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.

Crop and landscape heterogeneity increase biodiversity in agricultural landscapes: A global review and meta-analysis.

Agricultural intensification not only increases food production but also drives widespread biodiversity decline. Increasing landscape heterogeneity has been suggested to increase biodiversity across habitats, while increasing crop heterogeneity may support biodiversity within agroecosystems. These spatial heterogeneity effects can be partitioned into compositional (land-cover type diversity) and configurational heterogeneity (land-cover type arrangement), measured either for the crop mosaic or across the landscape for both crops and semi-natural habitats. However, studies have reported mixed responses of biodiversity to increases in these heterogeneity components across taxa and contexts. Our meta-analysis covering 6397 fields across 122 studies conducted in Asia, Europe, North and South America reveals consistently positive effects of crop and landscape heterogeneity, as well as compositional and configurational heterogeneity for plant, invertebrate, vertebrate, pollinator and predator biodiversity. Vertebrates and plants benefit more from landscape heterogeneity, while invertebrates derive similar benefits from both crop and landscape heterogeneity. Pollinators benefit more from configurational heterogeneity, but predators favour compositional heterogeneity. These positive effects are consistent for invertebrates and vertebrates in both tropical/subtropical and temperate agroecosystems, and in annual and perennial cropping systems, and at small to large spatial scales. Our results suggest that promoting increased landscape heterogeneity by diversifying crops and semi-natural habitats, as suggested in the current UN Decade on Ecosystem Restoration, is key for restoring biodiversity in agricultural landscapes.

Isopod mouthpart traits respond to a tropical forest recovery gradient.

Functional trait ecology has the potential to provide generalizable and mechanistic predictions of ecosystem function from data of species distributions and traits. The traits that are selected should both respond to environmental factors and influence ecosystem functioning. Invertebrate mouthpart traits fulfill these criteria, but are seldom collected, lack standardized measurement protocols, and have infrequently been investigated in response to environmental factors. We surveyed isopod species that consume plant detritus, and tree communities in 58 plots across primary and secondary forests in Singapore. We measured body dimensions (body size traits), pereopod and antennae lengths (locomotory traits), dimensions of mandible structures (morphological mouthpart traits), and mechanical advantages generated by mandible shape (mechanical mouthpart traits) for six isopod species found in these plots and investigated if these traits respond to changes in tree community composition, tree diversity, and forest structure. Morphological mouthpart traits responded to a tree compositional gradient reflecting forest recovery degree. Mouthpart features associated with greater consumption of litter (broader but less serrated/rugose lacinia mobilis [an important cutting and chewing structure on the mandible]) were most prevalent in abandoned plantation and young secondary forests containing disturbance-associated tree species. Feeding strategies associated with fungi grazing (narrower and more serrated/rugose lacinia mobilis) were most prevalent in late secondary forests containing later successional tree species. Since morphological mouthpart traits likely also predict consumption and excretion rates of isopods, these traits advance our understanding of environment-trait-ecosystem functioning relationships across contrasting tropical forest plots that vary in composition, disturbance history, and post-disturbance recovery.

A meta-analysis reveals that dragonflies and damselflies can provide effective biological control of mosquitoes.

