Quantifying the impact of Psylliodes chrysocephala injury on the productivity of oilseed rape.

BACKGROUND: Current European Union and United Kingdom legislation prohibits the use of neonicotinoid insecticidal seed treatments in oilseed rape (OSR, Brassica napus). This ban, and the reduction in efficacy of pyrethroid insecticide sprays due to resistance, has exacerbated pest pressure from the cabbage stem flea beetle (Psylliodes chrysocephala) in winter OSR. We quantified the direct impact of P. chrysocephala injury on the productivity of OSR. Leaf area was removed from young plants to simulate differing intensities of adult feeding injury alone or in combination with varying larval infestation levels. RESULTS: OSR can compensate for up to 90% leaf area loss at early growth stages, with no meaningful effect on yield. Significant impacts were observed with high infestations of more than five larvae per plant; plants were shorter, produced fewer flowers and pods, with fewer seeds per pod which had lower oil content and higher glucosinolate content. Such effects were not recorded when five larvae or fewer were present. CONCLUSION: These data confirm the yield-limiting potential of the larval stages of P. chrysocephala but suggest that the current action thresholds which trigger insecticide application for both adult and larval stages (25% leaf area loss and five larvae/plant, respectively) are potentially too low as they are below the physiological injury level where plants can fully compensate for damage. Further research in field conditions is needed to define physiological thresholds more accurately as disparity may result in insecticide applications that are unnecessary to protect yield and may in turn exacerbate the development and spread of insecticide resistance in P. chrysocephala. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Banker Plant Bonuses? The Benefits and Risks of Including Brassicas in Field Margins to Promote Conservation Biocontrol of Specialist Pests in Oilseed Rape.

European agri-environment schemes include the use of flower-rich field margins to promote on-farm biodiversity, but species mixtures rarely include Brassicaceae. As pests of oilseed rape (OSR; Brassica napus) and their parasitoids are mostly brassica specialists, including brassica 'banker plants' in the mixtures would help support these important biocontrol agents and improve pest control throughout the crop rotation. We assessed the potential of six brassicaceous plants (replicated plots grown in the field) to enhance populations of parasitoids of OSR pests whilst minimising proliferation of their pest hosts. Fodder radish (Raphanus sativus) facilitated high production of parasitoids of the pollen beetle pest (Brassicogethes aeneus) but may proliferate Ceutorhynchus weevil pests due to low parasitism. Turnip rape (B. rapa) and the B. rapa hybrid 'Tyfon' showed potential to perform a trap cropping function for pests, but their early flowering phenology resulted in B. aeneus larvae escaping parasitisation, potentially assisting proliferation of this pest. Forage rape B. napus exhibited similarly high B. aeneus parasitoid production characteristics to R. sativus but did not potentiate problems with other pests, indicating that it would be a favourable banker plant option. Careful selection of plants in field margin mixtures is therefore needed to maximise their benefits and ideally the whole crop pest-beneficial complex needs to be studied, as focus on a single major pest risks unintended consequences with other pest problems.

Quantifying inherent predictability and spatial synchrony in the aphid vector Myzus persicae: field-scale patterns of abundance and regional forecasting error in the UK.

BACKGROUND: Sugar beet is threatened by virus yellows, a disease complex vectored by aphids that reduces sugar content. We present an analysis of Myzus persicae population dynamics with and without neonicotinoid seed treatment. We use 6 years' yellow water trap and field-collected aphid data and two decades of 12.2 m suction-trap aphid migration data. We investigate both spatial synchrony and forecasting error to understand the structure and spatial scale of field counts and why forecasting aphid migrants lacks accuracy. Our aim is to derive statistical parameters to inform regionwide pest management strategies. RESULTS: Spatial synchrony, indicating the coincident change in counts across the region over time, is rarely present and is best described as stochastic. Uniquely, early season field populations in 2019 did show spatial synchrony to 90 km compared to the overall average weekly correlation length of 23 km. However, 70% of the time series were spatially heterogenous, indicating patchy between-field dynamics. Field counts lacked the same seasonal trend and did not peak in the same week. Forecasts tended to under-predict mid-season log10 counts. A strongly negative correlation between forecasting error and the proportion of zeros was shown. CONCLUSION: Field populations are unpredictable and stochastic, regardless of neonicotinoid seed treatment. This outcome presents a problem for decision-support that cannot usefully provide a single regionwide solution. Weighted permutation entropy inferred that M. persicae 12.2 m suction-trap time series had moderate to low intrinsic predictability. Early warning using a migration model tended to predict counts at lower levels than observed. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Oilseed rape (Brassica napus) as a resource for farmland insect pollinators: quantifying floral traits in conventional varieties and breeding systems.

