Sex differences in the acoustic structure of terrestrial alarm calls in vervet monkeys (Chlorocebus pygerythrus).
Chlorocebus pygerythrus
alarm call
bioacoustics
call structure
communication
predator model
sexual selection
Journal
American journal of primatology
ISSN: 1098-2345
Titre abrégé: Am J Primatol
Pays: United States
ID NLM: 8108949
Informations de publication
Date de publication:
20 Aug 2024
20 Aug 2024
Historique:
revised:
19
07
2024
received:
26
09
2023
accepted:
27
07
2024
medline:
20
8
2024
pubmed:
20
8
2024
entrez:
20
8
2024
Statut:
aheadofprint
Résumé
The alarm calls of vervet monkeys (Chlorocebus pygerythrus) have been the subject of considerable focus by researchers, owing primarily to the purported referential qualities of different alarm call types. With this focus on reference, acoustic variation among calls elicited by the same range of predators has typically been overlooked. Specifically, at least one type of alarm call-the terrestrial alarm-was described over 50 years ago as being acoustically distinct between males and females-a description that has largely eluded more systematic scrutiny. Here, we provide a quantitative acoustic analysis and comparison of terrestrial alarm calls produced by adult male and female vervet monkeys. We use a random forest model to determine which acoustic variables best distinguish between the calls of males and females, and use an unsupervised clustering technique to objectively determine whether alarms produced by each sex fall into discrete types. We found that the calls of males and females differed most in frequency-based parameters, with male alarms containing more energy at lower frequencies relative to females. Calls produced by males were also of longer duration, and consisted of longer individual call elements relative to female calls. While calls generally fell into clusters associated with either male or female alarms, we found that some fell into atypical clusters given the caller's sex, and that the clusters themselves showed evidence of intergradation. We discuss these results in terms of potential differences in the function of, and motivation for, calling by males and females. We emphasize the need for a more holistic approach to the classification of vocal signals that considers contextual, functional, and structural variation.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e23674Subventions
Organisme : Killam Trusts
Organisme : Faculty of Graduate Studies at the University of Calgary
Organisme : National Research Foundation (South Africa) grants
Organisme : Natural Sciences and Engineering Research Council of Canada
Informations de copyright
© 2024 The Author(s). American Journal of Primatology published by Wiley Periodicals LLC.
Références
Arcadi, A. C. (1996). Phrase structure of wild chimpanzee pant hoots: Patterns of production and interpopulation variability. American Journal of Primatology, 39(3), 159–178. https://doi.org/10.1002/(SICI)1098-2345(1996)39:3<159::AID-AJP2>3.0.CO;2-Y
Arnedo, L. F., Mendes, F. D. C., & Strier, K. B. (2010). Sex differences in vocal patterns in the Northern muriqui (Brachyteles hypoxanthus). American Journal of Primatology, 72(2), 122–128. https://doi.org/10.1002/ajp.20761
Van Belle, S. (2015). Female participation in collective group defense in black howler monkeys (Alouatta pigra). American Journal of Primatology, 77(6), 595–604. https://doi.org/10.1002/ajp.22380
Bernstein, S. K., Sheeran, L. K., Wagner, R. S., Li, J.‐H., & Koda, H. (2016). The vocal repertoire of Tibetan macaques (Macaca thibetana): A quantitative classification. American Journal of Primatology, 78(9), 937–949. https://doi.org/10.1002/ajp.22564
Breiman, L. (2001). Random forests. Machine Learning, 45, 5–32.
Briseño‐Jaramillo, M., Biquand, V., Estrada, A., & Lemasson, A. (2017). Vocal repertoire of free‐ranging black howler monkeys’ (Alouatta pigra): Call types, contexts, and sex‐related contributions. American Journal of Primatology, 79(5), e22630. https://doi.org/10.1002/ajp.22630
Bürkner, P.‐C. (2017). brms: An R package for Bayesian multilevel models using stan. Journal of statistical software, 80, 1–28. https://doi.org/10.18637/jss.v080.i01
Caro, T. M. (2005). Antipredator defenses in birds and mammals. University of Chicago Press.
