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Control Failure Likelihood and Spatial Dependence of Insecticide Research Article Received: 19 August 2010 Revised: 9 December 2010 Accepted: 14 December 2010 Published online in Wiley Online Library: 10 March 2011 (wileyonlinelibrary.com) DOI 10.1002/ps.2131 Control failure likelihood and spatial dependence of insecticide resistance in the tomato pinworm, Tuta absoluta Gerson A Silva,a Marcelo C Picanc¸o,a Leandro Bacci,b AndreLuizBCrespo,´ a Jander F Rosadoa and Raul Narciso C Guedesa∗ Abstract BACKGROUND: Insecticide resistance is a likely cause of field control failures of Tuta absoluta, but the subject has been little studied. Therefore, resistance to ten insecticides was surveyed in seven representative field populations of this species. The likelihood of control failures was assessed, as well as weather influence and the spatial dependence of insecticide resistance. RESULTS: No resistance or only low resistance levels were observed for pyrethroids (bifenthrin and permethrin), abamectin, spinosad, Bacillus thuringiensis and the mixture deltamethrin + triazophos (<12.5-fold). In contrast, indoxacarb exhibited moderate levels of resistance (up to 27.5-fold), and chitin synthesis inhibitors exhibited moderate to high levels of resistance (up to 222.3-fold). Evidence of control failures was obtained for bifenthrin, permethrin, diflubenzuron, teflubenzuron, triflumuron and B. thuringiensis. Weather conditions favour resistance to some insecticides, and spatial dependence was observed only for bifenthrin and permethrin. CONCLUSION: Insecticide resistance in field populations of the tomato pinworm prevails for the insecticides nowadays most frequently used against them – the chitin synthesis inhibitors (diflubenzuron, triflumuron and teflubenzuron). Local selection favoured by weather conditions and dispersal seem important for pyrethroid resistance evolution among Brazilian populations of T. absoluta and should be considered in designing pest management programmes. c 2011 Society of Chemical Industry Keywords: insect growth regulators; insecticide resistance distribution; vegetable crops; Brazil; pest control 1INTRODUCTION insecticides were also reported in Chile.11,13 These studies, The tomato pinworm Tuta absoluta (Meyrick) (Lepidoptera: however, do not go beyond the survey of insecticide resistance Gelechiidae) is native to South America, from the region and eventual study of mechanisms of abamectin and cartap circumscribed by Ecuador, the Andes mountain range north of resistance using insecticide synergists.9,10 They neglected the the Chilean border and the Pacific coast.1 It is the main tomato potential influence of weather on insecticide resistance and its insect pest in South America,2,3 and was introduced in Europe spatial distribution, which can potentially allow the recognition of in 2006 through Spain. From Spain it quickly spread throughout main areas prone to problems of insecticide resistance. most of Europe and soon reached Mediterranean Africa, where it Theobjectiveofthepresentstudywastosurveyresistancelevels has caused large tomato crop losses.4,5 of representative populations of the tomato pinworm T. absoluta The tomato pinworm larva compromises tomato productivity from the main tomato-producing regions in Brazil to the main by consuming the leaf mesophyll and damaging the stalk, flowers insecticides currently used and recommended. Furthermore, the and fruits.2,3,6 The consequence of such losses has been extensive likelihood of insecticide control failures in the surveyed insect insecticide field use (and overuse) to minimise the damage populations was assessed, as well as weather influence and caused by the pinworm. However, insecticide applications are the spatial dependence of insecticide resistance in the tomato not always as efficient as expected for controlling this insect pinworm. pest species.7,8 The evolution of insecticide resistance in South American populations of the pinworm is one reason for the low ∗ insecticide control efficacy.8–12 Correspondence to: Raul Narciso C Guedes, Departamento de Biologia Animal, Universidade Federal de Vic¸osa, Vic¸osa, MG 36571-000, Brazil. There are only a few studies focusing on the detection of E-mail: [email protected] insecticide resistance among populations of T.absoluta. Resistance to abamectin, cartap, methamidophos and permethrin were a Departamento de Biologia Animal, Universidade Federal de Vic¸osa, Vic¸osa,MG, reported earlier in Brazil,8–10 while resistance to abamectin, Brazil deltamethrin and methamidophos were also detected later in b Departamento de Engenharia Agronomica,ˆ Universidade Federal de Sergipe, 913 Argentina.12 Resistance to organophosphates and pyrethroid Aracaju, SE, Brazil Pest Manag Sci 2011; 67: 913–920 www.soci.org c 2011 Society of Chemical Industry www.soci.org GA Silva et al. Figure 1. Sampling sites of the field populations of the tomato pinworm Tuta absoluta. 