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Project title Review of pest control in UK pepper crops Project number: PC284 Project leader: Dr. Pat Croft Report: Final report, September 2008 Previous report Key staff: Dr. Pat Croft Location of project: STC Research Foundation, Cawood, Selby, North Yorkshire YO8 3TZ Project coordinator: Gary Taylor, Tom Salmon Date project commenced: 1 st April 2008 Date project completed (or expected completion date): 30 th September 2008 Key words: Peppers, Biological control, crop pests, review Whilst reports issued under the auspices of the HDC are prepared from the best available information, neither the authors nor the HDC can accept any responsibility for inaccuracy or liability for loss, damage or injury from the application of any concept or procedure discussed. The contents of this publication are strictly private to HDC members. No part of this publication may be presented, copied or reproduced in any form or by any means without prior written permission of the Horticultural Development Company. 2008 Agriculture and Horticulture Development Board

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Project title Review of pest control in UK pepper

crops

Project number: PC284

Project leader: Dr. Pat Croft

Report: Final report, September 2008

Previous report

Key staff: Dr. Pat Croft

Location of project: STC Research Foundation, Cawood, Selby, North Yorkshire YO8 3TZ

Project coordinator: Gary Taylor, Tom Salmon

Date project commenced: 1st April 2008

Date project completed (or expected completion date):

30th September 2008

Key words: Peppers, Biological control, crop pests, review

Whilst reports issued under the auspices of the HDC are prepared from the best available information, neither the authors nor the HDC can accept any responsibility for inaccuracy or liability for loss, damage or injury from the

application of any concept or procedure discussed.

The contents of this publication are strictly private to HDC members. No part of this publication may be presented, copied or reproduced in any form or by any means without prior written permission of the Horticultural Development

Company.

2008 Agriculture and Horticulture Development Board

The results and conclusions in this report are based on an investigation conducted over a six month period. The review includes information from project collaborators, academic and more general literature searches. The review therefore presents an overview of the various sources of information.

2008 Agriculture and Horticulture Development Board

AUTHENTICATION

We declare that this work was done under our supervision according to the procedures described herein and that the report represents a true and accurate record of the results obtained.

Dr. Pat CroftProject LeaderSTCRF

Signature ............................................................Date ............................................

Report authorised by:

Dr. Martin McPhersonScience DirectorSTCRF

Signature ............................................................Date ............................................

2008 Agriculture and Horticulture Development Board

CONTENTS

Page

Grower summary:

Headline 1

Background and expected deliverables 1

Summary and main conclusions 1

Action points for growers 5

Science section 6

Introduction 6

Section A: Pests 7

Section B: Biocontrol agents 10

Section C: Chemicals 17

Conclusions 22

Glossary 23

Acknowledgements 23

References 23

2008 Agriculture and Horticulture Development Board

Grower summary

Headline

The project has pulled together information from members of the Pepper Technology Group and project collaborators (Fargro, Koppert Biological Systems, Syngenta Bioline, BCP Certis). The review highlights the need for new and more robust biocontrol programmes to achieve the Pepper Technology Group’s aim of pesticide free production.

Background and expected deliverables

The current use of biological control agents within protected pepper crops has been subject to problems and disruption among many growers. These changes include increasing problems in controlling familiar species and the occurrence of new species of pest.

Aphids are becoming an increasing problem, and the subsequent need for control using chemical treatments frequently results in the disruption of other biological control programmes. The species of aphid currently causing problems is the glasshouse and potato aphid Aulacorthum solani. Rapid growth of large populations of this species has been experienced and the current programme of biological agents is ineffective.

Thrips populations are also beginning to become an increasing problem for growers at planting. For other growers, unexpected growth in the pest population later in the season means that the current biocontrol programme fails to provide adequate control.

In addition pepper growers are increasingly experiencing problems with the glasshouse leaf hopper for which the currently available biological agents are limited in their success. Mealybug (Pseudococcus viburni) has also become a pest for some pepper growers.

Summary of the project and main conclusions

This project provides a first step in the review of pest control in UK peppers. The project’s aim is to identify the main concerns and problems for UK pepper growers and thereby provide an overview of the different

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problems and possible solutions. The review highlights possible solutions to provide robust systems for pest

control. The review explores the possible interaction of the different growing

regimes for peppers and the growth of pest populations. The project has discussed with collaborators appropriate changes to

current, or the development of new, programmes that could provide more robust solutions for growers.

The effectiveness of predators and parasitoids as biological control agents can be constrained by a range of factors including the availability of prey/hosts; lack of alternative food sources, as well as various mortality factors. In Conservation Biological Control we seek to support natural enemies by modifying the agro-environment in a way that removes or minimizes these impediments. This review considers the potential for improving biological agents and pest reduction through nutritional improvement.

The project identifies new chemistry that could contribute to effective pest reduction in conventional and organic crops.

Improvement to biological control programmes

A common disruption to successful biocontrol programmes is the use of insecticides. Frequent over-use of some products has caused resistance in pests for some nurseries. In addition some products that are used for specific pests have produced an increase in non-target pests, usually as a consequence of the lethal and sub-lethal effects on the biocontrol agents.

