Advertisement

International Journal of Primatology

, Volume 32, Issue 3, pp 566–586 | Cite as

Seasonal Changes in Feeding Ecology and Activity Patterns of Two Sympatric Mouse Lemur Species, the Gray Mouse Lemur (Microcebus murinus) and the Golden-brown Mouse Lemur (M. ravelobensis), in Northwestern Madagascar

  • Sandra Thorén
  • Franziska Quietzsch
  • Doreen Schwochow
  • Lalandy Sehen
  • Christopher Meusel
  • Kate Meares
  • Ute Radespiel
Article

Abstract

Because closely related species are likely to be ecologically similar owing to common ancestry, they should show some degree of differentiation in order to coexist. We studied 2 morphologically similar congeneric species, the golden-brown mouse lemur (Microcebus ravelobensis) and the gray mouse lemur (M. murinus). These species are found in partial sympatry in the dry deciduous forest in northwestern Madagascar. We investigated whether 1) feeding niche differentiation and/or 2) a reduction in locomotor activity during periods of food shortage, which might reflect an energy saving strategy, can explain the coexistence of these 2 lemur species. To obtain feeding and behavioral data, we conducted focal observations of 11 female Microcebus murinus and 9 female M. ravelobensis during 11 months from 2007 to 2008 and collected fecal samples for 6 mo. We monitored the phenology of 272 plant specimens and trapped arthropods to determine food availability. Results revealed interspecific differences in 1) relative proportion of consumed food resources, resulting in a merely partial dietary overlap, and in 2) relative importance of seasonally varying food resources throughout the year. In addition, females of Microcebus murinus showed a reduction in locomotor activity during the early dry season, which might reflect an energy-saving strategy and might further reduce potential competition with M. ravelobensis over limited food resources. To conclude, a combination of interspecific feeding niche differentiation and differences in locomotor activity appears to facilitate the coexistence of Microcebus murinus and M. ravelobensis.

Keywords

Activity budget Diet Feeding ecology Niche differentiation Seasonality 

Notes

Acknowledgments

We thank the Department des Eaux et Forêts (DEF), the members of CAFF/CORE, the University of Antananarivo (D. Rakotondravony and the late O. Ramilijaona), and the Association pour la Gestion des Aires Protégées (ANGAP) for permission to work in the Ankarafantsika National Park. We also thank the staff of the National Park for their continuous support. We thank Blanchard Randrianambinina, Solofo Rasoloharijaona, and Romule Rakotondravony for their valuable help during the study. Many thanks go to Sonja Kunath, Miriam Linnenbrink, Pièrre Razafindraibe, Fanomezantsoa Rakotonirina, and Roger Randrimparany for their enthusiastic help during data collection. The Durrell Wildlife Preservation Trust is acknowledged for providing the climate data of Ampijoroa. We also thank Albert Melber, who helped with arthropod identification; Roger Edmont for botanical expertise; Angie Faust for proofreading the manuscript; and the editor and 2 anonymous reviewers for helpful comments on the manuscript. All field handling and sampling procedures adhered to the legal requirements of Madagascar and were approved by the Ministry of Water and Forests. We have complied with the ethical standards for the treatment of primates and with the national laws and research rules formulated by the Malagasy authorities.

