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Evolutionary Origins of Primate Vocal Communication: Diversity, Flexibility, and Complexity of Vocalizations in Basal Primates

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Primate Hearing and Communication

Part of the book series: Springer Handbook of Auditory Research ((SHAR,volume 63))

Abstract

This chapter explores the importance of vocalizations in basal primates for modeling the evolutionary origins of primate social communication. A rich diversity in acoustic structures and signals, extending into the ultrasonic range, is used to govern various ecological and social challenges in their networks with varying degrees of social cohesiveness. Vocalizations convey information on specific emotions and on species, population, group, kin, and individual identity. Comparisons within the same phylogenetic group put forth the notion that natural selection limits cross-taxa vocal flexibility and favors universals in acoustic structure, whereas sexual and kin selection drive divergence. Bioacoustic research on vocal ontogeny depicted a babbling period with high vocal plasticity and an unexpected capability in adults to adapt their vocalizations to fluctuating background noise. Using a comparative bioacoustic approach, this chapter illuminates extraordinary cross-taxa variation in the acoustic spaces open for signal evolution and reveals that predation risk specifically shapes the acoustic space used. Comparison of vocal repertoire size, taken as an indicator of vocal complexity, reveals wide cross-taxa variation in call types and a striking variation in both solitary-ranging nocturnal and group-living diurnal species. The phylogenetic hypothesis and the social complexity hypothesis cannot fully explain this variation. Altogether, basal primates exhibit unique diversity, complexity, and flexibility of vocalizations for social communication, providing promising new avenues to trace the evolutionary origins of primate communication.

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References

  • Ackermann, H., Hage, S. R., & Ziegler, W. (2014). Brain mechanisms of acoustic communication in humans and nonhuman primates: An evolutionary perspective. Behavioral and Brain Sciences, 37(6), 529–546.

    Article  PubMed  Google Scholar 

  • Altenmüller, E., Schmidt, S., & Zimmermann, E. (2013). Evolution of emotional communication: From sounds in nonhuman mammals to speech and music in man. Oxford: Oxford University Press.

    Book  Google Scholar 

  • Ambrose, L. (2003). Three acoustic forms of Allen’s galagos (Primates; Galagonidae) in the Central African region. Primates, 44, 25–39.

    PubMed  Google Scholar 

  • Andrew, R. J. (1963). The origin and evolution of the calls and facial expressions of the primates. Behaviour, 20, 1–109.

    Article  Google Scholar 

  • August, P. V., & Anderson, J. G. T. (1987). Mammal sounds and motivation-structural rules: A test of the hypothesis. Journal of Mammalogy, 68(1), 1–9.

    Article  Google Scholar 

  • Bearder, S. K. (2007). A comparison of calling patterns in two nocturnal primates, Otolemur crassicaudatus and Galago moholi, as a guide to predation risk. In S. L. Gursky & K. A. I. Nekaris (Eds.), Primate anti-predator strategies (pp. 206–221). New York: Springer Science+Business Media.

    Chapter  Google Scholar 

  • Bearder, S. K., & Doyle, G. A. (1974). Field and laboratory studies of social organization in bushbabies (Galago senegalensis). Journal of Human Evolution, 3(1), 37–50. doi:10.1016/0047-2484(74)90105-5.

    Article  Google Scholar 

  • Becker, M., Buder, E., Bakeman, R., Price, M., & Ward, J. (2003a). Infant response to mother call patterns in Otolemur garnettii. Folia Primatologica, 74, 301–311.

    Article  Google Scholar 

  • Becker, M. L., Buder, E. H., & Ward, J. P. (2003b). Spectrographic description of vocalizations in captive Otolemur garnettii. International Journal of Primatology, 24(2), 415–446.

    Article  Google Scholar 

  • Bolt, L. M. (2013). Squealing rate indicates dominance rank in the male ring-tailed lemur (Lemur catta). American Journal of Primatology, 75(12), 1174–1184. doi:10.1002/ajp.22179.

    PubMed  Google Scholar 

  • Boughman, J. W. (2002). How sensory drive can promote speciation. Trends in Ecology and Evolution, 17(12), 571–577.

    Article  Google Scholar 

  • Braune, P., Schmidt, S., & Zimmermann, E. (2005). Spacing and group coordination in a nocturnal primate, the golden brown mouse lemur (Microcebus ravelobensis): The role of olfactory and acoustic signals. Behavioral Ecology and Sociobiology, 58, 587–596.

    Article  Google Scholar 

  • Braune, P., Schmidt, S., & Zimmermann, E. (2008). Acoustic divergence in the communication of cryptic species of nocturnal primates (Microcebus spp.) BMC Biology, 6, 19.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bregman, A. S. (1990). Auditory scene analysis: The perceptual organization of sound. Cambridge, MA: The MIT Press.

