Impoverished encoding of speaker identity in spontaneous laughter

Our ability to perceive person identity from other human voices has been described as prodigious. However, emerging evidence points to limitations in this skill. In this study, we investigated the recent and striking finding that identity perception from spontaneous laughter - a frequently occurring and important social signal in human vocal communication - is significantly impaired relative to identity perception from volitional (acted) laughter. We report the findings of an experiment in which listeners made speaker discrimination judgements from pairs of volitional and spontaneous laughter samples. The experimental design employed a range of different conditions, designed to disentangle the effects of laughter production mode versus perceptual features on the extraction of speaker identity. We find that the major driving factor of reduced accuracy for spontaneous laughter is not its perceived emotional quality but rather its distinct production mode, which is phylogenetically homologous with other primates. These results suggest that identity-related information is less successfully encoded in spontaneously produced (laughter) vocalisations. We therefore propose that claims for a limitless human capacity to process identity-related information from voices may be linked to the evolution of volitional vocal control and the emergence of articulate speech.     

The ontogeny of human laughter

Human adult laughter is characterized by vocal bursts produced predominantly during exhalation, yet apes laugh while exhaling and inhaling. The current study investigated our hypothesis that laughter of human infants changes from laughter similar to that of apes to increasingly resemble that of human adults over early development. We further hypothesized that the more laughter is produced on the exhale, the more positively it is perceived. To test these predictions, novice (n = 102) and expert (phonetician, n = 15) listeners judged the extent to which human infant laughter (n = 44) was produced during inhalation or exhalation, and the extent to which they found the laughs pleasant and contagious. Support was found for both hypotheses, which were further confirmed in two pre-registered replication studies. Likely through social learning and the anatomical development of the vocal production system, infants'' initial ape-like laughter transforms into laughter similar to that of adult humans over the course of ontogeny.     

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.     

Primate phonation: Anterior cingulate lesion effects on response rate and acoustical structure

Four juvenile rhesus monkeys (Macaca mulatta) that were conditioned to emit a discriminative vocal response underwent unilateral and bilateral lesions of anterior cingulate gyrus in stepwise sequence. Pre- and post-lesion measures of vocal response rate and acoustical features (call duration, amplitude, and fundamental frequency) were obtained for the conditioned task and for vocalization in the home colony (spontaneous vocalization). Unilateral lesions produced little consistent change in spontaneous “coo” vocalization rate and call duration. Conditioned vocalization of the monkeys exhibited no significant change in rate at this stage, although call duration was reduced significantly. Bilateral lesions produced no further modifications in acoustic properties of spontaneous calls, while the vocal rate decreased slightly. Conditioned calls were not significantly altered in acoustic features at this stage, although the discriminative vocalization rate was significantly decreased for all monkeys. The results indicate limited control over vocal motor systems by anterior cingulate cortex, while suggesting that this region participates in initiation of voluntary phonation.     

Cross-Taxa Similarities in Affect-Induced Changes of Vocal Behavior and Voice in Arboreal Monkeys

Measuring the affective state of an individual across species with comparable non-invasive methods is a current challenge in animal communication research. This study aims to explore to which extent affect intensity is conveyed in the vocal behaviours of three nonhuman primate species (Campbell''s monkeys, De Brazza''s monkeys, red-capped mangabeys), which vary in body size, ecological niche and social system. Similarly in the three species, we experimentally induced a change in captive social groups'' affect by locking all group members together in their outside enclosure. The two experimental conditions which varied in affect intensity consisted in imposing a pre-reunion 90 mn-separation by splitting up the respective group into two subgroups (High affect condition) or not (Low affect condition). We measured call rates as well as voice features at the time of reunion in both conditions. The three studied species reacted in a very similar way. Across species, call rates changed significantly between the behaviourally defined states. Furthermore, contact call duration and, to some extent, voice pitch increased. Our results suggest, for the first time in arboreal Old World monkeys, that affect intensity is conveyed reliably in vocal behaviour and specific acoustic characteristics of voice, irrespective of body size and ecological niche differences between species. Cross-taxa similarities in acoustic cues of affect intensity point to phylogenetic constraints and inheritance from a common ancestor, whereas variations in vocal behaviour and affect intensity-related acoustic cues between species may be an adaptation to specific social requirements and depend on social systems. Our findings as well as a comparison with published works on acoustic communication in other vertebrate groups support the hypothesis that affect intensity in human voice originates from precursors already found deep inside the vertebrate phylogeny.     