Oilseed rape (OSR; Brassica napus L.) is a major crop in temperate regions and provides an important source of nutrition to many of the yield-enhancing insect flower visitors that consume floral nectar. The manipulation of mechanisms that control various crop plant traits for the benefit of pollinators has been suggested in the bid to increase food security, but little is known about inherent floral trait expression in contemporary OSR varieties or the breeding systems used in OSR breeding programmes. We studied a range of floral traits in glasshouse-grown, certified conventional varieties of winter OSR to test for variation among and within breeding systems. We measured 24-h nectar secretion rate, amount, concentration and ratio of nectar sugars per flower, and sizes and number of flowers produced per plant from 24 varieties of OSR representing open-pollinated (OP), genic male sterility (GMS) hybrid and cytoplasmic male sterility (CMS) hybrid breeding systems. Sugar concentration was consistent among and within the breeding systems; however, GMS hybrids produced more nectar and more sugar per flower than CMS hybrid or OP varieties. With the exception of ratio of fructose/glucose in OP varieties, we found that nectar traits were consistent within all the breeding systems. When scaled, GMS hybrids produced 1.73 times more nectar resource per plant than OP varieties. Nectar production and amount of nectar sugar in OSR plants were independent of number and size of flowers. Our data show that floral traits of glasshouse-grown OSR differed among breeding systems, suggesting that manipulation and enhancement of nectar rewards for insect flower visitors, including pollinators, could be included in future OSR breeding programmes.

Mass seasonal bioflows of high-flying insect migrants.

Migrating animals have an impact on ecosystems directly via influxes of predators, prey, and competitors and indirectly by vectoring nutrients, energy, and pathogens. Although linkages between vertebrate movements and ecosystem processes have been established, the effects of mass insect "bioflows" have not been described. We quantified biomass flux over the southern United Kingdom for high-flying (>150 meters) insects and show that ~3.5 trillion insects (3200 tons of biomass) migrate above the region annually. These flows are not randomly directed in insects larger than 10 milligrams, which exploit seasonally beneficial tailwinds. Large seasonal differences in the southward versus northward transfer of biomass occur in some years, although flows were balanced over the 10-year period. Our long-term study reveals a major transport process with implications for ecosystem services, processes, and biogeochemistry.

Dedicated biomass crops can enhance biodiversity in the arable landscape.

Suggestions that novel, non-food, dedicated biomass crops used to produce bioenergy may provide opportunities to diversify and reinstate biodiversity in intensively managed farmland have not yet been fully tested at the landscape scale. Using two of the largest, currently available landscape-scale biodiversity data sets from arable and biomass bioenergy crops, we take a taxonomic and functional trait approach to quantify and contrast the consequences for biodiversity indicators of adopting dedicated biomass crops on land previously cultivated under annual, rotational arable cropping. The abundance and community compositions of biodiversity indicators in fields of break and cereal crops changed when planted with the dedicated biomass crops, miscanthus and short rotation coppiced (SRC) willow. Weed biomass was consistently greater in the two dedicated biomass crops than in cereals, and invertebrate abundance was similarly consistently higher than in break crops. Using canonical variates analysis, we identified distinct plant and invertebrate taxa and trait-based communities in miscanthus and SRC willows, whereas break and cereal crops tended to form a single, composite community. Seedbanks were shown to reflect the longer term effects of crop management. Our study suggests that miscanthus and SRC willows, and the management associated with perennial cropping, would support significant amounts of biodiversity when compared with annual arable crops. We recommend the strategic planting of these perennial, dedicated biomass crops in arable farmland to increase landscape heterogeneity and enhance ecosystem function, and simultaneously work towards striking a balance between energy and food security.

Flight performance of actively foraging honey bees is reduced by a common pathogen.

