Pump and sway: Wild primates use compliant supports as a tool to augment leaping in the canopy.

OBJECTIVES: Despite qualitative observations of wild primates pumping branches before leaping across gaps in the canopy, most studies have suggested that support compliance increases the energetic cost of arboreal leaping, thus limiting leaping performance. In this study, we quantified branch pumping behavior and tree swaying in wild primates to test the hypothesis that these behaviors improve leaping performance. MATERIALS AND METHODS: We recorded wild colobine monkeys crossing gaps in the canopy and quantitatively tracked the kinematics of both the monkey and the compliant support during behavioral sequences. We also empirically measured the compliance of a sample of locomotor supports in the monkeys' natural habitat, allowing us to quantify the resonant properties of substrates used during leaping. RESULTS: Analyses of three recordings show that adult red colobus monkeys (Piliocolobus tephrosceles) use branch compliance to their advantage by actively pumping branches before leaping, augmenting their vertical velocity at take-off. Quantitative modeling of branch resonance periods, based on empirical measurements of support compliance, suggests that monkeys specifically employed branch pumping on relatively thin branches with protracted periods of oscillation. Finally, an additional four recordings show that both red colobus and black and white colobus monkeys (Colobus guereza) utilize tree swaying to cross large gaps, augmenting horizontal velocity at take-off. DISCUSSION: This deliberate branch manipulation to produce a mechanical effect for stronger propulsion is consistent with the framework of instrumental problem-solving. To our knowledge, this is the first study of wild primates which quantitatively shows how compliant branches can be used advantageously to augment locomotor performance.

High levels of infant handling by adult males in Rwenzori Angolan colobus (Colobus angolensis ruwenzorii) compared to two closely related species, C. guereza and C. vellerosus.

Infant handling (holding or carrying) by adult males is rare in mammals; however, high levels have been reported in some primates. Though infant handling is a costly behaviour, there are many benefits that male handlers can accrue. Infant handling by males is most conspicuous in platyrrhines and tends to be uncommon in catarrhines. In the latter species, research on male-infant interactions has focused on low-cost behaviours, such as proximity and grooming. However, to better understand the evolution of infant handling by males, more data on its occurrence across the Primate order are essential, even in species where it is relatively uncommon. We compare the occurrence of infant handling by males in three closely related species of catarrhine: Colobus vellerosus, C. guereza, and C. angolensis ruwenzorii. We collected focal animal samples on infants to quantify infant handling rates and durations, and found that adult male C. a. ruwenzorii handled infants much more frequently and for much longer than males in the other two species. We discuss how C. a. ruwenzorii's unique social organization may explain high levels of infant handling by adult males in this species. More long-term and detailed comparisons of infant handling across species and populations will shed light on how sociality has shaped the evolution of this behaviour in the Primate order.

Effect of enclosure expansion on the activity budgets of eastern black-and-white colobus monkeys, Colobus guereza.

Behavior is one of the most observable and informative indicators of animal welfare. This study used behavioral observation methodologies to evaluate the impact of an enclosure expansion on the activity budgets of a group of three eastern black-and-white colobus monkeys, Colobus guereza, housed at the Adelaide Zoo in South Australia. Instantaneous scan sampling methods were used to record the monkeys' behavior before and after they were given access to new aerial walkways at 2-min intervals between 8:30 a.m. and 4:30 p.m., over a total of 109 h (66 baseline hours, 43 post-expansion hours). Broad state behaviors (e.g., social, moving, resting, interacting, and feeding) were recorded and were used to generate activity budgets. Locomotion, feeding, and social behaviors increased following the addition of the aerial walkways, along with an overall increase in activity, attributed to the larger area and increased complexity of the environment. Results indicate that the addition of aerial walkways was effective for increasing the behavioral repertoire in colobus monkeys, aligning activity budgets more closely with their wild counterparts, and increasing active and affiliative behaviors.

Selecting between iron-rich and clay-rich soils: a geophagy field experiment with black-and-white colobus monkeys in the Budongo Forest Reserve, Uganda.