High-Pitched Notes during Vocal Contests Signal Genetic Diversity in Ocellated Antbirds

Animals use honest signals to assess the quality of competitors during aggressive interactions. Current theory predicts that honest signals should be costly to produce and thus reveal some aspects of the phenotypic or genetic quality of the sender. In songbirds, research indicates that biomechanical constraints make the production of some acoustic features costly. Furthermore, recent studies have found that vocal features are related to genetic diversity. We linked these two lines of research by evaluating if constrained acoustic features reveal male genetic diversity during aggressive interactions in ocellated antbirds (Phaenostictus mcleannani). We recorded the aggressive vocalizations of radiotagged males at La Selva Biological Station in Costa Rica, and found significant variation in the highest frequency produced among individuals. Moreover, we detected a negative relationship between the frequency of the highest pitched note and vocalization duration, suggesting that high pitched notes might constrain the duration of vocalizations through biomechanical and/or energetic limitations. When we experimentally exposed wild radiotagged males to simulated acoustic challenges, the birds increased the pitch of their vocalization. We also found that individuals with higher genetic diversity (as measured by zygosity across 9 microsatellite loci) produced notes of higher pitch during aggressive interactions. Overall, our results suggest that the ability to produce high pitched notes is an honest indicator of male genetic diversity in male-male aggressive interactions.     

Perceptual salience of acoustic differences between conspecific and allospecific vocalizations in African collared-doves

In speciation events, species-distinct vocal signals can diverge acoustically in many ways. Signal receivers have to be able to distinguish conspecific from allospecific vocalizations, and the perceptual salience of acoustic features is therefore expected to be an important factor in the evolution of such vocalizations. We tested how dissimilar the species-identifying perch-coos of 12 closely related turtle-dove species (genus Streptopelia) are, as perceived by one of its members, S. roseogrisea. With operant, psychoacoustic methods we trained six doves to respond only to their conspecific coo. Responses to the perch-coos of the 12 other dove species were used as a measure of their perceptual similarity to conspecific perch-coos. Turtle-doves differentiated between the allospecific coos: some were perceived as more similar to their own species' coo than others. With multiple regression analysis we identified three acoustic features that correlated with these differences in perceptual similarity: coo duration, minimum frequency and Wiener entropy. In contrast to findings in other bird species, duration was by far the most important feature in the discrimination between conspecific and allospecific vocalizations for S. roseogrisea. The results suggest that this is due not only to the coos of the various species differing in duration but also to a comparatively high perceptibility of the differences in duration. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Vocal divergence between two disjunct populations of Giant Antshrike (Batara cinerea) is related to environmental conditions

Variation in the avian vocal signals emitted may have a significant impact on species evolution. Vocal divergence in suboscine species like Giant Antshrike (Batara cinerea) may be associated with selective adaptation, since learning has little influence on vocal development and variation in acoustic structure cannot be attributed to learning deviation. Consequently, tracheophone suboscine species are ideal subjects to explore vocal variation, since cultural evolution does not seem to influence vocal variation in this group. Environmental conditions may determine the selection of vocal features because acoustic transmission could be attenuated under certain conditions of temperature, humidity and vegetation cover. Here, we examined vocalizations of Giant Antshrike and assessed possible acoustic variations between two disjunct groups (Andean and Atlantic), correlating the differences to the environmental structure. Univariate and multivariate analysis show temporal and spectral differences between both groups. Andean individuals produce vocalizations with longer duration, faster trill rates, shorter syllable duration and higher frequencies. Environmental features are different between the two populations, and they are correlated to the acoustic structure of vocalizations. Temporal variations arise directly from climatic influence, while spectral divergence could be a secondary effect of morphological adaptation to habitat structure.     

Pygmy Marmosets Modify Call Structure When Paired

Pygmy marmosets ( Cebuella pygmaea ) modified the structure of their trill vocalizations in response to pairing with a new mate. Prior to pairing, individual marmosets displayed different acoustic parameters of trill structure. Within the first 6 wk after pairing, three of four pairs produced trills that were more homogeneous between mates. Pairs that had the greatest individual difference in trill structure prior to pairing displayed convergence on a greater number of parameters than pairs having fewer differences in prepairing trill structure. The vocal structure following pairing remained highly stable in the two pairs that could be recorded 3 yr after initial pairing. Changes in trill structure that occurred within the first 6 wk after pairing were greater than spontaneous changes that occurred during baseline control recording sessions on the same animals. These results suggest that nonhuman primates show subtle modification of vocal structure, especially in response to changes in social environment. Similar findings have been reported in birds and other mammals.     

Why Do People Laugh during Dog–Human Play Interactions?

