# Human infant cries communicate distress and elicit sex stereotypes: Cross cultural evidence

Clément Cornec, Nicolas Mathevon, Katarzyna Pisanski, Don Entani, Claude Monghiemo, Blanchard Bola, Victor Planas-Bielsa, David Reby, Florence Levréro

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Clément Cornec, Nicolas Mathevon, Katarzyna Pisanski, Don Entani, Claude Monghiemo, et al. Human infant cries communicate distress and elicit sex stereotypes: Cross cultural evidence. Evolution and Human Behavior, 2024, 45, pp.48 - 57. 10.1016/j.evolhumbehav.2023.08.004. hal-04861069

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# Human infant cries communicate distress and elicit sex stereotypes: Cross cultural evidence

Clément Cornec<sup>a, *</sup>, Nicolas Mathevon<sup>a</sup>, Katarzyna Pisanski<sup>a, e</sup>, Don Entani<sup>b</sup>,

Claude Monghiemo<sup>b</sup>, Blanchard Bola<sup>c</sup>, Victor Planas-Bielsa<sup>d</sup>, David Reby<sup>a</sup>, Florence Levréro<sup>a</sup>

## ARTICLE INFO

Keywords:

Human evolution

Vocal communication

Voice perception

Nonverbal vocalisation

Cross-cultural research

Parent-infant relationship

## ABSTRACT

The degree to which culture and context contribute to variability in human behaviour is a critical scientific question. While most research in the human behavioural sciences is based on WEIRD samples, the last decade has seen a rise in research on traditionally under-represented populations, including small-scall societies, to demonstrate reproducibility of results. Considering this framework as a major objective, here we explore cross-cultural ubiquity in the production and perception of human baby cries, focusing on remote rural communities in the Democratic Republic of Congo, compared to analogous data from French and British samples. Through acoustic analysis of Congolese baby cries recorded in natural discomfort (bath) and pain (vaccine) contexts, combined with psychoacoustic experiments on Congolese adult listeners, we show that distress is reliably encoded in the acoustic cry signal, namely in nonlinear acoustic phenomena. Despite the absence of sexual dimorphism in cries, low-pitched cries are more often perceived as produced by boys than girls, and cries experimentally attributed to boys are perceived as expressing more distress than the same cries experimentally attributed to girls. Having obtained similar results in European samples, this study provides compelling evidence that these voice-based stereotypes are stable and robust, observed across extremely distinct human populations.

## 1. Introduction

The human voice carries cues to a variety of biological and social dimensions of a speaker including sex, age, body size, dominance, and perceived masculinity or femininity (Pisanski & Bryant, 2019, for review). This vital information is communicated largely by nonverbal acoustic properties of the vocal signal, most notably fundamental frequency ($f_0$) that is determined by the rate of vocal fold vibration and affects the perceived pitch of a voice (Titze, 2000). While human adults exhibit the most sexually dimorphic $f_0$ of all great ape species (Puts et al., 2016), sex differences in voice pitch do not emerge until puberty (Harries, Walker, Williams, Hawkins, & Hughes, 1997). Indeed, pre-pubertal boys and girls produce cries and speech of similar pitch regardless of their biological sex (Lee, Potamianos, & Narayanan, 1999; Reby, Levréro, Gustafsson, & Mathevon, 2016).

Research has consistently shown strong perceptual stereotypes

associated with high or low $f_0$, wherein men and women whose voices are characterised by relatively low pitch are generally judged by listeners to be more dominant, physically larger, stronger and more masculine than those whose voices are higher-pitched, and these stereotypes appear to be partly determined by anatomical and physiological mechanisms that constrain $f_0$ production (reviewed in Aung & Puts, 2020; Kreiman & Sidtis, 2011; Pisanski & Bryant, 2019). Yet, pitch-based stereotypes are not limited to the voices of adults. Recent research has shown that British listeners associate low pitch with masculinity in the speech of pre-pubertal children (Cartei et al., 2020), and British and French listeners attribute low-pitched cries to baby boys and high pitched-cries to baby girls (Reby et al., 2016), despite no biological foundation to these sex biases. Listeners also judge baby boys who produce relatively high-pitched cries as less masculine (Reby et al., 2016). If we combine these findings with evidence that inter-individual differences in $f_0$ remain stable throughout the lifespan, from infancy to

<footnote><sup>a</sup> ENES Bioacoustics Research Lab, CRNL, CNRS UMR5292, Inserm UMR_S 1028, University of Saint-Etienne, Saint-Etienne, France</footnote>

<footnote><sup>b</sup> NGO Mbou-Mon-Tour, Democratic Republic of the Congo</footnote>

<footnote><sup>c</sup> Hospital of Tshumberby, Democratic Republic of the Congo</footnote>

<footnote><sup>d</sup> Centre Scientifique de Monaco, Département de Biologie Polaire, 98000, MC, Monaco</footnote>

<footnote><sup>e</sup> Centre National de la Recherche Scientifique, Laboratoire Dynamique du Langage, Université Lyon 2, France</footnote>

<footnote>* Corresponding author at: ENES Bioacoustics Research Lab, University of Saint-Etienne, 23 rue Paul Michelon, 42023 Saint-Etienne, cedex 2, France.
E-mail address: clement.cornec@univ-st-etienne.fr (C. Cornec).</footnote>
childhood (Levrero, Mathevon, Pisanski, Gustafsson, & Reby, 2018) and into adulthood (Fouquet, Pisanski, Mathevon, & Reby, 2016), it appears that social judgments based on the pitch of our voices may be attributed to us the moment we produce our first cries.

