- Research Article
- Open Access
Dietary flexibility of Bale monkeys (Chlorocebus djamdjamensis) in southern Ethiopia: effects of habitat degradation and life in fragments
BMC Ecology volume 18, Article number: 4 (2018)
Understanding 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).
We 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%).
We 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.
Habitat loss and degradation by humans are the major threats to biodiversity worldwide [1, 2]. Widespread disturbance to formerly intact forests, particularly in the tropics, is resulting in increasing fragmentation of habitats and biological populations . Given that the global human population is expected to continue to increase in the coming decades, resulting habitat alterations may cause the extinction of thousands of species, including many mammals [4,5,6]. Habitat degradation modifies vegetation composition and structure, consequently reducing habitat quality and food availability for species inhabiting an area [6,7,8,9,10]. This decrease in food availability, in turn, lowers the carrying capacity of populations, and, in extreme cases, results in extirpation or extinction [7, 8, 11].
Currently, many populations are restricted to small isolated forest patches surrounded by human-dominated landscapes [12,13,14]. The persistence of these populations, therefore, depends on their ability to cope with change and the minimum size and quality of fragments required to sustain them [15,16,17]. One of the central challenges that must be overcome by populations in fragments is meeting their dietary needs in habitats in which the diversity and abundance of plant species has been substantially altered [7, 11, 18].
Among mammals, specialist species are declining across the world and are at higher risk of extinction or extirpation than generalist species . Specialist folivores are particularly threatened  because they tend to be forest-dwelling, arboreal, and/or sensitive to changes in forest structure [14, 21,22,23,24]. Examples include marsupials like koalas (Phascolarctos cinereus) and greater gliders (Petauroides volans) that feed primarily on Eucalyptus , giant pandas (Ailuropoda melanoleuca) and red pandas (Ailurus fulgens) that feed almost exclusively on bamboo [14, 21] and primates like bamboo lemurs (Hapalemur spp., Prolemur simus) and golden monkeys (Cercopithecus mitis kandti) that feed mostly on bamboo [25, 26]. Bamboo specialist mammals, in particular, often have special morphological, anatomical, behavioural and ecological adaptations to cope with diets rich in cellulose and toxic plant secondary metabolites (PSMs), including cyanide [27, 28]. Food choice in mammalian folivores is influenced by multiple factors, including the availability of specific food items or species within their habitat (e.g., [29, 30]), and the energy, protein, fiber and toxic PSM concentrations in foods [31, 32]. While dietary specialists, including some specialist folivores, are generally associated with narrow ecological tolerances [24, 33, 34] some taxa exhibit enough ecological flexibility to cope with habitat degradation [35,36,37].
Although habitat degradation is increasingly common in tropical forests , intensive studies comparing the feeding ecology within species of populations in continuous versus fragmented forests are lacking for most mammals, including most specialist folivores. However, a handful of such studies have been carried out on tropical primates. Dietary responses to degradation and life in fragments among primates are varied, though common strategies include increasing consumption of (1) abundant fallback foods like leaves (Alouatta palliata: [39, 40], Ateles geoffroyi: , Propithecus diadema: ), (2) foods from secondary growth species, including lianas and climbers (Ateles geoffroyi: , Alouatta palliata: ) or graminoids and forbs (Hapalemur griseus: , H. meridionalis: ), or (3) human crops and exotic species: (Alouatta guariba clamitans: , Macaca sylvanus: ). Furthermore, some primate taxa persist in forest fragments by increasing the plant species richness of their diet (Alouatta pigra: , Cercopithecus mitis boutourlinii: ) while others cope by eating a less species rich diet (Propithecus diadema: , Ateles geoffroyi: ). In some cases, fragments are too small or primates lack the ecological plasticity to survive on the foods present, resulting in widespread local extirpation of populations from their former habitats (Trachypithecus pileatus, Macaca assamensis and Hoolock hoolock: ).
Understanding the dietary responses of individual species to habitat degradation and life in fragments is therefore crucial to designing and implementing appropriate species-based management strategies [51, 52], especially for dietary specialists which are expected to be less flexible at coping with degradation of their habitats than generalist species [24, 53]. For example, until now, no research has yet been conducted to assess the effects of habitat degradation and life in fragments on the feeding strategies of the Bale monkey (Chlorocebus djamdjamensis), an arboreal dietary specialist endemic to the montane forests of the southern Ethiopian Highlands. The Bale monkey is unusual among primates and other mammals for its intense specialization on a single species of bamboo (Arundinaria alpina), which accounts for 77% of its diet in continuous forest [54, 55]. The Bale monkey is thought to be at high risk of extirpation because of its specialized niche, small geographic distribution, and the ongoing deforestation occurring across much of its range [54, 56,57,58]. As a result, the species is currently classified as Vulnerable by the International Union for Conservation of Nature (IUCN) .
In its high degree of specialization, the Bale monkey appears to provide a striking contrast to its five sister species: vervet monkeys (Chlorocebus pygerythrus), grivet monkeys (C. aethiops), green monkeys (C. sabaeus), Malbrouck monkeys (C. cynosuros) and tantalus monkeys (C. tantalus). Two of these sister species, vervets and grivets, are also native—though not endemic—to Ethiopia and are parapatric to Bale monkeys [59, 60]. All members of the genus Chlorocebus, except Bale monkeys, are terrestrial generalists that consume varied omnivorous diets and inhabit a wide range of savanna woodland and grassland habitats over large geographic ranges in equatorial or southern Africa [61,62,63]. Incidentally, an analogous situation exists among monkeys in the genus Cercopithecus where one taxon, the golden monkey (Cercopithecus mitis kandti), is a bamboo specialist while other taxa, including other C. mitis subspecies, tend to be dietary and habitat generalists [63, 64].
Intriguingly, the recent discovery of Bale monkey populations during surveys in a few dozen heavily-degraded forest fragments, some with little bamboo left , suggested the species might be of greater ecological flexibility than previously believed [54,55,56, 65]. This unexpected discovery created the need to evaluate the strategies the monkeys employ in response to habitat degradation and life in fragments by comparing groups inhabiting fragmented habitats with those in continuous forest. We therefore undertook a study comparing the activity, ranging, and dietary patterns of Bale monkeys in fragmented and continuous forests. We recently published evidence that Bale monkeys in fragmented habitats adopt an energy minimization strategy—moving less, feeding less, resting more, and traveling over shorter distances per hour than conspecifics in continuous forest . Along with examining energetic responses to degradation, we sought to determine the dietary strategies Bale monkeys use to cope with the relative scarcity of bamboo in fragments.
The specific aims of the study described here were thus to assess the effects of habitat degradation and life in fragments on (1) habitat quality and temporal patterns of food availability and (2) Bale monkey dietary composition, diversity and selectivity by comparing the feeding ecology between populations in continuous and fragmented forests. We also sought to (3) compare the patterns of dietary flexibility exhibited by Bale monkeys in our study with those of their five sister Chlorocebus species , as well as with those of other bamboo-eating mammals, including several other primates (e.g., Cercopithecus mitis kandti , Macaca assamensis , Prolemur simus , Hapalemur spp. ) and red and giant pandas [14, 34, 69]. We hypothesized that any reduction in habitat quality in forest fragments would strongly influence the feeding strategies of Bale monkeys. In particular, we predicted that the anticipated lower abundance of bamboo in fragments  would lead Bale monkeys there to consume a greater diversity of food items, plant species and growth forms, including human foods on nearby farms, than conspecifics in continuous forest. We also predicted that Bale monkeys in continuous forest would be bamboo specialists , but that conspecifics in fragments would exploit diets more similar to those of other more generalized Chlorocebus species [61, 70].
Study site and habitat characteristics
We carried out our study in the continuous Odobullu Forest (06°50′–6°56′N and 40°06′–40°12′E) and two forest fragments (6°44′–06°45′N and 38°48′–38°51′E) in the southern Ethiopian Highlands . Odobullu Forest (hereafter continuous forest) is a large forest within which bamboo is abundant. It covers 141 km2 (14,100 ha) at elevations ranging from 1500 m to 3300 m asl and lies east of Bale Mountains National Park . The continuous forest consists of four habitat types: mostly bamboo forest and tree-dominated forest but also shrubland and occasional grasslands . It is partially protected by a privately-owned hunting company, Ethiopian Rift Valley Safaris, and disturbance in the home range of our study groups is uncommon due to the steep terrain and remoteness of the area.