Charlton, B. D., Reby, D., & McComb, K. (2007). Female perception of size‐related formant shifts in red deer, Cervus elaphus. Animal Behaviour, 74(4), 707–714. https://doi.org/10.1016/j.anbehav.2006.09.021
Charrad, M., Ghazzali, N., Boiteau, V., & Niknafs, A. (2014). NbClust: An R package for determining the relevant number of clusters in a data set. Journal of statistical software, 61, 1–36. https://doi.org/10.18637/jss.v061.i06
Chawla, N. V., Bowyer, K. W., Hall, L. O., & Kegelmeyer, W. P. (2002). SMOTE: Synthetic minority over‐sampling technique. Journal of Artificial Intelligence Research, 16, 321–357. https://doi.org/10.1613/jair.953
Croll, D. A., Clark, C. W., Acevedo, A., Tershy, B., Flores, S., Gedamke, J., & Urban, J. (2002). Only male fin whales sing loud songs. Nature, 417(6891), 809. https://doi.org/10.1038/417809a
Delgado, R. A. (2006). Sexual selection in the loud calls of male primates: Signal content and function. International Journal of Primatology, 27(1), 5–25. https://doi.org/10.1007/s10764-005-9001-4
Deshpande, A., van de Waal, E., & Zuberbühler, K. (2023). Context‐dependent alarm responses in wild vervet monkeys. Animal Cognition, 26(4), 1199–1208. https://doi.org/10.1007/s10071-023-01767-0
Dixson, A. F. (1998). Primate sexuality: Comparative studies of the prosimians, monkeys, apes, and human beings. Oxford University Press.
Dubreuil, C., Barrett, L., Henzi, P. S., Notman, H., & Pavelka, M. S. M. (2023). Age differences in the responses of vervet monkeys, Chlorocebus pygerythrus, to terrestrial alarm calls. Animal Behaviour, 201, 87–100. https://doi.org/10.1016/j.anbehav.2023.04.014
Dubreuil, C., Notman, H., & Pavelka, M. S. M. (2015). Sex differences in the use of whinny vocalizations in spider monkeys (Ateles geoffroyi). International Journal of Primatology, 36, 412–428. https://doi.org/10.1007/s10764-015-9832-6
Dubreuil, C. J. (2019). The acoustic structure and ontogeny of vervet monkey vocalizations. [PhD Thesis]. University of Calgary.
Ducheminsky, N., Henzi, S. P., & Barrett, L. (2014). Responses of vervet monkeys in large troops to terrestrial and aerial predator alarm calls. Behavioral Ecology, 25(6), 1474–1484. https://doi.org/10.1093/beheco/aru151
Enstam, K. L., & Isbell, L. A. (2002). Comparison of responses to alarm calls by patas (Erythrocebus patas) and vervet (Cercopithecus aethiops) monkeys in relation to habitat structure. American Journal of Physical Anthropology, 119(1), 3–14. https://doi.org/10.1002/ajpa.10104
Fichtel, C., & Hammerschmidt, K. (2002). Responses of redfronted lemurs to experimentally modified alarm calls: Evidence for Urgency‐Based changes in call structure. Ethology, 108(9), 763–778. https://doi.org/10.1046/j.1439-0310.2002.00816.x
Fichtel, C., & Kappeler, P. M. (2002). Anti‐predator behavior of group‐living Malagasy primates: Mixed evidence for a referential alarm call system. Behavioral Ecology and Sociobiology, 51, 262–275. https://doi.org/10.1007/s00265-001-0436-0
Fischer, J. (2017). Primate vocal production and the riddle of language evolution. Psychonomic Bulletin & Review, 24(1), 72–78. https://doi.org/10.3758/s13423-016-1076-8
Fischer, J., Hammerschmidt, K., Cheney, D. L., & Seyfarth, R. M. (2001). Acoustic features of female chacma baboon barks. Ethology, 107(1), 33–54. https://doi.org/10.1111/j.1439-0310.2001.00630.x
Fischer, J., Hammerschmidt, K., Cheney, D. L., & Seyfarth, R. M. (2002). Acoustic features of male baboon loud calls: Influences of context, age, and individuality. The Journal of the Acoustical Society of America, 111(3), 1465–1474. https://doi.org/10.1121/1.1433807
