Male Hamadryas Research Articles

Osteology of the Hamadryas Baboon (Papio hamadryas).

Besides living as a free-ranging primate in the horn of Africa and the Arabian Peninsula, the hamadryas baboon has an important place in zoos and can be found in biomedical research centers worldwide. To be valuable as a non-human primate laboratory model for man, its anatomy should be portrayed in detail, allowing for the correct interpretation and translation of obtained research results. Reviewing the literature on the use of the baboon in biomedical research revealed that very limited anatomical works on this species are available. Anatomical atlases are incomplete, use archaic nomenclature and fail to provide high-definition color photographs. Therefore, the skeletons of two male hamadryas baboons were prepared by manually removing as much soft tissues as possible followed by maceration in warm water to which enzyme-containing washing powder was added. The bones were bleached with hydrogen peroxide and degreased by means of methylene chloride. Photographs of the various bones were taken, and the anatomical structures were identified using the latest version of the Nomina Anatomica Veterinaria. As such, the present article shows 31 annotated multipanel figures. The skeleton of the hamadryas baboon generally parallels the human skeleton, but some remarkable differences have been noticed. If these are taken into consideration when evaluating the results of experiments using the hamadryas baboon, justified conclusions can be drawn.

Analysis of the Ability to Skill Formation and Stability of the Formed Skill in Mature Male Rhesus Monkeys (Macaca mulatta) and Hamadryas Baboons (Papio hamadryas).

A comparative study of the ability to form a skill, the dynamics of its formation, and repeatability in sexually mature male rhesus monkeys (Macaca mulatta) and hamadryas baboons (Papio hamadryas) was carried out. It was found that male hamadryas baboons of the study group demonstrate higher learning ability, training level, and repeatability of the formed skill compared to the studied male rhesus monkeys. At the same time, animals of both species demonstrated similar dynamics of skill formation.

Respect for males amid suppression of females: Selective use of aggression and fitness correlates in the male-dominated society of hamadryas baboons

Hamadryas baboons (Papio hamadryas) are a useful model for human social evolution for multiple reasons, including their multilevel society, intense cross-sex bonds, and intermale tolerance. Their most stable social grouping, the one-male unit (OMU)—comprising a leader male, females, and sometimes follower males—is formed via successive takeovers of individual females by males. While takeovers occur via both aggressive and non-aggressive mechanisms, aggressive herding is common during and after takeovers and appears crucial in maintaining OMUs. Here we use behavioral and demographic data from Filoha, Ethiopia to examine the relationship between aggressive takeovers and fitness correlates. We found no relationship between a male's percentage of takeovers that were aggressive and his presumed number of infants sired, nor his number of females or followers. However, we did find that a leader male's average intensity of aggression toward both other males and females around the time of a takeover was negatively related to his presumed number of infants sired. In addition, a leader male's average intensity of aggression toward other males was negatively related to his maximum number of followers. Finally, leader males exhibited more intense aggression toward females in interband, compared to intraband, takeovers. Our findings suggest that (1) leader males who limit their aggression toward other males may have greater success in attracting followers, thereby increasing their fitness via enhanced defense of the OMU; (2) exceptionally aggressive takeovers may lead to lower birth rates via female reproductive suppression; and (3) the extent to which males use aggression toward females depends on the context in which the takeover occurs. Overall, these results both suggest that hamadryas males use aggression selectively and underscore the ubiquity of intermale tolerance and female suppression in the hamadryas social system. This study lends insight into the interplay between male–female and male–male social dynamics during human evolution.

Сравнение способности к обучению макаков резусов ( Macaca mulatta ) и павианов гамадрилов ( Papio hamadryas ) в свете создания модели когнитивной эволюции приматов

A comparative study of the learning ability in two species of lower monkeys, rhesus monkeys (Macaca mulatta) and hamadryas baboons (Papio hamadryas), was used as a hypothetical model for the development of cognitive abilities in primates during such an evolutionary event as the transition from an arboreal lifestyle to a terrestrial one. It was found that in male rhesus monkeys the average level of learning was 68.5 ± 5.8%, in male hamadryas baboons - 78.0 ± 3.1%. The median of the distribution of learning, which characterizes the maximum number of continuous correct decisions, in rhesus monkeys is 17.0% (interquartile range, IQR = 11.0); in hamadryas baboons - 40.0% (IQR = 15.5). In the studied groups of monkeys, certain differences were found in the dynamics of skill formation. Our results illustrate the advantages of terrestrialism as a factor contributing to evolution towards rationality, and are in the best possible way with the ecological hypothesis of the development of cognitive abilities.

