Chimpanzees (Pan troglodytes) in savanna landscapes.

Chimpanzees (Pan troglodytes) are the only great apes that inhabit hot, dry, and open savannas. We review the environmental pressures of savannas on chimpanzees, such as food and water scarcity, and the evidence for chimpanzees' behavioral responses to these landscapes. In our analysis, savannas were generally associated with low chimpanzee population densities and large home ranges. In addition, thermoregulatory behaviors that likely reduce hyperthermia risk, such as cave use, were frequently observed in the hottest and driest savanna landscapes. We hypothesize that such responses are evidence of a "savanna landscape effect" in chimpanzees and offer pathways for future research to understand its evolutionary processes and mechanisms. We conclude by discussing the significance of research on savanna chimpanzees to modeling the evolution of early hominin traits and informing conservation programs for these endangered apes.

Social hair plucking is a grooming convention in a group of captive bonobos (Pan paniscus).

Hair plucking is observed in many captive primate species and is often characterized as an abnormal behavior. However, this behavior may be both self-directed and social and may have different etiologies. Early research in captive macaques (Macaca mulatta) described the aggressive nature of social hair plucking while more recent observations did not find an association with aggression or grooming, but the behavior was initiated most frequently by individuals with more secure dominance rank. Here, we investigate patterns of social hair plucking in a group of captive bonobos at the Columbus Zoo. We tested the hypothesis that social plucking reflects the dominance hierarchy by examining the association between social plucking and grooming, dominance, and kinship. We collected 128 h of grooming data on 16 captive bonobos using all-occurrence sampling. We ran three Mantel tests between a directed grooming matrix and (1) a plucking matrix, (2) a matrix reflecting dominance, and (3) matrix of relatedness. Grooming and hair plucking were significantly correlated (r = 0.25, p < 0.01), however, there was no association between plucking and dominance (r = - 0.04, p = 0.67), or plucking and relatedness (r = 0.07, p = 0.24). These results support the hypothesis that social plucking in bonobos is a grooming convention and is unrelated to dominance.

Prevalence and characteristics of hair plucking in captive bonobos (Pan paniscus) in North American zoos.

When primates exhibit hair loss and are observed to engage in self or social hair plucking (a rapid jerking away of the hair shaft and follicle by the hand or mouth, often accompanied by inspection, and consumption) the altered appearance, and behavior patterns are thought to reflect individual physiological, and psychological well-being. Hair loss and hair plucking occur in many captive primate species, including all of the great apes. We present the first survey of this behavior among captive bonobos (N = 88; 50 females and 38 males) in seven zoos in the United States. We found that 43% of the population engaged in this behavior pattern and discounting youngsters (who are not observed to hair pluck until the age of five), 58% of individuals hair plucked. Of the individuals who hair plucked, 97% engaged in social plucking, whereas 46% engaged in self-directed plucking. We regressed the occurrence of hair plucking with multiple predictor variables using binary logistic regression and multimodel inference to determine which predictors best explained the prevalence of self-directed and social plucking. We also analyzed publicly available data on hair plucking in captive chimpanzees. We found that the occurrence of another abnormal behavior, age, origin, and pelage condition best explained self-directed plucking in bonobos. Social plucking was explained by age, origin, pelage, and sex. Our analysis of chimpanzee hair plucking revealed that plucking is strongly influenced by rearing and sex. This study demonstrates that hair plucking is more prevalent in captive bonobos compared to captive chimpanzees and gorillas, however, the covariates associated with hair plucking for each species are different. Our data suggest a potential link between self-directed plucking and well-being. However, the higher prevalence and etiology of social hair plucking is more difficult to explain.

Laterality of Grooming and Tool Use in a Group of Captive Bonobos (Pan paniscus).

Humans exhibit population level handedness for the right hand; however, the evolution of this behavioral phenotype is poorly understood. Here, we compared the laterality of a simple task (grooming) and a complex task (tool use) to investigate whether increasing task difficulty elicited individual hand preference among a group of captive bonobos (Pan paniscus). Subjects were 17 bonobos housed at the Columbus Zoo and Aquarium. Laterality of grooming was recorded using group scans; tool use was recorded using all-occurrence sampling. Grooming was characterized as unimanual or bimanual, and both tasks were scored as right-handed or left-handed. Most individuals did not exhibit significant hand preference for unimanual or bimanual (asymmetrical hand use) grooming, although 1 individual was lateralized for each. For the 8 subjects who engaged in termite fishing enough for statistical testing, 7 individuals exhibited significant laterality and strong individual hand preference. Four subjects preferred their left hand, 3 preferred their right, and 1 had no preference. Grooming, a simple behavior, was not lateralized in this group, yet a more complex behavior revealed a strong individual hand preference, and these results are congruent with other recent findings that demonstrate complex tasks elicit hand preference in bonobos.

