Publications

Abstract

Rhythm is a fundamental feature characterizing communicative displays, and recent studies showed that primate songs encompass categorical rhythms falling on small integer ratios observed in humans. We individually assessed the presence and sexual dimorphism of rhythmic categories, analyzing songs emitted by 39 wild indris. Considering the intervals between the units given during each song, we extracted 13556 interval ratios and found three peaks (at around 0.33, 0.47, and 0.70). Two peaks indicated rhythmic categories corresponding to small integer ratios (1:1, 2:1). All individuals showed a peak at 0.70, and
most showed those at 0.47 and 0.33. In addition, we found sex differences in the peak at 0.47 only, with males showing lower values than females. This work investigates the presence of individual rhythmic categories in a non-human species; further research may highlight the significance of rhythmicity and untie selective pressures that guided its evolution across species, including humans.

Abstract

Since the discovery that rhythmic abilities are universal in humans, temporal features of vocal communication have greatly interested researchers studying animal communication. Rhythmic patterns are a valuable tool for species discrimination, mate choice, and individual recognition. A recent study showed that bird songs and human music share rhythmic categories when a signal's temporal intervals are distributed categorically rather than uniformly. Following that study, we aimed to investigate whether songs of indris (Indri indri), the only singing lemur, may show similar features. We measured the inter-onset intervals (tk), delimited by the onsets of two consecutive units, and the rhythmic ratios between these intervals (rk), calculated by dividing an interval by itself plus its adjacent, and finded a three-cluster distribution. Two clusters corresponded to rhythmic categories at 1:1 and 1:2, and the third approached a 2:1 ratio. Our results demonstrated for the first time that another primate besides humans produces categorical rhythms, an ability likely evolved convergently among singing species such as songbirds, indris, and humans. Understanding which communicative features are shared with other species is fundamental to understanding how they have evolved. In this regard, thanks to the simplicity of data processing and interpretation, our study relied on an accessible analytical approach that could open up new branches of the investigation into primate communication, leading the way to reconstruct a phylogeny of rhythm abilities across the entire order.

Abstract

The field of bioacoustics is rapidly developing and characterized by diverse methodologies, approaches and aims. For instance, bioacoustics encompasses studies on the perception of pure tones in meticulously controlled laboratory settings, documentation of species’ presence and activities using recordings from the field, and analyses of circadian calling patterns in animal choruses. Newcomers to the field are confronted with a vast and fragmented literature, and a lack of accessible reference papers or textbooks. In this paper we contribute towards filling this gap. Instead of a classical list of “dos” and “don’ts”, we review some key papers which, we believe, embody best practices in several bioacoustic subfields. In the first three case studies, we discuss how bioacoustics can help identify the ‘who’, ‘where’ and ‘how many’ of animals within a given ecosystem. Specifically, we review cases in which bioacoustic methods have been applied with success to draw inferences regarding species identification, population structure, and biodiversity. In fourth and fifth case studies, we highlight how structural properties in signal evolution can emerge via ecological constraints or cultural transmission. Finally, in a sixth example, we discuss acoustic methods that have been used to infer predator–prey dynamics in cases where direct observation was not feasible. Across all these examples, we emphasize the importance of appropriate recording parameters and experimental design. We conclude by highlighting common best practices across studies as well as caveats about our own overview. We hope our efforts spur a more general effort in standardizing best practices across the subareas we’ve highlighted in order to increase compatibility among bioacoustic studies and inspire cross-pollination across the discipline.

Abstract

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)’.

Abstract

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. A recent hypothesis suggests that allometry-breaking animals cluster into two groups: those with anatomical adaptations to their vocal tracts and those capable of learning new sounds (vocal learners). Here we test this hypothesis by probing vocal tract allometry in a proven mammalian vocal learner, the harbour seal (Phoca vitulina). We test whether vocal tract structures and body size scale allometrically in 68 individuals. We find that both body length and body weight accurately predict vocal tract length and one tracheal dimension. Independently, body length predicts vocal fold length while body weight 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 allometric constraints, lending support to our hypothesis. 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. Species capable of producing non-allometric signals while their vocal tract scales allometrically, like seals, may then use non-morphological allometry-breaking mechanisms. We suggest that seals, and potentially other vocal learning mammals, may achieve allometry-breaking through developed neural control over their vocal organs.

