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Biology subjects

James, L. S.

Publications and source records attributed to James, L. S..

10 recordsLinked to original sources

BirdCODE: Detecting bird communication at scale

Deep learning-based animal sound identification is regularly applied to large audio datasets for ecological monitoring and citizen science, but existing methods lack the fine temporal resolution required to extract insights into animal communication from these same datasets. Here we introduce Bird Communication Detector (BirdCODE), a deep learning model that detects and classifies the vocalizations of over 9000 bird species with precise temporal boundaries, a several hundredfold increase the number of species over previous bioacoustic sound event detection models. In extensive benchmarking, BirdCODE achieves state-of-the-art performance in detection and classification of bird sounds. Applying BirdCODE to 1.3M citizen-science recordings, we present four case studies of how BirdCODE-computed sound event boundaries can be used to carry out phylogenetic analyses, to describe geographic and temporal variation in acoustic communication, and to characterize cross-species interactions. Together, these demonstrate how BirdCODE can enable large-scale, data-driven studies of bird communication. Model code, weights, and predictions are publicly available.

bioinformatics↗

Repertoire-wide contextual mapping reveals signal functions in cooperatively breeding crows

Communication structures society, and is likewise shaped by relationships and shared tasks; yet, for most socially complex species, we know little of their full vocal repertoire and its functions. We investigated how communication structures the who, what, and when of social interactions in cooperative carrion crows - group-living birds who rely on coordinated behaviors, as in chick care. Leveraging machine learning to integrate large-scale data from crow-borne audio-loggers and nest cameras, we charted the vocal repertoire across 24 cooperative groups and mapped all discovered call types to behaviors and social context. We found that crows used a rich repertoire across three domains of joint behavior - flocking, chick care, and territorial display. Relatively quiet call types were abundant and included close-range calls that may coordinate chick care by announcing nest visits. Our study demonstrates how combining continuous-capture data and machine learning can reveal a holistic understanding of how vocalizations function across contexts.

animal behavior and cognition↗

Zebra finch females flexibly communicate with each other and with AI-driven acoustic interaction models

Vocal interactions are fundamental for social functioning across animals, including humans. The diverse rules underlying these exchanges remain largely unknown, and emerging AI technologies offer promising avenues for investigation. We used computational tools to collect and analyze >1,000 hours of vocal interactions between female zebra finches and discovered that their interactions were characterized by correlated call production and structure, rapid acoustic modulation, and response selectivity. To test these interaction rules, we developed a generative audio large language model (ZF-AIM Acoustic Interaction Model) that engaged in real-time vocal exchanges with birds. When birds interacted with ZF-AIM, their vocal production and flexibility recapitulated key naturalistic features, which did not happen with non-interactive playbacks. Targeted ablations of ZF-AIM revealed that call timing and structure differentially contribute to natural vocal interactions. Using these AI-animal interactions, we demonstrate how AI can be leveraged to reveal fundamental rules underlying animal communication.

animal behavior and cognition↗

Humans share acoustic preferences with other animals

Many animals produce sounds during courtship and receivers prefer some sounds over others. Shared ancestry and convergent evolution may generate similarities in preference across species and could underlie Darwins conjecture that some animals "have nearly the same taste for the beautiful as we have". Here, we show that humans share acoustic preferences with a wide range of animals, that the strength of human preferences correlates with that in other animals, and that human responses are quicker when in agreement with animals. Furthermore, we found greatest agreement in preference for adorned, evolutionarily ancestral, and lower frequency sounds. Humans music listening experience was associated with preferences. These results are consistent with theories arguing that biases in sensory and cognitive processing sculpt acoustic preferences and confirm Darwins century-old hunch about the conservation of aesthetics in nature.

animal behavior and cognition↗

If memory serves: Multisensory male display improves female memory during mate sampling