    Google Scholar 

  • Brumm, H., Voss, K., Köllmer, I., & Todt, D. (2004). Acoustic communication in noise: Regulation of call characteristics in a New World monkey. Journal of Experimental Biology, 207, 443–448.

    Article  PubMed  Google Scholar 

  • Burton, J. A., & Nietsch, A. (2010). Geographical variation in duet songs of Sulawesi tarsiers: Evidence for new cryptic species in south and southeast Sulawesi. International Journal of Primatology, 31(6), 1123–1146.

    Article  Google Scholar 

  • Butynski, T., Kingdon, J., & Kalina, J. (2013). Mammals of Africa. New York: Bloomsbury Publishing.

    Google Scholar 

  • Caeiro, C. C., Waller, B. M., Zimmermann, E., Burrows, A. M., & Davila-Ross, M. (2013). OrangFACS: A muscle-based facial movement coding system for orangutans (Pongo spp.) International Journal of Primatology, 34(1), 115–129.

    Article  Google Scholar 

  • Charles-Dominique, P., & Martin, R. D. (1972). Behavior and ecology of nocturnal prosimians. Zeitschrift fuer Tierpsychologie, 9, 1–89.

    Google Scholar 

  • Cheney, D. L., & Wrangham, R. W. (1987). Predation. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.), Primate societies (pp. 227–239). Chicago, IL: University of Chicago Press.

    Google Scholar 

  • Cherry, J. A., Izard, M. K., & Simons, E. L. (1987). Description of ultrasonic vocalizations of the mouse lemur (Microcebus murinus) and the fat-tailed dwarf lemur (Cheirogaleus medius). American Journal of Primatology, 13, 181–185.

    Article  Google Scholar 

  • Clark, A. B. (1988). Interspecific differences and discrimination in auditory and olfactory signals of Galago crassicaudatus and Galago garnettii. International Journal of Primatology, 9(6), 557–571.

    Article  Google Scholar 

  • Dagosto, M., Gebo, D. L., & Dolino, C. N. (2003). The natural history of the Philippine tarsier (Tarsius syrichta). In P. C. Wright, E. L. Simons, & S. Gursky (Eds.), Tarsiers: Past, present, and future (pp. 237–259). New Brunswick, NJ: Rutgers University Press.

    Google Scholar 

  • Darwin, C. (1872). The expression of the emotions in man and animals. New York: D. Appleton and Company.

    Book  Google Scholar 

  • Endler, J. A. (1992). Signals, signal conditions, and the direction of evolution. American Naturalist, 139, S125–S153.

    Article  Google Scholar 

  • Fay, R. R. (1988). Hearing in vertebrates: A psychophysics databook. Winnetka, IL: Hill-Fay Associates.

    Google Scholar 

  • Fichtel, C. (2008). Ontogeny of conspecific and heterospecific alarm call recognition in wild Verreaux’s sifakas (Propithecus verreauxi verreauxi). American Journal of Primatology, 70, 127–135.

    Article  PubMed  Google Scholar 

  • Fichtel, C. (2012). Predation. In J. C. Mitani, J. Call, P. M. Kappeler, R. Palombit, & J. B. Silk (Eds.), The evolution of primate societies (pp. 169–194). Chicago, IL: University of Chicago Press.

    Google Scholar 

  • Fichtel, C., & Hammerschmidt, K. (2002). Responses of redfronted lemurs to experimentally modified alarm calls: Evidence for urgency-based changes in call structure. Ethology, 108, 763–777.

    Article  Google Scholar 

  • Fichtel, C., & Kappeler, P. M. (2002). Anti-predator behavior of group-living Malagasy primates: Mixed evidence for a referential alarm call system. Behavioral Ecology and Sociobiology, 51, 262–275.

    Article  Google Scholar 

  • Fitch, W. T. (2010). The evolution of language. New York: Cambridge University Press.

    Book  Google Scholar 

  • Fleagle, J. G. (2013). Primate adaptation and evolution (3rd ed.). San Diego, CA: Academic Press.

    Google Scholar 

  • Freeberg, T. M., Dunbar, R. I. M., & Ord, T. J. (2012). Social complexity as a proximate and ultimate factor in communicative complexity. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 367(1597), 1785–1801. doi:10.1098/rstb.2011.0213.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gamba, M., & Giacoma, C. (2007). Quantitative acoustic analysis of the vocal repertoire of the crowned lemur. Ethology Ecology & Evolution, 19(4), 323–343.

    Article  Google Scholar 

  • Gamba, M., Friard, O., & Giacoma, C. (2012a). Vocal tract morphology determines species-specific features in vocal signals of Lemurs (Eulemur). International Journal of Primatology, 33(6), 1453–1466.

    Article  Google Scholar 

  • Gamba, M., Colombo, C., & Giacoma, C. (2012b). Acoustic cues to caller identity in lemurs: A case study. Journal of Ethology, 30(1), 191–196. doi:10.1007/s10164-011-0291-z.