Before using an insecticide, the possible side effects on biological control agents should be considered. Anticipating the side effects of insecticides could benefit biological control programmes. However, as mentioned above the data on the effects of insecticides on beneficials is incomplete and conflicting and will vary with the screening methods employed. Even products with a short persistence can have a deleterious effect on the numbers of beneficials that have built up over time within a crop, and to achieve an equivalent population of biological control agents could either take too long or be too expensive.

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There is a range of predatory mites available and their performances are affected by temperature and humidity. Improvements in their efficacy may be achieved through adjusting the selection of agents to meet the changing temperatures/humidities within the crop. Similarly some parasitoid species perform more efficiently at different temperatures.

Most biological control agents require a suitable food source to increase life span and numbers of offspring produced. Pepper flowers have pollen and nectar, but the quality, quantity and accessibility to all beneficials needs to be verified, and also whether additional food sources could improve some biological control systems.

Problems in biocontrol programmes

Pest control programmes have been developed for most pest species in protected peppers, but some programmes are not proving to be sufficiently robust and reduced chemical input would present a challenge for controlling some pest species. Section B of the Science Section discusses the biological programmes and their gaps for most commonly occurring pest groups.

Over several growing seasons, changing climate will affect external insect populations and, as a consequence, the most prominent pest problem for growers changes. The following three groups of pest have been the most troublesome in recent seasons.

Aphid control A common problem to all growers is the control of aphids, especially the

aphid Aulacorthum solani, and particularly where growers wish to pursue a chemical free practice.

To achieve sustainable aphid control in pepper crops the addition of other species of predators and/or parasitoids may be required. The review has provided information on additional agents that could be considered but the benefits of adding these to general aphid control programmes needs verification. The industry could also benefit from the introduction of new aphid parasitoid/predator species, some of which may be non-native and therefore would require the pursuit of a licence.

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Hyperparasitism presents an increasing problem for some growers. Part of this problem may be accounted for by the crops (and weeds) and their pests that are grown in the vicinity if the glasshouse. There is also a possible contribution to the hyperparasitoid population from banker plants. Aphid control could be improved if methods for eliminating hyperparasitism were developed.

Leafhopper control Leafhoppers present a problem in some crops, particularly for growers in

the south of England. The uses of chemical products against leafhopper have disrupted the biological control programmes for other pests. However recent applications of Steward (Indoxacarb) would appear to have produced effective all round control.

There are currently no consistently effective biocontrol agents for leafhopper. Information on available agents and rates are discussed in Section B of the Science Section. However, further work on effective biological control is required. Physical methods, such as sticky traps and suctioning systems will contribute to the overall control of leafhopper.

Leafhoppers move into glasshouses from the surrounding vegetation and the management of these external areas may also provide part of the solution to the pest populations.

Thrips control The breakdown of the thrips control programmes has several sources:

invasion of the glasshouse from external crops, reduction in biocontrol agents due to chemical programmes for other pests, large thrips populations at the end of the season results in and subsequent high infestation levels at start of the following season. It is also speculated that Mypex may allow better survival of thrips between crops.

High rates of Orius laevigatus have succeeded in reducing large thrips populations for several growers, and have achieved control for growers with TSWV problems. However, the costs of such programme are extremely high and therefore more cost-effective biocontrol programmes

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for high or virus transmitting thrips populations are required. (Section B of the Science Section discusses these issues and possible solutions.)

Research suggests that virus problems can be alleviated through the management of vegetation surrounding the glasshouse, assuming that plants from propagation are virus free.

External controls

Pest problems do vary with individual growers and certainly the sudden occurrence of pests is usually correlated to external crops to that particular glasshouse and therefore can be very specific to a grower.

Entry into the LEAF scheme requires that growers should maintain areas around the glasshouses for increasing biodiversity. Management of field margins is beginning to be developed in horticultural field crops across Europe. Management of these margins meets the requirements of farmers to reduce pest pressure/insecticide input through the increase of beneficials whilst maintaining low labour. It is possible that the applications for these methods may provide some glasshouse growers with similar benefits by reducing pests and increasing beneficial insects.

However large pest invasions due to external crops will always remain a problem for some growers. Screening vents, which has been shown to prevent pest infestations in protected lettuce crops (HDC PC132) whilst effective can prove to be prohibitively expensive. Therefore programmes with reduced or no chemical input for such influxes needs to be further investigated.

Action Points for growers

The review provides growers with an overview of pests, biocontrol agents and insecticides in protected peppers.

Growers can use the review for information on additional biocontrol agents that may provide solutions to pest problems, discussions with

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representatives from biocontrol agencies and further evaluations of these biocontrol agents would be required.

The PTG goal of achieving pesticide free production requires more robust biological control programmes to be developed for some pests, such as aphids.

Biological control programmes need to be developed for some pests, eg leafhopper.

