Exploitation of interspecific signals to deter oviposition by spotted-wing drosophila

The worldwide invasive fruit pest, Drosophila suzukii, commonly known as spotted wing drosophila (SWD), has spread from Southeast Asia in recent years, causing damage to fruit crops in many countries. The fly was first detected in the UK in Southern England (2012) and its population has subsequently increased and spread north, causing loss of fruit estimated at £20-£30 million pa. All four berry crops are affected (raspberry, strawberry, blueberry and blackberry), in addition to stone fruit (especially cherries). The threat caused by SWD means that many growers are forced to apply increased numbers of applications of insecticides. This strategy is not sustainable for the long term: there are already restrictions aimed at minimizing insecticide residues in fresh produce and preventing the emergence of resistance. Spraying insecticides also compromises the management programmes that growers follow to control other pests, which often include using beneficial natural enemies to reduce pest populations to acceptable levels.

In this three-year research project, we will exploit the strong natural interspecific interactions between SWD and its sister species within the Drosophila melanogaster species group to develop a novel approach to control of the pest. The project will identify new chemical oviposition deterrents that can be applied within the cropping area to deter fruit damage by SWD as a new component of IPM strategies.

The existence of these interspecific oviposition deterrents and their effects on SWD have been demonstrated in our recent experiments. Egg-laying (oviposition behaviour) by SWD was very strongly inhibited following previous exposure of the substrate (fruit or artificial media) to egg-laying by D. melanogaster. Even low numbers of D. melanogaster (five mated females) had strong and persistent inhibitory effects on SWD, with 87% fewer SWD eggs deposited on the substrate that was previously exposed to D. melanogaster, compared with unexposed substrates. This suggests that SWD detect a chemical signal released by D. melanogaster and that this chemical communication between the species results in very strong inhibition of egg laying by the pest.

In this research programme, we will investigate which stage of D. melanogaster (adults or eggs) releases the chemical signals that are responsible for reducing egg-laying by SWD. We will extract the active chemicals from D. melanogaster (and other Drosophila species if these prove to be more effective) and apply the signals (without D. melanogaster individuals present) to egg-laying substrates to demonstrate that the chemical alone is responsible for deterring SWD. We will investigate how SWD detect the active chemical and show whether this is via smell (of relatively volatile chemicals) or taste (non-volatile), by investigating responses of flies that have sense organs missing (removed surgically) or not working (due to genetic modification). This will identify the sense organs responsible for the detection of the chemical deterrent (e.g. the antennae or the mouthparts). We will also record electrical responses of these sense organs to components of extracts that have been separated out (e.g. using chromatography techniques). Combined with other analytical chemistry techniques, we will identify the chemical structure of the active chemical signal for synthesis in the laboratory. Behavioural and electrophysiological effects on SWD will be tested to confirm egg laying deterrent activity, initially, in small-scale lab studies and then in the field on raspberry and strawberry crops. In consultation with growers and representatives from industry, we will design new approaches to pest management that include deploying oviposition deterrents. This research programme will therefore lead to the discovery of new scientifically valuable information on insect signalling and the implementation of new approaches to crop protection.

The spotted wing drosophila, Drosophila suzukii (SWD), is the most serious pest threatening global horticulture and UK fruit production. This invasive species lays its eggs in fresh fruit, meaning growers are increasingly using insecticides for crop protection. Recently published work from NIAB EMR has shown SWD avoid ovipositing in fruit and media previously exposed to the co-occurring species Drosophila melanogaster. This BBSRC-IPA project will elucidate the source and chemical nature of this deterrent and determine the method through which it is perceived by SWD. The results will elucidate how this important pest species has evolved to avoid co-occurring species, and how this behaviour can be exploited for crop protection.

