Publications

Abstract

The appreciation of music is a universal trait of humankind.1,2,3 Evidence supporting this notion includes the ubiquity of music across cultures4,5,6,7 and the natural predisposition toward music that humans display early in development.8,9,10 Are we musical animals because of species-specific predispositions? This question cannot be answered by relying on cross-cultural or developmental studies alone, as these cannot rule out enculturation.11 Instead, it calls for cross-species experiments testing whether homologous neural mechanisms underlying music perception are present in non-human primates. We present music to two rhesus monkeys, reared without musical exposure, while recording electroencephalography (EEG) and pupillometry. Monkeys exhibit higher engagement and neural encoding of expectations based on the previously seeded musical context when passively listening to real music as opposed to shuffled controls. We then compare human and monkey neural responses to the same stimuli and find a species-dependent contribution of two fundamental musical features—pitch and timing12—in generating expectations: while timing- and pitch-based expectations13 are similarly weighted in humans, monkeys rely on timing rather than pitch. Together, these results shed light on the phylogeny of music perception. They highlight monkeys’ capacity for processing temporal structures beyond plain acoustic processing, and they identify a species-dependent contribution of time- and pitch-related features to the neural encoding of musical expectations.

Abstract

Biological structures are defined by rigid elements, such as bones, and elastic elements, like muscles and membranes. Computer vision advances have enabled automatic tracking of moving animal skeletal poses. Such developments provide insights into complex time-varying dynamics of biological motion. Conversely, the elastic soft-tissues of organisms, like the nose of elephant seals, or the buccal sac of frogs, are poorly studied and no computer vision methods have been proposed. This leaves major gaps in different areas of biology. In primatology, most critically, the function of air sacs is widely debated; many open questions on the role of air sacs in the evolution of animal communication, including human speech, remain unanswered. To support the dynamic study of soft-tissue structures, we present a toolkit for the automated tracking of semi-circular elastic structures in biological video data. The toolkit contains unsupervised computer vision tools (using Hough transform) and supervised deep learning (by adapting DeepLabCut) methodology to track inflation of laryngeal air sacs or other biological spherical objects (e.g., gular cavities). Confirming the value of elastic kinematic analysis, we show that air sac inflation correlates with acoustic markers that likely inform about body size. Finally, we present a pre-processed audiovisual-kinematic dataset of 7+ hours of closeup audiovisual recordings of siamang (Symphalangus syndactylus) singing. This toolkit (https://github.com/WimPouw/AirSacTracker) aims to revitalize the study of non-skeletal morphological structures across multiple species.

Abstract

Harbor seals (Phoca vitulina) are more solitary than many other pinnipeds. Yet, they are capable of vocal learning, a form of social learning. Most extant literature examines social animals when investigating social learning, despite sociality not being a prerequisite. Here, we report two formerly silent harbor seals who initiated vocalizations, after having repeatedly observed a conspecific receiving food rewards for vocalizing. Our observations suggest both social and vocal learning in a group of captive harbor seals, a species that lives semi-solitarily in the wild. We propose that, in this case, social learning acted as a shortcut to acquiring food rewards compared to the comparatively costly asocial learning.

Abstract

Background

Which mammals show vocal learning abilities, e.g., can learn new sounds, or learn to use sounds in new contexts? Vocal usage and comprehension learning are submodules of vocal learning. Specifically, vocal usage learning is the ability to learn to use a vocalization in a new context; vocal comprehension learning is the ability to comprehend a vocalization in a new context. Among mammals, harbor seals (Phoca vitulina) are good candidates to investigate vocal learning. Here, we test whether harbor seals are capable of vocal usage and comprehension learning.

Results

We trained two harbor seals to (i) switch contexts from a visual to an auditory cue. In particular, the seals first produced two vocalization types in response to two hand signs; they then transitioned to producing these two vocalization types upon the presentation of two distinct sets of playbacks of their own vocalizations. We then (ii) exposed the seals to a combination of trained and novel vocalization stimuli. In a final experiment, (iii) we broadcasted only novel vocalizations of the two vocalization types to test whether seals could generalize from the trained set of stimuli to only novel items of a given vocal category. Both seals learned all tasks and took ≤ 16 sessions to succeed across all experiments. In particular, the seals showed contextual learning through switching the context from former visual to novel auditory cues, vocal matching and generalization. Finally, by responding to the played-back vocalizations with distinct vocalizations, the animals showed vocal comprehension learning.

Conclusions

It has been suggested that harbor seals are vocal learners; however, to date, these observations had not been confirmed in controlled experiments. Here, through three experiments, we could show that harbor seals are capable of both vocal usage and comprehension learning.

Abstract

Formants, or resonance frequencies of the upper vocal tract, are an essential part of acoustic communication. Articulatory gestures—such as jaw, tongue, lip, and soft palate movements—shape formant structure in human vocalizations, but little is known about how nonhuman mammals use those gestures to modify formant frequencies. Here, we report a case study with an adult male harbor seal trained to produce an arbitrary vocalization composed of multiple repetitions of the sound wa. We analyzed jaw movements frame-by-frame and matched them to the tracked formant modulation in the corresponding vocalizations. We found that the jaw opening angle was strongly correlated with the first (F1) and, to a lesser degree, with the second formant (F2). F2 variation was better explained by the jaw angle opening when the seal was lying on his back rather than on the belly, which might derive from soft tissue displacement due to gravity. These results show that harbor seals share some common articulatory traits with humans, where the F1 depends more on the jaw position than F2. We propose further in vivo investigations of seals to further test the role of the tongue on formant modulation in mammalian sound production.

