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Sensory Basis of Food Detection in Wild Microcebus murinus

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Abstract

Very little is known about how nocturnal primates find their food. Here we studied the sensory basis of food perception in wild-caught gray mouse lemurs (Microcebus murinus) in Madagascar. Mouse lemurs feed primarily on fruit and arthropods. We established a set of behavioral experiments to assess food detection in wild-born, field-experienced mouse lemurs in short-term captivity. Specifically, we investigated whether they use visual, auditory, and motion cues to find and to localize prey arthropods and further whether olfactory cues are sufficient for finding fruit. Visual cues from motionless arthropod dummies were not sufficient to allow reliable detection of prey in choice experiments, nor did they trigger prey capture behavior when presented on the feeding platform. In contrast, visual motion cues from moving prey dummies attracted their attention. Behavioral observations and experiments with live and recorded insect rustling sounds indicated that the lemurs make use of prey-generated acoustic cues for foraging. Both visual motion cues and acoustic prey stimuli on their own were sufficient to trigger approach and capture behavior in the mouse lemurs. For the detection of fruit, choice experiments showed that olfactory information was sufficient for mouse lemurs to find a piece of banana. Our study provides the first experimental data on the sensory ecology of food detection in mouse lemurs. Further research is necessary to address the role of sensory ecology for food selection and possibly for niche differentiation between sympatric Microcebus species.

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References

  • Arlettaz, R., Jones, G., & Racey, P. A. (2001). Effect of acoustic clutter on prey detection by bats. Nature, 414, 742–745.

    Article  PubMed  CAS  Google Scholar 

  • Atsalis, S. (1998). Feeding ecology of the brown mouse lemurs, Microcebus rufus. Folia Primatologica, 69, 406–407.

    Article  Google Scholar 

  • Bicca-Marques, J. C., & Garber, P. A. (2004). Use of spatial, visual, and olfactory information during foraging in wild nocturnal and diurnal anthropoids: A field experiment comparing Aotus, Callicebus, and Saguinus. American Journal of Primatology, 62, 171–187.

    Article  PubMed  Google Scholar 

  • Cartmill, M. (1972). Arboreal adaptations and the origin of the order Primates. In R. Tuttle (Ed.), The functional and evolutionary biology of the primates (pp. 97–122). Chicago: Aldine Atherton.

    Google Scholar 

  • Cartmill, M. (1974). Rethinking primate origins. Science, 184, 436–443.

    Article  PubMed  CAS  Google Scholar 

  • Cartmill, M. (1992). New views on primate origins. Evolutionary Anthropology, 1, 105–111.

    Article  Google Scholar 

  • Charles-Dominique, P. (1972). Ecologie et vie sociale de Galago demidovii (Fischer 1808; Prosimii). Zeitschrift für Tierpsychologie, 9, 7–41.

    Google Scholar 

  • Charles-Dominique, P. (1977). Ecology and behaviour of nocturnal primates. New York: Columbia University Press.

    Google Scholar 

  • Coleman, M. N., & Ross, C. F. (2004). Primate auditory diversity and its influence on hearing performance. Anatomical Record Part A, 281A, 1123–1137.

    Article  Google Scholar 

  • Coles, R. B., Guppy, A., Anderson, M. E., & Schlegel, P. (1989). Frequency sensitivity and directional hearing in the gleaning bat Plecotus auritus (Linnaeus 1758). Journal of Comparative Physiology A, 165, 269–280.

    Article  CAS  Google Scholar 

  • Corbin, G. D., & Schmid, J. (1995). Insect secretions determine habitat use patterns by a female lesser mouse lemur Microcebus murinus. American Journal of Primatology, 37, 317–324.

    Article  Google Scholar 

  • Crompton, R. H. (1995) Visual predation, habitat structure and the ancestral primate niche. In L. Alterman, G. A. Doyle & M. K. Izard (Eds.), Creatures of the dark: The nocturnal prosimians. (pp. 11–30). New York: Plenum.

    Google Scholar 

  • Dominy, N. J. (2004). Fruits, fingers, and fermentation: The sensory cues available to foraging primates. Integrative and Comparative Biology, 44, 295–303.