Given that human laughter has been posited to signal playfulness to dogs, nonserious social incongruity, and positive affect, laughter should occur during incongruous contexts in an affectively positive, nonserious social activity such as dog–human play. A total of 116 laughs in relation to dogs were discerned on videotapes of 46 dog–human play interactions in the US, 23 with familiar and 23 with unfamiliar pairs. Laughter occurred during 61% of interactions, and always expressed positive affect. Contexts in which laughter occurred (in decreasing frequency) were failure of the dog during play, or to play at all or as the person wanted; exaggerated or unexpected engagement by the dog; excretion; unexpected success by the dog in obtaining an object; and, once, threat from the dog. Laughter never induced play, and usually occurred when a dog was not playing. Women laughed more than men, especially for a male audience when playing with their own dog. In all contexts, participants experienced incongruous events; contexts were nonserious, except for the dog's threat, where laughter signaled friendliness. These data are largely consistent with laughter signaling positive affect and awareness of (usually nonserious) social incongruity, and inconsistent with laughter signaling playfulness to dogs.     

Perception of male caller identity in Koalas (Phascolarctos cinereus): acoustic analysis and playback experiments

The ability to signal individual identity using vocal signals and distinguish between conspecifics based on vocal cues is important in several mammal species. Furthermore, it can be important for receivers to differentiate between callers in reproductive contexts. In this study, we used acoustic analyses to determine whether male koala bellows are individually distinctive and to investigate the relative importance of different acoustic features for coding individuality. We then used a habituation-discrimination paradigm to investigate whether koalas discriminate between the bellow vocalisations of different male callers. Our results show that male koala bellows are highly individualized, and indicate that cues related to vocal tract filtering contribute the most to vocal identity. In addition, we found that male and female koalas habituated to the bellows of a specific male showed a significant dishabituation when they were presented with bellows from a novel male. The significant reduction in behavioural response to a final rehabituation playback shows this was not a chance rebound in response levels. Our findings indicate that male koala bellows are highly individually distinctive and that the identity of male callers is functionally relevant to male and female koalas during the breeding season. We go on to discuss the biological relevance of signalling identity in this species' sexual communication and the potential practical implications of our findings for acoustic monitoring of male population levels.     

Vocal Production by a Language-Competent Pan paniscus

Human spoken language and nonhuman primate vocalization systems have traditionally been regarded as qualitatively different from one another with respect to their semanticity and the way in which individuals acquire and utilize these signals. However, recent studies of the vocal behaviors of both captive and free-ranging monkeys and apes suggest that this dichotomy may not be unequivocal. We examined the vocalizations produced by a linguistically-competent adult male bonobo (Pan paniscus) named Kanzi. We analyzed his vocalizations during communicative interactions with humans in order to determine whether they vary systematically according to the semantic context in which they are produced. We determined semantic contexts based upon a vocalization's co-occurrence with predefined behavioral correlates. Spectrographic and statistical analyses revealed that acoustic structure is similar among the vocalizations that occurred within a specific semantic context and structural differences are evident between the vocalizations produced in different contexts. The results provide evidence that, during communicative interactions with humans, Kanzi modulates his vocal output on both the temporal and spectral levels.     

Vocal individual discrimination in Japanese monkeys

The present study determines which features of the coo call are used by Japanese monkeys Macaca fuscata for vocal individual discrimination. First, two female Japanese monkeys were trained to discriminate conspecific individuals vocally, using an operant conditioning. Using as stimuli three unknown individuals with 30 calls per individual, the two monkeys succeeded in discriminating new call exemplars from the three stimulus individuals. A discriminant analysis performed on calls used as stimuli indicated that start frequency of the fundamental and call duration were variables that can differentiate individuals efficiently. Then, playbacks of acoustically modified signals were used to indicate which vocal features are used by monkeys for the individual discrimination. Stimuli signals containing modified pitch or duration, or filtered so as to keep only the fundamental component, were tested. Results indicated that Japanese monkeys use multiple acoustical cues to perform vocal individual discrimination, including at least pitch, call duration, and harmonics. However, harmonics seem to be less important for discrimination than pitch and call duration.     

Noise-Induced Frequency Modifications of Tamarin Vocalizations: Implications for Noise Compensation in Nonhuman Primates

Previous research suggests that nonhuman primates have limited flexibility in the frequency content of their vocalizations, particularly when compared to human speech. Consistent with this notion, several nonhuman primate species have demonstrated noise-induced changes in call amplitude and duration, with no evidence of changes to spectral content. This experiment used broad- and narrow-band noise playbacks to investigate the vocal control of two call types produced by cotton-top tamarins (Saguinus Oedipus). In ‘combination long calls’ (CLCs), peak fundamental frequency and the distribution of energy between low and high frequency harmonics (spectral tilt) changed in response to increased noise amplitude and bandwidth. In chirps, peak and maximum components of the fundamental frequency increased with increasing noise level, with no changes to spectral tilt. Other modifications included the Lombard effect and increases in chirp duration. These results provide the first evidence for noise-induced frequency changes in nonhuman primate vocalizations and suggest that future investigations of vocal plasticity in primates should include spectral parameters.     

