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Age and social affinity effects on contact call interactions in free-ranging spider monkeys

  • M. Briseno-Jaramillo
  • G. Ramos-Fernández
  • T. M. Palacios-Romo
  • J. R. Sosa-López
  • A. Lemasson
Original Article
Part of the following topical collections:
  1. An evolutionary perspective on the development of primate sociality

Abstract

Nonhuman primates’ vocal repertoire has shown little plasticity, with immatures producing adult-like acoustic structures. Yet, the use of different call types shows a degree of socially dependent flexibility during development. In several nonhuman primate species, group members exchange contact calls respecting a set of social and temporal rules that may be learned (e.g., overlap avoidance, turn-taking, social selection of interacting partners, and call type matching). Here, we study the use of contact calls in free-living adult and immature (old and young) spider monkeys (Ateles geoffroyi). We focused our study in two contact call types of the species’ repertoire: whinnies and high-whinnies. Our results suggest that individuals in all age classes produced both call types, with immatures producing less frequently the whinny call type. Immature individuals exchanged calls less often than adults, although their contribution increased with age. Conversely, mature individuals regulated their emissions by (1) exchanging more calls with their preferred affiliative partner and (2) matching the call type, while immatures did not. Our results show that contact call usage changes during development and suggest that adult rules might be learned. We argue that call matching is a “conversational rule” that young individuals acquire with apparent call-type-dependent variations during development. Our findings support the idea that social factors influence vocal development in nonhuman primates.

Significance statement

We studied the social rules underlying vocal interaction patterns in free-ranging spider monkeys. We found that, while both immature (old and young) and mature individuals were able to produce the two species contact call types, they differed strongly in the way they used them. Matures called more often and exchanged more, while the vocal response rates of immature individuals increased with age. Also, mature individuals exchanged preferentially with their close associates and matched their call types while immatures did not. As in other species, we predict that these exchange patterns serve as a social rule to maintain and strengthen social bonds between individuals. We discuss our findings in light of the probable role of social learning during acquisition of the appropriate context of calling and of the response to others’ calls. These findings support the idea that social influences guide vocal development in nonhuman primates.

Keywords

Acoustic matching Call exchanges New World monkeys Vocal communication Vocal learning 

Notes

Acknowledgments

We thank the Comisión Nacional de Áreas Naturales Protegidas of Mexico (CONANP) and the Environmental agency of Mexico (Dirección General de Vida Silvestre, SEMARNAT) for the permission we received to work at the Otoch Ma’ax Yetel Kooh reserve. We are grateful to the staff members of the Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional Unidad Oaxaca, Instituto Politécnico Nacional and of the Animal and Human Ethology Laboratory for their support with the logistics.

We thank Filippo Aureli, Colleen M. Schaffner and Laura G. Vick for sharing the management of the long-term project at Punta Laguna. We are also very grateful to the field assistants Augusto, Eulogio and Macedonio Canul and to Veronique Biquand for their statistic support. We are very grateful to Federica Amici and Anja Widdig for their invitation to the special issue “An evolutionary perspective on the development of primate sociality”, and to Anja Widdig and two anonymous reviewers for their very constructive comments that helped to improve the manuscript.

Funding

Our research was supported by grants from Consejo Nacional de Ciencia y Tecnología (CONACYT) through a chair fellowship granted to JRSL at CIIDIR (researcher number 1640; project number 1781). MBJ received a postdoctoral fellowship from CONACYT (scholar number 220762), and GRF an Exploration Grant from National Geographic (WW-R008-17).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. Our study adhered to the legal requirements for field observations of animals in Mexico. Protocols were approved by the Direccion General de Vida Silvestre (SEMARNAT, permit #SGPA/DGVS/1405/15). The Direccion General de Vida Silvestre is a subdivision of the Mexican government that oversees the ethical treatment of wildlife and only authorizes studies where data is collected according to this treatment.

