BASSA: New software tool reveals hidden details in visualisation of low-frequency animal sounds.

The study of animal sounds in biology and ecology relies heavily upon time-frequency (TF) visualisation, most commonly using the short-time Fourier transform (STFT) spectrogram. This method, however, has inherent bias towards either temporal or spectral details that can lead to misinterpretation of complex animal sounds. An ideal TF visualisation should accurately convey the structure of the sound in terms of both frequency and time, however, the STFT often cannot meet this requirement. We evaluate the accuracy of four TF visualisation methods (superlet transform [SLT], continuous wavelet transform [CWT] and two STFTs) using a synthetic test signal. We then apply these methods to visualise sounds of the Chagos blue whale, Asian elephant, southern cassowary, eastern whipbird, mulloway fish and the American crocodile. We show that the SLT visualises the test signal with 18.48%-28.08% less error than the other methods. A comparison between our visualisations of animal sounds and their literature descriptions indicates that the STFT's bias may have caused misinterpretations in describing pygmy blue whale songs and elephant rumbles. We suggest that use of the SLT to visualise low-frequency animal sounds may prevent such misinterpretations. Finally, we employ the SLT to develop 'BASSA', an open-source, GUI software application that offers a no-code, user-friendly tool for analysing short-duration recordings of low-frequency animal sounds for the Windows platform. The SLT visualises low-frequency animal sounds with improved accuracy, in a user-friendly format, minimising the risk of misinterpretation while requiring less technical expertise than the STFT. Using this method could propel advances in acoustics-driven studies of animal communication, vocal production methods, phonation and species identification.

Intra and interspecific audience effect on domestic dogs' behavioural displays and facial expressions.

The aim of the current study was to investigate the influence of both intra- and interspecific audiences on dogs' facial expressions and behaviours. Forty-six dogs were exposed to three test conditions in which a food reward, initially available, was denied when in the presence of either a human (Human condition) or a dog audience (Dog condition), or in the absence of a visible audience (Non-social condition). Salivary cortisol was collected to evaluate the stress/arousal activation in the different conditions. Compared to the Non-social condition, the presence of a conspecific evoked more facial expressions, according to the DogFACS (Facial Action Coding System, an anatomically based tool to analyze facial expressions in domestic dogs), (EAD105-Ears downward), displacement behaviours (AD137-Nose licking, AD37-Lip wiping), tail wagging, whining, and panting (AD126). When facing a conspecific, dogs assumed a more avoidant attitude, keeping a distance and not looking at the stimuli, compared to when in the presence of the human partner. Dogs also exhibited more facial expressions (EAD102-Ears Adductor, EAD104-Ears Rotator), displacement behaviours (AD137-Nose licking, AD37-Lip wiping), panting (AD126) and whining when facing the conspecific than the human partner. Post-test cortisol was not influenced by any condition, and no association between pre-test cortisol and behavioural variables was found, thus strong differences in the levels of stress/arousal were unlikely to be responsible for differences in behavior between conditions. Considering the current results in the context of the available literature, we suggest that the higher displacement behaviors exhibited with the conspecifics were likely due to an increased level of uncertainty regarding the situations.

Ultrafast sound production mechanism in one of the smallest vertebrates.

Motion is the basis of nearly all animal behavior. Evolution has led to some extraordinary specializations of propulsion mechanisms among invertebrates, including the mandibles of the dracula ant and the claw of the pistol shrimp. In contrast, vertebrate skeletal movement is considered to be limited by the speed of muscle, saturating around 250 Hz. Here, we describe the unique propulsion mechanism by which Danionella cerebrum, a miniature cyprinid fish of only 12 mm length, produces high amplitude sounds exceeding 140 dB (re. 1 µPa, at a distance of one body length). Using a combination of high-speed video, micro-computed tomography (micro-CT), RNA profiling, and finite difference simulations, we found that D. cerebrum employ a unique sound production mechanism that involves a drumming cartilage, a specialized rib, and a dedicated muscle adapted for low fatigue. This apparatus accelerates the drumming cartilage at over 2,000 g, shooting it at the swim bladder to generate a rapid, loud pulse. These pulses are chained together to make calls with either bilaterally alternating or unilateral muscle contractions. D. cerebrum use this remarkable mechanism for acoustic communication with conspecifics.

