Puppy whines mediate maternal behavior in domestic dogs.

In mammals, offspring vocalizations typically encode information about identity and body condition, allowing parents to limit alloparenting and adjust care. But how do these vocalizations mediate parental behavior in species faced with the problem of rearing not one, but multiple offspring, such as domestic dogs? Comprehensive acoustic analyses of 4,400 whines recorded from 220 Beagle puppies in 40 litters revealed litter and individual (within litter) differences in call acoustic structure. By then playing resynthesized whines to mothers, we showed that they provided more care to their litters, and were more likely to carry the emitting loudspeaker to the nest, in response to whine variants derived from their own puppies than from strangers. Importantly, care provisioning was attenuated by experimentally moving the fundamental frequency (fo, perceived as pitch) of their own puppies' whines outside their litter-specific range. Within most litters, we found a negative relationship between puppies' whine fo and body weight. Consistent with this, playbacks showed that maternal care was stronger in response to high-pitched whine variants simulating relatively small offspring within their own litter's range compared to lower-pitched variants simulating larger offspring. We thus show that maternal care in a litter-rearing species relies on a dual assessment of offspring identity and condition, largely based on level-specific inter- and intra-litter variation in offspring call fo. This dual encoding system highlights how, even in a long-domesticated species, vocalizations reflect selective pressures to meet species-specific needs. Comparative work should now investigate whether similar communication systems have convergently evolved in other litter-rearing species.

A practical guide to calculating vocal tract length and scale-invariant formant patterns.

Formants (vocal tract resonances) are increasingly analyzed not only by phoneticians in speech but also by behavioral scientists studying diverse phenomena such as acoustic size exaggeration and articulatory abilities of non-human animals. This often involves estimating vocal tract length acoustically and producing scale-invariant representations of formant patterns. We present a theoretical framework and practical tools for carrying out this work, including open-source software solutions included in R packages soundgen and phonTools. Automatic formant measurement with linear predictive coding is error-prone, but formant_app provides an integrated environment for formant annotation and correction with visual and auditory feedback. Once measured, formants can be normalized using a single recording (intrinsic methods) or multiple recordings from the same individual (extrinsic methods). Intrinsic speaker normalization can be as simple as taking formant ratios and calculating the geometric mean as a measure of overall scale. The regression method implemented in the function estimateVTL calculates the apparent vocal tract length assuming a single-tube model, while its residuals provide a scale-invariant vowel space based on how far each formant deviates from equal spacing (the schwa function). Extrinsic speaker normalization provides more accurate estimates of speaker- and vowel-specific scale factors by pooling information across recordings with simple averaging or mixed models, which we illustrate with example datasets and R code. The take-home messages are to record several calls or vowels per individual, measure at least three or four formants, check formant measurements manually, treat uncertain values as missing, and use the statistical tools best suited to each modeling context.

Vocal tract shape variation contributes to individual vocal identity in African penguins.

Variation in formant frequencies has been shown to affect social interactions and sexual competition in a range of avian species. Yet, the anatomical bases of this variation are poorly understood. Here, we investigated the morphological correlates of formants production in the vocal apparatus of African penguins. We modelled the geometry of the supra-syringeal vocal tract of 20 specimens to generate a population of virtual vocal tracts with varying dimensions. We then estimated the acoustic response of these virtual vocal tracts and extracted the centre frequency of the first four predicted formants. We demonstrate that: (i) variation in length and cross-sectional area of vocal tracts strongly affects the formant pattern, (ii) the tracheal region determines most of this variation, and (iii) the skeletal size of penguins does not correlate with the trachea length and consequently has relatively little effect on formants. We conclude that in African penguins, while the variation in vocal tract geometry generates variation in resonant frequencies supporting the discrimination of conspecifics, such variation does not provide information on the emitter's body size. Overall, our findings advance our understanding of the role of formant frequencies in bird vocal communication.

Grey wolves (Canis lupus) discriminate between familiar and unfamiliar human voices.

