PhD opportunity

For Indonesian students only:

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PhD position

Impact of tourism on the interplay between social dynamics and vocal communication in crested Macaques

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Keywords: Bioacoustics, Communicative network, Social Network, Social Relationships, Primates. 

Duration: 3 years

Funding coverage: ENES Lab

Nationality: Indonesian

Required Academic background: Master thesis in biology; skills in field work and data analysis

Language: English

Expecting starting date: some flexibility between October 2026 and January 2027

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The proposed project aims to uncover the impact of tourism and human presence on the patterning of vocal exchange and the diversity and complexity of vocalisations in wild crested macaques (Macaca nigra) in North Sulawesi, Indonesia. It will be supervised by Prof Nicolas Mathevon and Dr Cedric Girard-Buttoz.

Ecotourism and human presence have noticeable, often deleterious, impacts on primate physiology1,2, activity budgets3,4, and ranging patterns3. Whether tourism also affects primate social behaviour and communication, two key aspects of their natural behaviour, however, remains largely overlooked.   

Communication, and in particular vocal communication, is a critical dimension of animal sociality, as it often serves as a mediating pathway triggering other social interactions5. In turn, as stated by the social complexity hypothesis for communicative complexity (SCHCC), the complexity of the group's social dynamics should affect the production pattern and the complexity of the signals6,7. Here, vocalisations are particularly important because they enable communication beyond the visual range and are exceptionally suited to coordinate action over long distances.

To date, the impact of tourism on primate vocal communication has principally been quantified via crude changes in calling rates8,9. To our knowledge, detailed analyses of how human presence alters fine-scale acoustic properties or group-wide vocal exchange patterns are entirely lacking. If anthropogenic pressures, such as tourism, alter group social dynamics, these changes should, as predicted by the SCHCC, manifest as shifts in vocal complexity. Assessing both parameters jointly is thus paramount for fully capturing the impact of tourism on animals' natural behaviour. Such an assessment will also help to develop effective tourism regulation plans.

This PhD project bridges this gap by investigating the impact of tourism on the interplay between social and vocal communication complexity in crested macaques. Crested macaques are among the most tolerant macaque species (grade 4 on a scale from 1-410,11) and exhibit a more complex, more flexible usage of calls12 but also of visual signals13 as compared to grade 1 macaque species. These findings are in line with the general prediction of the SCHCC that individuals in a tolerant social system, such as crested macaques, experience a high degree of social uncertainty due to the absence of strictly linear dominance hierarchies and fixed rules governing their social interactions that select for more fluid and possibly more complex communication systems.

By shifting the scientific lens from between-species comparisons to fine-scale between-group and between-individual dynamics, this project addresses two complementary axes:

• Axis 1 (Conservation-Oriented): Quantifying how varying levels of tourist pressure shape vocal communication across different social groups and within individuals over time.

• Axis 2 (Theory-Oriented): Utilising tourism as a pseudo-experiment that may disrupt natural sociality, allowing a direct test of the SCHCC by tracking the covariation between social dynamics and communicative complexity.

The study will be conducted on three wild groups of crested macaques in the Tangkoko Natural Reserve, North Sulawesi, Indonesia, that experience varying levels of anthropogenic pressure:

• Group 1 (N = 32 adults): high tourist pressure with daily visitors.

• Group 2 (N = 27 adults): moderate tourist pressure with occasional visitors.

• Group 3 (N = 28 adults): no tourist pressure.

This study will focus solely on adult individuals to eliminate developmental confounds. A PhD student will conduct 6-h (half-day) focal observations on a given individual, 5 days a week for 9 months. This will lead to 2340 h of focal recording in total (27 h per individual). During the focal observation, the student will record all vocalisation emitted by the focal subject as well as any vocalisation from other individuals ad-libitum when the caller's identity and the general context of the vocalisation can be established. In addition, the student will continuously record the focal individual's activity and all social interactions with any conspecifics. In tourist-exposed groups, the observer will precisely quantify the presence and impact of tourism (number of tourists, distance to the monkeys, and intrusive behaviours such as solicitation or food provisioning).

After the field period, the student will be hosted by the ENES Bioacoustics Lab (Centre de Recherche en Neuroscience de Lyon, CNRS, Inserm) in Saint-Etienne, France, to analyse the behavioural and vocal data. The ENES team is an internationally renowned group in bioacoustics that continually develops state-of-the-art acoustic analytical tools15–20 (articles in Current Biology, PNAS, Sc. Adv., Nature Com., etc). The ENES team’s qualitative impact is evident in its role as a major European training hub (International Master of Bioacoustics21, Bioacoustics Winter School22, Tropical Bioacoustics School23) and its influence on the field through open tools58,59. In addition to enabling in-depth acoustic analysis of the macaque’s vocalisation, the PhD student will find an exceptional environment for their training and networking in bioacoustics.

