Elucidating how environmental and social constraints shape the evolution of communication and the ability to produce and perceive sensory signals bearing single or multiple information in both animals and humans is one of the most interesting challenges of modern science. Our team proposes a comparative and experimental view to tackle this question, developing an alliance between research on animal behavior in the field and investigations in the lab.
Our research goes along 5 axes: a phylogenetic axis with a comparative approach of communication systems throughout the vertebrate phylum (fish, crocodiles, birds and mammals); a developmental axis considering how the production and perception of sensory signals is modulated across the life span; a social complexity axis focusing on one hand on “simple” communication and social systems found in fish and crocodiles, and on the other hand on complex or highly complex ones in birds and mammals including Humans; a trans-disciplinary axis investigating processes from the brain to the behavioral level; and an applied axis where our approach is valued to assess the impacts of human activities on animals’ behavior and serves to propose wildlife management solutions that integrate the ethological dimension. The research activity of the ENES team has been focused on acoustic signals (bioacoustics) since many years, and now extends to other sensory channels (olfactory and visual).
Along our five axes, we develop the following eight specific research strands:
Strand 1: Human non-verbal vocalizations
The information encoded in human baby’s cries remains poorly understood, and the factors driving the perception of cries by adult listeners have not been thoroughly investigated. In collaboration with fMRI neuroscientists and pediatricians, we have started a long-term, multilevel (from behavior to brain) investigation centered on the coding (production) and decoding (perception) of this communicative signal. The ultimate question concerns the evolutionary processes that drive the structure and function of the crying signal of human babies, and the extent to which this signal and the response it triggers in caregivers have an adaptive value. Using dedicated sound analysis tools to compare the structure of cries of babies recorded in various conditions of stress, we have identified vocal ‘roughness’, a composite acoustic factor characterizing the level of aperiodicity of the cries, that differs between different levels of discomfort or pain. Besides, we showed that both mothers and fathers can reliably recognize their baby from their cries, and that the only crucial factor affecting this ability is the amount of time spent by the parent with their own baby (research published in Nature Communications). We investigated the consequences of sex stereotypes on adults’ perception of babies’ cries and found that the vocal dimorphism characterizing the voice of adult speakers (men are lower-pitched than women) is generalized by adult listeners to their perception of babies’ cries: low-pitched cries of 3-month old babies are more likely to be attributed to boys and high-pitched cries to girls by adult listeners, despite the absence of sex differences in pitch at this age. We are now expanding our research to other non-verbal vocalizations, aiming at exploring the functional significance of human voice variation.
Among animals living in social groups, individuals form communication networks essential to mediate their social interactions. We aim at deciphering the mechanisms by which the social fabric is maintained over the scale of an individual’s lifetime. We explored this question by studying the vocal communication of three non-human primates known for their complex social relationships (mandrill, gorilla, and bonobo) and a marine mammal demonstrating one of the most competitive breeding systems, the northern elephant seal. We found that mandrills and bonobos demonstrate some degree of vocal plasticity. Indeed, mandrills’ calls contain information about genetic relatedness and the degree of familiarity between individuals, and that individuals rely on these vocal signals to discriminate unknown kin from non-kin (results published in Nature Communications). We found a similar plasticity in bonobos and showed that these apes demonstrate vocal recognition of social partners, even if they have been separated for five years. We also showed that gorilla can follow primitive forms of conversational rules. Besides, we demonstrated that northern elephant seal males memorize and recognize the unique tempo and timbre of their rivals’ voices, and use this rhythmic information to individually identify competitors (results published in Current Biology). We are currently investigating the role of vocal signals in structuring the social network of bonobos, and how these signals interact with other communication channels, in particular olfaction. In the elephant seals, we are investigating both the acoustic interactions between mothers and pups, and the development of vocal behavior in males. We are also expanding this strand of research to polygynous deer, a group of mammals characterized by a unique diversity of vocal anatomies, vocal signals and social structures.
Acoustic communication and pair-bonding in birds. The coordination of behaviors between mates is a central aspect of the biology of monogamous pair bond and may rely on acoustic communication. Focusing on the zebra finch and using a multidisciplinary approach involving bioacoustics, behavioral biology, ecology, physiology and in-vivo electrophysiology, we investigated how acoustic communication participates in pair bond formation and maintenance, and what are the consequences of pair bonding on individual auditory perception and acoustic communication. We showed that bird mates use call exchanges at the nest to organize bi-parental care and adapt this calling behavior to maintain its efficiency during periods of increased background noise. We also found that vocal exchanges help maintaining the pair-bond in diverse situations. Remarkably, we demonstrated that the stress-induced calls of males provoke both behavioral and physiological changes in their female partner, providing the first evidence for emotional contagion in a songbird species.
Auditory scene analysis by a songbird. One of the most complex tasks performed by sensory systems is "scene analysis": the interpretation of complex signals as behaviorally relevant objects. The study of this problem, universal to species and sensory modalities, is particularly challenging in audition, where sounds from various sources and localizations, degraded by propagation through the environment, sum to form a single acoustical signal. We studied how the individual signature coded in the zebra finch long distance contact call degrades with propagation, and how the zebra finch brain integrates individual and distance information. We demonstrated that the individual signature of zebra finches’ calls is very resistant to propagation-induced degradation. Using operant conditioning experiments, we showed that female birds are experts at discriminating between the degraded vocal signatures of two males, and that they can improve their ability if they can train over increasing distances. Finally, we showed that this impressive discrimination ability also occurs at the neural level: we found a population of neurons in the avian auditory forebrain that discriminate individual voices with various degrees of propagation-induced degradation without prior familiarization or training (result published in J. Neuroscience).
