Abstract
The relatively fixed vocal structure of nonhuman primates stands in stark contrast to humans. However, primate vocal–plasticity studies are particularly limited by ethical and logistic constraints. As an alternative approach, we take advantage of a confirmed howler hybrid zone (Alouatta palliata × A. pigra) to compare the effects of genetic ancestry and experience on vocal variation. Deviations from a tight phenotype–ancestry correlation can indicate potential plasticity. We also tested whether temporal features (e.g., syllable number, calling rate) show more plasticity than acoustic features (e.g., peak frequency, bandwidth) which might be morphologically constrained. Using 29 microsatellite markers, most hybrid male subjects fell at the extremes of the genetic ancestry distribution, consistent with the entire population’s distribution. We then analyzed 182 howling bouts and 231 loud call recordings from 33 male hybrid and purebred subjects from sympatric and allopatric populations. Acoustic features of hybrid calls clustered with calls from genetically similar purebred males, and calls from the only genetically intermediate hybrid in our sample fell between the two acoustic extremes, suggesting a strong effect of ancestry. However, temporal features tended to converge in sympatry (e.g., vocalizations from purebred A. palliata in the hybrid zone were more pigra-like than vocalizations from allopatric A. palliata, and indistinguishable from sympatric palliata-like and intermediate hybrid vocalizations). Our study shows that, at least for temporal features, primate vocal plasticity can extend beyond intrapopulation variation, consistent with a growing body of research suggesting that primate vocalizations may be more flexible than traditionally assumed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aguiar, L. M. (2010). Sistema social de grupos mistos de espécies de bugios (Alouatta caraya e A. clamitans) e potenciais híbridos no Alto Rio Paraná, sul do Brasil. PhD Dissertation, Federal University of Paraná, Brazil.
Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49(3), 227–266. https://doi.org/10.1163/156853974X00534.
Audacity Team. (2015). Audacity(R): Free audio editor and recorder, version 2.1.0. http://web.audacityteam.org/copyright (Accessed April 1, 2015).
Baker, M. C. (2008). Analysis of a cultural trait across an avian hybrid zone: Geographic variation in plumage morphology and vocal traits in the Australian ringneck parrot (Platycercus zonarius). The Auk, 125(3), 651–662. https://doi.org/10.1525/auk.2008.07111.
Barton, N. H., & Hewitt, G. M. (1985). Analysis of hybrid zones. Annual Review of Ecology and Systematics, 16(1), 113–148. https://doi.org/10.1146/annurev.es.16.110185.000553.
Bergman, T. J. (2013). Speech-like vocalized lip-smacking in geladas. Current Biology, 23(7), R268–R269. https://doi.org/10.1016/j.cub.2013.02.038.
Bergman, T. J., Cortés-Ortiz, L., Dias, P. A. D., Ho, L., Adams, D., Canales-Espinosa, D., & Kitchen, D. M. (2016). Striking differences in the loud calls of howler monkey sister species (A. palliata and A. pigra). American Journal of Primatology, 78(7), 755–766. https://doi.org/10.1002/ajp.22539.
Bicca-Marques, J. C., & Calegaro-Marques, C. (1995). Locomotion of black howlers in a habitat with discontinuous canopy. Folia Primatologica, 64(1-2), 55–61. https://doi.org/10.1159/000156833.
Boë, L. J., Berthommier, F., Legou, T., Captier, G., Kemp, C., Sawallis, T. R., Becker, Y., Rey, A., & Fagot, J. (2017). Evidence of a vocalic proto-system in the baboon (Papio papio) suggests pre-hominin speech precursors. PLoS One, 12(1), e0169321. https://doi.org/10.1371/journal.pone.0169321.
Boersma, P., & Weenink, D. (2013). Praat: Doing phonetics by computer, version 5.3.51. http://www.praat.org/ (Accessed April 1, 2015).
Brockelman, W. Y., & Schilling, D. (1984). Inheritance of stereotyped gibbon calls. Nature, 312(5995), 634–636. https://doi.org/10.1038/312634a0.
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(3), 443–448. https://doi.org/10.1242/jeb.00768.
Buerkle, C. (2005). Maximum-likelihood estimation of a hybrid index based on molecular markers. Molecular Ecology Notes, 5(3), 684–687. https://doi.org/10.1111/j.1471-8286.2005.01011.x.
