Ben A. Woodcock

Functional traits as indicators of biodiversity response to land use changes across ecosystems and organisms.

Rigorous and widely applicable indicators of biodiversity are needed to monitor the responses of ecosystems to global change and design effective conservation schemes. Among the potential indicators of biodiversity, those based on the functional traits of species and communities are interesting because they can be generalized to similar habitats and can be assessed by relatively rapid field assessment across eco-regions. Functional traits, however, have as yet been rarely considered in current common monitoring schemes. Moreover, standardized procedures of trait measurement and analyses have almost exclusively been developed for plants but different approaches have been used for different groups of organisms. Here we review approaches using functional traits as biodiversity indicators focussing not on plants as usual but particularly on animal groups that are commonly considered in different biodiversity monitoring schemes (benthic invertebrates, collembolans, above ground insects and birds). Further, we introduce a new framework based on functional traits indices and illustrate it using case studies where the traits of these organisms can help monitoring the response of biodiversity to different land use change drivers. We propose and test standard procedures to integrate different components of functional traits into biodiversity monitoring schemes across trophic levels and disciplines. We suggest that the development of indicators using functional traits could complement, rather than replace, the existent biodiversity monitoring. In this way, the comparison of the effect of land use changes on biodiversity is facilitated and is expected to positively influence conservation management practices.

Wildlife-friendly farming increases crop yield: evidence for ecological intensification.

Ecological intensification has been promoted as a means to achieve environmentally sustainable increases in crop yields by enhancing ecosystem functions that regulate and support production. There is, however, little direct evidence of yield benefits from ecological intensification on commercial farms growing globally important foodstuffs (grains, oilseeds and pulses). We replicated two treatments removing 3 or 8% of land at the field edge from production to create wildlife habitat in 50–60 ha patches over a 900 ha commercial arable farm in central England, and compared these to a business as usual control (no land removed). In the control fields, crop yields were reduced by as much as 38% at the field edge. Habitat creation in these lower yielding areas led to increased yield in the cropped areas of the fields, and this positive effect became more pronounced over 6 years. As a consequence, yields at the field scale were maintained—and, indeed, enhanced for some crops—despite the loss of cropland for habitat creation. These results suggested that over a 5-year crop rotation, there would be no adverse impact on overall yield in terms of monetary value or nutritional energy. This study provides a clear demonstration that wildlife-friendly management which supports ecosystem services is compatible with, and can even increase, crop yields.

Country-specific effects of neonicotinoid pesticides on honey bees and wild bees

Damage confirmed Early studies of the impacts of neonicotinoid insecticides on insect pollinators indicated considerable harm. However, lingering criticism was that the studies did not represent field-realistic levels of the chemicals or prevailing environmental conditions. Two studies, conducted on different crops and on two continents, now substantiate that neonicotinoids diminish bee health (see the Perspective by Kerr). Tsvetkov et al. find that bees near corn crops are exposed to neonicotinoids for 3 to 4 months via nontarget pollen, resulting in decreased survival and immune responses, especially when coexposed to a commonly used agrochemical fungicide. Woodcock et al., in a multicounty experiment on rapeseed in Europe, find that neonicotinoid exposure from several nontarget sources reduces overwintering success and colony reproduction in both honeybees and wild bees. These field results confirm that neonicotinoids negatively affect pollinator health under realistic agricultural conditions. Science, this issue p. 1395, p. 1393; see also p. 1331 Bee health is affected by neonicotinoids under field-realistic conditions across crops conditions. Neonicotinoid seed dressings have caused concern world-wide. We use large field experiments to assess the effects of neonicotinoid-treated crops on three bee species across three countries (Hungary, Germany, and the United Kingdom). Winter-sown oilseed rape was grown commercially with either seed coatings containing neonicotinoids (clothianidin or thiamethoxam) or no seed treatment (control). For honey bees, we found both negative (Hungary and United Kingdom) and positive (Germany) effects during crop flowering. In Hungary, negative effects on honey bees (associated with clothianidin) persisted over winter and resulted in smaller colonies in the following spring (24% declines). In wild bees (Bombus terrestris and Osmia bicornis), reproduction was negatively correlated with neonicotinoid residues. These findings point to neonicotinoids causing a reduced capacity of bee species to establish new populations in the year following exposure.

Impacts of neonicotinoid use on long-term population changes in wild bees in England

Wild bee declines have been ascribed in part to neonicotinoid insecticides. While short-term laboratory studies on commercially bred species (principally honeybees and bumblebees) have identified sub-lethal effects, there is no strong evidence linking these insecticides to losses of the majority of wild bee species. We relate 18 years of UK national wild bee distribution data for 62 species to amounts of neonicotinoid use in oilseed rape. Using a multi-species dynamic Bayesian occupancy analysis, we find evidence of increased population extinction rates in response to neonicotinoid seed treatment use on oilseed rape. Species foraging on oilseed rape benefit from the cover of this crop, but were on average three times more negatively affected by exposure to neonicotinoids than non-crop foragers. Our results suggest that sub-lethal effects of neonicotinoids could scale up to cause losses of bee biodiversity. Restrictions on neonicotinoid use may reduce population declines.

The importance of sward architectural complexity in structuring predatory and phytophagous invertebrate assemblages

Abstract 1. Although the importance of plant community assemblages in structuring invertebrate assemblages is well known, the role that architectural complexity plays is less well understood. In particular, direct empirical data for a range of invertebrate taxa showing how functional groups respond to plant architecture is largely absent from the literature.

