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

BMC EcologyBMC series – open, inclusive and trusted201818:4

https://doi.org/10.1186/s12898-018-0161-4

Received: 21 June 2017

Accepted: 29 January 2018

Published: 6 February 2018

Abstract

Background

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).

Results

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%).

Conclusions

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.

Keywords

BambooContinuous forestFeeding ecologyFragmented forestHuman-wildlife conflictSpecialist folivore

Background

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 [3]. 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 [46]. Habitat degradation modifies vegetation composition and structure, consequently reducing habitat quality and food availability for species inhabiting an area [610]. 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 [1214]. 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 [1517]. 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 [19]. Specialist folivores are particularly threatened [20] because they tend to be forest-dwelling, arboreal, and/or sensitive to changes in forest structure [14, 2124]. Examples include marsupials like koalas (Phascolarctos cinereus) and greater gliders (Petauroides volans) that feed primarily on Eucalyptus [23], 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 [3537].

Although habitat degradation is increasingly common in tropical forests [38], 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: [41], Propithecus diadema: [42]), (2) foods from secondary growth species, including lianas and climbers (Ateles geoffroyi: [41], Alouatta palliata: [43]) or graminoids and forbs (Hapalemur griseus: [44], H. meridionalis: [45]), or (3) human crops and exotic species: (Alouatta guariba clamitans: [46], Macaca sylvanus: [47]). Furthermore, some primate taxa persist in forest fragments by increasing the plant species richness of their diet (Alouatta pigra: [48], Cercopithecus mitis boutourlinii: [49]) while others cope by eating a less species rich diet (Propithecus diadema: [42], Ateles geoffroyi: [41]). 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: [50]).

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, 5658]. As a result, the species is currently classified as Vulnerable by the International Union for Conservation of Nature (IUCN) [56].

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 [6163]. 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 [57], suggested the species might be of greater ecological flexibility than previously believed [5456, 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 [66]. 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 [63], as well as with those of other bamboo-eating mammals, including several other primates (e.g., Cercopithecus mitis kandti [67], Macaca assamensis [68], Prolemur simus [26], Hapalemur spp. [26]) 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 [57] 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 [54], but that conspecifics in fragments would exploit diets more similar to those of other more generalized Chlorocebus species [61, 70].

Methods

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 [66]. 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 [54]. The continuous forest consists of four habitat types: mostly bamboo forest and tree-dominated forest but also shrubland and occasional grasslands [55]. 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 [66]. 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 [57]. 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 [57]. The forest fragments are separated from the continuous forest by ~ 160 km [66].

Study groups

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) [66], 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%) [66]. 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 [66].

Climate

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).
Figure 1
Fig. 1

Monthly temperature and rainfall patterns in continuous forest and one forest fragment. Monthly temperature (mean, mean minimum and mean maximum) and rainfall patterns at Odobullu continuous forest (2758 m asl) and Kokosa (Patchy) forest fragment (2634 m asl) from July 2013 to June 2014

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 [71]. 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) [72].

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 [66] 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 [54]. 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 [66].

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., [73]), 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 [72].

Feeding ecology

We collected activity data from July 2013 to June 2014 using instantaneous scan sampling [74] at 15-min intervals for up to 5 min duration, typically from 0700 to 1730 [66]. 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 [54]. 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 [66]. 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 [66]. 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 [72]. 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) [71] using the software PAST [75]. 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 [76] using EstimateS [77]. 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).

Statistical analyses

We conducted all statistical tests using R version 3.3.2 [78] 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 [75] 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 [79]. 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 [80]. 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 [81]. 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.

Results

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.
Figure 2
Fig. 2

Differences in the monthly availability indices (units/ha) of major food items between Bale monkey groups in continuous forest (Continuous A, [Cont_A], Continuous B, [Cont_B]) and forest fragments (Patchy and Hilltop)

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).
Figure 3
Fig. 3

Box plots showing dietary diversity, evenness, dominance and similarity indices among groups in continuous forest and fragments. Box plots show variations among groups in continuous forest (Continuous A, [Cont_A], Continuous B, [Cont_B]) and forest fragments (Patchy and Hilltop) in a Shannon–Wiener dietary diversity index, H′, b dietary plant species evenness index, c dietary plant species dominance index, D and d between-month dietary plant species similarity index. Dots represent the corresponding data set in each study group, the line in the box indicates the median of the corresponding index value, and the box shows the 25 and 75% interquartile. Vertical dotted lines represent the acceptable range with IQD (interquartile distance) multiplied by 1.5. All groups showed significant differences (P < 0.01)

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.
Figure 4
Fig. 4

The proportion of feeding records devoted to different food items by the four Bale monkey groups. N = 12 months, mean ± SE: BYL bamboo young leaves, NBYL non-bamboo young leaves, BSH bamboo shoots, FL flowers, FR fruit, ST stems, PT petioles, S seeds, IN insects, OS others

