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Zuberbühler, Klaus

Nom
Zuberbühler, Klaus
Affiliation principale
Fonction
Professeur ordinaire
Email
klaus.zuberbuehler@unine.ch
Identifiants
https://libra.unine.ch/handle/123456789/670
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0000-0001-8378-088X

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  • Publication
    Restriction temporaire
    Rethinking the evolution of vocal complexity: structured call sequences in olive colobus monkeys
    (Neuchâtel : Université de Neuchâtel, 2025)
    Gallot, Quentin 
    ;
    Zuberbühler, Klaus 
    Selon la théorie actuelle, les systèmes de communication complexes émergent principalement en réponse à deux pressions de sélection, soit sociale, soit écologique. La première, que l'on peut appeler “l'hypothèse de la complexité sociale”, postule que la communication complexe émerge principalement chez des espèces ayant des structures sociales complexes qui nécessitent une coordination et une négociation fréquentes entre individus d’un même groupe. La seconde, que l'on peut nommer “l'hypothèse de la complexité écologique”, suggère que les pressions environnementales, particulièrement la prédation, favorisent l’émergence d’une communication complexe. Ces deux hypothèses ont été testées principalement chez des espèces hautement sociales vivant en grands groupes avec une organisation complexe telle que la dynamique de fission-fusion, laissant des lacunes significatives dans notre compréhension de l'évolution de la complexité dans les systèmes de communication d’espèces formant de petits groupes cohésifs. Plusieurs espèces avec des structures sociales relativement simples et une pression de prédation faible présentent néanmoins des systèmes de communication remarquablement complexes. Les displays élaborés de chants chez les gibbons, par exemple, soulèvent des questions quant à savoir si ces deux cadres théoriques expliquent de manière exhaustive l'ensemble des phénomènes observés, et suggèrent que des forces sélectives supplémentaires pourraient influencer l'évolution vers des systèmes de communication complexes. Les colobes olive constituent un modèle idéal pour approfondir cette problématique. Contrairement à de nombreux primates, les colobes olive sont une espèce hautement cryptique, ils manifestent très peu de comportements affiliatifs ou agonistiques et vivent en petits groupes, des facteurs traditionnellement associés à des systèmes de communication simples. En étudiant empiriquement la communication vocale de cette espèce dans une forêt tropicale d'Afrique de l'Ouest, cette thèse vise à mieux comprendre la relation évolutive entre la communication des primates et les pressions sélectives conduisant à leur complexification. Pour aborder cette question, j'ai d'abord exploré le répertoire vocal des colobes olive. Conformément aux prédictions des hypothèses de complexité sociale et écologique, j'ai trouvé un système de communication très limité composé de seulement deux types de cris. Cependant, j'ai également découvert un système combinatoire étonnamment riche dans lequel les deux types de cris étaient assemblés en séquences structurées syntaxiquement, pour faire référence à différents dangers (aigles, léopards et chutes d'arbres). Le contenu de cette étude est publié sous Gallot et al. (2024). Dans une deuxième étude complémentaire, j'ai examiné si et comment les différentes séquences de cris permettaient aux auditeurs de faire des prédictions sur les référents à l’origine des cris d’alerte. En utilisant des concepts de la théorie de l'information, divergence de Kullback-Leibler et analyses de gain de prédiction, j'ai identifié une grammaire simple permettant un traitement incrémental. Plus précisément, les cris initiaux dans les séquences discriminaient de façon fiable les menaces urgentes des non-urgentes, tandis que les positions ultérieures augmentaient la spécificité référentielle concernant les principaux types de prédateurs, aigles, léopards, et autres dangers. Ces résultats, publiés dans Gallot et al. (2025), ont fourni la preuve que la communication des primates non-humains est structurée d’une manière permettant un traitement prédictif de l’information, ce qui a des implications sur le fonctionnement du cerveau des primates en général et, par extension, sur les origines évolutives du langage. Dans une troisième étude, j'ai examiné la relation entre socialité et complexité vocale à travers une gamme plus large de contextes, y compris des situations non dangereuses. Ici, des données observationnelles ont été recueillies auprès d'un groupe de colobes olive semi-habitué. J'ai pu documenter que ces singes produisaient