    Article  Google Scholar 

  • Dominy, N. J., Lucas, P. W., Osorio, D., & Yamashita, N. (2001). The sensory ecology of primate food perception. Evolutionary Anthropology, 10, 171–186.

    Article  Google Scholar 

  • Dominy, N. J., Ross, C. F., & Smith, T. D. (2004). Evolution of the special senses in primates: Past, present and future. Anatomical Record Part A, 281A, 1078–1082.

    Article  Google Scholar 

  • Doyle, G. A. (1974). Behavior of prosimians. In A. M. Schrier & F. Stollnitz (Eds.), Behavior of nonhuman primates (pp. 155–353). New York: Academic Press.

    Google Scholar 

  • Dusenbery, D. B. (1992). Sensory ecology. New York: Freeman and Company.

    Google Scholar 

  • Erickson, C. J. (1991). Percussive foraging in the aye-aye, Daubentonia madagascarensis. Animal Behavior, 41, 793–801.

    Article  Google Scholar 

  • Erickson, C. J. (1994). Tap-scanning and extractive foraging in aye-ayes, Daubentonia madagascarensis. Folia Primatologica, 62, 125–135.

    CAS  Google Scholar 

  • Erickson, C. J., Nowicki, S., Dollar, L., & Goehring, N. (1998). Percussive foraging: Stimuli for prey location by aye-ayes (Daubentonia madagascarensis). International Journal of Primatology, 19, 111–122.

    Article  Google Scholar 

  • Faure, P. A., & Barclay, R. M. R. (1992). The sensory basis of prey detection by the long-eared bat, Myotis evotis, and the consequences for prey selection. Animal Behavior, 44, 31–39.

    Article  Google Scholar 

  • Fuzessery, Z. M., Buttenhoff, P., Andrews, B., & Kennedy, J. M. (1993). Passive sound localization of prey by the pallid bat (Antrozous pallidus). Journal of Comparative Physiology A, 171, 767–777.

    Article  CAS  Google Scholar 

  • Goerlitz, H. R., & Siemers, B. M. (2007). Sensory ecology of prey rustling sounds: acoustical features and their classification by wild grey mouse lemurs. Functional Ecology, 21, 143–153.

    Google Scholar 

  • Harcourt, C., & Thornbach, J. (1990). Lemurs of Madagascar and the Comores. The IUCN Red Data Book. Gland (Schweiz), Cambridge: IUCN – The World Conservation Union.

    Google Scholar 

  • Harste, L. V., Wright, P. C., & Jernvall, J. (1997). Microcebus rufus feeding behaviour in the south-eastern rain forest of Madagascar. Primate Eye, 62, 6–7.

    Google Scholar 

  • Hladik, C. M. (1979). Diet and ecology of prosimians. In G. A. Doyle & R. D. Martin (Eds.), The study of prosimian behaviour (pp. 307–357). New York: Academic Press.

    Google Scholar 

  • Hladik, C. M., Charles-Dominque, 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 (Eds.), Nocturnal malagasy primates (pp. 41–73). New York: Academic Press.

    Google Scholar 

  • Howe, H. F., & Smallwood, J. (1982). Ecology of seed dispersal. Annual Review of Ecology and Systematics, 13, 201–228.

    Article  Google Scholar 

  • Kappeler, P. M., Rasoloarison, R. M., Razafimanantsoa, L., Walter, L., & Roos, C. (2005). Morphology, behaviour and molecular evolution of giant mouse lemurs (Mirza spp.) Gray, 1870, with description of a new species. Primate Report, 71, 3–26.

    Google Scholar 

  • Kirk, C. E. (2004). Comparative morphology of the eye in primates. Anatomical Record Part A, 281A, 1095–1103.

    Article  Google Scholar 

  • Korine, C., & Kalko, E. K. V. (2005). Fruit detection and discrimination by small fruit-eating bats (Phyllostomidae): Echolocation call design and olfaction. Behavioral Ecology Sociobiology, 59, 12–23.

