Global hotspots of traded phylogenetic and functional diversity.

Wildlife trade is a multibillion-dollar industry1 targeting a hyperdiversity of species2 and can contribute to major declines in abundance3. A key question is understanding the global hotspots of wildlife trade for phylogenetic (PD) and functional (FD) diversity, which underpin the conservation of evolutionary history4, ecological functions5 and ecosystem services benefiting humankind6. Using a global dataset of traded bird and mammal species, we identify that the highest levels of traded PD and FD are from tropical regions, where high numbers of evolutionary distinct and globally endangered species in trade occur. The standardized effect size (ses) of traded PD and FD also shows strong tropical epicentres, with additional hotspots of mammalian ses.PD in the eastern United States and ses.FD in Europe. Large-bodied, frugivorous and canopy-dwelling birds and large-bodied mammals are more likely to be traded whereas insectivorous birds and diurnally foraging mammals are less likely. Where trade drives localized extinctions3, our results suggest substantial losses of unique evolutionary lineages and functional traits, with possible cascading effects for communities and ecosystems5,7. Avoiding unsustainable exploitation and lost community integrity requires targeted conservation efforts, especially in hotspots of traded phylogenetic and functional diversity.

High sensitivity of tropical forest birds to deforestation at lower altitudes.

Habitat conversion is a major driver of tropical biodiversity loss, but its effects are poorly understood in montane environments. While community-level responses to habitat loss display strong elevational dependencies, it is unclear whether these arise via elevational turnover in community composition and interspecific differences in sensitivity or elevational variation in environmental conditions and proximity to thermal thresholds. Here we assess the relative importance of inter- and intraspecific variation across the elevational gradient by quantifying how 243 forest-dependent bird species vary in sensitivity to landscape-scale forest loss across a 3000-m elevational gradient in the Colombian Andes. We find that species that live at lower elevations are strongly affected by loss of forest in the nearby landscape, while those at higher elevations appear relatively unperturbed, an effect that is independent of phylogeny. Conversely, we find limited evidence of intraspecific elevational gradients in sensitivity, with populations displaying similar sensitivities to forest loss, regardless of where they exist in a species' elevational range. Gradients in biodiversity response to habitat loss thus appear to arise via interspecific gradients in sensitivity rather than proximity to climatically limiting conditions.

Tropical land-use change alters trait-based community assembly rules for dung beetles and birds.

Tropical rainforest disturbance and conversion are critical drivers of biodiversity loss. A key knowledge gap is understanding the impacts of habitat modification on mechanisms of community assembly, which are predicted to respond differently between taxa and across spatial scales. We use a null model approach to detect trait assembly of species at local- and landscape-scales, and then subdivide communities with different habitat associations and foraging guilds to investigate whether the detection of assembly mechanisms varies between groups. We focus on two indicator taxa, dung beetles and birds, across a disturbance gradient of primary rainforest, selectively logged rainforest, and oil palm plantations in Borneo, Southeast Asia. Random community assembly was predominant for dung beetles across habitats, whereas trait convergence, indicative of environmental filtering, occurred across the disturbance gradient for birds. Assembly patterns at the two spatial scales were similar. Subdividing for habitat association and foraging guild revealed patterns hidden when focusing on the overall community. Dung beetle forest specialists and habitat generalists showed opposing assembly mechanisms in primary forest, community assembly of habitat generalists for both taxa differed with disturbance intensity, and insectivorous birds strongly influenced overall community assembly relative to other guilds. Our study reveals the sensitivity of community assembly mechanisms to anthropogenic disturbance via a shift in the relative contribution of stochastic and deterministic processes. This highlights the need for greater understanding of how habitat modification alters species interactions and the importance of incorporating species' traits within assessments.

Replacing low-intensity cattle pasture with oil palm conserves dung beetle functional diversity when paired with forest protection.

