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Accurate density estimations of threatened animal populations is essential for management and conservation. This is particularly critical for species living in patchy and altered landscapes, as is the case for most tropical forest primates. In this study, we used a hierarchical modelling approach that incorporates the effect of environmental covariates on both the detection (i.e. observation) and the state (i.e. abundance) processes of distance sampling. We applied this method to already published data on three arboreal primates of the Udzungwa Mountains of Tanzania, including the endangered and endemic Udzungwa red colobus (Procolobus gordonorum). The area is a primate hotspot at continental level. Compared to previous, 'canonical' density estimates, we found that the inclusion of covariates in the modelling makes the inference process more informative, as it takes in full account the contrasting habitat and protection levels among forest blocks. The correction of density estimates for imperfect detection was especially critical where animal detectability was low. Relative to our approach, density was underestimated by the canonical distance sampling, particularly in the less protected forest. Group size had an effect on detectability, determining how the observation process varies depending on the socio-ecology of the target species. Lastly, as the inference on density is spatially-explicit to the scale of the covariates used in the modelling, we could confirm that primate densities are highest in low-to-mid elevations, where human disturbance tend to be greater, indicating a considerable resilience by target monkeys in disturbed habitats. However, the marked trend of lower densities in unprotected forests urgently calls for effective forest protection.

Non-lethal parasite infections are common in wildlife, but there is little information on their clinical consequences. Here, we pair infection data from a ubiquitous soil-transmitted helminth, the whipworm (genus Trichuris), with activity data from a habituated group of wild red colobus monkeys (Procolobus rufomitratus tephrosceles) in Kibale National Park, Uganda. We use mixed-effect models to examine the relationship between non-lethal parasitism and red colobus behaviour. Our results indicate that red colobus increased resting and decreased more energetically costly behaviours when shedding whipworm eggs in faeces. Temporal patterns of behaviour also changed, with individuals switching behaviour less frequently when whipworm-positive. Feeding frequency did not differ, but red colobus consumption of bark and two plant species from the genus Albizia, which are used locally in traditional medicines, significantly increased when animals were shedding whipworm eggs. These results suggest self-medicative plant use, although additional work is needed to verify this conclusion. Our results indicate sickness behaviours, which are considered an adaptive response by hosts during infection. Induction of sickness behaviour in turn suggests that these primates are clinically sensitive to non-lethal parasite infections.

Parasites and infectious diseases are well-known threats to primate populations. The main objective of this study was to provide baseline data on fecal parasites in the cercopithecid monkeys inhabiting Côte d’Ivoire’s Taï National Park. Seven of eight cercopithecid species present in the park were sampled: Cercopithecus diana, Cercopithecus campbelli, Cercopithecus petaurista, Procolobus badius, Procolobus verus, Colobus polykomos, and Cercocebus atys. We collected 3142 monkey stool samples between November 2009 and December 2010. Stool samples were processed by direct wet mount examination, formalin-ethyl acetate concentration, and MIF (merthiolate, iodine, formalin) concentration methods. Slides were examined under microscope and parasite identification was based on the morphology of cysts, eggs, and adult worms. A total of 23 species of parasites was recovered including 9 protozoa (Entamoeba coli, Entamoeba histolytica/dispar, Entamoeba hartmanni, Endolimax nana, Iodamoeba butschlii, Chilomastix mesnili, Giardia sp., Balantidium coli, and Blastocystis sp.), 13 nematodes (Oesophagostomum sp., Ancylostoma sp., Anatrichosoma sp., Capillariidae Gen. sp. 1, Capillariidae Gen. sp. 2, Chitwoodspirura sp., Subulura sp., spirurids [cf Protospirura muricola], Ternidens sp., Strongyloides sp., Trichostrongylus sp., and Trichuris sp.), and 1 trematode (Dicrocoelium sp.). Diversity indices and parasite richness were high for all monkey taxa, but C. diana, C. petaurista, C. atys, and C. campbelli exhibited a greater diversity of parasite species and a more equitable distribution. The parasitological data reported are the first available for these cercopithecid species within Taï National Park. Les maladies parasitaires et infectieuses sont des menaces très connues pour les populations de primates. L’objectif principal de cette étude était de fournir des données de base sur les parasites intestinaux des primates non-humains du Parc National de Taï en Côte d’Ivoire. Sept des huit espèces de cercopithécidés vivant dans le parc ont été échantillonnées : Cercopithecus diana, Cercopithecus campbelli, Cercopithecus petaurista, Procolobus badius, Procolobus verus, Colobus polykomos and Cercocebus atys. Nous avons collecté 3142 échantillons de selles de singes de novembre 2009 à décembre 2010. Les échantillons de selles ont été traités par la technique d’examen direct, les méthodes de concentration formol-éthyl acétate et MIF (merthiolate, iode, formol). Les lames ont été examinées au microscope et l’identification des parasites a été basée sur la morphologie des kystes, des œufs et des vers adultes. Au total, 23 espèces de parasites ont été trouvées, dont 9 protozoaires (Entamoeba coli, Entamoeba histolytica/dispar, Entamoeba hartmanni, Endolimax nana, Iodamoeba butschlii, Chilomastix mesnili, Giardia sp., Balantidium coli et Blastocystis sp.), 13 nématodes (Oesophagostomum sp., Ancylostoma sp., Anatrichosoma sp., Capillariidae Gen. sp. 1, Capillariidae Gen. sp. 2, Chitwoodspirura sp., Subulura sp., Spiruridae [cf. Protospirura muricola], Ternidens sp., Strongyloides sp., Trichostrongylus sp. et Trichuris sp.), et un trématode (Dicrocoelium sp.). L’indice de diversité et la richesse parasitaire étaient élevés pour tous les taxa de singes, mais C. diana, C. petaurista, C. atys and C. campbelli ont enregistré une plus grande diversité et une distribution plus équitable des espèces de parasites. Les données parasitologiques que nous rapportons sont les premières disponibles pour ces espèces de singes du Parc National de Taï.