Hair plucking, stress, and urinary cortisol among captive bonobos (Pan paniscus).

Hair plucking has been observed in many captive primate species, including the great apes; however, the etiology of this behavioral pattern is poorly understood. While this behavior has not been reported in wild apes, an ethologically identical behavior in humans, known as trichotillomania, is linked to chronic psychosocial stress and is a predominantly female disorder. This study examines hair plucking (defined here as a rapid jerking away of the hair shaft and follicle by the hand or mouth, often accompanied by inspection and consumption of the hair shaft and follicle) in a captive group of bonobos (N = 13) at the Columbus Zoo and Aquarium in Columbus, Ohio. Plucking data were collected using behavior and all-occurrence sampling; 1,450 social and self-directed grooming bouts were recorded during 128 hr of observation. Twenty-one percent of all grooming bouts involved at least one instance of plucking. Urine samples (N = 55) were collected and analyzed for the stress hormone cortisol. Analyses of urinary cortisol levels showed a significant positive correlation between mean cortisol and self-directed plucking for females (r = 0.88, P < 0.05) but not for males (r = -0.73, P = 0.09). These results demonstrate an association between relative self-directed hair plucking and cortisol among female bonobos. This is the first study to investigate the relationship between hair plucking and cortisol among apes. Overall, these data add to our knowledge of a contemporary issue in captive ape management. Zoo Biol. 35:415-422, 2016. © Wiley Periodicals, Inc.

Grips and hand movements of chimpanzees during feeding in Mahale Mountains National Park, Tanzania.

It has long been assumed that stone tool making was a major factor in the evolution of derived hominin hand morphology. However, stresses on the hand associated with food retrieval and processing also have been recognized as relevant early hominin behaviors that should be investigated. To this end, chimpanzee food manipulation was videotaped in the Mahale Mountains National Park, Tanzania. Grips and hand movements by 39 chimpanzees were analyzed for arboreal and terrestrial feeding involving 10 food-types and associated vegetation. It was predicted that (1) new grips would be found that had not been observed in captivity, (2) forceful precision grips would be absent from the repertoire, as in captivity, and (3) precision handling would be observed. New grips involving the full thumb and buttressed index finger, and a new integrated pattern of grips and forceful hand movements were discovered, associated with feeding on large fruits and meat. Participation of the full thumb in these grips, rather than the distal thumb and fingers, throws light on feeding behaviors that may have become increasingly significant factors in the evolution of derived hominin thumb morphology. The proximal thumb stabilizes food with the flexed index finger against the pull of the teeth and provides leverage in breaking food into portions. Isolated qualitative observations of possibly forceful pinch by the thumb and side of the index finger highlight the need for comparative quantitative data to test whether humans are unique in forceful precision gripping capability. Precision handling was not seen.

Chimpanzees (Pan troglodytes verus) and their mammalian sympatriates: Mt. Assirik, Niokolo-Koba National Park, Senegal.

In intact, mosaic ecosystems, chimpanzees are sympatric with a wide range of other mammals, which may be predators, prey, or competitors. We delve beyond the nominal data of species lists to interval-level data on 35 medium-bodied and large-bodied mammals encountered at a hot, dry, and open field site in far West Africa. Frequency of encounter, habitat where found, and number of individuals encountered are analysed for species for which enough data were accumulated. Further, we compare findings over three periods (1976-1979, 2000, 2012). Species most often encountered were those normally classed as typical savanna forms. Even a crude classification into forest, woodland, and grassland ecotypes yields differences in species likely to meet apes. Comparison of encounter rates over time was surprisingly congruent, although not all species seen in the 1970s survived to the 2000s. Overall, Assirik's mammalian fauna is comparable to palaeo-faunal guilds sympatric with various extinct hominins.

Selective insectivory at Toro-Semliki, Uganda: comparative analyses suggest no 'savanna' chimpanzee pattern.

