Physiological flexibility and acclimation to food shortage in a heterothermic primate

Journal of Experimental Biology

Volumn 214, Issue 4, 2011, Pages 551-560

  Canale, Cindy I ^a   Perret, Martine ^a   Théry, Marc ^a   Henry, Pierre Yves ^a  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

Calorie restriction; Climate change; Energy saving; Extreme climatic event; Food availability; Microcebus murinus; Phenotypic plasticity; Thermoregulation

Indexed keywords

HYDROCORTISONE;

ADAPTATION; ANIMAL; ARTICLE; BODY WEIGHT; CHEIROGALEIDAE; CLIMATE CHANGE; ENERGY METABOLISM; FOOD DEPRIVATION; LOCOMOTION; PHYSIOLOGY; SEASON; STATISTICAL MODEL; THERMOREGULATION; URINE;

ADAPTATION, BIOLOGICAL; ANIMALS; BODY TEMPERATURE REGULATION; BODY WEIGHT; CHEIROGALEIDAE; CLIMATE CHANGE; ENERGY METABOLISM; FOOD DEPRIVATION; HYDROCORTISONE; LINEAR MODELS; LOCOMOTION; SEASONS;

LEMURIDAE; MICROCEBUS MURINUS; PRIMATES;

EID: 79951505321     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.046987     Document Type: Article

References (80)