References

  1. Amarasekare, P. (2003). Competitive coexistence in spatially structured environments: A synthesis. Ecology Letters, 6, 1109–1122.CrossRefGoogle Scholar
  2. Atsalis, S. (1999). Seasonal fluctuations in body fat and activity levels in a rain-forest species of mouse lemur, Microcebus rufus. International Journal of Primatology, 20, 883–910.CrossRefGoogle Scholar
  3. Azevedo, F. C. C., Lester, V., Gorsuch, W., Lariviere, S., Wirsing, A. J., & Murray, D. L. (2006). Dietary breadth and overlap among five sympatric prairie carnivores. Journal of Zoology, 269, 127–135.CrossRefGoogle Scholar
  4. Bearder, S. K., & Doyle, G. A. (1974). Ecology of bushbabies Galago senegalensis and Galago crassicaudatus, with some notes on their behaviour in the field. PLoS Biology, 109–130.Google Scholar
  5. Behmer, S. T., & Joern, A. (2008). Coexisting generalist herbivores occupy unique nutritional feeding niches. Proceedings of the National Academy of Sciences of the United States of America, 105, 1977–1982.PubMedCrossRefGoogle Scholar
  6. Brown, Jr. W. L., & Wilson, E. O. (1956). Character displacement. Systematic Zoology, 49–64.Google Scholar
  7. Chase, J. M., & Leibold, M. A. (2003). Ecological niches: Linking classical and contemporary approaches. Chicago: University of Chicago Press.Google Scholar
  8. Cox, C. B., & Moore, P. D. (2000). Biogeography: An ecological and evolutionary approach. Oxford: Blackwell Scientific Press.Google Scholar
  9. Dammhahn, M., & Kappeler, P. M. (2005). Social system of Microcebus berthae, the world’s smallest primate. International Journal of Primatology, 26, 407–435.CrossRefGoogle Scholar
  10. Dammhahn, M., & Kappeler, P. M. (2008a). Small-scale coexistence of two mouse lemur species (Microcebus berthae and M, murinus) within a homogeneous competitive environment. Oecologia, 157, 473–483.PubMedCrossRefGoogle Scholar
  11. Dammhahn, M., & Kappeler, P. M. (2008b). Comparative feeding ecology of sympatric Microcebus berthae and M. murinus. International Journal of Primatology, 29, 1567–1589.CrossRefGoogle Scholar
  12. Dammhahn, M., & Kappeler, P. M. (2010). Scramble or contest competition over food in solitarily foraging mouse lemurs (Microcebus spp.): New insights from stable isotopes. American Journal of Physical Anthropology, 141, 181–189.PubMedGoogle Scholar
  13. Dausmann, K. H., Glos, J., Ganzhorn, J. U., & Heldmaier, G. (2004). Hibernation in a tropical primate. Nature, 429, 825–826.PubMedCrossRefGoogle Scholar
  14. Dausmann, K. H., Glos, J., Ganzhorn, J. U., & Heldmaier, G. (2005). Hibernation in the tropics: Lessons from a primate. Journal of Comparative Physiology B, 175, 147–155.CrossRefGoogle Scholar
  15. Fietz, J., & Ganzhorn, J. U. (1999). Feeding ecology of the hibernating primate Cheirogaleus medius: How does it get so fat? Oecologia, 121, 157–164.CrossRefGoogle Scholar
  16. Ganzhorn, J. U. (1988). Food partitioning among Malagasy Primates. Oecologia, 75, 436–450.CrossRefGoogle Scholar
  17. Ganzhorn, J. U. (1989). Niche separation of seven lemur species in the eastern rainforest of Madagascar. Oecologia, 79, 279–286.CrossRefGoogle Scholar
  18. Ganzhorn, J. U., Wright, P. C., & Ratsimbazafy, J. (1999). Primate communities: Madagascar. In J. G. Fleagle, C. Janson, & K. E. Reed (Eds.), Primate communities (pp. 75–89). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  19. Garcia, J. T., & Arroyo, B. E. (2005). Food-niche differentiation in sympatric Hen Circus cyaneus and Montagu’s Harriers Circus pygargus. Ibis, 147, 144–154.CrossRefGoogle Scholar
  20. Gause, G. F. (1934). The struggle for existence. Baltimore: Williams & Wilkins.Google Scholar
  21. Génin, F. (2008). Life in unpredictable environments: First investigation of the natural history of Microcebus griseorufus. International Journal of Primatology, 29, 303–321.CrossRefGoogle Scholar
  22. 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 Primatologica, 69, 342–356.CrossRefGoogle Scholar
  23. Hardin, G. (1960). The competitive exclusion principle. Science, 131, 1292–1297.PubMedCrossRefGoogle Scholar
  24. Hladik, C. M., Charles-Dominique, P., & Petter, J. J. (1980). Feeding strategies of five nocturnal prosimians in the dry forest of the west coast of Madagascar. In P. Charles-Dominique, H. M. Cooper, A. Hladik, C. M. Hladik, E. Pages, G. F. Pariente, A. Petter-Rousseaux, A. Schilling, & J. J. Petter (Eds.), Nocturnal Malagasy primates: Ecology, physiology and behaviour (pp. 41–73). New York: Academic.Google Scholar
