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Captures of MFO-resistant Cydia pomonella adults as affected by lure, crop management system and flight

Published online by Cambridge University Press:  26 October 2015

D. Bosch ,
M.A. Rodríguez  and
J. Avilla
D. Bosch*
Affiliation:
Institut Recerca i Tecnologia Agroalimentària (IRTA), Av. Alcalde Rovira Roure, 191, 25198 Lleida, Spain
M.A. Rodríguez
Affiliation:
Universidad de Concepción, Castilla 160-C, Concepción, Chile
J. Avilla
Affiliation:
Department of Crop and Forest Sciences, Agrotecnio, University of Lleida, Rovira Roure, 191, 25198 Lleida, Spain
*
* Author for correspondence Phone: +34 973 702633 Fax: +34 973 238301 E-mail: dolors.bosch@irta.cat
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Abstract

The main resistance mechanism of codling moth (Cydia pomonella) in the tree fruit area of Lleida (NE Spain) is multifunction oxidases (MFO). We studied the frequency of MFO-resistant adults captured by different lures, with and without pear ester, and flights in orchards under different crop management systems. The factor year affected codling moth MFO-resistance level, particularly in the untreated orchards, highlighting the great influence of codling moth migration on the spread of resistance in field populations. Chemical treatments and adult flight were also very important but mating disruption technique showed no influence. The second adult flight showed the highest frequency, followed by the first flight and the third flight. In untreated orchards, there were no significant differences in the frequency of MFO-resistant individuals attracted by Combo and BioLure. Red septa lures baited with pear ester (DA) captured sufficient insects only in the first generation of 2010, obtaining a significantly lower proportion of MFO-resistant adults than Combo and BioLure. In the chemically treated orchards, in 2009 BioLure caught a significantly lower proportion of MFO-resistant adults than Combo during the first and third flight, and also than DA during the first flight. No significant differences were found between the lures or flights in 2010. These results cannot support the idea of a higher attractiveness of the pear ester for MFO-resistant adults in the field but do suggest a high influence of the response to the attractant depending on the management of the orchard, particularly with regard to the use of chemical insecticides.

Keywords

Cydia pomonellamixed function oxidasesmonitoringpear estercodlemonecrop managementadult flight

Information

Type
Research Papers
Information
Bulletin of Entomological Research , Volume 106 , Issue 1 , February 2016 , pp. 54 - 62
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Copyright
Copyright © Cambridge University Press 2015 

Introduction

The codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae), the main pest for apple, pear and walnut crops worldwide, has usually been controlled with insecticides. In Spain, organophosphates have been widely used for more than 30 years, but since the late 1990s, control of the pest through the use of insecticides has become more difficult due to the development of resistance (Bosch et al., Reference Bosch, Voltes, Riedl, Torà, Sarasúa and Avilla1999). At present, the control strategy for codling moth relies on the combined use of chemicals and mating disruption, especially in problematic orchards. Mating disruption has been applied extensively in the Ebro Valley since approximately 2007 and was applied in 2009 on more than 10,000 ha, of which, according to the distributors, 5450 ha were in Lleida, accounting for 68% of the production area. These figures were approximately the same in 2011 (Agriculture Department, personal communication). Pest population monitoring is a crucial component of any integrated pest management program. To monitor the phenology of codling moth in the field, the use of traps baited with 1 mg (in chemical orchards) or 10 mg (in mating disruption orchards) of (E,E)-8,10-dodecadien-1-ol (codlemone) has been extensive. However, in some cases, the lack of catches in the traps was unreliable (false negative), and particularly in mating disruption orchards it is necessary to check fruits to discard fruit infestations and not rely only on the trap catches. In Light et al. (Reference Light, Knight, Henrick, Rajapaska, Lingren, Dickens, Reynolds, Buttery, Merrill, Roitman and Campbell2001), described a pear-derived kairomone (pear ester), ethyl (2E, 4Z)-2,4-decadienoate, which attracted C. pomonella male and female adults. Recently, the use of a synthetic lure baited with a combination of 3 mg of this kairomone and 3 mg of codlemone, CM-DA Combo®, has been quickly replacing the use of 10 mg codlemone lures in mating disruption orchards because it catches a higher number of moths (Torà et al., Reference Torà, Dolset, Almacelles, Garcia de Otazo, Saló, Avilla, Bosch, Llombart, Batllori and Vilajeliu2009; Joshi et al., Reference Joshi, Hull, Rajotte, Krawczyk and Bohnenblust2011).

C. pomonella has developed resistance to a wide range of insecticides in almost all productive apple areas in the world (Sauphanor et al., Reference Sauphanor, Brosse, Monier and Bouvier1998, Reference Sauphanor, Brosse, Bouvier, Speich, Micoud and Martinet2000; Fuentes-Contreras et al., Reference Fuentes-Contreras, Reyes, Barros and Sauphanor2007; Ioratti et al., Reference Ioratti, Tasin, Charmillot, Reyes and Sauphanor2007; Reuveny & Cohen, Reference Reuveny and Cohen2004; Stará & Kocourek, Reference Stará and Kocourek2007; Soleño et al., Reference Soleño, Anguiano, de D'Angelo, Cichon, Fernandez and Montagna2008, Reference Soleño, Anguiano, Cichon, Garrido and Montagna2012; Knight, Reference Knight2010; Rodríguez et al., Reference Rodríguez, Bosch, Sauphanor and Avilla2010, Reference Rodríguez, Bosch and Avilla2012). A high frequency of resistant codling moth individuals has been detected in most of the problematic orchards in the tree fruit area of Lleida (NE Spain) (Rodríguez et al., Reference Rodríguez, Bosch and Avilla2011). Insect resistance may be due to the detoxification of the insecticides by three enzymatic complexes (mixed function oxidases (MFO), glutation transferases (GST) and esterases (EST)), or to structural changes (mutations) in the insecticide target protein that make the protein less sensitive to the insecticide (the acetylcholinesterase (AChE) mutation in the case of organophosphates and carbamates, described by Cassanelli et al., (Reference Cassanelli, Reyes, Rault, Manicardi and Sauphanor2006), and the knockdown resistance (kdr) mutation in the voltage-gated sodium channel in the case of pyrethroids, described by Brun-Barale et al., (Reference Brun-Barale, Bouvier, Pauron, Bergé and Sauphanor2005)). An increased production of MFO enzymes in adults and larvae was involved in the insecticide detoxification in all the field populations of the area tested (Rodríguez et al., Reference Rodríguez, Bosch, Sauphanor and Avilla2010, Reference Rodríguez, Bosch and Avilla2012). GST were also detected, and EST were detected only in larvae (Rodríguez et al., Reference Rodríguez, Bosch and Avilla2011). These results cannot be generalized to all the codling moth populations in the area, but confirm that it is a real and increasing problem that may interfere with the management of the orchards.

