The impact of spike timing precision and spike emission reliability on decoding accuracy.

Precisely timed and reliably emitted spikes are hypothesized to serve multiple functions, including improving the accuracy and reproducibility of encoding stimuli, memories, or behaviours across trials. When these spikes occur as a repeating sequence, they can be used to encode and decode a potential time series. Here, we show both analytically and in simulations that the error incurred in approximating a time series with precisely timed and reliably emitted spikes decreases linearly with the number of neurons or spikes used in the decoding. This was verified numerically with synthetically generated patterns of spikes. Further, we found that if spikes were imprecise in their timing, or unreliable in their emission, the error incurred in decoding with these spikes would be sub-linear. However, if the spike precision or spike reliability increased with network size, the error incurred in decoding a time-series with sequences of spikes would maintain a linear decrease with network size. The spike precision had to increase linearly with network size, while the probability of spike failure had to decrease with the square-root of the network size. Finally, we identified a candidate circuit to test this scaling relationship: the repeating sequences of spikes with sub-millisecond precision in area HVC (proper name) of the zebra finch. This scaling relationship can be tested using both neural data and song-spectrogram-based recordings while taking advantage of the natural fluctuation in HVC network size due to neurogenesis.

Bat2Web: A Framework for Real-Time Classification of Bat Species Echolocation Signals Using Audio Sensor Data.

Bats play a pivotal role in maintaining ecological balance, and studying their behaviors offers vital insights into environmental health and aids in conservation efforts. Determining the presence of various bat species in an environment is essential for many bat studies. Specialized audio sensors can be used to record bat echolocation calls that can then be used to identify bat species. However, the complexity of bat calls presents a significant challenge, necessitating expert analysis and extensive time for accurate interpretation. Recent advances in neural networks can help identify bat species automatically from their echolocation calls. Such neural networks can be integrated into a complete end-to-end system that leverages recent internet of things (IoT) technologies with long-range, low-powered communication protocols to implement automated acoustical monitoring. This paper presents the design and implementation of such a system that uses a tiny neural network for interpreting sensor data derived from bat echolocation signals. A highly compact convolutional neural network (CNN) model was developed that demonstrated excellent performance in bat species identification, achieving an F1-score of 0.9578 and an accuracy rate of 97.5%. The neural network was deployed, and its performance was evaluated on various alternative edge devices, including the NVIDIA Jetson Nano and Google Coral.

What's special about human speech? A student exercise for comparing speech production between humans and chimpanzees.

Modern humans and chimpanzees share a common ancestor on the phylogenetic tree, yet chimpanzees do not spontaneously produce speech or speech sounds. The lab exercise presented in this paper was developed for undergraduate students in a course entitled "What's Special About Human Speech?" The exercise is based on acoustic analyses of the words "cup" and "papa" as spoken by Viki, a home-raised, speech-trained chimpanzee, as well as the words spoken by a human. The analyses allow students to relate differences in articulation and vocal abilities between Viki and humans to the known anatomical differences in their vocal systems. Anatomical and articulation differences between humans and Viki include (1) potential tongue movements, (2) presence or absence of laryngeal air sacs, (3) presence or absence of vocal membranes, and (4) exhalation vs inhalation during production.

Multimodal communication and audience directedness in the greeting behaviour of semi-captive African savannah elephants.

Many species communicate by combining signals into multimodal combinations. Elephants live in multi-level societies where individuals regularly separate and reunite. Upon reunion, elephants often engage in elaborate greeting rituals, where they use vocalisations and body acts produced with different body parts and of various sensory modalities (e.g., audible, tactile). However, whether these body acts represent communicative gestures and whether elephants combine vocalisations and gestures during greeting is still unknown. Here we use separation-reunion events to explore the greeting behaviour of semi-captive elephants (Loxodonta africana). We investigate whether elephants use silent-visual, audible, and tactile gestures directing them at their audience based on their state of visual attention and how they combine these gestures with vocalisations during greeting. We show that elephants select gesture modality appropriately according to their audience's visual attention, suggesting evidence of first-order intentional communicative use. We further show that elephants integrate vocalisations and gestures into different combinations and orders. The most frequent combination consists of rumble vocalisations with ear-flapping gestures, used most often between females. By showing that a species evolutionarily distant to our own primate lineage shows sensitivity to their audience's visual attention in their gesturing and combines gestures with vocalisations, our study advances our understanding of the emergence of first-order intentionality and multimodal communication across taxa.

