Rapid assessment of insect pollination services to inform decision-making.

Pollinator declines have prompted efforts to assess how land-use change affects insect pollinators and pollination services in agricultural landscapes. Yet many tools to measure insect pollination services require substantial landscape-scale data and technical expertise. In expert workshops, 3 straightforward methods (desk-based method, field survey, and empirical manipulation with exclusion experiments) for rapid insect pollination assessment at site scale were developed to provide an adaptable framework that is accessible to nonspecialist with limited resources. These methods were designed for TESSA (Toolkit for Ecosystem Service Site-Based Assessment) and allow comparative assessment of pollination services at a site of conservation interest and in its most plausible alternative state (e.g., converted to agricultural land). We applied the methods at a nature reserve in the United Kingdom to estimate the value of insect pollination services provided by the reserve. The economic value of pollination services provided by the reserve ranged from US$6163 to US$11,546/year. The conversion of the reserve to arable land would provide no insect pollination services and a net annual benefit from insect-pollinated crop production of approximately $1542/year (US$24∙ha-1 ∙year-1 ). The methods had wide applicability and were readily adapted to different insect-pollinated crops: rape (Brassica napus) and beans (Vicia faba) crops. All methods were rapidly employed under a low budget. The relatively less robust methods that required fewer resources yielded higher estimates of annual insect pollination benefit.

Diversidad y Conservación de Gasterópodos Subterráneos de Agua Dulce en los Estados Unidos y en México Resumen Las declinaciones de los polinizadores han impulsado los esfuerzos por evaluar cómo el cambio del uso de suelo afecta a los insectos polinizadores y los servicios de polinización en los paisajes agrícolas. Aun así, muchas de las herramientas para medir los servicios de los insectos polinizadores requieren datos sustanciales a escala de paisaje y el conocimiento de expertos. Desarrollamos tres métodos sencillos (método de gabinete, censo de campo y manipulación empírica con experimentos de exclusión) durante algunos talleres de expertos para la evaluación rápida de la polinización por insectos a escala de sitio con el objetivo de proporcionar un marco de trabajo adaptable y accesible para quienes no son especialistas y cuentan con recursos limitados. Estos métodos fueron diseñados para TESSA (Toolkit for Ecosystem Service Site-Based Assessment, en inglés) y permiten la evaluación comparativa de los servicios de polinización en los sitios de interés para la conservación y su estado alternativo más plausible (p. ej.: convertido a suelo agrícola). Aplicamos los métodos en una reserva natural del Reino Unido para estimar el valor de los servicios de polinización por insectos que proporciona la reserva. El valor económico de los servicios de polinización que proporciona la reserva varió desde US$6,163 a US$11,546 al año-1 . La conversión de la reserva a suelo arable no proporcionaría servicios de polinización por insectos, pero sí un beneficio anual neto a partir de la producción de cultivos polinizados por insectos de aproximadamente $1,542 al año-1 (US$24 ha-1 año-1 ). Los métodos tuvieron una aplicabilidad generalizada y estaban ya adaptados a los diferentes cultivos polinizados por insectos: cultivos de colza (Brassica napus) y habas (Vicia faba). Todos los métodos pudieron usarse con bajo presupuesto. Los métodos relativamente menos robustos que requirieron menos recursos produjeron estimados más elevados del beneficio anual de la polinización por insectos.

Rethinking the food system for human health in the Anthropocene.

The current global food system is becoming increasingly unsustainable and is having negative impacts on planetary and human health. It is essential that human health is placed at the centre of a redesigned food system, as that will also help ensure planetary health.

Replanting of first-cycle oil palm results in a second wave of biodiversity loss.