The ability to discriminate between different individuals based on identity cues, which is important to support the social behaviour of many animal species, has mostly been investigated in conspecific contexts. A rare example of individual heterospecific discrimination is found in domestic dogs, who are capable of recognising their owners' voices. Here, we test whether grey wolves, the nearest wild relative of dogs, also have the ability to distinguish familiar human voices, which would indicate that dogs' ability is not a consequence of domestication. Using the habituation-dishabituation paradigm, we presented captive wolves with playback recordings of their keepers' and strangers' voices producing either familiar or unfamiliar phrases. The duration of their response was significantly longer when presented with keepers' voices than with strangers' voices, demonstrating that wolves discriminated between familiar and unfamiliar speakers. This suggests that dogs' ability to discriminate between human voices was probably present in their common ancestor and may support the idea that this is a general ability of vertebrates to recognise heterospecific individuals. Our study also provides further evidence for familiar voice discrimination in a wild animal in captivity, indicating that this ability may be widespread across vertebrate species.

Nonlinear vocal phenomena affect human perceptions of distress, size and dominance in puppy whines.

While nonlinear phenomena (NLP) are widely reported in animal vocalizations, often causing perceptual harshness and roughness, their communicative function remains debated. Several hypotheses have been put forward: attention-grabbing, communication of distress, exaggeration of body size and dominance. Here, we use state-of-the-art sound synthesis to investigate how NLP affect the perception of puppy whines by human listeners. Listeners assessed the distress, size or dominance conveyed by synthetic puppy whines with manipulated NLP, including frequency jumps and varying proportions of subharmonics, sidebands and deterministic chaos. We found that the presence of chaos increased the puppy's perceived level of distress and that this effect held across a range of representative fundamental frequency (fo) levels. Adding sidebands and subharmonics also increased perceived distress among listeners who have extensive caregiving experience with pre-weaned puppies (e.g. breeders, veterinarians). Finally, we found that whines with added chaos, subharmonics or sidebands were associated with larger and more dominant puppies, although these biases were attenuated in experienced caregivers. Together, our results show that nonlinear phenomena in puppy whines can convey rich information to human listeners and therefore may be crucial for offspring survival during breeding of a domesticated species.

Harsh is large: nonlinear vocal phenomena lower voice pitch and exaggerate body size.

A lion's roar, a dog's bark, an angry yell in a pub brawl: what do these vocalizations have in common? They all sound harsh due to nonlinear vocal phenomena (NLP)-deviations from regular voice production, hypothesized to lower perceived voice pitch and thereby exaggerate the apparent body size of the vocalizer. To test this yet uncorroborated hypothesis, we synthesized human nonverbal vocalizations, such as roars, groans and screams, with and without NLP (amplitude modulation, subharmonics and chaos). We then measured their effects on nearly 700 listeners' perceptions of three psychoacoustic (pitch, timbre, roughness) and three ecological (body size, formidability, aggression) characteristics. In an explicit rating task, all NLP lowered perceived voice pitch, increased voice darkness and roughness, and caused vocalizers to sound larger, more formidable and more aggressive. Key results were replicated in an implicit associations test, suggesting that the 'harsh is large' bias will arise in ecologically relevant confrontational contexts that involve a rapid, and largely implicit, evaluation of the opponent's size. In sum, nonlinearities in human vocalizations can flexibly communicate both formidability and intention to attack, suggesting they are not a mere byproduct of loud vocalizing, but rather an informative acoustic signal well suited for intimidating potential opponents.

Roars, groans and moans: Anatomical correlates of vocal diversity in polygynous deer.

Eurasian deer are characterized by the extraordinary diversity of their vocal repertoires. Male sexual calls range from roars with relatively low fundamental frequency (hereafter fo ) in red deer Cervus elaphus, to moans with extremely high fo in sika deer Cervus nippon, and almost infrasonic groans with exceptionally low fo in fallow deer Dama dama. Moreover, while both red and fallow males are capable of lowering their formant frequencies during their calls, sika males appear to lack this ability. Female contact calls are also characterized by relatively less pronounced, yet strong interspecific differences. The aim of this study is to examine the anatomical bases of these inter-specific and inter-sexual differences by identifying if the acoustic variation is reflected in corresponding anatomical variation. To do this, we investigated the vocal anatomy of male and female specimens of each of these three species. Across species and sexes, we find that the observed acoustic variability is indeed related to expected corresponding anatomical differences, based on the source-filter theory of vocal production. At the source level, low fo is associated with larger vocal folds, whereas high fo is associated with smaller vocal folds: sika deer have the smallest vocal folds and male fallow deer the largest. Red and sika deer vocal folds do not appear to be sexually dimorphic, while fallow deer exhibit strong sexual dimorphism (after correcting for body size differences). At the filter level, the variability in formants is related to the configuration of the vocal tract: in fallow and red deer, both sexes have evolved a permanently descended larynx (with a resting position of the larynx much lower in males than in females). Both sexes also have the potential for momentary, call-synchronous vocal tract elongation, again more pronounced in males than in females. In contrast, the resting position of the larynx is high in both sexes of sika deer and the potential for further active vocal tract elongation is virtually absent in both sexes. Anatomical evidence suggests an evolutionary reversal in larynx position within sika deer, that is, a secondary larynx ascent. Together, our observations confirm that the observed diversity of vocal behaviour in polygynous deer is supported by strong anatomical differences, highlighting the importance of anatomical specializations in shaping mammalian vocal repertoires. Sexual selection is discussed as a potential evolutionary driver of the observed vocal diversity and sexual dimorphisms.