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%).
Table 1

Annual percentage of feeding records on different food items from each plant species among the four Bale monkey groups

Family

Percentage of feeding records for each food item

Species consumed

Growth form

BYL

NBYL

SH

FL

FR

ST

PT

S

IN

OS

Total

Continuous A

 Poaceae

Arundinaria alpina

Bamboo

57.69

19.66

2.02

79.37

 Rubiaceae

Galiniera saxifraga

Tree

0.15

7.38

7.53

 Sterculiaceae

Dombeya torrida

Tree

5.96

5.96

 Asteraceae

Mikaniopsis clematoides

Liana

2.37

0.06

2.43

 Urticaceae

Urera hypselodendron

Liana

0.03

0.85

0.89

 Poaceae

Bothriochloa radicans

Graminoid

0.72

0.06

0.78

 Vitaceae

Cypostemma adenocaule

Liana

0.20

0.20

 Rubiaceae

Galium spurium

Forb

0.16

0.16

 Rosaceae

Rubus apetalus

Shrub

0.03

0.06

0.03

0.12

 Asclepiadaceae

Oxystelma bornouense

Liana

0.06

0.06

 Sapindaceae

Allophylus macrobotrys

Tree

0.06

0.06

 Acanthaceae

Acanthopale pubescens

Forb

0.03

0.03

 

Insects

 

2.42

2.42

 Total

  

57.69

3.76

19.66

5.96

7.50

0.88

2.42

2.14

100.00

Continuous B

 Poaceae

Arundinaria alpina

Bamboo

64.20

17.59

1.26

83.05

 Rubiaceae

Galiniera saxifraga

Tree

0.19

0.03

5.36

5.58

 Sterculiaceae

Dombeya torrida

Tree

4.51

4.51

 Asteraceae

Mikaniopsis clematoides

Liana

2.16

2.16

 Urticaceae

Urera hypselodendron

Liana

0.26

1.74

2.00

 Poaceae

Bothriochloa radicans

Graminoid

0.63

0.05

0.68

 Vitaceae

Cypostemma adenocaule

Liana

0.43

0.43

 Acanthaceae

Acanthopale pubescens

Forb

0.08

0.08

 

Insects

 

1.50

1.50

 Total

  

64.20

3.76

17.59

4.54

5.36

1.74

1.50

1.31

100.00

Patchy fragment

 Poaceae

Arundinaria alpina

Bamboo

15.70

13.34

1.14

30.18

 Apiaceae

Centellia asiatica

Forb

12.76

12.76

 Rubiaceae

Galiniera saxifraga

Tree

0.05

7.35

7.39

 Rosaceae

Rubus apetalus

Shrub

0.04

6.08

0.82

6.94

 Poaceae

Cynodon dactylon

Graminoid

3.85

0.86

4.71

 Fabaceae

Trifolium tembense

Forb

4.16

4.16

 Rubiaceae

Canthium oligocarpum

Tree

0.17

0.23

3.49

0.03

3.91

 Poaceae

Hordeum vulgare a

Graminoid

0.17

3.44

3.61

 Poaceae

Poa annua

Graminoid

0.96

2.28

3.25

 Myrsinaceae

Maesa lanceolata

Tree

2.74

0.36

3.10

 Aquifo liaceae

Ilex mitis

Tree

0.48

0.43

0.22

1.02

2.15

 Musaceae

Ensete ventricosum a

Forb

0.09

1.00

0.87

1.96

 Papilionaceae

Erythrina brucei

Tree

0.32

0.68

0.10

0.02

1.11

 Poaceae

Zea mays a

Graminoid

1.05

0.05

1.09

 Apiaceae

Agrocharis melanantha

Forb

0.98

0.98

 Asteraceae

Carduus schimperi

Forb

0.33

0.02

0.51

0.85

 Urticaceae

Urera hypselodendron

Liana

0.19

0.59

0.78

 Asteraceae

Bothriocline schimperi

Shrub

0.62

0.62

 Araceae

Arisaema schimperianum

Forb

0.12

0.40

0.52

 Poaceae

Pennisetum thunbergii

Graminoid

0.40

0.40

 Poaceae

Bothriochloa radicans

Graminoid

0.37

0.37

 Caryophyllaceae

Drymaria cordata

Forb

0.33

0.02

0.35

 Amaryllidaceae

Allium sp.