Chimpanzee (Pan troglodytes) insectivory across Africa is ubiquitous. Insects provide a significant nutritional payoff and may be important for chimpanzees in dry, open habitats with narrow diets. We tested this hypothesis at Semliki, Uganda, a long-term dry study site. We evaluated prospects for insectivory by measuring insect abundance along de novo transects and trails, monitoring social insect colonies, and surveying available raw materials for elementary technology. We determined the frequency and nature of insectivory through behavioral observation and fecal analysis. We then compared our results with those from 15 other long-term chimpanzee study sites using a cluster analysis. We found that Semliki chimpanzees are one of the most insectivorous populations studied to date in terms of frequency of consumption, but they are very selective in their insectivory, regularly consuming only weaver ants (Oecophylla longinoda) and honey and bees from hives of Apis mellifera. This selectivity obtains despite having a full range of typical prey species available in harvestable quantities. We suggest that Semliki chimpanzees may face ecological time constraints and therefore bias their predation toward prey taxa that can be quickly consumed. Geographical proximity correlated with the results of the cluster analysis, while rainfall, a relatively gross measure of environment, did not. Because broad taxonomic groups of insects were used in analyses, prey availability was unlikely to have a strong effect on this pattern. Instead, we suggest that transmission of cultural knowledge may play a role in determining chimpanzee prey selection across Africa. Further study is needed to test these hypotheses.

Handedness is more than laterality: lessons from chimpanzees.

Is human handedness unique? That is, do our nearest living relations, chimpanzee and bonobo (Pan spp.) show species-wide handedness, as is seen in living Homo sapiens? The answer may depend on definition: Handedness (congruence across subjects and across tasks) should be distinguished from hand preference (within subject and task), manual specialization (within subject, across tasks), and task specialization (across subjects, within task). Comparison is required at both population and species level. Several methodological issues (e.g., ecological validity) are crucial, as are major confounding variables (e.g., bimanuality). The behavioral manual laterality of chimpanzees is well-studied in a variety of contexts. Especially important is tool use, which seems to enhance extent of lateralization, but this varies both within and across populations. There is much evidence for task specialization in chimpanzees, but no conclusive evidence of handedness in the strictest sense. Thus, human handedness seems to be unique among living hominoids.

Community composition, correlations among taxa, prevalence, and richness in gastrointestinal parasites of baboons in Senegal, West Africa.

Studies of gastrointestinal parasite prevalence in Papio have either focused on a single troop or compared prevalence among troops that share migrants but differ in degree of human contact. Little is known about the extent of variation in prevalence where obvious factors that may drive prevalence (e.g., human contact) are absent, so it is difficult to interpret variation when these factors are present. To address this issue, we studied troops of Guinea baboons (Papio papio) that had almost no contact with humans or domesticated species of plants or animals. We tested the null hypotheses that community composition, richness, and prevalence would be similar between groups in two comparisons: (1) between troops in the same locality with no known differences in drivers of prevalence, and (2) between samples at the same location taken more than 20 years apart. We collected anonymous fecal samples from two troops of baboons living in a wilderness site, Mt. Assirik, in the Niokolo-Koba National Park, Republic of Senegal, West Africa. We collected samples from two valleys and analyzed prevalence and richness with respect to place and time. Both prevalence and richness were similar in the two valleys, but significant changes emerged in both prevalence and community composition compared with the previous survey in 1978-1979. We also found that the nematode Enterobius and a fluke, Watsonius, co-occurred within hosts more frequently than expected. This phenomenon has not been previously noted in the literature, and it suggests common environmental drivers or facilitation among these parasites.

Ranging behavior of Mahale chimpanzees: a 16 year study.

We have analyzed the ranging patterns of the Mimikire group (M group) of chimpanzees in the Mahale Mountains National Park, Tanzania. During 16 years, the chimpanzees moved over a total area of 25.2 or 27.4 km(2), as estimated by the grid-cell or minimum convex polygon (MCP) methods, respectively. Annually, the M group used an average of 18.4 km(2), or approximately 70 %, of the total home-range area. The chimpanzees had used 80 % of their total home range after 5 years and 95 % after 11 years. M group chimpanzees were observed more than half of the time in areas that composed only 15 % of their total home range. Thus, they typically moved over limited areas, visiting other parts of their range only occasionally. On average, the chimpanzees used 7.6 km(2) (in MCP) per month. Mean monthly range size was smallest at the end of the rainy season and largest at the end of the dry season, but there was much variability from year to year. The chimpanzees used many of the same areas every year when Saba comorensis fruits were abundant between August and January. In contrast, the chimpanzees used several different areas of their range in June. Here range overlap between years was relatively small. Over the 16 years of the study we found that the M group reduced their use of the northern part of their range and increased their frequency of visits to the eastern mountainous side of their home range. Changes in home-range size correlated positively with the number of adult females but not with the number of adult males. This finding does not support a prediction of the male-defended territory model proposed for some East African chimpanzee unit-groups.

