Comparing behaviours induced by natural memory retrieval and optogenetic reactivation of an engram ensemble in mice.

Memories are thought to be stored within sparse collections of neurons known as engram ensembles. Neurons active during a training episode are allocated to an engram ensemble ('engram neurons'). Memory retrieval is initiated by external sensory or internal cues present at the time of training reactivating engram neurons. Interestingly, optogenetic reactivation of engram ensemble neurons alone in the absence of external sensory cues is sufficient to induce behaviour consistent with memory retrieval in mice. However, there may exist differences between the behaviours induced by natural retrieval cues or artificial engram reactivation. Here, we compared two defensive behaviours (freezing and the syllable structure of ultrasonic vocalizations, USVs) induced by sensory cues present at training (natural memory retrieval) and optogenetic engram ensemble reactivation (artificial memory retrieval) in a threat conditioning paradigm in the same mice. During natural memory recall, we observed a strong positive correlation between freezing levels and distinct USV syllable features (characterized by an unsupervised algorithm, MUPET (Mouse Ultrasonic Profile ExTraction)). Moreover, we observed strikingly similar behavioural profiles in terms of freezing and USV characteristics between natural memory recall and artificial memory recall in the absence of sensory retrieval cues. Although our analysis focused on two behavioural measures of threat memory (freezing and USV characteristics), these results underscore the similarities between threat memory recall triggered naturally and through optogenetic reactivation of engram ensembles. This article is part of a discussion meeting issue 'Long-term potentiation: 50 years on'.

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.

Social experiences shape song preference learning independently of developmental exposure to song.

Communication governs the formation and maintenance of social relationships. The interpretation of communication signals depends not only on the signal's content but also on a receiver's individual experience. Experiences throughout life may interact to affect behavioural plasticity, such that a lack of developmental sensory exposure could constrain adult learning, while salient adult social experiences could remedy developmental deficits. We investigated how experiences impact the formation and direction of female auditory preferences in the zebra finch. Zebra finches form long-lasting pair bonds and females learn preferences for their mate's vocalizations. We found that after 2 weeks of cohabitation with a male, females formed pair bonds and learned to prefer their partner's song regardless of whether they were reared with ('normally reared') or without ('song-naive') developmental exposure to song. In contrast, females that heard but did not physically interact with a male did not prefer his song. In addition, previous work has found that song-naive females do not show species-typical preferences for courtship song. We found that cohabitation with a male ameliorated this difference in preference. Thus, courtship and pair bonding, but not acoustic-only interactions, strongly influence preference learning regardless of rearing experience, and may dynamically drive auditory plasticity for recognition and preference.

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.

Parental developmental experience affects vocal learning in offspring.

Cultural and genetic inheritance combine to enable rapid changes in trait expression, but their relative importance in determining trait expression across generations is not clear. Birdsong is a socially learned cognitive trait that is subject to both cultural and genetic inheritance, as well as being affected by early developmental conditions. We sought to test whether early-life conditions in one generation can affect song acquisition in the next generation. We exposed one generation (F1) of nestlings to elevated corticosterone (CORT) levels, allowed them to breed freely as adults, and quantified their son's (F2) ability to copy the song of their social father. We also quantified the neurogenetic response to song playback through immediate early gene (IEG) expression in the auditory forebrain. F2 males with only one corticosterone-treated parent copied their social father's song less accurately than males with two control parents. Expression of ARC in caudomedial nidopallium (NCM) correlated with father-son song similarity, and patterns of expression levels of several IEGs in caudomedial mesopallium (CMM) in response to father song playback differed between control F2 sons and those with a CORT-treated father only. This is the first study to demonstrate that developmental conditions can affect social learning and neurogenetic responses in a subsequent generation.

A population of neurons selective for human voice in the monkey brain.

Many animals can extract useful information from the vocalizations of other species. Neuroimaging studies have evidenced areas sensitive to conspecific vocalizations in the cerebral cortex of primates, but how these areas process heterospecific vocalizations remains unclear. Using fMRI-guided electrophysiology, we recorded the spiking activity of individual neurons in the anterior temporal voice patches of two macaques while they listened to complex sounds including vocalizations from several species. In addition to cells selective for conspecific macaque vocalizations, we identified an unsuspected subpopulation of neurons with strong selectivity for human voice, not merely explained by spectral or temporal structure of the sounds. The auditory representational geometry implemented by these neurons was strongly related to that measured in the human voice areas with neuroimaging and only weakly to low-level acoustical structure. These findings provide new insights into the neural mechanisms involved in auditory expertise and the evolution of communication systems in primates.

Juvenile social play predicts adult reproductive success in male bottlenose dolphins.

For over a century, the evolution of animal play has sparked scientific curiosity. The prevalence of social play in juvenile mammals suggests that play is a beneficial behavior, potentially contributing to individual fitness. Yet evidence from wild animals supporting the long-hypothesized link between juvenile social play, adult behavior, and fitness remains limited. In Western Australia, adult male bottlenose dolphins (Tursiops aduncus) form multilevel alliances that are crucial for their reproductive success. A key adult mating behavior involves allied males using joint action to herd individual females. Juveniles of both sexes invest significant time in play that resembles adult herding-taking turns in mature male (actor) and female (receiver) roles. Using a 32-y dataset of individual-level association patterns, paternity success, and behavioral observations, we show that juvenile males with stronger social bonds are significantly more likely to engage in joint action when play-herding in actor roles. Juvenile males also monopolized the actor role and produced an adult male herding vocalization ("pops") when playing with females. Notably, males who spent more time playing in the actor role as juveniles achieved more paternities as adults. These findings not only reveal that play behavior provides male dolphins with mating skill practice years before they sexually mature but also demonstrate in a wild animal population that juvenile social play predicts adult reproductive success.

