Bale Monkey Research Articles

Whole Genome Analysis Reveals Evolutionary History and Introgression Events in Bale Monkeys.

Background/Objective: The Bale monkey (Chlorocebus djamdjamensis) is a threatened primate species endemic to Ethiopia and, in contrast to other members of the genus Chlorocebus, lives at high altitudes and feeds mainly on bamboo. Two populations of the species are present, one in continuous bamboo forest (CF) in the eastern part of the species' range, and the other in fragmented forest (FF) in the western part. Based on mitochondrial DNA and phenotypic characteristics, previous studies have suggested introgression by parapatric congeners into the FF population but not into the CF population. The objective of this study was to gain insights into the evolutionary history of Bale monkeys and their potential genetic adaptations to high altitudes and for bamboo consumption. Methods: We sequenced the whole genomes of individuals from both populations and compared their genomes with those of the other five Chlorocebus species. We applied phylogenetic methods and conducted population demographic simulations to elucidate their evolutionary history. A genome-wide analysis was conducted to assess gene flow and identify mutations potentially associated with adaptations to high altitudes and for bamboo metabolism. Results: Our analyses revealed Bale monkeys as the sister clade to Chlorocebus aethiops and showed that gene flow occurred between C. aethiops and FF but not between C. aethiops and CF. In addition, we detected non-synonymous mutations in genes potentially associated with the adaptation to high altitudes (EPAS1) in both populations and with the adaptation for bamboo metabolism (TAS2R16, MPST, and TST) mainly in the CF population. Conclusions: Our study provides insights into the evolutionary history of a threatened primate species and reveals the genetic basis for its adaptions to unique environments and for diet specialization.

The role of Dodola Community Conservation Area for large mammal conservation, Ethiopia

The role of community conservation areas for large mammals is rarely evaluated. We investigated the species richness and frequency of sightings of large mammals in the Dodola Community Conservation Area. The study area was stratified into three habitat types, and 49 lines transect was laid (27 Dry evergreen Afromontane forests, 20 Sub-afro-alpine habitats, and 2 plantation forests) based on the topography, land use, and vegetation cover of the study area. A total of 24 species of large mammals were identified and recorded in the study area. Though the community conservation area is home to diverse species of mammals, including some endemic and endangered ones such as mountain nyala and Bale Monkey, human encroachment, agriculture, and overgrazing are prominent in the area, putting huge pressure on flora and fauna. Therefore, we recommend the participatory approach be strengthened to ensure sustainable coexistence between people and wildlife.

The value of flagship and umbrella species for restoration and sustainable development: Bale monkeys and bamboo forest in Ethiopia

Forest loss and degradation are the most significant threats to terrestrial biodiversity in the tropics. Promoting flagship or umbrella species is a strategy that can be used to conserve intact forests and restore degraded ecosystems, conserve biodiversity, and achieve sustainable development goals. The Bale monkey (Chlorocebus djamdjamensis) is an arboreal, forest-dwelling, threatened primate restricted to a small range in the southern Ethiopian Highlands, which relies mostly on a single species of bamboo (Arundinaria alpina) and prefers bamboo forest habitat. Most of the Bale monkey’s range lies outside protected areas and most of its historical bamboo forest habitat is degraded or destroyed. The conservation of Bale monkeys and bamboo is highly inter-dependent; however, the value of using the Bale monkey as a flagship or umbrella species for forest restoration has not been evaluated. Here we use geographic range overlap and geospatial modeling to evaluate Bale monkeys as a flagship and/or umbrella species. We also assess if conservation intervention on behalf of Bale monkeys can help restore bamboo forest, while simultaneously providing a wide range of socioeconomic and environmental benefits. We found that Bale monkeys share their range with 52 endemic and/or threatened vertebrate species and at least 9 endemic and/or threatened plant species. Our results show that Bale monkeys meet both the flagship and umbrella species criteria to restore bamboo forest and conserve threatened co-occurring species. Since bamboo is fast-growing and can be harvested every year, we suggest that a science-based sustainable harvest and management regime for bamboo would help to improve the livelihood of both the local community and Ethiopians in general without significantly affecting the long-term survival of Bale monkeys and regional biodiversity. Further, a conservation management strategy protecting and restoring bamboo forest has the potential to achieve at least six of the 17 United Nations Sustainable Development Goals.