Social Brain Perspectives on the Social and Evolutionary Neuroscience of Human Language.

Human language and social cognition are two key disciplines that have traditionally been studied as separate domains. Nonetheless, an emerging view suggests an alternative perspective. Drawing on the theoretical underpinnings of the social brain hypothesis (thesis of the evolution of brain size and intelligence), the social complexity hypothesis (thesis of the evolution of communication), and empirical research from comparative animal behavior, human social behavior, language acquisition in children, social cognitive neuroscience, and the cognitive neuroscience of language, it is argued that social cognition and language are two significantly interconnected capacities of the human species. Here, evidence in support of this view reviews (1) recent developmental studies on language learning in infants and young children, pointing to the important crucial benefits associated with social stimulation for youngsters, including the quality and quantity of incoming linguistic information, dyadic infant/child-to-parent non-verbal and verbal interactions, and other important social cues integral for facilitating language learning and social bonding; (2) studies of the adult human brain, suggesting a high degree of specialization for sociolinguistic information processing, memory retrieval, and comprehension, suggesting that the function of these neural areas may connect social cognition with language and social bonding; (3) developmental deficits in language and social cognition, including autism spectrum disorder (ASD), illustrating a unique developmental profile, further linking language, social cognition, and social bonding; and (4) neural biomarkers that may help to identify early developmental disorders of language and social cognition. In effect, the social brain and social complexity hypotheses may jointly help to describe how neurotypical children and adults acquire language, why autistic children and adults exhibit simultaneous deficits in language and social cognition, and why nonhuman primates and other organisms with significant computational capacities cannot learn language. But perhaps most critically, the following article argues that this and related research will allow scientists to generate a holistic profile and deeper understanding of the healthy adult social brain while developing more innovative and effective diagnoses, prognoses, and treatments for maladies and deficits also associated with the social brain.

BovineTalk: machine learning for vocalization analysis of dairy cattle under the negative affective state of isolation.

There is a critical need to develop and validate non-invasive animal-based indicators of affective states in livestock species, in order to integrate them into on-farm assessment protocols, potentially via the use of precision livestock farming (PLF) tools. One such promising approach is the use of vocal indicators. The acoustic structure of vocalizations and their functions were extensively studied in important livestock species, such as pigs, horses, poultry, and goats, yet cattle remain understudied in this context to date. Cows were shown to produce two types of vocalizations: low-frequency calls (LF), produced with the mouth closed, or partially closed, for close distance contacts, and open mouth emitted high-frequency calls (HF), produced for long-distance communication, with the latter considered to be largely associated with negative affective states. Moreover, cattle vocalizations were shown to contain information on individuality across a wide range of contexts, both negative and positive. Nowadays, dairy cows are facing a series of negative challenges and stressors in a typical production cycle, making vocalizations during negative affective states of special interest for research. One contribution of this study is providing the largest to date pre-processed (clean from noises) dataset of lactating adult multiparous dairy cows during negative affective states induced by visual isolation challenges. Here, we present two computational frameworks-deep learning based and explainable machine learning based, to classify high and low-frequency cattle calls and individual cow voice recognition. Our models in these two frameworks reached 87.2 and 89.4% accuracy for LF and HF classification, with 68.9 and 72.5% accuracy rates for the cow individual identification, respectively.

Female Preferences for More Elaborate Signals Are an Emergent Outcome of Male Chorusing Interactions in Túngara Frogs.