2MATERIALANDMETHODS bioassays to prevent expression of insecticide tolerance due to 2.1 Insect populations the distinct environmental conditions at the sampling sites (i.e. The tomato pinworm populations were collected in commercial without a genetic basis). tomatofieldsfromsevendifferentsitesbelongingtothreeBrazilian biomes – semi-arid, Brazilian savannah and Atlantic forest (Fig. 1). 2.2 Insecticides These biomes represent the Brazilian macroregions of tomato Ten insecticides were used in the present study. Six insecticides cultivation. The laboratory colonies were established from at were neurotoxic (concentration of active ingredient indicated): least 200 field-collected individuals from each sampling site and abamectin 18 g L−1 EC (emulsifiable concentrate) (Syngenta, Sao˜ maintained in large numbers to minimise loss of genetic variability. Paulo,Brazil),bifenthrin100 g L−1 EC(FMCBrasil,Campinas,Brazil), ◦ The populations were reared in a laboratory at 25 ± 0.5 C, with a deltamethrin 10 g L−1 EC + triazophos 350 g L−1 EC (Bayer SA, relative air humidity of 75 ± 5% and a photophase of 12 h. Each Sao˜ Paulo, Brazil), indoxacarb 300 g L−1 WG (water-dispersible population was reared in four wooden cages (40 × 40 × 40 cm) granules) (Du Pont, Barueri, Brazil), permethrin 500 g L−1 EC (Syn- covered with organza: one for oviposition, one with first- and genta, Sao˜ Paulo, Brazil) and spinosad 480 g L−1 SC (suspendable second-instar larvae, one with third- and fourth-instar larvae concentrate) (Dow AgroSciences, Sao˜ Paulo, Brazil). Three were and one for pupation and adult emergence. The larvae were insect growth regulators inhibiting chitin synthesis: difluben- fed with tomato leaves from plants of the Santa Clara cultivar, zuron 250 g L−1 WP (wettable powder) (Crompton Ltd, Rio Claro, cultivated under greenhouse conditions without any insecticide Brazil), teflubenzuron 150 g L−1 SC (BASF, Guaratingueta,´ Brazil) 14 −1 914 application. Only insects reared for at least one generation in and triflumuron 250 g L WP (Bayer, Sao˜ Paulo, Brazil). The re- the laboratory (usually between two and four) were used in the maining insecticide consisted of spores of the bacterium Bacillus wileyonlinelibrary.com/journal/ps c 2011 Society of Chemical Industry Pest Manag Sci 2011; 67: 913–920 Control failures and spatial distribution of insecticide-resistant Tuta absoluta www.soci.org thuringiensis var. kurstaki strain HD-1 (33.60 g L−1 SC; 17 600 iu g−1; caused by the recommended label rate of each insecticide (mid- Abbott Laboratories/FMC Química Brasil Ltda, Uberada, Brazil). concentration from the registered range) and the lower threshold These products represent the main groups of insecticides rec- at LC80 estimated for each compound. The 80% mortality was ommended for managing the tomato pinworm in Brazil, except used as reference because this is the minimum level of efficacy for the insecticide mixture deltamethrin + triazophos, which was required for registration of an insecticidal compound in Brazil being tested against this insect.15,16 by the Ministry of Agriculture.21 Therefore, this is the minimum expected level of efficacy without control failure due to insecticide 2.3 Insecticide resistance bioassays resistance. The insecticide mortality caused by the label rate Twodistinctstrategiesforconcentration–responsebioassayswere was considered to be significantly lower than 80% when the carried out, one for neurotoxic insecticides and the other for recommended rate was lower than the lower threshold of the chitin synthesis inhibitors and B. thuringiensis. This was necessary 95% fiducial interval of the LC80 of the insecticide for the tested because neurotoxic insecticides exhibit quick action and affect all insect population. The registered and recommended label rates of the respective active ingredients in Brazil were: 0.18 mg mL−1 for larval instars of T. absoluta. In contrast, chitin synthesis inhibitors −1 −1 and B. thuringiensis exhibit stronger activity against the first- and abamectin, 0.072 mg mL for B. thuringiensis,0.05mgmL for bifenthrin, 0.032 mg mL−1 for deltamethrin + triazophos second-instar larvae but exhibit slower insecticidal activity than −1 neurotoxic insecticides.17,18 (preliminary recommendation), 0.4 mg mL for diflubenzuron, 0.024 mg mL−1 for indoxacarb, 0.5 mg mL−1 for permethrin, 0.06 mg mL−1 for spinosad, 0.0375 mg mL−1 for teflubenzuron 2.3.1 Neurotoxic insecticides and 0.15 mg mL−1 for triflumuron. Tomato leaflets were immersed for 5 s in insecticide solution and shade dried for 2 h. The leaves were subsequently placed in petri 2.5 Relationship between weather conditions dishes (9 cm diameter × 2 cm height) with inner walls coated with and insecticide
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