Leopard predation on gelada monkeys at Guassa,Ethiopia

Predation is widely believed to exert strong selective pressure on primate behavior and ecology but is difficult to study and rarely observed. In this study, we describe seven encounters between lone wild leopards (Panthera pardus) and herds of geladas (Theropithecus gelada) over a 6-year period in an intact Afroalpine grassland ecosystem at the Guassa Community Conservation Area, Ethiopia. Three encounters consisted of attempted predation on geladas by leopards, one of which was successful. All three attacks occurred in low-visibility microhabitats (dominated by tussock graminoids, mima mounds, or tall shrubs) that provided leopards with hidden viewsheds from which to ambush geladas. An additional four encounters did not result in an attempted attack but still document the consistently fearful responses of geladas to leopards. In encounters with leopards, geladas typically gave alarm calls (n = 7 of 7 encounters), reduced interindividual distances (n = 5), and collectively fled towards or remained at their sleeping cliffs (n = 7), the only significant refugia in the open-country habitat at Guassa. Geladas did not engage in mobbing behavior towards leopards. Encounters with leopards tended to occur on days when gelada herd sizes were small, raising the possibility that leopards, as ambush hunters, might stalk geladas on days when fewer eyes and ears make them less likely to be detected. We compare the behavioral responses of geladas to leopards at Guassa with those previously reported at Arsi and the Simien Mountains and discuss how gelada vulnerability and responses to leopards compare with those of other primate species living in habitats containing more refugia. Lastly, we briefly consider how living in multilevel societies may represent an adaptive response by geladas and other open-country primates to predation pressure from leopards and other large carnivores.     

Blood protein variation of a new population of gelada baboons (Theoropithecus gelada), in the Southern Rift Valley, Arsi Region, Ethiopia

Blood protein polymorphism of gelada baboon (Theropithecus gelada) to the south of the Rift Valley, Arsi Region, were examined for 36 genetic loci using three electrophoresis techniques for 48 blood samples from three localities, and compared with the northern geladas. New variant alleles and genetic markers of Hb-α, PA-2, and TBPA loci were detected. The distribution patterns of the variant alleles of Hb-α, PA-2, TBPA, Pi, Gc, PGM-II, and TBPA loci were localized in the geographic regions of south and north gelada populations, respectively. Genetic variability of southern geladas was estimated as P_poly=0.083 and , which was comparable to northern geladas. A remarkably high genetic differentiation between the two geographic populations was shown byNei's genetic distance=0.071 and G_ST value=0.420. Our results of genetic analysis suggest that the southern and northern gelada populations have been separated for several hundred thousand years, and gene flow between the two geographic populations is severely restricted. The southern gelada baboon may be regarded as a distinct subspecies.     

The synchronization of voices by gelada monkeys

Evidence is presented from recordings made from captive gelada monkeys (Theropithecus gelada) that these monkeys are capable of synchronizing the onsets of their own vocal sounds to the anticipated onsets of sounds produced by other gelada voices. The possibility is discussed that in order to synchronize the onsets of their own sounds to the anticipated onsets of sounds made by other voices, such gelada voices have to possess the ability to “figure out” the tempo and rhythm of the vocal strings produced by the other voices and precisely control the timing of their own voices. It is suggested that geladas do synchronize their voices by using precise temporal and rhythmical controls on the outputs of their voices that are analogous to the temporal and rhythmical abilities humans use in many of the supra-segmental aspects of speech.     

