Search

In apes and humans, neutrophil to lymphocyte ratio (NLR) can be used as a predictive indicator of a variety of clinical conditions, longevity, and physiological stress. In chimpanzees specifically, NLR systematically varies with age, rearing, sex, and premature death, indicating that NLR may be a useful diagnostic tool in assessing primate health. To date, just one very recent study has investigated NLR in old world monkeys and found lower NLR in males and nursery-reared individuals, as well as a negative relationship between NLR and disease outcomes. Given that baboons are increasingly used as research models, we aimed to characterize NLR in baboons by providing descriptive data and examinations of baboon NLR heritability, and of the relationships between NLR, age, rearing, and sex in 387 olive baboons (Papio anubis) between 6 months and 19 years of age. We found that (1) mother-reared baboons had higher NLRs than nursery-reared baboons; (2) females had higher NLRs than males; and (3) there was a quadratic relationship between NLR and age, such that middle-aged individuals had the highest NLR values. We also examined NLR as a function of transport to a new facility using a subset of the data. Baboons exhibited significantly higher transport NLRs compared to routine exam NLRs. More specifically, adult baboons had higher transport NLRs than routine NLRs, whereas juveniles showed no such difference, suggesting that younger animals may experience transport stress differently than older animals. We also found that transport NLR was heritable, whereas routine NLR was not, possibly suggesting that stress responses (as indicated in NLR) have a strong genetic component. Consistent with research in humans and chimpanzees, these findings suggest that NLR varies with important biological and life history variables and that NLR may be a useful health biomarker in baboons., (© 2024 Wiley Periodicals LLC.)

The marginal value theorem is an optimal foraging model that predicts how efficient foragers should respond to both their ecological and social environments when foraging in food patches, and it has strongly influenced hypotheses for primate behavior. Nevertheless, experimental tests of the marginal value theorem have been rare in primates and observational studies have provided conflicting support. As a step towards filling this gap, we test whether the foraging decisions of captive chimpanzees (Pan troglodytes) adhere to the assumptions and qualitative predictions of the marginal value theorem. We presented 12 adult chimpanzees with a two-patch foraging environment consisting of both low-quality (i.e., low-food density) and high-quality (i.e., high-food density) patches and examined the effect of patch quality on their search behavior, foraging duration, marginal capture rate, and its proxy measures: giving-up density and giving-up time. Chimpanzees foraged longer in high-quality patches, as predicted. In contrast to predictions, they did not depress high-quality patches as thoroughly as low-quality patches. Furthermore, since chimpanzees searched in a manner that fell between systematic and random, their intake rates did not decline at a steady rate over time, especially in high-quality patches, violating an assumption of the marginal value theorem. Our study provides evidence that chimpanzees are sensitive to their rate of energy intake and that their foraging durations correlate with patch quality, supporting many assumptions underlying primate foraging and social behavior. However, our results question whether the marginal value theorem is a constructive model of chimpanzee foraging behavior, and we suggest a Bayesian foraging framework (i.e., combining past foraging experiences with current patch sampling information) as a potential alternative. More work is needed to build an understanding of the proximate mechanisms underlying primate foraging decisions, especially in more complex socioecological environments., (© 2020 Wiley Periodicals LLC.)

