Felicity A. Edwards

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.

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.

Functional attributes change but functional richness is unchanged after fragmentation of Brazilian Atlantic forests

Summary1. Fragmentation of tropical forests is one of the greatest threats to global biodiversity. Understand-ing how biological and functional attributes of communities respond to fragmentation and, in turn,whether ecosystem functioning is impacted upon are critical steps for assessing the long-term effectsand conservation values of forest fragments. Ecosystem functioning can be inferred through func-tional diversity metrics, including functional richness, evenness and divergence, which collectivelyquantify the range, distribution and uniqueness of functional traits within a community.2. Our study was carried out in forest remnants of the Brazilian Atlantic rain forest, which is a glo-bal hotspot of threatened biodiversity that has undergone massive deforestation and fragmentation.We focus on trees, which play critical functional roles in forest structure, food provisioning and car-bon storage, to examine community organization and functional diversity across a gradient of frag-mentation, from small to large fragments and at edge versus interior habitats.3. The interiors of small fragments have marginally higher species richness, but similar communitystructures, to the interiors of bigger fragments. In contrast, fragment edges suffered significant lossesof species and changes in community structure, relative to fragment interiors.4. Despite shifts in community organization, functional richness was not impacted by fragmentation,with the same number of functions provided independent of fragment size or proximity to edge.However, functional evenness and functional divergence both increased with decreasing fragmentsize, while fragment edges had lower functional evenness than interiors did, indicating that the abun-dance and dominance of functional traits has changed, with negative implications for functionalredundancy and ecosystem resilience. At fragment edges, large-fruited trees, critical as resources forfauna, were replaced by early successional, small-seeded species. The influence of fragment sizewas smaller, with a reduction in very large-fruited trees in small fragments counterbalanced byincreased numbers of fleshy- and medium-fruited trees. Wood density was not impacted by fragmen-tation.5. Synthesis. These results suggest that the interiors of even small fragments can contain importantbiodiversity, ecosystem functions and carbon stores, offering potential opportunities for cobenefitsunder existing carbon markets. Retaining forest fragments is an important conservation strategywithin the highly threatened Brazilian Atlantic forest biome.Key-words: carbon, fauna resources, fragmented landscape, functional diversity, functional traitattributes, species richness, tableland Atlantic rain forest, wood density

Does logging and forest conversion to oil palm agriculture alter functional diversity in a biodiversity hotspot

Forests in Southeast Asia are rapidly being logged and converted to oil palm. These changes in land-use are known to affect species diversity but consequences for the functional diversity of species assemblages are poorly understood. Environmental filtering of species with similar traits could lead to disproportionate reductions in trait diversity in degraded habitats. Here, we focus on dung beetles, which play a key role in ecosystem processes such as nutrient recycling and seed dispersal. We use morphological and behavioural traits to calculate a variety of functional diversity measures across a gradient of disturbance from primary forest through intensively logged forest to oil palm. Logging caused significant shifts in community composition but had very little effect on functional diversity, even after a repeated timber harvest. These data provide evidence for functional redundancy of dung beetles within primary forest and emphasize the high value of logged forests as refugia for biodiversity. In contrast, conversion of forest to oil palm greatly reduced taxonomic and functional diversity, with a marked decrease in the abundance of nocturnal foragers, a higher proportion of species with small body sizes and the complete loss of telecoprid species (dung-rollers), all indicating a decrease in the functional capacity of dung beetles within plantations. These changes also highlight the vulnerability of community functioning within logged forests in the event of further environmental degradation.

Selective-logging and oil palm: multitaxon impacts, biodiversity indicators, and trade-offs 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.

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.

EDITOR'S CHOICE: Surrounding habitats mediate the trade-off between land-sharing and land-sparing agriculture in the tropics

1. Two strategies are often promoted to mitigate the effects of agricultural expansion on biodiversity: one integrates wildlife-friendly habitats within farmland (land sharing), and the other intensifies farming to allow the offset of natural reserves (land sparing). Their relative merits for biodiversity protection have been subject to much debate, but no previous study has examined whether trade-offs between the two strategies depend on the proximity of farmed areas to large tracts of natural habitat. 2. We sampled birds and dung beetles across contiguous forests and agricultural landscapes (low-intensity cattle farming) in a threatened hotspot of endemism: the Colombian Choco-Andes. We test the hypothesis that the relative biodiversity benefits of either strategy depend partially on the degree to which farmlands are isolated from large contiguous blocks of forest. 3. We show that distance from forest mediates the occurrence of many species within farmland. For the majority of species, occurrence on farmland depends on both isolation from forest and the proportionate cover of small-scale wildlife-friendly habitats within the farm landscape, with both variables having a similar overall magnitude of effect on occurrence probabilities. 4. Simulations suggest that the biodiversity benefits of land sharing decline significantly with increasing distance from forest, but land sparing benefits remain consistent. In farm management units situated close to large contiguous forest (<500 m), land sharing is predicted to provide equal benefits to land sparing, but land sparing becomes increasingly superior in management units situated further from forest (1500 m). The predicted biodiversity benefits of land sparing are similar across all distances, provided that sparing mechanisms genuinely deliver protection for contiguous forest tracts. 5. Synthesis and applications: the persistence of bird and dung beetle communities in low-intensity pastoral agriculture is strongly linked to the proximity of surrounding contiguous forests. Land-sharing policies that promote the integration of small-scale wildlife-friendly habitats might be of limited benefit without simultaneous measures to protect larger blocks of natural habitat, which could be achieved via land-sparing practices. Policymakers should carefully consider the extent and distribution of remaining contiguous natural habitats when designing agri-environment schemes in the tropics.

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.

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

Nitrogen isotope signatures (δ15N) provide powerful measures of the trophic positions of individuals, populations and communities. Obtaining reliable consumer δ15N values depends upon controlling for spatial variation in plant δ15N values, which form the trophic ‘baseline’. However, recent studies make differing assumptions about the scale over which plant δ15N values vary, and approaches to baseline control differ markedly. We examined spatial variation in the δ15N values of plants and ants sampled from eight 150-m transects in both unlogged and logged rainforests. We then investigated whether ant δ15N values were related to variation in plant δ15N 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 δ15N baselines varied by the equivalent of one trophic level within each forest type. Correcting ant δ15N 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 δ15N values.

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.