Behavioural response to boat noise weakens the strength of a trophic link in coral reefs.

In oceans, the noise generated by human activities has reached phenomenal proportions, with considerable harmful effects on marine life. Measuring this impact to achieve a sustainable balance for highly vulnerable marine ecosystems, such as coral reefs, is a critical environmental policy objective. Here, we demonstrate that anthropogenic noise alters the interactions of a coral reef fish with its environment and how this behavioural response to noise impairs foraging. In situ observations on the Moorea reef revealed that the damselfish Dascyllus emamo reacts to boat passage by moving closer to its coral bommie, considerably reducing the volume of water available to search for prey. Using boat noise playback experiments in microcosms, we studied D. emamo's behaviour and modeled its functional response (FR), which is the relationship between resource use and resource density, when feeding on juvenile shrimps. Similar to field observations, noise reduced D. emamo's spatial occupancy, accompanied by a lower FR, indicating a reduction in predation independent of prey density. Overall, noise-induced behavioural changes are likely to influence predator-prey interaction dynamics and ultimately the fitness of both protagonists. While there is an urgent need to assess the effect of anthropogenic noise on coral reefs, the ecological framework of the FR approach combined with behavioural metrics provides an essential tool for evaluating the cascading effects of noise on nested ecological interactions at the community level.

Pain cues override identity cues in baby cries.

Baby cries can convey both static information related to individual identity and dynamic information related to the baby's emotional and physiological state. How do these dimensions interact? Are they transmitted independently, or do they compete against one another? Here we show that the universal acoustic expression of pain in distress cries overrides individual differences at the expense of identity signaling. Our acoustic analysis show that pain cries, compared with discomfort cries, are characterized by a more unstable source, thus interfering with the production of identity cues. Machine learning analyses and psychoacoustic experiments reveal that while the baby's identity remains encoded in pain cries, it is considerably weaker than in discomfort cries. Our results are consistent with the prediction that the costs of failing to signal distress outweigh the cost of weakening cues to identity.

Windy events detection in big bioacoustics datasets using a pre-trained Convolutional Neural Network.

Passive Acoustic Monitoring (PAM), which involves using autonomous record units for studying wildlife behaviour and distribution, often requires handling big acoustic datasets collected over extended periods. While these data offer invaluable insights about wildlife, their analysis can present challenges in dealing with geophonic sources. A major issue in the process of detection of target sounds is represented by wind-induced noise. This can lead to false positive detections, i.e., energy peaks due to wind gusts misclassified as biological sounds, or false negative, i.e., the wind noise masks the presence of biological sounds. Acoustic data dominated by wind noise makes the analysis of vocal activity unreliable, thus compromising the detection of target sounds and, subsequently, the interpretation of the results. Our work introduces a straightforward approach for detecting recordings affected by windy events using a pre-trained convolutional neural network. This process facilitates identifying wind-compromised data. We consider this dataset pre-processing crucial for ensuring the reliable use of PAM data. We implemented this preprocessing by leveraging YAMNet, a deep learning model for sound classification tasks. We evaluated YAMNet as-is ability to detect wind-induced noise and tested its performance in a Transfer Learning scenario by using our annotated data from the Stony Point Penguin Colony in South Africa. While the classification of YAMNet as-is achieved a precision of 0.71, and recall of 0.66, those metrics strongly improved after the training on our annotated dataset, reaching a precision of 0.91, and recall of 0.92, corresponding to a relative increment of >28 %. Our study demonstrates the promising application of YAMNet in the bioacoustics and ecoacoustics fields, addressing the need for wind-noise-free acoustic data. We released an open-access code that, combined with the efficiency and peak performance of YAMNet, can be used on standard laptops for a broad user base.

Puppy whines mediate maternal behavior in domestic dogs.