Dragonfly/damselfly naiads have the potential to control mosquitoes, and indirectly the diseases they carry, due to their extensive predation on mosquito larvae. Experimental studies have measured the effectiveness of individual dragonfly/damselfly naiads in controlling mosquitoes by introducing them to mosquito larvae and counting the number of larvae eaten in a given time period (i.e. predation success). Without a quantitative synthesis, however, such individual measures are unable to provide a generalized estimation about the effectiveness of dragonflies/damselflies as biological mosquito control agents. To achieve this, we assembled a database containing 485 effect sizes across 31 studies on predation successes of 47 species of commonly found dragonfly/damselfly naiads on nine species of mosquito larvae belonging to Aedes, Anopheles and Culex. These studies covered 14 countries across Asia, Africa and South and North America, where mosquitoes are the vectors of Chikungunya, Dengue, Japanese encephalitis, Lymphatic filariasis, Malaria, Rift Valley fever, West Nile fever, Yellow fever and Zika. Using this database, we conducted a meta-analysis to estimate the average predation success per day by a single individual dragonfly/damselfly naiad on these mosquito larvae as a generalized measure of the effectiveness of dragonflies/damselflies for mosquito control. We also built an interaction network for predator-dragonflies/damselflies and prey-mosquitoes and the diseases they vector to understand the functioning of this important predator-prey network. Our results showed that mosquito larvae were significantly reduced through predation by dragonfly/damselfly naiads. Within experimental containers, a single individual dragonfly/damselfly naiad can eat on average 40 (95% confidence intervals [CIs] = 20, 60) mosquito larvae per day, equivalent to a reduction of the mosquito larval population by 45% (95% CIs = 30%, 59%) per day. The average predation success did not significantly vary among Aedes, Anopheles and Culex mosquitoes or among the four (I-IV) mosquito larval stages. These results provide strong evidence that dragonflies/damselflies can be effective biological control agents of mosquitoes, and environmental planning to promote them could lower the risk of spreading mosquito-borne diseases in an environmentally friendly and cost-effective manner.

A trait-based framework for dung beetle functional ecology.

Traits are key for understanding the environmental responses and ecological roles of organisms. Trait approaches to functional ecology are well established for plants, whereas consistent frameworks for animal groups are less developed. Here we suggest a framework for the study of the functional ecology of animals from a trait-based response-effect approach, using dung beetles as model system. Dung beetles are a key group of decomposers that are important for many ecosystem processes. The lack of a trait-based framework tailored to this group has limited the use of traits in dung beetle functional ecology. We review which dung beetle traits respond to the environment and affect ecosystem processes, covering the wide range of spatial, temporal and biological scales at which they are involved. Dung beetles show trait-based responses to variation in temperature, water, soil properties, trophic resources, light, vegetation structure, competition, predation and parasitism. Dung beetles' influence on ecosystem processes includes trait-mediated effects on nutrient cycling, bioturbation, plant growth, seed dispersal, other dung-based organisms and parasite transmission, as well as some cases of pollination and predation. We identify 66 dung beetle traits that are either response or effect traits, or both, pertaining to six main categories: morphology, feeding, reproduction, physiology, activity and movement. Several traits pertain to more than one category, in particular dung relocation behaviour during nesting or feeding. We also identify 136 trait-response and 77 trait-effect relationships in dung beetles. No response to environmental stressors nor effect over ecological processes were related with traits of a single category. This highlights the interrelationship between the traits shaping body-plans, the multi-functionality of traits, and their role linking responses to the environment and effects on the ecosystem. Despite current developments in dung beetle functional ecology, many knowledge gaps remain, and there are biases towards certain traits, functions, taxonomic groups and regions. Our framework provides the foundations for the thorough development of trait-based dung beetle ecology. It also serves as an example framework for other taxa.

Tropical forest dung beetle-mammal dung interaction networks remain similar across an environmental disturbance gradient.

Conservation outcomes could be greatly enhanced if strategies addressing anthropogenic land-use change considered the impacts of these changes on entire communities as well as on individual species. Examining how species interactions change across gradients of habitat disturbance allows us to predict the cascading consequences of species extinctions and the response of ecological networks to environmental change. We conducted the first detailed study of changes in a commensalist network of mammals and dung beetles across an environmental disturbance gradient, from primary tropical forest to plantations, which varied in above-ground carbon density (ACD) and mammal communities. Mammal diversity changed only slightly across the gradient, remaining high even in oil palm plantations and fragmented forest. Dung beetle species richness, however, declined in response to lower ACD and was particularly low in plantations and the most disturbed forest sites. Three of the five network metrics (nestedness, network specialization and functionality) were significantly affected by changes in dung beetle species richness and ACD, but mammal diversity was not an important predictor of network structure. Overall, the interaction networks remained structurally and functionally similar across the gradient, only becoming simplified (i.e. with fewer dung beetle species and fewer interactions) in the most disturbed sites. We suggest that the high diversity of mammals, even in disturbed forests, combined with the generalist feeding patterns of dung beetles, confer resilience to the commensalist dung beetle-mammal networks. This study highlights the importance of protecting logged and fragmented forests to maintain interaction networks and potentially prevent extinction cascades in human-modified systems.

