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Vocal Communication in Woolly Monkeys (Lagothrix lagothricha lugens) in Cueva de los Guacharos National Park, Colombia

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The Woolly Monkey

Abstract

Vocal communication represents several advantages for primates. Numerous studies have shown that there are different factors that affect vocal behavior. Here, we combined classic and bioacoustics methods to provide the first comprehensive analysis of the acoustic structure and the vocal behavior of a wild population of woolly monkeys (Lagothrix lagothricha lugens). This species is of special interest because it is one of the few neotropical primates whose vocal communication is still not understood completely. Results indicated that factors, such as the time of the day, activity, age, and sex, had major influences on the vocal behavior of the woolly monkey. We also show evidence of how call rates changed, between highland and lowland woolly monkey populations, due to intrinsic differences of each location. Acoustic structure analyses of two types of vocalizations show consistent acoustic differences among the calls of individuals in some features (i.e., call duration and high, low, and final frequency). These differences may enable woolly monkeys to distinguish between the calls of different group members. Finally, clear differences between age (juvenile vs. adult) and sex (male vs. female) classes were found, based on the structure of the alarm call.

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References

  • Arnedo LF (2010) Patterns of acoustic variation of the staccato and neigh vocalizations of the northern muriqui (Brachyteles hypoxanthus). Dissertation, University of Wisconsin, Wisconsin

    Google Scholar 

  • Arnedo LF, Mendes FDC, Strier KB (2010) Sex differences in vocal patterns in the northern muriqui (Brachyteles hypoxanthus). Am J Primatol 72:122–128

    PubMed  Google Scholar 

  • Bergey C, Patel ER (2008) A preliminary vocal repertoire of the greater bamboo lemur (Prolemur simus): Classification and contexts. Nexus 1(1):69–84

    Google Scholar 

  • Bezerra BM, Souto AS, Oliveira MA, Halsey LG (2009) Vocalizations of wild common marmosets are influenced by diurnal and ontogenetic factors. Primates 50:231–237

    Article  PubMed  Google Scholar 

  • Bouchet H, Blois-Heulin C, Lemasson A (2012) Age- and sex-specific patterns of vocal behavior in De Brazza’s monkeys (Cercopithecus neglectus). Am J Primatol 74:12–28

    Article  PubMed  Google Scholar 

  • Bradbury CH, Vehrencamp SL (2011) Principles of animal communication, 2nd edn. Sinauer, Sunderland

    Google Scholar 

  • Brumm H, Voss K, Köllmer I, Todt D (2004) Acoustic communication in noise: regulation of call characteristics in a New World monkey. J Exp Biol 207:443–448

    Article  PubMed  Google Scholar 

  • Casamitjana J (2002) The vocal repertoire of the woolly monkey Lagothrix lagothricha. Bioacoustics 13:1–19

    Article  Google Scholar 

  • Ceugniet M, Izumi A (2004) Vocal individual discrimination in Japanese monkeys. Primates 45:119–128

    Article  PubMed  Google Scholar 

  • Chapman CA, Lefebvre L (1990) Manipulating foraging group size: spider monkey food calls at fruiting trees. Anim Behav 39:891–896

    Article  Google Scholar 

  • Chapman CA, Weary DM (1990) Variability in spider monkey’s vocalizations may provide basis for individual recognition. Am J Primatol 22:279–284

    Article  Google Scholar 

  • Clay Z, Smith CL, Blumstein DT (2012) Food-associated vocalizations in mammals and birds: what do these calls really mean? Anim Behav 83:323–330

    Article  Google Scholar 

  • Cornick LA, Markowitz H (2002) Diurnal vocal patterns of the black howler monkey (Alouatta pigra) at Lamanai, Belize. J Mammal 83:159–166

    Article  Google Scholar 

  • Davila-Ross M, Geissmann T (2009) Circadian long call distribution in wild orangutans. Rev Primatol 1:1–10

    Google Scholar 

  • de Boer B (2009) Acoustic analysis of primate air sacs and their effect on vocalization. J Acoust Soc Am 126:3329–3343

    Article  PubMed  Google Scholar 

  • de laTorres S, Snowdon CT (2002) Environmental correlates of vocal communication of wild pygmy marmosets, Cebuella pygmaea. Anim Behav 63:847–856

    Article  Google Scholar 

  • Defler TR (2010) Historia natural de los primates colombianos. Universidad Nacional de Colombia, Bogotá

    Google Scholar 

  • Di Bitetti MS (2003) Food-associated calls of tufted capuchin monkeys (Cebus apella nigritus) are functionally referential signals. Behaviour 140:565–592

    Article  Google Scholar 

  • Di Fiore A, Campbell CJ (2007) The atelines: Variation in ecology, behavior, and social organization. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Beader SK, Stumpf RM (eds) Primates in perspective, 2nd edn. Oxford University Press, New York, pp 155–185