In mammals, offspring vocalizations typically encode information about identity and body condition, allowing parents to limit alloparenting and adjust care. But how do these vocalizations mediate parental behavior in species faced with the problem of rearing not one, but multiple offspring, such as domestic dogs? Comprehensive acoustic analyses of 4,400 whines recorded from 220 Beagle puppies in 40 litters revealed litter and individual (within litter) differences in call acoustic structure. By then playing resynthesized whines to mothers, we showed that they provided more care to their litters, and were more likely to carry the emitting loudspeaker to the nest, in response to whine variants derived from their own puppies than from strangers. Importantly, care provisioning was attenuated by experimentally moving the fundamental frequency (fo, perceived as pitch) of their own puppies' whines outside their litter-specific range. Within most litters, we found a negative relationship between puppies' whine fo and body weight. Consistent with this, playbacks showed that maternal care was stronger in response to high-pitched whine variants simulating relatively small offspring within their own litter's range compared to lower-pitched variants simulating larger offspring. We thus show that maternal care in a litter-rearing species relies on a dual assessment of offspring identity and condition, largely based on level-specific inter- and intra-litter variation in offspring call fo. This dual encoding system highlights how, even in a long-domesticated species, vocalizations reflect selective pressures to meet species-specific needs. Comparative work should now investigate whether similar communication systems have convergently evolved in other litter-rearing species.

Influence of ambient water coloration on habitat and conspecific choice in the female Lake Malawi cichlid, Metriaclima zebra.

Female cichlid fish living in African great lakes are known to have sensory systems that are adapted to ambient light environments. These sensory system adaptations are hypothesized to have influenced the evolution of the diverse male nuptial coloration. In rock-dwelling Lake Malawi mbuna cichlids, however, the extent to which ambient light environments influence female sensory systems and potentially associated male nuptial coloration remains unknown. Yet, the ubiquitous blue flank coloration and UV reflection of male mbuna cichlids suggest the potential impacts of the blue-shifted ambient light environment on these cichlid's visual perception and male nuptial coloration in the shallow water depth in Lake Malawi. In the present study, we explored whether and how the sensory bias of females influences intersexual communication in the mbuna cichlid, Metriaclima zebra. A series of choice experiments in various light environments showed that M. zebra females 1) have a preference for the blue-shifted light environment, 2) prefer to interact with males in blue-shifted light environments, 3) do not show a preference between dominant and subordinate males in full-spectrum, long-wavelength filtered, and short-wavelength filtered light environments, and 4) show a "reversed" preference for subordinate males in the UV-filtered light environment. These results suggest that the visual perception of M. zebra females may be biased to the ambient light spectra in their natural habitat by local adaptation and that this sensory bias may influence the evolution of blue and UV reflective patterns in male nuptial coloration.

Is plant acoustic communication fact or fiction?

In recent years, the idea has flourished that plants emit and perceive sound and could even be capable of exchanging information through the acoustic channel. While research into plant bioacoustics is still in its infancy, with potentially fascinating discoveries awaiting ahead, here we show that the current knowledge is not conclusive. While plants do emit sounds under biotic and abiotic stresses such as drought, these sounds are high-pitched, of low intensity, and propagate only to a short distance. Most studies suggesting plant sensitivity to airborne sound actually concern the perception of substrate vibrations from the soil or plant part. In short, while low-frequency, high-intensity sounds emitted by a loudspeaker close to the plant seem to have tangible effects on various plant processes such as growth - a finding with possible applications in agriculture - it is unlikely that plants can perceive the sounds they produce, at least over long distances. So far, there is no evidence of plants communicating with each other via the acoustic channel.

Vocal tract shape variation contributes to individual vocal identity in African penguins.