Group size affects many aspects of the ecology and social organization of animals. We investigated group size stability for five primate species in Kibale National Park, Uganda from 1996 to 2011 at three nested spatial scales. Survey data indicated that group sizes did not change for most species, with the exception of red colobus monkeys (Procolobus rufomitratus), in which group size increased at all spatial scales. Mangabey (Lophocebus albigena) group size increased in old‐growth forest, but the sample size and increase were small. To augment this survey data, we collected several years of demographic data on three habituated groups of redtail monkeys (Cercopithecus ascanius), eight groups of black‐and‐white colobus (Colobus guereza), and one red colobus group. The red colobus group increased from 59 to 104 individuals, while redtail monkey and black‐and‐white colobus group sizes were stable, mirroring our survey results. To understand mechanisms behind group size changes in red colobus versus stability in other primates, we monitored forest dynamics at two spatial scales between 1990 and 2013, considered changes in predator population, and explored evidence of disease dynamics. The cumulative size of all trees and red colobus food trees increased over 24 yr, suggesting that changing food availability was driving group size changes for red colobus, while predation and disease played lesser roles. Overall, our results and evidence of changing primate densities suggest that the Kibale primate community is in a non‐equilibrium state. We suggest future conservation and management efforts take this into consideration.

Despite strong links between sociality and fitness that ultimately affect the size of animal populations, the particular social and ecological factors that lead to endangerment are not well understood. Here, we synthesize approximately 25 years of data and present new analyses that highlight dynamics in forest composition, food availability, the nutritional quality of food, disease, physiological stress and population size of endangered folivorous red colobus monkeys (Procolobus rufomitratus). There is a decline in the quality of leaves 15 and 30 years following two previous studies in an undisturbed area of forest. The consumption of a low-quality diet in one month was associated with higher glucocorticoid levels in the subsequent month and stress levels in groups living in degraded forest fragments where diet was poor was more than twice those in forest groups. In contrast, forest composition has changed and when red colobus food availability was weighted by the protein-to-fibre ratio, which we have shown positively predicts folivore biomass, there was an increase in the availability of high-quality trees. Despite these changing social and ecological factors, the abundance of red colobus has remained stable, possibly through a combination of increasing group size and behavioural flexibility.

