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.
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References
Aschoff J (1955) Jahresperiodik der Fortpflanzung beim Warmblüter. Stud Gen 8:742–776
Atsalis S (1999a) Diet of the brown mouse lemur (Microcebus rufus) in Ranomafana National Park, Madagascar. Int J Primatol 20:193–229
Atsalis S (1999b) Seasonal fluctuations in body fat and activity levels in a rain-forest species of mouse lemur, Microcebus rufus. Int J Primatol 20:883–910
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 51:61–78
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 168:540–548
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 114:492–498
Bartness TJ, Wade GN (1985) Photoperiodic control of seasonal body weight cycles in hamsters. Neurosci Biobehav Rev 9:599–612
Bercovitch FB (1989) Body size, sperm competition, and determinants of reproductive success in male savanna baboons. Evolution 43:1507–1521
Bronson FH (1989) Mammalian reproductive biology. University of Chicago Press, Chicago, Ill. pp 325
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:575–578
Dark J, Zucker I (1986) Photoperiodic regulation of body mass and fat reserves in the meadow vole. Physiol Behav 38:851–854
Fietz J (1998) Body mass in wild Microcebus murinus over the dry season. Folia Primatol 69:183–190
Ganzhorn JU, Schmid J (1998) Different population dynamics of Microcebus murinus in primary and secondary deciduous dry forests of Madagascar. Int J.Primatol 19:785–795
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 48:1–81
Geiser F, Ruf T (1995) Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiol Zool 68:935–966
Génin F, Perret M (2000) Photoperiod-induced changes in energy balance in gray mouse lemurs. Physiol Behav 71:315–321
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 69:342–356
Harcourt C, Thornback J (1990) Lemurs of Madagascar and the Comoros. The IUCN red data book. IUCN, Gland
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 130–139
IUCN (2002) Redlist. http://www.redlist.org.
Körtner G, Geiser F (2000) The temporal organization of daily torpor and hibernation: circadian and circannual rhythms. Chronobiol Int 17:103–128
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-R1018
Lutermann H (2001) Weibchenassoziationen und Fortpflanzungsstrategien beim Grauen Mausmaki (Microcebus murinus) in Nordwest-Madagaskar. PhD thesis, University of Hannover, Hannover
Martin RD (1972) A preliminary field-study of the lesser mouse lemur (Microcebus murinus J.F. Miller 1777). Z Tierpsychol 9:43–89
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 535–563
Mittermeier RA, Tattersall I, Konstant WR, Meyers D M, Mast RB (1994) Lemurs of Madagascar. Conservation International, Washington, DC, pp 356
Nagy TM, Negus NC (1993) Energy acquisition and allocation in male collared lemmings (Dicrostonyx groenlandicus): effects of photoperiod, temperature and diet quality. Physiol Zool 66:537–560
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 19:45–56
Perret M (1992) Environmental and social determinants of sexual function in the male lesser mouse lemur (Microcebus murinus ). Folia Primatol 59:1–25
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 22:5–24
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 119:981–989
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, Hannover
Radespiel U (2000) Sociality in the gray mouse lemur (Microcebus murinus) in northwestern Madagascar. Am J Primatol 51:21–40
Radespiel U, Zimmermann E (2001) Female dominance in captive gray mouse lemurs (Microcebus murinus). Am J Primatol 54:181–192
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 46:77–84
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 42:207–220
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 50:493–502
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, Madagascar
Rasoloarison RM, Goodman SM, Ganzhorn JU (2000) Taxonomic revision of mouse lemurs (Microcebus) in the western portions of Madagascar. Int J Primatol 21:963–1019
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]:19
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 24:47–64
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, Hannover
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 165–175
Schmid J (1999) Sex-specific differences in activity patterns and fattening in the gray mouse lemur (Microcebus murinus) in Madagascar. J Mammal 80:749–757
Schmid J (2001) Daily torpor in free-ranging gray mouse lemurs (Microcebus murinus) in Madagascar. Int J Primatol 22:1021–1031
Schmid J, Kappeler PM (1994) Sympatric mouse lemurs (Microcebus spp.) in western Madagascar. Folia Primatol 63:162–170
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 43:125–132
Siegel S (1987) Nichtparametrische statistische Methoden. Fachbuchhandlung für Psychologie, Eschborn pp 320
Sokal R, Rohlf (1995) Biometry, 3rd edn Freeman, New York
Stanger KF, Coffman BS, Izard MK (1995) Reproduction in Coquerel's dwarf lemur (Mirza coquereli). Am J Primatol 36:223–237
Steinlechner S, Niklowitz P (1992) Impact of photoperiod and melatonin on reproduction in small mammals. Anim Reprod Sci 30:1–18
Steinlechner S, Puchalski W (2002) Environmental signal processing and adaptation. In: Heldmaier G, Werner D (eds) SFB-Buch. Springer, Berlin Heidelberg New York pp 233–250
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)
Wrogemann D, Glatston AR (2001) Mouse lemur biology in breeding colonies: introduction. Int J Primatol 22:1–3
Wrogemann D, Zimmermann E (2001) Aspects of reproduction in the eastern rufous mouse lemur (Microcebus rufus) and their implications for captive management. Zoo Biol 20:157–167
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 22:91–108
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 97:11325–11330
Zimmermann E, Hafen TG (2001) Colony specificity in a social call of mouse lemurs (Microcebus ssp.). Am J Primatol 54:129–141
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 93:211–224
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 69:106–114
Zimmermann E, Masters J, Rumpler Y (2000a) Introduction to diversity and speciation in the Prosimii. Int J Primatol 21:789–791
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 21:837–852
Acknowledgements
We thank the 'Commission Tripartite' of the Malagasy Government and the Ministère des Eaux et Forêt, the Association National pour la Gestion des Aires Protégées, Conservation International, KfW and Professor Berthe Rakotosamimanana for their permission and logistical support to work in Madagascar. We thank Dr. Solofonirina Rasoloharijaona, Michel Bisoa, Jofetra Randrianarivony and Romain Rajaonirinaharison for their unflagging help and support in Ampijoroa and Mantadia and Elisabeth Engelke and Rüdiger Brüning for technical assistance. Stephan Steinlechner read the manuscript and gave helpful comments. This study was supported by the Volkswagenstiftung (I/72 968) and DAAD (Sandwich-Fellowship to B.R.).
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Randrianambinina, B., Rakotondravony, D., Radespiel, U. et al. 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 (2003). https://doi.org/10.1007/s10329-003-0046-8
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DOI: https://doi.org/10.1007/s10329-003-0046-8