Variation in formant frequencies has been shown to affect social interactions and sexual competition in a range of avian species. Yet, the anatomical bases of this variation are poorly understood. Here, we investigated the morphological correlates of formants production in the vocal apparatus of African penguins. We modelled the geometry of the supra-syringeal vocal tract of 20 specimens to generate a population of virtual vocal tracts with varying dimensions. We then estimated the acoustic response of these virtual vocal tracts and extracted the centre frequency of the first four predicted formants. We demonstrate that: (i) variation in length and cross-sectional area of vocal tracts strongly affects the formant pattern, (ii) the tracheal region determines most of this variation, and (iii) the skeletal size of penguins does not correlate with the trachea length and consequently has relatively little effect on formants. We conclude that in African penguins, while the variation in vocal tract geometry generates variation in resonant frequencies supporting the discrimination of conspecifics, such variation does not provide information on the emitter's body size. Overall, our findings advance our understanding of the role of formant frequencies in bird vocal communication.

Effect of Environmental Variables on African Penguin Vocal Activity: Implications for Acoustic Censusing.

Global biodiversity is in rapid decline, and many seabird species have disproportionally poorer conservation statuses than terrestrial birds. A good understanding of population dynamics is necessary for successful conservation efforts, making noninvasive, cost-effective monitoring tools essential. Here, we set out to investigate whether passive acoustic monitoring (PAM) could be used to estimate the number of animals within a set area of an African penguin (Spheniscus demersus) colony in South Africa. We were able to automate the detection of ecstatic display songs (EDSs) in our recordings, thus facilitating the handling of large datasets. This allowed us to show that calling rate increased with wind speed and humidity but decreased with temperature, and to highlight apparent abundance variations between nesting habitat types. We then showed that the number of EDSs in our recordings positively correlated with the number of callers counted during visual observations, indicating that the density could be estimated based on calling rate. Our observations suggest that increasing temperatures may adversely impact penguin calling behaviour, with potential negative consequences for population dynamics, suggesting the importance of effective conservation measures. Crucially, this study shows that PAM could be successfully used to monitor this endangered species' populations with minimal disturbance.

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.

Sound categorization by crocodilians.

Rapidly sorting the information contained in a stream of stimuli is a major challenge for animals. One cognitive mechanism for achieving this goal is categorization, where the receiving individual considers a continuous variation of a stimulus as belonging to discrete categories. Using playback experiments in a naturalistic setup, here we show that crocodiles confronted with an acoustic continuum ranging from a frog call to a crocodile call classify each acoustic variant into one of these two categories, establishing a meaningful boundary where no acoustic boundary exists. With GO/NO-GO experiments, we then observe that this boundary is defined along the continuum following learning. We further demonstrate that crocodilians rely on the spectral envelope of sounds to categorize stimuli. This study suggests that sound categorization in crocodilians is a pre-wired faculty allowing rapid decision-making and highlights the learning-dependent plasticity involved in defining the boundary between sound categories.

Infant cries convey both stable and dynamic information about age and identity.

What information is encoded in the cries of human babies? While it is widely recognized that cries can encode distress levels, whether cries reliably encode the cause of crying remains disputed. Here, we collected 39201 cries from 24 babies recorded in their homes longitudinally, from 15 days to 3.5 months of age, a database we share publicly for reuse. Based on the parental action that stopped the crying, which matched the parental evaluation of cry cause in 75% of cases, each cry was classified as caused by discomfort, hunger, or isolation. Our analyses show that baby cries provide reliable information about age and identity. Baby voices become more tonal and less shrill with age, while individual acoustic signatures drift throughout the first months of life. In contrast, neither machine learning algorithms nor trained adult listeners can reliably recognize the causes of crying.

Adults learn to identify pain in babies' cries.

Because the expression of pain in babies' cries is based on universal acoustic features, it is assumed that adult listeners should be able to detect when a crying baby is experiencing pain1-3. We report that detecting that a baby's cry expresses pain actually requires learning through experience. Our psychoacoustic experiments reveal that adults with no experience of caring for babies are unable to identify whether a baby's cry is a pain cry induced by vaccination or a mild discomfort cry recorded during a bath, even when they are familiar with the discomfort cries from this particular baby. In contrast, people with prior experience of babies - parents or professional caregivers - identify a familiar baby's pain cries without having heard these cries before. Parents of very young children are even able to identify the pain cries of a baby who is completely unfamiliar to them. Exposure through caregiving and/or parenting thus shapes the auditory and cognitive abilities involved in decoding the information conveyed by the baby's communication signals.

