Managing insecticide resistance: the good, the bad and the ugly

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1 As submitted 22/11/13 Managing insecticide resistance: the good, the bad and the ugly Steve Foster, Senior Research Scientist Rothamsted Research 5

2 The Good Total Global Insecticide Sales (2010)

3 Myzus persicae Response to neonicotinoids

4 Frequency of Myzus persicae field samples containing mobile aphids (10 ppm imidacloprid screening) % samples Year Response of Myzus persicae field samples to screening dose of imidacloprid compared to Nic standard clones 8.0 Mobility (probits) Mobility (percentage) samples 2011 samples 2012 samples 2013 samples Log concentration (ppm) Nic-S Nic-R Nic-R + Nic-R ++ (SR) Nic-R ++ (RR)

5 Response to pymetrozine Response of field and protected samples to screening dose of pymetrozine in comparison with baseline 8.0 Mobility (probits) Mobility (percentage) Up to (to 5585,5584) Log concentration (ppm) S Baseline 30 ppm

6 Response to flonicamid Response of field and protected samples to screening dose of flonicamid in comparison with baseline 8.0 Mobility (probits) Mobility (percentage) Up to Log concentration (ppm) 2013 S Baseline 30 ppm

7 Response to spirotetramat Response of field and protected samples to screening dose of spirotetramat in comparison with baseline Mobility (probits) Mobility (percentage) Up to Log concentration (ppm) S Baseline 20 ppm

8 Response to cyantraniliprole Response of field and protected samples to screening dose of cyantraniliprole in comparison with baseline Mobility (probits) Mobility (percentage) Up to Log concentration (ppm) S Baseline 30 ppm

9 Summary of Myzus persicae resistance in the UK No overall upward trend in frequency of M. persicae carrying low (Nic-R) neonicotinoid resistance or evidence of aphids with strong (Nic-R ++ ) resistance in the UK. There should therefore be no control failures when neonicotinoids are applied at rates recommended for aphids. No resistance to pymetrozine, flonicamid, spirotetramat (a tetramic acid derivative) or cyantraniliprole (a diamide). Screening live aphids for their response to different compounds remains very important. Fitness costs associated with insecticide resistance

10 INSECTICIDES NO INSECTICIDES ADVANTAGES DRAWBACKS ADVANTAGES DRAWBACKS

11 Reduced response to aphid alarm pheromone is associated with some forms of insecticide resistance

12 Time to leave! There s nothing to worry about.. Susceptible Resistant

13 The Bad New super-kdr mutation A decrease in the frequency of kdr aphids has occurred despite the continued usage of pyrethroids in the UK an inconsistency that is explained by the discovery that M. persicae carries another, previously unknown target site mutation conferring resistance to pyrethroids. This is a variant of the old super-kdr type, but involves the amino acid methionine changing to leucine instead of threonine at the super-kdr position (i.e. it is M918L instead of M918T). Testing has shown that it has been common in the UK and parts of northern Europe in recent years, hence being called M918Lne (as opposed to M918Lse which is found in southern Europe). The common O and P micro-satellite M. persicae genotypes possess this new target site mutation in the heterozygous form (along with MACE resistance).

14 Myzus persicae field samples containing MACE, kdr and super-kdr aphids % samples containing resistant aphids Year MACE kdr super kdr ne Myzus persicae suction trap catches in 2013 showed a late spring migration and poor autumn migration.

15 English M. persicae suction-trapped resistance genotypes (MACE/kdr) Sus/Sus MACE/Sus Sus/kdr MACE/kdr (404) (338) (382) (481) 3% 3% 85% 86% 11% 10% 1% 1% 0.6% 0.9% 88% 98% 11% 0.9% 0.4% 0.2% English M. persicae suction-trapped resistance genotypes (MACE/super-kdr ne ) 2013 (350) Sus/Sus 3.4% MACE/Sus 2.6% Sus/super-kdr 0.3% MACE/super-kdr 93.7%

16 English M. persicae suction-trapped resistance genotypes (MACE/kdr) Sus/Sus MACE/Sus MACE/super Sus/kdr MACE/kdr (404) (338) (382) (481) 3% 85% 11% 1% 3% 86% 10% 1% 0.6% 0.9% 88% 98% 11% 0.9% 0.4% 0.2% UK Myzus persicae field population O Type P Type > 90% of the UK population

17 Time taken for strong resistance to neonicotinoids to evolve Tobacco whitefly Glasshouse whitefly Colorado potato beetle Brown planthopper Aphids Years Nic-R ++ Myzus persicae in mainland Europe

18 Monitoring for R81T (neonicotinoid R) mutation in Myzus persicae populations in Europe Nic-SS Nic-SR Nic-RR?? LC 50 responses of Myzus persicae clones in imidacloprid topical bioassays (ordered by Resistance Factor) Table 2. LC 50 responses of M. persicae clones in topical bioassays applying imidacloprid (ordered by Resistance Factor) Clone Nic Cat a N b c LC 50 95% CL c Slope d RF e Viability f SS 4106A S a SS 4255A S a SS 926B R b SS T13 R b SS Sel4 R b T25 R b SS T43 R bc SS T52 R c SS 5191A R c SS Sel2 R c SR 5485A R ` 3,460 2,241-6,194 d 1.3 >8, SR SPN R ,528 1,511-20,382 de 1.0 >8, RR 5444B R ,412 6,690-75,695 e 0.9 >30,000 6,000 RR FRC R ,426 7, ,613 e 0.8 >30,000 6, R a Neonicotinoid Resistance Category allocated on basis of topical LC50. b Total number of aphids tested (including untreated controls). c Concentration (ppm) resulting in 50% aphids dead or irreversibly poisoned. d Confidence Limits at 95%; values followed by the same letter do not differ significantly (i.e. they overlap). e Resistance Factor of clone LC50/LC50 for 4106A. f Highest dose (ppm) where viable offspring were produced.