Fischer, J., Kitchen, D. M., Seyfarth, R. M., & Cheney, D. L. (2004). Baboon loud calls advertise male quality: acoustic features and their relation to rank, age, and exhaustion. Behavioral Ecology and Sociobiology, 56(2), 140–148. https://doi.org/10.1007/s00265-003-0739-4
Fischer, J., Metz, M., Cheney, D. L., & Seyfarth, R. M. (2001). Baboon responses to graded bark variants. Animal Behaviour, 61(5), 925–931. https://doi.org/10.1006/anbe.2000.1687
Fischer, J., Noser, R., & Hammerschmidt, K. (2013). Bioacoustic field research: A primer to acoustic analyses and playback experiments with primates. American Journal of Primatology, 75(7), 643–663. https://doi.org/10.1002/ajp.22153
Fischer, J., Wadewitz, P., & Hammerschmidt, K. (2017). Structural variability and communicative complexity in acoustic communication. Animal Behaviour, 134, 229–237. https://doi.org/10.1016/j.anbehav.2016.06.012
Fitch, W. T., & Hauser, M. D. (2003). Unpacking “Honesty”: Vertebrate vocal production and the evolution of acoustic signals. In A. M. Simmons, R. R. Fay, & A. N. Popper(Eds.), Acoustic communication (Vol. 16, pp. 65–137). Springer‐Verlag. https://doi.org/10.1007/0-387-22762-8_3
Fontaine, J. R. J., Scherer, K. R., Roesch, E. B., & Ellsworth, P. C. (2007). The world of emotions is not two‐dimensional. Psychological Science, 18(12), 1050–1057. https://doi.org/10.1111/j.1467-9280.2007.02024.x
Fuller, J. L. (2014). The vocal repertoire of adult male blue monkeys (Cercopithecus mitis stulmanni): A quantitative analysis of acoustic structure. American Journal of Primatology, 76(3), 203–216. https://doi.org/10.1002/ajp.22223
Fuller, J. L., & Cords, M. (2017). Multiple functions and signal concordance of the pyow loud call of blue monkeys. Behavioral Ecology and Sociobiology, 71(1), 19. https://doi.org/10.1007/s00265-016-2230-z
Gabry, J., & Mahr, T. (2022). bayesplot: Plotting for Bayesian models (R package version 1.10.0) [Computer software]. https://mc-stan.org/bayesplot/
Gabry, J., Simpson, D., Vehtari, A., Betancourt, M., & Gelman, A. (2019). Visualization in Bayesian workflow. Journal of the Royal Statistical Society Series A: Statistics in Society, 182, 389–402. https://doi.org/10.1111/rssa.12378
Gautier, J.‐P., & Gautier‐Hion, A. (1977). Communication in Old World monkeys, In How animals communicate (p. 890). Indiana University Press. https://univ-rennes.hal.science/hal-01371645.
Gelman, A., & Carlin, J. (2014). Beyond power calculations: assessing type S (Sign) and type M (Magnitude) errors. Perspectives on Psychological Science, 9(6), 641–651.
Goudbeek, M., & Scherer, K. (2010). Beyond arousal: Valence and potency/control cues in the vocal expression of emotion. The Journal of the Acoustical Society of America, 128(3), 1322–1336. https://doi.org/10.1121/1.3466853
Hammerschmidt, K., & Fischer, J. (1998). The vocal repertoire of barbary macaques: A quantitative analysis of a graded signal system. Ethology, 104(3), 203–216. https://doi.org/10.1111/j.1439-0310.1998.tb00063.x
Harris, T. R., Fitch, W. T., Goldstein, L. M., & Fashing, P. J. (2006). Black and white colobus monkey (Colobus guereza) roars as a source of both honest and exaggerated information about body mass. Ethology, 112(9), 911–920. https://doi.org/10.1111/j.1439-0310.2006.01247.x
Hohmann, G. (1991). Comparative analyses of age‐ and sex‐specific patterns of vocal behaviour in four species of old world monkeys. Folia Primatologica, 56(3), 133–156. https://doi.org/10.1159/000156538
Kassambara, A. (2017). Practical guide to cluster analysis in R: Unsupervised machine learning. Vol. 1. Sthda.
Kassambara, A. (2018). Machine learning essentials: Practical guide in R. STHDA.
Kaufman, L., & Rousseeuw, P. J. (2009). Finding groups in data: An introduction to cluster analysis. John Wiley & Sons.
