General Enquiries on This Form Should Be Made To: Defra, Procurements and Contracts Division (Science R&D Team) Telephone No

General enquiries on this form should be made to: Defra, Procurements and Contracts Division (Science R&D Team) Telephone No. 0207 238 5734 E-mail: [email protected] SID 5 Research Project Final Report

 Note In line with the Freedom of Information Act 2000, Defra aims to place the results Project identification of its completed research projects in the public domain wherever possible. The PS2718 SID 5 (Research Project Final Report) is 1. Defra Project designed to capture the information on code the results and outputs of Defra-funded research in a format that is easily 2. Project title publishable through the Defra website. A SID 5 must be completed for all projects. Review of factors including pest biology and control strategies that may explain the increased This form is in Word format and the importance of the leaf miner Scaptomyza flava boxes may be expanded or reduced, as appropriate. 3. Contractor ADAS UK Ltd  ACCESS TO INFORMATION organisation(s) The information collected on this form will be stored electronically and may be sent to any part of Defra, or to individual researchers or organisations outside Defra for the purposes of reviewing the project. Defra may also disclose the information to any outside organisation acting as an agent authorised by Defra to 54. Total Defra project costs £ 17,000 process final research reports on its (agreed fixed price) behalf. Defra intends to publish this form on its website, unless there are strong 03/01/2011 reasons not to, which fully comply with 5. Project: start date ...... exemptions under the Environmental Information Regulations or the Freedom 31/03/2011 of Information Act 2000. end date ...... Defra may be required to release information, including personal data and commercial information, on request under the Environmental Information Regulations or the Freedom of Information Act 2000. However, Defra will not permit any unwarranted breach of confidentiality or act in contravention of its obligations under the Data Protection Act 1998. Defra or its appointed agents may use the name, address or other details on your form to contact you in connection with occasional customer research aimed at improving the processes through which Defra works with its contractors.

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Executive Summary 7. The executive summary must not exceed 2 sides in total of A4 and should be understandable to the intelligent non-scientist. It should cover the main objectives, methods and findings of the research, together with any other significant events and options for new work.

SID 5 (Rev. 07/10) Page 2 of 22 The leaf miner Scaptomyza flava (Fallén) (Diptera: Drosophilidae) has, in recent years, become an increasingly important pest of cruciferous crops. Symptoms have occurred in a wide range of crops, with serious commercial damage occurring in baby-leaf salad crops such as rocket, tatsoi and mizuna as well as in watercress. Crop damage is caused by adult females, which puncture the leaf surface with their ovipositor (egg-laying tube) to feed or lay eggs, and by the larvae, which produce the characteristic white 'corridor-blotch' mines when feeding between the upper and lower surfaces of the leaf.

Oilseed rape crops have also been subject to a large increase in damage symptoms caused by S. flava in 2009 and 2010. The puncturing and leaf mines found in autumn on establishing crops have caused considerable concern amongst growers. However, this damage is not thought to affect crop performance and so there is no apparent need to target S. flava on oilseed rape with insecticide applications.

Scaptomyza flava is a native insect and has not previously been regarded as a pest of major economic importance. The recent increase in damage caused by S. flava is unusual and this project, therefore, was instigated to ascertain the reasons for this change, by reviewing the literature as well as collating expert knowledge/opinion.

This review had the following objectives:

To review agronomic practices in cruciferous crops where increases in incidence of Scaptomyza flava damage have been seen, in order to identify any recent changes in insecticide use.

To determine the frequency of incidental insecticide exposure that Scaptomyza flava may receive in different cruciferous crops.

To compare the biology of Scaptomyza flava with other species of leaf miner including Liriomyza spp. and Phytomyza spp. to consider why S. flava has increased in importance while other leaf miner species have not.

To review the natural enemies of Scaptomyza flava to determine their potential importance in controlling populations of this species of leaf miner.

Pesticide usage statistics indicate that baby-leaf salad crops typically receive repeated insecticide applications to control key pests such as brassica flea beetles and turnip sawfly. Although the number of these applications made to each crop is limited by the short period between sowing and harvest (a few weeks), crops are intensively managed and if pest pressure is high insecticides may be applied as often as twice a week. In addition, baby-leaf salad crops are typically grown sequentially, either on different sites within a given area or on the same land, and so insecticides may be applied regularly in one location over a longer period.

Given the different cropping patterns it is difficult to directly compare insecticide use on baby-leaf salad crops with other potential hosts for S. flava. However, insecticide use on brassica vegetable crops is similar in terms of application timing and the fact that multiple applications are applied in a season. Most insecticides are used on baby-leaf salad crops and vegetable brassicas in the summer and autumn when S. flava is likely to present. Fewer insecticide applications are made to oilseed rape crops and their timing is often outside the summer months when S. flava is most conspicuous.

Insecticide use on crops in which S. flava may be found has been dominated for the past 10 years by the use of pyrethroids. Pyrethroid resistance has developed in other pests (e.g. peach- potato aphid and pollen beetle) of cruciferous crops. Recent HDC-funded research has indicated that pyrethroid resistance may have now developed in S. flava. It seems likely then that the emergence of S. flava as an important pest of cruciferous crops has coincided with the widespread occurrence of pyrethroid resistance in the species.

Insecticide use in baby-leaf salad crops has until recently been targeted against pests such as

SID 5 (Rev. 07/10) Page 3 of 22 brassica flea beetles (Phyllotreta spp.) and turnip sawfly (Athalia rosae) rather than S. flava. Therefore, S. flava has received incidental exposure to insecticides. Given the dominance of pyrethroid insecticides, most notably deltamethrin, which have contact activity only, it seems likely that it is the adult stage of the fly that has been subject to most exposure. Though the larva within the leaf-mine is relatively well protected from pyrethroid applications there is some evidence to suggest that contact may occur at this stage of the pest’s life cycle as well.

Six species of leaf miner are known to feed on members of the Brassicaceae in Britain. Four of these six species, including S. flava, are polyphagous, feeding on host-plants from a range of plant families, while three species, again including S. flava, have been recorded from a wide range of species within the Brassicaceae family. There is however no information available in the literature that may help to explain why S. flava has increased in importance and not another leaf miner species.

There is little information in the literature on the biology of S. flava. We know only that there are several generations in a year and that adults and mines are seen between June/July and September/October. In addition, development times on cruciferous crops are not available nor do we know if successive generations move between crops and, if so, over what distance.

Like other species of leaf miner attacking cruciferous crops, S. flava is attacked by natural enemies including at least eight species of hymenopteran parasitoid. A species of Dacnusa that was previously collected by an agronomist from an S. flava-infested rocket crop was identified by the Natural History Museum as probably either D. scaptomyzae or D. temula during this study. However, there is a lack of information available on the role that parasitoids may play in regulating populations of S. flava in natural and agricultural environments.

Repeated insecticide applications applied to baby-leaf salad crops are likely to have disrupted natural control of S. flava populations. The degree to which parasitism has been disrupted through insecticide applications would depend on the susceptibility of the parasitoid species to insecticides. To date there is no data to describe the impact of insecticide applications on parasitoids attacking S. flava in Britain. However, commercially-available parasitoids used for controlling other leaf miner species on protected crops are very susceptible to pyrethroid insecticides.

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Introduction

The leaf miner Scaptomyza flava has, in recent years, become an increasingly important pest of cruciferous crops. Symptoms have occurred in a wide range of brassicas such as oilseed rape,

SID 5 (Rev. 07/10) Page 4 of 22 cauliflower, calabrese and cabbage, and serious commercial damage has occurred in baby-leaf salad crops such as rocket, tatsoi and mizuna as well as in watercress. Crop damage is caused by adult females, which puncture the leaf surface with their ovipositor to feed or lay eggs, and by the larvae, which produce the characteristic white 'corridor-blotch' mines when feeding between the upper and lower epidermes of the leaf.

In 2009 leaf miner damage caused serious economic losses to producers of baby-leaf salad crops and watercress in central, eastern and southern England. Some growers have since reported damage caused by this pest as early as 2005 while it is also likely that much damage was initially misdiagnosed. Multiple puncture holes made in the harvestable leaves by the adult female fly were the major symptom, with occasional leaf mines also developing. In severe cases up to 40% of leaves were damaged, causing crop write-off or extra pack house costs. In 2010 an HDC-funded study (FV 376) confirmed that S. flava was responsible for the damage seen rather than an Agromyzid leaf miner (Lole, in prep). Further work completed as part of this study suggested that S. flava collected from a rocket crop in East Anglia were resistant to pyrethroid insecticides.