Kokosa forest fragment (hereafter Patchy fragment) consists of degraded bamboo with large trees set amidst a matrix of human settlement, cultivated land, shrubland and grazing land. It covers an area of 162 ha and ranges in elevation from 2534 m to 2780 m asl. Most of Patchy fragment is privately owned by local people, though a portion is owned by the community collectively . Selective logging of bamboo is common today.
Afursa forest fragment (hereafter Hilltop fragment) is set upon a hilltop and consists of a mix of secondary forest, shrubland, and Eucalyptus plantation with graminoid and forb cover underneath. Bamboo has been nearly extirpated. Hilltop fragment covers an area of 34 ha at elevations ranging from 2582 m to 2790 m asl and is surrounded by an anthropogenic matrix of cultivated lands, pastures and human settlements. Currently, the district government forbids cutting of trees and use of the fragment for grazing. The edge of the fragment, especially the Eucalyptus plantation, is still used illegally for grazing. Both the Patchy and Hilltop fragments were dominated by bamboo forest only three decades ago . The distance between Hilltop and Patchy fragments is 9 km and they have been separated from one another by human settlement, grazing land and agriculture for many decades . The forest fragments are separated from the continuous forest by ~ 160 km .
We selected four Bale monkey groups for this study: two groups within the continuous bamboo forest (hereafter Continuous A and Continuous B) with overlapping home ranges (29% overlap for Continuous A; 47% overlap for Continuous B) , one group in the Patchy fragment (Patchy group) and one group in the Hilltop fragment (Hilltop group). The home ranges of continuous forest groups (Continuous A and Continuous B) consisted of exclusively bamboo forest (53.7 and 55.6%) and mixed bamboo forest habitats (46.3 and 44.4%). In contrast, the home ranges of fragment groups consisted of more variable habitat types. Patchy group’s range consisted of five habitat classes: grazing land (37.9%), shrubland (29.5%), mixed bamboo forest (17.1%), tree-dominated forest (8.0%) and cultivated land (7.5%) while Hilltop group’s range consisted of four habitat classes: shrubland (50.4%), tree-dominated forest (22.7%), Eucalyptus plantation (24.3%) and grazing land (2.7%) . A.M. and two assistants habituated these groups to human observers for 4 months from March to June 2013 by following each group from dawn to dusk on a near daily basis. We identified 10–15 members of each focal group by their distinctive natural markings (e.g., coat color, facial features, tail shape). Group sizes were: Continuous A, 65 individuals; Continuous B, 38 individuals; Patchy, 28 individuals; and Hilltop, 23 individuals .
We recorded climatic data at the continuous forest (Fly campsite, elevation 2758 m asl; 1.5–2.0 km from the two study groups) and at Patchy fragment (Kokosa campsite, elevation 2634 m asl; 1.5 km from Patchy fragment). We measured daily rainfall using Oregon wireless rain gauges and recorded the daily maximum and minimum temperatures using Taylor digital waterproof maximum/minimum thermometers. We assumed that the rainfall and temperature patterns are similar in each of the two fragments because they are both small, located only 9 km apart, occur at similar elevations, and are oriented in the same north–south and east–west directions. We calculated the monthly and annual rainfall for the period July 2013 to June 2014. We also used the daily maximum and minimum temperatures to calculate monthly means for these variables and calculated annual means by taking the averages of the monthly means.
Though annual rainfall was higher in the fragments (1676 mm SE ± 20.6) than in the continuous forest (1340 mm SE ± 24.8), this difference was not significant (ANOVA: df = 1; F = 2.31; P = 0.136) (Fig. 1). Both study areas were characterized by bimodal rainfall with a long wet season and a short dry season (Fig. 1) but rainfall was less strongly seasonal in the forest fragments than in the continuous forest (Fig. 1). Mean annual temperature (16.7 °C SE ± 0.4) was significantly higher in the forest fragments than in the continuous forest (14.7 °C SE ± 0.2) (ANOVA: df = 1; F = 48.71; P < 0.001).
Vegetation description and temporal patterns of food availability
To examine whether the diet of Bale monkeys was influenced by resource availability, we sampled the vegetation in the ranges of our study groups using two complementary techniques. First, we enumerated all large trees with diameter at breast height (DBH) ≥ 10 cm in 12–24, 50 m × 10 m vegetation quadrats along randomly selected vegetation transects in the home range of each study group. Within quadrats, we measured and recorded the species name, growth form and DBH (in cm) for each tree. Second, we also randomly selected 50% of the vegetation quadrats in each group’s range within which we counted and identified all plants ≥ 2 m tall to species level. This second vegetation enumeration technique enabled us to sample bamboo, shrubs and forbs that the monkeys depend on but that are < 10 cm DBH. For the bamboo sampled with this second technique, we also recorded the DBH of each culm.
In each group’s home range, we calculated the stem density for all plant species ≥ 2 m tall and basal area (cm2/ha) for all large tree species (DBH ≥ 10 cm) and bamboo. We assessed the degree of stem density overlap between the home ranges of the study groups using the Morisita–Horn similarity index, which takes into account both relative abundance and species richness . We classified plant growth forms into five categories: bamboo, trees, shrubs, lianas (including climbers and epiphytes), and forbs. To estimate the biomass of each large tree species and bamboo, we calculated the basal area (BA) of each tree species from the DBH recorded using the formula (BA = [0.5 × DBH]2 × π) .
To evaluate temporal changes in the availability of potential food resources, we carried out monthly phenological assessments over an annual cycle for selected food plant species found at each of the study sites (see  for additional details). These species were selected for monitoring because they had been food species for Bale monkeys in a previous 8-month study in continuous forest at Odobullu . At the start of our study, we marked and identified 10–15 individuals of these food species which included: trees (DBH ≥ 10 cm), bamboo (A. alpina), and shrubs. We assigned every monitored plant a relative abundance score for each of its potential food items (young leaves, mature leaves, flowers, ripe fruits, and shoots) via visual inspection, using binoculars where necessary. Relative abundance score ranged from 0 (item absent from plant) to 8 (plant fully laden with the item) at intervals of 1 .
We analyzed phenological data from eight species: five trees (Canthium oligocarpum, Dombeya torrida, Galiniera saxifraga, Hagenia abyssinica, and Ilex mitis), two shrubs (Rubus apetalus and Bothriocline schimperi) and bamboo (A. alpina). Ultimately, these species cumulatively accounted for 92.6% of the diet of Continuous A; 93.4% for Continuous B, 50.9% for Patchy and 44.5% for Hilltop groups. The lower contribution of monitored plants to the diets of fragment groups resulted from these groups consuming much less bamboo as well as a greater variety of food species, including difficult-to-monitor insects, graminoids and forbs (cf., ), than continuous forest groups. We calculated the monthly mean phenological scores for young leaves, fruits, flowers, and shoots for each individual plant species. We calculated the monthly food availability index (FAI) for each plant part by multiplying the mean phenology scores of species i with the mean basal area of species i and density of the corresponding species i per ha .
We collected activity data from July 2013 to June 2014 using instantaneous scan sampling  at 15-min intervals for up to 5 min duration, typically from 0700 to 1730 . During scans, when a monkey was observed feeding, we recorded the type of food item, growth form and species. We recorded food items as bamboo young leaves, bamboo mature leaves, non-bamboo young leaves (from all species other than bamboo), non-bamboo mature leaves, bamboo shoots, bamboo branchlets (young and thin stems emerging from branches), roots, flowers, fruits, seeds, stems, petioles, insects or mushrooms. We recorded plant growth form as tree, bamboo, shrub, liana (including climbers and epiphytes), forb, or graminoid (grass or sedge). Although most food species consumed were identified in the field, species that could not be identified were collected for taxonomic identification at the National Herbarium in Addis Ababa. We recorded a food item as insects when the monkey was observed manipulating tree bark, searching through dead leaves or directly consuming insects . We collected 28,583 individual records (hereafter records) during 2085 h of observation (Continuous A = 441; Continuous B = 432; Patchy fragment = 601; Hilltop fragment = 611) over the 12-month study period . Feeding accounted for 15,302 of these records: Continuous A, 3027 records (monthly mean ± SD records = 252.3 ± 58.8); Continuous B, 3086 records (257.2, ± 72.2); Patchy fragment, 5239 records (436.6 ± 61.5); and Hilltop fragment, 3950 records (329.2 ± 68.1). Feeding accounted for 54.9% of Continuous A’s, 56.2% of Continuous B’s, 51.5% of Patchy’s and 53.2% of Hilltop’s overall activity budget . Monthly sampling effort was evenly distributed among groups throughout the year.