Kitchen, D. M., Cheney, D. L., & Seyfarth, R. M. (2003a). Female Baboons’ responses to Male loud calls. Ethology, 109(5), 401–412. https://doi.org/10.1046/j.1439-0310.2003.00878.x
Kitchen, D. M., da Cunha, R., Holzmann, I., & Oliveira, D. (2015). Function of loud calls in Howler Monkeys. 369–399. https://doi.org/10.1007/978-1-4939-1957-4_14
Kitchen, D. M., Seyfarth, R. M., Fischer, J., & Cheney, D. L. (2003b). Loud calls as indicators of dominance in male baboons (Papio cynocephalus ursinus). Behavioral Ecology and Sociobiology, 53(6), 374–384. https://doi.org/10.1007/s00265-003-0588-1
Kuhn, M., Wing, J., Weston, S., Williams, A., Keefer, C., Engelhardt, A., Cooper, T., Mayer, Z., Kenkel, B.R Core Team, Benesty, M., Lescarbeau, R., Ziem, A., Scrucca, L., Tang, Y., Candan, C., & Hunt, T. (2023). caret: Classification and regression training (6.0‐94) [Computer software]. https://cran.r-project.org/web/packages/caret/index.html
Lemasson, A., Guilloux, M., Rizaldi, A. A., Barbu, S., Lacroix, A., & Koda, H. (2013). Age‐ and sex‐dependent contact call usage in Japanese macaques. Primates, 54(3), 283–291. https://doi.org/10.1007/s10329-013-0347-5
Liaw, A., & Wiener, M. (2002). Classification and regression by randomforest. R News, 2, 18–22.
De Luna, A. G., Sanmiguel, R., Fiore, A. D., & Fernandez‐Duque, E. (2010). Predation and predation attempts on red titi monkeys (Callicebus discolor) and equatorial sakis (Pithecia aequatorialis) in amazonian Ecuador. Folia Primatologica, 81(2), 86–95. https://doi.org/10.1159/000314948
Makowski, D., Ben‐Shachar, M., & Lüdecke, D. (2019). bayestestR: describing effects and their uncertainty, existence and significance within the Bayesian framework. Journal of Open Source Software, 4(40), 1541.
Manser, M. B. (2001). The acoustic structure of suricates’ alarm calls varies with predator type and the level of response urgency. Proceedings of the Royal Society of London. Series B: Biological Sciences, 268(1483), 2315–2324. https://doi.org/10.1098/rspb.2001.1773
Marler, P., & Tenaza, R. (1977). Signaling behavior of apes with special reference to vocalization. In T. A. Sebeok (Ed.), How Animals Communicate. Indiana University Press. https://cir.nii.ac.jp/crid/1571980074908895872
Marten, K., & Marler, P. (1977). Sound transmission and its significance for animal vocalization: I. temperate habitats. Behavioral Ecology and Sociobiology, 2, 271–290.
Matrosova, V. A., Volodin, I. A., Volodina, E. V., & Babitsky, A. F. (2007). Pups crying bass: Vocal adaptation for avoidance of age‐dependent predation risk in ground squirrels? Behavioral Ecology and Sociobiology, 62(2), 181–191. https://doi.org/10.1007/s00265-007-0452-9
Meise, K., Keller, C., Cowlishaw, G., & Fischer, J. (2011). Sources of acoustic variation: Implications for production specificity and call categorization in chacma baboon (Papio ursinus) grunts. The Journal of the Acoustical Society of America, 129(3), 1631–1641. https://doi.org/10.1121/1.3531944
Mitani, J. C., & Stuht, J. (1998). The evolution of nonhuman primate loud calls: Acoustic adaptation for long‐distance transmission. Primates, 39(2), 171–182. https://doi.org/10.1007/BF02557729
Mohr, T., van de Waal, E., Zuberbühler, K., & Mercier, S. (2023). Juvenile vervet monkeys rely on others when responding to danger. Animal Cognition, 26(4), 1443–1447. https://doi.org/10.1007/s10071-023-01765-2
Morton, E. S. (1975). Ecological sources of selection on avian sounds. The American Naturalist, 109(965), 17–34.
Morton, E. S. (1977). On the occurrence and significance of motivation‐structural rules in some bird and mammal sounds. The American Naturalist, 111(981), 855–869. https://doi.org/10.1086/283219
Notman, H., & Rendall, D. (2005). Contextual variation in chimpanzee pant hoots and its implications for referential communication. Animal Behaviour, 70(1), 177–190. https://doi.org/10.1016/j.anbehav.2004.08.024
Owren, M. J., & Bernacki, R. H. (1988). The acoustic features of vervet monkey alarm calls. The Journal of the Acoustical Society of America, 83(5), 1927–1935.
