Abstract
Primates use different types of vocalizations in a variety of contexts. Some of the most studied types have been the long distance or loud calls. These vocalizations have been associated with mate defense, mate attraction, and resource defense, and it is plausible that sexual selection has played an important role in their evolution. Focusing on identified individuals of known sex and age, we evaluated the sexual dimorphism in a type of loud calls (hoots) in a population of wild owl monkeys (Aotus azarae) in Argentina. We found evidence of sexual dimorphism in call structure, with females and males only emitting one type of call, each differing in dominant frequency and Shannon entropy. In addition, both age-related and sex-specific differences in call usage were also apparent in response to the removal of one group member. Future acoustic data will allow us to assess if there are individual characteristics and if the structure of hoot calls presents differences in relation to the social condition of owl monkeys or specific sex responses to variants of hoot calls’ traits. This will provide deeper insights into the evolution of vocal mechanisms regulating pair bonding and mate choice strategies in this and other primate species.
Similar content being viewed by others
References
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48. https://doi.org/10.18637/jss.v067.i01
Benz JJ, French J, Leger DW (1990) Sex differences in vocal structure in a callitrichid primate, Leontopithecus rosalia. Am J Primatol 21:257–264
Caselli CB, Mennill DJ, Gestich CC, Setz EZF, Bicca-Marques JC (2015) Playback responses of socially monogamous black-fronted titi monkeys to simulated solitary and paired intruders. Am J Primatol 77(11):1135–1142. https://doi.org/10.1002/ajp.22447
Caselli CB, Ayres PHB, Castro SCN, Souto A, Schiel N, Miller CT (2018) The role of extragroup encounters in a Neotropical, cooperative breeding primate, the common marmoset: a field playback experiment. Anim Behav 136:137–146. https://doi.org/10.1016/j.anbehav.2017.12.009
Cowlishaw G (1996) Sexual selection and information content in gibbon song bouts. Ethology 102:272–284
Delgado RA (2006) Sexual selection in the loud calls of male primates: signal content and function. Int J Primatol 27(1):5–25. https://doi.org/10.1007/s10764-005-9001-4
Epple G (1974) Olfactory communication in South American primates. Ann N Y Acad Sci 237:261–278
Fernandez-Duque E (2011) Rensch’s rule, Bergmann’s effect and adult sexual dimorphism in wild monogamous owl monkeys (Aotus azarai) of Argentina. Am J Phys Anthropol 146:38–48. https://doi.org/10.1002/ajpa.21541
Fernandez-Duque E (2016) Social monogamy in wild owl monkeys (Aotus azarae) of Argentina: the potential influences of resource distribution and ranging patterns. Am J Primatol 78(3):355–371. https://doi.org/10.1002/ajp.22397
Fernandez-Duque E, Huck M (2013) Till death (or an intruder) do us part: intrasexual-competition in a monogamous primate. PLoS One 8:1–5. https://doi.org/10.1371/journal.pone.0053724
Fernandez-Duque E, Rotundo M (2003) Field methods for capturing and marking Azarai night monkeys. Int J Primatol 24(5):1113–1120
Fernandez-Duque M, Chapman CA, Glander KE, Fernandez-Duque E (2017) Darting primates: steps toward procedural and reporting standards. Int J Primatol. https://doi.org/10.1007/s10764-017-9963-z
Fernández-Duque E, de la Iglesia H, Erkert HG (2010) Moonstruck primates: owl monkeys (Aotus) need moonlight for nocturnal activity in their natural environment. PLoS One 5(9):e12572. https://doi.org/10.1371/journal.pone.0012572
Gamba M, Torti V, Estienne V, Randrianarison RM, Valente D, Rovara P et al (2016) The Indris have got rhythm! Timing and pitch variation of a primate song examined between sexes and age classes. Front Neurosci 10:249. https://doi.org/10.3389/fnins.2016.00249
Garcia M, Herbst CT, Bowling DL, Dunn JC, Fitch WT (2017) Acoustic allometry revisited: morphological determinants of fundamental frequency in primate vocal production. Sci Rep 7(1):1–11. https://doi.org/10.1038/s41598-017-11000-x
Ghazanfar AA, Hauser MD (1996) The neuroethology of primate vocal communication: substrates for the evolution of speech. J Neurosci Res Nat 38(344):187–211. http://www.asifg.mycpanel.princeton.edu/publications/pdfs/Ghazanfar%20%26%20Hauser%20-%20neuroethology.pdf. Accessed 28 Feb 2018
Helenbrook WD, Preston L, Linck NA, Quirk M, Suarez JA (2018) Bioacoustic of the black-headed night monkey, Aotus nigriceps. Neotrop Primates 24(1):29–33
