Riccardo Bommarco

Extinction debt: a challenge for biodiversity conservation

Local extinction of species can occur with a substantial delay following habitat loss or degradation. Accumulating evidence suggests that such extinction debts pose a significant but often unrecognized challenge for biodiversity conservation across a wide range of taxa and ecosystems. Species with long generation times and populations near their extinction threshold are most likely to have an extinction debt. However, as long as a species that is predicted to become extinct still persists, there is time for conservation measures such as habitat restoration and landscape management. Standardized long-term monitoring, more high-quality empirical studies on different taxa and ecosystems and further development of analytical methods will help to better quantify extinction debt and protect biodiversity.

RAPID EVOLUTION OF AN INVASIVE PLANT

Exotic plants often face different conditions from those experienced where they are native. The general issue of how exotics respond to unfamiliar environments within their new range is not well understood. Phenotypic plasticity has historically been seen as the primary mechanism enabling exotics to colonize large, environmentally diverse areas. However, new work indicates that exotics can evolve quickly, suggesting that contemporary evolution may be more important in invasion ecology than previously appreciated. To determine the influence of contemporary evolution, phenotypic plasticity, and founder ef- fects in affecting phenotypic variation among introduced plants, we compared the size, fecundity, and leaf area of St. Johns wort ( Hypericum perforatum) collected from native European and introduced western and central North American populations in common gardens in Washington, California, Spain, and Sweden. We also determined genetic rela- tionships among these plants by examining variation in amplified fragment length poly- morphism (AFLP) markers. There was substantial genetic variation among introduced populations and evidence for multiple introductions of H. perforatum into North America. Across common gardens in- troduced plants were neither universally larger nor more fecund than natives. However, within common gardens, both introduced and native populations exhibited significant lat- itudinally based clines in size and fecundity. Clines among introduced populations broadly converged with those among native populations. Introduced and native plants originating from northern latitudes generally outperformed those originating from southern latitudes when grown in northern latitude gardens of Washington and Sweden. Conversely, plants from southern latitudes performed best in southern gardens in Spain and California. Clinal patterns in leaf area, however, did not change between gardens; European and central North American plants from northern latitudes had larger leaves than plants from southern latitudes within these regions in both Washington and California, the two gardens where this trait was measured. Introduced plants did not always occur at similar latitudes as their most closely related native progenitor, indicating that pre-adaptation (i.e., climate matching) is unlikely to be the sole explanation for clinal patterns among introduced populations. Instead, results suggest that introduced plants are evolving adaptations to broad-scale environmental conditions in their introduced range.

Ecological intensification: harnessing ecosystem services for food security

Rising demands for agricultural products will increase pressure to further intensify crop production, while negative environmental impacts have to be minimized. Ecological intensification entails the environmentally friendly replacement of anthropogenic inputs and/or enhancement of crop productivity, by including regulating and supporting ecosystem services management in agricultural practices. Effective ecological intensification requires an understanding of the relations between land use at different scales and the community composition of ecosystem service-providing organisms above and below ground, and the flow, stability, contribution to yield, and management costs of the multiple services delivered by these organisms. Research efforts and investments are particularly needed to reduce existing yield gaps by integrating context-appropriate bundles of ecosystem services into crop production systems.

Stability of pollination services decreases with isolation from natural areas despite honey bee visits

Sustainable agricultural landscapes by definition provide high magnitude and stability of ecosystem services, biodiversity and crop productivity. However, few studies have considered landscape effects on the stability of ecosystem services. We tested whether isolation from florally diverse natural and semi-natural areas reduces the spatial and temporal stability of flower-visitor richness and pollination services in crop fields. We synthesised data from 29 studies with contrasting biomes, crop species and pollinator communities. Stability of flower-visitor richness, visitation rate (all insects except honey bees) and fruit set all decreased with distance from natural areas. At 1 km from adjacent natural areas, spatial stability decreased by 25, 16 and 9% for richness, visitation and fruit set, respectively, while temporal stability decreased by 39% for richness and 13% for visitation. Mean richness, visitation and fruit set also decreased with isolation, by 34, 27 and 16% at 1 km respectively. In contrast, honey bee visitation did not change with isolation and represented > 25% of crop visits in 21 studies. Therefore, wild pollinators are relevant for crop productivity and stability even when honey bees are abundant. Policies to preserve and restore natural areas in agricultural landscapes should enhance levels and reliability of pollination services.

Habitat fragmentation causes immediate and time‐delayed biodiversity loss at different trophic levels

Intensification or abandonment of agricultural land use has led to a severe decline of semi-natural habitats across Europe. This can cause immediate loss of species but also time-delayed extinctions, known as the extinction debt. In a pan-European study of 147 fragmented grassland remnants, we found differences in the extinction debt of species from different trophic levels. Present-day species richness of long-lived vascular plant specialists was better explained by past than current landscape patterns, indicating an extinction debt. In contrast, short-lived butterfly specialists showed no evidence for an extinction debt at a time scale of c. 40 years. Our results indicate that management strategies maintaining the status quo of fragmented habitats are insufficient, as time-delayed extinctions and associated co-extinctions will lead to further biodiversity loss in the future.