Owren, M. J., & Rendall, D. (2001). Sound on the rebound: Bringing form and function back to the forefront in understanding Nonhuman primate vocal signaling.
Pasternak, G., Brown, L. R., Kienzle, S., Fuller, A., Barrett, L., & Henzi, S. P. (2013). Population ecology of vervet monkeys in a high latitude, semi‐arid riparian woodland. Koedoe, 55(1), 9. https://doi.org/10.4102/koedoe.v55i1.1078
Pradhan, G. R., Engelhardt, A., Van Schaik, C. P., & Maestripieri, D. (2006). The evolution of female copulation calls in primates: A review and a new model. Behavioral Ecology and Sociobiology, 59(3), 333–343. https://doi.org/10.1007/s00265-005-0075-y
Price, T., Wadewitz, P., Cheney, D., Seyfarth, R., Hammerschmidt, K., & Fischer, J. (2015). Vervets revisited: A quantitative analysis of alarm call structure and context specificity. Scientific Reports, 5(1), Article 1. https://doi.org/10.1038/srep13220
R Core Team. (2022). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/
Rendall, D. (2021). Aping language: Historical perspectives on the quest for semantics, syntax, and other rarefied properties of human language in the communication of primates and other animals. Frontiers in Psychology, 12, 675172.
Riede, T., & Titze, I. R. (2008). Vocal fold elasticity of the Rocky Mountain elk (Cervus elaphus nelsoni) – producing high fundamental frequency vocalization with a very long vocal fold. Journal of Experimental Biology, 211(0 13), 2144–2154. https://doi.org/10.1242/jeb.017004
Russell, J. A. (1994). Is there universal recognition of emotion from facial expression? A review of the cross‐cultural studies. Psychological Bulletin, 115(1), 102–141.
Schad, L., Dongre, P., Van De Waal, E., & Fischer, J. (2023). Alarm barks of male vervet monkeys as displays of male quality [Preprint], Animal Behavior and Cognition. https://doi.org/10.1101/2023.06.08.544199
Seyfarth, R. M., & Cheney, D. L. (1980). The ontogeny of vervet monkey alarm calling behavior: A preliminary report. Zeitschrift für Tierpsychologie, 54(1), 37–56.
Seyfarth, R., & Cheney, D. (1990). The assessment by vervet monkeys of their own and another species' alarm calls. Animal Behaviour, 40(4), 754–764. https://doi.org/10.1016/S0003-3472(05)80704-3
Seyfarth, R. M., & Cheney, D. L. (1986). Vocal development in vervet monkeys. Animal Behaviour, 34(6), 1640–1658. https://doi.org/10.1016/S0003-3472(86)80252-4
Seyfarth, R. M., Cheney, D. L., Bergman, T., Fischer, J., Zuberbühler, K., & Hammerschmidt, K. (2010). The central importance of information in studies of animal communication. Animal Behaviour, 80(1), 3–8. https://doi.org/10.1016/j.anbehav.2010.04.012
Seyfarth, R. M., Cheney, D. L., & Marler, P. (1980a). Monkey responses to three different alarm calls: evidence of predator classification and semantic communication. Science, 210(4471), 801–803. https://doi.org/10.1126/science.7433999
Seyfarth, R. M., Cheney, D. L., & Marler, P. (1980b). Vervet monkey alarm calls: Semantic communication in a free‐ranging primate. Animal Behaviour, 28(4), 1070–1094.
Snowdon, C. T. (2004). Sexual selection and communication. In P. M. Kappeler, & C. P. van Schaik (Eds.), Sexual selection in primates: New and comparative perspectives (pp. 57–70). Cambridge University Press.
Stoeger, A. S., Mietchen, D., Oh, S., de Silva, S., Herbst, C. T., Kwon, S., & Fitch, W. T. (2012). An Asian elephant imitates human speech. Current Biology, 22(22), 2144–2148. https://doi.org/10.1016/j.cub.2012.09.022
Struhsaker, T. T. (1967). Auditory communication among vervet monkeys (Cercopithecus aethiops). In S. A. Altmann (Ed.), Social communication among primates (pp. 281–324). University of Chicago Press.
