Effects of human disturbances on wildlife behaviour and consequences for predator-prey overlap in Southeast Asia.

Some animal species shift their activity towards increased nocturnality in disturbed habitats to avoid predominantly diurnal humans. This may alter diel overlap among species, a precondition to most predation and competition interactions that structure food webs. Here, using camera trap data from 10 tropical forest landscapes, we find that hyperdiverse Southeast Asian wildlife communities shift their peak activity from early mornings in intact habitats towards dawn and dusk in disturbed habitats (increased crepuscularity). Our results indicate that anthropogenic disturbances drive opposing behavioural adaptations based on rarity, size and feeding guild, with more nocturnality among the 59 rarer specialists' species, more diurnality for medium-sized generalists, and less diurnality for larger hunted species. Species turnover also played a role in underpinning community- and guild-level responses, with disturbances associated with markedly more detections of diurnal generalists and their medium-sized diurnal predators. However, overlap among predator-prey or competitor guilds does not vary with disturbance, suggesting that net species interactions may be conserved.

Landscape-scale benefits of protected areas for tropical biodiversity.

The United Nations recently agreed to major expansions of global protected areas (PAs) to slow biodiversity declines1. However, although reserves often reduce habitat loss, their efficacy at preserving animal diversity and their influence on biodiversity in surrounding unprotected areas remain unclear2-5. Unregulated hunting can empty PAs of large animals6, illegal tree felling can degrade habitat quality7, and parks can simply displace disturbances such as logging and hunting to unprotected areas of the landscape8 (a phenomenon called leakage). Alternatively, well-functioning PAs could enhance animal diversity within reserves as well as in nearby unprotected sites9 (an effect called spillover). Here we test whether PAs across mega-diverse Southeast Asia contribute to vertebrate conservation inside and outside their boundaries. Reserves increased all facets of bird diversity. Large reserves were also associated with substantially enhanced mammal diversity in the adjacent unprotected landscape. Rather than PAs generating leakage that deteriorated ecological conditions elsewhere, our results are consistent with PAs inducing spillover that benefits biodiversity in surrounding areas. These findings support the United Nations goal of achieving 30% PA coverage by 2030 by demonstrating that PAs are associated with higher vertebrate diversity both inside their boundaries and in the broader landscape.

The rise of hyperabundant native generalists threatens both humans and nature.

In many disturbed terrestrial landscapes, a subset of native generalist vertebrates thrives. The population trends of these disturbance-tolerant species may be driven by multiple factors, including habitat preferences, foraging opportunities (including crop raiding or human refuse), lower mortality when their predators are persecuted (the 'human shield' effect) and reduced competition due to declines of disturbance-sensitive species. A pronounced elevation in the abundance of disturbance-tolerant wildlife can drive numerous cascading impacts on food webs, biodiversity, vegetation structure and people in coupled human-natural systems. There is also concern for increased risk of zoonotic disease transfer to humans and domestic animals from wildlife species with high pathogen loads as their abundance and proximity to humans increases. Here we use field data from 58 landscapes to document a supra-regional phenomenon of the hyperabundance and community dominance of Southeast Asian wild pigs and macaques. These two groups were chosen as prime candidates capable of reaching hyperabundance as they are edge adapted, with gregarious social structure, omnivorous diets, rapid reproduction and high tolerance to human proximity. Compared to intact interior forests, population densities in degraded forests were 148% and 87% higher for wild boar and macaques, respectively. In landscapes with >60% oil palm coverage, wild boar and pig-tailed macaque estimated abundances were 337% and 447% higher than landscapes with <1% oil palm coverage, respectively, suggesting marked demographic benefits accrued by crop raiding on calorie-rich food subsidies. There was extreme community dominance in forest landscapes with >20% oil palm cover where two pig and two macaque species accounted for >80% of independent camera trap detections, leaving <20% for the other 85 mammal species >1 kg considered. Establishing the population trends of pigs and macaques is imperative since they are linked to cascading impacts on the fauna and flora of local forest ecosystems, disease and human health, and economics (i.e., crop losses). The severity of potential negative cascading effects may motivate control efforts to achieve ecosystem integrity, human health and conservation objectives. Our review concludes that the rise of native generalists can be mediated by specific types of degradation, which influences the ecology and conservation of natural areas, creating both positive and detrimental impacts on intact ecosystems and human society.