Graminoid

0.22

0.05

0.27

 Polygonaceae

Rumex nepalensis

Forb

0.26

0.26

 Fabaceae

Trifolium substerraneum

Forb

0.23

0.23

 Solanaceae

Solanum tuberosum a

Forb

0.20

0.02

0.22

 Poaceae

Deschampsia caespitosa

Graminoid

0.21

0.21

 Rosaceae

Hagenia abyssinica

Tree

0.19

0.19

 Oleaceae

Jasminum abyssinicum

Liana

0.08

0.10

0.18

 Casuarinaceae

Casuarina equisetifolia

Tree

0.15

0.15

 Myrsinaceae

Embelia schimperi

Liana

0.03

0.09

0.02

0.14

 Cucurbitaceae

Lagenaria abyssinica

Liana

0.14

0.14

 Balsaminaceae

Impatiens hochstetteri

Forb

0.12

0.12

 Poaceae

Avena fatua

Graminoid

0.11

0.11

 Rubiaceae

Galium spurium

Forb

0.10

0.10

 Cupressaceae

Juniperus procera

Tree

0.09

0.09

 Agaricaceae

Mushroom

Fungi

0.09

0.09

 Poaceae

Snowdenia polystacha

Graminoid

0.09

0.09

 Asclepiadaceae

Oxystelma bornouense

Liana

0.08

0.08

 Asteraceae

Vernonia sp.

Shrub

0.06

0.06

 Compositae

Lactuca glandulifera

Liana

0.06

0.06

 Lamiaceae

Pycnostachys eminii

Shrub

0.06

0.06

 Poaceae

Cyperus rigidifolius

Graminoid

0.05

0.05

 Asteraceae

Carduus leptacanthus

Forb

0.04

0.04

 Poaceae

Eleusine floccifolia

Graminoid

0.04

0.04

 Lamiaceae

Plectranthus alpinus

Forb

0.02

0.02

 Asphodelaceae

Kniphofia sp.

Forb

0.02

0.02

 Lamiaceae

Plectranthus garckeanus

Forb

0.02

0.02

 

Unidentified Grass

Graminoid

1.63

1.63

 

Unidentified Herb

Forb

0.85

0.85

 

Insects

 

3.34

3.34

 Total

  

15.70

29.19

14.34

1.00

21.58

7.15

0.29

6.08

3.34

1.32

100.00

Hilltop fragment

 Poaceae

Bothriochloa radicans

Graminoid

15.27

15.27

 Rubiaceae

Galiniera saxifraga

Tree

11.73

0.05

11.77

 Rosaceae

Rubus apetalus

Shrub

7.47

1.95

9.41

 Rosaceae

Hagenia abyssinica

Tree

8.44

8.44

 Asteraceae

Bothriocline schimperi

Shrub

8.06

8.06

 Apiaceae

Centellia asiatica

Forb

7.92

7.92

 Aquifoliaceae

Ilex mitis

Tree

2.28

3.51

5.79

 Apiaceae

Haplosciadium abyssinicum

Forb

3.52

3.52

 Urticaceae

Urera hypselodendron

Liana

0.71

1.69

2.40

 Poaceae

Arundinaria alpina

Bamboo

1.34

0.27

1.61

 Commelinaceae

Commelina sp.

Forb

0.31

1.11

1.42

 Fabaceae

Trifolium tembense

Forb

1.08

1.08

 Asteraceae

Crassocephalum macropappus

Forb

0.79

0.21

1.00

 Cupressaceae

Juniperus procera

Tree

1.00

1.00

 Lamiaceae

Plectranthus alpinus

Forb

0.22

0.07

0.59

0.88

 Poaceae

Poa annua

Graminoid

0.19

0.50

0.69

 Urticaceae

Pilea rivularis

Forb

0.17

0.33

0.50

 Poaceae

Cynodon dactylon

Graminoid

0.49

0.49

 Caryophyllaceae

Drymaria cordata

Forb

0.29

0.11

0.39

 Balsaminaceae

Impatiens hochstetteri

Forb

0.04

0.34

0.38

 Asteraceae

Mikaniopsis clematoides

Liana

0.11

0.22

0.33

 

Keshansho

Graminoid

0.33

0.33

 Asteraceae

Carduus schimperi

Forb

0.11

0.09

0.20

 Asteraceae

Vernonia rueppellii

Shrub

0.02

0.11

0.13

 Solanaceae

Discopodium penninervium

Tree

0.04

0.09

0.13

 Papilionaceae

Erythrina brucei

Tree

0.03

0.10

0.12

 Rosaceae

Alchemilla fischeri

Forb

0.12

0.12

 Poaceae

Zea mays a

Graminoid

0.11

0.11

 Olaeaceae

Jasminum abyssinicum

Liana

0.11

0.11

 Asteraceae

Echinops sp.

Forb

0.09

0.09

 Urticaceae

Girardinia bullosa

Forb

0.09

0.09

 Capparaceae

Ritchiea albersii

Tree

0.05

0.05

 Urticaceae

Urtica simensis

Forb

0.04

0.04

 Agaricaceae

Agaricaceae sp.

