Loud Calls in Nocturnal Prosimians: Structure, Evolution and Ontogeny

  • Elke Zimmermann


Loud, long-distance or advertisement calls belong to the most distinctive primate vocalizations. They travel over long distances and have been described in virtually every genus. Thus, they are found in almost all families of strepsirhines (e.g., Petter and Charles-Dominique, 1979; Zimmermann, 1990, in press, for reviews) and anthropoids (tarsiers: e.g., Niemitz, 1984; marmosets and tamarins: e.g., Snowdon, 1989; cebids: e.g., Oppenheimer,1977; Robinson, 1981; Sekulic, 1982; cercopithecids: e.g., Byrne, 1982; Gautier and Gautier, 1977; Hohmann, 1991; Waser, 1982; gibbons: e.g., Deputte, 1982; Marshall and Marshall, 1976; Mitani, 1992; apes: e.g., Boehm, 1989; Hohmann and Fruth, this volume; Marier and Tenaza, 1977; Mitani and Nishida, 1993). Since loud calls have a highly stereotypic and species-specific vocal pattern across all primate taxa, they are often used in combination with reproductive or biochemical characters to identify species within monomorphic species groups, to clarify the status in polymorphic species or to develop inferences about phylogeny (e.g., Struhsaker, 1970, for guenons; Oates and Trocco, 1983, and Struhsaker, 1981, for Colobus monkeys; Haimoff et al., 1982, Marshall and Marshall, 1976, Marshall and Sugardjito, 1986, for gibbons; Snowdon et al., 1986, for golden lion tamarins; Gautier, 1988, for guenons; Zimmermann et al., 1988, Zimmermann, 1990, for bushbabies; Niemitz et al., 1991, for tarsiers; Macedonia and Stanger, submitted, for diurnal lemurs).


Mouse Lemur Advertisement Call Acoustic Structure Vocal Communication Loud Call 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Andrew, R.J., 1963, The origin and evolution of the calls and facial expressions of the primates, Behaviour 20: 1–109.CrossRefGoogle Scholar
  2. Bailey, W.J., 1991, “The Acoustic Behavior of Insects”, Chapman and Hall, London.Google Scholar
  3. Baker, M.C. and Cunningham, M.A., 1985, The biology of bird-song dialects, Behay. Brain Sci. 8: 85–133.CrossRefGoogle Scholar
  4. Barre, V., Lebec, A., Petter, J.-J., and Albingnac, R., 1988, Etude du Microcèbe par radiotracking dans le forêt de l’Ankarafantsika, in: “L’Equilibre des Ecosystèmes Forêstiers à Madagascar”, L. Rakotovao, V. Barre and J. Sayer, eds., IUCN, Gland.Google Scholar
  5. Barrett, E.B.M., 1984, “The ecology of sonic nocturnal arboreal mammals in the rain forest of peninsular Malaysia”, PhD thesis, University of Cambridge, unpubl.Google Scholar
  6. Bearder, S.K., 1974, “Aspects of the Ecology and Behaviour of the Thick-Tailed Bushbaby (Galago crassicaudatus), PhD thesis, Univ. of Witwatersrand, Johannesburg, unpubl.Google Scholar
  7. Bearder, S.K., 1987, Lorises, bushbabics and tarsiers: Diverse societies in solitary foragers, in: “Primate Societies”, B.B. Smuts, D.L. Cheney, R.M. Seyfarth, R.W.Wrangham and T.T.Struhsaker, eds., Univ. Chicago Press, Chicago.Google Scholar
  8. Benson, B., Binz, H., and Zimmermann, E. 1992, Vocalizations of infant and developing tree shrews (Tupaia belangen), J. Hamm. 73: 106–119.Google Scholar
  9. Boehm, Ch., 1989, Methods for isolating chimpanzee vocal communication, in: “Understanding Chimpanzees”, P.G. Heltne and L.A. Marquardt, eds., Harvard Univ. Press, Cambridge.Google Scholar
