Abstract
In order to remain stable, dispersed social groups have to solve two fundamental problems: the coordination of movement and cohesiveness within a group and the spacing between the groups. Here, we investigate mechanisms involved in intra-group coordination and inter-group spacing using the golden brown mouse lemur, Microcebus ravelobensis, as a model for a nocturnal, solitary foraging mammal with a dispersed social system. By means of radiotelemetry and bioacoustics we studied the olfactory and vocal behaviour during nocturnal dispersal and reunion of five sleeping groups.
All groups used 3–17 sleeping sites exclusively, suggesting a sleeping site-related territoriality and competition for them. The occurrence of olfactory and vocal behaviour showed an asymmetrical temporal distribution. Whereas marking behaviour was observed exclusively during dispersal, a particular call type, the trill, was used by all groups during reunions. Interestingly, these trills carried group-specific signatures.
Our findings provide the first empirical evidence for nocturnal primates in a natural environment that olfactory signals represent an important mechanism to regulate the distribution of different groups in space, whereas acoustic signals control intra-group cohesion and coordination.
Similar content being viewed by others
References
Barre V, Lebec A, Petter J-J, Albignac R (1988) Étude du Microcèbe par radiotracking dans la forêt de l’Ankarafantsika. Deuxième Séance Technique 61–71
Bart J, Fligner MA, Notz WI (1998) Sampling and statistical methods for behavioural ecologists. Cambridge University Press, Cambridge, pp 177–187
Bearder SK, Doyle GA (1974) Field and laboratory studies of social organization in bushbabies (Galago senegalensis). J Hum Evol 3:37–50
Bearder SK, Ambrose L, Harcourt C, Honess P, Perkin A, Pimley E, Pullen S, Svoboda N (2003) Species-typical patterns of infant contact, sleeping site use and social cohesion among nocturnal primates in Africa. Folia Primatol 74:337–354
Boinski S, Garber PA (2000) On the move: how and why animals travel in groups. The University of Chicago Press, Chicago
Boughman JW (1997) Greater spear-nosed bats give group-distinctive calls. Behav Ecol Sociobiol 40:61–70
Boughman JW, Wilkinson GS (1998) Greater spear-nosed bats discriminate group mates by vocalizations. Anim Behav 55:1717–1732
Braune P, Polenz S, Zietemann V, Zimmermann E (2001) Species-specific signaling in two sympatrically living nocturnal primates, the grey and the golden brown mouse lemur (Microcebus murinus and Microcebus ravelobensis), in Northwestern Madagsacar. Adv Ethol 36:126
Buesching CD, Heistermann M, Hodges JK, Zimmermann E (1998) Multimodal oestrus advertisement in a small nocturnal prosimian, Microcebus murinus. Folia Primatol 69:295–308
Charles-Dominique P (1977) Ecology and behaviour of nocturnal primates. Columbia University Press, New York
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, Schilling A, Petter JJ (eds) Nocturnal Malagasy primates. Ecology, physiology, and behavior. Academic Press, New York, pp 75–95
Cheney DL, Seyfarth RM (1982) Recognition of individuals within and between groups of free-ranging vervet monkeys. Am Zool 22:519–529
Couzin I, Krause J (2003) Self-organization and collective behavior in vertebrates. Adv Study Behav 32:1–75
de Waal FBM, Tyack PL (2003) Animal social complexity: intelligence, culture, and individualized societies. Harvard University Press, Cambridge, MA
Dörrie M, Schmidt S, Suba M, Sripathi K (2001) Contact calls of the bat, Megaderma lyra: a comparison between an Indian and a Sri Lankan population. Zoology 104:5
Egnor SER, Hauser MD (2004) A paradox in the evolution of primate vocal learning. Trends Neurosci 27:649–654
Fietz J (1999) Monogamy as a rule rather than exception in nocturnal lemurs: the case of the fat-tailed dwarf lemur, Cheirogaleus medius. Ethology 105:259–272
Fleagle JG, Janson C, Reed KE (1999) Primate communities. Cambridge University Press, Cambridge
Glatson AR (1983) Olfactory communication in the Lesser Mouse Lemur (Microcebus murinus). In: Seth PK (ed) Perspectives in primate biology. Today & Tomorrow’s Printers and Publishers, New Delhi, pp 63–73
Hafen TG (1998) Dialekte bei Lemuren: bioakustische, morphometrische und molekulargenetische Untersuchungen zur intraspezifischen Variabilität beim grauen Mausmaki (Microcebus murinus). Cuvillier Verlag, Göttingen