AbstractIn chorusing species, conspecific interference exerts strong selection on signal form and timing to maximize conspicuousness and attractiveness within the signaling milieu. We investigated how túngara frog calling strategies were influenced by varied social environments and male phenotypes and how calling interactions influenced female preferences. When chorusing, túngara frog calls consist of a whine typically followed by one to three chucks. In experimental choruses we saw that as chorus size increased, calls increasingly had their chucks overlapped by the high-amplitude beginning section of other callers' whines. Playback experiments revealed that such overlap reduced the attractiveness of calls to females but that appending additional chucks mitigated this effect. Thus, more elaborate calls were preferred when calls suffered overlap, although they were not preferred when overlap was absent. In response to increasing risk of overlap in larger choruses, males increased call elaboration. However, males overwhelmingly produced two-chuck calls in even the largest choruses, despite our results suggesting that additional chucks would more effectively safeguard calls. Furthermore, aspects of male phenotypes predicted to limit call elaboration had negligible or uncertain effects, suggesting that other constraints are operating. These results highlight how complex interrelations among signal form, signaling interactions, and the social environment shape the evolution of communication in social species.

Too much information? Males convey parasite levels using more signal modalities than females utilise.

Elaborate sexual signals are thought to have evolved and be maintained to serve as honest indicators of signaller quality. One measure of quality is health, which can be affected by parasite infection. Cnemaspis mysoriensis is a diurnal gecko that is often infested with ectoparasites in the wild, and males of this species express visual (coloured gular patches) and chemical (femoral gland secretions) traits that receivers could assess during social interactions. In this paper, we tested whether ectoparasites affect individual health, and whether signal quality is an indicator of ectoparasite levels. In wild lizards, we found that ectoparasite level was negatively correlated with body condition in both sexes. Moreover, some characteristics of both visual and chemical traits in males were strongly associated with ectoparasite levels. Specifically, males with higher ectoparasite levels had yellow gular patches with lower brightness and chroma, and chemical secretions with a lower proportion of aromatic compounds. We then determined whether ectoparasite levels in males influence female behaviour. Using sequential choice trials, wherein females were provided with either the visual or the chemical signals of wild-caught males that varied in ectoparasite level, we found that only chemical secretions evoked an elevated female response towards less parasitised males. Simultaneous choice trials in which females were exposed to the chemical secretions from males that varied in parasite level further confirmed a preference for males with lower parasites loads. Overall, we find that although health (body condition) or ectoparasite load can be honestly advertised through multiple modalities, the parasite-mediated female response is exclusively driven by chemical signals.

Backgrounds and the evolution of visual signals.

Color signals which mediate behavioral interactions across taxa and contexts are often thought of as color 'patches' - parts of an animal that appear colorful compared to other parts of that animal. Color patches, however, cannot be considered in isolation because how a color is perceived depends on its visual background. This is of special relevance to the function and evolution of signals because backgrounds give rise to a fundamental tradeoff between color signal detectability and discriminability: as its contrast with the background increases, a color patch becomes more detectable, but discriminating variation in that color becomes more difficult. Thus, the signal function of color patches can only be fully understood by considering patch and background together as an integrated whole.

Do Poisonous Plants in Pastures Communicate Their Toxicity? Meta-Study and Evaluation of Poisoning Cases in Central Europe.

One of the possible roles of secondary plant metabolites, including toxins, is facilitating plant-animal communication. Lethal cases of pasture poisoning show that the message is not always successfully conveyed. As the focus of poisoning lies in the clinical aspects, the external circumstances of pasture poisoning are widely unknown. To document poisoning conditions in cattle, sheep, goats, and horses on pastures and to compile a checklist of plants involved in either poisoning or co-existence (zero poisoning), published case reports were evaluated as primary sources. The number of affected animal individuals was estimated within abundance classes from 0 to more than 100. The checklist of poisonous plants comprised 52 taxa. Of these, 13 taxa were deemed safe (no reference was found indicating poisoning), 11 taxa were associated with evidence-based zero poisoning (positive list), and 28 taxa were associated with poisoning (negative list). Nine plant taxa caused poisoning in more than 100 animal individuals. Zero poisoning accounted for 40% and poisoning accounted for 60% of a total of 85 cases. Poisoning was most often associated with a limited choice of feed (24.7%), followed by overgrazing (12.9%), seasonally scarce feed (10.6%), and co-ingestion of grass (4.7%). Hunger interferes with plant-animal co-existence, while zero poisoning improves it. In conclusion, poisonous plants in pastures may communicate their toxicity if the animals have enough alternative feed plants. An individual animal might utterly perceive the communication of toxicity by the plant species but be forced to ignore the message owing to a limited choice of feed options.