Declining resilience of ecosystem functions under biodiversity loss

The composition of species communities is changing rapidly through drivers such as habitat loss and climate change, with potentially serious consequences for the resilience of ecosystem functions on which humans depend. To assess such changes in resilience, we analyse trends in the frequency of species in Great Britain that provide key ecosystem functions—specifically decomposition, carbon sequestration, pollination, pest control and cultural values. For 4,424 species over four decades, there have been significant net declines among animal species that provide pollination, pest control and cultural values. Groups providing decomposition and carbon sequestration remain relatively stable, as fewer species are in decline and these are offset by large numbers of new arrivals into Great Britain. While there is general concern about degradation of a wide range of ecosystem functions, our results suggest actions should focus on particular functions for which there is evidence of substantial erosion of their resilience.

Effects of vegetation structure and floristic diversity on detritivore, herbivore and predatory invertebrates within calcareous grasslands

Calcareous grasslands in Europe have shown wide scale declines in their extent and quality as a result of modern agricultural practices, increased atmospheric eutrophication and lack of management. In addition to being a key habitat for specialist plants, calcareous grasslands are also important for many threatened invertebrates. In this UK based study, we investigated the impact of military vehicle activity, floral species richness and vegetation structure on assemblages of detritivore, herbivore and predatory invertebrates. We also consider the impact that disturbance by military vehicle activity on the proportion of invertebrate species capable of flight, a surrogate for dispersal ability. Sward height was negatively correlated with detritivore, herbivore and predator species richness. Herbivores species richness was positively correlated with both forb and grass species richness. Spatial variation in the number of plant species was negatively correlated with herbivore species richness. Those sites most heavily disturbed by military vehicle activity supported the lowest proportions of flightless invertebrates. Successful management for calcareous grassland invertebrates should aim to maintain short swards with high floristic diversity, in terms of both the forbs and grasses. It should be noted, however, that these findings refer to principally surface rather than sward active invertebrates. While disturbance associated with military vehicle activity was not found to affect invertebrate species richness, it has negative consequences for the structure of invertebrate assemblages by selecting against invertebrates with low dispersal ability. To support invertebrate diversity in calcareous grasslands we emphasise the need for variety in the timing and type of management applied to promote heterogeneity in sward structure.

Science into practice – how can fundamental science contribute to better management of grasslands for invertebrates?

Abstract.  1. Grasslands are diverse and extensive but are declining in extent in some parts of the globe. Grassland invertebrates can be numerically abundant and are crucial to ecosystem functioning through their roles in herbivory, nutrient cycling and pollination. Most European grasslands are modified through agricultural practices. Indeed, semi‐natural grasslands, which often host the most diverse invertebrate assemblages, have suffered catastrophic losses over the last century.

Grazing alters insect visitation networks and plant mating systems

Summary 1. Many flowering plant species have a facultative or obligate dependence on insect pollination for reproductive success. Anthropogenic disturbance may alter these species interactions, but the extent to which structural changes to plant-pollinator networks affect plant species mating systems is not well understood. 2. We used long-term livestock grazing of a birch wood ecosystem to test whether disturbance of this semi-natural habitat altered floral resources, the structure of plant–insect visitation networks and the mating system of a focal plant species, Cirsium palustre. 3. Grazed habitat had a higher species richness of floral resources for pollinators. Visitation networks in grazed habitats were larger, more diverse, with an increase in the number of pollinators per plant species. Controlling for sampling effects, however, showed networks in grazed habitats were less nested and revealed a positive correlation between network connectance and floral species richness. 4. Network connectance was negatively related to C. palustre outcrossing rate within grazed and ungrazed sites. However, on average, the effects of grazing, including greater mean connectance, produced higher overall outcrossing rates and more pollen donors compared with ungrazed habitat. The number of different pollen donors, spatial genetic structure and mating among close relatives were all correlated with greater extent of suitable C. palustre habitat in the landscape, consistent with the effects of increasing plant population size but limited seed dispersal. 5. Pre-adaptation of C. palustre to disturbance coupled with a preponderance of highly dispersive flies attracted to the greater food resources in grazed habitat is a likely mechanism underpinning this increased pollen transport. 6. Habitat modification by long-term mammalian grazing fundamentally shifted visitation network structure and the state of a plant mating system, indicating how ecosystem disturbance can cascade across levels of biological organization through altered interspecific interactions. Cirsium palustre retains flexibility to bias reproduction towards selfing where pollen donor diversity is limited; such reproductive flexibility may be an important mechanism structuring plant populations in human-modified landscapes.

National patterns of functional diversity and redundancy in predatory ground beetles and bees associated with key UK arable crops

1. Invertebrates supporting natural pest control and pollination ecosystem services are crucial to world-wide crop production. Understanding national patterns in the spatial structure of natural pest control and pollination can be used to promote effective crop management and contribute to long-term food security. 2. We mapped the species richness and functional diversity of ground beetles and bees to provide surrogate measures of natural pest control and pollination for Great Britain. Func- tional diversity represents the value and range of morphological and behavioural traits that support ecosystem services. We modelled the rate at which functional diversity collapsed in response to species extinctions to provide an index of functional redundancy. 3. Deficits in functional diversity for both pest control and pollination were found in areas of high arable crop production. Ground beetle functional redundancy was positively corre- lated with the landscape cover of semi-natural habitats where extinctions were ordered by body size and dispersal ability. For bees, functional redundancy showed a weak positive cor- relation with semi-natural habitat cover where species extinctions were ordered by feeding specialization. 4. Synthesis and applications. Increasingly, evidence suggests that functionally diverse assem- blages of ground beetles and bees may be a key element to strategies that aim to support pol- lination and natural pest control in crops. If deficits in both functional diversity and redundancy in areas of high crop production are to be reversed, then targeted implementation of agri-environment schemes that establish semi-natural habitat may provide a policy mecha- nism for supporting these ecosystem services.