aussi, et de manière extensive, des séquences vocales en dehors des contextes de prédation, malgré leur mode de vie généralement cryptique. J'ai ensuite comparé les séquences vocales produites dans ces situations non dangereuses avec le précédent jeu de données expérimentales collectées en réponse à différents dangers. J'ai trouvé une complexité syntaxique plus grande dans les situations non dangereuses par rapport aux événements dangereux et un effet spatial prononcé. La complexité syntaxique était spécifiquement plus élevée en périphérie du domaine vital par rapport à son centre, vraisemblablement parce que les émetteurs des séquences de cris tentaient de communiquer avec des membres absents de leur groupe (lors de visites de courte durée dans des groupes voisins). J'ai pu en conclure que "l'hypothèse de la complexité sociale" nécessite des modifications, dans le sens où la complexité d’un système de communication vocal peut émerger non seulement pour réguler et coordonner les interactions sociales à courte distance, mais aussi pour maintenir un réseau social sur de longues distances. En conclusion, ces résultats démontrent qu'une communication vocale complexe, basée sur la production de séquences de cris, peut évoluer chez des espèces ayant des structures sociales simples et un faible risque de prédation, remettant en question les vues traditionnelles sur la relation entre socialité et communication. Bien que les colobes olive ne possèdent qu'un répertoire vocal très limité, ils sont capables de créer des séquences structurées syntaxiquement pouvant transmettre des informations spécifiques sur de longues distances. Ce type de communication est adapté non seulement pour référer aux prédateurs et autres dangers, mais aussi pour maintenir le contact entre des membres du groupe spatialement dispersés. Avec ces résultats, j'espère contribuer à une compréhension plus large des diverses voies évolutives vers la complexité dans la communication animale et à approfondir notre compréhension de la façon dont certaines variables sociales agissent comme pressions de sélection. ABSTRACT According to current theory, complex communication systems mostly evolve in response to two major selection pressures rooted in either social or ecological challenges. The first one, which may be called the ‘social complexity ypothesis’, posits that sophisticated communication emerges primarily in species with intricate social structures that require frequent coordination and negotiation among group members. The second one, which may be termed the ‘ecological complexity hypothesis’, suggests that environmental pressures, particularly predation, drive the evolution of complex signalling. The two hypotheses have predominantly been tested in highly social species living in big groups with complex group organisation such as fission-fusion dynamics, leaving significant gaps in our understanding of how communication complexity evolves in species with small cohesive groups. Several species with relatively simple social structures and minimal predation pressure nevertheless exhibit remarkably complex communication systems. The elaborate song displays of gibbons, for instance, raises the questions of whether these two theoretical frameworks comprehensively explain the full range of observed phenomena, and suggests that additional selective forces may be influencing the evolution of communicative complexity in ways not fully captured by current models. Olive colobus monkeys provide an ideal model species to further investigate the problem. Unlike many primates, olive colobus monkeys are a highly cryptic species but they also show very little affiliative or agonistic behaviours and live in small group sizes—factors traditionally associated with simple communication systems. By empirically investigating the vocal communication system of this species in a West African rainforest, this thesis aims to better understand the evolutionary relationship between primate communication and the selective pressures driving their complexification. To address this, I first explored the vocal repertoire of olive colobus monkeys. In line with predictions from the social and ecological complexity hypotheses, I found a limited communication system consisting of only two call types. However, I also discovered an unexpectedly rich combinatorial system in which the two call types were assembled into syntactically structured sequences to refer to different dangers—eagles, leopards and falling trees. The content of this study is published as Gallot et al. (2024). In a second follow-up study, I examined whether and how the different call sequences allowed listeners to make predictions about the