Hammerschmidt K, Todt D (1995) Individual differences in vocalisations of young Barbary macaques (Macaca sylvanus): a multi-parametric analysis to identify critical cues in acoustic signalling. Behaviour 132:381–399
Harcourt C (1991) Diet and behaviour af a nocturnal lemur, Avahi laniger, in the wild. J Zool Lond 223:667–674
Hauser MD (1996) The evolution of communication. MIT Press, Cambridge, MA
Hopp SL, Jablonski P, Brow JL (2001) Recognition of group membership by voice in Mexican jays, Aphelocoma ultramarina. Anim Behav 62:297–303
Janson C (2000) Spatial movement strategies: theory, evidence, and challenges. In: Boinski S, Garber PA (eds) On the move: how and why animals travel in groups. The University of Chicago Press, Chicago, pp 165–203
Kappeler PM, van Schaik CP (2002) Evolution of primate social systems. Int J Primatol 23:707–740
Kerth G, Safi K, König B (2002) Mean colony relatedness is a poor predictor of colony structure and female philopatry in the communally breeding Bechstein’s bat (Myotis bechsteinii). Behav Ecol Sociobiol 52:203–210
Marler P, Hobbett L (1975) Individuality in a long-range vocalization of wild chimpanzees. Z Tierpsychol 38:97–109
Mertl-Millhollen AS (1988) Olfactory demarcation of territorial but not home range boundaries by Lemur catta. Folia Primatol 50:175–187
Mundinger PC (1982) Microgeographic and macrogeographic variation in the acquired vocalizations of birds. In: Kroodsma DE, Miller EH, Ouellet H (eds) Acoustic communication in birds, vol. 2. Song learning and its consequences. Academic Press, New York, pp 147–208
Müller AE (1999) Social organization of the fat-tailed dwarf lemur (Cheirogaleus medius) in Northwestern Madagascar. In: Rakotosamimanana B, Rasamimanana H, Ganzhorn JU, Goodman SM (eds) New directions in lemur studies. Kluwer /Plenum, New York, pp 139–157
Müller AE, Thalmann U (2000) Origin and evolution of primate social organisation: a reconstruction. Biol Rev 75:405–435
Müller AE, Thalmann U (2002) Biology of the fat-tailed dwarf lemur (Cheirogaleus medius E. Goeffroy 1812): new results from the field. Evol Anthropol 11(Suppl.1):79–82
Nowicki S (1989) Vocal plasticity in captive black-capped chickadees: the acoustic basis and rate of call convergence. Anim Behav 37:64–73
Pastorini J, Martin RD, Ehresmann P, Zimmermann E, Forstner MJR (2001) Molecular phylogeny of the lemur family cheirogaleidae (Primates) based on mitochondrial DNA sequences. Mol Phylogenet Evol 19:45–56
Peters C (1999) Intrasexuelle Konkurrenz bei grauen Mausmaki-Männchen (Microcebus murinus) in Nordwest-Madagaskar. Diploma-thesis, University of Hannover, Germany
Polenz S (2000) Akustisches und soziales Verhalten des goldbraunen Mausmakis (Microcebus ravelobensis) während der Paarungszeit. Diploma-thesis, University of Hannover, Germany
Radespiel U (2000) Sociality in the gray mouse lemur (Microcebus murinus) in northwestern Madagascar. Am J Primatol 51:21–40
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 (2003) Species-specific usage of sleeping sites in two sympatric mouse lemur species (Microcebus murinus and Microcebus ravelobensis) in Northwestern Madagascar. Am J Primatol 59:139–151
Radhakrishna S, Singh M (2002) Social behaviour of the slender loris (Loris tardigradus lydekkerianus). Folia Primatol 73:181–196
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
Rasoloharijaona S, Rakotosamimanana B, Randrianambinina B, Zimmermann E (2003) Pair-specific usage of sleeping sites and their implications for social organization in a nocturnal malagasy primate, the Milne Edwards’ sportive lemur (Lepilemur edwardsi). Am J Phys Anthropol 122:251–258
Rendall D, Rodman P, Emond RE (1996) Vocal recognition of individuals and kin in free-ranging rhesus monkeys. Anim Behav 51:1007–1015
Scherrer JA, Wilkinson GS (1993) Evening bat isolation calls provide evidence for heritable signatures. Anim Behav 46:847–860
Schilling A (1979) Olfactory communication in Prosimians. In: Doyle GA, Martin RD (eds) The Study of Prosimian Behavior. Academic Press, New York, San Francisco, London, pp 461–542
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: Lorenzo WR, Goodman SM (eds) Diversité et Endémisme à Madagascar. Société de Biogéographie, Paris, pp 165–175
Schülke O, Kappeler PM (2003) So near and yet so far: territorial pairs but low cohesion between pair partners in a nocturnal lemur, Phaner furcifer. Anim Behav 65:331–343
Seitz E (1969) Die Bedeutung geruchlicher Orientierung beim Plumplori Nycticebus coucang Boddaert 1785 (Prosimii, Lorisidae). Z Tierpsychol 26:73–103