  25. Houle, A., Vickery, W. L., & Chapman, C. A. (2006). Testing mechanisms of coexistence among two species of frugivorous primates. The Journal of Animal Ecology, 75, 1034–1044.PubMedCrossRefGoogle Scholar
  26. Joly, M., & Zimmermann, E. (2007). First evidence for relocation of stationary food resources during foraging in a strepsirhine primate (Microcebus murinus). American Journal of Primatology, 69, 1045–1052.PubMedCrossRefGoogle Scholar
  27. Kobbe, S., & Dausmann, K. H. (2009). Hibernation in Malagasy mouse lemurs as a strategy to counter environmental challenge. Die Naturwissenschaften, 96, 1221–1227.PubMedCrossRefGoogle Scholar
  28. Krebs, C. J. (1989). Niche overlap and diet analysis. Ecological methodology (pp. 371–407). New York: HarperCollins.Google Scholar
  29. 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. Journal of Zoology, 271, 88–98.CrossRefGoogle Scholar
  30. Lahann, P. (2008). Habitat utilization of three sympatric cheirogaleid lemur species in a littoral rain forest of southeastern Madagascar. International Journal of Primatology, 29, 117–134.CrossRefGoogle Scholar
  31. Mester, S. (2006). Populationsdynamik nachtaktiver Kleinlemuren (Microcebus murinus und M. ravelobensis) in Nordwest-Madagaskar. Doctoral dissertation, University of Veterinary Medicine, Hannover, Germany.Google Scholar
  32. Mittermeier, R. A., Konstant, W. R., Hawkins, F., Louis, E. E., Langrand, O., Ratsimbazafy, J., et al. (2008). Lemur diversity in Madagascar. International Journal of Primatology, 29, 1607–1656.CrossRefGoogle Scholar
  33. Olivieri, G., Zimmermann, E., Randrianambinina, B., Rasoloharijaona, S., Rakotondravony, D., Guschanski, K., et al. (2007). The ever-increasing diversity in mouse lemurs: Three new species in north and northwestern Madagascar. Molecular Phylogeny and Evolution, 43, 309–327.CrossRefGoogle Scholar
  34. Peres, C. A. (1993). Diet and feeding ecology of saddle-back (Saguinus fuscicollis) and moustached (S. mystax) tamarins in an Amazonian terra firme forest. Journal of Zoology, 230, 567–592.CrossRefGoogle Scholar
  35. Petter, J. J. (1962). Ecological and behavioural studies of Madagascar lemurs in the field. Annals of the New York Academy of Sciences, 102, 267–281.PubMedCrossRefGoogle Scholar
  36. Pianka, E. R. (1973). The structure of lizard communities. Annual Review of Ecology and Systematics, 4, 53–74.CrossRefGoogle Scholar
  37. Radespiel, U. (1998). Die soziale Organisation des grauen Mausmakis (Microcebus murinus, J. F. Miller 1777). Eine freilandbiologische und labor-experimentelle Studie, Doctoral dissertation, University of Hannover, Germany.Google Scholar
  38. Radespiel, U. (2006). Ecological diversity and seasonal adaptations of mouse lemurs (Microcebus spp.). In L. Gould & M. L. Sauther (Eds.), Lemur ecology and adaptation (pp. 211–233). New York: Springer.Google Scholar
  39. Radespiel, U., Reimann, W., Rahelinirina, M., & Zimmermann, E. (2006). Feeding ecology of sympatric mouse lemur species in northwestern Madagascar. International Journal of Primatology, 27, 311–321.CrossRefGoogle Scholar
  40. Rakotondravony, R., & Radespiel, U. (2009). Varying patterns of coexistence of two mouse lemur species (Microcebus ravelobensis and M. murinus) in a heterogeneous landscape. American Journal of Primatology, 71, 928–938.PubMedCrossRefGoogle Scholar
  41. 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.PubMedCrossRefGoogle Scholar
  42. Rasoazanabary, E. (2004). A preliminary study of mouse lemurs in the Beza Mahafaly Special Reserve, southwest Madagascar. Lemur News, 9, 4–7.Google Scholar
  43. Rasolofoson, D., Rakotondratsimba, G., Rakotonirainy, O., Rakotozafy, L., Ratsimbazafy, J., Rabetafika, L., et al. (2007). Influences des pressions anthropiques sur les lé-muriens d’Anantaka, dans la partie est du Plateau de Makira, Maroantsetra, Madagascar. Madagascar Conservation and Development, 2, 21–27.Google Scholar
  44. Reimann, W. E. (2002). Koexistenz und Nahrungsökologie von Weibchen des grauen und goldbraunen Mausmakis (Microcebus murinus und M. ravelobensis) in Nordwest-Madagaskar. Doctoral dissertation, University of Veterinary Medicine, Hannover.Google Scholar