Fluorescence imaging in evaluating the revascularization of heterotopically transplanted primate trachea segment

Objective:to assess the potentials of using indocyanine green fluorescence angiography in evaluating revascularization of tissue-engineered construct that was obtained from the decellularized biological matrix of primate trachea, including using mesenchymal stem cells, after heterotopic tracheal allotransplantation.Material and methods.Tracheas were obtained from two male hamadryas baboons. After decellularization, 4 cm segments of tracheas were implanted under the lateral part of the latissimus dorsi in two healthy primates, one after recellularization with mesenchymal stem cells (animal 1), and the second without recellularization (animal 2). Immunosuppressive therapy was not performed. Blood flow in the transplanted segment of the trachea was evaluated 60 days after transplantation by surgical isolation of the flap of the latissimus dorsi with the transplanted segment of the trachea, while maintaining blood flow through the thoracodorsal artery. Indocyanine green near-infrared fluorescence angiography was visualized using a FLUM-808 multispectral fluorescence organoscope.Results.Sixty days after implantation, the tracheal cartilaginous framework macroscopically appeared to be intact in both animals, tightly integrated into the muscle tissue. The framework retained its natural color. After intravenous injection of indocyanine green, the tracheal vessels were visualized in both animals. Intercartilaginous vessels and portions of the cartilaginous semi-rings devoid of vessels were clearly distinguished. The entire implanted segment was almost uniformly vascularized. No local disruptions in blood supply were observed. The fluorescence brightness of the tracheal vessels was 193 ± 17 cu and 198 ± 10 cu in animals 1 and 2, respectively. The average muscle brightness in the implantation zone was 159 ± 9 cu and 116 ± 8 cu in animals 1 and 2, respectively.Conclusion. Indocyanine green fluorescence angiography is characterized by high-contrast images and high sensitivity. This facilitates vascular patency visualization and allows to assess the degree of neoangiogenesis after experimental transplantation of the tracheal segment, at different stages of experiment, without euthanizing the animal.

Comparison of the Cognitive Capacities of Immature and Young Mature Male Hamadryas Baboons

Studies of the dynamics of cognitive processes in experiments on primates can be useful for establishing the biological roots of mental processes occurring in adolescents. Experiments were performed using 12 male hamadryas baboons (Papio hamadryas) aged from 45 to 67 months. Levels of cognitive capacities were determined in males using the following tests: tests for the ability to establish the position of a reward in space, which can be defined as “spatial” tests; tests for learning ability; a test for exploratory activity. Results obtained from comparison of cognitive capacities in immature and young mature male hamadryas baboons showed that some of the cognitive capacities were age-dependent and that there was no synchronicity in the development of cognitive capacities. In particular, mature males were significantly more successful in solving “spatial” tests than males under the age of puberty. There were no differences in solutions to tests for exploratory activity and the ability to learn skills between immature and young mature males.

Correlation of Cognitive Abilities of Male Hamadryas Baboon with Age and Hierarchical Status.

We studied the correlation between the rank and age of baboons (n=12) with their cognitive abilities. A positive correlation was found between performances of different tests by male. The ability to solve the tests related to bait placement depended on the age of the males and age-related hierarchical status. Four-year-old males performed these tests in 52% of cases, whereas five-year-old males, who reached a higher hierarchical status by this age solved with them in 93% of cases. In the tests for exploratory activity and the ability to learn skills, the differences between the four-year-olds and the five-year-old males are not received.