Seyfarth RM, Cheney DL (1997) Some general features of vocal development in nonhuman primates. In: Snowdon CT, Hausberger M (eds) Social influences on vocal development. Cambridge University Press, Cambridge, pp 249–273
Snowdon CT, Cleveland J (1980) Individual recognition of contact calls by pygmy marmosets. Anim Behav 28:717–727
Stanger KF (1995) Vocalizations of some cheirogaleid prosimians evaluated in a phylogenetic context. In: Alterman L, Doyle GA, Izard MK (eds) Creatures of the dark: the nocturnal prosimians. Plenum Press, New York, pp 353–376
Sterling EJ, Richard AF (1995) Social organization in the aye-aye (Daubentonia madagascariensis) and the perceived distinctiveness of nocturnal primates. In: Alterman L, Doyle GA, Izard MK (eds) Creatures of the dark: the nocturnal prosimians. Plenum Press, New York, pp 439–451
Swaisgood RR, Lindburg DG, Zhou X, Owen MA (2000) The effects of sex, reproductive condition and context on discrimination of conspecific odours by giant pandas. Anim Behav 60:227–237
van Schaik CP, van Hooff JARAM (1983) On the ultimate causes of primate social systems. Behaviour 85:91–117
Watwood SL, Tyack PL, Wells RS (2004) Whistle sharing in paired male bottlenose dolphins, Tursiops truncatus. Behav Ecol Sociobiol 55:531–543
Weidt A, Hagenah N, Randrianambinina B, Radespiel U, Zimmermann E (2004) Social organization of the golden brown mouse lemur (Microcebus ravelobensis). Am J Phys Anthropol 123:40–51
Winter P, Handley P, Ploog D, Schott D (1973) Ontogeny of squirrel monkey calls under normal conditions and under acoustic isolation. Behaviour 67:230–239
Wrangham RW (1987) Evolution of social structure. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate Societies. The University of Chicago Press, Chicago, London, pp 282–296
Wyatt TD (2003) Pheromones and animal behaviour: communication by smell and taste. Cambridge University Press, Cambridge
Zietemann V (2001) Artendiversität bei Mausmakis: die Bedeutung der akustischen Kommunikation. PhD thesis, University of Hannover, Germany
Zimmermann E (1985a) The vocal repertoire of the adult Senegal bushbaby (Galago senegalensis senegalensis). Behaviour 94:212–233
Zimmermann E (1985b) Vocalizations and associated behaviors in adult slow loris (Nycticebus coucang). Folia Primatol 44:52–64
Zimmermann E (1992) Vocal communication by non-human primates. In: Jones S, Martin R, Pilbeam D (eds) The Cambridge encyclopedia of human evolution. Cambridge University Press, Cambridge, pp 124–127
Zimmermann E (1995) Acoustic communication in nocturnal prosimians. In: Altermann L, Doyle GA, Izard MK (eds) Creatures of the dark. Plenum Press, New York, pp 311–330
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, Vorobieva E, Wrogemann D, Hafen T (2000) Use of fingerprinting for species-discrimination of the gray (Microcebus murinus) and the rufous mouse lemur (Microcebus rufus). Int J Primatol 5:837–852
Zinner D, Hilgartner RD, Kappeler PM, Pietsch T, Ganzhorn JU (2003) Social organization of Lepilemur ruficaudatus. Int J Primatol 24:869–888
Zöfel P (1992) Statistik in der Praxis. Gustav Fischer Verlag, Stuttgart, Germany
Acknowledgements
We thank the Commission Tripartite of the Malagasy government, the Departement des Eaux et Forêts and the Association pour la Gestion des Aires for their permission to work in Ampijoroa and Prof. Berthe Rakotosamimanana and Dr. Daniel Rakotondravony, Faculté des Sciences, Université d’Antananarivo for logistic support. For field assistance, we thank Andrea Weidt, Katja Wallmeyer and Julia Schwarzer. The latter also contributed to the sound analysis. Dagmar Söndgerath gave helpful comments for statistical analysis. We thank the anonymous reviewers for helpful comments on earlier versions of the manuscript. The study complies with the current laws of Madagascar and was funded by the German Research Council (GK 289; Zi 345/12) and the Volkswagen Foundation (VW I/76968)
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by C. Nunn
Rights and permissions
About this article
Cite this article
Braune, P., Schmidt, S. & Zimmermann, E. Spacing and group coordination in a nocturnal primate, the golden brown mouse lemur (Microcebus ravelobensis): the role of olfactory and acoustic signals. Behav Ecol Sociobiol 58, 587–596 (2005). https://doi.org/10.1007/s00265-005-0944-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-005-0944-4