Abstract

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.

Abstract

Dance is ubiquitous among humans and has received attention from several disciplines. Ethnographic documentation suggests that dance has a signaling function in social interaction. It can influence mate preferences and facilitate social bonds. Research has provided insights into the proximate mechanisms of dance, individually or when dancing with partners or in groups. Here, we review dance research from an evolutionary perspective. We propose that human dance evolved from ordinary (non-communicative) movements to communicate socially relevant information accurately. The need for accurate social signaling may have accompanied increases in group size and population density. Because of its complexity in production and display, dance may have evolved as a vehicle for expressing social and cultural information. Mating-related qualities and motives may have been the predominant information derived from individual dance movements, whereas group dance offers the opportunity for the exchange of socially relevant content, for coordinating actions among group members, for signaling coalitional strength, and for stabilizing group structures. We conclude that, despite the cultural diversity in dance movements and contexts, the primary communicative functions of dance may be the same across societies.

Abstract

The development of rhythmicity is foundational to communicative and social behaviours in humans and many other species, and mechanisms of synchrony could be conserved across species. The goal of the current paper is to explore evolutionary hypotheses linking vocal learning and beat synchronization through genomic approaches, testing the prediction that genetic underpinnings of birdsong also contribute to the aetiology of human interactions with musical beat structure. We combined state-of-the-art-genomic datasets that account for underlying polygenicity of these traits: birdsong genome-wide transcriptomics linked to singing in zebra finches, and a human genome-wide association study of beat synchronization. Results of competitive gene set analysis revealed that the genetic architecture of human beat synchronization is significantly enriched for birdsong genes expressed in songbird Area X (a key nucleus for vocal learning, and homologous to human basal ganglia). These findings complement ethological and neural evidence of the relationship between vocal learning and beat synchronization, supporting a framework of some degree of common genomic substrates underlying rhythm-related behaviours in two clades, humans and songbirds (the largest evolutionary radiation of vocal learners). Future cross-species approaches investigating the genetic underpinnings of beat synchronization in a broad evolutionary context are discussed.

Abstract

This theme issue assembles current studies that ask how and why precise synchronization and related forms of rhythm interaction are expressed in a wide range of behaviour. The studies cover human activity, with an emphasis on music, and social behaviour, reproduction and communication in non-human animals. In most cases, the temporally aligned rhythms have short—from several seconds down to a fraction of a second—periods and are regulated by central nervous system pacemakers, but interactions involving rhythms that are 24 h or longer and originate in biological clocks also occur. Across this spectrum of activities, species and time scales, empirical work and modelling suggest that synchrony arises from a limited number of coupled-oscillator mechanisms with which individuals mutually entrain. Phylogenetic distribution of these common mechanisms points towards convergent evolution. Studies of animal communication indicate that many synchronous interactions between the signals of neighbouring individuals are specifically favoured by selection. However, synchronous displays are often emergent properties of entrainment between signalling individuals, and in some situations, the very signallers who produce a display might not gain any benefit from the collective timing of their production.

Abstract

What are the origins of musical rhythm? One approach to the biology and evolution of music consists in finding common musical traits across species. These similarities allow biomusicologists to infer when and how musical traits appeared in our species1
. A parallel approach to the biology and evolution of music focuses on finding statistical universals in human music2
. These include rhythmic features that appear above chance across musical cultures. One such universal is the production of categorical rhythms3
, defined as those where temporal intervals between note onsets are distributed categorically rather than uniformly2
,4
,5
. Prominent rhythm categories include those with intervals related by small integer ratios, such as 1:1 (isochrony) and 1:2, which translates as some notes being twice as long as their adjacent ones. In humans, universals are often defined in relation to the beat, a top-down cognitive process of inferring a temporal regularity from a complex musical scene1
. Without assuming the presence of the beat in other animals, one can still investigate its downstream products, namely rhythmic categories with small integer ratios detected in recorded signals. Here we combine the comparative and statistical universals approaches, testing the hypothesis that rhythmic categories and small integer ratios should appear in species showing coordinated group singing3
. We find that a lemur species displays, in its coordinated songs, the isochronous and 1:2 rhythm categories seen in human music, showing that such categories are not, among mammals, unique to humans3

