Positive reinforcement training affects hematologic and serum chemistry values in captive chimpanzees (Pan troglodytes)

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.     

Resocialization of a group of ex-laboratory chimpanzees, Pan troglodytes.

In order to determine if socially deprived chimpanzees could establish an integrated social unit and reproduce, a group of wild-born individuals from a single-cage laboratory environment were released onto a small island in a South Florida tourist park in 1975. The present study was undertaken during June and July of 1988 to evaluate the long term results of the experiment and to document the reproductive history of the chimpanzees since their release on the island. The evidence presented in this paper suggests that it is possible for laboratory chimpanzees to be resocialized and to reproduce successfully.     

Effects of cognitive challenge on self-directed behaviors by chimpanzees (Pan troglodytes)

In primates, including humans, scratching and other self-directed behaviors (SDBs) have recently been reported to be differentially displayed as a function of social interactions, anxiety-related drugs, and response outcomes during learning tasks. Yet few studies have focused on the factors influencing SDBs in our closest living relatives, the chimpanzees (Pan troglodytes). Furthermore, no previous experimental study has examined handedness of SDBs as a function of changes in task difficulty. Using matching-to-sample tasks of varying difficulty, the present study examines the effect of manipulations of task difficulty on rates, handedness, and type of SDBs in an experimental study of eight chimpanzees. SDBs were categorized as rubs, gentle scratches, and rough scratches. SDBs increased during difficult discriminations, but only for subjects who started the experiment on an easy discrimination; subjects who started on a difficult discrimination exhibited no differential rates of SDBs as a function of task difficulty. There was a tendency to exhibit relatively more SDBs with the right hand in the more difficult task. Rates of SDBs decreased after auditory feedback signals, suggesting a link between SDBs and uncertainty. Rubs were directed more to the face (trigeminal), and gentle and rough scratches more to the body (spinothalamic), suggesting that face-directed SDBs may index a different motivational basis than scratches. Taken together, these results extend previous research on SDBs to the domain of cognitive stress in nonsocial contexts, demonstrating that SDBs are sensitive to manipulations of task difficulty in chimpanzees.     

Detection and molecular characterization of foamy viruses in Central African chimpanzees of the Pan troglodytes troglodytes and Pan troglodytes vellerosus subspecies

BACKGROUND: Foamy viruses are exogenous retroviruses that are highly endemic in non-human primates (NHPs). Recent studies, mainly performed in North America, indicated frequent simian foamy virus (SFV) infection in persons occupationally exposed to NHPs. This zoonotic infection was demonstrated mainly after bites by chimpanzees [Pan troglodytes (P. t.)] of the West African P. t. verus subspecies in primatology centers or zoos in the USA. METHODS: We studied 32 chimpanzees from the Central African subspecies P. t. troglodytes and P. t. vellerosus, originating from Cameroon (29 cases) or Gabon (3 cases). We screened first plasma or sera of the animals with a Western blot detecting the SFVs Gag doublet proteins. Then, we performed two nested polymerase chain reactions (PCRs) amplifying a fragment of the integrase and LTR regions and, finally, we made phylogenetical analyses on the sequences obtained from the integrase PCR products. RESULTS: By serological and/or molecular assays, we detected foamy viruses (FVs) infection in 14 chimpanzees. Sequence comparison and phylogenetic analyses of a 425 bp fragment of the integrase gene obtained for 10 of the 14 positive apes, demonstrated a wide diversity of new FVs strains that belong phylogenetically either to the P. t. troglodytes or P. t. vellerosus foamy viral clade. CONCLUSIONS: This study shows that chimpanzees living in these areas of Central Africa are infected by several specific foamy viruses. This raises, in such regions, the potential risk of a human retroviral infection of zoonotic origin linked to chimpanzees contacts, as already exemplified for STLV-1 and SIV infections.     

