Primates

, Volume 44, Issue 4, pp 321–331 | Cite as

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

  • Blanchard Randrianambinina
  • Daniel Rakotondravony
  • Ute Radespiel
  • Elke Zimmermann
Original Article

Abstract

To investigate for the first time the relationship between contrasting patterns of seasonal changes of the environment and activity, body mass and reproduction for small nocturnal primates in nature, we compared a population of golden brown mouse lemur (Microcebus ravelobensis) in a dry deciduous forest of northwestern Madagascar and of the brown mouse lemur (Microcebus rufus) in an evergreen rain forest of eastern Madagascar. Both species live under similar photoperiodic conditions. Golden brown mouse lemurs (GBML) were active during the whole period (May to December) irrespective of changing environmental conditions. In contrast, a part of the population of brown mouse lemurs (BML) showed prolonged seasonal torpor, related to body mass during periods of short day length and low ambient temperatures. Differences between species might be due to differences in ambient temperature and food supply. Body weight and tail thickness (adipose tissue reserve) did not show prominent differences between short and long photoperiods in GBML, whereas both differ significantly in BML, suggesting species-specific differences in the photoperiodically driven control of metabolism. Both species showed a seasonal reproduction. The rate of growth and size of the testes were similar and preceded estrous onset in both species suggesting a photoperiodic control of reproduction in males. The estrous onset in females occurred earlier in GBML than in BML. Estrous females were observed over at least 4 months in the former, but in only 1 month in the latter species. Intraspecific variation of estrous onset in GBML may be explained by body mass. Interspecific variation of female reproduction indicates species-specific differences in the control of reproduction. Thus, environmentally related differences in annual rhythms between closely related small nocturnal lemurs emerged that allow them to cope with contrasting patterns of seasonal changes in their habitats.