Gut microbiota diversity has become the subject of extensive research in human and nonhuman animals, linking diversity and composition to gut function and host health. Because wild primates are good indicators of tropical ecosystem health, we developed the idea that they are a suitable model to observe the consequences of advancing global change (e.g., habitat degradation) on gut microbiota. So far, most of the studies focus mainly on gut bacteria; however, they are not the only component of the gut: fungi also serve essential functions in gut homeostasis. Here, for the first time, we explore and measure diversity and composition of both bacterial and fungal microbiota components of two tropical primate species living in highly different habitat types (intact versus degraded forests). Results on their microbiota diversity and composition are discussed in light of conservation issues and potential applications. Human exploitation and destruction of tropical resources are currently threatening innumerable wild animal species, altering natural ecosystems and thus, food resources, with profound effects on gut microbiota. Given their conservation status and the importance to tropical ecosystems, wild nonhuman primates make excellent models to investigate the effect of human disturbance on the diversity of host-associated microbiota. Previous investigations have revealed a loss of fecal bacterial diversity in primates living in degraded compared to intact forests. However, these data are available for a limited number of species, and very limited information is available on the fungal taxa hosted by the gut. Here, we estimated the diversity and composition of gut bacterial and fungal communities in two primates living sympatrically in both human-modified and pristine forests in the Udzungwa Mountains of Tanzania. Noninvasively collected fecal samples of 12 groups of the Udzungwa red colobus ( Procolobus gordonorum ) ( n  = 89), a native and endangered primate (arboreal and predominantly leaf-eating), and five groups of the yellow baboon ( Papio cynocephalus ) ( n  = 69), a common species of least concern (ground-feeding and omnivorous), were analyzed by the V1-V3 region of the 16S rRNA gene (bacterial) and ITS1-ITS2 (fungal) sequencing. Gut bacterial diversities were associated with habitat in both species, most likely depending on their ecological niches and associated digestive physiology, dietary strategies, and locomotor behavior. In addition, fungal communities also show distinctive traits across hosts and habitat type, highlighting the importance of investigating this relatively unexplored gut component. IMPORTANCE Gut microbiota diversity has become the subject of extensive research in human and nonhuman animals, linking diversity and composition to gut function and host health. Because wild primates are good indicators of tropical ecosystem health, we developed the idea that they are a suitable model to observe the consequences of advancing global change (e.g., habitat degradation) on gut microbiota. So far, most of the studies focus mainly on gut bacteria; however, they are not the only component of the gut: fungi also serve essential functions in gut homeostasis. Here, for the first time, we explore and measure diversity and composition of both bacterial and fungal microbiota components of two tropical primate species living in highly different habitat types (intact versus degraded forests). Results on their microbiota diversity and composition are discussed in light of conservation issues and potential applications.

Growing threats to primates in tropical forests make robust and long-term population abundance assessments increasingly important for conservation. Concomitantly, monitoring becomes particularly relevant in countries with primate habitat. Yet monitoring schemes in these countries often suffer from logistic constraints and/or poor rigor in data collection, and a lack of consideration of sources of bias in analysis. To address the need for feasible monitoring schemes and flexible analytical tools for robust trend estimates, we analyzed data collected by local technicians on abundance of three species of arboreal monkey in the Udzungwa Mountains of Tanzania (two Colobus species and one Cercopithecus), an area of international importance for primate endemism and conservation. We counted primate social groups along eight line transects in two forest blocks in the area, one protected and one unprotected, over a span of 11 years. We applied a recently proposed open metapopulation model to estimate abundance trends while controlling for confounding effects of observer, site, and season. Primate populations were stable in the protected forest, while the colobines, including the endemic Udzungwa red colobus, declined severely in the unprotected forest. Targeted hunting pressure at this second site is the most plausible explanation for the trend observed. The unexplained variability in detection probability among transects was greater than the variability due to observers, indicating consistency in data collection among observers. There were no significant differences in both primate abundance and detectability between wet and dry seasons, supporting the choice of sampling during the dry season only based on minimizing practical constraints. Results show that simple monitoring routines implemented by trained local technicians can effectively detect changes in primate populations in tropical countries. The hierarchical Bayesian model formulation adopted provides a flexible tool to determine temporal trends with full account for any imbalance in the data set and for imperfect detection.