1. Anderson, D. R., Burnham, K. P. and White, G. C. (1998). Comparison of Akaike information criterion and consistent Akaike information criterion for model selection and statistical inference from capture-recapture studies. J. Appl. Stat. 25, 263-282. (Pubitemid 128506716)
2. Aujard, F., Perret, M. and Vanier, G. (1998). Thermoregulatory responses to variations of photoperiod and ambient temperature in the lesser mouse lemur: a primitive or an advanced adaptive character?. J. Comp. Physiol. B 168, 540-548. (Pubitemid 28490389)
3. Beniston, M. and Jungo, P. (2002). Shifts in the distributions of pressure, temperature and moisture and changes in the typical weather patterns in the Alpine region in response to the behavior of the North Atlantic Oscillation. Theor. Appl. Climatol. 71, 29-42. (Pubitemid 34152644)
4. Bowler, K. (2005). Acclimation, heat shock and hardening. J. Therm. Biol. 30, 125-130. (Pubitemid 40247733)
5. Bowler, K. and Terblanche, J. S. (2008). Insect thermal tolerance: what is the role of ontogeny, ageing and senescence? Biol. Rev. 83, 339-355. (Pubitemid 352020260)
6. Boyles, J. G., Dunbar, M. B., Storm, J. J. and Brack, V. (2007). Energy availability influences microclimate selection of hibernating bats. J. Exp. Biol. 210, 4345-4350.
7. Bozinovic, F., Munoz, J. L. P., Naya, D. E. and Cruz-Neto, A. P. (2007). Adjusting energy expenditures to energy supply: food availability regulates torpor use and organ size in the Chilean mouse-opossum Thylamys elegans. J. Comp. Physiol. B 177, 393-400. (Pubitemid 46625356)
8. 2 upset the current balance? Science 278, 1582-1588. (Pubitemid 27516269)
9. Canale, C. I. and Henry, P. Y. (2010). Adaptive phenotypic plasticity and resilience of vertebrates to increasing climatic unpredictability. Clim. Res. 43, 135-147.
10. Chaffee, R. R. J. (1966). On experimental selection for super-hibernating and nonhibernating lines of Syrian hamsters. J. Theor. Biol. 12, 151-154.
11. Charmantier, A., McCleery, R. H., Cole, L. R., Perrins, C., Kruuk, L. E. B. and Sheldon, B. C. (2008). Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320, 800-803. (Pubitemid 351929630)
12. Chown, S. L. and Gaston, K. J. (2008). Macrophysiology for a changing world. Proc. Biol. Sci. 275, 1469-1478. (Pubitemid 351693541)
13. Cornish, E. R. and Mrosovsky, N. (1965). Activity during food deprivation and satiation of six species rodents. Anim. Behav. 13, 242-248.
14. Dammhahn, M. and Kappeler, P. (2008). Comparative feeding ecology of sympatric Microcebus berthaeand Microcebus murinus. Int. J. Primatol. 29, 1567-1589.
15. Dewar, R. E. and Richard, A. F. (2007). Evolution in the hypervariable environment of Madagascar. Proc. Natl. Acad. Sci. USA 104, 13723-13727. (Pubitemid 350003387)
16. Durant, J. M., Hjermann, D. O., Ottersen, G. and Stenseth, N. C. (2007). Climate and the match or mismatch between predator requirements and resource availability. Clim. Res. 33, 271-283. (Pubitemid 351728296)
17. Easterling, D. R., Meehl, G. A., Parmesan, C., Changnon, S. A., Karl, T. R. and Mearns, L. O. (2000). Climate extremes: Observations, modelling, and impacts. Science 289, 2068-2074.
18. Ganzhorn, J. U., Klaus, S., Ortmann, S. and Schmid, J. (2003). Adaptations to seasonality: some primates and nonprimates examples. In Primate Life Histories and Sociobiology (ed. P. M. Kappeler and M. E. Pereira), pp. 132-148. Chicago: University of Chicago Press.
19. Geiser, F. (2004a). Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu. Rev. Physiol. 66, 239-274. (Pubitemid 40614445)
20. Geiser, F. (2004b). The role of torpor in the life of arid zone mammals. Aust. Mammal. 26, 125-134. (Pubitemid 41268411)
21. Geiser, F. and Ferguson, C. (2001). Intraspecific differences in behaviour and physiology: effects of captive breeding on patterns of torpor in feathertail gliders. J. Comp. Physiol. B 171, 569-576. (Pubitemid 32948796)
22. Geiser, F. and Ruf, T. (1995). Hibernation versus daily torpor in mammals and birdsphysiological variables and classification of torpor patterns. Physiol. Zool. 68, 935-966. (Pubitemid 3017960)
23. Geiser, F. and Turbill, C. (2009). Hibernation and daily torpor minimize mammalian extinctions. Naturwissenschaften 96, 1235-1240.
24. Génin, F. and Perret, M. (2000). Photoperiod-induced changes in energy balance in gray mouse lemurs. Physiol. Behav. 71, 315-321. (Pubitemid 32058836)
25. Génin, F. and Perret, M. (2003). Daily hypothermia in captive grey mouse lemurs (Microcebus murinus): effects of photoperiod and food restriction. Comp. Biochem. Physiol. B 136, 71-81. (Pubitemid 36980804)
26. Ghalambor, C. K., McKay, J. K., Carroll, S. P. and Reznick, D. N. (2007). Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21, 394-407. (Pubitemid 46802146)
27. Gienapp, P., Teplitsky, C., Alho, J. S., Mills, J. A. and Merila, J. (2008). Climate change and evolution: disentangling environmental and genetic responses. Mol. Ecol. 17, 167-178. (Pubitemid 350292455)
28. Gilbert, C., McCafferty, D., Le Maho, Y., Giroud, S., Blanc, S. and Ancel, A. (2010). One for all and all for one: the energetic benefits of huddling in endotherms. Biol. Rev. 85, 545-569.
