De Gregorio, Chiara

Gamba, Marco

Giacoma, Cristina

Longondraza, Miaretsoa

Torti, Valeria

Valente, Daria

Zanoli, Anna

English

DE GREGORIO, Chiara

Miaretsoa, L.

Institutional Research Information System University of Turin

07 January 2022AperTO - Archivio Istituzionale Open Access dell'Università di TorinoOriginal Citation:SEXUAL DIMORPHIC CHORUSING IN THE WILD INDRISPublisher:Published version:DOI:10.17617/2.3190925Terms of use:Open Access(Article begins on next page)Anyone can freely access the full text of works made available as "Open Access". Works made available under aCreative Commons license can be used according to the terms and conditions of said license. Use of all other worksrequires consent of the right holder (author or publisher) if not exempted from copyright protection by the applicable law.Availability:Ravignani A., Barbieri C., Flaherty M., Jadoul Y., Lattenkamp E., Little A., Martins M., Mudd K., Verhoef T.This is the author's manuscriptThis version is available http://hdl.handle.net/2318/1736938 since 2020-12-22T11:03:39Z   SEXUAL DIMORPHIC CHORUSING IN THE WILD INDRIS VALERIA TORTI1, DARIA VALENTE1, CHIARA DE GREGORIO1, ANNA ZANOLI1, LONGONDRAZA MIARETSOA1, CRISTINA GIACOMA1, MARCO GAMBA1. *Corresponding Author: valeria.torti@unito.it 1Life Sciences and Systems Biology, University of Torino, Torino, Italy   Animals can produce vocal rhythms in an interactive, coordinated manner (Couzin 2018). Comparing structural, spectral and temporal features across species (Fitch 2000) may help in reconstructing the evolutionary history of human speech (Ravignani and Norton 2017). Singing primates (Geissmann, 2000), which produce elaborated and complex sequences of vocalizations, are of particular interest for this topic. Similarly to humans, indris (Indri indri) assemble simple units into more complex structures to convey different information. Individuals react differently to different songs, confirming the presence of functionally referential communication systems (Clark et al. 2006). Indris are the only singing lemurs and emit songs whose most distinctive portions are “descending phrases”, made of 2-5 units. Mated indris have been reported to sing in pairs, to enhance pair-bonding and defend their territories (Pollock, 1986; Torti et al., 2013; Bonadonna et al., 2017). Songs may have the form of a chorus whenever the subadult members of the groups also utter their contribution in a precise and coordinated manner (Torti et al., 2018). Indri songs exhibit turn-taking between individuals of different sexes and a variable degree of overlap between group members (Gamba et al., 2016). Songs have various functions depending on the context in which are emitted (Torti et al., 2013), and they are used for both inter and intra-group communication. We recorded spontaneous vocalizations of 8 groups of indris at the Maromizaha New Protected Area (18°56′S, 48°27′E), from 2008 to 2018. Focal animal sampling (Altmann, 1974) allowed the attribution of each vocal profile to a signaler. To investigate the timing and rhythm of songs, we measured the amount of co-singing between different individual contributions (percentage of overlap;    Gamba et al. 2014) and the inter onset intervals (IOIs, duration between the starting points of two successive notes in the same song; Gamba et al. 2016) of adjacent units (Sasahara et al., 2015). We extracted the pitch contour and labeled each unit using the phrase in which it was emitted and the sex of the emitter. We then calculated the similarity across different individual songs using the Levenshtein distance. Finally, we classified song units in phrases through DTW and clustering analyses (Gamba et al. 2018). Our results show that: a) indris can synchronize their utterances showing non-random overlap between singers, with an overlapping rate of the pair contributions that changes according to the number of singers in the chorus; b) both dominant and non-dominant indris can coordinate their calls and there is evidence for an ability of precise timing during song emission; c) indri songs show the presence of sex dimorphism, both in the overall timing and repertoire size than in the unit and phrase structure, with females being more flexible than males in their contributions, and d) the structure of phrases possess individually distinctive characteristics. In line with previous findings (De Gregorio et al., 2018), we observed that indris within a group coordinate on average more than 70% of their contributions suggesting that duetting is indeed associated with pair cohesion, as a proxy of the strength of the pair bond (Geissmann & Orgeldinger, 2000). The most consistent portion of the song, made of ascending or descending sequences of units, shows reliable timing and pitch variation, a crucial feature of birdsong and human speech (Levinson & Holler, 2014). We found support for our prediction that the phrase structure of songs varied between reproductive males and females. The presence of pitch sex dimorphism in nonhuman primate vocal signals is rare and is identified as a prerequisite in the evolution of human perceptual abilities (Patel, 2010). It appears that