    Article  Google Scholar 

  • Gamba, M., Favaro, L., Torti, V., Sorrentino, V., & Giacoma, C. (2011). Vocal tract flexibility and variation in the vocal output in wild indris. Bioacoustics, 20(3), 251–265.

    Article  Google Scholar 

  • Geissmann, T., & Mutschler, T. (2006). Diurnal distribution of loud calls in sympatric wild indris (Indri indri) and ruffed lemurs (Varecia variegata): Implications for call functions. Primates, 47(4), 393–396. doi:10.1007/s10329-006-0189-5.

    Article  PubMed  Google Scholar 

  • Giacoma, C., Sorrentino, V., Rabarivola, C., & Gamba, M. (2010). Sex differences in the song of Indri indri. International Journal of Primatology, 31(4), 539–551.

    Article  Google Scholar 

  • Goodman, S. M., O'Connor, S., & Langrand, O. (1993). A review of predation on lemurs: Implications for the evolution of social behavior in small, norturnal primates. In P. M. Kappeler & J. U. Ganzhorn (Eds.), Lemur social systems and their ecological basis (pp. 51–66). New York: Plenum Press.

    Chapter  Google Scholar 

  • Gosset, D., Fornasieri, I., & Roeder, J. J. (2003). Acoustic structure and contexts of emission of vocal signals by black lemurs. Evolution of Communication, 4(2), 225–251.

    Article  Google Scholar 

  • Groves, C., & Shekelle, M. (2010). The genera and species of Tarsiidae. International Journal of Primatology, 31(6), 1071–1082. doi:10.1007/s10764-010-9443-1.

    Article  Google Scholar 

  • Gursky, S. L., & Nekaris, K. A. I. (2007). Primate anti-predator strategies. New York: Springer Science+Business Media.

    Book  Google Scholar 

  • Hafen, T., Neveu, H., Rumpler, Y., Wilden, I., & Zimmermann, E. (1998). Acoustically dimorphic advertisement calls separate morphologically and genetically homogenous populations of the grey mouse lemur (Microcebus murinus). Folia Primatologica, 69(Suppl.1), 342–356.

    Article  Google Scholar 

  • Hage, S. R. (2013). Audio-vocal interactions during vocal communication in squirrel monkeys and their neurobiological implications. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, 199(7), 663–668.

    Article  PubMed  Google Scholar 

  • Hartig, G., Churakov, G., Warren, W. C., Brosius, J., et al. (2013). Retrophylogenomics place tarsiers on the evolutionary branch of anthropoids. Scientific Reports, 3. doi:10.1038/srep01756.

  • Harvey, P. H., & Pagel, M. D. (1991). The comparative method in evolutionary biology. Oxford: Oxford University Press.

    Google Scholar 

  • Horvath, J. E., Weisrock, D. W., Embry, S. L., Fiorentino, I., et al. (2008). Development and application of a phylogenomic toolkit: Resolving the evolutionary history of Madagascar’s lemurs. Genome Research, 18(3), 489–499. doi:10.1101/Gr.7265208.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jolly, A. (1966). Lemur social behavior and primate intelligence—Step from prosimian to monkey intelligence probably took place in a social context. Science, 153(3735), 501–506. doi:10.1126/science.153.3735.501.

    Article  CAS  PubMed  Google Scholar 

  • Junqua, J. C. (1996). The influence of acoustics on speech production: A noise-induced stress phenomenon known as the Lombard reflex. Speech Communication, 20(1-2), 13–22. doi:10.1016/S0167-6393(96)00041-6.

    Article  Google Scholar 

  • Kappeler, P. M. (2012). The behavioral ecology of strepsirrhines and tarsiers. In J. C. Mitani, J. Call, P. M. Kappeler, R. A. Palombit, & J. B. Silk (Eds.), The evolution of primate societies (pp. 7–28). Chicago, IL: University of Chicago Press.

    Google Scholar 

  • Kessler, S. E., Scheumann, M., Nash, L. T., & Zimmermann, E. (2012). Paternal kin recognition in the high frequency/ultrasonic range in a solitary foraging mammal. BMC Ecology, 12(1), 26. doi:10.1186/1472-6785-12-26.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kessler, S. E., Radespiel, U., Hasiniaina, A. I. F., Leliveld, L. M. C., & Nash, L. T. (2014). Modeling the origins of mammalian sociality: Moderate evidence for matrilineal signatures in mouse lemur vocalizations. Frontiers in Zoology, 11, 14.

    Article  PubMed  PubMed Central  Google Scholar 

  • Klopfer, P. H. (1977). Communication in prosimians. In T. A. Sebeok (Ed.), How animals communicate (pp. 841–850). Bloomington, IN: Indiana University Press.