Using a new video rating tool to crowd-source analysis of behavioural reaction to stimuli.

Quantifying the intensity of animals' reaction to stimuli is notoriously difficult as classic unidimensional measures of responses such as latency or duration of looking can fail to capture the overall strength of behavioural responses. More holistic rating can be useful but have the inherent risks of subjective bias and lack of repeatability. Here, we explored whether crowdsourcing could be used to efficiently and reliably overcome these potential flaws. A total of 396 participants watched online videos of dogs reacting to auditory stimuli and provided 23,248 ratings of the strength of the dogs' responses from zero (default) to 100 using an online survey form. We found that raters achieved very high inter-rater reliability across multiple datasets (although their responses were affected by their sex, age, and attitude towards animals) and that as few as 10 raters could be used to achieve a reliable result. A linear mixed model applied to PCA components of behaviours discovered that the dogs' facial expressions and head orientation influenced the strength of behaviour ratings the most. Further linear mixed models showed that that strength of behaviour ratings was moderately correlated to the duration of dogs' reactions but not to dogs' reaction latency (from the stimulus onset). This suggests that observers' ratings captured consistent dimensions of animals' responses that are not fully represented by more classic unidimensional metrics. Finally, we report that overall participants strongly enjoyed the experience. Thus, we suggest that using crowdsourcing can offer a useful, repeatable tool to assess behavioural intensity in experimental or observational studies where unidimensional coding may miss nuance, or where coding multiple dimensions may be too time-consuming.

Baby cry recognition is independent of motherhood but improved by experience and exposure.

Neurobiological changes affecting new mothers are known to support the development of the mother-infant relationship (the 'maternal brain'). However, which aspects of parenting are actually mother-specific and which rely on general cognitive abilities remains debated. For example, refuting earlier findings, a recent study demonstrated that fathers identify their own baby from their cries just as well as mothers. Here we show that this performance is independent not only of sex, but also of parenthood status. We found that mothers' ability to recognize their newborn from their cries increased rapidly within few days postpartum, with highly multiparous mothers performing better. However, both male and female non-parents could similarly recognize an assigned baby, even after a very short exposure. As in mothers, both the initial amount of experimental exposure to the baby's cries (learning opportunity) and prior experience of caring for infants (auditory expertise) affected participants' performance. We thus suggest that, rather than being female-specific or motherhood-dependent, the ability to recognize a baby from their cries derives from general auditory and learning skills. By being available to non-parents of both sexes, it may contribute to the caregiving flexibility required for efficient cooperative breeding in humans.

"This Is What a Mechanic Sounds Like": Children's Vocal Control Reveals Implicit Occupational Stereotypes.

In this study, we explored the use of variation in sex-related cues of the voice to investigate implicit occupational stereotyping in children. Eighty-two children between the ages of 5 and 10 years took part in an imitation task in which they were provided with descriptions of nine occupations (three traditionally male, three traditionally female, and three gender-neutral professions) and asked to give voices to them (e.g., "How would a mechanic say . . . ?"). Overall, children adapted their voices to conform to gender-stereotyped expectations by masculinizing (lowering voice pitch and resonance) and feminizing (raising voice pitch and resonance) their voices for the traditionally male and female occupations, respectively. The magnitude of these shifts increased with age, particularly in boys, and was not mediated by children's explicit stereotyping of the same occupations. We conclude by proposing a simple tool based on voice pitch for assessing levels of implicit occupational-gender stereotyping in children.