Swan, D. C., & Hare, J. F. (2008). Signaler and receiver ages do not affect responses to Richardson's ground squirrel alarm calls. Journal of Mammalogy, 89(4), 889–894. https://doi.org/10.1644/07-MAMM-A-228.1
Tallet, C., Linhart, P., Policht, R., Hammerschmidt, K., Šimeček, P., Kratinova, P., & Špinka, M. (2013). Encoding of situations in the vocal repertoire of Piglets (Sus scrofa): A comparison of discrete and graded classifications. PLoS One, 8(8), e71841. https://doi.org/10.1371/journal.pone.0071841
Taylor, A. M., & Reby, D. (2010). The contribution of source–filter theory to mammal vocal communication research. Journal of Zoology, 280(3), 221–236. https://doi.org/10.1111/j.1469-7998.2009.00661.x
Townsend, S. W., & Manser, M. B. (2013). Functionally referential communication in mammals: The past, present and the future. Ethology, 119(1), 1–11. https://doi.org/10.1111/eth.12015
Turner, T. R., Anapol, F., & Jolly, C. J. (1997). Growth, development, and sexual dimorphism in vervet monkeys (Cercopithecus aethiops) at four sites in Kenya. American Journal of Physical Anthropology, 103(1), 19–35. https://doi.org/10.1002/(SICI)1096-8644(199705)103:1<19::AID-AJPA3>3.0.CO;2-8
Vernes, S. C., Kriengwatana, B. P., Beeck, V. C., Fischer, J., Tyack, P. L., ten Cate, C., & Janik, V. M. (2021). The multi‐dimensional nature of vocal learning. Philosophical Transactions of the Royal Society, B: Biological Sciences, 376(1836), 20200236. https://doi.org/10.1098/rstb.2020.0236
Volodina, E. V., Matrosova, V. A., & Volodin, I. A. (2011). An unusual effect of maturation on the alarm call fundamental frequency in two species of ground squirrels. Bioacoustics, 20, 87–98. https://doi.org/10.1080/09524622.2011.9753634
Wadewitz, P., Hammerschmidt, K., Battaglia, D., Witt, A., Wolf, F., & Fischer, J. (2015). Characterizing vocal repertoires—Hard vs. soft classification approaches. PLoS One, 10(4), e0125785. https://doi.org/10.1371/journal.pone.0125785
Warkentin, K. J., Keeley, A. T., & Hare, J. F. (2001). Repetitive calls of juvenile Richardson's ground squirrels (Spermophilus richardsonii) communicate response urgency. Canadian Journal of Zoology, 79(4), 569–573. https://doi.org/10.1139/cjz-79-4-569
Wheeler, B. C. (2009). Monkeys crying wolf? Tufted capuchin monkeys use anti‐predator calls to usurp resources from conspecifics. Proceedings of the Royal Society B: Biological Sciences, 276(1669), 3013–3018. https://doi.org/10.1098/rspb.2009.0544
Wheeler, B. C., & Fischer, J. (2012). Functionally referential signals: A promising paradigm whose time has passed. Evolutionary Anthropology: Issues, News, and Reviews, 21(5), 195–205. https://doi.org/10.1002/evan.21319
Wich, S., & Nunn, C. (2002). Do male “long‐distance calls” function in mate defense? A comparative study of long‐distance calls in primates. Behavioral Ecology and Sociobiology, 52, 474–484. https://doi.org/10.1007/s00265-002-0541-8
Wich, S. A., Koski, S., de Vries, H., & van Schaik, C. P. (2003). Individual and contextual variation in Thomas Langur male loud calls. Ethology, 109(1), 1–13. https://doi.org/10.1046/j.1439-0310.2003.00837.x
Zuberbühler, K. (2001). Predator‐specific alarm calls in Campbell's monkeys, cercopithecus campbelli. Behavioral Ecology and Sociobiology, 50(5), 414–422. https://doi.org/10.1007/s002650100383
Zuberbühler, K. (2002). Effects of natural and sexual selection on the evolution of guenon loud calls. In R. H. Tuttle (Ed.), The guenons: Diversity and adaptation in African monkeys (pp. 289–306). Springer.
Zuberbühler, K. (2009). Survivor signals: The biology and psychology of animal alarm calling. In Advances in the study of behavior (40, pp. 277–322). Elsevier. https://doi.org/10.1016/S0065-3454(09)40008-1
Zuberbühler, K., Noë, R., & Seyfarth, R. M. (1997). Diana monkey long‐distance calls: Messages for conspecifics and predators. Animal Behaviour, 53(3), 589–604. https://doi.org/10.1006/anbe.1996.0334