Inferring predator-prey interactions from camera traps: A Bayesian co-abundance modeling approach.

Predator-prey dynamics are a fundamental part of ecology, but directly studying interactions has proven difficult. The proliferation of camera trapping has enabled the collection of large datasets on wildlife, but researchers face hurdles inferring interactions from observational data. Recent advances in hierarchical co-abundance models infer species interactions while accounting for two species' detection probabilities, shared responses to environmental covariates, and propagate uncertainty throughout the entire modeling process. However, current approaches remain unsuitable for interacting species whose natural densities differ by an order of magnitude and have contrasting detection probabilities, such as predator-prey interactions, which introduce zero inflation and overdispersion in count histories. Here, we developed a Bayesian hierarchical N-mixture co-abundance model that is suitable for inferring predator-prey interactions. We accounted for excessive zeros in count histories using an informed zero-inflated Poisson distribution in the abundance formula and accounted for overdispersion in count histories by including a random effect per sampling unit and sampling occasion in the detection probability formula. We demonstrate that models with these modifications outperform alternative approaches, improve model goodness-of-fit, and overcome parameter convergence failures. We highlight its utility using 20 camera trapping datasets from 10 tropical forest landscapes in Southeast Asia and estimate four predator-prey relationships between tigers, clouded leopards, and muntjac and sambar deer. Tigers had a negative effect on muntjac abundance, providing support for top-down regulation, while clouded leopards had a positive effect on muntjac and sambar deer, likely driven by shared responses to unmodelled covariates like hunting. This Bayesian co-abundance modeling approach to quantify predator-prey relationships is widely applicable across species, ecosystems, and sampling approaches and may be useful in forecasting cascading impacts following widespread predator declines. Taken together, this approach facilitates a nuanced and mechanistic understanding of food-web ecology.

Megafauna extinctions produce idiosyncratic Anthropocene assemblages.

The "trophic downgrading of planet Earth" refers to the systematic decline of the world's largest vertebrates. However, our understanding of why megafauna extinction risk varies through time and the importance of site- or species-specific factors remain unclear. Here, we unravel the unexpected variability in remaining terrestrial megafauna assemblages across 10 Southeast Asian tropical forests. Consistent with global trends, every landscape experienced Holocene and/or Anthropocene megafauna extirpations, and the four most disturbed landscapes experienced 2.5 times more extirpations than the six least disturbed landscapes. However, there were no consistent size- or guild-related trends, no two tropical forests had identical assemblages, and the abundance of four species showed positive relationships with forest degradation and humans. Our results suggest that the region's megafauna assemblages are the product of a convoluted geoclimatic legacy interacting with modern disturbances and that some megafauna may persist in degraded tropical forests near settlements with sufficient poaching controls.

The ecology of the banded civet (Hemigalus derbyanus) in Southeast Asia with implications for mesopredator release, zoonotic diseases, and conservation.

Habitat loss and degradation threaten forest specialist wildlife species, but some generalist mesopredators exploit disturbed areas and human-derived food, which brings them into closer contact with humans. Mesopredator release is also important for human health for known zoonotic disease reservoirs, such as Asian civets (Viverridae family), since this group includes the intermediator species for the SARS-CoV-1 outbreak. Here we use camera trapping to evaluate the habitat associations of the widespread banded civet (Hemigalus derbyanus) across its range in Southeast Asia. At the regional scale, banded civet detections among published studies were positively associated with forest cover and negatively associated with human population. At the local scale (within a landscape), hierarchical modeling of new camera trapping showed that abundance was negatively associated with forest loss and positively associated with distance to rivers. These results do not support mesopredator release and suggest a low likelihood overlap with humans in degraded habitats and, therefore, a low risk of zoonotic disease transmission from this species in the wild. We also estimate that banded civet distribution has contracted to under 21% of its currently recognized IUCN Red List range, only 12% of which falls within protected areas, and a precipitous recent decline in population size. Accordingly, we suggest the banded civet's Red List status should be re-evaluated in light of our findings.

Common palm civets Paradoxurus hermaphroditus are positively associated with humans and forest degradation with implications for seed dispersal and zoonotic diseases.