Vocal repertoire of cooperatively breeding Smooth‐billed Anis

Calls are functionally diverse signals that mediate behavior in a wide variety of contexts in both passerines and non‐passerines. However, the call‐based acoustic communication systems of non‐passerines have received less attention from investigators than those of passerines. We examined the vocal repertoire of Smooth‐billed Anis (Crotophaga ani), cooperatively breeding cuckoos that live in groups with multiple breeding pairs. We recorded calls from 22 groups over two breeding seasons at the Cabo Rojo National Wildlife Refuge in Puerto Rico. We identified 11 call types and one group vocalization, and used an automated sound measurement program to quantify their acoustic features. Discriminant function analysis (DFA) correctly classified 74.2% of calls based on these features. The vocal repertoire of Smooth‐billed Anis is larger than that reported for the three other species in the subfamily Crotophaginae. Smooth‐billed Anis have at least two alarm calls, two nest‐specific calls, and one nest defense call. We also identified one possible signal of aggressive intent, one possible appeasement signal, and two calls that may communicate identity. The relatively large vocal repertoire of Smooth‐billed Anis and association of distinct call types with different functions and contexts supports the main prediction of the social complexity hypothesis, i.e., species with more complex social systems will have more complex communication systems.     

Trade-offs in the production of animal vocal sequences: insights from the structure of wild chimpanzee pant hoots

Background

Vocal sequences - utterances consisting of calls produced in close succession - are common phenomena in animal communication. While many studies have explored the adaptive benefits of producing such sequences, very little is known about how the costs and constraints involved in their production affect their form. Here, we investigated this issue in the chimpanzee (Pan troglodytes schweinfurthii) pant hoot, a long and structurally complex vocal sequence comprising four acoustically distinct phases – introduction, build-up, climax and let-down.

Results

We found that in each of these phases, and for the sequence as a whole, there was a negative relationship between the number of calls produced and their average duration. There was also a negative relationship between the total duration of some adjacent phases. Significant relationships between the fundamental frequency of calls and their number or duration were found for some phases of the sequence, but the direction of these relationships differed between particular phases.

Conclusions

These results indicate that there are trade-offs in terms of signal duration at two levels in pant-hoot production: between call number and duration, and between the relative durations of successive phases. These trade-offs are likely to reflect biomechanical constraints on vocal sequence production. Phase-specific trade-offs also appear to occur between fundamental frequency and call number or duration, potentially reflecting that different phases of the sequence are associated with distinct types of information, linked in different ways to call pitch. Overall, this study highlights the important role of costs and constraints in shaping the temporal and acoustic structure of animal vocal sequences.

     

The evolution of nonhuman primate loud calls: Acoustic adaptation for long-distance transmission

Many nonhuman primates produce species-typical loud calls used to communicate between and within groups over long distances. Given their observed spacing functions, primate loud calls are likely to show acoustic adaptations to increase their propagation over distance. Here we evaluate the hypothesis that primates emit loud calls at relatively low sound frequencies to minimize their attenuation. We tested this hypothesis within and between species. First, we compared the frequencies of loud calls produced by each species with those of other calls from their vocal repertoires. Second, we investigated the relationship between loud call frequency and home range size across a sample of primate species. Comparisons indicated that primates produce loud calls at lower frequencies than other calls within their vocal repertoires. In addition, a significant negative relationship exists between loud call frequency and home range size among species. The relationship between call frequency and range size holds after controlling for the potentially confounding effects of body size and phylogeny. These results are consistent with the hypothesis that nonhuman primates produce loud calls at relatively low frequencies to facilitate their transmission over long distances.     

How Listeners Weight Acoustic Cues to Intonational Phrase Boundaries

The presence of an intonational phrase boundary is often marked by three major acoustic cues: pause, final lengthening, and pitch reset. The present study investigates how these three acoustic cues are weighted in the perception of intonational phrase boundaries in two experiments. Sentences that contained two intonational phrases with a critical boundary between them were used as the experimental stimuli. The roles of the three acoustic cues at the critical boundary were manipulated in five conditions. The first condition featured none of the acoustic cues. The following three conditions featured only one cue each: pause, final lengthening, and pitch reset, respectively. The fifth condition featured both pause duration and pre-final lengthening. A baseline condition was also included in which all three acoustic cues were preserved intact. Listeners were asked to detect the presence of the critical boundaries in Experiment 1 and judge the strength of the critical boundaries in Experiment 2. The results of both experiments showed that listeners used all three acoustic cues in the perception of prosodic boundaries. More importantly, these acoustic cues were weighted differently across the two experiments: Pause was a more powerful perceptual cue than both final lengthening and pitch reset, with the latter two cues perceptually equivalent; the effect of pause and the effects of the other two acoustic cues were not additive. These results suggest that the weighting of acoustic cues contributes significantly to the perceptual differences of intonational phrase boundary.