An evaluation of the efficacy of video displays for use with chimpanzees (Pan troglodytes)

Video displays for behavioral research lend themselves particularly well to studies with chimpanzees (Pan troglodytes), as their vision is comparable to humans', yet there has been no formal test of the efficacy of video displays as a form of social information for chimpanzees. To address this, we compared the learning success of chimpanzees shown video footage of a conspecific compared to chimpanzees shown a live conspecific performing the same novel task. Footage of an unfamiliar chimpanzee operating a bidirectional apparatus was presented to 24 chimpanzees (12 males, 12 females), and their responses were compared to those of a further 12 chimpanzees given the same task but with no form of information. Secondly, we also compared the responses of the chimpanzees in the video display condition to responses of eight chimpanzees from a previously published study of ours, in which chimpanzees observed live models. Chimpanzees shown a video display were more successful than those in the control condition and showed comparable success to those that saw a live model. Regarding fine-grained copying (i.e. the direction that the door was pushed), only chimpanzees that observed a live model showed significant matching to the model's methods with their first response. Yet, when all the responses made by the chimpanzees were considered, comparable levels of matching were shown by chimpanzees in both the live and video conditions.     

Variables influencing the origins of diverse abnormal behaviors in a large sample of captive chimpanzees (Pan troglodytes)

The developmental origin of abnormal behaviors is generally associated with early rearing environments that lack sufficient physical and sensory stimulation. However, other factors should also be considered. A large sample of captive chimpanzees (128 males and 140 females) was surveyed for the presence or absence of 18 abnormal behaviors. Origin variables included the subject's source (zoo, pet, performer, or laboratory), rearing (mother‐ or hand‐reared), and sex. Animals were assessed while held at the Primate Foundation of Arizona, University of Texas M. D. Anderson Cancer Center, or White Sands Research Center. There was a confound among origin variables; more hand‐reared animals than expected were from laboratories. Logistic regression tested the relationship of rearing and source, with sex as a secondary predictor variable, to each of the abnormal behaviors. There was no clear association between any abnormal behavior and source. However, for coprophagy, relative to animals from the laboratory, zoo animals tended to show a higher prevalence, while performers tended to show a lower prevalence (when rearing and sex were controlled). Rocking and self‐sucking were significantly more likely in hand‐reared animals. Coprophagy and depilation of self were significantly more likely in mother‐reared animals. When rearing and source were statistically controlled, the only significant sex difference was a higher prevalence of coprophagy in females and a higher prevalence of rocking in males. In a second, smaller sample of 25 males and 33 females from Southwest Foundation for Biomedical Research, no significant sex association was found for coprophagy, urophagy, rocking, or self‐depilation. In this second sample, coprophagy was also significantly more likely in mother‐reared than hand‐reared subjects. The association of some abnormal behaviors with mother‐rearing suggests that some form of social learning may be involved in the origin of some of these behavior patterns. This indicates that some abnormal behaviors may not be always be indicative of reduced psychological well‐being in captive chimpanzees. Am. J. Primatol. 48:15–29, 1999. © 1999 Wiley‐Liss, Inc.     

Language-trained chimpanzees (Pan troglodytes) delay gratification by choosing token exchange over immediate reward consumption

Token exchange inherently introduces an element of delay between behavior and reward and so token studies may help us better understand delay of gratification and self-control. To examine this possibility, we presented three language-trained chimpanzees with repeated choices involving different foods that could be eaten immediately or lexigram (graphic symbol) tokens that represented (and could be traded for) foods later. When both options were foods, chimpanzees always chose more preferred foods over less preferred foods. When both options were lexigram tokens representing those same foods, performance remained the same as chimpanzees selected the higher value token and then traded it for food. Then, when faced with choosing a token that could be traded later or choosing a food item that could be eaten immediately, most chimpanzees learned to make whatever response led to the more preferred food. They did this even when that meant selecting a high value lexigram token that could be traded only 2 to 3 min later instead of a medium value, but immediately available, food item. Thus, chimpanzees flexibly selected tokens even though such selections necessarily delayed gratification and required forgoing immediately available food. This finding illustrates the utility of symbolic token exchange for assessing self-control in nonhuman animals.     