Candiotti, A., Zuberbühler, K., & Lemasson, A. (2012). Convergence and divergence in Diana monkey vocalizations. Biology Letters, 8(3), 382–385. https://doi.org/10.1098/rsbl.2011.1182.
Chow, C. P., Mitchell, J. F., & Miller, C. T. (2015). Vocal turn-taking in a non-human primate is learned during ontogeny. Proceedings of the Royal Society B: Biological Sciences, 282(1807), 20150069. https://doi.org/10.1098/rspb.2015.0069.
Cody, M. L. (1969). Convergent characteristics among sympatric populations: A possible relation to inter-specific territoriality. Condor, 71, 222–239.
Cohen, J. (1992). A power primer. Psychological Bulletin, 112(1), 155–159. https://doi.org/10.1037/0033-2909.112.1.155.
Cortés-Ortiz, L., Duda Jr., T. J., Canales-Espinosa, D., García-Orduna, F., Rodríguez-Luna, E., & Bermingham, E. (2007). Hybridization in large-bodied new world primates. Geneticss, 176(4), 2421–2425. https://doi.org/10.1534/genetics.107.074278.
Cortés-Ortiz, L., Agostini, I., Aguiar, L. M., Kelaita, M., Silva, F. E., & Bicca-Marques, J. C. (2015). Hybridization in howler monkeys: Current understanding and future directions. In M. M. Kowalewski, P. A. Garber, L. Cortés-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Adaptive radiation, systematics, and morphology (pp. 107–132). Developments in primatology: Progress and prospects. New York: Springer science+business media.
Crockford, C., Herbinger, I., Vigilant, L., & Boesh, C. (2004). Wild chimpanzees produce group-specific calls: A case for vocal learning? Ethology, 110(3), 221–243. https://doi.org/10.1111/j.1439-0310.2004.00968.x.
de Boer, B., & Fitch, T. W. (2010). Computer models of vocal tract evolution: an overview and critique. Adaptive Behavior, 18(1), 36–47. https://doi.org/10.1177/1059712309350972.
de la Torre, S., & Snowdon, C. T. (2009). Dialects in pygmy marmosets? Population variation in call structure. American Journal of Primatology, 71(4), 333–342. https://doi.org/10.1002/ajp.20657.
Dunn, J. C., Halenar, L. B., Davies, T. G., Cristobal-Azkarate, J., Reby, D., Sykes, D., Dengg, S., Fitch, W. T., & Knapp, L. A. (2015). Evolutionary trade-off between vocal tract and testes dimensions in howler monkeys. Current Biology, 25(21), 2839–2844. https://doi.org/10.1016/j.cub.2015.09.029.
Dunteman, G. H., & Ho, M. H. R. (2006). An introduction to generalized linear models. Thousand Oaks: SAGE Publications. https://doi.org/10.4135/9781412983273.
Elowson, A. M., & Snowdon, C. T. (1994). Pygmy marmosets, Cebuella pygmaea, modify vocal structure in response to changed social environment. Animal Behaviour, 47(6), 1267–1277. https://doi.org/10.1006/anbe.1994.1175.
Ey, E., & Fischer, J. (2011). Keeping in contact: Flexibility in calls of olive baboons. In V. Sommer, & C. Ross (Eds.), Primates of Gashaka: Socioecology and Conservation in Nigeria’s Biodiversity Hotspot (pp. 413–436). Developments in primatology: Progress and prospects. New York: Springer science+business media.
Ey, E., Rahn, C., Hammerschmidt, K., & Fischer, J. (2009). Wild female olive baboons adapt their grunt vocalizations to environmental conditions. Ethology, 115(5), 493–503. https://doi.org/10.1111/j.1439-0310.2009.01638.x.
Fischer, J., Hammerschmidt, K., & Todt, D. (1998). Local variation in barbary macaque shrill barks. Animal Behaviour, 56(3), 623–629. https://doi.org/10.1006/anbe.1998.0796.
Fitch, W. T. (1997). Vocal tract length and formant frequency dispersion correlate with body size in rhesus macaques. Journal of the Acoustical Society of America, 102(2), 1213–1222. https://doi.org/10.1121/1.421048.
Fitch, W. T. (2017). Empirical approaches to the study of language evolution. Psychonomic Bulletin & Review, 24(1), 3–33. https://doi.org/10.3758/s13423-017-1236-5.
