Abstract
Distress calls are an acoustically variable group of vocalizations ubiquitous in mammals and other animals. Their presumed function is to recruit help, but there has been much debate on whether the nature of the disturbance can be inferred from the acoustics of distress calls. We used machine learning to analyse episodes of distress calls of wild infant chimpanzees. We extracted exemplars from those distress call episodes and examined them in relation to the external event triggering them and the distance to the mother. In further steps, we tested whether the acoustic variants were associated with particular maternal responses. Our results suggest that, although infant chimpanzee distress calls are highly graded, they can convey information about discrete problems experienced by the infant and about distance to the mother, which in turn may help guide maternal parenting decisions. The extent to which mothers rely on acoustic cues alone (versus integrate other contextual-visual information) to decide upon intervening should be the focus of future research.
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Code is available at: https://github.com/ChristophDahl/Chimpanzee-Distress-Calls
References
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–266
Arcadi AC, Wrangham RW (1999) Infanticide in chimpanzees: review of cases and a new within-group observation from the Kanyawara study group in Kibale National Park. Primates 40:337–351
Barajas-Montiel SE, Reyes-Garcia CA (2006) Fuzzy support vector machines for automatic infant cry recognition. In: Intelligent Computing in Signal Processing and Pattern Recognition. Springer, pp 876–881
Bard KA (2000) Crying in infant primates: Insights into the development of crying in chimpanzees. In: Barr RG et al (eds) Crying as a sign, a symptom, and a signal: clinical emotional and developmental aspects of infant and toddler crying. Mac Keith Press, London, p 157
Bayart F, Hayashi KT, Faull KF et al (1990) Influence of maternal proximity on behavioral and physiological responses to separation in infant rhesus monkeys (Macaca mulatta). Behav Neurosci 104:98
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300
Boll S (1979) Suppression of acoustic noise in speech using spectral subtraction. IEEE Trans Acoust Speech Signal Process 27:113–120
Brennan M, Kirkland J (1982) Classification of infant cries using descriptive scales. Infant Behav Dev 5:341–346
Briefer EF (2012) Vocal expression of emotions in mammals: mechanisms of production and evidence. J Zool. https://doi.org/10.1111/j.1469-7998.2012.00920.x@10.1111/(ISSN)1469-7998.SoundProduction
Caldara R, Abdi H (2006) Simulating the ‘other-race’effect with autoassociative neural networks: further evidence in favor of the face-space model. Perception 35:659–670
Chang C-Y, Li J-J (2016) Application of deep learning for recognizing infant cries. In: 2016 IEEE International Conference on Consumer Electronics-Taiwan (ICCE-TW). IEEE, pp 1–2
Chang C-C, Lin C-J (2011) LIBSVM: a library for support vector machines. ACM Trans Intell Syst Technol (TIST) 2:1–27
Choqueuse V (2020) Vuvuzela sound denoising algorithm. Version 1.2.0.0URL https://fr.mathworks.com/matlabcentral/fileexchange/27912-vuvuzela-sound-denoising-algorithm?focused=b421486c-db15-d58a-6f4d-5026e5f66319&tab=function
Christensson K, Cabrera T, Christensson E et al (1995) Separation distress call in the human neonate in the absence of maternal body contact. Acta Paediatr 84:468–473
Crockford C, Wittig RM, Mundry R, Zuberbühler K (2012) Wild chimpanzees inform ignorant group members of danger. Curr Biol 22:142–146. https://doi.org/10.1016/j.cub.2011.11.053
Crockford C, Wittig RM, Zuberbühler K (2017) Vocalizing in chimpanzees is influenced by social-cognitive processes. Sci Adv 3:e1701742. https://doi.org/10.1126/sciadv.1701742
Crockford C, Gruber T, Zuberbühler K (2018) Chimpanzee quiet hoo variants differ according to context. R Soc Open Sci 5:172066
Dahl CD, Wyss C, Zuberbühler K, Bachmann I (2018) Social information in equine movement gestalts. Anim Cogn 21:583–594
Deng L, Li X (2013) Machine learning paradigms for speech recognition: an overview. IEEE Trans Audio Speech Lang Process 21:1060–1089
