We present the spectrographic description of the vocal repertoire of the Philippine tarsier (Tarsius syrichta fraterculus), a solitary living nocturnal primate for which a very limited information about acoustic communication exists to date. The majority of vocalizations were performed around sunset and, less frequently, at sunrise. We identified eight call types. Five calls recorded during communication between adults included three long-distance calls—loud call, smack-whistle, and whistle—then a soft locust-like chirp and a bird-like trill. Two other calls—cheep and twitter—were recorded during mother-infant communication. One distress call was emitted by adults during handling. All calls were performed in the 9752？Hz to more than 22？kHz frequency range. This study provides the first evidence of individual variation in the long-distance calls performed by tarsiers. Moreover, our study provides a basis for future comparison within as well as between tarsier species taxonomy. Bioacoustic methods can be used in monitoring of these cryptic species and determining their distribution range. Thus, bioacoustic studies can help to improve conservation strategies of different population/species. 1. Introduction Many nonhuman primates use vocalizations as a primary mode of communication. Following studies of monkey and apes, investigators have begun to understand the role of the auditory communication in nocturnal, mainly strepsirhine, primates during the past decades, for example, [1–9]. Similarly to anthropoid primates, strepsirhines use vocalizations to contact conspecifics, announce territorial boundaries, or announce a potential threat. Vocalization is also used in spacing and group coordination [7, 10–12]. The most conspicuous signals that are most commonly researched during studies of primate communication are the long-distance calls, often referred as loud calls. Long-distance calls have received much attention from researchers studying nocturnal primate communication; however, complete acoustic repertoires including the close-range communication between conspecifics of nocturnal primates have only been described for a limited number of species (e.g., bush babies [1, 7], greater bamboo lemur [13], and crowned lemur [2]). Tarsiers are small nocturnal primates native to Asia. The Philippine tarsier (Tarsius syrichta) is the only species living in the Philippines. Due to the nocturnal and cryptic nature of tarsiers, vocalizations and scent marking have been recognized as main modes of communication [14, 15]. A recent morphological study of the brain
References
[1]
M. L. Becker, E. H. Buder, and J. P. Ward, “Spectrographic description of vocalizations in captive Otolemur garnettii,” International Journal of Primatology, vol. 24, no. 2, pp. 415–446, 2003.
[2]
M. Gamba and C. Giacoma, “Quantitative acoustic analysis of the vocal repertoire of the crowned lemur,” Ethology Ecology & Evolution, vol. 19, no. 4, pp. 323–343, 2007.
[3]
M. Gamba and C. Giacoma, “Key issues in the study of primate acoustic signals, an update,” Journal of Anthropological Sciences, vol. 88, pp. 215–220, 2010.
[4]
T. Geissmann and T. Mutschler, “Diurnal distribution of loud calls in sympatric wild indris (Indri indri) and ruffed lemurs (Varecia variegata): implications for call functions,” Primates, vol. 47, no. 4, pp. 393–396, 2006.
[5]
J. M. Macedonia, “Individuality in a contact call of the ringtailed lemur (Lemur catta),” American Journal of Primatology, vol. 11, no. 2, pp. 163–179, 1986.
[6]
J. C. Masters, “Loud calls of Galago crassicaudatus and G. garnettii and their relation to habitat structure,” Primates, vol. 32, no. 2, pp. 153–167, 1991.
[7]
E. Zimmermann, “The vocal repertoire of the adult senegal bush baby (Galago senegalensis),” Behaviour, vol. 94, no. 3-4, pp. 212–322, 1985.
[8]
E. Zimmermann, “Differentiation of vocalizations in bushbabies (Galaginae) and the significance for assessing phylogenetic relationships,” Journal of Zoological Systematics and Evolutionary Research, vol. 28, no. 3, pp. 217–239, 1990.
[9]
E. Zimmermann, E. Vorobieva, D. Wrogemann, and T. Hafen, “Use of vocal fingerprinting for specific discrimination of gray (Microcebus murinus) and rufous mouse lemurs (Microcebus rufus),” International Journal of Primatology, vol. 21, no. 5, pp. 837–852, 2000.