19 Nic-SR and Nic-RR Myzus persicae now being found on adjacent herbaceous hosts to peach (eggplant and pepper) No apparent fitness costs, in the form of reduced alarm pheromone response or vulnerability to parasitoid attack associated with Nic-SR or -RR Myzus persicae

20 Studies of pyrethroid resistance in the grain aphid, Sitobion avenae Sitobion avenae Important pest on wheat, barley (oats) Reduces grain yield Transmits BYDV Previous good control with pyrethroids

21 Lambda-cyhalothrin spray failures reported against grain Sitobion avenae in England in June 2011 Sodium channel mutations implicated in pyrethroid resistance outside V410M L1014F L1014S L1014H S5 M1524I F1538I I II III IV inside S1 S2 S3 S4 S5 S6 S1 S2 S3 S4 C785R E453K S6 S1 S2 S3 S4 S5 S6 S1 S2 S3 S4 S5 S6 L932F A1410V COOH NH2 M918T L925I T929I/V E1553G D1549V Anopheles gambiae Aphis gossypii Bemisia tabaci Blattella germanica Boophilus microplus Ctenocephalides felis Culex pipiens Drosophila melanogaster Helicoverpa armigera Heliothis virescens Hematobia irritans Leptinotarsa decemlineata Musca domestica Myzus persicae Pediculus capitis Plutella xylostella 1 0 resistance mutation 2 0 resistance mutation effects not characterised

22 outside I II L1014F L1014S III M1524I F1538I V410M IV L1014H S5 S1 S2 S3 S4 S5 S6 inside S1 S2 S3 S4 C785R E453K S6 S1 S2 S3 S4 S5 S6 S1 S2 S3 S4 S5 S6 L932F A1410V COOH NH2 M918T L925I T929I/V E1553G D1549V 2011 Sitobion avenae sample contained classic kdr mutation: L1014F Mechanism-specific diagnostics TaqMan PCR

23 Bioassay approach Application Coating Bioassay 5h scoring Response to lambda-cyhalothrin S. avenae Clone LC 50 ng ai/cm 2 Resistance Factor SS Baseline (Suffolk, 2011) 0.08 ( ) a 1 SR (Norfolk, 2011) 3.21 ( ) b 36 SR (Norfolk, 2012) 3.24 ( ) b 39

24 What about Grain aphids in the UK population? Suction trap sites Newcastle Preston Wellesbourne Kirton Broom s Barn Hereford Starcross Rothamsted Writtle Wye

25 kdr-sr and -SS Sitobion avenae in suction trap samples in 2012 kdr (SR) resistant WT (SS) susceptible Suction trap sites Number of aphids tested Frequency of kdr SR Sitobion avenae in three suction traps ( ) % kdr SR aphids Broom s Barn Kirton Rothamsted Suction Trap Sites * *No data for 2009 and 2010 at Rothamsted

26 So far, all Grain aphid kdr-sr aphids have scored as one clone (using microsatellite marker testing). This is a common clone found in Scotland and also found in the first set of English aphid samples tested. Data from Brian Fenton and Gaynor Malloch, James Hutton Institute kdr-sr Grain aphids have also been found in: Ireland and Germany A few samples received from Denmark and the USA (Kentucky) contained only kdr-ss aphids

27 October 2013 Knock-down resistance (kdr) in Grain Aphids This IRAG Guideline provides advice on the control of grain aphid ( Sitobion avenae) populations that may contain individuals with knockdown - resistance (kdr) to pyrethroid insecticides commonly used for aphid control on UK cereals. SP Foster, VL Paul, R Slater, I Denholm, L Field & MS Williamson A mutation (L1014F) in the voltage-gated sodium channel of the Grain aphid, Sitobion avenae, associated with resistance to pyrethroid insecticides. Due to be published in Pest Management Science

28 and The Ugly Neonicotinoid restriction as seed treatments from December 2013 This will mainly affect OSR with growers probably using more pyrethroids and/or pymetrozine. Myzus persicae are currently mostly super-kdr in the UK so they should be poorly controlled by pyrethroids unless there is a big change in the population. Pymetrozine can be applied once in the autumn and provides protection for approximately 2 weeks. Application timing is crucial and HGCA aphid alerts help identify when to spray If problems with virus control (e.g. TuYV) then ensue, some growers MAY even stop growing OSR. This will have negative implications for bee foraging

29 Cabbage Stem Flea Beetle Courtesy Alan Dewar Courtesy Alan Dewar Courtesy Alan Dewar 30 th September, 2013 Ninety per cent of pesticides under threat from EU bee plans Syngenta has warned up to 90% of pesticides currently available to EU farmers could be banned under European Commission plans to widen its approach to protecting bees from agrochemicals.

30 To combat resistance we need as many insecticides with different Modes of Action as we can have! HGCA publications

31 Acknowledgements: AHDB-HGCA AHDB (Horticulture) AHDB (Potato Council) ADAS Bayer CropScience BBSRC Belchim British Beet Research Organisation Certis Chemicals Regulation Directorate Dewar Crop Protection DuPont NuFarm (UK) Ltd Sumitomo/InterFarm Syngenta Special thanks to: Rothamsted Insect Survey Suzanne Clark Diana Cox Ian Denholm Mark Mallott Linda Oliphant Deepa Paliwal Martin Williamson Thank you

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