References

  1. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267CrossRefPubMedGoogle Scholar
  2. Arlet M, Jubin R, Masataka N, Lemasson A (2015) Grooming-at-a-distance by exchanging calls in non-human primates. Biol Lett 11:20150711CrossRefPubMedPubMedCentralGoogle Scholar
  3. Arriaga G, Zhou EP, Jarvis ED (2012) Of mice, birds, and men: the mouse ultrasonic song system has some features similar to humans and song-learning birds. PLoS One 7:e46610CrossRefPubMedPubMedCentralGoogle Scholar
  4. Aureli F, Schaffner CM (2008) Social interactions, social relationships and the social system of spider monkeys. In: Campbell CJ (ed) Spider monkeys: behavior, ecology and evolution of the genus Ateles. Cambridge University Press, Cambridge, pp 236–265CrossRefGoogle Scholar
  5. Aureli F, Schaffner CM, Boesch C et al (2008) Fission-fusion dynamics: new research frameworks. Curr Anthropol 49:627–654Google Scholar
  6. Bates D, Mächler M, Bolker B, Walker S (2015). “Fitting Linear Mixed-Effects Models Using lme4.” J Stat Softw 67: 1–48.  https://doi.org/10.18637/jss.v067.i01.
  7. Bezerra BM, da Silva Souto A, de Oliveira MAB, Halsey LG (2009) Vocalisations of wild common marmosets are influenced by diurnal and ontogenetic factors. Primates 50:231–237CrossRefPubMedGoogle Scholar
  8. Biben M, Symmes D, Masataka N (1986) Temporal and structural analysis of affiliative vocal exchanges in squirrel monkeys (Saimiri sciureus). Behaviour 98:259–273CrossRefGoogle Scholar
  9. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135CrossRefPubMedGoogle Scholar
  10. 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 74:12–28CrossRefPubMedGoogle Scholar
  11. Bouchet H, Laporte M, Candiotti A, Lemasson A (2013) Flexibilité vocale sous influences sociales chez les primates non-humains. Rev Primatol 5:53Google Scholar
  12. Bouchet H, Koda H, Lemasson A (2017) Age-dependent change in attention paid to vocal exchange rules in Japanese macaques. Anim Behav 129:81–92CrossRefGoogle Scholar
  13. Boughman JW (1998) Vocal learning by greater spear–nosed bats. Proc R Soc Lond B 265(1392):227–233CrossRefGoogle Scholar
  14. Boughman JW, Moss CF (2003) Social sounds: vocal learning and development of mammal and bird calls. In: Megela-Simmons A, Popper AN, Fay R (eds) Acoustic communication. Springer, New York, pp 138–224CrossRefGoogle Scholar
  15. 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. Behav Ecol Sociobiol 58:587–596CrossRefGoogle Scholar
  16. Briefer EF, McElligott AG (2012) Social effects on vocal ontogeny in an ungulate, the goat, Capra hircus. Anim Behav 83:991–1000CrossRefGoogle Scholar
  17. Candiotti A, Zuberbuhler K, Lemasson A (2012) Convergence and divergence in Diana monkey vocalizations. Biol Lett 8:382–385CrossRefPubMedPubMedCentralGoogle Scholar
  18. Chapman CA, Weary DM (1990) Variability in spider monkeys’ vocalizations may provide basis for individual recognition. Am J Primatol 22:279–284CrossRefGoogle Scholar
  19. Chen HC, Kaplan G, Rogers LJ (2009) Contact calls of common marmosets (Callithrix jacchus): influence of age of caller on antiphonal calling and other vocal responses. Am J Primatol 71:165–170CrossRefPubMedGoogle Scholar
  20. Cheney DL, Seyfarth RM (1992) How monkeys see the world: inside the mind of another species. University of Chicago Press, ChicagoGoogle Scholar
  21. Chow CP, Mitchell JF, Miller CT (2015) Vocal turn-taking in a non-human primate is learned during ontogeny. Proc R Soc B 282:20150069CrossRefPubMedGoogle Scholar
  22. Crockford C, Herbinger I, Vigilant L, Boesch C (2004) Wild chimpanzees produce group-specific calls: a case for vocal learning? Ethology 110:221–243CrossRefGoogle Scholar
  23. de la Torre S, Snowdon CT (2009) Dialects in pygmy marmosets? Population variation in call structure. Am J Primatol 71:333–342CrossRefPubMedGoogle Scholar