Squirrel monkeys are a long-standing biomedical model, with multiple species and subspecies housed in research facilities. Few studies have examined the developmental differences between these subspecies, which may affect research outcomes. The primate neonatal neurobehavioral assessment was completed at 2 weeks of age with 279 dam-reared squirrel monkeys (188 Saimiri boliviensis boliviensis, 45 S. b. peruviensis, and 46 Saimiri. sciureus sciureus). Activity, orientation to stimuli, state control, and motor maturity scores, as well as startle responses and number of vocalizations were compared across subspecies and sex using factorial analysis of covariance (ANCOVAs) controlling for birthweight. There were no differences in orientation or motor maturity scores (p > .05) among the three subspecies or between sexes; however, there were significant subspecies differences in motor activity and state control scores. Of the three subspecies, S. s. sciureus has the lowest state control and activity scores (p < .05). They also had the most exaggerated startle response/aversion to a sudden loud noise, vocalized significantly less, and were less likely to resist restraint during the assessment (p < .05). The three subspecies of squirrel monkeys did not differ in motor development and attention to external stimuli but were significantly different in state control and activity levels. Overall S. s. sciureus were less active, agitated, irritable, and easier to console compared to S. b. boliviensis and S. b. peruviensis. This supports field research on socioecology which documented different social structure and behavior in wild populations of S. s. sciureus compared to S. b. boliviensis and S. b. peruviensis., (© 2019 Wiley Periodicals, Inc.)

Due to advances in captive nonhuman primate (NHP) medical care, the number of geriatric chimpanzees (≥35-years old) is growing. With old age comes a variety of physical conditions, including arthritis, stroke, and mobility impairments. Programs aimed at enhancing the welfare of geriatric chimpanzees are now quite common, but there are few published empirical evaluations of the efficacy of such programs. The current study aimed to create, implement, and evaluate the effects of participation in a physical therapy (PT) program on physical health, mobility, welfare, and behavior. Nine chimpanzees with mobility impairments participated in personalized PT routines (using positive reinforcement training) twice per week for 5 months. Additionally, nine control chimpanzees (non-mobility-impaired, matched with PT chimpanzees on age and gender) participated in body exam behavior sessions (also using positive reinforcement training) twice per week. All chimpanzees were rated on 14 health, well-being, and behavior items, as well as level of mobility throughout the PT program. Chimpanzees that participated in the PT program showed significant increases in ratings of physical health, well-being, and activity levels across phases of the program. Furthermore, compared to control chimpanzees, PT chimpanzees showed significant increases in ratings of ease of movement. Because raters were not blind to physical therapy treatment, our results represent an initial evaluation of the program that may suggest that participation in the PT program has physical, behavioral, and welfare benefits. Assessments of novel geriatric-focused care strategies and programs are essential to further enhance the welfare of the captive chimpanzee population, which is currently comprised of many geriatric animals, whose proportion of the captive population will only increase., (© 2020 Wiley Periodicals, Inc.)

The weekend effect hypothesis proposes that captive primates are more likely to give birth during times of low disturbance and reduced staff activity. The hypothesis specifically predicts that laboratory-housed primates will be more likely to give birth during the weekend than weekdays when staff activity is reduced. To date, support for the weekend effect hypothesis has been mixed and based on studies with relatively few subjects. To further examine the hypothesis, we analyzed the birthing patterns of three genera of laboratory-housed primates: squirrel monkeys (Saimiri species, N = 2,090 births), owl monkeys (Aotus species, N = 479 births), and rhesus macaques (Macaca mulatta, N = 2,047 births). Contrary to predictions derived from the weekend effect hypothesis, the frequencies of births during weekends for all taxa were not significantly different from rates that would be expected by chance. However, while there was no variance across days of the week, all three taxa gave birth at nighttime, when staff was absent. This parallels reports of births in wild and captive monkeys, both diurnal and nocturnal, which are more likely to give birth during the night; plausibly a time when the environmental and social disturbance is lowest and the mother is safest to bond with her newborn infant. As all births occurred at night, we also explored the relationship between the lunar cycle and the timing of births timing. While the diurnal primates (i.e., Saimiri and Macaca) were no more likely to give birth on "bright" nights than "dark" nights, owl monkeys (Aotus) had a much higher frequency of births on bright nights than darker ones, and at rates that deviated from chance. Our data provide a more detailed understanding on how the environment may influence captive monkey births but do not support the oft-cited weekend effect hypothesis., (© 2019 Wiley Periodicals, Inc.)

