Mating Disruption or Mass Trapping, Compared With Chemical Insecticides, for Suppression of Chilo suppressalis

Transcription

1 Mating Disruption or Mass Trapping, Compared With Chemical Insecticides, for Suppression of Chilo suppressalis (Lepidoptera: Crambidae) in Northeastern China Author(s): Ri-Zhao Chen, Michael G. Klein, Cheng-Fa Sheng, Qi-Yun Li, Yu Li, Lan-Bing Li, and Xing Hung Source: Journal of Economic Entomology, 107(5): Published By: Entomological Society of America URL: BioOne ( is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne s Terms of Use, available at Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.

2 FIELD AND FORAGE CROPS Mating Disruption or Mass Trapping, Compared With Chemical Insecticides, for Suppression of Chilo suppressalis (Lepidoptera: Crambidae) in Northeastern China RI-ZHAO CHEN, 1 MICHAEL G. KLEIN, 2,3,4 CHENG-FA SHENG, 5 QI-YUN LI, 6 YU LI, 1 LAN-BING LI, 1 AND XING HUNG 1 J. Econ. Entomol. 107(5): 1828Ð1838 (2014); DOI: ABSTRACT Asiatic rice borer, Chilo suppressalis (Walker), larvae cause extensive crop losses worldwide. Because chemical control is problematic, and sex pheromone applications are a valuable management tactic in China, judicious timing of a minimal density of pheromone dispensers is important in developing a cost-effective C. suppressalis IPM program. During JuneÐOctober in 2011, 20, 30, 40, and 50 dispensers per hectare for mass trapping, and 200, 300, 400, and 500 dispensers per hectare for mating disruption were placed in northeastern China rice Þelds. Based on those results, only the two highest mass trapping densities were used in 2012Ð2013. The 40, 50, and 500 dispenser densities reduced egg masses to 2.0 per 100 tillers, compared with 9.5 in the insecticide-treated plots in 2011Ð2013. The reduced oviposition resulted in 85% reduction of larval damage, which was comparable with the currently used insecticides, dimethoate and deltamethrin (0.35 kg/ha), which gave no egg reduction, but 80 and 89% reduction in larval damage. The 40 and 500 densities are recommended to Chinese rice farmers for mass trapping and mating disruption programs, respectively. KEY WORDS sex attractant, Asiatic rice borer, rice stem borer, striped stem borer, rice damage Rice is one of the ChinaÕs most important crops, and is grown on ha, or 42% of the crop land (Dale 1994, Huang and Zhang 2002, Chen et al. 2010). Some 100 insect species damage rice plants throughout the world (Pathak 1967, 1968, 1977; Grist and Lever 1969; Khan et al. 1991). The Asiatic rice borer, Chilo suppressalis (Walker), is distributed throughout China, especially in the northeast (Pathak 1968, 1977; Grist and Lever 1969; Chen et al. 2003). The Asiatic rice borer is also found in Europe, East Asia, India, and Indonesia, where it is a serious problem in rice production, and is also known as the striped stem borer or rice stem borer (Poitout and Bues 1978, Cork and Hall 1998, Muralidharan and Pasalu 2006). Asiatic rice borer has two generations per year in northeastern China. Adults occur from about mid- May to early October, with irregular population peaks (Chen et al. 2003), causing consistent damage over the rice plantõs entire growing cycle. Asiatic rice borer females normally ßy from 2100 to 2300 hours, and lay 1 College of Agronomy, Jilin Agricultural University, 2888 Xincheng Rd., Changchun , Jilin Province, China. 2 Department of Entomology, The Ohio State University, Wooster, OH Present address: P.O. Box 1104 Heber, AZ Corresponding author, klein.10@osu.edu. 5 State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing , China. 6 Jilin Agricultural Academy of Science, Cai Yu Rd., Changchun , Jilin Province, China. two to three egg masses (each containing 70 eggs) on the leaf tips. During the tillering stage of rice, larvae sever the vascular system, causing the interior leaf of the tiller to wilt and thus create a dead heart. In the ßowering stage, panicles are severed at their base, creating white heads with unþlled grains (Chen and Klein 2012). Chinese rice farmers normally suppress Asiatic rice borer with insecticides such as synthetic pyrethroids and organophosphates, which are only effective between egg hatch and plant penetration by the young larvae (Sasmal et al. 1983, Tao et al. 2006, He et al. 2008, Huang et al. 2011, Chen and Klein 2012). This restriction results in serious difþculties in timing insecticides application and has resulted in excessive chemical use for Asiatic rice borer suppression. This has resulted in serious damage to the environment and consumersõ health. Recently, most pyrethroids and organophosphates, especially the commonly used Thimet, have been banned by The Chinese Agriculture Ministry and Insecticides (Public notice: 194,199,322). The above restrictions have favored the use of sex pheromones in either mass trapping or mating disruption as nonchemical Asiatic rice borer control methods, and make them good choices for avoiding the negative effects described above. This also makes them a good Þt for IPM programs which use a combination of biological, mechanical, cultural, and chemical means to control pests while reducing pesticide resistance and limiting chemical exposure. Mass trap /14/1828Ð1838$04.00/ Entomological Society of America