Geophagy, the intentional consumption of soil, has been observed in humans and numerous other animal species. Geophagy has been posited to be adaptive, i.e., consumed soil protects against gastrointestinal distress and/or supplements micronutrients. We conducted a field experiment in the Budongo Forest, Uganda, to investigate geophagic behaviors, including soil preference, the quantity of soil eaten, and competition for access to preferred soils. We placed pairs of artificial tree stumps at two existing geophagy sites. One stump contained soil from the surrounding area, Sonso, that could supplement bioavailable iron. The other stump contained soil from a neighboring community, Waibira, that was richer in clay minerals, which could provide protection from plant secondary compounds. We monitored activity and engagement with the stumps for 10 days using camera traps. After 5 days, we reversed the type of soil that was in the stumps at both sites (i.e., a crossover design). Only Colobus guereza (black-and-white colobus monkeys) interacted with the stumps. These monkeys used visual and olfactory cues to select between the two soils and exclusively ate the clay-rich soil, consuming 9.67 kg of soil over 4.33 h. Our findings lend the greatest plausibility to the protection hypothesis. Additionally, monkeys competed for access to the stumps, and 13% of the videos captured aggression, including pushing, excluding, and chasing other individuals from the experimental stumps. Nine episodes of vigilance and flight behavior were also observed. Given that intentionally ingested soil is a valuable resource that may confer health benefits, geophagy sites should be conserved and protected.

Melengestrol acetate contraceptive implant use in colobus monkeys (Colobus guereza): Patterns through time and differences in reproductive potential and live births.

Melengestrol acetate (MGA) implants are progestin-based reversible contraceptives used to manage fertility in zoo populations. Although it is recommended that MGA implants should be replaced every 2 years, the duration of efficacy has not been systematically evaluated in most species. Anecdotal reports for Old World monkeys indicate that reproduction may be suppressed longer if the implant is not removed. This study uses Guereza colobus monkey (Colobus guereza) as a model Old World monkey species to examine the effects of MGA implants on reproductive potential. In particular, we investigate whether the probability of reproducing (pR) and rates of stillbirth differ among (1) non-implanted females, (2) females who have had MGA implants removed, and (3) females whose implants were left in past expiration. We found no significant difference in pR between non-implanted and implant-removed groups, but when implants were left in past expiration, the pR was significantly lower than in other groups. Both parity and age significantly impacted pR for the non-implanted group (i.e., younger females and those who were parous increased pR), but neither were significant factors for the implant-removed group. Stillbirth rates were significantly higher post-contraception as compared with pre-contraception. These results support similar analyses in other taxa that show a shorter time to reversal after MGA contraception when implants are removed, making this a good contraceptive option for females likely to receive a breeding recommendation, especially when a more predictable time to reversal is important.

Diet and Activity Budget in Colobus angolensis ruwenzorii at Nabugabo, Uganda: Are They Energy Maximizers?

INTRODUCTION: Colobine monkeys are specialized folivores that use foregut fermentation to digest leaves. The slow process of fermentation forces them to spend a lot of time resting and to minimize their energy expenditure to subsist on a lower-quality diet. METHODS: We recorded the diet and activity budget of Colobus angolensis ruwenzorii, which form a three-tiered multi-level society, at Lake Nabugabo, Uganda, over 12 months using scan sampling on adults and subadults, to determine whether they utilize the energy minimization strategy typical of colobines. RESULTS: We found that the annual diet was primarily comprised of high-quality food resources (young leaves 65% and fruit 31%), and fruits were the only plant part the monkeysselected when available. Both the fruits and young leaves of some species were preferred food items in some months, and mature leaf consumption correlated negatively with preferred food availability. Mature leaves appear to be a fallback food for this population but are rarely relied upon (3%). The C. a. ruwenzoriiat Nabugabo spent less time resting (40%) and more time moving (25%) than is typical for other species of black-and-white colobus. DISCUSSION/CONCLUSION: The high-quality diet of this population appears to allow them to utilize an energy maximization strategy. Their reliance on food items that tend to be clumped in space and time likely explains the frequent fission-fusion behaviour that we observe between core units. Our findings demonstrate that the foraging strategies of colobines may be more flexible than was previously thought and illustrate how food availability and distribution can impact primate social organization.