The relationship between forage material and levels of coprophagy in captive chimpanzees (Pan troglodytes)

Although coprophagy is practiced in the wild by chimpanzees (Pan troglodytes), it occurs more frequently and under more varied circumstances in captivity. This study was designed to determine if different forage materials and amount of residual undigested grain particles found in the feces might cause an increase in coprophagous behavior in those animals which already exhibited the behavior. A possible effect of availability of seed pits and fibrous leaves for “wadge” making, a typical chimpanzee behavior, on levels of coprophagy was also considered. Observations for coprophagous behavior were conducted on 65 juvenile, adolescent, and adult chimpanzees. Coprophagy levels were significantly lower with popcorn than either chicken scratch or sweet feed. A significant increase in coprophagy was noted for all weeks of forage types when tested against the wadge weeks. Residual grain content analysis showed no significant difference in coprophagous behavior between any of the testing conditions. Decreasing levels of coprophagous behaviors may be assisted by the provision of wadge materials. © 1992 Wiley-Liss, Inc.     

Analysis of hematologic findings in healthy and sick adult chimpanzees (Pan troglodytes)

In order to assess the validity of interspecies extrapolation of hematological information, reference values obtained on 63 captive adult chimpanzees were compared with normal values for man. The discriminative power of both chimpanzee and human reference values was tested by the ability of each to identify abnormalities in the blood in 15 sick chimpanzees. The results indicated that human criteria could be applied to most chimpanzee red cell values but species differences were found in erythrocyte sedimentation rates and neutrophil counts.     

Innovative social behavior in chimpanzees (Pan troglodytes)

We present evidence of agonistic buffering in captive chimpanzees, recorded from 1993 until 2005, mainly from ad libitum sampling in over 2000 hr of observation. A total of 33 agonistic buffering episodes were analyzed for context and effects of this complex social behavior. Agonistic buffering was directed at the whole chimpanzee colony as they supported an individual who initially received aggression from the alpha male, independently of the victim's age, sex or social rank. Chimpanzee agonistic buffering behavior is compared with that in other nonhuman primate species, and we describe some particularities of chimpanzee agonistic buffering: the status of the buffers used-socially important offspring such as those from the alpha female-and the social rank of the adult male responsible for the buffering episode-alpha male. Possible functions for this behavior in chimpanzees are suggested as appeasement of group members in a particularly crowded captive setting, and/or as a "forced reconciliation" mechanism. Chimpanzees exhibit behavioral flexibility by adapting themselves to new social and physical situations and use novel behavior to achieve social benefits.     

Assessing the effects of cognitive experiments on the welfare of captive chimpanzees (Pan troglodytes) by direct comparison of activity budget between wild and captive chimpanzees

We investigated the effects of cognitive experiments by direct comparison of activity budgets between wild and captive chimpanzees. One goal of captive management is to ensure that the activity budgets of captive animals are as similar as possible to those of their wild counterparts. However, such similarity has rarely been achieved. We compared the activity budget among three groups of chimpanzees: wild chimpanzees in Bossou (Guinea, n = 10), and captive chimpanzees who participated in cognitive experiments (experimental chimpanzees, n = 6) or did not participate in the experiments (nonexperimental chimpanzees, n = 6) at the Primate Research Institute (Japan). The experimental chimpanzees voluntarily participated in computer‐controlled cognitive tasks and small pieces of fruits were provided as rewards. The data from captivity were obtained on the experimental days (weekdays) and nonexperimental days (weekends). In both study sites, we followed each chimpanzee from about 7 a.m. until the time when chimpanzees started to rest in the evening. The behaviors were recorded every 1 min. The results showed that on weekdays, feeding time and resting time of the experimental chimpanzees were almost the same as those of wild chimpanzees. However, for the nonexperimental chimpanzees, feeding time was significantly shorter and resting time was longer than those of the wild chimpanzees. In contrast, no difference was found in feeding time or resting time of the two groups of captive chimpanzees on weekends. The results suggested that the cognitive experiments worked as an efficient method for food‐based enrichment. Am. J. Primatol. 73:1231–1238, 2011. © 2011 Wiley Periodicals, Inc.     