Accurate estimations of the abundance of threatened animal populations are required for assessment of species’ status and vulnerability and conservation planning. However, density estimation is usually difficult and resource demanding, so researchers often collect data at local scales. However, anthropogenic pressures most often have landscape-level effects, for example, through habitat loss and fragmentation. We applied hierarchical distance sampling (HDS) to transect count data to determine the effect of habitat and anthropogenic factors on the density of 3 arboreal primate species inhabiting 5 distinct tropical forests across a landscape of 19,000 km² in the Udzungwa Mountains of Tanzania. We developed a novel, multiregion extension of HDS that allowed us to model density and detectability jointly across forests without losing site-specific information. For all species, the effect of anthropogenic disturbance on density was overwhelmingly negative among metapopulations: -0.63 Angolan colobus (Colobus angolensis palliatus) (95% Bayesian CI -1.03 to -0.27), -0.54 Udzungwa red colobus (Procolobus gordonorum) (-0.89 to -0.22), and -0.33 Sykes’ monkey (Cercopithecus mitis monoides) (-0.63 to -0.07). Some responses to habitat factors were shared, notably the negative effect of elevation and the positive effect of climber coverage. These results are important for conservation science and practice because: the among-populations negative responses to anthropogenic disturbance provides a foundation for development of conservation plans that hold at the landscape scale, which is a comprehensive and cost-efficient approach; the among-species consistency in responses suggests conservation measures may be generalized at the guild level, which is especially relevant given the functional importance of primates in tropical rainforests; and the greater primate densities in areas at low elevation, which are closer to human settlements, point to specific management recommendations, such as the creation of buffer zones and prioritization of areas for protection. Se requieren estimaciones correctas del tamaño de las poblaciones de animales amenazados para evaluar el estado y la vulnerabilidad de las especies y así planear su conservación. Sin embargo, la estimación de la densidad es usualmente complicada y demanda recursos, así que los investigadores con frecuencia recolectan la información a escala local, a pesar de que la presión antropogénica suele tener efectos a nivel del paisaje; por ejemplo, la pérdida del hábitat y la fragmentación. Aplicamos un muestro jerárquico a distancia (HDS, en inglés) para contar datos por transecto y determinar el efecto de los factores del hábitat y los factores antropogénicos sobre la densidad de tres especies de primates arbóreos en un paisaje de 19,000 km² en las montañas de Udzungwa en Tanzania. Desarrollamos una novedosa extensión multiregión de HDS que nos permitió modelar en conjunto la densidad y la facilidad de detección en los bosques sin perder información específica del sitio. Para todas las especies, el efecto de la perturbación antropogénica sobre la densidad fue abrumadoramente negativa entre las metapoblaciones: -0.63 para el colobo angoleño (Colobus angolensis palliatus) (95% bayesiano CI de -1.03 a -0.27), -0.54 para el colobo rojo de Udzungwa (Procolobus gordonorum) (de -0.89 a -0.22), y -0.33 para el mono de Syke (Cercopithecus mitis monoides) (de -0.63 a -0.07). Los monos compartieron algunas respuestas a los factores de hábitat, notoriamente los efectos negativos de la elevación y el efecto positivo de la cobertura de plantas trepadoras. Estos resultados son importantes para la ciencia y práctica de la conservación ya que: las respuestas negativas a las perturbaciones antropogénicas entre las poblaciones proporcionan los cimientos para el desarrollo de planes de conservación que serán válidos a nivel de paisaje, la cual es una estrategia completa y rentable; la consistencia de las respuestas entre las especies sugiere que las medidas de conservación pueden estar generalizadas a nivel de gremio, lo cual es de suma relevancia dada la importancia funcional de los primates en los bosques tropicales; y la densidad mayor de primates en áreas con elevación baja, las cuales están próximas a los asentamientos humanos, señalan hacia recomendaciones específicas de manejo, como la creación de zonas de amortiguamiento y la priorización de áreas para proteger. 物种瀕危等级、易危性的评估及保护规划需要对濒危动物种群数量进行准确估计。但是密度估计通常 较为困难，且对资源的需求较高，因此研究者一般只能收集局部尺度的数据。然而，人为压カ的影响常常是景观 尺度的，例如导致生境丧失和破碎化。我们在坦桑尼亚乌德宗瓦山脉(Udzungwa Mountains) 19,000平方千米 的景观尺度中，采用分层距离取样法收集样带计数数据，确定了生境和人为因素对三种栖息在五个不同的热带 森林树栖灵长类物种种群密度的影响。我们发展了一种新的多区域分层距离取样法，可以在不丟失位置特异信 息的情况下对跨越多个森林的物种种群密度和可探测性统一建模。对所有这三个物神来说人为干扰对集合种 群密度的影响整体上都是负面的:安哥拉抚猴(Colobus angolensis palliatus)为- ひ63 (95 % 贝叶斯置信区间 为-1.03到-0.27),，乌德宗瓦红抚猴(Procolobus gordonorum)为-0.54 (95 % 贝叶斯置信区间为-0.89到 -0.22);青猴(Cercopithecus mitis monoides)为-ひ33 (95 % 贝叶斯置信区间为-0.63 到-0.07) 0 它们对生 境因素的响应有共同之此特别是海拔的负面影响和攀缘植物覆盖度的积极作用。这些结果对保护科学和实践 十分重要，因为种群间对人为干扰共同的负面响应为发展景观尺度上的保护计划提供了基础，这样的保护实践更 为全面且成本效益高; 物种间的响应一致性刺表明保护措施可能可以推广到多物种水平，考虑到灵长类动物对热 带雨林的重要功能，这一点意文重大; 而灵长类在海拔低、与人类居住地较近的地区密度更高，这指明了具体的 管理鐵例如确立缓冲区和优先保护区域。

