Gummivory in Cheirogaleids: Primitive Retention or Adaptation to Hypervariable Environments?

  • Fabien G. S. Génin
  • Judith C. Masters
  • Jorg U. Ganzhorn
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)


Gummivory in cheirogaleids, apart from the specialist gummivore Phaner, is often viewed as a fall-back diet; animals are forced to consume gums when other foods are unavailable. We propose an alternative explanation that cheirogaleid gummivory is an adaptation to hypervariable environments. First, we compared morphological adaptations to gummivory evinced by cheirogaleids and other gummivorous primates. Despite convergent trends, adaptations to gummivory are quite variable. Second, a long-term field study of the reddish-grey mouse lemur, Microcebus griseorufus, in the highly variable xerophytic forest of southern Madagascar reveals this species to be the most specialized gummivore of all known mouse lemurs. Third, a comparison of the nutritional composition of gums and fruits consumed by M. griseorufus shows these two food types to be of equivalent nutritive content. Gums consumed by M. griseorufus are exuded all year round, increasing the predictability of food availability in a hypervariable habitat, while fruit availability exhibits high intra- and inter-annual variation. Finally, we compared the global distributions of gummivorous mammals with a map of the regions subject to El Niño-related droughts, which indicated a strong congruence between gummivory and hypervariability.


Mouse Lemur Nutritive Content Tooth Comb Interdental Space Spiny Forest 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Fabien Génin thanks the Fondation Fyssen and the CNRS for funding; Jean and Henri de Heaulme for their welcome in Berenty and Analabe private reserves; and Annette Hladik, Njaka, Genevievy, Eden Rabeson, and Bruno Simmen for their help. Judith Masters’ research is funded by the National Research Foundation under Grant number 2053615. Any opinion, findings, and conclusions or recommendations expressed in this material are those of the authors, and the NRF does not accept any liability in regard thereto. She thanks the following curators and collections managers for access to their collections: Drs Darrin Lunde (AMNH, New York), Suzanne MacLaren (CMNH, Pittsburgh), William Stanley (FMNH, Chicago), Christiane Denys (MNHN, Paris), Paula Jenkins (NHM, London), and Marc Herremanns and Wim Wendelin (RMCA, Tervuren). Joerg Ganzhorn’s research was funded by the DFG/BMZ (Ga 342/14-1) and carried out under the Accord de Collaboration between ANGAP (now Madagascar National Parks), the Département Biologie Animale of the Université d’Antananarivo, and the Department of Biology, Hamburg University. He thanks Professors Olga Ramilijaona and Daniel Rakotondravony for their help at various stages of the study.


