Processing of novel food reveals payoff and rank-biased social learning in a wild primate.

Social learning-learning from others-is the basis for behavioural traditions. Different social learning strategies (SLS), where individuals biasedly learn behaviours based on their content or who demonstrates them, may increase an individual's fitness and generate behavioural traditions. While SLS have been mostly studied in isolation, their interaction and the interplay between individual and social learning is less understood. We performed a field-based open diffusion experiment in a wild primate. We provided two groups of vervet monkeys with a novel food, unshelled peanuts, and documented how three different peanut opening techniques spread within the groups. We analysed data using hierarchical Bayesian dynamic learning models that explore the integration of multiple SLS with individual learning. We (1) report evidence of social learning compared to strictly individual learning, (2) show that vervets preferentially socially learn the technique that yields the highest observed payoff and (3) also bias attention toward individuals of higher rank. This shows that behavioural preferences can arise when individuals integrate social information about the efficiency of a behaviour alongside cues related to the rank of a demonstrator. When these preferences converge to the same behaviour in a group, they may result in stable behavioural traditions.

Social contact behaviors are associated with infection status for Trichuris sp. in wild vervet monkeys (Chlorocebus pygerythrus).

Social grooming in the animal kingdom is common and serves several functions, from removing ectoparasites to maintaining social bonds between conspecifics. We examined whether time spent grooming with others in a highly social mammal species was associated with infection status for gastrointestinal parasites. Of six parasites detected, one (Trichuris sp.) was associated with social grooming behaviors, but more specifically with direct physical contact with others. Individuals infected with Trichuris sp. spent significantly less time grooming conspecifics than those not infected, and time in direct contact with others was the major predictor of infection status. One model correctly predicted infection status for Trichuris sp. with a reliability of 95.17% overall when the variables used were time spent in direct contact and time spent grooming others. This decrease in time spent grooming and interacting with others is likely a sickness behavior displayed by individuals with less energy or motivation for non-essential behaviors. This study emphasizes the possible links between host behavior and parasitic infections and highlights the need for an understanding of a study population's parasitic infections when attempting to interpret animal behavior.

Comparison of Direct and Indirect Methods of Measuring Arterial Blood Pressure in Healthy, Anesthetized African Green Monkeys (Chlorocebus aethiops).

Quantitative blood pressure measurement is a critical parameter for assessing cardiovascular health, monitoring physiologic status under anesthesia, and making clinical decisions. The placement of an arterial catheter is the most accurate way to measure blood pressure, but is invasive and perhaps uncomfortable for the patient, requires sedation or anesthesia, and is technically challenging for staff. Noninvasive devices and methods, including oscillometry, high-definition oscillometry, and Doppler flow can be used to measure blood pressure. However, the American College of Veterinary Internal Medicine guidelines state that blood pressure should be measured using devices that have been validated in the species of interest and under the circumstances in which the measurement is being made. The alternatives listed above have not been validated in this manner. The objective of this study was to compare indirect ultrasonic Doppler flow detection and oscillometric blood pressure measures with direct arterial measurement in 8 healthy, anesthetized African green monkeys using the methods of Bland-Altman to assess agreement. Our results indicated that neither Doppler flow nor oscillometry consistently estimates direct blood pressure measurements in anesthetized African green monkeys. In 6 female monkeys, which weighed less than the 2 male subjects, the indirect Doppler measurement more closely predicted direct mean arterial pressure, indicating Dop- pler flow may be useful for monitoring mean arterial pressure in small patients.

The consistency of individual centrality across time and networks in wild vervet monkeys.

Previous primate social network studies largely limited their focus to grooming and/or aggression networks, particularly among adult females. In addition, the consistency of individuals' network centrality across time and/or different networks has received little attention, despite this being critical for a global understanding of dynamic social structure. Here, we analyzed the grooming, aggression, and play social networks of a group of 26-28 wild vervet monkeys (Chlorocebus pygerythrus), including adults and juveniles, over two periods of 6 months. We collected data on grooming, play, and aggression using focal animal sampling with instantaneous recording and ad libitum sampling. We examined whether individuals' network centralities were consistent over the two periods and across networks, as well as the effect of age, sex, and dominance rank on three individual centrality metrics in each network and within each study period. We found that individuals were quite consistent in their network position from 1 year to the next despite changes in group composition. However, their network centralities were not correlated across networks, except for Strength and weighted Eigenvector centrality between grooming and aggression networks. We also found that in the aggression network, high-rankers showed the highest centrality in most network metrics (e.g., Degree, Strength, and Eigenvector centrality) and compared to males, females were most central in 2017 but not in 2018. In the grooming network, high-ranking females had the highest Eigenvector centrality, whereas in the play network, juvenile males had the highest Eigenvector centrality. Our findings corroborate previous findings on vervet monkeys. In addition, they show that individuals' network centralities may vary among networks and over time; thus highlighting the effect of sociodemographics and behaviors' functions on the group level dynamics of social behavior.