    Google Scholar 

  • Di Fiore A, Fleischer RC (2005) Social behavior, reproductive strategies, and population genetic structure of Lagothrix poeppigii. Int J Primatol 26:1137–1173

    Article  Google Scholar 

  • Di Fiore A, Strier KB (2004) Flexibility in social organization in atelin primates. Folia Primatol 75:140–141

    Google Scholar 

  • Eisenberg JF (1976) Communication mechanism and social integration in the black spider monkey, Ateles fusciceps robustus and related species. Smithson Contrib Zool 213:1–108

    Article  Google Scholar 

  • Ey E, Pfefferle D, Fischer J (2007) Do age- and sex-related variations reliably reflect body size in nonhuman primate vocalizations? A review. Primates 48:253–267

    Article  CAS  PubMed  Google Scholar 

  • Fedigan LM, Baxter MJ (1984) Sex differences and social organization in free-ranging spider monkeys (Ateles geoffroyi). Primates 25(3):279–294

    Article  Google Scholar 

  • Fitch WT (1997) Vocal tract length and formant frequency dispersion correlate with body size in rhesus macaques. J Acoust Soc Am 102:1213–1222

    Article  CAS  PubMed  Google Scholar 

  • Fitch WT, Hauser MD (1995) Vocal production in nonhuman primates: acoustics, physiology and functional constraints on “honest” advertising. Am J Primatol 37:191–219

    Article  Google Scholar 

  • Gonzalez M, Stevenson PR (2009) Patterns of daily movement, activities and diet in woolly monkeys (genus Lagothrix): A comparison between sites and methodologies. In: Potoki E, Krasinski J (eds) Primatology: theories, methods and research. Nova Science Publishers Inc, New York, pp 171–186

    Google Scholar 

  • Hauser MD (1992) Costs of deception: cheaters are punished in rhesus monkeys (Macaca mulatta). Proc Nat Acad Sci U S A 89:12137–12139

    Article  CAS  Google Scholar 

  • Hauser MD (1993) The evolution of nonhuman primate vocalizations: Effects of phylogeny, body weight and motivational state. Am Nat 142:528–542

    Article  CAS  PubMed  Google Scholar 

  • Hohmann G (1991) Comparative analyses of age- and sex-specific patterns of vocal behaviour in four species of Old World Monkeys. Folia Primatol 56:133–156

    Article  CAS  PubMed  Google Scholar 

  • Koda H, Shimooka Y, Sugiura H (2008) Effects of caller activity and habitat visibility on contact call rate of wild Japanese Macaques (Macaca fuscata). Am J Primatol 70:1055–1063

    Article  PubMed  Google Scholar 

  • Kondo N, Watanabe S (2009) Contact calls: information and social function. Jpn Psychol Res 51:197–208

    Article  Google Scholar 

  • Lazaro-Perea C (2001) Intergroup interactions in wild common marmosets, Callithrix jacchus: territorial defense and assessment of neighbours. Anim Behav 62:11–21

    Article  Google Scholar 

  • Lemasson A, Gandon E, Hausberger M (2010) Attention to elders’ voice in non-human primates. Biol Lett 6:325–328

    Article  PubMed Central  Google Scholar 

  • Link A, Di Fiore A, Spehar SN (2009) Female-directed aggression and social control in spider monkeys. In: Muller MN, Wrangham RW (eds) Sexual coercion in primates and humans: an evolutionary perspective on male aggression against females. Harvard University Press, Cambridge, pp 157–183

    Google Scholar 

  • Mackinnon J (1974) The behavior and ecology of wild orangutans (Pongo pygmaeus). Anim Behav 22:3–74

    Article  Google Scholar 

  • Marler P, Hobbett L (1975) Individuality in a long-range vocalization of wild chimpanzees. Z Tierpsychol 38:97–109

    Article  Google Scholar 

  • McComb K, Semple S (2005) Co-evolution of vocal communication and sociality in primates. Biol Lett 1:381–385

    Article  PubMed Central  PubMed  Google Scholar 

  • Mendes FDC, Ades C (2004) Vocal sequential exchanges and intragroup spacing in the Northern Muriqui Brachyteles arachnoides hypoxanthus. An Acad Bras Ciênc 76(2):399–404

    Article  PubMed  Google Scholar 

  • Meyer D, Hodges JK, Wijaya A, Roos C, Hammerschmidt K (2012) Acoustic structure of male loud-calls support molecular phylogeny of Sumatran and Javanese leaf monkeys (genus Presbytis). BMC Evol Biol 12:16