Abstract

The search for common characteristics between the musical abilities of humans and other animal species is still taking its first steps. One of the most promising aspects from a comparative point of view is the analysis of rhythmic components, which are crucial features of human communicative performance but also well-identifiable patterns in the vocal displays of other species. Therefore, the study of rhythm is becoming essential to understand the mechanisms of singing behavior and the evolution of human communication. Recent findings provided evidence that particular rhythmic structures occur in human music and some singing animal species, such as birds and rock hyraxes, but only 2 species of nonhuman primates have been investigated so far (Indri indri and Hylobates lar). Therefore, our study aims to consistently broaden the list of species studied regarding the presence of rhythmic categories. We investigated the temporal organization in the singing of 3 species of crested gibbons (Nomascus gabriellae, Nomascus leucogenys, and Nomascus siki) and found that the most prominent rhythmic category was isochrony. Moreover, we found slight variation in songs’ tempo among species, with N. gabriellae and N. siki singing with a temporal pattern involving a gradually increasing tempo (a musical accelerando), and N. leucogenys with a more regular pattern. Here, we show how the prominence of a peak at the isochrony establishes itself as a shared characteristic in the small apes considered so far.

Abstract

Animal songs differ from calls in function and structure, and have comparative and translational value, showing similarities to human music. Rhythm in music is often distributed in quantized classes of intervals known as rhythmic categories. These classes have been found in the songs of a few nonhuman species but never in their calls. Are rhythmic categories song-specific, as in human music, or can they transcend the song–call boundary? We analyze the vocal displays of one of the few mammals producing both songs and call sequences: Indri indri. We test whether rhythmic categories (a) are conserved across songs produced in different contexts, (b) exist in call sequences, and (c) differ between songs and call sequences. We show that rhythmic categories occur across vocal displays. Vocalization type and function modulate deployment of categories. We find isochrony (1:1 ratio, like the rhythm of a ticking clock) in all song types, but only advertisement songs show three rhythmic categories (1:1, 1:2, 2:1 ratios). Like songs, some call types are also isochronous. Isochrony is the backbone of most indri vocalizations, unlike human speech, where it is rare. In indri, isochrony underlies both songs and hierarchy-less call sequences and might be ancestral to both.

Abstract

Research on language evolution is an established subject area yet permeated by terminological controversies about which topics should be considered pertinent to the field and which not. By consequence, scholars focusing on language evolution struggle in providing precise demarcations of the discipline, where even the very central notions of evolution and language are elusive. We aimed at providing a data-driven characterisation of language evolution as a field of research by relying on quantitative analysis of data drawn from 697 reviews on 255 submissions from the Joint Conference on Language Evolution 2022 (Kanazawa, Japan). Our results delineate a field characterized by a core of main research topics such as iconicity, sign language, multimodality. Despite being explored within the framework of language evolution research, only very recently these topics became popular in linguistics. As a result, language evolution has the potential to emerge as a forefront of linguistic research, bringing innovation to the study of language. We also see the emergence of more recent topics like rhythm, music, and vocal learning. Furthermore, the community identifies cognitive science, primatology, archaeology, palaeoanthropology, and genetics as key areas, encouraging empirical rather than theoretical work. With new themes, models, and methodologies emerging, our results depict an intrinsically multidisciplinary and evolving research field, likely adapting as language itself.

Abstract

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.

Abstract

Bioacoustics increasingly relies on large datasets and computational methods. The need to batch-process large amounts of data and the increased focus on algorithmic processing require software tools. To optimally assist in a bioacoustician’s workflow, software tools need to be as simple and effective as possible. Five years ago, the Python package Parselmouth was released to provide easy and intuitive access to all functionality in the Praat software. Whereas Praat is principally designed for phonetics and speech processing, plenty of bioacoustics studies have used its advanced acoustic algorithms. Here, we evaluate existing usage of Parselmouth and discuss in detail several studies which used the software library. We argue that Parselmouth has the potential to be used even more in bioacoustics research, and suggest future directions to be pursued with the help of Parselmouth.

Abstract

Multimodal rhythmic signalling abounds across animal taxa. Studying its mechanisms and functions can highlight adaptive components in highly complex rhythmic behaviours, like dance and music. Pinnipeds, such as the harbour seal, Phoca vitulina, are excellent comparative models to assess rhythmic capacities. Harbour seals engage in rhythmic percussive behaviours which, until now, have not been described in detail. In our study, eight zoo-housed harbour seals (two pups, two juveniles and four adults) were passively monitored by audio and video during their pupping/breeding season. All juvenile and adult animals performed percussive signalling with their fore flippers in agonistic conditions, both on land and in water. Flipper slap sequences produced on the ground or on the seals' bodies were often highly regular in their interval duration, that is, were quasi-isochronous, at a 200–600 beats/min pace. Three animals also showed significant lateralization in slapping. In contrast to slapping on land, display slapping in water, performed only by adult males, showed slower tempo by one order of magnitude, and a rather motivic temporal structure. Our work highlights that percussive communication is a significant part of harbour seals' behavioural repertoire. We hypothesize that its forms of rhythm production may reflect adaptive functions such as regulating internal states and advertising individual traits.