Dezecache G, Crockford C, Zuberbühler K (2019) The development of communication in alarm contexts in wild chimpanzees. Behav Ecol Sociobiol 73:104. https://doi.org/10.1007/s00265-019-2716-6
Eggeling WJ (1947) Observations on the ecology of the Budongo rain forest Uganda. J Ecol 34:20–87
Ephraim Y, Malah D (1984) Speech enhancement using a minimum-mean square error short-time spectral amplitude estimator. IEEE Trans Acoust Speech Signal Process 32:1109–1121
Fedurek P, Zuberbühler K, Dahl CD (2016) Sequential information in a great ape utterance. Sci Rep 6:38226
Fischer J (1998) Barbary macaques categorize shrill barks into two call types. Anim Behav 55:799–807
Fröhlich M, Hobaiter C (2018) The development of gestural communication in great apes. Behav Ecol Sociobiol 72:194
Fröhlich M, Wittig RM, Pika S (2016) Should I stay or should I go? Initiation of joint travel in mother–infant dyads of two chimpanzee communities in the wild. Anim Cogn 19:483–500
Fröhlich M, Wittig RM, Pika S (2019) The ontogeny of intentional communication in chimpanzees in the wild. Dev Sci 22:e12716
Fuller BF (1991) Acoustic discrimination of three types of infant cries. Nurs Res 40:156–160
Gerencsér L, Vásárhelyi G, Nagy M et al (2013) Identification of behaviour in freely moving dogs (Canis familiaris) using inertial sensors. PLoS ONE 8:e77814
Gilbert HR, Robb MP (1996) Vocal fundamental frequency characteristics of infant hunger cries: birth to 12 months. Int J Pediatr Otorhinolaryngol 34:237–243
Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Harvard University Press, Cambridge
Green PA, Brandley NC, Nowicki S (2020) Categorical perception in animal communication and decision-making. Behav Ecol. https://doi.org/10.1093/beheco/araa004
Hobaiter C, Byrne RW (2011) The gestural repertoire of the wild chimpanzee. Anim Cogn 14:745–767
Hobaiter C, Byrne RW (2014) The meanings of chimpanzee gestures. Curr Biol 24:1596–1600
Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70
Illingworth RS (1955) Crying in Infants and Children. Br Med J 1:75–78
Kelleher JD, Mac Namee B, D’arcy A (2015) Fundamentals of machine learning for predictive data analytics: algorithms, worked examples, and case studies. MIT press, Cambridge
Levréro F, Mathevon N (2013) Vocal signature in wild infant chimpanzees. Am J Primatol 75:324–332
Libbrecht MW, Noble WS (2015) Machine learning applications in genetics and genomics. Nat Rev Genet 16:321–332
Lingle S, Riede T (2014) Deer mothers are sensitive to infant distress vocalizations of diverse mammalian species. Am Nat 184:510–522
Lingle S, Wyman MT, Kotrba R et al (2012) What makes a cry a cry? A review of infant distress vocalizations. Curr Zool 58:698–726
Logan B (2000) Mel frequency cepstral coefficients for music modeling. In: Ismir. pp 1–11
Lowe AE, Hobaiter C, Newton-Fisher NE (2019) Countering infanticide: chimpanzee mothers are sensitive to the relative risks posed by males on differing rank trajectories. Am J Phys Anthropol 168:3–9
Lowe AE, Hobaiter C, Asiimwe C et al (2020) Intra-community infanticide in wild, eastern chimpanzees: a 24-year review. Primates 61:69–82
MacLean PD (1985) Brain evolution relating to family, play, and the separation call. Arch Gen Psychiatry 42:405–417
May B, Moody DB, Stebbins WC (1989) Categorical perception of conspecific communication sounds by Japanese macaques, Macaca fuscata. J Acoust Soc Am 85:837–847. https://doi.org/10.1121/1.397555
Mielke A, Zuberbühler K (2013) A method for automated individual, species and call type recognition in free-ranging animals. Anim Behav 86:475–482
Mohri M, Rostamizadeh A, Talwalkar A (2018) Foundations of machine learning. MIT press, Cambridge
Müller E, Hollien H, Murry T (1974) Perceptual responses to infant crying: identification of cry types. J Child Lang 1:89–95
Newman JD (2007) Neural circuits underlying crying and cry responding in mammals. Behav Brain Res 182:155–165
Nithya B, Ilango V (2017) Predictive analytics in health care using machine learning tools and techniques. In: 2017 International Conference on Intelligent Computing and Control Systems (ICICCS). IEEE, pp 492–499
Olsson F (2009) A literature survey of active machine learning in the context of natural language processing
