Call combination production is linked to the social environment in Western Australian magpies (Gymnorhina tibicen dorsalis).

It has recently become clear that some language-specific traits previously thought to be unique to humans (such as the capacity to combine sounds) are widespread in the animal kingdom. Despite the increase in studies documenting the presence of call combinations in non-human animals, factors promoting this vocal trait are unclear. One leading hypothesis proposes that communicative complexity co-evolved with social complexity owing to the need to transmit a diversity of information to a wider range of social partners. The Western Australian magpie (Gymnorhina tibicen dorsalis) provides a unique model to investigate this proposed link because it is a group-living, vocal learning species that is capable of multi-level combinatoriality (independently produced calls contain vocal segments and comprise combinations). Here, we compare variations in the production of call combinations across magpie groups ranging in size from 2 to 11 birds. We found that callers in larger groups give call combinations: (i) in greater diversity and (ii) more frequently than callers in smaller groups. Significantly, these observations support the hypothesis that combinatorial complexity may be related to social complexity in an open-ended vocal learner, providing an important step in understanding the role that sociality may have played in the development of vocal combinatorial complexity. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Cognitive constraints on vocal combinatoriality in a social bird.

A critical component of language is the ability to recombine sounds into larger structures. Although animals also reuse sound elements across call combinations to generate meaning, examples are generally limited to pairs of distinct elements, even when repertoires contain sufficient sounds to generate hundreds of combinations. This combinatoriality might be constrained by the perceptual-cognitive demands of disambiguating between complex sound sequences that share elements. We test this hypothesis by probing the capacity of chestnut-crowned babblers to process combinations of two versus three distinct acoustic elements. We found babblers responded quicker and for longer toward playbacks of recombined versus familiar bi-element sequences, but no evidence of differential responses toward playbacks of recombined versus familiar tri-element sequences, suggesting a cognitively prohibitive jump in processing demands. We propose that overcoming constraints in the ability to process increasingly complex combinatorial signals was necessary for the productive combinatoriality that is characteristic of language to emerge.

Call combinations and compositional processing in wild chimpanzees.

Through syntax, i.e., the combination of words into larger phrases, language can express a limitless number of messages. Data in great apes, our closest-living relatives, are central to the reconstruction of syntax's phylogenetic origins, yet are currently lacking. Here, we provide evidence for syntactic-like structuring in chimpanzee communication. Chimpanzees produce "alarm-huus" when surprised and "waa-barks" when potentially recruiting conspecifics during aggression or hunting. Anecdotal data suggested chimpanzees combine these calls specifically when encountering snakes. Using snake presentations, we confirm call combinations are produced when individuals encounter snakes and find that more individuals join the caller after hearing the combination. To test the meaning-bearing nature of the call combination, we use playbacks of artificially-constructed call combinations and both independent calls. Chimpanzees react most strongly to call combinations, showing longer looking responses, compared with both independent calls. We propose the "alarm-huu + waa-bark" represents a compositional syntactic-like structure, where the meaning of the call combination is derived from the meaning of its parts. Our work suggests that compositional structures may not have evolved de novo in the human lineage, but that the cognitive building-blocks facilitating syntax may have been present in our last common ancestor with chimpanzees.

Multi-level combinatoriality in magpie non-song vocalizations.

Comparative studies conducted over the past few decades have provided important insights into the capacity for animals to combine vocal segments at either one of two levels: within- or between-calls. There remains, however, a distinct gap in knowledge as to whether animal combinatoriality can extend beyond one level. Investigating this requires a comprehensive analysis of the combinatorial features characterizing a species' vocal system. Here, we used a nonlinear dimensionality reduction analysis and sequential transition analysis to quantitatively describe the non-song combinatorial repertoire of the Western Australian magpie (Gymnorhina tibicen dorsalis). We found that (i) magpies recombine four distinct acoustic segments to create a larger number of calls, and (ii) the resultant calls are further combined into larger call combinations. Our work demonstrates two levels in the combining of magpie vocal units. These results are incongruous with the notion that a capacity for multi-level combinatoriality is unique to human language, wherein the combining of meaningless sounds and meaningful words interactively occurs across different combinatorial levels. Our study thus provides novel insights into the combinatorial capacities of a non-human species, adding to the growing evidence of analogues of language-specific traits present in the animal kingdom.