Sudden and severe declines in honey bee (Apis mellifera) colony health in the US and Europe have been attributed, in part, to emergent microbial pathogens, however, the mechanisms behind the impact are unclear. Using roundabout flight mills, we measured the flight distance and duration of actively foraging, healthy-looking honey bees sampled from standard colonies, before quantifying the level of infection by Nosema ceranae and Deformed Wing Virus complex (DWV) for each bee. Neither the presence nor the quantity of N. ceranae were at low, natural levels of infection had any effect on flight distance or duration, but presence of DWV reduced flight distance by two thirds and duration by one half. Quantity of DWV was shown to have a significant, but weakly positive relation with flight distance and duration, however, the low amount of variation that was accounted for suggests further investigation by dose-response assays is required. We conclude that widespread, naturally occurring levels of infection by DWV weaken the flight ability of honey bees and high levels of within-colony prevalence are likely to reduce efficiency and increase the cost of resource acquisition. Predictions of implications of pathogens on colony health and function should take account of sublethal effects on flight performance.

Temperature-activity relationships in Meligethes aeneus: implications for pest management.

BACKGROUND: Pollen beetle (Meligethes aeneus F.) management in oilseed rape (Brassica napus L.) has become an urgent issue in the light of insecticide resistance. Risk prediction advice has relied upon flight temperature thresholds, while risk assessment uses simple economic thresholds. However, there is variation in the reported temperature of migration, and economic thresholds vary widely across Europe, probably owing to climatic factors interacting with beetle activity and plant compensation for damage. The effect of temperature on flight, feeding and oviposition activity of M. aeneus was examined in controlled conditions. RESULTS: Escape from a release vial was taken as evidence of flight and was supported by video observations. The propensity to fly followed a sigmoid temperature-response curve between 6 and 23 °C; the 10, 25 and 50% flight temperature thresholds were 12.0-12.5 °C, 13.6-14.2 °C and 15.5-16.2 °C, respectively. Thresholds were slightly higher in the second of two flight bioassays, suggesting an effect of beetle age. Strong positive relationships were found between temperature (6-20 °C) and the rates of feeding and oviposition on flower buds of oilseed rape. CONCLUSION: These temperature relationships could be used to improve M. aeneus migration risk assessment, refine weather-based decision support systems and modulate damage thresholds according to rates of bud damage.

So near and yet so far: harmonic radar reveals reduced homing ability of Nosema infected honeybees.

Pathogens may gain a fitness advantage through manipulation of the behaviour of their hosts. Likewise, host behavioural changes can be a defence mechanism, counteracting the impact of pathogens on host fitness. We apply harmonic radar technology to characterize the impact of an emerging pathogen--Nosema ceranae (Microsporidia)--on honeybee (Apis mellifera) flight and orientation performance in the field. Honeybees are the most important commercial pollinators. Emerging diseases have been proposed to play a prominent role in colony decline, partly through sub-lethal behavioural manipulation of their hosts. We found that homing success was significantly reduced in diseased (65.8%) versus healthy foragers (92.5%). Although lost bees had significantly reduced continuous flight times and prolonged resting times, other flight characteristics and navigational abilities showed no significant difference between infected and non-infected bees. Our results suggest that infected bees express normal flight characteristics but are constrained in their homing ability, potentially compromising the colony by reducing its resource inputs, but also counteracting the intra-colony spread of infection. We provide the first high-resolution analysis of sub-lethal effects of an emerging disease on insect flight behaviour. The potential causes and the implications for both host and parasite are discussed.

The ontogeny of bumblebee flight trajectories: from naïve explorers to experienced foragers.

Understanding strategies used by animals to explore their landscape is essential to predict how they exploit patchy resources, and consequently how they are likely to respond to changes in resource distribution. Social bees provide a good model for this and, whilst there are published descriptions of their behaviour on initial learning flights close to the colony, it is still unclear how bees find floral resources over hundreds of metres and how these flights become directed foraging trips. We investigated the spatial ecology of exploration by radar tracking bumblebees, and comparing the flight trajectories of bees with differing experience. The bees left the colony within a day or two of eclosion and flew in complex loops of ever-increasing size around the colony, exhibiting Lévy-flight characteristics constituting an optimal searching strategy. This mathematical pattern can be used to predict how animals exploring individually might exploit a patchy landscape. The bees' groundspeed, maximum displacement from the nest and total distance travelled on a trip increased significantly with experience. More experienced bees flew direct paths, predominantly flying upwind on their outward trips although forage was available in all directions. The flights differed from those of naïve honeybees: they occurred at an earlier age, showed more complex looping, and resulted in earlier returns of pollen to the colony. In summary bumblebees learn to find home and food rapidly, though phases of orientation, learning and searching were not easily separable, suggesting some multi-tasking.

