Male Chimpanzees Research Articles

Identification of a protanomalous chimpanzee by molecular genetic and electroretinogram analyses

We determined the structures of long (L)-wavelength-sensitive and middle (M)-wavelength-sensitive opsin gene array of 58 male chimpanzees and we investigated relative sensitivity to red and green lights by electroretinogram flicker photometry. One subject had protanomalous color vision, while others had normal color vision. Unlike in humans, a polymorphic difference in the copy number of the genes and a polymorphic base substitution at amino acid position 180 were not frequently observed in chimpanzees.

Cryo-banking of great ape spermatozoa using human protocols and variation among males

To develop a resource of great ape sperm cells and test the hypothesis that great ape males, like human males, differ in production of sperm cells and in rates of sperm cell survival after exposure to similar processing for cryopreservation. Prospective trial in a cohort of normal male chimpanzees. Seven male chimpanzees ranging in age from 9.9 to 24.2 years were trained to provide semen samples using an artificial vagina. Samples were removed from the plastic sleeve of the device and placed into conical centrifuge tubes. The liquid fraction of semen was removed within 30 minutes and mixed with an equal volume of human commercial transport medium containing egg yolk and buffer (Refrigeration Medium, Irvine Scientific). Samples were transported to the andrology lab for semen analysis and cryopreservation. Briefly, the diluted semen was assayed, then mixed with an equal volume of glycerol containing cryopreservation medium (Freezing Medium, Irvine Scientific) and loaded into half cc straws with labeled handles. Straws were placed into a controlled-rate, nitrogen vapor freezing machine for slow cooling to -7 degrees C, seeding, cooling to -80 degrees C at -10 degrees/min and plunging into liquid nitrogen. A straw from each sample was subsequently thawed, diluted with culture medium, concentrated by centrifugation, and diluted to the original volume of the straw for assay of motility via CASA system. During a 20-month interval 93 semen samples from seven males were obtained for analysis and potential cryopreservation. Individual males provided between 5 and 29 samples. Males differed significantly (pyr<0.000005) in the number of sperm cells provided in each sample from averages of 79, 88, 454, 1858, 1138, 678, and 1640 million and in the percentage of motile cells available for cryopreservation from averages of 48, 4, 32, 27, 13, 18, and 47 percent. Between 5 and 26 samples were cryopreserved for each male. The ratio of progressive motility after thaw and washing compared to pre-freeze levels differed (p=0.03) between males (0.43, 0.16, 0.33, 0.23, 0.41, 0.30, and 0.17) and was not related to number of sperm in the ejaculate or the initial motility. Currently, 531 straws with estimated yields after thaw of 3,686 million motile cells have been banked for research uses and seven males are trained to provide samples on demand. These procedures have been extended to another great ape species, the bonobo. Male chimpanzees of varying ages can be trained to provide semen samples for analysis, research, and cryopreservation. Once trained, animals can be induced with rewards to provide samples on a regular basis. A cryo-bank has been developed with sperm cells from seven males. Even with delays of 3 to 6 hours between collection and initiation of processing for cryopreservation, progressively motile sperm cells survive standardized cryopreservation and thawing protocols. However, sperm survival rates vary significantly among males.

Dominance rank and fecal testosterone levels in adult male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda.

In an attempt to describe hormone-behavior interactions in a sample of wild male chimpanzees, we quantified testosterone in 67 fecal samples obtained from 22 adult male chimpanzees at Ngogo, Kibale National Park, Uganda. A mixed-model methodology that controlled for age-class identified a significant positive association between testosterone levels and dominance rank. The results are consistent with those reported from a separate, smaller chimpanzee community in the same population in a study that analyzed testosterone levels in urine [Muller & Wrangham, 2004]. As in that earlier study, our results held during a period of social stability, which is not consistent with predictions of the "challenge hypothesis." We concur with Muller and Wrangham [2004] that the challenge hypothesis requires modification to explain the chimpanzee data, because fission-fusion sociality in chimpanzees makes challenges unpredictable. We also discuss the utility of fecal samples and a mixed-model statistical method for behavioral endocrinology studies.

Why do male chimpanzees defend a group range?

