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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 km 2 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., (© 2018 Society for Conservation Biology.)

The application of distance sampling to primate density estimation is challenging and susceptible to estimation biases, mainly due to the difficulties of properly accounting for variation in species' detectability and of accurately sampling the spread of the social groups. We apply a hierarchical distance sampling approach to primate data, to account for a comprehensive set of environmental covariates of both detectability and abundance, and we propose a novel field routine to measure the spread of groups during transect sampling. We confirm the good potential of this approach, given we obtained refined estimates of primate density (as measured by the Akaike Information Criterion) in comparison to estimates from models without covariates., (© 2017 Wiley Periodicals, Inc.)

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., (© 2016 by the Ecological Society of America.)

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.

The Udzungwa Mountains are one of the most important areas in Africa for primate diversity and conservation, with two endemic monkeys (Udzungwa red colobus Procolobus gordonorum and Sanje mangabey Cercocebus [galeritus] sanjei), and the near-endemic kipunji monkey Rungwecebus kipunji, a new genus and species discovered in 2004 and found in Udzungwa and Southern Highlands. With six species of galagos, or bushbabies, the area is also of exceptional importance for nocturnal primates. The form of Mountain galago Galagoides orinus occurring in the Udzungwa Mountains appears to be distinct on the base of vocalizations, and further work will be required to assess its taxonomic status. The primate community reflects the overall, exceptional biodiversity of these isolated and ancient mountains. The Udzungwa are part of the Eastern Arc mountain chain, a centre of global importance for biodiversity and endemism. Of all the Eastern Arc Mountain blocks, the Udzungwa have the largest forested area, widest altitudinal gradient and greatest habitat diversity. We review current knowledge on the diversity and distribution of the primate community of the Udzungwa Mountains, with an emphasis on ecology and conservation.

Determining ecological predictors of primate abundance is important for both theoretical and applied conservation management. For forest primates, research has focused on comparisons of primate abundance and vegetation in different forest blocks or forest compartments with different management histories. However, great variation in primate abundance often occurs within single forests, especially in mountainous areas or in areas with habitat mosaics due to past disturbance. Here we assess, for the first time, the usefulness and limitations of small-scale, within-transect analysis of vegetative parameters as predictors of primate abundance in a very heterogeneous forest habitat in the Udzungwa Mountains of Tanzania. Relative abundance of four species of diurnal primates was recorded over a period of 2.5 years by walking three census transects 48 times each. Tree size, density, species composition, and food plants were measured along the same census lines. The fine-scale relationship between primate abundance and vegetative variables was analyzed through generalized linear modeling applied to 58 segments of these three census lines. Each segment was 200 m in length. For all four primate species, we found significant associations between their abundance and selected vegetative variables. The abundance of the endemic and endangered Udzungwa red colobus Procolobus gordonorum was positively related to mean basal area of large trees (diameter at breast height greater than 20 cm) and to the species richness of their food plants. Considering the very great variation in primate abundance that was recorded among segments of the census lines, our approach proved useful in predicting the relationship between primate abundance and small-scale habitat differences. The main limitation of this study, however, was the relatively low-predictive power of the models for some species, especially the Angolan colobus Colobus angolensis. We discuss the potential reasons for this problem and suggest possible improvements for future studies.

Anthropogenic activities driving tropical forests' loss imperil global biodiversity and provision of ecosystem services. In this context, systematic monitoring programs evaluating wildlife trends are essential. Non‐human primates are relevant conservation targets since they represent vital components of tropical forests by serving as pollinators and seed dispersers. Here, we present primate group counts data collected over 19 years in a primate hotspot in Tanzania. We analyzed data with a hierarchical dynamic model accounting for imperfect detection that estimates local group abundance and temporal rates of change, to assess whether habitat protection explained trends of the arboreal and diurnal Peters' Angola colobus (Colobus angolensis palliatus), Udzungwa red colobus (Piliocolobus gordonorum), and Tanzania Sykes' monkey (Cercopithecus mitis subsp. moloneyi). We targeted populations occurring in two forest blocks with contrasting protection regimes, with one block impacted by targeted poaching of the two Colobus species. We found that these latter species were much less abundant in the more human impacted forest, underwent a rapid decline, and subsequently remained at low abundance and without signs of recovery once this forest was granted greater protection. Instead, Sykes' abundance did not differ between forests, and improved protection was associated with a slight increase in abundance. Age class composition for social groups of both Colobus species differed between forests, indicating altered births and survivorship rates in the impacted forest. Results suggest that targeted hunting can prevent recovery for several years and even after increased habitat protection. Our approach appears valuable to monitor population dynamics over the long term, highlighting species‐specific variations in both vulnerability to anthropogenic disturbance and recovery patterns in primate populations. [ABSTRACT FROM AUTHOR]