The review also lists approved chemicals for protected peppers. The reports provides information on the longer term use of chemical

products listed in relation to the replacement Directive for 91/414EC. This is an ongoing situation and developments have occurred since the submission of this report, for a more recent product status growers can look at the following web site: http://www.pesticides.gov.uk/uploadedfiles/Web_Assets/PSD/Revised_Impact_Report_1_Dec_2008(final).pdf

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Science section

Introduction

The following review provides information gathered from discussions with growers and project collaborators; Professor Felix Wackers (Lancaster University) and representatives from BCP Certis, Fargro, Koppert Biological Systems and Syngenta Bioline. In addition, information has been gathered from a review of academic and general literature sources.

The aim of the review is to give an overview of pest control in protected peppers as requested by the Pepper Technology Group (PTG), covering the biological and chemical methods currently used, highlighting problems and other relevant information.

The pests, biocontrol agents and chemicals that are used in protected pepper crops are outlined in sections A, B and C.

Section A identifies the common pest problems encountered by pepper growers.

Section B covers the biocontrol agents that are currently used in protected peppers. The section also provides information on the biology and environmental requirements for some of these agents which may help in the timing of their application to ensure their most effective use. Also listed are biocontrol agents that are not currently being used but could be considered as part of a package that could target specific pests in protected peppers.

Section C lists the insecticides approved for use in protected peppers. Information is also provided, where it is known, on the side effects of insecticides on biocontrol agents. Unfortunately this information is incomplete and often contradictory. IPM programmes could be improved if the integration of some insecticides to biocontrol programmes was better managed using robust data on their side effects. Section C also provides some information on the replacement of the EC Directive 91/414 and the possible consequences for products that are currently being used in protected crops.

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Section D summarises the findings of the review and suggest the gaps that exist for growers to reduce insecticides and residues

Section A. Pests

AphidsTwo species of aphid, Myzus persicae (peach-potato aphid) and Aulacorthum solani (foxglove or glasshouse potato aphid), are considered the most commonly occurring species in peppers, although Macrosiphum euphorbiae (potato aphid) also occurs occasionally.

Aulacorthum solani (glasshouse potato aphid): This species of aphid is now regarded as a major aphid pest on peppers as a result of the lower tolerated numbers of the pest. A salivary toxin has been described in Aulacorthum solani (Damsteegt and Voegtlin, 1990) that produces a yellow mottling on the leaves and fruit and as result even low numbers of the aphid are a problem for growers.

Myzus persicae (peach potato aphid):A commonly occurring aphid pest for pepper growers. It can be controlled using the parasitoid Aphidius colemani and the predatory midge Aphidoletes aphidimyza. However the use of certain chemical products has had negative side effects on some biocontrol agents resulting in a subsequent increase in the aphid population.

M. persicae can also become a problem if it develops resistance to chemical products. Too frequent applications of pirimicarb and pyrethrum based products have produced resistance in this species for some growers.

Macrosiphum euphorbiae (potato aphid): This large species of aphid occurs occasionally within peppers, but is not regarded as severe a problem as the two aforementioned species. The parasitoid Aphidius ervi and predatory midge Aphidoletes aphidimyza are used to control this aphid.

Spidermites (Tetranychus urticae)

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Spidermites are not such a big problem for growers as aphids in pepper crops. However after the application of a pyrethrum product, spidermites became a problem for one grower suggesting that the previous low densities were being maintained by predators that were then subsequently affected by the chemical product. For other growers there were more regular problems with spidermites that were controlled biologically and with the occasional applications of spot treatments of chemical products. Because of the smooth leaf surface of peppers the biological agents can usually work effectively in this crop. In addition the use of ‘pest in first’ method has been very successfully used by growers where there is a consistent spidermite problem but this method requires careful monitoring of the crop, the pest and the predator.

ThripsTwo species of thrips are found in pepper crops, Frankliniella occidentalis (WFT) and Thrips tabaci (onion thrips), with WFT causing the most damage.

Until recently thrips were relatively easily controlled by pepper growers, the programmes devised by the biocontrol companies provided effective control of this pest. However there have been recent problems with thrips. Some problems stem from the use of insecticides targeting other pests (aphids, leafhoppers) that subsequently produces lethal or sub-lethal effects (such as reduced egg laying or lifespan) on the biological control agents and a subsequent increase in thrips numbers.

In addition early season infestations of thrips into crops can be problematic as recently introduced biological control agents are not present in sufficiently high enough numbers to control the pest. Early infestations can be a result of thrips activity in crops near to the glasshouse. Early season infestations can also stem from large thrips populations surviving between crops. The origins of some of these large populations of thrips originate from the chemical intervention to reduce other pests in the previous season.

The contribution of Mypex on the floor to the success of between crop survival of large number of thrips is unknown; it is possible that the application of treatments to the Mypex may be required.

Virus

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In addition to the increasing incidents of thrips problems there is also the risk of virus transmission, with the recent incident of Tomato Spotted Wilt Virus (TSWV) during this season in UK peppers. TSWV, a type of Topsovirus, uses thrips as the only vector. The adult and 2nd instar larvae transmit the virus from plant to plant, but it is the smaller 1st instar and early 2nd instar larvae that pick up the virus from the plant. Reducing the ability of 1st instars to pick up the virus will reduce transmission by the adult.

