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

There are some historical divisions in methods, rationales, and purposes between
studies on comparative cognition and behavioural ecology. In turn, the interaction between
these two branches and studies from mathematics, computation and neuroscience is not
usual. In this short piece, we attempt to build bridges among these disciplines. We present a
series of interconnected vignettes meant to illustrate how a more interdisciplinary approach
looks like when successful, and its advantages. Concretely, we focus on a recent topic,
namely animal rhythms in interaction, studied under different approaches. We showcase 5
research efforts, which we believe successfully link 5 particular Scientific areas of rhythm
research conceptualized as: Social neuroscience, Detailed rhythmic quantification,
Ontogeny, Computational approaches and Spontaneous interactions. Our suggestions will
hopefully spur a ‘Comparative rhythms in interaction’ field, which can integrate and
capitalize on knowledge from zoology, comparative psychology, neuroscience, and
computation.

Abstract

One of the most controversial hypotheses in cognitive science is the Chomskyan evolutionary conjecture that language arose instantaneously in humans through a single mutation. Here we analyze the evolutionary dynamics implied by this hypothesis, which has never been formalized before. The hypothesis supposes the emergence and fixation of a single mutant (capable of the syntactic operation Merge) during a narrow historical window as a result of frequency-independent selection under a huge fitness advantage in a population of an effective size no larger than ~15 000 individuals. We examine this proposal by combining diffusion analysis and extreme value theory to derive a probabilistic formulation of its dynamics. We find that although a macro-mutation is much more likely to go to fixation if it occurs, it is much more unlikely a priori than multiple mutations with smaller fitness effects. The most likely scenario is therefore one where a medium number of mutations with medium fitness effects accumulate. This precise analysis of the probability of mutations occurring and going to fixation has not been done previously in the context of the evolution of language. Our results cast doubt on any suggestion that evolutionary reasoning provides an independent rationale for a single-mutant theory of language.

Abstract

Acoustic allometry is the study of how animal vocalisations reflect their body size. A key aim of this research is to identify outliers to acoustic allometry principles and pinpoint the evolutionary origins of such outliers. A parallel strand of research investigates species capable of vocal learning, the experience-driven ability to produce novel vocal signals through imitation or modification of existing vocalisations. Modification of vocalizations is a common feature found when studying both acoustic allometry and vocal learning. Yet, these two fields have only been investigated separately to date. Here, we review and connect acoustic allometry and vocal learning across mammalian clades, combining perspectives from bioacoustics, anatomy and evolutionary biology. Based on this, we hypothesize that, as a precursor to vocal learning, some species might have evolved the capacity for volitional vocal modulation via sexual selection for ‘dishonest’ signalling. We provide preliminary support for our hypothesis by showing significant associations between allometric deviation and vocal learning in a dataset of 164 mammals. Our work offers a testable framework for future empirical research linking allometric principles with the evolution of vocal learning.

Abstract

Communicating species identity is a key component of many animal signals. However, whether selection for species recognition systematically increases signal diversity during clade radiation remains debated. Here we show that in woodpecker drumming, a rhythmic signal used during mating and territorial defense, the amount of species identity information encoded remained stable during woodpeckers’ radiation. Acoustic analyses and evolutionary reconstructions show interchange among six main drumming types despite strong phylogenetic contingencies, suggesting evolutionary tinkering of drumming structure within a constrained acoustic space. Playback experiments and quantification of species discriminability demonstrate sufficient signal differentiation to support species recognition in local communities. Finally, we only find character displacement in the rare cases where sympatric species are also closely related. Overall, our results illustrate how historical contingencies and ecological interactions can promote conservatism in signals during a clade radiation without impairing the effectiveness of information transfer relevant to inter-specific discrimination.

Abstract

Processing of recursion has been proposed as the foundation of human linguistic ability. Yet this ability may be shared with other domains, such as the musical or rhythmic domain. Lindenmayer grammars (L-systems) have been proposed as a recursive grammar for use in artificial grammar experiments to test recursive processing abilities, and previous work had shown that participants are able to learn such a grammar using linguistic stimuli (syllables). In the present work, we used two experimental paradigms (a yes/no task and a two-alternative forced choice) to test whether adult participants are able to learn a recursive Lindenmayer grammar composed of drum sounds. After a brief exposure phase, we found that participants at the group level were sensitive to the exposure grammar and capable of distinguishing the grammatical and ungrammatical test strings above chance level in both tasks. While we found evidence of participants’ sensitivity to a very complex L-system grammar in a non-linguistic, potentially musical domain, the results were not robust. We discuss the discrepancy within our results and with the previous literature using L-systems in the linguistic domain. Furthermore, we propose directions for future music cognition research using L-system grammars.

Abstract

Timing is an essential parameter influencing many behaviours. A previous study demonstrated a high sensitivity of a phocid, the harbour seal (Phoca vitulina), in discriminating time intervals. In the present study, we compared the harbour seal’s timing abilities with the timing abilities of an otariid, the South African fur seal (Arctocephalus pusillus pusillus). This comparison seemed essential as phocids and otariids differ in many respects and might, thus, also differ regarding their timing abilities. We determined time difference thresholds for sub- and suprasecond time intervals marked by a white circle on a black background displayed for a specific time interval on a monitor using a staircase method. Contrary to our expectation, the timing abilities of the fur seal and the harbour seal were comparable. Over a broad range of time intervals, 0.8–7 s in the fur seal and 0.8–30 s in the harbour seal, the difference thresholds followed Weber’s law. In this range, both animals could discriminate time intervals differing only by 12 % and 14 % on average. Timing might, thus be a fundamental cue for pinnipeds in general to be used in various contexts, thereby complementing information provided by classical sensory systems. Future studies will help to clarify if timing is indeed involved in foraging decisions or the estimation of travel speed or distance.