[10]
S. K. Bearder, “Physical and social diversity among nocturnal primates: a new view based on long term research,” Primates, vol. 40, no. 1, pp. 267–282, 1999.
[11]
P. Braune, S. Schmidt, and E. Zimmermann, “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, vol. 58, no. 6, pp. 587–596, 2005.
[12]
S. Rasoloharijaona, B. Randrianambinina, P. Braune, and E. Zimmermann, “Loud calling, spacing, and cohesiveness in a nocturnal primate, the Milne Edwards' sportive lemur (Lepilemur edwardsi),” American Journal of Physical Anthropology, vol. 129, no. 4, pp. 591–600, 2006.
[13]
C. Bergey and E. Patel, “A preliminary vocal repertoire of the greater bamboo lemur (Prolemur simus): classification and contexts,” Nexus, vol. 1, pp. 69–84, 2008.
[14]
J. R. MacKinnon and K. S. MacKinnon, “The behavior of wild spectral tarsiers,” International Journal of Primatology, vol. 1, no. 4, pp. 361–379, 1980.
[15]
I. Neri-Arboleda, P. Stott, and N. P. Arboleda, “Home ranges, spatial movements and habitat associations of the Philippine tarsier (Tarsius syrichta) in Corella, Bohol,” Journal of Zoology, vol. 257, no. 3, pp. 387–402, 2002.
[16]
P. Y. Wong, C. E. Collins, and J. H. Kaas, “Overview of sensory systems of Tarsius,” International Journal of Primatology, vol. 31, no. 6, pp. 1002–1031, 2010.
[17]
S. Merker and C. P. Groves, “Tarsius lariang: a new primate species from Western Central Sulawesi,” International Journal of Primatology, vol. 27, no. 2, pp. 465–485, 2006.
[18]
C. Niemitz, Biology of Tarsiers, Gustav Fisher, Stuttgart, Germany, 1984.
[19]
C. Niemitz, A. Nietsch, S. Warter, and Y. Rumpler, “Tarsius dianae: a new primate species from central Sulawesi (Indonesia),” Folia Primatologica, vol. 56, no. 2, pp. 105–116, 1991.
[20]
A. Nietsch, “Duet vocalizations among different populations of Sulawesi tarsiers,” International Journal of Primatology, vol. 20, no. 4, pp. 567–583, 1999.
[21]
A. Nietsch, “Outline of the vocal behavior of Tarsius spectrum: call features, associated behaviors, and biological functions,” in Tarsiers: Past, Present, and Future, P. C. Wright, E. L. Simons, and S. Gursky, Eds., pp. 196–220, Rutgers University Press, New Brunswick, NJ, USA, 2003.
[22]
C. Niemitz, “Outline of the behaviour of Tarsius bancanus,” in The Study of Prosimian Behavior, G. A. Doyle and R. D. Martin, Eds., pp. 631–660, Academic Press, New York, NY, USA, 1979.
[23]
I. Yustian, Ecology and Conservation Status of Tarsius bancanus saltator on Belitung Island, Indonesia, Cuvillier, G？ttingen, Germany, 2007.
[24]
R. H. Crompton and P. M. Andau, “Ranging, activity rhythms, and sociality in free-ranging Tarsius bancanus: a preliminary report,” International Journal of Primatology, vol. 8, no. 1, pp. 43–71, 1987.
[25]
C. H. Wharton, “The tarsier in captivity,” Journal of Mammalogy, vol. 31, no. 3, pp. 260–268, 1950.
[26]
P. C. Wright and E. L. Simons, “Calls of the Mindanao tarsier,” American Journal of Physical Anthropology, vol. 63, p. 236, 1984.
[27]
M. Gamba, C. Colombo, and C. Giacoma, “Acoustic cues to caller identity in lemurs: a case study,” Journal of Ethology, vol. 30, no. 1, pp. 191–196, 2012.
[28]
C. T. Snowdon and J. Cleveland, “Individual recognition of contact calls by pygmy marmosets,” Animal Behaviour, vol. 28, no. 3, pp. 717–727, 1980.