Abstract

Recursive procedures that allow placing a vocal signal inside another of a similar kind provide a neuro-computational blueprint for syntax and phonology in spoken language and human song. There are, however, no known vocal sequences among nonhuman primates arranged in self-embedded patterns that evince vocal recursion or potential incipient or evolutionary transitional forms thereof, suggesting a neuro-cognitive transformation exclusive to humans. Here, we uncover that wild flanged male orangutan long calls feature rhythmically isochronous call sequences nested within isochronous call sequences, consistent with two hierarchical strata. Remarkably, three temporally and acoustically distinct call rhythms in the lower stratum were not related to the overarching rhythm at the higher stratum by any low multiples, which suggests that these recursive structures were neither the result of parallel non-hierarchical procedures nor anatomical artifacts of bodily constraints or resonances. Findings represent a case of temporally recursive hominid vocal combinatorics in the absence of syntax, semantics, phonology, or music. Second-order combinatorics, ‘sequences within sequences’, involving hierarchically organized and cyclically structured vocal sounds in ancient hominids may have preluded the evolution of recursion in modern language-able humans.

Abstract

Tail wagging is a conspicuous behaviour in domestic dogs (Canis familiaris). Despite how much meaning humans attribute to this display, its quantitative description and evolutionary history are rarely studied. We summarize what is known about the mechanism, ontogeny, function and evolution of this behaviour. We suggest two hypotheses to explain its increased occurrence and frequency in dogs compared to other canids. During the domestication process, enhanced rhythmic tail wagging behaviour could have (i) arisen as a by-product of selection for other traits, such as docility and tameness, or (ii) been directly selected by humans, due to our proclivity for rhythmic stimuli. We invite testing of these hypotheses through neurobiological and ethological experiments, which will shed light on one of the most readily observed yet understudied animal behaviours. Targeted tail wagging research can be a window into both canine ethology and the evolutionary history of characteristic human traits, such as our ability to perceive and produce rhythmic behaviours.

Abstract

Sound and movement are entangled in animal communication. This is obviously true in the case of sound-constituting vibratory movements of biological structures which generate acoustic waves. A little less obvious is that other moving structures produce the energy required to sustain these vibrations. In many species, the respiratory system moves to generate the expiratory flow which powers the sound-constituting movements (sound-powering movements). The sound may acquire additional structure via upper tract movements, such as articulatory movements or head raising (sound-filtering movements). Some movements are not necessary for sound production, but when produced, impinge on the sound-producing process due to weak biomechanical coupling with body parts (e.g., respiratory system) that are necessary for sound production (sound-impinging movements). Animals also produce sounds contingent with movement, requiring neuro-physiological control regimes allowing to flexibly couple movements to a produced sound, or coupling movements to a perceived external sound (sound-contingent movement). Here, we compare and classify the variety of ways sound and movements are coupled in animal communication; our proposed framework should help structure previous and future studies on this topic.

Abstract

Several animal species prefer consonant over dissonant sounds, a building block of musical scales and harmony. Could consonance and dissonance be linked, beyond music, to the emotional valence of vocalizations? We extracted the fundamental frequency from calls of young chickens with either positive or negative emotional valence, i.e. contact, brood and food calls. For each call, we calculated the frequency ratio between the maximum and the minimum values of the fundamental frequency, and we investigated which frequency ratios occurred with higher probability. We found that, for all call types, the most frequent ratios matched perfect consonance, like an arpeggio in pop music. These music-like intervals, based on the auditory frequency resolution of chicks, cannot be miscategorized into contiguous dissonant intervals. When we analysed frequency ratio distributions at a finer-grained level, we found some dissonant ratios in the contact calls produced during distress only, thus sounding a bit jazzy. Complementing the empirical data, our computational simulations suggest that physiological constraints can only partly explain both consonances and dissonances in chicks’ phonation. Our data add to the mounting evidence that the building blocks of human musical traits can be found in several species, even phylogenetically distant from us.

Abstract

Animal vocal communication often relies on call sequences. The temporal patterns of such sequences can be adjusted to other callers, follow complex rhythmic structures or exhibit a metronome-like pattern (i.e., isochronous). How regular are the temporal patterns in animal signals, and what influences their precision? If present, are rhythms already there early in ontogeny? Here, we describe an exploratory study of Cape fur seal (Arctocephalus pusillus pusillus) barks—a vocalisation type produced across many pinniped species in rhythmic, percussive bouts. This study is the first quantitative description of barking in Cape fur seal pups. We analysed the rhythmic structures of spontaneous barking bouts of pups and adult females from the breeding colony in Cape Cross, Namibia. Barks of adult females exhibited isochrony, that is they were produced at fairly regular points in time. Instead, intervals between pup barks were more variable, that is skipping a bark in the isochronous series occasionally. In both age classes, beat precision, that is how well the barks followed a perfect template, was worse when barking at higher rates. Differences could be explained by physiological factors, such as respiration or arousal. Whether, and how, isochrony develops in this species remains an open question. This study provides evidence towards a rhythmic production of barks in Cape fur seal pups and lays the groundwork for future studies to investigate the development of rhythm using multidimensional metrics.