The National Institutes of Health and the Association of Zoos and Aquariums recommend that captive chimpanzees be housed in multi-male, multi-female, age-diverse groups of no less than seven individuals. These recommendations are rooted in the idea that captive chimpanzee groups should be modeled after free-ranging, wild, fission-fusion chimpanzee societies. However, captive chimpanzees do not face the environmental pressures faced by wild chimpanzees, including food scarcity, inter-group competition, and predation. As such, it has been posited that wild, natural conditions may not be the most relevant metric for defining optimal captive chimpanzee group sizes and compositions. Additionally, captive housing poses a set of restrictions on group sizes and compositions, including the need to balance large, multi-male groups with space per animal limitations and intra-group aggression. In the present study, we examined the behavioral effects of group size, within-group age range, and percentage of males in the group. We collected 713 hr of focal animal samples across 120 captive chimpanzees housed in social groups of 4-10 individuals using a 58-behavior ethogram. Chimpanzees housed in groups with a large age range exhibited less inactivity and more locomotion than chimpanzees housed in groups with smaller age ranges. Additionally, chimpanzees in groups of ≥7 with less than half males showed the highest levels of locomotion. Lastly, chimpanzees in groups of ≥7 with at least half males showed the highest levels of affiliation. There were no other significant differences in behavior as a function of these variables or their interactions. These findings lend some support to the existing group size and composition recommendations, providing empirical evidence that there may be certain advantages to housing captive chimpanzees in larger groups with a more diverse age range and/or more males. These results also have practical implications for behavioral management programs across captive settings., (© 2019 Wiley Periodicals, Inc.)

Space per animal, or animal density, and enclosure type are important elements of functionally appropriate captive environments (FACEs) for chimpanzees. The National Institutes of Health (NIH) recommends that captive chimpanzees be maintained in areas of >250 ft 2 /animal. Several studies have investigated chimpanzee behavior in relation to space per animal, but only two studies have examined these variables while attempting to hold environmental complexity constant. Both have found few, if any, significant differences in behavior associated with increased space per animal. The NIH does not provide recommendations pertaining to enclosure type. Although Primadomes™ and corrals are considered acceptable FACE housing, no studies have investigated chimpanzee behavior in relation to these two common types of enclosures. We examined the NIH space per animal recommendation, and the effects of enclosure type, while maintaining similar levels of environmental complexity. We used focal animal observations to record the behavior of 22 chimpanzees in three social groups following within-facility housing transfers. Chimpanzees that were moved from an area with space below the NIH recommendation to the same type of enclosure with space above the recommendation (dome to double dome) exhibited significantly more locomotion and behavioral diversity post-transfer. Chimpanzees that were moved from an area with space below the recommendation to a different type of enclosure with space above the recommendation (dome to corral) exhibited significant increases in foraging and behavioral diversity, and a decrease in rough scratching. Lastly, chimpanzees that were moved from an area above the recommendation to a different enclosure type with space equal to the recommendation (corral to double dome) exhibited an increase in behavioral diversity. These results add to the body of literature that addresses the concept of specific minimum space requirements per chimpanzee, and highlight the need for more empirical investigation of the relationship between space per chimpanzee, behavior, and welfare., (© 2018 Wiley Periodicals, Inc.)