Indicator plants that are proven to be more attractive to the thrips than the crop itself and develop earlier symptoms have been used by some growers in the US to give early warnings of the presence of the virus within the glasshouse. It has also been suggested that weed reduction in the perimeter of the glasshouse is important for thrips and virus suppression (Cho et al., 1986).

There is also the suggestion that the virus may be transmitted through the root system in re-circulating systems (eg. NFT) (Buttner et al., 2008) though the relative importance of this compared to transmission by WFT is not known.

LeafhopperEmpoasca decipiens (green leafhopper) and Hauptidia maroccana (greenhouse leafhopper) are an increasing problem for some pepper growers. The use of insecticides against this pest frequently disrupts the biological control of other pests. Leafhopper did not present a problem as yet to growers in the North of the UK.

Currently there is no robust biocontrol programme for control of this pest. As with many pest species the vegetation in the surrounding areas of the glasshouse can be a source of infestation if it contains plants that are breeding sites for the pest. Reduction of leafhopper breeding sites outside the glasshouse could assist in reductions of its populations as suggested for thrips; however research would be required to determine which plants and their impact on the pest populations.

CaterpillarsA problem for some growers. The occurrence of this problem is dependent on the crops that are grown in the vicinity of the glasshouse. Generally can be controlled using application of different products including Dipel (Bacillus thuringiensis).

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Intermittent pestsA range of pests occur that are either brief in their duration and therefore not a major problem or not a commonly occurring pest. These include mealybugs (Pseudococcus viburni), capsid bug (Lygus tripustulatis), and broad mite (Polyphagotarsonemus latus). Glasshouse white fly (Trialeurodes vaporariorum), which although will go on pepper plants, is not currently a problem for UK pepper growers.

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Section B. Biocontrol agents

Biological control agents currently used for aphidsAphidius colemani: An effective parasitoid of M. persicae. Most eggs are laid in the first three days of the adult life which can be of up to 10 days. The parasitoid is however less effective at high temperatures because parasitism decreases above constant 250C (Toussidou et al., 1999, Zamani et al., 2007).

Hyperparasitism is said to occur when a parasitoid is parasitised by another species of parasitoid. When this occurs in peppers it results in a reduction in A. colemani and an increase in the aphid population. Hyperparasitoids will naturally invade glasshouses, usually in the summer and when aphid numbers have been high as they are attracted to aphid honeydew. The increasing problems over successive growing seasons for some growers suggest that hyperparasitoids are overwintering as parasitised aphids either within or in the vicinity of the glasshouse. It is also possibly exacerbated by the continuous use of banker plants that could maintain a hyperparasitoid population

Aphidius ervi: A large parasitoid supplied for use against the larger species of aphids A. solani and M. euphorbiae. However, because of the low tolerance threshold for A. solani due to the symptoms caused by toxic saliva in the pepper, A. ervi frequently does not provide sufficient levels of control. As with the parasitoid A. colemani this species of parasitoid is also less effective at high temperatures (research demonstrates that constant 250C is critical) (Malina and Praslicka, 2008) and it is also susceptible to hyperparasitism.

Predatory midge (Aphidoletes aphidimyza): The larval stage of the midge is a predator of aphids. It is used by some growers when several species of aphid have been recorded in the crop. The adult female is nocturnal and chooses to lay eggs usually in areas where there are aphids and where there is high humidity which can mean a preference for lower parts of the crop canopy.

The presence of honeydew produced by aphids is an important food source for the adult midge, prolonging its life and the number of offspring it produces. This

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suggests that the predator will be more effective at higher aphid densities when there is a good food source for the adult midge.

It is possible that the provision of a suitable nectar source could improve the performance of the adult midge at lower densities of aphid. However nectar is already present in pepper flowers but the quantity varies considerably with varieties and time of day. (Rabionowitch, et. al. 1993). In addition the quality of the honeydew produced by the aphids can vary with plant species and that can have a dramatic influence on the effectiveness of the predatory midges (Kuo, 1977). To improve the performance of biological control agents the provision of appropriate food needs to be further understood within the glasshouse environment.

Hover flies (Episyrphus balteatus): At present this predator is being released as part of a general mix applied to control aphid populations in organic productions. When comparing hoverflies to the predatory midge A. aphidimyza, hoverflies can potentially lay more eggs and the nocturnal feeding larvae can consume more aphids (A. aphidimyza consumes 10-100 aphids whereas a hoverfly larva can consume an average 300-500 aphids if it is in the vicinity of aphid colonies) (Malais and Ravensberg, 2003). Adult female hoverflies also need a food source pollen and nectar to survive and produce offspring.

Despite their potential, hoverflies are generally not thought to be successful within the glasshouse environment and as a result are not commonly used in the UK. Hoverfly larvae are only effective on smooth haired plants such as peppers and do not do well on ‘long haired’ leaves such as in cucumbers and tomatoes.