  10. Brown, C.H., 1989, The active space of blue monkey and grey-cheeked mangabey vocalizations, Anim. Behay. 37, 1023–1034.CrossRefGoogle Scholar
  11. Brown, C.H. and Gomez, R., 1992, Functional design features in primate vocal signals: The acoustic habitat and sound distortion, in: “Topics in Primatology, Vol. 1”, T. Nishida, W. C. McGrew, P. Marier, M. Pickfort and F. de Waal, eds., Univ. Tokyo Press. Tokyo.Google Scholar
  12. Byrne, R.W., 1982, Distance vocalizations of Guinea baboons (Papio papio) in Senegal: An analysis of function, Behaviour 75: 283–312.Google Scholar
  13. Cavalli-Sforza, L., Piazza, A., Menozzi, P., and Mountain, J.L., 1988, Reconstruction of human evolution: Bringing together genetic, archaeologic and linguistic data, Proc. Nat. Acad. Sci. 85: 6002–6006.PubMedCrossRefGoogle Scholar
  14. Charles-Dominique, P., 1977, “Ecology and Behaviour of Nocturnal Primates”, New York Columbia Univ. Press, New York.Google Scholar
  15. Cheney, D. L. and Seyfarth, R.M., 1990, “How Monkeys See the World”, Univ. Chicago Press, Chicago.Google Scholar
  16. Cheney, D.L. and Wrangham, R.W., 1987, Predation, in: “Primate Societies”, B.B. Smuts, D.L. Cheney, R.M. Seyfarth, R.W. Wrangham and T.T.Struhsaker, eds., Univ. Chicago Press, Chicago.Google Scholar
  17. Crystal, D., 1992, “The Cambridge Encyclopedia of Language”, Cambridge Univ. Press, Cambridge.Google Scholar
  18. Deputte, B.L., 1982, Duetting in male and female songs of the white-cheeked gibbon (Hylobates concolor), in: “Primate Communication”, Ch. T. Snowdon, Ch.H. Brown and M.R. Petersen, eds., Cambridge Univ. Press, Cambridge.Google Scholar
  19. Fay, R.R., 1988, “Hearing in Vertebrates. A Psychophysics Databook”, Hill Fay Ass., Winnetka.Google Scholar
  20. Elowson, A.M., Snowdon, C.T., and Sweet, C.J.,1992, Ontogeny of trill and J-call vocalizations in the pygmy marmoset, Cebuella pvgmaea, Animr. Behay. 43: 703–715.Google Scholar
  21. Gautier, J.P., 1988, Interspecific affinities among guenons as deduced from vocalizations, in: “A Primate Radiation: Evolutionary Biology of the African Guenons”, A. Gautier-Hion, F. Bourliere, J.-P. Gautier and J. Kingdon, eds., Cambridge Univ. Press, Cambridge.Google Scholar
  22. Gautier, J.P. and Gautier, A., 1977, Communication in Old World monkeys, in: “How Animals Communicate”, T.A. Seboek, ed., Indiana Univ. Press, Bloomington.Google Scholar
  23. Gautier, J.P. and Gautier, A., 1988, Vocal quavering: A basis for recognition in forest guenons, in: “Primate Vocal Communication”, D. Todt, P. Goedeking and D. Symmes, eds., Springer, Heidelberg.Google Scholar
  24. Goodman, S.M., O’Connor, S., and Langrand, O., 1993, A review of predation on lemurs: Implications for the evolution of social behavior in small nocturnal primates, in: “Lemur Social Systems and their Ecological Basis”, P.M. Kappeler and J.U. Ganzhorn, eds., Plenum Press, New York.Google Scholar
  25. Gould, S.J. and Lewontin, R.P.C., 1979, The spandrels of San Marco and the Panglossian paradigm: A critique of the adaptive program, Proc. R. Soc. London B 205: 581–598.CrossRefGoogle Scholar
  26. Gouzoules, S., Gouzoules, H., and Marier, P., 1984, Rhesus monkey (Macaca mulatta) screams:Google Scholar
  27. Representational signalling in the recruitment of agonistic aid, Anim. Behay. 32: 182–192.Google Scholar
  28. Green, S., 1975, Variation of vocal pattern with social situation in the Japanese monkey (Macaca fuscata). A field study, in: “Primate Behavior, Vol. 4”, L.A. Rosenblum, Academic Press, New York.Google Scholar
