Economic behaviours among non-human primates

Do we have any valid reasons to affirm that non-human primates display economic behaviour in a sufficiently rich and precise sense of the phrase? To address this question, we have to develop a set of criteria to assess the vast array of experimental studies and field observations on individual cognitive and behavioural competences as well as the collective organization of non-human primates. We review a sample of these studies and assess how they answer to the following four main challenges. (i) Do we see any economic organization or institutions emerge among groups of non-human primates? (ii) Are the cognitive abilities, and often biases, that have been evidenced as underlying typical economic decision-making among humans, also present among non-human primates? (iii) Can we draw positive lessons from performance comparisons among primate species, humans and non-humans but also across non-human primate species, as elicited by canonical game-theoretical experimental paradigms, especially as far as economic cooperation and coordination are concerned? And (iv) in which way should we improve models and paradigms to obtain more ecological data and conclusions? Articles discussed in this paper most often bring about positive answers and promising perspectives to support the existence and prevalence of economic behaviours among non-human primates.This article is part of the theme issue ‘Existence and prevalence of economic behaviours among non-human primates’.     

Transitive inference in non-human animals: an empirical and theoretical analysis

Transitive inference has long been considered one of the hallmarks of human deductive reasoning. Recent reports of transitive-like behaviors in non-human animals have prompted a flourishing empirical and theoretical search for the mechanism(s) that may mediate this ability in non-humans. In this paper, I begin by describing the transitive inference tasks customarily used with non-human animals and then review the empirical findings. Transitive inference has been demonstrated in a wide variety of species, and the signature effects that usually accompany transitive inference in humans (the serial position effect and the symbolic distance effect) have also been found in non-humans. I then critically analyze the most prominent models of this ability in non-human animals. Some models are cognitive, proposing for instance that animals use the rules of formal logic or form mental representations of the premises to solve the task, others are based on associative mechanisms such as value transfer and reinforcement and non-reinforcement. Overall, I argue that the reinforcement-based models are in a much better empirical and theoretical position. Hence, transitive inference in non-human animals should be considered a property of reinforcement history rather than of inferential processes. I finalize by shedding some light on some promising lines of research.     

From proto-mimesis to language: evidence from primatology and social neuroscience.

How can we reconcile the conception of language as a conventional-normative semiotic system with a perception/action-based account of its structure and meaning? And why should linguistic meaning--as opposed to linguistic expression--be so closely related to motor activity and its neural underpinnings, as suggested by recent findings? A conceptual framework and evolutionary scenario building on the concept of bodily mimesis [Zlatev, J., 2005. What's in a schema? Bodily mimesis and the grounding of language. In: Hampe, B. (Ed.), From Perception to Meaning: Image Schemas in Cognitive Linguistics. Mouton de Gruyter, Berlin, pp. 313-343] imply answers to these questions. The article presents evidence for a particular evolutionary stage model by reviewing recent evidence on the capacity of non-human primates for intersubjectivity, imitation and gestural communication, and from neuroscientific studies of these capacities in monkeys and human subjects. It is argued that "mirror neuron" systems can subserve basic motoric and social capacities, but they need to be considerably extended in order to provide an efficient basis for bodily mimesis, and even more so for language. It is argued that while language may be ultimately "grounded" in perception and action, it is essential not to try to reduce it to them.     

Do young rhesus macaques know what others see?: A comparative developmental perspective