Leech blood-meal invertebrate-derived DNA reveals differences in Bornean mammal diversity across habitats.

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.

Support for the habitat amount hypothesis from a global synthesis of species density studies.

Decades of research suggest that species richness depends on spatial characteristics of habitat patches, especially their size and isolation. In contrast, the habitat amount hypothesis predicts that (1) species richness in plots of fixed size (species density) is more strongly and positively related to the amount of habitat around the plot than to patch size or isolation; (2) habitat amount better predicts species density than patch size and isolation combined, (3) there is no effect of habitat fragmentation per se on species density and (4) patch size and isolation effects do not become stronger with declining habitat amount. Data on eight taxonomic groups from 35 studies around the world support these predictions. Conserving species density requires minimising habitat loss, irrespective of the configuration of the patches in which that habitat is contained.

Sexual selection predicts the persistence of populations within altered environments.

The effect of sexual selection on species persistence remains unclear. The cost of bearing ornaments or armaments might increase extinction risk, but sexual selection can also enhance the spread of beneficial alleles and increase the removal of deleterious alleles, potentially reducing extinction risk. Here we investigate the effect of sexual selection on species persistence in a community of 34 species of dung beetles across a gradient of environmental disturbance ranging from old growth forest to oil palm plantation. Horns are sexually selected traits used in contests between males, and we find that both horn presence and relative size are strongly positively associated with species persistence and abundance in altered habitats. Testes mass, an indicator of post-copulatory selection, is, however, negatively linked with the abundance of species within the most disturbed habitats. This study represents the first evidence from a field system of a population-level benefit from pre-copulatory sexual selection.

Dung beetle-mammal associations: methods, research trends and future directions.

Dung beetles are increasingly used as a study taxon-both as bioindicators of environmental change, and as a model system for exploring ecosystem functioning. The advantages of this focal taxon approach are many; dung beetles are abundant in a wide range of terrestrial ecosystems, speciose, straightforward to sample, respond to environmental gradients and can be easily manipulated to explore species-functioning relationships. However, there remain large gaps in our understanding of the relationship between dung beetles and the mammals they rely on for dung. Here we review the literature, showing that despite an increase in the study of dung beetles linked to ecosystem functioning and to habitat and land use change, there has been little research into their associations with mammals. We summarize the methods and findings from dung beetle-mammal association studies to date, revealing that although empirical field studies of dung beetles rarely include mammal data, those that do, indicate mammal species presence and composition has a large impact on dung beetle species richness and abundance. We then review the methods used to carry out diet preference and ecosystem functioning studies, finding that despite the assumption that dung beetles are generalist feeders, there are few quantitative studies that directly address this. Together this suggests that conclusions about the effects of habitat change on dung beetles are based on incomplete knowledge. We provide recommendations for future work to identify the importance of considering mammal data for dung beetle distributions, composition and their contributions to ecosystem functioning; a critical step if dung beetles are to be used as a reliable bioindicator taxon.

Global dung webs: high trophic generalism of dung beetles along the latitudinal diversity gradient.

At the global scale, species diversity is known to strongly increase towards the equator for most taxa. According to theory, a higher resource specificity of consumers facilitates the coexistence of a larger number of species and has been suggested as an explanation for the latitudinal diversity gradient. However, only few studies support the predicted increase in specialisation or even showed opposite results. Surprisingly, analyses for detritivores are still missing. Therefore, we performed an analysis on the degree of trophic specialisation of dung beetles. We summarised 45 studies, covering the resource preferences of a total of 994503 individuals, to calculate the dung specificity in each study region. Our results highlighted a significant (4.3-fold) increase in the diversity of beetles attracted to vertebrate dung towards the equator. However, their resource specificity was low, unrelated to diversity and revealed a highly generalistic use of dung resources that remained similar along the latitudinal gradient.