    Google Scholar 

  • Knörnschild, M. (2014). Vocal production learning in bats. Current Opinion in Neurobiology, 28, 80–85. doi:10.1016/j.conb.2014.06.014.

    Article  PubMed  CAS  Google Scholar 

  • Kulahci, I. G., Rubenstein, D. I., & Ghazanfar, A. A. (2015). Lemurs groom-at-a-distance through vocal networks. Animal Behaviour, 110, 179–186.

    Article  Google Scholar 

  • Lehman, S. M., Radespiel, U., & Zimmermann, E. (2016). Dwarf and mouse lemurs of Madagascar: Biology, behavior, and conservation biogeography of the Cheirogaleidae. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Leliveld, L. M. C., Scheumann, M., & Zimmermann, E. (2011). Acoustic correlates of individuality in the vocal repertoire of a nocturnal primate (Microcebus murinus). The Journal of the Acoustical Society of America, 129(4), 2278–2288.

    Article  PubMed  Google Scholar 

  • Linn, S. N. (2013). Mother-offspring communication in grey mouse lemurs (Microcebus murinus) during reunions. M.S. thesis, University of Veterinary Medicine Hannover, Hannover, Germany.

    Google Scholar 

  • Macedonia, J. M. (1986). Individuality in a contact call of the ringtailed lemur (Lemur catta). American Journal of Primatology, 11, 163–179.

    Article  Google Scholar 

  • Macedonia, J. M. (1990). What is communicated in the antipredator calls of lemurs: Evidence from playback experiments with ringtailed and ruffed lemurs. Ethology, 86, 177–190.

    Article  Google Scholar 

  • Macedonia, J. M. (1993). The vocal repertoire of the ring-tailed lemur (Lemur catta). Folia Primatologica, 61(4), 186–217.

    Article  CAS  Google Scholar 

  • Macedonia, J. M., & Stanger, K. F. (1994). Phylogeny of the Lemuridae revisited—Evidence from communication signals. Folia Primatologica, 63(1), 1–43. doi:10.1159/000156787.

    Article  CAS  Google Scholar 

  • Macedonia, J. M., & Taylor, L. L. (1985). Subspecific divergence in a loud call of the ruffed lemur (Varecia variegata). American Journal of Primatology, 9, 295–304.

    Article  Google Scholar 

  • Maretti, G., Sorrentino, V., Finomana, A., Gamba, M., & Giacoma, C. (2010). Not just a pretty song: An overview of the vocal repertoire of Indri indri. Journal of Anthropological Sciences, 88, 151–165.

    PubMed  Google Scholar 

  • Martin, R. D., & Ross, C. F. (2005). The evolutionary and ecological context of primate vision. In J. J. Kremers (Ed.), The primate visual system: A comparative approach (pp. 1–36). New York: John Wiley & Sons..

    Google Scholar 

  • Masters, J. C. (1991). Loud calls of Galago crassicaudatus and G. garnettii and their relation to habitat structure. Primates, 32(2), 153–167.

    Article  Google Scholar 

  • Matsui, A., Rakotondraparany, F., Munechika, I., Hasegawa, M., & Horai, S. (2009). Molecular phylogeny and evolution of prosimians based on complete sequences of mitochondrial DNAs. Gene, 441(1-2), 53–66. doi:10.1016/j.gene.2008.08.024.

    Article  CAS  PubMed  Google Scholar 

  • McComb, K., & Semple, S. (2005). Coevolution of vocal communication and sociality in primates. Biology Letters, 1, 381–385.

    Article  PubMed  PubMed Central  Google Scholar 

  • Méndez-Cárdenas, M. G., & Zimmermann, E. (2009). Duetting—A mechanism to strengthen pair bonds in a dispersed pair-living primate (Lepilemur edwardsi)? American Journal of Physical Anthropology, 139(4), 523–532. doi:10.1002/ajpa.21017.

    Article  PubMed  Google Scholar 

  • Méndez-Cárdenas, M., Randrianambinina, B., Rabesandratana, A., Rasoloharijaona, S., & Zimmermann, E. (2008). Geographic variation in loud calls of sportive lemurs (Lepilemur ssp.) and their implication for conservation. American Journal of Primatology, 70(9), 828–838.

    Article  PubMed  Google Scholar 

  • Merker, S., & Groves, C. P. (2006). Tarsius lariang: A new primate species from western Central Sulawesi. International Journal of Primatology, 27(2), 465–485.

    Article  Google Scholar 

  • Merker, S., Driller, C., Perwitasari-Farajallah, D., Pamungkas, J., & Zischler, H. (2009). Elucidating geological and biological processes underlying the diversification of Sulawesi tarsiers. Proceedings of the National Academy of Sciences of the United States of America, 106(21), 8459–8464.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Merker, S., Driller, C., Dahruddin, H., Wirdateti, Sinaga, W., et al. (2010). Tarsius wallacei: A new tarsier species from Central Sulawesi occupies a discontinuous range. International Journal of Primatology, 31(6), 1107–1122.