Fitch, W. T., & Fritz, J. B. (2006). Rhesus macaques spontaneously perceive formants in conspecific vocalizations. Journal of the Acoustical Society of America, 120(4), 2132–2141. https://doi.org/10.1121/1.2258499.
Fitch, W. T., Neubauer, J., & Herzel, H. (2002). Calls out of chaos: The adaptive significance of nonlinear phenomena in mammalian vocal production. Animal Behaviour, 63(3), 407–418. https://doi.org/10.1006/anbe.2001.1912.
Fitch, W. T., de Boer, B., Mathur, N., & Ghazanfar, A. A. (2016). Monkey vocal tracts are speech-ready. Science Advances, 2(12), e1600723. https://doi.org/10.1126/sciadv.1600723.
Gamba, M., & Giacoma, C. (2006). Vocal tract modeling in a prosimian primate: The black and white ruffed lemur. Acta Acustica United with Acustica, 92, 749–755.
Garnier, M., Wolfe, J., Henrich, N., & Smith, J. (2008). Interrelationship between vocal effort and vocal tract acoustics: a pilot study. In: Proceedings of the Annual Conference of the International Speech Communication Association, Interspeech, pp. 2302–2305.
Geissmann, T. (1984). Inheritance of song parameters in the gibbon song, analysed in 2 hybrid gibbons (Hylobates pileatus× H. lar). Folia Primatologica, 42(3-4), 216–235. https://doi.org/10.1159/000156165.
Haavie, J., Borge, T., Bures, S., Garamszegi, L. Z., Lampe, H. M., Moreno, J., Qvarnström, A., Török, J., & Saetre, G. P. (2004). Flycatcher song in allopatry and sympatry: Convergence, divergence and reinforcement. Journal of Evolutionary Biology, 17(2), 227–237. https://doi.org/10.1111/j.1420-9101.2003.00682.x.
Hammerschmidt, K., & Fischer, J. (2008). Constraints in primate vocal production. In U. Griebel & K. Oller (Eds.), The evolution of communicative creativity: From fixed signals to contextual flexibility (pp. 93–119). Cambridge: The MIT Press. https://doi.org/10.7551/mitpress/9780262151214.003.0005.
Hammerschmidt, K., Newman, J. D., Champoux, M., & Suomi, S. J. (2000). Changes in rhesus macaque ‘coo’ vocalizations during early development. Ethology, 106(10), 873–886. https://doi.org/10.1046/j.1439-0310.2000.00611.x.
Hammerschmidt, K., Freudenstein, T., & Jürgens, U. (2001). Vocal development in squirrel monkeys. Behaviour, 138(9), 1179–1204. https://doi.org/10.1163/156853901753287190.
Ho, L., Cortés-Ortiz, L., Dias, P. A. D., Canales-Espinosa, D., Kitchen, D. M., & Bergman, T. J. (2014). Effect of ancestry on behavioral variation in two species of howler monkeys (Alouatta pigra and A. palliata) and their hybrids. American Journal of Primatology, 76(9), 855–867. https://doi.org/10.1002/ajp.22273.
Hopkins, M. E. (2013). Relative dominance and resource availability mediate mantled howler (Alouatta palliata) spatial responses to neighbors’ loud calls. International Journal of Primatology, 34(5), 1032–1054. https://doi.org/10.1007/s10764-013-9713-9.
Hsiao, M. D., Solomon, N. P., Luschei, E. S., & Titze, I. R. (1994). Effect of subglottic pressure in fundamental frequency of the canine larynx with active muscle tension. Annals of Otology, Rhinology & Laryngology , 103, 817–821.
IUCN (2017). IUCN Red List of Threatened Species. Version 2016.3. www.iucnredlist.org (Accessed April 3, 2017).
Janik, V. M. (2014). Cetacean vocal learning and communication. Current Opinion in Neurobiology, 28, 60–65. https://doi.org/10.1016/j.conb.2014.06.010.
Janik, V. M., & Slater, P. J. B. (1997). Vocal learning in mammals. Advances in the Study of Behaviour, 26, 59–100. https://doi.org/10.1016/S0065-3454(08)60377-0.
Janik, V. M., & Slater, P. J. B. (2000). The different roles of social learning in vocal communication. Animal Behaviour, 60(1), 1–11. https://doi.org/10.1006/anbe.2000.1410.