We assessed dietary composition for each month by determining the proportion of different food items, growth forms and species consumed in each study group. We then calculated annual consumption of food items, growth forms and species as the means of the 12 monthly values for each category. We combined four food items (mature leaves, branchlets, roots and mushrooms) into the category “other” in our analyses because each individually accounted for < 1% of the overall percentage of feeding records. We also compared the identity and contributions of the top five plant species in the diets of each group. We calculated the relative dietary preference (i.e., food selection ratios) by dividing the proportion of annual percentage of feeding records on a particular species i by the percentage stem density of species i in the study group’s home range. A selected food species is consumed more frequently than expected based on its proportional representation in the group’s home range . A food selection ratio of 1 indicates no selectivity for that food plant species, < 1 indicates a food species is avoided and > 1 indicates a food species is selected. We were only able to calculate selection ratios for trees, bamboo, shrubs, and lianas because stem density cannot be evaluated using the same methods for graminoids and forbs.
To estimate the annual plant species richness of the diet for each study group, we pooled the data from all sampling months within each group. We calculated within-month and annual dietary diversity indices for each group using the Shannon–Wiener index (H′), dominance index (D) and evenness index (J)  using the software PAST . To assess differences in inter-month dietary similarity among groups in continuous forest and forest fragments, we calculated the inter-month Morisita–Horn’s similarity indices (CH) of each group  using EstimateS . To assess the annual diet overlap among groups in continuous forest and forest fragments, we also calculated between group Morisita–Horn similarity indices. The index (CH) ranges from 0 (no diet overlap) to 1 (complete diet overlap).
We conducted all statistical tests using R version 3.3.2  with significance level set at P ≤ 0.05 unless otherwise stated. We tested data for normality and homogeneity of variances using the Shapiro–Wilk and Levene tests, respectively. We initially calculated and compared variables for each study group individually and examined the differences using the one-way analysis of variance (ANOVA) model followed by the Tukey honest significant difference (HSD) post hoc test. When the results for both groups within continuous forest and fragments were similar, we combined these groups for data analysis unless otherwise stated.
The completeness of plant species recorded in the diet is dependent on sample size. Therefore, we constructed a sample-based rarefaction curve plotting species richness with sampling effort (number of observation days) using PAleontological STatistics (PAST) software  to perform a valid comparison of dietary species richness among groups. To examine differences in monthly Shannon–Wiener dietary diversity indices among groups in continuous forest and forest fragments, we conducted a one-way analysis of variance (ANOVA) using the log transformed monthly values as replicas. To examine differences in monthly dietary dominance and evenness indices between continuous forest and fragment groups, we used a generalized linear model (GLM) with a quasibinomial error distribution and logit link-function as recommended for proportional data . We also used a GLM with a quasibinomial error distribution and logit link-function to test for differences in between-month Morisita–Horn similarity indices among groups. We identified differences among groups by post hoc multiple comparisons using function ‘glht’ from R package multcomp . We used a one-way ANOVA to test for differences in the percentage consumption of each food item and growth form between continuous forest and fragment groups. We applied logit transformations of proportion data before statistical analysis to normalize the data as recommended by Warton and Hui . We used linear regressions to assess whether the availability of non-bamboo young leaves, bamboo young leaves, fruits, flowers, and bamboo shoots was a good predictor of their consumption in each study group.
Vegetation description and temporal variation in resource availability
The vegetation in the ranges of Bale monkey groups inhabiting forest fragments was more diverse (55 species) than in the ranges of groups in continuous forest (23 species) (Additional file 1). We found 24 tree, 14 shrub, 11 liana, 4 forb, 1 bamboo, and 1 fern species in the home ranges of fragment groups but only 12 tree, 2 shrub, 7 liana, 1 forb and 1 bamboo species in the ranges of continuous forest groups (Additional file 1). The ranges of the two continuous forest groups were much more similar in plant species composition and abundance (19 of 23 species shared, Morisita–Horn similarity index = 0.99) than the ranges of the two fragment groups (28 of 55 species shared, Morisita–Horn similarity index = 0.40).
Bale monkey foods were much more abundant in continuous forest than in fragments. Monthly food availability indices of bamboo young leaves (ANOVA: F = 544.00, df = 1, P < 0.001), non-bamboo young leaves (ANOVA: F = 17.17, df = 1, P < 0.001), and fruits (ANOVA: F = 4.19, df = 1, P = 0.05) were all significantly higher in continuous forest than in forest fragments (Fig. 2). Bamboo young leaves were abundant throughout the year in continuous forest, consistently available at low levels in Patchy fragment, and consistently scarce in Hilltop fragment. However, there was no difference in the availability indices of flowers (ANOVA: F = 1.44, df = 1, P = 0.243) and bamboo shoots (ANOVA: F = 0.88, df = 1, P = 0.357) between continuous forest and fragment groups.
Dietary species richness, diversity and similarity
Overall, at least 65 plant species (1 bamboo, 12 trees, 5 shrubs, 8 lianas, ≥ 25 forbs and ≥ 14 graminoids) were food sources for Bale monkeys. They also ate one species of mushroom and presumably many unidentified species of insects. Dietary species richness was much higher in groups inhabiting forest fragments (≥ 61 species: Patchy ≥ 47 species; Hilltop ≥ 35 species) than in groups inhabiting continuous forests (12 species: Continuous A = 12 species; Continuous B = 8 species). The rarefaction curves for dietary plant species richness reached a plateau for each of the four study groups, suggesting we sampled intensively enough to obtain robust values for dietary species richness in all groups (Additional file 2).
The mean monthly Shannon–Wiener diversity index (H′) of food species was significantly higher in fragments than in continuous forest (ANOVA: F = 178.60, df = 1, P < 0.001; Fig. 3a). However, mean monthly dietary species evenness (J) was not significantly different between groups inhabiting fragments and those in continuous forest (GLM: F = 0.35, df = 1, P = 0.555; Fig. 3b). Lastly, mean monthly food plant species dominance was significantly higher for groups inhabiting continuous forest than for those in fragments (GLM: F = 163.60, df = 1, P < 0.001; Fig. 3c). Between-month dietary species similarity was significantly greater for groups in continuous forest than for groups in forest fragments (GLM: F = 380.80, df = 1, P < 0.001; Fig. 3d). Annual dietary species overlap was much lower between the two fragment groups (21 of 61 species shared; Morisita–Horn similarity index = 0.36) than for the groups in continuous forest (8 of 12 species shared; Morisita–Horn similarity index = 0.99).
Food item consumption
Groups in continuous forest spent significantly more time feeding on bamboo young leaves (61.1% vs. 8.5%; ANOVA: F = 54.19; P < 0.001), and significantly less time feeding on non-bamboo young leaves (3.8% vs. 30.8%; ANOVA: F = 44.66; P < 0.001), fruits (6.4% vs. 21.4%; ANOVA: F = 19.66; P = 0.001), stems (1.3% vs. 13.5%; ANOVA: F = 31.15; P < 0.001), petioles (0.0% vs. 4.5%; ANOVA: F = 20.00; P < 0.001), seeds (0.0% vs. 3.2%; ANOVA: F = 10.95; P = 0.002), and insects (2.0% vs. 8.4%; ANOVA: F = 10.45; P = 0.002) than groups in forest fragments (Fig. 4). Most of the difference in insect consumption between continuous forest and fragment groups was driven by Hilltop group (13.7%; Patchy: 3.3%; Continuous A: 2.4%; Continuous B: 1.5%). There was no difference in the consumption of bamboo shoots (18.8% vs. 7.2%; ANOVA: F = 0.001; P = 0.975), flowers (4.9% vs. 1.9%; ANOVA: F = 0.01; P = 0.941), and ‘other’ items (1.7% vs. 0.7%; ANOVA: F = 0.25; P = 0.619) between continuous forest and fragment groups.