    Article  Google Scholar 

  • Mittermeier, R. A., Louis Jr., E. E., Richardson, M., Schwitzer, C., et al. (2010). Lemurs of Madagascar (3rd ed.). Arlington, VA: Conservation International.

    Google Scholar 

  • Morton, E. S. (1975). Ecological sources of selection on avian sounds. American Naturalist, 109, 17–34.

    Article  Google Scholar 

  • Morton, E. S. (1977). On the occurrence and significance of motivation-structural rules in some bird and mammal sounds. American Naturalist, 111, 855–869.

    Article  Google Scholar 

  • Müller, A. E., & Thalmann, U. (2000). Origin and evolution of primate social organisation: A reconstruction. Biological Reviews, 75, 405–435.

    Article  PubMed  Google Scholar 

  • Nash, L. T., & Harcourt, C. S. (1986). Social organization of galagos in Kenyan coastal forests. 2. Galago garnettii. American Journal of Primatology, 10(4), 357–369. doi:10.1002/ajp.1350100407.

    Article  Google Scholar 

  • Neri-Arboleda, I., Stott, P., & Arboleda, N. P. (2002). Home ranges, spatial movements and habitat associations of the Philippine tarsier (Tarsius syrichta) in Corella, Bohol. Journal of Zoology, 257, 387–402.

    Article  Google Scholar 

  • Newman, J. D., Depeine, C. D., & Becker, M. L. (2013). Variation in strepsirrhine infant isolation calls and its evolutionary implications. In J. Masters, M. Gamba, & F. Génin (Eds.), Leaping ahead: Advances in prosimian biology (pp. 279–286). New York: Springer Science+Business Media.

    Google Scholar 

  • Niemitz, C. (1984). Vocal communication of two tarsier species (Tarsius bancanus and Tarsius spectrum). In C. Niemitz (Ed.), Biology of tarsiers (pp. 129–141). Stuttgart: Gustav Fischer Verlag.

    Google Scholar 

  • Niemitz, C., Nietsch, A., Warter, S., & Rumpler, Y. (1991). Tarsius dianae: A new primate species from central Sulawesi (Indonesia). Folia Primatologica, 56, 105–116.

    Article  CAS  Google Scholar 

  • Nietsch, A. (1999). Duet vocalizations among different populations of Sulawesi tarsiers. International Journal of Primatology, 20(4), 567–583.

    Article  Google Scholar 

  • Nietsch, A. (2003). Outline of the vocal behavior of Tarsius spectrum: Call features, associated behaviors, and biological functions. In P. C. Wright, E. L. Simons, & S. Gursky (Eds.), Tarsiers: Past, present, and future (pp. 196–220). New Brunswick, NJ: Rutgers University Press.

    Google Scholar 

  • Oda, R. (2002). Individual distinctiveness of the contact calls of ring-tailed lemurs. Folia Primatologica, 73, 132–136.

    Article  Google Scholar 

  • Ord, T. J., & Garcia-Porta, J. (2012). Is sociality required for the evolution of communicative complexity? Evidence weighed against alternative hypotheses in diverse taxonomic groups. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 367(1597), 1811–1828. doi:10.1098/rstb.2011.0215.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pages, E. (1980). Ethoecology of Microcebus coquereli during the dry season. In P. Charles-Dominique (Ed.), Nocturnal Malagasy primates: Ecology, physiology, and behavior (pp. 97–116). New York: Academic Press.

    Google Scholar 

  • Parr, L. A., Waller, B. M., & Fugate, J. (2005). Emotional communication in primates: Implications for neurobiology. Current Opinion in Neurobiology, 15, 716–720.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patel, E. R., & Owren, M. J. (2012). Silky sifaka (Propithecus candidus) “zzuss” vocalizations: Sexual dimorphism, individuality, and function in the alarm call of a monomorphic lemur. The Journal of the Acoustical Society of America, 132(3), 1799–1810. doi:10.1121/1.4740475.

    Article  PubMed  Google Scholar 

  • Pereira, M. E., & Macedonia, J. M. (1991). Ringtailed lemur anti-predator calls denote predator class, not response urgency. Animal Behaviour, 41(3), 543–544.

    Article  Google Scholar 

  • Pereira, M. E., Seeligson, M. L., & Macedonia, J. M. (1988). The behavioral repertoire of the black-and-white ruffed lemur, Varecia variegata variegata (Primates, Lemuridae). Folia Primatologica, 51(1), 1–32. doi:10.1159/000156353.