  24. de Waal FBM (1996) Macaque social culture: development and perpetuation of affiliative networks. J Comp Psychol 110:147–154CrossRefPubMedGoogle Scholar
  25. Dunbar RIM (2003) The origin and subsequent evolution of language. In: Kirby S (ed) Christiansen MH. Studies in the evolution of language. Language Evolution, Oxford University Press, New York, pp 219–234Google Scholar
  26. Eisenberg JF (1976) Communication mechanisms and social integration in the black spider monkey, Ateles fusciceps robustus, and related species. Sm C Zool 213:1–108Google Scholar
  27. Elowson AM, Snowdon CT (1994) Pygmy marmosets, Cebuella pygmaea, modify vocal structure in response to changed social environment. Anim Behav 47:1267–1277CrossRefGoogle Scholar
  28. Elowson AM, Snowdon CT, Sweet CJ (1992) Ontogeny of trill and J-call vocalizations in the pygmy marmoset, Cebuella pygmaea. Anim Behav 43:703–715CrossRefGoogle Scholar
  29. Elowson AM, Snowdon CT, Lazaro-Perea C (1998) Infant’babbling’in a nonhuman primate: complex vocal sequences with repeated call types. Behaviour 135:643–664CrossRefGoogle Scholar
  30. Ey E, Pfefferle D, Fischer J (2007) Do age- and sex-related variations reliably reflect body size in non-human primate vocalizations? A review. Primates 48:253–267CrossRefPubMedGoogle Scholar
  31. Farabaugh SM, Linzenbold A, Dooling RJ (1994) Vocal plasticity in budgerigars (Melopsittacus undulatus): evidence for social factors in the learning of contact calls. J Comp Psychol 108:81–92CrossRefPubMedGoogle Scholar
  32. Fedigan LM, Baxter MJ (1984) Sex differences and social organization in free-ranging spider monkeys (Ateles geoffroyi). Primates 25:279–294CrossRefGoogle Scholar
  33. Garber PA, Pruetz JD, Isaacson J (1993) Patterns of range use, range defense, and intergroup spacing in moustached tamarin monkeys (Saguinus mystax). Primates 34:11–25CrossRefGoogle Scholar
  34. Gautier JP, Gautier A (1977) Communication in old world monkeys. In: Sebeok TA (ed) How animals communicate. Indiana University Press, Bloomington, pp 890–964Google Scholar
  35. Geary DC (2003) Hommes, femmes: l’évolution des différences sexuelles humaines. De Boeck, ParisGoogle Scholar
  36. Geissmann T (1984) Inheritance of song parameters in the gibbon song, analysed in 2 hybrid gibbons (Hylobates pileatus and H. lar). Folia Primatol 42:216–235CrossRefGoogle Scholar
  37. Geissmann T (1999) Duet songs of the siamang, Hylobates syndactylus: II. Testing the pair-bonding hypothesis during a partner exchange. Behaviour 136:1005–1039CrossRefGoogle Scholar
  38. Giles H, Coupland N, Coupland I (1991) Accommodation theory: communication, context, and consequence. In: Giles H, Coupland J, Coupland N (eds) Context of accommodation: developments in applied sociolinguistics. Cambridge University Press, Cambridge, pp 1–68CrossRefGoogle Scholar
  39. Goldstein MH, Schwade JA (2008) Social feedback to infants’ babbling facilitates rapid phonological learning. Psychol Sci 19:515–523CrossRefPubMedPubMedCentralGoogle Scholar
  40. Gouzoules H, Gouzoules S (1989) Design features and developmental modification of pigtail macaque, Macaca nemestrina, agonistic screams. Anim Behav 37:383–401CrossRefGoogle Scholar
  41. 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 Primatol 69:342–356CrossRefPubMedGoogle Scholar
  42. Hammerschmidt K, Fischer J (2008) Constraints in primate vocal production. In: Griebel U, Oller K (eds) The evolution of communicative creativity: from fixed signals to contextual flexibility. The MIT Press, Cambridge, MA, pp 93–119Google Scholar
  43. Hammerschmidt K, Jürgens U, Freudenstein T (2001) Vocal development in squirrel monkeys. Behaviour 138:1179–1204CrossRefGoogle Scholar
  44. Hauser MD (1989) Ontogenetic changes in the comprehension and production of vervet monkey (Cercopithecus aethiops) vocalizations. J Comp Psychol 103:149–158CrossRefGoogle Scholar