Negative pleiotropic effects of insecticide resistance in codling moth, such as different development rates (Boivin et al., Reference Boivin, Chabert-d'Hières, Bouvier, Beslay and Sauphanor2001, Reference Boivin, Bouvier, Chadoeuf, Beslay and Sauphanor2003a ) and critical photoperiod for inducing diapause (Boivin et al., Reference Boivin, Bouvier, Chadoeuf, Beslay and Sauphanor2005), may affect the proportion of resistant insects present in the field during the different generations. These alterations have also been reported in other Lepidoptera species such as Plutella xylostella (L.) (Lepidoptera: Plutellidae) and Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) (Han et al., Reference Han, Zhang, Shen, Liu, Ren and Gao2012; Ribeiro et al., Reference Ribeiro, Wanderley-Teixeira, Ferreira, Teixeira and Siqueira2014). Negative effects on sexual communication, such as low pheromone production by females and lower ability of males to detect the pheromone source, have also been detected (Poullot et al., Reference Poullot, Beslay, Bouvier and Sauphanor2001; Trimble et al., Reference Trimble, El-Sayed and Pree2004). Nevertheless, Frérot et al. (Reference Frérot, Beslay, Malosse, Renou, Coupard, Bouvier and Sauphanor1999) and Poullot et al. (Reference Poullot, Beslay, Bouvier and Sauphanor2001) found that the level of attraction of the codling moth sex pheromone in the traps for released susceptible and resistant males in the orchards and in a wind tunnel was the same. Sauphanor et al. (Reference Sauphanor, Franck, Lasnier, Toubon, Beslay, Boivin, Bouvier and Renou2007) demonstrated a higher attraction of MFO-resistant male moths in pure kairomone-baited traps in apple orchards.

The aim of this work was to determine the frequency of MFO-resistant C. pomonella adults captured by different lures, with and without kairomone, and during the different flights in orchards under different crop management systems. The general state of the resistance in the area with regard to MFO activity is also noted.

Material and methods

Insects and attractants

Field codling moth catches were obtained in 20 and 25 field orchards in 2009 and 2010, respectively. Five orchards were classified as chemically untreated (UN, abandoned or organic orchards), eight as chemically treated (CH) and 32 as pheromone mating disruption orchards supplemented with chemical insecticides (MD + CH). The plots were distributed throughout the production area of Lleida (Catalonia, NE Spain), with a maximum distance of 60 km between them. The Spanish susceptible strain (S_Spain) was used as a reference to determine the level above which an insect was recorded as resistant. This threshold was the highest 7-ethoxycoumarin-O-deethylation (ECOD) activity value corresponding to 90% of the S_Spain–analyzed individuals. S_Spain was collected from an abandoned apple orchard in Lleida in 1992, and it has been reared since then using a semi-artificial dehydrated apple diet at the Sustainable Plant Protection Laboratory of the UdL-IRTA Centre for R&D (University of Lleida, Institute for Food and Agricultural Research and Technology, Lleida, Spain).

The three codling moth attractants compared were BioLure™ CM 10X (Suterra) (named BioLure, loaded with 10 mg of (E, E)-8, 10-dodecadien-1-ol [codlemone]), Pherocon CM-DA Combo™ (named Combo, a mixture of 3.0 mg of codlemone and 3.0 mg of ethyl (2E, 4Z)-2,4- decadienoate) and red septa lures baited with pear ester (named DA, 3.0 mg of pear ester). The traps were revised once a week and well maintained and the attractants were changed approximately every 8 weeks. The maximum period of time in which adults were analyzed was 4 weeks for each generation to avoid catching and analyzing adults from different generations in the same trap. The moment to begin the analysis was decided on the basis of the phenological model used in the area and was approximately 1 week after the prediction of the beginning of each adult flight. During these periods the adult field catches were taken to the laboratory twice a week in order to obtain as many live adults as possible.

Enzymatic activity

The adult MFO activity was determined with an in vivo protocol (Rodríguez et al., Reference Rodríguez, Bosch and Avilla2012) using ECOD in a black microplate of 96 wells. The dissected abdomens of the adults were placed individually in a well containing 100 µl of phosphate buffer (50 mm, pH 7.2) and 7-ethoxycoumarin (7OH) (0.4 mm). After 4 h of incubation at 30°C, the reaction was stopped by adding 100 µl of glycine buffer (pH 10.4, 10−4 m) with ethanol (v/v). Before the incubation a minimum of 10% of the wells of each microplate were used as controls and received the glycine buffer to stop the reaction. The ECOD activity was measured by fluorescence with a 380 nm excitation filter and a 465 nm emission filters and was expressed as pg of 7OH insect−1 min−1.

Data analysis

The differences between the absolute frequencies of resistant individuals according to the different attractants, adult flights, management systems and years were compared using a Pearson chi-square (χ2) test. Moths were classified as resistant if their MFO enzyme activity exceeded the highest activity value corresponding to 90% of S_Spain individuals (Reyes et al., Reference Reyes, Frank, Charmillot, Ioriatti, Olivares, Pasqualini and Sauphanor2007).

Results

The three periods of codling moth trap catches in 2009 were 6–26 May, 30 June to 30 Julyand 18 August to 1 September. It was considered that the adults caught in these periods belonged to the first, second and third flights, respectively. In 2010, the three periods were 5–31 May, 13 July–16 August and 23 August–20 September (fig. 1). BioLure- and Combo-baited traps tracked in a similar way the moth flights during the two seasons in mating disruption and non-mating disruption orchards. In 2009, the number of catches was in general higher than in 2010 and the three flight peaks were also more evident in the flight curve. The flight curve obtained with DA is not represented in fig. 1 due to the low number of captures. The maximum number of catches per trap and week was recorded both years in non-mating disruption orchards, in Bio traps in 2009 and Combo traps in 2010, resulting in 38.3 and 9.5 moths, respectively. The second flight always showed a lower number of catches than the first, and the third flight was always very short, especially in 2009.

Fig. 1.