Voice pitch also influences judgments of emotional and motivational states. Similar to the acoustic signals of other vertebrate species (Morton, 1977), low pitch in men's and women's voices is typically perceived as signalling aggression and threat (Aung & Puts, 2020; Ohala, 1994), whereas high pitch is consistently associated with stress, distress, and pain (Kelly et al., 2017; Pisanski & Sorokowski, 2020; Raine, Pisanski, Simner, & Reby, 2018). These perceptual biases again appear to generalise to the cries of human infants. Despite no robust relationship between the mean $f_0$ of a baby's cry and their apparent level of distress (Koutseff et al., 2018), French and English adult listeners have been shown to erroneously associate higher pitched cries with higher levels of discomfort (Kelly et al., 2017; Koutseff et al., 2018; Reby et al., 2016). Moreover, there is some evidence that European listeners may show a sex bias in their perceptions of discomfort from babies' cries. Indeed, Reby et al. (2016) found that the exact same cries, synthetically lowered in pitch, were perceived as representing more distress when male listeners thought they were produced by baby boys rather than girls. This suggests that some listeners may overestimate discomfort in boys' cries, possibly because those listeners (erroneously) expect that the cries of baby boys should be lower-pitched than those of baby girls.

Such mistattributions are surprising given the evolutionary relevance of the cry. Crying is a vital built-in survival mechanism for the highly dependent human baby, designed to attract and maintain the attention of the listener, typically the caregiver, and thus to elicit aid. Crying in infants is often triggered by pain, discomfort, hunger or separation from parents or caregivers (Lockhart-Bouron Anikin et al., 2023; Soltis, 2004). Acoustic analyses have shown that although $f_0$ does not robustly predict distress in infant cries, with the exception of extremely high-pitched cries signalling severe pain (Bellieni, Sisto, Cordelli, & Buonocore, 2004), nonlinear acoustic phenomena may provide a much more reliable index of the infant's ostensible level of distress. Nonlinear phenomena include sidebands, subharmonics, frequency jumps, vibrato-like frequency modulation and deterministic chaos (Fitch, Neubauer, & Herzel, 2002), all of which contribute to the perceptual harshness or roughness of cries. Research has linked nonlinearities in the vocal signals of non-human mammals to the behavioural responses of listeners (Blumstein & Recapet, 2009; Reby & Charlton, 2012; Townsend & Manser, 2011), and has also shown that the proportion of nonlinear phenomena in human adult vocalisations (e.g., screams, roars, moans) predicts their perceived aversiveness and emotional intensity (Anikin, 2019). Nonlinearities also appear to increase with distress or arousal in babies' cries (Facchini, Bellieni, Marchettini, Pulselli, & Tiezzi, 2005; Koutseff et al., 2018; Leger, Thompson, Merritt, & Benz, 1996; Tiezzi, Pulselli, & Facchini, 2004; Yoo, Buder, Bowman, Bidelman, & Oller, 2019), and to influence French parents' perceptions of distress (Koutseff et al., 2018).

Problematically, research on the human voice, like the vast majority of research in the human behavioural sciences, has been restricted to Western, Educated, Industrialized, Rich, and Democratic societies (WEIRD, Henrich, Heine, & Norenzayan, 2010a, 2010b). It thus remains unknown whether the results truly represent ‘human behaviour’, or rather, are a product of culture-specific norms and mass media exposure to western sociocultural stereotypes. While cross-cultural studies provide preliminary evidence that listeners perceive prosodic patterns or emotions from adult speech similarly across cultures (Bryant & Barrett, 2007; Bryant & Barrett, 2008; Bryant, Liénard, & Clark Barrett, 2012), few empirical studies have tested whether human nonverbal vocalisations such as cries, laughs, and roars share common acoustic forms and perceptual functions across cultures (but see Gendron, Roberson, van der Vyver, & Barrett, 2014). Among the exceptions are studies by Bryant et al. (2016), showing a capacity in adult listeners from 24 different societies to discriminate co-laughter produced by friends

versus strangers, and by Sauter, Eisner, Calder, and Scott (2010); Sauter, Eisner, Ekman, and Scott (2015) and Laukka et al. (2013) who provide preliminary evidence of cross-cultural decoding of a range of positive and negative affective vocalisations produced by adults. While (Bornstein et al., 1992, 2017; Bornstein, Cote, Haynes, Suwalsky, & Bakeman, 2012) provide evidence that mothers from different cultures respond similarly to the behavioural signals of their babies, including vocalisations, the authors did not test which acoustic parameters drive these responses. Critically, thus, no research has examined the information encoded in cries of babies outside of the western hemisphere, including small-scale societies, nor tested whether adult listeners in such communities can infer the emotional content of the cries, thus greatly limiting the generalisability of previous work.

Here, we examine the production and perception of babies' cries in small-scale communities in the Democratic Republic of the Congo. In these small rural villages, where child mortality is high (infant mortality rate 68 per 1000 live births, UNESCO 2018), large families residing closely together share childcare duties. We conduct an extensive acoustic analysis of cries produced by Congolese babies in low- and high-distress contexts (bath and vaccination, respectively) and, using both natural and resynthesised cry stimuli, we conduct a series of psycho-acoustic field experiments on a representative sample of 123 Congolese adult listeners to test several key predictions: (i) actual distress levels in Congolese babies' cries will be encoded by an increase in nonlinear phenomena, not $f_0$; (ii) the acoustic structure of babies' cries will not differ between boys and girls; yet (iii) cries with synthetically lowered pitch will more often be perceived by listeners as produced by boys than girls; (iv) adult listeners' judgments of distress will be higher for vaccination cries than for bath cries; (v) cries with synthetically raised pitch will be judged as higher in distress; and (vi) cries experimentally attributed to boys will be perceived as expressing more distress than those same cries experimentally attributed to girls.

## 2. Methods

All procedures are in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The study was approved by the local ethic committee (Kinshasa School of Public Health, University of Kinshasa: ESP/CE/55B).