Kelaita, M., & Cortés-Ortiz, L. (2013). Morphology of genetically-confirmed Alouatta pigra × A. palliata hybrids from a natural hybrid zone in tabasco, Mexico. American Journal of Physical Anthropology, 150(2), 223–234. https://doi.org/10.1002/ajpa.22196.
Kenyon, H. L., Toews, D. P. L., & Irwin, D. E. (2011). Can song discriminate between MacGillivray's and mourning warblers in a narrow hybrid zone? The Condor, 113(3), 655–663. https://doi.org/10.1525/cond.2011.100182.
Kirschel, A. N. G., Blumstein, D. T., & Smith, T. B. (2009). Character displacement of song and morphology in African tinkerbirds. Proceedings of the National Academy of Sciences of the USA, 106(20), 8256–8261. https://doi.org/10.1073/pnas.0810124106.
Kitchen, D. M. (2000). Aggression and assessment among social groups of Belizean black howler monkeys (Alouatta pigra). PhD Dissertation, University of Minnesota.
Kitchen, D. M., da Cunha, R. G. T., Holzmann, I., & de Oliveira, D. A. G. (2015). Function of loud calling in howler monkeys. In M. M. Kowalewski, P. A. Garber, L. Cortés-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Adaptive radiation, systematics, and morphology (pp. 369–402). Developments in primatology: Progress and prospects. New York: Springer science+business media.
Knörnschild, M. (2014). Vocal production learning in bats. Current Opinion in Neurobiology, 28, 80–85. https://doi.org/10.1016/j.conb.2014.06.014.
Lameira, A. R., Maddieson, I., & Zuberbühler, K. (2014). Primate feedstock for the evolution of consonants. Trends in Cognitive Sciences, 18(2), 60–62. https://doi.org/10.1016/j.tics.2013.10.013.
Leary, C. J. (2001). Evidence of convergent character displacement in release vocalizations of Bufo fowleri and Bufo terrestris (Anura; Bufonidae). Animal Behaviour, 61(2), 431–438. https://doi.org/10.1006/anbe.2000.1597.
Lemasson, A., Ouattara, K., Petit, E. J., & Zuberbühler, K. (2011). Social learning of vocal structure in a nonhuman primate? BMC Evolutionary Biology, 11(1), 362. https://doi.org/10.1186/1471-2148-11-362.
Levréro, F., Carrete-Vega, G., Herbert, A., Lawabi, I., Courtiol, A., Willaume, E., Kappeler, P. M., & Charpentier, M. J. E. (2015). Social shaping of voices does not impair phenotype matching of kinship in mandrills. Nature Communications, 6, 7609. https://doi.org/10.1038/ncomms8609.
Lieberman, P. H., Klatt, D. H., & Wilson, W. H. (1969). Vocal tract limitations on the vowel repertoires of rhesus monkey and other nonhuman primates. Science, 164(3884), 1185–1187. https://doi.org/10.1126/science.164.3884.1185.
Liénard, J. S., & Di Benedetto, M. G. (1999). Effect of vocal effort on spectral properties of vowels. Journal of the Acoustical Society of America, 106(1), 411–422. https://doi.org/10.1121/1.428140.
Long, A. M., Moore, N. P., & Hayden, T. J. (1998). Vocalizations in red deer (Cervus elaphus), sika deer (Cervus nippon), and red × sika hybrids. Journal of Zoology, 244, 123–134.
Maeda, T., & Mastataka, N. (1987). Locale-specific vocal behaviour of the tamarin (Saguinus i. labiatus). Ethology, 75, 25–30.
Marshall, A. J., Wrangham, R. W., & Arcadi, A. C. (1999). Does learning affect the structure of vocalizations in chimpanzees? Animal Behaviour, 58(4), 825–830. https://doi.org/10.1006/anbe.1999.1219.
Mitani, J. C., & Gros-Louis, J. (1998). Chorusing and call convergence in chimpanzees: Tests of three hypotheses. Behaviour, 135(8), 1041–1064. https://doi.org/10.1163/156853998792913483.
Mitani, J., Hasegawa, T., Gros-Louis, J., Marler, P., & Byrne, R. (1992). Dialects in wild chimpanzees? American Journal of Primatology, 27(4), 233–243. https://doi.org/10.1002/ajp.1350270402.
Mitani, J. C., Hunley, K. L., & Murdoch, M. E. (1999). Geographic variation in the calls of wild chimpanzees: A reassessment. American Journal of Primatology, 47(2), 133–151. https://doi.org/10.1002/(SICI)1098-2345(1999)47:2<133::AID-AJP4>3.0.CO;2-I.