Consumption of different growth forms
In forest fragments, a total of 10 tree, 1 bamboo, 5 shrub, 7 liana, 24 forb, 14 graminoid and 1 mushroom species were food sources for Bale monkeys whereas in continuous forest only 3 tree, 1 bamboo, 1 shrub, 4 liana, 2 forb, and 1 graminoid species were food sources for the monkeys. Groups in fragments spent less time feeding on bamboo (15.9% vs. 81.2%; ANOVA: F = 68.77, P < 0.001) and more time feeding on trees (22.7% vs. 11.8%; ANOVA: F = 3.30, P = 0.029), shrubs (12.7% vs. 0.1%; ANOVA: F = 337.10, P < 0.001), forbs (21.0% vs. 0.1%; ANOVA: F = 345.20, P < 0.001), and graminoids (17.1% vs. 0.7%; ANOVA: F = 98.33, P < 0.001) than groups in continuous forest (Additional file 3). There was no significant difference in the consumption of lianas (2.1% vs. 4.1%; ANOVA: F = 1.06, P = 0.309) between continuous forest and fragment groups (Additional file 3).
Top five species consumption
The cumulative percentage of the annual diet accounted for by the top five plant species was much higher in groups inhabiting continuous forest (continuous A = 96.2%; Continuous B = 97.3%) than in groups in fragments (Patchy = 62.0%; Hilltop = 50.4%). Bamboo (Arundinaria alpina) was the top food species consumed in both continuous forest groups (Mean = 81.2%) and in Patchy fragment group (30.2%) but was only the 10th most eaten food species in Hilltop fragment group (1.6%). Instead, in Hilltop fragment where bamboo was especially rare, a grass, Bothriochloa radicans, was the top plant species (15.3%) in the annual diet (Table 1). Bothriochloa radicans was only a minor (< 1%) dietary species for the other study groups, though 5 other graminoid species were more commonly consumed than B. radicans by the group in Patchy fragment. Galiniera saxifraga, a tree, was the second most frequent food source in continuous forest (Mean = 6.6%) and Hilltop fragment (11.8%) and the third most frequent food source in Patchy fragment group (7.4%).
The selection ratios of bamboo, tree, shrub, and liana food species accounting for > 0.5% of the annual diets of the study groups are presented in Table 2. Despite its dominance in the diets of the continuous forest groups, bamboo (Arundinaria alpina) had selection ratios of just below 1.00 in continuous forest (Continuous A = 0.94 and Continuous B = 0.95) owing to its extremely high stem density in this forest type. Although they ate much less bamboo, the fragment groups also exhibited comparable selection ratios to those of the continuous groups for bamboo (Patchy = 0.76; Hilltop: 1.00). The most selected plant species by both continuous forest groups was the tree Dombeya torrida with selection ratios of 6.78 (Continuous A) and 12.19 (Continuous B), respectively. For the fragment groups, the most selected food species were the trees Erythrina brucei (27.83) in Patchy fragment and Hagenia abyssinica (10.42) in Hilltop fragment. However, it should be noted that the top food species in the diet of Hilltop group was a graminoid species, B. radicans, for which a selection ratio could not be calculated. The one species that exhibited consistently high selection ratios and ranked among the top three species for dietary selectivity across groups was the tree Galiniera saxifraga (Continuous A: 2.20, 2nd rank; Continuous B: 1.85, 3rd rank; Patchy: 3.73, 2nd rank; Hilltop: 2.68, 3rd rank) from which Bale monkeys ate primarily fruits.
Temporal variability in food item availability and consumption
Bamboo young leaf and shoot consumption were significantly correlated with availability over time in Continuous groups A and B and in Patchy fragment group (Table 3). It is possible that similar relationships between these variables also existed in Hilltop fragment, but we did not track changes in bamboo abundance over time here because of the low density and small sizes of individuals of bamboo at this site. The consumption of fruits and flowers were also significantly correlated with availability for both groups inhabiting continuous forest and fruit consumption was significantly correlated with availability for Hilltop fragment group (Table 3).
Dietary responses to habitat degradation by Bale monkeys compared to other primates
Habitat degradation affects plant species richness, diversity and structure in forest fragments, ultimately reducing the availability of food resources for many primate species [48, 82, 83]. Specifically, the destruction or degradation of mature continuous forest promotes the growth in light gaps of pioneer species including fast-growing graminoids, forbs, shrubs, lianas and trees [9, 44, 84,85,86]. In our study, Bale monkeys in fragments exploited many of these pioneer species (Table 1), broadening their diet to include a far greater diversity of plant species (indigenous, exotic, and/or cultivated) and growth forms than conspecifics in continuous forest.
Primates inhabiting fragments frequently eat a higher percentage of leaves than conspecifics in continuous forest [41, 42, 46, 49]. Bale monkeys, however, ate a much lower percentage of leaves in fragments than in continuous forest largely because of the lower availability of bamboo in the former. In fragments, Bale monkeys modified their diet by increasing consumption of fruits, stems, petioles and insects as well as the leaves of a number of species other than bamboo. Interestingly, the much higher fruit consumption in fragments occurred despite fruit being significantly less available in fragments than in continuous forest.
Another common dietary response to habitat degradation among primates is to consume more secondary successional species, including shrubs, forbs, or graminoids [39, 41,42,43,44, 87]. The Bale monkeys in our study clearly fit this pattern, obtaining more than half their diet from shrubs, forbs, and graminoids in forest fragments (Additional file 3).
Primates in fragments also exhibit a tendency to consume exotic species and/or human crops from surrounding human matrix [46, 47, 88], a habitat absent from the ranges of conspecifics in continuous forest. Bale monkeys in both fragments in our study engaged in crop-raiding, though the group in Patchy fragment, whose range included more areas of human use , had a diet containing a higher overall percentage of crops. Farmer responses to crop raiding by Bale monkeys included throwing stones, hunting with spears, chasing them with dogs, or positioning scarecrows in cultivated areas (Mekonnen, personal observation). In addition to crops, Bale monkeys in fragments also consumed bamboo planted near the homes of local people, triggering additional human-monkey conflict, particularly at Patchy fragment (Mekonnen, personal observation).
Lastly, the species richness of primate diets in fragments often differs from in continuous forests, increasing substantially for some primates (e.g., Alouatta pigra ; Cercopithecus mitis boutourlinii ), while decreasing for others (e.g., Ateles geoffroyi ; Propithecus diadema ). Bale monkeys appear to adopt the former approach, consuming many more plant—and probably insect—species in fragments. The strategy of continuous forest Bale monkeys to focus primarily on bamboo is simply not an option for monkeys in fragments where bamboo populations have been degraded or almost eradicated and the monkeys must diversify their diet to survive.
Dietary flexibility in Bale monkeys relative to other Chlorocebus species
Several of the Chlorocebus species are well-studied and eat varied diets with the top food item ranging from fruit in Nigerian (C. tantalus: ) and Senegalese (C. sabaeus: ) populations to gum or flowers in Kenyan populations (C. pygerythrus: [70, 91, 92]) (Table 4). Among Chlorocebus, Bale monkeys (C. djamdjamensis) are unique in their heavy reliance on the young leaves and shoots of bamboo in relatively undisturbed continuous forest habitats.
