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Keywords:

  • thrips;
  • insecticide resistance;
  • Thysanoptera;
  • resistance management;
  • IPM

Abstract

  1. Top of page
  2. Abstract
  3. 1 INTRODUCTION
  4. 2 INSECTICIDE RESISTANCE IN FRANKLINIELLA OCCIDENTALIS
  5. 3 CONDITIONS THAT PROMOTE RESISTANCE
  6. 4 IMPROVED INSECTICIDE RESISTANCE MANAGEMENT
  7. 5 CONCLUSIONS
  8. Acknowledgements
  9. REFERENCES

Western flower thrips (WFT), Frankliniella occidentalis (Pergande), is an economically important pest of a wide range of crops grown throughout the world. Insecticide resistance has been documented in many populations of WFT. Biological and behavioural characteristics and pest management practices that promote insecticide resistance are discussed. In addition, an overview is provided of the development of insecticide resistance in F. occidentalis populations and the resistance mechanisms involved. Owing to widespread resistance to most conventional insecticides, a new approach to insecticide resistance management (IRM) of F. occidentalis is needed. The IRM strategy proposed consists of two parts. Firstly, a general strategy to minimise the use of insecticides in order to reduce selection pressure. Secondly, a strategy designed to avoid selection of resistance mechanisms, considering cross-resistance patterns and resistance mechanisms. Copyright © 2008 Society of Chemical Industry


1 INTRODUCTION

  1. Top of page
  2. Abstract
  3. 1 INTRODUCTION
  4. 2 INSECTICIDE RESISTANCE IN FRANKLINIELLA OCCIDENTALIS
  5. 3 CONDITIONS THAT PROMOTE RESISTANCE
  6. 4 IMPROVED INSECTICIDE RESISTANCE MANAGEMENT
  7. 5 CONCLUSIONS
  8. Acknowledgements
  9. REFERENCES

Western flower thrips (WFT), Frankliniella occidentalis (Pergande), arrived in Spain in 19861 and has become one of the major insect pests of vegetable, fruit and ornamental crops.2 WFT is a serious insect pest, feeding on a wide range of crops throughout the world and causing substantial economic crop losses.3 WFT reduces crop yields by direct feeding damage and by transmitting the tospoviruses impatiens necrotic spot virus (INSV) and tomato spotted wilt virus (TSWV).

Frankliniella occidentalis can be difficult to control. Use of insecticides has been the primary strategy for controlling WFT, especially in virus-sensitive crops, where a great number of specific treatments are applied against it. However, the range of insecticides and formulations that are effective against WFT is limited. Insecticide resistance has been documented in a number of chemical classes, including the organochlorines, organophosphates, carbamates, pyrethroids and spinosyns.4–15

Owing to the high cost of insecticides, including research, registration and production, it is important to preserve existing insecticides by developing and implementing resistance management strategies. The objective of the following perspective is to discuss insecticide resistance issues associated with WFT populations and propose strategies to minimise the prospect of insecticide resistance.

2 INSECTICIDE RESISTANCE IN FRANKLINIELLA OCCIDENTALIS

  1. Top of page
  2. Abstract
  3. 1 INTRODUCTION
  4. 2 INSECTICIDE RESISTANCE IN FRANKLINIELLA OCCIDENTALIS
  5. 3 CONDITIONS THAT PROMOTE RESISTANCE
  6. 4 IMPROVED INSECTICIDE RESISTANCE MANAGEMENT
  7. 5 CONCLUSIONS
  8. Acknowledgements
  9. REFERENCES

2.1 Development of resistance

Insecticide resistance is a complex and intractable problem.3 Not surprisingly, since the mid-1980s, resistance in WFT populations has been the focus of much research following its establishment and spread in greenhouses and outdoor-production agriculture.3