Field data confirm the ability of a biophysical model to predict wild primate body temperature.

In the face of climate change there is an urgent need to understand how animal performance is affected by environmental conditions. Biophysical models that use principles of heat and mass transfer can be used to explore how an animal's morphology, physiology, and behavior interact with its environment in terms of energy, mass and water balances to affect fitness and performance. We used Niche Mapper™ (NM) to build a vervet monkey (Chlorocebus pygerythrus) biophysical model and tested the model's ability to predict core body temperature (Tb) variation and thermal stress against Tb and behavioral data collected from wild vervets in South Africa. The mean observed Tb in both males and females was within 0.5 °C of NM's predicted Tbs for 91% of hours over the five-year study period. This is the first time that NM's Tb predictions have been validated against field data from a wild endotherm. Overall, these results provide confidence that NM can accurately predict thermal stress and can be used to provide insight into the thermoregulatory consequences of morphological (e.g., body size, shape, fur depth), physiological (e.g. Tb plasticity) and behavioral (e.g., huddling, resting, shade seeking) adaptations. Such an approach allows users to test hypotheses about how animals adapt to thermoregulatory challenges and make informed predictions about potential responses to environmental change such as climate change or habitat conversion. Importantly, NM's animal submodel is a general model that can be adapted to other species, requiring only basic information on an animal's morphology, physiology and behavior.

Infrared thermography cannot be used to approximate core body temperature in wild primates.

Understanding the physiological processes that underpin primate performance is key if we are to assess how a primate might respond when navigating new and changing environments. Given the connection between a mammal's ability to thermoregulate and the changing demands of its thermal environment, increasing attention is being devoted to the study of thermoregulatory processes as a means to assess primate performance. Infrared thermography can be used to record the body surface temperatures of free-ranging animals. However, some uncertainty remains as to how these measurements can be used to approximate core body temperature. Here, we use data collected from wild vervet monkeys (Chlorocebus pygerythrus) to examine the relationship between infrared body surface temperature, core body (intra-abdominal) temperature, and local climate, to determine to what extent surface temperatures reflect core body temperature. While we report a positive association between surface and core body temperature-a finding that has previously been used to justify the use of surface temperature measurements as a proxy for core temperature regulation-when we controlled for the effect of the local climate in our analyses, this relationship was no longer observed. That is, body surface temperatures were solely predicted by local climate, and not core body temperatures, suggesting that surface temperatures tell us more about the environment a primate is in, and less about the thermal status of its body core in that environment. Despite the advantages of a noninvasive means to detect and record animal temperatures, infrared thermography alone cannot be used to approximate core body temperature in wild primates.

Anatomy of nerve fiber bundles at micrometer-resolution in the vervet monkey visual system.

Although the primate visual system has been extensively studied, detailed spatial organization of white matter fiber tracts carrying visual information between areas has not been fully established. This is mainly due to the large gap between tracer studies and diffusion-weighted MRI studies, which focus on specific axonal connections and macroscale organization of fiber tracts, respectively. Here we used 3D polarization light imaging (3D-PLI), which enables direct visualization of fiber tracts at micrometer resolution, to identify and visualize fiber tracts of the visual system, such as stratum sagittale, inferior longitudinal fascicle, vertical occipital fascicle, tapetum and dorsal occipital bundle in vervet monkey brains. Moreover, 3D-PLI data provide detailed information on cortical projections of these tracts, distinction between neighboring tracts, and novel short-range pathways. This work provides essential information for interpretation of functional and diffusion-weighted MRI data, as well as revision of wiring diagrams based upon observations in the vervet visual system.

