1. Calibrating indices of animal abundance to true densities is critical in wildlife studies especially when direct density estimations are precluded by high costs, lack of required data or model ...parameters, elusiveness and rarity of target species. For studies deploying camera traps, the use of photographic rate (photographs per sampling time) as an index of abundance potentially applies to the majority of terrestrial mammals where individual recognition, and hence capture—recapture analysis, are unfeasible. The very few studies addressing this method have either been limited by lack of independence between trapping rates and density estimations, or because they combined different species, thus introducing potential bias in camera trap detection rates. This study uses a single model species from several sites to analyse calibration of trapping rates to independently derived estimations of density. The study also makes the first field test of the method by Rowcliffe et al. (2008) for density derivation from camera trapping rates based on modelling animal-camera contacts. 2. We deployed camera traps along line transects at six sites in the Udzungwa Mountains of Tanzania and correlated trapping rates of Harvey's duiker Cephalophus harveyi with densities estimated from counts made along the same transects. 3. We found a strong, linear relationship (R² = 0·90) between trapping rate and density. Sampling precision analysis indicates that camera trapping rates reach satisfactory precision when trapping effort amounts to 250-300 camera days. Density estimates using Rowcliffe et al.'s (2008) gas model conversion are higher than from transect censuses; we discuss the possible reasons and stress the need for more field tests. 4. Synthesis and applications. Subject to rigorous and periodic calibration, and standardization of sampling procedures in time and over different sites, camera trapping rate is shown to be, in this study, a valid index of density in the target species. Comparative data indicate that this may also apply to forest ungulates in general. The method has great potential for standardizing monitoring programmes and reducing the costs of wildlife surveys, especially in remote areas.
Medium-to-large mammals within tropical forests represent a rich and functionally diversified component of this biome; however, they continue to be threatened by hunting and habitat loss. Assessing ...these communities implies studying species' richness and composition, and determining a state variable of species abundance in order to infer changes in species distribution and habitat associations. The Tropical Ecology, Assessment and Monitoring (TEAM) network fills a chronic gap in standardized data collection by implementing a systematic monitoring framework of biodiversity, including mammal communities, across several sites. In this study, we used TEAM camera trap data collected in the Udzungwa Mountains of Tanzania, an area of exceptional importance for mammal diversity, to propose an example of a baseline assessment of species' occupancy. We used 60 camera trap locations and cumulated 1,818 camera days in 2009. Sampling yielded 10,647 images of 26 species of mammals. We estimated that a minimum of 32 species are in fact present, matching available knowledge from other sources. Estimated species richness at camera sites did not vary with a suite of habitat covariates derived from remote sensing, however the detection probability varied with functional guilds, with herbivores being more detectable than other guilds. Species-specific occupancy modelling revealed novel ecological knowledge for the 11 most detected species, highlighting patterns such as 'montane forest dwellers', e.g. the endemic Sanje mangabey (Cercocebus sanjei), and 'lowland forest dwellers', e.g. suni antelope (Neotragus moschatus). Our results show that the analysis of camera trap data with account for imperfect detection can provide a solid ecological assessment of mammal communities that can be systematically replicated across sites.
Determining correlates of density for large carnivores is important to understand their ecological requirements and develop conservation strategies. Of several earlier density studies conducted ...globally, relatively few addressed a scale (usually >1000 km2) that allows inference on correlates of density over heterogeneous landscapes. We deployed 164 camera trap stations covering ~2500 km2 across five areas characterized by broadly different vegetation cover in the Udzungwa Mountains, Tanzania, to investigate correlates of density for a widespread and adaptable carnivore, the leopard (Panthera pardus). We modelled data in a spatially explicit capture-recapture framework, with both biotic and abiotic covariates hypothesised to influence density. We found that leopard density increased with distance to protected area boundary (mean±SE estimated effect = 0.44±0.20), a proxy for both protected area extent and distance from surrounding human settlements. We estimated mean density at 4.22 leopards/100 km2 (85% CI = 3.33‒5.35/100 km2), with no variation across habitat types. Results indicate that protected area extent and anthropogenic disturbance limit leopard populations whereas no support was found for prey availability and trap array as drivers of leopard density. Such vulnerability is relevant to the conservation of the leopard, which is generally considered more resilient to human disturbance than other large cats. Our findings support the notion that protected areas are important to preserve viable population of leopards, increasingly so in times of unprecedented habitat fragmentation. Protection of buffer zones smoothing the abrupt impact of human activities at reserve edges also appears of critical conservation relevance.
