Crocodile perception of distress in hominid baby cries.

It is generally argued that distress vocalizations, a common modality for alerting conspecifics across a wide range of terrestrial vertebrates, share acoustic features that allow heterospecific communication. Yet studies suggest that the acoustic traits used to decode distress may vary between species, leading to decoding errors. Here we found through playback experiments that Nile crocodiles are attracted to infant hominid cries (bonobo, chimpanzee and human), and that the intensity of crocodile response depends critically on a set of specific acoustic features (mainly deterministic chaos, harmonicity and spectral prominences). Our results suggest that crocodiles are sensitive to the degree of distress encoded in the vocalizations of phylogenetically very distant vertebrates. A comparison of these results with those obtained with human subjects confronted with the same stimuli further indicates that crocodiles and humans use different acoustic criteria to assess the distress encoded in infant cries. Interestingly, the acoustic features driving crocodile reaction are likely to be more reliable markers of distress than those used by humans. These results highlight that the acoustic features encoding information in vertebrate sound signals are not necessarily identical across species.

Improving the workflow to crack Small, Unbalanced, Noisy, but Genuine (SUNG) datasets in bioacoustics: The case of bonobo calls.

Despite the accumulation of data and studies, deciphering animal vocal communication remains challenging. In most cases, researchers must deal with the sparse recordings composing Small, Unbalanced, Noisy, but Genuine (SUNG) datasets. SUNG datasets are characterized by a limited number of recordings, most often noisy, and unbalanced in number between the individuals or categories of vocalizations. SUNG datasets therefore offer a valuable but inevitably distorted vision of communication systems. Adopting the best practices in their analysis is essential to effectively extract the available information and draw reliable conclusions. Here we show that the most recent advances in machine learning applied to a SUNG dataset succeed in unraveling the complex vocal repertoire of the bonobo, and we propose a workflow that can be effective with other animal species. We implement acoustic parameterization in three feature spaces and run a Supervised Uniform Manifold Approximation and Projection (S-UMAP) to evaluate how call types and individual signatures cluster in the bonobo acoustic space. We then implement three classification algorithms (Support Vector Machine, xgboost, neural networks) and their combination to explore the structure and variability of bonobo calls, as well as the robustness of the individual signature they encode. We underscore how classification performance is affected by the feature set and identify the most informative features. In addition, we highlight the need to address data leakage in the evaluation of classification performance to avoid misleading interpretations. Our results lead to identifying several practical approaches that are generalizable to any other animal communication system. To improve the reliability and replicability of vocal communication studies with SUNG datasets, we thus recommend: i) comparing several acoustic parameterizations; ii) visualizing the dataset with supervised UMAP to examine the species acoustic space; iii) adopting Support Vector Machines as the baseline classification approach; iv) explicitly evaluating data leakage and possibly implementing a mitigation strategy.

Social pressure drives "conversational rules" in great apes.

In the last decade, two hypotheses, one on the evolution of animal vocal communication in general and the other on the origins of human language, have gained ground. The first hypothesis argues that the complexity of communication co-evolved with the complexity of sociality. Species forming larger groups with complex social networks have more elaborate vocal repertoires. The second hypothesis posits that the core of communication is represented not only by what can be expressed by an isolated caller, but also by the way that vocal interactions are structured, language being above all a social act. Primitive forms of conversational rules based on a vocal turn-taking principle are thought to exist in primates. To support and bring together these hypotheses, more comparative studies of socially diverse species at different levels of the primate phylogeny are needed. However, the majority of available studies focus on monkeys, primates that are distant from the human lineage. Great apes represent excellent candidates for such comparative studies because of their phylogenetic proximity to humans and their varied social lives. We propose that studying vocal turn-taking in apes could address several major gaps regarding the social relevance of vocal turn-taking and the evolutionary trajectory of this behaviour among anthropoids. Indeed, how the social structure of a species may influence the vocal interaction patterns observed among group members remains an open question. We gathered data from the literature as well as original unpublished data (where absent in the literature) on four great ape species: chimpanzees Pan troglodytes, bonobos Pan paniscus, western lowland gorillas Gorilla gorilla gorilla and Bornean orang-utans Pongo pygmaeus. We found no clear-cut relationship between classical social complexity metrics (e.g. number of group members, interaction rates) and vocal complexity parameters (e.g. repertoire size, call rates). Nevertheless, the nature of the society (i.e. group composition, diversity and valence of social bonds) and the type of vocal interaction patterns (isolated calling, call overlap, turn-taking-based vocal exchanges) do appear to be related. Isolated calling is the main vocal pattern found in the species with the smallest social networks (orang-utan), while the other species show vocal interactions that are structured according to temporal rules. A high proportion of overlapping vocalisations is found in the most competitive species (chimpanzee), while vocal turn-taking predominates in more tolerant bonobos and gorillas. Also, preferentially interacting individuals and call types used to interact are not randomly distributed. Vocal overlap ('chorusing') and vocal exchange ('conversing') appear as possible social strategies used to advertise/strengthen social bonds. Our analyses highlight that: (i) vocal turn-taking is also observed in non-human great apes, revealing universal rules for conversing that may be deeply rooted in the primate lineage; (ii) vocal interaction patterns match the species' social lifestyle; (iii) although limited to four species here, adopting a targeted comparative approach could help to identify the multiple and subtle factors underlying social and vocal complexity. We believe that vocal interaction patterns form the basis of a promising field of investigation that may ultimately improve our understanding of the socially driven evolution of communication.