The importance of species identity and interactions for multifunctionality depends on how ecosystem functions are valued.

Studies investigating how biodiversity affects ecosystem functioning increasingly focus on multiple functions measured simultaneously ("multifunctionality"). However, few such studies assess the role of species interactions, particularly under alternative environmental scenarios, despite interactions being key to ecosystem functioning. Here we address five questions of central importance to ecosystem multifunctionality using a terrestrial animal system. (1) Does the contribution of individual species differ for different ecosystem functions? (2) Do inter-species interactions affect the delivery of single functions and multiple functions? (3) Does the community composition that maximizes individual functions also maximize multifunctionality? (4) Is the functional role of individual species, and the effect of interspecific interactions, modified by changing environmental conditions? (5) How do these roles and interactions change under varying scenarios where ecosystem services are weighted to reflect different societal preferences? We manipulated species' relative abundance in dung beetle communities and measured 16 functions contributing to dung decomposition, plant productivity, nutrient recycling, reduction of greenhouse gases, and microbial activity. Using the multivariate diversity-interactions framework, we assessed how changes in species identity, composition, and interspecific interactions affected these functions in combination with an environmental driver (increased precipitation). This allowed us to identify key species and interactions across multiple functions. We then developed a desirability function approach to examine how individual species and species mixtures contribute to a desired state of overall ecosystem functioning. Species contributed unequally to individual functions, and to multifunctionality, and individual functions were maximized by different community compositions. Moreover, the species and interactions important for maintaining overall multifunctionality depended on the weight given to individual functions. Optimal multifunctionality was context-dependent, and sensitive to the valuation of services. This combination of methodological approaches allowed us to resolve the interactions and indirect effects among species that drive ecosystem functioning, revealing how multiple aspects of biodiversity can simultaneously drive ecosystem functioning. Our results highlight the importance of a multifunctionality perspective for a complete assessment of species' functional contributions.

Long-term crop residue application maintains oil palm yield and temporal stability of production.

Crop residue management is an important agricultural practice that has a high potential to improve soil health and optimize crop production. Compared to annual crops, relatively little is known about crop residue management effects on the yield and temporal stability of perennial crop production. This study focused on oil palm (Elaeis guineensis), an important tropical crop that had expanded rapidly over the past decades. We aimed to understand the effects of applying a major oil palm residue, the empty fruit bunch, on crop yield and temporal stability of production. We compared 15 years of crop yield performance from a field trial in Sumatra, Indonesia. The treatments included empty fruit bunch application of three application rates (30, 60, and 90 t ha-1 year-1), and a reference treatment of chemical fertilizers with no addition of empty fruit bunch. Compared to the reference treatment, the cumulative crop yield over 15 years under low, medium, and high application rates of empty fruit bunch increased by 2.4, 5.9, and 4.8%, respectively. The annual crop yield and temporal stability in production were not significantly different between treatments. Soil organic carbon was significantly higher under medium application rate of empty fruit bunch compared to that under the chemical fertilizer treatment. Soil organic carbon and relative humidity were positively associated with annual crop yield with a time lag of 2 years. This study is the first to show that both crop yield and temporal variability of oil palm production can be maintained under crop residue application, compared to chemical fertilizer treatment. Furthermore, climatic conditions had strong effects on the temporal variability of oil palm production. These findings will inform the design of optimal empty fruit bunch application schemes that enhance sustainable intensification of oil palm cultivation.

Functional identity and diversity of animals predict ecosystem functioning better than species-based indices.