    Article  CAS  Google Scholar 

  • Perelman, P., Johnson, W. E., Roos, C., Seuánez, H. N., et al. (2011). A molecular phylogeny of living primates. PLoS Genetics, 7(3), e1001342. doi:10.1371/journal.pgen.1001342.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petter, J. J., & Charles-Dominique, P. (1979). Vocal communication in prosimians. In G. A. Doyle & R. D. Martin (Eds.), The study of prosimian behavior (pp. 247–305). New York: Academic Press.

    Chapter  Google Scholar 

  • Petter, J. J., Albignac, R., & Rumpler, Y. (1977). Faune de Madagascar 44: Mammiferes, Lemuriens (primates prosimiens). Paris: Ostrom CNRS.

    Google Scholar 

  • Pflüger, F. J., & Fichtel, C. (2012). On the function of redfronted lemur’s close calls. Animal Cognition, 15(5), 823–831.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pollard, K. A., & Blumstein, D. T. (2012). Evolving communicative complexity: Insights from rodents and beyond. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 367(1597), 1869–1878. doi:10.1098/rstb.2011.0221.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pollock, J. I. (1986). The song in the indris (Indri indri; Primates: Lemuroidea): Natural history, form and function. International Journal of Primatology, 7(3), 225–264.

    Article  Google Scholar 

  • Radespiel, U. (2000). Sociality in the gray mouse lemur (Microcebus murinus) in northwestern Madagascar. American Journal of Primatology, 51, 21–40.

    Article  CAS  PubMed  Google Scholar 

  • Ramanankirahina, R., Joly, M., & Zimmermann, E. (2011). Peaceful primates: Affiliation, aggression, and the question of female dominance in a nocturnal pair-living lemur (Avahi occidentalis). American Journal of Primatology, 73(12), 1261–1268. doi:10.1002/ajp.20998.

    Article  PubMed  Google Scholar 

  • Ramanankirahina, R., Joly, M., & Zimmermann, E. (2012). Seasonal effects on sleeping site ecology in a nocturnal pair-living lemur (Avahi occidentalis). International Journal of Primatology, 33(2), 428–439.

    Article  Google Scholar 

  • Ramanankirahina, R., Joly, M., Scheumann, M., & Zimmermann, E. (2015). The role of acoustic signaling for spacing and group coordination in a nocturnal, pair-living primate, the western woolly lemur (Avahi occidentalis). American Journal of Physical Anthropology, 159(3), 466–477. doi:10.1002/ajpa.22898.

    Article  PubMed  Google Scholar 

  • Ramsier, M. A. (2013). Evolution of auditory sensitivity among strepsirrhine primates. In J. Masters, M. Gamba, & F. Génin (Eds.), Leaping ahead: Advances in prosimian biology (pp. 265–270). New York: Springer Science+Business Media.

    Google Scholar 

  • Ramsier, M. A., & Dominy, N. J. (2012). Receiver bias and the acoustic ecology of aye-ayes (Daubentonia madagascariensis). Communicative and Integrative Biology, 5(6), 637–640. doi:10.4161/cib.21509.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ramsier, M. A., Cunningham, A. J., Finneran, J. J., & Dominy, N. J. (2012a). Social drive and the evolution of primate hearing. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 367(1597), 1860–1868.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ramsier, M. A., Cunningham, A. J., Moritz, G. L., Finneran, J. J., et al. (2012b). Primate communication in the pure ultrasound. Biology Letters, 8(4), 508–511.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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). American Journal of Physical Anthropology, 122(3), 251–258. doi:10.1002/ajpa.10281.

    Article  PubMed  Google Scholar 

  • Rasoloharijaona, S., Randrianambinina, B., Braune, P., & Zimmermann, E. (2006). Loud calling, spacing, and cohesiveness in a nocturnal primate, the Milne Edwards’ sportive lemur (Lepilemur edwardsi). American Journal of Physical Anthropology, 129, 591–600.

    Article  PubMed  Google Scholar 

  • Řeháková-Petrů, M., Policht, R., & Peške, L. (2012). Acoustic repertoire of the Philippine tarsier (Tarsius syrichta fraterculus) and individual variation of long-distance calls. International Journal of Zoology, 2012, 10. Article ID 602401.

    Article  Google Scholar 

  • Richard, A. F. (1985). Primates in nature. New York: W.H. Freeman and Company.

    Google Scholar 

  • Ross, C. (2003). Life history, infant care strategies, and brain size in primates. In P. M. Kappeler & M. E. Pereira (Eds.), Primate life histories and socioecology (pp. 266–284). Chicago, IL: University of Chicago Press.

    Google Scholar 

  • Scheumann, M., Rabesandratana, A., & Zimmermann, E. (2007a). Predation, communication, and cognition in lemurs. In S. L. Gursky & K. A. I. Nekaris (Eds.), Primate anti-predator strategies (pp. 100–126). New York: Springer Science+Business Media.

    Chapter  Google Scholar 

  • Scheumann, M., Zimmermann, E., & Deichsel, G. (2007b). Context-specific calls signal infants’ needs in a strepsirrhine primate, the gray mouse lemur (Microcebus murinus). Developmental Psychobiology, 49, 708–718.

