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.

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.

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.

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.

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.

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.

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.

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.

Do penguins' vocal sequences conform to linguistic laws?

Information compression is a general principle of human language: the most frequent words are shorter in length (Zipf's Law of Brevity) and the duration of constituents decreases as the size of the linguistic construct increases (Menzerath-Altmann Law). Vocal sequences of non-human primates have been shown to conform to both these laws, suggesting information compression might be a more general principle. Here, we investigated whether display songs of the African penguin, which mediate recognition, intersexual mate choice and territorial defence, conform with these laws. Display songs are long, loud sequences combining three types of syllables. We found that the shortest type of syllable was the most frequent (with the shortest syllable being repeated stereotypically, potentially favouring signal redundancy in crowded environments). We also found that the average duration of the song's constituents was negatively correlated with the size of the song (a consequence of increasing the relative number of the shortest syllable type, rather than reducing the duration across all syllable types, thus preserving the communication of size-related information in the duration of the longest syllable type). Our results provide the first evidence for conformity to Zipf's and Menzerath-Altmann Laws in the vocal sequences of a non-primate species, indicating that these laws can coexist with selection pressures specific to the species' ecology.

Single Neurons in the Avian Auditory Cortex Encode Individual Identity and Propagation Distance in Naturally Degraded Communication Calls.

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. Here we investigated in a songbird model, the zebra finch, the neural substrate for ranging and identifying a single source. We relied on ecologically and behaviorally relevant stimuli, contact calls, to investigate the neural discrimination of individual vocal signature as well as sound source distance when calls have been degraded through propagation in a natural environment. Performing electrophysiological recordings in anesthetized birds, we found neurons in the auditory forebrain that discriminate individual vocal signatures despite long-range degradation, as well as neurons discriminating propagation distance, with varying degrees of multiplexing between both information types. Moreover, the neural discrimination performance of individual identity was not affected by propagation-induced degradation beyond what was induced by the decreased intensity. For the first time, neurons with distance-invariant identity discrimination properties as well as distance-discriminant neurons are revealed in the avian auditory cortex. Because these neurons were recorded in animals that had prior experience neither with the vocalizers of the stimuli nor with long-range propagation of calls, we suggest that this neural population is part of a general-purpose system for vocalizer discrimination and ranging.SIGNIFICANCE STATEMENT Understanding how the brain makes sense of the multitude of stimuli that it continually receives in natural conditions is a challenge for scientists. Here we provide a new understanding of how the auditory system extracts behaviorally relevant information, the vocalizer identity and its distance to the listener, from acoustic signals that have been degraded by long-range propagation in natural conditions. We show, for the first time, that single neurons, in the auditory cortex of zebra finches, are capable of discriminating the individual identity and sound source distance in conspecific communication calls. The discrimination of identity in propagated calls relies on a neural coding that is robust to intensity changes, signals' quality, and decreases in the signal-to-noise ratio.

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.

Dog-directed speech: why do we use it and do dogs pay attention to it?

Pet-directed speech is strikingly similar to infant-directed speech, a peculiar speaking pattern with higher pitch and slower tempo known to engage infants' attention and promote language learning. Here, we report the first investigation of potential factors modulating the use of dog-directed speech, as well as its immediate impact on dogs' behaviour. We recorded adult participants speaking in front of pictures of puppies, adult and old dogs, and analysed the quality of their speech. We then performed playback experiments to assess dogs' reaction to dog-directed speech compared with normal speech. We found that human speakers used dog-directed speech with dogs of all ages and that the acoustic structure of dog-directed speech was mostly independent of dog age, except for sound pitch which was relatively higher when communicating with puppies. Playback demonstrated that, in the absence of other non-auditory cues, puppies were highly reactive to dog-directed speech, and that the pitch was a key factor modulating their behaviour, suggesting that this specific speech register has a functional value in young dogs. Conversely, older dogs did not react differentially to dog-directed speech compared with normal speech. The fact that speakers continue to use dog-directed with older dogs therefore suggests that this speech pattern may mainly be a spontaneous attempt to facilitate interactions with non-verbal listeners.

Learning to cope with degraded sounds: female zebra finches can improve their expertise in discriminating between male voices at long distances.

Reliable transmission of acoustic information about individual identity is of critical importance for pair bond maintenance in numerous monogamous songbirds. However, information transfer can be impaired by environmental constraints such as external noise or propagation-induced degradation. Birds have been shown to use several adaptive strategies to deal with difficult signal transmission contexts. Specifically, a number of studies have suggested that vocal plasticity at the emitter's level allows birds to counteract the deleterious effects of sound degradation. Although the communication process involves both the emitter and the receiver, perceptual plasticity at the receiver's level has received little attention. Here, we explored the reliability of individual recognition by female zebra finches (Taeniopygia guttata), testing whether perceptual training can improve discrimination of degraded individual vocal signatures. We found that female zebra finches are proficient in discriminating between calls of individual males at long distances, and even more so when they can train themselves with increasingly degraded signals over time. In this latter context, females succeed in discriminating between males as far as 250 m. This result emphasizes that adaptation to adverse communication conditions may involve not only the emitter's vocal plasticity but also the receptor's decoding process through on-going learning.

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.

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.

The relevance of temporal cues in a fish sound: a first experimental investigation using modified signals in cichlids.

Playback experiments have been a useful tool for studying the function of sounds and the relevance of different sound characteristics in signal recognition in many different species of vertebrates. However, successful playback experiments in sound-producing fish remain rare, and few studies have investigated the role of particular sound features in the encoding of information. In this study, we set-up an apparatus in order to test the relevance of acoustic signals in males of the cichlid Metriaclima zebra. We found that territorial males responded more to playbacks by increasing their territorial activity and approaching the loudspeaker during and after playbacks. If sounds are used to indicate the presence of a competitor, we modified two sound characteristics, that is, the pulse period and the number of pulses, in order to investigate whether the observed behavioural response was modulated by the temporal structure of sounds recorded during aggressive interactions. Modified sounds yielded little or no effect on the behavioural response they elicited in territorial males, suggesting a high tolerance for variations in pulse period and number of pulses. The biological function of sounds in M. zebra and the lack of responsiveness to our temporal modifications are discussed.

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.

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.

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.