Daily singing of adult songbirds functions to maintain song performance independently of auditory feedback and age.

Many songbirds learn to produce songs through vocal practice in early life and continue to sing daily throughout their lifetime. While it is well-known that adult songbirds sing as part of their mating rituals, the functions of singing behavior outside of reproductive contexts remain unclear. Here, we investigated this issue in adult male zebra finches by suppressing their daily singing for two weeks and examining the effects on song performance. We found that singing suppression decreased the pitch, amplitude, and duration of songs, and that those song features substantially recovered through subsequent free singing. These reversible song changes were not dependent on auditory feedback or the age of the birds, contrasting with the adult song plasticity that has been reported previously. These results demonstrate that adult song structure is not stable without daily singing, and suggest that adult songbirds maintain song performance by preventing song changes through physical act of daily singing throughout their life. Such daily singing likely functions as vocal training to maintain the song production system in optimal conditions for song performance in reproductive contexts, similar to how human singers and athletes practice daily to maintain their performance.

Vocal complexity in the long calls of Bornean orangutans.

Vocal complexity is central to many evolutionary hypotheses about animal communication. Yet, quantifying and comparing complexity remains a challenge, particularly when vocal types are highly graded. Male Bornean orangutans (Pongo pygmaeus wurmbii) produce complex and variable "long call" vocalizations comprising multiple sound types that vary within and among individuals. Previous studies described six distinct call (or pulse) types within these complex vocalizations, but none quantified their discreteness or the ability of human observers to reliably classify them. We studied the long calls of 13 individuals to: (1) evaluate and quantify the reliability of audio-visual classification by three well-trained observers, (2) distinguish among call types using supervised classification and unsupervised clustering, and (3) compare the performance of different feature sets. Using 46 acoustic features, we used machine learning (i.e., support vector machines, affinity propagation, and fuzzy c-means) to identify call types and assess their discreteness. We additionally used Uniform Manifold Approximation and Projection (UMAP) to visualize the separation of pulses using both extracted features and spectrogram representations. Supervised approaches showed low inter-observer reliability and poor classification accuracy, indicating that pulse types were not discrete. We propose an updated pulse classification approach that is highly reproducible across observers and exhibits strong classification accuracy using support vector machines. Although the low number of call types suggests long calls are fairly simple, the continuous gradation of sounds seems to greatly boost the complexity of this system. This work responds to calls for more quantitative research to define call types and quantify gradedness in animal vocal systems and highlights the need for a more comprehensive framework for studying vocal complexity vis-à-vis graded repertoires.

Exploring the role of vocalizations in regulating group dynamics.

Because of the diverging needs of individuals, group life can lead to disputes and competition, but it also has many advantages, such as reduced predation risk, information sharing and increased hunting success. Social animals have to maintain group cohesion and need to synchronize activities, such as foraging, resting, social interactions and movements, in order to thrive in groups. Acoustic signals are highly relevant for social dynamics, some because they are long-ranging and others because they are short-ranging, which may serve important within-group functions. However, although there has been an increase in studies concentrating on acoustic communication within groups in the past decade, many aspects of how vocalizations relate to group dynamics are still poorly understood. The aim of this review is to present an overview of our current knowledge on the role of vocalizations in regulating social group dynamics, identify knowledge gaps and recommend potential future research directions. We review the role that vocalizations play in (i) collective movement, (ii) separation risk and cohesion maintenance, (iii) fission-fusion dynamics, and (iv) social networks. We recommend that future studies aim to increase the diversity of studied species and strengthen the integration of state-of-the-art tools to study social dynamics and acoustic signals. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

The power of sound: unravelling how acoustic communication shapes group dynamics.