Across many taxa, males gather in leks to perform multisensory courtship displays for females. At a lek, changes in the sensory scene over the course of mate evaluation are inevitable. This dynamic nature makes a females ability to recall the location of individual signalers an important component of female mate choice. It is hypothesized that complex (especially multimodal) displays may improve a females ability to remember and thus discriminate amongst potential mates. To test this hypothesis, we presented female tungara frogs (Physalaemus (=Engystomops) pustulosus) with male calls (auditory) and robotic frogs (visual) that could later be obstructed from view via the lowering of blinds. Specifically, we asked if the visual component of a multimodal display improves the ability of a receiver to remember a signaler. While our initial experiment did not find memory instantiation in female frogs, subsequent experiments with a longer presentation time and a brief period of silence successfully instantiated memories in females. Moreover, females continued to demonstrate significant preferences for calls associated with the visual cue even after 25 s following the obstruction of the visual stimulus (robotic frog). Thus, we propose that the duration of presentation and/or the silent period impact memory capability. Silence is common in choruses, and our data suggest that complex, multisensory stimuli may have evolved to help females remember their preferred mate even with such fluctuations in signal production. LAY SUMMARYMultisensory signals function to stimulate one or more of a receivers senses, and in doing so, may make signalers more memorable to receivers. Multisensory signals are common in mating displays, including the advertisement of a male tungara frog: a call (acoustic) and a vocal sac inflation (visual). Here, we demonstrate that female tungara frogs were more likely to remember a multisensory male display over a unisensory display, but only after fluctuations in the signals intensity.

animal behavior and cognition↗

Pervasive patterns in the songs of passerine birds resemble human music universals and are linked with production and cognitive mechanisms

Music is a complex learned behavior that is ubiquitous among humans, and many musical patterns are shared across geography and cultures ("music universals"). Knowing whether these universals are specific to humans or shared with other animals is important to understand how production-related factors (motor biases and constraints) or cognitive factors (learning) contribute to the emergence of these acoustic patterns. Bird song is often described as an animal analogue of human music, and some studies of individual avian species highlight acoustic similarities between bird song and music. However, expansive and comparative approaches are necessary to identify universal patterns within bird song, reveal mechanisms associated with these patterns, and draw parallels to music universals. Here, we adopt such an approach and analyze the prevalence of acoustic patterns (sequences) across [~]300 species of passerines, spanning both oscines (songbirds; vocal learners) and their sister clade, suboscines (passerines that produce songs that are not learned), as well as within a global corpus of human vocal music. This approach allowed us to directly test hypotheses that phonation mechanisms or vocal learning shape the emergence of universal patterns. We first document acoustic patterns that were widely shared across passerines and similar to music universals (e.g., small pitch intervals), highlighting the role of shared vocal production mechanisms in these patterns. Consistent with a contribution of vocal learning, we observed patterns (e.g., alternation in durations) there were more similar between oscines and humans than between suboscines and humans. Interestingly, we also discovered patterns (e.g., pitch alternation) that were inconsistent with a contribution of vocal learning and were more similar between suboscines and humans than between oscines and humans. This research provides the broadest evidence of shared universals in vocal performance across birds and humans and highlights convergent mechanisms shaping communication patterns.

animal behavior and cognition↗

Temporal variability enhances vocal learning

Species-typical behaviors are organized into species-typical patterns, and deviations away from these patterns often diminish the strength of behavioral and sensory responses to such stimuli. In songbirds like the zebra finch, species-typical songs consist of acoustic elements (syllables) arranged into stereotyped (i.e., highly predictable) sequences with stereotyped timing. However, the degree to which deviations away from these stereotyped temporal patterns modulate the strength of vocal learning (i.e., the fidelity of vocal imitation) remains unknown. Here we tutored 123 juvenile zebra finches with stimuli that varied in the stereotypy of syllable sequencing and timing. In contrast to the prediction that deviations away from species-typical stereotypy would diminish vocal learning, deviations from sequence or timing stereotypy did not decrease how well juveniles imitated the acoustic structure of syllables. Moreover, presenting syllables in species-atypical sequences (i.e., randomized syllable sequences) enhanced vocal imitation in birds that were tutored later in development. This unexpected enhancement of birdsong learning by sequence variability resembles the effects of contextual diversity on speech acquisition and indicates that such variability can benefit learning even for very stereotyped behaviors. SIGNIFICANCE STATEMENTLittle is known about the degree to which the temporal patterning of acoustic elements ("syllables") modulates vocal learning and imitation. We tested the contribution of temporal variability in syllable sequencing and timing, hypothesizing that deviations away from species-typical stereotypy (predictability) in syllable sequence and timing patterns would diminish the strength of vocal learning. In contrast to our predictions, deviations from sequence and timing stereotypy did not decrease vocal learning. Moreover, presenting syllables in random sequences enhanced vocal imitation in birds that were tutored later in development. This unexpected finding highlights that sequence complexity can potentiate vocal learning in individuals with more developed vocal control, resembling how complexity and ability interact to modulate various forms of learning in humans.

