Abstract
Exudates represent an important component of the natural diets of small-bodied primates. For mouse lemurs, the impact of forest type and seasonal predictability on gum consumption has recently been intensively investigated. The goal of our study was to extend our knowledge regarding the seasonality of feeding ecology of Microcebus murinus, first, to investigate the relative consumption of gum and hemipteran honeydew, a sap-derived product, and, second to assess respective foraging strategies in a highly seasonal and quite predictable environment. We hypothesized that (1) food resources vary according to the season, (2) gum and honeydew represent keystone food resources during periods of food scarcity, and (3) lemurs revisit productive stationary feeding sites during the period of food scarcity. We studied gray mouse lemurs in the dry deciduous forest of the Ankarafantsika National Park in northwestern Madagascar. We radio-collared seven M. murinus females and performed focal observations on their feeding behavior during the end of the dry and the beginning of the rainy season. During the dry season, the period of food scarcity, mouse lemurs mainly consumed gum and honeydew. Subjects revisited the same feeding sites within the same and over several nights. During the rainy season, the period of food abundance, lemurs consumed mainly nectar from shrub flowers and did not show gum or honeydew feeding. To our knowledge, the consumption of honeydew by lemurs is a unique case of sap feeding by proxy in a mammal. Further investigations will focus on the characterization of the ecological consequences of such an interaction between mouse lemurs, hemipteran larvae, and host plants.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267
Atsalis S (2008) A natural history of the brown mouse lemur. Prentice Hall, Upper Saddle River, NJ
Bearder SK, Martin RD (1980) Acacia gum and its use by bushbabies, Galago senegalensis (Primates: Lorisidae). Int J Primatol 1:103–128
Beggs JR, Wilson PR (1991) The kaka Nestor meridionalis, a New Zealand parrot endangered by introduced wasps and possums. Biol Cons 56:23–38
Charles-Dominique P, Petter JJ (1980) Ecology and social life of Phaner furcifer. In: Charles-Dominique P, Cooper HM, Hladik A, Hladik CM, Pages E, Pariente GF, Petter-Rousseaux A, Petter JJ, Schilling A (eds) Nocturnal Malagasy primates. Academic, New York
Chouteau P (2004) The impacts of logging on the microhabitats used by two species of couas in the western forest of Madagascar. C R Biologies 327:1157–1170
Coimbra-Filho AF, Mittermeier RA (1976) Exudate-eating and tree-gouging in marmosets. Nature 262:630
Corbin GD, Schmid J (1995) Insect secretions determine habitat use patterns by a female lesser mouse lemur (Microcebus murinus). Am J Primatol 37:317–324
Dammhahn M, Kappeler PM (2008) Comparative feeding ecology of sympatric Microcebus berthae and M. murinus. Int J Primatol 29:1567–1589
Delabie JHC (2001) Trophobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an overview. Neotrop Entomol 30:501–516
Douglas AE (2006) Phloem-sap feeding by animals: problems and solutions. J Exp Bot 57:747–754
Edwards EP (1982) Hummingbirds feeding on an excretion produced by scale insects. Condor 84:122
Fölling M, Knogge C, Bohme W (2001) Geckos are milking honeydew-producing planthoppers in Madagascar. J Nat Hist 35:279–284
Gaze PD, Clout MN (1983) Honeydew and its importance to birds in beech forests of South Island, New Zealand. N Z J Ecol 6:33–37
Génin F (2003) Female dominance in competition for gum trees in the grey mouse lemur Microcebus murinus. Rev Ecol (Terre Vie) 58:397–410
Génin F (2008) Life in unpredictable environments: first investigation of the natural history of Microcebus griseorufus. Rev Ecol (Terre Vie) 58:397–410
Greenberg R, Caballero CM, Bichier P (1993) Defense of Homopteran honeydew by birds in the Mexican highlands and other warm temperate forests. Oikos 68:519–524
Gullan PJ (1997) Relationships with ants. In: Ben-Dov Y, Hodgson CJ (eds) Soft scale insects – their biology, natural enemies and control. Elsevier Science B.V., Amsterdam
Heymann EW, Smith AC (1999) When to feed on gums: temporal patterns of gummivory in wild tamarins, Saguinus mystax and Saguinus fuscicollis (Callitrichinae). Zoo Biol 18:459–471
Hladik CM, Charles-Dominique P, Petter JJ (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, Hladik CM, Pages E, Pariente GF, Petter-Rousseaux A, Petter JJ, Schilling A (eds) Nocturnal Malagasy primates. Academic, New York
Hölldobler B, Wilson EO (1990) The ants. The Belknap Press of the Harvard University Press, Cambridge, MA
Hooge PN, Eichenlaub B, Solomon E (1999) The animal movement program. Version ver. 1.1. USGS, Alaska Biological Science Center, Anchorage