Meeting rising demand for oil palm whilst minimizing the loss of tropical biodiversity and associated ecosystem functions is a core conservation challenge. One potential solution is focusing the expansion of high-yielding crops on presently low-yielding farmlands alongside protecting nearby tropical forests that can enhance provision of ecosystem functions. A key question is how this solution would impact invertebrate functional diversity. We focus on oil palm in the Colombian Llanos, where plantations are replacing improved cattle pastures and forest fragments, and on dung beetles, which play key functional roles in nutrient cycling and secondary seed dispersal. We show that functional richness and functional diversity of dung beetles is greater in oil palm than in cattle pasture, and that functional metrics did not differ between oil palm and remnant forest. The abundance-size class profile of dung beetles in oil palm was more similar to forest than to pasture, which had lower abundances of the smallest and largest dung beetles. The abundance of tunneling and rolling dung beetles did not differ between oil palm and forest, while higher forest cover increased the abundance of diurnal and generalist-feeding beetles in oil palm landscapes. This suggests that prioritizing agricultural development on low-yielding cattle pasture will have positive effects on functional diversity and highlights the need for forest protection to maintain ecosystem functioning within agricultural landscapes.

Sparing land for secondary forest regeneration protects more tropical biodiversity than land sharing in cattle farming landscapes.

Effectively managing farming to meet food demand is vital for the future of biodiversity.1,2 Increasing yields on existing farmland can allow the abandonment (sparing) of low-yielding areas that subsequently recover as secondary forest.2-5 A key question is whether such "secondary sparing" conserves biodiversity more effectively than retaining wildlife-friendly habitat within farmland ("land sharing"). Focusing on the Colombian Choco-Andes, a global hotspot of threatened biodiversity,6 and on cattle farming, we examined the outcomes of secondary sparing and land sharing via simulated scenarios that maintained constant landscape-wide production and equal within-pasture yield: (1) for species and functional diversity of dung beetles and birds; (2) for avian phylogenetic diversity; and (3) across different stages of secondary forest regeneration, relative to spared primary forests. Sparing older secondary forests (15-30 years recovery) promotes substantial species, functional, and phylogenetic (birds only) diversity benefits for birds and dung beetles compared to land sharing. Species of conservation concern had higher occupancy estimates under land-sparing compared to land-sharing scenarios. Spared secondary forests accumulated equivalent diversity to primary forests for dung beetles within 15 years and within 15-30 years for birds, highlighting the need for longer term protection to maximize the biodiversity gains of secondary sparing. Promoting the recovery and protection of large expanses of secondary forests under the land-sparing model provides a critical mechanism for protecting tropical biodiversity, with important implications for concurrently assisting in the delivery of global targets to restore 350 million hectares of forested landscapes.7,8.

Secondary forest fragments offer important carbon and biodiversity cobenefits.

Tropical forests store large amounts of carbon and high biodiversity, but are being degraded at alarming rates. The emerging global Forest and Landscape Restoration (FLR) agenda seeks to limit global climate change by removing carbon dioxide from the atmosphere through the growth of trees. In doing so, it may also protect biodiversity as a free cobenefit, which is vital given the massive shortfall in funding for biodiversity conservation. We investigated whether natural forest regeneration on abandoned pastureland offers such cobenefits, focusing for the first time on the recovery of taxonomic diversity (TD), phylogenetic diversity (PD) and functional diversity (FD) of trees, including the recovery of threatened and endemic species richness, within isolated secondary forest (SF) fragments. We focused on the globally threatened Brazilian Atlantic Forest, where commitments have been made to restore 1 million hectares under FLR. Three decades after land abandonment, regenerating forests had recovered ~20% (72 Mg/ha) of the above-ground carbon stocks of a primary forest (PF), with cattle pasture containing just 3% of stocks relative to PFs. Over this period, SF recovered ~76% of TD, 84% of PD and 96% of FD found within PFs. In addition, SFs had on average recovered 65% of threatened and ~30% of endemic species richness of primary Atlantic forest. Finally, we find positive relationships between carbon stock and tree diversity recovery. Our results emphasize that SF fragments offer cobenefits under FLR and other carbon-based payments for ecosystem service schemes (e.g. carbon enhancements under REDD+). They also indicate that even isolated patches of SF could help to mitigate climate change and the biodiversity extinction crisis by recovering species of high conservation concern and improving landscape connectivity.

The impact of secondary forest regeneration on ground-dwelling ant communities in the Tropical Andes.