Foraging postures are a potential communicative signal in female bonobos.

Body postures are essential in animal behavioural repertoires and their communicative role has been assessed in a wide array of taxa and contexts. Some body postures function as amplifiers, a class of signals that increase the detection likelihood of other signals. While foraging on the ground, bonobos (Pan paniscus) can adopt different crouching postures exposing more or less of their genital area. To our knowledge, their potential functional role in the sociosexual life of bonobos has not been assessed yet. Here we show, by analysing more than 2,400 foraging events in 21 captive bonobos, that mature females adopt a rear-exposing posture (forelimb-crouch) and do so significantly more often when their anogenital region is swollen than during the non-swollen phase. In contrast, mature males almost completely avoid this posture. Moreover, this strong difference results from a diverging ontogeny between males and females since immature males and females adopt the forelimb-crouch at similar frequencies. Our findings suggest that the forelimb-crouch posture may play a communicative role of amplification by enhancing the visibility of female sexual swellings, a conspicuous signal that is very attractive for both males and females. Given the high social relevance of this sexual signal, our study emphasizes that postural signalling in primates probably deserves more attention, even outside of reproductive contexts.

Breaking conversational rules matters to captive gorillas: A playback experiment.

Across human cultures, conversations are regulated by temporal and social rules. The universality of conversational rules suggests possible biological bases and encourages comparisons with the communicative interactions of nonhuman animals. Unexpectedly, few studies have focused on other great apes despite evidence of proto-conversational rules in monkeys, thus preventing researchers from drawing conclusions on potential evolutionary origins of this behaviour. A previous study showed however that western lowland gorillas engage in soft call interactions that seem temporally- and socially-ruled. Indeed, interactions occurred mainly between individuals close in age who followed a preset response delay, thus preventing call overlap. Here, we experimentally investigated the presence of these rules in a captive gorilla group, using a violation-of-expectation paradigm. Head orientation responses suggest that the respect of response delay matters to subjects, but the importance of the interlocutors' age proximity appeared less clear. The intensity of the response varied with subjects' age in a context-dependent way, supporting a possible role of learning. Our findings support the growing number of studies highlighting the importance of vocal turn-taking in animals and a possible sociogenesis of this ability. The capacity to "converse" might have been a key step in the co-evolution of communication and complex sociality.

Baby cry recognition is independent of motherhood but improved by experience and exposure.

Neurobiological changes affecting new mothers are known to support the development of the mother-infant relationship (the 'maternal brain'). However, which aspects of parenting are actually mother-specific and which rely on general cognitive abilities remains debated. For example, refuting earlier findings, a recent study demonstrated that fathers identify their own baby from their cries just as well as mothers. Here we show that this performance is independent not only of sex, but also of parenthood status. We found that mothers' ability to recognize their newborn from their cries increased rapidly within few days postpartum, with highly multiparous mothers performing better. However, both male and female non-parents could similarly recognize an assigned baby, even after a very short exposure. As in mothers, both the initial amount of experimental exposure to the baby's cries (learning opportunity) and prior experience of caring for infants (auditory expertise) affected participants' performance. We thus suggest that, rather than being female-specific or motherhood-dependent, the ability to recognize a baby from their cries derives from general auditory and learning skills. By being available to non-parents of both sexes, it may contribute to the caregiving flexibility required for efficient cooperative breeding in humans.