### 2.1. Participants

Participants included 36 Congolese babies whose cries were audio recorded (average age 3 months or 96 ± 31 days), and 123 Congolese adults (mean estimated age 32 ± 8 years) who judged the perceived sex and/or distress level of these babies based on their cries. These sample sizes of recorded babies and adult listeners in playback experiments were selected to closely resemble those of Reby et al. (2016) who conducted similar studies on European samples, examining both acoustic indices of distress in European babies' cries and running comparable playback experiments on European adult listeners who judged distress and sex from those cries. Our sample sizes are thus large enough to detect similar effect sizes if they are also present in the Congolese samples. Note that, in the Congolese villages where we collected data, there is no precise system for tracking age and ages were estimated by adult listeners and parents of babies. Participation in the playback experiments was limited to those aged approximately 20 to 67 years of age. All participants were recruited from a local majority Téké ethnic group residing in the remote forest-savanna mosaic in the Bolobo Territory of the western Democratic Republic of Congo. This area is located in the Mai-Ndombe District of the Bandundu Province, 300 km north of Kinshasa. The study was carried out in six locations covering an area of approximately 100 km2: Embirima, Ndwa, Lewo, Mbee, Nkoo and Tshumbiri. Téké people, also referred to as Bateke, speak the Téké and Lingala languages.
## 2.2. Stimuli

Following previous work on European samples (Koutseff et al., 2018; Reby et al., 2016), baby cries were recorded in one of two contexts: while being bathed by their parents at home, corresponding to mild discomfort, or during a vaccination session, corresponding to more severe discomfort or pain (Fig. 1).

In the discomfort context, we recorded spontaneous bath cries from 9 boys and 9 girls in the villages of Embirima, Mbee and Nkoo. In the pain context, a separate group of 9 boys and 9 girls were recorded while being held by their mother and receiving an injection of the Pneumococcal Conjugate Vaccine (PCV-13, Prevenar 13®) given by a nurse. These recordings were carried out at the health posts of the Embirima, Ndwa, Lewo and Nkoo villages and the Tshumbiri hospital. Vaccination, free and compulsory for all babies in the DR Congo, is carried out according to a vaccination schedule imposed by the country. Recorded babies received two successive vaccinations in the following systematic order: pentavalent vaccine (for diphteria, tetanus and whooping cough) given in the baby's thigh, and the Pneumococcal Conjugate Vaccine given in the baby's other thigh. Less than a minute elapsed between each injection.

All cries were audio recorded digitally with a dynamic, omnidirectional microphone (Sennheiser MD42) positioned approximately 30 cm from the baby's face and connected to a Zoom Handy Recorder H4n (Zoom, Japan: 44.1 kHz sampling frequency, 32-bits resolution, mono, WAV format). Cries were extracted from raw sound recordings using PRAAT (Boersma & Weenink, 2018). To carry out the acoustic analysis, for each baby, we randomly extracted one discomfort cry within the cry sequence, and the first cry produced in response to the PCV-13 vaccination, from each baby (Koutseff et al., 2018). All cry stimuli were amplitude normalized using Avisoft SAS LabPro software, version 5.2.07

(Avisoft Bioacoustics, Germany), wherein the amplitude waveform of the WAV files was centred around 0 and normalized to 75% of the maximal amplitude.

## 2.3. Acoustic analyses of cries

All cries were acoustically analysed. This included 18 cries from 18 babies (9 girls and 9 boys) recorded in the discomfort context and 18 cries from 18 babies (9 girls and 9 boys) recorded in the pain context. To analyse the acoustic structure of cries, we used a series of custom-built scripts (Charlton, Zhihe, & Snyder, 2009; Reby & McComb, 2003) in PRAAT DSP package v. 6.0.31 (Boersma & Weenink, 2018). These procedures have previously been successfully applied to characterise acoustic variation in babies' cries (Gustafsson, Levréro, Reby, & Mathevon, 2013; Koutseff et al., 2018; Reby et al., 2016). The program batch processed the analyses in distinct procedures (PRAAT commands are indicated in brackets) that extracted 15 acoustic features (listed and defined in Table S1).

In a first step of the procedure, we extracted a range of $f_0$ related parameters derived from the $f_0$ contour of each call using the cross-correlation method ([Sound: To pitch (cc) command], time step = 0.01 s, pitch floor = 60 Hz, pitch ceiling = 3000 Hz). We systematically inspected the extracted pitch contour and verified it using a narrow band spectrogram displaying the first 2000 Hz of the signal. Spurious octave jumps were manually corrected by selecting the appropriate $f_0$ candidate values in the edited pitch object. In the relatively rare segments including double vibration (where a weak subharmonic equal to half the $f_0$ is present), the $f_0$ was systematically preferred over the subharmonic. When deterministic chaos was present, we 'unvoiced' incorrect $f_0$ values. Each extracted $f_0$ contour (pitch object) was saved as a text file for future reference. These numerical representations were used to

<figure><img src="image_2.png" /></figure>

<figure><img src="image_3.png" /><figcaption>**Fig. 1.** Acoustic structure of baby cries. Spectrograms (x-axis = time in seconds; y-axis = frequency in Hertz). (A) cry recorded during a bath (discomfort context). (B–D) cries recorded during vaccination events (painful context). Pain cries have a less-defined harmonic structure, with a high proportion of various nonlinear acoustic phenomena including sidebands (SB), periodic vibrato-like frequency modulation (VFM), subharmonics (SH), deterministic chaos (CH) and frequency jumps (FJ). Figure prepared with Seewave R package (Sueur, Aubin, & Simonis, 2008).</figcaption></figure>

<figure><img src="image_4.png" /></figure>

<figure><img src="image_5.png" /></figure>
derive the following parameters: mean $f_0$, max $f_0$, min $f_0$, $f_0$ start, $f_0$ end, $f_0$ Abs Slope. Additionally, to characterise $f_0$ modulation within each cry, we measured the $f_0$ var., Sum var., FM rate and FM extent.

