Michael J. Owren

What do animal signals mean

Animal communication studies often use analogies to human language and related constructs such as information encoding and transfer. This commonality is evident even when research goals are very different, for example when primate vocalizations are proposed to have word-like meaning, or sexually selected signals are proposed to convey information about a signaller’s underlying quality. We consider some of the ambiguities and limitations inherent in such informational approaches to animal communication as background to advocating alternatives. The alternatives eschew language-based metaphors and broader informational constructs and focus instead on concrete details of signal design as they reflect and interact with established sensory, physiological and psychological processes that support signalling and responding in listeners. The alternatives we advocate also explicitly acknowledge the different roles and often divergent interests of signallers and perceivers that can yield fundamental asymmetries in signalling interactions, and they therefore shift the focus of interpretations of animal communication from informing others to influencing others.

Reconstructing the Evolution of Laughter in Great Apes and Humans

Human emotional expressions, such as laughter, are argued to have their origins in ancestral nonhuman primate displays. To test this hypothesis, the current work examined the acoustics of tickle-induced vocalizations from infant and juvenile orangutans, gorillas, chimpanzees, and bonobos, as well as tickle-induced laughter produced by human infants. Resulting acoustic data were then coded as character states and submitted to quantitative phylogenetic analysis. Acoustic outcomes revealed both important similarities and differences among the five species. Furthermore, phylogenetic trees reconstructed from the acoustic data matched the well-established trees based on comparative genetics. Taken together, the results provide strong evidence that tickling-induced laughter is homologous in great apes and humans and support the more general postulation of phylogenetic continuity from nonhuman displays to human emotional expressions. Findings also show that distinctively human laughter characteristics such as predominantly regular, stable voicing and consistently egressive airflow are nonetheless traceable to characteristics of shared ancestors with great apes.

Two organizing principles of vocal production: Implications for nonhuman and human primates.

Vocal communication in nonhuman primates receives considerable research attention, with many investigators arguing for similarities between this calling and speech in humans. Data from development and neural organization show a central role of affect in monkey and ape sounds, however, suggesting that their calls are homologous to spontaneous human emotional vocalizations while having little relation to spoken language. Based on this evidence, we propose two principles that can be useful in evaluating the many and disparate empirical findings that bear on the nature of vocal production in nonhuman and human primates. One principle distinguishes production‐first from reception‐first vocal development, referring to the markedly different role of auditory‐motor experience in each case. The second highlights a phenomenon dubbed dual neural pathways, specifically that when a species with an existing vocal system evolves a new functionally distinct vocalization capability, it occurs through emergence of a second parallel neural pathway rather than through expansion of the extant circuitry. With these principles as a backdrop, we review evidence of acoustic modification of calling associated with background noise, conditioning effects, audience composition, and vocal convergence and divergence in nonhuman primates. Although each kind of evidence has been interpreted to show flexible cognitively mediated control over vocal production, we suggest that most are more consistent with affectively grounded mechanisms. The lone exception is production of simple, novel sounds in great apes, which is argued to reveal at least some degree of volitional vocal control. If also present in early hominins, the cortically based circuitry surmised to be associated with these rudimentary capabilities likely also provided the substrate for later emergence of the neural pathway allowing volitional production in modern humans. Am. J. Primatol. 73:530–544, 2011.

Sexual selection on male vocal fundamental frequency in humans and other anthropoids

In many primates, including humans, the vocalizations of males and females differ dramatically, with male vocalizations and vocal anatomy often seeming to exaggerate apparent body size. These traits may be favoured by sexual selection because low-frequency male vocalizations intimidate rivals and/or attract females, but this hypothesis has not been systematically tested across primates, nor is it clear why competitors and potential mates should attend to vocalization frequencies. Here we show across anthropoids that sexual dimorphism in fundamental frequency (F0) increased during evolutionary transitions towards polygyny, and decreased during transitions towards monogamy. Surprisingly, humans exhibit greater F0 sexual dimorphism than any other ape. We also show that low-F0 vocalizations predict perceptions of mens dominance and attractiveness, and predict hormone profiles (low cortisol and high testosterone) related to immune function. These results suggest that low male F0 signals condition to competitors and mates, and evolved in male anthropoids in response to the intensity of mating competition.

GSU Praat Tools: Scripts for modifying and analyzing sounds using Praat acoustics software

The Praat acoustics program (Boersma, 2001) is powerful freeware that is widely used by behavioral scientists working with digital sound. This article describes GSU Praat Tools, a script package that helps simplify and automate such work. The routines use Praat’s scripting language to create new menus and commands within the existing interface, and can operate either on individual files or in batch mode. The new functions facilitate selecting, displaying, editing, filtering, and otherwise modifying sounds, quantifying acoustic features, and saving results in text-based data files. The package includes an installation script and user’s manual, and is available free from psyvoso.googlepages.com/softwaredownload.