Physiological and perceptual correlates of masculinity in children's voices.

Low frequency components (i.e. a low pitch (F0) and low formant spacing (ΔF)) signal high salivary testosterone and height in adult male voices and are associated with high masculinity attributions by unfamiliar listeners (in both men and women). However, the relation between the physiological, acoustic and perceptual dimensions of speakers' masculinity prior to puberty remains unknown. In this study, 110 pre-pubertal children (58 girls), aged 3 to 10, were recorded as they described a cartoon picture. 315 adults (182 women) rated children's perceived masculinity from the voice only after listening to the speakers' audio recordings. On the basis of their voices alone, boys who had higher salivary testosterone levels were rated as more masculine and the relation between testosterone and perceived masculinity was partially mediated by F0. The voices of taller boys were also rated as more masculine, but the relation between height and perceived masculinity was not mediated by the considered acoustic parameters, indicating that acoustic cues other than F0 and ΔF may signal stature. Both boys and girls who had lower F0, were also rated as more masculine, while ΔF did not affect ratings. These findings highlight the interdependence of physiological, acoustic and perceptual dimensions, and suggest that inter-individual variation in male voices, particularly F0, may advertise hormonal masculinity from a very early age.

Do penguins' vocal sequences conform to linguistic laws?

Information compression is a general principle of human language: the most frequent words are shorter in length (Zipf's Law of Brevity) and the duration of constituents decreases as the size of the linguistic construct increases (Menzerath-Altmann Law). Vocal sequences of non-human primates have been shown to conform to both these laws, suggesting information compression might be a more general principle. Here, we investigated whether display songs of the African penguin, which mediate recognition, intersexual mate choice and territorial defence, conform with these laws. Display songs are long, loud sequences combining three types of syllables. We found that the shortest type of syllable was the most frequent (with the shortest syllable being repeated stereotypically, potentially favouring signal redundancy in crowded environments). We also found that the average duration of the song's constituents was negatively correlated with the size of the song (a consequence of increasing the relative number of the shortest syllable type, rather than reducing the duration across all syllable types, thus preserving the communication of size-related information in the duration of the longest syllable type). Our results provide the first evidence for conformity to Zipf's and Menzerath-Altmann Laws in the vocal sequences of a non-primate species, indicating that these laws can coexist with selection pressures specific to the species' ecology.

Dogs perceive and spontaneously normalize formant-related speaker and vowel differences in human speech sounds.

Domesticated animals have been shown to recognize basic phonemic information from human speech sounds and to recognize familiar speakers from their voices. However, whether animals can spontaneously identify words across unfamiliar speakers (speaker normalization) or spontaneously discriminate between unfamiliar speakers across words remains to be investigated. Here, we assessed these abilities in domestic dogs using the habituation-dishabituation paradigm. We found that while dogs habituated to the presentation of a series of different short words from the same unfamiliar speaker, they significantly dishabituated to the presentation of a novel word from a new speaker of the same gender. This suggests that dogs spontaneously categorized the initial speaker across different words. Conversely, dogs who habituated to the same short word produced by different speakers of the same gender significantly dishabituated to a novel word, suggesting that they had spontaneously categorized the word across different speakers. Our results indicate that the ability to spontaneously recognize both the same phonemes across different speakers, and cues to identity across speech utterances from unfamiliar speakers, is present in domestic dogs and thus not a uniquely human trait.

Voice pitch modulation in human mate choice.

Inter-individual differences in human fundamental frequency ( F0, perceived as voice pitch) predict mate quality and reproductive success, and affect listeners' social attributions. Although humans can readily and volitionally manipulate their vocal apparatus and resultant voice pitch, for instance, in the production of speech sounds and singing, little is known about whether humans exploit this capacity to adjust the non-verbal dimensions of their voices during social (including sexual) interactions. Here, we recorded full-length conversations of 30 adult men and women taking part in real speed-dating events and tested whether their voice pitch (mean, range and variability) changed with their personal mate choice preferences and the overall desirability of each dating partner. Within-individual analyses indicated that men lowered the minimum pitch of their voices when interacting with women who were overall highly desired by other men. Men also lowered their mean voice pitch on dates with women they selected as potential mates, particularly those who indicated a mutual preference (matches). Interestingly, although women spoke with a higher and more variable voice pitch towards men they selected as potential mates, women lowered both voice pitch parameters towards men who were most desired by other women and whom they also personally preferred. Between-individual analyses indicated that men in turn preferred women with lower-pitched voices, wherein women's minimum voice pitch explained up to 55% of the variance in men's mate preferences. These results, derived in an ecologically valid setting, show that individual- and group-level mate preferences can interact to affect vocal behaviour, and support the hypothesis that human voice modulation functions in non-verbal communication to elicit favourable judgements and behaviours from others, including potential mates.