Anogenital distance as a measure of male competitive ability in Rwenzori Angolan colobus.

Anogenital distance (AGD) is positively correlated to fetal androgen exposure and developmental masculinization in mammals. Independent of overall body size, AGD shows a strong positive correlation with male fertility and in rodents, AGD is a good indicator of male competitive ability and is associated with female choice. We hypothesized that AGD will also predict male competitive ability in non-human primates. To test this, we measured AGD noninvasively with a parallel laser in a wild population of Angolan colobus monkeys (Colobus angolensis ruwenzorii) in Uganda and correlated to it to their social structure. C. angolensis ruwenzorii form a multilevel society with both one-male/multifemale units (OMUs) and multimale/multifemale units (MMUs). We compared AGD in males from five OMUs and six MMUs and related it to their fecal androgen metabolite concentrations, dominance rank and body size, and to the number of females in their unit. Males in OMUs had greater access to females, so were predicted to have longer AGDs, but this was not found. AGD also did not correlate overall with mean fecal androgen metabolites in MMUs. However, AGD was correlated with dominance rank in MMUs, demonstrating that higher-ranking males in these multimale units had longer AGDs. Body size did not show the same relationship with dominance rank, suggesting that male rank was not just a reflection of absolute male size. Our findings indicate that AGD predicts male competitive ability in this species and that it may be a useful correlate throughout the non-human primates. These results also support the idea that prenatal androgen exposure increases the likelihood of the expression of behaviors that maintain high dominance rank.

The diet and feeding behavior of the black-and-white colobus (Colobus guereza) in the Kalinzu Forest, Uganda.

One of the goals for primate feeding ecology is to understand the factors that affect inter- and intra-specific variations. Therefore, a detailed description of basic feeding ecology in as many populations as possible is necessary and warrants further understanding. The black-and-white colobus (Colobus guereza) or guereza is widely distributed in Africa and is one of the well-studied colobines in terms of their feeding; they demonstrate considerable variation in their diets in response to local conditions. We studied the diet of a group of guerezas in the Kalinzu Forest, Uganda, for over 30 consecutive months using behavioral observation (4308 h in total), phenology, and vegetation surveys. A total of 31 plant species were consumed by the study group. This study group was predominantly folivorous; the majority of their feeding time was involved in feeding on young leaves (87%). However, during certain times of the year, fruits and seeds accounted for 45% of monthly feeding time. Young leaves of Celtis durandii were by far the most important food, which constituted 58% of the total feeding records. There was a significant increase in the consumption of fruits and flowers once young leaf availability was low, but their consumption of fruits did not significantly increase even when fruit availability was high. Their monthly dietary diversity increased as the number of available plants with young leaves declined, suggesting that much of the dietary diversity in the study group may be attributable to the young leaf portion of their diet. Our findings may help contribute to a better understanding of the dietary adaptations and feeding ecology of guerezas in response to local environmental conditions.

Diet, feeding behavior, and jaw architecture of Taï monkeys: Congruence and chaos in the realm of functional morphology.

We review feeding and mandibular anatomy in a community of West African monkeys. We use field observations, food material property data, and skeletal specimens from the Ivory Coast's Taï Forest to explore the factors that shape mandibular architecture in colobines and cercopithecines. Despite excellent geographic control across our sample, the fit between bone form (as conventionally described) and functional activity (as we perceive it) is not spectacular. We present a thought experiment to assess how well we could reconstruct diet in the Taï monkeys if we only had skeletons and teeth to study. This exercise indicated that we would be correct about half the time. Our analyses reinforce the notion that diet is anything but a monolithic variable and that better success at relating mandibular form to food must incorporate information on ingestive and processing behavior, geometric and material properties of foods, and both material and structural data on jaws themselves.

A multi-level society comprised of one-male and multi-male core units in an African colobine (Colobus angolensis ruwenzorii).

