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Research ArticleReceived: 9 September 2010 Revised: 19 November 2010 Accepted: 19 November 2010 Published online in Wiley Online Library: 26 January 2011

(wileyonlinelibrary.com) DOI 10.1002/ps.2101

Pyrethroid resistance monitoring in Europeanpopulations of pollen beetle (Meligethes spp.):a coordinated approach through theInsecticide Resistance Action Committee (IRAC)Russell Slater,a∗ Steve Ellis,b Jean-Paul Genay,c Udo Heimbach,d

Gerald Huart,e Michel Sarazin,f Chris Longhurst,g Andreas Muller,d

Ralf Nauen,h Jean Luc Risoni and Fabrice Robinj

Abstract

BACKGROUND: Pollen beetle (Meligethes spp.) is a major pest of European oilseed rape crops. Its resistance to pyrethroidinsecticides has been recorded in samples of beetles collected in Europe since at least 1999, and problems with the control ofthe beetle in the field have been widely reported. In 2007, a Pollen Beetle Working Group was formed through the InsecticideResistance Action Committee (IRAC) in order to coordinate efforts for surveying pyrethroid resistance development.

RESULTS: The results of the first 3 years of the pollen beetle pyrethroid susceptibility survey using a laboratory test arepresented in this paper. Resistant beetle samples were collected from 20 of the 21 countries surveyed, with a general trend ofincreasing frequency and spread of resistant samples in European oilseed-rape-growing regions.

CONCLUSION: Pyrethroid-resistant beetles dominate in Western and Central Europe and are becoming established in the Northand East, the main oilseed-rape-growing areas of Europe. The development and spread of pyrethroid-resistant pollen beetleshighlights the need for effective management strategies for oilseed rape insect pests.c© 2011 Society of Chemical Industry

Keywords: pollen beetle; Meligethes aeneus; pyrethroid resistance; susceptibility monitoring; IRAC; oilseed rape

1 INTRODUCTIONOilseed rape is an economically and politically valuable crop inEurope. Its importance has seen an approximate 60% increasein the area grown since 2000. However, European oilseed rapeproduction has been under threat from one of its major pests,pollen beetle (Meligethes spp.). In high numbers, this beetle cancause significant damage to the plant. Heavy attacks from thebeetles can cause a major loss in yield, with some growers innorthern Germany experiencing a 100% loss of the crop in 2006.Pollen beetles have traditionally been controlled with broad-spectrum insecticides, but the removal of organophosphates as acontrol option had until recently left pyrethroids as the only classof insecticides registered in many countries.1 – 4

Resistance to insecticides was first reported in 1967 in Polishpopulations of Meligethes aeneus Fabricius.5 However, the firstcases of resistance to pyrethroids were recorded during 1999in north-eastern France,6,7 but pyrethroid-resistant beetles mayhave been present in significant numbers as early as 1997.1

Subsequently they have been located in many of the oilseed-rape-growing parts of Europe by many researchers using a variety ofmethods to measure pyrethroid susceptibility.8,9

∗ Correspondence to: Russell Slater, Syngenta Crop Protection, Werk Stein,Schaffhauserstrasse, CH-4332, Stein, Switzerland.E-mail: Russell.Slater@syngenta.com

a Syngenta Crop Protection, Werk Stein, Stein, Switzerland

b ADAS, High Mowthorpe, Yorkshire, UK

c NuFarm, Gennevilliers, France

d JKI Institute for Plant Protection in Field Crops and Grassland, Braunschweig,Germany

e Maktheshim Agan France, Sevres Cedex, France

f FMC, Chemical-Agricultural Products Group, Brussels, Belgium

g DOW Agrosciences, European Development Centre, Abingdon, Oxfordshire, UK

h Bayer Crop Science AG, Research Insecticides, Monheim, Germany

i DuPont de Nemours France, Centre Europeen de Recherche et Developpement,Nambsheim, France

j BASF, BASF SE, Li555, Limburgerhof, Germany

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In 2007, a Pollen Beetle Working Group was formed through theInsecticide Resistance Action Committee (IRAC). This action groupbrought together representatives from agrochemical companies,government regulators and advisors, academics and researchinstitutes to work together to provide fundamental informationand advice that would allow for effective resistance and pestmanagement of pollen beetle and other oilseed rape pests.The European resistance monitoring programme, which utilisesa simple, common methodology, was organised to provideinformation on the current distribution and intensity of pyrethroid-resistant beetles within Europe.