Oilseed rape crops were also subject to a large increase in damage symptoms caused by S. flava in both 2009 and 2010. The puncturing and leaf mines visible in establishing crops in the autumn caused considerable concern amongst growers, but subsequent crop performance seemed unaffected and there is no apparent need to target S. flava on this crop with insecticides.

Scaptomyza flava is a native insect and has not previously been regarded as a pest of major economic importance. However, the recent increase in damage caused by S. flava is unusual and this project, therefore, was instigated to ascertain the reasons for this change by reviewing the literature as well as collation of expert knowledge/opinion.

Aims & Objectives

1. To review agronomic practices in cruciferous crops where increases in incidence of Scaptomyza flava damage have been seen, to identify any recent changes in insecticide use.

A review of recent changes in insecticide use in a range of brassica crops has been completed. This review considered the frequency of insecticide applications made to different crops as well as the insecticide products used. CRD Pesticide Usage Survey data together with information provided by growers has been used.

2. To determine the frequency of incidental insecticide exposure that Scaptomyza flava may receive in different cruciferous crops.

CRD Pesticide Usage Survey data, together with information provided by growers and advisors working in a range of cruciferous crops including oilseed rape and baby leaf salads, has been used to identify typical insecticide use. By considering insecticide use together with S. flava life cycle information the potential for incidental insecticide exposure has been evaluated.

3. To compare the biology of Scaptomyza flava with other species of leaf miner including Liriomyza spp. and Phytomyza spp. to consider why S. flava has increased in importance while these other leaf miner species have not.

Several species of leaf miner are known to attack cruciferous crops grown in Britain. These include Agromyzidae of the genera Liriomyza, Phytomyza and Chromatomyia as well as Drosophilidae belonging to the genus Scaptomyza. The biology of these species has been reviewed to consider why S. flava has emerged as an important pest and not any other species of leaf miner.

4. To complete a review of the natural enemies of Scaptomyza flava to determine their potential importance in controlling populations of this species of leaf miner.

A literature review of natural enemies of S. flava has been completed in order to determine the degree to which predators and parasitoids are likely to regulate populations of this species of leaf

SID 5 (Rev. 07/10) Page 5 of 22 miner. Where the information exists, particular emphasis has been given to the susceptibility of these natural enemies to insecticides.

Review

Review of agronomic practices in cruciferous crops where increases in incidence of Scaptomyza flava damage have been seen to identify any recent changes in insecticide use.

Pesticide usage statistics

The Pesticide Usage Survey collects quantitative and qualitative data on pesticides used in agriculture, horticulture and food storage (http://www.pesticides.gov.uk/environment.asp?id=69). This data has been collected since 1985 and so provides information on trends in pesticide usage over the past 25 years. These trends have been investigated for cruciferous crops known to be attacked by S. flava including baby-leaf salad crops, vegetable brassicas and oilseed rape.

Data on the number of insecticide applications made to baby-leaf salad crops is grouped with lettuce and other leafy salad crops on the Pesticide Usage Statistics website (http://pusstats.csl.gov.uk/index.cfm). The data for this group indicates that crops typically receive repeated insecticide applications (Table 1). As baby-leaf salad crops represent only a proportion of this group of crops the Pesticide Usage Survey team were contacted to provide details of insecticide usage relating specifically to these crops. This data is based on smaller sample size but shows that baby-leaf salad crops received on average 4.9 insecticide applications in 2003 and 2.0 applications in 2007. It is unclear if the reduced number of insecticide applications in 2007 compared with 2003 reflects a trend to reduced insecticide usage or the small sample size from which this data is taken.

Table 1. Proportion (%) of lettuce and other leafy salad crop area receiving different numbers of insecticide applications (Source: http://pusstats.csl.gov.uk/index.cfm)

No. of insecticide applications 1999 2003 2007 0 7 17 12 1 17 11 13 2 13 19 9 3 14 13 13 4 17 24 18 >4 30 16 35

Pesticide Usage Survey reports for Outdoor Vegetable Crops have been published in 2007 (report no. 219), 2003 (report no. 195) and 1999 (report 163). Again data for baby-leaf salad crops is incorporated into a larger group of crops ‘other outdoor vegetables’. Baby-leaf salad crops make up only around 15% of the crop area of this group. These reports summarise the target of the insecticide applications where they were given. Between 1999 and 2007 the most common reason for insecticide applications to this group of crops was to control flea beetles, aphids and caterpillars. These reports also chart the rapid increase in pyrethroid use in this group of crops, rising from 1000 treated hectares in 1999 to 9000 treated hectares in 2007. The Pesticide Usage Survey team again provided insecticide data specific to baby-leaf salad crops for 2003 and 2007. Here deltamethrin was by far the most widely used insecticide while total pyrethroid use increased from 52% of the insecticide-treated area in 2003 to 71% of the treated area in 2007.

Data on the number of insecticide applications applied to vegetable brassica crops (Table 2) is also available from the Pesticide Usage Statistics website (http://pusstats.csl.gov.uk/index.cfm). The proportion of the crop area receiving different numbers of insecticide applications has remained consistent between 1999 and 2007. In 2003 and 2007 there was a relatively even split between crops receiving one, two, three or more than four insecticide applications. By comparison with 1999 the data for 2003 and 2007 suggests a slight reduction in the number of insecticide applications.

SID 5 (Rev. 07/10) Page 6 of 22

Table 2. Proportion (%) of brassica vegetables crop area receiving different numbers of insecticide applications (Source: http://pusstats.csl.gov.uk/index.cfm)

No. of insecticide applications 1999 2003 2007 0 15 13 20 1 17 16 15 2 18 18 20 3 14 15 16 4 7 17 8 >4 29 21 21

The Pesticide Usage Survey reports for Outdoor Vegetable Crops published in 2007 (report no. 219), 2003 (report no. 195) and 1999 (report no. 163) provide details of the stated targets of these applications. Over this period the main targets of these applications have remained broadly the same; aphids and caterpillars as well as flea beetles and cabbage root fly. Timing of these applications varies with crop (including calabrese, cauliflower and Brussels sprouts) but the majority of the insecticide applications were made in the summer or autumn. Again insecticide use was dominated by use of pyrethroids including lambda-cyhalothrin, deltamethrin and bifenthrin. Other insecticides used included pirimicarb and pymetrozine.

Data on the number of insecticide applications applied to oilseed crops (mainly oilseed rape) (Table 3) is again available from the Pesticide Usage Statistics website (http://pusstats.csl.gov.uk/index.cfm). The data shows a consistent pattern between 2000 and 2008 with the majority of crops receiving one or two insecticide applications.

Table 3. Proportion (%) of oilseed crop area receiving different numbers of insecticide applications (Source: http://pusstats.csl.gov.uk/index.cfm)

No. of insecticide applications 2000 2002 2004 2006 2008 0 33 23 19 17 20 1 33 34 32 34 30 2 24 26 28 27 29 3 7 11 12 16 13 4 2 5 6 5 5 >4 1 1 3 1 3

The Pesticide Usage Survey reports for Arable Crops published in 2008 (report no. 224), 2006 (report no. 213), 2004 (report no. 202), 2002 (report no. 187) and 2000 (report no. 171) provide details of the stated targets of these applications. Over this period the main targets have remained the same; cabbage stem flea beetle, pollen beetle, aphids, pod midge and seed weevil. The timing of these applications is typically in the autumn (September, October and November), when winter oilseed rape crops establish and are sprayed against cabbage stem flea beetle and aphids, and spring (April and May) when crops come into flower and are most likely to be treated for the control of pollen beetle and seed weevil.

Insecticide use in oilseed rape crops has been dominated since 2000 by the use of pyrethroids including cypermethrin, lambda-cyhalothrin and tau-fluvalinate. However, more recently the emergence of pyrethroid-resistant pollen beetle has resulted in a greater range of active ingredients being available for control of this pest including thiacloprid, acetamiprid, indoxacarb and pymetrozine, and it is likely that use of the pyrethroids on this crop will reduce as a result. In addition, there is increasing use of insecticide seed treatments in place of traditional autumn spray applications. These seed treatments contain a neonicotinoid such as clothianidin, imidacloprid or thiamethoxam but may also include the pyrethroid beta-cyfluthrin. The most recent survey of pesticide usage on oilseed rape, concerning usage in 2010, is not yet complete and the results are not available at the time of writing.