Acoustic signalling is a key mode of communication owing to its instantaneousness and rapid turnover, its saliency and flexibility and its ability to function strategically in both short- and long-range contexts. Acoustic communication is closely intertwined with both collective behaviour and social network structure, as it can facilitate the coordination of collective decisions and behaviour, and play an important role in establishing, maintaining and modifying social relationships. These research topics have each been studied separately and represent three well-established research areas. Yet, despite the close connection of acoustic communication with collective behaviour and social networks in natural systems, only few studies have focused on their interaction. The aim of this theme issue is therefore to build a foundation for understanding how acoustic communication is linked to collective behaviour, on the one hand, and social network structure on the other, in non-human animals. Through the building of such a foundation, our hope is that new questions in new avenues of research will arise. Understanding the links between acoustic communication and social behaviour seems crucial for gaining a comprehensive understanding of sociality and social evolution. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

In pop pursuit: social bond strength predicts vocal synchrony during cooperative mate guarding in bottlenose dolphins.

Vocal communication is an emblematic feature of group-living animals, used to share information and strengthen social bonds. Vocalizations are also used to coordinate group-level behaviours in many taxa, but little is known of the factors that may influence vocal behaviour during cooperative acts. Allied male Indo-Pacific bottlenose dolphins (Tursiops aduncus) use the 'pop' vocalization as a coercive signal when working together to herd single oestrous females. Using long-term association and acoustic data, we examined the influence of social and non-social factors on pop use by allied male dolphins in this context. Neither pop rate nor pop bout duration were influenced by any of the factors examined. However, allied males with stronger social bonds engaged in higher rates of vocal synchrony; whereby they actively matched the timing of their pop production. Hence, social bond strength influenced pop use in a cooperative context, suggesting dual functions of pop use: to induce the female to remain close, and to promote social bond maintenance and cooperation among males. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

The ecology of zebra finch song and its implications for vocal communication in multi-level societies.

Acoustic signalling is crucial in affecting movements and in social interactions. In species with dynamic social structures, such as multi-level societies, acoustic signals can provide a key mechanism allowing individuals to identify and find or avoid each other and to exchange information. Yet, if the spacing between individuals regularly exceeds the maximum signalling range, the relation between movements and signals becomes more complex. As the best-studied songbird in captivity, the zebra finch (Taeniopygia castanotis) is a species with individually distinct songs that are audible over just a few metres and a widely ranging dynamic multi-level social organization in the wild, raising questions on the actual role of its song in social cohesion and coordination. Here, we provide an overview of birdsong in social organizations (networks) and use the ecology of the zebra finch and male song to discuss how singing can facilitate social cohesion and coordination in species where the signal range is very short. We raise the question of the extent to which zebra finches are a representative species to understand the function of song in communication, and we broaden current views on the function of birdsong and its individual signature. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Hidden social complexity behind vocal and acoustic communication in non-avian reptiles.

Social interactions are inevitable in the lives of most animals, since most essential behaviours require interaction with conspecifics, such as mating and competing for resources. Non-avian reptiles are typically viewed as solitary animals that predominantly use their vision and olfaction to communicate with conspecifics. Nevertheless, in recent years, evidence is mounting that some reptiles can produce sounds and have the potential for acoustic communication. Reptiles that can produce sound have an additional communicative channel (in addition to visual/olfactory channels), which could suggest they have a higher communicative complexity, the evolution of which is assumed to be driven by the need of social interactions. Thus, acoustic reptiles may provide an opportunity to unveil the true social complexity of reptiles that are usually thought of as solitary. This review aims to reveal the hidden social interactions behind the use of sounds in non-avian reptiles. Our review suggests that the potential of vocal and acoustic communication and the complexity of social interactions may be underestimated in non-avian reptiles, and that acoustic reptiles may provide a great opportunity to uncover the coevolution between sociality and communication in non-avian reptiles. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

The relative contribution of acoustic signals versus movement cues in group coordination and collective decision-making.

To benefit from group living, individuals need to maintain cohesion and coordinate their activities. Effective communication thus becomes critical, facilitating rapid coordination of behaviours and reducing consensus costs when group members have differing needs and information. In many bird and mammal species, collective decisions rely on acoustic signals in some contexts but on movement cues in others. Yet, to date, there is no clear conceptual framework that predicts when decisions should evolve to be based on acoustic signals versus movement cues. Here, we first review how acoustic signals and movement cues are used for coordinating activities. We then outline how information masking, discrimination ability (Weber's Law) and encoding limitations, as well as trade-offs between these, can identify which types of collective behaviours likely rely on acoustic signals or movement cues. Specifically, our framework proposes that behaviours involving the timing of events or expression of specific actions should rely more on acoustic signals, whereas decisions involving complex choices with multiple options (e.g. direction and destination) should generally use movement cues because sounds are more vulnerable to information masking and Weber's Law effects. We then discuss potential future avenues of enquiry, including multimodal communication and collective decision-making by mixed-species animal groups. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamic'.