The methodology was developed by the working group onthe basis of previous methods used by Syngenta Crop Protection,Bayer CropScience and the German Expert Committee on PesticideResistance – Insecticides (ECPR-I). Similar methods were alsodeveloped by INRA and other research institutes in France.10

The method is based on an insecticide-coated glass vial andprovides a rapid indication of the susceptibility of a pollen beetlepopulation to pyrethroid insecticides. This simple method hasallowed the mapping of pyrethroid-resistant samples across largeareas by the group and other contributing researchers to generatea susceptibility overview for 2007–2009.

2 METHODS2.1 Sample collectionPollen beetle (Meligethes spp.) samples were collected from diverselocations across the oilseed-rape-growing regions of Europebetween March and July of each study year. Samples were notselected on the basis of treatment history and reports of resistancebut according to availability of suitably sized populations of beetlesat the single location. Beetles collected from an individual fieldwere considered as a single sample, and approximately 150 adultbeetles were collected across the infested field. Beetles werestored (20 ± 2 ◦C) in an aerated plastic container that had drypaper towelling placed at the bottom to prevent excess moisture,or in perforated plastic bags. Oilseed rape leaves plus two or threerape inflorescences were added to the container as a food sourceand to provide shelter during transportation. The insects werenot subjected to excessive temperature, humidity or starvationstress after collection, and physical handling of the beetles wasreduced to a minimum. On arrival in the laboratory, the beetleswere released into a ventilated holding cage and left to recoverovernight.

2.2 IRAC susceptibility test method No. 11-v2Glass vials with an internal surface area of 20–80 cm2 were usedas vessels for this study. Prior to testing, the inner surface of theglass vials was coated with technical-grade lambda-cyhalothrinwhich had been dissolved in acetone. Three treatments wereutilised: 0.075 µg cm−2 (100% of the typical field application rateof 7.5 g AI ha−1), 0.015 µg cm−2 (20% rate) and an acetone-onlysolution (control treatment). Insecticide solutions were preparedto provide the required test concentrations, and then 500–1500 µL(depending on the vial size, with the solution covering the baseof the vial when placed horizontally) of solution was added toeach test vial and rotated on a rolling bank at room temperatureuntil the acetone was completely evaporated. A minimum of tworeplicates of each concentration and control were used. A totalof 10–20 adult beetles were added to each test vial before thevial was capped and stored at 20 ± 2 ◦C. The number of beetles

Table 1. Susceptibility categories utilised for determining pollenbeetle susceptibility to pyrethroids

Concentration(% of label rate)

Severely affectedbeetles (%) Classication Code

100 100 Highly susceptible

20 100

100 100 Susceptible

20 100

100 100 to 90 Moderately resistant

100 90 to 50 Resistant

100 50 Highly resistant

1

2

4

5

3≥≥

<<<

<

severely affected (dead and moribund) was scored after 24 h.Results were expressed as percentage affected. If more than 20%of the beetles in the control treatment were affected, then thestudy was considered as being invalid.

A susceptibility rating scheme (Table 1) was used to categorisethe test sample as being: highly susceptible, susceptible, moder-ately resistant, resistant or highly resistant. Although not presentedin this paper, these susceptibility categories have been validatedalongside pyrethroid efficacy field trials to demonstrate that re-duced efficacy in the glass vial assay correlated with equivalentreduced performance in the field (Slater R, unpublished).