    Article  Google Scholar 

  • Laska, M., Seibt, A., & Weber, A. (2000). “Microsmatic” primates revisited: Olfactory sensitivity in the squirrel monkey. Chemical Senses, 25, 47–53.

    Article  PubMed  CAS  Google Scholar 

  • Luft, S., Curio, E., & Tacud, B. (2003). The use of olfaction in the foraging behaviour of the golden-mantled flying fox, Pteropus pumilus, and the greater musky fruit bat, Ptenochirus jagori (Megachiroptera: Pteropodidae). Naturwissenschaften, 90, 84–87.

    PubMed  CAS  Google Scholar 

  • MacKinnon, J., & MacKinnon, K. (1980). The behaviour of wild spectral tarsiers. International Journal of Primatology, 1, 361–379.

    Google Scholar 

  • Martin, R. D. (1972). A preliminary field-study of the lesser mouse lemur (Microcebus murinus J.F. Miller 1777). Zeitschrift für Tierpsychologie, 9, 43–89.

    Google Scholar 

  • Martin, R. D. (1973). A review of the behaviour and ecology of the lesser mouse lemur (Microcebus murinus J. F. Miller 1777). In R. P. Michael & J. H. Crook (Eds.), Comparative ecology and behaviour of primates (pp. 1–68). London: Academic Press.

    Google Scholar 

  • Nekaris, K. A. I. (2005). Foraging behaviour of the slender loris (Loris lydekkerianus lydekkerianus): Implications for theories of primate origins. Journal of Human Evolution, 49, 289–300.

    Article  PubMed  CAS  Google Scholar 

  • Niaussat, M. M., & Petter, J. J. (1980). Etude de la sensibilité auditive d’un lémurien malgache: Microcebus murinus (J.-F. Miller, 1777). Mammalia, 44, 553–558.

    Google Scholar 

  • Niemitz, C. (1979). Outline of the behavior of Tarsius bancanus. In G. A. Doyle & R.D. Martin (Eds.), The Study of Prosimian Behavior (pp. 631–660). New York: Academic Press.

    Google Scholar 

  • Obrist, M. K., Fenton, M. B., Eger, J. L., & Schlegel, P. A. (1993). What ears do for bats: A comparative study of pinna sound pressure transformation in Chiroptera. Journal of Experimental Biology, 180, 119–152.

    PubMed  CAS  Google Scholar 

  • Pariente, G. F. (1974). Importance respective du repérage visuel et auditif (absence d’écholocation) chez Microcebus murinus. Mammalia, 38, 1–6.

    Article  Google Scholar 

  • Petter, J. J. (1978). Ecological and physiological adaptions of five sympatric nocturnal lemurs to seasonal variations in food production. In D.J. Chivers & J. Herbert (Eds.), Recent Advances in Primatology, Vol 1: Behaviour (pp. 211–223). New York: Academic Press.

    Google Scholar 

  • Radespiel, U., Reimann, W., Rahelinirina, M., & Zimmermann, E. (2006). Feeding ecology of sympatric mouse lemur species in northwestern Madagascar. International Journal of Primatol, 27, 311–321.

    Article  Google Scholar 

  • Rakotonirina (1996). Composition and structure of a dry forest on sandy soils near Morondava. In J. U. Ganzhorn & J. P. Sorg (Eds.), Ecology and Economy of a Tropical Dry Forest in Madagascar (pp. 81–87). Göttingen: Erich Goltze GmbH & Co KG.

    Google Scholar 

  • Ramanamanjato, J. B., & Ganzhorn, J. U. (2001). Effects of forest fragmentation, introduced Rattus rattus and the role of exotic tree plantations and secondary vegetation for the conservation of an endemic rodent and a small lemur in littoral forests of southeastern Madagascar. Animal Conservation, 4, 175–183.

    Article  Google Scholar 

  • Rasoloarison, R. M., Goodman. S. M., & Ganzhorn, J. U. (2000). Taxonomic revision of mouse lemurs (Microcebus) in the western portions of Madagascar. International Journal of Primatology, 21, 963–1019.

    Article  Google Scholar 

  • Schmid, J., & Kappeler, P. M. (1994). Sympatric mouse lemurs (Microcebus spp.) in western Madagascar. Folia Primatologica, 63, 162–170.