Heymann EW (2003) Monogamy in new world primates: What can patterns of olfactory communication tell us? In: Reichard UH, Boesch C (eds) Monogamy: mating strategies and partnerships in birds, humans and other mammals. Cambridge University Press, Cambridge, pp 248–261
Huck M, Fernandez-Duque E (2012) When dads help: male behavioral care during primate infant development. In: Clancy KBH, Hinde K, Rutherford JN (eds) Building babies: primate development in proximate and ultimate perspective. Springer, New York, pp 361–385. https://doi.org/10.1007/978-1-4614-4060-4_16
Huck Maren, Fernandez-Duque E (2017) The floater’s dilemma: use of space by wild solitary Azara’s owl monkeys, Aotus azarae, in relation to group ranges. Anim Behav 127:33–41. https://doi.org/10.1016/j.anbehav.2017.02.025
Huck M, Rotundo M, Fernandez-Duque E (2011) Growth and development in wild owl monkeys (Aotus azarai) of Argentina. Int J Primatol 32(5):1133–1152. https://doi.org/10.1007/s10764-011-9530-y
Huck M, Fernandez-Duque E, Babb P, Schurr T (2014a) Correlates of genetic monogamy in socially monogamous mammals: insights from Azara’s owl monkeys. Proc R Soc B 281(1782):20140195. https://doi.org/10.1098/rspb.2014.0195
Huck Maren, Van Lunenburg M, Dávalos V, Rotundo M, Di Fiore A, Fernandez-Duque E (2014b) Double effort: parental behavior of wild Azara’s owl monkeys in the face of twins. Am J Primatol 76(7):629–639. https://doi.org/10.1002/ajp.22256
Huck M, Juarez CP, Rotundo MA, Dávalos VM, Fernandez-Duque E (2017) Mammals and their activity patterns in a forest area in the Humid Chaco, northern Argentina. Check List 13(4):363–378. https://doi.org/10.15560/13.4.363
Juarez CP, Rotundo MA, Berg W, Fernández-Duque E (2011) Costs and benefits of radio-collaring on the behavior, demography, and conservation of owl monkeys (Aotus azarai) in Formosa, Argentina. Int J Primatol 32(1):69–82. https://doi.org/10.1007/s10764-010-9437-z
Kantha SS, Koda H, Suzuki J (2009) Owl monkey vocalizations at the Primate Research Institute, Inuyama. Neotrop Primates 16(1):43–46. https://doi.org/10.1896/044.016.0110
Mccomb K, Semple S (2005) Coevolution of vocal communication and sociality in primates. Biol Lett 1:381–385. https://doi.org/10.1098/rsbl.2005.0366
McConnell PB, Snowdon CT (1986) Vocal interactions between unfamiliar groups of captive cotton-top tamarins. Behaviour 97:273–296
McLanahan EB, Green KM (1977) The vocal repertoire and an analysis of the contexts of vocalizations in Leontopithecus rosalia. In: Kleiman DG (ed) The biology and conservation of the Callitrichidae. Smithsonian Institution Press, Washington, D. C., pp 251–269
Mitani JC (1990) Experimental field studies of Asian ape social systems. Int J Primatol 11:103–126
Moynihan MH (1964) Some behavior patterns of platyrrhine monkeys: I. the night monkey (Aotus trivirgatus). Smithson Misc Collect 146(5):1–84
Müller AE, Anzenberger G (2002) Duetting in the titi monkey Callicebus cupreus: structure, pair specificity and development of duets. Folia Primatol 73(2–3):104–115. https://doi.org/10.1159/000064788
Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82(4):591–605
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(1):37–54. https://doi.org/10.1002/ajp.1350300104
Porter TA (1994) The development and maintenance of heterosexual pairs associations in cotton-top tamarins (Saguinus oedipus). Dissertation, University of Wisconsin, Madison
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). Am J Phys Anthropol 129:591–600. https://doi.org/10.1002/ajpa.20342
Robinson J (1979) An analysis of the organization of vocal communication in the titi monkey Callicebus moloch. Z Fur Tierpsychol 49:381–403
Rotundo M, Fernandez-Duque E, Giménez M (2002) Cuidado biparental en el mono de noche (Aotus azarai azarai) de Formosa, Argentina. Neotrop Primates 10:70–72
Rotundo M, Fernandez-Duque E, Dixson AF (2005) Infant development and parental care in free-ranging Aotus azarai azarai in Argentina. Int J Primatol 26(6):1459–1473
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):1–7. https://doi.org/10.1016/j.yhbeh.2004.09.004
Sekulic R (1982) The function of howling in red howler monkeys (Alouatta seniculus). Behaviour 81:38–54
Seyfarth RM, Cheney DL, Marler P (1980) Vervet monkey alarm calls: semantic communication in a free-ranging primate. Anim Behav 28(4):1070–1094. https://doi.org/10.1016/S0003-3472(80)80097-2
Smith AS, Birnie AK, Lane KR, French JA (2009) Production and perception of sex differences in vocalizations of Wied’s black-tufted-ear marmosets (Callithrix kuhlii). Am J Primatol 71(4):324–332. https://doi.org/10.1002/ajp.20656
Snowdon CT (1989) Vocal communication in new world monkeys. J Hum Evol 18(7):611–633. https://doi.org/10.1016/0047-2484(89)90097-3