Abstract

Both music and language are found in all known human societies, yet no studies have compared similarities and differences between song, speech, and instrumental music on a global scale. In this Registered Report, we analyzed two global datasets: (i) 300 annotated audio recordings representing matched sets of traditional songs, recited lyrics, conversational speech, and instrumental melodies from our 75 coauthors speaking 55 languages; and (ii) 418 previously published adult-directed song and speech recordings from 209 individuals speaking 16 languages. Of our six preregistered predictions, five were strongly supported: Relative to speech, songs use (i) higher pitch, (ii) slower temporal rate, and (iii) more stable pitches, while both songs and speech used similar (iv) pitch interval size and (v) timbral brightness. Exploratory analyses suggest that features vary along a “musi-linguistic” continuum when including instrumental melodies and recited lyrics. Our study provides strong empirical evidence of cross-cultural regularities in music and speech.

Abstract

thebeat is a Python package for working with temporal sequences and rhythms in the behavioral and cognitive sciences, as well as in bioacoustics. It provides functionality for creating experimental stimuli, and for visualizing and analyzing temporal data. Sequences, sounds, and experimental trials can be generated using single lines of code. thebeat contains functions for calculating common rhythmic measures, such as interval ratios, and for producing plots, such as circular histograms. thebeat saves researchers time when creating experiments, and provides the first steps in collecting widely accepted methods for use in timing research. thebeat is an open-source, on-going, and collaborative project, and can be extended for use in specialized subfields. thebeat integrates easily with the existing Python ecosystem, allowing one to combine our tested code with custom-made scripts. The package was specifically designed to be useful for both skilled and novice programmers. thebeat provides a foundation for working with temporal sequences onto which additional functionality can be built. This combination of specificity and plasticity should facilitate research in multiple research contexts and fields of study.

Abstract

Rhythmic patterns in interactive contexts characterize human behaviours such as conversational turn-taking. These timed patterns are also present in other animals, and often described as rhythm. Understanding fine-grained temporal adjustments in interaction requires complementary quantitative methodologies. Here, we showcase how vocal interactive rhythmicity in a non-human animal can be quantified using a multi-method approach. We record vocal interactions in harbour seal pups (Phoca vitulina) under controlled conditions. We analyse these data by combining analytical approaches, namely categorical rhythm analysis, circular statistics and time series analyses. We test whether pups' vocal rhythmicity varies across behavioural contexts depending on the absence or presence of a calling partner. Four research questions illustrate which analytical approaches are complementary versus orthogonal. For our data, circular statistics and categorical rhythms suggest that a calling partner affects a pup's call timing. Granger causality suggests that pups predictively adjust their call timing when interacting with a real partner. Lastly, the ADaptation and Anticipation Model estimates statistical parameters for a potential mechanism of temporal adaptation and anticipation. Our analytical complementary approach constitutes a proof of concept; it shows feasibility in applying typically unrelated techniques to seals to quantify vocal rhythmic interactivity across behavioural contexts.

Abstract

Learning can occur via trial and error; however, learning from conspecifics is faster and more efficient. Social animals can easily learn from conspecifics, but how do less social species learn? In particular, birds provide astonishing examples of social learning of vocalizations, while vocal learning from conspecifics is much less understood in mammals. We present a hypothesis aimed at solving an apparent paradox: how can harbor seals (Phoca vitulina) learn their song when their whole lives are marked by loose conspecific social contact? Harbor seal pups are raised individually by their mostly silent mothers. Pups' first few weeks of life show developed vocal plasticity; these weeks are followed by relatively silent years until sexually mature individuals start singing. How can this rather solitary life lead to a learned song? Why do pups display vocal plasticity at a few weeks of age, when this is apparently not needed? Our hypothesis addresses these questions and tries to explain how vocal learning fits into the natural history of harbor seals, and potentially other less social mammals. We suggest that harbor seals learn during a sensitive period within puppyhood, where they are exposed to adult males singing. In particular, we hypothesize that, to make this learning possible, the following happens concurrently: (1) mothers give birth right before male singing starts, (2) pups enter a sensitive learning phase around weaning time, which (3) coincides with their foraging expeditions at sea which, (4) in turn, coincide with the peak singing activity of adult males. In other words, harbor seals show vocal learning as pups so they can acquire elements of their future song from adults, and solitary adults can sing because they have acquired these elements as pups. We review the available evidence and suggest that pups learn adult vocalizations because they are born exactly at the right time to eavesdrop on singing adults. We conclude by advancing empirical predictions and testable hypotheses for future work.

Abstract

Studies of rhythm processing and of reward have progressed separately, with little connection between the two. However, consistent links between rhythm and reward are beginning to surface, with research suggesting that synchronization to rhythm is rewarding, and that this rewarding element may in turn also boost this synchronization. The current mini review shows that the combined study of rhythm and reward can be beneficial to better understand their independent and combined roles across two central aspects of cognition: 1) learning and memory, and 2) social connection and interpersonal synchronization; which have so far been studied largely independently. From this basis, it is discussed how connections between rhythm and reward can be applied to learning and memory and social connection across different populations, taking into account individual differences, clinical populations, human development, and animal research. Future research will need to consider the rewarding nature of rhythm, and that rhythm can in turn boost reward, potentially enhancing other cognitive and social processes.

