Isochrony in barks of Cape fur seal (Arctocephalus pusillus pusillus) pups and adults.

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.

thebeat: A Python package for working with rhythms and other temporal sequences.

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.

Recursive self-embedded vocal motifs in wild orangutans.

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.

Language is the most powerful communication tool known in nature. By combining a finite set of elements, it allows us to encode infinite messages. This enables communication about virtually anything, from alerting others to potential dangers, to recommending a favourite book. The prevailing theory of the last 70 years suggests that this ability rests on a computational process in the brain that is unique to humans, known as recursion. Recursion enables humans to produce and place a language element or pattern of elements inside another element or pattern of the same kind. In this way, a clause can be embedded inside another 'carrier' clause to extend a thought, argument, or scenario, for example, "the dog, which chased the cat, was barking". While recursion offers a simple, yet potent, explanation for the endless possibilities of language, how and why recursion ­ and by extension language ­ emerged in humans but no other animals remains a mystery. Lameira et al. observed vocal patterns in wild orangutans that appeared to be composed of different elements. As orangutans and other great apes are our closest living relatives, they represent the most realistic model for studying the ability of human ancestors to use and comprehend language. Therefore, Lameira et al. set out to determine if this was a case of vocal patterning embedded within a similar vocal pattern, which could indicate that recursion underpins production of these calls. Analysing recordings of long calls made by wild male orangutans showed that they are organized as two layers, where calls with a regular beat (or tempo) are produced within another "carrier" call of a different tempo. Up to three different call types, each with their own signature tempo, can occur within the same carrier call. Further analysis confirmed these call types were unrelated to the carrier. The findings of Lameira et al. demonstrate that orangutans produce recursive vocal sequences that could represent a possible precursor to recursion in humans, offering a potential avenue for studying how recursion, and ultimately language, evolved in humans. In the future, better understanding of how language evolved may help to refine machine learning algorithms that aim to recognize, predict or generate text.

Why do dogs wag their tails?

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.

Neural encoding of musical expectations in a non-human primate.

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.

Modelling the emergence of synchrony from decentralized rhythmic interactions in animal communication.

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.

PyGellermann: a Python tool to generate pseudorandom series for human and non-human animal behavioural experiments.

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 .

The evolution of social timing.

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.

Voices in the ocean.

Toothed whales evolved a third way of making sounds similar to that of land mammals and birds.

Measuring rhythms of vocal interactions: a proof of principle in harbour seal pups.

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. This article is part of a discussion meeting issue 'Face2face: advancing the science of social interaction'.

Spontaneous vocal coordination of vocalizations to water noise in rooks (Corvus frugilegus): An exploratory study.

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.

Hoover the talking seal.

Diandra Duengen and colleagues introduce Hoover, a male harbor seal famous for his imitation of human speech.

High-fidelity transmission of auditory symbolic material is associated with reduced right-left neuroanatomical asymmetry between primary auditory regions.

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.

Isochrony and rhythmic interaction in ape duetting.

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.

Spontaneous rhythm discrimination in a mammalian vocal learner.

Rhythm and vocal production learning are building blocks of human music and speech. Vocal learning has been hypothesized as a prerequisite for rhythmic capacities. Yet, no mammalian vocal learner but humans have shown the capacity to flexibly and spontaneously discriminate rhythmic patterns. Here we tested untrained rhythm discrimination in a mammalian vocal learning species, the harbour seal (Phoca vitulina). Twenty wild-born seals were exposed to music-like playbacks of conspecific call sequences varying in basic rhythmic properties. These properties were called length, sequence regularity, and overall tempo. All three features significantly influenced seals' reaction (number of looks and their duration), demonstrating spontaneous rhythm discrimination in a vocal learning mammal. This finding supports the rhythm-vocal learning hypothesis and showcases pinnipeds as promising models for comparative research on rhythmic phylogenies.

Vocal tract allometry in a mammalian vocal learner.