Mean weekly codling moth adults caught in mating disruption (MD) and non-MD orchards using BioLureTM CM 10X and Pherocon CM-DA ComboTM lures and period of time (rectangle area) when the MFO activity was measured in each flight (gray area). Number of traps =30 (2009) and 58 (2010). Solid bars show the beginning of each generation.

The percentages of MFO-resistant insects obtained in 2009 and 2010 in the orchards with different management systems using the attractants BioLure and Combo are shown in table 1. The value of the MFO threshold obtained using the S-Spain population was 23.92 pg 7OH adult−1 min−1. In both years and with both attractants, the UN orchards obtained a significantly lower proportion of resistant insects than the CH and the MD + CH orchards, and the CH orchards obtained the same proportion of resistant insects as the CH + MD orchards (BioLure 2009, UN–CH, dF = 1; χ2 = 7.24 and P = 0.007; UN–MD + CH, dF = 1; χ2 = 10.00 and P = 0.002; CH–MD + CH, dF = 1; χ2 = 0.09 and P = 0.762; BioLure 2010, UN–CH, dF = 1; χ2 = 65.57 and P = 5.60 × 10−16; UN–MD + CH, dF = 1; χ2 = 121.96 and P = 2.35 × 10−28; CH–MD + CH, dF = 1; χ2 = 0.14 and P = 0.705; Combo 2009, UN–CH, dF = 1; χ2 = 33.39 and P = 7.5 × 10−9; UN–MD + CH, dF = 1; χ2 = 28.55 and P = 9.15 × 10−8; CH–MD + CH, dF = 1; χ2 = 3.68 and P = 0.055; Combo 2010: UN–CH, dF = 1; χ2 = 84.21 and P = 4.46 × 10−20; UN–MD + CH, dF = 1; χ2 = 103.80 and P = 2.23 × 10−24; CH–MD + CH, dF = 1; χ2 = 1.16 and P = 0.282). It can also be seen in table 1 that there was always numerically higher number of MFO-resistant moths in 2009 than in 2010. These differences were significant in the UN orchards for BioLure attractant and in the chemically treated orchards (CH and CH + MD) for Combo attractant (BioLure, UN orchards 2009–2010, dF = 1; χ2 = 9.50 and P = 0.002; CH orchards 2009–2010, dF = 1; χ2 = 0.04 and P = 0.839; MD + CH orchards 2009–2010, dF = 1; χ2 = 1.99 and P = 0.158; Combo, UN orchards 2009–2010, dF = 1; χ2 = 2.04 and P = 0.153; CH orchards 2009–2010, dF = 1; χ2 = 9.37 and P = 0.002; MD + CH orchards 2009–2010, dF = 1; χ2 = 18.84 and P = 1.41 × 10−5).

Table 1.

Percentage of MFO-resistant codling moth adults caught in 2009 and 2010 in orchards with different management systems in the area of Lleida in traps baited with BioLure™ CM 10X and Pherocon CM-DA Combo™.

UN, untreated orchards; CH, chemically treated orchards; MD + CH, mating disruption orchards supported by chemical treatments.

For each attractant, numbers followed by the same lower case letter on the same column are not significantly different (P < 0.05). For each attractant and management system, numbers followed by the same upper case letter on the same line are not significantly different (P < 0.05).

The frequencies of resistant individuals caught during the three adult flights in the orchards with different management systems during the 2 years of the assay are shown in table 2. There were no significant differences between the frequency of MFO-resistant adults captured in the different flights in the UN orchards, in spite of the higher proportion of resistant adults in the second flight in both years (2009, 1st–2nd flight, dF = 1; χ2 = 1.30 and P = 0.255; 2010, 1st–2nd flight, dF = 1; χ2 = 2.86 and P = 0.091; 1st–3rd flight, dF = 1; χ2 = 0.11 and P = 0.745; 2nd–3rd flight, dF = 1; χ2 = 3.32 and P = 0.069). In the CH and CH + MD orchards, the second adult flight was the one with the highest proportion of MFO-resistant adults and the differences from the first flight were always significant. The third flight was the one with the lowest frequencies of MFO-resistant adults in 2009, but in 2010 it was the first flight which had the lowest frequency (2009, CH orchards, 1st–2nd flight, dF = 1; χ2 = 9.99 and P = 0.002; 1st–3rd flight, dF = 1; χ2 = 6.35 and P = 0.012; 2nd–3rd flight, dF = 1; χ2 = 24.83 and P = 6.27 × 10−7; 2009, MD + CH orchards: 1st–2nd flight, dF = 1; χ2 = 5.85 and P = 0.016; 1st–3rd flight, dF = 1; χ2 = 4.99 and P = 0.025; 2nd–3rd flight, dF = 1; χ2 = 13.22 and P = 2.77 × 10−4; 2010, CH orchards, 1st–2nd flight, dF = 1; χ2 = 4.04 and P = 0.045; 1st–3rd flight, dF = 1; χ2 = 1.18 and P = 0.277; 2nd–3rd flight, dF = 1; χ2 = 0.01 and P = 0.922; 2010, MD + CH orchards, 1st–2nd flight, dF = 1; χ2 = 8.78 and P = 0.003; 1st–3rd flight, dF = 1; χ2 = 5.03 × 10−4 and P = 0.982; 2nd–3rd flight, dF = 1; χ2 = 1.85 and P = 0.174).

Table 2.

Percentage of MFO-resistant codling moth adults caught in the three flights of the years 2009 and 2010 in orchards with different management systems in the area of Lleida.

UN, untreated orchards; CH, chemically treated orchards; MD + CH, mating disruption orchards supported by chemical treatments.

For each year and management system, numbers followed by the same lower case letter on the same line are not significantly different (P < 0.05).

As the year, the adult flight and the application of treatments in the orchards influenced the amount of MFO-resistant codling moths in the field, all these factors were taken into account to study the influence of the lure in the frequency of MFO-resistant individuals captured in the traps (figs 2 and 3). From this moment the CH and CH + MD orchards were considered as chemically treated orchards.

Fig. 2.

Percentage of MFO-resistant codling moth adults in the three field flights captured by delta traps lured with Pherocon CM-DA ComboTM, BioLureTM CM 10X and the pear ester DA (3.0 mg of pear ester) in two untreated and 18 treated orchards of the production area of Lleida during the year 2009. Number within the brackets represents the number of insects processed.

Fig. 3.

Percentage of MFO-resistant codling moth adults in the three field flights captured by delta traps lured with Pherocon CM-DA ComboTM, BioLureTM CM 10X and the pear ester DA (3.0 mg of pear ester) in untreated (three orchards) and treated orchards (22 orchards) of the production area of Lleida during the year 2010. Numbers within the brackets represent the number of insects processed.

