Automated echolocation classifiers vary in accuracy for northeastern U.S. bat species.

Acoustic surveys of bat echolocation calls are an important management tool for determining presence and probable absence of threatened and endangered bat species. In the northeastern United States, software programs such as Bat Call Identification (BCID), Kaleidoscope Pro (KPro), and Sonobat can automatically classify ultrasonic detector sound files, yet the programs' accuracy in correctly classifying calls to species has not been independently assessed. We used 1,500 full-spectrum reference calls with known identities for nine northeastern United States bat species to test the accuracy of these programs using calculations of Positive Predictive Value (PPV), Negative Predictive Value (NPV), Sensitivity (SN), Specificity (SP), Overall Accuracy, and No Information Rate. We found that BCID performed less accurately than other programs, likely because it only operates on zero-crossing data and may be less accurate for recordings converted from full-spectrum to zero-crossing. NPV and SP values were high across all species categories for SonoBat and KPro, indicating these programs' success at avoiding false positives. However, PPV and SN values were relatively low, particularly for individual Myotis species, indicating these programs are prone to false negatives. SonoBat and KPro performed better when distinguishing Myotis species from non-Myotis species. We expect less accuracy from these programs for acoustic recordings collected under normal working conditions, and caution that a bat acoustic expert should verify automatically classified files when making species-specific regulatory or conservation decisions.

Machine learning with taxonomic family delimitation aids in the classification of ephemeral beaked whale events in passive acoustic monitoring.

Passive acoustic monitoring is an essential tool for studying beaked whale populations. This approach can monitor elusive and pelagic species, but the volume of data it generates has overwhelmed researchers' ability to quantify species occurrence for effective conservation and management efforts. Automation of data processing is crucial, and machine learning algorithms can rapidly identify species using their sounds. Beaked whale acoustic events, often infrequent and ephemeral, can be missed when co-occurring with signals of more abundant, and acoustically active species that dominate acoustic recordings. Prior efforts on large-scale classification of beaked whale signals with deep neural networks (DNNs) have approached the class as one of many classes, including other odontocete species and anthropogenic signals. That approach tends to miss ephemeral events in favor of more common and dominant classes. Here, we describe a DNN method for improved classification of beaked whale species using an extensive dataset from the western North Atlantic. We demonstrate that by training a DNN to focus on the taxonomic family of beaked whales, ephemeral events were correctly and efficiently identified to species, even with few echolocation clicks. By retrieving ephemeral events, this method can support improved estimation of beaked whale occurrence in regions of high odontocete acoustic activity.

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.

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.

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'.

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.

Male proboscis monkey cranionasal size and shape is associated with visual and acoustic signalling.

The large nose adorned by adult male proboscis monkeys is hypothesised to serve as an audiovisual signal of sexual selection. It serves as a visual signal of male quality and social status, and as an acoustic signal, through the expression of loud, low-formant nasalised calls in dense rainforests, where visibility is poor. However, it is unclear how the male proboscis monkey nasal complex, including the internal structure of the nose, plays a role in visual or acoustic signalling. Here, we use cranionasal data to assess whether large noses found in male proboscis monkeys serve visual and/or acoustic signalling functions. Our findings support a visual signalling function for male nasal enlargement through a relatively high degree of nasal aperture sexual size dimorphism, the craniofacial region to which nasal soft tissue attaches. We additionally find nasal aperture size increases beyond dental maturity among male proboscis monkeys, consistent with the visual signalling hypothesis. We show that the cranionasal region has an acoustic signalling role through pronounced nasal cavity sexual shape dimorphism, wherein male nasal cavity shape allows the expression of loud, low-formant nasalised calls. Our findings provide robust support for the male proboscis monkey nasal complex serving both visual and acoustic functions.

Cetaceans are the next frontier for vocal rhythm research.

While rhythm can facilitate and enhance many aspects of behavior, its evolutionary trajectory in vocal communication systems remains enigmatic. We can trace evolutionary processes by investigating rhythmic abilities in different species, but research to date has largely focused on songbirds and primates. We present evidence that cetaceans-whales, dolphins, and porpoises-are a missing piece of the puzzle for understanding why rhythm evolved in vocal communication systems. Cetaceans not only produce rhythmic vocalizations but also exhibit behaviors known or thought to play a role in the evolution of different features of rhythm. These behaviors include vocal learning abilities, advanced breathing control, sexually selected vocal displays, prolonged mother-infant bonds, and behavioral synchronization. The untapped comparative potential of cetaceans is further enhanced by high interspecific diversity, which generates natural ranges of vocal and social complexity for investigating various evolutionary hypotheses. We show that rhythm (particularly isochronous rhythm, when sounds are equally spaced in time) is prevalent in cetacean vocalizations but is used in different contexts by baleen and toothed whales. We also highlight key questions and research areas that will enhance understanding of vocal rhythms across taxa. By coupling an infraorder-level taxonomic assessment of vocal rhythm production with comparisons to other species, we illustrate how broadly comparative research can contribute to a more nuanced understanding of the prevalence, evolution, and possible functions of rhythm in animal communication.