Plooij FX, Bygott D, Sackett GP (1984) The behavioral development of free-living chimpanzee babies and infants. Ablex Norwood, NJ
Porter FL, Miller RH, Marshall RE (1986) Neonatal pain cries: effect of circumcision on acoustic features and perceived urgency. Child Dev 57:790–802
Reynolds V (2005) The chimpanzees of the Budongo forest: Ecology, behaviour and conservation. OUP, Oxford
Riecken D (2000) Introduction: personalized views of personalization. Commun ACM 43:26–28
Saraswathy J, Hariharan M, Yaacob S, Khairunizam W (2012) Automatic classification of infant cry: A review. In: 2012 International Conference on Biomedical Engineering (ICoBE). pp 543–548
Schel AM, Townsend SW, Machanda Z et al (2013) Chimpanzee alarm call production meets key criteria for intentionality. PLoS ONE 8:e76674. https://doi.org/10.1371/journal.pone.0076674
Sebe N, Cohen I, Garg A, Huang TS (2005) Machine learning in computer vision. Springer, New York
Soltis J (2004) The signal functions of early infant crying. Behav Brain Sci 27:443–458
Tajiri Y, Yabuwaki R, Kitamura T, Abe S (2010) Feature extraction using support vector machines. In: International Conference on Neural Information Processing. Springer, pp 108–115
Townsend SW, Slocombe KE, Thompson ME, Zuberbühler K (2007) Female-led infanticide in wild chimpanzees. Curr Biol 17:R355–R356
Turesson HK, Ribeiro S, Pereira DR et al (2016) Machine learning algorithms for automatic classification of marmoset vocalizations. PLoS ONE 11:e0163041
Versteegh M, Kuhn J, Synnaeve G et al (2016) Classification and automatic transcription of primate calls. J Acoust Soc Am 140:26–30
Wasz-Höckert O, Partanen TJ, Vuorenkoski V et al (1964) The identification of some specific meanings in infant vocalization. Experientia 20:154–154
Watts DP, Mitani JC (2000) Infanticide and cannibalism by male chimpanzees at Ngogo, Kibale National Park, Uganda. Primates 41:357–365
Weary DM, Lawson GL, Thompson BK (1996) Sows show stronger responses to isolation calls of piglets associated with greater levels of piglet need. Anim Behav 52:1247–1253. https://doi.org/10.1006/anbe.1996.0272
Wiener SG, Bayart F, Faull KF, Levine S (1990) Behavioral and physiological responses to maternal separation in squirrel monkeys (Saimiri sciureus). Behav Neurosci 104:108
Wiesenfeld AR, Malatesta CZ, Deloach LL (1981) Differential parental response to familiar and unfamiliar infant distress signals. Infant Behav Dev 4:281–295
Wiltschko AB, Johnson MJ, Iurilli G et al (2015) Mapping sub-second structure in mouse behavior. Neuron 88:1121–1135
Zeskind PS, Sale J, Maio ML et al (1985) Adult perceptions of pain and hunger cries: a synchrony of arousal. Child Dev 56:549–554
Acknowledgments
We thank the Uganda Wildlife Authority (UWA) and the Uganda National Council for Science and Technology (UNCST) for permission to conduct the study, and Geoffrey Muhanguzi, Caroline Asiimwe, Sam Adue and Monday M’Botella for their support in the field. We are grateful to two anonymous Reviewers, the Editor and Bahar Tuncgenc for helpful comments on the manuscript.
Funding
We are grateful to the Royal Zoological Society of Scotland for providing core funding to the Budongo Conservation Field Station. This research was supported by funding from the European Union’s Seventh Framework Programme for research, technological development and demonstration (Grant agreement no 283871), a Fyssen Foundation post-doctoral fellowship awarded to GD, the Swiss National Science Foundation (PZ00P3_154741) and Start up-funding of the Taipei Medical University (108-6402-004-112) awarded to CDD.
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GD, KZ and MDR designed the research; GD collected the data; GD analysed the behavioural data; CDD implemented the acoustic extraction and the machine learning procedure; all Authors contributed to the writing of the manuscript.
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Dezecache, G., Zuberbühler, K., Davila-Ross, M. et al. A machine learning approach to infant distress calls and maternal behaviour of wild chimpanzees. Anim Cogn 24, 443–455 (2021). https://doi.org/10.1007/s10071-020-01437-5
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DOI: https://doi.org/10.1007/s10071-020-01437-5