The first reports of resistance were associated with toxaphene applied to cotton,16 and since then there have been instances of lack of insecticide efficacy from all the major chemical classes owing to frequent applications.7 Because of the low damage threshold on crops susceptible to TSWV, insecticides are widely used to control WFT. However, the indiscriminate use of insecticides, the short generation time of WFT, its high fecundity and its haplodiploid reproduction system have resulted in the development of resistance to insecticides in a number of classes (Table 1). For example, among the organophosphates, resistance has been reported to chlorpyrifos,4, 7, 14 acephate,5, 9, 14 dimethoate,7 diazinon,8 malathion,9, 14 methamidophos,12 dichlorvos14 and methidathion.14 Insecticide resistance has been reported to certain carbamates, such as to methomyl,4, 7, 8, 14 methio- carb,5, 10–12, 14, 17 bendiocarb,8, 9 carbosulfan10 and formetanate.12, 17 Insecticide resistance has also been documented to the pyrethroids permethrin,4, 8 bifenthrin,4 fenpropanate,7 cyfluthrin,7 cyper- methrin,8, 14 fenvalerate,8 deltamethrin9, 12 and acrina- thrin.12, 17 Finally, resistance has been demonstrated to abamectin,4, 10, 14 endosulfan,5, 12, 14 DDT,8 imidacloprid,8 amitraz,8 fipronil13, 14 and spino- sad.13–15

Table 1. Insecticide resistance mechanismsa reported in Frankliniella occidentalis
InsecticideReduced penetrationP450bEsterasesGSTsbAltered AChEbKnockdownAltered nAChRb
  • a

    + indirect evidence; + + not well clarified; + + + well clarified or numerous evidence.

  • b

    P450 = cytochrome-P450 monooxygenases; GSTs = glutathioneS-transferases; AChE = acetylcholinesterase; nAChR = nicotinic acetylcholine receptor.

Organophosphates
Diazinon + + +8, 20 + + +20 
Carbamates
Bendiocarb + + +8, 21 
Formetanate + + +18 
Methiocarb + + +11, 18+ +11, 23, 24+ +11+ +11 
Pyrethroids
Acrinathrin + + +18+ +23 
Deltamethrin + + +9 
Fenvalerate+ + +22+ + +8, 22 +22 
Permethrin + + +4 +4 
Spinosyns
Spinosad + +15

In order to control WFT in greenhouses, some farmers apply up to 19 sprays at 3–4 day intervals throughout the growing season (9 months), which increases the development of insecticide resistance. In Almeria and Murcia (Spain), moderate to high levels of resistance have been detected to the insecticides methiocarb, formetanate and acrinathrin after intensive use.12 These WFT populations exhibited resistance to acrinathrin, reaching high levels in both field and laboratory conditions.17 Formetanate and methiocarb resistance was also detected, although at moderate levels.17

The rate at which WFT develops resistance is a concern when using insecticides. Severe resistance problems associated with other insecticides12, 17, 18 and high spinosad efficacy caused spinosad overuse in some areas, where as many as ten applications per crop (1.5 crops per year) were made.15 This overuse has resulted in resistant WFT populations in the greenhouses of south-eastern Spain, which is an area of very intensive insecticide use.15 Similarly, frequent applications of spinosad throughout the USA has led to the development of resistant WFT populations there.19

Moreover, there are not many effective insecticides registered for control of WFT, making rotation difficult. In addition, host crops are in continuous production, and resistant WFT may migrate within and among crops, thus increasing exposure to insecticide sprays.

2.2 Resistance mechanisms

Resistance in WFT populations is associated with both enhanced detoxification and modification of target sites.4–15 Two different resistance mechanisms have been reported in WFT populations from south-eastern Spain.15, 18 One is associated with enhanced detoxification by monooxygenases, conferring resistance to acrinathrin, methiocarb and formetanate.12, 17, 18 The other, based on altered target site, confers resistance to spinosad.15

Resistance to different insecticides has been demonstrated in many WFT populations.4–15 Cross-resistance to insecticides within the same chemical class and to those in other chemical classes suggests a metabolic resistance mechanism. Different resistance mechanisms such as monooxygenases,4, 8, 9, 11, 18, 20–22 esterases,11, 23 glutathione S-transferases,11 altered acetylcholinesterase (AChE),11, 20, 24 reduced penetra- tion,22 knockdown resistance4, 22 and altered target site15 may contribute to resistance in WFT populations (Table 1). Nevertheless, recent research18 indicates that the major resistance mechanism to most insecticide classes in WFT populations is metabolic, piperonyl butoxide (PBO)-suppressible and mediated by cytochrome-P450 monooxygenases.18 However, other mechanisms including GST, esterases, altered AChE and reduced penetration may also contribute to insecticide resistance.