Intriguingly, our study revealed that C. djamdjamensis inhabiting fragments consumed diets more comparable to those of the other less specialized Chlorocebus species than to continuous forest-dwelling C. djamdjamensis populations. For example, percentages of fruit and graminoid consumption by C. djamdjamensis in fragments were similar to those reported for East African C. pygerythrus populations (Table 4). Further, levels of invertebrate consumption by the Hilltop group of C. djamdjamensis mirrored levels of invertebrate consumption by C. sabaeus in West Africa (Table 4). Lastly, C. tantalus’s diet in West Africa was 2–3 times more species rich than the diets of C. djamdjamensis in continuous forest though actually somewhat less species rich than the diets of C. djamdjamensis in fragments (Table 4). Though the one dietary commonality among C. djamdjamensis groups in our study was a greater reliance on leaves than in any of the other Chlorocebus spp. (maximum 25% of the diet), consumption of leaves still varied widely among C. djamdjamensis groups.
The remarkable dietary flexibility exhibited by C. djamdjamensis in fragments has at least two possible explanations. First, they may retain some of the ancestral ecological flexibility characteristic of other members of the genus Chlorocebus, only expressing this plasticity when habitat degradation requires them to diversify their diets beyond primarily bamboo and a handful of other species. A second possibility is that genetic introgression (hybridization) between C. djamdjamensis and parapatric C. aethiops and C. pygerythrus in fragmented forest areas [57, 60, 93] endows some C. djamdjamensis populations with the ability to radically alter their diets in fragments.
Bamboo consumption across bamboo eating mammals
Adaptation to bamboo-dominated forests and diets appears to have evolved at least six times among the mammals: giant pandas in China [34, 94], red pandas in India, Nepal, Bhutan, Myanmar, and China , bamboo lemurs (Hapalemur/Prolemur spp.) in Madagascar [26, 95], Assamese macaques (Macaca assamensis) in China [68, 96], golden monkeys in Uganda and Rwanda [67, 97], and Bale monkeys in Ethiopia (this study; Table 5). Most of the primate taxa are members of ecologically-flexible genera (Macaca: ; Chlorocebus: ) or species (Cercopithecus mitis: [64, 99]), while giant and red pandas belong to different more specialized families in the order Carnivora . Among the other bamboo-eating primates, the closest phylogenetically and geographically to Chlorocebus djamdjamensis is Cercopithecus mitis kandti (Table 5). Both taxa feed primarily on a single species of African highland bamboo (Arundinaria alpina) though C. mitis kandti rely on it less than C. djamdjamensis populations in continuous forest and more than C. djamdjamensis populations in fragmented forest ([54, 100]; This study).
Giant and red pandas are arguably the best known obligate specialist folivores, exploiting diets consisting almost entirely of bamboo [34, 94]. Neither species exhibits an ability to cope with intensive habitat degradation [34, 94]. Among primates, some bamboo lemurs appear to be the most inclined towards extreme specialization . In particular, the greater bamboo lemur (Prolemur simus) consumes a diet of 95% bamboo  and does not appear to exist outside of bamboo forest habitat [101, 102]. P. simus also relies heavily on an unusually cyanogenic bamboo species  and is probably the only ‘obligate specialist’ on bamboo among the bamboo-eating primates. Indeed, recent studies of several other bamboo lemurs (Hapalemur spp.) found they can survive in habitats without bamboo, consuming more species-rich diets in these habitats, including a high percentage of graminoids in the cases of H. alaotrensis  and H. meridionalis . The increased consumption of graminoids by these Hapalemur spp. provides an interesting parallel to the Bale monkeys in our study, which also consumed more graminoids at fragmented sites where bamboo is scarce. Overall, it appears that, with the exception of Prolemur simus, bamboo eating primates are more dietarily flexible than giant and red pandas. This pattern is consistent with the evidence that the bamboo feeding adaptation in pandas is much older than it is for any of the bamboo feeding primates (e.g., [69, 93,94,95]).
Implications for conservation and management
Our study revealed that, like most other bamboo-eating primates, Bale monkeys have the flexibility to cope with changes in the identity and abundance of foods resulting from habitat degradation and loss of bamboo, at least over the short-term. More intensive long-term studies of Bale monkeys in both fragmented and continuous habitats are, however, needed to examine and address some of the potential drawbacks of life in fragments. The greatest conservation concern raised by our study is that of human-monkey conflict at fragmented sites, especially at Patchy fragment. As in many other sites where primates crop raid , humans near fragments in our study sometimes responded to Bale monkey crop raiding in a manner that put Bale monkeys at risk, hunting them with spears and dogs. A more detailed study of this human-monkey conflict and its impact on Bale monkey survivorship in fragments should be a priority along with developing and implementing strategies to mitigate this conflict . Any Bale monkey habitat restoration programs undertaken at fragments should focus on increasing fragment sizes, minimizing edge effects, incorporating matrix habitats into management plans, and mitigating human monkey-conflict (cf., [88, 106]). Moreover, the remaining continuous bamboo forest habitat in the southern Ethiopian Highlands should be protected from further deforestation both to best ensure the long-term persistence of Bale monkeys  and to prevent the functional homogenization of biodiversity in this important region for conservation [19, 107].
Bale monkeys in fragments have smaller group sizes, and experience lower food availability and habitat quality relative to those in continuous forest (; This study). Consequently, they consume more diverse species-rich diets, including more secondary and cultivated food resources. While Bale monkeys are the only specialized members of a genus, Chlorocebus, whose other five species are all ecological generalists, we hypothesize that they have either retained the ancestral Chlorocebus ability to fall back on a generalist diet where necessary or that populations in fragments have reacquired this ability through interbreeding with parapatric grivet (C. aethiops) or vervet (C. pygerythrus) populations. Despite the encouraging dietary flexibility documented among Bale monkeys in our study, the long-term conservation prospects for populations in forest fragments remain unclear and will require long-term population monitoring and conservation actions to ensure their persistence in the southern Ethiopian Highlands.
Centre for Ecological and Evolutionary Synthesis
International Union for Conservation of Nature
diameter at breast height
- H’ :
- D :
- J :
- CH :
Morisita–Horn’s similarity index
analysis of variance
- Tukey HSD:
Tukey honest significant difference test
generalized linear model
plant secondary metabolites
bamboo young leaves
non-bamboo young leaves
young leaves except bamboo and grass
Hansen MC, Potapov PV, Moore R, Hancher M, Turubanova S, Tyukavina A, Thau D, Stehman S, Goetz S, Loveland T. High-resolution global maps of 21st-century forest cover change. Science. 2013;342:850–3.
Newbold T, Hudson LN, Hill SLL, Contu S, Lysenko I, Senior RA, Borger L, Bennett DJ, Choimes A, Collen B, et al. Global effects of land use on local terrestrial biodiversity. Nature. 2015;520:45–50.
Watson James EM, Shanahan Danielle F, Di Marco M, Allan J, Laurance William F, Sanderson Eric W, Mackey B, Venter O. Catastrophic declines in wilderness areas undermine global environment targets. Curr Biol. 2016;26:2929–34.
Tilman D, Clark M, Williams DR, Kimmel K, Polasky S, Packer C. Future threats to biodiversity and pathways to their prevention. Nature. 2017;546:73–81.
Joppa L, O’Connor B, Visconti P, Smith C, Geldmann J, Hoffmann M, Watson JE, Butchart SH, Virah-Sawmy M, Halpern BS. Filling in biodiversity threat gaps. Science. 2016;352:416–8.
Laurance WF, Sayer J, Cassman KG. Agricultural expansion and its impacts on tropical nature. Trends Ecol Evol. 2014;29:107–16.
Wei FW, Swaisgood R, Hu YB, Nie YG, Yan L, Zhang ZJ, Qi DW, Zhu LF. Progress in the ecology and conservation of giant pandas. Conserv Biol. 2015;29:1497–507.
Arroyo-Rodríguez V, Mandujano S. Forest fragmentation modifies habitat quality for Alouatta palliata. Int J Primatol. 2006;27:1079–96.
Laurance WF, Nascimento HE, Laurance SG, Andrade AC, Fearnside PM, Ribeiro JE, Capretz RL. Rain forest fragmentation and the proliferation of successional trees. Ecology. 2006;87:469–82.
Wilson MC, Chen X-Y, Corlett RT, Didham RK, Ding P, Holt RD, Holyoak M, Hu G, Hughes AC, Jiang L, et al. Habitat fragmentation and biodiversity conservation: key findings and future challenges. Landsc Ecol. 2016;31:219–27.