SID 5 (Rev. 07/10) Page 7 of 22

Pesticide usage by baby-leaf salad crop growers

Neither Scaptomyza flava nor any other species of leaf miner has historically been considered to be a major pest of baby-leaf salad crops. Therefore, until relatively recently insecticide applications have not been targeted against these insects. Baby-leaf salad crops are, however, subject to attack by insect pests, primarily brassica flea beetles (Phyllotreta spp.) and turnip sawfly (Athalia rosae). As a result, baby-leaf salad crops have received regular insecticide applications. The frequency of insecticide applications is to some extent determined by the time of the year and pest pressure but is ultimately driven by increasingly stringent requirements for crop quality. Crop quality requirements refer to leaf blemishes caused by insect feeding (including leaf punctures and mines) as well as the presence of ‘foreign’ bodies that may include both the pest and beneficial insects such as predators or parasitoids.

Baby-leaf salad crops are reliant on specific off-label approvals (SOLAs) for pesticide availability. SOLAs are required because these crops present only a small market to agrochemical companies, making the registration of products for this sector generally uneconomic. For example, only fatty acids and lambda-cyhalothrin currently have on-label approval for use on rocket while maltodextrin, pyrethrins and Beauveria bassiana have approval on all edible crops. There are, however, currently several insecticide products with SOLAs for use on rocket and other leafy brassica crops (Table 4).

Table 4. Insecticide active ingredients available for foliar application through specific off-label approvals (SOLAs) for use on outdoor baby-leaf salad crops and watercress

Active Insecticide class Rocket Tatsoi Mizuna Watercress ingredient alpha- pyrethroid    cypermethrin deltamethrin pyrethroid   lambda- pyrethroid    cyhalothrin pirimicarb carbamate    diflubenzuron benzamide    acetamiprid neonicotinoid  thiacloprid neonicotinoid    spirotetramat tetramic acid  pymetrozine azomethine    spinosad naturalyte    Bacillus microbial     thuringiensis var kurstaki Bacillus microbial  thuringiensis var israelensis

The pyrethroid insecticides have been favoured above the other available insecticides on baby-leaf salad crops for several reasons. They are effective, with a quick knock-down capability which is useful in eliminating transient contaminants from the crop. They have a short harvest interval (e.g. for deltamethrin there is no specified harvest interval) and there may be no limit to the number of treatments that can be applied (e.g. deltamethrin). They are also cheap. None of the other available pesticides have all of these features.

Baby-leaf salad growers have in recent years experienced significant losses as a result of puncture holes produced by adult female S. flava. Growers have been unable to reduce damage caused by this pest to commercially acceptable levels through insecticide use alone. As a result several growers are now using netting to physically exclude S. flava from the crop. This approach has proved to be effective in reducing leaf puncture damage but represents a considerable financial investment in the purchase and deployment of the netting. However, one advantage of using netting is that other pests, such as flea beetles and turnip sawfly, are also excluded from the crop, and it also circumvents the problem of few alternative, effective pesticides being available. By using netting, insecticide applications may be

SID 5 (Rev. 07/10) Page 8 of 22 reduced and may only be needed to kill insects trapped when the netting was initially used to cover the crop.

Pesticide efficacy

Most baby-leaf salad growers reported significant damage caused by S. flava in 2009 and 2010. However, significant damage caused by this pest has been noted by some growers as early as 2005 (Emmett, pers. comm.). Baby-leaf salad growers are primarily located along the south coast, mainly in Kent, Sussex and Hampshire, as well as in East Anglia. Despite this limited geographic distribution growers have reported different levels of damage caused by this pest at different sites. For example, one grower considered S. flava to be more of a problem in crops grown in Kent than those grown in neighbouring Sussex.

The fact that growers of baby-leaf salad crops have been unable to prevent leaf puncture damage through insecticide use is in part explained by the difficulty in targeting adult S. flava. Adult female flies puncturing sprayed leaves may ultimately die but may still have caused significant damage before this occurs. In addition, crops such as rocket are fast growing, producing fresh leaves in just a few days. As a result, contact-acting insecticides, such as pyrethroids, need to be re-applied regularly to limit damage to new leaves.

In a recent HDC funded study (FV 376) a range of insecticides (Table 5) as well as a netting treatment were compared for their efficacy in controlling leaf puncture damage caused by S. flava (Lole, in prep). None of the insecticides tested significantly reduced leaf puncture damage compared with the untreated control. By comparison, the netting treatment significantly reduced the level of leaf puncture damage.

Table 5. Insecticides tested for efficacy in reducing leaf puncture damage caused by Scaptomyza flava as part of HDC project FV376

Active ingredient Insecticide class deltamethrin pyrethroid dimethoate organophosphate garlic extract plant extract fatty acids soap cyazypyr anthranilic diamide thiacloprid neonicotinoid spirotetramat tetramic acid spinosad naturalyte

Growers noted control failures when pyrethroid insecticides were sprayed against S. flava in 2009 and 2010. Therefore, as part of project FV 376 a preliminary investigation into pyrethroid resistance in S. flava was completed. Here pollen beetle pyrethroid resistance testing kits were used. These kits consist of vials coated internally with different rates of lambda-cyhalothrin and in a modification from the pollen beetle testing method a small piece of damp filter paper was added to each vial during the test to ensure high humidity. Results from this experiment found that mortality of adult S. flava was not significantly increased compared with the untreated control when field-caught flies were placed in vials coated with a field-equivalent rate (0.075 µg/cm2) of lambda-cyhalothrin. Only the highest rate of lambda-cyhalothrin tested (0.375 µg/cm2) significantly increased mortality of the flies.

Insecticide efficacy experiments completed in New Zealand identified a number of insecticides (Table 6) that were effective at killing adult female S. flava under laboratory conditions (Martin et al. 2006). These laboratory bioassays were completed by exposing the adult female to leaves treated with an insecticide and recording mortality after 48 hrs. In a second bioassay, in which young larvae within a leaf-mine were dipped into an insecticide solution, the same group of insecticides was found to be effective. The ability to kill the larvae in the leaf mine should in part reflect the trans-laminar or systemic activity of an insecticide. The pyrethroid, deltamethrin, does not have trans-laminar or systemic properties and so its ability to kill larvae within the leaf-mine is surprising, although it should be noted that dipping a leaf in an insecticide solution does not directly mimic the field situation. The ability of

SID 5 (Rev. 07/10) Page 9 of 22 deltamethrin to kill leaf miner larvae within the mine has previously been reported for agromyzid leaf miners (Richter & Tsegaye, 1988; Zhang et al. 1999). This could be due to some of the insecticide entering the leaf mines through oviposition punctures or larval exit holes after foliar application, as this is known to occur when entomopathgenic nematodes are applied for the control of the tomato leaf miner, Liriomyza bryoniae on tomato (Bennison et al 2007).

Table 6. Insecticides shown to be effective at killing adult and larval stages of Scaptomyza flava under laboratory conditions (Source: Martin et al. 2006)

Active ingredient Insecticide class abamectin avermectins acephate organophosphate deltamethrin pyrethroid endosulfan organophosphate fipronil phenylpyrazole indoxacarb oxadiazine maldison organophosphate methamidophos organophosphate spinosad naturalyte

Martin et al. also tested seven of these insecticides under field conditions. Despite the encouraging results from the laboratory only one insecticide, abamectin, was consistent in significantly reducing the percentage of leaves with leaf mines. Deltamethrin and fipronil were also effective when applied to pak choi, but not joi choi, in one of the two trials completed. No record was made of the effect that the insecticides had on leaf puncture damage in this study. It should also be noted that abamectin is not currently approved for use outdoors in the UK on baby-leaf salad crops and was not included in the recent HDC-funded trial.

There appear to be no records of observations of the efficacy of insecticide applications (sprays or seed dressings) in controlling S. flava on oilseed rape.

Determine the frequency of incidental insecticide exposure that Scaptomyza flava may receive in different cruciferous crops.