Abstract

The last few years have revealed that several species may share the building blocks of Musicality with humans. The recognition of these building blocks (e.g., rhythm, frequency variation) was a necessary impetus for a new round of studies investigating rhythmic variation in animal vocal displays. Singing primates are a small group of primate species that produce modulated songs ranging from tens to thousands of vocal units. Previous studies showed that the indri, the only singing lemur, is currently the only known species that perform duet and choruses showing multiple rhythmic categories, as seen in human music. Rhythmic categories occur when temporal intervals between note onsets are not uniformly distributed, and rhythms with a small integer ratio between these intervals are typical of human music. Besides indris, white-handed gibbons and three crested gibbon species showed a prominent rhythmic category corresponding to a single small integer ratio, isochrony. This study reviews previous evidence on the co-occurrence of rhythmic categories in primates and focuses on the prospects for a comparative, multimodal study of rhythmicity in this clade.

Abstract

Rhythmicity in the millisecond to second range is a fundamental building block of communication and coordinated movement. But how widespread are rhythmic capacities across species, and how did they evolve under different environmental pressures? Comparative research is necessary to answer these questions but has been hindered by limited crosstalk and comparability among results from different study species.
Most acoustics studies do not explicitly focus on characterising or quantifying rhythm, but many are just a few scrapes away from contributing to and advancing the field of comparative rhythm research. Here, we present an eight-level rhythm reporting framework which details actionable steps researchers can take to report rhythm-relevant metrics. Levels fall into two categories: metric reporting and data sharing. Metric reporting levels include defining rhythm-relevant metrics, providing point estimates of temporal interval variability, reporting interval distributions, and conducting rhythm analyses. Data sharing levels are: sharing audio recordings, sharing interval durations, sharing sound element start and end times, and sharing audio recordings with sound element start/end times.
Using sounds recorded from a sperm whale as a case study, we demonstrate how each reporting framework level can be implemented on real data. We also highlight existing best practice examples from recent research spanning multiple species. We clearly detail how engagement with our framework can be tailored case-by-case based on how much time and effort researchers are willing to contribute. Finally, we illustrate how reporting at any of the suggested levels will help advance comparative rhythm research.
This framework will actively facilitate a comparative approach to acoustic rhythms while also promoting cooperation and data sustainability. By quantifying and reporting rhythm metrics more consistently and broadly, new avenues of inquiry and several long-standing, big picture research questions become more tractable. These lines of research can inform not only about the behavioural ecology of animals but also about the evolution of rhythm-relevant phenomena and the behavioural neuroscience of rhythm production and perception. Rhythm is clearly an emergent feature of life; adopting our framework, researchers from different fields and with different study species can help understand why.

Abstract

To communicate, an animal's strategic timing of rhythmic signals is crucial. Evolutionary, game-theoretical, and dynamical systems models can shed light on the interaction between individuals and the associated costs and benefits of signalling at a specific time. Mathematical models that study rhythmic interactions from a strategic or evolutionary perspective are rare in animal communication research. But new inspiration may come from a recent game theory model of how group synchrony emerges from local interactions of oscillatory neurons. In the study, the authors analyse when the benefit of joint synchronization outweighs the cost of individual neurons sending electrical signals to each other. They postulate there is a benefit for pairs of neurons to fire together and a cost for a neuron to communicate. The resulting model delivers a variant of a classical dynamical system, the Kuramoto model. Here, we present an accessible overview of the Kuramoto model and evolutionary game theory, and of the 'oscillatory neurons' model. We interpret the model's results and discuss the advantages and limitations of using this particular model in the context of animal rhythmic communication. Finally, we sketch potential future directions and discuss the need to further combine evolutionary dynamics, game theory and rhythmic processes in animal communication studies.

Abstract

Objective

Researchers in animal cognition, psychophysics, and experimental psychology need to randomise the presentation order of trials in experimental sessions. In many paradigms, for each trial, one of two responses can be correct, and the trials need to be ordered such that the participant’s responses are a fair assessment of their performance. Specifically, in some cases, especially for low numbers of trials, randomised trial orders need to be excluded if they contain simple patterns which a participant could accidentally match and so succeed at the task without learning.
Results

We present and distribute a simple Python software package and tool to produce pseudorandom sequences following the Gellermann series. This series has been proposed to pre-empt simple heuristics and avoid inflated performance rates via false positive responses. Our tool allows users to choose the sequence length and outputs a .csv file with newly and randomly generated sequences. This allows behavioural researchers to produce, in a few seconds, a pseudorandom sequence for their specific experiment. PyGellermann is available at https://github.com/YannickJadoul/PyGellermann.

Abstract

Most bioacoustics software is used to analyse the already collected acoustics data in batch, i.e., after the data-collecting phase of a scientific study. However, experiments based on animal training require immediate and precise reactions from the experimenter, and thus do not easily dovetail with a typical bioacoustics workflow. Bridging this methodological gap, we have developed a custom application to live-monitor the vocal development of harbour seals in a behavioural experiment. In each trial, the application records and automatically detects an animal's call, and immediately measures duration and acoustic measures such as intensity, fundamental frequency, or formant frequencies. It then displays a spectrogram of the recording and the acoustic measurements, allowing the experimenter to instantly evaluate whether or not to reinforce the animal's vocalisation. From a technical perspective, the rapid and easy development of this custom software was made possible by combining multiple open-source software projects. Here, we integrated the acoustic analyses from Parselmouth, a Python library for Praat, together with PyAudio and Matplotlib's recording and plotting functionality, into a custom graphical user interface created with PyQt. This flexible recombination of different open-source Python libraries allows the whole program to be written in a mere couple of hundred lines of code

