Brevity is not always a virtue in primate communication

Semple et al. (Semple et al. in press, Biol. Lett. (doi:10.1098/rsbl.2009.1062)) argued that the ‘law of brevity’ (an inverse relationship between word length and frequency of use) applies not only to human language but also to vocal signalling in non-human primates, because coding efficiency is paramount in both situations. We analysed the frequency of use of signals of different duration in the vocal repertoires of two Neotropical primate species studied in the wild—the common marmoset (Callithrix jacchus) and the golden-backed uakari (Cacajao melanocephalus). The key prediction of the law of brevity was not supported in either species: although the most frequently emitted calls were relatively brief, they were not the shortest signals in the repertoire. The costs and benefits associated with signals of different duration must be appreciated to understand properly their frequency of use. Although relatively brief vocal signals may be favoured by natural selection in order to minimize energetic costs, the very briefest signals may be ambiguous, contain reduced information or be difficult to detect or locate, and may therefore be selected against. Analogies between human language and vocal communication in animals can be misleading as a basis for understanding frequency of use, because coding efficiency is not the only factor of importance in animal communication, and the costs and benefits associated with different signal durations will vary in a species-specific manner.     

非人灵长类声音通讯的研究进展

声音通讯是非人灵长类研究一个重要的研究领域,有助于了解非人灵长类的社会行为、个体关系、行为进化和社会演化等,甚至对探究人类语言起源和进化等方面也具有十分重要的意义。本文通过对非人灵长类声音通讯的研究内容、影响因素和研究方法等进行了梳理,探讨非人灵长类声音通讯研究的前景和展望,旨在进一步推动国内非人灵长类声音通讯研究的深入,同时为相关研究提供借鉴和参考。     

Animal vocal sequences: not the Markov chains we thought they were

Many animals produce vocal sequences that appear complex. Most researchers assume that these sequences are well characterized as Markov chains (i.e. that the probability of a particular vocal element can be calculated from the history of only a finite number of preceding elements). However, this assumption has never been explicitly tested. Furthermore, it is unclear how language could evolve in a single step from a Markovian origin, as is frequently assumed, as no intermediate forms have been found between animal communication and human language. Here, we assess whether animal taxa produce vocal sequences that are better described by Markov chains, or by non-Markovian dynamics such as the ‘renewal process’ (RP), characterized by a strong tendency to repeat elements. We examined vocal sequences of seven taxa: Bengalese finches Lonchura striata domestica, Carolina chickadees Poecile carolinensis, free-tailed bats Tadarida brasiliensis, rock hyraxes Procavia capensis, pilot whales Globicephala macrorhynchus, killer whales Orcinus orca and orangutans Pongo spp. The vocal systems of most of these species are more consistent with a non-Markovian RP than with the Markovian models traditionally assumed. Our data suggest that non-Markovian vocal sequences may be more common than Markov sequences, which must be taken into account when evaluating alternative hypotheses for the evolution of signalling complexity, and perhaps human language origins.     

Attention to elders' voice in non-human primates

The observed respect and attention to elders'' speech in traditional cultures appears to have a ‘universal’ component which questions its possible biological bases. Animals present differential attention to the vocalizations of other individuals according to their characteristics but little is known about the potential propensity to pay more attention to vocalizations of elders. On the basis of several hundreds of vocal exchanges recorded, here we show that aged female Campbell''s monkeys (Cercopithecus campbelli), despite being significantly less ‘loquacious’ than their younger adult counterparts, elicit many more responses when calling. These findings show that attention to elders'' vocal production appears in non-human primates, leading to new lines of questioning on human culture and language evolution.     

Origin of symbol-using systems: speech,but not sign,without the semantic urge

Natural language—spoken and signed—is a multichannel phenomenon, involving facial and body expression, and voice and visual intonation that is often used in the service of a social urge to communicate meaning. Given that iconicity seems easier and less abstract than making arbitrary connections between sound and meaning, iconicity and gesture have often been invoked in the origin of language alongside the urge to convey meaning. To get a fresh perspective, we critically distinguish the origin of a system capable of evolution from the subsequent evolution that system becomes capable of. Human language arose on a substrate of a system already capable of Darwinian evolution; the genetically supported uniquely human ability to learn a language reflects a key contact point between Darwinian evolution and language. Though implemented in brains generated by DNA symbols coding for protein meaning, the second higher-level symbol-using system of language now operates in a world mostly decoupled from Darwinian evolutionary constraints. Examination of Darwinian evolution of vocal learning in other animals suggests that the initial fixation of a key prerequisite to language into the human genome may actually have required initially side-stepping not only iconicity, but the urge to mean itself. If sign languages came later, they would not have faced this constraint.     