Natural regeneration of abandoned farmland provides an important opportunity to contribute to global reforestation targets, including the Bonn Challenge. Of particular importance are the montane tropics, where a long history of farming, frequently on marginal soils, has rendered many ecosystems highly degraded and hotspots of extinction risk. Ants play crucial roles in ecosystem functioning, and a key question is how time since abandonment and elevation (and inherent temperature gradients therein) affect patterns of ant recovery within secondary forest systems. Focusing on the Colombian Andes across a 1300 m altitudinal gradient and secondary forest (2-30 years) recovering on abandoned cattle pastures, we find that over time ant community composition and species richness recovered towards that of primary forest. However, these relationships are strongly dependent on elevation with the more open and warmer pasturelands supporting more ants than either primary or secondary forest at a particular elevation. The loss of species richness and change in species composition with elevation is less severe in pasture than forests, suggesting that conditions within pasture and its remaining scattered trees, hedgerows and forest fragments, are more favourable for some species, which are likely in or near thermal debt. Promoting and protecting natural regenerating forests over the long term in the montane tropics will likely offer significant potential for returning ant communities towards primary forest levels.

The impact of logging roads on dung beetle assemblages in a tropical rainforest reserve.

The demand for timber products is facilitating the degradation and opening up of large areas of intact habitats rich in biodiversity. Logging creates an extensive network of access roads within the forest, yet these are commonly ignored or excluded when assessing impacts of logging on forest biodiversity. Here we determine the impact of these roads on the overall condition of selectively logged forests in Borneo, Southeast Asia. Focusing on dung beetles along > 40 km logging roads we determine: (i) the magnitude and extent of edge effects alongside logging roads; (ii) whether vegetation characteristics can explain patterns in dung beetle communities, and; (iii) how the inclusion of road edge forest impacts dung beetle assemblages within the overall logged landscape. We found that while vegetation structure was significantly affected up to 34 m from the road edge, impacts on dung beetle communities penetrated much further and were discernible up to 170 m into the forest interior. We found larger species and particularly tunnelling species responded more than other functional groups which were also influenced by micro-habitat variation. We provide important new insights into the long-term ecological impacts of tropical logging. We also support calls for improved logging road design both during and after timber extraction to conserve more effectively biodiversity in production forests, for instance, by considering the minimum volume of timber, per unit length of logging road needed to justify road construction. In particular, we suggest that governments and certification bodies need to highlight more clearly the biodiversity and environmental impacts of logging roads.

Optimizing carbon storage and biodiversity protection in tropical agricultural landscapes.

With the rapidly expanding ecological footprint of agriculture, the design of farmed landscapes will play an increasingly important role for both carbon storage and biodiversity protection. Carbon and biodiversity can be enhanced by integrating natural habitats into agricultural lands, but a key question is whether benefits are maximized by including many small features throughout the landscape ('land-sharing' agriculture) or a few large contiguous blocks alongside intensive farmland ('land-sparing' agriculture). In this study, we are the first to integrate carbon storage alongside multi-taxa biodiversity assessments to compare land-sparing and land-sharing frameworks. We do so by sampling carbon stocks and biodiversity (birds and dung beetles) in landscapes containing agriculture and forest within the Colombian Chocó-Andes, a zone of high global conservation priority. We show that woodland fragments embedded within a matrix of cattle pasture hold less carbon per unit area than contiguous primary or advanced secondary forests (>15 years). Farmland sites also support less diverse bird and dung beetle communities than contiguous forests, even when farmland retains high levels of woodland habitat cover. Landscape simulations based on these data suggest that land-sparing strategies would be more beneficial for both carbon storage and biodiversity than land-sharing strategies across a range of production levels. Biodiversity benefits of land-sparing are predicted to be similar whether spared lands protect primary or advanced secondary forests, owing to the close similarity of bird and dung beetle communities between the two forest classes. Land-sparing schemes that encourage the protection and regeneration of natural forest blocks thus provide a synergy between carbon and biodiversity conservation, and represent a promising strategy for reducing the negative impacts of agriculture on tropical ecosystems. However, further studies examining a wider range of ecosystem services will be necessary to fully understand the links between land-allocation strategies and long-term ecosystem service provision.

Sustainable management in crop monocultures: the impact of retaining forest on oil palm yield.