Nakagawa, S., & Cuthill, I. C. (2007). Effect size, confidence interval and statistical significance: A practical guide for biologists. Biological Reviews, 82(4), 591–605. https://doi.org/10.1111/j.1469-185X.2007.00027.x.
Newman, J., & Symmes, D. (1982). Inheritance and experience in the acquisition of primate acoustic behavior. In C. Snowden, C. Brown, & M. Peterson (Eds.), Primate communication (pp. 259–278). London: Academic Press.
Noor, M. A. F. (1999). Reinforcement and other consequences of sympatry. Heredity, 83(5), 503–508. https://doi.org/10.1038/sj.hdy.6886320.
Owren, M. J., Dieter, J. A., Seyfarth, R. M., & Cheney, D. L. (1993). Vocalizations of rhesus and Japanese macaques cross-fostered between species show evidence of only limited modification. Developmental Psychobiology, 26(7), 389–406. https://doi.org/10.1002/dev.420260703.
Owren, M. J., Amoss, R. T., & Rendall, D. (2011). Two organizing principles of vocal production: Implications for nonhuman and human primates. American Journal of Primatology, 7, 1–15.
Page, B., Goldsworthy, S. D., & Hindell, M. A. (2001). Vocal traits of hybrid fur seals: Intermediate to their parental species. Animal Behaviour, 61(5), 959–967. https://doi.org/10.1006/anbe.2000.1663.
Petkov, C. I., & Jarvis, E. (2012). Birds, primates, and spoken language origins: Behavioral phenotypes and neurobiological substrates. Frontiers in Evolutionary Neuroscience, 4, 12. https://doi.org/10.3389/fnevo.2012.00012.
Pfennig, K., & Pfennig, D. (2009). Character displacement: Ecological and reproductive responses to a common evolutionary problem. The Quarterly Review of Biology, 84(3), 253–276. https://doi.org/10.1086/605079.
Poole, J. H., Tyack, P. L., Stoeger-Horwath, A. S., & Watwood, S. (2005). Elephants capable of vocal learning. Nature, 434(7032), 455–456. https://doi.org/10.1038/434455a.
Prat, Y., Taub, M., & Yovel, Y. (2015). Vocal learning in a social mammal: Demonstrated by isolation and playback experiments in bats. Science Advances, 1(2), e1500019. https://doi.org/10.1126/sciadv.1500019.
Reichmuth, C., & Casey, C. (2014). Vocal learning in seals, sea lions, and walruses. Current Opinion in Neurobiology, 28, 66–71. https://doi.org/10.1016/j.conb.2014.06.011.
Riede, T., Herzel, H., Hammerschmidt, K., Brunnberg, L., & Tembrock, G. (2001). The harmonic-to-noise-ratio applied to dog barks. Journal of the Acoustical Society of America, 110(4), 2191–2197. https://doi.org/10.1121/1.1398052.
Riede, T., Bronson, E., Hatzikirou, B., & Zuberbühler, K. (2005). The production mechanisms of Diana monkey alarm calls: Morphological data and a model. Journal of Human Evolution, 48(1), 85–96. https://doi.org/10.1016/j.jhevol.2004.10.002.
Rukstalis, M., Fite, J. E., & French, J. A. (2003). c vocal structure in a callitrichid primate (Callithrix kuhlii). Ethology, 109(4), 327–340. https://doi.org/10.1046/j.1439-0310.2003.00875.x.
Secondi, J., Bretagnolle, V., Compagnon, C., & Faivre, B. (2003). Species-specific song convergence in a moving hybrid zone between two passerines. Biological Journal of the Linnean Society, 80(3), 507–517. https://doi.org/10.1046/j.1095-8312.2003.00248.x.
Seddon, N. (2005). Ecological adaptation and species recognition drives vocal evolution in neotropical suboscine birds. Evolution, 59(1), 200–215. https://doi.org/10.1111/j.0014-3820.2005.tb00906.x.
Seyfarth, R. M., & Cheney, D. L. (2010a). Primate vocal communication. In M. L. Platt & A. A. Ghazanfar (Eds.), Primate neuroethology (pp. 84–97). New York: Oxford University Press. https://doi.org/10.1093/acprof:oso/9780195326598.003.0005.