Reconciling conflicts in a one-male society: the case of geladas (<Emphasis Type="Italic">Theropithecus gelada</Emphasis>)

Animals derive benefits from living in social groups but sociality also has its costs in that animals must compete with others for resources and mating opportunities. To cope with the conflict aftermath and social damage caused by competitive aggression, several group-living species use a variety of peace-keeping strategies. The affinitive post-conflict reunion of former opponents, defined as reconciliation, is the primary peace-keeping mechanism. In this study, we provide evidence for the occurrence of reconciliation and test some hypotheses on this post-conflict mechanism in geladas (Theropithecus gelada), a species often neglected in the study of post-conflict dynamics. The conciliatory contacts were uniformly distributed across the different sex–class combinations. Different from baboons, geladas did not show any particular kind of affinitive reconciliation behaviour. Notwithstanding the presence of a linear hierarchy, the dominance relationships did not affect the reconciliation dynamics. According to the valuable relationship hypothesis, coalitionary support seems to be a good predictor for a high level of conciliatory contacts. Finally, at an immediate level reconciliation plays a role in reducing renewed attacks by aggressors, which sought conciliatory contact more frequently than victims. In conclusion, even though the study of post-conflict behaviour in geladas needs to be continued, the patchy nature of their social network is a good model for testing some of the theoretical assumptions about primate conflict resolution.     

Death among geladas (Theropithecus gelada): a broader perspective on mummified infants and primate thanatology

Despite intensive study in humans, responses to dying and death have been a neglected area of research in other social mammals, including nonhuman primates. Two recent reports [Anderson JR, Gillies A, Lock LC. 2010. Pan thanatology. Current Biology 20:R349–R351; Biro D, Humle T, Koops K, Souse C, Hayashi M, Matsuzawa T. 2010. Chimpanzee mothers at Bossou, Guinea carry the mummified remains of their dead infants. Current Biology 20:R351–R352] offered exciting new insights into behavior toward dying and dead conspecifics in our closest living relatives—chimpanzees. Here, we provide a comparative perspective on primate thanatology using observations from a more distant human relative—gelada monkeys (Theropithecus gelada)—and discuss how gelada reactions to dead and dying groupmates differ from those recently reported for chimpanzees. Over a 3.75‐year study period, we observed 14 female geladas at Guassa, Ethiopia carrying dead infants from 1 hr to ≥48 days after death. Dead infants were carried by their mothers, other females in their group, and even by females belonging to other groups. Like other primate populations in which extended (>10 days) infant carrying after death has been reported, geladas at Guassa experience an extreme climate for primates, creating conditions which may favor slower rates of decomposition of dead individuals. We also witnessed the events leading up to the deaths of two individuals and the responses by groupmates to these dying individuals. Our results suggest that while chimpanzee mothers are not unique among primates in carrying their dead infants for long periods, seemingly “compassionate” caretaking behavior toward dying groupmates may be unique to chimpanzees among nonhuman primates (though it remains unknown whether such “compassionate” behavior occurs outside captivity). Am. J. Primatol. 73:405–409, 2011. © 2010 Wiley‐Liss, Inc.     

On operationally defining reconciliation

Post-conflict reconciliatory behavior has been reported to occur with variable frequencies in different primate groups and species. Because different investigators have used different criteria to operationalize reconciliation, however, it is possible that the variation reported merely reflects different methods of study. To compare different groups and species in a meaningful way, an accurate operationalization of reconciliation is necessary. This study explores the correlation between operationally defined reconciliation (what observers recognize, such as friendly reunion) and functional reconciliation (behavior that restores a dyadic social relationship) in a group of captive long-tailed macaques, using results from an experiment originally undertaken to demonstrate the function of friendly reunions in restoring dyadic tolerance after aggression. In dyads of unrelated animals, reunions were equally effective in restoring tolerance whether they involved body contact, overt friendly gestures, or mere proximity. Classification of post-conflict reunions as “reconciliations” depends on comparisons with control observations; these comparisons have been carried out in several ways. Comparisons using the “n-minute rule” missed functional reconciliations, whereas those based on the “post-conflict/matched-control rule” appeared to lead to more accurate classification of functional reconciliations. Post-conflict reunions were equally effective in restoring tolerance whether they were initiated by the original aggressor or by the victim. An accurate operational definition of reconciliation, not a conservative one, is prerequisite to comparisons of the frequency of this behavior, and depends on empirical verification. This study suggests specific guidelines for an operational definition based on such verification. © 1993 Wiley-Liss, Inc.     