call-eliciting referents. Using concepts from information theory—Kullback-Leibler divergence and prediction gain analyses—I identified a simple grammar capable of incremental processing. Specifically, sequence-initial positions reliably discriminated urgent from non-urgent threats, while subsequent positions increased the referential specificity regarding the main predator types—eagles, leopards—and other non-predatory disturbances. These results, published in Gallot et al. (2025), provided evidence that non-human primate communication is structured in ways that make it adapted for predictive processing, which has some implications about how primate brains operate and, by extension, the early evolutionary roots of language. In a third study, I investigated the relationship between sociality and vocal complexity across a wider range of contexts, including non-dangerous situations. Here, observational data were collected from one semi-habituated olive colobus group. I was able to document that the monkeys also made extensive use of vocal sequences outside predation contexts, despite their generally cryptic lifestyle. I then compared the vocal sequences produced in these non-threatening situations with the previous experimental dataset collected in response to different dangers. I found greater syntactic complexity in non-dangerous situations compared to dangerous events and a pronounced spatial effect. Syntactic complexity was specifically greater in the home range periphery compared to the centre, presumably because callers were trying to communicate with absent group members on short-term visits to neighbouring groups. I discussed these patterns by concluding that the ‘social complexity hypothesis’ may require modifications, in the sense that complexity evolves not only for regulating and coordinating close-range social interactions but also for maintaining social networks over long distances. In conclusion, these findings demonstrate that complex and especially sequence-based vocal communication can evolve in species with seemingly simple social structures and low predation risk, challenging traditional views on the relationship between sociality and communication. Although olive colobus monkeys only possess a limited vocal repertoire, they are able to create syntactically structured sequences capable of conveying specific information over long distances. This type of communication is adapted not only to refer to predators and other dangers, but also to maintain contact between spatially dispersed group members. With these results I hope to contribute to a broader understanding of the diverse evolutionary pathways towards complexity in animal communication and to further our comprehension of how social variables act as selection pressures.
  • Publication
    Accès libre
    Predator-deterring alarm call sequences in Guereza colobus monkeys are meaningful to conspecifics
    (2010)
    Schel, Anne Marijke
    ;
    Candiottia, Agnès
    ;
    Zuberbühler, Klaus 
    Guereza colobus monkeys, Colobus guereza, produce acoustically conspicuous vocalizations, the roars, in response to their main predators, leopards, Panthera pardus, and crowned eagles, Stephanoaetus coronatus. Roaring alarm utterances generally consist of the same basic call types but differ in overall structural composition. Leopards trigger roaring alarms containing many roaring sequences of only a few calls each, while eagles trigger few sequences with many calls each. To investigate whether conspecifics extract meaning from these structural differences, we played back leopard and eagle alarm call sequences and compared the monkeys’ responses in terms of their locomotor, gaze and vocal behaviour with their responses to the corresponding predator vocalizations. Locomotor responses did not differ between playback conditions; movement was always towards the simulated caller with no clear patterns in the vertical plane. Gaze direction, however, was highly predator specific. When hearing leopard-related stimuli, monkeys were significantly more likely to scan the area beneath them than when hearing eagle-related stimuli, which caused more scanning above. Vocal response rates to conspecific alarms were generally low but comparable with rates to the corresponding predators. If monkeys called, however, they produced the matching call sequences. Overall, our results showed that Guerezas discriminated between predator alarm call sequences produced by unfamiliar conspecifics and responded to them in predator-specific ways. Since the sequences were composed of the same basic call types, we concluded that the monkeys attended to the compositional aspects of these utterances.