Resistance to insecticides in WFT populations has been associated with monooxygenase activity.4, 8, 9, 11, 15 For example, piperonyl butoxide (PBO), a microsomal monooxygenase inhibitor, has been used to increase the toxicity of permethrin to several field populations of WFT.4 The metabolic mechanisms of resistance to diazinon, bendiocarb and fenvalerate were shown to be suppressible by PBO, but not by DEF (S,S,S-tributyl phosphorotrithioate), an esterase inhibitor, suggesting an enhanced detoxification by monooxygenases.8 Synergism of deltamethrin by PBO has been reported.9 The addition of PBO did not synergise the activity of methiocarb against WFT populations exhibiting slight resistance.24 However, PBO synergised the activity of methiocarb against field populations with higher resistant factors.11

Studies based on biochemical methods have indicated that P450 monooxygenases confer insecticide resistance in WFT populations.20–22 In a diazinon-selected population, also more resistant to bendiocarb and fenvalerate,8 enhanced metabolism was mainly oxidative.20–22

The activities of esterases and GST have been evaluated in several WFT populations, although their role in insecticide resistance is not clear. In a diazinon-selected WFT population, esterase activity was slightly lower than in a susceptible reference population.20 Furthermore, staining for esterases following electrophoretic separation revealed more esterase bands in the susceptible WFT reference population. In addition, no differences were discovered in GST activity. Based on these results, it appears that esterases and GST are not involved in insecticide resistance. In a study with two populations of WFT from California and Denmark,24 the methiocarb-resistant population from Denmark displayed increased esterase activity compared with the Californian population, although the differences in esterase activity may be due to different expression levels of esterases not directly related to resistance.25 Additionally, it has been demonstrated that there was increased esterase activity in two of three methiocarb-resistant WFT populations compared with susceptible laboratory populations.11 However, these two WFT populations were collected from greenhouses, and thus any differences in esterase activity may be due to the variation in expression levels of esterases unrelated to resistance. Moreover, methiocarb selection in one laboratory population increased the level of methiocarb resistance but did not significantly increase esterase activity. Similar to esterases, GST activity is higher in field populations of WFT.11 Esterase activity has been evaluated in Spanish field populations of WFT.23 Field populations of WFT showed higher esterase activity than laboratory populations, according to other studies,11 and moderate methiocarb resistance corresponded well to carboxylesterase activity.23

The presence of altered acetylcholinesterase (AChE) has been studied in diazinon-selected WFT populations.20 For example, although the AChE level did not differ between the diazinon-selected and the reference WFT population, altered AChE with reduced sensitivity to diazoxon contributed to resistance in the selected population.20 Although the selected WFT population was also resistant to bendiocarb, no differences in bendiocarb sensitivity were evident between AChEs in the resistant and reference WFT populations.21 Selection for methiocarb, based on exposure, increased the level of methiocarb resistance and the AChE level.11 However, in field populations of WFT, a highly methiocarb-resistant population exhibited similar AChE levels when compared with a susceptible population. In contrast, laboratory methiocarb-selected WFT populations did not display reduced AChE sensitivity to methicoarb, dichlorvos or eserine, whereas the field populations did. Hence, the role of altered AChE (increased AChE activity and/or reduced AChE sensitivity) as a resistance mechanism against insecticides in WFT populations is not well understood.