Keywords

Seasonality Torpor Body mass Reproduction Mouse lemur 

References

  1. Aschoff J (1955) Jahresperiodik der Fortpflanzung beim Warmblüter. Stud Gen 8:742–776Google Scholar
  2. Atsalis S (1999a) Diet of the brown mouse lemur (Microcebus rufus) in Ranomafana National Park, Madagascar. Int J Primatol 20:193–229CrossRefGoogle Scholar
  3. Atsalis S (1999b) Seasonal fluctuations in body fat and activity levels in a rain-forest species of mouse lemur, Microcebus rufus. Int J Primatol 20:883–910Google Scholar
  4. Atsalis S (2000) Spatial distribution and population composition of the brown mouse lemur (Microcebus rufus) in Ranomafana National Park, Madagascar, and its implications for social organization. Am J Primatol 51:61–78CrossRefPubMedGoogle Scholar
  5. Aujard F, Perret M, Vannier G (1998) Thermoregulatory responses to variations of photoperiod and ambient temperature in the male lesser mouse lemur: a primitive or an advanced adaptive character? J Comp Physiol B 168:540–548Google Scholar
  6. Bartness TJ, Wade GN (1984) Photoperiodic control of body weight and energy metabolism in Syrian hamsters (Mesocricetus aurantus): role of pineal gland, melatonin, gonads and diet. Endocrinology 114:492–498PubMedGoogle Scholar
  7. Bartness TJ, Wade GN (1985) Photoperiodic control of seasonal body weight cycles in hamsters. Neurosci Biobehav Rev 9:599–612CrossRefPubMedGoogle Scholar
  8. Bercovitch FB (1989) Body size, sperm competition, and determinants of reproductive success in male savanna baboons. Evolution 43:1507–1521Google Scholar
  9. Bronson FH (1989) Mammalian reproductive biology. University of Chicago Press, Chicago, Ill. pp 325Google Scholar
  10. Canguilhem B, Masson-Pevet M, Koehl C, Pevet P, Bentz I (1988) Non-gonadal mediated effect of photoperiod on hibernation and body weight cycles of the European hamster. Comp Biochem Physiol 89A:575–578CrossRefGoogle Scholar
  11. Dark J, Zucker I (1986) Photoperiodic regulation of body mass and fat reserves in the meadow vole. Physiol Behav 38:851–854CrossRefPubMedGoogle Scholar
  12. Fietz J (1998) Body mass in wild Microcebus murinus over the dry season. Folia Primatol 69:183–190CrossRefGoogle Scholar
  13. Ganzhorn JU, Schmid J (1998) Different population dynamics of Microcebus murinus in primary and secondary deciduous dry forests of Madagascar. Int J.Primatol 19:785–795CrossRefGoogle Scholar
  14. Ganzhorn JU, Rakotosamimanana B, Hannah L, Hough J, Iyer L, Olivieri S, Rajaobelina S, Rodstrom C, Tilkin G (1997) Priorities for biodiversity conservation in Madagascar. Primate Rep 48:1–81Google Scholar
  15. Geiser F, Ruf T (1995) Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiol Zool 68:935–966Google Scholar
  16. Génin F, Perret M (2000) Photoperiod-induced changes in energy balance in gray mouse lemurs. Physiol Behav 71:315–321CrossRefPubMedGoogle Scholar
  17. Hafen T, Neveu H, Rumpler Y, Wilden I, Zimmermann E (1998) Acoustically dimorphic advertisement calls separate morphologically and genetically homogenous populations of the grey mouse lemur (Microcebus murinus). Folia Primatol 69:342–356PubMedGoogle Scholar
  18. Harcourt C, Thornback J (1990) Lemurs of Madagascar and the Comoros. The IUCN red data book. IUCN, GlandGoogle Scholar
  19. Heldmaier G (1989) Seaonal acclimatization of energy requirements in mammals: functional significance of body weight control, hypothermia, torpor and hibernation. In: Wieser W, Gnaiger E (eds) Energy transformations in cells and organisms. Georg Thieme, Stuttgart pp 130–139Google Scholar
  20. IUCN (2002) Redlist. http://www.redlist.org.Google Scholar
  21. Körtner G, Geiser F (2000) The temporal organization of daily torpor and hibernation: circadian and circannual rhythms. Chronobiol Int 17:103–128CrossRefGoogle Scholar
  22. Kriegsfeld LJ, Nelson RJ (1996) Gonadal and photoperiodic influences on body mass regulation in adult male and female prairie volves. Am J Physiol 270:R1013-R1018PubMedGoogle Scholar