The remarkable vocal anatomy of the koala (Phascolarctos cinereus): insights into low-frequency sound production in a marsupial species.

Koalas are characterised by a highly unusual vocal anatomy, with a descended larynx and velar vocal folds, allowing them to produce calls at disproportionately low frequencies. Here we use advanced imaging techniques, histological data, classical macroscopic dissection and behavioural observations to provide the first detailed description and interpretation of male and female koala vocal anatomy. We show that both males and females have an elongated pharynx and soft palate, resulting in a permanently descended larynx. In addition, the hyoid apparatus has a human-like configuration in which paired dorsal, resilient ligaments suspend the hyoid apparatus from the skull, while the ventral parts tightly connect to the descended larynx. We also show that koalas can retract the larynx down into the thoracic inlet, facilitated by a dramatic evolutionary transformation of the ventral neck muscles. First, the usual retractors of the larynx and the hyoid have their origins deep in the thorax. Secondly, three hyoid muscles have lost their connection to the hyoid skeleton. Thirdly, the genioglossus and geniohyoid muscles are greatly increased in length. Finally, the digastric, omohyoid and sternohyoid muscles, connected by a common tendinous intersection, form a guiding channel for the dynamic down-and-up movements of the ventral hyoid parts and the larynx. We suggest that these features evolved to accommodate the low resting position of the larynx and assist in its retraction during call production. We also confirm that the edges of the intra-pharyngeal ostium have specialised to form the novel, extra-laryngeal velar vocal folds, which are much larger than the true intra-laryngeal vocal folds in both sexes, but more developed and specialised for low frequency sound production in males than in females. Our findings illustrate that strong selection pressures on acoustic signalling not only lead to the specialisation of existing vocal organs but can also result in the evolution of novel vocal structures in both sexes.

The pitch of babies' cries predicts their voice pitch at age 5.

Voice pitch (fundamental frequency, F0) is a key dimension of our voice that varies between sexes after puberty, and also among individuals of the same sex both before and after puberty. While a recent longitudinal study indicates that inter-individual differences in voice pitch remain stable in men during adulthood and may even be determined before puberty (Fouquet et al. 2016 R. Soc. open sci.3, 160395. (doi:10.1098/rsos.160395)), whether these differences emerge in infancy remains unknown. Here, using a longitudinal study design, we investigate the hypothesis that inter-individual differences in F0 are already present in the cries of pre-verbal babies. While based on a small sample (n = 15), our results indicate that the F0 of babies' cries at 4 months of age may predict the F0 of their speech utterances at 5 years of age, explaining 41% of the inter-individual variance in voice pitch at that age in our sample. We also found that the right-hand ratio of the length of their index to ring finger (2D : 4D digit ratio), which has been proposed to constitute an index of prenatal testosterone exposure, was positively correlated with F0 at both 4 months and 5 years of age. These findings suggest that a substantial proportion of between-individual differences in voice pitch, which convey important biosocial information about speakers, may partly originate in utero and thus already be present soon after birth.

Dog-directed speech: why do we use it and do dogs pay attention to it?