  45. Herzog M, Hopf S (1984) Behavioral responses to species-specific warning calls in infant squirrel monkeys reared in social isolation. Am J Primatol 7:99–106CrossRefGoogle Scholar
  46. Hodun A, Snowdon CT, Soini P (1981) Subspecific variation in the long calls of the tamarin, Saguinus fusckollis. Z Tierpsychol 57:97–110CrossRefGoogle Scholar
  47. Hopkins WD, Taglialatela JP, Leavens DA (2007) Chimpanzees differentially produce novel vocalizations to capture the attention of a human. Anim Behav 73:281–286CrossRefPubMedPubMedCentralGoogle Scholar
  48. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363CrossRefPubMedGoogle Scholar
  49. Janik VM, Slater PJ (1997) Vocal learning in mammals. Adv Stud Behav 26:59–100CrossRefGoogle Scholar
  50. Katsu N, Yamada K, Nakamichi M (2014) Development in the usage and comprehension of greeting calls in a free-ranging group of Japanese macaques (Macaca fuscata). Ethology 120:1024–1034CrossRefGoogle Scholar
  51. 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 70:1055–1063CrossRefPubMedGoogle Scholar
  52. Koda H, Lemasson A, Oyakawa C, Pamungkas J, Masataka N (2013) Possible role of mother-daughter vocal interactions on the development of species-specific song in gibbons. PLoS One 8:e71432CrossRefPubMedPubMedCentralGoogle Scholar
  53. Korner-Nievergelt F, Roth T, Von Felten S, Guélat J, Almasi B, Korner-Nievergelt P (2015) Bayesian data analysis in ecology using linear models with R, bugs, and Stan. Academic Press, CambridgeGoogle Scholar
  54. Kulik L, Langos D, Widdig A (2016) Mothers make a difference: mothers develop weaker bonds with immature sons than daughters. PLoS One 11:e0154845CrossRefPubMedPubMedCentralGoogle Scholar
  55. Lameira AR, Hardus ME, Mielke A, Wich SA, Shumaker RW (2016) Vocal fold control beyond the species-specific repertoire in an orang-utan. Sci Rep 6:30315CrossRefPubMedPubMedCentralGoogle Scholar
  56. Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174CrossRefPubMedGoogle Scholar
  57. Laporte MN, Zuberbühler K (2011) The development of a greeting signal in wild chimpanzees. Dev Sci 14:1220–1234CrossRefPubMedGoogle Scholar
  58. Lazaro-Perea C (2001) Intergroup interactions in wild common marmosets, Callithrix jacchus: territorial defence and assessment of neighbours. Anim Behav 62:11–21CrossRefGoogle Scholar
  59. Lemasson A, Hausberger M (2004) Patterns of vocal sharing and social dynamics in a captive group of Campbell's monkeys (Cercopithecus campbelli campbelli). J Comp Psychol 118:347–359CrossRefPubMedGoogle Scholar
  60. Lemasson A, Gandon E, Hausberger M (2010) Attention to elders’ voice in non-human primates. Biol Lett 6:325–328CrossRefPubMedCentralGoogle Scholar
  61. Lemasson A, Ouattara K, Petit EJ, Zuberbühler K (2011a) Social learning of vocal structure in a nonhuman primate? BMC Evol Biol 11:362CrossRefPubMedPubMedCentralGoogle Scholar
  62. Lemasson A, Glas L, Barbu S, Lacroix A, Guilloux M, Remeuf K, Koda H (2011b) Youngsters do not pay attention to conversational rules: is this so for nonhuman primates? Sci Rep 1:22CrossRefPubMedPubMedCentralGoogle Scholar
  63. Lemasson A, Ouattara K, Zuberbühler K (2013a) Exploring the gaps between primate calls and human language. In: Botha R, Everaert M (eds) The evolutionary emergence of language: evidence and inference. Oxford University Press, Utrecht, pp 181–203CrossRefGoogle Scholar
  64. Lemasson A, Guilloux M, Barbu S, Lacroix A, Koda H (2013b) Age-and sex-dependent contact call usage in Japanese macaques. Primates 54:283–291CrossRefPubMedGoogle Scholar
  65. Lemasson A, Jubin R, Masataka N, Arlet M (2016) Copying hierarchical leaders’ voices? Acoustic plasticity in female Japanese macaques. Sci Rep 6:21289CrossRefPubMedPubMedCentralGoogle Scholar