Pesticide usage statistics indicate that baby-leaf salad crops typically receive repeated insecticide applications. Growers of baby-leaf salad crops contacted for this report have confirmed that repeated insecticide applications have been used to control insect pests. These applications are typically driven by increasingly stringent requirements for crop quality (growers indicate that a maximum of five feeding marks per leaf may be allowed) rather than yield. Furthermore, the high value of these crops means that repeated use of control measures can be justified financially.

Pesticide usage statistics and information provided by individual growers indicates that until recently insecticide applications to baby-leaf salad crops have not targeted S. flava or other species of leaf miner. Instead, insecticide applications have primarily been targeted against brassica flea beetles and turnip sawfly and so exposure of S. flava to these applications has been incidental. The pyrethroid insecticides remain effective against flea beetles and turnip sawfly and so have continued in use despite their failure to control S. flava.

Baby-leaf salad crops are of short duration, as little as one month being required between sowing and harvest. As a result, crops are grown sequentially throughout the year, with the first sowing in mid- to late March and the last harvest in early to mid-October. Although crops are grown sequentially, growers typically alternate between fields but if the same field is to be used more than once in a year the soil will often be sterilised between plantings.

Mines produced by S. flava are reported in the literature (Pitkin et al. 2011) and by growers to be seen from June/July through to September/October. They may be seen in oilseed rape crops even earlier than this, in April and May in the UK. As such, S. flava has potentially been subject to incidental insecticide exposure for much of the season. The frequency of incidental exposure reported by growers

SID 5 (Rev. 07/10) Page 10 of 22 may have been as often as twice a week, with pyrethroids being sprayed every 3-4 days. Therefore, despite the short duration of crops such as rocket up to six applications may still have been applied. Movement of S. flava between sequential baby-leaf salad crops has not been established, but the flies are strong fliers and growers report crops being subject to attack even when they are not adjacent to previous crops, suggesting that adult flies move readily between crops.

The majority of insecticide use in vegetable brassicas is in summer and autumn, so these insecticide application timings coincide with S. flava activity and are probably responsible for considerable selection pressure for resistance. In oilseed rape, most insecticide applications are made either in the spring, perhaps before S. flava is active, or in the autumn, at the very end of the season for this species. The selection pressure exerted on S. flava by these treatments, therefore, may be less, given the timing and the relatively small number of insecticide applications entailed now that seed dressings are replacing autumn-applied sprays. Having said this, the area of oilseed rape treated is much larger than the area of vegetable Cruciferae treated and perhaps the number of individual S. flava challenged on oilseed rape is therefore significant.

Incidental exposure of S. flava to pyrethroid insecticides is thought to primarily occur at the adult stage. This is because pyrethroids are contact insecticides that are not translaminar or systemic in the plant. As a result the egg and larval stages of S. flava largely escape pyrethroids. Despite this, a number of studies have found that the pyrethroid deltamethrin is effective against S. flava as well as agromyzid larvae in leaf-mines (Martin et al. 2006; Richter & Tsegaye, 1988; Zhang et al. 1999). As discussed previously, this could be due to some of the insecticide entering the leaf mine through oviposition punctures or larval exit holes.

The use of insecticide seed treatments on potential host-plants of S. flava is restricted to oilseed rape. These seed treatments contain a neonicotinoid that would move systemically through the plant as it establishes in the autumn, and one also contains the pyrethroid beta cyfluthrin. There would be potential for incidental insecticide exposure following the use of insecticidal seed dressings during the end of the S. flava activity period, but it is not known how effective these seed dressings are in controlling S. flava, either adults or larvae. The appropriate observations do not appear to have been made.

Comparison of the biology of Scaptomyza flava with other species of leaf miner including Liriomyza spp. and Phytomyza spp. to consider why S. flava has increased in importance while other leaf miner species have not.

Over 900 species of insect are recorded as miners of leaves, stems, flower heads and fruits of growing plants in Britain (Pitkin et al. 2011). The majority of insects recorded as miners in Britain are species of moth (Lepidoptera) but larvae of other insects including flies (Diptera), sawflies (Hymenoptera) and beetles (Coleoptera) also develop in this way.

Flies are the second-largest group of miners with over 340 species recorded (Pitkin et al. 2011). These species of fly are found in the following 11 families (Table 7).

Table 7. Fly families containing species of miner found in Britain

Family No. species Family No. species Agromyzidae 284 Psilidae 1 Anthomyiidae 37 Scathophagidae 4 Chironomidae 3 Sciaridae 2 Dolichopodidae 2 Syrphidae 1 Drosophilidae 5 Tephritidae 9 Ephydridae 10

These species of fly create mines as the larvae feed, grow and move through the leaf or stem. Leaf mines are usually visible but stem mines may be cryptic. Often the shape of the leaf mines is characteristic of certain species and this, together with an understanding of the species’ host range,

SID 5 (Rev. 07/10) Page 11 of 22 often allows for fairly reliable pest identification. Mines produced by dipteran species may be readily differentiated from other insects by the semi-circular exit hole cut through the leaf epidermis (Pitkin et al. 2011). Dipteran mining larvae (often referred to as maggots) also characteristically lack a head capsule and legs.

The majority of dipteran miners do not cause economic damage under normal conditions. However, a small number of species have previously been recorded as pests of agricultural or horticultural crops (Spencer, 1973; Gratwick, 1992). These include the beet leaf miner (Pegomya hyoscyami (Panzer)), the cabbage leaf miner (Phytomyza rufipes Meigen), the celery fly (Euleia heraclei (L.)), the tomato leaf miner (Liriomyza bryoniae (Kaltenbach)) and the chrysanthemum leaf miner (Chromatomyia syngenesiae (Hardy)). The non-indigenous South American leaf miner (Liriomyza huidobrensis) and American serpentine leaf miner (Liriomyza trifolii) have also caused problems on protected crops including the Chinese leafy salad crops choi sum and pak choi (Bennison et al 1999, 2007). These latter species are quarantine pests in the UK, are not established here and any suspected infestations must be reported to the Defra Plant Health and Seeds Inspectorate (PHSI).

This review focussed on two dipteran families, Drosophilidae and Agromyzidae, which are known to contain species that attack cruciferous crops. Another family, the Ephydridae, also contains two species, Hydrellia pubescens and Hydrellia ranunculi, which have been recorded from a cruciferous crop, watercress, although it is unclear if this record is from Britain.

Drosophilidae – contains five species of leaf miner, all of which are in the genus Scaptomyza (Table 8).

Table 8. Species of Drosophilidae miners in Britain and host plant families attacked (from Pitkin et al. 2011)

Species Hosts Scaptomyza flava (Fallén) Asteraceae, Brassicaceae, Papaveraceae, Resedaceae, Tropaeolacea, Violaceae Scaptomyza graminum (Fallén) Amaranthaceae, Brassicaeae, Caryophyllaceae, Chenopodiaceae, Fabaceae, Portulaceae, Scrophulariaceae Scaptomyza griseola (Zetterstedt) Brassicaceae, Caryophyllaceae, Potomogetonaceae Scaptomyza pallida (Zetterstedt) Liliaceae Scaptomyza sp. Unknown

Of these species of Scaptomyza, only S. flava, S. graminum and S. griseola are known to feed on plants belonging to the Brassicaceae and are considered in more detail below.

Scaptomyza flava (Fallén) has been recorded feeding on host plants belonging to a range of plant families in Britain, including the Asteraceae, Brassicaceae, Papaveraceae, Resedaceae, Tropaeolaceae and Violaceae (Stubbs & Chandler, 1978; Pitkin et al. 2011). The Brassicaceae host plants include garlic mustard (Alliaria petiolata), winter-cress (Barbarea vulgaris), turnip (Brassica rapa syn. campestris), cabbage (Brassica oleracea), wallflower (Cheiranthus sp.), common scurvygrass (Cochlearia officinalis), Lundy cabbage (Coincya wrightii), hare’s ear mustards (Conringia sp.), perennial wall-rocket (Diplotaxis tenuifolia), wallflower (Erysimum sp.), dittander (Lepidium latifolium), hoary stock (Mattiola incana), garden radish (Raphanus sativus), water-cress (Nasturtium officinale) and charlock (Sinapis arvensis), but there are many others.