Genetic distance from wolves affects family dogs' reactions towards howls.

Domestication dramatically changes behaviour, including communication, as seen in the case of dogs (Canis familiaris) and wolves (Canis lupus). We tested the hypothesis that domestication may affect an ancient, shared communication form of canids, the howling which seems to have higher individual variation in dogs: the perception and usage of howls may be affected by the genetic relatedness of the breeds to their last common ancestor with wolves ('root distance') and by other individual features like age, sex, and reproductive status. We exposed 68 purebred dogs to wolf howl playbacks and recorded their responses. We identified an interaction between root distance and age on the dogs' vocal and behavioural responses: older dogs from more ancient breeds responded longer with howls and showed more stress behaviours. Our results suggest that domestication impacts vocal behaviour significantly: disintegrating howling, a central, species-specific communication form of canids and gradually eradicating it from dogs' repertoire.

Declarative referential gesturing in a wild chimpanzee (Pan troglodytes).

Humans are argued to be unique in their ability and motivation to share attention with others about external entities-sharing attention for sharing's sake. Indeed, in humans, using referential gestures declaratively to direct the attention of others toward external objects and events emerges in the first year of life. In contrast, wild great apes seldom use referential gestures, and when they do, it seems to be exclusively for imperative purposes. This apparent species difference has fueled the argument that the motivation and ability to share attention with others is a human-specific trait with important downstream consequences for the evolution of our complex cognition [M. Tomasello, Becoming Human (2019)]. Here, we report evidence of a wild ape showing a conspecific an item of interest. We provide video evidence of an adult female chimpanzee, Fiona, showing a leaf to her mother, Sutherland, in the context of leaf grooming in Kibale Forest, Uganda. We use a dataset of 84 similar leaf-grooming events to explore alternative explanations for the behavior, including food sharing and initiating dyadic grooming or playing. Our observations suggest that in highly specific social conditions, wild chimpanzees, like humans, may use referential showing gestures to direct others' attention to objects simply for the sake of sharing. The difference between humans and our closest living relatives in this regard may be quantitative rather than qualitative, with ramifications for our understanding of the evolution of human social cognition.

From collocations to call-ocations: using linguistic methods to quantify animal call combinations.

Abstract: Emerging data in a range of non-human animal species have highlighted a latent ability to combine certain pre-existing calls together into larger structures. Currently, however, the quantification of context-specific call combinations has received less attention. This is problematic because animal calls can co-occur with one another simply through chance alone. One common approach applied in language sciences to identify recurrent word combinations is collocation analysis. Through comparing the co-occurrence of two words with how each word combines with other words within a corpus, collocation analysis can highlight above chance, two-word combinations. Here, we demonstrate how this approach can also be applied to non-human animal signal sequences by implementing it on artificially generated data sets of call combinations. We argue collocation analysis represents a promising tool for identifying non-random, communicatively relevant call combinations and, more generally, signal sequences, in animals. Significance statement: Assessing the propensity for animals to combine calls provides important comparative insights into the complexity of animal vocal systems and the selective pressures such systems have been exposed to. Currently, however, the objective quantification of context-specific call combinations has received less attention. Here we introduce an approach commonly applied in corpus linguistics, namely collocation analysis, and show how this method can be put to use for identifying call combinations more systematically. Through implementing the same objective method, so-called call-ocations, we hope researchers will be able to make more meaningful comparisons regarding animal signal sequencing abilities both within and across systems. Supplementary Information: The online version contains supplementary material available at 10.1007/s00265-022-03224-3.

Vocal signals facilitate cooperative hunting in wild chimpanzees.