We will conduct oviposition choice assays to determine whether D. melanogaster eggs or adults are the source of the oviposition deterrent, and if this effect is restricted to D. melanogaster, or common among other species which are sympatric with SWD. We will further elucidate the deterrent source through bioassays with chemical extractions from adults and eggs, and use of transgenic lines of D. melanogaster which do not produce cuticular hydrocarbons.

Determining if the deterrent is detected by SWD at a distance via olfaction or on contact via gustation is critical to its exploitation. Thus, we will repeat bioassays using SWD with ablated candidate sensory organs, and transgenic lines with non-functioning olfactory systems. Electrophysiological studies will be used to identify receptors responsible for detection, and to characterize compounds in extracts responsible for oviposition deterrence. These chemicals will be identified through mass-spectrometry, synthesized and then formulated for release as capsules, flakes or sprays which will be tested in semi-field trials for their effectiveness in protecting crops. A knowledge exchange programme will identify how this tool can be best applied by growers for crop protection.

The invasive fruit pest spotted wing drosophila, Drosophila suzukii, has spread from Southeast Asia to Europe and the US in recent years and become the most serious pest threatening the future of the horticulture industries in these countries. In the UK soft and stone fruit has a market value of £480 m and crop losses due to D. suzukii range from 25-100%. Current control measures rely extensively on synthetic insecticides, but regulatory restrictions, ecological impacts and likely future emergence of insecticide resistance make this strategy unsustainable in the longer term. This project will aim to determine the mechanisms through which SWD avoid ovipositing in fruit previously exposed to co-occurring Drosophila species, and how these can be exploited in management of the pest.

Grower Impact
The project is supported by Berry Garden Growers (BGG), the UK's leading berry and stone fruit production and marketing group with a market share of 30% and a year-round business supplying UK retailers. Current cost of control of D. suzukii in the UK is estimated at £20-30 m pa, arising from costs of monitoring, additional pesticide applications, insect mesh, impacts on IPM programmes against other pests and additional labour costs for frequent picking and removal of waste fruit. Growers will benefit from a new approach to control of the pest based on naturally-occurring chemicals that will be compatible with integrated pest management. This will contribute towards improved productivity and reduction of waste in the horticultural industry and help reduce the amount of conventional insecticides used.

Academic Impact
The results of this multidisciplinary project will benefit researchers investigating the role of chemical signals in mediating oviposition behaviour and interspecific interactions in insects in general. As a close relative of the model species D. melanogaster, there is global interest in how D. suzukii has evolved a different reproductive strategy, shifting from ovipositing on rotten fruit to fresh fruit, and the consequences for interspecific interactions between competing species. This project will provide evidence of the chemical and neurological basis through which D. suzukii detect the prior presence of D. melanogaster and other co-occurring species. This information can be applied directly to explore the genetic and evolutionary mechanisms resulting in divergence of ecological niches and reproductive isolation in Drosophila species.

Commercial Impact
As well as growers, economic beneficiaries of this project will include producers and processors of foods which require a supply of fresh, undamaged fruit, and vendors of fresh fruit and fruit products. Sustainable UK fruit production means vendors and processors will be less reliant on imported substitutes and less vulnerable to any future tariffs which this may incur.

Any pest control products arising from this project will require production and marketing by a commercial company which will benefit from sales throughout Europe and the US where D. suzukii occurs.

Wider Impact
This project supports the BBSRC Research in Agriculture and Food Security Strategic Framework, the Government's policy to protect crops while reducing the environmental impact of pesticides (A Green Future: Our 25 Year Plan to Improve the Environment) and the EU Sustainable Use of Pesticides Directive 2009/128/EC. Our technology will reduce the need for pesticides against D. suzukii, reducing pesticide residues in food and water, and negative impacts on economically-important beneficial insects, including pollinators, in crops. Ensuring fruit complies with international standards for pesticide residues is essential for both national consumption and external export.

Rural communities will benefit especially due to reduced threat of job losses and improved productivity in fruit growing regions, with further benefits across the UK where fruit is processed and sold.