Coevolution of vocal communication and sociality in primates

Understanding the rules that link communication and social behaviour is an essential prerequisite for discerning how a communication system as complex as human language might have evolved. The comparative method offers a powerful tool for investigating the nature of these rules, since it provides a means to examine relationships between changes in communication abilities and changes in key aspects of social behaviour over evolutionary time. Here we present empirical evidence from phylogenetically controlled analyses indicating that evolutionary increases in the size of the vocal repertoire among non-human primate species were associated with increases in both group size and time spent grooming (our measure of extent of social bonding).     

Vocal turn-taking in a non-human primate is learned during ontogeny

Conversational turn-taking is an integral part of language development, as it reflects a confluence of social factors that mitigate communication. Humans coordinate the timing of speech based on the behaviour of another speaker, a behaviour that is learned during infancy. While adults in several primate species engage in vocal turn-taking, the degree to which similar learning processes underlie its development in these non-human species or are unique to language is not clear. We recorded the natural vocal interactions of common marmosets (Callithrix jacchus) occurring with both their sibling twins and parents over the first year of life and observed at least two parallels with language development. First, marmoset turn-taking is a learned vocal behaviour. Second, marmoset parents potentially played a direct role in guiding the development of turn-taking by providing feedback to their offspring when errors occurred during vocal interactions similarly to what has been observed in humans. Though species-differences are also evident, these findings suggest that similar learning mechanisms may be implemented in the ontogeny of vocal turn-taking across our Order, a finding that has important implications for our understanding of language evolution.     

Language evolution and an emergent property

Much debate has been stimulated by the recent hypothesis that human language consists of a faculty that is shared with non-human animals (faculty of language in a broad sense; FLB) and a faculty that is specific to human language (faculty of language in a narrow sense; FLN). This hypothesis has encouraged a tendency to emphasize one component of FLN: the cognitive operation of recursion. In consequence, non-syntactical, yet unique, aspects of human language have been neglected. One of these properties consists of vocal learning that enables an abundance of learned syllables. I suggest that FLN is not an independent faculty, but an 'emergent' property, arising from interactions between several other non-syntactical subfaculties of FLB, including vocal learning ability.     

The origin of human multi-modal communication

One reason for the apparent gulf between animal and human communication systems is that the focus has been on the presence or the absence of language as a complex expressive system built on speech. But language normally occurs embedded within an interactional exchange of multi-modal signals. If this larger perspective takes central focus, then it becomes apparent that human communication has a layered structure, where the layers may be plausibly assigned different phylogenetic and evolutionary origins—especially in the light of recent thoughts on the emergence of voluntary breathing and spoken language. This perspective helps us to appreciate the different roles that the different modalities play in human communication, as well as how they function as one integrated system despite their different roles and origins. It also offers possibilities for reconciling the ‘gesture-first hypothesis’ with that of gesture and speech having evolved together, hand in hand—or hand in mouth, rather—as one system.     

Brevity is prevalent in bat short-range communication

Animal communication follows many coding schemes. Less is known about the coding strategy for signal length and rates of use in animal vocal communication. A generalized brevity (negative relation between signal length and frequency of use) is innovatively explored but remains controversial in animal vocal communication. We tested brevity for short-range social and distress sounds from four echolocating bats: adult black-bearded tomb bat Taphozous melanopogon, Mexican free-tailed bat Tadarida brasiliensis, adult greater horseshoe bat Rhinolophus ferrumequinum, and adult least horseshoe bat Rhinolophus pusillus. There was a negative association between duration and number of social but not distress calls emitted. The most frequently emitted social calls were brief, while most distress calls were long. Brevity or lengthiness was consistently selected in vocal communications for each species. Echolocating bats seem to have convergent coding strategy for communication calls. The results provide the evidence of efficient coding in bat social vocalizations, and lay the basis of future researches on the convergence for neural control on bats’ communication calls.     

Auditory–vocal mirroring in songbirds

Mirror neurons are theorized to serve as a neural substrate for spoken language in humans, but the existence and functions of auditory–vocal mirror neurons in the human brain remain largely matters of speculation. Songbirds resemble humans in their capacity for vocal learning and depend on their learned songs to facilitate courtship and individual recognition. Recent neurophysiological studies have detected putative auditory–vocal mirror neurons in a sensorimotor region of the songbird''s brain that plays an important role in expressive and receptive aspects of vocal communication. This review discusses the auditory and motor-related properties of these cells, considers their potential role on song learning and communication in relation to classical studies of birdsong, and points to the circuit and developmental mechanisms that may give rise to auditory–vocal mirroring in the songbird''s brain.     