Substantial research has shown that while some parasite infections can be fatal to hosts, most infections are sub-clinical and non-lethal. Such sub-clinical infections can nonetheless have negative consequences for the long-term fitness of the host such as reducing juvenile growth and the host's ability to compete for food and mates. With such effects, infected individuals are expected to exhibit behavioural changes. Here we use a parasite removal experiment to quantify how gastrointestinal parasite infections affect the behaviour of vervet monkeys (Chlorocebus aethiops) at Lake Nabugabo, Uganda. Behavioural profiles and the structure of nearest neighbour relationships varied significantly. As predicted, after deworming the duration of the resting events decreased, which is consistent with the idea that parasite infections are energetically costly. In contrast to what was predicted, we could not reject the null hypothesis and we observed no change in either the frequency or duration of grooming, but we found that the duration of travel events increased. A network analysis revealed that after deworming, individuals tended to have more nearest neighbours and hence probably more frequent interactions, with this effect being particularly marked for juveniles. The heightened response by juveniles may indicate that they are avoiding infected individuals more than other age classes because it is too costly to move energy away from growth. We consider that populations with high parasite burden may have difficulties developing social networks and behaviours that could have cascading effects that impact the population in general.

In light of the current biodiversity crisis, investigating the human impact on non-human primate gut biology is important to understanding the ecological significance of gut community dynamics across changing habitats and its role in conservation. Using traditional coproscopic parasitological techniques, we compared the gastrointestinal protozoan and metazoan symbiont richness of two primates: the Udzungwa red colobus ( Procolobus gordonorum ) and the yellow baboon ( Papio cynocephalus ). These species live sympatrically in both protected and unprotected forests within the Udzungwa Mountains of Tanzania with distinct ecological adaptations and diets. Our results showed that terrestrial and omnivorous yellow baboons had 2 (95% CI 1.47–2.73) and 3.78 (2.62–5.46) times higher gut symbiont richness (both including and excluding rare protozoans) compared to the arboreal and leaf-eating Udzungwa red colobus in unprotected and protected forest, respectively. We also found a consistent depletion of symbiont richness in red colobus living in the unprotected forest fragment compared to the continuous protected forests [the latter having 1.97 times (95% CI 1.33–2.92) higher richness], but not in yellow baboons. Richness reduction was particularly evident in the Udzungwa red colobus monkeys, confirming the pattern we reported previously for gut bacterial communities. This study demonstrates the impact of human activities even on the microbiodiversity of the intestinal tract of this species. Against the background of rapid global change and habitat degradation, and given the health benefits of intact gut communities, the decrease in natural gut symbionts reported here is worrying. Further study of these communities should form an essential part of the conservation framework.