29. Giroud, S., Blanc, S., Aujard, F., Bertrand, F., Gilbert, C. and Perret, M. (2008). Chronic food shortage and seasonal modulations of daily torpor and locomotor activity in the grey mouse lemur (Microcebus murinus). Am. J. Physiol. Reg. Integr. Comp. Physiol. 294, R1958-R1967.
30. Giroud, S., Perret, M., Gilbert, C., Zahariev, A., Goudable, J., Le Maho, Y., Oudart, H., Momken, I., Aujard, F. and Blanc, S. (2009). Dietary palmitate and linoleate oxidations, oxidative stress, and DNA damage differ according to season in mouse lemurs exposed to a chronic food deprivation. Am. J. Physiol. Reg. Integr. Comp. Physiol. 297, R950-R959.
31. Grigg, G. C., Beard, L. A. and Augee, M. L. (2004). The evolution of endothermy and its diversity in mammals and birds. Physiol. Biochem. Zool. 77, 982-997. (Pubitemid 40241043)
32. Gutman, R., Yosha, D., Choshniak, I. and Kronfeld-Schor, N. (2007). Two strategies for coping with food shortage in desert golden spiny mice. Physiol. Behav. 90, 95-102. (Pubitemid 44918007)
33. Hau, M., Wikelski, M. and Wingfield, J. C. (2000). Visual and nutritional food cues fine-tune timing of reproduction in a neotropical rainforest bird. J. Exp. Zool. 286, 494-504. (Pubitemid 30146921)
34. Heldmaier, G. and Ruf, T. (1992). Body temperature and metabolic-rate during natural hyporthemia in endotherms. J. Comp. Physiol. B 162, 696-706.
35. Hoffmann, A. A., Sorensen, J. G. and Loeschcke, V. (2003). Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. J. Therm. Biol. 28, 175-216. (Pubitemid 36383351)
36. Humphries, M. M., Thomas, D. W. and Kramer, D. L. (2003). The role of energy availability in mammalian hibernation: A cost-benefit approach. Physiol. Biochem. Zool. 76, 165-179. (Pubitemid 36774988)
37. Ingram, J. C. and Dawson, T. P. (2005). Climate change impacts and vegetation response on the island of Madagascar. Philos. Transact. A Math. Phys. Eng. Sci. 363, 55-59. (Pubitemid 40067103)
38. IPCC (2007). Climate change 2007: synthesis report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (ed. Core Writing Team, R. K. Pachauri and A. Reisinger). Geneva, Switzerland: IPCC.
39. Jury, M. R. (2003). The climate of Madagascar. In The Natural History of Madagascar, (eds. S. M. Goodman and J. P. Benstead), pp. 75-87, Chicago: The University of Chicago Press.
40. Kokurewicz, T. (2004). Sex and age related habitat selection and mass dynamics of Daubenton's bats Myotis daubentonii (Kuhl, 1817) hibernating in natural conditions. Acta Chiropt. 6, 121-144. (Pubitemid 39008030)
41. Lahann, P., Schmid, J. and Ganzhorn, J. U. (2006). Geographic variation in populations of Microcebus murinus in Madagascar: Resource seasonality or Bergmann's rule? Int. J. Primatol. 27, 983-999. (Pubitemid 44610607)
42. Liow, L. H., Fortelius, M., Lintulaakso, K., Mannila, H. and Stenseth, N. C. (2009). Lower extinction risk in sleep-or-hide mammals. Am. Nat. 173, 264-272.
43. Lovegrove, B. G. (2000). Daily heterothermy in mammals: coping with unpredictable environments. In Life in the Cold (ed. G. Heldmaier and M. Klingenspor), pp. 29-40. Berlin: Springer-Verlag.
44. Lovegrove, B. G., Raman, J. and Perrin, M. R. (2001). Daily torpor in elephant shrews (Macroscelidea: Elephantulus spp.) in response to food deprivation. J. Comp. Physiol. B 171, 11-21. (Pubitemid 32161018)
45. McKechnie, A. E. and Wolf, B. O. (2004). Partitioning of evaporative water loss in white-winged doves: plasticity in response to short-term thermal acclimation. J. Exp. Biol. 207, 203-210. (Pubitemid 38106725)
46. Munro, D. and Thomas, D. W. (2004). The role of polyunsaturated fatty acids in the expression of torpor by mammals: a review. Zoology 107, 29-48. (Pubitemid 40427890)
47. Naya, D. E., Veloso, C., Sabat, P. and Bozinovic, F. (2009). The effect of short-and long-term fasting on digestive and metabolic flexibility in the Andean toad, Bufo spinulosus. J. Exp. Biol. 212, 2167-2175.
48. Nussey, D. H., Postma, E., Gienapp, P. and Visser, M. E. (2005). Selection on heritable phenotypic plasticity in a wild bird population. Science 310, 304-306. (Pubitemid 41457194)
49. Olivieri, G., Zimmermann, E., Randrianambinina, B., Rasoloharijaona, S., Rakotondravony, D., Guschanski, K. and Radespiel, U. (2007). The everincreasing diversity in mouse lemurs: Three new species in north and northwestern Madagascar. Mol. Phylogenet. Evol. 43, 309-327. (Pubitemid 46484357)
50. Ortmann, S., Heldmaier, G., Schmid, J. and Ganzhorn, J. U. (1997). Spontaneous daily torpor in Malagasy mouse lemurs. Naturwissenschaften 84, 28-32. (Pubitemid 27080843)
51. Ostrowski, S., Williams, J. B., Mesochina, P. and Sauerwein, H. (2006). Physiological acclimation of a desert antelope, Arabian oryx (Oryx leucoryx), to longterm food and water restriction. J. Comp. Physiol. B 176, 191-201. (Pubitemid 43320228)
52. Parmesan, C. (2006). Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37, 637-669. (Pubitemid 44907632)
53. Perret, M. and Aujard, F. (2001a). Daily hypothermia and torpor in a tropical primate: synchronization by 24-h light-dark cycle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281, R1925-R1933.