Boat noise impedes vocalizations of wild plainfin midshipman fish.

Marine noise is recognised as a growing threat that can induce maladaptive behavioural changes in many aquatic animals, including fishes. The plainfin midshipman is a soniferous fish with a prolonged breeding period, during which males produce tonal hums that attract females, and grunts and growls during agonistic interactions. In this study, we used acoustic recordings to assess the effects of boat noise on the presence, peak frequencies, and durations of plainfin midshipman calls in the wild. We found that all three call types were less likely to occur, and the peak frequencies of hums and grunts increased in the presence of boat noise. We also show that loud and quiet boat noise affected plainfin midshipman vocalizations similarly. As anthropogenic noise is likely to increase in the ocean, it will be important to understand how such noise can affect communication systems, and consequently population health and resiliency.

Fear of the human 'super predator' in native marsupials and introduced deer in Australia.

Recent experiments have demonstrated that carnivores and ungulates in Africa, Asia, Europe and North America fear the human 'super predator' far more than other predators. Australian mammals have been a focus of research on predator naiveté because it is suspected they show atypical antipredator responses. To experimentally test if mammals in Australia also most fear humans, we quantified the responses of four native marsupials (eastern grey kangaroo, Bennett's wallaby, Tasmanian pademelon, common brushtail possum) and introduced fallow deer to playbacks of predator (human, dog, Tasmanian devil, wolf) or non-predator control (sheep) vocalizations. Native marsupials most feared the human 'super predator', fleeing humans 2.4 times more often than the next most frightening predator (dogs), and being most, and significantly, vigilant to humans. These results demonstrate that native marsupials are not naïve to the peril humans pose, substantially expanding the taxonomic and geographic scope of the growing experimental evidence that wildlife worldwide generally perceive humans as the planet's most frightening predator. Introduced fallow deer fled humans, but not more than other predators, which we suggest may result from their being introduced. Our results point to both challenges concerning marsupial conservation and opportunities for exploiting fear of humans as a wildlife management tool.

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.

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'.

Sex differences in the impact of social relationships on individual vocal signatures in grey mouse lemurs (Microcebus murinus).

Vocalizations coordinate social interactions between conspecifics by conveying information concerning the individual or group identity of the sender. Social accommodation is a form of vocal learning where social affinity is signalled by converging or diverging vocalizations with those of conspecifics. To investigate whether social accommodation is linked to the social lifestyle of the sender, we investigated sex-specific differences in social accommodation in a dispersed living primate, the grey mouse lemur (Microcebus murinus), where females form stable sleeping groups whereas males live solitarily. We used 482 trill calls of 36 individuals from our captive breeding colony to compare acoustic dissimilarity between individuals with genetic relatedness, social contact time and body weight. Our results showed that female trills become more similar the more time females spend with each other, independent of genetic relationship, suggesting vocal convergence. In contrast, male trills were affected more by genetic than social factors. However, focusing only on socialized males, increasing time as cage partners caused greater divergence in males' trills. Thus, grey mouse lemurs show the capacity for social accommodation, with females converging their trills to signal social closeness to sleeping group partners, whereas males do not adapt or diverge their trills to signal individual distinctiveness. 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'.

Not your private tête-à-tête: leveraging the power of higher-order networks to study animal communication.

Animal communication is frequently studied with conventional network representations that link pairs of individuals who interact, for example, through vocalization. However, acoustic signals often have multiple simultaneous receivers, or receivers integrate information from multiple signallers, meaning these interactions are not dyadic. Additionally, non-dyadic social structures often shape an individual's behavioural response to vocal communication. Recently, major advances have been made in the study of these non-dyadic, higher-order networks (e.g. hypergraphs and simplicial complexes). Here, we show how these approaches can provide new insights into vocal communication through three case studies that illustrate how higher-order network models can: (i) alter predictions made about the outcome of vocally coordinated group departures; (ii) generate different patterns of song synchronization from models that only include dyadic interactions; and (iii) inform models of cultural evolution of vocal communication. Together, our examples highlight the potential power of higher-order networks to study animal vocal communication. We then build on our case studies to identify key challenges in applying higher-order network approaches in this context and outline important research questions that these techniques could help answer. 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'.

Calling to the collective: contact calling rates within groups of disc-winged bats do not vary by kinship or association.

Many group-living animals coordinate social behaviours using contact calls, which can be produced for all group members or targeted at specific individuals. In the disc-winged bat, Thyroptera tricolor, group members use 'inquiry' and 'response' calls to coordinate daily movements into new roosts (furled leaves). Rates of both calls show consistent among-individual variation, but causes of within-individual variation remain unknown. Here, we tested whether disc-winged bats produce more contact calls towards group members with higher kinship or association. In 446 experimental trials, we recorded 139 random within-group pairs of one flying bat (producing inquiry calls for roost searching) and one roosting bat (producing response calls for roost advertising). Using generalized linear mixed-effect models (GLMM), we assessed how response and inquiry calling rates varied by sender, receiver, genetic kinship and co-roosting association rate. Calling rates varied consistently across senders but not by receiver. Response calling was influenced by inquiry calling rates, but neither calling rate was higher when the interacting pair had higher kinship or association. Rather than dyadic calling rates indicating within-group relationships, our findings are consistent with the hypothesis that bats produce contact calls to maintain contact with any or all individuals within a group while collectively searching for a new roost site. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.