Abstract
The fat-tailed dwarf lemur, Cheirogaleus medius, occurs in ecologically very different habitat types (rainforest and dry forest) across Madagascar. Its extraordinary biological characteristics, such as monogamy and long-term hibernation, allow us to investigate behavioral, ecological, and physiological flexibility of this species in populations across different ecological environments. This study aims to determine whether different life history and physiological traits show variation in adaptation to the differing ambient conditions or are conservative and influenced more by the organism's evolutionary history. We compared body masses, life history traits, social organization, and hibernation duration of two populations of C. medius, one from a littoral rainforest and one from the dry deciduous forest. We revealed clear geographical differences in the length of hibernation duration as well as, more surprisingly, in life history traits. We found that this species' reproductive strategies seem to be highly flexible. Animals in the rainforest can spend more time in the active state due to a shorter hibernation period, but have, in general, a shorter life expectancy due to higher mortality rates. Hence, they seem to maximize their total reproductive output with higher reproductive rates (larger litter sizes, greater number of litters). Home ranges and social organization, on the other hand, did not vary between habitats, suggesting that the general requirements of this species are independent of environmental conditions. In conclusion, some life history traits, formerly assumed to be genetically fixed parameters of primate species, prove in fact to be highly flexible. Different populations of the same species show distinct adaptations according to the prevailing conditions in order to maximize individual reproductive output.
Similar content being viewed by others
References
Barclay RMR, Harder LD (2003) Life histories of bats: life in the slow lane. In: Kunz TH, Fenton MB (eds) Bat ecology. University of Chicago Press, Chicago, pp 209–253
Barclay RMR, Ulmer J, MacKenzie CJA, Thompson MS, Olson L, McCool J, Cropley E, Poll G (2004) Variation in the reproductive rate of bats. Can J Zool 82:688–693
Blomberg SP, Garland T (2002) Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods. J Evol Biol 15:899–910
Bronson FH (1989) Mammalian reproductive biology. University of Chicago Press, Chicago
Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2004) Physiology: hibernation in a tropical primate—even in the wound-down hibernating state, this lemur can warm up without waking up. Nature 429:825–826
Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2005) Hibernation in the tropics: lessons from a primate. J Comp Physiol B 175:147–155
Dausmann KH, Glos J, Heldmaier G (2009) Energetics of tropical hibernation. J Comp Physiol B 179:345–357
Di Bitetti MS, Janson CH (2000) When will the stork arrive? Patterns of birth seasonality in neotropical primates. Am J Primatol 50:109–130
Dobson FS, Kjelgaard JD (1985) The influence of food resources on life history in Columbian ground squirrels. Can J Zool 63:2105–2109
Fietz J (1999) Monogamy as a rule rather than exception in nocturnal lemurs: the case of the fat-tailed dwarf lemur, Cheirogaleus medius. Ethol 105:259–272
Fietz O, Dausmann KH (2003) Costs and potential benefits of parental care in the nocturnal fat-tailed dwarf lemur (Cheirogaleus medius). Folia Primatol 74:246–258
Fietz J, Dausmann KH (2007) Big is beautiful: fat storage and hibernation as a strategy to cope with marked seasonality in the fat-tailed dwarf emur (Cheirogaleus medius). In: Gould L, Sauther ML (eds) Lemurs: ecology and adaptation. Springer, New York, pp 97–110
Fietz J, Ganzhorn JU (1999) Feeding ecology of the hibernating primate Cheirogaleus medius: how does it get so fat? Oecol 121:157–164
Fietz J, Zischler H, Schwiegk C, Tomiuk J, Dausmann KH, Ganzhorn JU (2000) High rates of extra-pair young in the pair-living fat-tailed dwarf lemur, Cheirogaleus medius. Behav Ecol Sociobiol 49:8–17
Foerg R (1982) Reproduction in Cheirogaleus medius. Folia Primatol 39:49–62
Ganzhorn JU, Goodman SM, Vincelette M (2007) Biodiversity, ecology and conservation of littoral ecosystems in southeastern Madagascar, Tolagnaro (Fort Dauphin). McArdle, Maryland
Grant JWA, Chapman CA, Richardson KS (1992) Defended versus undefended home range size of carnivores, ungulates and primates. Behav Ecol Sociobiol 31:149–161
Groeneveld LF, Weisrock DW, Rasoloarison RM, Yoder AD, Kappeler PM (2009) Species delimitation in lemurs: multiple genetic loci reveal low levels of species diversity in the genus Cheirogaleus. BMC Evol Biol 9:30