The function of nonlinear phenomena in meerkat alarm calls

Nonlinear vocal phenomena are a ubiquitous feature of human and non-human animal vocalizations. Although we understand how these complex acoustic intrusions are generated, it is not clear whether they function adaptively for the animals producing them. One explanation is that nonlinearities make calls more unpredictable, increasing behavioural responses and ultimately reducing the chances of habituation to these call types. Meerkats (Suricata suricatta) exhibit nonlinear subharmonics in their predator alarm calls. We specifically tested the ‘unpredictability hypothesis’ by playing back naturally occurring nonlinear and linear medium-urgency alarm call bouts. Results indicate that subjects responded more strongly and foraged less after hearing nonlinear alarm calls. We argue that these findings support the unpredictability hypothesis and suggest this is the first study in animals or humans to show that nonlinear vocal phenomena function adaptively.     

Sex hormone influence on human infants' sound characteristics: melody in spontaneous crying

The specific impact of sex hormones on brain development and acoustic communication is known from animal models. Sex steroid hormones secreted during early development play an essential role in hemispheric organization and the functional lateralization of the brain, e.g. language. In animals, these hormones are well-known regulators of vocal motor behaviour. Here, the association between melody properties of infants'' sounds and serum concentrations of sex steroids was investigated. Spontaneous crying was sampled in 18 healthy infants, averaging two samples taken at four and eight weeks, respectively. Blood samples were taken within a day of the crying samples. The fundamental frequency contour (melody) was analysed quantitatively and the infants'' frequency modulation skills expressed by a melody complexity index (MCI). These skills provide prosodic primitives for later language. A hierarchical, multiple regression approach revealed a significant, robust relationship between the individual MCIs and the unbound, bioactive fraction of oestradiol at four weeks as well as with the four-to-eight-week difference in androstenedione. No robust relationship was found between the MCI and testosterone. Our findings suggest that oestradiol may have effects on the development and function of the auditory–vocal system in human infants that are as powerful as those in vocal-learning animals.     

The origins of non-human primates' manual gestures

The increasing body of research into human and non-human primates' gestural communication reflects the interest in a comparative approach to human communication, particularly possible scenarios of language evolution. One of the central challenges of this field of research is to identify appropriate criteria to differentiate a gesture from other non-communicative actions. After an introduction to the criteria currently used to define non-human primates' gestures and an overview of ongoing research, we discuss different pathways of how manual actions are transformed into manual gestures in both phylogeny and ontogeny. Currently, the relationship between actions and gestures is not only investigated on a behavioural, but also on a neural level. Here, we focus on recent evidence concerning the differential laterality of manual actions and gestures in apes in the framework of a functional asymmetry of the brain for both hand use and language.     

Vocal production mechanisms in a non-human primate: morphological data and a model

Human beings are thought to be unique amongst the primates in their capacity to produce rapid changes in the shape of their vocal tracts during speech production. Acoustically, vocal tracts act as resonance chambers, whose geometry determines the position and bandwidth of the formants. Formants provide the acoustic basis for vowels, which enable speakers to refer to external events and to produce other kinds of meaningful communication. Formant-based referential communication is also present in non-human primates, most prominently in Diana monkey alarm calls. Previous work has suggested that the acoustic structure of these calls is the product of a non-uniform vocal tract capable of some degree of articulation. In this study we test this hypothesis by providing morphological measurements of the vocal tract of three adult Diana monkeys, using both radiography and dissection. We use these data to generate a vocal tract computational model capable of simulating the formant structures produced by wild individuals. The model performed best when it combined a non-uniform vocal tract consisting of three different tubes with a number of articulatory manoeuvres. We discuss the implications of these findings for evolutionary theories of human and non-human vocal production.     

Suffixation influences receivers' behaviour in non-human primates

Compared to humans, non-human primates have very little control over their vocal production. Nonetheless, some primates produce various call combinations, which may partially offset their lack of acoustic flexibility. A relevant example is male Campbell''s monkeys (Cercopithecus campbelli), which give one call type (‘Krak’) to leopards, while the suffixed version of the same call stem (‘Krak-oo’) is given to unspecific danger. To test whether recipients attend to this suffixation pattern, we carried out a playback experiment in which we broadcast naturally and artificially modified suffixed and unsuffixed ‘Krak’ calls of male Campbell''s monkeys to 42 wild groups of Diana monkeys (Cercopithecus diana diana). The two species form mixed-species groups and respond to each other''s vocalizations. We analysed the vocal response of male and female Diana monkeys and overall found significantly stronger vocal responses to unsuffixed (leopard) than suffixed (unspecific danger) calls. Although the acoustic structure of the ‘Krak’ stem of the calls has some additional effects, subject responses were mainly determined by the presence or the absence of the suffix. This study indicates that suffixation is an evolved function in primate communication in contexts where adaptive responses are particularly important.     