Reduced insecticide penetration in WFT populations has been evaluated as a resistance mechanism.22 In one study, fenvalerate penetrated more slowly into diazinon-selected WFT populations compared with a susceptible population, suggesting that reduced penetration confers resistance to fenvalerate. However, diazinon penetrated faster through the cuticle of a selected WFT population.20 Additionally, there were no differences in bendiocarb penetration between the two WFT populations.21

It has been suggested, based on indirect evidence of cross-resistance among pyrethroids and to pyrethroids and DDT, that pyrethroid resistance in WFT populations is due to knockdown resistance.4, 22, 25 However, pyrethroid resistance may actually be due to enhanced metabolism mediated by monooxygenases.18 Cross-resistance of WFT populations to pyrethroids and insecticides in other chemical classes has been extensively reported.4, 5, 8, 9, 12, 17 Enhanced rate of detoxification by monooxygenases has been considered a resistance mechanism of a number of pests to DDT,26 and it has more recently been suggested to explain the resistance of WFT populations to pyrethroids.4, 8, 9, 22

Resistance to insecticides from different chemical classes is common in WFT populations,4–15 even in those not specifically used for thrips control.5, 9 Although alternative resistance mechanisms such as esterases, GST, altered AChE and reduced penetration may contribute to WFT populations developing resistance to insecticides, monooxygenese activity seems to be the major mechanism of resistance (Table 1) to pyrethroids, organophosphates and carbamates.25

A recent study15 reported a new mechanism of resistance to spinosad in WFT populations. Synergists (PBO, DEF and DEM) used in vivo to block specific enzyme systems failed to enhance the toxicity of spinosad in resistant populations of WFT, indicating that metabolic mediated detoxification was not responsible for spinosad resistance. It is possible that the resistance mechanism to spinosad in WFT populations may be an altered target site, which agrees with a monogenic mode of inheritance.27

3 CONDITIONS THAT PROMOTE RESISTANCE

  1. Top of page
  2. Abstract
  3. 1 INTRODUCTION
  4. 2 INSECTICIDE RESISTANCE IN FRANKLINIELLA OCCIDENTALIS
  5. 3 CONDITIONS THAT PROMOTE RESISTANCE
  6. 4 IMPROVED INSECTICIDE RESISTANCE MANAGEMENT
  7. 5 CONCLUSIONS
  8. Acknowledgements
  9. REFERENCES

3.1 Characteristics of thrips biology

Frankliniella occidentalis is a highly polyphagous insect with a wide host range, feeding on more than 240 plant species in 62 different plant families, including ornamentals, fruits, vegetables and many agricultural crops.28 Robb et al.7 indicate that WFT are able to detoxify many types of plant toxins, which may predispose them to survive exposure from other xenobiotic compounds. Polyphagy implies a broad-spectrum enzyme system, which might degrade many different insecticides. The major resistance mechanism in F. occidentalis populations is metabolic, mediated by cytochrome-P450 monooxygenases,18 which confer cross-resistance among insecticide classes.

WFT has a short life cycle and high female fecundity, which enhance the potential to develop resistance. At temperatures between 20 and 25 °C, WFT require 2–3 weeks to develop from egg to adult, but at higher temperatures it takes less than 10 days.28, 29 WFT females can lay up to 250 eggs during their lifetime, depending on plant host and presence of pollen.29–31 WFT does not have discrete generations (multivoltine), so overlapping generations are typically present, which increases the exposure of the different life stages to insecticide applications and promotes insecticide resistance.32

Finally, WFT has a reproduction system based on haplodiploidy, whereby males are produced uniparentally from unfertilised, haploid eggs, and females are produced biparentally from fertilised, diploid eggs.33–35 Female WFT are diploid, whereas male WFT are haploid.34, 35 A primary consequence of a haplodiploid reproduction is that resistance genes arising by mutation are exposed to selection from the outset in hemizygous males, irrespective of intrinsic dominance or recessiveness,32 which tends to accelerate (although not always) resistance to insecticide development.33, 35–39 Results of a simulation model32 demonstrated that, when a resistance allele is dominant, semi-dominant or recessive, resistance develops at a similar rate in a haplodiploid reproduction, while recessiveness causes resistance development delay in corresponding diploid populations. When resistance alleles are dominant or nearly so, as acrinathrin resistance in WFT populations,40 another consequence of hemizygosity is to accelerate their rate of fixation, because the susceptible alleles are no longer shielded in males. WFT populations from south-eastern Spain have displayed a rapid resistance development to acrinathrin, reaching high levels under both field and laboratory conditions.17 Haplodiploidy may contribute to WFT populations developing resistance to newer insecticides, especially when exposed to high selection pressure, as occurred after the introduction of spinosad in south-eastern Spain,15 in spite of the fact that spinosad resistance is recessive.27