Groves CP (2000) The genus Cheirogaleus: unrecognized biodiversity in dwarf lemurs. Int J Primatol 21:943–962
Harris S, Cresswell WJ, Forde PG, Trewhella WJ, Woolard T, Wray S (1990) Home-range analysis using radio-tracking data—a review of problems and techniques particularly as applied to the study of mammals. Mamm Rev 20:97–123
Harvey PH, Clutton-Brock TH (1981) Primate home-range size and metabolic needs. Behav Ecol Sociobiol 8:151–155
Harvey PH, Clutton-Brock TH (1985) Life history variation in primates. Evol 39:559–581
Heldmaier G, Klingenspor M, Klaus S (2000) Life in the cold. Springer, Berlin
Ims RA (1990) On the adaptive value of reproductive synchrony as a predator-swamping strategy. Am Nat 136:485–498
Kappeler PM (1996) Causes and consequences of life-history variation among strepsirhine primates. Am Nat 148:868–891
Kappeler P, Pereira ME (2003) Primate life histories and socioecology. University of Chicago Press, Chicago
Lahann P (2007) Feeding ecology and seed dispersal of sympatric cheirogaleid lemurs (Microcebus murinus, Cheirogaleus medius, Cheirogaleus major) in the littoral rainforest of south-east Madagascar. J Zool 271:88–98
Lahann P (2008) Habitat utilization of three sympatric cheirogaleid lemur species in a littoral rain forest of southeastern Madagascar. Int J Primatol 29:117–134
Lahann P, Schmid J, Ganzhorn JU (2006) Geographic variation in populations of Microcebus murinus in Madagascar: resource seasonality or Bergmann's rule? Int J Primatol 27:983–999
Levin R (1968) Evolution in changing environments. Princeton University Press, Princeton
Lott DF (1984) Intraspecific variation in the social systems of wild vertebrates. Behav 88:266–325
Lovegrove BG, Genin F (2008) Torpor and hibernation in a basal placental mammal, the Lesser Hedgehog Tenrec Echinops telfairi. J Comp Physiol B 178:691–698
Loveridge AJ, Valeix M, Davidson Z, Murinagomo H, Fritz H, MacDonald DW (2009) Changes in home range size of African lions in relation to pride size and prey biomass in a semi-arid savanna. Ecography 32:953–962
Lyman CP, O'Brien RC, Greene GC, Papafrangos ED (1981) Hibernation and longevity in the Turkish hamster Mesocricetus brandti. Science 212:668–670
MacDonald DW (1997) The flexible social system of the golden jackal, Canis aureus. Behav Ecol Sociobiol 5:17–38
McLoughlin PD, Ferguson SH (2000) A hierarchical sequence of limiting factors may help explain variation in home range size. Ecoscience 7:123–130
McNab BK (1963) Bioenergetics and the determination of home range size. Am Nat 97:133–140
Mittermeier RA, Konstant WR, Hawkins F, Louis EE, Langrand O, Ratsimbazafy J, Rasoloarison RM, Ganzhorn J, Rajaobelina S, Tattersall I, Meyers DM (2006) Lemurs of Madagascar, 2nd edn. Conservation International, Washington, 520 p
Monson DH, Estes JA, Bodkin JL, Siniff DB (2000) Life history plasticity and population regulation in sea otters. Oikos 90:457–468
Muller AE (1999a) Aspects of social life in the fat-tailed dwarf lemur (Cheirogaleus medius): inferences from body weights and trapping data. Am J Primatol 49:265–280
Muller AE (1999b) Paternal investment in the monogamous fat-tailed dwarf lemur (Cheirogaleus medius) in northwestern Madagascar. Am J Phys Anthropol, Suppl. 28:207
Negus NC, Berger PJ (1987) Mammalian reproductive physiology: adaptive responses to changing environments. In: Genoways HH (ed) Current mammalogy, 1st edn. Plenum, New York, pp 149–173
Nicol S, Andersen NA (2002) The timing of hibernation in Tasmanian echidnas: why do they do it when they do? Comp Biochem Physiol 131:603–611
Olivieri G, Zimmermann E, Randrianambinina B, Rasoloharijaona S, Rakotondravony D, Guschanski K, Radespiel U (2007) The ever-increasing diversity in mouse lemurs: three new species in north and northwestern Madagascar. Mol Phylogenet Evol 43:309–327
Petter JJ (1978) Ecological and physiological adaptations of five sympatric nocturnal lemurs to seasonal variation in food production. In: Chivers DJ, Herbert J (eds) Recent advances in primatology. Academic, New York, pp 211–223
Pettorelli N, Gaillard JM, Yoccoz NG, Duncan P, Maillard D, Delorme D, van Laere G, Toigo C (2005) The response of fawn survival to changes in habitat quality varies according to cohort quality and spatial scale. J Anim Ecol 74:972–981
Pianka ER (1970) On r and K selection. Am Nat 104:592–597
Podlutsky AJ, Khritankov AM, Ovodov ND, Austad SN (2005) A new field record for bat longevity. J Gerontol Ser A: Biol Med Sci 60:1366–1368
Promislow DEL, Harvey PH (1990) Living fast and dying young—a comparative-analysis of life-history variation among mammals. J Zool 220:417–437
Radespiel U (2006) Ecological diversity and seasonal adaptations of mouse lemurs (Microcebus spp.). In: Gould LSML (ed) Lemurs: ecology and adaptation. Springer, Chicago, pp 211–234