Several mammalian species exhibit complex, nested social organizations, termed multi-level or modular societies. Multi-level societies comprise stable core units that fission and fuse with one another in a hierarchical manner, forming groups that vary in size over time. Among nonhuman primates, these social systems have been confirmed in several African papionin and Asian colobine species. We use data from August 2017 to July 2018 on individually-recognized Rwenzori Angolan colobus living near Lake Nabugabo, Uganda to document the first multi-level society in an African colobine. The study band comprised up to 135 individuals organized into 12 socially and spatially distinct core units that ranged in size from 4 to 23 individuals. These core units showed a strong affinity to one another, spending roughly 75% of their time together. Core units fissioned and fused non-randomly with one another throughout the day, leading to different combinations of core units being observed. Using association indices between core units, we employed hierarchical cluster analyses and permutation tests to show that some core units associated preferentially into clans. Thus, we confirm three tiers of social organization for Rwenzori Angolan colobus: core unit, clan, and band. The social organization of this subspecies is unlike any reported previously in a nonhuman primate, with about half the core units containing a single adult male and the others containing multiple reproductive adult males. The discovery of a unique primate multi-level society in a novel lineage could allow for a better understanding of the evolution of these complex social systems across the Animal Kingdom. Preliminary data show males transfer within the band and females transfer outside of the band, which is proposed for hominin multi-level societies. This subspecies could thus also provide insight into the selective pressures underlying multi-level societies in our own lineage.

Nutrient intake and balancing among female Colobus angolensis palliatus inhabiting structurally distinct forest areas: Effects of group, season, and reproductive state.

Understanding intraspecific behavioral and dietary variation is critical for assessing primate populations' abilities to persist in habitats characterized by increasing anthropogenic disturbances. While it is evident that some species exhibit considerable dietary flexibility (in terms of species-specific plant parts) in relation to habitat disturbance, it is unclear if primates are characterized by similar variation and flexibility regarding nutrient intake. This study examined the effects of group, season, and reproductive state on nutrient intake and balancing in adult female Colobus angolensis palliatus in the Diani Forest, Kenya. During July 2014 to December 2015, estimates of nutrient intake were recorded for eight females from three groups inhabiting structurally and ecologically distinct forest areas differing in tree species composition and density. There were differences in metabolizable energy (ME) and macronutrient intakes among groups, seasons, and reproductive states. Most notably, females inhabiting one of the more disturbed forest areas consumed less ME and macronutrients compared to females in the more intact forest area. Contrary to prediction, females in early lactation consumed significantly less ME and macronutrients compared to non-lactating and late lactation females. Despite differences in macronutrient intake, the relative contribution of macronutrients to ME were generally more conservative among groups, seasons, and reproductive states. Average daily intake ratios of non-protein energy to available protein ranged from approximately 3.5:1-4.3:1 among groups. These results indicate that female C. a. palliatus demonstrate a consistent nutrient balancing strategy despite significant intergroup differences in consumption of species-specific plant parts. Data from additional colobine species inhabiting different forest types are required to assess the extent to which nutrient balancing is constrained by phylogeny or is more flexible to local ecological conditions.

Integrating field and satellite data for spatially explicit inference on the density of threatened arboreal primates.

Spatially explicit models of animal abundance are a critical tool to inform conservation planning and management. However, they require the availability of spatially diffuse environmental predictors of abundance, which may be challenging, especially in complex and heterogeneous habitats. This is particularly the case for tropical mammals, such as nonhuman primates, that depend on multi-layered and species-rich tree canopy coverage, which is usually measured through a limited sample of ground plots. We developed an approach that calibrates remote-sensing imagery to ground measurements of tree density to derive basal area, in turn used as a predictor of primate density based on published models. We applied generalized linear models (GLM) to relate 9.8-ha ground samples of tree basal area to various metrics extracted from Landsat 8 imagery. We tested the potential of this approach for spatial inference of animal density by comparing the density predictions for an endangered colobus monkey, to previous estimates from field transect counts, measured basal area, and other predictors of abundance. The best GLM had high accuracy and showed no significant difference between predicted and observed values of basal area. Our species distribution model yielded predicted primate densities that matched those based on field measurements. Results show the potential of using open-access and global remote-sensing data to derive an important predictor of animal abundance in tropical forests and in turn to make spatially explicit inference on animal density. This approach has important, inherent applications as it greatly magnifies the relevance of abundance modeling for informing conservation. This is especially true for threatened species living in heterogeneous habitats where spatial patterns of abundance, in relation to habitat and/or human disturbance factors, are often complex and, management decisions, such as improving forest protection, may need to be focused on priority areas.