3.2 Agricultural/pest management practices

The evolution of resistance may be influenced by seasonality and relative abundance of treated and untreated plant hosts, and by migration patterns between or among hosts at different times of the year. In addition, the continuous availability of suitable host plants enables WFT populations to be active and reproduce throughout the year. Regional variation in production systems may impact upon the rate of resistance development and the effectiveness of resistance management recommendations. In Campo de Cartagena, an area of Murcia in south-eastern Spain, sweet pepper is the main crop grown in greenhouses. WFT overwinter on weeds, lettuce, artichoke, brassica and other crops, and then migrate into greenhouses (sweet pepper) and outdoor melons in the spring and summer. Of these crops, only lettuce and sweet pepper are treated frequently with insecticides to control WFT, as they are susceptible to TWSV. Therefore, the abundance of field crops provides a refuge for insects carrying susceptible genes. In addition, sweet pepper acreage employing biological agents to control WFT has recently increased from 4% in 1999 to 95% in 2006, which reduces selection pressure in WFT populations in Murcia.

In the neighbouring province of Almeria, where insecticide resistance is more severe,15 thrips host plants are continually present in greenhouses. Out of more than 30 000 ha of greenhouses (‘a plastic sea’), there are neither other crops nor weeds where susceptible WFT populations may take refuge. The continuous availability of crops that are intensively sprayed with insecticides throughout the year increases the risk of WFT developing resistance, providing near-ideal conditions for selecting resistance genes. In addition, there are low or even zero tolerance thresholds for WFT, thus promoting frequent spraying of insecticides and increasing selection pressure. As a consequence, it is no coincidence that WFT has rapidly developed resistance to newer insecticides such as spinosad.15

However, integrated pest management (IPM) practices are increasing in use, and biological control programmes are being implemented in Almeria, mainly owing to insecticide resistance in WFT populations. Greenhouses using biological control agents have increased from 3% in 2006 to 28% in 2007, which should reduce the selection pressure on WFT populations.

4 IMPROVED INSECTICIDE RESISTANCE MANAGEMENT

  1. Top of page
  2. Abstract
  3. 1 INTRODUCTION
  4. 2 INSECTICIDE RESISTANCE IN FRANKLINIELLA OCCIDENTALIS
  5. 3 CONDITIONS THAT PROMOTE RESISTANCE
  6. 4 IMPROVED INSECTICIDE RESISTANCE MANAGEMENT
  7. 5 CONCLUSIONS
  8. Acknowledgements
  9. REFERENCES

The PBO-suppressible metabolic resistance mechanism in WFT populations, which results in cross-resistance to three insecticides (formetanate, methiocarb and acrinathrin) applied for WFT control,18 indicates the need to rotate insecticides with different mechanisms of resistance, and/or use synergists that inhibit metabolic resistance. Applying low rates of a carbamate-based insecticide with acrinathrin may increase the susceptibility of WFT populations to pyrethroids.41

Spinosad resistance is not metabolic, but due to an altered target site.15 In addition, spinosad resistance in WFT populations declines significantly in the absence of selection pressure and in the presence of susceptible WFT populations.42 Lack of cross-resistance with other insecticides,15 the recessive nature of spinosad resistance27 and unstable resistance in the field42 mean that it is important to rotate spinosad with other insecticides such as acrinathrin, methiocarb or formetanate with different resistance mechanisms in order to reduce the development of insecticide resistance.

As such, an insecticide resistance management (IRM) strategy was implemented for Spanish greenhouse crops in 2005 by rotating insecticides with different resistance mechanisms. Some organophosphates (OPs) were incorporated in order to increase the number of compounds used. In laboratory studies, naled, chlorpyrifos-methyl and malathion did not show cross-resistance with pyrethroids and carbamates, nor with spinosad (unpublished data).