  66. Lemasson A, Pereira H, Levréro F (2018) Social basis of vocal interactions in western lowland gorillas (Gorilla G. gorilla). J Comp Psychol 132: 141–151.  https://doi.org/10.1037/com0000105
  67. Length RV (2016). Least-Squares Means: The R Package lsmeans. J Stat Softw 69: 1–33.  https://doi.org/10.18637/jss.v069.i01
  68. Levréro F, Touitou S, Fredet J, Guéry JP, Lemasson A (2015) Les liens sociaux façonnent le répertoire vocal des bonobos. Rev Primatol 6:44Google Scholar
  69. Lieblich AK, Symmes D, Newman JD, Shapiro M (1980) Development of the isolation peep in laboratory-bred squirrel monkeys. Anim Behav 28:1–9CrossRefGoogle Scholar
  70. Manson JH, Navarrete CD, Silk JB, Perry S (2004) Time-matched grooming in female primates? New analyses from two species. Anim Behav 67:493–500CrossRefGoogle Scholar
  71. Masataka N (1985) Development of vocal recognition of mothers in infant Japanese macaques. Dev Psychobiol 18(2):107–114CrossRefPubMedGoogle Scholar
  72. Masataka N (2003) The onset of language. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  73. Masataka N, Fujita K (1989) Vocal learning of Japanese and rhesus monkeys. Behaviour 109:191–199CrossRefGoogle Scholar
  74. Masataka N, Symmes D (1986) Effect of separation distance on isolation call structure in squirrel monkeys (Saimiri sciureus). Am J Primatol 10:271–278CrossRefGoogle Scholar
  75. McCowan B, Newman JD (2000) The role of learning in chuck call recognition by squirrel monkeys (Saimiri sciureus). Behaviour 137:279–300CrossRefGoogle Scholar
  76. Mendes FD, Ades C (2004) Vocal sequential exchanges and intragroup spacing in the northern Muriqui Brachyteles arachnoides hypoxanthus. An Acad Bras Ciênc 76:399–404CrossRefPubMedGoogle Scholar
  77. Mitani JC, Brandt KL (1994) Social factors influence the acoustic variability in the long-distance calls of male chimpanzees. Ethology 96:233–252CrossRefGoogle Scholar
  78. Mitani JC, Gros-Louis J (1998) Chorusing and call convergence in chimpanzees: tests of three hypotheses. Behaviour 135:1041–1064CrossRefGoogle Scholar
  79. Mitani JC, Hunley KL, Murdoch ME (1999) Geographic variation in the calls of wild chimpanzees: a reassessment. Am J Primatol 47:133–151CrossRefPubMedPubMedCentralGoogle Scholar
  80. Newman JD, Symmes D (1974) Vocal pathology in socially deprived monkeys. Dev Psychobiol 7:351–358CrossRefPubMedGoogle Scholar
  81. Nieuwenhuis R, te Grotenhuis M, Pelzer B (2012) Influence.ME: tools for detecting influential data in mixed effects models. R J 4:38–47Google Scholar
  82. Ordóñez-Gómez JD, Santillán-Doherty AM, Fischer J, Hammerschmidt K (2018) Acoustic variation of spider monkeys’ contact calls (whinnies) is related to distance between vocalizing individuals and immediate caller behavior. Am J Primatol 80:e22747CrossRefPubMedGoogle Scholar
  83. Ouattara K, Zuberbühler K, N'goran EK, Gombert JE, Lemasson A (2009a) The alarm call system of female Campbell’s monkeys. Anim Behav 78:35–44CrossRefGoogle Scholar
  84. Ouattara K, Lemasson A, Zuberbühler K (2009b) Campbell’s monkeys use affixation to alter call meaning. PLoS One 4:e7808CrossRefPubMedPubMedCentralGoogle Scholar
  85. Owren MJ, Dieter JA, Seyfarth RM, Cheney DL (1992) ‘Food’calls produced by adult female rhesus (Macaca mulatta) and Japanese (M. fuscata) macaques, their normally-raised offspring, and offspring cross-fostered between species. Behaviour 120:218–231CrossRefGoogle Scholar
  86. Pistorio AL, Vintch B, Wang X (2006) Acoustic analysis of vocal development in a New World primate, the common marmoset (Callithrix jacchus). J Acoust Soc Am 120:1655–1670CrossRefPubMedGoogle Scholar
  87. Poole JH, Tyack PL, Stoeger-Horwath AS, Watwood S (2005) Elephants are capable of vocal learning. Nature 434:455–456CrossRefPubMedGoogle Scholar
  88. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