Reactions to infant death by wild vervet monkeys (Chlorocebus pygerythrus) in KwaZulu-Natal, South Africa: prolonged carrying, non-mother carrying, and partial maternal cannibalism.

Observations of dead infant carrying have been reported for many primate species, and researchers have proposed several hypotheses to explain this behaviour. However, despite being a relatively well-studied species, reports of dead infant carrying in wild vervet monkeys (Chlorocebus pygerythrus) remain scarce. Here we report 14 observations of dead infant carrying by female vervet monkeys in a population at Mawana Game Reserve, KwaZulu-Natal, South Africa. Most of the females carried the dead infant for a day or less, but one female carried her infant for at least 14 days. In one case the maternal sister of a dead infant carried it after the death of their mother. We also report a case of mother-infant cannibalism: a female consumed part of her deceased infant's tail. Other post-mortem care-taking behaviours such as grooming, smelling and licking were also recorded. Of 97 recorded infant deaths in this study population since 2010, 14.4% are known to have elicited dead infant carrying, a proportion similar to that reported for other monkey species. We discuss our observations in relation to various hypotheses about this behaviour, including the post-parturition hormones hypothesis, learning to mother hypothesis, and unawareness of death hypothesis.

Arl4D-EB1 interaction promotes centrosomal recruitment of EB1 and microtubule growth.

ADP-ribosylation factor (Arf)-like 4D (Arl4D), one of the Arf-like small GTPases, functions in the regulation of cell morphology, cell migration, and actin cytoskeleton remodeling. End-binding 1 (EB1) is a microtubule (MT) plus-end tracking protein that preferentially localizes at the tips of the plus ends of growing MTs and at the centrosome. EB1 depletion results in many centrosome-related defects. Here, we report that Arl4D promotes the recruitment of EB1 to the centrosome and regulates MT nucleation. We first showed that Arl4D interacts with EB1 in a GTP-dependent manner. This interaction is dependent on the C-terminal EB homology region of EB1 and partially dependent on an SxLP motif of Arl4D. We found that Arl4D colocalized with γ-tubulin in centrosomes and the depletion of Arl4D resulted in a centrosomal MT nucleation defect. We further demonstrated that abolishing Arl4D-EB1 interaction decreased MT nucleation rate and diminished the centrosomal recruitment of EB1 without affecting MT growth rate. In addition, Arl4D binding to EB1 increased the association between the p150 subunit of dynactin and the EB1, which is important for MT stabilization. Together, our results indicate that Arl4D modulates MT nucleation through regulation of the EB1-p150 association at the centrosome.

The effects of data collection and observation methods on uncertainty of social networks in wild primates.

In social species, network centralities of group members shape social transmission and other social phenomena. Different factors have been found to influence the measurement of social networks, such as data collection and observation methods. In this study, we collected data on adults and juveniles and examined the effect of data collection method (ad libitum sampling vs. focal animal sampling) and observation method (interaction-grooming; play-vs. association-arm-length; 2 m; 5 m proximities-) on social networks in wild vervet monkeys. First, we showed using a bootstrapping method, that uncertainty of ad libitum grooming and play matrices were lesser than uncertainty of focal matrices. Nevertheless, grooming and play networks constructed from ad libitum and focal animal sampling were very similar and highly correlated. We improved the certainty of both grooming and play networks by pooling focal and ad libitum matrices. Second, we reported a high correlation between the proximity arm-length network and the focal grooming one making an arm-length proximity network a reasonable proxy for a grooming one in vervet monkeys. However, we did not find such a correlation between proximity networks and the play one. Studying the effects of methodological issues as data collection and observation methods can help improve understanding of what shapes social networks and which data collection method to choose to study sociality.

Keeping cool in the heat: Behavioral thermoregulation and body temperature patterns in wild vervet monkeys.