Abstract

Comparative studies of vocal learning and vocal non-learning animals can increase our understanding of the neurobiology and evolution of vocal learning and human speech. Mammalian vocal learning is understudied: most research has either focused on vocal learning in songbirds or its absence in non-human primates. Here we focus on a highly promising model species for the neurobiology of vocal learning: grey seals. We provide a neuroanatomical atlas (based on dissected brain slices and magnetic resonance images), a labelled MRI template, a 3D model with volumetric measurements of brain regions, and histological cortical stainings. Four main features of the grey seal brain stand out. (1) It is relatively big and highly convoluted. (2) It hosts a relatively large temporal lobe and cerebellum, structures which could support developed timing abilities and acoustic processing. (3) The cortex is similar to humans in thickness and shows the expected six-layered mammalian structure. (4) Expression of FoxP2 - a gene involved in vocal learning and spoken language - is present in deeper layers of the cortex. Our results could facilitate future studies targeting the neural and genetic underpinnings of mammalian vocal learning, thus bridging the research gap from songbirds to humans and non-human primates.Competing Interest StatementThe authors have declared no competing interest.

Abstract

A cross-species perspective can extend and provide testable predictions for Savage et al.’s
framework. Rhythm and melody, I argue, could bootstrap each other in the evolution of
musicality. Isochrony may function as a temporal grid to support rehearsing and learning
modulated, pitched vocalizations. Once this melodic plasticity is acquired, focus can shift back to refining rhythm processing and beat induction.

Abstract

How music and speech evolved is a mystery. Several hypotheses on their
origins, including one on their joint origins, have been put forward but rarely
tested. Here we report and comment on the first experiment testing the hypothesis
that speech and music bifurcated from a common system. We highlight strengths
of the reported experiment, point out its relatedness to animal work, and suggest
three alternative interpretations of its results. We conclude by sketching a future
empirical programme extending this work.

Abstract

This review paper discusses rhythmic dyadic interactions in social and sexual contexts. We report rhythmic interactions during communication within dyads, as found in humans, non-human primates, non-primate mammals, birds, anurans and insects. Based on the patterns observed, we infer adaptive explanations for the observed rhythm interactions and identify knowledge gaps. Across species, the social environment during ontogeny is a key factor in shaping adult signal repertoires and timing mechanisms used to regulate interactions. The degree of temporal coordination is influenced by the dynamic and strength of the dyadic interaction. Most studies of temporal structure in interactive signals mainly focus on one modality (acoustic and visual); we suggest more work should be performed on multimodal signals. Multidisciplinary approaches combining cognitive science, ethology and ecology should shed more light on the exact timing mechanisms involved. Taken together, rhythmic signalling behaviours are widespread and critical in regulating social interactions across taxa.

Abstract

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.

Abstract

* - indicates joint first authorship -
The ability to discriminate between familiar and unfamiliar calls may play a key role in pinnipeds’ communication and survival, as in the case of mother-pup interactions. Vocal discrimination abilities have been suggested to be more developed in pinniped species with the highest selective pressure such as the otariids; yet, in some group-living phocids, such as harbor seals (Phoca vitulina), mothers are also able to recognize their pup’s voice. Conspecifics’ vocal recognition in pups has never been investigated; however, the repeated interaction occurring between pups within the breeding season suggests that long-term vocal discrimination may occur. Here we explored this hypothesis by presenting three rehabilitated seal pups with playbacks of vocalizations from unfamiliar or familiar pups. It is uncommon for seals to come into rehabilitation for a second time in their lifespan, and this study took advantage of these rare cases. A simple visual inspection of the data plots seemed to show more reactions, and of longer duration, in response to familiar as compared to unfamiliar playbacks in two out of three pups. However, statistical analyses revealed no significant difference between the experimental conditions. We also found no significant asymmetry in orientation (left vs. right) towards familiar and unfamiliar sounds. While statistics do not support the hypothesis of an established ability to discriminate familiar vocalizations from unfamiliar ones in harbor seal pups, further investigations with a larger sample size are needed to confirm or refute this hypothesis.

