For several decades, primatologists have been interested in understanding how sympatric primate species are able to coexist. Most of our understanding of primate community ecology derives from the assumption that these animals interact predominantly with other primates. In this study, we investigate to what extent multiple community assembly hypotheses consistent with this assumption are supported when tested with communities of primates in isolation versus with communities of primates, birds, bats, and squirrels together. We focus on vertebrate communities on the island of Borneo, where we examine the determinants of presence or absence of species, and how these communities are structured. We test for checkerboard distributions, guild proportionality, and Fox's assembly rule for favored states, and predict that statistical signals reflecting interactions between ecologically similar species will be stronger when nonprimate taxa are included in analyses. We found strong support for checkerboard distributions in several communities, particularly when taxonomic groups were combined, and after controlling for habitat effects. We found evidence of guild proportionality in some communities, but did not find significant support for Fox's assembly rule in any of the communities examined. These results demonstrate the presence of vertebrate community structure that is ecologically determined rather than randomly generated, which is a finding consistent with the interpretation that interactions within and between these taxonomic groups may have shaped species composition in these communities. This research highlights the importance of considering the broader vertebrate communities with which primates co-occur, and so we urge primatologists to explicitly consider nonprimate taxa in the study of primate ecology.
The conversion of forest to agriculture continues to contribute to the loss and fragmentation of remaining orang-utan habitat. There are still few published estimates of orang-utan densities in these heavily modified agricultural areas to inform range-wide population assessments and conservation strategies. In addition, little is known about what landscape features promote orang-utan habitat use. Using indirect nest count methods, we implemented surveys and estimated population densities of the Northeast Bornean orang-utan (Pongo pygmaeus morio) across the continuous logged forest and forest remnants in a recently salvage-logged area and oil palm plantations in Sabah, Malaysian Borneo. We then assessed the influence of landscape features and forest structural metrics obtained from LiDAR data on estimates of orang-utan density. Recent salvage logging appeared to have a little short-term effect on orang-utan density (2.35 ind/km 2 ), which remained similar to recovering logged forest nearby (2.32 ind/km 2 ). Orang-utans were also present in remnant forest patches in oil palm plantations, but at significantly lower numbers (0.82 ind/km 2 ) than nearby logged forest and salvage-logged areas. Densities were strongly influenced by variation in canopy height but were not associated with other potential covariates. Our findings suggest that orang-utans currently exist, at least in the short-term, within human-modified landscapes, providing that remnant forest patches remain. We urge greater recognition of the role that these degraded habitats can have in supporting orang-utan populations, and that future range-wide analyses and conservation strategies better incorporate data from human-modified landscapes.
Anthropogenic habitat disturbance is a major threat to biodiversity worldwide. Yet, before population declines are detectable, individuals may suffer from chronic stress and impaired immunity in disturbed habitats, making them more susceptible to pathogens and adverse weather conditions. Here, we tested in a paleotropical forest with ongoing logging and fragmentation, whether habitat disturbance influences the body mass and immunity of bats. We measured and compared body mass, chronic stress (indicated by neutrophil to lymphocyte ratios) and the number of circulating immune cells between several bat species with different roost types living in recovering areas, actively logged forests, and fragmented forests in Sabah, Malaysia. In a cave-roosting species, chronic stress levels were higher in individuals from fragmented habitats compared with conspecifics from actively logged areas. Foliage-roosting species showed a reduced body mass and decrease in total white blood cell counts in actively logged areas and fragmented forests compared with conspecifics living in recovering habitats. Our study highlights that habitat disturbance may have species-specific effects on chronic stress and immunity in bats that are potentially related to the roost type. We identified foliage-roosting species as particularly sensitive to forest habitat deterioration. These species may face a heightened extinction risk in the near future if anthropogenic habitat alterations continue.