  1. Atsalis, S 1999. Diet of the brown mouse lemur (Microcebus rufus) in Ranonamafana National Park, Madagascar. Int J Primatol 20:193–229CrossRefGoogle Scholar
  2. Bearder, S.K. Martin, R.D 1980. Acacia gum and its use by bushbabies, Galago senegalensis (primates: lorisidae). Int J Primatol 1(2):103–128CrossRefGoogle Scholar
  3. Bollen, A. van Elsacker, L. and Ganzhorn J.U 2004. Tree dispersal strategies in the littoral forest of Sainte Luce (SE-Madagascar). Oecologia 139:604–616PubMedCrossRefGoogle Scholar
  4. Bollen, A. Donati, G 2005. Phenology of the littoral forest of Sainte Luce, Southeastern Madagascar. Biotropica 37:32–43CrossRefGoogle Scholar
  5. Charles-Dominique, P 1971. Eco-ethologie des Prosimiens du Gabon. Biol Gabon 7:121–228Google Scholar
  6. Charles-Dominique, P. Petter, J.J 1980. Ecology and social life of Phaner furcifer. In Charles-Dominique P, Cooper H.M, Hladik A et al. (eds) Nocturnal Malagasy primates: ecology, physiology and behaviour. Academic, New YorkGoogle Scholar
  7. Coimbra-Filho, A.F. Mittermeier, R.A 1976. Exudate-eating and tree-gouging in marmosets. Nature 262:630CrossRefGoogle Scholar
  8. Dammhahn, M. Kappeler, P.M 2008. Comparative ecology of sympatric Microcebus berthae and M. murinus. Int J Primatol 29(6):1567–1590CrossRefGoogle Scholar
  9. Dewar, R.E. Richard, A.F 2007. Evolution in the hypervariable environment of Madagascar. PNAS 104:13723–13727PubMedCrossRefGoogle Scholar
  10. Doyle, GA 1974. The behavior of the lesser bush-baby (Galago senegalensis moholi). In Martin RD, Doyle GA, Walker AC (eds) Posimian biology. University of Pittsburg Press, PittsburghGoogle Scholar
  11. Docherty, B.A. Alport, L.J. Bhatnagar, K.P. Burrows, A.M. and Smith, T.D 2010. Tongue morphology in infant and adult bushbabies (Otolemur spp.). In Burrows AM, Nash LT (eds) The evolution of exudativory in primates. Springer, New YorkGoogle Scholar
  12. Ganzhorn, J.U 1988. Food partitioning among Malagasy primates. Oecologia 75:436–450CrossRefGoogle Scholar
  13. Génin, F. 2008. Life in unpredictable environments: first investigation of the natural history of Microcebus griseorufus. Int J Primatol 29:303–321CrossRefGoogle Scholar
  14. Génin, F 2003. Female dominance in competition for gum trees in the grey mouse lemur. Rev Ecol 58:397–410Google Scholar
  15. Génin, F (in press) Venus in furs: female power in mouse lemur Microcebus murinus and M. griseorufus. In Masters J.C, Gamba M, Génin F (eds) Leaping ahead: advances in prosimian studies. Springer, New YorkGoogle Scholar
  16. Génin, F. Perret, M 2003. Daily hypothermia in captive grey mouse lemurs (Microcebus ­murinus): effects of photoperiod and food restriction. Comp Biochem Physiol B 136:71–81PubMedCrossRefGoogle Scholar
  17. Heymann, E.W. Smith, A.C 1999. When to feed on gums: temporal patterns of gummivory in wild tamarinds, Saguinus mystax and Saguinus fuscicollis (Callitrichinae). Zoo Biol 18:459–471CrossRefGoogle Scholar
  18. Hill, W.C.O. Rewell, R.E 1948. The caecum of primates: its appendages, mesenteries and blood supply. Trans Zool Soc London 26(3):199–254Google Scholar
  19. Hladik, C.M. Charles-Dominique, P. and Petter, J.J 1980. Feeding strategies of five nocturnal prosimians in the dry forest of the west coast of Madagascar. In Charles-Dominique P, Cooper HM, Hladik A et al. (eds) Nocturnal Malagasy primates: ecology, physiology and behaviour. Academic, New YorkGoogle Scholar
  20. Isbell, L.A 1998. Diet for a small primate: insectivory and gummivory in the (large) patas monkey (Erythrocebus patas pyrrhonotus). Am J Primatol 45:381–398PubMedCrossRefGoogle Scholar
  21. 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 271:88–98CrossRefGoogle Scholar
  22. Lemelin, P. Jungers, W.L 2007. Body size and scaling of the hands and feet of prosimian primates. Am J Phys Anthropol 133:828–840PubMedCrossRefGoogle Scholar