There were no significant differences in the frequency of MFO-resistant individuals attracted by Combo and BioLure in the UN orchards in either of the 2 years. The attractant DA captured enough insects to compare with the other two attractants only in the first flight of 2010, obtaining a significant lower proportion of MFO-resistant adults than Combo and BioLure (2009, 1st flight, Combo–BioLure, dF = 1; χ2 = 1.39 and P = 0.238; 2nd flight, Combo–BioLure, dF = 1; χ2 = 0.89 and P = 0.345; 2010, 1st flight, Combo–BioLure, dF = 1; χ2 = 0.08 and P = 0.784; Combo–DA, dF = 1; χ2 = 6.83 and P = 0.009; BioLure–DA, dF = 1; χ2 = 6.24 and P = 0.012; 2nd flight, Combo–BioLure, dF = 1; χ2 = 0.42 and P = 0.518; 3rd flight, Combo–BioLure, dF = 1; χ2 = 0.38 and P = 0.540). In the 2009, chemically treated orchards BioLure caught a significantly lower proportion of MFO-resistant adults than Combo during the first and third flights and also than DA during the first flight. There were no significant differences between the frequency of MFO-resistant insects attracted by the different lures during the three flights in 2010 (2009, 1st flight, Combo–BioLure, dF = 1; χ2 = 4.27 and P = 0.039; Combo–DA, dF = 1; χ2 = 0.53 and P = 0.466; BioLure–DA, dF = 1; χ2 = 3.90 and P = 0.048; 2nd flight, Combo–BioLure, dF = 1; χ2 = 0.49 and P = 0.482; Combo–DA, dF = 1; χ2 = 0.16 and P = 0.688; BioLure–DA, dF = 1; χ2 = 0.003 and P = 0.956; 3rd flight, Combo–BioLure, dF = 1; χ2 = 3.96 and P = 0.047; 2010, 1st flight, Combo–BioLure, dF = 1; χ2 = 0.29 and P = 0.593; Combo–DA, dF = 1; χ2 = 0.05 and P = 0.831; BioLure–DA, dF = 1; χ2 = 0.32 and P = 0.572; 2nd flight, Combo–BioLure, dF = 1; χ2 = 0.21 and P = 0.650; Combo–DA, dF = 1; χ2 = 2.55 and P = 0.110; BioLure–DA, dF = 1; χ2 = 2.06 and P = 0.152; 3rd flight, Combo–BioLure, dF = 1; χ2 = 0.02 and P = 0.883).

Discussion

The MFO-resistance level of codling moth in the field was affected by the year. In general, the frequency of MFO-resistant adults was higher in 2009 than in 2010. A higher number of catches obtained during the year usually led to a higher number of chemical treatments to control the pest and consequently a higher selection of insecticide-resistant individuals. The UN orchards, in this case abandoned and organic orchards, did not use insecticides to control codling moth and the organic orchards based their strategy on mating disruption and carpovirusine treatments. The frequency of MFO-resistant codling moth adults was higher in 2009 and lower in 2010 in the UN orchards. The lower number of captures obtained in 2009 may influence this result, but this result may also point out the great influence that can have the codling moth migration in the spread of resistance in field populations. Several dispersal behavior studies using mark–release–recapture and immunomarking methodologies found that the main proportion of adults dispersed within 60–80 m (Keil et al., Reference Keil, Gu and Dorn2001; Margaritopoulos et al., Reference Margaritopoulos, Voudouris, Olivares, Sauphanor, Mamuris, Tsitsipis and Franck2012), although a small proportion (7.4–20.0%) was able to fly up to several kilometers as an adaptive trait, in order to survive in case of habitat deterioration (Schumacher et al., Reference Schumacher, Weyeneth, Weber and Dorn1997a , Reference Schumacher, Weber, Hagger and Dorn b ; Keil et al., Reference Keil, Gu and Dorn2001). This capacity of dispersion may be responsible for the fluctuations in the presence of resistant adults in the untreated orchards which, in our area, were surrounded by treated orchards.

Presence or absence of chemical treatments in the orchards is the main factor affecting the frequency of MFO-resistant adults. No difference was found between orchards using codling moth mating disruption and those not using it. Mating disruption used without the support of chemical treatments is not sufficiently effective in the area of Lleida to control the pest because of an important constraint of this technique: the need for low population levels (Moffit & Westigard, Reference Moffit and Westigard1984; Vickers & Rothschild, Reference Vickers, Rothschild, van der Geest and Evenhuis1991). Therefore, the use of insecticides combined with mating disruption did not in general lead to a significant reduction in resistance selection.

The phenology of codling moth in the field depends on major abiotic factors such as temperature and day length (Shel'Deshova, Reference Shel'Deshova1967; Riedl & Croft, Reference Riedl and Croft1978; Steinberg et al., Reference Steinberg, Podoler and Applebaum1992) and biotic factors such as food availability (Brown et al., Reference Brown, Berryman and Bogyo1979; Riedl, Reference Riedl, Brown and Hodek1983). However, the application of insecticides may condition its phenology and cause behavioral and/or physiological damage to insects besides death (Buckingham et al., Reference Buckingham, Biggin, Sattelle, Brown and Sattelle2005; Davies et al., Reference Davies, Field, Usherwood and Williamson2007; Casida, Reference Casida2009; Tan et al., Reference Tan, Chen, Dong, Liu, Wang and Nieh2014). The different moth adult flights showed a significantly different proportion of MFO-resistant adults in chemically treated orchards (CH and MD + CH). The second adult flight had the highest frequency of resistant individuals. These adults came from the surviving neonate larvae affected by the chemical treatments applied in the orchards during the entire first adult flight. The first flight in the area of the assay lasted approximately 9 weeks in 2009 and 11 weeks in 2010, while the second and third flights lasted approximately 6–7 weeks and 4–5 weeks, respectively. The longer duration of the first flight usually means, in case of a medium or high population in the orchard, that a higher amount of insecticide treatments may be applied. The frequency of MFO-resistant first adult flight depends on the frequency of the second- and third-generation diapausing larvae of the previous year, and on their proportion, which in turn depends on the annual variation in climate conditions. Boivin et al. (Reference Boivin, Bouvier, Beslay and Sauphanor2004) stated that if the third generation in the field was not successfully completed, due to a sudden shorter summer or harvest, the second-generation diapausing cohorts were the only source for the genetic pool of the next spring generation. Also, in winter negative pleiotropic effects on the codling moth diapausing larvae associated with enhanced MFO levels may be expected (Boivin et al., Reference Boivin, Chabert-d'Hières, Bouvier, Beslay and Sauphanor2001). Deleterious effects in MFO-resistant pupae during diapause were also proved in Helicoverpa armigera (Hübner) (Daly, Reference Daly1993). The third adult flight showed the lowest frequency of MFO-resistant adults. Homozygous MFO-resistant individuals have slower developmental rates and earlier diapause timing than susceptible homozygotes and heterozygotes (Boivin et al., Reference Boivin, Bouvier, Beslay and Sauphanor2003b , Reference Boivin, Bouvier, Beslay and Sauphanor2004). We may therefore assume that the third flight was mainly formed by these more susceptible individuals that were able to produce an additional generation. Data from 2010 may also support this conclusion. The proportion of MFO-resistant individuals in 2010 was lower than in 2009, therefore a lower number of homozygous individuals can be expected in the field justifying the lack of significant differences against the three adult flights.

