Reproductive resilience to food shortage in a small heterothermic primate

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Canale, Cindy I ^a   Huchard, Elise ^b,c   Perret, Martine ^a   Henry, Pierre Yves ^a  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b GERMAN PRIMATE CENTER   (Germany)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN;

ADAPTIVE BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BREEDING; CALORIC RESTRICTION; CLIMATE CHANGE; CONTROLLED STUDY; ESTRUS; FEMALE; FERTILITY; FOOD AVAILABILITY; FOOD DEPRIVATION; FOOD SHORTAGE; FOREST; HABITAT QUALITY; LACTATION; LEMURIDAE; LITTER SIZE; MADAGASCAR; MALE; MATING SUCCESS; NONHUMAN; PREGNANCY; PRIMATE; PROGENY; REPRODUCTION; REPRODUCTIVE SUCCESS; WEANING;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CALORIC RESTRICTION; CHEIROGALEIDAE; ENERGY INTAKE; ESTRUS; FEMALE; MADAGASCAR; MALE; REPRODUCTION;

LEMUR; LEMURIDAE; MAMMALIA; MICROCEBUS MURINUS; PRIMATES;

EID: 84864668984     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041477     Document Type: Article

References (96)

1. Speakman JR, (2008) The physiological costs of reproduction in small mammals. Philosophical Transactions of the Royal Society B-Biological Sciences 363: 375-398.
2. Thompson SD, (1992) Gestation and lactation in small mammals: basal rate and the limits of energy use. In: Tomasi TE, Horton TH, editors. pp. 213-259 editors. Mammalian energetics. New York: Cornell University Press.
3. Zenuto RR, Antinuchi CD, Busch C, (2002) Bioenergetics of reproduction and pup development in a subterranean rodent (Ctenomys talarum). Physiological and Biochemical Zoology 75: 469-478.
4. Dammhahn M, Kappeler P, (2008) Comparative feeding ecology of sympatric Microcebus berthae and Microcebus murinus. International Journal of Primatology 29: 1567-1589.
5. Huchard E, Canale CI, Le Gros C, Perret M, Henry P-Y, et al. (2012) Convenience polyandry or convenience polygyny? Costly sexunder female control in a promiscuous primate. Proceedings of the Royal Society B-Biological Sciences 279: 1371-1379.
6. Kenagy GJ, (1987) Energy allocation for reproduction in the golden-mantled ground squirrel. In: Loudon A, Racey PA, editors. pp. 259-273 editors. Reproductive energetics in mammals. Oxford: Oxford University Press.
7. Gittleman JL, (1988) Energy allocation in mammalian reproduction. American Zoologist 28: 863-875.
8. Loudon ASI, Racey PA, (1987) Reproductive energetics in mammals. New York: Oxford University Press.
9. Clutton-Brock TH, Albon SD, Guinness FE, (1989) Fitness costs of gestation and lactation in wild mammals. Nature 337: 260-262.
10. Hammond KA, Diamond JM, (1992) An experimental test for the ceiling on sustained metabolic rate in lactating mice. Physiological Zoology 65: 952-977.
11. Rogowitz GL, (1996) Trade-offs in energy allocation during lactation. American Zoologist 36: 197-204.
12. Kunkele J, (2000) Energetics of gestation relative to lactation in a precocial rodent, the guinea pig (Cavia porcellus). Journal of Zoology 250: 533-539.
13. Stearns SC, (1992) The evolution of life histories. Oxford: Oxford University Press.
14. Williams G, editor (1966) Adaptation and natural selection. Princeton, NJ: Princeton University Press.
15. Visser ME, Both C, Lambrechts MM, (2004) Global climate change leads to mistimed avian reproduction. Advances in ecological research 35: 89-110.
16. Jonzén N, Lindén A, Ergon T, Knudsen E, others a, (2006) Rapid advance of spring arrival dates in long-distance migratory birds. Science 312: 1959-1961.
17. Durant JM, Hjermann DO, Ottersen G, Stenseth NC, (2007) Climate and the match or mismatch between predator requirements and resource availability. Climate Research 33: 271-283.
18. Schneider JE, (2004) Energy balance and reproduction. Physiology & Behavior 81: 289-317.
19. Wade GN, Schneider JE, Li H-Y, (1996) Control of fertility by metabolic cues. American Journal of Physiology 270: E1-19.
20. Fietz J, Kager T, Schauer S, (2009) Is energy supply the trigger for reproductive activity in male edible dormice (Glis glis)? Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology 179: 829-837.
21. Visser ME, (2008) Keeping up with a warming world; assessing the rate of adaptation to climate change. Proceedings of the Royal Society B-Biological Sciences 275: 649-659.