Song and genetic divergence within a subspecies of white-crowned sparrow (Zonotrichia leucophrys nuttalli).

Animal culture evolves alongside genomes, and the two modes of inheritance-culture and genes-interact in myriad ways. For example, stable geographic variation in culture can act as a reproductive barrier, thereby facilitating genetic divergence between "cultural populations." White-crowned sparrows (Zonotrichia leucophrys) are a well-established model species for bird song learning and cultural evolution, as they have distinct, geographically discrete, and culturally transmitted song types (i.e., song dialects). In this study, we tested the hypothesis that divergence between culturally transmitted songs drives genetic divergence within Nuttall's white-crowned sparrows (Z. l. nuttalli). In accordance with sexual selection theory, we hypothesized that cultural divergence between mating signals both preceded and generated genetic divergence. We characterized the population structure and song variation in the subspecies and found two genetically differentiated populations whose boundary coincides with a major song boundary at Monterey Bay, California. We then conducted a song playback experiment that demonstrated males discriminate between songs based on their degree of divergence from their local dialect. These results support the idea that discrimination against non-local songs is driving genetic divergence between the northern and southern populations. Altogether, this study provides evidence that culturally transmitted bird songs can act as the foundation for speciation by sexual selection.

Acoustic behavior of humpback whale calves on the feeding ground: Comparisons across age and implications for vocal development.

Studying sound production at different developmental stages can provide insight into the processes involved in vocal ontogeny. Humpback whales (Megaptera novaeangliae) are a known vocal learning species, but their vocal development is poorly understood. While studies of humpback whale calves in the early stages of their lives on the breeding grounds and migration routes exist, little is known about the behavior of these immature, dependent animals by the time they reach the feeding grounds. In this study, we used data from groups of North Atlantic humpback whales in the Gulf of Maine in which all members were simultaneously carrying acoustic recording tags attached with suction cups. This allowed for assignment of likely caller identity using the relative received levels of calls across tags. We analyzed data from 3 calves and 13 adults. There were high levels of call rate variation among these individuals and the results represent preliminary descriptions of calf behavior. Our analysis suggests that, in contrast to the breeding grounds or on migration, calves are no longer acoustically cryptic by the time they reach their feeding ground. Calves and adults both produce calls in bouts, but there may be some differences in bout parameters like inter-call intervals and bout durations. Calves were able to produce most of the adult vocal repertoire but used different call types in different proportions. Finally, we found evidence of immature call types in calves, akin to protosyllables used in babbling in other mammals, including humans. Overall, the sound production of humpback whale calves on the feeding grounds appears to be already similar to that of adults, but with differences in line with ontogenetic changes observed in other vocal learning species.

Transient sensorimotor projections in the developmental song learning period.

Memory recall and guidance are essential for motor skill acquisition. Like humans learning to speak, male zebra finches learn to sing by first memorizing and then matching their vocalization to the tutor's song (TS) during specific developmental periods. Yet, the neuroanatomical substrate supporting auditory-memory-guided sensorimotor learning has remained elusive. Here, using a whole-brain connectome analysis with activity-dependent viral expression, we identified a transient projection into the motor region, HVC, from neuronal ensembles responding to TS in the auditory forebrain, the caudomedial nidopallium (NCM), in juveniles. Virally induced cell death of the juvenile, but not adult, TS-responsive NCM neurons impaired song learning. Moreover, isolation, which delays closure of the sensory, but not the motor, learning period, did not affect the decrease of projections into the HVC from the NCM TS-responsive neurons after the song learning period. Taken together, our results suggest that dynamic axonal pruning may regulate timely auditory-memory-guided vocal learning during development.

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.

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.

Where's Whaledo: A software toolkit for array localization of animal vocalizations.

Where's Whaledo is a software toolkit that uses a combination of automated processes and user interfaces to greatly accelerate the process of reconstructing animal tracks from arrays of passive acoustic recording devices. Passive acoustic localization is a non-invasive yet powerful way to contribute to species conservation. By tracking animals through their acoustic signals, important information on diving patterns, movement behavior, habitat use, and feeding dynamics can be obtained. This method is useful for helping to understand habitat use, observe behavioral responses to noise, and develop potential mitigation strategies. Animal tracking using passive acoustic localization requires an acoustic array to detect signals of interest, associate detections on various receivers, and estimate the most likely source location by using the time difference of arrival (TDOA) of sounds on multiple receivers. Where's Whaledo combines data from two small-aperture volumetric arrays and a variable number of individual receivers. In a case study conducted in the Tanner Basin off Southern California, we demonstrate the effectiveness of Where's Whaledo in localizing groups of Ziphius cavirostris. We reconstruct the tracks of six individual animals vocalizing concurrently and identify Ziphius cavirostris tracks despite being obscured by a large pod of vocalizing dolphins.