Local migration of susceptible thrips from weeds and untreated crops has led to the success of this IRM strategy in Murcia. However, in Almeria, where insecticide resistance problems are much more severe, this IRM strategy is not sufficient to avoid or delay resistance development owing to high levels of resistance, the high frequency of insecticide applications, the continuous presence of hosts, the lack of refuges for susceptible populations and, definitively, a production system that permits a high pressure of selection. Clearly, resistance management involves the individual grower and extended collaboration.

An improved IRM strategy is necessary to control WFT populations with insecticides in areas with severe resistance problems. Multiple approaches to avoid resistance are recommended, as opposed to employing one tactic.43 The improved IRM strategy proposed here consists of a double approach. Firstly, a general strategy to minimise the use of insecticides in order to reduce insecticide selection pressure. This strategy is therefore designed to contend with the entire pest complex. Secondly, a specific strategy for WFT in order to avoid selection for resistance mechanisms.

4.1 Reduce insecticide selection pressure

The key to managing resistance is to reduce selection pressure. There is general agreement that reduced pesticide use is an essential element of any IRM.43, 44 The main goal is related to rationalising and optimising the way that the insecticides are applied. Therefore, it becomes necessary to optimise the use of insecticides, that is, to apply just the right number of treatments (not more nor less) that allows a suitable control of the pest complex. Any insecticide application in a crop influences the evolution of the insecticide resistance of WFT populations, even when thrips are not the target. It is especially important to avoid induced resistance in WFT populations owing to insecticide applications against other pests. Insecticide exposure could predispose WFT populations to resistance by the induction of detoxification enzymatic systems (‘that which does not kill you makes you stronger’). Therefore, it is important to minimise insecticide applications, and, in order to make this compatible with a suitable pest control, it is necessary to apply high-quality treatments. That is, fewer treatments but with greater precision.

These general strategies recommended to optimise insecticide use utilise the following tactics:

  • use insecticides only when required;

  • accurate and precise insecticide applications;

  • diversify control methods;

  • conserve natural enemies.

4.1.1 Use insecticides only when required

The best way to delay insecticide resistance is to use insecticides only when necessary, which reduces the selection pressure placed on WFT populations. This may be accomplished by scouting, which determines the population dynamics of WFT. Insecticides should be used only when the economic threshold is reached and when the natural mortality factors present in the environment are not capable of preventing the pest population from reaching the economic-injury level.45

4.1.2 Accurate and precise insecticide applications

Decisions on application rates and the numbers of applications per growing season should be made with the understanding that they affect the speed with which resistance will develop. Consistent with IPM principles, the Insecticide Resistance Action Committee (IRAC) recommends the following resistance guidelines [IRAC International (http://www.irac-online.org)]:

  • Scout to assist in timing of insecticide applications for maximum effect, by making applications when a high percentage of the population is at a vulnerable life stage.

  • Follow label application rates and intervals between applications in order to avoid increasing selection pressure.

  • In order to reduce selection pressure for non-target pests, avoid broad-spectrum insecticides when narrow or specific insecticides will work.

  • The pH of water used in tank mixes may need to be adjusted.

  • If necessary, add surfactants to enhance insecticide efficacy.

  • Spray nozzles and spray equipment should be calibrated and routinely checked.

  • Use appropriate application volumes and techniques recommended by local crop advisors.

  • Provide refuge for susceptible individuals in order to prevent a higher proportion of resistant WFT from dominating the population.

As for Bemisia tabaci Genn., during the 1990s,32 one response to increasing resistance in F. occidentalis was to screen numerous combinations of products for possible synergistic effects. Some mixtures of acrinathrin (pyrethroid) and carbamates proved remarkably effective in this respect, as shown by laboratory bioassay data.41 More studies are being carried out to find more synergist combinations (unpublished data). However, they should be recommended with caution, as was learned from the failure of mixtures against B. tabaci after their overuse.32, 46

4.1.3 Diversify control methods

Reducing insecticide use may still result in resistance, as existing WFT populations may already possess resistant genes owing to previous insecticide exposure.11 As such, it is important to implement alternative management strategies, including cultural control (proper watering and fertilisation, sanitation, disposal of plant residues, weed removal and crop rotation), physical control (microscreening), biological control (use of predators, parasitoids and pathogens), genetic control (host plant resistance) and biotechnical control (use of pheromone or colour traps).