Combinatorial Communication in Bacteria: Implications for the Origins of Linguistic Generativity

Combinatorial communication, in which two signals are used together to achieve an effect that is different to the sum of the effects of the component parts, is apparently rare in nature: it is ubiquitous in human language, appears to exist in a simple form in some non-human primates, but has not been demonstrated in other species. This observed distribution has led to the pair of related suggestions, that (i) these differences in the complexity of observed communication systems reflect cognitive differences between species; and (ii) that the combinations we see in non-human primates may be evolutionary pre-cursors of human language. Here we replicate the landmark experiments on combinatorial communication in non-human primates, but in an entirely different species, unrelated to humans, and with no higher cognition: the bacterium Pseudomonas aeruginosa. Using the same general methods as the primate studies, we find the same general pattern of results: the effect of the combined signal differs from the composite effect of the two individual signals. This suggests that advanced cognitive abilities and large brains do not necessarily explain why some species have combinatorial communication systems and others do not. We thus argue that it is premature to conclude that the systems observed in non-human primates are evolutionarily related to language. Our results illustrate the value of an extremely broad approach to comparative research.     

Experience-dependent emergence of a grouping bias

Humans share with non-human animals perceptual biases that might form the basis of complex cognitive abilities. One example comes from the principles described by the iambic–trochaic law (ITL). According to the ITL, sequences of sounds varying in duration are grouped as iambs, whereas sequences varying in intensity are grouped as trochees. These grouping biases have gained much attention because they might help pre-lexical infants bootstrap syntactic parameters (such as word order) in their language. Here, we explore how experience triggers the emergence of perceptual grouping biases in a non-human species. We familiarized rats with either long–short or short–long tone pairs. We then trained the animals to discriminate between sequences of alternating and randomly ordered tones. Results showed animals developed a grouping bias coherent with the exposure they had. Together with results observed in human adults and infants, these results suggest that experience modulates perceptual organizing principles that are present across species.     

Primate vocal communication: a useful tool for understanding human speech and language evolution?

Language is a uniquely human trait, and questions of how and why it evolved have been intriguing scientists for years. Nonhuman primates (primates) are our closest living relatives, and their behavior can be used to estimate the capacities of our extinct ancestors. As humans and many primate species rely on vocalizations as their primary mode of communication, the vocal behavior of primates has been an obvious target for studies investigating the evolutionary roots of human speech and language. By studying the similarities and differences between human and primate vocalizations, comparative research has the potential to clarify the evolutionary processes that shaped human speech and language. This review examines some of the seminal and recent studies that contribute to our knowledge regarding the link between primate calls and human language and speech. We focus on three main aspects of primate vocal behavior: functional reference, call combinations, and vocal learning. Studies in these areas indicate that despite important differences, primate vocal communication exhibits some key features characterizing human language. They also indicate, however, that some critical aspects of speech, such as vocal plasticity, are not shared with our primate cousins. We conclude that comparative research on primate vocal behavior is a very promising tool for deepening our understanding of the evolution of human speech and language, but much is still to be done as many aspects of monkey and ape vocalizations remain largely unexplored.     

Towards theoretical formalisms

This article deals with the relationship between vocabulary (total number of distinct oligomers or “words”) and text-length (total number of oligomers or “words”) for a coding DNA sequence (CDS). For natural human languages, Heaps established a mathematical formula known as Heaps’ law, which relates vocabulary to text-length. Our analysis shows that Heaps’ law fails to model this relationship for CDSs. Here we develop a mathematical model to establish the relationship between the number of type of words (vocabulary) and the number of words sampled (text-length) for CDSs, when non-overlapping nucleotide strings with the same length are treated as words. We use tangent-hyperbolic function, which captures the saturation property of vocabulary. Based on the parameters of the model, we formulate a mathematical equation, known as “equation of word organization”, whose parameters essentially indicate that nucleotide organization of coding sequences are different from one another. We also compare the word organization of CDSs with the random word distribution and conclude that a CDS is neither similar to a natural human language nor to a random one. Moreover, these sequences have their unique nucleotide organization and it is completely structured for specific biological functioning.