OBJECTIVES: Climate change is having a significant impact on biodiversity and increasing attention is therefore being devoted to identifying the behavioral strategies that a species uses to cope with climatic stress. We explore how wild vervet monkeys (Chlorocebus pygerythrus) respond to heat stress, and how behavioral adaptations are used to regulate body temperature. MATERIALS AND METHODS: We implanted wild vervet monkeys with temperature-sensitive data loggers and related the body temperature rhythms of these animals to their use of thermoregulatory behaviors. RESULTS: Environmental temperature had a positive effect on the mean, minima and maxima of daily body temperatures. Environmental temperature had a positive effect on the amount of time that vervet monkeys spent in the shade, and animals that spent more time in the shade had lower body temperature maxima. Drinking water did not have a proximate effect on body temperature, most likely a consequence of their regular access to drinking water. Body temperatures were observed to decrease after swimming events, but tended to return to pre-swim temperatures within 1 hr, suggesting a limited thermal benefit of this behavior. CONCLUSIONS: Our data support the view that vervet monkeys cope well in the heat, and use behavior as a means to aid thermoregulation. The ability of primates to be flexible in their use of thermoregulatory behaviors can contribute positively to their capacity to cope with environmental variability. However, given its broad effect on plant productivity and habitat loss, climate change is a major threat to species' biogeographical distribution and survival.

Playing it safe? Solitary vervet monkeys (Chlorocebus pygerythrus) choose high-quality foods more than those in competition.

An important goal in foraging ecology is to determine how biotic and abiotic variables impact the foraging decisions of wild animals and how they move throughout their multidimensional landscape. However, the interaction of food quality and feeding competition on foraging decisions is largely unknown. Here we examine the importance of food quality in a patch on the foraging decisions of wild vervet monkeys (Chlorocebus pygerythrus) at Lake Nabugabo, Uganda using a multidestination platform array. The overall nutritional composition of the vervet diet was assessed and found to be low in sodium and lipids, thus we conducted a series of experimental manipulations in which the array was varied in salt and oil content. Although vervets prioritized platforms containing key nutrients (i.e., sodium and lipids) overall, we found that solitary vervets prioritized nutrient-dense platforms more strongly than competing vervets. This finding was opposite to those in a similar experiment that manipulated food site quantity, suggesting that large, salient rewards may be worth competing over but slight differences in nutritional density may be only chosen when there are no potentially negative social consequences (i.e., aggression received). We also found that vervets chose platforms baited with oil-only, and oil combined with salt, but not salt-only, suggesting that energy was an important factor in food choice. Our findings demonstrate that when wild vervets detect differences in feeding patches that reflect nutritional composition, they factor these differences into their navigational and foraging decisions. In addition, our findings suggest that these nutritional differences may be considered alongside social variables, ultimately leading to the complex strategies we observed in this study.

Correlates of social role and conflict severity in wild vervet monkey agonistic screams.

Screams are acoustically distinct, high-pitched and high-amplitude calls, produced by many social species. Despite a wide range of production contexts, screams are characterised by an acoustic structure that appears to serve in altering the behaviour of targeted receivers during agonistic encounters. In chimpanzees, this can be achieved by callers producing acoustic variants that correlate with their identity, social role, relationship with the targeted recipient, the composition of the audience and the nature of the event. Although vervet monkeys (Chlorocebus pygerythrus) have been studied for decades, not much is known about their agonistic screams. Here, we examined agonistic screams produced by wild vervet monkeys to investigate the degree to which caller identity, social role and conflict severity affected call structure. We found that screams were both individually distinctive and dependent of the agonistic events. In particular, victim screams were longer and higher-pitched than aggressor screams, while screams produced in severe conflicts (chases, physical contact) had higher entropy than those in mild conflicts. We discuss these findings in terms of their evolutionary significance and suggest that acoustic variation might serve to reduce the aggression level of opponents, while simultaneously attracting potential helpers.

Primates are living links to our past: The contribution of comparative studies with wild vervet monkeys to the field of social cognition.

By studying the behavior of nonhuman primates, particularly in wild settings, researchers have been able to investigate a range of cognitive abilities, shedding light on the evolution of certain aspects of cognition and revealing potential evolutionary precursors of many capacities considered uniquely human. Vervet monkeys (Chlorocebus pygerythrus) have been widely investigated due to their prevalence and their suitability for experimental testing in the wild with an ecologically valid approach that is not possible with many other primates, especially apes. Here we review advances in the understanding of a number of cognitive and behavioral processes that have been gleaned from studies conducted with wild vervet monkeys over the past half century, primarily focusing on social cognitive abilities. We direct our attention to three major areas of study; communication, cooperation and trade, and social learning. We discuss how findings from this species have contributed (and continue to contribute) to our understanding of the evolution of human cognitive capacities and suggest future avenues of research with this species.