Competition between isolates of Zoophthora radicans co-infecting Plutella xylostella populations.

Interactions between Zoophthora radicans isolates were studied in vitro and in vivo during infection of Plutella xylostella larvae. We distinguished between isolates within infected hosts using PCR-RFLP. Isolates obtained from P. xylostella larvae (NW386 and NW250) were more virulent than isolates from other insect hosts. Isolate NW250 was most virulent at 27°C and isolate NW386 was most virulent at 22°C. In vitro growth of all isolates except NW386 was affected by the presence of other isolates. During in vivo interactions between NW250 and NW386, the isolate with the greatest conidial concentration at inoculation infected more larvae than its competitor. Dual infected larvae were only found in treatments where inoculation concentrations of conidia were high for both isolates. Where concentrations of conidia at inoculation were low for both isolates, only NW250 caused successful infection. The implications of these results for the ecology of Z. radicans are discussed.

Use of honey bees (Apis mellifera L.) to detect the presence of Mediterranean fruit fly (Ceratitis capitata Wiedemann) larvae in Valencia oranges.

BACKGROUND: When fruit deteriorates a characteristic profile of volatile chemicals is produced that is different from that produced by healthy fruits. The identification of such chemicals allows the possibility of monitoring the fruit for early signs of deterioration with biological sensors. The use of honey bees and other insects as biological sensors is well known. This study aimed to identify the volatiles produced by oranges infested with larvae of the Mediterranean fruit fly and to test the ability of honey bees, conditioned to this volatile chemical profile, to detect such oranges. RESULTS: Seventeen compounds that were present in higher concentrations in the volatile profiles of infested oranges than in those of insect-free fruits were mixed at the same relative concentrations as those in the collected volatiles of infested oranges. The synthetic mixture was used to train honey bees by classical Pavlovian conditioning and subsequent tests showed that they were then able to discriminate between medfly-infested and uninfested oranges. CONCLUSION: This study demonstrates an innovative way of detecting, at an early stage, the symptoms of damage to oranges by the Mediterranean fruit fly.

Trophic links between functional groups of arable plants and beetles are stable at a national scale.

1. There is an urgent need to accurately model how environmental change affects the wide-scale functioning of ecosystems, but advances are hindered by a lack of knowledge of how trophic levels are linked across space. It is unclear which theoretical approach to take to improve modelling of such interactions, but evidence is gathering that linking species responses to their functional traits can increase understanding of ecosystem dynamics. Currently, there are no quantitative studies testing how this approach might improve models of multiple, trophically interacting species, at wide spatial scales. 2. Arable weeds play a foundational role in linking food webs, providing resources for many taxa, including carabid beetles that feed on their seeds and weed-associated invertebrate prey. Here, we model associations between weeds and carabids across farmland in Great Britain (GB), to test the hypothesis that wide-scale trophic links between these groups are structured by their species functional traits. 3. A network of c. 250 arable fields, covering four crops and most lowland areas of GB, was sampled for weed, carabid and invertebrate taxa over 3 years. Data sets of these groups were closely matched in time and space, and each contained numerous species with a range of eco-physiological traits. The consistency of trophic linkages between multiple taxa sharing functional traits was tested within multivariate and log-linear models. 4. Robust links were established between the functional traits of taxa and their trophic interactions. Autumn-germinating, small-seeded weeds were associated with smaller, spring-breeding carabids, more specialised in seed feeding, whereas spring-germinating, large-seeded weeds were associated with a range of larger, autumn-breeding omnivorous carabids. These relationships were strong and dynamic, being independent of changes in invertebrate food resources and consistent across sample dates, crops and regions of GB. 5. We conclude that, in at least one system of interacting taxa, functional traits can be used to predict consistent, wide-scale trophic links. This conceptual approach is useful for assessing how perturbations affecting lower trophic levels are ramified throughout ecosystems and could be used to assess how environmental change affects a wider range of secondary consumers.