Sleeping Site and Tree Selection by Bale Monkeys (Chlorocebus djamdjamensis) at Kokosa Forest Fragment in Southern Ethiopia

Although selecting advantageous sleeping sites is crucial for nonhuman primates, the extent to which different factors contribute to their selection remains largely unknown for many species. We investigated hypotheses relating to predator avoidance, food access, and thermoregulation to explain the sleeping behavior of Bale monkeys (Chlorocebus djamdjamensis) occupying a degraded fragmented forest, Kokosa, in the southern Ethiopian Highlands. We found that the study group reused 11 out of 20 sleeping sites used during the 42 study days over a 6-month period. Sleeping sites were usually close to the last feeding trees of the day (mean distance =15.2 m) and/or the first feeding trees of the next morning (mean distance = 13.5 m). This may reflect an attempt to maximize feeding efficiency and reduce travel costs. Compared to the mean trees in the study area, sleeping trees were significantly shorter. Bale monkeys selected sleeping places in trees with high foliage density above and below them, lending support to the hypothesis that they select sleeping places that can conceal them from predators and at the same time offer shelter from cold weather. The monkeys also frequently huddled at night. Our results suggest that predator avoidance, access to food resources, and thermoregulation all likely influence the selection of sleeping sites by Bale monkeys.

Class and landscape level habitat fragmentation analysis in the Bale mountains national park, southeastern Ethiopia

The changes of natural habitat structure and function due to human interference is hastening worldwide, and it is compulsory to preserve biological resources in a protected system. This study aims to measure the landscape ecological structure and the extent of habitat fragmentation in the Bale mountains national park. The land use/land cover change was determined by interpreting the 1985, 1995, 2005 and 2017 Landsat images with ArcGIS 10.3, and the selected landscape structural metrics was analyzed using FRAGSTATS 4.2.1. All land cover classes showed a declining trend, except the farmland, and grassland depicted the highest area reduction. From 1985 to 2017 grassland, Erica, forestland, and afro-alpine were decreased by 9.36 %, 0.26 %, 0.06 %, and 0.01 %, respectively. Whereas, farmland was increased by 43.67 %. The study area was characterized as progressively fragmented since it was signified by the escalated value of patch number (40.22 %), area-weighted mean shape index (18.84 %), and edge density (22.27 %) and a declined value of mean patch size (28.68 %) and core area (10.60 %) over the study period. Considering this result, there was a high loss in area available for core dependent species, particularly for Mountain nyala in the grasslands and woodlands, Ethiopian wolf in afro-alpine regions, and Bale monkey in the bamboo forest. Both forestland and grassland need a conservation priority since these habitats were the most fragmented and habitat lost area.

Use of cultivated foods and matrix habitat by Bale monkeys in forest fragments: Assessing local human attitudes and perceptions.