Comparison between the anaesthetic effects of xylazine–ketamine and diazepam–ketamine: physiological and blood parameters in young hamadryas baboons (Papio hamadryas)

The objective of this study was to evaluate the anaesthetic effects on young hamadryas baboons (Papio hamadryas) of xylazine-ketamine (XK) compared to diazepam-ketamine (DK). Six healthy young male hamadryas baboons were first premedicated with xylazine HCl (0.5 mg/kg, IM) and anaesthetised 20 min later with ketamine (10 mg/kg, IM). After a 10-day washout period, the hamadryas baboons were premedicated with diazepam (1 mg/kg, IM) and anaesthetised 20 min later with ketamine (10 mg/kg, IM). The onset, duration, and the depth of anaesthesia were determined by recording palpebral, corneal, and jaw reflexes. The results showed a significant decrease in heart rate and rectal temperature after XK injection, while a significant reduction in respiratory rate was seen when using the DK protocol. A highly significant increase in the levels of glucose was observed with the XK regimen. Blood pressure decreased when using both anaesthetic regimens, but this reduction did not reach significant levels. The quality of recovery was better when using XK compared to DK. In conclusion, major complications including bradycardia, hypothermia, and hyperglycaemia should be considered with a combination of XK. However, no complications other than bradypnea and hypercapnia should be expected when immobilising young hamadryas baboons with DK. No significant difference was observed in CBC, electrolytes, or lactate level between the anaesthesia protocols.

Contexts and consequences of takeovers in hamadryas baboons: Female parity, reproductive state, and observational evidence of pregnancy loss.

The evolutionary consequences of sexual selection and sexual conflict are epitomized in the hamadryas baboon, a species characterized by strong sexual dimorphism and intense male-male competition. Hamadryas males coerce individual females into reproductively exclusive one-male units via aggressive takeovers, and infants involved in such takeovers are at least four times more likely to be killed (or otherwise die) after takeovers compared to other times. Here we examine female reproductive state before and after takeovers to further investigate the determinants of takeovers and their impact on female reproduction. Our data set consists of 162 takeovers over a period of 20 years in a population of wild hamadryas baboons at Filoha, Ethiopia. Results show that, in contrast to their polygynandrous relatives, hamadryas males show no bias with regard to female reproductive state at the time of the takeover, but are more likely to take over nulliparous compared to multiparous females. In addition, these results reinforce previous findings demonstrating the high likelihood of infant loss after hamadryas takeovers and suggest that females may use an additional strategy of pregnancy termination to curtail investment in offspring that are very likely to die anyway. Thus, hamadryas males may target females with high future reproductive value and hamadryas females may employ counterstrategies to help mitigate the effects of sexual coercion and infanticide on their own fitness.

The rise and fall of leader males in a multi-level society: takeovers and tenures of male Hamadryas baboons.

As one means to maximize access to females, males of some species are intolerant of other males in social units, resulting in female defense polygyny, a mating system in which one male monopolizes mating access to as many females as he can for as long as possible. In such a system, the length of a male's tenure and the number of females he is able to acquire are important predictors of his reproductive success. Hamadryas baboons differ from many other taxa with female defense polygyny in that they acquire and lose females individually, thus patterns of acquisition and loss of females over time are additional factors contributing to a male's fitness. Here, we describe longitudinal patterns of female acquisition and loss over a 9-year period in a group of 250 wild hamadryas baboons. Complete tenures of leader males ranged from 310 to 2,160 days (N = 13) and results from a survival analysis yielded a median tenure length of 2,160 days, or 6 years (N = 49). The total number of females acquired, which increased with tenure length, ranged from 1 to 14 and averaged 3.5, and leader males acquired females both opportunistically and via challenging other males. The interval between acquisition of successive females ranged from 0 to 1,196 days with a median of 203, and males acquired all of their females less than halfway into their tenure. Females from outside of a leader male's social sphere (clan and band) were acquired relatively later in their tenure compared to females from within a male's social sphere. Leaders typically lost females gradually during the latter part of their tenure or all (or most) at once, suggesting an inverted U-shaped longitudinal arc of male competitive ability.