Conversion of forest to oil palm plantations results in a significant loss of biodiversity. Despite this, first-cycle oil palm plantations can sustain relatively high biodiversity compared to other crops. However, the long-term effects of oil palm agriculture on flora and fauna are unknown. Oil palm has a 25-year commercial lifespan before it must be replanted, due to reduced productivity and difficulty of harvesting. Loss of the complex vegetation structure of oil palm plantations during the replanting process will likely have impacts on the ecosystem at a local and landscape scale. However, the effect of replanting on biodiversity is poorly understood.Here, we investigate the effects of replanting oil palm on soil macrofauna communities. We assessed ordinal richness, abundance, and community composition of soil macrofauna in first- (25- to 27-year-old) and second-cycle oil palm (freshly cleared, 1-year-old, 3-year-old, and 7-year-old mature).Macrofauna abundance and richness drastically declined immediately after replanting. Macrofauna richness showed some recovery 7 years after replanting, but was still 19% lower than first-cycle oil palm. Macrofauna abundance recovered to similar levels to that of first-cycle oil palm plantations, 1 year after replanting. This was mainly due to high ant abundance, possibly due to the increased understory vegetation as herbicides are not used at this age. However, there were subsequent declines in macrofauna abundance 3 and 7 years after replanting, resulting in a 59% drop in macrofauna abundance compared to first-cycle levels. Furthermore, soil macrofauna community composition in all ages of second-cycle oil palm was different to first-cycle plantations, with decomposers suffering particular declines.After considerable biodiversity loss due to forest conversion for oil palm, belowground invertebrate communities suffer a second wave of biodiversity loss due to replanting. This is likely to have serious implications for soil invertebrate diversity and agricultural sustainability in oil palm landscapes, due to the vital ecosystem functions that soil macrofauna provide.

To what extent has sustainable intensification in England been achieved?

Agricultural intensification has significantly increased yields and fed growing populations across the planet, but has also led to considerable environmental degradation. In response an alternative process of 'Sustainable Intensification' (SI), whereby food production increases while environmental impacts are reduced, has been advocated as necessary, if not sufficient, for delivering food and environmental security. However, the extent to which SI has begun, the main drivers of SI, and the degree to which degradation is simply 'offshored' are uncertain. In this study we assess agroecosystem services in England and two contrasting sub-regions, majority-arable Eastern England and majority-pastoral South-Western England, since 1950 by analysing ecosystem service metrics and developing a simple system dynamics model. We find that rapid agricultural intensification drove significant environmental degradation in England in the early 1980s, but that most ecosystem services except farmland biodiversity began to recover after 2000, primarily due to reduced livestock and fertiliser usage decoupling from high yields. This partially follows the trajectory of an Environmental Kuznets Curve, with yields and GDP growth decoupling from environmental degradation above ~£17,000 per capita per annum. Together, these trends suggest that SI has begun in England. However, the lack of recovery in farmland biodiversity, and the reduction in UK food self-sufficiency resulting in some agricultural impacts being 'offshored', represent major negative trade-offs. Maintaining yields and restoring biodiversity while also addressing climate change, offshored degradation, and post-Brexit subsidy changes will require significant further SI in the future.

Riding on the wind: volatile compounds dictate selection of grassland seedlings by snails.

Background and Aims: Seedling herbivory is an important selective filter in many plant communities. The removal of preferred food plants by both vertebrate and, more commonly, invertebrate herbivores can destroy entire seedling cohorts, and consequently dictate plant community assembly. Nevertheless, our understanding of how and why some seedlings are more prone to herbivore attack than their neighbours remains limited. For seedlings, where even minor tissue damage is fatal, avoiding contact with herbivores is probably advantageous and, on this basis, volatile organic compounds (VOCs) are strong candidates to fulfil a primary defensive role. Methods: We quantified seedling selection by snails (Cornu aspersum) for 14 common, European grassland species. Seedling acceptability was subsequently compared with species-specific expression of constitutive secondary defence metabolites (CSDMs), and VOCs to determine their relative influence on seedling selection. Results: We found no relationship between seedling acceptability and CSDMs, but seedling selection was strongly associated with VOC profiles. Monoterpenes (specifically ß-ocimene) were identified as likely attractants, while green leaf volatiles (GLVs) (3-hexen-1-ol acetate) were strongly associated with low seedling acceptability. Conclusions: By elucidating a relationship between VOCs and seedling acceptability, we contradict a long-held, but poorly tested, assumption that seedling selection by herbivores in (semi-)natural plant communities centres on CSDMs. Instead, our results corroborate recent work showing how GLVs, including 3-hexen-1-ol acetate, deter crop seedling selection by molluscs. Although our failure to establish any early-ontogenetic relationship between VOCs and CSDMs also suggests that the former do not 'advertise' possession of the latter, we nevertheless reveal the role that VOCs play in defending seedlings against herbivory before lethal damage occurs.