Male chimpanzees, Pan troglodytes, cooperate to defend a community range within which resident females range in smaller core areas. There has been debate over exactly what males are defending, whether mates, territory or both. One hypothesis holds that males are defending mates, and that an increase in community range size will lead directly to the acquisition of more females. However, males frequently attack females as well as males at the edge of the community range. We examined 18 years of observational data on the Gombe chimpanzees to determine the behaviour of males during extragroup encounters, and the consequences of changes in community range size on the number of adult females and indirect measures of food availability. Males were always aggressive to males from other communities, and often attacked adult females, especially those that were not sexually receptive, were older, and/or had more than one offspring. The number of females did not increase with range size, but several measures suggested an increase in food availability with range size. These measures include more time spent in large foraging parties, higher encounter rates with resident females, more encounters with sexually receptive females and higher female reproductive rates. These findings suggest that males defend a feeding territory for their resident females and protect them from sexual harassment. Although a large range may eventually attract more females, this is not an immediate consequence of range expansion. Male number was not correlated with community range size.

Intracommunity Coalitionary Killing of an Adult Male Chimpanzee at Ngogo, Kibale National Park, Uganda

Intercommunity coalitionary killing of adult and adolescent males has been documented in two chimpanzee communities in the wild, and it was strongly suspected in a third. It may increase survivorship for the attackers, their mates, and their offspring by reducing the combined strength of hostile neighbors and/or by increasing territory size and food availability, and it may help the attackers to attract mates. Lethal coalitionary attacks by males on other male members of their own communities would not provide these benefits and are not expected, given the importance of cooperation among male community members in contests for dominance rank and in both defense and offense against neighboring males. Nevertheless, intracommunity coalitionary killings associated with struggles for alpha rank occur in the wild and in captivity, and observers have seen serious gang attacks on maturing adolescent and young adult males at Mahale and Budongo: the victim in the Budongo case was killed (Fawcett and Muhumuza, 2000). I describe a lethal attack on a young adult male by a large coalition of males from his community at Ngogo, Kibale National Park, Uganda. The Ngogo community is the largest known for chimpanzees and has an unusually large number of males. The attack was not related to a struggle for alpha rank: the victim was low-ranking and the community had a well-established alpha at the time. However, the victim had risen substantially in the male hierarchy over the past few years and might have appeared threatening to many higher-ranking males. Simultaneously, he associated relatively little with most other adult males, had relatively few grooming partners and was not well integrated into the male grooming network, and had no influential allies. The combination of these social factors with the unusual demographic circumstances – which presumably meant that mating competition was relatively high and the cost of losing one male relatively low – might have triggered the attack.

Wild Chimpanzees Produce Group‐Specific Calls: a Case for Vocal Learning?

AbstractVocal learning, where animals can modify the structure of their vocalizations as a result of experience, has been found in a range of birds and mammals. Although vocal learning is a fundamental aspect of developing spoken language, there is as yet little evidence that vocal learning occurs in primates. Here we examine whether vocal learning may occur in chimpanzees. We analysed whether wild male chimpanzees,Pan troglodytes verus,of four communities living in a similar habitat in the Taï Forest, Côte d'Ivoire, developed community specific pant hoots. If so, we expected males of three contiguous communities to have distinct pant hoots, while pant hoots of males from a fourth, distant community, located 70 km away, should only differ from those of the contiguous communities by chance. Our analysis confirmed these expectations. In addition, the acoustic distances between the pant hoots of pairs of individuals did not correlate with the genetic relatedness of those pairs, where genetic relatedness was determined using nuclear DNA analysis. Thus, neither habitat nor genetic differences accounted for the observation that there were acoustic differences in the pant hoot structure of males living in neighbouring communities, but not in those of males from a distant community. This suggests that chimpanzees may actively modify pant hoots to be different from their neighbours, providing support for the vocal learning hypothesis.

Behavioral Evidence for the Cutaneous Expression Of Emotion in a Chimpanzee (Pan Troglodytes)

AbstractSelf-directed behaviors (SDBs) are behavioral indicators of stress, but have received relatively little experimental scrutiny. The present study reports the distribution of SDBs in a 14-year-old male chimpanzee in relation to performance on a matching-to-sample task of varying difficulty. The rate of rubbing behaviors (self-touching with the hand without any raking motion of the fingernails) was positively correlated with performance, whereas scratching rates were negatively correlated with performance. SDBs were displayed predominantly with the left hand during sessions of high performance (low task difficulty), with a shift toward the right hand during sessions of low performance (high task difficulty). SDBs were exhibited relatively more with the right hand after incorrect responses (and secondary negative reinforcer) than after correct responses (and secondary positive reinforcer). Rubs directed to the face were displayed relatively more often to the right side after incorrect responses, compared to rubs displayed after correct responses, whereas scratching was directed relatively more often to the left side of the body after incorrect responses, compared to scratching displayed after correct responses. Rough scratching was displayed more quickly after auditory feedback on performance than were rubs or gentle scratches. Rubs were directed more to the face (trigeminal) and scratches more to the body (spinothalamic). Taken together, these results suggest that there may be asymmetrical central nervous system processing of negative emotion by chimpanzees during cognitive tasks.