Listeners Judge Talker Sex More Efficiently from Male Than from Female Vowels

Speech routinely provides cues as to the sex of the talker; in voiced sounds, these cues mainly reflect dimorphism in vocal anatomy. This dimorphism is not symmetrical, however, since during adolescent development, males specifically diverge from a previously shared trajectory with females. We therefore predicted that listeners would show a corresponding perceptual advantage for male sounds in talker-sex discrimination, a hypothesis tested using very brief, one- to eight-cycle vowel segments. The expected performance asymmetry was observed in threshold-like tests of multiple different vowels in Experiments 1–3, and a signal detection design in Experiment 4 helped rule out possible response bias effects. In confirming our counterintuitive prediction, the present study illustrates that a biological and evolutionary perspective can be helpful in understanding indexical cuing in speech.

The evolution of laughter in great apes and humans

It has long been claimed that human emotional expressions, such as laughter, have evolved from nonhuman displays. The aim of the current study was to test this prediction by conducting acoustic and phylogenetic analyses based on the acoustics of tickle-induced vocalizations of orangutans, gorillas, chimpanzees, bonobos, and humans. Results revealed both important similarities and differences among the various species’ vocalizations, with the phylogenetic tree reconstructed based on these acoustic data matching the well-established genetic relationships of great apes and humans. These outcomes provide evidence of a common phylogenetic origin of tickle-induced vocalizations in these taxa, which can therefore be termed “laughter” across all five species. Results are consistent with the claims of phylogenetic continuity of emotional expressions. Together with observations made on the use of laughter in great apes and humans, findings of this study further indicate that there were two main periods of selection-driven evolutionary change in laughter within the Hominidae, to a smaller degree, among the great apes and, most distinctively, after the separation of hominins from the last common ancestor with chimpanzees and bonobos.

Capuchin monkeys ( Cebus apella ) use positive, but not negative, auditory cues to infer food location

Nonhuman primates appear to capitalize more effectively on visual cues than corresponding auditory versions. For example, studies of inferential reasoning have shown that monkeys and apes readily respond to seeing that food is present (“positive” cuing) or absent (“negative” cuing). Performance is markedly less effective with auditory cues, with many subjects failing to use this input. Extending recent work, we tested eight captive tufted capuchins (Cebus apella) in locating food using positive and negative cues in visual and auditory domains. The monkeys chose between two opaque cups to receive food contained in one of them. Cup contents were either shown or shaken, providing location cues from both cups, positive cues only from the baited cup, or negative cues from the empty cup. As in previous work, subjects readily used both positive and negative visual cues to secure reward. However, auditory outcomes were both similar to and different from those of earlier studies. Specifically, all subjects came to exploit positive auditory cues, but none responded to negative versions. The animals were also clearly different in visual versus auditory performance. Results indicate that a significant proportion of capuchins may be able to use positive auditory cues, with experience and learning likely playing a critical role. These findings raise the possibility that experience may be significant in visually based performance in this task as well, and highlight that coming to grips with evident differences between visual versus auditory processing may be important for understanding primate cognition more generally.

Vocalizations as tools for influencing the affect and behavior of others

Abstract Emotional systems are central to the behavior of many animals, either as part of the impetus to behavioral action, or as an important accompaniment to it. In this chapter, we consider the role of the emotions, or affective systems construed more broadly, in vocal communication. We focus not on the role that affective systems might play in motivating calling, nor on the related issue of how vocal signals might then serve as indicators of caller emotional state. Instead, we focus on how vocal signals influence the affective systems of listeners in ways that steer and impel behavioral responding in them. We emphasize: (1) that affective systems can be important functional targets of signaling in animals, including humans; (2) that they include phylogenetically widespread neuro-affective sensitivity to some sounds; (3) that such sensitivity can impel responses from listeners in quite direct fashion, or combine with general processes of conditioning and learning to steer listener behavior more indirectly; and (4) that the effect that signals have on core affective processes and behavior in listeners can also serve to scaffold more complex communicative processes and outcomes.

A Serial Reaction Time (SRT) task with symmetrical joystick responding for nonhuman primates

The serial reaction time (SRT) task is a simple procedure in which participants produce differentiated responses to each of a series of stimuli presented at varying locations. Learning about stimulus order is revealed through decreased latencies for structured versus randomized sequences. Although widely used with humans and well suited to nonhumans, this paradigm is little used in comparative research. In the present article, we describe an SRT procedure that uses colored circles as stimuli, a circular layout of locations, and symmetrical joystick deflections as responses. In two experiments, we showed that four rhesus macaques (Macaca mulatta) learned to track sequences up to eight items long, with three animals showing faster responding to repeating sequences than to randomized versions. After extended training, these participants also showed evidence of faster responding at all positions within repeating sequences. This method minimizes response effort, equates effort and travel distance across stimulus locations, and is applicable to any joystick-capable species.