Abstract

The intergenerational stability of auditory symbolic systems, such as music, is thought to rely on brain processes that allow the faithful transmission of complex sounds. Little is known about the functional and structural aspects of the human brain which support this ability, with a few studies pointing to the bilateral organization of auditory networks as a putative neural substrate. Here, we further tested this hypothesis by examining the role of left–right neuroanatomical asymmetries between auditory cortices. We collected neuroanatomical images from a large sample of participants (nonmusicians) and analyzed them with Freesurfer’s surface-based morphometry method. Weeks after scanning, the same individuals participated in a laboratory experiment that simulated music transmission: the signaling games. We found that high accuracy in the intergenerational transmission of an artificial tone system was associated with reduced rightward asymmetry of cortical thickness in Heschl’s sulcus. Our study suggests that the high-fidelity copying of melodic material may rely on the extent to which computational neuronal resources are distributed across hemispheres. Our data further support the role of interhemispheric brain organization in the cultural transmission and evolution of auditory symbolic systems.

Abstract

How did rhythm originate in humans, and other species? One cross-cultural universal, frequently found in human music, is isochrony: when note onsets repeat regularly like the ticking of a clock. Another universal consists in synchrony (e.g. when individuals coordinate their notes so that they are sung at the same time). An approach to biomusicology focuses on similarities and differences across species, trying to build phylogenies of musical traits. Here we test for the presence of, and a link between, isochrony and synchrony in a non-human animal. We focus on the songs of one of the few singing primates, the lar gibbon (Hylobates lar), extracting temporal features from their solo songs and duets. We show that another ape exhibits one rhythmic feature at the core of human musicality: isochrony. We show that an enhanced call rate overall boosts isochrony, suggesting that respiratory physiological constraints play a role in determining the song's rhythmic structure. However, call rate alone cannot explain the flexible isochrony we witness. Isochrony is plastic and modulated depending on the context of emission: gibbons are more isochronous when duetting than singing solo. We present evidence for rhythmic interaction: we find statistical causality between one individual's note onsets and the co-singer's onsets, and a higher than chance degree of synchrony in the duets. Finally, we find a sex-specific trade-off between individual isochrony and synchrony. Gibbon's plasticity for isochrony and rhythmic overlap may suggest a potential shared selective pressure for interactive vocal displays in singing primates. This pressure may have convergently shaped human and gibbon musicality while acting on a common neural primate substrate. Beyond humans, singing primates are promising models to understand how music and, specifically, a sense of rhythm originated in the primate phylogeny.

Abstract

The ability to control one's vocal production is a major advantage in acoustic communication. Yet, not all species have the same level of control over their vocal output. Several bird species can interrupt their song upon hearing an external stimulus, but there is no evidence how flexible this behavior is. Most research on corvids focuses on their cognitive abilities, but few studies explore their vocal aptitudes. Recent research shows that crows can be experimentally trained to vocalize in response to a brief visual stimulus. Our study investigated vocal control abilities with a more ecologically embedded approach in rooks. We show that two rooks could spontaneously coordinate their vocalizations to a long-lasting stimulus (the sound of their small bathing pool being filled with a water hose), one of them adjusting roughly (in the second range) its vocalizations as the stimuli began and stopped. This exploratory study adds to the literature showing that corvids, a group of species capable of cognitive prowess, are indeed able to display good vocal control abilities.

Abstract

Sociality and timing are tightly interrelated in human interaction as seen in turn-taking or synchronised dance movements. Sociality and timing also show in communicative acts of other species that might be pleasurable, but also necessary for survival. Sociality and timing often co-occur, but their shared phylogenetic trajectory is unknown: How, when, and why did they become so tightly linked? Answering these questions is complicated by several constraints; these include the use of divergent operational definitions across fields and species, the focus on diverse mechanistic explanations (e.g., physiological, neural, or cognitive), and the frequent adoption of anthropocentric theories and methodologies in comparative research. These limitations hinder the development of an integrative framework on the evolutionary trajectory of social timing and make comparative studies not as fruitful as they could be. Here, we outline a theoretical and empirical framework to test contrasting hypotheses on the evolution of social timing with species-appropriate paradigms and consistent definitions. To facilitate future research, we introduce an initial set of representative species and empirical hypotheses. The proposed framework aims at building and contrasting evolutionary trees of social timing toward and beyond the crucial branch represented by our own lineage. Given the integration of cross-species and quantitative approaches, this research line might lead to an integrated empirical-theoretical paradigm and, as a long-term goal, explain why humans are such socially coordinated animals.

Abstract

Dance is an icon of human expression. Despite astounding diversity around the world’s cultures and dazzling abundance of reminiscent animal systems, the evolution of dance in the human clade remains obscure. Dance requires individuals to interactively synchronize their whole-body tempo to their partner’s, with near-perfect precision. This capacity is motorically-heavy, engaging multiple neural circuitries, but also dependent on an acute socio-emotional bond between partners. Hitherto, these factors helped explain why no dance forms were present amongst nonhuman primates. Critically, evidence for conjoined full-body rhythmic entrainment in great apes that could help reconstruct possible proto-stages of human dance is still lacking. Here, we report an endogenously-effected case of ritualized dance-like behaviour between two captive chimpanzees – synchronized bipedalism. We submitted video recordings to rigorous time-series analysis and circular statistics. We found that individual step tempo was within the genus’ range of “solo” bipedalism. Between-individual analyses, however, revealed that synchronisation between individuals was non-random, predictable, phase concordant, maintained with instantaneous centi-second precision and jointly regulated, with individuals also taking turns as “pace-makers”. No function was apparent besides the behaviour’s putative positive social affiliation. Our analyses show a first case of spontaneous whole-body entrainment between two ape peers, thus providing tentative empirical evidence for phylogenies of human dance. Human proto-dance, we argue, may have been rooted in mechanisms of social cohesion among small groups that might have granted stress-releasing benefits via gait-synchrony and mutual-touch. An external sound/musical beat may have been initially uninvolved. We discuss dance evolution as driven by ecologically-, socially- and/or culturally-imposed “captivity”.