Further evidence of a right hand advantage in motor skill by chimpanzees ( Pan troglodytes)

Asymmetries in motor skill when grasping small food items was evaluated in a sample of captive chimpanzees. In two experiments, error rates in grasping food were assessed when controlling for individual differences in grip morphology. In both experiments, chimpanzees were found to make more errors with the left compared to the right hand. Male chimpanzees were also found to make more errors compared to females. These results are discussed in the context of a presumed disassociation between hand preference and performance as indicators of cerebral dominance in motor functions.

Anesthetic Protocol For The Surgery On A Chimpanzee (Pan troglodytes)

An anesthetic protocol was designed for a 19 year-old mature male chimpanzee whose anesthetic risk was classified as ASA 3. His body weight was 65 kg. The scheduled surgical intervention was an amputation of the opposed finger of the right inferior extremity due to osteomyelitis caused by trauma with partial exposition of the phalange. The infection was approximately 10-12 days old.

Dominance, aggression and testosterone in wild chimpanzees: a test of the ‘challenge hypothesis’

The ‘challenge hypothesis’ posits that variation in male testosterone levels is more closely associated with aggression in reproductive contexts than it is with changes in reproductive physiology. Numerous bird studies support this idea, but few tests have been conducted with primates. We conducted behavioural observations and noninvasive hormone sampling of 11 male chimpanzees, Pan troglodytes schweinfurthii, in the Kanyawara study site, Kibale National Park, to test predictions of the challenge hypothesis. Results indicated that adult male chimpanzees showed significant testosterone increases during periods when parous females showed maximally tumescent sexual swellings. These periods were also marked by increased rates of male aggression. Male testosterone levels did not increase in the presence of maximally tumescent nulliparous females. Such females are less attractive to males: they are not mate-guarded, nor do rates of male aggression increase when they are swelling. Male chimpanzees copulate with parous and nulliparous females at similar rates, however, suggesting that testosterone increases in the presence of cycling parous females are associated with aggression rather than sexual behaviour. High-ranking chimpanzees were more aggressive than low-ranking males and produced higher levels of urinary testosterone. Thus, the predictions of the challenge hypothesis were generally upheld. This suggests that the hypothesis may have wider applicability among primates, including humans.

Dominance, cortisol and stress in wild chimpanzees ( Pan troglodytes schweinfurthii )

Field studies of endocrine function in a range of social mammals suggest that high dominance rank is commonly associated with elevated glucocorticoid production. This is puzzling, because in stable dominance hierarchies, high status is normally associated with social control and predictability, key predictors of low psychological stress. One solution to this problem may be that high rank is commonly associated with elevated energetic expenditure, leading to increased metabolic stress and glucocorticoid secretion. We conducted behavioural observations and non-invasive hormone sampling of male chimpanzees in Kibale National Park, Uganda, to examine the relationship between cortisol, dominance and stress in wild chimpanzees. Results indicate that male dominance rank positively correlated with urinary cortisol excretion in a stable dominance hierarchy. Cortisol excretion also correlated positively with rates of male aggression. We suggest that the relationship between cortisol and rank in chimpanzees may be driven by energetic factors rather than psychosocial ones. This interpretation is supported by the observation that urinary cortisol levels correlated negatively with food availability. These findings suggest that dominant chimpanzees experience significant metabolic costs that must be set against the presumed reproductive benefits of high rank. Metabolic stress may mediate the relationship between rank and cortisol in other social mammals.

Intergroup Relations in Chimpanzees

▪ Abstract In the 1970s, researchers provided the first detailed descriptions of intergroup conflict in chimpanzees. These observations stimulated numerous comparisons between chimpanzee violence and human warfare. Such comparisons have attracted three main objections: (a) The data supporting such comparisons are too few, (b) intergroup aggression is the result of artificial feeding by observers, and (c) chimpanzee data are irrelevant to understanding human warfare. Recent studies provide strong evidence against these criticisms. Data from the five long-term sites with neighboring groups show that intergroup aggression is a pervasive feature of chimpanzee societies, including sites where artificial feeding never took place. Recent studies have clarified questions about the functional goals and proximate mechanisms underlying intergroup aggression. Male chimpanzees compete with males in other groups over territory, food, and females, base their decisions to attack strangers on assessments of numerical strength, and strive for dominance over neighboring groups. Human males likewise compete over territory, food, and females and show a preference for low-risk attacks and intergroup dominance. Chimpanzee studies illustrate the promise of the behavioral biology approach for understanding and addressing the roots of violence in our own species.