A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems

Bees provide essential pollination services that are potentially affected both by local farm management and the surrounding landscape. To better understand these different factors, we modelled the relative effects of landscape composition (nesting and floral resources within foraging distances), landscape configuration (patch shape, interpatch connectivity and habitat aggregation) and farm management (organic vs. conventional and local-scale field diversity), and their interactions, on wild bee abundance and richness for 39 crop systems globally. Bee abundance and richness were higher in diversified and organic fields and in landscapes comprising more high-quality habitats; bee richness on conventional fields with low diversity benefited most from high-quality surrounding land cover. Landscape configuration effects were weak. Bee responses varied slightly by biome. Our synthesis reveals that pollinator persistence will depend on both the maintenance of high-quality habitats around farms and on local management practices that may offset impacts of intensive monoculture agriculture.

MEASURING BEE DIVERSITY IN DIFFERENT EUROPEAN HABITATS AND BIOGEOGRAPHICAL REGIONS

Bee pollinators are currently recorded with many different sampling methods. However, the relative performances of these methods have not been systematically evaluated and compared. In response to the strong need to record ongoing shifts in pollinator diversity and abundance, global and regional pollinator initiatives must adopt standardized sampling protocols when developing large-scale and long-term monitoring schemes. We systematically evaluated the performance of six sampling methods (observation plots, pan traps, standardized and variable transect walks, trap nests with reed internodes or paper tubes) that are commonly used across a wide range of geographical regions in Europe and in two habitat types (agricultural and seminatural). We focused on bees since they represent the most important pollinator group worldwide. Several characteristics of the methods were considered in order to evaluate their performance in assessing bee diversity: sample coverage, observed species richness, species richness estimators, collector biases (identified by subunit-based rarefaction curves), species composition of the samples, and the indication of overall bee species richness (estimated from combined total samples). The most efficient method in all geographical regions, in both the agricultural and seminatural habitats, was the pan trap method. It had the highest sample coverage, collected the highest number of species, showed negligible collector bias, detected similar species as the transect methods, and was the best indicator of overall bee species richness. The transect methods were also relatively efficient, but they had a significant collector bias. The observation plots showed poor performance. As trap nests are restricted to cavity-nesting bee species, they had a naturally low sample coverage. However, both trap nest types detected additional species that were not recorded by any of the other methods. For large-scale and long-term monitoring schemes with surveyors with different experience levels, we recommend pan traps as the most efficient, unbiased, and cost-effective method for sampling bee diversity. Trap nests with reed internodes could be used as a complementary sampling method to maximize the numbers of collected species. Transect walks are the principal method for detailed studies focusing on plant-pollinator associations. Moreover, they can be used in monitoring schemes after training the surveyors to standardize their collection skills.

Seed coating with a neonicotinoid insecticide negatively affects wild bees

Understanding the effects of neonicotinoid insecticides on bees is vital because of reported declines in bee diversity and distribution and the crucial role bees have as pollinators in ecosystems and agriculture. Neonicotinoids are suspected to pose an unacceptable risk to bees, partly because of their systemic uptake in plants, and the European Union has therefore introduced a moratorium on three neonicotinoids as seed coatings in flowering crops that attract bees. The moratorium has been criticized for being based on weak evidence, particularly because effects have mostly been measured on bees that have been artificially fed neonicotinoids. Thus, the key question is how neonicotinoids influence bees, and wild bees in particular, in real-world agricultural landscapes. Here we show that a commonly used insecticide seed coating in a flowering crop can have serious consequences for wild bees. In a study with replicated and matched landscapes, we found that seed coating with Elado, an insecticide containing a combination of the neonicotinoid clothianidin and the non-systemic pyrethroid β-cyfluthrin, applied to oilseed rape seeds, reduced wild bee density, solitary bee nesting, and bumblebee colony growth and reproduction under field conditions. Hence, such insecticidal use can pose a substantial risk to wild bees in agricultural landscapes, and the contribution of pesticides to the global decline of wild bees may have been underestimated. The lack of a significant response in honeybee colonies suggests that reported pesticide effects on honeybees cannot always be extrapolated to wild bees.

Life-history traits predict species responses to habitat area and isolation: a cross-continental synthesis

There is a lack of quantitative syntheses of fragmentation effects across species and biogeographic regions, especially with respect to species life-history traits. We used data from 24 independent studies of butterflies and moths from a wide range of habitats and landscapes in Europe and North America to test whether traits associated with dispersal capacity, niche breadth and reproductive rate modify the effect of habitat fragmentation on species richness. Overall, species richness increased with habitat patch area and connectivity. Life-history traits improved the explanatory power of the statistical models considerably and modified the butterfly species-area relationship. Species with low mobility, a narrow feeding niche and low reproduction were most strongly affected by habitat loss. This demonstrates the importance of considering life-history traits in fragmentation studies and implies that both species richness and composition change in a predictable manner with habitat loss and fragmentation.

Delivery of crop pollination services is an insufficient argument for wild pollinator conservation

There is compelling evidence that more diverse ecosystems deliver greater benefits to people, and these ecosystem services have become a key argument for biodiversity conservation. However, it is unclear how much biodiversity is needed to deliver ecosystem services in a cost-effective way. Here we show that, while the contribution of wild bees to crop production is significant, service delivery is restricted to a limited subset of all known bee species. Across crops, years and biogeographical regions, crop-visiting wild bee communities are dominated by a small number of common species, and threatened species are rarely observed on crops. Dominant crop pollinators persist under agricultural expansion and many are easily enhanced by simple conservation measures, suggesting that cost-effective management strategies to promote crop pollination should target a different set of species than management strategies to promote threatened bees. Conserving the biological diversity of bees therefore requires more than just ecosystem-service-based arguments.