Abstract

Many foundational questions in the psychology of music require cross-cultural approaches, yet the vast majority of work in the field to date has been conducted with Western participants and Western music. For cross-cultural research to thrive, it will require collaboration between people from different disciplinary backgrounds, as well as strategies for overcoming differences in assumptions, methods, and terminology. This position paper surveys the current state of the field and offers a number of concrete recommendations focused on issues involving ethics, empirical methods, and definitions of “music” and “culture.”

Abstract

Learning and processing natural language requires the ability to track syntactic relationships between words and phrases in a sentence, which are often separated by intervening material. These nonadjacent dependencies can be studied using artificial grammar learning paradigms and structured sequence processing tasks. These approaches have been used to demonstrate that human adults, infants and some nonhuman animals are able to detect and learn dependencies between nonadjacent elements within a sequence. However, learning nonadjacent dependencies appears to be more cognitively demanding than detecting dependencies between adjacent elements, and only occurs in certain circumstances. In this review, we discuss different types of nonadjacent dependencies in language and in artificial grammar learning experiments, and how these differences might impact learning. We summarize different types of perceptual cues that facilitate learning, by highlighting the relationship between dependent elements bringing them closer together either physically, attentionally, or perceptually. Finally, we review artificial grammar learning experiments in human adults, infants, and nonhuman animals, and discuss how similarities and differences observed across these groups can provide insights into how language is learned across development and how these language‐related abilities might have evolved.

Abstract

In response to: How to learn about teaching: An evolutionary framework for the study of teaching behavior in humans and other animals

Arguments about the nature of teaching have depended principally on naturalistic observation and some experimental work. Additional measurement tools, and physiological variations and manipulations can provide insights on the intrinsic structure and state of the participants better than verbal descriptions alone: namely, time-series analysis, and examination of the role of hormones and neuromodulators on the behaviors of teacher and pupil.

Abstract

Comparative pattern learning experiments investigate how different species find regularities in sensory input, providing insights into cognitive processing in humans and other animals. Past research has focused either on one species’ ability to process pattern classes or different species’ performance in recognizing the same pattern, with little attention to individual and species-specific heuristics and decision strategies. We trained and tested two bird species, pigeons (Columba livia) and kea (Nestor notabilis, a parrot species), on visual patterns using touch-screen technology. Patterns were composed of several abstract elements and had varying degrees of structural complexity. We developed a model selection paradigm, based on regular expressions, that allowed us to reconstruct the specific decision strategies and cognitive heuristics adopted by a given individual in our task. Individual birds showed considerable differences in the number, type and heterogeneity of heuristic strategies adopted. Birds’ choices also exhibited consistent species-level differences. Kea adopted effective heuristic strategies, based on matching learned bigrams to stimulus edges. Individual pigeons, in contrast, adopted an idiosyncratic mix of strategies that included local transition probabilities and global string similarity. Although performance was above chance and quite high for kea, no individual of either species provided clear evidence of learning exactly the rule used to generate the training stimuli. Our results show that similar behavioral outcomes can be achieved using dramatically different strategies and highlight the dangers of combining multiple individuals in a group analysis. These findings, and our general approach, have implications for the design of future pattern learning experiments, and the interpretation of comparative cognition research more generally.

Abstract

Humans have a strong proclivity for structuring and patterning stimuli: Whether in space or time, we tend to mentally order stimuli in our environment and organize them into units with specific types of relationships. A crucial prerequisite for such organization is the cognitive ability to discern and process regularities among multiple stimuli. To investigate the evolutionary roots of this cognitive capacity, we tested chimpanzees—which, along with bonobos, are our closest living relatives—for simple, variable distance dependency processing in visual patterns. We trained chimpanzees to identify pairs of shapes either linked by an arbitrary learned association (arbitrary associative dependency) or a shared feature (same shape, feature-based dependency), and to recognize strings where items related to either of these ways occupied the first (leftmost) and the last (rightmost) item of the stimulus. We then probed the degree to which subjects generalized this pattern to new colors, shapes, and numbers of interspersed items. We found that chimpanzees can learn and generalize both types of dependency rules, indicating that the ability to encode both feature-based and arbitrary associative regularities over variable distances in the visual domain is not a human prerogative. Our results strongly suggest that these core components of human structural processing were already present in our last common ancestor with chimpanzees.

Abstract

Flexibly adapting social behavior to social and environmental challenges helps to alleviate glucocorticoid (GC) levels, which may have positive fitness implications for an individual. For primates, the predominant social behavior is grooming. Giving grooming to others is particularly efficient in terms of GC mitigation. However, grooming is confined by certain limitations such as time constraints or restricted access to other group members. For instance, dominance hierarchies may impact grooming partner availability in primate societies. Consequently specific grooming patterns emerge. In despotic species focusing grooming activity on preferred social partners significantly ameliorates GC levels in females of all ranks. In this study we investigated grooming patterns and GC management in Barbary macaques, a comparably relaxed species. We monitored changes in grooming behavior and cortisol (C) for females of different ranks. Our results show that the C‐amelioration associated with different grooming patterns had a gradual connection with dominance hierarchy: while higher‐ranking individuals showed lowest urinary C measures when they focused their grooming on selected partners within their social network, lower‐ranking individuals expressed lowest C levels when dispersing their grooming activity evenly across their social partners. We argue that the relatively relaxed social style of Barbary macaque societies allows individuals to flexibly adapt grooming patterns, which is associated with rank‐specific GC management. Am. J. Primatol. 77:688–700, 2015