The method of release with this predator may be important to its success in the glasshouse. The larva is poor at searching for aphids if they are not in its immediate vicinity and therefore good dispersal of the predator by the grower is required. Hoverflies can be released directly into the glasshouse or reared on banker plants. Releases of this predator in the pupal stage into Spanish crops were not successful. The use of banker plants significantly increased the attraction of hoverflies into the glasshouse but this was not the species of hoverfly that is usually released (Episyrphus balteatus), but another naturally occurring species Sphaerophoria rueppellii (Pineda & Marcos-Garcia, 2008). Work by Pineda & Marcos-Garcia (2008) suggests that this latter species may be more

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tolerant of higher temperatures and drought conditions and therefore offers a more regular population each year.

In theory, according to its rate of prey consumption, this predator should provide a considerable contribution to aphid control. That is does not, may be because it is not suited to the glasshouse environment. Alternatively, perhaps the best method for its release has not yet been developed and needs further study. Or, as mentioned previously, the provision of adequate nutrition may be required.

The predatory bug Macrolophus caliginosus will consume high rates of hoverfly eggs and therefore could interfere with the success of the hoverfly to reduce aphid populations (Frechette et al., 2007)

Aphelinus abdominalis: A generalist parasitoid that will attack numerous species of aphid, but is most successful against the larger species of aphids such as A. solani. Not commonly used anymore and there are mixed views to the success of the parasitoid. It performs best at high temperatures, which could be an advantage in the summer where high temperatures can have negative effects on the two species of Aphidius. Another advantage is that the female adult parasitoid will also feed on aphids, eating about 40 aphids during its life. Because of its feeding activity the parasitoid is long lived and will lay a few eggs (5-10 per day) over a long period of up to about an average of 30 days (Jarosik et al., 1996, Malais and Ravensberg, 2003). Hyperparasitism is also less common in this species of parasitoid compared to the two species of Aphidius (see above).

The disadvantage of this parasitoid it has a long development period which slows down the growth of the parasitoid population. In addition it is poor at dispersal and is usually located where it is released and therefore needs to be dispersed by hand (Ferguson et al., 2006). However the parasitoid may provide an additional weapon to aphid control during the summer.

Lacewings (Chrysoperla carnea): A generalist predator that will eat spidermites, leafhopper nymphs, mealybugs and aphids. The larval stage is predatory, whereas the adult stage is non-predatory and requires pollen and nectar to increase its life span and egg production. The larva can consume approximately300-400 aphids per day. As

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with hoverflies, this predator has not been used successfully used within UK glasshouses.

Releases of the nocturnal adults are not successful, as adults tend to fly from the glasshouse without seeking out aphid populations and laying eggs. Lacewings are sold as either eggs glued to card, or as larvae. Research by Daane et al., 2005, showed that releases of the larval stage was more successful at reducing the numbers of variegated leafhopper in vine crops compared to releases of the egg.

There is the suggestion that the larval stage of lacewings is not successful on tall crops as it thought that if the larvae fall from the crop they are not successful at locating the prey again (Malais and Ravensberg, 2003). There is a reference to the species Chrysoperla rufilabris being a preferred species for glasshouse crops as they do better on tall plants (http://www.growercentral.com/UPLOADS/PDFS/lacewings).

As with the hoverflies, there is little use of this predator within the UK compared to other countries. Whether this simply reflects a potential that cannot be exploited in a glasshouse environment or the need for better release methods, alternative lacewing species or a supply of alternative food sources needs to be further investigated. Some research has focused on the use of chemical attractants used in the field to improve the performance of lacewings; there may be a possibility of using such products in glasshouse crops (James, 2006; Zhang et al., 2006).

Biological control agents for spidermitesPhytoseiulus persimilis: This specific spidermite predator is commonly and effectively used in pepper crops. However because this predator mite performs less well at high temperatures and low humidities the suggestion is that P. persimilis is a better predator in spring and the cooler parts of summer.

Feltiella acarisuga: A predatory midge, the non-predatory adult stage feeds on nectar/honeydew whilst the larval stage is predatory. The adult female will lay up to 100 eggs and prefers high spidermite densities and high humidities.

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Amblyseius (Iphiseius) degenerans: The predator operates best at low pest densities, but is less effective when spidermite population’s increase and webbing occurs.

Amblyseius (Typhlodromips) swirskii: This predatory mite is usually introduced for control of thrips and white fly. But it is a generalist predator and can also reduce spidermite populations. The high temperatures in pepper crops during the summer are preferred by this mite.

Amblyseius californicus: An effective predatory mite of spidermites, will exist in crops with low or no spidermite populations as it can utilise pollen as part of its diet, an advantage over P. persimilis. It is also more effective at the higher temperatures than is P. persimilis. However the mite will lay fewer eggs at moderate temperatures than P. persimilis and is less effective at dispersing within the crop than P. persimilis (Malais and Ravensberg, 1992)

Amblyseius andersoni: Has an advantage over P. persimilis if temperatures are low, such as the beginning and end of the season

Stethorus punctillum: A specific predatory beetle for spidermites that will eat all development stages of the pest. It is best at controlling spidermites when there are high pest densities. The larval stage does not do well in plants with long haired leaves, and therefore is very suited to pepper crops.