animal behavior and cognition↗

Fidelity of and biases in the developmental acquisition of song tempo in a songbird

The temporal organization of sounds used in social contexts can provide information about signal function and evoke varying responses in listeners (receivers). For example, music is a universal and learned human behavior that is characterized by different rhythms and tempos that can evoke disparate responses in listeners. Similarly, birdsong is a ubiquitous social behavior in birds that is learned during critical periods in development and used to evoke physiological and behavioral responses in listeners. Recent investigations have begun to reveal the breadth of universal patterns in birdsong and their similarity to common patterns in speech and music, but relatively little is known about the degree to which biological predispositions and developmental experiences interact to shape the temporal patterning of birdsong. Here, we investigated how biological predispositions modulate the acquisition and production of an important temporal feature of birdsong, namely the duration of silent intervals ("gaps") between vocal elements ("syllables"). Through analyses of semi-naturally raised and experimentally tutored zebra finches, we observed that juvenile zebra finches imitate the durations of the silent gaps in their tutors song with high fidelity and can "alter" the durations of gaps toward a central duration. When juveniles were experimentally tutored with stimuli containing a wide range of gap durations, we observed biases in the stereotypy but not in the central tendency of gap durations. Together, these studies demonstrate how biological predispositions and developmental experiences differently affect distinct temporal features of birdsong and highlight similarities in developmental plasticity across birdsong, speech, and music.

animal behavior and cognition↗

Introductory gestures before songbird vocal displays are shaped by learning and biological predispositions

Introductory gestures are present at the beginning of many animal displays. For example, lizards start their head-bobbing displays with introductory push-ups and animal vocal displays begin with introductory notes. Songbirds also begin their vocal displays by repeating introductory notes (INs) before producing their learned song and these INs are thought to reflect motor preparation. Between individuals of a given species, the acoustic structure of INs and the number of times INs are repeated before song varies considerably. While similar variation in songs between individuals is known to be a result of learning, whether INs are also learned remains poorly understood. Here, using natural and experimental tutoring with male zebra finches, we show that mean IN number and IN acoustic structure are learned from a tutor, independent of song learning. We also reveal biological predispositions in IN production; birds artificially tutored with songs lacking INs still repeated a short-duration syllable, thrice on average, before their songs. Overall, these results show that INs, just like elements in song, are shaped both by learning and biological predispositions and suggest multiple, independent, learning processes underlying the acquisition of complex vocal displays.

animal behavior and cognition↗

Behavioural responses to video and live presentations of females reveal a dissociation between performance and motivational aspects of birdsong

Understanding the regulation of social behavioural expression requires insight into motivational and performance aspects of social behaviours. While a number of studies have independently investigated motivational or performance aspects of social behaviours, few have examined how these aspects relate to each other. By comparing behavioural variation in response to live or video presentations of conspecific females, we analysed how variation in the motivation to produce courtship song covaries with variation in performance aspects of courtship song in male zebra finches (Taeniopygia guttata). Consistent with previous reports, we observed that male zebra finches were less motivated to produce courtship songs to videos of females than to live presentations of females. However, we found that acoustic features that reflect song performance were indistinguishable between songs produced to videos of females and songs produced to live presentations of females. For example, songs directed at video presentations of females were just as fast and stereotyped as songs directed at live females. These experimental manipulations and correlational analyses reveal a dissociation between motivational and performance aspects of birdsong and suggest a refinement of neural models of song production and control. In addition, they support the efficacy of videos to study both motivational and performance aspects of social behaviours.

animal behavior and cognition↗