Spatial variation in mandibular bone elastic modulus and its effect on structural bending stiffness: A test case using the Taï Forest monkeys.

OBJECTIVES: We investigated how heterogeneity in material stiffness affects structural stiffness in the cercopithecid mandibular cortical bone. We assessed (1) whether this effect changes the interpretation of interspecific structural stiffness variation across four primate species, (2) whether the heterogeneity is random, and (3) whether heterogeneity mitigates bending stress in the jaw associated with food processing. MATERIALS AND METHODS: The sample consisted of Taï Forest, Cote d'Ivoire, monkeys: Cercocebus atys, Piliocolobus badius, Colobus polykomos, and Cercopithecus diana. Vickers indentation hardness samples estimated elastic moduli throughout the cortical bone area of each coronal section of postcanine corpus. For each section, we calculated maximum area moment of inertia, Imax (structural mechanical property), under three models of material heterogeneity, as well as spatial autocorrelation statistics (Moran's I, IMORAN ). RESULTS: When the model considered material stiffness variation and spatial patterning, Imax decreased and individual ranks based on structural stiffness changed. Rank changes were not significant across models. All specimens showed positive (nonrandom) spatial autocorrelation. Differences in IMORAN were not significant among species, and there were no discernable patterns of autocorrelation within species. Across species, significant local IMORAN was often attributed to proximity of low moduli in the alveolar process and high moduli in the basal process. DISCUSSION: While our sample did not demonstrate species differences in the degree of spatial autocorrelation of elastic moduli, there may be mechanical effects of heterogeneity (relative strength and rigidity) that do distinguish at the species or subfamilial level (i.e., colobines vs. cercopithecines). The potential connections of heterogeneity to diet and/or taxonomy remain to be discovered.

Bone remodeling is reduced in high stress regions of the cercopithecoid mandible.

OBJECTIVES: Independent lines of evidence suggest that osteonal bone remodeling is a function of both mechanical (i.e., changes in stress) and non-mechanical (i.e., metabolic needs related to calcium liberation) factors. The degree to which secondary bone reflects mechanical factors, however, is incompletely understood despite the common assumption that the stress environment mediates remodeling activity. Here, we investigate whether there are remodeling differences between regions of primate mandibular bone known to have distinct stress environments. METHODS: Osteon density, osteon fragment density, and relative osteonal area are measured as indicators of remodeling activity from postcanine and symphyseal thin sections of four sympatric monkey species (N = 20 total) from Taï Forest, Côte d'Ivoire: Piliocolobus badius, Colobus polykomos, Cercocebus atys, Cercopithecus diana. Subfamily and regional effects were assessed by two-way ANOVA. RESULTS: Symphyseal bone has lower osteonal density, fragment density and relative osteonal area than postcanine bone in all species, indicating relatively low remodeling activity in symphyseal bone, despite the likelihood of relatively high stresses in its lingual cortex. Subfamily differences in postcanine remodeling are significant in that colobines exhibit greater remodeling than cercopithecines. DISCUSSION: The data suggest that high strains are not requisite for bone remodeling. How the lingual symphysis negotiates a high strain environment without the reparative benefit of remodeling is yet to be elucidated, but the data prompt reevaluation of the relationship of targeted remodeling to stress histories. Differences in osteonal bone density between taxa might reflect feeding or dietary influences on remodeling activity, but sample composition prevents parsing behavioral from other taxon-specific effects.

Hormonal correlates of life history characteristics in wild female Colobus vellerosus.