Abstract

To understand why music is structured the way it is, we need an explanation that accounts for both the universality and variability found in musical traditions. Here we test whether statistical universals that have been identified for melodic structures in music can emerge as a result of cultural adaptation to human biases through iterated learning. We use data from an experiment in which artificial whistled systems, where sounds were produced with a slide whistle, were learned by human participants and transmitted multiple times from person to person. These sets of whistled signals needed to be memorized and recalled and the reproductions of one participant were used as the input set for the next. We tested for the emergence of seven different melodic features, such as discrete pitches, motivic patterns, or phrase repetition, and found some evidence for the presence of most of these statistical universals. We interpret this as promising evidence that, similarly to rhythmic universals, iterated learning experiments can also unearth melodic statistical universals. More, ideally cross-cultural, experiments are nonetheless needed. Simulating the cultural transmission of artificial proto-musical systems can help unravel the origins of universal tendencies in musical structures.

Abstract

Sensitivity to dependencies (correspondences between distant items) in sensory stimuli plays a crucial role in human music and language. Here, we show that squirrel monkeys (Saimiri sciureus) can detect abstract, non-adjacent dependencies in auditory stimuli. Monkeys discriminated between tone sequences containing a dependency and those lacking it, and generalized to previously unheard pitch classes and novel dependency distances. This constitutes the first pattern learning study where artificial stimuli were designed with the species' communication system in mind. These results suggest that the ability to recognize dependencies represents a capability that had already evolved in humans’ last common ancestor with squirrel monkeys, and perhaps before.

Abstract

The possibility of achieving experimentally controlled, non-vocal acoustic production in non-human primates is a key step to enable the testing of a number of hypotheses on primate behavior and cognition. However, no device or solution is currently available, with the use of sensors in non-human animals being almost exclusively devoted to applications in food industry and animal surveillance. Specifically, no device exists which simultaneously allows: (i) spontaneous production of sound or music by non-human animals via object manipulation, (ii) systematical recording of data sensed from these movements, (iii) the possibility to alter the acoustic feedback properties of the object using remote control. We present two prototypes we developed for application with chimpanzees (Pan troglodytes) which, while fulfilling the aforementioned requirements, allow to arbitrarily associate sounds to physical object movements. The prototypes differ in sensing technology, costs, intended use and construction requirements. One prototype uses four piezoelectric elements embedded between layers of Plexiglas and foam. Strain data is sent to a computer running Python through an Arduino board. A second prototype consists in a modified Wii Remote contained in a gum toy. Acceleration data is sent via Bluetooth to a computer running Max/MSP. We successfully pilot tested the first device with a group of chimpanzees. We foresee using these devices for a range of cognitive experiments.

Abstract

Music is a pervasive phenomenon in human culture, and musical
rhythm is virtually present in all musical traditions. Research
on the evolution and cognitive underpinnings of rhythm
can benefit from a number of approaches. We outline key concepts
and definitions, allowing fine-grained analysis of rhythmic
cognition in experimental studies. We advocate comparative
animal research as a useful approach to answer questions
about human music cognition and review experimental evidence
from different species. Finally, we suggest future directions
for research on the cognitive basis of rhythm. Apart from
research in semi-natural setups, possibly allowed by “drum set
for chimpanzees” prototypes presented here for the first time,
mathematical modeling and systematic use of circular statistics
may allow promising advances.