[29]
D. D. Jorgensen and J. A. French, “Individuality but not stability in marmoset long calls,” Ethology, vol. 104, no. 9, pp. 729–742, 1998.
[30]
C. A. Chapman and D. M. Weary, “Variability in spider monkeys' vocalizations may provide basis for individual recognition,” American Journal of Primatology, vol. 22, no. 4, pp. 279–284, 1990.
[31]
R. Steenbeek and P. Assink, “Individual differences in long-distance calls of male wild Thomas langurs (Presbytis thomasi),” Folia Primatologica, vol. 69, no. 2, pp. 77–80, 1998.
[32]
S. A. Wich, S. Koski, H. de Vries, and C. P. Van Schaik, “Individual and contextual variation in Thomas langur male loud calls,” Ethology, vol. 109, no. 1, pp. 1–13, 2003.
[33]
R. A. Delgado, “Sexual selection in the loud calls of male primates: signal content and function,” International Journal of Primatology, vol. 27, no. 1, pp. 5–25, 2006.
[34]
M. ？eháková-Petr？, L. Pe？ke, and T. Daněk, “Predation on a wild Philippine tarsier (Tarsius syrichta),” Acta Ethologica. In press.
[35]
D. S. Jachowski and C. Pizzaras, “Introducing an innovative semi-captive environment for the Philippine tarsier (Tarsius syrichta),” Zoo Biology, vol. 24, no. 1, pp. 101–109, 2005.
[36]
M. Dagosto, D. L. Gebo, and C. Dolino, “Positional behavior and social organization of the Philippine tarsier (Tarsius syrichta),” Primates, vol. 42, no. 3, pp. 233–243, 2001.
[37]
J. Fischer, K. Hammerschmidt, D. L. Cheney, and R. M. Seyfarth, “Acoustic features of female chacma baboon barks,” Ethology, vol. 107, no. 1, pp. 33–54, 2001.
[38]
L. Schrader and K. Hammerschmidt, “Computer-aided analysis of acoustic parameters in animal vocalisations: a multi-parametric approach,” Bioacoustics, vol. 7, no. 4, pp. 247–265, 1997.
[39]
P. M. Waser and C. H. Brown, “Is there a “sound window” for primate communication?” Behavioral Ecology and Sociobiology, vol. 15, no. 1, pp. 73–76, 1984.
[40]
S. L. Gursky, “Infant care in the spectral tarsier (Tarsius spectrum) Sulawesi, Indonesia,” International Journal of Primatology, vol. 15, no. 6, pp. 843–853, 1994.
[41]
M. A. Ramsier, A. J. Cunningham, G. L. Moritz et al., “Primate communication in the pure ultrasound,” Biology Letters. In press.
[42]
R. Policht, A. Karad？os, and D. Frynta, “Comparative analysis of long-range calls in equid stallions (Equidae): are acoustic parameters related to social organization?” African Zoology, vol. 46, no. 1, pp. 18–26, 2011.
[43]
D. T. Blumstein and K. B. Armitage, “Does sociality drive the evolution of communicative complexity? A comparative test with ground-dwelling sciurid alarm calls,” American Naturalist, vol. 150, no. 2, pp. 179–200, 1997.
[44]
A. Le Roux, M. I. Cherry, and M. B. Manser, “The vocal repertoire in a solitary foraging carnivore, Cynictis penicillata, may reflect facultative sociality,” Naturwissenschaften, vol. 96, no. 5, pp. 575–584, 2009.
[45]
K. McComb and S. Semple, “Coevolution of vocal communication and sociality in primates,” Biology Letters, vol. 1, no. 4, pp. 381–385, 2005.
[46]
R. H. Crompton and P. M. Andau, “Locomotion and habitat utilization in free-ranging Tarsius bancanus: a preliminary report,” Primates, vol. 27, no. 3, pp. 337–355, 1986.