The rejuvenating effects of leuprolide acetate on the aged baboon's thymus

BackgroundWe have previously demonstrated that the juvenile thymus plays an essential role in tolerance induced by both renal transplantation and a short course of calcineurin inhibitors. Aged thymi have a decreased ability to induce tolerance. Luteinizing hormone-releasing hormone (LHRH) is known to pharmacologically rejuvenate the thymus in rodents. In order to develop a clinically applicable regimen of transplantation tolerance in adults, we sought to determine if thymic rejuvenation would occur with LHRH agonism in non-human primates. Methods and resultsThymic rejuvenation was evaluated by magnetic resonance imaging (MRI), histology, as well as in-vitro cellular and molecular tests. Four aged male hamadryas baboons underwent subcutaneous injection of a 3-month depot of Lupron (11.25mg; LI) and were followed for 3months. Thymi increased volumetrically by MRI. After LI, thymic cellularity markedly increased within the cortical and medullary thymus. Additionally, a significant increase in the CD4+/CD45RAhi+ population in the peripheral blood occurred for 50days after LI, and flow cytometry of thymic tissue revealed a large increase in the percentage of CD4+/CD8+ cells. TREC assay corroborated enhancement in thymic function. ConclusionThese data indicate that LI is associated with thymic rejuvenation in baboons, and further confirm that extrinsic factors play an important role in thymic rejuvenation in a non-human primate model.

First report on Aonchotheca annulosa Dujardin, 1845 (Nematoda, Capillariidae) in a Hamadryas baboon (Papio hamadryas) from a zoo in northern Turkey

A dead male Hamadryas baboon, Papio hamadryas, from a zoo in Samsun in northern Turkey was submitted for necropsy examination. Standard techniques were performed for necropsy and for parasitic identification. A total of 14 nematodes were recovered from the small intestine. All nematodes were identified as Aonchotheca annulosa. This nematode is most often reported from murid rodents under natural conditions. To date, little is known about the occurrence of A.annulosa in monkeys, with the exception of a single report in a capuchin monkey. This is the first record of A.annulosa from P.hamadryas.

Communication and Cognition in Primate Group Movement

We here review the communicative and cognitive processes underpinning collective group movement in animals. Generally, we identify 2 major axes to explain the dynamics of decision making in animal or human groups or aggregations: One describes whether the behavior is largely determined by simple rules such as keeping a specific distance from the neighbor, or whether global information is also factored in. The second axis describes whether or not the individual constituents of the group have overlapping or diverging interests. We then review the available evidence for baboons, which have been particularly well studied, but we also draw from further studies on other nonhuman primate species. Baboons and other nonhuman primates may produce specific signals in the group movement context, such as the notifying behavior of male hamadryas baboons at the departure from the sleeping site, or clear barks that are given by chacma baboons that have lost contact with the group or specific individuals. Such signals can be understood as expressions of specific motivational states of the individuals, but there is no evidence that the subjects intend to alter the knowledge state of the recipients. There is also no evidence for shared intentionality. The cognitive demands that are associated with decision making in the context of group coordination vary with the amount of information and possibly conflicting sources of information that need to be integrated. Thus, selective pressures should favor the use of signals that maintain group cohesion, while recipients should be selected to be able to make the decision that is in their own best interest in light of all the available information.

Copulation patterns in captive hamadryas baboons: a quantitative analysis.

For primates, as for many other vertebrates, copulation which results in ejaculation is a prerequisite for reproduction. The probability of ejaculation is affected by various physiological and social factors, for example reproductive state of male and female and operational sex-ratio. In this paper, we present quantitative and qualitative data on patterns of sexual behaviour in a captive group of hamadryas baboons (Papio hamadryas), a species with a polygynous–monandric mating system. We observed more than 700 copulations and analysed factors that can affect the probability of ejaculation. Multilevel logistic regression analysis and Akaike’s information criterion (AIC) model selection procedures revealed that the probability of successful copulation increased as the size of female sexual swellings increased, indicating increased probability of ovulation, and as the number of females per one-male unit (OMU) decreased. In contrast, occurrence of female copulation calls, sex of the copulation initiator, and previous male aggression toward females did not affect the probability of ejaculation. Synchrony of oestrus cycles also had no effect (most likely because the sample size was too small). We also observed 29 extra-group copulations by two non-adult males. Our results indicate that male hamadryas baboons copulated more successfully around the time of ovulation and that males in large OMUs with many females may be confronted by time or energy-allocation problems.