  29. Green, S., 1975, Dialects in Japanese monkeys: Vocal learning and cultural transmission of locale-specific vocal behavior? Z. Tierpsvchol. 38, 304–314.CrossRefGoogle Scholar
  30. Haimoff, E.H., Chivers, D.J., Gittins, S.P., and Whitten, A.J., 1982, A phylogeny of gibbons based on morphological and behavioural characters, Folia Primato!. 39: 213–237.CrossRefGoogle Scholar
  31. Harcourt, C. and Thornback, J., 1990, “Lemurs of Madagascar and the Comores”, IUCN, Gland.Google Scholar
  32. Harvey, P.H., Martin, R.D., and Clutton-Brock. T.H., 1987, Life histories in a comparative perspective, in: Primate Societies“, B.B. Smuts, D.L. Cheney, R.M. Seyfarth, R.W.Wrangham and T.T.Struhsaker, eds., Univ. Chicago Press, Chicago.Google Scholar
  33. Hauser, M.D., 1991, Sources of acoustic variation in rhesus macaques (Macaca mulatta) vocalizations, Ethology 89: 29–46.CrossRefGoogle Scholar
  34. Hauser, M.D., 1992, Articulatory and social factors influence the acoustic structure of rhesus monkey vocalizations: A learned mode of production, J. Acoust. Soc. Amer. 91: 2175–2179.CrossRefGoogle Scholar
  35. Hohmann, G., 1991, Comparative analysis of age-and sex-specific patterns of vocal behavior in four species of Old World monkeys, Folia Primatol. 56: 133–156.PubMedCrossRefGoogle Scholar
  36. Hodun, A., Snowdon, C.T., and Soini, P., 1981, Subspecific variation in the long calls of the tamarin, Saguinus fuscicollis, Z. Tier psvc%ol. 57: 97–110.CrossRefGoogle Scholar
  37. Jürgens, U., Hast, M., and Pratt, R., 1978, Effects of laryngeal nerve transection on squirrel monkey calls, J. Comp. Phvsiol. A 123: 23–29.CrossRefGoogle Scholar
  38. Krebs, J.R. and Davies, N.B., 1993, “An Introduction to Behavioural Ecology”, Blackwell Scientific Publ., Oxford.Google Scholar
  39. Kroodsma, D.E., 1982, Learning and the ontogeny of sound signals in birds, in: “Acoustic Communication in Birds, Vol. 2, Song Learning and its Consequences”, D.E. Kroodsma and E.H. Miller, eds., Academic Press, New York.Google Scholar
  40. Konishi, M.,1973, Locatable and nonlocatable acoustic signals for barn owls, American Nat. 107: 775–785.Google Scholar
  41. Konishi, M., 1985, Birdsong: from behavior to neuron, Ann. Rev. Neurosci. 8: 125–170.PubMedCrossRefGoogle Scholar
  42. Kugel, S., 1993, “Verhaltensbiologische und bioakustische Untersuchungen zur strukturellen Variabilität des Soziallauts ”Triller“ beim Mausmaki (Microcebus murinus), Diplomarbeit, Universität StuttgartHohenheim, unpubl.Google Scholar
  43. Kuhn, M., 1989, “Verhaltensbiologische Untersuchungen zur Ontogenese von Mausmakis (Microcebus murinus) mit besonderer Berücksichtigung der akustischen Kommunikation”, Diplomarbeit, Universität Stuttgart-Hohenheim, unpubl.Google Scholar
  44. Lieblich, A.K., Symmes, D., Newman, J.D., and Shapiro, M., 1980, Development of the isolation peep in laboratory-bred squirrel monkeys, Amin. Behay. 28: 1–9.CrossRefGoogle Scholar
  45. Macedonia, J.M. and Stanger, K.F., submitted, Phylogeny of the Lemuridae revisited: Evidence from communication signal structure, Folio Primatol.Google Scholar
  46. Maeda, T. and Masataka, N., 1987, Locale-specific vocal behaviour of the tamarin (Saguinus 1. labiatus), Ethology 75: 25–30.CrossRefGoogle Scholar
  47. Martin, R.D., 1972, A preliminary field-study of the Lesser Mouse Lemur (Microcebus murinus), Advances in Ethology 9: 43–90.Google Scholar