Polymerase chain reaction detection of Clostridium perfringens in feces from captive and wild chimpanzees, Pan troglodytes

Background For veterinary management of non‐human primates in captivity, and conservation of wild‐living primates, management of their health risks is necessary. Incidences of pathogenic bacteria in the fecal specimens are considered as one of the useful indicators for non‐invasive health monitoring. Methods We carried out the detection of Clostridium perfringens in feces from captive and wild chimpanzees by the rapid polymerase chain reaction method. Results The bacterium was detected in most fecal specimens (80%) in captive chimpanzees. Contrarily, the detection rate in the wild chimpanzees was low, with 23% (n = 12) of 53 fecal samples from the Bossou group, Guinea, and 1.2% (1/81) in the Mahale group, Tanzania. Conclusions These results show that the intestinal microflora differs between Pan populations under various living conditions, being influenced by their diet and environment.     

Blood pressure reference intervals for healthy adult chimpanzees (Pan troglodytes)

Background Cardiovascular disease is the primary cause of morbidity and mortality among captive chimpanzees. But there are no clinical definitions of normotension or hypertension in chimpanzees. Methods We analyzed 1 year of blood pressure (BP) data from a population of 261 healthy captive adult chimpanzees using a consistent set of criteria to ascertain health. Results Systolic BP varied by body weight. Diastolic BP varied by age. Median normotension was 126/63 mmHg, with an upper limit of 147/84 mmHg. We defined categories of pre‐hypertension (148/85—153/88 mmHg) and hypertension (≥154/89 mmHg). The prevalence of elevated BP was 15%. The relative risk of mortality was 2.60, compared to normotensive animals. Conclusions We used contemporary methods from human laboratory medicine to define reliable reference intervals for chimpanzee BP. Results allow accurate diagnosis of hypertension and pre‐hypertension, and demonstrate an effect of elevated BP on mortality.     

Familial incidence of multiple births in a colony of chimpanzees (Pan troglodytes)

This paper describes the incidence of multiple births in the Yerkes Chimpanzee colony for a period of about 63 years. Pedigrees are presented for all multiple births. They demonstrate the recurrence of twins in relatively few family lines which can be traced back to a small number of ancestors. The findings suggest that twinning is a family trait in chimpanzees and they support the hypothesis that the incidence of multiple births is genetically influenced in this colony. In addition, a relatively high level of inbreeding may have enhanced the incidence of multiple births in these family lines. Similar findings are known from human populations.     

Developing classification in action: II. Young chimpanzees (Pan troglodytes)

The development of spontaneous object manipulation in 5 chimpanzees (Pan troglodytes) from ages 15 to 54 months was investigated, focusing on formal properties of subjects’ acts and the objects they manipulated. Young chimpanzees’ manipulation progress from serial one-at-a-time acts on one object to parallel two-at-a-time acts on two or more objects. With age, simultaneous acts become increasingly transformational and identical or reciprocal to each other. Moreover, the class properties of objects manipulated simultaneously change. When presented with objects belonging to two different classes, subjects shift, with age, from manipulating different objects to manipulating identical or similar objects. In all these respects young chimpanzee’ development is similar to human infants’. In others it differs. Most especially, the onset age is later and the development is slower as well as less structurally complex.     

Asymmetries in postural control and locomotion in chimpanzees (Pan troglodytes)

Posture and locomotion are two of the most primitive and basic motor manifestations of an organism's behavior. Although the restrictions they impose on other motor functions are evident, few studies have considered the possibility of asymmetries in these behaviors in human and nonhuman primates, and how they might impact other asymmetries at higher functional levels. The aim of the current study was to explore in a group of 10 chimpanzees at the Madrid Zoo-Aquarium the degree of asymmetry in four behaviors related to locomotion (walking, ascending, descending, and brachiating) and four behaviors associated with posture (sitting, lying, hanging, and changing postures). Few subjects showed individual preferences, but significant trends in the group for some of the behaviors were found, including right-hand use when initiating quadruped walking, and left-hand use when descending and hanging. Some significant correlations also emerged: a negative one between walking and descending, and a positive one between walking and brachiating and between sitting and changing postures. No correlations were found between locomotor and postural modes. Although we cannot make generalizations on the population level at this time, these findings highlight the importance of considering postural and locomotion factors when studying motor asymmetries in primates.     