In a second step, two distinct smoothing algorithms ([Smooth command]) were performed on the pitch contour. With these algorithms, the number of inflection points was divided across the total duration of voiced segments in the cry. The first algorithm allowed a relatively broad bandwidth ([Smooth command, bandwidth = 25], corresponding to inflex25), to suppress very short-term frequency fluctuation while preserving minor intonation events (such as bleat-like frequency modulation). The second algorithm only allowed a narrow bandwidth ([Smooth command, bandwidth = 2], corresponding to inflex2), to characterise strong $f_0$ modulation.

A third procedure focused on the periodic quality of the signal and measured harmonicity ([To harmonicity (cc)], time step = 0.01 s, pitch floor = 60 Hz, silence threshold = 0.1, periods per window = 1) using the standard settings in PRAAT and an index of jitter ([Jitter (local) command], small fluctuation in periodicity measured as the average of ‘local’, ‘rap’ and ‘ppq5’ measures) and an index of shimmer ([Shimmer (local) command], small variation in amplitude between consecutive periods, measured as the average of ‘local’, ‘apq5’ and ‘apq11’ parameters in PRAAT) using the same settings as for the $f_0$ contour.

Nonlinear phenomena were manually measured via visual inspection of narrowband spectrograms. We computed the total percentage of nonlinear phenomena by summing the percentages of sidebands, periodic vibrato-like frequency modulation, subharmonics and deterministic chaos. Example waveforms and spectrograms of nonlinear phenomena are provided in Fig. 1.

Before extracting the vocal parameters, we added silences of 0.1 s to each side of the natural discomfort and pain cries.

## 2.4. Sound re-synthesis

We re-synthesised the fundamental frequency ($f_0$, perceived as voice pitch) of all extracted discomfort and pain cries using the PSOLA algorithm in PRAAT. PSOLA re-synthesis enables the independent rescaling of $f_0$ while leaving all other parameters of the signal unchanged, and is a well-established method for independently manipulating acoustic features in human speech signals and nonverbal vocalisations, including babies' cries (e.g. Reby et al., 2016). From each original natural cry, we created a set of vocal stimuli in which we manipulated mean $f_0$ based on the mean cry pitch $\pm n$ SD of our sample (where $n = 0, 1$ and $2$) (see also Reby et al., 2016). For re-synthesised discomfort cries, we thus manipulated mean $f_0$ values to 338 Hz, 390 Hz, 440 Hz, 492 Hz and 543 Hz, and for re-synthesised pain cries, to 309 Hz, 383 Hz, 458 Hz, 532 Hz and 607 Hz.

## 2.5. Playback experiments

Three playback experiments were performed on Congolese listeners. Two experiments tested for an effect of manipulated cry pitch on perceptions of sex and distress, and the third tested the prediction that experimentally attributed sex will causally affect perceptions of distress. All the cries we recorded and acoustically analysed were used in playback experiments. While not all listeners judged the full set of natural or synthetic cries, we ensured that each cry was judged by approximately the same number of listeners in each experiment.

All playback experiments were conducted in the Embirima village of the Democratic Republic of Congo. Sample sizes were 56 participants for experiment 1, 56 for experiment 2, and 60 for experiment 3; note that 49 participants took part in two experiments (identity of listeners was controlled in all statistical models). Participants were not the parents of the babies whose recordings were used for playback experiments, and in the majority of cases (30 of 36 cries), listeners lived in a different village than the recorded babies, ensuring that listeners would not be familiar with the cries. All participants were tested in individual sessions in a

quiet area, inside or outside their home, by authors CC or FL. All instructions were given in Lingala and/or Téké language according to the participants by a verified translator (DE) allowing us to carefully adapt our protocol for translatability, local conditions and social norms (Broesch et al., 2020). Cry stimuli were played to listeners by researchers CC or FL on a Zoom Handy Recorder H4n through Sennheiser HD205-II headphones at a comfortable sound level kept constant across stimuli and between participants. Each participant heard the same number of cry stimuli, presented in a random order. The participant was permitted to listen to the stimulus once more if they requested it. All playback experiments were double-blind.

### 2.5.1. Playback experiment 1: Effect of experimentally manipulated cry pitch on sex attribution

Fifty-six adults, all parents (28 fathers and 28 mothers) of babies <18-months of age, took part in the first playback experiment. A playback session included 48 cry stimuli, 8 natural discomfort cries from 8 babies (randomly chosen for each participant from the 18 babies recorded in the discomfort context) and 40 re-synthesised discomfort cries taken from the same 8 babies (for each resynthesised level of mean $f_0$: 338 Hz, 390 Hz, 440 Hz, 492 Hz and 543 Hz). Participants were verbally instructed to indicate the sex (boy or girl) of each baby based only on its cry immediately after hearing the cry. The experimentor (CC or FL) noted each response in a notebook.

### 2.5.2. Playback experiment 2: Effect of experimentally manipulated cry pitch on perceived distress

Fifty-six adults, all parents (28 fathers and 28 mothers) of babies <19-months of age, took part in the second playback experiment. The playback included 48 cry stimuli, 4 natural discomfort cries (randomly chosen for each participant from the 18 babies recorded in the discomfort context), 4 natural pain cries (randomly chosen for each participant from the 18 babies recorded in the pain context) and 40 re-synthesised discomfort cries taken from the same 8 babies (for each re-synthesised level of mean $f_0$: 338 Hz, 390 Hz, 440 Hz, 492 Hz and 543 Hz for re-synthesised discomfort cries; 309 Hz, 383 Hz, 458 Hz, 532 Hz and 607 Hz for re-synthesised pain cries). Participants categorised the distress expressed by the babies in each stimulus by choosing one of five distress labels presented on a visual analogue scale where 1 indicated no distress, 2 low distress, 3 medium distress, 4 strong distress and 5 indicated extremely severe distress. The interpretation of this scale was verified through pilot testing on a small sub-sample of Congolese villagers (Fig. S1).