Habitat loss and degradation can undermine wildlife communities and ecosystem functioning. However, certain generalist wildlife species like mesopredators and omnivores can exploit these disturbed habitats, sometimes leading to population increases (e.g. 'mesopredator release' in degraded areas). Although mesopredator release may cause negative effects on food webs and zoonotic disease management, some disturbance-tolerant species may help perpetuate important ecological interactions, such as seed dispersal. We evaluated the habitat associations of common palm civets Paradoxurus hermaphroditus, which are widespread generalist mesopredators in Southeast Asia. Common palm civets are also high-quality seed dispersers, and potential zoonotic disease hosts. We used published and new camera trapping data to map their probability of presence across Southeast Asia and evaluate regional-scale associations between capture rates and habitat variables such as elevation, ecoregion intactness and Human Footprint Index, among others. We also assessed the influence of habitat variables on their relative abundance at the local scale. At the regional scale, we found that common palm civets showed significant positive associations with landscapes characterized by lower ecoregion intactness, higher Human Footprint Index and lower elevations. At the local scale, their relative abundance showed a significant positive association with higher Human Footprint Index, but only to a certain point, after which it started decreasing. They also favoured lower elevations at the local scale. These multi-scale results indicate that common palm civets' abundance can increase under certain levels of human disturbances, consistent with the 'mesopredator release' hypothesis. This suggests they may be crucial seed dispersers in degraded forest landscapes, especially where more sensitive seed dispersers have disappeared. Our results are also consistent with previous studies reporting that habitat degradation increases populations of potential zoonotic disease hosts, and thus risks of transmission to humans.

Fungi and insects compensate for lost vertebrate seed predation in an experimentally defaunated tropical forest.

Overhunting reduces important plant-animal interactions such as vertebrate seed dispersal and seed predation, thereby altering plant regeneration and even above-ground biomass. It remains unclear, however, if non-hunted species can compensate for lost vertebrates in defaunated ecosystems. We use a nested exclusion experiment to isolate the effects of different seed enemies in a Bornean rainforest. In four of five tree species, vertebrates kill many seeds (13-66%). Nonetheless, when large mammals are excluded, seed mortality from insects and fungi fully compensates for the lost vertebrate predation, such that defaunation has no effect on seedling establishment. The switch from seed predation by generalist vertebrates to specialist insects and fungi in defaunated systems may alter Janzen-Connell effects and density-dependence in plants. Previous work using simulation models to explore how lost seed dispersal will affect tree species composition and carbon storage may require reevaluation in the context of functional redundancy within complex species interactions networks.

Wildlife disturbances as a source of conspecific negative density-dependent mortality in tropical trees.

Large vertebrates are rarely considered important drivers of conspecific negative density-dependent mortality (CNDD) in plants because they are generalist consumers. However, disturbances like trampling and nesting also cause plant mortality, and their impact on plant diversity depends on the spatial overlap between wildlife habitat preferences and plant species composition. We studied the impact of native wildlife on a hyperdiverse tree community in Malaysia. Pigs (Sus scrofa) are abnormally abundant at the site due to food subsidies in nearby farmland and they construct birthing nests using hundreds of tree saplings. We tagged 34 950 tree saplings in a 25 ha plot during an initial census and assessed the source mortality by recovering tree tags from pig nests (n = 1672 pig-induced deaths). At the stand scale, pigs nested in flat dry habitats, and at the local neighbourhood scale, they nested within clumps of saplings, both of which are intuitive for safe and efficient nest building. At the stand scale, flat dry habitats contained higher sapling densities and higher proportions of common species, so pig nesting increased the weighted average species evenness across habitats. At the neighbourhood scale, pig-induced sapling mortality was associated with higher heterospecific and especially conspecific sapling densities. Tree species have clumped distributions due to dispersal limitation and habitat filtering, so pig disturbances in sapling clumps indirectly caused CNDD. As a result, Pielou species evenness in 400 m2 quadrats increased 105% more in areas with pig-induced deaths than areas without disturbances. Wildlife induced CNDD and this supported tree species evenness, but they also drove a 62% decline in sapling densities from 1996 to 2010, which is unsustainable. We suspect pig nesting is an important feature shaping tree composition throughout the region.

When do Janzen-Connell effects matter? A phylogenetic meta-analysis of conspecific negative distance and density dependence experiments.