Collective signalling is shaped by feedbacks between signaller variation, receiver perception and acoustic environment in a simulated communication network.

Communication takes place within a network of multiple signallers and receivers. Social network analysis provides tools to quantify how an individual's social positioning affects group dynamics and the subsequent biological consequences. However, network analysis is rarely applied to animal communication, likely due to the logistical difficulties of monitoring natural communication networks. We generated a simulated communication network to investigate how variation in individual communication behaviours generates network effects, and how this communication network's structure feeds back to affect future signalling interactions. We simulated competitive acoustic signalling interactions among chorusing individuals and varied several parameters related to communication and chorus size to examine their effects on calling output and social connections. Larger choruses had higher noise levels, and this reduced network density and altered the relationships between individual traits and communication network position. Hearing sensitivity interacted with chorus size to affect both individuals' positions in the network and the acoustic output of the chorus. Physical proximity to competitors influenced signalling, but a distinctive communication network structure emerged when signal active space was limited. Our model raises novel predictions about communication networks that could be tested experimentally and identifies aspects of information processing in complex environments that remain to be investigated. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

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.

Behavioral responses to predator and heterospecific alarm calls are habitat-specific in Eurasian tree sparrows.

Acoustic communication plays a vital role in predator-prey interactions. Although habitat structure has been shown to affect anti-predator tactics, little is known about how animals vary their behaviors in response to predator calls or heterospecific alarm calls in different environments. Here we used sound playbacks to test the responses of Eurasian tree sparrows (Passer montanus) foraging in harvested/unharvested rice paddy and open residential area. In the first experiment, we tested their behavioral responses to dove calls, male common cuckoo (Cuculus canorus) calls, hawk-like calls mimicked by female common cuckoo, sparrowhawk (Accipiter nisus) calls, and human yell calls produced to scare birds (predator signal playbacks). In the second experiment, we tested their behavioral responses to the Japanese tit's (Parus minor) territorial songs and alarm calls (heterospecific alarm signal playbacks). Results showed that the tree sparrows had less fleeing in unharvested ripe rice paddy than in harvested rice paddy and open residential area. In predator signal playbacks, call type affected the escape behavior of sparrows in unharvested rice paddy and open residential area but not harvested rice paddy. In alarm signal playbacks, tit alarm calls evoked more fleeing than territorial songs in harvested rice paddy and open residential area but not unharvested rice paddy. These results suggest that anthropogenic habitat changes may influence avian anti-predator tactics.

Production of sounds by squirrelfish during symbiotic relationships with cleaner wrasses.

Examples of symbiotic relationships often include cleaning mutualisms, typically involving interactions between cleaner fish and other fish, called the clients. While these cleaners can cooperate by removing ectoparasites from their clients, they can also deceive by feeding on client mucus, a behavior usually referred to as "cheating behavior" that often leads to a discernible jolt from the client fish. Despite extensive studies of these interactions, most research has focused on the visual aspects of the communication. In this study, we aimed to explore the role of acoustic communication in the mutualistic relationship between cleaner fishes and nine holocentrid client species across four regions of the Indo-Pacific Ocean: French Polynesia, Guam, Seychelles, and the Philippines. Video cameras coupled with hydrophones were positioned at various locations on reefs housing Holocentridae fish to observe their acoustic behaviors during interactions. Our results indicate that all nine species of holocentrids can use acoustic signals to communicate to cleaner fish their refusal of the symbiotic interaction or their desire to terminate the cooperation. These sounds were predominantly observed during agonistic behavior and seem to support visual cues from the client. This study provides a novel example of acoustic communication during a symbiotic relationship in teleosts. Interestingly, these vocalizations often lacked a distinct pattern or structure. This contrasts with numerous other interspecific communication systems where clear and distinguishable signals are essential. This absence of a clear acoustic pattern may be because they are used in interspecific interactions to support visual behavior with no selective pressure for developing specific calls required in conspecific recognition. The different sound types produced could also be correlated with the severity of the client response. There is a need for further research into the effects of acoustic behaviors on the quality and dynamics of these mutualistic interactions.