Humans undergo robust ontogenetic shifts in the theory of mind capabilities. Are these developmental changes unique to human development or are they shared with other closely related non-human species? To explore this issue, we tested the development of the theory of mind capacities in a population of 236 infant and juvenile rhesus macaques (Macaca mulatta). Using a looking-time method, we examined what developing monkeys know about others’ perceptions. Specifically, we tested whether younger monkeys predict that a person will reach for an object where she last saw it. Overall, we found a significant interaction between a monkey's age and performance on this task (p = .014). Juvenile monkeys (between two and 5 years of age) show a nonsignificant trend towards human infant-like patterns of performance, looking longer during the unexpected condition as compared to the expected condition, though this difference is nonsignificant (p = .09). However, contrary to findings in human infants, infant rhesus macaques show a different trend. Infant monkeys on average look slightly longer on average during the expected condition than the unexpected condition, though this pattern was not significant (p = .06). Our developmental results in monkeys provide some hints about the development of the theory of mind capacities in non-humans. First, young rhesus macaques appear to show some interest in the perception of other agents. Second, young rhesus seems able to make predictions based on the visual perspective of another agent, though the developmental pattern of this ability is not as clear nor as robust as in humans. As such, though an understanding of others’ perceptions is early-emerging in human infants, it may require more experience interacting with other social agents in our non-human relatives.     

Mitochondrial and Nuclear Ribosomal DNA Evidence Supports the Existence of a New Trichuris Species in the Endangered Fran?ois’ Leaf-Monkey

The whipworm of humans, Trichuris trichiura, is responsible for a neglected tropical disease (NTD) of major importance in tropical and subtropical countries of the world. Whipworms also infect animal hosts, including pigs, dogs and non-human primates, cause clinical disease (trichuriasis) similar to that of humans. Although Trichuris species are usually considered to be host specific, it is not clear whether non-human primates are infected with T. trichiura or other species. In the present study, we sequenced the complete mitochondrial (mt) genome as well as the first and second internal transcribed spacers (ITS-1 and ITS-2) of Trichuris from the François’ leaf-monkey (langur), and compared them with homologous sequences from human- and pig-derived Trichuris. In addition, sequence comparison of a conserved mt ribosomal gene among multiple individual whipworms revealed substantial nucleotide differences among these three host species but limited sequence variation within each of them. The molecular data indicate that the monkey-derived whipworm is a separate species from that of humans. Future work should focus on detailed population genetic and morphological studies (by electron microscopy) of whipworms from various non-humans primates and humans.     

The disadvantage of combinatorial communication

Combinatorial communication allows rapid and efficient transfer of detailed information, yet combinatorial communication is used by few, if any, non-human species. To complement recent studies illustrating the advantages of combinatorial communication, we highlight a critical disadvantage. We use the concept of information value to show that deception poses a greater and qualitatively different threat to combinatorial signalling than to non-combinatorial systems. This additional potential for deception may represent a strategic barrier that has prevented widespread evolution of combinatorial communication. Our approach has the additional benefit of drawing clear distinctions among several types of deception that can occur in communication systems.     

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.     

Bemerkungen zur Evolution von., Sprachen bei Säugetieren1 Zur Variabilität innerartlicher Kommunikation bei Caniden