Scaptomyza flava is distributed throughout Britain and is widespread throughout continental Europe (Pitkin et al. 2011). In Britain mines produced by this species have typically been seen between July and October. These corridor-blotch mines are usually on the upper leaf surface and are whitish in colour. In smaller leaves the mine lies in the centre of the leaf and often touches the petiole, while in

SID 5 (Rev. 07/10) Page 12 of 22 larger leaves the mine is to one side of the mid-rib. Frass is usually deposited in green clumps near the margin of the mine. Larvae usually drop to the ground to pupate but sometimes a separate pupation mine is used.

Adults are generally most abundant in September (Pitkin et al. 2011), though sticky trapping in 2010 showed that local peaks of activity could occur in July or August. Mating in this species occurs following a courtship display by the male fly, which includes wing flapping (Shakeel et al. 2010). Mated females oviposit in punctures made within the lower surface of the leaf (Pitkin et al. 2011). The hatching larva initially moves toward the mid-rib, creating a long corridor. Once at the mid-rib the larva forms a large irregular blotch in the upper leaf surface with occasional excursions into the leaf blade. Several larvae may be present in the same mine and if the leaf is small the entire leaf may be occupied.

There is no information on the number of generations completed by this species in Britain, apart from references to ‘several generations’ in text books (Edwards & Heath, 1964; Alford, 1999).

Scaptomyza graminum (Fallén) has been recorded feeding on a single species, water-cress (Nasturtium officinale), within the Brassicaceae (Pitkin et al. 2011).

Scaptomyza graminum is distributed throughout Britain and is widespread throughout continental Europe (Pitkin et al. 2011). In Britain, mines produced by this species are typically found in March, June-July and September-October. The mines usually begin as a corridor in the upper surface as the larva moves to the mid-rib. The blotch is also in the upper surface but in small leaves may be full-depth. The blotch has broad lobes in which the frass typically accumulates. Several larvae may share a single mine. Once the larvae have completed their development they either pupate in the soil or in a separate pupation mine.

There appear to be at least two generations in Britain and adult flies are most abundant in July and October.

Scaptomyza griseola (Zetterstedt) has been recorded feeding on few host plant species including those belonging to the Brassicaceae, Caryophyllaceae and the Potomogetonaceae (Pitkin et al. 2011). The Brassicaceae host plants include species of Brassica and Sisymbrium.

Scaptomyza griseola is widely distributed throughout Britain and continental Europe (Pitkin et al. 2011). In Britain mines produced by this species are typically seen in July. Mines are similar to those produced by S. flava but the blotch has lower and upper surface parts and is full depth where these overlap. Larvae pupate in the ground.

Adults are most abundant in May and October and this species appears to have at least two generations a year.

Agromyzidae – contains 83% of dipteran mining species found in Britain, although the family also includes species with different life histories, including gall-formers as well as root- and seed-feeders. Spencer (1973) compiled a comprehensive checklist of host plants by family and their miners. Since this checklist was created a number of host-plant associations have been added or removed and a number of species new to Britain (Pitkin et al. 2011) have been recorded. The following section considers three genera of miner belonging to this family, namely Phytomyza, Liriomyza and Chromatomyia. Phytomyza is a large genus containing over 100 species found in Britain but only one, P. rufipes, feeds on members of the Brassicaceae. Liriomyza is also a large genus with over 40 species found in Britain but again only one native species, L. strigata, feeds on members of the Brassicaceae. The non-indigenous L. huidobrensis and L. trifolii have occasionally been introduced to the UK and also feed on members of the Brassicaceae, including protected Chinese leafy salad crops. However, as these species are non-indigenous they are not considered further in this review. Chromatomyia is a smaller genus with 22 species found in Britain, with one native species, C. horticola, that feeds on members of the Brassicaceae.

SID 5 (Rev. 07/10) Page 13 of 22

Phytomyza rufipes Meigen (cabbage leaf miner) is a specialist, feeding only on species belonging to the Brassicaceae (Spencer, 1973). Host plants include leaf mustard (Brassica juncea), swede and rapeseed (Brassica napus), kale (Brassica oleracea var. acephala), cauliflower (Brassica oleracea var. botrytis), cabbage (Brassica oleracea var. capitata), Brussels sprouts (Brassica oleracea var. gemmifera), broccoli (Brassica oleracea var. italica), and turnip (Brassica rapa) (Spencer, 1973; Pitkin et al. 2011).

Phytomyza rufipes is widely distributed throughout Britain and continental Europe as well as the USA and Canada (Pitkin et al. 2011). In Britain, mines are typically seen between May and June. The mine usually begins in the lower leaf surface and produces a corridor as it nears the mid-rib. The larva then bores into the mid-rib and sometimes into the petiole. Up to 10 larvae can be found in a single stalk (Spencer, 1973).

The adult flies typically appear in May or June (Spencer, 1973). Adult females oviposit in the leaf-blade, often close to a vein at the leaf margin. Each female may lay up to 81 eggs and on average lays five eggs per day. Eggs hatch in 3-4 days, larval development takes around 12 days and the pupal period lasts for 19 days. Pupation usually takes place in the soil and soil populations of 110,000 to 3,630,000 per hectare were reported in fields of swedes in Norfolk in 1949 (Spencer, 1973).

There are at least four generations a year and larvae may still be seen actively feeding in November (Spencer, 1973). Damage to young plants may result in malformations and yellowing of the heart leaves. Plants may recover, but if attacked at a young stage yield is likely to be affected. Damage to older plants is usually less important as it is the older, outer leaves that are damaged and these are often discarded at harvest.

Liriomyza strigata (Meigen) is highly polyphagous and has been recorded feeding on species belonging to the plant families Apiaceae, Asteraceae, Brassicaceae, Campanulaceae, Chenopodiaceae, Compositae, Convolvulaceae, Dipsacaceae, Euphorbiaceae, Fabaceae, Lamiaceae, Linaceae, Malvaceae, Papaveraceae, Polemoniaceae, Resedaceae, Valerianaceae and Violaceae (Spencer, 1973; Pitkin et al. 2011). The Brassicaceae host plants include Brassica spp. and shepherd’s purse (Capsella bursa-pastoris).

Liriomyza strigata is widely distributed throughout Britain and continental Europe (Pitkin et al. 2011). In Britain mines are typically seen between June and November. The adult fly lays eggs near to the leaf margin and the young larva initially mines the lower leaf surface before moving above the mid-rib to form the main mine (Spencer, 1973). The mines produced by this species are distinctive in that they sit above the mid-rib and have short lateral offshoots into the leaf blade. Frass appears in the mines as long strings (Spencer, 1973). The larvae leave the plant to pupate in the soil.

Young plants are not normally attacked and although L. strigata is common, large populations on a single plant are rarely found (Spencer, 1973). As a consequence there have been no records of L. strigata causing economic damage to crops, although the wide host-range of this species means that there remains the potential for it to become a pest. Naturally-occurring parasitoids are thought to exert effective control of L. strigata populations under normal conditions.

Chromatomyia (Phytomyza) horticola (Goureau) (pea leaf miner) is a highly polyphagous species, feeding on host plants belonging to the Apiaceae, Asteraceae, Brassicaceae, Campanulaceae, Cannabaceae, Chenopodiaceae, Cucurbitaceae, Fabaceae, Labiatae, Lamiaceae, Liliaceae, Linaceae, Malvaceae, Papaveraceae, Plantaginaceae, Resedaceae, Scrophulariaceae, Solanaceae and Valerianaceae (Spencer, 1973; Pitkin et al. 2011). The Brassicaceae host plants include garlic mustard (Alliaria petiolata), horse-radish (Armoracia rusticana), black mustard (Brassica nigra), field mustard (Brassica rapa), rapeseed (Brassica napus), cabbage (Brassica oleracea), shepherd’s purse (Capsella bursa-pastoris), Cheiranthus cheiri, Lundy cabbage (Coincya wrightii), garlic mustard (Conringia orientalis), dame’s violet (Hesperis matronalis), hoary cress (Lepidium draba), Sinapis sp., Sisymbrium assoanum, hedge mustard (Sisymbrium officinale) and Thlaspi spp.

SID 5 (Rev. 07/10) Page 14 of 22 Chromatomyia horticola is widely distributed throughout southern Britain and is also found throughout continental Europe. It is, however, more common in Mediterranean areas than in northern Europe. This species also occurs widely in Asia as well as parts of Africa (Spencer, 1973; Pitkin et al. 2011). In Britain mines are typically seen in late spring and autumn. While in Britain this species is thought to have two generations a year, in western Europe there may be 3-4. The mine is irregular-linear and occupies both the upper and lower parts of the leaf. Frass appears in the mines as isolated grains. At temperatures of 23-28°C, the larval period can be as short as 5-6 days. This species is characterised along with a few others by the type of pupation, which is in the leaf. The larva moves to the end of the mine before directing the anterior spiracles through the leaf epidermis. Pupation takes between seven and 15 days but may last for several months during aestivation or hibernation.