Snowdon CT (2017) Vocal communication in family-living and pair-bonded primates. In: Quam RM, Ramsier MA, Fay RR, Popper AN (eds) Primate hearing and communication. Springer, Cham, Switzerland, pp 141–174. https://doi.org/10.1007/978-3-319-59478-1_6
Spence-Aizenberg A, Kimball BA, Williams LE, Fernandez-Duque E (2018a) Chemical composition of glandular secretions from a pair-living monogamous primate: sex, age, and gland differences in captive and wild owl monkeys (Aotus spp.). Am J Primatol 80(2):e22730. https://doi.org/10.1002/ajp.22730
Spence-Aizenberg A, Williams LE, Fernandez-Duque E (2018b) Are olfactory traits in a pair-bonded primate under sexual selection? An evaluation of sexual dimorphism in Aotus nancymaae. Am J Phys Anthropol 116(4):884–894. https://doi.org/10.1002/ajpa.23487
Steenbeek R, Assink P, Wich S (1999) Tenure related changes in the wild Thomas’s langurs II: loud calls. Behaviour 136:627–650
Sueur J, Aubin T, Simonis C (2008) Seewave: a free modular tool for sound analysis and synthesis. Bioacoustics 18:213–226
R Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
Terleph TA, Malaivijitnond S, Reichard UH (2015) Lar gibbon (Hylobates lar) great call reveals individual caller identity. Am J Primatol 77(7):811–821. https://doi.org/10.1002/ajp.22406
Trivers RD (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871–1971. Heinemann, London, pp 136–179
van der Heide G, Fernandez-Duque E, Iriart D, Juárez CP (2012) Do forest composition and fruit availability predict demographic differences among groups of territorial owl monkeys (Aotus azarai)? Int J Primatol 33(1):184–207. https://doi.org/10.1007/s10764-011-9560-5
Wartmann FM, Juárez CP, Fernandez-Duque E (2014) Size, site fidelity, and overlap of home ranges and core areas in the socially monogamous owl monkey (Aotus azarae) of northern Argentina. Int J Primatol 35(5):919–939. https://doi.org/10.1007/s10764-014-9771-7
Wasserstein RL, Lazar NA (2016) ASA’s statement on p-values: context, process, and purpose. Am Stat 70(2):129–133
Whitehead J (1987) Vocally mediated reciprocity between neighboring groups of mantled howling monkeys (Alouatta palliata). Anim Behav 35:1615–1627
Wich SA, Nunn CL (2002) Do male “long-distance calls” function in mate defense? A comparative study of long-distance calls in primates. Behav Ecol Sociobiol 52(6):474–484. https://doi.org/10.1007/s00265-002-0541-8
Wich S, Becher F, Sterck EHM (2002) Playbacks of loud calls to wild Thomas langurs (Primates; Presbytis thomasi): the effect of familiarity. Behaviour 139(January):79–87. https://doi.org/10.1163/15685390252902292
Wich S, Assink PR, Sterck EHM (2004) Thomas Langurs (Presbytis thomasi) discriminate between calls of young solitary versus older group-living males: a factor in avoiding infanticide? Behaviour 141(January):41–51. https://doi.org/10.1163/156853904772746592
Wright PC (1985) The cost and benefits of nocturnality for Aotus trivirgatus (the Night Monkey). Dissertation. University of New York, New York
Ziliak S, McCloskey DN (2008) The cult of statistical significance: how the standard error is costing jobs, justice, and lives. University of Michigan Press, Ann Arbor, p 480
Zuberbühler K, Cheney DL, Seyfarth RM (1999) Conceptual semantics in a nonhuman primate. J Comp Psychol 113(1):33–42
Acknowledgements
AGDLC acknowledges support from the Leakey Foundation and the Owl Monkey Project. EFD acknowledges support for the Owl Monkey Project (OMP) from the Wenner-Gren Foundation, L.S.B. Leakey Foundation, National Geographic Society, NSF-BCS-0621020 (2006), RAPID-1219368 (2011), 1232349 (2012), 1503753 (2014), DDIG-1540255 (2015), 1743395 (2017), 1848954 (2019); NSF-REU 0837921, 0924352, 1026991, National Institute on Aging (P30 AG012836-19, NICHD R24 HD-044964-11), University of Pennsylvania Research Foundation, and Zoological Society of San Diego. Research by the OMP has been approved by the University of Pennsylvania, Yale University, the Formosa Province Council of Veterinarian Doctors, the Directorate of Wildlife, the Subsecretary of Ecology and Natural Resources and the Ministry of Production. We thank Bellamar Estancias and Fundación E.C.O. for the continued support of the OMP and all the researchers who assisted in the field. We would also like to thank anonymous reviewers for comments on previous versions of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Garcia de la Chica, A., Huck, M., Depeine, C. et al. Sexual dimorphism in the loud calls of Azara’s owl monkeys (Aotus azarae): evidence of sexual selection?. Primates 61, 309–319 (2020). https://doi.org/10.1007/s10329-019-00773-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10329-019-00773-6