### 2.5.3. Playback experiment 3: Effect of experimentally attributed baby sex on perceived distress

A new sample of sixty adults, all parents (30 fathers and 30 mothers) of a young child of maximum 4 years of age, took part in the third playback. All participants judged 32 stimuli which included natural discomfort cries ($n = 16$) and natural pain cries ($n = 16$). For half of the participants (“group 1”), we randomly assigned a sex (girl or boy) to each cry stimulus (8 natural discomfort and 8 natural pain cries were assigned as boys, and 8 natural discomfort and 8 natural pain cries were assigned as girls). For the other half of participants (“group 2”), we used the same stimuli but assigned the opposite sex to each cry compared to that assigned for group 1. Thus, each baby was assigned both sexes, one sex per listener group, and so the allocated sex matched the real sex of the baby in 50% of cases. Participants were instructed to indicate the distress they perceived for each baby cry immediately after hearing each cry by choosing one of five distress labels presented on a printed visual scale, where 1 indicated no distress, 2 low distress, 3 medium distress, 4 strong distress and 5 indicated extremely severe distress (Fig. S1).

Participants responded to a short oral questionnaire following the playback experiment indicating their own sex, age and provided an open-ended response to the questions: Do you think baby boys and girls cry differently? And if so, which vocal characteristics influenced your
judgment of the babies' sex? Do you think that babies cry differently
depending on the cause of the cry?

## 2.6. Statistical analysis

All statistical analyses were conducted using R version 3.6.1 (R Core Team, 2020).

### 2.6.1. Acoustic analyses of cries

We first used a Principal Component Analysis (PCA) to reduce the dimensionality of the acoustic dataset, and examine clustering among cry parameters. Missing data (5%) occurred when one vocal parameter in a given cry could not be measured mainly due to a high proportion of deterministic chaos. To consider a complete dataset, an imputation method was performed to process the missing data through the functions estim_ncpPCA and imputePCA from the missMDA R package (version 1.10, see Josse & Husson, 2016 for more details). Prior to executing the PCA, data were log-transformed for each category. We retained the principal components of the PCA with eigenvalues >1 (Kaiser's criterion).

To compare the acoustic structure of natural discomfort cries and natural pain cries, and to test for sexual dimorphism in cry structure, the scores of the retained principal components were confirmed for normality (Kolmogorov-Smirnov test) and used as input variables in the ANOVA (if residuals were normally distributed) or Wilcoxon signed-rank tests (if residuals were not normally distributed). PCAs were performed using the R packages 'FactoMineR' (Lê, Josse, & Husson, 2008) and 'Factoextra' (Kassambara & Mundt, 2020).

### 2.6.2. Playback experiments

We conducted a series of Generalised Linear Mixed Models (GLMMs) in R to examine the responses of listeners. For the first playback experiment, the GLMM tested whether the biological sex of the baby was a significant predictor of the sex attributed by adults judging natural discomfort cries. The real sex of each baby and the sex of the listener were included as fixed factors. We ran a second GLMM to test the effect of re-synthesised cry pitch ($f_0$) on sex attributions by adult listeners. The real sex of babies, the sex of the listener and the re-synthesised pitch level were included as fixed terms. In both GLMMs, we coded the response as a binary variable where 0 corresponds to an attribution of 'boy', and 1 corresponds to an attribution of 'girl'.

Two additional GLMMs were conducted for the second playback experiment. First, we tested if cry context (natural discomfort or pain cries) predicted perceived distress. Cry context, the sex of the baby and the sex of the listener were included as fixed terms. Another GLMM tested the effect of re-synthesised cry pitch ($f_0$) on perceived distress. Cry context, sex of the baby, sex of the listener, and the re-synthesised pitch level were included as fixed terms.

For the third playback experiment, we performed a GLMM to test the effect of experimentally attributed baby sex on the perception of distress level for natural discomfort and natural pain cries. The real sex of babies, the experimentally attributed sex of babies, the sex of the listener, the group of the listener (group 1 or 2), and the cry context (natural discomfort or pain cries) were included as fixed terms.

For playback experiment 1, the model was run using a log link function with a binomial distribution. For the second and third playback experiments, models were run using a Poisson family distribution. The identity of listeners was included as a random factor in all GLMMs to avoid pseudoreplication and account for noise from systematic individual differences in ratings. We used Akaike Information Criteria (AIC) to determine the best fitting models. GLMMs were performed using the function glmer of the 'lme4' package (Bates, Sarkar, Bates, & Matrix, 2007). The estimated marginal means were obtained using the 'modelbased' package (Makowski, Lüdecke, & Ben-Shachar, 2020) and vetted by SPSS 24 (IBM). The figures were obtained using the package 'ggplot2' (Wickham, Chang, & Wickham, 2016).

# 3. Results

## 3.1. Acoustic analyses of cries

A PCA examining the acoustic structure of babies' cries included 16 acoustic parameters measured from all cries produced by all 36 babies. The cumulative percentage of the four principal components (PCs) explained 78.4% of the total variance in cry acoustic structure (Table S2). Examination of the factor loadings (Table S2) revealed that cry frequency parameters ($f_0$-Abs-Slope, $f_0$ var., $f_0$ max, $f_0$ mean) and FM extent loaded highly on PC1. Periodicity parameters (harmonicity, jitter and shimer), nonlinear phenomena, and $f_0$ min loaded highly on PC2. Frequency modulation parameters (inflex 25 and 2, FM rate) and $f_0$ end loaded highly on PC3. Finally, $f_0$ start and Sum var. loaded highly on PC4.