Emerging infectious diseases (EIDs) are considered a major threat to global health. Most EIDs appear to result from increased contact between wildlife and humans, especially when humans encroach into formerly pristine habitats. Habitat deterioration may also negatively affect the physiology and health of wildlife species, which may eventually lead to a higher susceptibility to infectious agents and/or increased shedding of the pathogens causing EIDs. Bats are known to host viruses closely related to important EIDs. Here, we tested in a paleotropical forest with ongoing logging and fragmentation, whether habitat disturbance influences the occurrence of astro- and coronaviruses in eight bat species. In contrast to our hypothesis, anthropogenic habitat disturbance was not associated with corona- and astrovirus detection rates in fecal samples. However, we found that bats infected with either astro- or coronaviruses were likely to be coinfected with the respective other virus. Additionally, we identified two more risk factors influencing astrovirus shedding. First, the detection rate of astroviruses was higher at the beginning of the rainy compared to the dry season. Second, there was a trend that individuals with a poor body condition had a higher probability of shedding astroviruses in their feces. The identification of risk factors for increased viral shedding that may potentially result in increased interspecies transmission is important to prevent viral spillovers from bats to other animals, including humans.
Habitat degradation is pervasive across the tropics and is particularly acute in Southeast Asia, with major implications for biodiversity. Much research has addressed the impact of degradation on species diversity; however, little is known about how ecological interactions are altered, including those that constitute important ecosystem functions such as consumption of herbivores. To examine how rainforest degradation alters trophic interaction networks, we applied DNA metabarcoding to construct interaction networks linking forest-dwelling insectivorous bat species and their prey, comparing old-growth forest and forest degraded by logging in Sabah, Borneo. Individual bats in logged rainforest consumed a lower richness of prey than those in old-growth forest. As a result, interaction networks in logged forests had a less nested structure. These network structures were associated with reduced network redundancy and thus increased vulnerability to perturbations in logged forests. Our results show how ecological interactions change between old-growth and logged forests, with potentially negative implications for ecosystem function and network stability.
Tropical forest ecosystems are facing unprecedented levels of degradation, severely compromising habitat suitability for wildlife. Despite the fundamental role biodiversity plays in forest regeneration, identifying and prioritizing degraded forests for restoration or conservation, based on their wildlife value, remains a significant challenge. Efforts to characterize habitat selection are also weakened by simple classifications of human-modified tropical forests as intact vs. degraded, which ignore the influence that three-dimensional (3D) forest structure may have on species distributions. Here, we develop a framework to identify conservation and restoration opportunities across logged forests in Borneo. We couple high-resolution airborne light detection and ranging (LiDAR) and camera trap data to characterize the response of a tropical mammal community to changes in 3D forest structure across a degradation gradient. Mammals were most responsive to covariates that accounted explicitly for the vertical and horizontal characteristics of the forest and actively selected structurally complex environments comprising tall canopies, increased plant area index throughout the vertical column, and the availability of a greater diversity of niches. We show that mammals are sensitive to structural simplification through disturbance, emphasizing the importance of maintaining and enhancing structurally intact forests. By calculating occurrence thresholds of species in response to forest structural change, we identify areas of degraded forest that would provide maximum benefit for multiple high-conservation value species if restored. The study demonstrates the advantages of using LiDAR to map forest structure, rather than relying on overly simplistic classifications of human-modified tropical forests, for prioritizing regions for restoration.
The application of metabarcoding to environmental and invertebrate-derived DNA (eDNA and iDNA) is a new and increasingly applied method for monitoring biodiversity across a diverse range of habitats. This approach is particularly promising for sampling in the biodiverse humid tropics, where rapid land-use change for agriculture means there is a growing need to understand the conservation value of the remaining mosaic and degraded landscapes. Here we use iDNA from blood-feeding leeches (Haemadipsa picta) to assess differences in mammalian diversity across a gradient of forest degradation in Sabah, Malaysian Borneo. We screened 557 individual leeches for mammal DNA by targeting fragments of the 16S rRNA gene and detected 14 mammalian genera. We recorded lower mammal diversity in the most heavily degraded forest compared to higher quality twice logged forest. Although the accumulation curves of diversity estimates were comparable across these habitat types, diversity was higher in twice logged forest, with more taxa of conservation concern. In addition, our analysis revealed differences between the community recorded in the heavily logged forest and that of the twice logged forest. By revealing differences in mammal diversity across a human-modified tropical landscape, our study demonstrates the value of iDNA as a noninvasive biomonitoring approach in conservation assessments.