3 RESULTS AND DISCUSSIONDuring the 3 years of study, over 1500 populations of pollenbeetle (Meligethes spp.) were collected from 21 different countriesand surveyed for their susceptibility to pyrethroid insecticides(Table 2). It is important to acknowledge that this study providesonly an indication of the susceptibility status of a selectedsample, which is likely to be heterogeneous both in individualbeetle susceptibility, species composition and possibly resistancemechanisms. Meligethes aeneus is the dominant species inEuropean oilseed rape crops (Kirk-Spriggs AH and Slater R,unpublished) and is the only species that has been identifiedto be resistant to pyrethroids; however, other species of pollenbeetle are present in different proportions throughout Europe,and the authors acknowledge that these are likely to have someinfluence on sample susceptibility.

Pyrethroid resistance was first identified in the Champagneregion of eastern France in 1999 and has spread throughout manyof the oilseed-rape-growing regions. This survey demonstratesthat resistant beetles continue to be dominant in this country.However, a comparison of previous unpublished surveys suggeststhat the highly resistant samples observed in 2000–2005 werenot as prominent during 2007–2009. This is an observationsupported by results from the French Pollen Beetle WorkingGroup, which reported highly resistant beetles at their peak in2000, with subsequent years’ observations showing a declinein the proportion until none was observed in 2004.11 The2009 IRAC survey confirms these observations, with moderatelyresistant and resistant samples dominating the major oilseed-rape-growing areas and susceptible samples found mainly in thefar south (Midi-Pyrenees) and west (Bretagne). In spite of thecontinued dominance of resistant samples in the 2009 survey,results suggest that susceptible samples can be found in centraland eastern France (Lorraine and Bourgogne) close to resistantsamples.

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Tab

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1136

559

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ce16

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696

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850

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566

Ger

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92

2817

3913

325

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80

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4327

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475

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367

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no

dat

a.

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Figure 1. European map demonstrating the spread of different pollen beetle susceptibilities in 2009.

Resistant samples dominate in countries along the northernEuropean coastline. One hundred percent of samples collected inBelgium and Denmark were pyrethroid resistant during the 3 yearsof the survey, and in Sweden for 2 years of the survey. In addition,more than 90% of samples were resistant in Poland and 80% in theNetherlands during the 2009 survey (Fig. 1). The reason for suchhigh levels of resistant samples is difficult to explain from the datagenerated in this study; however, proximity to the first recordedcases of the resistance, lack of available alternative insecticidemodes of action and agricultural practice should be considered.

In Germany, resistant samples of pollen beetle were firstidentified in the North, in the Schleswig-Holstein region,6 andwest in the Rhineland-Palatinate.3,7 In subsequent years, resistantsamples have spread to other parts of the country, with susceptiblesamples only found in central Germany during 2009 (North Rhine-Westphalia, Thuringia, Hessen and Lower Saxony). However,susceptibility of pollen beetle samples has remained evenlydistributed across the susceptibility categories used in this study,with a shift towards more resistant populations being observedover the period of monitoring. A slow shift in the dominanceof resistant samples was also observed in Austria (Fig. 2) andSwitzerland, where a high percentage of susceptible sampleswere observed in 2007, but subsequently resistant samples havespread and become more dominant.

The survey presented in this paper suggests a north-east spreadof resistant pollen beetles; however, the lack of samples frommore easterly countries in the earlier years of this study hasto be taken into account, as this may have some influence onthe data interpretation. Certainly, resistant samples are moredominant in Lithuania, Russia, Slovakia and Czech Republic duringthe final years of this study. Estonia, Finland, Hungary and Latviahave predominantly susceptible samples with some samples of

moderately resistant beetles, and only Romanian samples remain100% susceptible throughout the duration of the survey.

In spite of its proximity to areas of Europe that have had highpercentages of resistant beetle samples for a number of years,the first reported cases of pyrethroid resistance did not occur inthe United Kingdom until 2007 (Fig. 2). Subsequently, resistantsamples have been identified along the eastern coastline ofEngland. Nonetheless, susceptible samples remain dominant in theUnited Kingdom, and it may be speculated that the surroundingbody of water has provided a barrier to immigrant resistant beetlesfrom the rest of Europe.