Cooperation and communication likely coevolved in humans. However, the evolutionary roots of this interdependence remain unclear. We address this issue by investigating the role of vocal signals in facilitating a group cooperative behavior in an ape species: hunting in wild chimpanzees. First, we show that bark vocalizations produced before hunt initiation are reliable signals of behavioral motivation, with barkers being most likely to participate in the hunt. Next, we find that barks are associated with greater hunter recruitment and more effective hunting, with shorter latencies to hunting initiation and prey capture. Our results indicate that the coevolutionary relationship between vocal communication and group-level cooperation is not unique to humans in the ape lineage and is likely to have been present in our last common ancestor with chimpanzees.

The function and evolution of child-directed communication.

Humans communicate with small children in unusual and highly conspicuous ways (child-directed communication (CDC)), which enhance social bonding and facilitate language acquisition. CDC-like inputs are also reported for some vocally learning animals, suggesting similar functions in facilitating communicative competence. However, adult great apes, our closest living relatives, rarely signal to their infants, implicating communication surrounding the infant as the main input for infant great apes and early humans. Given cross-cultural variation in the amount and structure of CDC, we suggest that child-surrounding communication (CSC) provides essential compensatory input when CDC is less prevalent-a paramount topic for future studies.

Degraded and computer-generated speech processing in a bonobo.

The human auditory system is capable of processing human speech even in situations when it has been heavily degraded, such as during noise-vocoding, when frequency domain-based cues to phonetic content are strongly reduced. This has contributed to arguments that speech processing is highly specialized and likely a de novo evolved trait in humans. Previous comparative research has demonstrated that a language competent chimpanzee was also capable of recognizing degraded speech, and therefore that the mechanisms underlying speech processing may not be uniquely human. However, to form a robust reconstruction of the evolutionary origins of speech processing, additional data from other closely related ape species is needed. Specifically, such data can help disentangle whether these capabilities evolved independently in humans and chimpanzees, or if they were inherited from our last common ancestor. Here we provide evidence of processing of highly varied (degraded and computer-generated) speech in a language competent bonobo, Kanzi. We took advantage of Kanzi's existing proficiency with touchscreens and his ability to report his understanding of human speech through interacting with arbitrary symbols called lexigrams. Specifically, we asked Kanzi to recognise both human (natural) and computer-generated forms of 40 highly familiar words that had been degraded (noise-vocoded and sinusoidal forms) using a match-to-sample paradigm. Results suggest that-apart from noise-vocoded computer-generated speech-Kanzi recognised both natural and computer-generated voices that had been degraded, at rates significantly above chance. Kanzi performed better with all forms of natural voice speech compared to computer-generated speech. This work provides additional support for the hypothesis that the processing apparatus necessary to deal with highly variable speech, including for the first time in nonhuman animals, computer-generated speech, may be at least as old as the last common ancestor we share with bonobos and chimpanzees.

First observation of a chimpanzee with albinism in the wild: Social interactions and subsequent infanticide.

Albinism-the congenital absence of pigmentation-is a very rare phenomenon in animals due to the significant costs to fitness of this condition. Both humans and non-human individuals with albinism face a number of challenges, such as reduced vision, increased exposure to ultraviolet radiation, or compromised crypticity resulting in an elevated vulnerability to predation. However, while observations of social interactions involving individuals with albinism have been observed in wild non-primate animals, such interactions have not been described in detail in non-human primates (hereafter, primates). Here, we report, to our knowledge, the first sighting of an infant with albinism in wild chimpanzees (Pan troglodytes schweinfurthii), including social interactions between the infant, its mother, and group members. We also describe the subsequent killing of the infant by conspecifics as well as their behavior towards the corpse following the infanticide. Finally, we discuss our observations in relation to our understanding of chimpanzee behavior or attitudes towards individuals with very conspicuous appearances.

Speech segmentation: New dogs, old tricks?

A new study using electroencephalography and functional magnetic resonance imaging suggests that dogs and humans may segment speech in similar ways.