Use of quantitative PCR to understand within-host competition between two entomopathogenic fungi.

Interactions between the entomopathogenic fungi Zoophthora radicans and Pandora blunckii infecting larvae of Plutella xylostella were investigated. This is the first report to quantify within-host growth of one fungus in the presence of another competing for the same host resource using quantitative PCR (qPCR) at regular time points during the infection process. In larvae inoculated only with Z. radicans, there was a cumulative increase in the quantity of Z. radicans DNA throughout the time course of infection. However, in dual-inoculated larvae, there was an initial accelerated rate of growth of Z. radicans compared to when it was inoculated alone, but by the time of host death it had been effectively excluded by P. blunckii. The implications of these results for co-existence of these fungal pathogens in the field are discussed.

Pollination biology of fruit-bearing hedgerow plants and the role of flower-visiting insects in fruit-set.

BACKGROUND AND AIMS: In the UK, the flowers of fruit-bearing hedgerow plants provide a succession of pollen and nectar for flower-visiting insects for much of the year. The fruits of hedgerow plants are a source of winter food for frugivorous birds on farmland. It is unclear whether recent declines in pollinator populations are likely to threaten fruit-set and hence food supply for birds. The present study investigates the pollination biology of five common hedgerow plants: blackthorn (Prunus spinosa), hawthorn (Crataegus monogyna), dog rose (Rosa canina), bramble (Rubus fruticosus) and ivy (Hedera helix). METHODS: The requirement for insect pollination was investigated initially by excluding insects from flowers by using mesh bags and comparing immature and mature fruit-set with those of open-pollinated flowers. Those plants that showed a requirement for insect pollination were then tested to compare fruit-set under two additional pollination service scenarios: (1) reduced pollination, with insects excluded from flowers bagged for part of the flowering period, and (2) supplemental pollination, with flowers hand cross-pollinated to test for pollen limitation. KEY RESULTS: The proportions of flowers setting fruit in blackthorn, hawthorn and ivy were significantly reduced when insects were excluded from flowers by using mesh bags, whereas fruit-set in bramble and dog rose were unaffected. Restricting the exposure of flowers to pollinators had no significant effect on fruit-set. However, blackthorn and hawthorn were found to be pollen-limited, suggesting that the pollination service was inadequate in the study area. CONCLUSIONS: Ensuring strong populations of insect pollinators may be essential to guarantee a winter fruit supply for birds in UK hedgerows.

Competition and co-existence of Zoophthora radicans and Pandora blunckii, two co-occurring fungal pathogens of the diamondback moth, Plutella xylostella.

The entomopathogenic fungi Zoophthora radicans and Pandora blunckii co-occur in field populations of Plutella xylostella and, therefore, are likely to interact during the infection process. We have investigated the possible outcomes of these interactions in the laboratory. Using four isolates, two of each fungal species, inter-specific interaction experiments were done in Petri dishes and on intact plants. In Petri dish experiments, larvae were inoculated directly using sporulating mats of mycelium, both species had the same opportunity to infect and only the relative concentration of conidia of each pathogen species applied was manipulated. In the intact plant experiments, larvae were placed onto fungus-contaminated plants, inoculation was passive and the probability of infection by either or both species of fungi depended on larval activity and proximity to inoculum. In the Petri dish experiment, the species with the largest concentration of conidia out-competed the other regardless of virulence, and results were similar in the intact plant experiment. The ecological implications for competition or co-existence of these two pathogens in the field are discussed.

Using adult mosquitoes to transfer insecticides to Aedes aegypti larval habitats.