Fungi

0.03

0.03

 Crassulaceae

Crassula alsinoides

Forb

0.02

0.02

 

Sheshako

Shrub

0.02

0.02

 

Unidentified Grass

Graminoid

1.46

1.46

 

Unidentified Herb

Forb

0.88

0.88

 

Insects

 

13.68

13.68

 Total

  

1.34

33.49

0.27

2.59

21.02

18.50

8.59

0.50

13.68

0.03

100.00

aCultivated food species

Dietary preference

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.
Table 2

Selection ratios of food species contributing ≥ 0.5% to the diet of the four Bale monkey groups

Group

Species

Growth form

% of dieta

% of stem density

Selection ratio (rank)

Continuous A

Arundinaria alpina

Bamboo

79.37

84.74

0.94 (3)

Galiniera saxifraga

Tree

7.53

3.42

2.20 (2)

Dombeya torrida

Tree

5.96

0.88

6.78 (1)

Mikaniopsis clematoides

Liana

2.43

3.37

0.72 (4)

Urera hypselodendron

Liana

0.89

1.83

0.48 (5)

Continuous B

Arundinaria alpina

Bamboo

83.05

87.12

0.95 (5)

Galiniera saxifraga

Tree

5.58

3.02

1.85 (3)

Dombeya torrida

Tree

4.51

0.37

12.19 (1)

Mikaniopsis clematoides

Liana

2.16

0.49

4.37 (2)

Urera hypselodendron

Liana

2.00

2.00

1.00 (4)

Patchy fragment

Arundinaria alpina

Bamboo

30.18

39.59

0.76 (5)

Galiniera saxifraga

Tree

7.39

1.98

3.73 (2)

Rubus apetalus

Shrub

6.94

15.26

0.45 (8)

Canthium oligocarpum

Tree

3.91

1.48

2.64 (4)

Maesa lanceolata

Tree

3.10

4.52

0.69 (6)

Ilex mitis

Tree

2.15

0.64

3.36 (3)

Erythrina brucei

Tree

1.11

0.04

27.83 (1)

Urera hypselodendron

Liana

0.78

1.39

0.56 (7)

Bothriocline schimperi

Shrub

0.62

8.35

0.07 (9)

Hilltop fragment

Galiniera saxifraga

Tree

11.77

4.39

2.68 (3)

Rubus apetalus

Shrub

9.41

19.46

0.48 (8)

Hagenia abyssinica

Tree

8.44

0.81

10.42 (1)

Bothriocline schimperi

Shrub

8.06

15.01

0.54 (7)

Ilex mitis

Tree

5.79

4.71

1.23 (4)

Urera hypselodendron

Liana

2.40

3.27

0.73 (6)

Arundinaria alpina

Bamboo

1.61

1.61

1.00 (5)

Juniperus procera

Tree

1.00

0.16

6.25 (2)

Selection ratios of tree, bamboo, shrub, and liana are calculated for each group based on percentage of stem density accounted for by the plant species in continuous forest (Continuous A and Continuous B) and forest fragments (Patchy and Hilltop)

aRank ordered based on annual diet of plant species used for selection ratio. We were unable to calculate dietary preference for forbs and graminoids because their abundance could not be determined in the same manner as for the other plant growth forms

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).
Table 3

Linear regressions between food availability index and percentage consumption of plant food items among the four Bale monkey groups

Food item

Continuous

R2adj

P value

Fragments

R2adj

P value

Bamboo young leaves

Continuous A

0.26

0.052

Patchy

0.50

0.006

Continuous B

0.52

0.005

Hilltop

Non-bamboo young leaves

Continuous A

0.09

0.180

Patchy

0.07

0.204

Continuous B

0.12

0.145

Hilltop

− 0.07

0.634

Fruit

Continuous A

0.87

0.005

Patchy

0.25

0.060

Continuous B

0.85

< 0.001

Hilltop

0.55

0.004

Flower

Continuous A

0.64

0.023

Patchy

0.10

0.981

Continuous B

0.60

0.002

Hilltop

0.14

0.124

Bamboo shoots

Continuous A

0.86

< 0.001

Patchy

0.54

0.004

Continuous B

0.92

< 0.001

Hilltop

Bale monkey groups in continuous forest (Continuous A, Continuous B) and forest fragments (Patchy and Hilltop) (N = 12 months) (P value in italic indicates significant correlations)

Discussion

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, 8486]. 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, 4144, 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 [66], 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 [48]; Cercopithecus mitis boutourlinii [49]), while decreasing for others (e.g., Ateles geoffroyi [41]; Propithecus diadema [42]). 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: [89]) and Senegalese (C. sabaeus: [90]) 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.
Table 4

Percentage of feeding time devoted to different food items by wild populations of Chlorocebus

Species

Study length (mon)

Group (n or name)

