Early sexual maturity in male hamadryas baboons (Papio hamadryas hamadryas) and its reproductive implications

We present data on sexual maturity in young hamadryas baboon males (Papio hamadryas hamadryas) and its reproductive consequences in a large captive baboon colony. Hamadryas baboons live in a multilevel social system, with one-male units (OMUs) as the smallest social entity. Male leaders of OMUs are believed to monopolize matings within their OMUs; hence mating is believed to be polygynous and monandrous. In a captive colony of hamadryas baboons, we found evidence that young males less than 4 years old fathered at least 2.5% of 121 offspring born subsequent to vasectomy of all adult males, and males aged 4-5 years fathered at least 16.5% of the offspring. Additional evidence that these young males are able to sire offspring came from a morphological comparison of sperm from hamadryas males of different ages. The sperm of a 48-month-old hamadryas baboon were morphologically indistinguishable from viable sperm from adult males, whereas sperm from a 45-month-old male showed some aberrations. If successful copulations by adolescent males constitute a regular pattern even in free-ranging hamadryas baboons, a hamadryas male's chances to reproduce would not be limited to his role as an OMU leader as previously assumed, and a male's reproductive career would consist of two phases: the adolescent phase, and the OMU leader male phase.     

One-male units and clans in a colony of hamadryas baboons (Papio hamadryas hamadryas): effect of male number and clan cohesion on feeding success

In the multilevel societies of hamadryas baboons, adult males can be attached to single one-male units (OMUs) or to clans containing several such OMUs. This paper examines the effect of male number and rivalry between males within a clan on their ability to compete for access to a clumped food resource. The data come from a study of a multilevel colony of hamadryas baboons (Papio hamadryas hamadryas) housed at the Madrid Zoo. The colony consisted of 12 harem-holding males and 40 sexually mature females, and was organized into five single OMUs and two clans (containing three and four OMUs, respectively). The top-ranking male of one of the clans was removed and later reintroduced, so the study involved an analysis of the composition of clans and OMUs and of the males' use of the feeding area across three study periods: preseparation, separation, and reintroduction. The findings reported indicate that both males and females derived clear advantages in the context of contest competition for access to clumped food if they were members of clans, because the males and females from large clans had a feeding advantage over those from smaller clans and single OMUs. Furthermore, rivalry among males within the clan reduced their ability to compete for food against males outside their clan. This paper provides empirical evidence for one of the potential advantages that hamadryas males may enjoy if they are attached to clans, and also provides empirical support for the general hypothesis that a large number of males in a group may provide fitness-related benefits to the group members, provided they are able to cooperate with each other.     

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.     

A study on the social structure and dispersal patterns of hamadryas baboons living in a commensal group at Taif,Saudi Arabia

Three levels of hamadryas social structure—the one male unit (OMU), the band, and the troop—have been observed at all sites studied, but a fourth—the clan—has been observed at only one site, Erer-Gota, Ethiopia, during a longitudinal check of the dispersion of identified individuals. The clan is important since it appears to provide the basis for male philopatry, although comparative data is needed from other sites to confirm this. We studied a huge commensal group of hamadryas baboons (over 600 animals) in Saudi Arabia. We put ear tags on baboons between 1998 and 2004 and analyzed social structure, relying on the interactions of these tagged animals by focusing especially on their dispersal patterns from OMUs. OMU membership tended to be looser than that of the Ethiopian hamadryas. Females tended to shift between OMUs on an individual basis in our study group, whereas the collapse of an OMU was a major occasion of adult female transfer in Ethiopia. We found neither stable bands (a “band” in our study group was defined as a regional assemblage of OMUs) nor clans that lasted for several years. Some OMUs moved and transferred into neighboring areas over both the short and long term. Further, some post-adolescent males appeared to move out of the study area. The ratio of adult females in an OMU in our study group was larger than for any other documented study site, and this may be the reason for enhanced female transfer between OMUs. A large proportion of the adolescent females showed no clear membership to OMUs, and no “initial units” (commonly observed in Ethiopia) were discernible. The ease with which young males acquired adult females at the study site must have disrupted the formation of a clan, a “male-bonded society.”     