In 2009, treated orchards, BioLure was less attractive than the other lures containing pear ester during the first and the third generation, but these results were not confirmed in 2010, when all the attractants captured the same frequency of MFO-resistant adults. Conversely, in UN orchards BioLure always caught the same frequency of MFO-resistant individuals as Combo, but in 2010 in first flight – the only flight with sufficient captures – DA caught the lowest frequency of resistant insects. Sauphanor et al. (Reference Sauphanor, Franck, Lasnier, Toubon, Beslay, Boivin, Bouvier and Renou2007) found significantly higher mean MFO activity in first flight male adults captured in field traps baited with 40 mg of pear ester than in those captured in traps baited with 10 mg of codlemone. The differences remained in the chemical and organic orchards in both years. However, some differences in the tests may have influenced the results. Sauphanor et al. (Reference Sauphanor, Franck, Lasnier, Toubon, Beslay, Boivin, Bouvier and Renou2007) used the mean pg of 7OH formed per adult and minute to compare the level of resistance of the different orchard populations, whereas we considered that some high values in a few insects may significantly modify the average and preferred to use the frequency of resistant individuals as an indicator of the level of resistance in the orchards. Furthermore, in our study previous results led us to include females in the analysis. Rodríguez et al. (Reference Rodríguez, Bosch, Sauphanor and Avilla2010), in field adults from different orchards in the same production area, found no clear tendency in the enzymatic activity between sexes. The differences appeared at random and were due to higher values for males or for females depending on the orchards. Therefore, due to the low number of captures traditionally obtained with the pear ester alone in our area (Bosch & Avilla, Reference Bosch and Avilla2005), we decided to include the females to increase the number of captured adults analyzed in the DA attractant.

The opposite tendency in the attraction of MFO-resistant adults of pear ester in treated and untreated orchards may be influenced by the sublethal effect of insecticides. A list of identified effects of insecticide sublethal doses on the olfactory system of agricultural insect pests can be found in Tricoire-Leignel et al. (Reference Tricoire-Leignel, Thany, Gadenne and Anton2012). Field treatments with the ecdysteroid agonists tebufenozide and methoxyfenozide decrease male responses to pheromone in the tortricid moths Choristoneura fumiferana, C. rosaceana, Argyrotaenia velutinana, C. pomonella and Grapholita molesta (Hoelscher & Barrett, Reference Hoelscher and Barrett2003; Dallaire et al., Reference Dallaire, Labrecque, Marcotte, Bauce and Delisle2004; Barrett, Reference Barrett2008). Barrett (Reference Barrett2010) found that methoxyfenozide also disrupted responses of codling moth males to pear ester. Treatments with the organophosphate malathion decrease the ability of corn borer Ostrinia furnacalis males to respond to the female pheromone (Zhou et al., Reference Zhou, Du and Huang2005) and some pyrethroids disrupt the male attraction to the sex pheromone in the pink bollworm, Pectinophora gossypiella, the corn borer O. furnacalis and the noctuid Trichoplusia ni (Haynes & Baker, Reference Haynes and Baker1985; Haynes et al., Reference Haynes, Li and Baker1986; Moore, Reference Moore1988; Clark & Haynes, Reference Clark and Haynes1992; Wei & Du, Reference Wei and Du2004). In addition, pesticides could affect in a different way the chemical communication of susceptible and resistant insects. The alteration of sexual communication, a fitness component, imposed by insecticide resistance in some moth species is expected to contribute to the decline of resistance in the absence of insecticide (Delisle & Vincent, Reference Delisle and Vincent2002). Sauphanor et al. (Reference Sauphanor, Franck, Lasnier, Toubon, Beslay, Boivin, Bouvier and Renou2007) found that pear ester produced an enhanced or altered response in wind tunnel in codling moth adults with MFO and kdr resistance mechanisms. However, this response of kdr-resistant genotipes was not confirmed in the field. The enzymatic system mainly involved in insecticide detoxification in Spanish codling moth field populations, monooxygenases (Rodríguez et al., Reference Rodríguez, Bosch and Avilla2012), is also involved in the recognition of the host-plant (Feyresen, Reference Feyresen1999). Trimble et al. (Reference Trimble, El-Sayed and Pree2004) found that the proportion of azinphos-methyl-resistant males of obliquebanded leafrollers (C. rosaceana (Harris)) that located a synthetic pheromone source in the orchard was 32% lower than the proportion of susceptible males, while in the flight tunnel a similar proportion of susceptible and resistant males located the source. According to Sauphanor et al. (Reference Sauphanor, Franck, Lasnier, Toubon, Beslay, Boivin, Bouvier and Renou2007), the sensory or behavioral response to a semiochemical compound is more likely to be altered by a mutation affecting the nervous system than by a metabolic resistance.

Summarizing, in the field populations of the study area a general enhanced enzymatic MFO activity in all the chemically treated orchards was demonstrated. The frequency of MFO-resistant codling moth adults was more stable in these orchards than in the untreated orchards that showed a higher variability depending on the general frequency of MFO resistance in the year. These results proved the importance of dispersion of resistant adults in a neighboring production area. The role of the chemically untreated orchards as a reservoir of insecticide susceptible individuals must to be demonstrated. Our results cannot support the idea of a higher attractiveness of the pear ester for MFO-resistant adults in the field and point to a different response depending on the management of the orchards. In addition, the target mutations in sodium channel gene (kdr) and AChE1 proteins (AChE), respectively responsible for pyrethroid and organophosphate resistance, have been detected extensively in the Ebro Valley production area (Bosch et al., Reference Bosch, Avilla and Rodríguez2014). Further research is needed to clarify the possible incidence of a higher proportion of individuals in the field with the mutations (kdr and AChE) in response to different semiochemical compounds.