"An ape's view of the Oldowan" revisited.

In 1989, Wynn and McGrew published an explicit comparison between Oldowan technology and what was then known of chimpanzee technology. They compared the range and variety of tools, adaptive role of tools, carrying distances, spatial cognition, manufacturing procedures, and modes of learning. They concluded that everything archeologists had reconstructed about the behavior of Oldowan hominins could be accommodated within the ape adaptive grade; that is, a paraphyletic group united by overall similarities in anatomy and, in this case, behavior. The only Oldowan activities that were almost unknown for modern apes were the long-distance transport of objects and direct competition with carnivores, which was implied by meat acquisition activities. "In its general features Oldowan culture was ape, not human. Nowhere in this picture need we posit elements such as language, extensive sharing, division of labor, or pair-bonded families, all of which are part of the baggage carried by the term human."

Standardised protocol for primate faecal analysis.

Macroscopic analysis of primate faeces as a way to study diet is well established, but lack of standardisation of methods may handicap comparative studies of the resulting data. Here we present a proven technique, including equipment and supplies, protocol and procedure, that yields quantitative data suitable for systematic investigation within and across primate taxa. As the problems of habituation become more obvious, the application of such indirect methods may increase in usefulness.

Misuse of anecdotes in primatology: lessons from citation analysis.

This study analyzes the accuracy of anecdotes cited in behavioral primatology publications. Anecdotes (n=1 cases) recounting tool use were sought in the four main primatological journals. Citations of anecdotes in the scientific literature that met three criteria were systematically coded for recognition and accuracy. The results showed that 60% of the time, authors who cited anecdotes did not explicitly acknowledge them as such. To a lesser extent, the citations exaggerated the frequency of anecdotal events or misrepresented their status. For tool use specifically, the actor was misreported more often than the tool or its target. Multiple citations were incorrect more often than single citations. Overall, it seems that citation of anecdotes is problematic and may have far-reaching implications in terms of misleading overgeneralizations. Primatologists should take care in citing singular or rare events.

Social scratch: Another custom in wild chimpanzees?

Chimpanzees (Pan troglodytes schweinfurthii) in the Mahale Mountains National Park, Tanzania, scratch other individual's bodies while they groom them. This behavioral pattern of "social scratch" is another example of locality-specific social behavior, or custom, as it is not found in the Gombe National Park, Tanzania, about 150 km north of Mahale, nor has it been reported from any other sites of chimpanzee study. Frequency of social scratch was correlated with frequency of social grooming, but not with frequency of self-scratch. Frequencies of social scratch per grooming bout among adult and adoles-cent males, and from lactating females to infants or juveniles, were high, and among males, higher-ranking males especially received more. These facts indicate some social function of the behavior. Social scratch was directed mostly to the dorsal side of the body. However, when lactating females social scratched to infants or juveniles, they scratched other body parts. Social scratch was not lateralized to left or right. We present four hypotheses on the functional origin and on the learning process of this cultural behavioral pattern.

Hand preference in a captive island group of chimpanzees (Pan troglodytes).

Morphological cerebral asymmetries in chimpanzee brains, similar to those found in humans, in whom they are associated with speech and handedness, suggest the possibility of functional lateralization in the chimpanzee. This possibility was investigated by examining hand preferences in an island group of five chimpanzees on a series of unimanual and bimanual tasks that are diagnostic of human hand and cerebral dominance. Each subject was tested in a double compartment cage on three unimanual nonsequential, three unimanual sequential, and three bimanual coordination tasks. One of the three unimanual sequential tasks was a bar-press task that is analogous to the commonly used human finger-tapping task. For the unimanual tasks, exclusive of the bar-press, the chimpanzees showed a highly individualistic pattern of hand preference that did not change as a function of task complexity. On the bar-press task, four of five subjects produced higher rates with one hand compared to the other; however, relative hand performance on this task was unrelated to hand preference on the other unimanual tasks. For the group of subjects, performance rates did not differ between the left and right hands; however, a practice effect was observed for the right hand in all subjects. The bimanual tasks also revealed a complex pattern of individual handedness, with no trends apparent for the group as a whole. Consistent with previous findings, the results from these tests on this group of five chimpanzees suggest that cerebral morphological asymmetries in the chimpanzee are not associated with motor dominance as reflected in handedness.