Disease avoidance, and breeding group age and size condition the dispersal patterns of western lowland gorilla females.

Social dispersal is an important feature of population dynamics. When female mammals occur in polygynous groups, their dispersal decisions are conditioned by various female-, male-, and group-related factors. Among them, the influence of disease often remains difficult to assess. To address this challenge, we used long-term monitoring data from two gorilla populations (Gorilla gorilla gorilla) affected by infectious skin disease lesions. After controlling for other potentially influential factors, we investigated to which extent disease avoidance drives the dispersal decisions of gorilla females. We showed that the infection of a silverback of a breeding group by the skin disease increased the probability of adult females to emigrate. Moreover, adult females avoided breeding groups with a high prevalence of skin disease by emigrating from them and immigrating into healthier ones. Age of the breeding group was also an important factor. Adult females left older groups, near the end of a male tenure, to join younger ones led by younger fully grown silverbacks that could be of high reproductive and protective value. Our study highlights that, although females select for high-quality males, disease avoidance is a critical driver of their dispersion decision.

Social bonding drives vocal exchanges in Bonobos.

The origin of human speech is still a hotly debated topic in science. Evidence of socially-guided acoustic flexibility and proto-conversational rules has been found in several monkey species, but is lacking in social and cooperative great apes. Here we investigated spontaneous vocal interactions within a peaceful context in captive bonobos to reveal that vocal interactions obey temporally and social rules. Dyadic vocal interactions were characterized by call overlap avoidance and short inter-call intervals. Bonobos preferentially responded to conspecifics with whom they maintained close bonds. We also found that vocal sharing rate (production rate of shared acoustic variants within each given dyad) was mostly explained by the age difference of callers, as other individual characteristics (sex, kinship) and social parameters (affinity in spatial proximity and in vocal interactions) were not. Our results show that great apes spontaneously display primitive conversation rules guided by social bonds. The demonstration that such coordinated vocal interactions are shared between monkeys, apes and humans fills a significant gap in our knowledge of vocal communication within the primate phylogeny and highlights the universal feature of social influence in vocal interactions.

The pitch of babies' cries predicts their voice pitch at age 5.

Voice pitch (fundamental frequency, F0) is a key dimension of our voice that varies between sexes after puberty, and also among individuals of the same sex both before and after puberty. While a recent longitudinal study indicates that inter-individual differences in voice pitch remain stable in men during adulthood and may even be determined before puberty (Fouquet et al. 2016 R. Soc. open sci.3, 160395. (doi:10.1098/rsos.160395)), whether these differences emerge in infancy remains unknown. Here, using a longitudinal study design, we investigate the hypothesis that inter-individual differences in F0 are already present in the cries of pre-verbal babies. While based on a small sample (n = 15), our results indicate that the F0 of babies' cries at 4 months of age may predict the F0 of their speech utterances at 5 years of age, explaining 41% of the inter-individual variance in voice pitch at that age in our sample. We also found that the right-hand ratio of the length of their index to ring finger (2D : 4D digit ratio), which has been proposed to constitute an index of prenatal testosterone exposure, was positively correlated with F0 at both 4 months and 5 years of age. These findings suggest that a substantial proportion of between-individual differences in voice pitch, which convey important biosocial information about speakers, may partly originate in utero and thus already be present soon after birth.

Social basis of vocal interactions in western lowland gorillas (Gorilla g. gorilla).

Authors have raised the possibility of identifying primitive forms of conversational rules in monkeys: temporally ruled vocal interactions, call overlap avoidance, and socially based calling partner preferences. The question as to how these abilities have evolved in the primate lineage remains open to debate, particularly because studies based on apes are scarce and controversial. We studied a captive group of western lowland gorillas and tested the influence of caller characteristics and the type of bond between calling partners on vocal behavior based on the following: age, dominance, spatial proximity, sociopositive contact, and gaze. Four calling patterns that are call type dependent were identified: vocal interaction with and (more frequently) without call overlap, isolated calling, and repeated calling. Adult calls and grunts (contact calls) were predominant during vocal interactions, and the "response" delay was most often around half a second. The frequency of grunt dyadic exchanges was found to be linked to spatial proximity, gaze exchanges, and age proximity between calling partners. The dominance rank of callers determined the rate of contribution to these exchanges. These results show that some apes use rule-governed call exchanges and that these socially guided vocal interactions are more widespread than previously believed. (PsycINFO Database Record

Using demographic characteristics of populations to detect spatial fragmentation following suspected ebola outbreaks in great apes.