We will quantify key individual-level markers of social complexity, such as cooperation tendencies (e.g., rates of participation in coalitions24,25 and grooming26), tolerance levels (e.g., time spent co-feeding in proximity to a conspecific27,28), and differentiation of social relationships (quantified as the skew of the social bond strength across all partners29) – and model them against four core dimensions of vocal complexity:

1. Vocal repertoire size of single calls. We will use unsupervised machine learning approaches and clustering methods to re-evaluate the number of distinct call types in the vocal repertoire of crested macaques, building on a master’s thesis by M. Panggur, which described 12 different call types. We will investigate whether heavy tourism exposure results in changes in the number of stable acoustic clusters.

 

1. Degree of gradation between call types. Gradation between call types is an important component of vocal complexity12 because it allows flexibility in the message being conveyed30. We will use fuzzy clustering techniques31 to measure the degree of gradation between the single call types. While segmenting into call types is a usual way of analysing primate vocalisations, we will use specific signal analysis methods that allow us to measure continuous spectro-temporal features (e.g. Modulation Power Spectrum). To avoid forced discretisation, we will use unsupervised GMM models that provide “soft” probabilistic assignments, giving each vocalisation a membership probability to each note cluster. This statistical approach is well-suited to the continuous nature of animal vocalisations.

 

1. Structure and diversity of call sequences. Primates combine single calls into vocal sequences comprised of iterations of the same call type32 or of different call types15 to change the message being conveyed33,34. A larger repertoire of sequences thus allows for more nuanced social messaging. The diversity of these sequences will be assessed using a newly established Bayesian analytical framework developed by Cédric Girard-Buttoz in collaboration with Richard McElreath, allowing for the estimation of vocal sequence diversity for each individual while accounting for unbalanced sampling across individuals35. Beyond this global assessment, we will analyse in detail male loud calls, a vocal sequence composed of several call elements that function as a context-independent dominance signal and that vary in acoustic structure between males36. Since these calls serve long-distance communication, it is possible that macaques in the  groups more exposed to tourism modify the acoustic properties of their loud calls to adapt to anthropogenic noise, similar to how titi monkeys adjusted the acoustic properties of their vocalisations to mining noise37.   

 

1. Communication network: We will quantify individual communicative networks by tracking the recipients of soft directed calls and the timing of vocal exchanges (who replies to whom). These communicative networks will then be mapped onto the social networks. We will then quantify how tourism affects the social dynamics and the flow of acoustic information within the group.

Requirements and qualifications

The successful candidate will have a Master's degree in biology, psychology, anthropology, ecology or any related field. They should have previous fieldwork experience collecting behavioural or ecological data on wild mammals, preferably primates, or at least a strong interest in spending prolonged time in the field. They must be fully fluent in English to facilitate their integration into the ENES team. Theoretical and/or practical background in bioacoustics and ethology is a plus. The successful candidate should be dedicated to learning new analytical and computational tools, including AI tools for analysing vocalisations, and have a strong interest in computer / statistics coding.   

 

Contacts: If you are interested, please contact Prof Nicolas Mathevon (nicolas.mathevon@ephe.psl.eu) and Dr Cedric Girard-Buttoz (cedric.girard-buttoz@cnrs.fr).

 

References

1.         Maréchal, L. et al. Impacts of tourism on anxiety and physiological stress levels in wild male Barbary macaques. Biol. Conserv. 144, 2188–2193 (2011).

2.         Bertrand, D. A. et al. Effects of Tourist and Researcher Presence on Fecal Glucocorticoid Metabolite Levels in Wild, Habituated Sulawesi Crested Macaques (Macaca nigra). Animals 13, 2842 (2023).

3.         Badiella-Giménez, N., Kankam, B. & Badiella, L. Influence of visitors on the time budget, ranging and strata use of Lowe’s Monkey. Cercopithecus Lowei (2021).

4.         Rodríguez-Peña, O. N., Oropeza Sánchez, M. T. & González-Di Pierro, A. M. “Variable Effects of Tourist Presence on the Activity Budget of Alouatta pigra”. Trop. Conserv. Sci. 16, 19400829231188622 (2023).

5.         Laidre, M. E. & Johnstone, R. A. Animal signals. Curr. Biol. 23, R829–R833 (2013).

6.         Freeberg, T. M., Dunbar, R. I. M. & Ord, T. J. Social complexity as a proximate and ultimate factor in communicative complexity. Philos. Trans. R. Soc. B Biol. Sci. 367, 1785–1801 (2012).

7.         Peckre, L., Kappeler, P. M. & Fichtel, C. Clarifying and expanding the social complexity hypothesis for communicative complexity. Behav. Ecol. Sociobiol. 73, 11 (2019).

8.         Treves, A. & Brandon, K. Tourist impacts on the behavior of black howling monkeys (Alouatta pigra) at Lamanai, Belize. Commensalism Confl. Primate-Hum. Interface 146–167 (2005).

9.         Pérez-Galicia, S., Miranda-Anaya, M., Canales-Espinosa, D. & Muñoz-Delgado, J. Visitor effect on the behavior of a group of spider monkeys (Ateles geoffroyi) maintained at an island in Lake Catemaco, Veracruz/Mexico. Zoo Biol. 36, 360–366 (2017).