Simultaneous recording of ultrasonic vocalizations and sniffing from socially interacting individual rats using a miniature microphone.

Vocalizations are pivotal in mammalian communication, especially in humans. Rodents accordingly rely on ultrasonic vocalizations (USVs) that reflect their internal state as a primary channel during social interactions. However, attributing vocalizations to specific individuals remains challenging, impeding internal state assessment. Rats emit 50-kHz USVs to indicate positive states and intensify sniffing during alertness and social interactions. Here, we present a method involving a miniature microphone attached to the rat nasal cavity that allows to capture both male and female individual rat vocalizations and sniffing patterns during social interactions. We found that while the emission of 50-kHz USVs increases during close interactions, these signals lack specific behavioral associations. Moreover, a previously unreported low-frequency vocalization type marking rat social interactions was uncovered. Finally, different dynamics of sniffing and vocalization activities point to distinct underlying internal states. Thus, our method facilitates the exploration of internal states concurrent with social behaviors.

Higher social tolerance is associated with more complex facial behavior in macaques.

The social complexity hypothesis for communicative complexity posits that animal societies with more complex social systems require more complex communication systems. We tested the social complexity hypothesis on three macaque species that vary in their degree of social tolerance and complexity. We coded facial behavior in >3000 social interactions across three social contexts (aggressive, submissive, affiliative) in 389 animals, using the Facial Action Coding System for macaques (MaqFACS). We quantified communicative complexity using three measures of uncertainty: entropy, specificity, and prediction error. We found that the relative entropy of facial behavior was higher for the more tolerant crested macaques as compared to the less tolerant Barbary and rhesus macaques across all social contexts, indicating that crested macaques more frequently use a higher diversity of facial behavior. The context specificity of facial behavior was higher in rhesus as compared to Barbary and crested macaques, demonstrating that Barbary and crested macaques used facial behavior more flexibly across different social contexts. Finally, a random forest classifier predicted social context from facial behavior with highest accuracy for rhesus and lowest for crested, indicating there is higher uncertainty and complexity in the facial behavior of crested macaques. Overall, our results support the social complexity hypothesis.

Listen to Us: Perceptions of Animal Voice and Agency.

In many contexts, the interests of nonhuman animals (hereafter "animals") are often overlooked or considered to be a lower priority than those of humans. While strong arguments exist for taking animal moral claims seriously, these largely go unheard due to dominant anthropocentric attitudes and beliefs. This study aimed to explore how animal interests might be best represented in the human world. We conducted interviews to investigate people's perceptions of what it means to speak for other animals and who can reliably represent animal interests. Using Grounded Theory analytical methods, we identified one major theme: "Animal voice", and its subthemes: "Animals do/do not have a voice", "Human language constructs realities and paradigms", and "Let animals speak". Our findings illustrate how human language constructs contribute to shaping the realities of animals by contextually defining them as voiceless. This has serious implications for animals, society, and the environment. Drawing parallels with the relevant literature, our results reflect calls for the social and political recognition of animal voice as fundamental to animal representation. We recommend future research to focus on developing ethical and compassionate approaches to understanding animal subjective experiences to empower and amplify animal voices.

Territorial behaviour of thrush nightingales outside the breeding season.