    Article  PubMed  Google Scholar 

  • Schopf, C. (2013). Acoustic communication in noise: The gray mouse lemur as a primate model. Ph.D. dissertation, Tierärztliche Hochschule, Institut für Zoologie, Hannover.

    Google Scholar 

  • Semple, S., & Higham, J. P. (2013). Primate signals: Current issues and perspectives. American Journal of Primatology, 75(7), 613–620. doi:10.1002/ajp.22139.

    Article  PubMed  Google Scholar 

  • Simmons, N. B., Seymour, K. L., Habersetzer, J., & Gunnell, G. F. (2008). Primitive early eocene bat from Wyoming and the evolution of flight and echolocation. Nature, 451(7180), 818–821. doi:10.1038/nature06549.

  • Stanger, K. F. (1993). Structure and function of the vocalizations of nocturnal prosimians (Cheirogaleidae). Ph.D. dissertation, Eberhard-Karls-Universität, Tübingen, Germany.

    Google Scholar 

  • Stanger, K. F., & Macedonia, J. M. (1994). Vocalizations of aye-ayes (Daubentonia madagascariensis) in captivity. Folia Primatologica, 62(1-3), 160–169. doi:10.1159/000156773.

    Article  CAS  Google Scholar 

  • Tandy, J. M. (1976). Communication in Galago crassicaudatus. Primates, 17(4), 513–526.

    Article  Google Scholar 

  • Tattersall, I. (1979). Patterns of activity in the Mayotte lemur, Lemur fulvus mayottensis. Journal of Mammalogy, 60(2), 314–323. doi:10.2307/1379802.

    Article  Google Scholar 

  • Thalmann, U. (2003). Avahi, woolly lemurs, Avahy, Fotsy-fe, Ampongy, Tsarafangitra, Dadintsifaky. In S. M. Goodman & J. P. Benstead (Eds.), The natural history of Madagascar (pp. 1340–1342). Chicago, IL: University of Chicago Press.

    Google Scholar 

  • Thierry, B., Iwaniuk, A. N., & Pellis, S. M. (2000). The influence of phylogeny on the social behaviour of macaques (Primates: Cercopithecidae, genus Macaca). Ethology, 106, 713–728.

    Article  Google Scholar 

  • Torti, V., Gamba, M., Rabemananjara, Z. H., & Giacoma, C. (2013). The songs of the indris (Mammalia: Primates: Indridae): Contextual variation in the long-distance calls of a lemur. Italian Journal of Zoology, 80(4), 596–607.

    Article  Google Scholar 

  • Trillmich, J., Fichtel, C., & Kappeler, P. M. (2004). Coordination of group movements in wild verreaux’s sifakas (Propithecus verreauxi). Behaviour, 141, 1103–1120.

    Article  Google Scholar 

  • Veselka, N. (2010). A bony connection signals laryngeal echolocation in bats. Nature, 463, 939–942. doi:10.1038/nature08737.

    Article  CAS  PubMed  Google Scholar 

  • Ward, S. C., & Sussman, R. W. (1979). Correlates between locomotor anatomy and behavior in two sympatric species of Lemur. American Journal of Primatology, 50(4), 575–590.

    CAS  Google Scholar 

  • Wheeler, B. C., & Fischer, J. (2015). The blurred boundaries of functional reference: A response to Scarantino & Clay. Animal Behaviour, 100, E9–E13. doi:10.1016/j.anbehav.2014.11.007.

    Article  Google Scholar 

  • Wiens, F., & Zitzmann, A. (2003). Social structure of the solitary slow loris Nycticebus coucang (Lorisidae). Journal of Zoology, 261, 35–46. doi:10.1017/S0952836903003947.

    Article  Google Scholar 

  • Wilkins, M. R., Seddon, N., & Safran, R. J. (2013). Evolutionary divergence in acoustic signals: Causes and consequences. Trends in Ecology & Evolution, 28(3), 156–166.

    Article  Google Scholar 

  • Wright, P. C., & Simons, E. L. (1984). Calls of the Mindanao tarsier (Tarsius syrichta). American Journal of Physical Anthropology, 63(2), 236.

    Google Scholar 

  • Yoder, A. D. (1997). Back to the future: A synthesis of strepsirrhine systematics. Evolutionary Anthropology, 6(1), 11–22.

    Article  Google Scholar 

  • Zimmermann, E. (1981). First record of ultrasound in two prosimian species. Naturwissenschaften, 68(10), 531–532.

    Article  Google Scholar 

  • Zimmermann, E. (1985). Vocalizations and associated behaviors in adult slow loris (Nycticebus coucang). Folia Primatologica, 44(1), 52–64. doi:10.1159/000156197.