  45. Rendigs, A., Radespiel, U., Wrogemann, D., & Zimmermann, E. (2003). Relationship between microhabitat structure and distribution of mouse lemurs (Microcebus spp.) in Northwestern Madagascar. International Journal of Primatology, 24, 47–64.CrossRefGoogle Scholar
  46. Renkonen, O. (1938). Statistisch-ökologische Untersuchungen über die terrestrische Käferwelt der finnischen Bruchmoore. Annales Botanici Societatis Zoologicae Botanicae Fennicae Vanamo, 6, 1–231.Google Scholar
  47. 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 W. R. Lourenço & S. M. Goodman (Eds.), Diversité et endémisme à Madagascar (pp. 165–175). Mémoires de la Société de Biogéographie, Paris.Google Scholar
  48. Schmid, J. (1999). Sex-specific differences in activity patterns and fattening in the gray mouse lemur (Microcebus murinus) in Madagascar. Journal of Mammalogy, 749–757.Google Scholar
  49. Schmid, J. (2000). Daily torpor in the grey mouse lemur (Microcebus murinus) in Madagascar: Energetical consequences and biological significance. Oecologia, 123, 175–183.CrossRefGoogle Scholar
  50. Schmid, J., & Ganzhorn, J. U. (2009). Optional strategies for reduced metabolism in gray mouse lemurs. Die Naturwissenschaften, 96, 737–741.PubMedCrossRefGoogle Scholar
  51. Schmid, J., & Kappeler, P. M. (1998). Fluctuating sexual dimorphism and differential hibernation by sex in a primate, the gray mouse lemur (Microcebus murinus). Behavioral Ecology and Sociobiology, 43, 125–132.CrossRefGoogle Scholar
  52. Schmid, J., & Kappeler, P. M. (2005). Physiologieal adaptations to seasonality. In D. K. Brockman & C. P. van Schaik (Eds.), Primate seasonality: Implications for human Evolution (pp. 129–155). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  53. Schmid, J., Ruf, T., & Heldmaier, G. (2000). Metabolism and temperature regulation during daily torpor in the smallest primate, the pygmy mouse lemur (Microcebus myoxinus) in Madagascar. Journal of Comparative Physiology B, 170, 59–68.CrossRefGoogle Scholar
  54. Schülke, O., & Ostner, J. (2007). Physiological ecology of cheirogaleid primates: Variation in hibernation and torpor. Acta Ethologica, 10, 13–21.CrossRefGoogle Scholar
  55. Schwab, D. (2000). A preliminary study of spatial distribution and mating system of pygmy mouse lemurs (Microcebus cf myoxinus). American Journal of Primatology, 51, 41–60.PubMedCrossRefGoogle Scholar
  56. Schwab, D., & Ganzhorn, J. U. (2004). Distribution, population structure and habitat use of Microcebus berthae compared to those of other sympatric cheirogalids. International Journal of Primatology, 25, 307–330.CrossRefGoogle Scholar
  57. Statistica Version 6.1 (2004). StatSoft® Inc., Tulsa, USA.Google Scholar
  58. Sushma, H. S., & Singh, M. (2006). Resource partitioning and interspecific interactions among sympatric rain forest arboreal mammals of the Western Ghats, India. Behavioral Ecology, 17, 479.CrossRefGoogle Scholar
  59. Thalmann, U. (2001). Food resource characteristics in two nocturnal lemurs with different social behavior: Avahi occidentalis and Lepilemur edwardsi. International Journal of Primatology, 22, 287–324.CrossRefGoogle Scholar
  60. Trivers, R. L. (1972). Sexual selection and the descent of man. In B. Campbell (Ed.), Parental investment and sexual selection (pp. 136–179). Chicago: Aldine.Google Scholar
  61. Weidt, A. (2001). Ökologie und Sozialbiologie von Weibchen des goldbraunen Mausmakis (Microcebus ravelobensis) während der Trockenzeit in Nordwest Madagaskar. Diploma thesis, Göttingen University, Göttingen, Germany.Google Scholar
  62. Yoder, A. D., Burns, M. M., & Génin, F. (2002). Molecular evidence of reproductive isolation in sympatric sibling species of mouse lemurs. International Journal of Primatology, 23, 1335–1343.CrossRefGoogle Scholar
  63. 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 Primatologica, 69, 106–114.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Sandra Thorén
    • 1
  • Franziska Quietzsch
    • 1
  • Doreen Schwochow
    • 2
  • Lalandy Sehen
    • 3
    • 4
  • Christopher Meusel
    • 1
  • Kate Meares
    • 1
  • Ute Radespiel
    • 1
  1. 1.Institute of ZoologyUniversity of Veterinary Medicine HanoverHanoverGermany
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of CaliforniaLos AngelesUSA
  3. 3.Institute of ZoologyUniversity of Veterinary Medicine HanoverHanoverGermany
  4. 4.Department of Botany, Faculty of ScienceUniversity of AntananarivoAntananarivoMadagascar

Personalised recommendations