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.

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.

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.

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.

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.

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.

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.

Meaningful call combinations and compositional processing in the southern pied babbler.

Language's expressive power is largely attributable to its compositionality: meaningful words are combined into larger/higher-order structures with derived meaning. Despite its importance, little is known regarding the evolutionary origins and emergence of this syntactic ability. Although previous research has shown a rudimentary capability to combine meaningful calls in primates, because of a scarcity of comparative data, it is unclear to what extent analog forms might also exist outside of primates. Here, we address this ambiguity and provide evidence for rudimentary compositionality in the discrete vocal system of a social passerine, the pied babbler (Turdoides bicolor). Natural observations and predator presentations revealed that babblers produce acoustically distinct alert calls in response to close, low-urgency threats and recruitment calls when recruiting group members during locomotion. On encountering terrestrial predators, both vocalizations are combined into a "mobbing sequence," potentially to recruit group members in a dangerous situation. To investigate whether babblers process the sequence in a compositional way, we conducted systematic experiments, playing back the individual calls in isolation as well as naturally occurring and artificial sequences. Babblers reacted most strongly to mobbing sequence playbacks, showing a greater attentiveness and a quicker approach to the loudspeaker, compared with individual calls or control sequences. We conclude that the sequence constitutes a compositional structure, communicating information on both the context and the requested action. Our work supports previous research suggesting combinatoriality as a viable mechanism to increase communicative output and indicates that the ability to combine and process meaningful vocal structures, a basic syntax, may be more widespread than previously thought.

Experimental Evidence for Phonemic Contrasts in a Nonhuman Vocal System.

The ability to generate new meaning by rearranging combinations of meaningless sounds is a fundamental component of language. Although animal vocalizations often comprise combinations of meaningless acoustic elements, evidence that rearranging such combinations generates functionally distinct meaning is lacking. Here, we provide evidence for this basic ability in calls of the chestnut-crowned babbler (Pomatostomus ruficeps), a highly cooperative bird of the Australian arid zone. Using acoustic analyses, natural observations, and a series of controlled playback experiments, we demonstrate that this species uses the same acoustic elements (A and B) in different arrangements (AB or BAB) to create two functionally distinct vocalizations. Specifically, the addition or omission of a contextually meaningless acoustic element at a single position generates a phoneme-like contrast that is sufficient to distinguish the meaning between the two calls. Our results indicate that the capacity to rearrange meaningless sounds in order to create new signals occurs outside of humans. We suggest that phonemic contrasts represent a rudimentary form of phoneme structure and a potential early step towards the generative phonemic system of human language.

Element repetition rates encode functionally distinct information in pied babbler 'clucks' and 'purrs'.

Human language is a recombinant system that achieves its productivity through the combination of a limited set of sounds. Research investigating the evolutionary origin of this generative capacity has generally focused on the capacity of non-human animals to combine different types of discrete sounds to encode new meaning, with less emphasis on meaning-differentiating mechanisms achieved through potentially simpler temporal modifications within a sequence of repeated sounds. Here we show that pied babblers (Turdoides bicolor) generate two functionally distinct vocalisations composed of the same sound type, which can only be distinguished by the number of repeated elements. Specifically, babblers produce extended 'purrs' composed of, on average, around 17 element repetitions when drawing young offspring to a food source and truncated 'clucks' composed of a fixed number of 2-3 elements when collectively mediating imminent changes in foraging site. We propose that meaning-differentiating temporal structuring might be a much more widespread combinatorial mechanism than currently recognised and is likely of particular value for species with limited vocal repertoires in order to increase their communicative output.

Language evolution: syntax before phonology?

Phonology and syntax represent two layers of sound combination central to language's expressive power. Comparative animal studies represent one approach to understand the origins of these combinatorial layers. Traditionally, phonology, where meaningless sounds form words, has been considered a simpler combination than syntax, and thus should be more common in animals. A linguistically informed review of animal call sequences demonstrates that phonology in animal vocal systems is rare, whereas syntax is more widespread. In the light of this and the absence of phonology in some languages, we hypothesize that syntax, present in all languages, evolved before phonology.

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'.

Syntax-like Structures in Maternal Contact Calls of Chestnut-Crowned Babblers (Pomatostomus ruficeps).

The combination of meaning-bearing units (e.g., words) into higher-order structures (e.g., compound words and phrases) is integral to human language. Despite this central role of syntax in language, little is known about its evolutionary progression. Comparative data using animal communication systems offer potential insights, but only a handful of species have been identified to combine meaningful calls together into larger signals. We investigated a candidate for syntax-like structure in the highly social chestnut-crowned babbler (Pomatostomus ruficeps). Using a combination of behavioral observations, acoustic analyses, and playback experiments, we test whether the form and function of maternal contact calls is modified by combining the core "piping" elements of such calls with at least one other call element or call. Results from the acoustic analyses (236 analysed calls from 10 individuals) suggested that piping call elements can be flexibly initiated with either "peow" elements from middle-distance contact calls or adult "begging" calls to form "peow-pipe" and "beg-pipe" calls. Behavioral responses to playbacks (20 trials to 7 groups) of natural peow-pipe and beg-pipe calls were comparable to those of artificially generated versions of each call using peow elements and begging calls from other contexts. Furthermore, responses to playbacks (34 trials to 7 groups) of the three forms of maternal contact calls (piping alone, peow-pipe, beg-pipe) differed. Together these data suggest that meaning encoded in piping calls is modified by combining such calls with begging calls or peow elements used in other contexts and so provide rare empirical evidence for syntactic-like structuring in a nonhuman animal.

Chimpanzee gestural exchanges share temporal structure with human language.

Humans regularly engage in efficient communicative conversations, which serve to socially align individuals1. In conversations, we take fast-paced turns using a human-universal structure of deploying and receiving signals which shows consistent timing across cultures2. We report here that chimpanzees also engage in rapid signal-to-signal turn-taking during face-to-face gestural exchanges with a similar average latency between turns to that of human conversation. This correspondence between human and chimpanzee face-to-face communication points to shared underlying rules in communication. These structures could be derived from shared ancestral mechanisms or convergent strategies that enhance coordinated interactions or manage competition for communicative 'space'.

Social monitoring via close calls in meerkats.

Social monitoring of the actions of group members is thought to be a key development associated with group living. Humans constantly monitor the behaviour of others and respond to them in a flexible way depending on past interactions and the current social context. While other primates have also been reported to change their behaviour towards other group members flexibly based on the current state of their relationship, empirical evidence is typically linked to contextually specific events such as aggressive or reproductive interactions. In the cooperatively breeding meerkat (Suricata suricatta), we investigated whether subordinate females use frequently emitted, non-agonistic close calls to monitor the location of the dominant female and whether they subsequently adjust their response based on recent social interactions during conflict and non-conflict periods. Subjects discriminated between the close calls of the dominant female and control playbacks, responding by approaching the loudspeaker and displaying submissive behaviour only if they were currently threatened by eviction. Our results suggest that meerkats assess the risk for aggressive interactions with close associates depending on social circumstances, and respond accordingly. We argue that social monitoring based on non-agonistic cues is probably a common mechanism in group-living species that allows the adjustment of behaviour depending on variation in relationships.

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.

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.

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.

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.