BYL

OYL

ML

BSH

GRB

TL

FR

S

TF

FL

ST

GU

AP

OS

No. spp

Site, Country

Reference

Chlorocebus djamdjamensis

12

CA

57.7

3.1

0.5

19.7

0.7

81.7

7.5

0.0

7.5

6.0

0.9

0.0

2.4

1.6

12

Odobullu (CF), Ethiopia

This study

C. djamdjamensis

12

CB

64.2

3.2

0.4

17.6

0.6

86.0

5.4

0.0

5.4

4.5

1.7

0.0

1.5

0.9

8

Odobullu (CF), Ethiopia

This study

C. djamdjamensis

12

Patchy

15.7

21.4

0.0

14.3

7.8

59.2

21.6

6.1

27.2

1.0

7.2

0.0

3.3

1.6

47

Kokosa (FF), Ethiopia

This study

C. djamdjamensis

12

Hilltop

1.3

15.8

0.1

0.3

17.7

35.2

21.0

0.5

21.5

2.6

18.5

0.0

13.7

8.5a

35

Afursa (FF), Ethiopia

This study

C. djamdjamensis

8

2

73.0

7.2

1.1

1.5

0.9

82.8

9.6

0.0

9.6

3.1

1.4

0.0

2.3

0.9

11

Odobullu (CF), Ethiopia

Mekonnen et al. [54]

C. pygerythrus

11

2

0.0

0.8

0.0

4.7

5.5

7.0

10.2

17.2

7.6

8.0

47.9

0.7

13.1

Laikipia (Acacia xanthophloea Woodland), Kenya

Isbell et al. [61]

C. pygerythrus

11

2

0.0

3.2

0.0

3.4

6.6

1.7

6.6

8.3

2.3

0.0

39.5

7.5

35.8

Laikipia (A. drepanolobium Woodland), Kenya

Isbell et al. [61]

C. pygerythrus

9

3

0.0

0.0

26.6

11.1

2.6

13.7

0.0

0.0

30.0

7.7

0.2

Amboseli, Kenya

Wrangham and Waterman [91]

C. pygerythrus

26

1

0.0

0.0

8.3

8.3

5.8

19.6

25.4

44.7

0.0

0.0

0.0

1.3

Saumburu-Isiolo, Kenya

Whitten [70]

C. sabaeus

  

0.0

0.0

0.0

50.2

12.8

63.0

13.0

0.0

0.0

13.1

10.9

Mt. Assirik, Senegal

Harrison [90]

C. tantalus

11

1

0.0

0.0

0.0

20.5

49.2

0.0

49.2

5.3

0.0

0.0

25.1

0.0

28

Ngel Nyaki, Nigeria

Agmen et al. [89]

BYL bamboo young leaves, OYL young leaves except bamboo and grass, ML mature leaves, BSH bamboo shoots, GRL grass blades, TL total leaves, FR fruits, S seeds, TF total fruits, FL flowers, ST stems, PT petioles, GU gum, AP animal prey, OS others

Habitat: CF continuous forest, FF fragmented forest

a8.3 petiole

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 [69], 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: [98]; Chlorocebus: [63]) or species (Cercopithecus mitis: [64, 99]), while giant and red pandas belong to different more specialized families in the order Carnivora [69]. 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).
Table 5

Percentage of feeding time devoted to different food items and bamboo species by Bale monkeys, bamboo lemurs and other bamboo-eating primates

Species

Study length (month)

YL

ML

SH

GRB

TL

ST

FL

FR

S

TF

AP

OS

Bamboo

No. of species

Habitat

Site, Country

Reference

Chlorocebus djamdjamensis (CA)

12

60.7

0,5

19.7

0.7

81.7

0.9

6.0

7.5

0.0

7.5

2.4

1.6

79.4b

12

Montane bamboo forest, CF

Odobullu, Ethiopia

This study

C. djamdjamensis (CB)

12

67.3

0.4

17.6

0.6

86.0

1.7

4.5

5.4

0.0

5.4

1.5

0.9

83.1b

8

Montane bamboo forest, CF

Odobullu, Ethiopia

This study

C. djamdjamensis (PF)

12

37.7

0.0

14.3

7.8

59.2

7.2

1.0

21.6

6.1

27.2

3.3

1.6

30.2b

47

Fragmented forest, FF

Kokosa, Ethiopia

This study

C. djamdjamensis (HF)

12

17.1

0.1

0.3

17.7

35.2

18.5

2.6

21.0

0.5

21.5

13.7

8.63

1.6b

35

Fragmented montane forest FF

Afursa, Ethiopia

This study

C. djamdjamensis

8

79.3

1.1

1.5

0.9

82.8

1.4

3.1

9.6

9.6

2.3

0.9

76.7b

11

Montane bamboo forest, CF

Odobullu, Ethiopia

Mekonnen et al. [54]

Cercopithecus mitis kandti a

8

44.0

0.1

0.0

44.1

3.4

14.8

22.5

22.5

14.3

1.1

52.4b

16

Montane bamboo forest

Mgahinga, Uganda

Twinomugisha et al. [100]

Hapalemur aureus

24

0.0

91

4

4

5

78c

≥21

Submontane rain forest

Ranomafana, Madagascar

Tan [26]