Rhizosphere Bacterial Communities Differ According to Fertilizer Regimes and Cabbage (Brassica oleracea var. capitata L.) Harvest Time, but Not Aphid Herbivory.

Rhizosphere microbial communities are known to be highly diverse and strongly dependent on various attributes of the host plant, such as species, nutritional status, and growth stage. High-throughput 16S rRNA gene amplicon sequencing has been used to characterize the rhizosphere bacterial community of many important crop species, but this is the first study to date to characterize the bacterial and archaeal community of Brassica oleracea var. capitata. The study also tested the response of the bacterial community to fertilizer type (organic or synthetic) and N dosage (high or low), in addition to plant age (9 or 12 weeks) and aphid (Myzus persicae) herbivory (present/absent). The impact of aboveground herbivory on belowground microbial communities has received little attention in the literature, and since the type (organic or mineral) and amount of fertilizer applications are known to affect M. percicae populations, these treatments were applied at agricultural rates to test for synergistic effects on the soil bacterial community. Fertilizer type and plant growth were found to result in significantly different rhizosphere bacterial communities, while there was no effect of aphid herbivory. Several operational taxonomic units were identified as varying significantly in abundance between the treatment groups and age cohorts. These included members of the S-oxidizing genus Thiobacillus, which was significantly more abundant in organically fertilized 12-week-old cabbages, and the N-fixing cyanobacteria Phormidium, which appeared to decline in synthetically fertilized soils relative to controls. These responses may be an effect of accumulating root-derived glucosinolates in the B. oleracea rhizosphere and increased N-availability, respectively.

Something in the air? The impact of volatiles on mollusc attack of oilseed rape seedlings.

BACKGROUND AND AIMS: Mounting concerns about balancing food security with the environmental impacts of agro-chemical use underpin the need to better understand the mechanisms by which crop plants, particularly during the vulnerable seedling stage, attract or repel herbivores. METHODS: The feeding preferences of the mollusc Helix aspersa were determined for several oilseed rape (Brassica napus) cultivars and a rank order of acceptability was established. This was compared with glucosinolate concentrations and volatile organic compound (VOC) profiles to determine whether seedling acceptability to molluscs was linked to either form of defence. KEY RESULTS: While VOC profiles for each oilseed rape cultivar could be separated by canonical discriminant analysis and associated with mollusc feeding preferences, glucosinolate profiles were unrelated to snail feeding behaviour. A mixture of monoterpenes (α-pinene, ß-myrcene and δ-3-carene) was identified as a putative attractant, while a blend of the green leaf volatiles 3-hexen-1-ol, 3-hexen-1-ol acetate and the monoterpene α-terpinene was identified as a putative repellent mix. Added to the VOC profile of oilseed rape seedlings, the 'repellent' mix reduced mollusc selection, while the 'attractant' mix had no effect. CONCLUSIONS: Despite the widespread assumption that seedling selection by generalist herbivores is governed by chemical defence and taste, we show that olfactory cues may be more important. Oilseed rape may be atypical of wild plants, but our ability to identify repellent volatile organic compounds that can influence snail olfactory selection points to new methods for crop protection using modified VOC profiles during the vulnerable seedling stage.

The Effects of Diesel Exhaust Pollution on Floral Volatiles and the Consequences for Honey Bee Olfaction.

There is growing evidence of a substantial decline in pollinators within Europe and North America, most likely caused by multiple factors such as diseases, poor nutrition, habitat loss, insecticides, and environmental pollution. Diesel exhaust could be a contributing factor to this decline, since we found that diesel exhaust rapidly degrades floral volatiles, which honey bees require for flower recognition. In this study, we exposed eight of the most common floral volatiles to diesel exhaust in order to investigate whether it can affect volatile mediated plant-pollinator interaction. Exposure to diesel exhaust altered the blend of common flower volatiles significantly: myrcene was considerably reduced, ß-ocimene became undetectable, and ß-caryophyllene was transformed into its cis-isomer isocaryophyllene. Proboscis extension response (PER) assays showed that the alterations of the blend reduced the ability of honey bees to recognize it. The chemically reactive nitrogen oxides fraction of diesel exhaust gas was identified as capable of causing degradation of floral volatiles.