The mammalian gastrointestinal tract harbours a highly complex ecosystem composed of a variety of micro- (bacteria, fungi, viruses, protozoans) and macro-organisms (helminths). Although most microbiota research focuses on the variation of single gut components, the crosstalk between components is still poorly characterized, especially in hosts living under natural conditions. We investigated the gut micro-biodiversity (bacteria, fungi and helminths) of 158 individuals of two wild non-human primates, the Udzungwa red colobus (Procolobus gordonorum) and the yellow baboon (Papio cynocephalus). These species have contrasting diets and lifestyles, but live sympatrically in both human-impacted and pristine forests in the Udzungwa Mountains of Tanzania. Using non-invasive faecal pellets, helminths were identified using standard microscopy while bacteria and fungi were characterized by sequencing the V1–V3 variable region of the 16S rRNA gene for bacteria and the ITS1–ITS2 fragment for fungi. Our results show that both diversity and composition of bacteria and fungi are associated with variation in helminth presence. Although interactions differed by habitat type, in both primates we found that Strongyloides was negatively associated and Trichuris was positively associated with bacterial and fungal richness. To our knowledge, this is one of the few studies demonstrating an interaction between helminth and gut microbiota communities in wild non-human primates. [ABSTRACT FROM AUTHOR]

Primates are one of the most threatened groups of mammals. Understanding their patterns of population occurrence and abundance, especially in response to threats, is critical for informing conservation action. The crested black macaque Macaca nigra is the only Critically Endangered species of Sulawesi's seven endemic macaques. Little is known about its distribution or its response to deforestation and hunting. We conducted a camera-trap survey across the entire species range using an occupancy-based analytical approach to (1) establish the first range-wide baseline of occurrence, (2) investigate how environmental and anthropogenic factors influence occurrence, (3) identify priority conservation subpopulations, and (4) test the efficacy of the sampling and analytical protocol for temporal monitoring of M. nigra using occupancy as the state variable. From 9,753 camera-trap days, M. nigra was detected on 473 days at 77 of the 111 camera locations. Species occupancy was 0.66 and highest inside protected areas and closed canopy forest. We identified eight distinct subpopulations, based on distribution and forest fragment size. To inform future monitoring, we used a power analysis to determine if our effort would allow us to detect inter-annual occupancy declines of 10%, and found that 90 camera locations surveyed for 3 months (8,100 camera days) across three consecutive seasons is the effort required to detect such change with 80% certainty. Our study underscores the importance of well-managed protected areas and intact forests for the long-term survival of the crested black macaque, and tests the effectiveness of camera traps to monitor primates at the landscape scale. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

Gastrointestinal parasites colonizing the mammalian gut influence the host immune system and health. Parasite infections, mainly helminths, have been studied intensively in both humans and non-human animals, but relatively rarely within a conservation framework. The Udzungwa red colobus monkey (Procolobus gordonorum) is an endangered endemic primate species living in the Udzungwa Mountains of Tanzania, a global biodiversity hotspot. Since this endemic primate species is highly sensitive to human disturbance, here we investigate whether habitat type (driven by natural and human-induced factors) is associated with helminth diversity. Using standard flotation and sedimentation techniques, we analyzed 251 fecal samples belonging to 25 social groups from four different forest blocks within the Udzungwa Mountains. Five parasitic helminth taxa were recovered from Udzungwa red colobus, including Trichuris sp., Strongyloides fulleborni, S. stercoralis, a strongylid nematode and Colobenterobius sp. We used Generalized Linear Mixed Models to explore the contribution of habitat type, altitude and fecal glucocorticoid levels (as biomarkers of stress) in predicting gut parasite variation. Although some parasites (e.g., Trichuris sp.) infected more than 50% of individuals, compared to others (e.g., Colobenterobius sp.) that infected less than 3%, both parasite richness and prevalence did not differ significantly across forests, even when controlling for seasonality. Stress hormone levels also did not predict variation in parasite richness, while altitude could explain it resulting in lower richness at lower altitudes. Because human activities causing disturbance are concentrated mainly at lower altitudes, we suggest that protection of primate forest habitat preserves natural diversity at both macro- and microscales, and that the importance of the latter should not be underestimated. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