Subcutaneous thermal sensor microchip validation in vervet monkeys (Chlorocebus pygerythrus) during normothermic and hypothermic situations.

BACKGROUND: Internal temperature data are essential for clinical evaluation in veterinary medicine. During the last decade, new thermometry devices have been developed. Identification microchips with a temperature sensor offer double utility to clinicians by satisfying animal identification regulations and providing a non-invasive method for temperature measurement. METHODS: During this study, 26 healthy vervet monkeys (Chlorocebus pygerythrus) were implanted with a subcutaneous temperature transponding microchip. For each monkey, internal temperature measurements from the microchip and from an anaesthetic monitor (rectal sensor) were recorded every 5 minutes during an anaesthetic procedure. RESULTS: In this study, there were 83 paired samples obtained under normothermic conditions and another 72 paired samples obtained under hypothermic conditions, with interclass correlation coefficients of 0.79 and 0.69, respectively, between the two temperature measurement approaches. CONCLUSION: Measurements obtained using the examined microchip thermal sensor exhibited good and excellent correlation with rectal temperature measurements under hypothermic and normothermic conditions, respectively.

Natural variation in fetal cortisol exposure is associated with neonatal body mass in captive vervet monkeys (Chlorocebus aethiops).

Poor maternal condition during gestation is commonly associated with impaired fetal growth in humans and other animals. Although elevated maternal glucocorticoids (GCs) are often implicated as the mechanism of intrauterine growth stunting, the direct contribution of maternal GCs remains unclear because enzymatic conversion of GCs at the placenta may limit the ability of maternal hormones to reach the fetus. Further, because previous studies on gestational stress have often employed synthetic GCs, which cross the placenta unobstructed, it remains unknown whether naturalistic endogenous GC elevations will have similar effects. Here, we use an unmanipulated colony of captive vervet monkeys (N = 18 mother-offspring dyads) to examine how maternal condition predicts maternal gestational hormones, and how these in turn predict neonatal body mass, especially in comparison with total prenatal hormone exposure as measured from neonatal hair. We focused on GCs and dehydroepiandrosterone-sulfate (DHEAS), an additional steroid suspected to influence growth. We found that measures of poor maternal condition (low body mass and low parity) were not associated with elevations in maternal GCs or DHEAS. Furthermore, only fetal GC exposure predicted neonatal body mass, while neither maternal GCs, nor maternal or fetal DHEAS, had any effect. Surprisingly, neonates exposed to higher gestational GCs were larger, rather than smaller at birth. Taken together, these results suggest that GC concentrations within a more naturalistic range may be positively rather than negatively associated with neonatal body mass. Further, the effect of maternal gestational GCs on neonatal mass may be modulated by placental control of GC exposure.

Characterization of glucose-stimulated insulin release protocols in african green monkeys (Chlorocebus aethiops).

BACKGROUND: Management of diabetes remains a major health and economic challenge, demanding test systems in which to develop new therapies. These studies assessed different methodologies for determining glucose tolerance in green monkeys. METHODS: Twenty-eight African green monkeys between 4 and 24 years old underwent single or repeat intravenous glucose tolerance testing (IVGTT), oral glucose tolerance testing (OGTT), and/or graded glucose infusion testing. RESULTS: Geriatric monkeys exhibited glucose intolerance with impaired glucose-stimulated insulin secretion following IVGTT. Repeat IVGTT and OGTT assessments were inconsistent. Monkeys with low glucose-stimulated insulin secretion after graded glucose infusion exhibited elevated blood glucose levels. CONCLUSION: IVGTT and graded glucose infusion protocols revealed differences in glucose tolerance among green monkeys at single time points, including age-dependent differences suggestive of shifts in pancreatic beta-cell functional capacity, but care should be applied to study design and the interpretation of data in the setting of longitudinal studies.

Assessment of Male Reproductive Skew via Highly Polymorphic STR Markers in Wild Vervet Monkeys, Chlorocebus pygerythrus.