Comparing natural discomfort and pain cries showed a significant difference only for the second acoustic component, representing cry roughness induced mainly by perturbation parameters and nonlinear phenomena (Anova, $F_{1,34} = 18.3, p < 0.001$, Fig. S2). Here, cry roughness was higher for natural pain cries than for natural discomfort cries (Fig. S2). No difference was found for the other acoustic components, indicating that, as predicted, voice pitch parameters did not differ between pain and distress cries.

Comparing cries produced by girls and boys showed no significant differences in any acoustic components, regardless of cry context (Fig. S3).

## 3.2. Playback experiment 1: Effect of experimentally manipulated cry pitch on sex attribution

The rate of correct sex identification from natural discomfort cries was around 50% (chance level) for both fathers (53% for boys' cries and 54% for girls' cries) and mothers (49% for boys' cries and 48% for girls' cries). The GLMM confirmed that for trials involving natural discomfort cries, neither the baby's sex ($\beta$ = 0.15, SE = 0.16, z(448) = 0.78, $p$ = 0.44), nor the participant's sex ($\beta$ = -0.08, SE = 0.19, z(448) = -0.43, $p$ = 0.67) were significant predictors of whether participants correctly judged the baby's sex (Table S3, Fig. 2A).

Despite a lack of confirmed sex differences in the acoustic structure of babies' cries, all participants, with the exception of one woman ($n$ = 122), when completing the post-experiment questionnaire, indicated that they thought that baby boys and baby girls cry differently. The majority of participants (72%, $n$ = 89) reported that they think boys cry more loudly than girls, and 23% ($n$ = 28) reported that they think the cries of boys are lower-pitched than those of girls (Table S4). Indeed, in trials involving re-synthesised discomfort cries, the mean pitch level of the cry significantly influenced the sex attributed by adult listeners (GLMM: $\beta$ = -0.43, SE = 0.04, z(2240) = -9.64, $p$ < 0.001, Table S5). As predicted, we found that lower-pitched cries were attributed mainly to boys and higher-pitched cries mainly to girls (Fig. 2). Neither the baby's sex ($\beta$ = -0.11, SE = 0.09, z(2240) = -1.23, $p$ = 0.22), nor the listener's sex ($\beta$ = -0.05, SE = 0.09, z(2290) = -0.53, $p$ = 0.6), were significant predictors of the attributed sex (Table S4).

## 3.3. Playback experiment 2: Effect of experimentally manipulated cry pitch on perceived distress

Except 3, all but 3 participants (97.6%, $n$ = 120) responded that they think babies cry differently depending on the cause of the cry.

In trials involving natural discomfort and natural pain cries, cry context (discomfort or pain) was a significant predictor of distress ratings ($\beta$ = 1.03, SE = 0.05, z(448) = 3.41, $p$ < 0.001, Table S6). Adult listeners rated natural pain cries as expressing more distress than natural discomfort cries (Fig. 3). The baby's sex ($\beta$ = 0.01, SE = 0.05, z(448) = 0.25, $p$ = 0.8) and the listener's sex ($\beta$ = -0.01, SE = 0.05, z(448) = -0.18, $p$ = 0.86) did not predict perceived distress (Table S6).
<figure><img src="image_6.png" /><figcaption>**Fig. 2.** Pitch-dependent attribution of baby's sex by adult listeners (Playback experiment 1). (A) Sex attributed by adult participants (28 men and 28 women) listening to natural cries of unfamiliar babies, where correct sex identification is not different from chance (50%) due to a lack of sexual dimorphism in babies' cries. (B) Sex attributed by adult participants (28 men and 28 women) to each of five mean pitch re-synthesised cry variants (x-axis: mean $f_o$ variants = 338, 390, 440, 492 and 543 Hz; y-axis: sex attribution). The mean pitch level of the cry influences the sex attributed by the listener, with higher pitched cries more likely to be attributed to girls than to boys. (C) Examples of re-synthesised variants from the same cry exemplar. Data derive from estimated marginal means of GLMMs.</figcaption></figure>

<figure><img src="image_7.png" /><figcaption>**Fig. 3.** Effect of cry pitch on perceived distress by adult listeners (Playback experiment 2). (A) Distress rating by adult participants (28 men and 28 women) listening to natural cries of unfamiliar babies. Cry context is a significant predictor of distress ratings. (B) Distress ratings by adult participants (28 men and 28 women) for each of 10 mean pitch re-synthesised cry variants (x-axis: mean $f_o$ variants of cries recorded during a bath (discomfort context) and during a vaccination (pain context); y-axis: mean distress rating. The higher the mean manipulated $f_o$, the higher the distress rating given by the listener, with pain cries correctly rated as more painful than discomfort cries.</figcaption></figure>

In trials involving re-synthesised discomfort and pain cries, cry context ($\beta$ = 0.16, SE = 0.02, z(448) = 6.4, p < 0.001, Table S7) and re-synthesised $f_o$ ($\beta$ = 0.0003, SE = 0.0001, z(448) = 2.44, p = 0.015, Table S7) significantly predicted ratings of distress by adult listeners. Adult listeners rated higher-pitched cries as expressing more distress than lower-pitched cries (Fig. 3). Neither the baby's sex ($\beta$ = -0.004, SE = 0.03, z(448) = -0.18, p = 0.86), nor the listener's sex ($\beta$ = -0.04, SE = 0.03, z(448) = -1.53, p = 0.13) were significant predictors of perceived distress (Table S7).