Documenting primate life history characteristics is important because it provides information about traits that affect the timing and rate of reproduction in these long-lived species. This study describes the hormonal correlates of female reproductive events and quantifies for the first time key life history variables for Colobus vellerosus, using hormonal and observational data. This study also biologically validates that the reproductive events determined in the hormone profiles correspond to observed reproductive events for each female. We collected behavioural data on 18 females in our four study groups during 12 months (May 2012-2013) at the Boabeng-Fiema Monkey Sanctuary, using 10-min continuous focal and ad libitum sampling. We concurrently collected faecal samples (n = 1866) every 2-3 days from these 18 females (prepubescent n = 2, cycling n = 2, lactating n = 12, pregnant, n = 7, and post-reproductive n = 1) and extracted oestrogen (E2) and progesterone (P) metabolites in the field using solid-phase extraction cartridges. We created a hormone profile for each female by analyzing 1586 of our samples for E2 using radio-immuno assays, and P using enzyme-immunoassays at the Wisconsin National Primate Research Center. Mean ovarian cycle length was 24 days ± 1 (n = 2 cycles). Mean gestation length was 23 weeks (range = 21-25 weeks, n = 2 complete pregnancies). For females whose infants survived to nutritional independence, the mean inter-birth interval (IBI) was significantly longer than for females whose infants died prior to reaching nutritional independence (Mann-Whitney U Test; U = 14.5, p = 0.006; IBI surviving infants: 17.75 months, range = 8-20.75 months, n = 11 vs. IBI infant death: 11.89 months, range = 8-18.5 months, n = 9). The values for most life history traits reported in this study are similar to those documented in other similarly sized colobine species. Some values are on the lower end of the range for similarly sized colobines; C. vellerosus shows a cycle of 24 days and gestation length of 5.75 months vs. a range of 24-29 days for cycle length and 5.25-7.5 months for gestation length in other colobines. This may be due to C. vellerosus' smaller body size, or their limited access to higher quality food resources.

The role of leaf toughness on foraging efficiency in Angola black and white colobus monkeys (Colobus angolensis palliatus).

OBJECTIVES: Examining the relationships among foraging behavior, food mechanical properties, and masticatory morphology is a bourgeoning research topic among behavioral ecologists and functional morphologists. The purpose of this study was to assess the degree to which leaf toughness influences foraging efficiency with regard to ingestion rate, masticatory investment, and masticatory rate. METHODS: Diet and feeding data were collected on adults from three groups of Colobus angolensis palliatus in the Diani Forest, Kenya, from July 2014 to December 2015. Ingestion rates were estimated by counting the number of items consumed during feeding bouts and multiplying this value by the mean mass of a particular food item. The number of mastications was also counted during 3-5 minute focal periods. Mechanical toughness of commonly eaten young leaves (n = 27 species) and mature leaves (n = 13 species) was recorded using a toughness tester equipped with a razor blade. RESULTS: Ingestion rates (g/min) negatively correlated with leaf toughness (r(2) = 0.73; p < 0.01) while masticatory investment (chews/g) positively correlated with leaf toughness (r(2) = 0.72; p < 0.01). Chewing rate (chews/min) was remarkably consistent regardless of leaf species and toughness values (r(2) = 0.09; p = 0.07). DISCUSSION: Our findings highlight the degree to which toughness values can vary among leaves and how this variation can dramatically influence ingestion rates and chewing efficiency in black and white colobus monkeys. Studies that link food mechanical properties with oral processing behaviors will ultimately provide important context for understanding craniofacial and dentognathic traits in primates.

A unique case of extra-group infant adoption in free-ranging Angola black and white colobus monkeys (Colobus angolensis palliatus).

Infant adoption has been reported in a variety of primate taxa both in captive and natural settings. Adoption by females may be adaptive by increasing inclusive fitness via shared genes between adoptive mother and adoptee or by providing valuable maternal practice which, in turn, may increase the female's future reproductive success. Others have argued that adoption may be non-adaptive and the result of a general attraction toward infants. Our study examines a unique case of adoption by an adult female Angola black and white colobus monkey (Colobus angolensis palliatus) who adopted an extra-group infant alongside her own biological infant. We compare infant behaviors and mother-infant interactions between biological infant and adoptee and then compare both biological infant and adoptee behavioral profiles to those of infants under normal circumstances. Data were collected from July 2014 to June 2015 on three habituated groups in the Diani Forest of Kenya. Scan sampling and pooled data were used to create daily and monthly behavioral profiles for the biological infant and adoptee, as well as a mean monthly profile of four infants under normal circumstances. Data include time spent (1) clinging to mother/adoptive mother, (2) clinging to another individual, (3) behaving independently, and (4) behaving in close proximity to mother/adoptive mother. Initially, the adoptee struggled to achieve behavioral profiles consistent with those of the biological infant and normal colobus infants of the same age as he spent significantly more time moving independently and significantly less time clinging to the adoptive mother. After the mysterious death of the biological infant in mid-January 2015, the adoptee assumed a behavioral profile similar to that of infants under normal conditions. This case does not support adaptive hypotheses for adoption (i.e., inclusive fitness or learning to mother). Instead, because the biological infant died, possibly due to the presence of the adoptee, we argue that this case of infant adoption was non-adaptive. Ultimately, this adoption appears to have been an outcome of the adoptee's persistent desire to be cared for and the female's strong propensity to engage in allomaternal behavior.