Over the last two decades, a considerable number of studies have shown that the vocalisations of animals, and the nonverbal components of human speech, contain acoustic cues (including voice pitch and formant spacing) to a wide range of crucial physical or social attributes (e.g. body size, strength, dominance, attractiveness, etc) that are relevant to sexual and social interactions and ultimately affect reproductive success. However, very little research has investigated how and when these inter-individual differences arise in animal and human vocalisations, whether they are inherited, whether they remain stable throughout the lifespan, and whether they remain consistent across call types. We have started to investigate the early development of inter-individual differences in voice characteristics. Our first results indicate that inter-individual differences in pitch (F0) arise in the vocalisations of newborns, remain stable throughout development, and possibly into adulthood. We are currently pursuying our investigations on the early development of mammals’ voice characteristics, and will consider the possible interactions between the development of acoustic, olfactory and visual abilities, on both the production and reception sides.
The sensory world of crocodiles. The acoustic signals of crocodilians play a major role in the first stages of life. Indeed parental care, which is present in all crocodilians, relies strongly on acoustic interactions between mothers (sometimes fathers) and their young. In addition to guarding the nest, females help hatchlings to go out of the eggs, guard them against potential predators, and occasionally move the pod to new nursery areas. Our team has been investigating the communication processes that coordinate mother’s and juveniles’ behaviors for a decade. More recently, we identified embedded information about the emitter’s size in juvenile calls, and experimentally demonstrated that Nile crocodile mothers breeding in the wild are less receptive to the calls of larger juveniles. Using synthetized sounds, we further showed that female’s reaction depends on call pitch, an important cue bearing size information. Besides, we investigated how crocodiles deal with decision conflicts emerging from concurrent stimuli from different sensory channels. We found that inputs from one sensory modality (e.g. audition) may modulate the perception and behavioral reaction to another (e.g. olfaction). Being at the interface of air and water, crocodiles experience a peculiar situation since both environments strongly differ regarding their sound transmission properties. We are currently investigating how crocodiles cope with noise masking effect and accurately localize a sound source in their amphibious environment.
Multi-modal communication in fish. Communication is essential during social interactions including animal conflicts and it is often a complex process involving multiple sensory channels or modalities. How different sensory modalities interplay during agonistic interactions remains largely unknown in fish. To tackle this question, we studied the behavioral responses to both the composite multimodal signal and each unimodal component. We found that acoustic signals alone do not elicit agonistic behavioral response in our model, the cichlid fish Metriaclima zebra. Conversely, the visual perception of a competitor is sufficient to trigger males’ aggressiveness. However, sound stimuli modulate the intensity of aggressive response. We are currently investigating multi-modal communication (acoustic, olfaction, vision) in cichlids. In collaboration, we have also started a project aiming to compare acoustic communication in the two morphs of the fish Astyanax mexicanus: the normal, river-dwelling fish; and the blind, cave-adapted fish, hypothesizing that acoustic communication may have evolved in cavefish during adaptation to the subterranean environment, possibly as compensation for the lack of visual communication in the dark.
This strand explores how acoustic pollution modulates animal behavior and between-species interactions. Individual responses to noise are well documented but how they translate to higher integration levels and affect species coexistence and community stability remains unknown. Moreover, while the effects of noise have been largely scrutinized in terrestrial and marine organisms, our knowledge remains scarce on fresh waters. We intent to characterize the spatio-temporal features of anthropogenic noise in freshwater habitats (lakes) and test, under controlled conditions, the behavioral (organism level) and functional (interaction level) responses to noise using a theoretical framework that gathers approaches and concepts from ethology and community ecology. We focus on fish-invertebrate trophic links, and want to expand our investigations to more sophisticated interaction networks (food chains). In another line of research, we are working on the meagre, a fish of commercial interest, investigating its hearing physiology (evoked potentials) in noisy soundscapes. In the future, we will consider assessing the impact of olfactory noise (e.g., contaminants) on the perception of key odorants or odour mixtures represented as sensory objects.
In the context of increased societal awareness of the crucial importance of companion animals to human well-being, research on human-animal interactions has exploded in recent years. Yet, while we use verbal signals to communicate our intentions to train, manage or establish long-term bonds with other species, the extent of animals’ abilities to extract meaningful information from our vocal signals as well as our strategies to communicate information are poorly understood. Recently, we investigated pet-directed speech, a peculiar speaking pattern with higher pitch and slower tempo, similar to infant-directed speech which is known to engage infants’ attention (study published in Proc.R.Soc.B). We are currently investigating how we use our voices in a range of interactions with animals (e.g. dogs), making the assumption that the modulation of primary acoustic cues to size/dominance plays a central role in communicating affect, intent and direct attention.
Bioacoustics is an emergent and important tool used for monitoring animal populations and our team is more and more solicited by national and regional parks, as well as other organizations in charge of wildlife management (e.g. Office de la Chasse et de la Faune Sauvage). Considering that one of our missions as a public research team is to ensure the transfer of scientific knowledge, we have started to developing strong links with these organisations. Our primary aim is to develop wildlife management solutions that rely on bioacoustic methods. Our main project has revolved around the acoustic monitoring of populations of rock ptarmigans Lagopus muta (an endangered bird species) in the French Alps and the Pyreneans. The main challenge is to develop a portable solution allowing acoustic monitoring of territorial males and the monitoring of biodiversity dynamics. With the ultimate aim of calibrating a census tool using bioacoustic automatic recorders, we firstly assessed the individual variability of males’ calls, identifying acoustic features that allow a reliable discrimination between individuals. We then set up a triangulation method that takes into account the peculiar sound transmission constraints of mountainous areas. Beside its applied facet, this line of research brings first-hand data on acoustic communication networks in birds.