  23. Lindenmayer, D 2002. Gliders of Australia: a natural history. UNSW Press, SydneyGoogle Scholar
  24. Martinez del Rio, C. Baker, H.G. and Baker, I 1992. Ecological and evolutionary implications of digestive processes: bird preferences and the sugar constituents of floral nectar and fruit pulp. Experientia 48:554–561Google Scholar
  25. Masters, J.C. Brothers, D.J 2002. Lack of congruence between morphological and molecular data in reconstructing the phylogeny of Galagonidae. Am J Phys Anthropol 117:79–93PubMedCrossRefGoogle Scholar
  26. Masters, J.C. Rayner, R.J 1993. Competition and macroevolution: the ghost of competition yet to come? Biol J Lin Soc 49:87–98CrossRefGoogle Scholar
  27. Meier, B. Albignac, R 1991. Rediscovery of Allocebus trichotis Günther 1875 (primates) in northeast Madagascar. Folia Primatol 56:57–63PubMedCrossRefGoogle Scholar
  28. Mittermeier, R.A. Konstant, W.R. Hawkins, F.E. Louis, E.E. Langrand, O. Ratsimbazafy, J. Rasoloarison, R. Ganzhorn, J.U. Rajaobelina, S. Tattersall, I. and Meyers, D.M 2006. Lemurs of Madagascar. Second edition. Conservation International, Washington, DCGoogle Scholar
  29. Nash, L.T 1986. Dietary, behavioral, and morphological aspects of gummivory in primates. Yearb Phys Anthropol 29:113–137CrossRefGoogle Scholar
  30. Pagès, E 1980. Ethoecology of Microcebus coquereli during the dry season. In Charles-Dominique P, Cooper H.M, Hladik A et al. (eds) Nocturnal malagasy primates: ecology, physiology and behavior. Academic, New YorkGoogle Scholar
  31. Peres, C.A 2000. Identifying keystone plant resources in tropical forests: the case of gums from Parkia pods. J Trop Ecol 16:287–317CrossRefGoogle Scholar
  32. Petter, J. Albignac, R. and Rumpler, Y 1977. Mammifères Lémuriens (Primates Prosimiens). Faune de Madagascar, vol 44. ORSTOM CNRS, ParisGoogle Scholar
  33. Pickford, M. Senut, B 2000. Geology and palaeobiology of the Namib desert Southwestern Africa. Ministry of Mines and Energy, Windhoek. Memoir 18, vol 1, Geological survey of NamibiaGoogle Scholar
  34. Radespiel, U. Reimann, W. Rahelinirina, M. and Zimmermann, E 2006. Feeding ecology of sympatric mouse lemur species in northwestern Madagascar. Int J Primatol 27:311–321CrossRefGoogle Scholar
  35. Rasoloarison, R.M. Goodman, S.M. and Ganzhorn, J.U 2000. Taxonomic revision of mouse lemurs (Microcebus) in the western portions of Madagascar. Int J Primatol 21:963–1019CrossRefGoogle Scholar
  36. Sauer, E.G.F. Sauer, E.M 1963. The southwest African bush-baby of the Galago senegalensis group. J Southwest Afr Sci Soc 16:5–35Google Scholar
  37. Schatz, G.E 2001. Generic tree flora of Madagascar. Royal Botanic Gardens, Kew and Missouri Botanical Garden, LondonGoogle Scholar
  38. Stephenson I.R. Bearder S.K. Donati G. and Karlsson, J 2010. A guide to galago diversity: getting a grip on how best to chew gum. In Burrows A.M, Nash L.T (eds) The evolution of exudativory in primates. Springer, New YorkGoogle Scholar
  39. Tan, C.L. Drake, J.H 2001. Evidence of tree gouging and exudate eating in pygmy slow loris (Nycticebus pygmaeus). Folia Primatol 72:37–39PubMedCrossRefGoogle Scholar
  40. Viguier, B 2004. Functional adaptations in the craniofacial morphology of Malagasy primates: shape variations associated with gummivory in the family Cheirogaleidae. Ann Anat 186:495–501PubMedCrossRefGoogle Scholar
  41. Vinyard, C.J. Wall, C.E. Williams, S.H. and Hylander W.L 2003. Comparative functional analysis of skull morphology of tree-gouging primates. Am J Phys Anthropol 120:153–170PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Fabien G. S. Génin
    • 1
  • Judith C. Masters
  • Jorg U. Ganzhorn
  1. 1.Department of ZoologyUniversity of Fort HareAliceSouth Africa

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