  89. Ramos-Fernández G (2005) Vocal communication in a fission-fusion society: do spider monkeys stay in touch with close associates? Int J Primatol 26:1077–1092CrossRefGoogle Scholar
  90. Ramos-Fernández 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 220–235CrossRefGoogle Scholar
  91. Ramos-Fernández G, Ayala-Orozco B (2003) Population size and habitat use of spider monkeys at Punta Laguna, Mexico. In: Marsh LK (ed) Primates in fragments. Ecology and conservation. Springer, Boston, pp 191–209CrossRefGoogle Scholar
  92. Ramos-Fernández G, Aureli F, Schaffner CM, Vick LG (2018) Ecología, comportamiento y conservación de los monos araña (Ateles geoffroyi): 20 años de estudio en Punta Laguna, México. In: Urbani B, Kowalewski M, Cunha RGT, de la Torre S, Cortés-Ortiz L (eds) La primatología en Latinoamérica 2 – A primatologia na America Latina 2. In: Tomo II Costa Rica-Venezuela. Instituto Venezolano de Investigaciones Científicas (IVIC), Caracas, pp 531–543Google Scholar
  93. Riede T, Bronson E, Hatzikirou H, Zuberbühler K (2005) Vocal production mechanisms in a non-human primate: morphological data and a model. J Hum Evol 48:85–96CrossRefPubMedGoogle Scholar
  94. Roupe SL, Pistorio A, Wang X (2003) Vocal plasticity induced by auditory deprivation in the common marmoset. Program no. 627.7, abstract viewer and itinerary planner. Society for Neuroscience online, In: Egnor SR, Hauser MD (2004) A paradox in the evolution of primate vocal learning. Trends Neurosci 27: 649–654Google Scholar
  95. Roush RS, Snowdon CT (1994) Ontogeny of food-associated calls in cotton-top tamarins. Anim Behav 47:263–273CrossRefGoogle Scholar
  96. Roush RS, Snowdon CT (2001) Food transfer and development of feeding behavior and food-associated vocalizations in cotton-top tamarins. Ethology 107:415–429CrossRefGoogle Scholar
  97. Rukstalis M, French JA (2005) Vocal buffering of the stress response: exposure to conspecific vocalizations moderates urinary cortisol excretion in isolated marmosets. Horm Behav 47:1–7CrossRefPubMedPubMedCentralGoogle Scholar
  98. Seyfarth RM, Cheney DL (1986) Vocal development in vervet monkeys. Anim Behav 34:1640–1658CrossRefGoogle Scholar
  99. Seyfarth RM, Cheney DL (1997) Some general features on vocal development in nonhuman primates. In: Snowdon CT, Hausberger M (eds) Social influences on vocal development. Cambridge University Press, Cambridge, pp 249–273CrossRefGoogle Scholar
  100. Shimooka Y, Campbell C, Di Fiore A, Felton A, Izawa K, Link A, Nishimura A, Ramos-Fernandez G, Wallace R (2008) Demography and group composition of Ateles. In: Campbell CJ (ed) Spider Monkeys, Behavior, Ecology and Evolution of the Genus Ateles. Cambridge University Press, Cambridge, pp 329–350CrossRefGoogle Scholar
  101. Slater KY, Schaffner CM, Aureli F (2009) Sex differences in the social behavior of wild spider monkeys (Ateles geoffroyi yucatanensis). Am J Primatol 71:21–29CrossRefPubMedGoogle Scholar
  102. Snowdon CT (2009) Plasticity of communication in nonhuman primates. Adv Study Behav 40:239–276CrossRefGoogle Scholar
  103. Snowdon CT, Cleveland J (1984) “Conversations” among pygmy marmosets. Am J Primatol 7:15–20CrossRefGoogle Scholar
  104. Snowdon CT, Elowson AM (1999) Pygmy marmosets modify call structure when paired. Ethology 105:893–908CrossRefGoogle Scholar
  105. Snowdon CT, Elowson AM (2001) ‘Babbling’ in pygmy marmosets: development after infancy. Behaviour 138:1235–1248CrossRefGoogle Scholar
  106. Snowdon CT, Elowson AM, Roush RS (1997) Social influences on vocal development in New World primates. In: Snowdon CT, Hausberger M (eds) Social influences on vocal development. Cambridge University Press, Cambridge, pp 234–248CrossRefGoogle Scholar
  107. Spehar SN, Di Fiore A (2013) Loud calls as a mechanism of social coordination in a fission–fusion taxon, the white-bellied spider monkey (Ateles belzebuth). Behav Ecol Sociobiol 67:947–961CrossRefGoogle Scholar