Acknowledgements

The authors would like to express their sincere thanks to the fruit growers who gave us access to their orchards and to the grower advisors of the different areas (ADV technicians) who helped identifying the best orchards for the assay. This study was supported by grants AGL2010-17486/AGR and AGL2013-49164 of the Spanish Ministry for Science and Innovation.

References

Barrett, B.A. (2008) Assessment of methoxyfenozide exposure on the sexual attractiveness and responsiveness of adult codling moth, Cydia pomonella (L.), in small orchard blocks. Pest Management Science 64, 916–922.Google Scholar
Barrett, B.A. (2010) Exposure to methoxyfenozide treated surfaces reduces the responsiveness of adult male codling moth (Lepidoptera: Tortricidae) to codlemone and pear ester lures in a wind tunnel. Journal of Economic Entomology 103, 1704–1710.Google Scholar
Boivin, T., Chabert-d'Hières, C., Bouvier, J.C., Beslay, D. & Sauphanor, B. (2001) Pleiotropy of insecticide resistance in the codling moth, Cydia pomonella . Entomolgia Experimentalis et Applicata 99, 381–386.Google Scholar
Boivin, T., Bouvier, J.C., Chadoeuf, J., Beslay, D. & Sauphanor, B. (2003 a) Constraints on adaptative mutations in the codling moth Cydia pomonella (L.): measuring fitness trade-offs and natural selection. Heredity 90, 107–113.Google Scholar
Boivin, T., Bouvier, J.C., Beslay, D. & Sauphanor, B. (2003 b) Phenological segregation of insecticide-resistant genotypes in the codling moth Cydia pomonella (Lepidoptera: Tortricidae): a case study of ecological divergences associated with adaptive changes in populations. Genetical Research 81, 177.CrossRefGoogle ScholarPubMed
Boivin, T., Bouvier, J.C., Beslay, D. & Sauphanor, B. (2004) Variability in diapause propensity within populations of temperate insect species: interactions between insecticide resistance genes and photoperiodism. Biological Journal of the Linnean Society 83, 341–351.Google Scholar
Boivin, T., Bouvier, J.C., Chadoeuf, J., Beslay, D. & Sauphanor, B. (2005) Modelling the interactions between phenology and insecticide resistance genes in the codling moth Cydia pomonella . Pest Management Science 61, 53–67.Google Scholar
Bosch, D. & Avilla, J. (2005) Manejo de fincas en confusión sexual de carpocapsa Cydia pomonella (L.) mediante trampas de feromona y de (2E, 4Z)-2,4-decadienoato de etilo. p. 47 in Book of Abstracts of the IV Congreso Nacional de Entomología Aplicada – X Jornadas Científicas de la Sociedad Española de Entomología Aplicada organisez by Sociedad Española de Entomologia Aplicada, 17–21 October 2005, Bragança, Portugal.Google Scholar
Bosch, D., Voltes, M.T., Riedl, H., Torà, R., Sarasúa, M.J. & Avilla, J. (1999) Evaluación de la resistencia de poblaciones españolas de carpocapsa (Cydia pomonella L.) a metil-azinfos. Phytoma España 109, 40–51.Google Scholar
Bosch, D., Avilla, J. & Rodríguez, M.A. (2014) Occurrence of target-site mutations and PSMO enzymatic detoxification in adults of codling moth, Cydia pomonella (L.), from Spanish field populations. in Book of Abstracts of the Joint Meeting of the sub-Groups “Pome fruit arthropods” and “Stone fruits”, 6–9th October, Vienna, Austria.Google Scholar
Brown, G.C., Berryman, A.A. & Bogyo, T.P. (1979) Density-dependent induction of diapause in the codling moth, Cydia pomonella (Olthreutinae; Tortricidae). Canadian Entomologist 111, 431–433.CrossRefGoogle Scholar
Brun-Barale, A., Bouvier, J.C., Pauron, D., Bergé, J.B. & Sauphanor, B. (2005) Involvement of a sodium channel mutation in pyrethroid resistance in Cydia pomonella (L.) and development of diagnostic test. Pest Management Science 61, 549–554.Google Scholar
Buckingham, S.D., Biggin, P.C., Sattelle, B.M., Brown, L.A. & Sattelle, D.B. (2005) Insect GABA receptors: splicing, editing, and targeting by antiparasitic sand insecticides. Molecular Pharmacology 68, 942–951.Google Scholar
Casida, J.E. (2009) Pest toxicology: the primary mechanisms of pesticide action. Chemical Research in Toxicology 22, 609–619.Google Scholar
Cassanelli, S., Reyes, M., Rault, M., Manicardi, G.C. & Sauphanor, B. (2006) Acetylcholinesterase mutation in an insecticide-resistant population of the codling moth Cydia pomonella (L.). Insect Biochemistry Molecular Biology 36, 642–653.CrossRefGoogle Scholar
Clark, D. & Haynes, K. (1992) Sublethal effects of cypermethrin on chemical communication, courtship, and oviposition in the cabbage-looper (Lepidoptera, Noctuidae). Journal of Economic Entomology 85, 1771–1778.Google Scholar
Dallaire, R., Labrecque, A., Marcotte, M., Bauce, E. & Delisle, J. (2004) The sublethal effects of tebufenozide on the precopulatory and copulatory activities of Choristoneura fumiferana and C. rosaceana . Entomologia Experimentalis et Applicata 112, 169–181.Google Scholar
Daly, J.C. (1993) Ecology and genetics of insecticide resistance in Helicoverpa armigera: interactions between selection and gene flow. Genetica 90, 217–226.Google Scholar
Davies, T.G., Field, L.M., Usherwood, P.N. & Williamson, M.S. (2007) DDT, pyrethrins, pyrethroids and insect sodium channels. IUBMB Life 59, 151–162.Google Scholar
Delisle, J. & Vincent, C. (2002) Modified pheromone communication associated with insecticidal resistance in the obliquebanded leafroller, Choristoneura rosaceana (Lepidoptera: Tortricidae). Chemical Ecology 12, 47–51.Google Scholar
Feyresen, R. (1999) Insect P450 enzymes. Annual Review of Entomology 44, 507–533.Google Scholar
Frérot, B., Beslay, D., Malosse, C., Renou, M., Coupard, H., Bouvier, J.C. & Sauphanor, B. (1999) Insecticide resistance and sexual pheromones in codling moth, Cydia pomonella L. pp. 97–105 in Proceedings of the fifth International Conference on Pests in Agriculture organized by Association Nationale de Protection des Plantes, 7–9 December 1999, Montpellier, France.Google Scholar
Fuentes-Contreras, E., Reyes, M., Barros, W. & Sauphanor, B. (2007) Evaluation of azinphos-methyl resistance and activity of detoxifying enzymes in codling moth (Lepidoptera: Tortricidae) from Central Chile. Journal of Economic Entomology 100, 551–556.Google Scholar
Han, W., Zhang, S., Shen, F., Liu, M., Ren, C. & Gao, X. (2012) Residual toxicity and sublethal effects of chlorantraniliprole on Plutella xylostella (Lepidoptera: Plutellidae). Pest Management Science 68, 1184–1190.Google Scholar
Haynes, K. & Baker, T. (1985) Sublethal effects of permethrin on the chemical communication-system of the pinkbollworm moth, Pectinophora gossypiella . Archives of Insect Biochemistry and Physiology 2, 283–293.Google Scholar
Haynes, K., Li, W. & Baker, T. (1986) Control of pink-bollworm moth (Lepidoptera, Gelechiidae) with insecticides and pheromones (attracticide) – lethal and sublethal effects. Journal of Economic Entomology 7, 1466–1471.Google Scholar
Hoelscher, J. & Barrett, B. (2003) Effects of methoxyfenozide treated surfaces on the attractiveness and responsiveness of adult leafrollers. Entomologia Experimentalis et Applicata 107, 133–140.Google Scholar
Ioratti, C., Tasin, M., Charmillot, J.P., Reyes, M. & Sauphanor, B. (2007) Early detection of resistance to tebufenocide in field populations of Cydia pomonella L.: methods and mechanisms. Journal of Applied Entomology 131, 453–459.Google Scholar
Joshi, N.K., Hull, L.A., Rajotte, E.G., Krawczyk, G. & Bohnenblust, E. (2011) Evaluating sex-pheromone and kairomone based lures for attracting codling moth adults in mating disruption versus conventionally managed apple orchards in Pennsylvania. Pest Management Science 67, 1332–1337.Google Scholar
Keil, S., Gu, H.N. & Dorn, S. (2001) Response of Cydia pomonella to selection on mobility: laboratory evaluation and field verification. Ecological Entomology 26, 495–501.Google Scholar