A case of infanticide in a recently found gelada population in Arsi, Ethiopia

There have been no reports of infanticide in wild gelada baboons and it has been argued that infanticide is not necessary in geladas, since the birth interval of female gelada can be shortened after takeover of a unit by a new leader male without infanticide. However, we observed an instance of infanticide in a newly-found wild gelada population in the Arsi Region of Ethiopia. After a leader male of the unit was severely wounded by a leopard attack, he was quite weakened. The second male of the unit, a young adult male, became the leader of the unit three weeks later, but the former leader continued to stay in the unit as a second male. After a week, two other adult males joined the unit which, therefore, came to include four adult males. The infanticide took place nine days later. The perpetrator was one of the immigrant males and he showed great interest in the mother of the unweaned victim infant. Although the perpetrator copulated with her after the infanticide, the usurper was found to own all three adult females after two weeks following the infanticide; i.e. the perpetrator could not own any female. The wounded former leader showed conspicuous protective behavior towards the victim's mother and the dead infant. One possible explanation for the occurrence of infanticide in this population of geladas is as follows. Gelada males in this area may be able to join units more easily to form multi-male units but then have shorter tenure in the units. Facing the unstable condition of units, they may sometimes engage in infanticide to increase their breeding opportunities, even before becoming a leader.     

Geographic distribution of microsatellite alleles in geladas (Primates,Cercopithecidae): Evidence for three evolutionary units

The subspecific taxonomy and distribution of geladas (Theropithecus gelada Rüppell, 1835) remains uncertain. Recent molecular studies based on mitochondrial sequence data revealed a geographically structured, three-deme population, suggesting that there are three evolutionary units of geladas. However, mitochondrial distributions do not always recover population relationships, particularly in taxa with a complex history of isolation and gene flow. We therefore analysed the nuclear genetic population structure of the global gelada population based on 20 microsatellite loci in 43 samples from across its geographic range. F_ST values, a STRUCTURE analysis and a principal coordinate analysis (PCoA) confirmed the three-deme population structure corresponding to the mitochondrial population structure. Therefore, our analyses provide additional support for three evolutionary units in geladas, corresponding to (a) a northern (north of Lake Tana, primarily in the Simien Mountains, previously classified as Theropithecus gelada gelada Rüppell, 1835), (b) a central (between Addis Ababa and the highlands east of Lake Tana, previously classified as Theropithecus gelada obscurus Heuglin, 1863) and (c) a southern (south of the Rift Valley, previously tentatively classified as Theropithecus gelada arsi Shotake et al., 2016, Anthropological Science, 124, 157) population. These results pave the way for future conservation decisions and highlight that the gelada population boundaries need more fine-grained genetic sampling and phenotypic analyses, in particular for their taxonomic ranking.     

Defining Higher Levels in the Multilevel Societies of Geladas (Theropithecus gelada)

Multilevel societies, identified by two or more nested levels (or modules) of organization, have been touted as some of the most complex social systems. However, few empirical studies have effectively quantified the association patterns that delineate the various levels in such societies. In particular, the multiple levels of gelada society were first described >3 decades ago, yet no operational definitions exist for the higher levels, i.e., levels above the one-male unit. In geladas, multiple units form aggregations that fission and fuse throughout the day, and throughout the year, blurring the distinctions between previously described higher social levels: teams, bands, and communities. Here we use 5?yr of data on the daily composition of a population of geladas living in the Simien Mountains National Park, Ethiopia to test the hypothesis that higher levels of gelada organization are discrete entities. If gelada aggregations are nothing more than a group of units that share a home range, then we expect a continuous distribution of unit association. If, however, gelada aggregations are indeed discrete organizational levels, then we expect discontinuity in the patterns of association. We found significant discontinuity at the 50% association level, indicating a sharp distinction between members of the same band (>50% association) and members of the same community (<50% association). We also found evidence that recently fissioned units form teams that associate significantly more than other band members. Thus, despite their extremely fluid social organization, gelada social levels are nevertheless clearly identifiable and quantifiable. Based on these results, we suggest that gelada society is an extremely flexible, multilevel society with fission–fusion dynamics, and as such gelada society presents an unusual example for understanding the evolution of modular societies.     