Old-growth tropical forests are widely recognized as being immensely important for their biodiversity and high biomass1. Conversely, logged tropical forests are usually characterized as degraded ecosystems2. However, whether logging results in a degradation in ecosystem functions is less clear: shifts in the strength and resilience of key ecosystem processes in large suites of species have rarely been assessed in an ecologically integrated and quantitative framework. Here we adopt an ecosystem energetics lens to gain new insight into the impacts of tropical forest disturbance on a key integrative aspect of ecological function: food pathways and community structure of birds and mammals. We focus on a gradient spanning old-growth and logged forests and oil palm plantations in Borneo. In logged forest there is a 2.5-fold increase in total resource consumption by both birds and mammals compared to that in old-growth forests, probably driven by greater resource accessibility and vegetation palatability. Most principal energetic pathways maintain high species diversity and redundancy, implying maintained resilience. Conversion of logged forest into oil palm plantation results in the collapse of most energetic pathways. Far from being degraded ecosystems, even heavily logged forests can be vibrant and diverse ecosystems with enhanced levels of ecological function.
Delivering the Sustainable Development Goals (SDGs) requires balancing demands on land between agriculture (SDG 2) and biodiversity (SDG 15). The production of vegetable oils and, in particular, palm oil, illustrates these competing demands and trade-offs. Palm oil accounts for ~40% of the current global annual demand for vegetable oil as food, animal feed and fuel (210 Mt), but planted oil palm covers less than 5-5.5% of the total global oil crop area (approximately 425 Mha) due to oil palm's relatively high yields. Recent oil palm expansion in forested regions of Borneo, Sumatra and the Malay Peninsula, where >90% of global palm oil is produced, has led to substantial concern around oil palm's role in deforestation. Oil palm expansion's direct contribution to regional tropical deforestation varies widely, ranging from an estimated 3% in West Africa to 50% in Malaysian Borneo. Oil palm is also implicated in peatland draining and burning in Southeast Asia. Documented negative environmental impacts from such expansion include biodiversity declines, greenhouse gas emissions and air pollution. However, oil palm generally produces more oil per area than other oil crops, is often economically viable in sites unsuitable for most other crops and generates considerable wealth for at least some actors. Global demand for vegetable oils is projected to increase by 46% by 2050. Meeting this demand through additional expansion of oil palm versus other vegetable oil crops will lead to substantial differential effects on biodiversity, food security, climate change, land degradation and livelihoods. Our Review highlights that although substantial gaps remain in our understanding of the relationship between the environmental, socio-cultural and economic impacts of oil palm, and the scope, stringency and effectiveness of initiatives to address these, there has been little research into the impacts and trade-offs of other vegetable oil crops. Greater research attention needs to be given to investigating the impacts of palm oil production compared to alternatives for the trade-offs to be assessed at a global scale.
Invertebrates are dominant species in primary tropical rainforests, where their abundance and diversity contributes to the functioning and resilience of these globally important ecosystems. However, more than one-third of tropical forests have been logged, with dramatic impacts on rainforest biodiversity that may disrupt key ecosystem processes. We find that the contribution of invertebrates to three ecosystem processes operating at three trophic levels (litter decomposition, seed predation and removal, and invertebrate predation) is reduced by up to one-half following logging. These changes are associated with decreased abundance of key functional groups of termites, ants, beetles and earthworms, and an increase in the abundance of small mammals, amphibians and insectivorous birds in logged relative to primary forest. Our results suggest that ecosystem processes themselves have considerable resilience to logging, but the consistent decline of invertebrate functional importance is indicative of a human-induced shift in how these ecological processes operate in tropical rainforests.