    Article  PubMed Central  PubMed  Google Scholar 

  • Mitani JC, Stuht J (1998) The evolution of nonhuman primate laud calls: acoustic adaptation for long-distance transmission. Primates 39:171–182

    Article  Google Scholar 

  • Mitani JC, Gross-Louis J, Macedonia J (1996) Selection for acoustic individuality within the vocal repertoire of wild chimpanzees. Int J Primatol 17:569–583

    Article  Google Scholar 

  • Neal OJ (2009) Responses to the audio broadcasts of predator vocalizations by eight sympatric primates in Suriname, South America. Dissertation, Kent State University, Kent

    Google Scholar 

  • Norcross JL, Newman JD (1993) Context and gender-specific differences in the acoustic structure of common marmoset (Callithrix jacchus) phee calls. Am J Primatol 30:37–54

    Article  Google Scholar 

  • Pereira ME (1986) Maternal recognition of juvenile offspring coo vocalizations in Japanese macaques. Anim Behav 34(3):935–937

    Article  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Ramos-Fernandez G (2005) Vocal communication in a fission-fusion society: do spider monkeys stay in touch with close associates. Int J Primatol 26:1077–1092

    Article  Google Scholar 

  • Ramos-Fernandez G (2008) Communication in spider monkeys: the function and mechanisms underlying the use of the whinny. In: Campbell CJ (ed) Spider monkeys: behavior, ecology and evolution of the genus Ateles. Cambridge University Press, Cambridge, pp 220–1235

    Google Scholar 

  • Range F, Fischer J (2004) Vocal repertoire of sooty mangabeys (Cercocebus torquatus atys) in the Taï National Park. Ethol 110:301–321

    Article  Google Scholar 

  • Reynolds V, Reynolds F (1965) Chimpanzees of the Budongo forest. In: DeVore I (ed) Primate behavior. Holt, Rinehart and Winston, New York, p 368–424.

    Google Scholar 

  • Riede T (2010) Elasticity and stress relaxation of rhesus monkey (Macaca mulatta) vocal folds. J Exp Biol 213:2924–2932

    Article  PubMed Central  PubMed  Google Scholar 

  • Roy S, Miller CT, Gottscg D, Wang X (2011) Vocal control by the common marmoset in the presence of interfering noise. J Exp Biol 214:3619–3629

    Article  PubMed Central  PubMed  Google Scholar 

  • Seyfarth RM, Cheney DL (1997) Behavioral mechanisms underlying vocal communication in nonhuman primates. Anim Learn Behav 25:249–267

    Article  Google Scholar 

  • Snowdon CT (2009) Plasticity of communication in nonhuman primates. Adv Study Behav 40:239–276

    Article  Google Scholar 

  • Snowdon CT, Brown CH, Petersen MR (1982) Primate communication. Cambridge University Press, Cambridge

    Google Scholar 

  • Spehar SN, Di Fiore A (2013) Loud calls as a mechanism of social coordination in a fission-fusion taxon, the white-bellied spider monkeys (Ateles belzebuth). Behav Ecol Sociobiol 67:947–961

    Article  Google Scholar 

  • Spehar SN, Mathewson P, Di Fiore A (2008) The male spider monkey loud call: A means of mate attraction and mate choice?. XXIInd Congress of the International Primatological Society, Edinburgh

    Google Scholar 

  • Sproul C, Palleroni A, Hauser MD (2006) Cottontop tamarin, Saguinas oedipus, alarm calls contain sufficient information for recognition of individual identity. Anim Behav 72:1379–1385

    Article  Google Scholar 

  • Stevens J, Gilby IC (2004) A conceptual framework for nonkin food sharing: timing and currency of benefits. Anim Behav 67:603–614

    Article  Google Scholar 

  • Stevenson PR (1996) Censos diurnos de mamíferos y algunas aves de gran tamaño en el Parque Nacional Tinigua, Colombia. Universitas Scientarum 3:267–281

    Google Scholar 

  • Stevenson PR (1997) Vocal behavior of woolly monkeys (Lagothrix lagothricha) at Tinigua National Park, Colombia. Field Stud Fauna Flora La Macarena Colomb 10:17–27

    Google Scholar 

  • Stevenson PR (2006) Activity and ranging patterns of Colombian woolly monkeys in north-western Amazonia. Primates 47:239–247

    Article  PubMed  Google Scholar 

  • Stevenson PR (2007) Estimates of the number of seeds dispersed by population of primates in a lowland forest in western Amazonia. In: Dennis AJ, Schupp EW, Green RJ, Westcott DW (eds) Seed dispersal: theory and its application in a changing world. CAB international, Wallingford, pp 340–362

    Chapter  Google Scholar 

  • Stevenson PR, Castellanos MC (2000) Feeding rates and daily path range of Colombian woolly monkeys as evidence for between and within group competition. Folia Primatol 71:399–408