H. griseus

13

0.3

6.3

89.1

0.0

95.7

0.4

1.2

1.2

2.7

89.1c

12

Domain forest

Ranomafana, Madagascar

Overdorff et al. [108]

H. griseus

24

92

5

5

3

72c

≥ 24

Submontane rain forest

Ranomafana, Madagascar

Tan [26]

H. meridionalis (n = 3)

12

8.8

0.0

0.0

34.3

43.1

23.9

12.8

18.6

0.0

18.6

 

1.6

0.0

72

Fragmented littoral forest

Mandena, Madagascar

Eppley et al. [45]

Prolemur simus

24

98

0.5

0.5

1.5

95c

7

Submontane rain forest

Ranomafana, Madagascar

Tan [26]

Macaca assamensis

12

75.5

1.8

0.0

77.3

1.3

20.1

0.1

20.2

1.3

71.2d

78

Limestone seasonal rain forest

Nonggang, China

Huang et al. [96]

M. assamensis

12

74.1

3.3

0.0

77.4

2.7

17.4

17.4

2.5

48.7d

69

Limestone seasonal rain forest

Nonggang, China

Zhou et al. [68]

YL young leaves, ML mature leaves, SH shoots, GRB grass blades, TL total leaves, ST stems, PT petioles, FL flowers, FR fruits, S seeds, TF total fruits, AP animal prey, OS other

aFrom Table 1 in Twinomugisha et al. [100], we took the average of the values for groups G and N during Time 1 (January–September 1998) and then averaged that value with the value for Time 2 (January–August 2003)

b Arundinaria alpina

c Cathariostachys madagascariensis

d Several bamboo species

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 [26]. In particular, the greater bamboo lemur (Prolemur simus) consumes a diet of 95% bamboo [26] and does not appear to exist outside of bamboo forest habitat [101, 102]. P. simus also relies heavily on an unusually cyanogenic bamboo species [95] 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 [103] and H. meridionalis [36]. 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, 9395]).

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 [104], 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 [105]. 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 [93] and to prevent the functional homogenization of biodiversity in this important region for conservation [19, 107].

Conclusions

Bale monkeys in fragments have smaller group sizes, and experience lower food availability and habitat quality relative to those in continuous forest ([66]; 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.

Abbreviations

CEES: 

Centre for Ecological and Evolutionary Synthesis

IUCN: 

International Union for Conservation of Nature

DBH: 

diameter at breast height

BA: 

basal area

H’

Shannon–Wiener index

D

dominance index

J

evenness index

CH

Morisita–Horn’s similarity index

PAST: 

PAleontological Statistics

ANOVA: 

analysis of variance

Tukey HSD: 

Tukey honest significant difference test

GLM: 

generalized linear model

SE: 

standard error

vs.: 

versus

Cont_A: 

Continuous A

Cont_B: 

Continuous B

IQD: 

interquartile distance

PSMs: 

plant secondary metabolites

BYL: 

bamboo young leaves

NBYL: 

non-bamboo young leaves

BSH: 

bamboo shoots

FL: 

flowers

FR: 

fruit

ST: 

stems

PT: 

petioles

S: 

seeds

IN: 

insects

OS: 

others

OYL: 

young leaves except bamboo and grass

ML: 

mature leaves

BSH: 

bamboo shoots

GRL: 

grass blades

TL: 

total leaves

TF: 

total Fruits

GU: 

gum

AP: 

animal prey

CF: 

continuous forest

FF: 

fragmented forest

sp.: 

species

Declarations

Authors’ contributions

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.

Acknowledgements

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.

Competing interests

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

Not applicable.

Ethics approval and consent to participate

Not applicable.

Funding

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.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Oslo, Norway
(2)
Department of Zoological Sciences, Addis Ababa University, Addis Ababa, Ethiopia
(3)
Department of Anthropology and Environmental Studies Program, California State University Fullerton, Fullerton, USA