Chapman CA, Chapman LJ, Jacob AL, Rothman JM, Omeja P, Reyna-Hurtado R, Hartter J, Lawes MJ. Tropical tree community shifts: implications for wildlife conservation. Biol Conserv. 2010;143:366–74.
da Silva LG, Ribeiro MC, Hasui É, da Costa CA, da Cunha RGT. Patch size, functional isolation, visibility and matrix permeability influences Neotropical primate occurrence within highly fragmented landscapes. PLoS ONE. 2015;10:e0114025.
Gardner TA, Barlow J, Chazdon R, Ewers RM, Harvey CA, Peres CA, Sodhi NS. Prospects for tropical forest biodiversity in a human-modified world. Ecol Lett. 2009;12:561–82.
Linderman MA, An L, Bearer S, He G, Ouyang Z, Liu J. Modeling the spatio-temporal dynamics and interactions of households, landscapes, and giant panda habitat. Ecol Model. 2005;183:47–65.
Fahrig L. Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst. 2003;34:487–515.
Onderdonk DA, Chapman CA. Coping with forest fragmentation: the primates of Kibale National Park, Uganda. Int J Primatol. 2000;21:587–611.
Lawes MJ, Mealin PE, Piper SE. Patch occupancy and potential metapopulation dynamics of three forest mammals in fragmented afromontane forest in South Africa. Conserv Biol. 2000;14:1088–98.
Dunn JC, Cristobal-Azkarate J, Vea JJ. Differences in diet and activity pattern between two groups of Alouatta palliata associated with the availability of big trees and fruit of top food taxa. Am J Primatol. 2009;71:654–62.
Clavel J, Julliard R, Devictor V. Worldwide decline of specialist species: toward a global functional homogenization? Front Ecol Environ. 2011;9:222–8.
Shipley LA, Forbey JS, Moore BD. Revisiting the dietary niche: when is a mammalian herbivore a specialist? Integr Comp Biol. 2009;49:274–90.
Panthi S, Khanal G, Acharya KP, Aryal A, Srivathsa A. Large anthropogenic impacts on a charismatic small carnivore: insights from distribution surveys of red panda Ailurus fulgens in Nepal. PLoS ONE. 2017;12:e0180978.
de Almeida-Rocha JM, Peres CA, Oliveira LC. Primate responses to anthropogenic habitat disturbance: a pantropical meta-analysis. Biol Conserv. 2017;215:30–8.
Fisher DO, Blomberg SP, Owens IPF. Extrinsic versus intrinsic factors in the decline and extinction of Australian marsupials. Proc R Soc B Biol Sci. 2003;270:1801–8.
Harcourt AH, Coppeto S, Parks S. Rarity, specialization and extinction in primates. J Biogeogr. 2002;29:445–56.
Twinomugisha D, Chapman CA. Golden monkey populations decline despite improved protection in Mgahinga Gorilla National Park, Uganda. Afr J Ecol. 2007;45:220–4.
Tan CL. Group composition, home range size, and diet of three sympatric bamboo lemur species (genus Hapalemur) in Ranomafana National Park. Madagascar. Int J Primatol. 1999;20:547–66.
Eppley TM, Tan CL, Arrigo-Nelson SJ, Donati G, Ballhorn DJ, Ganzhorn JU. High energy or protein concentrations in food as possible offsets for cyanide consumption by specialized bamboo lemurs in Madagascar. Int J Primatol. 2017;38:881–99.
Wei F, Hu Y, Yan L, Nie Y, Wu Q, Zhang Z. Giant pandas are not an evolutionary cul-de-sac: evidence from multidisciplinary research. Mol Biol Evol. 2015;32:4–12.
Ganzhorn JU, Arrigo- Nelson SJ, Carrai V, Chalise MK, Donati G, Droescher I, Eppley TM, Irwin MT, Koch F, Koenig A, et al. The importance of protein in leaf selection of folivorous primates. Am J Primatol. 2017;79:1–13.
Fashing PJ, Dierenfeld ES, Mowry CB. Influence of plant and soil chemistry on food selection, ranging patterns, and biomass of Colobus guereza in Kakamega Forest, Kenya. Int J Primatol. 2007;28:673–703.
Moore BD, Foley WJ. Tree use by koalas in a chemically complex landscape. Nature. 2005;435:488–90.
Villalba JJ, Provenza FD. Learning and dietary choice in herbivores. Rangel Ecol Manag. 2009;62:399–406.
Kamilar JM, Paciulli LM. Examining the extinction risk of specialized folivores: a comparative study of colobine monkeys. Am J Primatol. 2008;70:816–27.
Schaller GB. Giant pandas of Wolong. Chicago: University of Chicago press; 1985.
Nowak K, Lee PC. “Specialist” primates can be flexible in response to habitat alteration. In: Marsh LK, Chapman CA, editors. Primates in fragments: complexity and resilience. New York: Springer; 2013. p. 199–211.
Eppley TM, Donati G, Ramanamanjato JB, Randriatafika F, Andriamandimbiarisoa LN, Rabehevitra D, Ravelomanantsoa R, Ganzhorn JU. The use of an invasive species habitat by a small folivorous primate: implications for lemur conservation in Madagascar. PLoS ONE. 2015;10:e0140981.
Melzer A, Cristescu R, Ellis W, FitzGibbon S, Manno G. The habitat and diet of koalas (Phascolarctos cinereus) in Queensland. Aust Mammal. 2014;36:189–99.
Estrada A, Garber PA, Rylands AB, Roos C, Fernandez-Duque E, Di Fiore A, Nekaris KAI, Nijman V, Heymann EW, Lambert JE. Impending extinction crisis of the world’s primates: Why primates matter. Sci Adv. 2017;3:e1600946.
Bicca-Marques JC. How do howler monkeys cope with habitat fragmentation? In: Marsh LK, editor. Primates in fragments: complexity and resilience. New York: Plenum Publishers; 2003. p. 283–303.
Tutin CEG. Fragmented living: behavioural ecology of primates in a forest fragment in the Lopé Reserve, Gabon. Primates. 1999;40:249.
Chaves OM, Stoner KE, Arroyo-Rodriguez V. Differences in diet between spider monkey groups living in forest fragments and continuous forest in Mexico. Biotropica. 2012;44:105–13.
Irwin MT. Feeding ecology of Propithecus diadema in forest fragments and continuous forest. Int J Primatol. 2008;29:95–115.
Dunn JC, Asensio N, Arroyo-Rodríguez V, Schnitzer S, Cristóbal-Azkarate J. The ranging costs of a fallback food: liana consumption supplements diet but increases foraging effort in howler monkeys. Biotropica. 2012;44:705–14.
Grassi C. Variability in habitat, diet, and social structure of Hapalemur griseus in Ranomafana National Park, Madagascar. Am J Phys Anthropol. 2006;131:50–63.
Eppley TM, Donati G, Ganzhorn JU. Determinants of terrestrial feeding in an arboreal primate: the case of the southern bamboo lemur (Hapalemur meridionalis). Am J Phys Anthropol. 2016;161:328–42.
Chaves OM, Bicca-Marques JC. Feeding strategies of brown howler monkeys in response to variations in food availability. PLoS ONE. 2016;11:e0145819.
Maibeche Y, Moali A, Yahi N, Menard N. Is diet flexibility an adaptive life trait for relictual and peri-urban populations of the endangered primate Macaca sylvanus? PLoS ONE. 2015;10:e0118596.
Rivera A, Calmé S. Forest fragmentation and its effects on the feeding ecology of black howlers (Alouatta pigra) from the Calakmul area in Mexico. In: Estrada A, Garber PA, Pavelka MSM, Luecke L, editors. New perspectives in the study of Mesoamerican primates: distribution, ecology, behavior, and conservation. New York: Springer; 2006. p. 189–213.
Tesfaye D, Fashing PJ, Bekele A, Mekonnen A, Atickem A. Ecological flexibility in Boutourlini’s blue monkeys (Cercopithecus mitis boutourlinii) in Jibat Forest, Ethiopia: a comparison of habitat use, ranging behavior, and diet in intact and fragmented forest. Int J Primatol. 2013;34:615–40.