4 SUMMARY AND CONCLUSIONPyrethroid resistance in European populations of M. aeneuscontinue to spread, with resistant beetles found in 20 of the 21countries surveyed over the 3 year period of monitoring. Whetherresistant beetles originated at a single source and have spread orthere have been multiple simultaneous selections for resistance inseveral locations is open to debate, but it seems clear that the pest’smobility and the continued selection of resistant individuals withwidespread pyrethroid use has allowed resistant forms to becomedominant in the oilseed-rape-growing regions of Europe. In spiteof this widespread resistance, pyrethroids still play an importantrole in managing oilseed rape pests. There are few alternatives topyrethroids for the control of other pests in this crop, includingflea beetles (Psylliodes spp. and Phyllotreta spp.), stem and seedweevils (Ceutorhynchus spp.) and brassica pod midge (Dasineurabrassicae Winnertz), and, in some regions where susceptible pollenbeetles dominate, pyrethroids are still an effective control option.

Chemical control options for pollen beetle have becomemore diverse in recent years, with other insecticide modesof action being re-registered, or registered in response tothe development of pyrethroid resistance. Registrations of

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Figure 2. Change in pollen beetle pyrethroid susceptibility between 2007 and 2009.

neonicotinoid-, organophosphate-, spinosyn- and oxadiazine-based insecticides provide alternative control options for oilseedrape growers in some countries, and it is recommended by theauthors that these insecticides be utilised alongside pyrethroidsas part of an effective resistance management strategy. Pestmanagement should be based on the rotation of insecticidemodes of action as part of a chemical control programme whileobserving locally established pest thresholds and optimising theuse of non-chemical control when possible.

The IRAC Pollen Beetle Working Group recommends the segre-gation of the oilseed crop cycle into two segments: prefloweringand flowering. During the preflowering period, which is the mostvulnerable period for pollen beetle damage, growers have achoice of insecticide control solutions depending on the pestspresent and the resistance status of the pollen beetles. Whenpollen beetles are not present, growers can use pyrethroid-,neonicotinoid- or organophosphate-based insecticides to con-trol other pests, depending on the targeted species and localregistrations of each product. If only susceptible pollen bee-tles are present, then growers can choose between pyrethroid-,neonicotinoid-, organophosphate- and oxadiazine-based insecti-cides, again depending on targeted species and registrations. Ifmultiple applications of insecticides are required during this pe-riod, then insecticide modes of action should be used in rotationwith no one mode of action used sequentially. If pyrethroid-resistant pollen beetles are known to be present in the crop orlocality, then the use of pyrethroids is not recommended as theprimary method of control for any of the target pests. During theflowering period, the use of organophosphate and oxadiazine isnot approved, and therefore the control of pests during this periodis restricted to neonicotinoids and pyrethroids, where approvedfor use. If pyrethroid-resistant beetles are present, pyrethroid in-secticides are not recommended as the primary control method,although in some countries they may be the only control methodavailable. Again, insecticide modes of action should be rotatedwith no sequential applications of the same mode of action.Throughout the crop cycle, only two applications of each insecti-cide mode of action are recommended and applications shouldonly be made when locally recommended pest thresholds areexceeded. If aphid control is necessary during the period when

pollen beetles are present in the crop, aphicides not belonging tothe neonicotinoid, organophosphate or pyrethroid mode of actionclass are recommended. Further details on the IRAC oilseed raperesistance management guidelines are given on the IRAC website(www.irac-online.org).

ACKNOWLEDGEMENTSThe authors listed in this paper have been the key representativesof the companies, institutes and organisations that have acted asmembers of the IRAC Pollen Beetle Working Group during its 3 yearexistence. However, this is by no means a comprehensive list ofimportant contributors to this project, with hundreds of individualsfrom many organisations and European countries involved. Theauthors would like to apologise to all those not listed, but at thesame time would like to thank them all for their contributionswhich have made this project a success.

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