Knight, A.L. (2010) Cross-resistance between azinphos-methyl and acetamiprid in populations of codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae), from Washington State. Pest Management Science 66, 865–874.Google Scholar
Light, D.M., Knight, A.L., Henrick, C.A., Rajapaska, D., Lingren, B., Dickens, J.C., Reynolds, K.M., Buttery, R.G., Merrill, G., Roitman, J. & Campbell, B.C. (2001) A pear derived kairomone with pheromonal potency that attracts male and female codling moth, Cydia pomonella (L.). Naturwissenschaften 88, 333–338.Google Scholar
Margaritopoulos, J.T., Voudouris, C.C., Olivares, J., Sauphanor, B., Mamuris, Z., Tsitsipis, J.A. & Franck, P. (2012) Dispersal ability in codling moth: mark–release–recapture experiments and kinship analysis. Agricultural and Forest Entomology 14, 399–407.Google Scholar
Moffit, H.R. & Westigard, P.H. (1984) Suppression of the codling moth (Lepidoptera: Tortricidae) population on pears in southern Oregon through mating disruption with sex pheromone. Journal of Economic Entomology 77, 1513–1519.Google Scholar
Moore, R. (1988) Inhibition of chemical communication between male and female bollworms (Lepidoptera, Noctuidae) by sublethal amounts of permethrin. Journal of Economic Entomology 81, 78–82.Google Scholar
Poullot, D., Beslay, D., Bouvier, J.C. & Sauphanor, B. (2001) Is attract and kill technology potent against resistant Lepidoptera? Pest Management Science 57, 729–736.Google Scholar
Reuveny, H. & Cohen, E. (2004) Resistance of the codling moth Cydia pomonella (L.) (Lep., Tortricidae) to pesticides in Israel. Journal of Applied Entomology 128, 645–651.CrossRefGoogle Scholar
Reyes, M., Frank, P., Charmillot, J.P., Ioriatti, C., Olivares, J., Pasqualini, E. & Sauphanor, B. (2007) Diversity of insecticide resistance mechanisms and spectrum in European populations of the codling moth, Cydia pomonella . Pest Management Science 63, 890–902.Google Scholar
Ribeiro, L.M.S., Wanderley-Teixeira, V., Ferreira, H.N., Teixeira, A.A.C. & Siqueira, H.A.A. (2014) Fitness costs associated with field evolved resistance to chlorantraniliprole in Plutella xylostella (Lepidoptera: Plutellidae). Bulletin of Entomological Research 104, 88–96.Google Scholar
Riedl, H. (1983) Analysis of codling moth phenology in relation to latitude, climate and food availability. pp. 233–252 in Brown, V.K. & Hodek, I., (Ed.) Diapause and Life Cycle Strategies in Insects. The Hague, Dr. W. Junk.Google Scholar
Riedl, H. & Croft, B.A. (1978) The effects of photoperiod and effective temperatures on the seasonal phenology of the codling moth (Lepidoptera: Tortricidae). Canadian Entomologist 110, 455–470.Google Scholar
Rodríguez, M.A., Bosch, D., Sauphanor, B. & Avilla, J. (2010) Susceptibility to organophosphate insecticides and activity of detoxifying enzymes Spanish populations of Cydia pomonella (Lepidoptera: Tortricidae). Journal of Economic Entomology 103, 482–491.CrossRefGoogle ScholarPubMed
Rodríguez, M.A., Bosch, D. & Avilla, J. (2011) Resistance of Spanish codling moth (Cydia pomonella (L.), Lepidoptera: Tortricidae) populations to insecticides and activity of detoxifying enzymatic systems. Entomologia Experimentalis et Applicata 138, 184–192.Google Scholar
Rodríguez, M.A., Bosch, D. & Avilla, J. (2012) Azinphos-methyl and carbaryl resistance in adults of the codling moth (Cydia pomonella (L.), Lepidoptera: Tortricidae) from Northeastern of Spain. Pesticide Biochemistry and Physiology 103, 43–48.Google Scholar
Sauphanor, B., Brosse, V., Monier, C. & Bouvier, J.C. (1998) Differencial ovicidal and larvicidal resistance to benzoylureas in the codling moth, Cydia pomonella . Entomologia Experimentalis et Applicata 88, 247–253.Google Scholar
Sauphanor, B., Brosse, V., Bouvier, J.C., Speich, P., Micoud, A. & Martinet, C. (2000) Monitoring resistance to diflubenzuron and deltametrin in French codling moth populations (Cydia pomonella). Pest Management Science 56, 74–82.Google Scholar
Sauphanor, B., Franck, P., Lasnier, T., Toubon, J.F., Beslay, D., Boivin, T., Bouvier, J.C. & Renou, M. (2007) Insecticide resistance may enhance the response to a host-plant volatile kairomone for the codling moth, Cydia pomonella (L.). Naturwissenschaften 94, 449–458.Google Scholar
Schumacher, P., Weyeneth, A., Weber, D.C. & Dorn, S. (1997 a) Long flights in Cydia pomonella L. (Lepidoptera: Tortricidae) measured by a flight mill: influence of sex, mating status and age. Physiological Entomology 22, 149–160.Google Scholar
Schumacher, P., Weber, D.C., Hagger, C. & Dorn, S. (1997 b) Heritability of flight distance for Cydia pomonella . Entomologia Experimentalis et Applicata 85, 169–175.Google Scholar
Shel'Deshova, G.G. (1967) Ecological factors determining distribution of the codling moth Laspeyresia pomonella (Lepidoptera: Tortricidae). Entomological Review 46, 349–361.Google Scholar
Soleño, J., Anguiano, L., de D'Angelo, A.P., Cichon, L., Fernandez, D. & Montagna, C. (2008) Toxicological and biochemical response to azinphosmethyl in Cydia pomonella L. (Lepidoptera: Tortricidae) among orchards from the Argentinian Patagonia. Pest Management Science 64, 964–970.Google Scholar
Soleño, J., Anguiano, O.L., Cichon, L.B., Garrido, S.A. & Montagna, C.M. (2012) Geographic variability in response to azinphos-methyl in field-collected populations of Cydia pomonella (Lepidoptera: Tortricidae) from Argentina. Pest Management Science 68, 1451–1457.Google Scholar
Stará, J. & Kocourek, F. (2007) Insecticidal resistance and cross-resistance in populations of Cydia pomonella (Lepidoptera: Tortricidae) in Central Europe. Journal of Economic Entomology 100, 1587–1595.Google Scholar
Steinberg, S., Podoler, H. & Applebaum, S.W. (1992) Diapause induction in the codling moth, Cydia pomonella: effect of prediapause temperatures. Entomologia Experimentalis et Applicata 62, 131–137.Google Scholar
Tan, K., Chen, W., Dong, S., Liu, X., Wang, Y. & Nieh, J.C. (2014) Imidacloprid alters foraging and decreases bee avoidance of predators. PLoS ONE 9, e102725. doi: 10.1371/journal.pone.0102725.Google Scholar
Torà, R., Dolset, A., Almacelles, J., Garcia de Otazo, J., Saló, X., Avilla, J., Bosch, D., Llombart, R., Batllori, L. & Vilajeliu, M. (2009) Métodos alternativos de control de plagas. Confusión sexual para carpocapsa en manzano y peral. Dossier Técnico Formación y assessoramiento del sector agroalimentario 38, 8–17.Google Scholar
Tricoire-Leignel, H., Thany, S.H., Gadenne, C. & Anton, S. (2012) Pest insect olfaction in an insecticide-contaminated environment: info-disruption or hormesis effect. Frontiers in Physiology 3, 1–6.CrossRefGoogle ScholarPubMed
Trimble, R.M., El-Sayed, A.M. & Pree, D.J. (2004) Impact of sub-lethal residues of azinphos-methyl on the pheromone-communication systems of insecticide-susceptible and insecticide-resistant obliquebanded leafrollers Choristoneura rosaceana (Lepidoptera: Tortricidae). Pesticide Management Science 60, 660–668.Google Scholar
Vickers, R.A. & Rothschild, G.H.I. (1991) Use of sex pheromone for control of codling moth. pp. 339–354 in van der Geest, L.P.S. & Evenhuis, H.H. (Eds) Tortricid Pests: their Biology, Natural Enemies and Control. Elsevier, Amsterdam, The Netherlands.Google Scholar
Wei, H. & Du, J. (2004) Sublethal effects of larval treatment with deltamethrin on moth sex pheromone communication system of the Asian corn borer, Ostrinia furnacalis . Pesticide Biochemistry and Physiology 80, 12–20.Google Scholar
Zhou, H., Du, J. & Huang, Y. (2005) Effects of sublethal doses of malathion on responses to sex pheromones by male Asian corn borer moths, Ostrinia furnacalis (Guenée). Journal of Chemical Ecology 31, 1645–1656.Google Scholar
Figure 0

