Matthew R. Heintz

Facial expression categorization by chimpanzees using standardized stimuli

The ability to recognize and accurately interpret facial expressions are critical social cognition skills in primates, yet very few studies have examined how primates discriminate these social signals and which features are the most salient. Four experiments examined chimpanzee facial expression processing using a set of standardized, prototypical stimuli created using the new ChimpFACS coding system. First, chimpanzees were found to accurately discriminate between these expressions using a computerized matching-to-sample task, and recognition was impaired for all but one expression category when they were inverted. Third, a multidimensional scaling analysis examined the perceived dissimilarity among these facial expressions revealing 2 main dimensions, the degree of mouth closure and extent of lip-puckering and retraction. Finally, subjects were asked to match each facial expression category using only individual component features. For each expression category, at least 1 component movement was more salient or representative of that expression than the others. However, these were not necessarily the only movements implicated in subjects overall pattern of errors. Therefore, similar to humans, both configuration and component movements are important during chimpanzee facial expression processing.

Validation of a cortisol enzyme immunoassay and characterization of salivary cortisol circadian rhythm in chimpanzees (Pan troglodytes).

Monitoring concentrations of stress hormones is an important tool for behavioral research and conservation for animals both in the wild and captivity. Glucocorticoids can be measured in mammals as an indicator of stress by analyzing blood, feces, urine, hair, feathers, or saliva. The advantages of using saliva for measuring cortisol concentrations are three‐fold: it is minimally invasive, multiple samples can be collected from the same individual in a short timeframe, and cortisol has a relatively short response time in saliva as compared with other materials. The purpose of this study was to: (1) conduct an adrenocorticotropic hormone (ACTH) challenge as a physiological validation for an enzyme immunoassay to measure salivary cortisol in chimpanzees and (2) characterize the circadian rhythm of salivary cortisol in chimpanzees. We determined that salivary cortisol concentrations peaked 45 min following the ACTH challenge, which is similar to humans. Also, salivary cortisol concentrations peaked early in the morning and decreased throughout the day. We recommend that saliva collection may be the most effective method of measuring stress reactivity and has the potential to complement behavioral, cognitive, physiological, and welfare studies. Am. J. Primatol. 73:903–908, 2011.

Boys will be boys: sex differences in wild infant chimpanzee social interactions

Sex differences in the behaviour of human children are a hotly debated and often controversial topic. However, several recent studies have documented a biological basis to key aspects of child social behaviour. To further explore the evolutionary basis of such differences, we investigated sex differences in sociability in wild chimpanzee, Pan troglodytes schweinfurthii, infants at Gombe National Park, Tanzania. We used a long-term data set on mother-infant behaviour to analyse the diversity of infant chimpanzee social partners from age 30 to 36 months. Male infants (N = 12) interacted with significantly more individuals than female infants did (N = 8), even when maternal sociability was controlled for. Furthermore, male infants interacted with significantly more adult males than female infants did. Our data indicate that the well-documented sex differences in adult chimpanzee social tendencies begin to appear quite early in development. Furthermore, these data suggest that the behavioural sex differences of human children are fundamentally rooted in our biological and evolutionary heritage.

Facial expression recognition in rhesus monkeys, Macaca mulatta

The ability to recognize and accurately interpret facial expressions is critically important for nonhuman primates that rely on these nonverbal signals for social communication. Despite this, little is known about how nonhuman primates, particularly monkeys, discriminate between facial expressions. In the present study, seven rhesus monkeys were required to discriminate four categories of conspecific facial expressions using a matching-to-sample task. In experiment 1, the matching pair showed identical photographs of facial expressions, paired with every other expression type as the nonmatch. The identity of the nonmatching stimulus monkey differed from the one in the sample. Subjects performed above chance on session 1, with no difference in performance across the four expression types. In experiment 2, the identity of all three monkeys differed in each trial, and a neutral portrait was also included as the nonmatching stimulus. Monkeys discriminated expressions across individual identity when the non-match was a neutral stimulus, but they had difficulty when the nonmatch was another expression type. We analysed the degree to which specific feature redundancy could account for these error patterns using a multidimensional scaling analysis which plotted the perceived dissimilarity between expression dyads along a two-dimensional axis. One axis appeared to represent mouth shape, stretched open versus funnelled, while the other appeared to represent a combination of lip retraction and mouth opening. These features alone, however, could not account for overall performance and suggest that monkeys do not rely solely on distinctive features to discriminate among different expressions.

Sex Differences in Wild Chimpanzee Behavior Emerge during Infancy

The role of biological and social influences on sex differences in human child development is a persistent topic of discussion and debate. Given their many similarities to humans, chimpanzees are an important study species for understanding the biological and evolutionary roots of sex differences in human development. In this study, we present the most detailed analyses of wild chimpanzee infant development to date, encompassing data from 40 infants from the long-term study of chimpanzees at Gombe National Park, Tanzania. Our goal was to characterize age-related changes, from birth to five years of age, in the percent of observation time spent performing behaviors that represent important benchmarks in nutritional, motor, and social development, and to determine whether and in which behaviors sex differences occur. Sex differences were found for indicators of social behavior, motor development and spatial independence with males being more physically precocious and peaking in play earlier than females. These results demonstrate early sex differentiation that may reflect adult reproductive strategies. Our findings also resemble those found in humans, which suggests that biologically-based sex differences may have been present in the common ancestor and operated independently from the influences of modern sex-biased parental behavior and gender socialization.

Validation of a field technique and characterization of fecal glucocorticoid metabolite analysis in wild chimpanzees (Pan troglodytes).