Diesel exhaust rapidly degrades floral odours used by honeybees.

Honeybees utilise floral odours when foraging for flowers; we investigated whether diesel exhaust pollution could interrupt these floral odour stimuli. A synthetic blend of eight floral chemicals, identified from oilseed rape, was exposed to diesel exhaust pollution. Within one minute of exposure the abundances of four of the chemicals were significantly lowered, with two components rendered undetectable. Honeybees were trained to recognise the full synthetic odour mix; altering the blend, by removing the two chemicals rendered undetectable, significantly reduced the ability of the trained honeybees to recognize the altered odour. Furthermore, we found that at environmentally relevant levels the mono-nitrogen oxide (NOx) fraction of the exhaust gases was a key facilitator of this odour degradation. Such changes in recognition may impact upon a honeybee's foraging efficiency and therefore the pollination services that they provide.

Do asexual morphs of the peach-potato aphid, Myzus persicae, utilise the aphid sex pheromone? Behavioural and electrophysiological responses of M. persicae virginoparae to (4aS,7S,7aR)-nepetalactone and its effect on aphid performance.

The aphid sex pheromone component (4aS,7S,7aR)-nepetalactone is considered to be a potential tool for enhancing biological control of aphids. Studies have confirmed its potential to attract parasitoids, increase parasitism rates in the field and also alter the spatial distribution of parasitoids. An important aspect that has been overlooked is the impact that the introduction of nepetalactone may have on aphid populations already present in field or glasshouse environments. The most prevalent pest aphid populations in glasshouse and field environments are the asexual morphs, which are capable of exponential growth if populations are not controlled. The short-term implications of the sex pheromone on asexual aphids were observed through their behavioural response. Using Y-tube olfactometry, it is shown that virginoparae of the peach-potato aphid, Myzus persicae, are repelled by high concentrations of nepetalactone. Long-term effects of the pheromone which may span the aphid's life, or even generations, were assessed via mean relative growth rate (MRGR) and the intrinsic rate of natural increase (rm). Electroantennography also demonstrated that asexual female aphids are able to detect aphid sex pheromone components. To our knowledge, this is the first time it has been reported that M. persicae virginoparae are able to detect aphid sex pheromone components or that their behavioural response and/or performance has been studied. The implications of these results and their significance in understanding semiochemical communication are discussed.

Navigating the perfect storm: research strategies for socialecological systems in a rapidly evolving world.

The 'Perfect Storm' metaphor describes a combination of events that causes a surprising or dramatic impact. It lends an evolutionary perspective to how social-ecological interactions change. Thus, we argue that an improved understanding of how social-ecological systems have evolved up to the present is necessary for the modelling, understanding and anticipation of current and future social-ecological systems. Here we consider the implications of an evolutionary perspective for designing research approaches. One desirable approach is the creation of multi-decadal records produced by integrating palaeoenvironmental, instrument and documentary sources at multiple spatial scales. We also consider the potential for improved analytical and modelling approaches by developing system dynamical, cellular and agent-based models, observing complex behaviour in social-ecological systems against which to test systems dynamical theory, and drawing better lessons from history. Alongside these is the need to find more appropriate ways to communicate complex systems, risk and uncertainty to the public and to policy-makers.

Commercializing genetically modified crops under EU regulations: objectives and barriers.

Agriculture faces serious problems in feeding 9 billion people by 2050: production must be increased and ecosystem services maintained under conditions for growing crops that are predicted to worsen in many parts of the world. A proposed solution is sustainable intensification of agriculture, whereby yields are increased on land that is currently cultivated, so sparing land to deliver other ecosystem services. Genetically modified (GM) crops are already contributing to sustainable intensification through higher yields and lower environmental impacts, and have potential to deliver further significant improvements. Despite their widespread successful use elsewhere, the European Union (EU) has been slow to introduce GM crops: decisions on applications to import GM commodities are lengthy, and decision-making on applications to cultivate GM crops has virtually ceased. Delayed import approvals result in economic losses, particularly in the EU itself as a result of higher commodity prices. Failure to grant cultivation approvals costs EU farmers opportunities to reduce inputs, and results in loss of agricultural research and development from the EU to countries such as the United States and China. Delayed decision-making in the EU ostensibly results from scientific uncertainty about the effects of using GM crops; however, scientific uncertainty may be a means to justify a political decision to restrict cultivation of GM crops in the EU. The problems associated with delayed decision-making will not improve until there is clarity about the EU's agricultural policy objectives, and whether the use of GM crops will be permitted to contribute to achieving those objectives.