Spatial release from masking in crocodilians.

Ambient noise is a major constraint on acoustic communication in both animals and humans. One mechanism to overcome this problem is Spatial Release from Masking (SRM), the ability to distinguish a target sound signal from masking noise when both sources are spatially separated. SRM is well described in humans but has been poorly explored in animals. Although laboratory tests with trained individuals have suggested that SRM may be a widespread ability in vertebrates, it may play a limited role in natural environments. Here we combine field experiments with investigations in captivity to test whether crocodilians experience SRM. We show that 2 species of crocodilians are able to use SRM in their natural habitat and that it quickly becomes effective for small angles between the target signal source and the noise source, becoming maximal when the angle exceeds 15∘. Crocodiles can therefore take advantage of SRM to improve sound scene analysis and the detection of biologically relevant signals.

Nonlinear vocal phenomena affect human perceptions of distress, size and dominance in puppy whines.

While nonlinear phenomena (NLP) are widely reported in animal vocalizations, often causing perceptual harshness and roughness, their communicative function remains debated. Several hypotheses have been put forward: attention-grabbing, communication of distress, exaggeration of body size and dominance. Here, we use state-of-the-art sound synthesis to investigate how NLP affect the perception of puppy whines by human listeners. Listeners assessed the distress, size or dominance conveyed by synthetic puppy whines with manipulated NLP, including frequency jumps and varying proportions of subharmonics, sidebands and deterministic chaos. We found that the presence of chaos increased the puppy's perceived level of distress and that this effect held across a range of representative fundamental frequency (fo) levels. Adding sidebands and subharmonics also increased perceived distress among listeners who have extensive caregiving experience with pre-weaned puppies (e.g. breeders, veterinarians). Finally, we found that whines with added chaos, subharmonics or sidebands were associated with larger and more dominant puppies, although these biases were attenuated in experienced caregivers. Together, our results show that nonlinear phenomena in puppy whines can convey rich information to human listeners and therefore may be crucial for offspring survival during breeding of a domesticated species.

Voice-mediated interactions in a megaherbivore.

Planet Earth is becoming increasingly difficult for large animal species to inhabit. Yet, these species are of major importance for the functioning of the biosphere and their progressive disappearance is accompanied by profound negative alterations of ecosystems1 (Supplemental information). To implement effective conservation measures, it is essential to have a detailed knowledge of the biology of these species. Here, we show that the hippopotamus Hippopotamus amphibius, an iconic African megaherbivore for which little is known about social communication, uses vocal recognition to manage relationships between territorial groups. We conducted playback experiments on groups of hippos and observed their response to vocalizations from an individual of the same group (familiar), a group from the same lake (neighbor) and a distant group (stranger). We found that stranger vocalizations induced a stronger behavioral reaction than the other two stimuli. In addition to showing that hippos are able to identify categories of conspecifics based on vocal signatures, our study demonstrates that hippo groups are territorial entities that behave less aggressively toward their neighbors than toward strangers. These new behavioral data suggest that habituation playbacks prior to conservation translocation operations may help reduce the risk of conflict between individuals that have never seen each other.

Maternal responses to pup calls in a high-cost lactation species.