Tropical agriculture is expanding rapidly at the expense of forest, driving a global extinction crisis. How to create agricultural landscapes that minimise the clearance of forest and maximise sustainability is thus a key issue. One possibility is protecting natural forest within or adjacent to crop monocultures to harness important ecosystem services provided by biodiversity spill-over that may facilitate production. Yet this contrasts with the conflicting potential that the retention of forest exports dis-services, such as agricultural pests. We focus on oil palm and obtained yields from 499 plantation parcels spanning a total of ≈23,000 ha of oil palm plantation in Sabah, Malaysian Borneo. We investigate the relationship between the extent and proximity of both contiguous and fragmented dipterocarp forest cover and oil palm yield, controlling for variation in oil palm age and for environmental heterogeneity by incorporating proximity to non-native forestry plantations, other oil palm plantations, and large rivers, elevation and soil type in our models. The extent of forest cover and proximity to dipterocarp forest were not significant predictors of oil palm yield. Similarly, proximity to large rivers and other oil palm plantations, as well as soil type had no significant effect. Instead, lower elevation and closer proximity to forestry plantations had significant positive impacts on oil palm yield. These findings suggest that if dipterocarp forests are exporting ecosystem service benefits or ecosystem dis-services, that the net effect on yield is neutral. There is thus no evidence to support arguments that forest should be retained within or adjacent to oil palm monocultures for the provision of ecosystem services that benefit yield. We urge for more nuanced assessments of the impacts of forest and biodiversity on yields in crop monocultures to better understand their role in sustainable agriculture.

Land-sharing versus land-sparing logging: reconciling timber extraction with biodiversity conservation.

Selective logging is a major driver of rainforest degradation across the tropics. Two competing logging strategies are proposed to meet timber demands with the least impact on biodiversity: land sharing, which combines timber extraction with biodiversity protection across the concession; and land sparing, in which higher intensity logging is combined with the protection of intact primary forest reserves. We evaluate these strategies by comparing the abundances and species richness of birds, dung beetles and ants in Borneo, using a protocol that allows us to control for both timber yield and net profit across strategies. Within each taxonomic group, more species had higher abundances with land-sparing than land-sharing logging, and this translated into significantly higher species richness within land-sparing concessions. Our results are similar when focusing only on species found in primary forest and restricted in range to Sundaland, and they are independent of the scale of sampling. For each taxonomic group, land-sparing logging was the most promising strategy for maximizing the biological value of logging operations.

Selective­logging and oil palm: multitaxon impacts, biodiversity indicators, and trade­offs for conservation planning.

Strong global demand for tropical timber and agricultural products has driven large-scale logging and subsequent conversion of tropical forests. Given that the majority of tropical landscapes have been or will likely be logged, the protection of biodiversity within tropical forests thus depends on whether species can persist in these economically exploited lands, and if species cannot persist, whether we can protect enough primary forest from logging and conversion. However, our knowledge of the impact of logging and conversion on biodiversity is limited to a few taxa, often sampled in different locations with complex land-use histories, hampering attempts to plan cost-effective conservation strategies and to draw conclusions across taxa. Spanning a land-use gradient of primary forest, once- and twice-logged forests, and oil palm plantations, we used traditional sampling and DNA metabarcoding to compile an extensive data set in Sabah, Malaysian Borneo for nine vertebrate and invertebrate taxa to quantify the biological impacts of logging and oil palm, develop cost-effective methods of protecting biodiversity, and examine whether there is congruence in response among taxa. Logged forests retained high species richness, including, on average, 70% of species found in primary forest. In contrast, conversion to oil palm dramatically reduces species richness, with significantly fewer primary-forest species than found on logged forest transects for seven taxa. Using a systematic conservation planning analysis, we show that efficient protection of primary-forest species is achieved with land portfolios that include a large proportion of logged-forest plots. Protecting logged forests is thus a cost-effective method of protecting an ecologically and taxonomically diverse range of species, particularly when conservation budgets are limited. Six indicator groups (birds, leaf-litter ants, beetles, aerial hymenopterans, flies, and true bugs) proved to be consistently good predictors of the response of the other taxa to logging and oil palm. Our results confidently establish the high conservation value of logged forests and the low value of oil palm. Cross-taxon congruence in responses to disturbance also suggests that the practice of focusing on key indicator taxa yields important information of general biodiversity in studies of logging and oil palm.

Reliable, verifiable and efficient monitoring of biodiversity via metabarcoding.

To manage and conserve biodiversity, one must know what is being lost, where, and why, as well as which remedies are likely to be most effective. Metabarcoding technology can characterise the species compositions of mass samples of eukaryotes or of environmental DNA. Here, we validate metabarcoding by testing it against three high-quality standard data sets that were collected in Malaysia (tropical), China (subtropical) and the United Kingdom (temperate) and that comprised 55,813 arthropod and bird specimens identified to species level with the expenditure of 2,505 person-hours of taxonomic expertise. The metabarcode and standard data sets exhibit statistically correlated alpha- and beta-diversities, and the two data sets produce similar policy conclusions for two conservation applications: restoration ecology and systematic conservation planning. Compared with standard biodiversity data sets, metabarcoded samples are taxonomically more comprehensive, many times quicker to produce, less reliant on taxonomic expertise and auditable by third parties, which is essential for dispute resolution.