Infectious diseases of animals and plants: an interdisciplinary approach.

Animal and plant diseases pose a serious and continuing threat to food security, food safety, national economies, biodiversity and the rural environment. New challenges, including climate change, regulatory developments, changes in the geographical concentration and size of livestock holdings, and increasing trade make this an appropriate time to assess the state of knowledge about the impact that diseases have and the ways in which they are managed and controlled. In this paper, the case is explored for an interdisciplinary approach to studying the management of infectious animal and plant diseases. Reframing the key issues through incorporating both social and natural science research can provide a holistic understanding of disease and increase the policy relevance and impact of research. Finally, in setting out the papers in this Theme Issue, a picture of current and future animal and plant disease threats is presented.

Parasitoids select plants more heavily infested with their caterpillar hosts: a new approach to aid interpretation of plant headspace volatiles.

Plants produce volatile organic compounds (VOCs) in response to herbivore attack, and these VOCs can be used by parasitoids of the herbivore as host location cues. We investigated the behavioural responses of the parasitoid Cotesia vestalis to VOCs from a plant-herbivore complex consisting of cabbage plants (Brassica oleracea) and the parasitoids host caterpillar, Plutella xylostella. A Y-tube olfactometer was used to compare the parasitoids' responses to VOCs produced as a result of different levels of attack by the caterpillar and equivalent levels of mechanical damage. Headspace VOC production by these plant treatments was examined using gas chromatography-mass spectrometry. Cotesia vestalis were able to exploit quantitative and qualitative differences in volatile emissions, from the plant-herbivore complex, produced as a result of different numbers of herbivores feeding. Cotesia vestalis showed a preference for plants with more herbivores and herbivore damage, but did not distinguish between different levels of mechanical damage. Volatile profiles of plants with different levels of herbivores/herbivore damage could also be separated by canonical discriminant analyses. Analyses revealed a number of compounds whose emission increased significantly with herbivore load, and these VOCs may be particularly good indicators of herbivore number, as the parasitoid processes cues from its external environment.

Plant nutrient supply determines competition between phytophagous insects.

Indirect competition is often mediated by plant responses to herbivore feeding damage and is common among phytophagous insect species. Plant-mediated responses may be altered by abiotic conditions such as nutrient supply, which can affect plant growth, morphology, and the concentration of primary and secondary metabolites. Nutrient supply can be manipulated by the type and amount of fertilizer applied to a plant. Brassica oleracea plants were grown in several types of fertilizer, including those commonly used in sustainable and conventional agricultural systems. The occurrence of indirect competition between two phytophagous species from different feeding guilds (a phloem-feeder and leaf-chewer) was assessed. The leaf-chewer reduced aphid populations on plants growing in most fertilizer treatments, but not on those in the ammonium nitrate fertilizer treatment, which caused the highest concentration of foliar nitrogen. The potential consequences of our findings are discussed for phytophagous species in conventional and sustainable agricultural systems.

Varying responses of insect herbivores to altered plant chemistry under organic and conventional treatments.

The hypothesis that plants supplied with organic fertilizers are better defended against insect herbivores than those supplied with synthetic fertilizers was tested over two field seasons. Organic and synthetic fertilizer treatments at two nitrogen concentrations were supplied to Brassica plants, and their effects on the abundance of herbivore species and plant chemistry were assessed. The organic treatments also differed in fertilizer type: a green manure was used for the low-nitrogen treatment, while the high-nitrogen treatment contained green and animal manures. Two aphid species showed different responses to fertilizers: the Brassica specialist Brevicoryne brassicae was more abundant on organically fertilized plants, while the generalist Myzus persicae had higher populations on synthetically fertilized plants. The diamondback moth Plutella xylostella (a crucifer specialist) was more abundant on synthetically fertilized plants and preferred to oviposit on these plants. Glucosinolate concentrations were up to three times greater on plants grown in the organic treatments, while foliar nitrogen was maximized on plants under the higher of the synthetic fertilizer treatments. The varying response of herbivore species to these strong differences in plant chemistry demonstrates that hypotheses on defence in organically grown crops have over-simplified the response of phytophagous insects.