Reply to comment on "Nonadjacent dependency processing in monkeys, apes, and humans".

Rawski et al. revisit our recent findings suggesting the latent ability to process nonadjacent dependencies ("Non-ADs") in monkeys and apes. Specifically, the authors question the relevance of our findings for the evolution of human syntax. We argue that (i) these conclusions hinge upon an assumption that language processing is necessarily hierarchical, which remains an open question, and (ii) our goal was to probe the foundational cognitive mechanisms facilitating the processing of syntactic Non-ADs-namely, the ability to recognize predictive relationships in the input.

Nonadjacent dependency processing in monkeys, apes, and humans.

The ability to track syntactic relationships between words, particularly over distances ("nonadjacent dependencies"), is a critical faculty underpinning human language, although its evolutionary origins remain poorly understood. While some monkey species are reported to process auditory nonadjacent dependencies, comparative data from apes are missing, complicating inferences regarding shared ancestry. Here, we examined nonadjacent dependency processing in common marmosets, chimpanzees, and humans using "artificial grammars": strings of arbitrary acoustic stimuli composed of adjacent (nonhumans) or nonadjacent (all species) dependencies. Individuals from each species (i) generalized the grammars to novel stimuli and (ii) detected grammatical violations, indicating that they processed the dependencies between constituent elements. Furthermore, there was no difference between marmosets and chimpanzees in their sensitivity to nonadjacent dependencies. These notable similarities between monkeys, apes, and humans indicate that nonadjacent dependency processing, a crucial cognitive facilitator of language, is an ancestral trait that evolved at least ~40 million years before language itself.

An exploration of Menzerath's law in wild mountain gorilla vocal sequences.

Menzerath's law, traditionally framed as a negative relationship between the size of a structure and its constituent parts (e.g. sentences with more clauses have shorter clauses), is widespread across information-coding systems ranging from human language and the vocal and gestural sequences of primates and birds, to the building blocks of DNA, genes and proteins. Here, we analysed an extensive dataset of 'close-call' sequences produced by wild mountain gorillas (Gorilla beringei beringei, no. individuals = 10, no. sequences = 2189) to determine whether, in accordance with Menzerath's law, a negative relationship existed between the number of vocal units in a sequence and the duration of its constituent units. We initially found positive evidence for this but, on closer inspection, the negative relationship was driven entirely by the difference between single- and multi-unit (two to six unit) sequences. Once single-unit sequences were excluded from the analysis, we identified a relationship in the opposite direction, with longer sequences generally composed of longer units. The close-call sequences of mountain gorillas therefore represent an intriguing example of a non-human vocal system that only partially conforms to the predictions of Menzerath's law.

Dwarf mongoose alarm calls: investigating a complex non-human animal call.

Communication plays a vital role in the social lives of many species and varies greatly in complexity. One possible way to increase communicative complexity is by combining signals into longer sequences, which has been proposed as a mechanism allowing species with a limited repertoire to increase their communicative output. In mammals, most studies on combinatoriality have focused on vocal communication in non-human primates. Here, we investigated a potential combination of alarm calls in the dwarf mongoose (Helogale parvula), a non-primate mammal. Acoustic analyses and playback experiments with a wild population suggest: (i) that dwarf mongooses produce a complex call type (T3) which, at least at the surface level, seems to comprise units that are not functionally different to two meaningful alarm calls (aerial and terrestrial); and (ii) that this T3 call functions as a general alarm, produced in response to a wide range of threats. Using a novel approach, we further explored multiple interpretations of the T3 call based on the information content of the apparent comprising calls and how they are combined. We also considered an alternative, non-combinatorial interpretation that frames T3 as the origin, rather than the product, of the individual alarm calls. This study complements previous knowledge of vocal combinatoriality in non-primate mammals and introduces an approach that could facilitate comparisons between different animal and human communication systems.

Chestnut-crowned babbler calls are composed of meaningless shared building blocks.