Abstract

We contrast two related hypotheses of the evolution of dance: H1: Maternal bipedal walking influenced the fetal experience of sound and associated movement patterns; H2: The human transition to bipedal gait produced more isochronous/predictable locomotion sound resulting in early music-like behavior associated with the acoustic advantages conferred by moving bipedally in pace. The cadence of walking is around 120 beats per minute, similar to the tempo of dance and music. Human walking displays long-term constancies. Dyads often subconsciously synchronize steps. The major amplitude component of the step is a distinctly produced beat. Human locomotion influences, and interacts with, emotions, and passive listening to music activates brain motor areas. Across dance-genres the footwork is most often performed in time to the musical beat. Brain development is largely shaped by early sensory experience, with hearing developed from week 18 of gestation. Newborns reacts to sounds, melodies, and rhythmic poems to which they have been exposed in utero. If the sound and vibrations produced by footfalls of a walking mother are transmitted to the fetus in coordination with the cadence of the motion, a connection between isochronous sound and rhythmical movement may be developed. Rhythmical sounds of the human mother locomotion differ substantially from that of nonhuman primates, while the maternal heartbeat heard is likely to have a similar isochronous character across primates, suggesting a relatively more influential role of footfall in the development of rhythmic/musical abilities in humans. Associations of gait, music, and dance are numerous. The apparent absence of musical and rhythmic abilities in nonhuman primates, which display little bipedal locomotion, corroborates that bipedal gait may be linked to the development of rhythmic abilities in humans. Bipedal stimuli in utero may primarily boost the ontogenetic development. The acoustical advantage hypothesis proposes a mechanism in the phylogenetic development.

Abstract

Time is one crucial dimension conveying information in animal communication. Evolution has shaped animals’ nervous systems to produce signals with temporal properties fitting their socio-ecological niches. Many quantitative models of mechanisms underlying rhythmic behaviour exist, spanning insects, crustaceans, birds, amphibians, and mammals. However, these computational and mathematical models are often presented in isolation. Here, we provide an overview of the main mathematical models employed in the study of animal rhythmic communication among conspecifics. After presenting basic definitions and mathematical formalisms, we discuss each individual model. These computational models are then compared using simulated data to uncover similarities and key differences in the underlying mechanisms found across species. Our review of the empirical literature is admittedly limited. We stress the need of using comparative computer simulations – both before and after animal experiments – to better understand animal timing in interaction. We hope this article will serve as a potential first step towards a common computational framework to describe temporal interactions in animals, including humans.

Abstract

The study of human language is progressively moving toward comparative and interactive frameworks, extending the concept of turn‐taking to animal communication. While such an endeavor will help us understand the interactive origins of language, any theoretical account for cross‐species turn‐taking should consider three key points. First, animal turn‐taking must incorporate biological studies on animal chorusing, namely how different species coordinate their signals over time. Second, while concepts employed in human communication and turn‐taking, such as intentionality, are still debated in animal behavior, lower level mechanisms with clear neurobiological bases can explain much of animal interactive behavior. Third, social behavior, interactivity, and cooperation can be orthogonal, and the alternation of animal signals need not be cooperative. Considering turn‐taking a subset of chorusing in the rhythmic dimension may avoid overinterpretation and enhance the comparability of future empirical work.

Abstract

Puppyhood is a very active social and vocal period in a harbor seal's life Phoca vitulina. An important feature of vocalizations is their temporal and rhythmic structure, and understanding vocal timing and rhythms in harbor seals is critical to a cross-species hypothesis in evolutionary neuroscience that links vocal learning, rhythm perception, and synchronization. This study utilized analytical techniques that may best capture rhythmic structure in pup vocalizations with the goal of examining whether (1) harbor seal pups show rhythmic structure in their calls and (2) rhythms evolve over time. Calls of 3 wild-born seal pups were recorded daily over the course of 1-3 weeks; 3 temporal features were analyzed using 3 complementary techniques. We identified temporal and rhythmic structure in pup calls across different time windows. The calls of harbor seal pups exhibit some degree of temporal and rhythmic organization, which evolves over puppyhood and resembles that of other species' interactive communication. We suggest next steps for investigating call structure in harbor seal pups and propose comparative hypotheses to test in other pinniped species.

Abstract

Comparative research investigating how nonhuman animals generalize patterns of auditory stimuli often uses sequences of human speech syllables and reports limited generalization abilities in animals. Here, we reverse this logic, testing humans with stimulus sequences tailored to squirrel monkeys. When test stimuli are familiar (human voices), humans succeed in two types of generalization. However, when the same structural rule is instantiated over unfamiliar but perceivable sounds within squirrel monkeys’ optimal hearing frequency range, human participants master only one type of generalization. These findings have methodological implications for the design of comparative experiments, which should be fair towards all tested species’ proclivities and limitations.