### 3.4. Playback experiment 3: Effect of experimentally attributed baby sex on perceived distress

In trials involving natural discomfort and natural pain cries, cry context was a significant predictor of distress ratings (GLMM: $\beta$ = 0.28, SE = 0.06, z(1920) = 4.93, p < 0.001, Table S8). Adult listeners rated natural pain cries as expressing more distress than natural discomfort cries. The experimentally attributed sex of the baby was also a significant predictor of distress ratings, wherein mothers and fathers rated putative boys' cries as expressing more distress than putative girls' cries for both natural discomfort and natural pain cries ($\beta$ = 0.29, SE = 0.06, z
(1920) = 5.03, *p* < 0.001, Table S8 and Fig. 4). The baby's real sex (β = 0.07, SE = 0.06, z(1920) = 1.21, *p* = 0.23), the listener's sex (β = 0.07, SE = 0.11, z(1920) = 0.07, *p* = 0.95) and group (β = −0.02, SE = 0.11, z (1920) = −0.18, *p* = 0.86) did not predict perceived distress (Table S8).

4. Discussion

The key aim of this study, by comparing acoustic analyses of babies'
cries and results of psychoacoustic experiments to data obtained from
western countries (Koutseff et al., 2018; Reby et al., 2016), was to assess
whether the acoustic form of babies' cries and their perception by adults
are preserved across diverse cultures. First, our results reveal no major
differences between Congolese and European populations in the
acoustic structure of babies' cries, showing a lack of sexual dimorphism
and a lack of reliable pitch cues to distress. Second, we show that the
ability of adult listeners to discriminate between broad levels of distress
encoded in babies' cries, namely in nonlinear acoustic phenomena, is
likewise cross-culturally preserved. Third, we show that similar
perceptual biases and sex stereotypes affect adult listeners' in-
terpretations of babies' cries in two radically different sociocultural
environments, supporting the cross-cultural generalisability of these
cognitive biases.

Distress vocalisations produced by many taxonomically and ecologically diverse mammalian species share critical acoustic patterns,

selected to communicate distress (Hadjistavropoulos & Craig, 2002; Lingle, Wyman, Kotrba, Teichroeb, & Romanow, 2012). In turn, listeners' sensitivity to this acoustic structure appears to be broadly shared across diverse species (Custance & Mayer, 2012; Lingle & Riede, 2014; McComb, Taylor, Wilson, & Charlton, 2009; Tallet, Špinka, Maruscakovà, & Simecek, 2010; Tallet et al., 2013 but more contrasted in Kelly et al., 2017). It is therefore not surprising that our detailed acoustic analyses, like previous studies on human infant cries (Facchini et al., 2005; Koutseff et al., 2018; Leger et al., 1996; Tiezzi et al., 2004), human adult volitional pain vocalisations (Raine et al., 2018), or non-human mammalian vocalisations (Jovanovic & Gouzoules, 2001; Levine, Johnson, & Gonzalez, 1985; Stoeger, Charlton, Kratochvil, & Fitch, 2011), show that an increase in ostensible distress level is accompanied by higher levels of nonlinear acoustic phenomena. This is due to irregular or chaotic vocal fold vibration that in turn causes the vocal signal to sound perceptually rough (Fitch et al., 2002; Jiang, Zhang, & Stern, 2001). Nonlinearities in babies' cries have been shown to be dynamic and to change along a continuum that reflects the baby's distress-related arousal, and so could potentially inform parents about the offspring's level of instant need (Koutseff et al., 2018).

We show that Congolese mothers and fathers reliably distinguish distress levels encoded in babies' cries, and yet, biases affect their perception of the acoustic structure of the cry and thus their perception of distress intensity. Indeed, despite the absence of reliable cues to arousal in cry pitch (this study, Koutseff et al., 2018; but see Boero, Bianchi, Volpe, Marcello, & Lenti, 1998), experimentally increasing this highly salient acoustic dimension significantly increased perceived distress levels. In line with this result, other studies on 'WEIRD' populations have found that relatively higher-pitched cries are generally judged as expressing more discomfort or distress (Dessureau, Olson, & Thompson, 1998; Reby et al., 2016) and as more painful or urgent (Craig, Grunau, & Aquan-Assee, 1988; Dessureau et al., 1998; Porter, Miller, & Marshall, 1986; Zeskind & Collins, 1987; but more contrasted in Zeifman, 2004). Such pitch biases also hold true in perceptions of pain from human adult vocalisations (Raine et al., 2018). Notably, while pitch parameters do not correlate linearly with actual distress levels in baby cries, very high-pitched crying is associated with chronic and severe pathology (Frodi & Senchak, 1990; Lester, Boukydis, Garcia-Coll, Hole, & Peucker, 1992; Zeskind & Lester, 1978) or extreme distress when an 'alarm' threshold of pain is reached (Bellieni et al., 2004). Baby cries characterised by an abnormally high pitch are indeed also perceived as more urgent, aversive, grating, sick, distressing, piercing, discomforting, distracting and arousing compared to cries produced by new-borns within a normal pitch range (Frodi & Senchak, 1990; B. M. Lester et al., 1992; Zeskind & Lester, 1978).

In many western cultures, pre-conceived gender-based expectations and sex-typed behaviours toward sons or daughters are evident immediately after birth. Indeed, a baby's biological sex affects adult's perceptions of the infants physical and behavioural traits (Lambert, Yackley, & Hein, 1971; Rubin, Provenzano, & Luria, 1974) and predicts their responses to solicitation (Cherry & Lewis, 1976; Condry, Condry, & Pogatshnik, 1983; Lewis & Weinraub, 1979). In line with these early sociopsychological studies, our results also highlight early-appearing parental expectations concerning sex-specific differences in a biological signal: the cry. Indeed, although we manipulated only the pitch of the cry, preserving all other acoustic characteristics (e.g., duration, amplitude, or nonlinear phenomena), this targeted modification significantly affected the sex attributed to a baby by adult listeners. We show that Congolese parents, like European parents (Reby et al., 2016), are more likely to attribute higher pitched cries to girls, and lower pitched cries to boys.