With biodiversity facing unparalleled threats from anthropogenic disturbance, knowledge on the occurrences of species and communities provides for an effective and fast approach to assess their ...status and vulnerability. Disturbance is most prominent at the landscape-level, for example through habitat loss from large-scale resource extraction or agriculture. However, addressing species responses to habitat changes at the landscape-scale can be difficult and cost-ineffective, hence studies are mostly conducted at single areas or habitat patches. Moreover, there is a relative lack of studies on communities, as opposed to focal species, despite the former may carry more comprehensive information. Here, we used a multi-region, multi-species hierarchical occupancy model to study a meta-community of mammals detected by camera traps across five distinct areas within a heterogeneous landscape in Tanzania, and aimed to assess responses to human disturbance and environmental variables. Estimated species richness did not vary significantly across different areas, even though these held broadly different habitats. Moreover, we found remarkable consistency in the positive effect of distance to human settlements, a proxy for anthropogenic disturbance, on community occupancy. The positive effect of body size and the positive effect of proximity to rivers on community occupancy were also shared by communities. Results yield conservation relevance because: (1) the among-communities consistency in responses to anthropogenic disturbance, despite the heterogeneity in sampled habitats, indicates that conservation plans designed at the landscape-scale may represent a comprehensive and cost-efficient approach; (2) the consistency in responses to environmental factors suggests that multi-species models are a powerful method to study ecological patterns at the landscape-level.
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.
Nonhuman primates, our closest biological relatives, play important roles in the livelihoods, cultures, and religions of many societies and offer unique insights into human evolution, biology, ...behavior, and the threat of emerging diseases. They are an essential component of tropical biodiversity, contributing to forest regeneration and ecosystem health. Current information shows the existence of 504 species in 79 genera distributed in the Neotropics, mainland Africa, Madagascar, and Asia. Alarmingly, ~60% of primate species are now threatened with extinction and ~75% have declining populations. This situation is the result of escalating anthropogenic pressures on primates and their habitats-mainly global and local market demands, leading to extensive habitat loss through the expansion of industrial agriculture, large-scale cattle ranching, logging, oil and gas drilling, mining, dam building, and the construction of new road networks in primate range regions. Other important drivers are increased bushmeat hunting and the illegal trade of primates as pets and primate body parts, along with emerging threats, such as climate change and anthroponotic diseases. Often, these pressures act in synergy, exacerbating primate population declines. Given that primate range regions overlap extensively with a large, and rapidly growing, human population characterized by high levels of poverty, global attention is needed immediately to reverse the looming risk of primate extinctions and to attend to local human needs in sustainable ways. Raising global scientific and public awareness of the plight of the world's primates and the costs of their loss to ecosystem health and human society is imperative.
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.
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.
Although male and female mammals differ in biological traits and functional needs, the contribution of this sexual dimorphism to variations in gut bacteria and fungi (gut microbiota) in relation to ...habitat type has not been fully examined. To understand whether the combination of sex and habitat affects gut microbiota variation, we analyzed 40 fecal samples of wild yellow baboons (Papio cynocephalus) living in contrasting habitat types (intact, well-protected vs. fragmented, less protected forests) in the Udzungwa Mountains of Tanzania. Sex determination was performed using the marker genes SRY (Sex-determining Region Y) and DDX3X-DDX3Y (DEAD-Box Helicase 3). Samples were attributed to 34 individuals (19 females and 15 males) belonging to five social groups. Combining the results of sex determination with two amplicon sequencing datasets on bacterial (V1-V3 region of the 16S rRNA gene) and fungal (ITS2) gut communities, we found that overall, baboon females had a significantly higher gut bacterial richness compared to males. Beta diversity estimates indicated that bacterial composition was significantly different between males and females, and this was true for individuals from both well- and less protected forests. Our results highlight the combined role of sex and habitat type in shaping variation in gut microbial communities in wild non-human primates.
Terrestrial mammals are a key component of tropical forest communities as indicators of ecosystem health and providers of important ecosystem services. However, there is little quantitative ...information about how they change with local, regional and global threats. In this paper, the first standardized pantropical forest terrestrial mammal community study, we examine several aspects of terrestrial mammal species and community diversity (species richness, species diversity, evenness, dominance, functional diversity and community structure) at seven sites around the globe using a single standardized camera trapping methodology approach. The sites—located in Uganda, Tanzania, Indonesia, Lao PDR, Suriname, Brazil and Costa Rica—are surrounded by different landscape configurations, from continuous forests to highly fragmented forests. We obtained more than 51 000 images and detected 105 species of mammals with a total sampling effort of 12 687 camera trap days. We find that mammal communities from highly fragmented sites have lower species richness, species diversity, functional diversity and higher dominance when compared with sites in partially fragmented and continuous forest. We emphasize the importance of standardized camera trapping approaches for obtaining baselines for monitoring forest mammal communities so as to adequately understand the effect of global, regional and local threats and appropriately inform conservation actions.