    Article  CAS  Google Scholar 

  • Siemers, B. M., & Güttinger, R. (2006). Prey conspicuousness can explain apparent prey selectivity. Current Biology, 16, R157–R159.

    Article  PubMed  CAS  Google Scholar 

  • Siemers, B. M., & Schnitzler, H.-U. (2004). Echolocation signals reflect niche differentiation in five sympatric congeneric bat species. Nature, 429, 657–661.

    Article  PubMed  CAS  Google Scholar 

  • Siemers, B. M., & Swift, S. (2006). Differences in sensory ecology contribute to resource partitioning in the bats Myotis bechsteinii and Myotis nattereri (Chiroptera: Vespertilionidae). Behavioral Ecology and Sociobiology, 59, 373–380.

    Article  Google Scholar 

  • Sorg, J. P., & Rohner, U. (1996). Climate and tree phenology of the dry deciduous forest of Kirindy Forest. In J. U. Ganzhorn and J. U. Sorg (Eds.), Ecology and economy of a Tropical Dry Forest in Madagascar (pp. 57–80). Göttingen: Erich Goltze Gmbh & Co KG.

    Google Scholar 

  • Stephens, D. W., & Krebs, J. R. (1986). Foraging theory. New Jersey: Princeton University Press.

    Google Scholar 

  • Sussman, R. W. (1978). Nectar-feeding by prosimians and its evolutionary and ecological implications. In D. J. Chivers & K. A. Josey (Eds.), Recent Advances in Primatology Vol. 3: Evolution (pp. 119–125). New York: Academic Press.

    Google Scholar 

  • Yoder, A. D., Rasoloarison, R. M., Goodman, S. M., Irwin, J. A., Atsalis, S., Ravosa, M. J., Ganzhorn, J. U. (2000). Remarkable species diversity in Malagasy mouse lemurs (primates, Microcebus). Proceedings of the National Academy of Sciences, 97, 11325–11330.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

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Acknowledgments

A National Geographic Society grant to BMS and JUG (7198-02) funded our research. We captured subjects and conducted behavioral studies under license from the Ministère de l’Evironnement des Eaux et Forets, Madagascar and complied with Malagasy laws. We thank the Direction des Eaux et Forêts and the Commision Tripartie for authorization of our research. We thank QIT Madagascar Minerals for providing excellent logistics at Fort Dauphin and Mandena. We especially thank Mme. Manon Vincelette. Likewise, we acknowledge the logistic support at Morondava and Kirindy provided by the German Primate Centre (DPZ) and the University of Antananarivo. Special thanks go to Prof. Peter Kappeler and Leon Razafimananatsoa. For invaluable help and company in the field we thank our colleagues Brigitte Raharivololona, Refahly Ernest, Malala Raharimanga, and Tiana Andrianjanahary. We thank Ingrid Kaipf for producing Fig. 1 and an anonymous referee for very constructive and supportive comments on an earlier version of the article.

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  1. Björn M. Siemers

    Present address: Sensory Ecology Group, Max Planck Institute for Ornithology, 82319, Seewiesen, Germany

Authors and Affiliations

  1. Tierphysiologie, Zoologisches Institut, University of Tübingen, Tübingen, Germany

    Björn M. Siemers & Holger R. Goerlitz

  2. Departement Biologie Animale, University of Antananarivo, Antananarivo, Madagascar

    Eric Robsomanitrandrasana, Daniel Rakotondravony & Olga Ramilijaona

  3. Biozentrum Grindel, University of Hamburg, Hamburg, Germany

    Marcus Piep & Jörg U. Ganzhorn

  4. QIT Madagascar Minerals, Fort Dauphin, Madagascar

    Jean-Baptiste Ramanamanjato

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  1. Björn M. Siemers
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Siemers, B.M., Goerlitz, H.R., Robsomanitrandrasana, E. et al. Sensory Basis of Food Detection in Wild Microcebus murinus . Int J Primatol 28, 291–304 (2007). https://doi.org/10.1007/s10764-007-9135-7

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