Alternative routes to the leader male role in a multi-level society: follower vs. solitary male strategies and outcomes in hamadryas baboons

The nested one-male units (OMUs) of the hamadryas baboon are part of a complex social system in which "leader" males achieve near exclusive mating access by forcibly herding females into permanent consortships. Within this multi-level social system (troops, bands, clans and OMUs) are two types of prereproductive males--the follower and solitary male--whose different trajectories converge on the leader role. Here we compare OMU formation strategies of followers, who associate with a particular OMU and may have social access to females, with those of solitary males, who move freely within the band and do not associate regularly with OMUs. Data were derived from 42 OMU formations (16 by followers and 26 by solitary males) occurring over 8 years in a hamadryas baboon band at the Filoha site in Ethiopia. "Initial units" (IUs) with sexually immature females (IU strategy) were formed by 44% of followers and 46% of solitary males. The remaining followers took over mature females when their leader was deposed (challenge strategy) or disappeared (opportunistic strategy), or via a seemingly peaceful transfer (inheritance strategy). Solitary males took over mature females from other clans and bands, but mainly from old, injured or vanished leaders within their clan (via both the challenge and opportunistic strategies). Former followers of an OMU were more successful at taking over females from those OMUs than any other category of male. Despite this advantage enjoyed by ex-follower leaders, ex-solitary leaders were equally capable of increasing their OMU size at a comparable rate in their first 2 years as a leader. These results demonstrate the potential for males to employ both multiple roles (follower vs. solitary male) and multiple routes (IU, inheritance, challenge, opportunistic) to acquire females and become a leader male in a mating system characterized by female defense polygyny in a competitive arena.     

The fourth level of social structure in a multi‐level society: ecological and social functions of clans in hamadryas baboons

Hamadryas baboons are known for their complex, multi‐level social structure consisting of troops, bands, and one‐male units (OMUs) [Kummer, 1968. Social organization of hamadryas baboons. Chicago: The University of Chicago Press. 189p]. Abegglen [1984. On socialization in hamadryas baboons: a field study. Lewisburg, PA: Bucknell University Press. 207p.] observed a fourth level of social structure comprising several OMUs that rested near one another on sleeping cliffs, traveled most closely together during daily foraging, and sometimes traveled as subgroups independently from the rest of the band. Abegglen called these associations “clans” and suggested that they consisted of related males. Here we confirm the existence of clans in a second wild hamadryas population, a band of about 200 baboons at the Filoha site in lowland Ethiopia. During all‐day follows from December 1997 through September 1998 and March 2005 through February 2006, data were collected on activity patterns, social interactions, nearest neighbors, band fissions, and takeovers. Association indices were computed for each dyad of leader males, and results of cluster analyses indicated that in each of the two observation periods this band comprised two large clans ranging in size from 7 to 13 OMUs. All band fissions occurred along clan lines, and most takeovers involved the transfer of females within the same clan. Our results support the notion that clans provide an additional level of flexibility to deal with the sparse distribution of resources in hamadryas habitats. The large clan sizes at Filoha may simply be the largest size that the band can split into and still obtain enough food during periods of food scarcity. Our results also suggest that both male and female relationships play a role in the social cohesion of clans and that males exchange females within clans but not between them. Am. J. Primatol. 71:948–955, 2009. © 2009 Wiley‐Liss, Inc.     

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.     