The use of one or a combination of these alternative management strategies may reduce the need for insecticides, thus decreasing the selection pressure placed on WFT populations.

4.1.4 Conserve natural enemies

It is important that insecticides are compatible with natural enemies, so that both strategies may be used in conjunction. Unfortunately, current insecticides used for WFT control, excluding spinosad, are not compatible with natural enemies. Alternatively, the use of biological controls or chemical controls in different crop periods may reduce insecticide selection pressure.

4.2 Avoid resistance mechanism selection

Usually, IRM strategies have been designed on the basis of rotation of insecticides with different modes of action. However, insecticide resistance is related not only to modes of action but also to resistance mechanisms. Rotation of modes of action avoids selection for altered target sites but not for other resistance mechanisms, such as metabolic resistance. An IRM strategy based on resistance mechanisms, considering cross-resistance patterns, has yet to be designed for WFT. Here, the key is to know which resistance mechanism is selected by each insecticide, in order to avoid inadvertent selection for particular resistance mechanisms. Functionally, the tactic involves avoiding the tank mix or the repeated use of the same insecticide, or insecticides with cross-resistance (with the same resistance mechanism).

Broadbent and Pree9 suggested rotating insecticides with different modes of action after each generation. To control WFT in greenhouses, Robb and Parrella47 recommend rotation of compounds with different modes of action every 4–6 weeks, thereby only exposing two or three generations to the same mode of action. A resistance management strategy based on rotating modes of action was introduced in Australia,48 with three consecutive applications of the same insecticide at 3–6 day intervals, followed at least 2 weeks later by another series of three applications using an insecticide with a different mode of action.

These strategies assume that there is no degree of cross-resistance between products with different modes of action. However, a metabolic resistance mechanism may confer resistance to insecticides with a different mode of action. Cross-resistance between carbamates and pyrethroids has been reported in WFT populations with a different metabolic resistance mechanism.17 In contrast, carbamates and OPs have the same mode of action but no cross-resistance in WFT populations (unpublished data). Thus, there could be considerable risk in depending on a rotation strategy based on modes of action. Therefore, rotation of insecticides may be effective in delaying development of resistance if the insecticides used select for different resistance mechanisms, but it is essential to ensure that successive generations are not exposed to related compounds with cross-resistance. If the resistance mechanisms and cross-resistance patterns are not identified, then rotation schemes should generally encompass as many insecticides with different modes of action as possible.

The rotation suggested here as IRM strategy for WFT control is the alternation of the metabolic resistance mechanism for pyrethroids (acrinathrin) and carbamates (methiocarb and formetanate) on the one hand with the altered target site mechanism for spinosyns (spinosad) on the other, with the application of OPs in between owing to their lack of cross-resistance with the other mechanisms. An example of this rotation could be: methiocarb, malathion, spinosad, naled, formetanate and chlorpyrifos-methyl.

Mixtures of products are often applied so that individuals are exposed simultaneously to more than one toxicant. Mixtures require several important assumptions: resistance is monogenic and functionally recessive, no cross-resistance is present, resistant individuals are rare and of equal persistence and there is some untreated population.43, 44 In WFT populations it is difficult to meet all these assumptions, so the use of mixtures will probably increase the rate of resistance development.