[47]
S. Gursky, “Group size and composition in the spectral tarsier, Tarsius spectrum: implication for social structure,” Tropical Biodiversity, vol. 3, pp. 57–62, 1995.
[48]
S. Gursky, “Determinants of gregariousness in the spectral tarsier (prosimian: Tarsius spectrum),” Journal of Zoology, vol. 256, no. 3, pp. 401–410, 2002.
[49]
S. Gursky, “Associations between adult spectral tarsiers,” American Journal of Physical Anthropology, vol. 128, no. 1, pp. 74–83, 2005.
[50]
M. Shekelle and I. Arboleda, Tarsius syrichta. In: IUCN 2011. IUCN Red list of threatened species. Version 2011, 2008.
[51]
P. K. McGregor, T. M. Peake, M. Gilbert, et al., “Communication behaviour and conservation,” in Behaviour and Conservation, L. M. Gosling and W. J. Sutherland, Eds., pp. 261–282, Cambridge University Press, Cambridge, UK, 2000.
[52]
A. M. R. Terry, T. M. Peake, and P. K. McGregor, “The role of vocal individuality in conservation,” Frontiers in Zoology, vol. 2, no. 1, 2005.
[53]
P. Braune, S. Schmidt, and E. Zimmermann, “Acoustic divergence in the communication of cryptic species of nocturnal primates (Microcebus ssp.),” BMC Biology, vol. 6, article 19, 2008.
[54]
J. A. Burton and A. Nietsch, “Geographical variation induet songs of Sulawesi tarsiers: evidence for new cryptic species in South and Southeast Sulawesi,” International Journal of Primatology, vol. 31, no. 6, pp. 1123–1146, 2010.
[55]
J. C. Mitani and J. Gros-Louis, “Species and sex differences in the screams of chimpanzees and bonobos,” International Journal of Primatology, vol. 16, no. 3, pp. 393–411, 1995.
[56]
M. Méndez-Cárdenas, B. Randrianambinina, A. Rabesandratana, S. Rasoloharijaona, and E. Zimmermann, “Geographic variation in loud calls of sportive lemurs (Lepilemur ssp.) and their implications for conservation,” American Journal of Primatology, vol. 70, no. 9, pp. 828–838, 2008.
[57]
A. Nietsch and M. L. Kopp, “Role of vocalization in species differentiation of Sulawesi tarsiers,” Folia Primatologica, vol. 69, supplement 1, pp. 371–378, 1998.
[58]
J. F. Oates and T. F. Trocco, “Taxonomy and phylogeny of black-and-white colobus monkeys. Inferences from an analysis of loud call variation,” Folia Primatologica, vol. 40, no. 1-2, pp. 83–113, 1983.
[59]
C. T. Snowdon, A. Hodun, A. L. Rosenberger, and A. F. Coimbra-Filho, “Long-call structure and its relation to taxonomy in lion tamarins,” American Journal of Primatology, vol. 11, no. 3, pp. 253–261, 1986.
[60]
M. Shekelle, C. Groves, S. Merker, and J. Supriatna, “Tarsius tumpara: a new tarsier species from Siau Island, North Sulawesi,” Primate Conservation, vol. 23, pp. 55–64, 2008.
[61]
M. Shekelle and A. Salim, Tarsius tumpara. In: IUCN 2011. IUCN Red list of threatened species. Version 2011.2, 2011.
[62]
D. Brandon-Jones, A. A. Eudey, T. Geissmann et al., “Asian primate classification,” International Journal of Primatology, vol. 25, no. 1, pp. 97–164, 2004.
[63]
L. R. Heaney, “Zoogeographic evidence for middle and late Pleistocene land bridges to the Philippine Islands,” Modern Quaternary Research in Southeast Asia, vol. 9, pp. 127–144, 1985.
[64]
M. Dagosto, D. L. Gebo, and C. N. Dolino, “The natural history of the Philippine tarsier (Tarsius syrichta),” in Tarsiers: Past, Present, and Future, P. C. Wright, E. L. Simons, and S. Gursky, Eds., pp. 237–259, Rutgers University Press, New Brunswick, NJ, USA, 2003.