Primates inhabiting human-modified landscapes often exploit matrix habitat to supplement their diet with cultivated foods, at times resulting in economic losses and conflict with local people. Understanding human-nonhuman primate interactions and the attitudes and perceptions of local people towards crop feeding species are crucial to designing effective species-based management plans. Over a 12-month period, we used scan sampling to study the consumption of cultivated foods and matrix use patterns by two habituated groups of Bale monkeys (Chlorocebus djamdjamensis), Ethiopian-endemic bamboo specialists, in two forest fragments (Kokosa and Afursa) set amidst human settlements and farmland in the southern Ethiopian Highlands. Further, we conducted interviews with local people to document their attitudes and perceptions towards Bale monkeys at the two sites. We found that Bale monkeys at Kokosa, a more degraded habitat by most measures, consumed significantly more cultivated foods than their counterparts at Afursa. Moreover, Bale monkeys at Kokosa spent significantly more time in the matrix than in the forest habitat, while monkeys at Afursa spent significantly less time in the matrix than in the forest habitat. Not surprisingly, local people displayed a more negative attitude towards monkeys inhabiting Kokosa than those inhabiting Afursa. The differences in Bale monkey cultivated food consumption and matrix use patterns-as well as in local people's attitudes and perceptions towards Bale monkeys-between Kokosa and Afursa are probably associated with differences in habitat structure, degree of habitat alteration, and land-use practices between the sites. We conclude that to ensure long-term coexistence between Bale monkeys and local people in human-modified landscapes, it is vital to incorporate nearby matrix habitats into management plans and to work closely with local communities to develop effective nonlethal crop protection strategies, thereby reducing the likelihood of negative interactions between Bale monkeys and humans.

Population genetic structure and evolutionary history of Bale monkeys (Chlorocebus djamdjamensis) in the southern Ethiopian Highlands

BackgroundSpecies with a restricted geographic distribution, and highly specialized habitat and dietary requirements, are particularly vulnerable to extinction. The Bale monkey (Chlorocebus djamdjamensis) is a little-known arboreal, bamboo-specialist primate endemic to the southern Ethiopian Highlands. While most Bale monkeys inhabit montane forests dominated by bamboo, some occupy forest fragments where bamboo is much less abundant. We used mitochondrial DNA (mtDNA) sequences to analyse the genetic structure and evolutionary history of Bale monkeys covering the majority of their remaining distribution range. We analysed 119 faecal samples from their two main habitats, continuous forest (CF) and fragmented forests (FF), and sequenced 735 bp of the hypervariable region I (HVI) of the control region. We added 12 orthologous sequences from congeneric vervets (C. pygerythrus) and grivets (C. aethiops) as well as animals identified as hybrids, previously collected in southern Ethiopia.ResultsWe found strong genetic differentiation (with no shared mtDNA haplotypes) between Bale monkey populations from CF and FF. Phylogenetic analyses revealed two distinct and highly diverged clades: a Bale monkey clade containing only Bale monkeys from CF and a green monkey clade where Bale monkeys from FF cluster with grivets and vervets. Analyses of demographic history revealed that Bale monkey populations (CF and FF) have had stable population sizes over an extended period, but have all recently experienced population declines.ConclusionsThe pronounced genetic structure and deep mtDNA divergence between Bale monkey populations inhabiting CF and FF are likely to be the results of hybridization and introgression of the FF population with parapatric Chlorocebus species, in contrast to the CF population, which was most likely not impacted by hybridization. Hybridization in the FF population was probably enhanced by an alteration of the bamboo forest habitat towards a more open woodland habitat, which enabled the parapatric Chlorocebus species to invade the Bale monkey's range and introgress the FF population. We therefore propose that the CF and FF Bale monkey populations should be managed as separate units when developing conservation strategies for this threatened species.

Flexibility in positional behavior, strata use, and substrate utilization among Bale monkeys (Chlorocebus djamdjamensis) in response to habitat fragmentation and degradation.