Vector control is a key means of combating mosquito-borne diseases and the only tool available for tackling the transmission of dengue, a disease for which no vaccine, prophylaxis, or therapeutant currently exists. The most effective mosquito control methods include a variety of insecticidal tools that target adults or juveniles. Their successful implementation depends on impacting the largest proportion of the vector population possible. We demonstrate a control strategy that dramatically improves the efficiency with which high coverage of aquatic mosquito habitats can be achieved. The method exploits adult mosquitoes as vehicles of insecticide transfer by harnessing their fundamental behaviors to disseminate a juvenile hormone analogue (JHA) between resting and oviposition sites. A series of field trials undertaken in an Amazon city (Iquitos, Peru) showed that the placement of JHA dissemination stations in just 3-5% of the available resting area resulted in almost complete coverage of sentinel aquatic habitats. More than control mortality occurred in 95-100% of the larval cohorts of Aedes aegypti developing at those sites. Overall reductions in adult emergence of 42-98% were achieved during the trials. A deterministic simulation model predicts amplifications in coverage consistent with our observations and highlights the importance of the residual activity of the insecticide for this technique.

Identification of human-derived volatile chemicals that interfere with attraction of the Scottish biting midge and their potential use as repellents.

The Scottish biting midge, Culicoides impunctatus (Diptera: Ceratopogonidae), is a major pest in Scotland, causing a significant impact to the Scottish tourist and forestry industries. C. impunctatus is a generalist feeder, preferring to feed on large mammals, and is notorious for its attacks on humans. Until now, there was anecdotal evidence for differential attraction of female host-seeking C. impunctatus to individual human hosts, and the mechanism for this phenomenon was unknown. Using extracts of human odor collected by air entrainment, electroantennogram recordings to identify the physiologically active components, followed by behavioral assays, we show, for the first time, the differential attraction of female C. impunctatus to human odors and the chemical basis for this phenomenon. Certain chemicals, found in greater amounts in extracts that cause low attractiveness to midges, elicit a repellent effect in laboratory assays and repellency trials in the field. Differences in the production of these natural human-derived compounds could help to explain differential "attractiveness" between different human hosts. A mixture of two compounds in particular, 6-methyl-5-hepten-2-one and geranylacetone [(E)-6,10-dimethylundeca-5,9-dien-2-one], showed significant repellency (87, 77.4, 74.2, and 31.6% at hours 0, 1, 2, and 3, respectively) in the field and have the potential to be developed as novel repellents.

Identification of human-derived volatile chemicals that interfere with attraction of Aedes aegypti mosquitoes.

It is known that human individuals show different levels of attractiveness to mosquitoes. In this study, we investigated the chemical basis for low attractiveness. We recorded behaviors of Aedes aegypti toward the hands of human volunteers and toward the volatile chemicals produced by their bodies. Some individuals, and their corresponding volatiles, elicited low upwind flight, relative attraction, and probing activity. Analyzing the components by gas chromatography coupled to electrophysiological recordings from the antennae of Aedes aegypti, enabled the location of 33 physiologically relevant compounds. The results indicated that higher levels of specific compounds may be responsible for decreased "attractiveness." In behavioral experiments, five of the compounds caused a significant reduction in upwind flight of Aedes aegypti to attractive human hands. Thus, unattractiveness of individuals may result from a repellent, or attractant "masking," mechanism.

National-scale metacommunity dynamics of carabid beetles in UK farmland.

1. Understanding the wide-scale processes controlling communities across multiple sites is a foremost challenge of modern ecology. Here, data from a nation-wide network of field sites are used to describe the metacommunity dynamics of arable carabid beetles. This is done by modelling how communities are structured at a local level, by changes in the environment of the sampled fields and, at a regional level, by fitting spatial parameters describing latitudinal and longitudinal gradients. 2. Local and regional processes demonstrated independent and significant capacities for structuring communities. Within the local environment, crop type was found to be the primary determinant of carabid community composition. The regional component included a strong response to a longitudinal gradient, with significant increases in diversity in an east-to-west direction. 3. Carabid metacommunities seem to be structured by a combination of species sorting dynamics, operating at two different, but equally important, spatial scales. At a local scale, species are sorted along a resource gradient determined by crop type. At a wider spatial scale species appear to be sorted along a longitudinal gradient. 4. Nation-wide trends in communities coincided with known gradients of increased homogeneity of habitat mosaics and agricultural intensification. However, more work is required to understand fully how communities are controlled by the interaction of crops with changes in landscape structure at different spatial scales. 5. We conclude that crop type is a powerful determinant of carabid biodiversity, but that it cannot be considered in isolation from other components of the landscape for optimal conservation policy.