The adult female fly may lay a total of up to 350 eggs and up to 50 in a single day (Spencer, 1973). The adult female may make up to 154 feeding puncture holes on a single Pisum sp. leaf, although this may be exceptional and other researchers have recorded up to 38 puncture holes.

In Britain, C. horticola has been associated with pea crops and severe damage caused by this species has been reported (Spencer, 1973). Mining damage usually causes leaf withering and premature dropping. The feeding puncture holes may also cause appreciable damage to the leaf. Despite this damage mature crops are usually able to tolerate even heavy infestations. Naturally-occurring parasitoids are thought to control numbers of this species under normal conditions.

It should be noted that C. horticola is indistinguishable from C. syngenesiae in the shape of the mine or the adult fly (Pitkin et al. 2011). Only by examining the male genitalia can these species be differentiated. As a result there is the potential for these species to have been misidentified and it is generally unclear from which host parasitoids have been reared from. However, where records of the host-plant are also taken then discrimination should be possible, at least for the Brassicaceae, which is not a host for C. syngenesiae.

A review of the natural enemies of Scaptomyza flava to determine their potential importance in controlling populations of this species of leaf miner.

Leaf miners belonging to the Agromyzidae, such as P. rufipes and L. strigata are thought to be well controlled by their natural enemy complex under normal conditions (Spencer, 1973). There is little information on the importance of natural enemies in controlling populations of S. flava in Britain. However, anecdotal evidence from Thanet, Kent suggests that parasitism may be important in reducing populations of this leaf miner later in the season (Emmett pers. comm.). The species responsible for the parasitism seen in Thanet has been identified through this study by the Natural History Museum as a braconid species, Dacnusa sp. (probably either D. scaptomyzae or D. temula). Other species of parasitoid (Table 9) attacking S. flava that we have records for are all chalcidoids (Pitkin et al. 2011).

Table 9. Hymenopteran parasitoids recorded attacking Scaptomyza flava in Britain (Source: Pitkin et al. 2011)

Species Family Chrysocharis pallipes Eulophidae Chrysocharis viridis Eulophidae Cyrtogaster vulgaris Pteromalidae Halticoptera patellana Pteromalidae Halticoptera smaragdina Pteromalidae Spalangiopelta alata Pteromalidae Dacnusa scaptomyzae Braconidae Dacnusa temula Braconidae

Of the parasitoids listed in Table 9 it is interesting to note that four of the eight species are recorded attacking other species of leaf miner that feed on members of the Brassicaceae (Table 10). Indeed, these four parasitoids appear to be able to attack leaf miners belonging to different families. Despite this it should be remembered that each of the alternate leaf miner hosts is also attacked by other

SID 5 (Rev. 07/10) Page 15 of 22 parasitoid species that do not also attack S. flava. There is also a lack of information on the relative importance of each parasitoid species for each leaf miner species feeding on a cruciferous crop.

Table 10. Hymenopteran parasitoids recorded attacking Scaptomyza flava and other leaf miner species feeding on members of the Brassicaceae in Britain (Source: Pitkin et al. 2011).

Species Alternate host Chrysocharis pallipes Scaptomyza graminum Liriomyza strigata Chrysocharis viridis Chromatomyia horticola Cyrtogaster vulgaris Chromatomyia horticola Halticoptera smaragdina Phytomyza rufipes

Spencer (1973) suggested that the normal control of leaf miners belonging to the Agromyzidae by parasitoids could be disrupted in a number of ways. Firstly, Spencer suggested that there may be a loss of synchrony between emergence of the parasitoid and its host or that parasitoid numbers may be reduced due to disease or unfavourable climatic conditions. These disruptions are usually short lived before the pest is brought back under control by parasitoids. Spencer also suggested that long-term use of insecticides may disrupt natural parasitoid control of Agromyzid species. Here there are a number of examples including the tomato leaf miner Liriomyza bryoniae, which first caused severe damage to tomato in the Lea Valley in Hertfordshire, England in 1948 (Speyer & Parr, 1948). The damage caused by this leaf miner was due to the fact that the Braconid parasitoids that normally regulated populations of this species were more susceptible to DDT than the leaf miner host. In current production of protected tomato and other crops susceptible to various species of leaf miner, including ornamental crops and herbs, the commercially-available parasitoids Dacnusa sibirica and Diglyphus isaea are routinely released for leaf miner control. These parasitoids can give very effective control of leaf miners if managed carefully (Sampson & Walker 1998) and as long as only selective pesticides are used on the crops, within Integrated Pest Management (IPM) programmes. D. sibirica and D. isaea have also given promising control of L. huidobrensis on protected lettuce, choi sum and pak choi (Bennison et al 1999).

In New Zealand, where S. flava is considered to be a pest of brassica crops as well as pea and gypsophila, experiments have been completed to test the impact of insecticides on a larval/pupal parasitoid (Martin & MacDonald, 2009). Asobara persimilis (Braconidae) has been recorded to achieve high levels of parasitism of S. flava in New Zealand (this species is not found in Britain). In laboratory bioassays, A. persimilis adults were exposed to dry residues of insecticides applied to leaf discs and mortality was recorded after 48 hours. Endosulfan (cyclodiene organochlorine), fipronil (phenyl pyrazole), indoxacarb, maldison (organophosphate) and methamidophos (organophosphate) killed 100% of parasitoids. Acephate (organophosphate) and pirimicarb (carbamate) produced mortality rates that were significantly lower than for the insecticides killing 100% of the parasitoids but that were still higher than for the water control. Abamectin (avermectin), Bacillus thuringiensis aizawai, pymetrozine and spinosad (spinosyn) produced mortality rates that did not differ significantly from the water control.

In field experiments, insecticides were applied every two weeks after the first leaf mines had been seen (Martin & MacDonald, 2009). In this way each crop was sprayed three times before harvest. Insecticides tested included abamectin, acephate, deltamethrin, endosulfan, fipronil, indoxacarb and spinosad. By collecting treated leaves of joi choi or pak choi sum (Brassica rapa chinensis) with blotch mines it was possible to record the numbers of S. flava and parasitoids successfully emerging from leaves collected from each insecticide treatment. In each of the trials completed, with one exception of spinosad for one trial, significantly more pupae were collected from untreated plots than from those treated with an insecticide. Between 77 and 98% of the pupae collected from untreated plots successfully emerged as either a fly or a parasitoid. However, the proportion of flies and parasitoids varied widely from 5 to 98% of the pupae collected emerging as flies and 0 to 82% of the pupae emerging as parasitoids. Given such large variation for the untreated control it is not possible to conclude whether the insecticide applications affected rates of parasitism. However it is true that parasitoids successfully emerged from leaves treated with each of the insecticides tested. This includes insecticides such as endosulfan, fipronil and indoxacarb that killed 100% of adult parasitoids that were

SID 5 (Rev. 07/10) Page 16 of 22 exposed to residues of these chemicals in the laboratory. This result would appear to support the view that the adult parasitoid is the most susceptible life-stage to insecticide applications.

Although parasitoids are likely to be most important natural enemy of leaf miners in terms of controlling population size, other predatory insects may also feed on leaf miners. These often generalist predators include species of wasp and ant, which may open the leaf to access the larva in the mine. Other predators such as predatory bugs can use their piercing mouthparts to attack the larva beneath the leaf epidermis. Entomopathogenic nematodes have also been used for control of leaf miners in protected crops including tomato, chrysanthemum, protected lettuce and Chinese brassicas (Williams & MacDonald 1995).

Discussion

Assessment of agronomic practices in cruciferous crops where increases in incidence of Scaptomyza flava damage have been seen to identify any recent changes in insecticide use.

Pesticide usage statistics indicate that baby-leaf salad crops typically receive repeated insecticide applications. Over recent years the level of insecticide use will have varied depending upon pest pressure. Indeed, grower information points to frequent insecticide applications to control key pests. While the number of these applications applied to each baby-leaf salad crop would have been limited by the short duration of these crops, the sequential planting of crops would mean that through the year insecticide use may have been extremely high. However, the geographic distribution of these applications would vary between growers depending on whether land was re-cropped within a season.