Monitoring adrenocortical activity in wild primate populations is critical, given the well‐documented relationship between stress, health, and reproduction. Although many primate studies have quantified fecal glucocorticoid metabolite (FGM) concentrations, it is imperative that researchers validate their method for each species. Here, we describe and validate a technique for field extraction and storage of FGMs in wild chimpanzees (Pan troglodytes). Our method circumvents many of the logistical challenges associated with field studies while yielding similar results to a commonly used laboratory method. We further validate that our method accurately reflects stress physiology using an adrenocorticotropic hormone challenge in a captive chimpanzee and an FGM peak at parturition in a wild subject. Finally, we quantify circadian patterns for FGMs for the first time in this species. Understanding these patterns may allow researchers to directly link specific events with the stress response. Am. J. Primatol. 75:57‐64, 2013.

The perception of unfamiliar faces and houses by chimpanzees : Influence of rotation angle

The inversion effect, or impaired recognition of upside-down faces, is used as evidence supporting the configural processing of faces. Human studies report a linear relationship between face-discrimination performance and orientation, such that recognition is more difficult as faces are rotated away from their typical viewpoint. Previous studies on chimpanzees also support a configural bias for processing faces, particularly faces for which subjects have developed expertise. In the present study, we examined the influence of expertise and rotation angle on the visual perception of faces in chimpanzees. Six subjects were presented with unaltered and blurred conspecific faces and houses in five orientation angles. A computerized paradigm was used to further delineate the nature of configural face processing in this species. The data were consistent with those reported in humans: chimpanzees showed a significant linear impairment when discriminating conspecific faces as they rotated away from their upright orientation. No inversion effect was observed for discriminations involving houses. Thus, chimpanzees, like humans, show a face-specific inversion effect that is linearly affected by angle of orientation, suggesting that their visual processing of faces is strongly influenced by the extraction of configural cues and closely resembles the perceptual strategies of humans.

Discrimination of faces and houses by rhesus monkeys: the role of stimulus expertise and rotation angle

The face inversion effect, or impaired recognition of upside down compared to upright faces, is used as a marker for the configural processing of faces in primates. The inversion effect in humans and chimpanzees is strongest for categories of stimuli for which subjects have considerable expertise, primarily conspecifics’ faces. Moreover, discrimination performance decreases linearly as faces are incrementally rotated from upright to inverted. This suggests that rotated faces must be transformed, or normalized back into their most typical viewpoint before configural processing can ensue, and the greater the required normalization, the greater the likelihood of errors resulting. Previous studies in our lab have demonstrated a general face inversion effect in rhesus monkeys that was not influenced by expertise. Therefore, the present study examined the influence of rotation angle on the visual perception of face and nonface stimuli that varied in their level of expertise to further delineate the processes underlying the inversion effect in rhesus monkeys. Five subjects discriminated images in five orientation angles. Results showed significant linear impairments for all stimulus categories, including houses. However, compared to the upright images, only rhesus faces resulted in worse performance at rotation angles greater than 45°, suggesting stronger configural processing for stimuli for which subjects had the greatest expertise.

Maternal effects on offspring stress physiology in wild chimpanzees

Early life experiences are known to influence hypothalamic‐pituitary‐adrenal (HPA) axis development, which can impact health outcomes through the individuals ability to mount appropriate physiological reactions to stressors. In primates, these early experiences are most often mediated through the mother and can include the physiological environment experienced during gestation. Here, we investigate stress physiology of dependent offspring in wild chimpanzees for the first time and examine whether differences in maternal stress physiology are related to differences in offspring stress physiology. Specifically, we explore the relationship between maternal rank and maternal fecal glucocorticoid metabolite (FGM) concentration during pregnancy and early lactation (first 6 months post‐partum) and examine whether differences based on maternal rank are associated with dependent offspring FGM concentrations. We found that low‐ranking females exhibited significantly higher FGM concentrations during pregnancy than during the first 6 months of lactation. Furthermore, during pregnancy, low‐ranking females experienced significantly higher FGM concentrations than high‐ranking females. As for dependent offspring, we found that male offspring of low‐ranking mothers experienced stronger decreases in FGM concentrations as they aged compared to males with high‐ranking mothers or their dependent female counterparts. Together, these results suggest that maternal rank and FGM concentrations experienced during gestation are related to offspring stress physiology and that this relationship is particularly pronounced in males compared to females. Importantly, this study provides the first evidence for maternal effects on the development of offspring HPA function in wild chimpanzees, which likely relates to subsequent health and fitness outcomes. Am. J. Primatol. 80:e22525, 2018.

Maternal Behavior and Physiological Stress Levels in Wild Chimpanzees (Pan troglodytes schweinfurthii)

Individual differences in maternal behavior toward, and investment in, offspring can have lasting consequences, particularly among primate taxa characterized by prolonged periods of development over which mothers can exert substantial influence. Given the role of the neuroendocrine system in the expression of behavior, researchers are increasingly interested in understanding the hormonal correlates of maternal behavior. Here, we examined the relationship between maternal behavior and physiological stress levels, as quantified by fecal glucocorticoid metabolite (FGM) concentrations, in lactating chimpanzees, Pan troglodytes schweinfurthii, at Gombe National Park, Tanzania. After accounting for temporal variation in FGM concentrations, we found that mothers interacted socially (groomed and played) with and nursed their infants more on days when FGM concentrations were elevated compared to days when FGM concentrations were within the range expected given the time of year. However, the proportion of time mothers and infants spent in contact did not differ based on FGM concentrations. These results generally agree with the suggestion that elevated GC concentrations are related to maternal motivation and responsivity to infant cues and are the first evidence of a hormonal correlate of maternal behavior in a wild great ape.