Biological control agents for thripsOrius laevigatus/majusculus: These predatory bugs have provided thrips control for many growers. The predators provide adequate control of thrips when in combination with predatory mites. Of the two species O. laevigatus is the most commonly used because unlike O. majusculus it does not enter a prolonged period of inactivity (diapause) induced by short day lengths. Recently large populations of O. laevigatus have been released to control thrips problems (including virus carrying thrips) and these programmes have been successful but the financial cost is extremely high.

Amblyseius (Neoseiulus) cucumeris and Amblyseius (Typhlodromips) swirskii:

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These two predatory species of mite are provided to growers for thrips control. A. cucumeris is a commonly and successfully used predator. A. swirskii is relative new to the UK, and operates similarly to A. cucumeris, but is less successful at low temperatures but more successful at high temperatures.

Biological control agents for leafhopperAnagrus atomatus; An egg parasitoid of leafhopper. Generally the use of this parasitoid has not provided effective reduction in the leafhopper populations. Often the recommended density to release the parasitoid is at 1/m2, higher densities (10/0.04m2 or the equivalent of 250/m2) have achieved 64% levels of parasitism (Agboka et al., 2002); however the economics of releasing at this density are currently prohibitive.

Predators: Because the leafhopper adult and it nymphs are fast not many predators can provide effective control. Lacewings (Chrysoperla spp.) will predate on the slower young instars of the leafhopper and may possibly contribute to some reduction in the leafhopper numbers. Research by Daane et al. (2005) showed that releases of the lacewing larval stage were more successful at reducing the numbers of variegated leafhopper in vine crops compared to releases of the egg. Macrolophus caliginosus can also contribute to some reduction in leafhopper numbers.

Sticky traps: Sticky traps present a physical system of removing some of the adult leafhoppers. Some research on E. decipiens in cotton showed that the height of the traps relative to the crop can play an important role in the numbers of adults that will be trapped (Atakan and Canhilal, 2004). Therefore it is also possible that the position of the sticky traps relative to the pepper crop maybe important in the number of leafhoppers successfully trapped.

There is also the possibility of other physical removal systems such as hovering/sucking up large populations of the leafhopper.

Fungal entomopathogens: The fungal pathogens Metarhizium anisopliae strain Ma43 and Paecilomyces fumosoroseus strain Pfr12 have effectively reduced leafhopper (E. decipiens) in

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laboratory assays (Tounou et al., 2003). However, further applied studies in the semi field phase along with commercial validity of these products needs to be examined.

Biological control for caterpillarsA range of moths will attack pepper crops and therefore the generalist parasitoid Trichogramme brassicae can be used. It is an egg parasitoid of a wide range of species. In addition the predator Macrolophus caliginosus will also consume moth eggs. But a robust biocontrol programme for caterpillars is currently difficult due to the requirement of spotting the adult populations earlier enough for the egg parasitoid to be introduced and be effective. Effective monitoring systems need to be developed, the use of pheromones to trap some moths (eg silver y) have already been developed. But not all species have these systems.

Biological control for intermittent pest speciesBroad mitePredatory mite Amblyseius cucumeris is effective against broad mite.

Capsid bugAs yet there is not a biocontrol programme for capsid bug. The pest is usually chemically controlled with Calypso (thiacloprid) or Chess (Pymetrozine).

MealybugThere are possible biocontrol agents or physical/barrier systems that may possibly contribute to an insecticide free programme for mealybug control, but the biocontrol programmes have not yet been thoroughly investigated.

Pseudaphycus maculipennis: This non-native parasitoid is a specific parasitoid for the species of mealybug found in pepper crops (Pseudococcus viburni-Obscure mealybug). Currently can only be released for licence and licence available for one year. There are no plans to renew this licence.

Lacewings (Chrysoperla carnea):

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A generalist predator that will eat spidermites, leafhopper nymphs, mealybugs and aphids. In a previous project (HDC PC161) lacewing larvae were demonstrated in laboratory bioassays to be effective predators upon larvae of the obscure mealybug, the most commonly occurring species in protected crops. However the predator was not trialed in the glasshouse. However there are reports of the importance of lacewings within glasshouses and against the longtailed mealybug (Weeden et al., 2007).

Physical barriers: The application of products that provide a physical barrier to movement of the early active stages of the mealybug have been successful in preventing mealybugs moving onto plant material for some pepper growers.

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Section C. Chemicals

The list of chemical products for pepper crops has been produced from the Liaison web site and from discussions with growers and representatives from BCP Certis, Fargro, Koppert Biological Systems and Syngenta Bioline. The list does not distinguish between products that are Approved or are SOLA products, and which products are for use in soil or hydroponics crops. Growers would need to obtain further clarification for which products fall into the relevant category for them and for recent changes that may include the new MRL legislation (EC Regulation 396/2005) which came into force on the 1st September 2008. The information on each product lists the pests for which the products are Approved. Information is also given if the product is found to be effective against additional pests but the statutory conditions for Approval for application must be met.