Sharma N, Madhusudan MD, Sinha A. Local and landscape correlates of primate distribution and persistence in the remnant lowland rainforests of the upper Brahmaputra Valley, Northeastern India. Conserv Biol. 2014;28:95–106.
Fan PF, Fei HL, Scott MB, Zhang W, Ma CY. Habitat and food choice of the critically endangered cao vit gibbon (Nomascus nasutus) in China: implications for conservation. Biol Conserv. 2011;144:2247–54.
Marsh LK. Primates in fragments: ecology and conservation. New York: Kluwer Academic Publishers; 2003.
Benchimol M, Peres CA. Anthropogenic modulators of species–area relationships in Neotropical primates: a continental-scale analysis of fragmented forest landscapes. Divers Distrib. 2013;19:1339–52.
Mekonnen A, Bekele A, Fashing PJ, Hemson G, Atickem A. Diet, activity patterns, and ranging ecology of the Bale monkey (Chlorocebus djamdjamensis) in Odobullu Forest, Ethiopia. Int J Primatol. 2010;31:339–62.
Mekonnen A, Bekele A, Hemson G, Teshome E, Atickem A. Population size and habitat preference of the vulnerable Bale monkey Chlorocebus djamdjamensis in Odobullu Forest and its distribution across the Bale Mountains, Ethiopia. Oryx. 2010;44:558–63.
Butynski TM, Gippoliti S, Kingdon J, De Jong Y. Chlorocebus djamdjamensis. The IUCN red list of threatened species 2008: e.T4240A10699069. https://0-dx-doi-org.brum.beds.ac.uk/10.2305/IUCN.UK.2008.RLTS.T4240A10699069.en. 2008. Accessed 02 Nov 2017.
Mekonnen A, Bekele A, Fashing PJ, Lernould JM, Atickem A, Stenseth NC. Newly discovered Bale monkey populations in forest fragments in southern Ethiopia: evidence of crop raiding, hybridization with grivets, and other conservation threats. Am J Primatol. 2012;74:423–32.
Mekonnen A, Jaffe KE. Bale Mountains monkey Chlorocebus djamdjamensis Neumann 1902. In: Rowe N, Mayers M, editors. All the world’s primates. Charlestown: Pogonias Press; 2016. p. 473–4.
Anandam MV, Bennett EL, Davenport TRB, Davies NJ, Detwiler KM, Engelhardt A, Eudey AA, Gadsby EL, Groves CP, Healy A, et al. Family Cercopithecidae (Old World monkeys)—species accounts of Cercopithecidae. In: Mittermeier RA, Rylands AB, Wilson DE, editors. Handbook of the mammals of the world Vol 3 Primates. Barcelona: Lynx Edicions; 2013. p. 628–753.
Haus T, Akom E, Agwanda B, Hofreiter M, Roos C, Zinner D. Mitochondrial diversity and distribution of African green monkeys (Chlorocebus Gray, 1870). Am J Primatol. 2013;75:350–60.
Isbell LA, Pruetz JD, Young TP. Movements of vervets (Cercopithecus aethiops) and patas monkeys (Erythrocebus patas) as estimators of food resource size, density, and distribution. Behav Ecol Sociobiol. 1998;42:123–33.
Barrett AS, Barrett L, Henzi P, Brown LR. Resource selection on woody plant species by vervet monkeys (Chlorocebus pygerythrus) in mixed-broad leaf savanna. Afr J Wildl Res. 2016;46:14–21.
Jaffe KE, Isbell LA. The guenons: polyspecific associations in socioecological perspective. In: Campbell CJ, Fuentes AF, MacKinnon KC, Bearder SK, Stumpf RM, editors. Primates in perspective. 2nd ed. New York: Oxford University Press; 2011. p. 277–300.
Butynski TM. Comparative ecology of blue monkeys (Cercopithecus mitis) in high-and low-density subpopulations. Ecol Monogr. 1990;60:1–26.
Carpaneto GM, Gippoliti S. Primates of the Harenna Forest, Ethiopia. Primate Conserv. 1994;11:12–5.
Mekonnen A, Fashing PJ, Bekele A, Hernandez-Aguilar RA, Rueness EK, Nguyen N, Stenseth NC. 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. Am J Primatol. 2017;79:e22644.
Twinomugisha D, Basuta GI, Chapman CA. Status and ecology of the golden monkey (Cercopithecus mitis kandti) in Mgahinga Gorilla National Park, Uganda. Afr J Ecol. 2003;41:47–55.
Zhou Q, Wei H, Huang Z, Huang C. Diet of the Assamese macaque Macaca assamensis in limestone habitats of Nonggang, China. Curr Zool. 2011;57:18–25.
Hu Y, Wu Q, Ma S, Ma T, Shan L, Wang X, Nie Y, Ning Z, Yan L, Xiu Y. Comparative genomics reveals convergent evolution between the bamboo-eating giant and red pandas. Proc Natl Acad Sci. 2017;114:1081–6.
Whitten PL. Diet and dominance among female vervet monkeys (Cercopithecus aethiops). Am J Primatol. 1983;5:139–59.
Krebs CJ. Ecological methodology. California: Benjamin/Cummings Menlo Park; 1999.
Fashing PJ. Feeding ecology of guerezas in the Kakamega Forest, Kenya: the importance of Moraceae fruit in their diet. Int J Primatol. 2001;22:579–609.
Fashing PJ, Nguyen N, Venkataraman VV, Kerby JT. Gelada feeding ecology in an intact ecosystem at Guassa, Ethiopia: variability over time and implications for theropith and hominin dietary evolution. Am J Phys Anthropol. 2014;155:1–16.
Altmann J. Observational study of behavior: sampling methods. Behaviour. 1974;49:227–67.
Hammer Ø, Harper D, Ryan P. PAST-palaeontological statistics, ver. 1.89. Oslo: University of Oslo; 2009. p. 1–31.
Horn HS. Measurement of “overlap” in comparative ecological studies. Am Nat. 1966;100:419–24.
Colwell RK. EstimateS: statistical estimation of species richness and shared species from samples. version 9.1.0. http://viceroy.eeb.uconn.edu/estimates/. 2013.
R Development Core Team. R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. http://www.r-project.org/ 2016.
Crawley MJ. The R book. Chichester: Wiley; 2012.
Hothorn T, Bretz F, Westfall P. Simultaneous inference in general parametric models. Biom J. 2008;50:346–63.
Warton DI, Hui FK. The arcsine is asinine: the analysis of proportions in ecology. Ecology. 2011;92:3–10.
Boyle SA, Zartman CE, Spironello WR, Smith AT. Implications of habitat fragmentation on the diet of bearded saki monkeys in central Amazonian forest. J Mammal. 2012;93:959–76.
Eppley TM, Verjans E, Donati G. Coping with low-quality diets: a first account of the feeding ecology of the southern gentle lemur, Hapalemur meridionalis, in the Mandena littoral forest, southeast Madagascar. Primates. 2011;52:7–13.
Tan CL. Behavior and ecology of gentle lemurs (genus Hapalemur). In: Gould L, Sauther ML, editors. Lemurs: ecology and adaptation. New York: Springer; 2006. p. 369–81.
Laurance WF, Pérez-Salicrup D, Delamônica P, Fearnside PM, D’Angelo S, Jerozolinski A, Pohl L, Lovejoy TE. Rain forest fragmentation and the structure of Amazonian liana communities. Ecology. 2001;82:105–16.
Tabarelli M, Aguiar AV, Girao LC, Peres CA, Lopes AV. Effects of pioneer tree species hyperabundance on forest fragments in northeastern Brazil. Conserv Biol. 2010;24:1654–63.
Cristóbal-Azkarate J, Arroyo-Rodríguez V. Diet and activity pattern of howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: effects of habitat fragmentation and implications for conservation. Am J Primatol. 2007;69:1013–29.
Anderson J, Rowcliffe JM, Cowlishaw G. Does the matrix matter? A forest primate in a complex agricultural landscape. Biol Conserv. 2007;135:212–22.