Objectives: Dental eruption schedules have been closely linked to life history variables. Here we examine a sample of 50 perinatal primates (28 species) to determine whether life history traits correlate with relative tooth size at birth., Materials and Methods: Newborn primates were studied using serial histological sectioning. Volumes of deciduous premolars (dp 2 -dp 4 ), replacement teeth (if any), and permanent molars (M 1-2/3 ) of the upper jaw were measured and residuals from cranial length were calculated with least squares regressions to obtain relative dental volumes (RDVs)., Results: Relative dental volumes of deciduous or permanent teeth have an unclear relationship with relative neonatal mass in all primates. Relative palatal length (RPL), used as a proxy for midfacial size, is significantly, positively correlated with larger deciduous and permanent postcanine teeth. However, when strepsirrhines alone are examined, larger RPL is correlated with smaller RDV of permanent teeth. In the full sample, RDVs of deciduous premolars are significantly negatively correlated with relative gestation length (RGL), but have no clear relationship with relative weaning age. RDVs of molars lack a clear relationship with RGL; later weaning is associated with larger molar RDV, although correlations are not significant. When strepsirrhines alone are analyzed, clearer trends are present: longer gestations or later weaning are associated with smaller deciduous and larger permanent postcanine teeth (only gestational length correlations are significant)., Discussion: Our results indicate a broad trend that primates with the shortest RGLs precociously develop deciduous teeth; in strepsirrhines, the opposite trend is seen for permanent molars. Anthropoids delay growth of permanent teeth, while strepsirrhines with short RGLs are growing replacement teeth concurrently. A comparison of neonatal volumes with existing information on extent of cusp mineralization indicates that growth of tooth germs and cusp mineralization may be selected for independently., (© 2017 Wiley Periodicals, Inc.)

Chimpanzees (Pan troglodytes) demonstrate much cultural diversity in the wild, yet a majority of novel behaviors do not become group-wide traditions. Since many such novel behaviors are introduced by low-ranking individuals, a bias toward copying dominant individuals ("rank-bias") has been proposed as an explanation for their limited diffusion. Previous experimental work showed that chimpanzees (Pan troglodytes) preferentially copy dominant over low-rank models. We investigated whether low ranking individuals may nevertheless successfully seed a beneficial behavior as a tradition if there are no "competing" models. In each of four captive groups, either a single high-rank (HR, n = 2) or a low-rank (LR, n = 2) chimpanzee model was trained on one method of opening a two-action puzzle-box, before demonstrating the trained method in a group context. This was followed by 8 hr of group-wide, open-access to the puzzle-box. Successful manipulations and observers of each manipulation were recorded. Barnard's exact tests showed that individuals in the LR groups used the seeded method as their first-choice option at significantly above chance levels, whereas those in the HR groups did not. Furthermore, individuals in the LR condition used the seeded method on their first attempt significantly more often than those in the HR condition. A network-based diffusion analysis (NBDA) revealed that the best supported statistical models were those in which social transmission occurred only in groups with subordinate models. Finally, we report an innovation by a subordinate individual that built cumulatively on existing methods of opening the puzzle-box and was subsequently copied by a dominant observer. These findings illustrate that chimpanzees are motivated to copy rewarding novel behaviors that are demonstrated by subordinate individuals and that, in some cases, social transmission may be constrained by high-rank demonstrators., (© 2017 Wiley Periodicals, Inc.)

Social housing has often been recommended as one-way to address the psychological well-being of captive non-human primates. Published reports have examined methods to socialize compatible animals by forming pairs or groups. Successful socialization rates vary depending on the species, gender, and environment. This study presents a retrospective look at pairing attempts in two species of owl monkeys, Aotus nancymaae and A. azarae, which live in monogamous pairs in the wild. The results of 477 pairing attempt conducted with captive, laboratory housed owl monkeys and 61 hr of behavioral observations are reported here. The greatest success pairing these owl monkeys occurred with opposite sex pairs, with an 82% success rate. Opposite sex pairs were more successful when females were older than males. Female-female pairs were more successful than male-male (MM) pairs (62% vs 40%). Successful pairs stayed together between 3 and 7 years before the animals were separated due to social incompatibility. Vigilance, eating, and sleeping during introductions significantly predicted success, as did the performance of the same behavior in both animals. The results of this analysis show that it is possible to give captive owl monkeys a social alternative even if species appropriate social partners (i.e., opposite sex partners) are not available. The focus of this report is a description of one potential way to enhance the welfare of a specific new world primate, the owl monkey, under laboratory conditions. More important is how the species typical social structure of owl monkeys in nature affects the captive management of this genus. Am. J. Primatol. 79:e22521, 2017. © 2015 Wiley Periodicals, Inc., (© 2016 Wiley Periodicals, Inc.)