  • Publication
    Accès libre
    Responses to leopards are independent of experience in Guereza colobus monkeys
    (2009)
    Schel, Anne Marijke
    ;
    Zuberbühler, Klaus 
    How primates learn to recognise the predatory species from their animate world is a largely unresolved problem. We conducted predator encounter experiments with wild Guereza colobus monkeys of the Sonso area of Budongo Forest, Uganda. The monkeys are hunted by crowned eagles and chimpanzees, but not leopards, which have been locally extinct for decades. Despite their unfamiliarity with this predator, monkeys reliably produced appropriate anti-predator behaviour to leopards, which was indistinguishable from that of a neighbouring population, where leopards are present. In both populations, monkeys produced the same vocal responses and predator-specific alarm calls, although leopard-naïve monkeys were more inclined to approach when hearing a leopard than monkeys that were familiar with this predator. Control experiments showed that the monkeys’ response pattern was not due to the effects of unfamiliarity or conspicuousness of the experimental stimuli. Natural selection appears to have endowed these primates with a cognitive capacity to recognise direct signs of leopard presence as inherently dangerous requiring specific anti-predator responses.
  • Publication
    Accès libre
    The alarm call system of female Campbell's monkeys
    (2009)
    Ouattara, Karim
    ;
    Zuberbühler, Klaus 
    ;
    N'Goran, Koffi J.-N
    ;
    Gombert, Jean-Emile
    Field studies on male forest guenon alarm-calling behaviour have revealed a number of intricacies about how these primates use vocalizations to protect themselves from predation. In these species, the vocal behaviour of adult females is often different from that of the males, but little systematic work has been done. Here, we describe the alarm call system of female Campbell's monkeys, Cercopithecus campbelli, in their natural forest habitat in western Ivory Coast. We found that in response to disturbing events, females produced three basic alarm call types, ‘wak-oos’, ‘hoks’ and acoustically variable ‘trill’ calls, consisting of repeated and rapidly ascending (RRA) pulses, which varied systematically in the temporal and frequency domains. Using observational and experimental data we were able to demonstrate that the RRA calls consisted of four acoustic variants, which could be associated with specific contexts, allowing listeners to draw inferences about the type of disturbance experienced by the caller. We also compared the alarm call behaviour of free-ranging individuals with published results from captivity. As predicted, captive individuals failed to produce predator-specific alarm calls, but they also produced an RRA variant in response to humans that was absent in the wild. We discuss the relevance of these findings in terms of their broader potential impact on evolutionary theories of primate communication.
  • Publication
    Accès libre
    Campbell's monkeys concatenate vocalizations into context-specific call sequences
    (2009)
    Ouattara, Karim
    ;
    Lemasson, Alban
    ;
    Zuberbühler, Klaus 
    Primate vocal behavior is often considered irrelevant in modeling human language evolution, mainly because of the caller's limited vocal control and apparent lack of intentional signaling. Here, we present the results of a long-term study on Campbell's monkeys, which has revealed an unrivaled degree of vocal complexity. Adult males produced six different loud call types, which they combined into various sequences in highly context-specific ways. We found stereotyped sequences that were strongly associated with cohesion and travel, falling trees, neighboring groups, nonpredatory animals, unspecific predatory threat, and specific predator classes. Within the responses to predators, we found that crowned eagles triggered four and leopards three different sequences, depending on how the caller learned about their presence. Callers followed a number of principles when concatenating sequences, such as nonrandom transition probabilities of call types, addition of specific calls into an existing sequence to form a different one, or recombination of two sequences to form a third one. We conclude that these primates have overcome some of the constraints of limited vocal control by combinatorial organization. As the different sequences were so tightly linked to specific external events, the Campbell's monkey call system may be the most complex example of ‘proto-syntax’ in animal communication known to date.
  • Publication
    Accès libre
    Male blue monkeys alarm call in response to danger experienced by others
    (2008)
    Papworth, Sarah
    ;
    Böse, Anne-Sophie
    ;
    Barker, Jessica
    ;
    Schel, Anne Marijke
    ;
    Zuberbühler, Klaus 
    Male blue monkeys (Cercopithecus mitis stuhlmanni) of Budongo Forest, Uganda, produce two acoustically distinct alarm calls: hacks to crowned eagles (Stephanoaetus coronatus) and pyows to leopards (Panthera pardus) and a range of other disturbances. In playback experiments, males responded to leopard growls exclusively with a series of pyows and to eagle shrieks predominantly with hacks. Responses to playbacks of these alarm call series matched the responses to the corresponding predators, suggesting that the calls conveyed something about the nature of the threat. When responding to a series of hacks, indicating an eagle, males responded predominately with hacks, but produced significantly more calls if their group members were close to the playback stimulus than far away, regardless of their own position. When responding to a series of pyows, indicating a range of disturbances, males responded with pyows, but call rates were independent of the distance of other group members. The results suggest that males took into account the degree of danger experienced by other group members.