Studies of the effects of habitat fragmentation and degradation on primate positional behavior, strata use, and substrate utilization offer valuable insights into the behavioral and ecological flexibility of primates whose habitats have undergone extensive anthropogenic disturbance. In this study, we evaluated how positional behavior, strata use, and substrate utilization differed between Bale monkeys (Chlorocebus djamdjamensis)-bamboo-eating cercopithecids endemic to the southern Ethiopian Highlands-occupying continuous versus fragmented forests. Bale monkeys in forest fragments (where bamboo had been degraded or eradicated) spent significantly more time on the ground and in understory strata whereas those in continuous forest spent significantly more time in the middle and upper strata. Bale monkeys in forest fragments also spent significantly more time walking and galloping and significantly less time climbing than those in continuous forest. Our results suggest that, unlike the primarily arboreal Bale monkeys in continuous forest, Bale monkeys in forest fragments should be characterized as semi-terrestrial. In response to habitat disturbance in fragments, we observed a greater emphasis on terrestrial foraging and travel among Bale monkeys in these human altered habitats, which may put them at greater risk of predation and conflict with nearby human populations. Bale monkeys in fragments exhibit flexibility in their positional behavioral repertoire and their degree of terrestriality is more similar to their sister taxa in Chlorocebus than to Bale monkeys in continuous forest. These findings suggest that habitat alteration may compel Bale monkeys to exhibit semi-terrestrial behaviors crucial for their persistence in human-modified habitats. Our results contribute to a growing body of literature on primate behavioral responses to anthropogenic modification of their habitats and provide information that can contribute to the design of appropriate conservation management plans.

Dietary flexibility of Bale monkeys (Chlorocebus djamdjamensis) in southern Ethiopia: effects of habitat degradation and life in fragments

BackgroundUnderstanding the effects of habitat modification on the feeding strategies of threatened species is essential to designing effective conservation management plans. Bale monkeys (Chlorocebus djamdjamensis) are endemic to the rapidly shrinking montane forests of the southern Ethiopian Highlands. Most populations inhabit continuous bamboo forest subsisting largely on the young leaves and shoots of a single species of bamboo. Because of habitat disturbance in recent decades, however, there are now also several dozen small populations inhabiting isolated forest fragments where bamboo has been degraded. During 12-months, we assessed Bale monkey responses to habitat degradation by comparing habitat composition, phenological patterns, and feeding ecology in a largely undisturbed continuous forest (Continuous groups A and B) and in two fragments (Patchy and Hilltop groups).ResultsWe found that habitat quality and food availability were much lower in fragments than in continuous forest. In response to the relative scarcity of bamboo in fragments, Bale monkeys spent significantly less time feeding on the young leaves and shoots of bamboo and significantly more time feeding on non-bamboo young leaves, fruits, seeds, stems, petioles, and insects in fragments than in continuous forest. Groups in fragments also broadened their diets to incorporate many more plant species (Patchy: ≥ 47 and Hilltop: ≥ 35 species)—including several forbs, graminoids and cultivated crops—than groups in continuous forest (Continuous A: 12 and Continuous B: 8 species). Nevertheless, bamboo was still the top food species for Patchy group (30% of diet) as well as for both continuous forest groups (mean = 81%). However, in Hilltop group, for which bamboo was especially scarce, Bothriochloa radicans (Poaceae), a grass, was the top dietary species (15% of diet) and bamboo ranked 10th (2%).ConclusionsWe demonstrate that Bale monkeys are more dietarily flexible than previously thought and able to cope with some degradation of their primary bamboo forest habitat. However, crop raiding and other terrestrial foraging habits more common among fragment groups may place them at greater risk of hunting by humans. Thus, longitudinal monitoring is necessary to evaluate the long-term viability of Bale monkey populations in fragmented habitats.

Ecological plasticity in the gastrointestinal microbiomes of Ethiopian Chlorocebus monkeys

Human activities can cause habitat degradation that may alter the types and quality of available food resources and thus influence the microbiomes of wild animal populations. Furthermore, seasonal shifts in food availability may cause adaptive responses in the gut microbiome to meet the need for different metabolic capabilities. Here, we demonstrate local-scale population structure in the gastrointestinal microbiotas of Chlorocebus monkeys, in southern Ethiopia, in response to varying degrees of human encroachment. We further provide evidence of adaptation to ecological conditions associated with the dry and wet seasons, and show seasonal effects to be more pronounced in areas with limited human activity. Finally, we report species-level microbiota differences between the endemic Ethiopian Bale monkey, an ecological specialist, and generalist Chlorocebus species from the same geographical region.