Maternal behaviours disrupted by Gprasp2 deletion modulate neurodevelopmental trajectory in progeny.

Autism spectrum disorders (ASDs) are known to present sex-specific differences. At the same time, understanding how maternal behaviours are affected by pathogenic mutations is crucial to translate research efforts since rearing may recursively modulate neurodevelopment phenotype of the progeny. In this work, we focused on the effects of Gprasp2 deletion in females and its impact in progeny care and development. Female mice, wild-type (WT), Gprasp2+/- (HET) or Gprasp2-/- (KO) mutants and their progeny were used and behavioural paradigms targeting anxiety, memory, maternal care, and other social behaviours were performed. Analysis of communication was carried out through daily recordings of ultrasonic vocalizations in isolated pups and cross-fostering experiments were performed to understand the effect of maternal genotype in pup development. We found that Gprasp2-/- females presented striking impairments in social and working memory. Females also showed disruptions in maternal care, as well as physiological and molecular alterations in the reproductive system and hypothalamus, such as the structure of the mammary gland and the expression levels of oxytocin receptor (OxtR) in nulliparous versus primiparous females. We observed alterations in pup communication, particularly a reduced number of calls in Gprasp2 KO pups, which resulted from an interaction effect of the dam and pup genotype. Cross-fostering mutant pups with wild-type dams rescued some of the early defects shown in vocalizations, however, this effect was not bidirectional, as rearing WT pups with Gprasp2-/- dams was not sufficient to induce significant phenotypical alterations. Our results suggest Gprasp2 mutations perturb social and working memory in a sex-independent manner, but impact female-specific behaviours towards progeny care, female physiology, and gene expression. These changes in mutant dams contribute to a disruption in early stages of progeny development. More generally, our results highlight the need to better understand GxE interactions in the context of ASDs, when female behaviour may present a contributing factor in postnatal neurodevelopmental trajectory.

Zebra finch song parameters are affected by the breeding status of the male, but not temperature variability.

Bird song is a crucial feature for mate choice and reproduction. Song can potentially communicate information related to the quality of the mate, through song complexity, structure or finer changes in syllable characteristics. It has been shown in zebra finches that those characteristics can be affected by various factors including motivation, hormone levels or extreme temperature. However, although the literature on zebra finch song is substantial, some factors have been neglected. In this paper, we recorded male zebra finches in two breeding contexts (before and after pairing) and in two ambient temperature conditions (stable and variable) to see how those factors could influence song production. We found strong differences between the two breeding contexts: compared to their song before pairing, males that were paired had lower song rate, syllable consistency, frequency and entropy, while surprisingly the amplitude of their syllables increased. Temperature variability had an impact on the extent of these differences, but did not directly affect the song parameters that we measured. Our results describe for the first time how breeding status and temperature variability can affect zebra finch song, and give some new insights into the subtleties of the acoustic communication of this model species.

Superfast Lombard response in free-flying, echolocating bats.

Acoustic cues are crucial to communication, navigation, and foraging in many animals, which hence face the problem of detecting and discriminating these cues in fluctuating noise levels from natural or anthropogenic sources. Such auditory dynamics are perhaps most extreme for echolocating bats that navigate and hunt prey on the wing in darkness by listening for weak echo returns from their powerful calls in complex, self-generated umwelts.1,2 Due to high absorption of ultrasound in air and fast flight speeds, bats operate with short prey detection ranges and dynamic sensory volumes,3 leading us to hypothesize that bats employ superfast vocal-motor adjustments to rapidly changing sensory scenes. To test this hypothesis, we investigated the onset and offset times and magnitude of the Lombard response in free-flying echolocating greater mouse-eared bats exposed to onsets of intense constant or duty-cycled masking noise during a landing task. We found that the bats invoked a bandwidth-dependent Lombard response of 0.1-0.2 dB per dB increase in noise, with very short delay and relapse times of 20 ms in response to onsets and termination of duty-cycled noise. In concert with the absence call time-locking to noise-free periods, these results show that free-flying bats exhibit a superfast, but hard-wired, vocal-motor response to increased noise levels. We posit that this reflex is mediated by simple closed-loop audio-motor feedback circuits that operate independently of wingbeat and respiration cycles to allow for rapid adjustments to the highly dynamic auditory scenes encountered by these small predators.

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.