Bonding between mothers and their young is fundamental to mammalian reproductive behaviour and individual fitness. In social systems where the risk of confusing filial and non-filial offspring is high, mothers should demonstrate early, strong and consistent responses to their kin throughout the period of offspring dependence, irrespective of maternal traits. We tested this hypothesis through playback experiments in the northern elephant seal Mirounga angustirostris, a phocid species that breeds in high-density colonies. We found that mothers recognized their offspring throughout lactation and as early as 1-2 days after parturition. Measures of experience (age) and temperament (aggressivity) did not predict their response strength to filial playback treatments, nor did pup age or sex. Some mothers showed great consistency in behavioural responses throughout the lactation period, while others were less predictable. The strength of a female's response did not influence her pup's weaning weight; however, more consistent females weaned pups of higher mass. This is a rare demonstration of individual recognition among phocid mothers and their offspring, and suggests that consistency in maternal responsiveness may be an important social factor influencing the pup's growth and survival.

Effect of pitch range on dogs' response to conspecific vs. heterospecific distress cries.

Distress cries are emitted by many mammal species to elicit caregiving attention. Across taxa, these calls tend to share similar acoustic structures, but not necessarily frequency range, raising the question of their interspecific communicative potential. As domestic dogs are highly responsive to human emotional cues and experience stress when hearing human cries, we explore whether their responses to distress cries from human infants and puppies depend upon sharing conspecific frequency range or species-specific call characteristics. We recorded adult dogs' responses to distress cries from puppies and human babies, emitted from a loudspeaker in a basket. The frequency of the cries was presented in both their natural range and also shifted to match the other species. Crucially, regardless of species origin, calls falling into the dog call-frequency range elicited more attention. Thus, domestic dogs' responses depended strongly on the frequency range. Females responded both faster and more strongly than males, potentially reflecting asymmetries in parental care investment. Our results suggest that, despite domestication leading to an increased overall responsiveness to human cues, dogs still respond considerably less to calls in the natural human infant range than puppy range. Dogs appear to use a fast but inaccurate decision-making process to determine their response to distress-like vocalisations.

Evolution of communication signals and information during species radiation.

Communicating species identity is a key component of many animal signals. However, whether selection for species recognition systematically increases signal diversity during clade radiation remains debated. Here we show that in woodpecker drumming, a rhythmic signal used during mating and territorial defense, the amount of species identity information encoded remained stable during woodpeckers' radiation. Acoustic analyses and evolutionary reconstructions show interchange among six main drumming types despite strong phylogenetic contingencies, suggesting evolutionary tinkering of drumming structure within a constrained acoustic space. Playback experiments and quantification of species discriminability demonstrate sufficient signal differentiation to support species recognition in local communities. Finally, we only find character displacement in the rare cases where sympatric species are also closely related. Overall, our results illustrate how historical contingencies and ecological interactions can promote conservatism in signals during a clade radiation without impairing the effectiveness of information transfer relevant to inter-specific discrimination.

Experience modulates an insect's response to anthropogenic noise.

In response to anthropogenic noise, vertebrates express modified acoustic communication signals either through individual plasticity or local population adaptation. In contrast, how insects respond to this stressor is poorly studied. Field crickets Gryllus bimaculatus use acoustic signals to attract and locate mates and are commonly found in noisy roadside environments, offering a powerful system to study the effects of anthropogenic noise on insect communication. Rapid repetition of sexual calls (chirps) is essential to attract females, but calling incurs energetic costs and attracts predators. As a result, males are predicted to reduce calling rates when background noise is high. Here, we combine observations and experimental playbacks to show that the responses of field cricket males to anthropogenic noise also depend on their previous experience with passing cars. First, we show that males living on highway edges decrease their chirp rate in response to passing cars. To assess whether this behavioral response depends on previous exposure to car noise, we then broadcast recordings of car noise to males located at different distances from the road and, therefore, with different previous exposure to car noise. Although all tested individuals responded to broadcasted traffic noise, males closest to the road decreased their chirp rate less than individuals calling further from the road. These results suggest that regular exposure to anthropogenic noise may decrease individuals' sensitivity and behavioral responses to noise, allowing them to maintain effective signaling rates. Behavioral plasticity modulated by experience may thus allow some insect species to cope with human-induced environmental stressors.