When rotating insecticides it is assumed that the frequency of individuals that are resistant to one insecticide will decline during the application of the other product. This may occur if there is negative cross-resistance, a fitness cost associated with resistance or movement of susceptible individuals into the population.43, 44 Resistance alleles do not always produce detectable levels of lowered fitness. It is likely that natural selection will increase the number of ‘modifying genes’ that restore fitness to individuals carrying resistance alleles. Therefore, where a widespread resistance to most conventional insecticides is established, a single-tactic strategy of resistance mechanism rotation will not work, as is happening in Almeria. It is then necessary to incorporate other chemical tactics to the rotational strategy. With the majority of insecticides affected by resistance to varying degrees, compounds with less exploited modes of action are assuming major importance as components of thrips control programmes. Although insect growth regulators (IGRs) can also be vulnerable to resistance, they are unlikely to show cross-resistance with other compounds, and exhibit more favourable environmental profiles. IGRs act primarily against immature stages of thrips. Towards the end of the second larval stage, F. occidentalis larvae stop feeding and move down the plant into the soil to pupate. The thrips pass through two ‘pupal’ stages (propupal and pupal). IGR applied as a soil treatment by drip irrigation or sprayed onto the soil could prove effective against a different life stage than other insecticide treatments (unpublished data). These characteristics, coupled with a high degree of species selectivity, make them ideally suited as rotation partners in control programmes that place emphasis on the preservation of natural enemies and coexisting pest species.49

5 CONCLUSIONS

  1. Top of page
  2. Abstract
  3. 1 INTRODUCTION
  4. 2 INSECTICIDE RESISTANCE IN FRANKLINIELLA OCCIDENTALIS
  5. 3 CONDITIONS THAT PROMOTE RESISTANCE
  6. 4 IMPROVED INSECTICIDE RESISTANCE MANAGEMENT
  7. 5 CONCLUSIONS
  8. Acknowledgements
  9. REFERENCES

Owing to widespread insecticide resistance to most conventional insecticides, proper stewardship of existing insecticides is essential so that control of WFT can be achieved. However, thrips are not the only pest in the crop, so the strategy should therefore be designed to contend with the entire pest complex present.

The improved IRM strategy proposed here consists of a double approach. Firstly, a general strategy to minimise and optimise the use of insecticides in order to reduce insecticide pressure. This general strategy has to be designed for each crop, but four guidelines are recommended: insecticides used only when required, accurate and precise insecticide applications, diversification of control methods and conservation of natural enemies.

Secondly, a WFT-specific strategy is proposed in order to avoid selection of resistance mechanisms, considering cross-resistance patterns and resistance mechanisms. Here, the key is to know which resistance mechanism is selected by each insecticide, in order to avoid inadvertent selection for particular resistance mechanisms. Functionally, the tactic involves avoiding the tank mix or the repeated use of the same insecticide or insecticides with cross-resistance (with the same resistance mechanism). However, where widespread resistance to most conventional insecticides is well established, a rotational strategy of resistance mechanisms will not be enough, and other chemical tactics and cultural, physical and biological control approaches will need to be incorporated.

Acknowledgements

  1. Top of page
  2. Abstract
  3. 1 INTRODUCTION
  4. 2 INSECTICIDE RESISTANCE IN FRANKLINIELLA OCCIDENTALIS
  5. 3 CONDITIONS THAT PROMOTE RESISTANCE
  6. 4 IMPROVED INSECTICIDE RESISTANCE MANAGEMENT
  7. 5 CONCLUSIONS
  8. Acknowledgements
  9. REFERENCES

The authors acknowledge anonymous referees for reviews and comments on the manuscript. Research on insecticide resistance in Frankliniella occidentalis at Universidad Politécnica de Cartagena (Spain) has been supported by the Spanish Ministry of Education and Science—CICYT and FEDER (1FD1997-2342-C02-02, AGL2002-04190-C02-02, AGL2005-07492-C02-01) and Fundación Séneca (Agencia Regional de Ciencia y Tecnología, Región de Murcia) (00604/PI/04).

REFERENCES

  1. Top of page
  2. Abstract
  3. 1 INTRODUCTION
  4. 2 INSECTICIDE RESISTANCE IN FRANKLINIELLA OCCIDENTALIS
  5. 3 CONDITIONS THAT PROMOTE RESISTANCE
  6. 4 IMPROVED INSECTICIDE RESISTANCE MANAGEMENT
  7. 5 CONCLUSIONS
  8. Acknowledgements
  9. REFERENCES
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