Effects of elevated carbon dioxide and ozone on volatile terpenoid emissions and multitrophic communication of transgenic insecticidal oilseed rape (Brassica napus).

Does transgenically incorporated insect resistance affect constitutive and herbivore-inducible terpenoid emissions and multitrophic communication under elevated atmospheric CO(2) or ozone (O(3))? This study aimed to clarify the possible interactions between allocation to direct defences (Bacillus thuringiensis (Bt) toxin production) and that to endogenous indirect defences under future climatic conditions. Terpenoid emissions were measured from vegetative-stage non-Bt and Bt Brassica napus grown in growth chambers under control or doubled CO(2), and control (filtered air) or 100 ppb O(3). The olfactometric orientation of Cotesia vestalis, an endoparasitoid of the herbivorous diamondback moth (Plutella xylostella), was assessed under the corresponding CO(2) and O(3) concentrations. The response of terpenoid emission to CO(2) or O(3) elevations was equivalent for Bt and non-Bt plants, but lower target herbivory reduced herbivore-inducible emissions from Bt plants. Elevated CO(2) increased emissions of most terpenoids, whereas O(3) reduced total terpenoid emissions. Cotesia vestalis orientated to host-damaged plants independent of plant type or CO(2) concentration. Under elevated O(3), host-damaged non-Bt plants attracted 75% of the parasitoids, but only 36.8% of parasitoids orientated to host-damaged Bt plants. Elevated O(3) has the potential to perturb specialized food-web communication in Bt crops.

Elevated atmospheric ozone increases concentration of insecticidal Bacillus thuringiensis (Bt) Cry1Ac protein in Bt Brassica napus and reduces feeding of a Bt target herbivore on the non-transgenic parent.

Sustained cultivation of Bacillus thuringiensis (Bt) transgenic crops requires stable transgene expression under variable abiotic conditions. We studied the interactions of Bt toxin production and chronic ozone exposure in Bt cry1Ac-transgenic oilseed rape and found that the insect resistance trait is robust under ozone elevations. Bt Cry1Ac concentrations were higher in the leaves of Bt oilseed rape grown under elevated ozone compared to control treatment, measured either per leaf fresh weight or per total soluble protein of leaves. The mean relative growth rate of a Bt target herbivore, Plutella xylostella L. larvae was negative on Bt plants in all ozone treatments. On the non-transgenic plants, larval feeding damage was reduced under elevated ozone. Our results indicate the need for monitoring fluctuations in Bt toxin concentrations to reveal the potential of ozone exposure for altering dosing of Bt proteins to target and non-target herbivores in field environments experiencing increasing ozone pollution.

Investigations into plant biochemical wound-response pathways involved in the production of aphid-induced plant volatiles.

Feeding damage to plants by insect herbivores induces the production of plant volatiles, which are attractive to the herbivores natural enemies. Little is understood about the plant biochemical pathways involved in aphid-induced plant volatile production. The aphid parasitoid Diaeretiella rapae can detect and respond to aphid-induced volatiles produced by Arabidopsis thaliana. When given experience of those volatiles, it can learn those cues and can therefore be used as a novel biosensor to detect them. The pathways involved in aphid-induced volatile production were investigated by comparing the responses of D. rapae to volatiles from a number of different transgenic mutants of A. thaliana, mutated in their octadecanoid, ethylene or salicylic acid wound-response pathways and also from wild-type plants. Plants were either undamaged or infested by the peach-potato aphid, Myzus persicae. It is demonstrated that the octadecanoid pathway and specifically the COI1 gene are required for aphid-induced volatile production. The presence of salicylic acid is also involved in volatile production. Using this model system, in combination with A. thaliana plants with single point gene mutations, has potential for the precise dissection of biochemical pathways involved in the production of aphid-induced volatiles.