References

  1. 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.PubMedView ArticleGoogle Scholar
  2. 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.PubMedView ArticleGoogle Scholar
  3. 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.PubMedView ArticleGoogle Scholar
  4. 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.PubMedView ArticleGoogle Scholar
  5. 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.PubMedView ArticleGoogle Scholar
  6. Laurance WF, Sayer J, Cassman KG. Agricultural expansion and its impacts on tropical nature. Trends Ecol Evol. 2014;29:107–16.PubMedView ArticleGoogle Scholar
  7. 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.PubMedView ArticleGoogle Scholar
  8. Arroyo-Rodríguez V, Mandujano S. Forest fragmentation modifies habitat quality for Alouatta palliata. Int J Primatol. 2006;27:1079–96.View ArticleGoogle Scholar
  9. 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.PubMedView ArticleGoogle Scholar
  10. 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.View ArticleGoogle Scholar
  11. 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.View ArticleGoogle Scholar
  12. 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.PubMedPubMed CentralView ArticleGoogle Scholar
  13. 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.PubMedView ArticleGoogle Scholar
  14. 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.View ArticleGoogle Scholar
  15. Fahrig L. Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst. 2003;34:487–515.View ArticleGoogle Scholar
  16. Onderdonk DA, Chapman CA. Coping with forest fragmentation: the primates of Kibale National Park, Uganda. Int J Primatol. 2000;21:587–611.View ArticleGoogle Scholar
  17. 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.View ArticleGoogle Scholar
  18. 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.PubMedView ArticleGoogle Scholar
  19. Clavel J, Julliard R, Devictor V. Worldwide decline of specialist species: toward a global functional homogenization? Front Ecol Environ. 2011;9:222–8.View ArticleGoogle Scholar
  20. Shipley LA, Forbey JS, Moore BD. Revisiting the dietary niche: when is a mammalian herbivore a specialist? Integr Comp Biol. 2009;49:274–90.PubMedView ArticleGoogle Scholar
  21. 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.PubMedPubMed CentralView ArticleGoogle Scholar
  22. de Almeida-Rocha JM, Peres CA, Oliveira LC. Primate responses to anthropogenic habitat disturbance: a pantropical meta-analysis. Biol Conserv. 2017;215:30–8.View ArticleGoogle Scholar
  23. 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.View ArticleGoogle Scholar
  24. Harcourt AH, Coppeto S, Parks S. Rarity, specialization and extinction in primates. J Biogeogr. 2002;29:445–56.View ArticleGoogle Scholar
  25. Twinomugisha D, Chapman CA. Golden monkey populations decline despite improved protection in Mgahinga Gorilla National Park, Uganda. Afr J Ecol. 2007;45:220–4.View ArticleGoogle Scholar
  26. 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.View ArticleGoogle Scholar
  27. 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.View ArticleGoogle Scholar
  28. 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.PubMedView ArticleGoogle Scholar
  29. 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.View ArticleGoogle Scholar
  30. 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.View ArticleGoogle Scholar
  31. Moore BD, Foley WJ. Tree use by koalas in a chemically complex landscape. Nature. 2005;435:488–90.PubMedView ArticleGoogle Scholar
  32. Villalba JJ, Provenza FD. Learning and dietary choice in herbivores. Rangel Ecol Manag. 2009;62:399–406.View ArticleGoogle Scholar
  33. Kamilar JM, Paciulli LM. Examining the extinction risk of specialized folivores: a comparative study of colobine monkeys. Am J Primatol. 2008;70:816–27.PubMedView ArticleGoogle Scholar
  34. Schaller GB. Giant pandas of Wolong. Chicago: University of Chicago press; 1985.Google Scholar
  35. 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.View ArticleGoogle Scholar
  36. 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.PubMedPubMed CentralView ArticleGoogle Scholar
  37. 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.Google Scholar
  38. 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.PubMedPubMed CentralGoogle Scholar
  39. 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.View ArticleGoogle Scholar
  40. Tutin CEG. Fragmented living: behavioural ecology of primates in a forest fragment in the Lopé Reserve, Gabon. Primates. 1999;40:249.PubMedView ArticleGoogle Scholar
  41. 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.View ArticleGoogle Scholar
  42. Irwin MT. Feeding ecology of Propithecus diadema in forest fragments and continuous forest. Int J Primatol. 2008;29:95–115.View ArticleGoogle Scholar
  43. 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.View ArticleGoogle Scholar
  44. 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.PubMedView ArticleGoogle Scholar
  45. 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.PubMedView ArticleGoogle Scholar
  46. Chaves OM, Bicca-Marques JC. Feeding strategies of brown howler monkeys in response to variations in food availability. PLoS ONE. 2016;11:e0145819.PubMedPubMed CentralView ArticleGoogle Scholar
  47. 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.PubMedPubMed CentralView ArticleGoogle Scholar
  48. 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.View ArticleGoogle Scholar
  49. 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.View ArticleGoogle Scholar
  50. 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.PubMedView ArticleGoogle Scholar
  51. 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.View ArticleGoogle Scholar
  52. Marsh LK. Primates in fragments: ecology and conservation. New York: Kluwer Academic Publishers; 2003.View ArticleGoogle Scholar
  53. 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.View ArticleGoogle Scholar
  54. 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.View ArticleGoogle Scholar
  55. 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.View ArticleGoogle Scholar