  48. Marier, P., 1955, Characteristics of some animal calls, Nature 176: 6–8.CrossRefGoogle Scholar
  49. Marier, P, 1975, Bird song and speech development: Could there be parallels? Amer. Scient. 58: 669–673.Google Scholar
  50. Marier, P., 1990, Song learning: The interface between behavior and neuroethology. Phil. Trans. R. Soc. Lond. B 329, 109–114.CrossRefGoogle Scholar
  51. Marier, P. and Tenaza, R., 1977, Signalling behavior of apes with special reference to vocalization, in: “How animals communicate ”, T.A. Seboek, ed., Indiana Univ. Press, Bloomington.Google Scholar
  52. Marshall, J.T. and Marshall, E.R., 1976, Gibbons and their territorial songs, Science 193: 235–237.PubMedCrossRefGoogle Scholar
  53. Marshall, J.T. and Sugardjito, J., 1986, Gibbon systematics, in: “Comparative Primate Biology, Vol.1:Google Scholar
  54. Systematics, Evolution and Anatomy“, D. Swindler and J. Erwin, eds., Alan R. Liss, New York.Google Scholar
  55. Mascagni, O. and Doyle, G.A., 1993, Infant distress vocalizations in the South African Lesser bushbaby (Galago nroholi), Int. J. Primatol. 14: 41–60.CrossRefGoogle Scholar
  56. Maurus, M., Streit, K.M., Barclay, D., Wiesner, E., and Kühlmorgen, B., 1988, A new approach to finding components essential for intraspecific communication, in: “Primate Vocal Communication”, D. Todt, P. Goedeking and D. Symmes, Springer, London.Google Scholar
  57. Mitani, J.C., 1992, Singing behavior of male gibbons: Field observations and experiments, in: “Topics in Primatology, Vol. 1, Human Origins”, T. Nishida, W.C. McGrew, P. Marier, M. Pickford and F.B.M. de Waal, eds., Univ. Tokyo Press, Tokyo.Google Scholar
  58. Mitani, J.C., Hasegawa, T., Gros-Louis, J., Marier, P., and Byrne, R., 1992, Dialects in wild chimpanzees? Am. J. Primatol. 27: 233–243.CrossRefGoogle Scholar
  59. Mitani, J.C.and Nishida, T. 1993, Contexts and social correlates of long-distance calling by male chimpanzees, -bain. Behay. 45: 735–746.CrossRefGoogle Scholar
  60. Nash, L.T., Bearder. S.K., and Olson, T.R., 1989, Synopsis of Galago species characteristics, Mt. J. Primatol. 10: 57–80.Google Scholar
  61. Niaussat, M.M. and Petter. J.J., 1980, Etude de la sensibilité auditive d’un lémurien malgache: Microcebus murinus, Manunalia 44: 553–558.Google Scholar
  62. Niemitz, C., 1984, “The Biology of Tarsiers”, Gustav Fischer Verlag, Stuttgart.Google Scholar
  63. Niemitz, C., Nietsch, A., Waiter, S., and Rumpler, Y., 1991, Tarsius dianae: A new primate species from Central Sulawesi (Indonesia), Folio Primatol. 56: 105–116.CrossRefGoogle Scholar
  64. Oates, J.F. and Trocco, T.F., 1983, Taxonomy and phylogeny of black-and -white colobus monkeys: Inferences from an analysis of loud call variation, Folia Primatol. 40: 83–113.PubMedCrossRefGoogle Scholar
  65. Oher, D.K., Wieman, L.A., Doyle, W.J., and Ross, C., 1976, Infant babbling and speech, J. Child Lang. 3: 1–11.Google Scholar
  66. Oppenheimer, J.R., 1977, Communication in New World monkeys, in: “How Animals Communicate”, T.A. Seboek, ed., Indiana Univ. Press, Bloomington.Google Scholar
  67. Oster, G.E. and Wilson, E.O., 1979, “ Caste and Ecology in Social Insects”, Princeton Univ. Press, Princeton.Google Scholar