Comparing insecticide use between baby-leaf salad crops and other crops which may serve as host- plants for S. flava is difficult due to differences in cropping practice. Pesticide usage statistics suggest that insecticide use on baby-leaf salad crops has been similar to insecticide use on vegetable brassica crops in recent years. Insecticide use on oilseed rape crops is much lower than on baby-leaf salad crops. In addition, the timing of some insecticide use on oilseed rape crops may fall outside the time of the year when S. flava are typically recorded.

The period from 1999 to 2007 has been dominated by the use of pyrethroid insecticides on all crops which may be attacked by S. flava. Pyrethroids are fast-acting contact insecticides that are effective against a wide range of insect pests. Although pyrethroids have relatively short persistence against pests they are very damaging to populations of natural enemies and are persistent for over eight weeks e.g. to the leaf miner parasitoid Dacnusa sibirica (www.biobest.be). Pyrethroids are therefore generally not considered to be compatible with IPM programmes. Therefore, use of pyrethroids will disrupt natural control of S. flava populations by predators and parasitoids.

The widespread and repeated use of pyrethroid insecticides has led to resistance developing in a number of key pests including species of aphid (e.g. peach-potato aphid, Myzus persicae), species of whitefly (e.g. glasshouse whitefly, Trialeurodes vaporariorum), thrips (e.g. western flower thrips, Frankliniella occidentalis) and beetle (pollen beetle, Meligethes aeneus). Development of pyrethroid resistance in S. flava has yet to be confirmed, however, preliminary studies completed as part of HDC project FV 376 indicate that it may have developed. In this study pollen beetle test kits (vials coated with lambda-cyhalothrin) were adapted for use to test for resistance in an S. flava population. More testing is required using S. flava collected from cropped and un-cropped areas to establish if pyrethroid resistance has indeed developed in this species.

The greatest change to agronomic practice in baby-leaf salad crops has occurred following the emergence of S. flava as an important pest. The reliance on repeated insecticide applications has been replaced to some extent by the use of crop covers to physically protect the crop from this pest. This is important because results from the recent HDC study suggest that insecticide applications alone are unlikely to reduce leaf puncture damage to commercially-acceptable levels.

SID 5 (Rev. 07/10) Page 17 of 22 Further research

Confirm the presence and extent of pyrethroid resistance in S. flava populations collected from cropped (included baby-leaf salad crops, brassica vegetables and oilseed rape) and un-cropped environments.

Determine the frequency of incidental insecticide exposure that Scaptomyza flava may receive in different crops of Brassicaceae.

The incidental insecticide exposure that S. flava may receive is dependent on other pests that may also attack host plants. As such, the level of incidental insecticide exposure will vary throughout the season as well as between years. However, the timing and frequency of insecticide use on baby-leaf salad crops appears to represent the highest risk of insecticide exposure. The risk of insecticide exposure in vegetable brassicas appears also to be high given the timing of insecticide applications to these crops. By contrast, insecticide use on oilseed rape appears to be less likely to cause repeated incidental exposure of S. flava.

The majority of incidental insecticide exposure is likely to affect adult S. flava. Exposure would be either through direct contact with the spray or with residues on the leaf surface. Larvae and eggs within the leaf are more likely to escape exposure to pyrethroid applications, although there is some evidence to suggest that the pyrethroid deltamethrin may contact larvae within the leaf mine in some way, possibly by entering the mine through leaf miner oviposition punctures or larval exit holes.

Further research

Investigate whether the pyrethroid deltamethrin does contact leaf miner larvae feeding within the leaf. In addition, if contact occurs does this represent an effective control or present a resistance risk by exposing larvae to low doses of this insecticide.

There is a limited amount of information on the biology of each of the six species of dipteran leaf miner that feed on members of the Brassicaceae in Britain. It is therefore difficult to identify differences in species biology which might explain the increased importance of S. flava while the other species considered have remained relatively obscure.

Four of the six species, including S. flava, are polyphagous, feeding on host plants from a range of plant families. Only S. graminum and P. rufipes are specialists, feeding only on members of the Brassicaceae in Britain. While all six species have been recorded feeding on members of the Brassicaceae, only three, S. flava, P. rufipes and C. horticola, have been recorded from a wide range of species within this family.

While there is some information on when mines and adults of each species may be seen in Britain there is little information on the number of generations completed in a normal year. The information that is available suggests that there are relatively few generations of these species, with at least two generations of S. graminum, S. griseola and C. horticola and at least four generations of P. rufipes. There does not appear to be any specific information in the literature for S. flava or L. strigata, although textbooks (Alford, 1999; Edwards & Heath, 1964) refer to ‘several generations’. The number of generations a species completes each year is important because species with multiple generations may evolve faster and are often more likely to respond to selection pressures such as the use of insecticides.

There is some information in the literature for C. horticola and P. rufipes on development times but it is not clear how this relates to host plant and, in particular, development on Brassicaceae. For S. flava there does not seem to be any information in the literature on development times.

SID 5 (Rev. 07/10) Page 18 of 22

No information could be found on the migratory behaviours of these species. It is therefore unclear how readily each species is likely to move between crops and over what distance. Although S. flava and several of the other species considered are polyphagous it is also unclear whether larvae developing on a crucifer develop into adults that are more likely to lay eggs in a crucifer. This information would be of use when considering the importance of alternate hosts sustaining populations of each species.

Further research

Determine the number of generations of S. flava completed in a year. Determine how quickly S. flava develops on a range of cruciferous crops. Investigate migratory behaviour of S. flava to determine potential for S. flava to move between cruciferous crops throughout the season.

A review of the natural enemies of Scaptomyza flava to determine their potential importance in controlling populations of this species of leaf miner.

Like other species of leaf miner attacking cruciferous crops, S. flava is attacked by natural enemies including at least eight species of hymenopteran parasitoid. At least one of these species (either Dacnusa scaptomyzae or D. temula) may be important in reducing populations of S. flava later in the season. However, there is a general lack of information on the role that parasitoids may play in regulating populations of this species of leaf miner in natural and agricultural environments.

The importance of parasitoids in reducing crop damage associated with feeding by S. flava is in part limited by the strict quality controls associated with many baby-leaf brassica crops. Indeed, Martin & MacDonald (2009) noted that even where 82% parasitism was recorded levels of damage still exceeded those that are considered to be commercially acceptable. Despite this parasitoids may be important in reducing leaf miner populations in the farm landscape and so may be important in reducing the numbers of S. flava invading crops. The species of parasitoid is relevant to limiting leaf miner damage, as those which feed externally on leaf miner larvae in the mine, e.g. Diglyphus isaea, can ‘stop’ short leaf mines before the young leaf miner larvae have done much feeding. In contrast, those that develop inside leaf miner larvae e.g. Dacnusa spp, are slower to stop the mining as they need to complete their development inside the host before the mine is ‘stopped’. In protected ornamentals and herbs where cosmetic appearance of the leaves is important for marketing, releases of D. isaea can allow quality standards to be met as long as conditions are suitable for their establishment in the crop.

Insecticide use has been implicated in disrupting the normal control of Agromyzid leaf miners by parasitoids. The situation with S. flava may be similar, particularly if parasitoids attacking this leaf miner are more susceptible to the insecticides applied. Work done in New Zealand with A. persimilis suggests that once inside their host, parasitoids that develop inside the host leaf miner larva may be relatively safe from insecticide applications (Martin & MacDonald, 2009). However, the adult stage of this parasitoid appears to be vulnerable to the residues of several insecticides, although others caused mortality that was no higher than the water control.

Parasitoids are likely to be the most important group of natural enemies in controlling S. flava populations, although leaf miner larvae may also be predated on by generalist predators. Disruption of the normal control exerted by natural enemies may have contributed to the increased incidence of S. flava but other factors such as insecticide resistance are also likely to be responsible.

Further research

Identify species of parasitoid attacking S. flava in different cropping systems including baby-leaf salad, brassica vegetable and oilseed rape crops. Determine the potential importance of natural enemies in controlling S. flava populations and agronomic factors, specifically insecticide use, which may limit their effectiveness. Determine the effect of using crop covers on the incidence of natural enemies attacking S. flava. Determine whether commercially-available leaf miner parasitoids such as Diglyphus isaea and Dacnusa sibirica successfully parasitise S. flava.