Impacts of habitat loss and fragmentation on the activity budget, ranging ecology and habitat use of Bale monkeys (Chlorocebus djamdjamensis) in the southern Ethiopian Highlands

Understanding the extent to which primates in forest fragments can adjust behaviorally and ecologically to changes caused by deforestation is essential to designing conservation management plans. During a 12-month period, we studied the effects of habitat loss and degradation on the Ethiopian endemic, bamboo specialist, Bale monkey (Chlorocebus djamdjamensis) by comparing its habitat quality, activity budget, ranging ecology and habitat use in continuous forest and two fragments. We found that habitat loss and fragmentation resulted in major differences in vegetation composition and structure between forest types. We also found that Bale monkeys in continuous forest spent more time feeding and traveling and less time resting and socializing than monkeys in fragments. Bale monkeys in continuous forest also had higher movement rates (m/hr) than monkeys in fragments. Bale monkeys in continuous forest used exclusively bamboo and mixed bamboo forest habitats while conspecifics in fragments used a greater variety of habitats including human use areas (i.e., matrix). Our findings suggest that Bale monkeys in fragments use an energy minimization strategy to cope with the lower availability of the species' primary food species, bamboo (Arundinaria alpina). We contend that Bale monkeys may retain some of the ancestral ecological flexibility assumed to be characteristic of the genus Chlorocebus, within which all extant species except Bale monkeys are regarded as ecological generalists. Our results suggest that, like other bamboo eating primates (e.g., the bamboo lemurs of Madagascar), Bale monkeys can cope with a certain threshold of habitat destruction. However, the long-term conservation prospects for Bale monkeys in fragments remain unclear and will require further monitoring to be properly evaluated.

Mitochondrial diversity and distribution of African green monkeys (chlorocebus gray, 1870).

African green monkeys (Chlorocebus) represent a widely distributed and morphologically diverse primate genus in sub-Saharan Africa. Little attention has been paid to their genetic diversity and phylogeny. Based on morphological data, six species are currently recognized, but their taxonomy remains disputed. Here, we aim to characterize the mitochondrial (mt) DNA diversity, biogeography and phylogeny of African green monkeys. We analyzed the complete mitochondrial cytochrome b gene of 126 samples using feces from wild individuals and material from zoo and museum specimens with clear geographical provenance, including several type specimens. We found evidence for nine major mtDNA clades that reflect geographic distributions rather than taxa, implying that the mtDNA diversity of African green monkeys does not conform to existing taxonomic classifications. Phylogenetic relationships among clades could not be resolved suggesting a rapid early divergence of lineages. Several discordances between mtDNA and phenotype indicate that hybridization may have occurred in contact zones among species, including the threatened Bale monkey (Chlorocebus djamdjamensis). Our results provide both valuable data on African green monkeys’ genetic diversity and evolution and a basis for further molecular studies on this genus. Am. J. Primatol. 75:350-360, 2013. © 2013 Wiley Periodicals, Inc.

Newly Discovered Bale Monkey Populations in Forest Fragments in Southern Ethiopia: Evidence of Crop Raiding, Hybridization With Grivets, and Other Conservation Threats