OBJECTIVES: Demographic crashes due to emerging diseases can contribute to population fragmentation and increase extinction risk of small populations. Ebola outbreaks in 2002-2004 are suspected to have caused a decline of more than 80% in some Western lowland gorilla (Gorilla gorilla gorilla) populations. We investigated whether demographic indicators of this event allowed for the detection of spatial fragmentation in gorilla populations. MATERIALS AND METHODS: We collected demographic data from two neighbouring populations: the Lokoué population, suspected to have been affected by an Ebola outbreak (followed from 2001 to 2014), and the Romani population, of unknown demographic status before Ebola outbreaks (followed from 2005 to 2014). RESULTS: Ten years after the outbreak, the Lokoué population is slowly recovering and the short-term demographic indicators of a population crash were no longer detectable. The Lokoué population has not experienced any additional demographic perturbation over the past decade. The Romani population did not show any of the demographic indicators of a population crash over the past decade. Its demographic structure remained similar to that of unaffected populations. DISCUSSION: Our results highlighted that the Ebola disease could contribute to fragmentation of gorilla populations due to the spatially heterogeneous impact of its outbreaks. The demographic structure of populations (i.e., age-sex and group structure) can be useful indicators of a possible occurrence of recent Ebola outbreaks in populations without known history, and may be more broadly used in other emerging disease/species systems. Longitudinal data are critical to our understanding of the impact of emerging diseases on wild populations and their conservation.

Sex stereotypes influence adults' perception of babies' cries.

BACKGROUND: Despite widespread evidence that gender stereotypes influence human parental behavior, their potential effects on adults' perception of babies' cries have been overlooked. In particular, whether adult listeners overgeneralize the sex dimorphism that characterizes the voice of adult speakers (men are lower-pitched than women) to their perception of babies' cries has not been investigated. METHODS: We used playback experiments combining natural and re-synthesised cries of 3 month-old babies to investigate whether the interindividual variation in the fundamental frequency (pitch) of cries affected adult listeners' identification of the baby's sex, their perception the baby's femininity and masculinity, and whether these biases interacted with their perception of the level of discomfort expressed by the cry. RESULTS: We show that low-pitched cries are more likely to be attributed to boys and high-pitched cries to girls, despite the absence of sex differences in pitch. Moreover, low-pitched boys are perceived as more masculine and high-pitched girls are perceived as more feminine. Finally, adult men rate relatively low-pitched cries as expressing more discomfort when presented as belonging to boys than to girls. CONCLUSION: Such biases in caregivers' responses to babies' cries may have implications on children's immediate welfare and on the development of their gender identity.

Enduring voice recognition in bonobos.

Long-term social recognition is vital for species with complex social networks, where familiar individuals can encounter one another after long periods of separation. For non-human primates who live in dense forest environments, visual access to one another is often limited, and recognition of social partners over distances largely depends on vocal communication. Vocal recognition after years of separation has never been reported in any great ape species, despite their complex societies and advanced social intelligence. Here we show that bonobos, Pan paniscus, demonstrate reliable vocal recognition of social partners, even if they have been separated for five years. We experimentally tested bonobos' responses to the calls of previous group members that had been transferred between captive groups. Despite long separations, subjects responded more intensely to familiar voices than to calls from unknown individuals - the first experimental evidence that bonobos can identify individuals utilising vocalisations even years after their last encounter. Our study also suggests that bonobos may cease to discriminate between familiar and unfamiliar individuals after a period of eight years, indicating that voice representations or interest could be limited in time in this species.

How Ebola impacts social dynamics in gorillas: a multistate modelling approach.