  108. Sugiura H, Masataka N (1995) Temporal and acoustic flexibility in vocal exchanges of coo calls in Japanese macaques (Macaca fuscata). In: Zimmermann E, Newman JD, Jürgens U (eds) Current topics in primate vocal communication. Springer, Boston, MA, pp 121–140CrossRefGoogle Scholar
  109. Symington MM (1987) Sex ratio and maternal rank in wild spider monkeys: when daughters disperse. Behav Ecol Sociobiol 20:421–425CrossRefGoogle Scholar
  110. Symmes D, Biben M (1988) Conversational vocal exchanges in squirrel monkeys. In: Todt D, Goedeking P, Symmes D (eds) Primate vocal communication. Springer, Berlin, pp 123–132CrossRefGoogle Scholar
  111. Takahashi DY, Narayanan DZ, Ghazanfar AA (2013) Coupled oscillator dynamics of vocal turn-taking in monkeys. Curr Biol 23:2162–2168CrossRefPubMedGoogle Scholar
  112. Takahashi DY, Fenley AR, Teramoto Y, Narayanan DZ, Borjon JI, Holmes P, Ghazanfar AA (2015) The developmental dynamics of marmoset monkey vocal production. Science 349:734–738CrossRefPubMedGoogle Scholar
  113. Talmage-Riggs G, Winter P, Ploog D, Mayer W (1972) Effect of deafening on the vocal behavior of the squirrel monkey (Saimiri sciureus). Folia Primatol 17:404–420CrossRefPubMedGoogle Scholar
  114. Tanaka T, Sugiura H, Masataka N (2006) Cross-sectional and longitudinal studies of the development of group differences in acoustic features of coo calls in two groups of Japanese macaques. Ethology 112:7–21CrossRefGoogle Scholar
  115. Teixidor P, Byrne RW (1999) The ‘whinny’ of spider monkeys: individual recognition before situational meaning. Behaviour 136:279–308CrossRefGoogle Scholar
  116. Tyack PL, Sayigh LS (1997) Vocal learning in cetaceans. In: Snowdon CT, Hausberger M (eds) Social influences on vocal development. Cambridge University Press, Cambridge, pp 208–233CrossRefGoogle Scholar
  117. Vick LG (2008) Immaturity in spider monkeys: a risky business. In: Campbell CJ (ed) Spider Monkeys, Behavior, Ecology and Evolution of the Genus Ateles. Cambridge University Press, Cambridge, pp 288–328CrossRefGoogle Scholar
  118. Volodin I, Volodina E, Frey R, Carranza J, Torres-Porras J (2013) Spectrographic analysis points to source–filter coupling in rutting roars of Iberian red deer. Acta Ethol 16:57–63CrossRefGoogle Scholar
  119. Watson KS, Townsend WS, Schel MA, Wilke C, Wallace KE, Cheng L, West V, Slocombe EK (2015) Vocal learning in the functionally referential food grunts of chimpanzees. Curr Biol 25:495–499CrossRefPubMedGoogle Scholar
  120. Winter P, Handley P, Ploog D, Schott D (1973) Ontogeny of squirrel monkey calls under normal conditions and under acoustic isolation. Behaviour 47:230–239CrossRefPubMedGoogle Scholar
  121. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Zero-truncated and zero-inflated models for count data. In: Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (eds) Mixed effects models and extensions in ecology with R. Springer, Berlin, pp 261–293CrossRefGoogle Scholar

Copyright information

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Authors and Affiliations

  • M. Briseno-Jaramillo
    • 1
  • G. Ramos-Fernández
    • 2
    • 3
  • T. M. Palacios-Romo
    • 1
  • J. R. Sosa-López
    • 1
  • A. Lemasson
    • 4
  1. 1.CONACYT-Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional Unidad Oaxaca (CIIDIR)Instituto Politécnico NacionalOaxacaMexico
  2. 2.Instituto de Investigaciones en Matemáticas Aplicadas y en SistemasUniversidad Nacional Autónoma de MéxicoMexico CityMexico
  3. 3.Unidad Profesional Interdisciplinaria en Ingeniería y Tecnologías AvanzadasInstituto Politécnico NacionalMexico CityMexico
  4. 4.Univ Rennes, Ethologie Animale et Humaine, PaimpontPaimpontFrance

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