The Janzen-Connell (J-C) hypothesis suggests that specialised natural enemies cause distance- or density-dependent mortality among host plants and is regarded as an important mechanism for species coexistence. However, there remains debate about whether this phenomenon is widespread and how variation is structured across taxa and life stages. We performed the largest meta-analysis of experimental studies conducted under natural settings to date. We found little evidence of distance-dependent or density-dependent mortality when grouping all types of manipulations. Our analysis also reveals very large variation in response among species, with 38.5% of species even showing positive responses to manipulations. However, we found a strong signal of distance-dependent mortality among seedlings but not seed experiments, which we attribute to (a) seedlings sharing susceptible tissues with adults (leaves, wood, roots), (b) seedling enemies having worse dispersal than seed enemies and (c) seedlings having fewer physical and chemical defences than seeds. Both density- and distance-dependent mortality showed large variation within genera and families, suggesting that J-C effects are not strongly phylogenetically conserved. There were no clear trends with latitude, rainfall or study duration. We conclude that J-C effects may not be as pervasive as widely thought. Understanding the variation in J-C effects provides opportunities for new discoveries that will refine our understanding of J-C effects and its role in species coexistence.

Global signal of top-down control of terrestrial plant communities by herbivores.

The theory of "top-down" ecological regulation predicts that herbivory suppresses plant abundance, biomass, and survival but increases diversity through the disproportionate consumption of dominant species, which inhibits competitive exclusion. To date, these outcomes have been clear in aquatic ecosystems but not on land. We explicate this discrepancy using a meta-analysis of experimental results from 123 native animal exclusions in natural terrestrial ecosystems (623 pairwise comparisons). Consistent with top-down predictions, we found that herbivores significantly reduced plant abundance, biomass, survival, and reproduction (all P < 0.01) and increased species evenness but not richness (P = 0.06 and P = 0.59, respectively). However, when examining patterns in the strength of top-down effects, with few exceptions, we were unable to detect significantly different effect sizes among biomes, based on local site characteristics (climate or productivity) or study characteristics (study duration or exclosure size). The positive effects on diversity were only significant in studies excluding large animals or located in temperate grasslands. The results demonstrate that top-down regulation by herbivores is a pervasive process shaping terrestrial plant communities at the global scale, but its strength is highly site specific and not predicted by basic site conditions. We suggest that including herbivore densities as a covariate in future exclosure studies will facilitate the discovery of unresolved macroecology trends in the strength of herbivore-plant interactions.

Publisher Correction: Sumatran tiger survival threatened by deforestation despite increasing densities in parks.

In the original version of the Article, reference 18 was incorrectly numbered as reference 30, and references 19 to 30 were incorrectly numbered as 18 to 29. These errors have now been corrected in the PDF and HTML versions of the manuscript.

Sumatran tiger survival threatened by deforestation despite increasing densities in parks.

The continuing development of improved capture-recapture (CR) modeling techniques used to study apex predators has also limited robust temporal and cross-site analyses due to different methods employed. We develop an approach to standardize older non-spatial CR and newer spatial CR density estimates and examine trends for critically endangered Sumatran tigers (Panthera tigris sumatrae) using a meta-regression of 17 existing densities and new estimates from our own fieldwork. We find that tiger densities were 47% higher in primary versus degraded forests and, unexpectedly, increased 4.9% per yr from 1996 to 2014, likely indicating a recovery from earlier poaching. However, while tiger numbers may have temporarily risen, the total potential island-wide population declined by 16.6% from 2000 to 2012 due to forest loss and degradation and subpopulations are significantly more fragmented. Thus, despite increasing densities in smaller parks, we conclude that there are only two robust populations left with >30 breeding females, indicating Sumatran tigers still face a high risk of extinction unless deforestation can be controlled.

Cross-boundary subsidy cascades from oil palm degrade distant tropical forests.

Native species that forage in farmland may increase their local abundances thereby affecting adjacent ecosystems within their landscape. We used two decades of ecological data from a protected primary rainforest in Malaysia to illutrate how subsidies from neighboring oil palm plantations triggered powerful secondary 'cascading' effects on natural habitats located >1.3 km away. We found (i) oil palm fruit drove 100-fold increases in crop-raiding native wild boar (Sus scrofa), (ii) wild boar used thousands of understory plants to construct birthing nests in the pristine forest interior, and (iii) nest building caused a 62% decline in forest tree sapling density over the 24-year study period. The long-term, landscape-scale indirect effects from agriculture suggest its full ecological footprint may be larger in extent than is currently recognized. Cross-boundary subsidy cascades may be widespread in both terrestrial and marine ecosystems and present significant conservation challenges.