    Article  CAS  PubMed  Google Scholar 

  • Stevenson PR, Quiñones MJ, Ahumada JA (1998) Effects of fruit patch availability on feeding subgroup size and spacing patterns in four primate species, at Tinigua National Park, Colombia. Int J Primatol 19:313–324

    Article  Google Scholar 

  • Stevenson PR, Quiñones MJ, Ahumada JA (2000) Influence of fruit availability on ecological overlap among four neotropical primates at Tinigua National Park, Colombia. Biotropica 32(3):533–544

    Article  Google Scholar 

  • Stevenson PR, Castellanos MC, Garavito MX, Pizarro JC (2002) Effects of seed dispersal by three ateline monkey species on seed germination at Tinigua National Park, Colombia. Int J Primatol 23:1187–1204

    Article  Google Scholar 

  • Struhsaker TT (1970) Phylogenetic implications of some vocalizations of Cercopithecus monkeys. In: Napier JR, Napier PH (eds) Old world monkeys: evolution, systematics and behavior. Academic , New York, pp 365–444

    Google Scholar 

  • Tabachnick BG, Fidell LS (1989) Using multivariate statistics. Harper and Row, New York

    Google Scholar 

  • Teichroeb JA, Sicotte P (2012) Cost-free vigilance during feeding in folivorous primates? Examining the effect of predation risk, scramble competition, and infanticide threat on vigilance in ursine colobus monkeys (Colobus vellerosus). Behav Ecol Sociobiol 66:453–466

    Article  Google Scholar 

  • Teixidor P, Byrne RW (1997) Can spider monkeys (Ateles geoffroyi) discriminate vocalizations of familiar individuals and strangers? Folia Primatol 68:254–264

    Article  CAS  PubMed  Google Scholar 

  • Teixidor P, Byrne RW (1999) The ‘whinny’ of spider monkeys: individual recognition before situational meaning. Behaviour 136:279–308

    Article  Google Scholar 

  • Trivers RL (1971) The evolution of reciprocal altruism. Q Rev Biol 46:35–57

    Article  Google Scholar 

  • Vargas S, León JJ, Ramírez MA, Galvis NF, Cifuentes E, Stevenson PR (2013) Population density and ecological traits of high land woolly monkeys at Cueva de los Guacharos National Park, Colombia. In: Krzton A, Gursky S, Grow NB (eds) High altitude primates. Springer Developments in Primatology. In press.

    Google Scholar 

  • Vásquez VH, Serrano MA (2009) Las áreas naturales protegidas de Colombia. Conservación Internacional—Colombia & fundación Biocolombia. Bogotá, Colombia. Xv + 696 pp

    Google Scholar 

  • Waser PM (1975) Individual recognition, intragroup cohesion and intergroup spacing: evidence from sound playback to forest monkeys. Behaviour 60:28–74

    Article  Google Scholar 

  • White FJ (1994) Food sharing in wild pygmy chimpanzees (bonobo), Pan paniscus. In: Roeder J, Thierry B, Anderson JR, Herrenschmidt N (eds) Current primatology, volume II: social development, learning and behaviour. Universite Louis Pasteur, Strasbourg, pp 1–10

    Google Scholar 

  • Whitehead JM (1989) The effect of the location of a simulated intruder on responses to long-distance vocalizations of mantled howling monkey, Alouatta palliata palliata. Behaviour 108:73–103

    Article  Google Scholar 

  • Wich SA, Assink PR, Becher F, Sterck EHM (2002) Playbacks of loud calls to wild Thomas langurs (Primates; Presbytis thomasi): the effect of location. Behaviour 139:65–78

    Article  Google Scholar 

  • Williams L (1967) Man and monkey. Andre Deutsch Ltd, London

    Google Scholar 

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Acknowledgments

This study was possible, thanks to the permits by Ministerio de Medio Ambiente y Desarrollo and logistic support from Unidad de Parques Nacionales, Universidad de Los Andes, and Carlos Cortés. Andrea Morales and Oscar Laverde collaborated in the acoustics analyses. And some of the students enrolled in the course on field techniques helped at the beginning of the project. We are grateful for the financial support from Primate Conservation Inc. and Margot Marsh Foundation for Biodiversity (Conservation International, Primate Action Fund).

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Correspondence to J. Julián León .

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León, J., Vargas, S., Ramírez, M., Galvis, N., Cifuentes, E., Stevenson, P. (2014). Vocal Communication in Woolly Monkeys (Lagothrix lagothricha lugens) in Cueva de los Guacharos National Park, Colombia. In: Defler, T., Stevenson, P. (eds) The Woolly Monkey. Developments in Primatology: Progress and Prospects, vol 39. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-0697-0_11

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