Information on tropical Asian vertebrates has traditionally been sparse, particularly when it comes to cryptic species inhabiting the dense forests of the region. Vertebrate populations are declining globally due to land-use change and hunting, the latter frequently referred as "defaunation." This is especially true in tropical Asia where there is extensive land-use change and high human densities. Robust monitoring requires that large volumes of vertebrate population data be made available for use by the scientific and applied communities. Camera traps have emerged as an effective, non-invasive, widespread, and common approach to surveying vertebrates in their natural habitats. However, camera-derived datasets remain scattered across a wide array of sources, including published scientific literature, gray literature, and unpublished works, making it challenging for researchers to harness the full potential of cameras for ecology, conservation, and management. In response, we collated and standardized observations from 239 camera trap studies conducted in tropical Asia. There were 278,260 independent records of 371 distinct species, comprising 232 mammals, 132 birds, and seven reptiles. The total trapping effort accumulated in this data paper consisted of 876,606 trap nights, distributed among Indonesia, Singapore, Malaysia, Bhutan, Thailand, Myanmar, Cambodia, Laos, Vietnam, Nepal, and far eastern India. The relatively standardized deployment methods in the region provide a consistent, reliable, and rich count data set relative to other large-scale pressence-only data sets, such as the Global Biodiversity Information Facility (GBIF) or citizen science repositories (e.g., iNaturalist), and is thus most similar to eBird. To facilitate the use of these data, we also provide mammalian species trait information and 13 environmental covariates calculated at three spatial scales around the camera survey centroids (within 10-, 20-, and 30-km buffers). We will update the dataset to include broader coverage of temperate Asia and add newer surveys and covariates as they become available. This dataset unlocks immense opportunities for single-species ecological or conservation studies as well as applied ecology, community ecology, and macroecology investigations. The data are fully available to the public for utilization and research. Please cite this data paper when utilizing the data.
Biodiversity continues to decline in the face of increasing anthropogenic pressures such as habitat destruction, exploitation, pollution and introduction of alien species. Existing global databases of species' threat status or population time series are dominated by charismatic species. The collation of datasets with broad taxonomic and biogeographic extents, and that support computation of a range of biodiversity indicators, is necessary to enable better understanding of historical declines and to project - and avert - future declines. We describe and assess a new database of more than 1.6 million samples from 78 countries representing over 28,000 species, collated from existing spatial comparisons of local-scale biodiversity exposed to different intensities and types of anthropogenic pressures, from terrestrial sites around the world. The database contains measurements taken in 208 (of 814) ecoregions, 13 (of 14) biomes, 25 (of 35) biodiversity hotspots and 16 (of 17) megadiverse countries. The database contains more than 1% of the total number of all species described, and more than 1% of the described species within many taxonomic groups - including flowering plants, gymnosperms, birds, mammals, reptiles, amphibians, beetles, lepidopterans and hymenopterans. The dataset, which is still being added to, is therefore already considerably larger and more representative than those used by previous quantitative models of biodiversity trends and responses. The database is being assembled as part of the PREDICTS project (Projecting Responses of Ecological Diversity In Changing Terrestrial Systems - http://www.predicts.org.uk). We make site-level summary data available alongside this article. The full database will be publicly available in 2015.
The PREDICTS project-Projecting Responses of Ecological Diversity In Changing Terrestrial Systems (www.predicts.org.uk)-has collated from published studies a large, reasonably representative database of comparable samples of biodiversity from multiple sites that differ in the nature or intensity of human impacts relating to land use. We have used this evidence base to develop global and regional statistical models of how local biodiversity responds to these measures. We describe and make freely available this 2016 release of the database, containing more than 3.2 million records sampled at over 26,000 locations and representing over 47,000 species. We outline how the database can help in answering a range of questions in ecology and conservation biology. To our knowledge, this is the largest and most geographically and taxonomically representative database of spatial comparisons of biodiversity that has been collated to date; it will be useful to researchers and international efforts wishing to model and understand the global status of biodiversity.