Long-term, medium-term and acute stress response of urban populations of Eurasian red squirrels affected by different levels of human disturbance.

Animals in urban areas often encounter novel and potentially stressful conditions. It is important to understand how wildlife cope with anthropogenic disturbance. To investigate this specific adaptation we live-trapped squirrels in two study sites in Warsaw: a forest reserve and an urban park and we estimated stress responses at three levels: long-term and medium-term stress (the level of stress hormones, i.e. cortisol and cortisone concentrations, in hair and feces) and acute reaction to human-induced stress (measured during handling with the aid of the three indices: breath rate, struggle rate, and vocalization). According to GLMM models no difference in the stress hormones level was found between the two populations. The only differences in cortisol concentrations clearly depended on the season, i.e. being higher in autumn and winter comparying to other seasons. There was no influence of sex, or reproductive status on stress hormones. Forest squirrels had significantly higher breath rates, suggesting they were more stressed by handling. There was no difference in the struggle rate between study areas, this index was mostly affected by season (i.e. being highest in winter). First-trapped squirrels vocalized less than during the subsequent trappings. Assumingly, during the first, and more stressful trapping, squirrels used 'freezing' and/or little vocalization, while during next captures they used alarm calls to warn conspecifics. Overall, we showed that the two squirrel populations differed only in terms of their breath rate. This suggests that they did not differ in medium-term and long-term stress in general, but they can differ in acute response to handling. This also suggests that both populations were similarly affected by environmental factors. The lack of clear effects may also be due to population heterogeneity. Thus, in order to assess the effects of anthropogenic stressors a broader range of indicators and diverse analytical methods, including behavioral analyses, should be employed.

Towards acoustic monitoring of bees: wingbeat sounds are related to species and individual traits.

Global pollinator decline urgently requires effective methods to assess their trends, distribution and behaviour. Passive acoustics is a non-invasive and cost-efficient monitoring tool increasingly employed for monitoring animal communities. However, insect sounds remain highly unexplored, hindering the application of this technique for pollinators. To overcome this shortfall and support future developments, we recorded and characterized wingbeat sounds of a variety of Iberian domestic and wild bees and tested their relationship with taxonomic, morphological, behavioural and environmental traits at inter- and intra-specific levels. Using directional microphones and machine learning, we shed light on the acoustic signature of bee wingbeat sounds and their potential to be used for species identification and monitoring. Our results revealed that frequency of wingbeat sounds is negatively related with body size and environmental temperature (between-species analysis), while it is positively related with experimentally induced stress conditions (within-individual analysis). We also found a characteristic acoustic signature in the European honeybee that supported automated classification of this bee from a pool of wild bees, paving the way for passive acoustic monitoring of pollinators. Overall, these findings confirm that insect sounds during flight activity can provide insights on individual and species traits, and hence suggest novel and promising applications for this endangered animal group. This article is part of the theme issue 'Towards a toolkit for global insect biodiversity monitoring'.

Contextual and combinatorial structure in sperm whale vocalisations.

Sperm whales (Physeter macrocephalus) are highly social mammals that communicate using sequences of clicks called codas. While a subset of codas have been shown to encode information about caller identity, almost everything else about the sperm whale communication system, including its structure and information-carrying capacity, remains unknown. We show that codas exhibit contextual and combinatorial structure. First, we report previously undescribed features of codas that are sensitive to the conversational context in which they occur, and systematically controlled and imitated across whales. We call these rubato and ornamentation. Second, we show that codas form a combinatorial coding system in which rubato and ornamentation combine with two context-independent features we call rhythm and tempo to produce a large inventory of distinguishable codas. Sperm whale vocalisations are more expressive and structured than previously believed, and built from a repertoire comprising nearly an order of magnitude more distinguishable codas. These results show context-sensitive and combinatorial vocalisation can appear in organisms with divergent evolutionary lineage and vocal apparatus.