In contrast to these perceptual biases, we did not find any acoustic
sex signature in babies' cries, including in pitch parameters. This cor-
roborates a large body of research showing that sexual dimorphism in
human voice pitch does not arise until puberty (Fuller & Horii, 1986;
Murry, Amundson, & Hollien, 1977; Reby et al., 2016) when a surge of

<figure><img src="image_8.png" /><figcaption>**Fig. 4.** Effect of baby's assigned sex on perceived distress by adult listeners' (30 fathers and 30 mothers; Playback experiment 3). Listeners rate the same cries as expressing more distress when perceived as having been produced by a baby boy than a girl, for both discomfort and pain cries.</figcaption></figure>
testosterone enlarges the male vocal folds and causes the voice pitch of males to drop nearly one octave lower than females (e.g., Harries et al., 1997). This lack of a reliable sex signature in the pitch of pre-pubertal individuals may explain why adult listeners cannot reliably discriminate the sex of an infant based on its cry (our study, Murry, Hollien, & Müller, 1975; Reby et al., 2016). Emphasising the importance of sex stereotypes, Reby et al. (2016) argue that adult listeners may erroneously generalise sex differences in the pitch of adult men's and women's voices to prepubertal individuals, where the relationships no longer hold, following other accounts of such pitch 'mis-attribution biases' (see e.g., Rendall, Vokey, & Nemeth, 2007).

Interestingly, beyond pitch, the majority of participants reported that they perceived loudness as the most important acoustic parameter for differentiating between boys' and girls' crying. Due to methodological constraints in standardising recording conditions, especially in the field, most studies conducted on babies' cries (including this study) have traditionally controlled for loudness in favor of spectral and temporal characteristics, not allowing for tests of its potential predictive power nor effects on listeners' judgments. However, this acoustic parameter is clearly essential for a full understanding of the information encoded in cries and represents an important acoustic parameter for further research in nonverbal vocal communication.

Reby et al. (2016) further show that perceived sex affects European adults' expectations of the level of negative arousal experienced by an infant: infants perceived to be male (regardless of their true biological sex) are judged as experiencing more discomfort than are infants perceived to be female, in cries experimentally manipulated to be higher pitched. Yet, the evidence of real sex differences in negative arousal are mixed. Some studies report that human female neonates are relatively more sensitive to painful stimuli (Bell & Costello, 1964; Guinsburg et al., 2000) but other studies have failed to replicate this finding (Owens & Todt, 1984; Stevens, Johnston, & Horton, 1994). Some studies also show that female infants cry longer following a pain stimulation than do male infants (Grunau & Craig, 1987; but see, Stevens et al., 1994), however, here again, this result is mixed (Fuller, 2002). Despite the lack of robust evidence for sex differences in pain responses, by randomly assigning a gender to each natural cry in a counter-balanced experimental design, here we found that Congolese mothers and fathers' judgments were significantly affected by the assigned (perceived) sex of the baby. Indeed, when listeners thought that the cry came from a boy, they rated both discomfort and pain cries as higher in distress than when they thought the same cry came from a girl. Interestingly, this result might reflect a cognitive double-bias. If listeners expect baby boys to cry with a lower pitch than girls (even though they do not), then a high-pitched cry might be perceived as comparatively even more high-pitched relative to its expected baseline when it is thought to have been produced by a boy, and thus as relatively more distressed.

Such perceptual sex biases can have real-life implications. They suggest that caregivers, regardless of their cultural background, may overestimate the distress encoded in boys' cries while underestimating distress levels expressed in girls' cries. Such gender biases could interfere with crucial dimensions of parental care, such as caregivers' assessment of babies' needs, and so may have a tangible impact on care provision.

## 5. Conclusion

Our results highlight cross-cultural preservation in the information encoded in babies' cries, in particular form-function relationships between cry structure and distress levels, and the factors driving the perception of this biologically relevant information by adult listeners. Despite the ability to decode crucial information such as the ostensible level of distress or pain, our playback experiments illustrate the powerful impact of perceptual biases on adult listeners' assessments of babies' cries. The present study expands our understanding of the potentially evolved perceptual mechanisms underlying parental assessments of babies' needs across diverse populations, and open an

important avenue for continued cross-cultural research testing critical questions about the evolution of human vocal behaviour.

## Funding

This work was financially supported by a research grant from the French National Research Agency (BABYCRY ANR-19-CE28-0014-01) to NM, the University of Lyon IDEXLYON grant as part of the 'Programme Investissements d'Avenir' (ANR-16-IDEX-0005) to DR, the program IDEXLYON (ANR-16-IDEX-0005) to FL, the Institut Universitaire de France (NM), and the University of Saint-Etienne.

## Authors' contributions

C. Cornec, F. Levréro, K. Pisanski, D. Reby and N. Mathevon conceived, designed and coordinated the study. F. Levréro, D. Reby and N. Mathevon allocated research funding. C. Cornec and E. Don collected data. C. Cornec and V. Planas-Bielsa carried out the statistical analyses and interpreted the data. C. Cornec, F. Levréro, K. Pisanski, D. Reby and N. Mathevon drafted the manuscript. C. Monghiemo and B. Bola supported the study implementation in the Bolobo Territory. All authors gave final approval for publication and agree to be held accountable for the work performed therein.

## Declaration of Competing Interest

The authors declare no competing interests.

## Data availability

The data associated with this research are available at https://doi.org/10.5061/dryad.m37pvmd5r.

## Acknowledgments

We are grateful to the NGO Mbou Mon-Tour for arranging logistical support in Kinshasa and Congolese villages, facilitating contact with persons in charge of dispensaries and access to the medical units scheduling vaccinations in various remote villages with which communication would otherwise be difficult. Lastly, we are extremely grateful to all the inhabitants of these villages and their chief for their warm welcome, kind assistance and patience during our visit.

## Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.evolhumbehav.2023.08.004.

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