Male reproductive strategies have been well studied in primate species where the ability of males to monopolize reproductive access is high. Less is known about species where males cannot monopolize mating access. Vervet monkeys (Chlorocebus pygerythrus) are interesting in this regard as female codominance reduces the potential for male monopolization. Under this condition, we assessed whether male dominance rank still influences male mating and reproductive success, by assigning paternities to infants in a population of wild vervets in the Eastern Cape, South Africa. To determine paternity, we established microsatellite markers from noninvasive fecal samples via cross-species amplification. In addition, we evaluated male mating and reproductive success for 3 groups over 4 mating seasons. We identified 21 highly polymorphic microsatellites (number of alleles = 7.5 ± 3.1 [mean ± SD], observed heterozygosity = 0.691 ± 0.138 [mean ± SD]) and assigned paternity to 94 of 97 sampled infants (96.9%) with high confidence. Matings pooled over 4 seasons were significantly skewed across 3 groups, although skew indices were low (B index = 0.023-0.030) and mating success did not correlate with male dominance. Paternities pooled over 4 seasons were not consistently significantly skewed (B index = 0.005-0.062), with high-ranking males siring more offspring than subordinates only in some seasons. We detected 6 cases of extra-group paternity (6.4%) and 4 cases of natal breeding (4.3%). Our results suggest that alternative reproductive strategies besides priority of access for dominant males are likely to affect paternity success, warranting further investigation into the determinants of paternity among species with limited male monopolization potential.

Payoff- and Sex-Biased Social Learning Interact in a Wild Primate Population.

Social learning in animals is now well documented, but few studies have determined the contexts shaping when social learning is deployed. Theoretical studies predict copying of conspecifics gaining higher payoffs [1-4], a bias demonstrated in primates only in captivity [5]. In the wild, research has shown selective attention toward the philopatric sex, a group's stable core [6]. Here, we report the first rigorous experimental test of the existence of a payoff bias in wild primates and its interaction with the sex of the model. We created a payoff bias in which an immigrant alpha male in each of three groups of wild vervet monkeys received five times more food upon opening a foraging box than did the philopatric alpha female, whereas in two control groups, male and female models received the same amount of food. We tested whether this payoff asymmetry would override the previously documented selective learning from resident females. Group members were tested after having watched both models. When both models received the same amount of food, audience members copied the female model significantly more than the male model, confirming previous findings. However, when a marked payoff bias was introduced, male, but not female, vervet monkeys significantly more often copied the male model receiving a higher payoff. These results demonstrate behavioral flexibility in the dispersing sex in these primates and suggest that the philopatric sex can afford to be more conservative in their social learning. Our findings show that multiple social-learning biases can coexist and interact within the same species.

Hepatic Vitamin A Concentrations in Vervets (Chlorocebus aethiops) Supplemented with Carotenoids Derived from Oil Palm.

Commonly used in biomedical research, vervets (Chlorocebus aethiops) are omnivorous but primarily meet their vitamin A requirements from provitamin A carotenoids. Hypervitaminosis A has occurred in vervets that consume feed high in preformed vitamin A. We investigated the vitamin A status of vervets supplemented daily with various antioxidants derived from palm oil. Male vervets (n = 40) were placed for 23 wk on a high-fat diet (34.9% energy) containing 645 µ g retinol activity equivalents (RAE), with 515 µ g RAE from preformed vitamin A. Vervets were randomized to 5 treatments (duration, 20 mo): control; 100 mg d-α-tocopheryl acetate; 100 mg oil palm (Elaeis guineensis)-derived vitamin E; 50 mg oil palm-derived vitamin E + 50 mg carotenoid complex + unrestricted palm-derived water-soluble antioxidants; and 5) unrestricted water-soluble antioxidants. Livers (n = 38) were analyzed for vitamin A, α-retinol (α-vitamin A), and carotenoids. Median hepatic vitamin A and total carotenoid concentrations were 6.49 µ mol/g and 4.30 nmol/g, respectively. Compared with controls, vervets fed the carotenoid complex had higher hepatic vitamin A (11.9 ± 5.1 µ mol/g), α -vitamin A (1.3 ± 0.7 µ mol/g), α -carotene (11.5 ± 5.3 nmol/g), ß-carotene (15.6 ± 8.6 nmol/g), and total carotenoids (28.1 ± 13.9 nmol/g) but lower lutein (0.66 ± 0.28 nmol/g) and zeaxanthin (0.24 ± 0.06 nmol). NHP may benefit from replacement of preformed vitamin A with carotenoids in feeds; however, bioconversion efficiency in these models should be investigated to determine optimal levels.