22. Bronson FH, (2009) Climate change and seasonal reproduction in mammals. Philosophical Transactions of the Royal Society B-Biological Sciences 364: 3331-3340.
23. Coppack T, Pulido F, (2004) Photoperiodic response and the adaptability of avian life cycles to environmental change. Advances in Ecological Research 35: 131-150.
24. Dawson A, (2008) Control of the annual cycle in birds: endocrine constraints and plasticity in response to ecological variability. Philosophical Transactions of the Royal Society B-Biological Sciences 363: 1621-1633.
25. Carey C, (2009) The impacts of climate change on the annual cycles of birds. Philosophical Transactions of the Royal Society B-Biological Sciences 364: 3321-3330.
26. Reed TE, Warzybok P, Wilson AJ, Bradley RW, Wanless S, et al. (2009) Timing is everything: flexible phenology and shifting selection in a colonial seabird. Journal of Animal Ecology 78: 376-387.
27. Canale CI, Henry P-Y, (2010) Adaptive phenotypic plasticity and resilience of vertebrates to increasing climatic unpredictability. Climate Research 43: 135-147.
28. Wingfield JC, Kelley JP, Angelier F, (2011) What are extreme environmental conditions and how do organisms cope with them? Current Zoology 57: 363-374.
29. Moreno J, Moller AP, (2011) Extreme climatic events in relation to global change and their impact on life histories. Current Zoology 57: 375-389.
30. Gill CJ, Rissman EF, (1997) Female sexual behavior is inhibited by short- and long-term food restriction. Physiology & Behavior 61: 387-394.
31. Temple JL, Schneider JE, Scott DK, Korutz A, Rissman EF, (2002) Mating behavior is controlled by acute changes in metabolic fuels. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 282: R782-R790.
32. Bronson FH, (1988) Effect of food manipulation on the gnrh-lh-estradiol axis of young female rats. American Journal of Physiology 254: R616-R621.
33. Hamilton GD, Bronson FH, (1985) Food restriction and reproductive development in wild house mice. Biology of Reproduction 32: 773-778.
34. Kauffman AS, Bojkowska K, Rissman EF, (2010) Critical periods of susceptibility to short-term energy challenge during pregnancy: Impact on fertility and offspring development. Physiology & Behavior 99: 100-108.
35. Wade GN, Schneider JE, (1992) Metabolic fuels and reproduction in female mammals. Neuroscience and Biobehavioral Reviews 16: 235-272.
36. Westman W, Kortner G, Geiser F, (2002) Developmental thermoenergetics of the dasyurid marsupial, Antechinus stuartii. Journal of Mammalogy 83: 81-90.
37. Elwood RW, (1992) Pup cannibalism in rodents: causes and consequences. In: Elgar MA, Crespi BJ, editors. pp. 299-322 editors. Cannibalism. Oxford: Oxford University Press.
38. Saether BE, Engen S, Møller AP, Weimerskirch H, Visser ME, et al. (2004) Life-history variation predicts the effects of demographic stochasticity on avian population dynamics. The American Naturalist 164: 793-802.
39. Martin K, Wiebe KL, (2004) Coping mechanisms of alpine and arctic breeding birds: Extreme weather and limitations to reproductive resilience. Integrative and Comparative Biology 44: 177-185.
40. Dewar RE, Richard AF, (2007) Evolution in the hypervariable environment of Madagascar. Proceedings of the National Academy of Sciences of the United States of America 104: 13723-13727.
41. Geiser F, Ruf T, (1995) Hibernation versus daily torpor in mammals and birds- physiological variables and classification of torpor patterns. Physiological Zoology 68: 935-966.
42. Heldmaier G, Ruf T, (1992) Body temperature and metabolic rate during natural hypothermia in endotherms. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology 162: 696-706.
43. Canale CI, Perret M, Thery M, Henry P-Y, (2011) Physiological flexibility and acclimation to food shortage in a heterothermic primate. Journal of Experimental Biology 214: 551-560.
44. Giroud S, Blanc S, Aujard F, Bertrand F, Gilbert C, et al. (2008) Chronic food shortage and seasonal modulations of daily torpor and locomotor activity in the grey mouse lemur (Microcebus murinus). American Journal of Physiology-Regulatory Integrative and Comparative Physiology 294: R1958-R1967.
45. Munn AJ, Kern P, McAllan BM, (2010) Coping with chaos: unpredictable food supplies intensify torpor use in an arid-zone marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata). Naturwissenschaften 97: 601-605.
46. Canale CI, Perret M, Henry P-Y, (2012) Torpor use during gestation and lactation in a primate. Naturwissenschaften 99: 159-163.