  68. Payne, R.B., 1981, Population structure and social behavior. Models for testing the ecological significance of song dialects, in: “Natural Selection and Social Behavior”, R.D. Alexander and D.W. Tinkle, eds., Chiron Press, New York.Google Scholar
  69. Pages-Feuillade, E., 1988, Modalités de l’occupation de l’espace et relation interindividuelles chez un prosimien nocturne malgache, Microcebus mruinrrs, Folio Primatol. 50: 204–220.CrossRefGoogle Scholar
  70. Perret, M., 1992, Environmental and social determinants of sexual function in the male Lesser Mouse Lemur (Microcebus nmrinus), Folio Primatol. 59: 1–25.CrossRefGoogle Scholar
  71. Petter, J.-J. and Charles-Dominique, P., 1979, Vocal communication in prosimians, in: “Prosimian Behaviour”, G.A. Doyle and R.D. Martin, eds. Academic Press, New York.Google Scholar
  72. Petter-Rousseaux, A., 1975, Activité sexuelle de Microcebus nrurinus soumis à des regimes photoperiodiques experimentaux, Ann. Biol. Animal. Biochim. Biophys. 153: 503–508.CrossRefGoogle Scholar
  73. Ploog, D., 1992, The evolution of vocal communication, in: Nonverbal Vocal Communication.Google Scholar
  74. Comparative and Developmental Approaches“, H. Papousek, U. Jürgens and M. Papousek, eds., Cambridge Univ. Press, Cambridge.Google Scholar
  75. Richard, A.F., 1987, Malagasy prosimians: Female dominance, in: “Primate Societies”, B.B. Smuts, D.L. Cheney, R.M. Seyfarth, R.W. Wrangham and T.T. Struhsaker, eds., Univ. Chicago Press, Chicago.Google Scholar
  76. Robinson, J.G.,1981, The regulation of inter-and intra-group spacing during boundary encounters in the titi monkey, Callicebus moloch. Primates 22: 161–172.Google Scholar
  77. Rohlf, R.R. and Sokal, F.J., 1981, “Biometry”, W.H.Freeman, New York.Google Scholar
  78. Ryan, M.J. and Brenowitz, E.A., 1985, The role of body size, phylogeny and ambient noise in the evolution of bird song, Amer. Natur. 126: 87–100.CrossRefGoogle Scholar
  79. Sekulic, R., 1982, The function of howling in red howler monkeys (Alouatta seniculus), Behaviour 81: 3854.CrossRefGoogle Scholar
  80. Snowdon, C.T., 1989, The structure and usage of long calls in marmosets and tamarins, in: “Perspectives in Primate Biology, Vol. 3”, P.K.Seth and S. Seth, eds., Today and Tomorrow’s Printers and Publ., New Delhi.Google Scholar
  81. Snowdon, C.T. and Elowson, M., 1992, Ontogeny of primate vocal communication, in: “Topics in Primatology, Vol. 1: Human Origins”, T. Nishida, W.C. McGrew, P. Mader, M. Pickford and F.B.M. de Waal, eds., Univ. Tokyo Press, Tokyo.Google Scholar
  82. Snowdon, C.T., French, J.A., and Cleveland, J., 1986, Ontogeny of primate vocalizations: Models from bird song and human speech, in: “Current Perspectives in Primate Social Behavior”, D.M. Taub and F.A. King, eds., Van Nostrand Reinhold, New York.Google Scholar
  83. Snowdon, C.T., Hodun, A.L., Rosenberger, A.L., and Coimbra-Filho, A.,1986, Long call structures and its relationships to taxonomy in lion-tailed tamarins. Amer. J. Primatol. 11: 253–262.Google Scholar
  84. Stanger, K.F., 1988, “Lautrepertoire und begleitendes Verhalten von nachtaktiven Halbaffen”, Diplomarbeit, University of Tübingen, unpubl.Google Scholar
  85. Stanger, K.F., 1993, “Structure and Function of Vocalizations of Nocturnal Prosimians”, PhD thesis, University of Tübingen, unpubl.Google Scholar
  86. Struhsaker, T.T., 1970, Phylogenetic implications of some vocalizations of Cercopithecus monkeys, in: “Old World Monkeys, Evolution, Systematics and Behavior”, J.R. Napier and P.H. Napier, eds., Academic Press, New York.Google Scholar