Remarks on the evolution of “languages” of mammals. The variability of the intraspecific communication of canids The canid species mainly considered in this study, the golden jackal (Canis aureus), the cojote (Canis latrans), and especially the wolf (Canis lupus) have an extremely variable species-specific intraspecific communication. Communities, but also differences between the species become evident; the wolf with its distinct social behavior has the greatest differentiation. These results make also clear, that forms of communication in mammals develop in evolutionary processes and events. A safe statement on the beginning of the forms of communication in canids cannot be given so far. This is also true for humans. The ideas of Lenneberg (1967) of the parallel and disjunct origin of the forms of communication in mammals has a high probability for higher systematic units, but on lower systematic level a gradual change can be observed. The forms of communication in mammals are highly differentiated structures, where specific pecularities of the brain are of a special importance. The observations on the variability of intraspecific communication of canids, representing nonhuman mammals, suggest to define “language” in a very general form. In this way, similarities, analogies, and differences between the species of mammals, inclusive man, can be seen more clearly. In only this way the material can be gained to answer the question, if the language of man has in principle exceptional position biologically. It is important for the valuation of forms of intraspecific communication, the “languages”, of mammals not to choose human theory of life and human thinking as a basis, but to start with the biological pecularities of the species. Also canids, as higher mammals, have the ability to abstract, a form of thinking. In their special, species-specific way also non-human mammals arrange their area of experience and thinking. They form for themselves a species-specific “theory of live”. This will of course be different from the human one, according to the systematic position and the biological environment of the species. It is generally accepted that man has special abilities of thinking, he possesses an extraordinary developed brain, compared to all other mammals. This must effect his communication, his language, and result in differences to other mammal species. Gipper (1977) pointed out especially these differences, but they should not be interpreted as differences in principle. Canids use different gestures and sounds for communication within the species; dialog relations can be observed. Different connections of gestures and sounds have different contents of information. It is remarkable that canids do not use their total abilities in using the means of communication in the same way. This is very striking in the change from the wolf, as the only ancestor, to the domestic dog. It is evident that the brain has a greater importance in developing intraspecific communication, than do the peculuarities of organs causing the understanding. A dependanc of intraspecific communication from the environment can be observed either in differences of wird species of canids as well as in the domestication. In the domestic dog, but also in other domestic animals, there is an increase in vocalisations. But the content of information of sounds and gestures decreases in domestication, expressions of arousal become more important. A remarkable plasticity of intraspecific communication becomes evident by domestication. The transformations can be evaluated in the sense of Kosswig (1963, 1965) as first stages of a regressive evolution. Experiments of cross-breeding canid species show exemplarily that forms of communication within these mammal species have a highly polygene regulation, and that processes of learning have an influence. Also from this point of view, no basic differences between nonhuman mammals and humans can be assured, especially when taking into account the facts and thoughts described by Lenneberg. The findings in the canids give useful hints for a better understanding of the human language and its relations to the forms of communication in other mammals. Altogether one can conclude that genetic variability, numerous recombinations, the synorganisation of the processes caused in this way, and natural selection plays definite role in the evolution of “languages”.     

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).     

Campbell's Monkeys Use Affixation to Alter Call Meaning

Human language has evolved on a biological substrate with phylogenetic roots deep in the primate lineage. Here, we describe a functional analogy to a common morphological process in human speech, affixation, in the alarm calls of free-ranging adult Campbell''s monkeys (Cercopithecus campbelli campbelli). We found that male alarm calls are composed of an acoustically variable stem, which can be followed by an acoustically invariable suffix. Using long-term observations and predator simulation experiments, we show that suffixation in this species functions to broaden the calls'' meaning by transforming a highly specific eagle alarm to a general arboreal disturbance call or by transforming a highly specific leopard alarm call to a general alert call. We concluded that, when referring to specific external events, non-human primates can generate meaningful acoustic variation during call production that is functionally equivalent to suffixation in human language.     

Take up the challenge! Opportunities for evolution research from resolving conflict in integrative taxonomy

What's in a species? The multiple connotations of the question tend to lack simple answers, and not surprisingly so. For example, speciation is a gradual process. Can we say when exactly a child has become an adult? We have precocious youngsters and late bloomers, and often, adults are in some ways childish. There are many triggers for and routes to adolescence. All this holds for speciation, and delimiting species can therefore be a tricky task. Recently, the field of integrative taxonomy has emerged—species delimitation based on multiple sources of evidence. Given that we expect species to exhibit peculiarities in at least one or a few aspects, might it be their alleles of a gene, their morphology, chemistry, behaviour, ecology, reproductive compatibility, or whatever, investigating not just one but several of these aspects makes it more likely that we capture such peculiarities. If the same pattern is found multiply, we talk about agreement among disciplines, and species delimitation is easy. But what if different disciplines tell different stories? Such disagreement makes species delimitation more difficult but is also an opportunity for evolutionary biology (Schlick‐Steiner et al. 2010). In this issue of Molecular Ecology, Andújar et al. (2014) present a comprehensive integrative‐taxonomic case study of Mesocarabus ground beetles including nomenclatural consequences. They resolve extensive disagreement among disciplines by invoking evolutionary explanations, and the process of conflict resolution thus advances knowledge on species boundaries and evolutionary processes simultaneously.     