47. Perret M, (2000) Reproduction saisonnière et succès reproducteur chez un prosimien malgache, Microcebus murinus. Primatologie 3: 45-84.
48. Eberle M, Kappeler P, (2004) Selected polyandry: female choice and intersexual conflict in a small nocturnal solitary primate (Microcebus murinus). Behavioral Ecology and Sociobiology 57: 91-100.
49. Kraus C, Eberle M, Kappeler PM, (2008) The costs of risky male behaviour: sex differences in seasonal survival in a small sexually monomorphic primate. Proceedings of the Royal Society B-Biological Sciences 275: 1635-1644.
50. Pearce-Higgins JW, Dennis P, Whittingham MJ, Yalden DW, (2010) Impacts of climate on prey abundance account for fluctuations in a population of a northern wader at the southern edge of its range. Global Change Biology 16: 12-23.
51. Canale CI, Henry P-Y, (2011) Energetic costs of the immune response and torpor use in a primate. Functional Ecology 25: 557-565.
52. Aujard F, Perret M, Vanier G, (1998) Thermoregulatory responses to variations of photoperiod and ambient temperature in the lesser mouse lemur: a primitive or an advanced adaptive character? Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology 168: 540-548.
53. Perret M, (1992) Environmental and social determinants of sexual function in the male lesser mouse lemur (Microcebus murinus). Folia Primatologica 59: 1-25.
54. Andres M, Solignac M, Perret M, (2003) Mating system in mouse lemurs: Theories and facts, using analysis of paternity. Folia Primatologica 74: 355-366.
55. Perret M, Colas S, (1997) Manipulation of sex ratio at birth and maternal investment in female mouse lemurs (Microcebus murinus, Primates). Applied Animal Behaviour Science 51: 275-283.
56. R Development Core Team (2008) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
57. Pinheiro JC, Bates DM, (2000) Mixed-effects models in S and S-Plus. New York: Springer Verlag.
58. Schielzeth H, Forstmeier W, (2009) Conclusions beyond support: overconfident estimates in mixed models. Behavioral Ecology 20: 416-420.
59. Zullinger EM, Ricklefs RE, Redford KH, (1984) Fitting sigmoidal equations to mammalian growth curves. Journal of Mammalogy 65: 607-636.
60. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM, (2009) Mixed effects models and extensions in ecology with R. New-York: Springer.
61. Carney EW, Zablotny CL, Marty MS, Crissman JW, Anderson P, et al. (2004) The effects of feed restriction during in utero and postnatal development in rats. Toxicological Sciences 82: 237-249.
62. Gomez D, Huchard E, Henry P-Y, Perret M, (2011) Mutual mate choice in a female-dominated and sexually monomorphic primate. American Journal of Physical Anthropology 147: 370-379.
63. Génin F, Perret M, (2000) Photoperiod-induced changes in energy balance in gray mouse lemurs. Physiology & Behavior 71: 315-321.
64. Perret M, Aujard F, (2001) Regulation by photoperiod of seasonal changes in body mass and reproductive function in gray mouse lemurs (Microcebus murinus): Differential responses by sex. International Journal of Primatology 22: 5-24.
65. Schmid J, (1999) Sex-specific differences in activity patterns and fattening in the gray mouse lemur (Microcebus murinus) in Madagascar. Journal of Mammalogy 80: 749-757.
66. Valencack TG, Tataruch F, Ruf T, (2009) Peak energy turnover in lactating European hares: the role of fat reserves. Journal of Experimental Biology 212: 231-237.
67. Drent RH, Daan S, (1980) The prudent parent- energetic adjustments in avian breeding. Ardea 68: 225-252.
68. Giroud S, Perret M, Stein P, Goudable J, Aujard F, et al. (2010) The grey mouse lemur uses season-dependent fat or protein sparing strategies to face chronic food restriction. PLoS One 5: e8823.
69. Genin F, Perret M, (2003) Daily hypothermia in captive grey mouse lemurs (Microcebus murinus): effects of photoperiod and food restriction. Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology 136: 71-81.
70. Racey PA, Speakman JR, (1987) The energy costs of pregnancy and lactation in heterothermic bats. Symposium of Ecological Society of London 57: 107-125.
71. Geiser F, (1996) Torpor in reproductive endotherms. In: Geiser F, Hulbert AJ, Nicol SC, editors. pp. 81-86 editors. Adaptations to the cold: Tenth International Hibernation Symposium: University of New England Press.
72. McLean JA, Speakman JR, (1999) Energy budgets of lactating and non-reproductive brown long-eared bats (Plecotus auritus) suggest females use compensation during lactation. Functional Ecology 13: 360-372.
73. Geiser F, (2008) Ontogeny and phylogeny of endothermy and torpor in mammals and birds. Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology 150: 176-180.