The socio‐genetics of a complex society: female gelada relatedness patterns mirror association patterns in a multilevel society

Multilevel societies with fission–fusion dynamics—arguably the most complex animal societies—are defined by two or more nested levels of organization. The core of these societies are modular social units that regularly fission and fuse with one another. Despite convergent evolution in disparate taxa, we know strikingly little about how such societies form and how fitness benefits operate. Understanding the kinship structure of complex societies could inform us about the origins of the social structure as well as about the potential for individuals in these societies to accrue indirect fitness benefits. Here, we combined genetic and behavioural data on geladas (Theropithecus gelada), an Old World Monkey, to complete the most comprehensive socio‐genetic analysis of a multilevel society to date. In geladas, individuals in the core social ‘units’, associate at different frequencies to form ‘teams’, ‘bands’ and, the largest aggregations, ‘communities’. Units were composed of closely related females, and females remained with their close kin during permanent fissions of units. Interestingly, female–female relatedness also significantly predicted between‐unit, between‐team and between‐band association patterns, while male–male relatedness did not. Thus, it is likely that the socio‐genetic structure of gelada society results from females maintaining associations with their female relatives during successive unit fissions—possibly in an attempt to balance the direct and indirect fitness benefits of group living. Overall, the persistence of associations among related females across generations appears to drive the formation of higher levels of gelada society, suggesting that females seek kin for inclusive fitness benefits at multiple levels of gelada society.     

Changes in unit structures and infanticide observed in Arsi geladas

In 1989 a new gelada baboon (Theropithecus gelada) population was found in Arsi, on the opposite side of the Rift Valley to that of the known gelada populations of Semien and Showa. Previous comparisons of units of the band at Gado Goro, Arsi, in the same season in consecutive years, indicated that unit structure is less stable among Arsi geladas as compared to the Semien population. Gelada units of the band at Gado-Goro were studied for 7 months in order to investigate the processes of social changes. Changes in unit structure were observed. Provisioning was carried out for 1.5 months at the beginning of the 7-month study period, in order to capture and obtain blood samples from the geladas. Following this, changes in male leadership of some units were observed, presumably as a consequence of the capture. However, natural changes also occurred. One change in unit structure occurred after a female gave birth, and changes in another unit occurred after the disappearance of the leader male. These changes involved female desertion of a unit, her subsequent transfer to a male unit, and culminated in the formation of a unit consisting of one female and one male. One successful and one attempted case of unification of units, and one case of change of a unit leader male are reported. These changes occurred among eight resident units in a period of 7 months (196 female months). Though the types of social changes were not much different from previous observations in Semien National Park, their frequencies seemed to be much higher. The characteristics of Arsi gelada social changes are proposed to be related to the small size of the units. We also describe a new confirmed case and one suspected case of infanticide, as well as one case of abortion at the time of male leader change.     

Feeding ecology and diet of the southern geladas (Theropithecus gelada obscurus) in human‐modified landscape,Wollo, Ethiopia

Studying the dietary flexibility of primates that live in human‐modified environments is crucial for understanding their ecological adaptations as well as developing management and conservation plans. Southern gelada (Theropithecus gelada obscurus) is an endemic little‐known subspecies of gelada that inhabits human‐modified landscapes in the northern central highlands of Ethiopia. During an 18‐month period, we conducted this intensive study in an unprotected area of a human‐modified landscape at Kosheme in Wollo to investigate the feeding ecology of southern geladas and their dietary responses to seasonal variations. We quantified the monthly and seasonal diet data from a band of southern geladas using instantaneous scan sampling method at 15‐min intervals, and green grass phenology and availability using visual inspection from the randomly selected permanent plots. The overall average diet of southern geladas at Kosheme constituted grass blades 55.4%, grass undergrounds 13.2%, grass bulbs 5.6%, grass seeds 5.4%, herb leaves 4.0, fruits 7.3%, and cereal crops 5.6%. Grass blade consumption increased with increasing green grass availability, while underground food consumption increased with decreasing green grass availability, and vice versa. Southern geladas spent significantly more time feeding on the grass blades and herb leaves and significantly less time on bulbs during the wet season than the dry season. Underground grass items (rhizomes and corms) were not consumed during the wet season, but made up 22.3% of the dry season diet. Thus, although grass blades are staple diet items for geladas, underground diet items are important “fallback foods” at Kosheme. Our result shows insights into the dietary flexibility southern geladas adopt to cope with human‐modified landscapes of the north‐central Ethiopian Highlands. Thus, the study contributes to a better understanding of how changing environments shape primate ecology and evolution.     