Raharivololona BM (2009) Intestinal parasite infection of the gray mouse lemur (Microcebus murinus, J.F. Miller, 1777) in the south-eastern littoral forest of Madagascar. Thesis, University Hamburg
Randrianambinina B, Rakotondravony D, Radespiel U, Zimmermann E (2003) Seasonal changes in general activity, body mass and reproduction of two small nocturnal primates: a comparison of the golden brown mouse lemur (Microcebus ravelobensis) in Northwestern Madagascar and the brown mouse lemur (Microcebus rufus) in Eastern Madagascar. Primates 44:321–331
Reznick D, Nunney L, Tessier A (2000) Big houses, big cars, superfleas and the costs of reproduction. TREE 15:421–425
Ricklefs RE, Wikelski M (2002) The physiology-life history nexus. TREE 17:462–468
Roberts RL, Williams JR, Wang AK, Carter CS (1998) Cooperative breedings and monogamy in prairie voles: influence of the sire and geographical variation. Anim Behav 55:1131–1140
Rohner C, Krebs CJ (1998) Response of great horned owls to experimental “hot spots” of snowshoe hare density. Auk 115:694–705
Saether BE, Andersen R, Hjeljord O, Heim M (1996) Ecological correlates of regional variation in life history of the moose Alces alces. Ecol 77:1493–1500
Sand H (1996) Life history patterns in female moose (Alces alces): the relationship between age, body size, fecundity and environmental conditions. Oecol 106:212–220
Sand H, Cederlund G (1996) Individual and geographical variation in age at maturity in female moose (Alces alces). Can J Zool 74:954–964
Schmid J (2000) Daily torpor in the gray mouse lemur (Microcebus murinus) in Madagascar: energetic consequences and biological significance. Oecol 123:175–183
Schmid J, Ganzhorn JU (2009) Optional strategies for reduced metabolism in gray mouse lemurs. Naturwissenschaften 96:737–741
Schmid J, Speakman JR (2000) Daily energy expenditure of the grey mouse lemur (Microcebus murinus): a small primate that uses torpor. J Comp Physiol B 170:633–641
Schmid J, Speakman JR (2009) Torpor and energetic consequences in free-ranging grey mouse lemurs (Microcebus murinus): a comparison of dry and wet forests. Naturwissenschaften 96:609–620
Schradin C, Pillay N (2005) Intraspecific variation in the spatial and social organization of the African striped mouse. J Mammal 86:99–107
Schülke O, Ostner J (2007) Physiological ecology of cheirogaleid primates: variation in hibernation and torpor. Acta Ethnol 10:13–21
Schwensow N, Fietz J, Dausmann KH, Sommer S (2007) Neutral versus adaptive genetic variation in parasite resistance: importance of major histocompatibility complex supertypes in a free-ranging primate. Heredity 99:265–277
Sorg J-P, Rohner U (1996) Climate and tree phenology of the dry deciduous forest of the Kirindy Forest. Primate Rep 46:57–80
Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Stearns SC (2000) Life history evolution: successes, limitations, and prospects. Naturwissenschaften 87:476–486
Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, Princeton
Sterling EJ, Nguyen N, Fashing PJ (2000) Spatial patterning in nocturnal prosimians: a review of methods and relevance to studies of sociality. Am J Primatol 51:3–19
Tattersall I (2007) Madagascar's lemurs: cryptic diversity or taxonomic inflation? Evol Anthropol 16:12–23
Wauters L, Dhondt AA (1989) Body weight, longevity and reproductive success in red squirrels (Sciurus vulgaris). J Anim Ecol 58:637–651
Wilkinson GS, South JM (2002) Life history, ecology, and longevity in bats. Aging Cell 1:124–131
Acknowledgements
We are grateful to the Commission Tripartite of the Malagasy Government, to the Département de Paléonthologie et Anthropologie et Biologie Animale of the Université d'Antananarivo and to the Ministère pour la Production Animale et des Eaux et Forêts for their permission to work in Madagascar. We thank Joanna Fietz for her help with manuscript, her comments, and the provision of data. We would like to acknowledge QIT Madagascar Minerals and the Centre de Formation Professionnelle Forestière de Morondava for their permission to work on their concessions. We thank Jörg Ganzhorn, the German Primate Centre and Peter Kappeler for their support. The study complies with the current laws of Madagascar and was supported by the DAAD and the DFG.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by G. Wilkinson
Rights and permissions
About this article
Cite this article
Lahann, P., Dausmann, K.H. Live fast, die young: flexibility of life history traits in the fat-tailed dwarf lemur (Cheirogaleus medius). Behav Ecol Sociobiol 65, 381–390 (2011). https://doi.org/10.1007/s00265-010-1055-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-010-1055-4