Territoriality is a common pattern of space use in animals that has fundamental consequences for ecological processes. In the tropics, all-year resident songbirds usually hold territories throughout the year, whereas most all-year resident temperate species are territorial only during the breeding season. In long-distance migrants, however, the situation is mostly unexplored. Here, we report findings from a Palaearctic-African migrant, the thrush nightingale Luscinia luscina. We found that only a fraction of the males was territorial in their East African winter quarters and that this was related to the stage of their song development. Individuals with full song were territorial towards other full songsters, but not towards birds that sang plastic song (i.e. an earlier stage of song development). Plastic singers were not territorial towards full songsters and often settled closely to territorial males. We suggest that territoriality of thrush nightingales in the winter quarters may be a by-product of rising testosterone levels that trigger song crystallization. Collectively, our study indicates that changes in territoriality can occur rapidly, giving rise to shifting proportions of territorial and non-territorial individuals in a population, which may lead to complex dynamics in settlement patterns and resulting ecological interactions.

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.

Wild nightingales flexibly match whistle pitch in real time.

Interactive vocal communication, similar to a human conversation, requires flexible and real-time changes to vocal output in relation to preceding auditory stimuli. These vocal adjustments are essential to ensuring both the suitable timing and content of the interaction. Precise timing of dyadic vocal exchanges has been investigated in a variety of species, including humans. In contrast, the ability of non-human animals to accurately adjust specific spectral features of vocalization extemporaneously in response to incoming auditory information is less well studied. One spectral feature of acoustic signals is the fundamental frequency, which we perceive as pitch. Many animal species can discriminate between sound frequencies, but real-time detection and reproduction of an arbitrary pitch have only been observed in humans. Here, we show that nightingales in the wild can match the pitch of whistle songs while singing in response to conspecifics or pitch-controlled whistle playbacks. Nightingales matched whistles across their entire pitch production range indicating that they can flexibly tune their vocal output along a wide continuum. Prompt whistle pitch matches were more precise than delayed ones, suggesting the direct mapping of auditory information onto a motor command to achieve online vocal replication of a heard pitch. Although nightingales' songs follow annual cycles of crystallization and deterioration depending on breeding status, the observed pitch-matching behavior is present year-round, suggesting a stable neural circuit independent of seasonal changes in physiology. Our findings represent the first case of non-human instantaneous vocal imitation of pitch, highlighting a promising model for understanding sensorimotor transformation within an interactive context. VIDEO ABSTRACT.

A multifaceted framework to establish the presence of meaning in non-human communication.

Does non-human communication, like language, involve meaning? This question guides our focus through an interdisciplinary review of the theories and terminology used to study meaning across disciplines and species. Until now, it has been difficult to apply the concept of meaning to communication in non-humans. This is partly because of the varied approaches to the study of meaning. Additionally, while there is a scholarly acknowledgement of potential meaning in non-human cognition, there is also scepticism when the topic of communication arises. We organise some of the key literature into a coherent framework that can bridge disciplines and species, to ensure that aspects of meaning are accurately and fairly compared. We clarify the growing view in the literature that, rather than requiring multiple definitions or being split into different types, meaning is a multifaceted yet still unified concept. In so doing, we propose that meaning is an umbrella term. Meaning cannot be summed up with a short definition or list of features, but involves multiple complexities that are outlined in our framework. Specifically, three global facets are needed to describe meaning: a Signal Meaning Facet, an Interactant Meaning Facet, and a Resultant Meaning Facet. Most importantly, we show that such analyses are possible to apply as much to non-humans as to humans. We also emphasise that meaning nuances differ among non-human species, making a dichotomous approach to meaning questionable. Instead, we show that a multifaceted approach to meaning establishes how meaning appears within highly diverse examples of non-human communication, in ways consistent with the phenomenon's presence in human non-verbal communication and language(s). Therefore, without further recourse to 'functional' approaches that circumvent the critical question of whether any non-human meaning exists, we show that the concept of meaning is suitable for evolutionary biologists, behavioural ecologists, and others to study, to establish exactly which species exhibit meaning in their communication and in what ways.

Grey wolves (Canis lupus) discriminate between familiar and unfamiliar human voices.