Anti-predator behavior of gelada baboons

The anti-predator behavior of gelada baboons has been observed to consist of simple flight (i.e. they flee to cliffs after becoming alarmed by potential predators). However, active antipredator behavior was observed in a recently found gelada population in Arsi, Ethiopia. This population showed frequent active counter-attacks and severe mobbing at predators. Males fought domestic dogs on the plain and exhibited a systematic mobbing behavior towards a leopard on the cliff face to chase it off. These active anti-predator behaviors are the first confirmed reports on gelada baboons and may provide a useful insight for the understanding of the process of evolutionary adaptation to highland habitats by gelada baboons, as well as for the origin of this small southern population.     

Diet and activity patterns of Arsi geladas in low-elevation disturbed habitat south of the Rift Valley at Indetu,Ethiopia

Understanding the basic natural history of threatened primate taxa is crucial to developing and implementing successful conservation strategies for them. Data on feeding ecology and activity patterns are particularly important for identifying the strategies through which primates invest time and foraging effort towards survival and reproduction at a given locale. Here, we report the results of the first study of the diet and activity budget of Arsi geladas, a population of < 1000 individuals endemic to a heavily disturbed region of the southern Ethiopian Highlands and believed to represent a new taxon of geladas. We conducted our research on a band of 34 individuals belonging to five, one-male units at Indetu, eastern Arsi, Ethiopia, from August 2010 to May 2011 (excluding March 2011). Feeding accounted for 41.7% of total scans, followed by moving (20.3%), resting (19.0%), and social behavior (19.0%). Feeding and moving increased and resting and socializing decreased during the dry season when food availability was probably lower than during the wet season. Geladas ate mostly graminoid leaves (51.7% of feeding scans) though they also consumed graminoid rhizomes (24.4%), forb tubers (7.1%), forb leaves (7.1%), cactus, shrub, and tree fruits (3.6%), graminoid corms (1.7%), forb roots (1.6%), and unidentified items (3.0%). Underground foods (corms, rhizomes, roots, and tubers) accounted for 22–47% (mean = 35%) of the monthly (n = 9) diet and were eaten slightly more during the wet season than during the dry season. Contributions of human crops to the gelada diet could not be quantified without creating conflict between farmers and researchers, though we did note that geladas visited farms on 5–10% of study days. Threats from farmers, children, and dogs limited the geladas’ access to crops once they entered the farms. Further research involving questionnaire surveys of farmers, direct observation of crop damage by geladas, and DNA metabarcoding of gelada feces are crucial to the development of strategies to mitigate human-gelada conflict in the densely populated Arsi Zone of Ethiopia.     

Adaptation to grass-eating in gelada baboons

Gelada faecal samples were analyzed for nutritional content and for particle size, and compared with similar data forPapio baboons, cattle, and zebra. Particle size in gelada is similar to that for zebra, larger than that for cattle and smaller than that for baboons. Gelada and baboons are less efficient than ungulates at extracting protein from their diet. The data on energy extraction are less easy to interpret and appear to be confounded by dietary and seasonal factors. It is suggested that gelada may be too large to compete effectively with ruminants in low altitude grassland habitats under the climatic conditions that have prevailed in eastern Africa since the late Pleistocene.     