    Article  Google Scholar 

  • Zimmermann, E. (1989a). Reproduction and behavioral development in slow loris (Nycticebus coucang). Human Evolution, 4, 171–179.

    Article  Google Scholar 

  • Zimmermann, E. (1989b). Aspects of reproduction, behavioral and vocal development of Senegal bushbabys (Galago senegalensis). International Journal of Primatology, 10, 1–16.

    Article  Google Scholar 

  • Zimmermann, E. (1990). Differentiation of vocalizations in bushbabies (Galaginae, Prosimiae, Primates) and the significance for assessing phylogenetic relationships. Zeitschrift fuer zoologische Systematik und Evolutionsforschung, 28, 217–239.

    Article  Google Scholar 

  • Zimmermann, E. (1991). Ontogeny of acoustic communication in prosimian primates. In A. Ehara, O. Takenaka, & M. Iwamoto (Eds.), Primatology today (pp. 337–340). Amsterdam: Elsevier.

    Google Scholar 

  • Zimmermann, E. (1995a). Acoustic communication in nocturnal prosimians. In L. Alterman, G. A. Doyle, & M. K. Izard (Eds.), Creatures of the dark: The nocturnal prosimians (pp. 311–330). New York: Plenum Press.

    Chapter  Google Scholar 

  • Zimmermann, E. (1995b). Loud calls in nocturnal prosimians: Structure, evolution and ontogeny. In E. Zimmermann, J. D. Newman, & U. Jürgens (Eds.), Current topics in primate vocal communication (pp. 47–72). New York: Plenum Press.

    Chapter  Google Scholar 

  • Zimmermann, E. (2010). Vocal expression of emotion in a nocturnal prosimian primate group, mouse lemurs. In S. M. Brudzynski (Ed.), Handbook of mammalian vocalization: An integrative neuroscience approach (pp. 215–226). New York: Academic Press.

    Chapter  Google Scholar 

  • Zimmermann, E. (2016). Acoustic divergence in communication of cheirogaleids with special emphasis to mouse lemurs. In S. M. Lehman, U. Radespiel, & E. Zimmermann (Eds.), Dwarf and mouse lemurs of Madagascar: Biology, behavior and conservation biogeography of the Cheirogaleidae (pp. 405–421). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Zimmermann, E., & Hafen, T. G. (2001). Colony specificity in a social call of mouse lemurs (Microcebus spp.). American Journal of Primatology, 54, 129–141.

    Article  CAS  PubMed  Google Scholar 

  • Zimmermann, E., & Radespiel, U. (2013). Primate life histories. In W. Henke & I. Tattersall (Eds.), Handbook of paleoanthropology (Vol. 3, pp. 1527–1592). Berlin: Springer Science+Business Media.

    Google Scholar 

  • Zimmermann, E., & Radespiel, U. (2014). Species concepts, diversity, and evolution in primates: Lessons to be learned from mouse lemurs. Evolutionary Anthropology, 23(1), 11–14. doi:10.1002/evan.21388.

    Article  PubMed  Google Scholar 

  • Zimmermann, E., Bearder, S. K., Doyle, G. A., & Andersson, A. B. (1988). Variations in vocal patterns of Senegal and South African lesser bushbabies and their implications for taxonomic relationships. Folia Primatologica (Basel), 51(2-3), 87–105.

    Article  CAS  Google Scholar 

  • Zimmermann, E., Leliveld, L. M. C., & Schehka, S. (2013). Toward the evolutionary roots of affective prosody in human acoustic communication: A comparative approach to mammalian voices. In E. Altenmüller, S. Schmidt, & E. Zimmermann (Eds.), Evolution of emotional communication: From sounds in nonhuman mammals to speech and music in man (pp. 116–132). Oxford: Oxford University Press.

    Chapter  Google Scholar 

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Acknowledgments

I thank Marissa Ramsier, Rolf Quam, and Art Popper for inviting me to contribute to this volume and for their constructive remarks. I further thank Sabine Schmidt, who commented on a previous version of this manuscript and helped to clarify some arguments, and Ute Radespiel and Marina Scheumann for their long-term collaboration. Sönke von den Berg and Tjard Bergmann are thanked for technical support. My research on acoustic communication in primates was supported by various resources (e.g., Deutscher Akademischer Austauschdienst [DAAD], Volkswagenstiftung [VW], Deutsche Forschungsgemeinschaft [DFG], and private sponsors).

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Elke Zimmermann states that she has no conflicts of interest.

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Zimmermann, E. (2017). Evolutionary Origins of Primate Vocal Communication: Diversity, Flexibility, and Complexity of Vocalizations in Basal Primates. In: Quam, R., Ramsier, M., Fay, R., Popper, A. (eds) Primate Hearing and Communication. Springer Handbook of Auditory Research, vol 63. Springer, Cham. https://doi.org/10.1007/978-3-319-59478-1_5

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