SID 5 (Rev. 07/10) Page 19 of 22

Conclusions

It seems likely that the development of pyrethroid resistance in S. flava is the main reason for the increased importance of this pest in recent years.

Scaptomyza flava has not been the target of insecticide applications until recently but is likely to have received incidental insecticide exposure in baby-leaf salad crops and brassica vegetable crops. In oilseed rape crops there are fewer insecticide applications and the timing of some applications may be either before or after S. flava is likely to enter the crop.

The potential for incidental insecticide exposure has been highest in baby-leaf brassica crops where applications may be made as often as twice a week.

There is no information to suggest a recent change in agronomic practice that may explain the increased importance of S. flava.

There is insufficient information on the biology of S. flava to explain why this and not another species of leaf miner has become an important pest of cruciferous crops in Britain.

Scaptomyza flava is known to be attacked by at least eight species of parasitoid. The potential role of these parasitoid species in regulating populations of S. flava has not been studied.

It seems likely that repeated insecticide use over many years has disrupted natural control of S. flava.

Many baby-leaf salad growers have responded to the increased importance of S. flava by physically covering their crops. This step has proved effective in protecting crops from this pest and may also serve to reduce the need for insecticide applications against other pests.

Concluding Remarks

The emergence of S. flava as an important pest of cruciferous crops is best explained by the probable development of pyrethroid resistance. In turn pyrethroid resistance, if proven, appears to be linked to the widespread use of this group of insecticides on all crops that may be fed on by S. flava. In addition, in the case of baby-leaf salad crops the use of pyrethroids over recent years has been intensive, with as many as two applications a week. Development of pyrethroid resistance in S. flava may therefore be more closely associated with insecticide use on a minor crop (baby-leaf salads) than on a major crop (oilseed rape).

The reasons for the emergence of S. flava as an important pest of cruciferous crops rather than one of the other five species of leaf miner known to feed on members of the Brassicaceae in Britain are not clear. There is limited information on the biology of these leaf miner species, including S. flava, which makes drawing any conclusions difficult. Similarly, while S. flava is known to be attacked by at least eight species of parasitoid it is not known how important these natural enemies are in controlling leaf miner populations. Similarly, it is not known to what extent insecticide use in cropped environments disrupts this natural control of S. flava populations.

SID 5 (Rev. 07/10) Page 20 of 22

References to published material 9. This section should be used to record links (hypertext links where possible) or references to other published material generated by, or relating to this project. Alford, D.V. (1999) A Textbook of Agricultural Entomology. Blackwell Science, Oxford, UK.

Bennison, J., Maulden, K. and Wardell, G. (1999). Integrated control of the South American leaf miner Liriomyza huidobrensis on UK glasshouse lettuce and Chinese leafy salad crops. IOBC Bulletin. 22: 9-12.

Bennison, J., Cheek, S. & Collins, D. (2007). Control of leaf miners on pot and bedding plants. HDC Factsheet 15/07.

BioBest (2011) Side-effects manual - http://www.biobest.be/neveneffecten/3/none/ - viewed on 30/03/2011.

Edwards, C.A. and Heath, G.W. (1964) The Principles of Agricultural Entomology. Chapman & Hall, London, UK.

Garthwaite, D.G. & Thomas, M.R. (2000). Pesticide usage survey report 171 – Arable Farm Crops in Great Britain 2000. London: Department for Environment, Food and Rural Affairs & Scottish Executive Rural Affairs Department.

Garthwaite, D.G., Thomas, M.R., Anderson, H. & Stoddart, H. (2004). Pesticide usage survey report 202 – Arable Farm Crops in Great Britain 2004. London: Department for Environment, Food and Rural Affairs & Scottish Executive Rural Affairs Department.

Garthwaite, D.G., Thomas, M.R., Dawson, A. & Stoddart, H. (2002). Pesticide usage survey report 187 – Arable Farm Crops in Great Britain 2002. London: Department for Environment, Food and Rural Affairs & Scottish Executive Rural Affairs Department.

Garthwaite, D.G., Thomas, M.R., Dawson, A., Stoddart, H. & Anderson, H. (2003). Pesticide usage survey report 195 – Outdoor Vegetable Crops in Great Britain 2007. London: Department for Environment, Food and Rural Affairs & Scottish Executive Rural Affairs Department.

Garthwaite, D.G., Thomas, M.R. & Dean, S. (1999). Pesticide usage survey report 163 – Outdoor Vegetable Crops in Great Britain 2007. London: Department for Environment, Food and Rural Affairs & Scottish Executive Rural Affairs Department.

Garthwaite, D.G., Thomas, M.R., Heywood, E. & Battersby, A. (2006). Pesticide usage survey report 213 – Arable Farm Crops in Great Britain 2006. London: Department for Environment, Food and Rural Affairs & Scottish Executive Rural Affairs Department.

Garthwaite, D.G., Thomas, M.R., Heywood, E., Battersby, A., Parrish, G. & Smith, L. (2007). Pesticide usage survey report 219 – Outdoor Vegetable Crops in Great Britain 2007. London: Department for Environment, Food and Rural Affairs & Scottish Executive Rural Affairs Department.

Garthwaite, D.G., Thomas, M.R., Parrish, G., Smith, L., Barker, I. (2008). Pesticide usage survey report 224 – Arable Farm Crops in Great Britain 2008. London: Department for Environment, Food and Rural Affairs & Scottish Executive Rural Affairs Department.

Lole, M.J. (in prep) Baby-leaf Cruciferae: leaf miner identification, biology and control. HDC report for FV 376.

Martin, N. & MacDonald, F. (2009) Evaluating the impact of insecticides on Scaptomyza flava and its parasitoid, Asobara persimilis. New Zealand Journal of Crop and Horticultural Science. 37: 243-252.

SID 5 (Rev. 07/10) Page 21 of 22 Martin, N. A., Workman, P. J. & Hedderley, D. (2006) Susceptibility of Scaptomyza flava (Diptera: Drosophilidae) to insecticides. New Zealand Plant Protection. 59: 228-234.

Pitkin, B., Ellis, W., Plant, C. & Edmunds, R. (2011) The leaf and stem mines of British flies and other insects - http://ukflymines.co.uk/ - viewed on 10/03/2011.

Pesticide Usage Statistics - http://pusstats.csl.gov.uk/index.cfm - viewed on 11/03/2011.

Pesticide Usage Survey - http://www.pesticides.gov.uk/environment.asp?id=69 – viewed on 11/03/2011.

Richter, S. & Tsegaye, Y. (1988) Rearing Liriomyza trifolii Burgess on Phaseolus vulgaris L. in the laboratory and the development of a test method. Beitrage zur Tropischen Landwirtschaft und Veterinarmedizin. 26: 387-394.

Sampson, C. & Walker, P. (1988). Improved control of Liriomyza bryoniae using an action threshold for the release of Diglyphus isaea in protected tomato crops. Med. Fac. Landbouww. Univ. Gent 63/2b: 415-422.

Shakeel, M., He, X. Z., Martin, N. A., Hanan, A. & Wang, Q. (2010) Mating behaviour of the European leafminer Scaptomyza flava (Diptera: Drosophilidae). New Zealand Plant Protection. 63: 108-112.

Spencer, K. A. (1973) Agromyzidae (Diptera) of Economic Importance. Series Entomologica, Vol. 9. Dr. W. Junk B. V., The Hague, The Netherlands.

Speyer, E. R. & Parr, W. J. (1948) Tomato leaf-miner (Liriomyza solani, Hering). Ibid. 34: 43-51.

Stubbs, A. & Chandler, P. (Eds.) (1978) A Dipterist’s Handbook. The Amateur Entomologist, Vol. 15. The Amateur Entomologists’ Society, Hanworth, UK.

Williams, E.C. & MacDonald, O.C. (1995). Critical factors required by the nematode Steinernema feltiae for the control of leaf miners Liriomyza huidobrensis, L. bryoniae and Chromatomyia syngenesiae. Annals of Applied Biology. 127: 329-341.

Zhang, Y., Zhu, G., Ju. & Xu, B. (1999) Study on the sensitivity of Liriomyza sativae larvae to insecticides. Plant Protection. 25: 10-11.

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