Behavioural development in a matching-to-sample task and token use by an infant chimpanzee reared by his mother.

We investigated the behavioural and cognitive development of a captive male infant chimpanzee, Ayumu, raised by his mother, Ai. Here we report Ayumu's achievements up to the age of 2 years and 3 months, in the context of complex computer-controlled tasks. From soon after birth, Ayumu had been present during an experiment performed by his mother. The task consisted of two phases, a matching-to-sample task in which she received token rewards, and the insertion of these tokens into a vending machine to obtain food rewards. Ayumu himself received no reward or encouragement from humans for any of the actions he exhibited during the experiment. At the age of 9 months and 3 weeks, Ayumu performed his first matching-to-sample trial. At around 1 year and 3 months, he began to perform them consistently. Also during this period, he frequently stole food rewards from his mother. At 2 years and 3 months, Ayumu succeeded for the first time in inserting a token into the vending machine. Once he had succeeded in using a token, he performed both phases of the task in sequence 20 times consecutively. The infant's behaviour was not shaped by food rewards but by a strong motivation to copy his mother's behaviour. Our observations of Ayumu thus mirror the learning processes shown by wild chimpanzees.

Diurnal patterns of urinary steroid excretion in wild chimpanzees.

Urinary testosterone and cortisol concentrations were quantified in a large number of samples (>500) collected from wild male chimpanzees (n=11) over the course of 1 year. For both steroids, urinary concentrations were higher and more variable in the morning than in the afternoon. Urinary creatinine levels showed no such diurnal pattern. These patterns are consistent with studies of steroid excretion in humans and gorillas. This study emphasizes the importance of considering time of day as a confounding variable in field studies of primate endocrine function. It also suggests that if a small number of samples are to be used to characterize an individual's basal steroid levels, afternoon samples may be preferable because they show less intra-individual variability.

Context-specific calls in wild chimpanzees, Pan troglodytes verus: analysis of barks

Context-specific calls, which have a distinct acoustic structure and are selectively produced in specific contexts, are a prerequisite for calls that function referentially. Functionally referential calls, which convey information to conspecifics about objects and events in the external world, have been found in a number of species, notably primates. Evidence of context-specific calls in apes, however, is largely absent. We analysed whether the barks of wild male chimpanzees in the Taı Forest, Côte d'Ivoire, are context specific. We examined the acoustic structure of barks, and other calls produced in association with barks, in six contexts, using discriminant function analysis. Chimpanzees produced context-specific signals in two ways. First, they produced two acoustically graded bark subtypes, in hunt and snake contexts, respectively. Second, they produced context-specific signal combinations of barks with acoustically different call types or drums. These signal combinations increased specificity levels in three of the six contexts to over 90%, a level similar to the classic vervet monkey, Cercophithecus aethiops, predator alarm calls. Furthermore, specific chimpanzee signals were produced in contexts other than alarm, such as travel and hunting, where the potential benefits of evolving specific calls are less obvious. These signals may convey specific context information to listeners, and thus function referentially; however, to confirm this, analyses of listeners' responses are required. The results show that two strategies for producing context-specific signals seem to have evolved in a species other than humans: chimpanzees produce context-specific bark subtypes and context-specific signal combinations. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.

&lt;Note&gt; Eleven-Year Old Male Chimpanzee Outranks Ex-Alpha Adult Male at Bossou

Dominance among chimpanzees (Pan troglodytes) is usually measured by the pant-grunting vocalization directed from the subordinate to the dominant (1, 2). Although a linear dominance hierarchy exists among most adult males, some dyadic relationships are ambiguous (1, 3). In contrast, there is a distinctive social gap between adult males and adolescent males, i.e. all adolescents pant-grunt to all adults (4). Adolescence in male chimpanzees is thus a period between sexual maturity and social maturity which is achieved at about 15 years of age (5, 6, 7 but see 8). We report here the case of YL, a young male at Bossou, who outranked an old ex-alpha adult male TA and became the beta male at the age of 11 years, and who also showed insubordination to the alpha male FF.

