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 individual's 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. © 2016 Wiley Periodicals, Inc.

Non-invasive quantification of immunoglobulin A in chimpanzees (Pan troglodytes schweinfurthii) at Gombe National Park, Tanzania.

Immunoglobulin A (IgA) is the primary antibody responsible for mucosal defense in mammals and has been used as a marker for chronic stress and immune status. Therefore, this antibody may provide a more reliable indicator of an individual's immunocompetence than is currently available through other methods. Immunoglobulin A has never before been quantified in a wild population of non-human primates using non-invasive sample collection techniques. In this study, we present methodology for non-invasive IgA extraction in the field and provide quantification of mean fecal IgA concentrations in wild chimpanzees (Pan troglodytes schweinfurthii). During the study period (November 2009-October 2010), we collected fecal samples (N = 1463) from 59 individuals at Gombe National Park, Tanzania. We modified a field extraction technique for steroidal hormones to extract IgA from the fecal samples and then quantified mean IgA concentrations (ng/g) using a commercial human IgA enzyme immunoassay. Mean IgA concentration varied among individuals but not by sex or reproductive status. Mature animals tended toward higher mean IgA concentration than immature. Mean IgA concentration differed by quartile season, following a similar pattern previously observed for respiratory illness rates in this population, with the late dry season having significantly higher averages than the late wet. A circadian rhythm was also evident with mean IgA concentrations higher in samples collected in the latter half of the day. These demographic and temporal patterns of IgA concentration provide baseline values necessary to interpret future results, which may be combined with other health values to better understand the role of health and long-term stress in wild great ape populations. Am. J. Primatol. 80:e22558, 2018. © 2016 Wiley Periodicals, Inc.

The relationship between social play and developmental milestones in wild chimpanzees (Pan troglodytes schweinfurthii).

Social play is common among many group-living animals, but the benefits are not well understood. Proposed benefits include increased muscle coordination as the result of increased locomotor versatility and development, and strengthened social bonds through interactions with like-aged individuals. In this study, we used 33 years of long-term behavioral data on infant chimpanzees in Gombe National Park, Tanzania, to examine these potential benefits of social play, specifically how the percentage of time engaged in social play relates to motor and social developmental milestones. We predicted that infants who engaged in more social play would achieve motor and social milestones at younger ages. We found that individuals that spent more time engaging in social play achieved the motor milestones of riding dorsally and traveling independently at earlier ages. Additionally, we found that the amount of play was correlated with earlier ages for reaching the social milestones of spatial independence from mother, first grooming of non-maternal kin, and first observed mating attempt. This is the first study in great apes to demonstrate a relationship between play behavior and developmental milestones, supporting the hypotheses that play provides motor, and social benefits.

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.

The Benefits of Increased Space and Habitat Complexity for the Welfare of Zoo-Housed King Penguins (Aptenodytes patagonicus).

Zoos and aquariums accredited by the Association of Zoos and Aquariums embrace animal welfare as a foundational principle of habitat design. Modern habitats are designed to provide animals with choices and agency over their environment, and to encourage species-appropriate behavior and space use. In 2016, the Detroit Zoological Society opened the Polk Penguin Conservation Center, a 3065.80 m2 facility that features a naturalistic design. The building was designed to optimize animal welfare by incorporating various substrates, nesting sites, and a 1234 kL pool with elements of underwater complexity. The facility houses a mixed-species group of penguins that were previously housed in a smaller habitat that opened in 1968. Between 2015 and 2022, we opportunistically monitored the behavior of ten king penguins (Aptenodytes patagonicus) as they moved back and forth between the two buildings while additional modifications were made to the new habitat. We collected 695 h of behavioral observations and 10,416 h of data from flipper-mounted time-depth recorders. We found that the king penguins spent less time engaged in aggression and more time engaged in swimming and positive social behaviors in the redesigned space. They also spent less time in proximity to other species of penguins and more time alone. These behavioral trends suggest that increased space and environmental complexity had positive welfare benefits for these penguins.

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.

Exploratory Investigation of Infrared Thermography for Measuring Gorilla Emotional Responses to Interactions with Familiar Humans.

Interactions between zoo professionals and animals occur regularly and are believed to be enriching for animals. Little empirical information exists on how animals perceive these interactions, and particularly how the interactions affect the emotional states of animals. Infrared thermography (IRT) has shown some promise in the assessment of emotions in a variety of species, but further research is needed to determine if this method is useful in a zoo setting. We conducted a pilot study to determine if IRT is a valid measure of the emotional responses to routine interactions (positive reinforcement training and cognitive tasks, compared to a control condition) with familiar humans on three western lowland gorillas at the Detroit Zoo. We measured nasal temperatures associated with emotional change using IRT. To examine the validity of the IRT data, we collected saliva samples for hormone analysis before and after each condition, in addition to behavioral data during the interactions and control condition. Decreases in nasal temperatures for two gorillas and an increase in the third indicate that arousal changed consistently within individuals following the interactions but not the control condition. Pre-post cortisol levels and oxytocin concentrations decreased for all conditions, but the decreases seen did not differ among the conditions. The gorillas were highly engaged in the interactions, and two produced more grumble vocalizations during the human-animal interactions (HAIs) compared to the control condition. Additionally, the gorillas performed self-directed behaviors more often during the control condition, also suggesting HAIs were not a negative experience. In summary, we were able to measure changes in arousal using IRT, but we were unable to determine the emotional valence of these changes based on the additional indicators employed. Additionally, the inconsistency across these measures precluded firm conclusions about either the validity of IRT for measuring emotion in this context or how the interactions impacted these gorillas. These findings highlight the challenges of using IRT to measure emotional states in non-human animals, and we discuss further steps necessary to apply this method in future studies.