Acoustic allometry occurs when features of animal vocalisations can be predicted from body size measurements. Despite this being considered the norm, allometry sometimes breaks, resulting in species sounding smaller or larger than expected for their size. A recent hypothesis suggests that allometry-breaking mammals cluster into two groups: those with anatomical adaptations to their vocal tracts and those capable of learning new sounds (vocal learners). Here, we tested which mechanism is used to escape from acoustic allometry by probing vocal tract allometry in a proven mammalian vocal learner, the harbour seal (Phoca vitulina). We tested whether vocal tract structures and body size scale allometrically in 68 young individuals. We found that both body length and body mass accurately predict vocal tract length and one tracheal dimension. Independently, body length predicts vocal fold length while body mass predicts a second tracheal dimension. All vocal tract measures are larger in weaners than in pups and some structures are sexually dimorphic within age classes. We conclude that harbour seals do comply with anatomical allometric constraints. However, allometry between body size and vocal fold length seems to emerge after puppyhood, suggesting that ontogeny may modulate the anatomy-learning distinction previously hypothesised as clear cut. We suggest that seals, and perhaps other species producing signals that deviate from those expected from their vocal tract dimensions, may break allometry without morphological adaptations. In seals, and potentially other vocal learning mammals, advanced neural control over vocal organs may be the main mechanism for breaking acoustic allometry.

A cross-species framework to identify vocal learning abilities in mammals.

Vocal production learning (VPL) is the experience-driven ability to produce novel vocal signals through imitation or modification of existing vocalizations. A parallel strand of research investigates acoustic allometry, namely how information about body size is conveyed by acoustic signals. Recently, we proposed that deviation from acoustic allometry principles as a result of sexual selection may have been an intermediate step towards the evolution of vocal learning abilities in mammals. Adopting a more hypothesis-neutral stance, here we perform phylogenetic regressions and other analyses further testing a potential link between VPL and being an allometric outlier. We find that multiple species belonging to VPL clades deviate from allometric scaling but in the opposite direction to that expected from size exaggeration mechanisms. In other words, our correlational approach finds an association between VPL and being an allometric outlier. However, the direction of this association, contra our original hypothesis, may indicate that VPL did not necessarily emerge via sexual selection for size exaggeration: VPL clades show higher vocalization frequencies than expected. In addition, our approach allows us to identify species with potential for VPL abilities: we hypothesize that those outliers from acoustic allometry lying above the regression line may be VPL species. Our results may help better understand the cross-species diversity, variability and aetiology of VPL, which among other things is a key underpinning of speech in our species. This article is part of the theme issue 'Voice modulation: from origin and mechanism to social impact (Part II)'.

Vocal plasticity in harbour seal pups.

Vocal plasticity can occur in response to environmental and biological factors, including conspecifics' vocalizations and noise. Pinnipeds are one of the few mammalian groups capable of vocal learning, and are therefore relevant to understanding the evolution of vocal plasticity in humans and other animals. Here, we investigate the vocal plasticity of harbour seals (Phoca vitulina), a species with vocal learning abilities observed in adulthood but not puppyhood. To evaluate early mammalian vocal development, we tested 1-3 weeks-old seal pups. We tailored noise playbacks to this species and age to induce seal pups to shift their fundamental frequency (f0), rather than adapt call amplitude or temporal characteristics. We exposed individual pups to low- and high-intensity bandpass-filtered noise, which spanned-and masked-their typical range of f0; simultaneously, we recorded pups' spontaneous calls. Unlike most mammals, pups modified their vocalizations by lowering their f0 in response to increased noise. This modulation was precise and adapted to the particular experimental manipulation of the noise condition. In addition, higher levels of noise induced less dispersion around the mean f0, suggesting that pups may have actively focused their phonatory efforts to target lower frequencies. Noise did not seem to affect call amplitude. However, one seal showed two characteristics of the Lombard effect known for human speech in noise: significant increase in call amplitude and flattening of spectral tilt. Our relatively low noise levels may have favoured f0 modulation while inhibiting amplitude adjustments. This lowering of f0 is unusual, as most animals commonly display no such f0 shift. Our data represent a relatively rare case in mammalian neonates, and have implications for the evolution of vocal plasticity and vocal learning across species, including humans. This article is part of the theme issue 'Voice modulation: from origin and mechanism to social impact (Part I)'.