Emerging infectious diseases can induce rapid changes in population dynamics and threaten population persistence. In socially structured populations, the transfers of individuals between social units, for example, from breeding groups to non-breeding groups, shape population dynamics. We suggest that diseases may affect these crucial transfers. We aimed to determine how disturbance by an emerging disease affects demographic rates of gorillas, especially transfer rates within populations and immigration rates into populations. We compared social dynamics and key demographic parameters in a gorilla population affected by Ebola using a long-term observation data set including pre-, during and post-outbreak periods. We also studied a population of undetermined epidemiological status in order to assess whether this population was affected by the disease. We developed a multistate model that can handle transition between social units while optimizing the number of states. During the Ebola outbreak, social dynamics displayed increased transfers from a breeding to a non-breeding status for both males and females. Six years after the outbreak, demographic and most of social dynamics parameters had returned to their initial rates, suggesting a certain resilience in the response to disruption. The formation of breeding groups increased just after Ebola, indicating that environmental conditions were still attractive. However, population recovery was likely delayed because compensatory immigration was probably impeded by the potential impact of Ebola in the surrounding areas. The population of undetermined epidemiological status behaved similarly to the other population before Ebola. Our results highlight the need to integrate social dynamics in host-population demographic models to better understand the role of social structure in the sensitivity and the response to disease disturbances.

Fathers are just as good as mothers at recognizing the cries of their baby.

Previous investigations of parents' abilities to recognize the cries of their own babies have identified substantial and significant sex differences, with mothers showing greater correct recognition rates than fathers. Such sex differences in parenting abilities are common in non-human mammals and usually attributed to differential evolutionary pressures on male and female parental investment. However, in humans the traditional concept of 'maternal instinct' has received little empirical support and is incongruous given our evolutionary past as cooperative breeders. Here we use a controlled experimental design to show that both fathers and mothers can reliably and equally recognize their own 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. These results highlight the importance of exposure and learning in the development of this ability, which may rely on shared auditory and cognitive abilities rather than sex-specific innate predispositions.

Vocal signature in wild infant chimpanzees.

A large array of communication signals supports the fission/fusion social organization in chimpanzees, and among them the acoustic channel plays a large part because of their forest habitat. Adult vocalizations convey social and ecological information to their recipients allowing them to obtain cues about an ongoing event from calls only. In contrast to adult vocalizations, information encoded in infant calls had been hardly investigated. Studies mainly focused on vocal development. The present article aims at assessing the acoustic cues that support individual identity coding in infant chimpanzees. By analyzing recordings performed in the wild from seven 3-year-old infant chimpanzees, we showed that their calls support a well-defined individual vocal signature relying on spectral cues. To assess the reliability of the signature across the calls of an individual, we defined two subsets of recordings on the basis of the characteristics of the frequency modulation (whimpers and screams) and showed that both call types present a reliable vocal signature. Early vocal signature may allow the mother and other individuals in the group to identify the infant caller when visual contact is broken. Chimpanzee mothers may have developed abilities to cope with changing vocal signatures while their infant, still vulnerable, gains in independence in close habitat.

Recovery potential of a western lowland gorilla population following a major Ebola outbreak: results from a ten year study.

Investigating the recovery capacity of wildlife populations following demographic crashes is of great interest to ecologists and conservationists. Opportunities to study these aspects are rare due to the difficulty of monitoring populations both before and after a demographic crash. Ebola outbreaks in central Africa have killed up to 95% of the individuals in affected western lowland gorilla (Gorilla gorilla gorilla) populations. Assessing whether and how fast affected populations recover is essential for the conservation of this critically endangered taxon. The gorilla population visiting Lokoué forest clearing, Odzala-Kokoua National Park, Republic of the Congo, has been monitored before, two years after and six years after Ebola affected it in 2004. This allowed us to describe Ebola's short-term and long-term impacts on the structure of the population. The size of the population, which included around 380 gorillas before the Ebola outbreak, dropped to less than 40 individuals after the outbreak. It then remained stable for six years after the outbreak. However, the demographic structure of this small population has significantly changed. Although several solitary males have disappeared, the immigration of adult females, the formation of new breeding groups, and several birth events suggest that the population is showing potential to recover. During the outbreak, surviving adult and subadult females joined old solitary silverbacks. Those females were subsequently observed joining young silverbacks, forming new breeding groups where they later gave birth. Interestingly, some females were observed joining silverbacks that were unlikely to have sired their infant, but no infanticide was observed. The consequences of the Ebola outbreak on the population structure were different two years and six years after the outbreak. Therefore, our results could be used as demographic indicators to detect and date outbreaks that have happened in other, non-monitored gorilla populations.