indri male’s song has a more fixed pattern, whereas females could adjust their contribution, in agreement with findings on the white-cheeked gibbons N. leucogenys (Deputte, 1982), on baboons and Japanese macaques (Lemasson et al., 2011; Lemasson et al., 2016). Our results also show that strong individuality is encoded in the indris’ phrases, thus the potential to provide conspecifics with emitter’s identity cues. Studies on rhythm and synchrony in primates have historically been focused on anthropoid species (Ravignani, 2019), with poor investigation on prosimian vocal behavior. Our study suggests that the indris are a good model for further investigations of the evolution of human speech features, because of the turn-taking between individuals and the variable degree of overlap, commonly identified as traits of modern human communication.    References Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227–267. Arnold K., & Zuberbühler K. (2006). Language evolution: semantic combinations in primate calls. Nature, 18, 441(7091):303. Bonadonna G., Torti V., Sorrentino V., Randrianarison R.M., Zaccagno M., Gamba M., Tan C.L., Giacoma C. (2017). Territory exclusivity and intergroup encounters in Indri indri upon methodological tuning. The European Zoological Journal, 84(1), 238-251. Couzin I.D. (2018). Synchronization: The Key to Effective Communication in Animal Collectives. Trends in Cognitive Sciences, 22(10), 844-846. De Gregorio C., Zanoli A., Valente D., TortiV., Bonadonna G., Randrianarison R.M., Giacoma C., Gamba M. (2018). Female indris determine the rhythmic structure of the song and sustain a higher cost when the chorus size increases. Current Zoology, zoy058. Deputte, B. (1982). Duetting in male and female songs of the white-checked gibbon (Hylobates con-color leucogenys). In C.T. Snowdon, C.H. Brown, & M. Peterses (Eds.), Primate Communication (pp. 67-93). Cambridge Univ. Press, Cambridge. Fitch W.T. (2000). The Evolution of Speech: A Comparative Review. Trends in Cognitive Sciences , 4(7), 258–267. Gamba M., Torti V., Estienne V., Randrianarison R.M., Valente D., Rovara P., Bonadonna G., Friard O., Giacoma C. (2016). The Indris Have Got Rhythm! Timing and Pitch Variation of a Primate Song Examined between Sexes and Age Classes. Frontiers in Neuroscience, 10: 249.  Gamba M., Torti V., Valente D., De Gregorio C., Friard O., Giacoma C. (2018). Primate songs and their relevance in the study of language evolution. In C. Cuskley, M. Flaherty, L. McCrohon, H. Little, A. Ravignani, T. Verhoef, The Evolution of Language. Proceedings of the 12th International Conference on the Evolution of Language (Evolang12) (pp.134-136). Evolang 12 Organizing Committee. Geissmann, T. (2000). Gibbon songs and human music from an evolutionary perspective. In N. Wallin, B. Merker and S. Brown (Eds.), The origins of music (pp. 103-123). Cambridge, MA: MIT Press. Geissmann T., & Orgeldinger, M. (2000). The relationship between duet songs and pair bonds in siamangs, Hylobates syndactylus. Animal Behaviour, 60(6), 805-809. Lemasson, A., Ouattara , K., Petit, E.J., & Zuberbühler, K., (2011).  Social learning of vocal structure in a nonhuman primate? BMC Evolutionary Biology, 11:362.   Lemasson, A., Jubin, R., Masataka, N.,  & Arlet, M. (2016). Copying hierarchical leaders’ voices? Acoustic plasticity in female Japanese macaques. Scientific Reports, 6:21289.    Levinson S.C., & Holler, J. (2014). The origin of human multi-modal communication. Philosophical Transactions of The Royal Society B Biological Sciences, 369(1651). Marler, P. (2000). Origins of music and speech: Insights from animals. In N. Wallin, B. Merker and S. Brown (Eds.), The Origins of Music (pp. 31– 48). Cambridge, MA: MIT Press. Patel, A.D. (2010). Music, biological evolution, and the brain. In M. Bailar (Eds.), Emerging Disciplines (pp. 91-144). Houston, TX: Rice UP. Pollock, J.I. (1986). The song of the Indris (Indri indri; Primates: Lemuroidea): natural history, form and function. International Journal of Primatology, 7, 225-267. Ravignani A., Norton P. (2017). Measuring rhythmic complexity: A primer to quantify and compare temporal structure in speech, movement, and animal vocalizations. Journal of Language Evolution, 2(1), 4-19. Ravignani, A. (2019). Rhythm and synchrony in animal movement and communication. Current Zoology, 65(1), 77–81. Sasahara, K., Tchernichovski, O., Takahasi, M., Suzuki, K., and Okanoya, K. (2015). A rhythm landscape approach to the developmental dynamics of birdsong. Journal of the Royal Society Interface, 12:20150802. Torti V., Gamba M., Rabemananjara Z.H., Giacoma C. (2013). The song of the indris: contextual variation in the long distance calls of a lemur. Italian Journal of Zoology, 80(4), 596-607. Torti V., Valente D., De Gregorio C., Comazzi C., Miaretsoa L., Ratsimbazafy J., Giacoma C., Gamba M. (2018). Call and be counted! Can we reliably estimate the number of callers in the indri's (Indri indri) song? PLoS ONE, 13(8).    

SEXUAL DIMORPHIC CHORUSING IN THE WILD INDRIS

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SEXUAL DIMORPHIC CHORUSING IN THE WILD INDRIS

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