Until recently, the Bale monkey (Chlorocebus djamdjamensis), an arboreal primate endemic to the southern Ethiopian highlands, remained virtually unstudied, and its distribution pattern inadequately documented. To broaden our knowledge of the species' distribution and abundance, we carried out interviews with local people and total count surveys for Bale monkeys across 67 fragmented forest sites in human-dominated landscapes in the Oromia and Southern Nations, Nationalities, and People's Regions, Ethiopia. From January 2010 to May 2011, we discovered 26 new Bale monkey populations inhabiting forest fragments at elevations ranging from 2,355 to 3,204 m asl. Across these populations, we recorded 37 groups ranging in size from 9 to 29 individuals (Mean = 19.5, SD = 4.5), for a total of 722 individuals. Black-and-white colobus monkeys (Colobus guereza) were sympatric with Bale monkeys at all sites, while grivet monkeys (Chlorocebus aethiops) were found only at sites where Bale monkeys did not occur. All of the newly discovered Bale monkey sites once contained bamboo forest, though at 35% of the sites bamboo forest had been eliminated during the past two decades. The persistence of Bale monkeys at fragmented sites lacking bamboo suggests greater habitat flexibility for the species than previously thought, though the long-term viability of populations both with and without bamboo remains uncertain. Human hunting in response to crop raiding, a behavior the monkeys engaged in at all sites, represents a major threat facing the newly discovered Bale monkey populations. Furthermore, despite their current lack of sympatry, apparently hybrid individuals between Bale monkeys and grivets were noted at three sites, posing yet another potential obstacle to Bale monkey conservation. Community conservation programs aimed at (1) protecting remaining habitat fragments, (2) planting bamboo and trees within and between fragments, and (3) reducing crop raiding represent the only hope for survival of the newly discovered Bale monkey populations.

Population size and habitat preference of the Vulnerable Bale monkeyChlorocebus djamdjamensisin Odobullu Forest and its distribution across the Bale Mountains, Ethiopia

AbstractThe Bale monkeyChlorocebus djamdjamensisis a little-known primate endemic to the south-eastern highlands of Ethiopia. From August 2007 to May 2008 we surveyed to determine the species' habitat preferences and population size in the Odobullu Forest and its range across the Bale Mountains. In Odobullu Forest a total of 136 transects of 1.8–3.0 km were surveyed over a total distance of 280 km. Bale monkey groups were encountered only in bamboo forest, suggesting that the species is a bamboo forest specialist. The density and population size of the Bale monkey in the bamboo forest of Odobullu Forest were estimated to be 121–141 km-2and 1,718–2,002, respectively. At a larger scale, we assessed the distribution of the Bale monkey in 40% of the bamboo forest across the Bale Mountains within the species’ altitudinal range of 2,400–3,250 m. We identified the areas to be surveyed using a 200 m digital elevation model and a 10-m resolution satellite image. We found the Bale monkey in five areas, three of which are previously unrecorded locations for the species. The Bale monkey is now categorized as Vulnerable on the IUCN Red List, partly based on the results of our surveys. Although extensive, our surveys did not cover all of the species’ potential habitat and further surveys are required across all of the bamboo forest of the Bale Mountains and Sidamo region (the western extension of the Bale Mountains).

Diet, Activity Patterns, and Ranging Ecology of the Bale Monkey (Chlorocebus djamdjamensis) in Odobullu Forest, Ethiopia

Bale monkeys (Chlorocebus djamdjamensis) are little-known primates endemic to the forests of the Bale Massif and Hagere Selam regions of Ethiopia. From August 2007 to May 2008, we conducted the first ever study of the species' behavior and ecology, focusing in particular on its diet, activity patterns, and ranging ecology in the Odobullu Forest. We studied 2 neighboring groups (group A: 55-60 members; group B: 46-50 members) and conducted behavioral scan samples on the first 2-5 individuals sighted at 15-min intervals. Feeding accounted for 65.7% of the activity budget, followed by moving (14.4%), resting (10.7%), social (7.1%), and other behaviors (2.4%). Overall diet during the study was dominated by young leaves (80.2%), though subjects also ate fruits (9.6%), flowers (3.1%), animal prey (2.3%), shoots (1.5%), stems (1.4%), mature leaves (1.1%), and roots (0.9%). Bale monkeys consumed only 11 plant species; of these, the top 5 species accounted for 94.3% of their diet. The top food item, bamboo (Arundinaria alpina), was responsible for a remarkable 76.7% of their diet, with most (95.2%) of the bamboo consumption consisting of young leaves. Mean daily path length for the study