  23. Lutermann H (2001) Weibchenassoziationen und Fortpflanzungsstrategien beim Grauen Mausmaki (Microcebus murinus) in Nordwest-Madagaskar. PhD thesis, University of Hannover, HannoverGoogle Scholar
  24. Martin RD (1972) A preliminary field-study of the lesser mouse lemur (Microcebus murinus J.F. Miller 1777). Z Tierpsychol 9:43–89Google Scholar
  25. Martin RD (1995) Prosimians: from obscurity to extinction? In: Alterman L, Doyle GA, Izard MK (eds) Creatures of the dark: the nocturnal prosimians. Plenum, New York, pp 535–563Google Scholar
  26. Mittermeier RA, Tattersall I, Konstant WR, Meyers D M, Mast RB (1994) Lemurs of Madagascar. Conservation International, Washington, DC, pp 356Google Scholar
  27. Nagy TM, Negus NC (1993) Energy acquisition and allocation in male collared lemmings (Dicrostonyx groenlandicus): effects of photoperiod, temperature and diet quality. Physiol Zool 66:537–560Google Scholar
  28. Pastorini J, Martin RD, Ehresmann P, Zimmermann E, Forstner MRJ (2001) Molecular phylogeny of the lemur family Cheirogaleidae (Primates) based on mitochondrial DNA sequences. Mol Phylogenet Evol 19:45–56CrossRefPubMedGoogle Scholar
  29. Perret M (1992) Environmental and social determinants of sexual function in the male lesser mouse lemur (Microcebus murinus ). Folia Primatol 59:1–25PubMedGoogle Scholar
  30. 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. Int J Primatol 22:5–24Google Scholar
  31. Perret M, Aujard F, Vannier G (1998) Influence of day length on metabolic rate and daily water loss in the male prosimian primate Microcebus murinus. Comp Biochem Physiol A 119:981–989CrossRefGoogle Scholar
  32. Radespiel U (1998) Die soziale Organisation des grauen Mausmakis (Microcebus murinus, J.F. Miller 1777): eine freilandökologische und laborexperimentelle Studie. PhD thesis, University of Hannover, HannoverGoogle Scholar
  33. Radespiel U (2000) Sociality in the gray mouse lemur (Microcebus murinus) in northwestern Madagascar. Am J Primatol 51:21–40PubMedGoogle Scholar
  34. Radespiel U, Zimmermann E (2001) Female dominance in captive gray mouse lemurs (Microcebus murinus). Am J Primatol 54:181–192CrossRefPubMedGoogle Scholar
  35. Radespiel U, Cepok S, Zietemann V, Zimmermann E (1998) Sex-specific usage patterns of sleeping sites in grey mouse lemurs (Microcebus murinus) in Northwestern Madagascar. Am J Primatol 46:77–84PubMedGoogle Scholar
  36. Radespiel U, Ehresmann P, Zimmermann E (2001a) Contest versus scramble competition for mates: the composition and spatial structure of a population of gray mouse lemurs (Microcebus murinus) in north-west Madagascar. Primates 42:207–220Google Scholar
  37. Radespiel U, Sarikaya Z, Zimmermann E, Bruford MW (2001b) Sociogenetic structure in a free-living nocturnal primate population: sex-specific differences in the grey mouse lemur (Microcebus murinus). Behav Ecol Sociobiol 50:493–502CrossRefGoogle Scholar
  38. Randrianambinina, B. (2001) Contribution à l'étude comparative de l'écoéthologie de deux microcèbes rouges de Madagascar Microcebus ravelobensis (Zimmermann et al. 1998) Microcebus rufus (Lesson, 1840). Doctorat de troisième cycle, Université d'Antananarivo, Antananarivo, MadagascarGoogle Scholar
  39. Rasoloarison RM, Goodman SM, Ganzhorn JU (2000) Taxonomic revision of mouse lemurs (Microcebus) in the western portions of Madagascar. Int J Primatol 21:963–1019CrossRefGoogle Scholar
  40. Reimann W, Zimmermann E (2002) Feeding ecology of females of two sympatric lemurs in northwestern Madagascar: Microcebus murinus and Microcebus ravelobensis. Zoology 105 [Suppl V]:19Google Scholar
  41. Rendings A, Radespiel U, Wrogemann D, Zimmermann E (2003) Relationship between microhabitat structure and distribution of mouse lemurs (Microcebus ssp.) of northwestern Madagascar. Int J Primatol 24:47–64CrossRefGoogle Scholar
  42. Schmelting B (2000) Saisonale Aktivität und Reproduktionsbiologie von Grauen Mausmaki-Männchen (Microcebus murinus, J.F. Miller 1777) in Nordwest-Madagaskar. PhD thesis, Tierärztliche Hochschule Hannover, HannoverGoogle Scholar