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。     

Introduction. The perception of speech: from sound to meaning

Spoken language communication is arguably the most important activity that distinguishes humans from non-human species. This paper provides an overview of the review papers that make up this theme issue on the processes underlying speech communication. The volume includes contributions from researchers who specialize in a wide range of topics within the general area of speech perception and language processing. It also includes contributions from key researchers in neuroanatomy and functional neuro-imaging, in an effort to cut across traditional disciplinary boundaries and foster cross-disciplinary interactions in this important and rapidly developing area of the biological and cognitive sciences.     

Kinship appeals and conservation social marketing

Increasing environmental problems and the need to obtain public support to help address them make effective appeals in conservation fundraising campaigns indispensable. However, social marketing messages based on data, characteristics of focal species, self-interest, and moral responsibility tend to work best on targeted, and so limited, audiences. As conservation organizations reach out to broader audiences, they will require strategies that appeal to more potential donors. This paper argues that use of kinship symbolism to describe non-human species should make conservation marketing campaigns more effective. Evolutionary theories of altruism predict the power of kinship-recognition cues in encouraging and reinforcing sacrifice in non-kin, unreciprocated contexts, and these cues can be manipulated in marketing campaigns to protect threatened species and resources. People often behave altruistically toward “fictive” kin, and the labeling of non-humans as kin in many traditional, small-scale societies appears to be associated with environmental resource management. Characterizing non-human species, and even non-living resources, as kin to humans in marketing campaigns may promote a willingness to contribute to conservation-related causes.     

Sexual arousal, is it for mammals only?

Sexual arousal has many dimensions and has consequently been defined in various ways. In humans, sexual arousal can be assessed based in part on verbal communication. In male non-human mammalian species, it has been argued that arousal can only be definitively inferred if the subject exhibits a penile erection in a sexual context. In non-mammalian species that lack an intromittent organ, as is the case for most avian species, the question of how to assess sexual arousal has not been thoroughly addressed. Based on studies performed in male Japanese quail, we argue that several behavioral or physiological characteristics provide suitable measures of sexual arousal in birds and probably also in other tetrapods. These indices include, the performance of appetitive sexual behavior in anticipation of copulation (although anticipation and arousal are not synonymous), the activation of specific brain area as identified by the detection of the expression of immediate early genes (fos, egr-1) or by 2-deoxygucose quantitative autoradiography, and above all, by the release of dopamine in the medial preoptic area as measured by in vivo dialysis. Based on these criteria, it is possible to assess in birds sexual arousal in its broadest sense but meeting the more restrictive definition of arousal proposed for male mammals (erection in an explicit sexual context) is and will probably remain impossible in birds until refinement of in vivo imaging techniques such fMRI allow us to match in different species, with and without an intromittent organ, the brain areas that are activated in the presence of specific stimuli.     

Affective responses in tamarins elicited by species-specific music

Theories of music evolution agree that human music has an affective influence on listeners. Tests of non-humans provided little evidence of preferences for human music. However, prosodic features of speech (‘motherese’) influence affective behaviour of non-verbal infants as well as domestic animals, suggesting that features of music can influence the behaviour of non-human species. We incorporated acoustical characteristics of tamarin affiliation vocalizations and tamarin threat vocalizations into corresponding pieces of music. We compared music composed for tamarins with that composed for humans. Tamarins were generally indifferent to playbacks of human music, but responded with increased arousal to tamarin threat vocalization based music, and with decreased activity and increased calm behaviour to tamarin affective vocalization based music. Affective components in human music may have evolutionary origins in the structure of calls of non-human animals. In addition, animal signals may have evolved to manage the behaviour of listeners by influencing their affective state.     