Social dynamics of the golden snub‐nosed monkey (Rhinopithecus roxellana): female transfer and one‐male unit succession

Among primates that form multilevel societies, understanding factors and mechanisms associated with the movement of individuals between groups, clans, and one‐male social units offers important insight into primate reproductive and social strategies. In this research we present data based on an 8‐year field study of a multilevel troop of Sichuan snub‐nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains of China. Our study troop contained 78–126 individuals, and was usually organized into 6–8 one‐male units (OMU). The majority of OMUs were composed of networks of unrelated females and their offspring. We found that 59.7% (43/72) of subadult and adult females in our study troop transferred between OMUs (n=66) or disappeared (n=7) from the troop. In the majority of cases, two or more females transferred together into new OMUs or troops. In R. roxellana, new OMUs formed in several ways. During 2001–2008, 16 adult males appeared in the study troop. Over this period, we observed 13 different males who became harem leaders either by taking over an existing harem or by attracting females from other OMUs into their harem. We also observed four OMUs from a neighboring troop to successfully immigrate into the study troop. The number of individuals in these newly immigrated OMUs was significantly smaller than that number of individuals in resident OMUs. During harem formation, fighting between adult males was rarely observed, and female mate choice appeared to play a crucial role in harem male recruitment and replacement. These results suggest that golden snub‐nosed monkeys are organized in a nonmatrilineal social system. Female mate choice and possibly incest avoidance appear to play important roles in female transfer, male tenure, and OMU stability. Am. J. Primatol. 71:670–679, 2009. © 2009 Wiley‐Liss, Inc.     

Behavioral variation and reproductive success of male baboons (Papio anubis x 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.     

Male dispersal in a provisioned multilevel group of Rhinopithecus roxellana in Shennongjia Nature Reserve, China

Most Old World monkeys show male-biased dispersal. We present the first systematic data on male dispersal in a provisioned multilevel group of Rhinopithecus roxellana, based on 4.5 years of field observations in Shennongjia National Nature Reserve, China. We evaluated both ultimate (inbreeding avoidance and male mating competition) and proximate (food availability and predation risk) factors influencing male dispersal. The focal group contained 34-53 individuals, in 3-4 one-male units (OMUs) and 1 all-male unit (AMU). We observed 37 dispersal events involving 10 of 11 adults, 7 of 8 subadults, and 7 of 15 juveniles. Most interunit transfers within the focal group occurred around the months of mating season. Adult males competed for the leader positions of OMUs mainly through aggressive takeovers, and young males transferred from the OMUs to the AMU at the median age of 41 months, forced out by leader males. No young males older than 4 years remained in natal or non-natal OMUs. The male mating competition hypothesis was supported. The young males emigrated voluntarily from the focal group at the average age of 58.6 months, and no young emigrating male was observed to return, suggesting inbreeding avoidance also played a role in the dispersal of young males. Most emigration/immigration events were parallel dispersal and occurred during intergroup encounters, suggesting increased predation risk during the dispersal period. Males were more likely to emigrate/immigrate during the months when preferred foods were most available. We compared the dispersal patterns in R. roxellana with those in gelada baboons and hamadryas baboons, both living in multilevel societies. Similar to R. roxellana, young male geladas disperse at puberty, but they may return and breed in their natal groups. Males in hamadryas also disperse, but much less commonly than in R. roxellana. Provisioning may have influenced results, and confirming studies on unprovisioned groups would be valuable.     

Human–hamadryas baboon (Papio hamadryas) conflict in the Wonchit Valley,South Wollo,Ethiopia

Understanding the extent of human–primate conflict is crucial to the development of conservation and management strategies. We carried out this study in an unprotected area of central Ethiopia to examine the magnitude of human–hamadryas baboon (Papio hamadryas) conflict and to assess the attitude of local farmers towards baboons in Wonchit Valley. In 2014, we interviewed 119 adult respondents using a structured questionnaire. Local farmers considered hamadryas baboons to be the major pest in the area. All respondents reported that hamadryas baboons caused crop raiding and small livestock predation in the region. Respondents reported that a shortage of fruit producing wild trees and ready availability of crops were the main causes of conflict between farmers and hamadryas baboons. We found that hamadryas baboons damaged cereal crops at dusk and dawn during full moonlight, and most (89.9%) respondents claimed that they were not interested in hamadryas baboon conservation. Our results indicate that human–hamadryas baboon conflict has a strongly negative impact on both baboon conservation and local farmers. We suggest that to mitigate the human–hamadryas baboon conflict, job opportunities such as beekeeping should be introduced in the region.     