The list also indicates where the products have a reported effect on biological control agents. However the information for the side effects on biological control agents is not complete. Not all biological control agents have been tested against all products. Different methods may be used to measure toxicity, and these different methods can produce varying degrees of toxicity to beneficials and even sometimes conflicting data. A useful guide and possible indication of effects of insecticides on biological control agents can be obtained from the following Websites Side effects - Koppert biological control natural pollination and Biobest - Side Effects.

In addition information is provided on the longer term use of the listed products in relation to the replacement EU Directive for 91/414EC as this may limit pesticide use in pepper crops. The EU Commission is introducing ‘hazard triggers’, comparative assessment and substitution for pesticides which if successful are likely to revoke or limit the use of many products. The EU Parliament may try to include further restrictions on the use of pesticides. The EU Commission and EU Parliamentary criteria relevant to the insecticides that are used in pepper crops are given below. The information has been taken from the recently produced impact assessment from PSD; ‘Assessment of the impact on crop production in the UK of the ‘cut off criteria’, and is therefore a speculative view of what could happen in the future and hence should be treated with some caution.

Abamectin (Dynamec)

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Contact/translaminar insecticide for WFT, mites and leafminer. The chemical acts as a nerve toxin relatively quickly paralysing insects. There is some contact activity against the insect but it is most effective when it is eaten by the pest.

Toxic to biological control agents. During the next review period of pesticide use within Europe abamectin is

an active ingredient listed as a possible candidate for substitution (EU Commission) or possibly non-approval (EU Parliament).

Acetamiprid (Gazelle). A chemical from the neonicotinoid group. Targets aphids and whitefly. There are possible long term residual effects on some beneficials,

particularly parasitoids. A possible candidate for substitution according to the EU Parliament

criteria

Buprofezin (Applaud) Is used for whitefly control but will also reduce leafhopper. The product inhibits the synthesis of the insect skeleton. Has been

successfully used in IPM over a period of time, but there are slight harmful effects recorded against some biological control agents (Stethorus punctillum, Aphidoletes aphidimyza).

Applaud use will be revoked approximately March 2009, with a use-up time to about September 2009.

Deltamethrin (eg. Agriguard, Decis). A broad spectrum pyrethroid insecticide. Very harmful to biological control agents and is persistent. The active is listed for non-approval in the EU Parliament and Commission

criteria.

Diflubenzuron (Dimilin Flo) A benzamide product that targets caterpillars. The product inhibits

skeleton production in insects. Reported as harmless against beneficial insects, but also records of it

being toxic to nymphs of Orius and Macrolophus caliginosus.

Dodecylphenol ethoxylate (Agri 50 E)

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A contact polysaccharide that works through blocking the respiratory holes (spiracles) of whiteflies and aphids.

Information on any side effects with biological control agents could not be sourced, but generally products that act by this physical method can be expected to have an affect on biological control agents if they are in direct contact with the product but only for a short period of time until the product dries.

Majestik A natural plant extract that controls insect pest (mites, aphids,

leafhoppers and whitefly) through physical means and therefore requires good contact with the pest.

Because of its simple physical activity it will also effect biological control insects, but this effect would be of short persistence.

Indoxacarb (Steward) Indoxacarb belongs to the new group of insecticides oxidiazines. It is a

broad spectrum caterpillar insecticide with activity against sucking pests such as leafhoppers.

Generally regarded as IPM compatible but it has been reported as reducing fecundity in P. persimilis (Bostanian and Akalach, 2006). There are also recorded toxic effects against Encarsia formosa, Macrolophus caliginosus, Aphidius colemani and Amblyseius swirskii.

May not be approved according to EU Parliament criteria.

Nicotine (eg Stalwart, Shreds) Broad spectrum insecticide that is a fast acting nerve toxin. Nicotine is

used primarily for insects with piercing and sucking mouthparts such as aphids, whiteflies, leafhoppers, thrips and mites.

Harmful to many beneficials but has short persistence.

Oxamyl (Vydate 10G) Oxamyl is a carbamate. It is a highly toxic broad spectrum compound,

working as a systemic and a contact. It very harmful biological control agents and is very persistent. Possibly a candidate for substitution (EU Commission) or non-approval (EU

Parliament)

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Pirimicarb (Aphox) Has contact, translaminar and fumigant activity against aphids. Resistance issues occur with frequent use of this chemical. Can be harmful to some beneficials but over a short period. Maybe candidate for substitution EU Commission or not approved

according to the EU Parliament criteria.

Pymetrozine (Chess) An effective aphicide that is an antifeedant to sucking insects, therefore

death is not instant. A useful IPM compatible product. There are records of possible low toxicity

to Macrolophus caliginosus and Orius spp. The use of Chess through the dripper system, as used in the Netherlands

could provide aphid control with a reduced rate of the product, and is under discussion for UK growers at present.

Pyrethrum/pyrethrin (eg Spruzit): Short persistent broad spectrum insecticides. Aphids, thrips, leafhopper.

The toxin causes an immediate knockdown or paralysis on contact. There are negative effects on biological control agents. Also there is a

reported increase in the fecundity of spider mites from the application of pyrethrin (Castagnoli, et al. 2002, 2004). However pyrethrins have a short persistence.

