Acquisition of predator knowledge from alarm calls via one-trial social learning in monkeys

León, Julián; Thiriau, Constance; Bodin, Clémentine; Crockford, Catherine; Zuberbühler, Klaus

doi:10.1016/j.isci.2022.104853

Cited by 7 publications

(5 citation statements)

References 39 publications

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“…Presumably, this was the result of a pruning mechanism by which juveniles learned to ignore irrelevant species . Social learning plays a key role (León et al 2022) but how exactly infants and juveniles obtain the relevant information from others is largely unknown. One key step in successful social learning when learning alarm call is to select appropriate models, i.e., individuals that are competent and reliable.…”

Section: Introductionmentioning

confidence: 99%

Juvenile vervet monkeys rely on others when responding to danger

et al. 2023

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Primate alarm calls are mainly hardwired but individuals need to adapt their calling behaviours according to the situation. Such learning necessitates recognising locally relevant dangers and may take place via their own experience or by observing others. To investigate monkeys alarm calling behaviour, we carried out a field experiment in which we exposed juvenile vervet monkeys to unfamiliar raptor models in the presence of audiences that differed in experience and reliability. We used audience age as a proxy for experience and relatedness as a proxy for reliability, while quantifying audience reactions to the models. We found a negative correlation between alarm call production and callers’ age. Adults never alarm called, compared to juveniles. We found no overall effect of audience composition and size, with juveniles calling more when with siblings than mothers or unrelated individuals. Finally, concerning audience reactions to the models, we observed juveniles remained silent with vigilant mothers and only alarm called with ignoring mothers, whereas we observed the opposite for siblings: juveniles remained silent with ignoring siblings and called with vigilant siblings. Despite the small sample size, juvenile vervet monkeys, confronted with unfamiliar and potentially dangerous raptors, seem to rely on others to decide whether to alarm call, demonstrating that the choice of the model may play an important key role in the ontogeny of primate alarm call behaviour.

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Section: Introductionmentioning

confidence: 99%

Juvenile vervet monkeys rely on others when responding to danger

et al. 2023

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“…Our results show that the development of alarm call comprehension, usage and production in mangabeys occurs during juvenile stage, which may be simultaneously refined by observing other individuals and through individual experience. In a recent study, we found that mangabeys can acquire predator knowledge from alarm calls by one-trial social learning (León et al 2022 ). Rapid individual learning and flexibility in alarm call usage have been also demonstrated in adult West African green monkeys when exposed to a novel threat, i.e., a remotely operated drone (Wegdell et al 2019 ).…”

Section: Discussionmentioning

confidence: 98%

“…After a few such exposures, the sound of the drone was already sufficient for subjects to respond appropriately, i.e., by immediately scanning the sky and running for cover. Two further studies involving potentially dangerous terrestrial threats have also provided evidence for rapid, one-trial social learning in monkeys (Deshpande et al 2022 ; León et al 2022 ). There is also evidence for more gradual learning, mainly supported by older observational studies (Castro and Snowdon 2000 : Saguinus oedipus ; Fichtel 2008 : Propithecus verreauxi verreauxi ; Fischer et al 2000 : Papio cynocephalus ursinus ; McCowan et al 2001 : Saimiri sciureus ; Ramakrishnan and Coss 2000 : Macaca radiata ), although it is often unknown what sorts of experiences individuals have had throughout their early lives.…”

Section: Introductionmentioning

confidence: 99%

Comprehension of own and other species’ alarm calls in sooty mangabey vocal development

León

Thiriau

Hobaiter

et al. 2023

Behav Ecol Sociobiol

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Primates understand the meaning of their own and other species’ alarm calls, but little is known about how they acquire such knowledge. Here, we combined direct behavioural observations with playback experiments to investigate two key processes underlying vocal development: comprehension and usage. Especifically, we studied the development of con- and heterospecific alarm call recognition in free-ranging sooty mangabeys, Cercocebus atys, across three age groups: young juveniles (1–2y), old juveniles (3–4y) and adults (> 5y). We observed that, during natural predator encounters, juveniles alarm called to a significantly wider range of species than adults, with evidence of refinement during the first four years of life. In the experiments, we exposed subjects to leopard, eagle and snake alarm calls given by other group members or sympatric Diana monkeys. We found that young juveniles’ locomotor and vocal responses were least appropriate and that they engaged in more social referencing (look at adults when hearing an alarm call) than older individuals, suggesting that vocal competence is obtained via social learning. In conclusion, our results suggest that alarm call comprehension is socially learned during the juvenile stage, with comprehension preceding appropriate usage but no difference between learning their own or other species’ alarm calls. Significance statement Under natural conditions, animals do not just interact with members of their own species, but usually operate in a network of associated species. However, ontogenetic research on primate communication frequently ignores this significant element. We studied the development of con- and heterospecific alarm call recognition in wild sooty mangabeys. We found that communicative competence was acquired during the juvenile stages, with alarm call comprehension learning preceding appropriate vocal usage and with no clear difference in learning of con- and heterospecific signals. We also found that, during early stages of life, social referencing, a proactive form of social learning, was key in the acquisition of competent alarm call behaviour. Our results show that primates equally learn to interpret alarm calls from their own and other species during their early stages of life and that this learning process is refined as the animals mature.

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“…visually) they may transmit this information through other modalities to their conspecifics (e.g. through acoustic or haptic signals and cues) ( Arnold et al, 2008 ; León et al, 2022 ). More generally, further integration of empirical and modelling work ( Harpaz et al, 2021 ) is needed to understand how the sensory capacities of different species shape their groups’ spatial structure and collective responses to the environment, and vice versa.…”

Section: The Concept Of ‘A Sensory Collective’mentioning

confidence: 99%

Sensory collectives in natural systems

Williams,

Sridhar,

Hurme

et al. 2023

eLife

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Groups of animals inhabit vastly different sensory worlds, or umwelten, which shape fundamental aspects of their behaviour. Yet the sensory ecology of species is rarely incorporated into the emerging field of collective behaviour, which studies the movements, population-level behaviours, and emergent properties of animal groups. Here, we review the contributions of sensory ecology and collective behaviour to understanding how animals move and interact within the context of their social and physical environments. Our goal is to advance and bridge these two areas of inquiry and highlight the potential for their creative integration. To achieve this goal, we organise our review around the following themes: (1) identifying the promise of integrating collective behaviour and sensory ecology; (2) defining and exploring the concept of a ‘sensory collective’; (3) considering the potential for sensory collectives to shape the evolution of sensory systems; (4) exploring examples from diverse taxa to illustrate neural circuits involved in sensing and collective behaviour; and (5) suggesting the need for creative conceptual and methodological advances to quantify ‘sensescapes’. In the final section, (6) applications to biological conservation, we argue that these topics are timely, given the ongoing anthropogenic changes to sensory stimuli (e.g. via light, sound, and chemical pollution) which are anticipated to impact animal collectives and group-level behaviour and, in turn, ecosystem composition and function. Our synthesis seeks to provide a forward-looking perspective on how sensory ecologists and collective behaviourists can both learn from and inspire one another to advance our understanding of animal behaviour, ecology, adaptation, and evolution.

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Acquisition of predator knowledge from alarm calls via one-trial social learning in monkeys

Cited by 7 publications

References 39 publications

Juvenile vervet monkeys rely on others when responding to danger

Juvenile vervet monkeys rely on others when responding to danger

Comprehension of own and other species’ alarm calls in sooty mangabey vocal development

Sensory collectives in natural systems

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