A core component of human language is its combinatorial sound system: meaningful signals are built from different combinations of meaningless sounds. Investigating whether nonhuman communication systems are also combinatorial is hampered by difficulties in identifying the extent to which vocalizations are constructed from shared, meaningless building blocks. Here we present an approach to circumvent this difficulty and show that a pair of functionally distinct chestnut-crowned babbler (Pomatostomus ruficeps) vocalizations can be decomposed into perceptibly distinct, meaningless entities that are shared across the 2 calls. Specifically, by focusing on the acoustic distinctiveness of sound elements using a habituation-discrimination paradigm on wild-caught babblers under standardized aviary conditions, we show that 2 multielement calls are composed of perceptibly distinct sounds that are reused in different arrangements across the 2 calls. Furthermore, and critically, we show that none of the 5 constituent elements elicits functionally relevant responses in receivers, indicating that the constituent sounds do not carry the meaning of the call and so are contextually meaningless. Our work, which allows combinatorial systems in animals to be more easily identified, suggests that animals can produce functionally distinct calls that are built in a way superficially reminiscent of the way that humans produce morphemes and words. The results reported lend credence to the recent idea that language's combinatorial system may have been preceded by a superficial stage where signalers neither needed to be cognitively aware of the combinatorial strategy in place, nor of its building blocks.

Multimodal communication and language origins: integrating gestures and vocalizations.

The presence of divergent and independent research traditions in the gestural and vocal domains of primate communication has resulted in major discrepancies in the definition and operationalization of cognitive concepts. However, in recent years, accumulating evidence from behavioural and neurobiological research has shown that both human and non-human primate communication is inherently multimodal. It is therefore timely to integrate the study of gestural and vocal communication. Herein, we review evidence demonstrating that there is no clear difference between primate gestures and vocalizations in the extent to which they show evidence for the presence of key language properties: intentionality, reference, iconicity and turn-taking. We also find high overlap in the neurobiological mechanisms producing primate gestures and vocalizations, as well as in ontogenetic flexibility. These findings confirm that human language had multimodal origins. Nonetheless, we note that in great apes, gestures seem to fulfil a carrying (i.e. predominantly informative) role in close-range communication, whereas the opposite holds for face-to-face interactions of humans. This suggests an evolutionary shift in the carrying role from the gestural to the vocal stream, and we explore this transition in the carrying modality. Finally, we suggest that future studies should focus on the links between complex communication, sociality and cooperative tendency to strengthen the study of language origins.

Combinatoriality in the vocal systems of nonhuman animals.

A key challenge in the field of human language evolution is the identification of the selective conditions that gave rise to language's generative nature. Comparative data on nonhuman animals provides a powerful tool to investigate similarities and differences among nonhuman and human communication systems and to reveal convergent evolutionary mechanisms. In this article, we provide an overview of the current evidence for combinatorial structures found in the vocal system of diverse species. We show that considerable structural diversity exits across and within species in the forms of combinatorial structures used. Based on this we suggest that a fine-grained classification and differentiation of combinatoriality is a useful approach permitting systematic comparisons across animals. Specifically, this will help to identify factors that might promote the emergence of combinatoriality and, crucially, whether differences in combinatorial mechanisms might be driven by variations in social and ecological conditions or cognitive capacities. This article is categorized under: Cognitive Biology > Evolutionary Roots of Cognition Linguistics > Evolution of Language.

Compositionality in animals and humans.

A key step in understanding the evolution of human language involves unravelling the origins of language's syntactic structure. One approach seeks to reduce the core of syntax in humans to a single principle of recursive combination, merge, for which there is no evidence in other species. We argue for an alternative approach. We review evidence that beneath the staggering complexity of human syntax, there is an extensive layer of nonproductive, nonhierarchical syntax that can be fruitfully compared to animal call combinations. This is the essential groundwork that must be explored and integrated before we can elucidate, with sufficient precision, what exactly made it possible for human language to explode its syntactic capacity, transitioning from simple nonproductive combinations to the unrivalled complexity that we now have.