Paul Woodcock

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.

The conservation value of South East Asia's highly degraded forests: evidence from leaf-litter ants

South East Asia is widely regarded as a centre of threatened biodiversity owing to extensive logging and forest conversion to agriculture. In particular, forests degraded by repeated rounds of intensive logging are viewed as having little conservation value and are afforded meagre protection from conversion to oil palm. Here, we determine the biological value of such heavily degraded forests by comparing leaf-litter ant communities in unlogged (natural) and twice-logged forests in Sabah, Borneo. We accounted for impacts of logging on habitat heterogeneity by comparing species richness and composition at four nested spatial scales, and examining how species richness was partitioned across the landscape in each habitat. We found that twice-logged forest had fewer species occurrences, lower species richness at small spatial scales and altered species composition compared with natural forests. However, over 80 per cent of species found in unlogged forest were detected within twice-logged forest. Moreover, greater species turnover among sites in twice-logged forest resulted in identical species richness between habitats at the largest spatial scale. While two intensive logging cycles have negative impacts on ant communities, these degraded forests clearly provide important habitat for numerous species and preventing their conversion to oil palm and other crops should be a conservation priority.

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.

Impacts of Intensive Logging on the Trophic Organisation of Ant Communities in a Biodiversity Hotspot

Trophic organisation defines the flow of energy through ecosystems and is a key component of community structure. Widespread and intensifying anthropogenic disturbance threatens to disrupt trophic organisation by altering species composition and relative abundances and by driving shifts in the trophic ecology of species that persist in disturbed ecosystems. We examined how intensive disturbance caused by selective logging affects trophic organisation in the biodiversity hotspot of Sabah, Borneo. Using stable nitrogen isotopes, we quantified the positions in the food web of 159 leaf-litter ant species in unlogged and logged rainforest and tested four predictions: (i) there is a negative relationship between the trophic position of a species in unlogged forest and its change in abundance following logging, (ii) the trophic positions of species are altered by logging, (iii) disturbance alters the frequency distribution of trophic positions within the ant assemblage, and (iv) disturbance reduces food chain length. We found that ant abundance was 30% lower in logged forest than in unlogged forest but changes in abundance of individual species were not related to trophic position, providing no support for prediction (i). However, trophic positions of individual species were significantly higher in logged forest, supporting prediction (ii). Consequently, the frequency distribution of trophic positions differed significantly between unlogged and logged forest, supporting prediction (iii), and food chains were 0.2 trophic levels longer in logged forest, the opposite of prediction (iv). Our results demonstrate that disturbance can alter trophic organisation even without trophically-biased changes in community composition. Nonetheless, the absence of any reduction in food chain length in logged forest suggests that species-rich arthropod food webs do not experience trophic downgrading or a related collapse in trophic organisation despite the disturbance caused by logging. These food webs appear able to bend without breaking in the face of some forms of anthropogenic disturbance.

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.

Debugging diversity - a pan-continental exploration of the potential of terrestrial blood-feeding leeches as a vertebrate monitoring tool

The use of environmental DNA (eDNA) has become an applicable noninvasive tool with which to obtain information about biodiversity. A subdiscipline of eDNA is iDNA (invertebrate‐derived DNA), where genetic material ingested by invertebrates is used to characterize the biodiversity of the species that served as hosts. While promising, these techniques are still in their infancy, as they have only been explored on limited numbers of samples from only a single or a few different locations. In this study, we investigate the suitability of iDNA extracted from more than 3,000 haematophagous terrestrial leeches as a tool for detecting a wide range of terrestrial vertebrates across five different geographical regions on three different continents. These regions cover almost the full geographical range of haematophagous terrestrial leeches, thus representing all parts of the world where this method might apply. We identify host taxa through metabarcoding coupled with high‐throughput sequencing on Illumina and IonTorrent sequencing platforms to decrease economic costs and workload and thereby make the approach attractive for practitioners in conservation management. We identified hosts in four different taxonomic vertebrate classes: mammals, birds, reptiles and amphibians, belonging to at least 42 different taxonomic families. We find that vertebrate blood ingested by haematophagous terrestrial leeches throughout their distribution is a viable source of DNA with which to examine a wide range of vertebrates. Thus, this study provides encouraging support for the potential of haematophagous terrestrial leeches as a tool for detecting and monitoring terrestrial vertebrate biodiversity.