Crossing the Red Sea: phylogeography of the hamadryas baboon, Papio hamadryas hamadryas

The hamadryas baboon (Papio hamadryas hamadryas) is found both in East Africa and western Arabia and is the only free-ranging nonhuman primate in Arabia. It has been hypothesized that hamadryas baboons colonized Arabia in the recent past and were possibly even transported there by humans. We investigated the phylogeography of hamadryas baboons by sequencing a portion of the control region of mtDNA in 107 baboons from four Saudi Arabian populations and combing these data with published data from Eritrean (African) P. h. hamadryas. Analysis grouped sequences into three distinct clades, with clade 1 found only in Arabia, clade 3 found only in Africa, but clade 2 found in both Arabian and African P. h. hamadryas and also in the olive baboon, P. h. anubis. Patterns of variation within Arabia are neither compatible with the recent colonization of Arabia, implying that baboons were not transported there by humans, nor with a northerly route of colonization of Arabia. We propose that hamadryas baboons reached Arabia via land bridges that have formed periodically during glacial maxima at the straits of Bab el Mandab in the southern Red Sea. We suggest that the genetic differentiation of Arabian from African populations suggests that Arabian populations have a higher conservation status than recognized previously.     

What role do olfactory cues play in chacma baboon mating?

The probability of ovulation in a number of primate species is associated with both visual and auditory cues. We use 18‐month behavioral data from two chacma baboon troops to provide the first systematic assessment of the possibility that olfactory cues are also involved. Using variance in the rate of olfactory inspection by males as a proxy for changes in the intensity of female vaginal odor, we found that rates of inspection were broadly correlated with changes in female fertility. Males inspected cycling females significantly more than anovulatory, noncycling females and swelling females significantly more than nonswollen cycling females. Rates of inspection peaked around the time at which males first started guarding females and were sustained until the detumescence of the female's sexual skin. We conclude, therefore, that olfactory cues represent one component of a multimodal signal of ovulation in chacma baboons. The possible reasons for such a multimodal signal are discussed. Am. J. Primatol. 71:493–502, 2009. © 2009 Wiley‐Liss, Inc.     

2D:4D digit ratio is not a biomarker of developmental programming in baboons (Papio hamadryas species)

We hypothesized second‐to‐fourth hand digit ratio (2D:4D) is a biomarker of developmental programming in 3 baboon groups: intrauterine growth restriction (7 females, 8 males), exposure during fetal life to synthetic glucocorticoids (4 females, 5 males), and controls (66 females, 20 males). 2D:4D was similar between sexes and groups.     

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.     

The Socioecology of Network Scaling Ratios in the Multilevel Society of Hamadryas Baboons (Papio hamadryas hamadryas)

Multilevel or modular societies characterize a range of mammalian taxa, allowing social groups to fission and fuse in response to ecological factors. The modular society of hamadryas baboons has previously been shown to consist of 4 levels: troop, band, clan, and one-male unit (OMU). A recent study by Hill et al. (Biology Letters 4:748–751, 2008) revealed a mean scaling ratio across successive levels of multilevel societies of ca. 3; this was consistent across elephants, orca, geladas, and hamadryas baboons. Here we reanalyze the scaling ratio for hamadryas baboons with previously unavailable data from Filoha. Our analysis revealed a mean scaling ratio for hamadryas of 3.28 without data on the hamadryas clan layer of organization at Filoha, but a ratio of 6.17 with these data included. This discrepancy is due to the large clan and band sizes at Filoha yielding a larger than average gap between the OMU and the clan. Further analysis revealed subsets of OMUs within clans, suggesting a 5th level of society in this population. When this 5th layer of social structure is included in the analysis, the scaling ratio at Filoha is consistent with that of other hamadryas populations and other taxa. These results suggest that a consistent mammalian scaling ratio can be used to detect previously hidden levels of organization within societies and to predict their sizes in taxa for which detailed behavioral data are not available.     