  • Publication
    Accès libre
    Leopard predation and primate evolution
    (2002)
    Zuberbühler, Klaus 
    ;
    Jenny, David
    Although predation is an important driving force of natural selection its effects on primate evolution are still not well understood, mainly because little is known about the hunting behaviour of the primates' various predators. Here, we present data on the hunting behaviour of the leopard (Panthera pardus), a major primate predator in the Tai"forest of Ivory Coast and elsewhere. Radio-tracking data showed that forest leopards primarily hunt for monkeys on the ground during the day. Faecal analyses confirmed that primates accounted for a large proportion of the leopards' diet and revealed in detail the predation pressure exerted on the eight different monkey and one chimpanzee species. We related the species-specific predation rates to various morphological, behavioural and demographic traits that are usually considered adaptations to predation (body size, group size, group composition, reproductive behaviour, and use of forest strata). Leopard predation was most reliably associated with density, suggesting that leopards hunt primates according to abundance. Contrary to predictions, leopard predation rates were not negatively, but positively, related to body size, group size and the number of males per group, suggesting that predation by leopards did not drive the evolution of these traits in the predicted way. We discuss these findings in light of some recent experimental data and suggest that the principal effect of leopard predation has been on primates' cognitive evolution.
  • Publication
    Accès libre
    The functional significance of Diana monkey 'clear' calls
    (2001)
    Uster, Dana
    ;
    Zuberbühler, Klaus 
    In their natural West African rainforest habitat, Diana monkeys continuously produce high rates of a close-range clear-sounding call, but the function of this behaviour is unknown. In other primate species, close-range calls are typically given in socially relevant situations, for example, to gain access to grooming partners or food. Quite contrarily, we tested a number of hypotheses and found that Diana monkey 'clear' calls primarily function to avoid predation. Call rates were significantly elevated when predation threat was high, for instance when the visibility was poor, when the group spread was large, when the group was not associated with other monkey species. or after alarm calls. Call rates were not significantly elevated, however, in circumstances of high social competition, for instance when the group spread was small, during resting phases, while feeding oil clumped food sources, or when foraging in the periphery where inter-group encounters were more likely to occur. Calling was contagious in that calls typically elicited vocal responses from out-of-sight group members within a few seconds. Because of this, callers can effectively monitor a much larger area than is visually accessible to single individuals, suggesting that Diana monkey clear calls act as an essential element in a mutualistic system of co-ordinated vigilance.
  • Publication
    Accès libre
    Interspecies semantic communication in two forest primates
    (2000)
    Zuberbühler, Klaus 
    West African Diana monkeys (Cercopithecus diana) and Campbell's monkeys (Cercopithecus campbelli) frequently form mixed-species associations. Males of both species produce acoustically distinct alarm calls to crowned eagles (Stephanoaetus coronalus) and leopards (Panthera pardus), two of their main predators. Field playback experiments were conducted to investigate whether Diana monkeys respond to Campbell's alarm calls and whether they understand the calls' semantic content. Diana monkeys responded to playback of Campbell's leopard or eagle alarm calls as though the original predator were present. In a second experiment, Diana monkeys were primed with either Campbell's eagle or leopard alarm calls and then subsequently probed with the vocalizations of a crowned eagle or a leopard. Results showed that monkeys used the semantic information conveyed by the Campbell's alarm calls to predict the presence of a predator. The data are consistent with the hypothesis that non-human primates are able to use acoustic signals of diverse origin as labels for underlying mental representations.