74. Daniel S, Korine C, Pinshow B, (2010) The use of torpor in reproductive female Hemprich's Long-Eared Bats (Otonycteris hemprichii). Physiological and Biochemical Zoology 83: 142-148.
75. Racey PA, Swift SM, (1981) Variations in gestation length in a colony of pipistrelle bats (Pipistrellus pipistrellus) from year to year. Journal of Reproduction and Fertility 61: 123-129.
76. Perret M, (1998) Energetic advantage of nest-sharing in a solitary primate, the lesser mouse lemur (Microcebus murinus). Journal of Mammalogy 79: 1093-1102.
77. Eberle M, Kappeler P, (2006) Family insurance: kin selection and cooperative breeding in a solitary primate (Microcebus murinus). Behavioral Ecology and Sociobiology 60: 582-588.
78. Turbill C, Geiser F, (2006) Thermal physiology of pregnant and lactating female and male long-eared bats, Nyctophilus geoffroyi and N gouldi. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology 176: 165-172.
79. Humphries MM, Thomas DW, Kramer DL, (2003) The role of energy availability in mammalian hibernation: a cost-benefit approach. Physiological and Biochemical Zoology 76: 165-179.
80. Lahann P, Schmid J, Ganzhorn JU, (2006) Geographic variation in populations of Microcebus murinus in Madagascar: resource seasonality or Bergmann's rule? International Journal of Primatology 27: 983-999.
81. Wright PC, (1999) Lemur traits and Madagascar ecology: Coping with an island environment. Yearbook of Physical Anthropology 1999, Vol 42: 31-72.
82. Kappeler PM, Fichtel C, (2012) Female reproductive competition in Eulemur rufifrons: eviction and reproductive restraint in a plurally breeding Malagasy primate. Molecular Ecology 21: 685-698.
83. Ingram JC, Dawson TP, (2005) Climate change impacts and vegetation response on the island of Madagascar. Philosophical Transactions of the Royal Society of London Series a-Mathematical Physical and Engineering Sciences 363: 55-59.
84. Laurien-Kehnen C, Trillmich F, (2004) Maternal food restriction delays weaning in the guinea pig, Cavia porcellus. Animal Behaviour 68: 303-312.
85. Wilde CJ, Knight CR, Racey PA, (1999) Influence of torpor on milk protein composition and secretion in lactating bats. Journal of Experimental Zoology 284: 35-41.
86. Audet D, Fenton MB, (1988) Heterothermy and the use of torpor by the bat Eptesicus fuscus (Chiroptera: Vespertilionidae): a field study. Physiological Zoology 61: 197-204.
87. Duverge PL, Jones G, Rydell J, Ransome RD, (2000) Functional significance of emergence timing in bats. Ecography 23: 32-40.
88. Hoying KM, Kunz TH, (1998) Variation in size at birth and postnatal growth in the insectivorous bat Pipistrellus subflavus (Chiroptera: Vespertilionidae). Journal of Zoology 245: 15-27.
89. Bauer B, Dittami J, Huber S, (2009) Effects of nutritional quality during early development on body weight and reproductive maturation of guinea pigs (Cavia aperea f. porcellus). General and Comparative Endocrinology 161: 384-389.
90. Bazhan NM, Makarova EN, Yakovleva TV, (1996) Deprivation of food during pregnancy and reproduction in the water vole (Arvicola terrestris). Journal of Mammalogy 77: 1078-1084.
91. Liang H, Zhang ZB, (2006) Food restriction affects reproduction and survival of F1 and F2 offspring of rat-like hamster (Cricetulus triton). Physiology & Behavior 87: 607-613.
92. Maestripieri D, Mateo JM, (2011) Maternal effects in mammals. Chicago: The University of Chicago Press.
93. Canale CI, (2010) Changements climatiques et réponses adaptatives: flexibilité phénotypique et compromis énergétiques chez un primate hétérotherme (Microcebus murinus). PhD dissertation, Université Pierre et Marie Curie, Paris, France.
94. Andreassen HP, Ims RA, (1990) Response of grey-sided voles Clethrionomys rufocanus to malnutrition: a combined laboratory and field experiment. Oikos 59: 107-114.
95. Criscuolo F, Monaghan P, Nasir L, Metcalfe NB, (2008) Early nutrition and phenotypic development: 'catch-up' growth leads to elevated metabolic rate in adulthood. Proceedings of the Royal Society B-Biological Sciences 275: 1565-1570.
96. Schwensow N, Eberle M, Sommer S, (2008) Compatibility counts: MHC-associated mate choice in a wild promiscuous primate. Proceedings of the Royal Society, Series B 275: 555-564.