  87. Struhsaker, T.T., 1981, Vocalizations, phylogeny and paleogeography of red colobus monkeys (Colobus badius), Aft. J. Ecol. 19: 265–283.CrossRefGoogle Scholar
  88. Vogel, C., 1973, Acoustical communication among free-ranging common Indian langurs (Presbytis ente!!us) in two different habitats of North India, Am. J. Phys. Anthrop. 38: 469–480.PubMedCrossRefGoogle Scholar
  89. Waser, P.M. and Waser, M.S., 1977, Experimental studies of primate vocalization: Specializations for long-distance propagation, Z. Tierpsychol. 43: 239–263.CrossRefGoogle Scholar
  90. Waser, P.M., 1982, The evolution of male loud calls among mangabeys and baboons, in: “Primate Communication”, C.T. Snowdon, C.H. Brown and M.R. Petersen, eds., Cambridge Univ. Press, Cambridge.Google Scholar
  91. Wickler, W., 1986, “Dialekte im Tierreich - Ihre Ursachen und Konsequenzen ”. Aschendorffsche Verlagsbuchhandlung, Münster.Google Scholar
  92. Wiley, R.H. and Richards, D.G., 1978, Physical constraints on acoustic communication in the atmosphere: Implications for animal vocalizations, Behay. Ecol. Sociobiol. 3: 69–94.CrossRefGoogle Scholar
  93. Winter, P., 1969, Dialects in squirrel monkeys: Vocalizations of the Roman arch type, Folia Primatol. 10: 216–229.PubMedCrossRefGoogle Scholar
  94. Zimmermann, E., 1981, First record of ultrasound in two prosimian species, Naturwissenschaften 68: 531.CrossRefGoogle Scholar
  95. Zimmermann, E., 1985a, Vocalizations and associated behaviours in adult slow loris (Nycticebus coucang), Folia primatol. 44: 52–64.CrossRefGoogle Scholar
  96. Zimmermann, E.,1985b, The vocal repertoire of the adult Senegal bushbaby (Galago senegalensis senegalensis), Behaviour 94: 211–233.Google Scholar
  97. Zimmermann, E., 1989a, Reproduction and behavioral development in slow loris (Nycticebus coucang), Human Evol. 4: 171–179.CrossRefGoogle Scholar
  98. Zimmermann, E.,1989b, Aspects of reproduction, behavioral and vocal development in Senegal bushbabies (Galago senegalensis), Intern. J. Primatol. 10: 1–16.Google Scholar
  99. Zimmermann, E., 1990, Differentiation of vocalizations in bushbabies (Galaginae) and the significance for assessing phylogenetic relationships, Z.Zool. Syst. Evol. 28: 217–239.CrossRefGoogle Scholar
  100. Zimmermann, E., 1991, Ontogeny of acoustic communication in prosimian primates, in: “Primatology today”, A. Ehara, T. Kimura, O. Takenaka and M. Iwamoto, eds., Elsevier, Amsterdam.Google Scholar
  101. Zimmermann, E., in press, Acoustic communication in nocturnal prosimians, in:“Creatures of the Dark. The biology of nocturnal prosimians”, K. Izard, L. Altermann and G.A. Doyle, eds., Plenum Press, New, York.Google Scholar
  102. Zimmermann, E., Bearder, S.K., Doyle, G.A., and Andersson, A., 1988. Variations in vocal patterns of Senegal and South African lesser bushbabies and their implications for taxonomic relationships, Folia Primatol. 51: 87–105.PubMedCrossRefGoogle Scholar
  103. Zimmermann, E. and Lerch, C., 1993, The complex acoustic design of an advertisement call in male mouse lemurs (Aficrocebus murinus) and sources of its variation, Ethology 93: 211–224.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1995

Authors and Affiliations

  • Elke Zimmermann
    • 1
  1. 1.Laboratory of BiocommunicationGerman Primate CenterGöttingenGermany

Personalised recommendations