A fundamental characteristic of human language is multimodality. In other words, humans use multiple signaling channels concurrently when communicating with one another. For example, people frequently produce manual gestures while speaking, and the words a person perceives are impacted by visual information. For this study, we hypothesized that similar to the way that humans regularly couple their spoken utterances with gestures and facial expressions, chimpanzees regularly produce vocalizations in conjunction with other communicative signals. To test this hypothesis, data were collected from 101 captive chimpanzees living in mixed-sex social groupings of seven to twelve individuals. A total of 2,869 vocal events were collected. The data indicate that approximately 50% of the vocal events were produced in conjunction with another communicative modality. In addition, approximately 68% were directed to a specific individual, and these directed vocalizations were more likely to include a signal from another communicative modality than were vocalizations that were not directed to a specific individual. These results suggest that, like humans, chimpanzees often pair their vocalizations with signals from other communicative modalities. In addition, chimpanzees appear to use their communicative signals strategically to meet specific socio-communicative ends, providing support for the growing literature that indicates that at least some chimpanzee vocal signaling is intentional., (© 2015 Wiley Periodicals, Inc.)

In captive research environments for nonhuman primates (NHP), social housing strategies are often in conflict with protocols designed to minimize disease transmission. This is particularly true in breeding colonies, and is especially relevant when attempting to eliminate specific pathogens from a population of primates. Numerous strategies have been used to establish such specific pathogen free (SPF) breeding colonies (primarily of macaques), ranging from nursery rearing of neonates to single housing of socially reared yearlings to the rearing of infants in large social groups. All these strategies attempt to balance the effects of the chosen socialization strategy on parameters related to disease transmission, including the ultimate elimination of the target pathogens. Such strategies may affect the overall disease states of NHP breeding colonies through selective breeding processes. This can occur either by creating subpopulations of animals that do not have target diseases (SPF colonies), but may have other issues; or by creating situations in which the "best" animals are sold and the breeding colony is stocked with animals that may be more disease susceptible than those that were sold. The disease states of NHP research colonies also may be affected by selective utilization programs, in which animals removed from the breeding colony for health/behavior reasons, are preferentially chosen for use in scientific investigations. Such utilization criteria raise the question of whether ideal subjects are being chosen for use in research. Finally, captive primate colonies, where both socialization and disease states are intensely managed, may provide opportunities for those testing predictions from models of the interactions of socialization and disease transmission in the evolution of wild populations of NHP. This would be especially true for some extreme conditions of these disease ecology models, given the exceedingly high social densities and levels of pathogen control that exist in many captive nonhuman primate colonies., (© 2011 Wiley Periodicals, Inc.)

Positive reinforcement training (PRT) techniques have received considerable attention for their stress reduction potential in the behavioral management of captive nonhuman primates. However, few published empirical studies have provided physiological data to support this position. To address this issue, PRT techniques were used to train chimpanzees (Pan troglodytes) to voluntarily present a leg for an intramuscular (IM) injection of anesthetic. Hematology and serum chemistry profiles were collected from healthy chimpanzees (n=128) of both sexes and various ages during their routine annual physical examinations over a 7-year period. Specific variables potentially indicative of acute stress (i.e., total white blood cell (WBC) counts, absolute segmented neutrophils (SEG), glucose (GLU) levels, and hematocrit (HCT) levels) were analyzed to determine whether the method used to administer the anesthetic (voluntary present for injection vs. involuntary injection) affected the physiological parameters. Subjects that voluntarily presented for an anesthetic injection had significantly lower mean total WBC counts, SEG, and GLU levels than subjects that were involuntarily anesthetized by more traditional means. Within-subjects analyses revealed the same pattern of results. This is one of the first data sets to objectively demonstrate that PRT for voluntary presentation of IM injections of anesthetic can significantly affect some of the physiological measures correlated with stress responses to chemical restraint in captive chimpanzees.