  56. Butynski TM, Gippoliti S, Kingdon J, De Jong Y. Chlorocebus djamdjamensis. The IUCN red list of threatened species 2008: e.T4240A10699069. https://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T4240A10699069.en. 2008. Accessed 02 Nov 2017.
  57. 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.PubMedView ArticleGoogle Scholar
  58. 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.Google Scholar
  59. 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.Google Scholar
  60. 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.PubMedPubMed CentralView ArticleGoogle Scholar
  61. 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.View ArticleGoogle Scholar
  62. 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.View ArticleGoogle Scholar
  63. 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.Google Scholar
  64. Butynski TM. Comparative ecology of blue monkeys (Cercopithecus mitis) in high-and low-density subpopulations. Ecol Monogr. 1990;60:1–26.View ArticleGoogle Scholar
  65. Carpaneto GM, Gippoliti S. Primates of the Harenna Forest, Ethiopia. Primate Conserv. 1994;11:12–5.Google Scholar
  66. 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.View ArticleGoogle Scholar
  67. 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.View ArticleGoogle Scholar
  68. 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.View ArticleGoogle Scholar
  69. 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.PubMedPubMed CentralView ArticleGoogle Scholar
  70. Whitten PL. Diet and dominance among female vervet monkeys (Cercopithecus aethiops). Am J Primatol. 1983;5:139–59.View ArticleGoogle Scholar
  71. Krebs CJ. Ecological methodology. California: Benjamin/Cummings Menlo Park; 1999.Google Scholar
  72. 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.View ArticleGoogle Scholar
  73. 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.PubMedView ArticleGoogle Scholar
  74. Altmann J. Observational study of behavior: sampling methods. Behaviour. 1974;49:227–67.PubMedView ArticleGoogle Scholar
  75. Hammer Ø, Harper D, Ryan P. PAST-palaeontological statistics, ver. 1.89. Oslo: University of Oslo; 2009. p. 1–31.Google Scholar
  76. Horn HS. Measurement of “overlap” in comparative ecological studies. Am Nat. 1966;100:419–24.View ArticleGoogle Scholar
  77. Colwell RK. EstimateS: statistical estimation of species richness and shared species from samples. version 9.1.0. http://viceroy.eeb.uconn.edu/estimates/. 2013.
  78. 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.
  79. Crawley MJ. The R book. Chichester: Wiley; 2012.View ArticleGoogle Scholar
  80. Hothorn T, Bretz F, Westfall P. Simultaneous inference in general parametric models. Biom J. 2008;50:346–63.PubMedView ArticleGoogle Scholar
  81. Warton DI, Hui FK. The arcsine is asinine: the analysis of proportions in ecology. Ecology. 2011;92:3–10.PubMedView ArticleGoogle Scholar
  82. 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.View ArticleGoogle Scholar
  83. 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.PubMedView ArticleGoogle Scholar
  84. 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.View ArticleGoogle Scholar
  85. 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.View ArticleGoogle Scholar
  86. 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.PubMedView ArticleGoogle Scholar
  87. 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.PubMedView ArticleGoogle Scholar
  88. Anderson J, Rowcliffe JM, Cowlishaw G. Does the matrix matter? A forest primate in a complex agricultural landscape. Biol Conserv. 2007;135:212–22.View ArticleGoogle Scholar
  89. 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.View ArticleGoogle Scholar
  90. Harrison MJ. Age and sex differences in the diet and feeding strategies of the green monkey, Cercopithecus sabaeus. Anim Behav. 1983;31:969–77.View ArticleGoogle Scholar
  91. 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.Google Scholar
  92. 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.PubMedView ArticleGoogle Scholar
  93. 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).Google Scholar
  94. 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.View ArticleGoogle Scholar
  95. Ballhorn DJ, Rakotoarivelo FP, Kautz S. Coevolution of cyanogenic bamboos and bamboo lemurs on Madagascar. PLoS ONE. 2016;11:e0158935.PubMedPubMed CentralView ArticleGoogle Scholar
  96. 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.PubMedView ArticleGoogle Scholar
  97. Twinomugisha D, Chapman CA. Golden monkey ranging in relation to spatial and temporal variation in food availability. Afr J Ecol. 2008;46:585–93.View ArticleGoogle Scholar
  98. Thierry B, Singh M, Kaumanns W. Macaque societies: a model for the study of social organization. Cambridge: Cambridge University Press; 2004.Google Scholar
  99. Cords M. Mixed-species association of Cercopithecus monkeys in the Kakamega Forest, Kenya. Univ Calif Publ Zool. 1987;1:1–109.Google Scholar
  100. 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.View ArticleGoogle Scholar
  101. 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.View ArticleGoogle Scholar
  102. 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.View ArticleGoogle Scholar
  103. 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.View ArticleGoogle Scholar
  104. Hill CM, Webber AD. Perceptions of nonhuman primates in human–wildlife conflict scenarios. Am J Primatol. 2010;72:919–24.PubMedView ArticleGoogle Scholar
  105. Hill CM, Wallace GE. Crop protection and conflict mitigation: reducing the costs of living alongside non-human primates. Biodivers Conserv. 2012;21:2569–87.View ArticleGoogle Scholar
  106. Estrada A, Raboy BE, Oliveira LC. Agroecosystems and primate conservation in the tropics: a review. Am J Primatol. 2012;74:696–711.PubMedView ArticleGoogle Scholar
  107. 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.PubMedView ArticleGoogle Scholar
  108. 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.PubMedView ArticleGoogle Scholar

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