Trophic flexibility and the persistence of understory birds in intensively logged rainforest.

Effects of logging on species composition in tropical rainforests are well known but may fail to reveal key changes in species interactions. We used nitrogen stable-isotope analysis of 73 species of understory birds to quantify trophic responses to repeated intensive logging of rainforest in northern Borneo and to test 4 hypotheses: logging has significant effects on trophic positions and trophic-niche widths of species, and the persistence of species in degraded forest is related to their trophic positions and trophic-niche widths in primary forest. Species fed from higher up the food chain and had narrower trophic-niche widths in degraded forest. Species with narrow trophic-niche widths in primary forest were less likely to persist after logging, a result that indicates a higher vulnerability of dietary specialists to local extinction following habitat disturbance. Persistence of species in degraded forest was not related to a species' trophic position. These results indicate changes in trophic organization that were not apparent from changes in species composition and highlight the importance of focusing on trophic flexibility over the prevailing emphasis on membership of static feeding guilds. Our results thus support the notion that alterations to trophic organization and interactions within tropical forests may be a pervasive and functionally important hidden effect of forest degradation.

Reduced-impact logging and biodiversity conservation: a case study from Borneo.

A key driver of rain forest degradation is rampant commercial logging. Reduced-impact logging (RIL) techniques dramatically reduce residual damage to vegetation and soils, and they enhance the long-term economic viability of timber operations when compared to conventionally managed logging enterprises. Consequently, the application of RIL is increasing across the tropics, yet our knowledge of the potential for RIL also to reduce the negative impacts of logging on biodiversity is minimal. We compare the impacts of RIL on birds, leaf-litter ants, and dung beetles during a second logging rotation in Sabah, Borneo, with the impacts of conventional logging (CL) as well as with primary (unlogged) forest. Our study took place 1-8 years after the cessation of logging. The species richness and composition of RIL vs. CL forests were very similar for each taxonomic group. Both RIL and CL differed significantly from unlogged forests in terms of bird and ant species composition (although both retained a large number of the species found in unlogged forests), whereas the composition of dung beetle communities did not differ significantly among forest types. Our results show little difference in biodiversity between RIL and CL over the short-term. However, biodiversity benefits from RIL may accrue over longer time periods after the cessation of logging. We highlight a severe lack of studies investigating this possibility. Moreover, if RIL increases the economic value of selectively logged forests (e.g., via REDD+, a United Nations program: Reducing Emissions from Deforestation and Forest Degradation in Developing Countries), it could help prevent them from being converted to agricultural plantations, which results in a tremendous loss of biodiversity.

Assessing trophic position from nitrogen isotope ratios: effective calibration against spatially varying baselines.

Nitrogen isotope signatures (δ(15)N) provide powerful measures of the trophic positions of individuals, populations and communities. Obtaining reliable consumer δ(15)N values depends upon controlling for spatial variation in plant δ(15)N values, which form the trophic 'baseline'. However, recent studies make differing assumptions about the scale over which plant δ(15)N values vary, and approaches to baseline control differ markedly. We examined spatial variation in the δ(15)N values of plants and ants sampled from eight 150-m transects in both unlogged and logged rainforests. We then investigated whether ant δ(15)N values were related to variation in plant δ(15)N values following baseline correction of ant values at two spatial scales: (1) using 'local' means of plants collected from the same transect and (2) using 'global' means of plants collected from all transects within each forest type. Plant δ(15)N baselines varied by the equivalent of one trophic level within each forest type. Correcting ant δ(15)N values using global plant means resulted in consumer values that were strongly positively related to the transect baseline, whereas local corrections yielded reliable estimates of consumer trophic positions that were largely independent of transect baselines. These results were consistent at the community level and when three trophically distinct ant subfamilies and eight abundant ant species were considered separately. Our results suggest that assuming baselines do not vary can produce misleading estimates of consumer trophic positions. We therefore emphasise the importance of clearly defining and applying baseline corrections at a scale that accounts for spatial variation in plant δ(15)N values.