Titi monkeys combine alarm calls to create probabilistic meaning

Berthet, Mélissa; Mesbahi, Geoffrey; Pajot, Aude; Cäsar, Cristiane; Neumann, Christof; Zuberbühler, Klaus

doi:10.1126/sciadv.aav3991

Cited by 30 publications

(39 citation statements)

References 30 publications

(54 reference statements)

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“…Then callers produced mixed sequences containing both A and B calls in combinatorial but non-permutational ways [43]. In subsequent playback experiments, it could be shown that sequences recorded under the four experimental conditions (aerial predator ground or canopy, terrestrial predator ground or canopy) elicited adequate behavioural responses (figure 4, [44]). One specific combinatorial feature, the proportion of B-call bigrams in the sequence, had a particularly strong impact on recipient responses, suggesting it served as a main carrier of meaning.…”

Section: (Iii) Combination Syntaxmentioning

confidence: 95%

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Syntax and compositionality in animal communication

Zuberbühler

2019

Phil. Trans. R. Soc. B

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Syntax has been found in animal communication but only humans appear to have generative, hierarchically structured syntax. How did syntax evolve? I discuss three theories of evolutionary transition from animal to human syntax: computational capacity, structural flexibility and event perception. The computation hypothesis is supported by artificial grammar experiments consistently showing that only humans can learn linear stimulus sequences with an underlying hierarchical structure, a possible by-product of computationally powerful large brains. The structural flexibility hypothesis is supported by evidence of meaning-bearing combinatorial and permutational signal sequences in animals, with sometimes compositional features, but no evidence for generativity or hierarchical structure. Again, animals may be constrained by computational limits in short-term memory but possibly also by limits in articulatory control and social cognition. The event categorization hypothesis, finally, posits that humans are cognitively predisposed to analyse natural events by assigning agency and assessing how agents impact on patients, a propensity that is reflected by the basic syntactic units in all languages. Whether animals perceive natural events in the same way is largely unknown, although event perception may provide the cognitive grounding for syntax evolution. This article is part of the theme issue ‘What can animal communication teach us about human language?’

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Section: (Iii) Combination Syntaxmentioning

confidence: 95%

“…Subjects looked more upwards when they were tested with sequences elicited by an aerial predator or by a predator in the canopy. Reproduced with permission from Berthet et al[44]. (Online version in colour.…”

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confidence: 99%

Syntax and compositionality in animal communication

Zuberbühler

2019

Phil. Trans. R. Soc. B

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“…For example, white-faced sakis (P. pithecia) respond to small terrestrial threats (small cats and some snakes) with alarm calls and mobbing behaviors but move lower in the canopy and remain motionless for long periods of time (i.e., "freezing") in response to large raptors (Buchanan, Mittermeier, & Roosmalen, 1981;Gleason & Norconk, 2002). In the only experimental study on pitheciids to date, black-fronted titi monkeys (Callicebus nigrifrons) have been shown to respond to terrestrial and aerial predator models with alarm call sequences that convey information about predator type and location in the forest matrix (Berthet et al, 2019;Cäsar, Byrne, Young, & Zuberbühler, 2012b;Cäsar, Zuberbühler, Young, & Byrne, 2013), and listeners can distinguish among conspecific alarm calls (Cäsar, Byrne, Hoppitt, et al, 2012a). Thus, pitheciid monkeys may exhibit anti-predator strategies adapted to the predator's hunting style and the level of perceived threat, but more systematic data are needed to assess the consistency of these responses across taxa.…”

Section: Introductionmentioning

confidence: 99%

Model vs. playback experiments: The impact of sensory mode on predator‐specific escape responses in saki monkeys