Most insects are highly susceptible to low concentrations of pyrethrins. The toxins cause immediate knockdown or paralysis on contact, but insects often metabolize them and recover.

Spinosad (Conserve). Spinosad is produced by a fermentation process of a microorganism. Short persistent broad spectrum insecticide against aphids, thrips,

leafhopper. The toxin causes an immediate knockdown or paralysis on contact with the pest.

Harmful to biological control agents, parasitoids are significantly more susceptible to spinosad than predatory insects. Predators generally suffer insignificant sub-lethal effects, whereas parasitoids suffer sub-lethal effects such as a loss in reproductive capacity and reduced life span. Residues degrade 3-7 days post application (Williams et al. 2003).

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Listed for substitution (EU Commission) or non-approval (EU parliament).

Teflubenzuron (Nemolt) Inhibits the synthesis of insect skeleton. Targets whitefly and caterpillars. Toxic, with varying levels to some beneficials (Aphidius spp., Orius sp. and

Macrolophus caliginosus). Candidate for substitution (EU parliament).

Spiromesifen (Oberon) A new product that targets whiteflies, spidermites and thrips. Oberon

contains the active substance spiromesifen that leads to inhibition of fat synthesis in the pest. Because Oberon is harmless to beneficial insects, it is an ideal component of IPM-programmes.The recommendation regarding timing of use is that the product should be applied as soon as the pest population starts to increase – i.e., before symptoms of damage (e.g. leaf discolouration) are seen

It is moderately toxic to some predatory species of mite (A. cucumeris and A. californicus). Has persistence in the region of about three weeks.

Thiacloprid (Calypso). A neonicotinoid that is used to target aphids, leafhoppers, capsids and

thrips. Moderately toxic to a range of beneficials, and very toxic to Orius and

Macrolophus caliginosus. Persistence is unknown. Listed for possible substitution (EU parliament)

New products

A number of new products are under development by the agrochemical industry, including products that target sucking insects such as aphids (also mealybugs and therefore possibly leafhopper).

There are also the possibilities of non-chemical products such as Kaolin particle film, available as Surround WP in Mediterranean countries which is very effective against sucking insects such as aphids and hoppers. However it’s potential in protected peppers would need to be examined.

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Conclusions

IPM programmes can be successfully applied to pepper crops due to the smoothness of the leaves and the food source in the flowers. However, chemical products remain an essential part of these IPM programmes, being used as spot treatments, or to bring pests to a level were biocontrol agents can work again.

There is no effective biocontrol programme for leafhopper, and therefore currently the control of this pest requires the use of insecticides.

Insecticides are also used against other pests, particularly aphids, where the biocontrol programmes are not consistently effective because of the range of species involved and the high rates of population growth of the pest. Chemical intervention for some pests (eg leafhopper and aphids) frequently has a knock on affect against biocontrol agents and can lead to increases in non-target pests, such as thrips.

Large thrips populations occur for several reasons (see section A). A successful biocontrol programme exists for thrips, but is subject to disruption from the use of insecticides. In addition a more economical biocontrol programme needs to be developed to cope with large thrips populations which can occur at different times throughout the growing season, or when virus problems occur.

Currently, growing peppers without the use of insecticides (due to their removal or to requirements for reduction in residues) would be difficult due to the reasons mentioned above.

A possible solution to some of the problems listed above could be the development of additional biocontrol programmes that take into account the predator/parasitoid performances with different environmental conditions, thereby having several programmes available for each pest.

The addition of biocontrol agents (including non-native species) to existing or additional programmes could also be of benefit particularly for aphid and leafhopper control, but this needs to be verified. The introduction into the UK of non-native species is increasingly difficult.

Insecticide free pest control programmes could be designed for some pests that optimally incorporate the use of physical methods, eg sticky traps, suction systems and the addition of biological products such as entomopathogens.

Solutions may also require further developments in optimising the performance of the biocontrol agents, not only tying their releases with

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environmental conditions but ensuring that adequate nutrition is also available.

Therefore the attainment of consistently insecticide free pepper crops would require additional biocontrol agents, additional biocontrol programmes and more robust existing programmes. Glossary

Diapause: Usually done by insects. It is a ‘sleep time’ that is different from hibernation as the animals do not grow during this time. Hyperparasitism: Parasitoids (see below) of other species of parasitoid, their offspring develop in or on the larvae of other parasitoids. Usually has a negative effect on parasitoid populations. Parasitoid: Insects whose offspring develop from feeding on other insects (hosts), either from within the body (endoparasitoid) or on the surface of the host (exoparasitoid).Sub-lethal: Insecticides can kill insects i.e. produce lethal effects. Some insecticides however do not kill insects; they effect the insect population through other methods, such as reducing the ability of the insect to produce or reducing the lifespan of the insect. These sub-lethal effects have an overall negative effect on the insect population. Acknowledgements

We would like to thank all the project collaborators from the pepper industry and the biocontrol companies for their input, in addition we would like to thank the contributions from the project coordinators Gary Taylor and Tom Salmon.

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