Feeding and oral processing behaviors of two colobine monkeys in Tai Forest, Ivory Coast.

We collected frequency data on oral processing behaviors during feeding in habituated groups of Western red colobus, Piliocolobus badius, and Western black and white, Colobus polykomos, ranging in the Ivory Coast's Tai National Park. During the sampling period, the diet of red colobus consisted of approximately 75% leaves compared to approximately 47% leaves and buds in black and white colobus. Black and white colobus chewed more frequently per ingestive event than did red colobus. Black and white colobus also employed their anterior teeth much more frequently than did red colobus, a difference attributed to the frequent consumption by C. polykomos of Pentaclethra macrophylla seeds and pods. A material analysis of these food items reveals that both the seed coating and seed flesh are quite soft; however, the pod housing the seeds is very tough. We argue that the pod's toughness, geometry, and fiber orientation collectively result in a food that is very difficult to process, resulting in long handling times and frequent, aggressive use of the incisors. We compare these data with those collected on another Tai primate-the sooty mangabey, Cercocebus atys-and demonstrate that during feeding, both colobine species use their incisors less than the mangabey, but that the cercopithecine chews less than either colobine. Combining data on oral processing behaviors with those on the material properties of items being ingested should lead to more informed interpretations of dentognathic morphology.

Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: implications for conservation.

The expansion of agriculture is shrinking pristine forest areas worldwide, jeopardizing the persistence of their wild inhabitants. The Udzungwa red colobus monkey (Procolobus gordonorum) is among the most threatened primate species in Africa. Primarily arboreal and highly sensitive to hunting and habitat destruction, they provide a critical model to understanding whether anthropogenic disturbance impacts gut microbiota diversity. We sampled seven social groups inhabiting two forests (disturbed vs. undisturbed) in the Udzungwa Mountains of Tanzania. While Ruminococcaceae and Lachnospiraceae dominated in all individuals, reflecting their role in extracting energy from folivorous diets, analysis of genus composition showed a marked diversification across habitats, with gut microbiota α-diversity significantly higher in the undisturbed forest. Functional analysis suggests that such variation may be associated with food plant diversity in natural versus human-modified habitats, requiring metabolic pathways to digest xenobiotics. Thus, the effects of changes in gut microbiota should not be ignored to conserve endangered populations.

Long-term declines in nutritional quality of tropical leaves.

Global change is affecting plant and animal populations and many of the changes are likely subtle and difficult to detect. Based on greenhouse experiments, changes in temperature and rainfall, along with elevated CO2, are expected to impact the nutritional quality of leaves. Here, we show a decline in the quality of tree leaves 15 and 30 years after two previous studies in an undisturbed area of tropical forest in Kibale National Park, Uganda. After 30 years in a sample of multiple individuals of ten tree species, the mature leaves of all but one species increased in fiber concentrations, with a mean increase of 10%; tagged individuals of one species increased 13% in fiber. After 15 years, in eight tree species the fiber of young leaves increased 15%, and protein decreased 6%. Like many folivores, Kibale colobus monkeys select leaves with a high protein-to-fiber ratio, so for these folivores declining leaf quality could have a major impact. Comparisons among African and Asian forests show a strong correlation between colobine biomass and the protein-to-fiber ratio of the mature leaves from common tree species. Although this model, predicts a 31% decline in monkey abundance for Kibale, we have not yet seen these declines.