Seyfarth, R. M., & Cheney, D. L. (2010b). Production, usage, and comprehension in animal vocalizations. Brain and Language, 115(1), 92–100. https://doi.org/10.1016/j.bandl.2009.10.003.
Sinnott, J. M., Stebbins, W. C., & Moody, D. B. (1975). Regulation of voice amplitude by the monkey. Journal of the Acoustical Society of America, 58(2), 412–414. https://doi.org/10.1121/1.380685.
Snowdon, C. T., & Elowson, A. M. (1999). Pygmy marmosets modify call structure when paired. Ethology, 105(10), 893–908. https://doi.org/10.1046/j.1439-0310.1999.00483.x.
Stoeger, A. S., & Manger, P. (2014). Vocal learning in elephants: Neural bases and adaptive context. Current Opinion in Neurobiology, 28, 101–107. https://doi.org/10.1016/j.conb.2014.07.001.
Sugiura, H. (1998). Matching of acoustic features during the vocal exchange of coo calls by Japanese macaques. Animal Behaviour, 55(3), 673–687. https://doi.org/10.1006/anbe.1997.0602.
Takahashi, D. Y., Fenley, A. R., Teramoto, Y., Narayanan, D. Z., Borjon, J. I., Holmes, P., & Ghazanfar, A. A. (2015). The developmental dynamics of marmoset monkey vocal production. Science, 349(6249), 734–738. https://doi.org/10.1126/science.aab1058.
ten Cate, C., & Rowe, C. (2007). Biases in signal evolution: Learning makes a difference. Trends in Ecology and Evolution, 22(7), 380–387. https://doi.org/10.1016/j.tree.2007.03.006.
Tyack, P. L. (2008). Convergence of calls as animals form social bonds, active compensation for noisy communication channels, and the evolution of vocal learning in mammals. Journal of Comparative Psychology, 122(3), 319–331. https://doi.org/10.1037/a0013087.
Tyack, P. L., & Sayigh, L. S. (1997). Vocal learning in cetaceans. In C. T. Snowdon & M. Hauserberger (Eds.), Social influences on vocal development (pp. 208–233). Cambridge: Cambridge University Press. https://doi.org/10.1017/CBO9780511758843.011.
Van Belle, S., Estrada, A., & Garber, P. A. (2013). Spatial and diurnal distribution of loud calling in black howlers (Alouatta pigra). International Journal of Primatology, 34(6), 1209–1224. https://doi.org/10.1007/s10764-013-9734-4.
Watson, S. K., Townsend, S. W., Schel, A. M., Wilke, C., Wallace, E. K., Cheng, L., West, V., & Slocombe, K. E. (2015). Vocal learning in the functionally referential food grunts of chimpanzees. Current Biology, 25(4), 495–499. https://doi.org/10.1016/j.cub.2014.12.032.
Whitehead, J. M. (1995). Vox Alouattinae: A preliminary survey of the acoustic characteristics of long-distance calls of howling monkeys. International Journal of Primatology, 16(1), 121–144. https://doi.org/10.1007/BF02700156.
Acknowledgements
This study was possible because of funding from National Science Foundation grants (BCS-0962807 and BCS-0962755). We also thank The Ohio State University, the University of Michigan, and Universidad Veracruzana for financial and in-kind assistance. We are grateful to the government of Mexico and the many landowners who allowed us to conduct this research. Our work was greatly assisted by Dara Adams, Antoinette Bode-Higgerson, Rosario Candelero Rueda, Roxann Chicalo, Alejandro Coyohua, Pamela Cruz Miros, Jason Ferrell, Alfredo Gόmez Martinez, Suzanna Hammond, Ana Peralta, Ariadna Rangel Negrín, Lucy Redfern Cummins, Cynthia Rodrίguez Maldonado, and Jay Schwartz. We also thank the editor-in-chief, the guest editor, and two anonymous reviewers for their valuable insights that greatly improved the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Guest Editors of the Special Issue
Electronic supplementary material
ESM 1
(PDF 561 kb)
Rights and permissions
About this article
Cite this article
Kitchen, D.M., Bergman, T.J., Dias, P.A.D. et al. Temporal but Not Acoustic Plasticity in Hybrid Howler Monkey (Alouatta palliata × A. pigra) Loud Calls. Int J Primatol 40, 132–152 (2019). https://doi.org/10.1007/s10764-017-0004-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10764-017-0004-8