Case Studies of the Impacts of Cataract Surgery on Crested Penguin Welfare.

As nonhuman animals age, geriatric individuals require additional care and veterinary support to ensure their well being. The focus on lifelong care is a relatively newer approach when providing good welfare, and few studies have examined how veterinary care impacts behavior at different ages or how best to accommodate geriatric individuals in zoos. The objectives of this study were to (a) assess both the immediate and long-term (one year later) behavioral impacts of cataract removal for macaroni (Eudyptes chrysolophus) and southern rockhopper (Eudyptes chrysocome) penguins; (b) compare the behavior of penguins following cataract surgery to that of other conspecifics in the same habitat; and (c) monitor the impacts of cataract surgery on swimming behavior using time-depth recorders. Individual responses to cataract removal differed in direction and magnitude, and these mixed results highlight that welfare is experienced and thus measured at the individual level. Positive responses included increased habitat use, increased time spent swimming, and increased rates of affiliative interactions. This study highlights the importance of assessing welfare impacts of veterinary interventions on geriatric individuals.

Rhesus monkeys (Macaca mulatta) lack expertise in face processing.

Faces are salient stimuli for primates that rely predominantly on visual cues for recognizing conspecifics and maintaining social relationships. While previous studies have shown similar face discrimination processes in chimpanzees and humans, data from monkeys are unclear. Therefore, three studies examined face processing in rhesus monkeys using the face inversion effect, a fractured face task, and an individual recognition task. Unlike chimpanzees and humans, the monkeys showed a general face inversion effect reflected by significantly better performance on upright compared to inverted faces (conspecifics, human and chimpanzees faces) regardless of the subjects' expertise with those categories. Fracturing faces alters first- and second-order configural manipulations whereas previous studies in chimpanzees showed selective deficits for second-order configural manipulations. Finally, when required to individuate conspecific's faces, i.e., matching two different photographs of the same conspecific, monkeys showed poor discrimination and repeated training. These results support evolutionary differences between rhesus monkeys and Hominoids in the importance of configural cues and their ability to individuate conspecifics' faces, suggesting a lack of face expertise in rhesus monkeys.

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 subject's overall pattern of errors. Therefore, similar to humans, both configuration and component movements are important during chimpanzee facial expression processing.

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.

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.

Boy 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.

Rank effects on social stress in lactating chimpanzees.

Given the deleterious consequences associated with chronic stress, individual differences in stress susceptibility can have important fitness implications. These differences may be explained in part by dominance status because high rank is typically associated with decreased aggression and improved nutrition. Here, we examined the relationship between dominance and social stress in lactating chimpanzees, Pan troglodytes schweinfurthii, at Gombe National Park, Tanzania. We did so by pairing daily demographic and behavioural data with faecal glucocorticoid metabolite (FGM) concentrations collected over 37 months. While there was no main effect of rank, interesting differences emerged by adult subgroup size and adult sex ratio (males/females). We found that differences in FGM concentrations between high- and low-ranking females were most pronounced as adult subgroup size and sex ratio increased. Low-ranking females had higher FGM concentrations in larger subgroups and in subgroups biased towards adult males; we observed no comparable change in FGM concentrations amongst high-ranking females. Because low-ranking females were the recipient of significantly more male aggression relative to females of high rank, these patterns may be driven by psychosocial stress in low-ranking females. There was no significant change in diet quality across subgroup sizes; this finding suggests that nutritional stressors were not driving differences in female FGM concentrations. Being susceptible to social stress has important fitness implications as it may constrain low-ranking females from 'choosing' optimal subgroups to take advantage of food resources and/or for the socialization of their offspring.

Visual kin recognition in nonhuman primates: (Pan troglodytes and Macaca mulatta): inbreeding avoidance or male distinctiveness?

Faces provide important information about identity, age, and even kinship. A previous study in chimpanzees reported greater similarity between the faces of mothers and sons compared with mothers and daughters, or unrelated individuals. This was interpreted as an inbreeding avoidance mechanism where females, the dispersing gender, should avoid mating with any male that resembles their mother. Alternatively, male faces may be more distinctive than female faces, biasing attention toward males. To test these hypotheses, chimpanzees and rhesus monkeys matched conspecifics' faces of unfamiliar mothers and fathers with their sons and daughters. Results showed no evidence of male distinctiveness, rather a cross-gender effect was found: chimpanzees were better matching moms with sons and fathers with daughters. Rhesus monkeys, however, showed an overwhelming bias toward male-distinctiveness. They were faster to learn male faces, performed better on father-offspring and parent-son trials, and were best matching fathers with sons. This suggests that for the rhesus monkey, inbreeding avoidance involves something other than facial phenotypic matching but that among chimpanzees, the visual recognition of facial similarities may play an important role.

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.

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 degrees , suggesting stronger configural processing for stimuli for which subjects had the greatest expertise.

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.

Three studies on configural face processing by chimpanzees.

Previous studies have demonstrated the sensitivity of chimpanzees to facial configurations. Three studies further these findings by showing this sensitivity to be specific to second-order relational properties. In humans, this type of configural processing requires prolonged experience and enables subordinate-level discriminations of many individuals. Chimpanzees showed evidence of a composite-like effect for conspecific but not human faces despite extensive experience with humans. Chimpanzee face recognition was impaired only when manipulations targeted second-order properties. Finally, face processing was impaired when individual features were blurred through pixelation. Results confirm that chimpanzee face discrimination, like humans, depends on the integrity of second-order relational properties.