Female “dispersal” in hamadryas baboons: Transfer among social units in a multilevel society

Unlike most cercopithecines, hamadryas baboons (Papio hamadryas hamadryas) are characterized by female-biased dispersal. To clarify this pattern within the context of their hierarchical social system (comprising one-male units, clans, bands, and troops), we report here 7 years of data on female transfers among social units in wild hamadryas baboons in Ethiopia. Female tenure in one-male units (OMUs) ranged from 1 to 2,556 days (N = 208) and survival analysis revealed a median tenure length of 1,217 days (40 months). Changes in OMU membership consisted almost exclusively of takeovers by males, not voluntary transfer. Of 130 takeovers, 67% occurred within the band and 33% across bands, and, of the 22 takeovers for which we have clan membership data, 77% occurred within, not between, clans. These results reinforce the notion that hamadryas female dispersal is not analogous to sex-biased dispersal in other taxa, because (1) at least in Ethiopian populations, females do not disperse voluntarily but are transferred, often forcibly, by males; (2) only dispersal between bands will promote gene flow, whereas females are most often rearranged within bands; (3) hamadryas females undergo social dispersal but not usually locational dispersal; and (4) while male hamadryas are far more philopatric than females, they have been observed to disperse. It thus appears that the ancestral baboon pattern of female philopatry and male dispersal has evolved into a system in which neither sex is motivated to disperse, but females are forcibly transferred by males, leading to female-mediated gene flow, and males more rarely disperse to find females.

Dominance relationships among male hamadryas baboons (Papio hamadryas)

The concept of dominance has been shown to be useful in describing and predicting social interactions in group-living animals. However, the dominance relationships among adult hamadryas males (Papio hamadryas) are poorly understood, and systematic data are missing from the literature. This study investigated dominance relationships among male hamadryas baboons by applying novel statistical techniques to systematic detailed data on agonistic interactions. We also analyzed the dominance relationship with male age and evaluated the association between dominance and access to mating partners (i.e. the number of adult females per one-male unit (OMU)), food resources (i.e. monopolization of feeding areas), and greeting interactions. The derived dominance indexes showed that, in general, leader males were dominant over followers, and that dominance ability did not correlate with male age. Individual dominance values were very close to each other, suggesting that dominance relationships among hamadryas males were not very rigid. In addition, dominance values were positively correlated with number of adult females per OMU but not with feeding priority. Finally, greeting interactions occurred more frequently between individuals with similar dominance values and with low levels of dominance decidedness. We suggest the need of further studies, especially in wild populations, to confirm our findings.

Cerebrospinal Fluid Monoaminergic Metabolites in Wild Papio anubis and P. hamadryas Are Concordant with Taxon-specific Behavioral Ontogeny

We used a cross-sectional sample to compare ontogenetic trajectories in the concentrations of monoamine neurotransmitter metabolites in cerebrospinal fluid of wild anubis (Papio anubis, n = 49) and hamadryas (P. hamadryas, n = 54) baboons to test the prediction that they would differ, especially in males, in association with their distinct behavioral ontogenies. Values of all 3 metabolites [3-methoxy-4-hydroxyphenylglycol (MHPG), the norepinephrine metabolite; 5-hydroxyindoleacetic acid (5-HIAA), the serotonin metabolite; and homovanillic acid (HVA), the dopamine metabolite] declined consistently with dentally-calibrated maturation, and few taxon-related differences were apparent among juveniles. Adult females were too few for adequate comparison, but a discriminant function suggested that they might differ by taxon. Adult males of the 2 species differed strikingly from juveniles and from each other. Contrary to our initial hypothesis, adult male anubis had significantly lower HVA and MHPG, and higher 5-HIAA levels, than predicted from the overall, age-related trend, and MHPG continued to decline with age among adults. As young adults, male hamadryas had low 5-HIAA and a high HVA/5-HIAA ratio, while older males [normatively one-male unit (OMU) leaders] showed a reversal in the trend, with 5-HIAA rising and the HVA/5-HIAA ratio tending to fall. We speculate that the results are related to the dispersing and philopatric ontogenies of anubis and hamadryas males, respectively. Adult male anubis, whose fitness depends on building social networks with nonkin, have high relative serotonin activity, commonly associated with greater social circumspection and skill. Young adult male hamadryas, living among agnatic kin and mating opportunistically, exhibit low 5-HIAA levels, generally associated with impulsivity and social irresponsibility. This reverses as a male approaches the age at which he is normatively the leader of a one-male unit (OMU), and his fitness depends on his maintaining stable relationships with other leaders and with females.