Characterization of 15 single nucleotide polymorphism markers for chimpanzees (Pan troglodytes)

We report the characterization of 15 new single nucleotide polymorphism markers for a threatened species, the chimpanzee (Pan troglodytes), developed using a targeted gene approach. These markers are derived from the Y chromosome and autosomal regions of the genome and show frequency differences between chimpanzee subspecies from central and western Africa. These single nucleotide polymorphism markers are the first to be designed for the genotyping of wild chimpanzee populations and will provide a useful addition to the genetic tools employed for the conservation management of this threatened species.     

Response of fecal cortisol to stress in captive chimpanzees (Pan troglodytes)

This study examined whether fecal cortisol could be used as an index of stress responses. The stress responsiveness of fecal cortisol was tested with a stressor known to stimulate adrenal activity, the stress of anesthesia. Daily fecal and urine samples were collected from four captive chimpanzees (Pan troglodytes) before and after anesthetizations with Telazol^®/Ketasat^®. Tests of assay validity indicated that cortisol was measurable in chimpanzee fecal extracts. Fecal cortisol concentrations were significantly elevated 2 days after anesthetization, with elevations in seven of the eight treatments. The posttreatment peak was significantly greater than baseline values in three of the four subjects. Both fecal concentrations and proportionate increases in response to stress were significantly correlated with the corresponding values in urinary cortisol, confirming the stressfulness of these procedures and the stress responsiveness of fecal cortisol. These findings provide evidence for the application of fecal cortisol as a noninvasive index of physiologic stress in nonhuman primates. Am. J. Primatol. 44:57–69, 1998. © 1998 Wiley-Liss, Inc.     

Grip preference, dermatoglyphics, and hand use in captive chimpanzees (Pan troglodytes)

This paper examined the association between grip type, hand use, and fingerprint patterns in a sample of captive chimpanzees. Grip type for simple reaching was assessed for the left and right hand and classified as thumb-index, middle-index, or single-digit responses. Fingerprint patterns were characterized as whorls, loops, or arches on each finger. The results indicated that chimpanzees exhibit significantly more thumb-index responses for the right compared to the left hand. In addition, thumb-index responses were more prevalent for subjects that had a whorl compared to a loop or arch on their thumb. The results suggest that fingerprint patterns are associated with individual differences in grasping type in chimpanzees as well as some variation in hand use.     

Fecal bacterial diversity of human‐habituated wild chimpanzees (Pan troglodytes schweinfurthii) at Mahale Mountains National Park,Western Tanzania

Although the intestinal flora of chimpanzees has not been studied, insight into this dynamic environment can be obtained through studies on their feces. We analyzed fecal samples from human‐habituated, wild chimpanzees at Mahale Mountains National Park, Tanzania, and compared microbial community profiles to determine if members of the same social group were similar. Between July and December 2007, we collected fresh fecal samples from 12 individuals: four juveniles, four adolescents, and four adults, including three parent–offspring pairs. Each sample was analyzed using Terminal‐Restriction Fragment Length Polymorphism of amplified 16S rRNA genes. Twelve different profiles were generated, having between 1 and 15 Terminal‐Restriction Fragments (T‐RFs). Overall, a total of 23 different T‐RFs were produced. Putative assignments of T‐RFs corresponded to the phyla Firmicutes (Clostridia, Bacilli, and Lactobacilli), Bacteroidetes, Tenericutes (Mollicutes Class), Actinobacteria, and Proteobacteria, as well as to uncultured or unidentified organisms. Firmicutes and Bacteroidetes phyla and Mollicutes Class were the most commonly assigned in 11, 8, and 8 of the samples, respectively, with this being the first report of Mollicutes in wild chimpanzees. Principal Components Analysis (PCA) revealed clustering of nine samples, and 80.5% of the diversity was accounted for by three samples. Morisita indices of community similarity ranged between 0.00 and 0.89, with dissimiliarity (<0.5) between most samples when compared two at a time. Our findings suggest that, although phylotypes are common among individuals, profiles among members of the same social group are host‐specific. We conclude that factors other than social group, such as kinship and age, may influence fecal bacterial profiles of wild chimpanzees, and recommend that additional studies be conducted. Am. J. Primatol. 72:566–574, 2010. © 2010 Wiley‐Liss, Inc.