Humans read emotional arousal in monkey vocalizations: evidence for evolutionary continuities in communication

Abstract

Humans and other mammalian species communicate emotions in ways that reflect evolutionary conservation and continuity, an observation first made by Darwin. One approach to testing this hypothesis has been to assess the capacity to perceive the emotional content of the vocalizations of other species. Using a binary forced choice task, we tested perception of the emotional intensity represented in coos and screams of infant and juvenile female rhesus macaques (Macaca mulatta) by 113 human listeners without, and 12 listeners with, experience (as researchers or care technicians) with this species. Each stimulus pair contained one high- and one low-arousal vocalization, as measured at the time of recording by stress hormone levels for coos and the degree of intensity of aggression for screams. For coos as well as screams, both inexperienced and experienced participants accurately identified the high-arousal vocalization at significantly above-chance rates. Experience was associated with significantly greater accuracy with scream stimuli but not coo stimuli, and with a tendency to indicate screams as reflecting greater emotional intensity than coos. Neither measures of empathy, human emotion recognition, nor attitudes toward animal welfare showed any relationship with responses. Participants were sensitive to the fundamental frequency, noisiness, and duration of vocalizations; some of these tendencies likely facilitated accurate perceptions, perhaps due to evolutionary homologies in the physiology of arousal and vocal production between humans and macaques. Overall, our findings support a view of evolutionary continuity in emotional vocal communication. We discuss hypotheses about how distinctive dimensions of human nonverbal communication, like the expansion of scream usage across a range of contexts, might influence perceptions of other species’ vocalizations.

Within the sound of trouble: Do humans use pitch to correctly assess emotional arousal across species?

“…The adult human subjects were played samples from 10 calls per species sourced. Again, the selection of call types used was also based on previous studies to allow comparison (Schötz et al, 2017;Schwartz & Gouzoules, 2022). Notably, the calls came from an array of contexts associated with various emotional states.…”

Pitch affects human (Homo sapiens) perception of emotional arousal from diverse animal calls.

“…Various factors have been examined to address this, including raters’ demographics, empathy, and familiarity with the vocalizer species, as well as phylogenetic distance between humans and the vocalizer species (Congdon et al, 2019; Filippi et al, 2017; Fritz et al, 2018; Greenall et al, 2022; Maruščáková et al, 2015; Nicastro & Owren, 2003; Parsons et al, 2019; Schwartz & Gouzoules, 2022; Scheumann et al, 2014). While the evidence for a role of these variables is mixed, judgments of emotional arousal are more consistently predicted by the acoustic structure of sounds, especially the fundamental frequency (F0) (Congdon et al, 2019; Filippi et al, 2017; Greenall et al, 2022; Kamiloǧlu et al, 2020; Kelly et al, 2017; Maruščáková et al, 2015; Schwartz & Gouzoules, 2022). The F0 of a vocalization is determined by the oscillation rate of the vocal folds, and is generally perceived by humans as the pitch of a sound.…”

“…While past research indicates a robust association between the F0 of a sound and human perception of vocalizer arousal, it is difficult to rule out a possible confounding effect of other acoustic features. For example, in a previous study, the F0 and noisiness of macaque screams were correlated, making it difficult to disentangle the effects of these parameters on listener perceptions (Schwartz & Gouzoules, 2022). Therefore, the present study experimentally examined the role of pitch in human perceptions of emotional arousal from calls of a diverse range of taxa.…”

“…To test the ubiquity of the pitch rule in human perception, stimuli included sounds produced by diverse taxa representing an array of phylogenetic distance from humans, including a primate (rhesus macaques, Macaca mulatta ), a familiar and unfamiliar carnivore (domestic cats, Felis domesticus , and northern fur seals, Callorhinus ursinus ), an avian (common ravens, Corvus corax ), an anuran (hourglass treefrogs, Dendropsophus ebraccatus ), and an invertebrate (prairie mole crickets, Gryllotalpa major ). Humans have demonstrated above-chance accuracy, and an apparent role of the F0, in perceptions of arousal from the vocalizations of rhesus macaques (Schwartz & Gouzoules, 2022), domestic cats (Nicastro & Owren, 2003), common ravens, and hourglass tree frogs (Congdon et al, 2019; Filippi et al, 2017). Furthermore, rhesus macaques, seals, and common ravens have been shown to exhibit the common association between vocalizer arousal and vocal F0 (Collins et al, 2011; Schwartz et al, 2022; Szipl et al, 2017).…”

“…In addition to vocalizer species, vocal F0 can be influenced by natural selection shaping signal structure, as well as vocalizer sex, body size, and age (Taylor & Reby, 2010), potentially reducing the accuracy of judgments made using the pitch rule. To speculate, this could contribute to the modest (though significantly above-chance) accuracy shown in several studies of heterospecific emotion perception, often 50%–60% on binary forced-choice tasks (Filippi et al, 2017; Greenall et al, 2022; Schwartz & Gouzoules, 2022). These considerations raise the question: how widely do humans apply the pitch rule, and to what extent does use of this heuristic depend on phylogeny and other factors?…”