Post-Conflict Affiliation in Barbary Macaques is Influenced by Conflict Characteristics and Relationship Quality, but Does Not Diminish Short-Term Renewed Aggression

Many group living primates have evolved mechanisms to repair their social relationships after conflicts ('reconciliation'). We analysed the post-conflict behaviour of female Barbary macaques, Macaca sylvanus , living in the enclosure 'La Forêt des Singes' at Rocamadour, France. Based on a sample of 914 conflicts, we investigated whether relationship (kinship, rank, affiliation, support and sex) and conflict characteristics (conflict intensity, context and duration) affected the quality and frequency of affiliative post-conflict interactions. Thirty-two per cent of all conflicts were followed by post-conflict affiliation. Rates of socio-positive interactions and support were better predictors of post-conflict affiliation than kinship or rank. Short conflicts were followed by post-conflict affiliation relatively more frequently, after a shorter latency, but only briefly, and such interactions were initiated by both parties equally frequently. The majority of affiliative post-conflict interactions occurred immediately after the end of the conflict. In sum, female Barbary macaques invest more in post-conflict affiliation with valuable partners, and they modulate their post-conflict behaviour in relation to conflict characteristics. Remarkably, affiliative post-conflict interactions increased the short-term probability of renewed aggression by the former aggressor to 16% compared with 9% for conflicts that were not followed by affiliative behaviour. Such renewed aggression after post-conflict affiliation occurred particularly frequently among females and after conflicts over food, suggesting that post-conflict affiliation sometimes falsely lures the former victim to stay in the vicinity, even at the risk of receiving renewed aggression.     

Aggression does not increase friendly contacts among bystanders in geladas (<Emphasis Type="Italic">Theropithecus gelada</Emphasis>)

Aggression within a social group may affect bystanders’ affinitive behaviour with other bystanders. After a conflict such affiliations, termed ‘quadratic’, may serve to reduce tension. This particular kind of conflict management has been found in hamadryas baboons. Following the classical and well-established approach for studying post-conflict behaviour [post-conflict/matched control method (PC/MC)], we collected behavioural data on a group of geladas (Theropithecus gelada) in order to check for the presence of quadratic affiliations. A total of 192 PC/MC pairs were collected on both adults and immature individuals. We did not find any increase of affiliation levels between bystanders during PC compared with MC condition. The distribution of affinitive quadratic interactions was not affected by either kinship or relationship quality of bystanders. Moreover, comparison of yawning and self-scratching behaviours (two of the typical non-primate displacement activities under stressful situations) recorded during PCs and MCs did not show any variation in the two conditions. Probably, due to the male tolerance and social cohesiveness in geladas, witnessing a fight does not necessarily induce a sufficient increase of tension in bystanders to be reduced by quadratic affiliation.     

Derived vocalizations of geladas (Theropithecus gelada) and the evolution of vocal complexity in primates

Primates are intensely social and exhibit extreme variation in social structure, making them particularly well suited for uncovering evolutionary connections between sociality and vocal complexity. Although comparative studies find a correlation between social and vocal complexity, the function of large vocal repertoires in more complex societies remains unclear. We compared the vocal complexity found in primates to both mammals in general and human language in particular and found that non-human primates are not unusual in the complexity of their vocal repertoires. To better understand the function of vocal complexity within primates, we compared two closely related primates (chacma baboons and geladas) that differ in their ecology and social structures. A key difference is that gelada males form long-term bonds with the 2-12 females in their harem-like reproductive unit, while chacma males primarily form temporary consortships with females. We identified homologous and non-homologous calls and related the use of the derived non-homologous calls to specific social situations. We found that the socially complex (but ecologically simple) geladas have larger vocal repertoires. Derived vocalizations of geladas were primarily used by leader males in affiliative interactions with 'their' females. The derived calls were frequently used following fights within the unit suggesting that maintaining cross-sex bonds within a reproductive unit contributed to this instance of evolved vocal complexity. Thus, our comparison highlights the utility of using closely related species to better understand the function of vocal complexity.