&lt;Note&gt; A Case of Infant Carrying by an Adult Male Chimpanzee in the Budongo Forest

&lt;Note&gt; A Case of Infant Carrying by an Adult Male Chimpanzee in the Budongo Forest

A longitudinal study on hand and wrist skeletal maturation in chimpanzees ( Pan troglodytes), with emphasis on growth in linear dimensions.

Skeletal maturation in the chimpanzee hand and wrist (the RUS system; radius, ulna, and short bones) was studied both longitudinally and cross-sectionally. Maturity states were evaluated in each of the 13 bones of the RUS system based on the TW2 method (Tanner and Whitehouse method), and the RUS score was calculated by the summation of scores for these bones. Individual variation was examined by means of residual curves and pseudo-velocity curves of RUS score and anterior trunk length (ATL). Norms of the age change pattern in RUS skeletal maturation and the growth of ATL were determined for each sex, and the relationships among ATL growth and skeletal and reproductive maturation were examined. We found a fairly good relationship between ATL growth and RUS skeletal maturation. Comparison of growth and development between humans and chimpanzees showed that growth characteristics are coupled with each other at puberty in male chimpanzees and in both sexes of humans. Although nutritional condition influenced ATL growth in infancy, it had no effect on the RUS maturational process. Social relationships appeared to influence both ATL growth and RUS maturation. Analyses on relationships between RUS skeletal maturation, ATL growth, and reproductive maturation, showed that RUS skeletal maturation is a good indicator of "physiological age".

Behavioral evidence of color vision deficiency in a protanomalia chimpanzee (Pan troglodytes).

Although color vision deficiency is very rare among Old World monkeys and apes, one male chimpanzee (Lucky) was identified as protanomalous by genetic and physiological analyses. This study assessed behavioral phenotypes of Lucky and four chimpanzees with normal color vision by discrimination task using the modified Ishihara pseudo-isochromatic plates. Lucky could not discriminate the stimuli that the other chimpanzees could. This is the first behavioral evidence of color vision deficiency in chimpanzees.

Urinary Testosterone Metabolite Levels in Bonobos: A Comparison with Chimpanzees in Relation to Social System

[Bonobo ( Pan paniscus ) social structure is characterized by partial female dominance, in contrast to the male dominated chimpanzee ( Pan troglodytes ) society. Furthermore, female bonobos exhibit more overt aggressiveness and a prolonged period of proceptivity during menstrual cycle compared to chimpanzees. Since dominance, aggressiveness and proceptivity are suggested to relate to high T levels, we expected T concentrations of bonobo females to be high. To test this, urinary T metabolite concentrations (measured by immunoreactive 5αandrostane-17α-ol-3-one) were determined, which reliably reflect T status in both species. We predicted a larger overlap between T metabolite concentrations of both sexes in bonobos compared to chimpanzees. Our results support this hypothesis. However, interspecific comparison for each sex revealed substantially lower T metabolite concentrations in bonobo males than in chimpanzee males, while female bonobos displayed levels about equal to those of chimpanzee females. It thus appears that low T metabolite levels in bonobo males are responsible for the large overlap instead of high T metabolite levels in bonobo females. In conclusion, this study suggests that quantitative sex differences in T levels may be predictive of social system. However, partial female dominance in bonobos is probably not mediated by high female T levels. Rather it appears that T levels of mainly male bonobos are adapted to social organization. We hope that these preliminary results ignite further research in this novel area., Bonobo ( Pan paniscus ) social structure is characterized by partial female dominance, in contrast to the male dominated chimpanzee ( Pan troglodytes ) society. Furthermore, female bonobos exhibit more overt aggressiveness and a prolonged period of proceptivity during menstrual cycle compared to chimpanzees. Since dominance, aggressiveness and proceptivity are suggested to relate to high T levels, we expected T concentrations of bonobo females to be high. To test this, urinary T metabolite concentrations (measured by immunoreactive 5αandrostane-17α-ol-3-one) were determined, which reliably reflect T status in both species. We predicted a larger overlap between T metabolite concentrations of both sexes in bonobos compared to chimpanzees. Our results support this hypothesis. However, interspecific comparison for each sex revealed substantially lower T metabolite concentrations in bonobo males than in chimpanzee males, while female bonobos displayed levels about equal to those of chimpanzee females. It thus appears that low T metabolite levels in bonobo males are responsible for the large overlap instead of high T metabolite levels in bonobo females. In conclusion, this study suggests that quantitative sex differences in T levels may be predictive of social system. However, partial female dominance in bonobos is probably not mediated by high female T levels. Rather it appears that T levels of mainly male bonobos are adapted to social organization. We hope that these preliminary results ignite further research in this novel area.]