  43. Schmelting B, Ehresmann P, Lutermann H, Randrianambinina B, Zimmermann E (2000) Reproduction of two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in north-west Madagascar: first results of a long term study. In: Lourenço WR, Goodman SM (eds) Diversité et Endémisme à Madagascar Mémoires de la Société de Biogéographie, Paris, pp 165–175Google Scholar
  44. Schmid J (1999) Sex-specific differences in activity patterns and fattening in the gray mouse lemur (Microcebus murinus) in Madagascar. J Mammal 80:749–757Google Scholar
  45. Schmid J (2001) Daily torpor in free-ranging gray mouse lemurs (Microcebus murinus) in Madagascar. Int J Primatol 22:1021–1031CrossRefGoogle Scholar
  46. Schmid J, Kappeler PM (1994) Sympatric mouse lemurs (Microcebus spp.) in western Madagascar. Folia Primatol 63:162–170PubMedGoogle Scholar
  47. Schmid J, Kappeler PM (1998) Fluctuating sexual dimorphism and differential hibernation by sex in a primate, the gray mouse lemur (Microcebus murinus). Behav Ecol Sociobiol 43:125–132CrossRefGoogle Scholar
  48. Siegel S (1987) Nichtparametrische statistische Methoden. Fachbuchhandlung für Psychologie, Eschborn pp 320Google Scholar
  49. Sokal R, Rohlf (1995) Biometry, 3rd edn Freeman, New YorkGoogle Scholar
  50. Stanger KF, Coffman BS, Izard MK (1995) Reproduction in Coquerel's dwarf lemur (Mirza coquereli). Am J Primatol 36:223–237Google Scholar
  51. Steinlechner S, Niklowitz P (1992) Impact of photoperiod and melatonin on reproduction in small mammals. Anim Reprod Sci 30:1–18Google Scholar
  52. Steinlechner S, Puchalski W (2002) Environmental signal processing and adaptation. In: Heldmaier G, Werner D (eds) SFB-Buch. Springer, Berlin Heidelberg New York pp 233–250Google Scholar
  53. Weidt A, Hagenah N, Randrianambinina B, Radespiel U, Zimmermann E (2003) The social organization of the golden brown mouse lemur (Microcebus ravelobensis). Am J Phys Anthrop (in press)Google Scholar
  54. Wrogemann D, Glatston AR (2001) Mouse lemur biology in breeding colonies: introduction. Int J Primatol 22:1–3Google Scholar
  55. Wrogemann D, Zimmermann E (2001) Aspects of reproduction in the eastern rufous mouse lemur (Microcebus rufus) and their implications for captive management. Zoo Biol 20:157–167CrossRefGoogle Scholar
  56. Wrogemann D, Radespiel U, Zimmermann E (2001) Comparison of reproductive characteristics and changes in body weight between captive populations of rufous and gray mouse lemurs. Int J Primatol 22:91–108Google Scholar
  57. Yoder AD, Rasoloarison RM, Goodman SM, Irwin JA, Atsalis S, Ravosa MJ, Ganzhorn JU (2000) Remarkable species diversity in Malagasy mouse lemurs (Primates, Microcebus). Proc Natl Acad Sci USA 97:11325–11330CrossRefPubMedGoogle Scholar
  58. Zimmermann E, Hafen TG (2001) Colony specificity in a social call of mouse lemurs (Microcebus ssp.). Am J Primatol 54:129–141CrossRefPubMedGoogle Scholar
  59. Zimmermann E, Lerch C (1993) The complex acoustic design of an advertisement call in male mouse lemurs (Microcebus murinus, Prosimii, Primates) and sources of its variation. Ethology 93:211–224Google Scholar
  60. Zimmermann E, Cepok S, Rakotoarison N, Zietemann V, Radespiel U (1998) Sympatric mouse lemurs in north-west Madagascar: a new rufous mouse lemur species (Microcebus ravelobensis). Folia Primatol 69:106–114PubMedGoogle Scholar
  61. Zimmermann E, Masters J, Rumpler Y (2000a) Introduction to diversity and speciation in the Prosimii. Int J Primatol 21:789–791CrossRefGoogle Scholar
  62. Zimmermann E, Vorobieva E, Wrogemann D, Hafen T (2000b) Use of vocal fingerprinting for specific discrimination of gray (Microcebus murinus) and rufous mouse lemurs (Microcebus rufus). Int J Primatol 21:837–852CrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer-Verlag 2003

Authors and Affiliations

  • Blanchard Randrianambinina
    • 1
    • 2
  • Daniel Rakotondravony
    • 2
  • Ute Radespiel
    • 1
  • Elke Zimmermann
    • 1
  1. 1.Institut für ZoologieTierärztliche Hochschule Hannover HannoverGermany
  2. 2.Départment de Biologie AnimaleUniversité d'AntananarivoAntananarivoMadagascar

Personalised recommendations