Armitage, K.B. (2005) Weather influences on demography of the yellow-bellied marmot (Marmota flaviventris). Journal of Zoology, 265, 73-79.
81. Shattuck, M.R. & Williams, S.A. (2010) Arboreality has allowed for the evolution of increased longevity in mammals. Proceedings of the National Academy of Sciences of the United States of America, 107, 4635-4639.
82. Sheriff, M.J., Kenagy, G.J., Richter, M., Lee, T., Tøien, Ø., Kohl, F. et al. (2010) Phenological variation in annual timing of hibernation and breeding in nearby populations of Arctic ground squirrels. Proceedings of the Royal Society of London. Series B, Biological Sciences, 278, 2369-2375.
83. Shipley, B. (2009) Confirmatory path analysis in a generalized multilevel context. Ecology, 90, 363-368.
84. Skalski, J.R., Hoffman, A. & Smith, S.G. (1993). Testing the significance of individual- and cohort-level covariates in animal survival studies. Marked Individuals in the Study of Bird Population (eds J.D. Lebreton & P.M. North ), pp. 9-28. Birkaüser, Basel, Switzerland.
85. Solomon, N.G. & French, J.A. (1997) The study of mammalian cooperative breeding. Cooperative Breeding in Mammals (eds N.G. Solomon & J.A. French ), pp. 1-10. Cambridge University Press, Cambridge, UK.
86. Stearns, S.C. (1992) The Evolution of Life Histories. Oxford University Press, Oxford, UK.
87. Tafani, M., Cohas, A., Bonenfant, C., Gaillard, J.-M. & Allainé, D. (2013) Decreasing litter size of marmots over time: a life history response to climate change? Ecology, 94, 580-586.
88. Toïgo, C., Gaillard, J.-M., Van Laere, G., Hewison, A.J.M. & Morellet, N. (2006) How does environmental variation influence body mass, body size, and body condition? Roe deer as a case study. Ecography, 29, 301-308.
89. Turbill, C., Bieber, C. & Ruf, T. (2011) Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proceedings of the Royal Society of London. Series B, Biological Sciences, 278, 3355-3363.
90. Türk, A. & Arnold, W. (1988) Thermoregulation as a limit to habitat use in Alpine marmots (Marmota marmota). Oecologia, 76, 544-548.
91. Van Horne, B., Olson, G.S., Schooley, R.L., Corn, J.G. & Burnham, K.P. (1997) Effects of drought and prolonged winter on Townsend's ground squirrel demography in shrubsteppe habitats. Ecological Monographs, 67, 295-315.
92. Wasser, D.E. & Sherman, P.W. (2010) Avian longevities and their interpretation under evolutionary theories of senescence. Journal of Zoology, 280, 103-155.
93. Welbergen, J.A., Klose, S.M., Markus, N. & Eby, P. (2008) Climate change and the effects of temperature extremes on Australian flying-foxes. Proceedings of the Royal Society of London. Series B, Biological Sciences, 275, 419-425.
94. White, G.C. & Burnham, K.P. (1997) Program MARK: survival estimation from populations of marked animals. Bird Study, 46, S120-S139.
95. Wilkinson, G.S. & South, J.M. (2002) Life history, ecology and longevity in bats. Aging Cell, 1, 124-131.
96. Williams, S.A. & Shattuck, M.R. (2015) Ecology, longevity and naked mole-rats: confounding effects of sociality? Proceedings of the Royal Society of London. Series B, Biological Sciences, 282, 20141664.