Fig. 1. Mean weekly codling moth adults caught in mating disruption (MD) and non-MD orchards using BioLureTM CM 10X and Pherocon CM-DA ComboTM lures and period of time (rectangle area) when the MFO activity was measured in each flight (gray area). Number of traps =30 (2009) and 58 (2010). Solid bars show the beginning of each generation.

Figure 1

Table 1. Percentage of MFO-resistant codling moth adults caught in 2009 and 2010 in orchards with different management systems in the area of Lleida in traps baited with BioLure™ CM 10X and Pherocon CM-DA Combo™.

Figure 2

Table 2. Percentage of MFO-resistant codling moth adults caught in the three flights of the years 2009 and 2010 in orchards with different management systems in the area of Lleida.

Figure 3

Fig. 2. Percentage of MFO-resistant codling moth adults in the three field flights captured by delta traps lured with Pherocon CM-DA ComboTM, BioLureTM CM 10X and the pear ester DA (3.0 mg of pear ester) in two untreated and 18 treated orchards of the production area of Lleida during the year 2009. Number within the brackets represents the number of insects processed.

Figure 4

Fig. 3. Percentage of MFO-resistant codling moth adults in the three field flights captured by delta traps lured with Pherocon CM-DA ComboTM, BioLureTM CM 10X and the pear ester DA (3.0 mg of pear ester) in untreated (three orchards) and treated orchards (22 orchards) of the production area of Lleida during the year 2010. Numbers within the brackets represent the number of insects processed.