Adams

Kitchen

2020

Ethology

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Although experimentally simulating predator presence helps improve sample sizes in studies of free‐ranging animals, few studies have examined whether auditory playbacks and visual models produce similar results. Additionally, it is unclear if anti‐predator strategies are specific to predator hunting styles in understudied Neotropical pitheciid primates, limiting what we can generalize about this phenomenon across this taxonomic order. We conducted predator simulation experiments to assess whether wild Rylands' bald‐faced saki monkeys (Pithecia rylandsi) recognize predators based solely on acoustic cues, exhibit predator‐specific responses to different predator types, and vary responses to presentations in different sensory modes. In our playback experiments, sakis had weak responses to non‐predator control vocalizations compared to jaguar growls and harpy eagle shrieks. In most predator playbacks, subjects' first glance corresponded to the direction from which simulated predators would typically attack (above vs. below). However, although sakis exhibited appropriate movement responses to harpy playbacks (i.e., descending canopy), they exhibited no clear movement patterns when presented with jaguar playbacks. In contrast, jaguar model experiments consistently elicited fast approaches, mobbing‐style responses, and long alarm calling bouts. Thus, if we had relied on playbacks alone, we might have concluded that sakis have only generalized responses to terrestrial ambush predators. In fact, in all variables measured (e.g., latency, number of calls, and response duration), models of both predator species elicited stronger reactions than playbacks. Results indicate that bald‐faced sakis can identify predators based solely on vocalizations, but do not exhibit predator‐specific escape responses to terrestrial predators based on acoustic cues alone. The differential response to playbacks and models calls into question the reliability of using acoustic‐only stimuli to assess the specificity of anti‐predator behavior to predator hunting styles in some primate species.

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“…In particular, information about predatory threats and an individual's related level of arousal has been demonstrated to be reflected by changes in the number of repeated elements or the inter-element intervals [5,6]. A few primate species have furthermore been described to combine distinct call types into larger sequences, where the proportional distribution of calls and transitional probabilities among call types contain contextual information [7,8]. However, the precise mechanisms underlying how the information in these large sequences is conveyed are often less clear.…”

Section: Introductionmentioning

confidence: 99%

“…neighbours versus strangers [14]. In contrast, call combinations have been demonstrated to contain meaningful, context-specific information based on the temporal ordering of the units contained in longer sequences [3,7]. For example, bonobos (Pan paniscus) combine five acoustically graded call types into longer, mixed sequences containing information about the type of food encountered [8].…”

Section: Introductionmentioning

confidence: 99%

Call order within vocal sequences of meerkats contains temporary contextual and individual information

2020

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Background The ability to recombine smaller units to produce infinite structures of higher-order phrases is unique to human language, yet evidence of animals to combine multiple acoustic units into meaningful combinations increases constantly. Despite increasing evidence for meaningful call combinations across contexts, little attention has been paid to the potential role of temporal variation of call type composition in longer vocal sequences in conveying information about subtle changes in the environment or individual differences. Here, we investigated the composition and information content of sentinel call sequences in meerkats (Suricata suricatta). While being on sentinel guard, a coordinated vigilance behaviour, meerkats produce long sequences composed of six distinct sentinel call types and alarm calls. We analysed recordings of sentinels to test if the order of the call types is graded and whether they contain additional group-, individual-, age- or sex-specific vocal signatures. Results Our results confirmed that the six distinct types of sentinel calls in addition to alarm calls were produced in a highly graded way, likely referring to changes in the perceived predation risk. Transitions between call types one step up or down the a priory assumed gradation were over-represented, while transitions over two or three steps were significantly under-represented. Analysing sequence similarity within and between groups and individuals demonstrated that sequences composed of the most commonly emitted sentinel call types showed high within-individual consistency whereby adults and females had higher consistency scores than subadults and males respectively. Conclusions We present a novel type of combinatoriality where the order of the call types contains temporary contextual information, and also relates to the identity of the caller. By combining different call types in a graded way over long periods, meerkats constantly convey meaningful information about subtle changes in the external environment, while at the same time the temporal pattern of the distinct call types contains stable information about caller identity. Our study demonstrates how complex animal call sequences can be described by simple rules, in this case gradation across acoustically distinct, but functionally related call types, combined with individual-specific call patterns.

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Titi monkeys combine alarm calls to create probabilistic meaning

Cited by 30 publications

References 30 publications

Syntax and compositionality in animal communication

Syntax and compositionality in animal communication

Model vs. playback experiments: The impact of sensory mode on predator‐specific escape responses in saki monkeys

Call order within vocal sequences of meerkats contains temporary contextual and individual information

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