Agmen FL, Chapman HM, Bawuro M. Seed dispersal by tantalus monkeys (Chlorocebus tantalus tantalus) in a Nigerian montane forest. Afr J Ecol. 2010;48:1123–8.
Harrison MJ. Age and sex differences in the diet and feeding strategies of the green monkey, Cercopithecus sabaeus. Anim Behav. 1983;31:969–77.
Wrangham R, Waterman P. Feeding behaviour of vervet monkeys on Acacia tortilis and Acacia xanthophloea: with special reference to reproductive strategies and tannin production. J Anim Ecol. 1981;50:715–31.
Isbell LA, Pruetz JD, Lewis M, Young TP. Locomotor activity differences between sympatric patas monkeys (Erythrocebus patas) and vervet monkeys (Cercopithecus aethiops): implications for the evolution of long hindlimb length in Homo. Am J Phys Anthropol. 1998;105:199–207.
Mekonnen A, Rueness EK, Stenseth NC, Fashing PJ, Bekele A, Hernandez-Aguilar RA, Missbach R, Haus T, Zinner D, Roos C. Population genetic structure and evolutionary history of Bale monkeys (Chlorocebus djamdjamensis) in the southern Ethiopian Highlands. BMC Evol Biol (in review).
Nie YG, Zhang ZJ, Raubenheimer D, Elser JJ, Wei W, Wei FW. Obligate herbivory in an ancestrally carnivorous lineage: the giant panda and bamboo from the perspective of nutritional geometry. Funct Ecol. 2015;29:26–34.
Ballhorn DJ, Rakotoarivelo FP, Kautz S. Coevolution of cyanogenic bamboos and bamboo lemurs on Madagascar. PLoS ONE. 2016;11:e0158935.
Huang Z, Huang C, Tang C, Huang L, Tang H, Ma G, Zhou Q. Dietary adaptations of Assamese macaques (Macaca assamensis) in limestone forests in Southwest China. Am J Primatol. 2015;77:171–85.
Twinomugisha D, Chapman CA. Golden monkey ranging in relation to spatial and temporal variation in food availability. Afr J Ecol. 2008;46:585–93.
Thierry B, Singh M, Kaumanns W. Macaque societies: a model for the study of social organization. Cambridge: Cambridge University Press; 2004.
Cords M. Mixed-species association of Cercopithecus monkeys in the Kakamega Forest, Kenya. Univ Calif Publ Zool. 1987;1:1–109.
Twinomugisha D, Chapman CA, Lawes MJ, Worman COD, Danish LM. How does the golden monkey of the Virungas cope in a fruit-scarce environment? In: Newton-Fisher NE, Notman H, Paterson JD, Reynolds V, editors. Primates of Western Uganda. New York: Springer; 2006. p. 45–60.
Wright PC, Johnson SE, Irwin MT, Jacobs R, Schlichting P, Lehman S, Louis EE Jr, Arrigo-Nelson SJ, Raharison JL, Rafalirarison RR. The crisis of the critically endangered greater bamboo lemur (Prolemur simus). Primate Conserv. 2008;23:5–17.
Olson ER, Marsh RA, Bovard BN, Randrianarimanana HL, Ravaloharimanitra M, Ratsimbazafy JH, King T. Habitat preferences of the critically endangered greater bamboo lemur (Prolemur simus) and densities of one of its primary food sources, Madagascar giant bamboo (Cathariostachys madagascariensis), in sites with different degrees of anthropogenic and natural disturbance. Int J Primatol. 2013;34:486–99.
Mutschler T. Folivory in a small-bodied lemur: the nutrition of the Alaotran gentle lemur (Hapalemur griseus alaotrensis). In: Rakotosamimanana B, Rasamimanana H, Ganzhorn JU, Goodman SM, editors. New directions in lemur studies. New York: Plenum Press; 1999. p. 221–39.
Hill CM, Webber AD. Perceptions of nonhuman primates in human–wildlife conflict scenarios. Am J Primatol. 2010;72:919–24.
Hill CM, Wallace GE. Crop protection and conflict mitigation: reducing the costs of living alongside non-human primates. Biodivers Conserv. 2012;21:2569–87.
Estrada A, Raboy BE, Oliveira LC. Agroecosystems and primate conservation in the tropics: a review. Am J Primatol. 2012;74:696–711.
Olden JD, LeRoy Poff N, Douglas MR, Douglas ME, Fausch KD. Ecological and evolutionary consequences of biotic homogenization. Trends Ecol Evol. 2004;19:18–24.
Overdorff DJ, Strait SG, Telo A. Seasonal variation in activity and diet in a small-bodied folivorous primate, Hapalemur griseus, in southeastern Madagascar. Am J Primatol. 1997;43:211–23.
AM designed the study with feedback from PJF, AB and NCS; AM collected and analysed the data and wrote the first draft of the manuscript; AM and PJF revised the manuscript extensively and AM, PJF, AB, RAHA, EKR and NCS all revised subsequent versions of the manuscript. All authors read and approved the final manuscript.
We would like to thank the People’s Trust for Endangered Species, International Foundation for Science, Conservation and Research Foundation, Primate Action Fund of Conservation International, and Fresno Chaffee Zoo for financial support to this project. This study would not have been possible without generous financial support to Addisu Mekonnen from the Norwegian State Educational Loan Fund (Lånekassen) under the Quota Scholarship program. Peter Fashing thanks the U.S.-Norway Fulbright Foundation for their support during the preparation of this manuscript and San Diego Zoo for their support of his long-term research endeavors in Ethiopia. We thank the Centre for Ecological and Evolutionary Synthesis (CEES) of the University of Oslo and the Department of Zoological Sciences of Addis Ababa University for logistical support. We are grateful to the Ethiopian Wildlife Conservation Authority, Oromia Region Forest and Wildlife Enterprise, Sidama and West Arsi Zone Agriculture Offices, and Goba, Kokosa and Arbegona District Agriculture Offices for granting permission to conduct this study. We thank Melaku Wondafrash and Assefa Hailu for taxonomic identification of plants. We are also grateful to our field research assistants, Mengistu Birhan and Mamar Dilnesa, for their invaluable help on this project. We thank Amera Moges and Sewalem Tsehay for additional assistance during field work. We also thank our local guides and camp attendants, Firdie Sultan, Omer Hajeleye, Hassen Wolle, Jemal Kedir, Mudie Kedir and Matiyos Yakob.
The authors declare that they have no competing interests.
Availability of data and materials
Nearly all the data are summarized in the manuscript itself. Please contact the corresponding author regarding any additional queries related to the dataset generated and analysed during the current study.
Consent for publication
Ethics approval and consent to participate
People’s Trust for Endangered Species, UK; International Foundation for Science, Sweden; Conservation and Research Foundation, USA; Primate Action Fund of Conservation International; USA and Fresno Chaffee Zoo, USA.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Stem density of all plant species (≥ 2 m tall) within vegetation quadrats in the home ranges of study groups. Continuous A (n = 9110 stems), Continuous B (n = 5410 stems), Patchy (n = 3388 stems) and Hilltop (n = 2312) groups (* exotic species).
Sample based rarefaction curves of plant species consumed by Bale monkeys among four study groups. Samples were collected in the continuous forest (Continuous A, N = 52 days (A); Continuous B, N = 54 days (B) and forest fragments (Patchy fragment, N = 62 days (C); Hilltop fragment, N = 67 days (D). The red (rarefaction) curves represent the cumulative number of plant species consumed by the study groups and blue curves represent the 95% confidence intervals.
The proportion of feeding records devoted to consuming different plant growth forms by the four study groups. Proportions were summarized from N = 12 months, mean ± SE.
About this article
Cite this article
Mekonnen, A., Fashing, P.J., Bekele, A. et al. Dietary flexibility of Bale monkeys (Chlorocebus djamdjamensis) in southern Ethiopia: effects of habitat degradation and life in fragments. BMC Ecol 18, 4 (2018). https://0-doi-org.brum.beds.ac.uk/10.1186/s12898-018-0161-4
- Continuous forest
- Feeding ecology
- Fragmented forest
- Human-wildlife conflict
- Specialist folivore