10.       Duboscq, J. et al. Social Tolerance in Wild Female Crested Macaques (Macaca nigra) in Tangkoko-Batuangus Nature Reserve, Sulawesi, Indonesia. Am. J. Primatol. 75, 361–375 (2013).

11.       Thierry, B. Unity in diversity: lessons from macaque societies. Evol. Anthropol. 16, 224–238 (2007).

12.       Rebout, N. et al. Tolerant and intolerant macaques show different levels of structural complexity in their vocal communication. Proc. R. Soc. B Biol. Sci. 287, 20200439 (2020).

13.       Maestripieri, D. Gestural communication in three species of macaques (Macaca mulatta, M. nemestrina, M. arctoides): Use of signals in relation to dominance and social context. Gesture 5, 57–73 (2005).

14.       Freeberg, T. M. Complexity in the Chick-a-Dee Call of Carolina Chickadees (Poecile Carolinensis): Associations of Context and Signaler Behavior to Call Structure. The Auk 125, 896–907 (2008).

15.       Girard-Buttoz, C. et al. Versatile use of chimpanzee call combinations promotes meaning expansion. Sci. Adv. 11, eadq2879 (2025).

16.       Perrier, L. et al. Ultrasonic signals support a large-scale communication landscape in wild mice. Curr. Biol. 35, 4837–4844 (2025).

17.       Massenet, M. et al. Puppy whines mediate maternal behavior in domestic dogs. Proc. Natl. Acad. Sci. 121, e2316818121 (2024).

18.       Thévenet, J. et al. Crocodile perception of distress in hominid baby cries. Proc. R. Soc. B Biol. Sci. 290, (2023).

19.       Thévenet, J., Grimault, N., Fonseca, P. & Mathevon, N. Voice-mediated interactions in a megaherbivore. Curr. Biol. 32, R70–R71 (2022).

20.       Garcia, M. et al. Evolution of communication signals and information during species radiation. Nat. Commun. 11, 4970 (2020).

21.       International Master of Bioacoustics. https://www.masterofbioacoustics.com/.

22.       Bioacoustics Winter School. ENES lab https://www.eneslab.com/bioacoustic-winter-school.

23.       Tropical Bioacoustics School. https://www.tropbioacschool.com.

24.       Surbeck, M. et al. Comparison of male conflict behavior in chimpanzees (Pan troglodytes) and bonobos (Pan paniscus), with specific regard to coalition and post-conflict behavior. Am. J. Primatol. 79, e22641 (2017).

25.       Nishida, T. & Hosaka, K. Coalition Strategies among Adult Male Chimpanzees of the Mahale Mountains, Tanzania. (1996).

26.       Girard-Buttoz, C. et al. Variable use of polyadic grooming and its effect on access to social partners in wild chimpanzees and bonobos. Anim. Behav. 168, 211–224 (2020).

27.       Senar, J. C., Camerino, M. & Metcalfe, N. B. Familiarity Breeds Tolerance: the Development of Social Stability in Flocking Siskins (Carduelis spinus). Ethology 85, 13–24 (1990).

28.       Dale, R., Range, F., Stott, L., Kotrschal, K. & Marshall-Pescini, S. The influence of social relationship on food tolerance in wolves and dogs. Behav. Ecol. Sociobiol. 71, 107 (2017).

29.       Surbeck Martin et al. Sex-specific association patterns in bonobos and chimpanzees reflect species differences in cooperation. R. Soc. Open Sci. 4, 161081 (2017).

30.       Lemasson, A. & Hausberger, M. Acoustic variability and social significance of calls in female Campbell’s monkeys (Cercopithecus campbelli campbelli). J. Acoust. Soc. Am. 129, 3341–3352 (2011).

31.       Fischer, J., Wadewitz, P. & Hammerschmidt, K. Structural variability and communicative complexity in acoustic communication. Anim. Behav. 134, 229–237 (2017).

32.       Le Floch, A. et al. Call combination order and iterations may shift meaning in sooty mangabey vocal sequences. BMC Biol. https://doi.org/10.1186/s12915-026-02528-4 (2026) doi:10.1186/s12915-026-02528-4.

33.       Suzuki, T. N. & Zuberbühler, K. Animal syntax. Curr. Biol. 29, R669–R671 (2019).

34.       Engesser, S. & Townsend, S. W. Combinatoriality in the vocal systems of nonhuman animals. WIREs Cogn. Sci. 10, e1493 (2019).

35.       Sigmundson, R. et al. Vocal sequence diversity and length remain stable across ontogeny in a catarrhine monkey (Cercocebus atys). Commun. Biol. 8, 1–13 (2025).

36.       Neumann, C., Assahad, G., Hammerschmidt, K., Perwitasari-Farajallah, D. & Engelhardt, A. Loud calls in male crested macaques, Macaca nigra: a signal of dominance in a tolerant species. Anim. Behav. 79, 187–193 (2010).

37.       Duarte, M. H. L., Kaizer, M. C., Young, R. J., Rodrigues, M. & Sousa-Lima, R. S. Mining noise affects loud call structures and emission patterns of wild black-fronted titi monkeys. Primates 59, 89–97 (2018).