Drastic biodiversity declines have raised concerns about the deterioration of ecosystem functions and have motivated much recent research on the relationship between species diversity and ecosystem functioning. A functional trait framework has been proposed to improve the mechanistic understanding of this relationship, but this has rarely been tested for organisms other than plants. We analysed eight datasets, including five animal groups, to examine how well a trait-based approach, compared with a more traditional taxonomic approach, predicts seven ecosystem functions below- and above-ground. Trait-based indices consistently provided greater explanatory power than species richness or abundance. The frequency distributions of single or multiple traits in the community were the best predictors of ecosystem functioning. This implies that the ecosystem functions we investigated were underpinned by the combination of trait identities (i.e. single-trait indices) and trait complementarity (i.e. multi-trait indices) in the communities. Our study provides new insights into the general mechanisms that link biodiversity to ecosystem functioning in natural animal communities and suggests that the observed responses were due to the identity and dominance patterns of the trait composition rather than the number or abundance of species per se.

Small-Mammal Genomics Highlights Viaducts as Potential Dispersal Conduits for Fragmented Populations.

Wildlife crossings are implemented in many countries to facilitate the dispersal of animals among habitats fragmented by roads. However, the efficacy of different types of habitat corridors remains poorly understood. We used a comprehensive sampling regime in two lowland dipterocarp forest areas in peninsular Malaysia to sample pairs of small mammal individuals in three treatment types: (1) viaduct sites, at which sampling locations were separated by a highway but connected by a vegetated viaduct; (2) non-viaduct sites, at which sampling locations were separated by a highway and not connected by a viaduct; and (3) control sites, at which there was no highway fragmenting the forest. For four small mammal species, the common tree shrew Tupaia glis, Rajah's spiny rat Maxomys rajah, Whitehead's spiny rat Maxomys whiteheadi and dark-tailed tree rat Niviventer cremoriventer, we used genome-wide markers to assess genetic diversity, gene flow and genetic structure. The differences in genetic distance across sampling settings among the four species indicate that they respond differently to the presence of highways and viaducts. Viaducts connecting forests separated by highways appear to maintain higher population connectivity than forest fragments without viaducts, at least in M. whiteheadi, but apparently not in the other species.

Life-history traits and landscape characteristics predict macro-moth responses to forest fragmentation.

How best to manage forest patches, mitigate the consequences of forest fragmentation, and enable landscape permeability are key questions facing conservation scientists and managers. Many temperate forests have become increasingly fragmented, resulting in reduced interior forest habitat, increased edge habitats, and reduced connectivity. Using a citizen science landscape-scale mark-release-recapture study on 87 macro-moth species, we investigated how both life-history traits and landscape characteristics predicted macro-moth responses to forest fragmentation. Wingspan, wing shape, adult feeding, and larval feeding guild predicted macro-moth mobility, although the predictive power of wingspan and wing shape depended on the species' affinity to the forest. Solitary trees and small fragments functioned as "stepping stones," especially when their landscape connectivity was increased, by being positioned within hedgerows or within a favorable matrix. Mobile forest specialists were most affected by forest fragmentation: despite their high intrinsic dispersal capability, these species were confined mostly to the largest of the forest patches due to their strong affinity for the forest habitat, and were also heavily dependent on forest connectivity in order to cross the agricultural matrix. Forest fragments need to be larger than five hectares and to have interior forest more than 100 m from the edge in order to sustain populations of forest specialists. Our study provides new insights into the movement patterns of a functionally important insect group, with implications for the landscape-scale management of forest patches within agricultural landscapes.

Trait-dependent response of dung beetle populations to tropical forest conversion at local and regional scales.

Comparative analyses that link information on species' traits, environmental change, and organism response have rarely identified unambiguous trait correlates of vulnerability. We tested if species' traits could predict local-scale changes in dung beetle population response to three levels of forest conversion intensity within and across two biogeographic regions (the Neotropics and Afro-Eurasian tropics). We combined biodiversity surveys, a global molecular phylogeny, and information on three species' traits hypothesized to influence vulnerability to forest conversion to examine (1) the consistency of beetle population response across regions, (2) if species' traits could predict this response, and (3) the cross-regional consistency of trait-response relationships. Most beetle populations declined following any degree of forest conversion; these declines were strongest for Neotropical species. The relationship between traits and population trend was greatly influenced by local and biogeographic context. We discuss the ability of species' traits to explain population trends and suggest several ways to strengthen trait-response models.