Abstract

Animal communication and motoric behavior develop over time. Often, this temporal dimension has communicative relevance and is organized according to structural patterns. In other words, time is a crucial dimension for rhythm and synchrony in animal movement and communication. Rhythm is defined as temporal structure at a second-millisecond time scale (Kotz et al. 2018). Synchrony is defined as precise co-occurrence of 2 behaviors in time (Ravignani 2017).

Rhythm, synchrony, and other forms of temporal interaction are taking center stage in animal behavior and communication. Several critical questions include, among others: what species show which rhythmic predispositions? How does a species’ sensitivity for, or proclivity towards, rhythm arise? What are the species-specific functions of rhythm and synchrony, and are there functional trends across species? How did similar or different rhythmic behaviors evolved in different species? This Special Column aims at collecting and contrasting research from different species, perceptual modalities, and empirical methods. The focus is on timing, rhythm and synchrony in the second-millisecond range.

Three main approaches are commonly adopted to study animal rhythms, with a focus on: 1) spontaneous individual rhythm production, 2) group rhythms, or 3) synchronization experiments. I concisely introduce them below (see also Kotz et al. 2018; Ravignani et al. 2018).

Abstract

Why does human speech have rhythm? As we cannot travel back in time to witness how speech developed its rhythmic properties and why humans have the cognitive skills to process them, we rely on alternative methods to find out. One powerful tool is the comparative approach: studying the presence or absence of cognitive/behavioral traits in other species to determine which traits are shared between species and which are recent human inventions. Vocalizations of many species exhibit temporal structure, but little is known about how these rhythmic structures evolved, are perceived and produced, their biological and developmental bases, and communicative functions. We review the literature on rhythm in speech and animal vocalizations as a first step toward understanding similarities and differences across species. We extend this review to quantitative techniques that are useful for computing rhythmic structure in acoustic sequences and hence facilitate cross‐species research. We report links between vocal perception and motor coordination and the differentiation of rhythm based on hierarchical temporal structure. While still far from a complete cross‐species perspective of speech rhythm, our review puts some pieces of the puzzle together.

Abstract

Alternative mathematical models predict differences in how animals adjust the timing of their calls. Differences can be measured as the effect of the timing of a conspecific call on the rate and period of calling of a focal animal, and the lag between the two. Here, I test these alternative hypotheses by tapping into harbor seals’ (Phoca vitulina) mechanisms for spontaneous timing. Both socioecology and vocal behavior of harbor seals make them an interesting model species to study call rhythm and timing. Here, a wild-born seal pup was tested in controlled laboratory conditions. Based on previous recordings of her vocalizations and those of others, I designed playback experiments adapted to that specific animal. The call onsets of the animal were measured as a function of tempo, rhythmic regularity, and spectral properties of the playbacks. The pup adapted the timing of her calls in response to conspecifics’ calls. Rather than responding at a fixed time delay, the pup adjusted her calls’ onset to occur at a fraction of the playback tempo, showing a relative-phase antisynchrony. Experimental results were confirmed via computational modeling. This case study lends preliminary support to a classic mathematical model of animal behavior—Hamilton’s selfish herd—in the acoustic domain.

Abstract

Recognizing that two elements within a sequence of variable length depend on each other is a key ability in understanding the structure of language and music. Perception of such interdependencies has previously been documented in chimpanzees in the visual domain and in human infants and common squirrel monkeys with auditory playback experiments, but it remains unclear whether it typifies primates in general. Here, we investigated the ability of common marmosets (Callithrix jacchus) to recognize and respond to such dependencies. We tested subjects in a familiarization-discrimination playback experiment using stimuli composed of pure tones that either conformed or did not conform to a grammatical rule. After familiarization to sequences with dependencies, marmosets spontaneously discriminated between sequences containing and lacking dependencies (‘consistent’ and ‘inconsistent’, respectively), independent of stimulus length. Marmosets looked more often to the sound source when hearing sequences consistent with the familiarization stimuli, as previously found in human infants. Crucially, looks were coded automatically by computer software, avoiding human bias. Our results support the hypothesis that the ability to perceive dependencies at variable distances was already present in the common ancestor of all anthropoid primates (Simiiformes).

Abstract

Strategies used in artificial grammar learning can shed light into the abilities of different species to extract regularities from the environment. In the A(X)nB rule, A and B items are linked, but assigned to different positional categories and separated by distractor items. Open questions are how widespread is the ability to extract positional regularities from A(X)nB patterns, which strategies are used to encode positional regularities and whether individuals exhibit preferences for absolute or relative position encoding. We used visual arrays to investigate whether cotton-top tamarins (Saguinusoedipus) can learn this rule and which strategies they use. After training on a subset of exemplars, two of the tested monkeys successfully generalized to novel combinations. These tamarins discriminated between categories of tokens with different properties (A, B, X) and detected a positional relationship between non-adjacent items even in the presence of novel distractors. The pattern of errors revealed that successful subjects used visual similarity with training stimuli to solve the task and that successful tamarins extracted the relative position of As and Bs rather than their absolute position, similarly to what has been observed in other species. Relative position encoding appears to be favoured in different tasks and taxa. Generalization, though, was incomplete, since we observed a failure with items that during training had always been presented in reinforced arrays, showing the limitations in grasping the underlying positional rule. These results suggest the use of local strategies in the extraction of positional rules in cotton-top tamarins.