The ability to discriminate between different individuals based on identity cues, which is important to support the social behaviour of many animal species, has mostly been investigated in conspecific contexts. A rare example of individual heterospecific discrimination is found in domestic dogs, who are capable of recognising their owners' voices. Here, we test whether grey wolves, the nearest wild relative of dogs, also have the ability to distinguish familiar human voices, which would indicate that dogs' ability is not a consequence of domestication. Using the habituation-dishabituation paradigm, we presented captive wolves with playback recordings of their keepers' and strangers' voices producing either familiar or unfamiliar phrases. The duration of their response was significantly longer when presented with keepers' voices than with strangers' voices, demonstrating that wolves discriminated between familiar and unfamiliar speakers. This suggests that dogs' ability to discriminate between human voices was probably present in their common ancestor and may support the idea that this is a general ability of vertebrates to recognise heterospecific individuals. Our study also provides further evidence for familiar voice discrimination in a wild animal in captivity, indicating that this ability may be widespread across vertebrate species.

Bottlenose dolphin mothers modify signature whistles in the presence of their own calves.

Human caregivers interacting with children typically modify their speech in ways that promote attention, bonding, and language acquisition. Although this "motherese," or child-directed communication (CDC), occurs in a variety of human cultures, evidence among nonhuman species is very rare. We looked for its occurrence in a nonhuman mammalian species with long-term mother-offspring bonds that is capable of vocal production learning, the bottlenose dolphin (Tursiops truncatus). Dolphin signature whistles provide a unique opportunity to test for CDC in nonhuman animals, because we are able to quantify changes in the same vocalizations produced in the presence or absence of calves. We analyzed recordings made during brief catch-and-release events of wild bottlenose dolphins in waters near Sarasota Bay, Florida, United States, and found that females produced signature whistles with significantly higher maximum frequencies and wider frequency ranges when they were recorded with their own dependent calves vs. not with them. These differences align with the higher fundamental frequencies and wider pitch ranges seen in human CDC. Our results provide evidence in a nonhuman mammal for changes in the same vocalizations when produced in the presence vs. absence of offspring, and thus strongly support convergent evolution of motherese, or CDC, in bottlenose dolphins. CDC may function to enhance attention, bonding, and vocal learning in dolphin calves, as it does in human children. Our data add to the growing body of evidence that dolphins provide a powerful animal model for studying the evolution of vocal learning and language.

Information Theory Opens New Dimensions in Experimental Studies of Animal Behaviour and Communication.

Over the last 40-50 years, ethology has become increasingly quantitative and computational. However, when analysing animal behavioural sequences, researchers often need help finding an adequate model to assess certain characteristics of these sequences while using a relatively small number of parameters. In this review, I demonstrate that the information theory approaches based on Shannon entropy and Kolmogorov complexity can furnish effective tools to analyse and compare animal natural behaviours. In addition to a comparative analysis of stereotypic behavioural sequences, information theory can provide ideas for particular experiments on sophisticated animal communications. In particular, it has made it possible to discover the existence of a developed symbolic "language" in leader-scouting ant species based on the ability of these ants to transfer abstract information about remote events.

GeoDanceHive: An Operational Hive for Honeybees Dances Recording.

Honeybees are known for their ability to communicate about resources in their environment. They inform the other foragers by performing specific dance sequences according to the spatial characteristics of the resource. The purpose of our study is to provide a new tool for honeybees dances recording, usable in the field, in a practical and fully automated way, without condemning the harvest of honey. We designed and equipped an outdoor prototype of a production hive, later called "GeoDanceHive", allowing the continuous recording of honeybees' behavior such as dances and their analysis. The GeoDanceHive is divided into two sections, one for the colony and the other serving as a recording studio. The time record of dances can be set up from minutes to several months. To validate the encoding and sampling quality, we used an artificial feeder and visual decoding to generate maps with the vector endpoints deduced from the dance information. The use of the GeoDanceHive is designed for a wide range of users, who can meet different objectives, such as researchers or professional beekeepers. Thus, our hive is a powerful tool for honeybees studies in the field and could highly contribute to facilitating new research approaches and a better understanding landscape ecology of key pollinators.