Abstract: Hunting and habitat degradation are universal threats to primates across the tropics, thus deciphering the relative impact of threats on population relative abundance is critical to predicting extinction risk and providing conservation recommendations. We studied diurnal primates over a period of nearly 6years in the Udzungwa Mountains of Tanzania, a site of global importance for primate conservation. We assessed how population relative abundance of five species (of which two are endemic and IUCN-Endangered) differed between two forest blocks that are similar in size and habitat types but contrast strongly in protection level, and how abundance changed during 2004–2009. We also measured habitat and disturbance parameters and, in the unprotected forest, evaluated hunting practices. We found significant differences in primates’ abundance between protected and unprotected forests, with the greater contrast being the lower abundance of colobine monkeys (Udzungwa red colobus and Angolan colobus) in the unprotected forest. At this site moreover, colobines declined to near-extinction over the study period. In contrast, two cercopithecines (Sanje mangabey and Sykes’ monkey) showed slightly higher abundance in the unprotected forest and did not decline significantly. We argue that escalating hunting in the unprotected forest has specifically impacted the canopy-dwelling colobus monkeys, although habitat degradation may also have reduced their abundance. In contrast, cercopithecines did not seem affected by the current hunting, and their greater ecological adaptability may explain the relatively higher abundance in the unprotected forest. We provide recommendations towards the long-term protection of the area. [Copyright &y& Elsevier]

This study investigates the species–area relationship (SAR) for forest monkeys in a biodiversity hotspot. The Udzungwa Mountains of Tanzania are well-suited to investigate the SAR, with seven monkey species in a range of fragment sizes (0.06–526 km2). We test the relationship between species richness and forest fragment size, relative to human and environmental factors. We distinguish resident and transitory species because the latter have an “effective patch size” beyond the area of forest. Forest area was the strongest (log-linear) predictor of species richness. However, forest area, elevation range and annual moisture index were intercorrelated. Previous knowledge of the relationship between elevation and tree communities suggests that the SAR is largely a result of habitat heterogeneity. Isolation by farmland (matrix habitat) also had a significant negative effect on species richness, probably exacerbated by hunting in small forests. The effect of area and isolation was less for transitory species. The human influence on species' presence/absence was negatively related to the extent of occurrence. Weaker relationships with temperature and precipitation suggest underlying climatic influences, and give some support for the influence of productivity. A reduced area relationship for smaller forests suggests that fragment sizes below 12–40 km2 may not be reliable for determining SAR in forest monkeys. Further practical implications are for management to encourage connectivity, and for future SAR research to consider residency, matrix classification and moisture besides precipitation. Am. J. Primatol. 72:325–336, 2010. © 2009 Wiley-Liss, Inc. [ABSTRACT FROM AUTHOR]

Many individual researchers have used line transect counts to estimate forest primate abundance. They have devoted less attention to the interpretation of line transect data obtained by several observers, as is often the case in long-term monitoring programs. We present primate relative abundance data that 5 observers collected over 6 yr (not continuous) along 4 different transects each 4 km long in the Mwanihana Forest, Udzungwa Mountains National Park, Tanzania. Total distance walked during transect repetitions is ca. 700 km. The species we saw most frequently was the endemic Udzungwa red colobus Procolobus gordonorum (mean 0.59 groups/km walked), followed by the Angolan black-and-white colobus Colobus angolensis (0.43 groups/km) and Sykes’s monkey Cercopithecus mitis (0.35 groups/km). We sighted the endemic Sanje mangabey Cercocebus galeritus sanjei and the yellow baboon Papio cynocephalus infrequently, the latter being confined to the deciduous forest parts of the transects. We analyzed sighting frequency by gross habitat type, transect, season, and observer. Interobserver differences in the relative abundance of each species were moderate and the few cases of significant variations were due to discordance of only 1 observer from the others. Estimated distances of primate group sightings differ significantly among observers, thus preventing us from deriving estimates of absolute density. Frequency distributions of distance-class intervals are not significantly different among observers, which may indicate gross interobserver consistency in the width of the area sampled. We conclude that unless consistency in data collection is checked, as we did for 2 observers who collected data simultaneously, potential interobserver differences remain an underlying source of variance in the results that cannot be separated from other sources of variance. [ABSTRACT FROM AUTHOR]

The correct is: Barelli C, Gonzalez-Astudillo V, Mundry R, Rovero F, Heistermann M, Hauffe HC, et al (2019) Altitude and human disturbance are associated with helminth diversity in an endangered primate, Procolobus gordonorum. Reference 1 Barelli C, Gonzalez-Astudillo V, Mundry R, Rovero F, Hauffe HC, Gillespie TR (2019) Altitude and human disturbance are associated with helminth diversity in an endangered primate, I Procolobus gordonorum i . [Extracted from the article]