Conflict management by hamadryas baboons (Papio hamadryas hamadryas) during crowding: a tension-reduction strategy

Primates change a variety of behavioral responses during short-term exposure to crowding. Under crowded conditions, rates of aggression, submissive behavior, and affiliative behavior may increase or decrease. Different patterns of change among these three categories of response have been interpreted as various coping "strategies" for managing the increased risk of conflict under crowded conditions. Grooming is of particular interest because this behavior is known to have a calming influence on the recipient and could be used to manage conflict under tense situations. A captive group of nine hamadryas baboons (Papio hamadryas hamadryas) composed of two harems was observed under short-term crowding to determine whether this species adopts conflict-management strategies similar to those described in other primates. The aggression, submission, affiliation, and displacement activities of the six adults in the group (two males and four females) were recorded, and behaviors in their small indoor quarters was compared with baseline behaviors in the outdoor section of their enclosure, which had over 10 times more space. Repeated-measures analysis of variance (ANOVA) was used to compare behavioral rates during crowding with baseline rates recorded immediately after crowding and during matched controls collected at the same time of day as the crowding sessions. Aggression and submission rates did not change significantly across conditions. Huddling together and proximity increased during crowding, and females increased grooming of their harem male during crowding. Displacement activities (e.g., pacing and self-grooming) increased during crowding, but scratching, an indicator of anxiety in primates, did not. The pattern of behavior exhibited by this group conforms to an active "tension-reduction" strategy in which animals successfully reduce the higher risk of aggression during crowding.     

Reconciliation in hamadryas baboons, Papio hamadryas: testing the relationships quality hypothesis

Post-conflict interactions between former opponents were investigated in a troop of hamadryas baboons, Papio hamadryas. This species is known for it's multilevel structure with evidently expressed hierarchy between males and females. Due to this fact hamadryas baboons represent an ideal object for testing the "relationship quality" hypothesis. The analyses were done on 436 PC-MC pairs of animals, which represented different social classes (harem male-female pairs, harem females, relatives, females from different harems. Male-male pairs, and female-subadult pairs). Reconciliation was practiced in different social classes of individuals: harem male-female pairs, harem female-female pairs, kin-kin pairs, male-male pairs, female-subadult pairs. Significant differences in the rate of reconciliatory tendency for different categories of interacting animals were found. Interactions between former opponents were highly selective. These may be interpreted as an indicator of the influence of the relation quality on the probability of reconciliation in hamadryas baboons.     

Osteopenia and osteoporosis in adult baboons (Papio hamadryas)

BACKGROUND: Little is known about the degree to which baboons, an important animal model in skeletal research, spontaneously experience age-related osteopenia and osteoporosis. METHODS: We measured bone mineral density (BMD) in 667 baboons, assigned T-scores to older animals based on sex-specific young adult reference groups, and compared reproductive history in older females with low BMD to those with normal BMD. RESULTS: Approximately 25% of older baboon females were osteopenic. No females or males were osteoporotic. Neither parity nor interbirth interval spine clearly distinguished low vs. normal BMD groups. Intersite correspondence in low BMD was highest between sites in the same region rather than sites of the same bone type. CONCLUSION: As with humans, osteopenia is common among older females. The absence of osteoporotic animals may be due to colony maintenance resulting in truncation of the aged population and selection for healthier animals in the oldest ranges.     

Ranging behavior,group size and behavioral flexibility in Ethiopian hamadryas baboons (Papio hamadryas hamadryas)

This study reports group size, home range size, daily path lengths, seasonal effects on ranging behavior and qualitative information on diet for a population of hamadryas baboons inhabiting the lowlands of the northern Rift Valley in central Ethiopia. The minimum home range size and daily path length for this population are similar to those reported for other populations of hamadryas baboons in Ethiopia and Saudi Arabia. Group sizes, however, are much larger than those in most other hamadryas populations for which published data are available. The large group sizes in this area may be related to the abundance of one food resource in particular, doum palm nuts. Overall, this study suggests that hamadryas baboons may be more flexible in some aspects of their behavioral ecology (e.g. group size) than in others (e.g. ranging behavior).