Post‐Conflict Non‐Aggressive Behaviours may be neither Friendly nor Conciliatory: Conflict Management of Male Hamadryas Baboons

AbstractThe relational model of conflict resolution predicts that after an aggressive conflict there should be a motivational shift from aggression to attraction. Most tests of the reconciliation hypothesis assume, however, that all non‐aggressive post‐conflict behaviours between former opponents are motivationally homogeneous and qualify as friendly reunions. In fact, although the hypothesis predicts an increased occurrence of friendly contacts after conflicts, in practice, however, post‐conflict reunions often include a mixture of contact and non‐contact behaviours. Most reconciliation studies either (often) assume a conciliatory function for post‐conflict reunions or (less often) test functional predictions. Finally, the valuable relationships hypothesis predicts that conciliatory rates should be relatively higher between friends and allies than between non‐friends/allies. In this paper, we use data on non‐aggressive interactions following conflicts between adult male hamadryas baboons that are neither friends nor allies to assess the implications of all these important but largely overlooked issues. The analyses of the rate and temporal relation of non‐contact greeting (NCTG) to anxiety‐related behaviours and side‐directed aggression as well as of the behaviours used during non‐aggressive interactions with male and female third‐parties suggest that the NCTG used by males after conflicts were neither motivationally friendly nor functionally conciliatory. We point out that the gestures exchanged during these post‐conflict NCTG can be interpreted as formalized signals of equal status and that the rate and form of the greetings used by male opponents are indicative of high relationship insecurity and incompatibility respectively. We conclude that although male hamadryas’ post‐conflict NCTG are not conciliatory they may serve to assess their opponents’ attitude and to negotiate the restoring of their pre‐conflict levels of peaceful but non‐amicable co‐existence.

Function of Notification in Papio hamadryas

Notification is a form of ritualized greeting behavior performed by adult male hamadryas baboons (Papio hamadryas). Originally observed in the wild when harem leaders signaled the direction of travel to their followers on daily foraging marches, its true function is unknown. Notification involves the approach of an adult male baboon to another male, the presentation of his hindquarters, then retreat. Researchers have previously linked notification to aggression avoidance, appeasement, and the dominance-subordination relationship between males. We observed instances of notification over 6 mo among 8 adult males in a troop of 61 captive-bred hamadryas baboons at Paignton Zoo Environmental Park, Devon, UK. We compared observation sessions in which notification occurred with matched control periods. We classified different forms of notification according to the recipient’s response: presenting, mounting, touching of the buttocks or genitals, or ignoring. Results suggest that different forms of notification may have different functions, including submission, alliance, and peacekeeping but not general greeting, recruitment, or appeasement.

Behavioral variation and reproductive success of male baboons (Papio anubis × Papio hamadryas) in a hybrid social group

We take advantage of an array of hybrid baboons (Papio anubis x Papio hamadryas) living in the same social group to explore the causes and consequences of different male mating strategies. Male hamadryas hold one-male units and exhibit a sustained, intense interest in adult females, regardless of the latter's reproductive state. Anubis baboons, by contrast, live in multi-male, multi-female groups where males compete for females only when the latter are estrous. These two taxa interbreed to form a hybrid zone in the Awash National Park, Ethiopia, where previous work has suggested that hybrid males have intermediate and ineffective behavior. Here, we first examine male mating strategies with respect to morphological and genetic measures of ancestry. We found significant relationships between behavioral measures and morphology; males with more hamadryas-like morphology had more hamadryas-like behavior. However, genetic ancestry was not related to behavior, and in both cases intermediates displayed a previously unreported level of behavioral variation. Furthermore, male behavior was unrelated to natal group. Second, we evaluated reproductive success by microsatellite-based paternity testing. The highest reproductive success was found for individuals exhibiting intermediate behaviors. Moreover, over nine years, some genetically and morphologically intermediate males had high reproductive success. We conclude that the behavior of hybrid males is therefore unlikely to be an absolute barrier to admixture in the region.