Investigations on anopheline mosquitoes close to the nest sites of chimpanzees subject to malaria infection in Ugandan highlands.

BACKGROUND: Malaria parasites (Plasmodium sp.), including new species, have recently been discovered as low grade mixed infections in three wild chimpanzees (Pan troglodytes schweinfurthii) sampled randomly in Kibale National Park, Uganda. This suggested a high prevalence of malaria infection in this community. The clinical course of malaria in chimpanzees and the species of the vectors that transmit their parasites are not known. The fact that these apes display a specific behaviour in which they consume plant parts of low nutritional value but that contain compounds with anti-malarial properties suggests that the apes health might be affected by the parasite. The avoidance of the night-biting anopheline mosquitoes is another potential behavioural adaptation that would lead to a decrease in the number of infectious bites and consequently malaria. METHODS: Mosquitoes were collected over two years using suction-light traps and yeast-generated CO(2) traps at the nesting and the feeding sites of two chimpanzee communities in Kibale National Park. The species of the female Anopheles caught were then determined and the presence of Plasmodium was sought in these insects by PCR amplification. RESULTS: The mosquito catches yielded a total of 309 female Anopheles specimens, the only known vectors of malaria parasites of mammalians. These specimens belonged to 10 species, of which Anopheles implexus, Anopheles vinckei and Anopheles demeilloni dominated. Sensitive DNA amplification techniques failed to detect any Plasmodium-positive Anopheles specimens. Humidity and trap height influenced the Anopheles capture success, and there was a negative correlation between nest numbers and mosquito abundance. The anopheline mosquitoes were also less diverse and numerous in sites where chimpanzees were nesting as compared to those where they were feeding. CONCLUSIONS: These observations suggest that the sites where chimpanzees build their nests every night might be selected, at least in part, in order to minimize contact with anopheline mosquitoes, which might lead to a reduced risk in acquiring malaria infections.

Response to begging calls by Zebra Finch parents: "first come, first served" rule may overcome a parental preference between chicks.

In birds, parents may provide differential food provisioning among offspring according to their sex. Here, we test the hypothesis that events linked to the fine dynamics of begging behaviour could modulate parental preferences. After evaluating the preference related to chick sex for each parent of six Zebra Finch Taeniopygia guttata pairs, we studied the possible modifications of this preference when offspring begging was asynchronous. Our observations show that male parents follow a "first come, first served" rule, whereas females keep their initial choice. Although this study remains preliminary due to the sample size, it underlines the potential importance of investigating fine temporal features of begging behaviour to fully understand parents' provisioning strategies.

How Ebola impacts genetics of Western lowland gorilla populations.

BACKGROUND: Emerging infectious diseases in wildlife are major threats for both human health and biodiversity conservation. Infectious diseases can have serious consequences for the genetic diversity of populations, which could enhance the species' extinction probability. The Ebola epizootic in western and central Africa induced more than 90% mortality in Western lowland gorilla population. Although mortality rates are very high, the impacts of Ebola on genetic diversity of Western lowland gorilla have never been assessed. METHODOLOGY/PRINCIPAL FINDINGS: We carried out long term studies of three populations of Western lowland gorilla in the Republic of the Congo (Odzala-Kokoua National Park, Lossi gorilla sanctuary both affected by Ebola and Lossi's periphery not affected). Using 17 microsatellite loci, we compared genetic diversity and structure of the populations and estimate their effective size before and after Ebola outbreaks. Despite the effective size decline in both populations, we did not detect loss in genetic diversity after the epizootic. We revealed temporal changes in allele frequencies in the smallest population. CONCLUSIONS/SIGNIFICANCE: Immigration and short time elapsed since outbreaks could explain the conservation of genetic diversity after the demographic crash. Temporal changes in allele frequencies could not be explained by genetic drift or random sampling. Immigration from genetically differentiated populations and a non random mortality induced by Ebola, i.e., selective pressure and cost of sociality, are alternative hypotheses. Understanding the influence of Ebola on gorilla genetic dynamics is of paramount importance for human health, primate evolution and conservation biology.