Coevolutionary aesthetics in human and biotic artworlds

This work proposes a coevolutionary theory of aesthetics that encompasses both biotic and human arts. Anthropocentric perspectives in aesthetics prevent the recognition of the ontological complexity of the aesthetics of nature, and the aesthetic agency of many non-human organisms. The process of evaluative coevolution is shared by all biotic advertisements. I propose that art consists of a form of communication that coevolves with its own evaluation. Art and art history are population phenomena. I expand Arthur Danto’s Artworld concept to any aesthetic population of producers and evaluators. Current concepts of art cannot exclusively circumscribe the human arts from many forms of non-human biotic art. Without assuming an arbitrarily anthropocentric perspective, any concept of art will need to engage with biodiversity, and either recognize many instances of biotic advertisements as art, or exclude some instances of human art. Coevolutionary aesthetic theory provides a heuristic account of aesthetic change in both human and biotic artworlds, including the coevolutionary origin of aesthetic properties and aesthetic value within artworlds. Restructuring aesthetics, art criticism, and art history without human beings at the organizing centers of these disciplines stimulate new progress in our understanding of art, and the unique human contributions to aesthetics and aesthetic diversity.     

Investigating the potential for call combinations in a lifelong vocal learner

The ability for humans to create seemingly infinite meaning from a finite set of sounds has likely been a critical component in our success as a species, allowing the unbounded communication of information. Syntax, the combining of meaningful sounds into phrases, is one of the primary features of language that enables this extensive expressivity. The evolutionary history of syntax, however, remains largely debated, and it is only very recently that comparative data for syntax in animals have been revealed. Here, we provide further evidence for a structural basis of potential syntactic‐like call combinations in the vocal communication system of a group‐living songbird. Acoustic analyses indicate that Western Australian magpies (Gymnorhina tibicen dorsalis) structurally combine generic alarm calls with acoustically distinct alert calls to produce an alarm alert sequence. These results are distinct from previous examples of call combinations as, to our knowledge, evidence for this capacity is yet to be demonstrated in the natural communication of a non‐human species that is capable of vocal learning throughout life. These findings offer prospects for experimental investigation into the presence and function of magpie call combinations, extending our understanding of animal vocal complexity.     

Concealing of facial expressions by a wild Barbary macaque (Macaca sylvanus)

Behavioural research on non-vocal communication among non-human primates and its possible links to the origin of human language is a long-standing research topic. Because human language is under voluntary control, it is of interest whether this is also true for any communicative signals of other species. It has been argued that the behaviour of hiding a facial expression with one’s hand supports the idea that gestures might be under more voluntary control than facial expressions among non-human primates, and it has also been interpreted as a sign of intentionality. So far, the behaviour has only been reported twice, for single gorilla and chimpanzee individuals, both in captivity. Here, we report the first observation of concealing of facial expressions by a monkey, a Barbary macaque (Macaca sylvanus), living in the wild. On eight separate occasions between 2009 and 2011 an adult male was filmed concealing two different facial expressions associated with play and aggression (“play face” and “scream face”), 22 times in total. The videos were analysed in detail, including gaze direction, hand usage, duration, and individuals present. This male was the only individual in his group to manifest this behaviour, which always occurred in the presence of a dominant male. Several possible interpretations of the function of the behaviour are discussed. The observations in this study indicate that the gestural communication and cognitive abilities of monkeys warrant more research attention.     

Definitions of pathogenicity and virulence in invertebrate pathology

Accurate definition and usage of terminology are critical to effective communication in science. In a recently published article, the clarity and consistency of the terms pathogenicity and virulence as used in invertebrate pathology were called into question, and a revision of these terms was proposed. Our objective was to examine definitions of pathogenicity and virulence and their use in invertebrate pathology, and respond to this article. Although usage of the terms pathogenicity and virulence varies, we found considerable consistency in the published definitions of these terms in the invertebrate pathology literature throughout the history of the discipline, as well as among related disciplines such as medicine and microbiology. We did not find the established definitions to be lacking in clarity or utility. Therefore, we recommend that the definition and use of these terms adhere to precedence. Specifically, pathogenicity is the quality or state of being pathogenic, the potential ability to produce disease, whereas virulence is the disease producing power of an organism, the degree of pathogenicity within a group or species. Pathogenicity is a qualitative term, an “all-or-none” concept, whereas virulence is a term that quantifies pathogenicity.