Hunt JH (2003) Cryptic herbivores of the rainforest canopy. Science 300:916–917
Jolly A, Sussman RW, Koyama N, Rasamimanana H (2006) Ringtailed lemur biology. Springer, New York
Joly M, Zimmermann E (2007) First evidence for relocation of stationary food resources during foraging in a strepsirhine primate (Microcebus murinus). Am J Primatol 69:1045–1052
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
Latta SC, Gampedr HA, Tietz JR (2001) Revising the convergence hypothesis of avian use of honeydew: evidence from Dominican subtropical dry season. Oikos 93:250–259
Martin RD (1973) Comparative ecology and behaviour of primates. In: Michael RP, Crook JH (eds) A review of the behaviour and ecology of the lesser mouse lemur (Microcebus murinus). Academic, London
Mittermeier RA, Ganzhorn JU, Konstant WR, Glander K, Tattersall I, Groves CP, Rylands AB, Hapke A, Ratsimbazafy J, Mayor MI, Louis EE, Rumpler Y, Schwitzer C, Rasoloarison RM (2008) Lemur diversity in Madagascar. Int J Primatol 29:1607–1656
Nash LT (1986) Dietary, behavioral, and morphological aspects of gummivory in primates. Am J Physic Anthr 29:113–137
Olivieri G, Randrianambinina B, Rakotondavony D, Zimmermann E, Radespiel U (2007) The ever-increasing diversity in mouse lemurs: three new species in north and northwestern Madagascar. Mol Phyl Evol 43:309–327
Pagès E (1980) Ethoecology of Microcebus coquereli during the dry season. In: Charles-Dominique P, Cooper HM, Hladik A, Hladik CM, Pagès E, Pariente GF, Petter-Rousseaux A, Petter JJ, Schilling A (eds) Nocturnal malagasy primates. Academic, New York
Petter JJ, Schilling A, Pariente G (1971) Observations éco-éthologiques sur les deux lémuriens malgaches nocturnes: Phaner furcifer et Microcebus coquereli. La Terre et la Vie 25:287–327
Radespiel U (2006) Ecological diversity and seasonal adaptations of mouse lemurs (Microcebus spp.). In: Gould L, Sauther ML (eds) Lemurs: ecology and adaptation. Springer, New York
Radespiel U, Reimann W, Rahelinirina M, Zimmermann E (2006) Feeding ecology of sympatric mouse lemur species in Northwestern Madagascar. Int J Primatol 27:311–321
Radespiel U, Olivieri G, Rasolofoson DW, Rakotondratsimba G, Rakotonirainy O, Rasoloharijaona S, Randrianambinina B, Ratsimbazafy JH, Ratelolahy F, Randriamboavonjy T, Rasolofoharivelo T, Craul M, Rakotozafy L, Randrianarison RM (2008) Exceptional diversity of mouse lemurs (Microcebus spp.) in the Makira region with the description of one new species. Am J Primatol 70:1033–1046
Ramirez M, Freese CH, Revilla J (1977) Feeding ecology of the pygmy marmoset, Cebuella pygmaea in Northeastern Peru. In: Kleinman DG (ed) The biology and conservation of the Callitrichidae. SI Press, Washington, DC
Rendigs A, Radespiel U, Wrogemann D, Zimmermann E (2003) Relationship between microhabitat structure and distribution of mouse lemurs (Microcebus spp.) in Northwestern Madagascar. Int J Primatol 24:47–64
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 W, Goodman S (eds) Diversité et endémisme à Madagascar. Société de Biogéographie, Paris
Styrsky JD, Eubanks MD (2007) Ecological consequences of interactions between ants and honeydew-producing insects. Proc Roy Soc B 274:151–164
Wilson SW (2005) Keys to the families of Fulgoromorpha with emphasis on planthoppers of potential economic importance in the Southeastern United States (Hemiptera: Auchenorrhyncha). Florida Entomol 88:464–481
Acknowledgments
We thank the Commission Tripartite of the Malagasy government, the Département des Eaux et Forêts, and the Association pour la Gestion des Aires for their permission to work in Ampijoroa. We also thank Dr. Daniel Rakotondravony, Faculté des Sciences, Université d’Antananarivo for logistic support. We thank the Durrell Wildlife Preservation Trust for the climatic data. For help in plant identification, we thank Hiroki Sato, University of Kyoto, Japan. For assistance in the field, we thank Dr. Blanchard Randrianambinina, Dr. Solofo Rasoloharijaona, Dr. Marina Scheumann, and Christian Schopf. The study complies with the current laws of Madagascar and was financially supported by the DAAD and financial support for women from the University of Veterinary Medicine Hannover.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2010 Springer Science+Business Media, LLC
About this chapter
Cite this chapter
Joly-Radko, M., Zimmermann, E. (2010). Seasonality in Gum and Honeydew Feeding in Gray Mouse Lemurs. In: Burrows, A., Nash, L. (eds) The Evolution of Exudativory in Primates. Developments in Primatology: Progress and Prospects. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-6661-2_7
Download citation
DOI: https://doi.org/10.1007/978-1-4419-6661-2_7
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4419-6660-5
Online ISBN: 978-1-4419-6661-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)