Pet-directed speech is strikingly similar to infant-directed speech, a peculiar speaking pattern with higher pitch and slower tempo known to engage infants' attention and promote language learning. Here, we report the first investigation of potential factors modulating the use of dog-directed speech, as well as its immediate impact on dogs' behaviour. We recorded adult participants speaking in front of pictures of puppies, adult and old dogs, and analysed the quality of their speech. We then performed playback experiments to assess dogs' reaction to dog-directed speech compared with normal speech. We found that human speakers used dog-directed speech with dogs of all ages and that the acoustic structure of dog-directed speech was mostly independent of dog age, except for sound pitch which was relatively higher when communicating with puppies. Playback demonstrated that, in the absence of other non-auditory cues, puppies were highly reactive to dog-directed speech, and that the pitch was a key factor modulating their behaviour, suggesting that this specific speech register has a functional value in young dogs. Conversely, older dogs did not react differentially to dog-directed speech compared with normal speech. The fact that speakers continue to use dog-directed with older dogs therefore suggests that this speech pattern may mainly be a spontaneous attempt to facilitate interactions with non-verbal listeners.

What makes a voice masculine: physiological and acoustical correlates of women's ratings of men's vocal masculinity.

Men's voices contain acoustic cues to body size and hormonal status, which have been found to affect women's ratings of speaker size, masculinity and attractiveness. However, the extent to which these voice parameters mediate the relationship between speakers' fitness-related features and listener's judgments of their masculinity has not yet been investigated. We audio-recorded 37 adult heterosexual males performing a range of speech tasks and asked 20 adult heterosexual female listeners to rate speakers' masculinity on the basis of their voices only. We then used a two-level (speaker within listener) path analysis to examine the relationships between the physiological (testosterone, height), acoustic (fundamental frequency or F0, and resonances or ΔF) and perceptual dimensions (listeners' ratings) of speakers' masculinity. Overall, results revealed that male speakers who were taller and had higher salivary testosterone levels also had lower F0 and ΔF, and were in turn rated as more masculine. The relationship between testosterone and perceived masculinity was essentially mediated by F0, while that of height and perceived masculinity was partially mediated by both F0 and ΔF. These observations confirm that women listeners attend to sexually dimorphic voice cues to assess the masculinity of unseen male speakers. In turn, variation in these voice features correlate with speakers' variation in stature and hormonal status, highlighting the interdependence of these physiological, acoustic and perceptual dimensions.

Response of red deer stags (Cervus elaphus) to playback of harsh versus common roars.

Red deer stags (Cervus elaphus) give two distinct types of roars during the breeding season, the "common roar" and the "harsh roar." Harsh roars are more frequent during contexts of intense competition, and characterized by a set of features that increase their perceptual salience, suggesting that they signal heightened arousal. While common roars have been shown to encode size information and mediate both male competition and female choice, to our knowledge, the specific function of harsh roars during male competition has not yet been studied. Here, we investigate the hypothesis that the specific structure of male harsh roars signals high arousal to competitors. We contrast the behavioral responses of free ranging, harem-holding stags to the playback of harsh roars from an unfamiliar competitor with their response to the playback of common roars from the same animal. We show that males react less strongly to sequences of harsh roars than to sequences of common roars, possibly because they are reluctant to escalate conflicts with highly motivated and threatening unfamiliar males in the absence of visual information. While future work should investigate the response of stags to harsh roars from familiar opponents, our observations remain consistent with the hypothesis that harsh roars may signal motivation during male competition, and illustrate how intrasexual selection can contribute to the diversification of male vocal signals.

Humans need auditory experience to produce typical volitional nonverbal vocalizations.

Human nonverbal vocalizations such as screams and cries often reflect their evolved functions. Although the universality of these putatively primordial vocal signals and their phylogenetic roots in animal calls suggest a strong reflexive foundation, many of the emotional vocalizations that we humans produce are under our voluntary control. This suggests that, like speech, volitional vocalizations may require auditory input to develop typically. Here, we acoustically analyzed hundreds of volitional vocalizations produced by profoundly deaf adults and typically-hearing controls. We show that deaf adults produce unconventional and homogenous vocalizations of aggression and pain that are unusually high-pitched, unarticulated, and with extremely few harsh-sounding nonlinear phenomena compared to controls. In contrast, fear vocalizations of deaf adults are relatively acoustically typical. In four lab experiments involving a range of perception tasks with 444 participants, listeners were less accurate in identifying the intended emotions of vocalizations produced by deaf vocalizers than by controls, perceived their vocalizations as less authentic, and reliably detected deafness. Vocalizations of congenitally deaf adults with zero auditory experience were most atypical, suggesting additive effects of auditory deprivation. Vocal learning in humans may thus be required not only for speech, but also to acquire the full repertoire of volitional non-linguistic vocalizations.