54. Perret, M. and Aujard, F. (2001b). Regulation by photoperiod of seasonal changes in body mass and reproductive function in gray mouse lemurs (Microcebus murinus): Differential responses by sex. Int. J. Primatol. 22, 5-24. (Pubitemid 32247813)
55. Pinheiro, J. C. and Bates, D. M. (2000). Mixed-effects Models in S and S-Plus. New York: Springer Verlag.
56. Pinheiro, J. C., Bates, D. M., DebRoy, S. and Sarkar, D. (2005). nlme: linear and nonlinear mixed-effects models. R package version 3. 1-83. Vienna, Austria: R Foundation for Statistical Computing.
57. Radespiel, U. (2006). Ecological diversity and seasonal adaptations of mouse lemurs (Microcebus spp.). In Lemurs: Ecology and Adaptation (ed. L. Gould and M. L. Sauther). Chicago: University of Chicago.
58. Rasoazanabary, E. (2006). Male and female activity patterns in Microcebus murinus during the dry season at Kirindy Forest, western Madagascar. Int. J. Primatol. 27, 437-464. (Pubitemid 43886385)
59. Ruf, T. (1991). Daily torpor in the Djungarian hamsters (Phodopus sungorus). Interactions with food-intake, activity and social behavior. J. Comp. Physiol. B 160.
60. Schielzeth, H. and Forstmeier, W. (2009). Conclusions beyond support: overconfident estimates in mixed models. Behav. Ecol. 20, 416-420.
61. Schmid, J. (2000). Daily torpor in the gray mouse lemur (Microcebus murinus) in Madagascar: energetic consequences and biological significance. Oecologia 123, 175-183. (Pubitemid 30308675)
62. Schmid, J. (2001). Daily torpor in free-ranging gray mouse lemurs (Microcebus murinus) in Madagascar. Int. J. Primatol. 22, 1021-1031. (Pubitemid 33066112)
63. Schmid, J. and Speakman, J. R. (2000). Daily energy expenditure of the grey mouse lemur (Microcebus murinus): a small primate that uses torpor. J. Comp. Physiol. B 170, 633-641. (Pubitemid 32065159)
64. Schmid, J., Ruf, T. and Heldmaier, G. (2000). Metabolism and temperature regulation during daily torpor in the smallest primate, the pigmy mouse lemur (Microcebus myoximus) on Madagascar. J. Comp. Physiol. B 170, 59-68. (Pubitemid 30351566)
65. Seebacher, F. (2005). A review of thermoregulation and physiological performance in reptiles: what is the role of phenotypic flexibility? J. Comp. Physiol. B 175, 453-461. (Pubitemid 41545607)
66. Séguy, M. and Perret, M. (2005). Factors affecting the daily rhythm of body temperature of captive mouse lemurs (Microcebus murinus). J. Comp. Physiol. B 175, 107-115. (Pubitemid 40374268)
67. Sherwin, C. M. (1998). Voluntary wheel running: a review and novel interpretation. Anim. Behav. 56, 11-27. (Pubitemid 28348956)
68. Stawski, C. and Geiser, F. (2010). Seasonality of torpor patterns and physiological variables of a free-ranging subtropical bat. J. Exp. Biol. 213, 393-399.
69. Stenseth, N. C., Mysterud, A., Ottersen, G., Hurrell, J. W., Chan, K. S. and Lima, M. (2002). Ecological effects of climate fluctuations. Science 297, 1292-1296. (Pubitemid 34913160)
70. Stenseth, N. C., Ottersen, G., Hurrell, J. W., Mysterud, A., Lima, M., Chan, K. S., Yoccoz, N. G. and Adlandsvik, B. (2003). Studying climate effects on ecology through the use of climate indices: the North Atlantic Oscillation, el Niño Southern Oscillation and beyond. Proc. Biol. Sci. 270, 2087-2096. (Pubitemid 37304034)
71. Stone, R. C., Hammer, G. L. and Marcussen, T. (1996). Prediction of global rainfall probabilities using phases of the southern oscillation index. Nature 384, 252-255.
72. Tomlinson, S., Withers, P. C. and Cooper, C. (2007). Hypothermia versus torpor in response to cold stress in the native Australian mouse Pseudomys hermannsburgensis and the introduced house mouse Mus musculus. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 148, 645-650. (Pubitemid 47484236)
73. Trenberth, K. E. and Hoar, T. J. (1997). El Nino and climate change. Geophys. Res. Lett. 24, 3057-3060. (Pubitemid 28147973)
74. Turbill, C., Kortner, G. and Geiser, F. (2008). Timing of the daily temperature cycle affects the critical arousal temperature and energy expenditure of lesser long-eared bats. J. Exp. Biol. 211, 3871-3878.
75. Walther, G. R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T. J. C., Fromentin, J. M., Hoegh-Guldberg, O. and Bairlein, F. (2002). Ecological responses to recent climate change. Nature 416, 389-395. (Pubitemid 34272866)
76. Wingfield, J. C. (2003). Control of behavioural strategies for capricious environments. Anim. Behav. 66, 807-815. (Pubitemid 37457975)
77. Wright, P. C. (1999). Lemur traits and Madagascar ecology: coping with an island environment. Yearb. Phys. Anthropol. 42, 31-72.
78. Zabala, A., Fernandez-Quintela, A., Macarulla, M. T., Simon, E., Rodriguez, V. M., Navarro, V. and Portillo, M. P. (2006). Effects of conjugated linoleic acid on skeletal muscle triacylglycerol metabolism in hamsters. Nutrition 22, 528-533.
79. Zhao, Z. J. and Wang, D. H. (2009). Plasticity in the physiological energetics of Mongolian gerbils is associated with diet quality. Physiol. Biochem. Zool. 82, 504-515.
80. Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A. and Smith, G. M. (2009). Mixed Effects Models and Extensions in Ecology with R. New York: Springer.