3 October 2014 CHEN ET AL.: PHEROMONE SUPPRESSION OF ASIATIC RICE BORER 1829 ping and mating disruption with sex pheromones can reduce the pest population by luring males into traps or permeating synthetic pheromones in the atmosphere to disrupt the mating process by decreasing the encounters between males and calling females (Casagrande 1993, Teng et al. 1993, Cardé and Minks 1995, Pingali and Roger 1995, Byers 2007, Litsinger 2009, Chen and Li 2011, Weinzierl et al. 2012, Chen et al. 2013). Both mating disruption and mass trapping can reduce pest populations, and have had fair success in the control of various insect pests, such as leafroller moths, Argyrotaenia velutinana (Walker) (Novak and Roelofs 1985), the oriental fruit moth (Rice and Kirsch 1990, Trimble et al. 2004), codling moth, Cydia pomonella L. (Mani and Schwaller 1992), tortricid moths (Stelinski et al. 2004), scolytid beetles (Byers 1999), and other invasive species (El-Sayed et al. 2006). In addition, the theoretical basis and modeling the mechanism of mating disruption and mass trapping have been evaluated (Cardé 1990; Cardé and Minks 1995; Miller et al. 2006a,b; Byers 2007, 2008). An effective attraction radius (EAR) is a primary parameter in mass trapping and mating disruption tests. Once an optimal EAR has been established, male moths can be effectively inßuenced by the dispenser plume or competitively attracted to pheromone dispensers rather than calling females (Daterman et al. 1982; Cardé 1990; Mani and Schwaller 1992; Stelinski et al. 2004; Miller et al. 2006a,b; Byers 2009). Field trials have been conducted for both mass trapping (Beevor et al. 1990, Tatsuki 1990, Kondo and Tanaka 1991, Casagrande 1993, Kondo et al. 1993, Su et al. 2003, Chen et al. 2006, Zheng 2007) and mating disruption of Asiatic rice borer (Gaston et al. 1967, Cardé and Minks 1995). In addition, mating disruption has been the primary choice for Asiatic rice borer management in Spain (Casagrande 1993, Howse 1998). In Jilin Province in northeastern China, mass trapping was conducted on 90,000 ha (or 1% of Þelds) in 2011, and on 1,000,000 ha in However, no information is available from China on the optimal EAR for mass trapping or mating disruption. Therefore, various dispenser densities were tested for mass trapping and mating disruption from 2011 to 2013 to determine the optimal densities of dispensers. The Asiatic rice borer sex pheromone was Þrst identiþed as a two-component blend of (Z)-11-hexadecenal and (Z)-13-octadecenal (Ohta et al. 1975, 1976; Nesbitt et al. 1975), and soon a third component, (Z)-9-hexadecenal, was discovered by Tatsuki et al. (1983). This blend, in a ratio of 48:6:5, of the Z11Ð16: Aldehyde, Z13Ð18: Aldehyde, and Z9Ð16: Aldehyde (Tatsuki 1990, Cork 2004), with an aldehyde stabilizing agent butylated hydroxytoluene (BHT), has been used in commercial controlled release formulations (Howse et al. 1998). Our objective here was to compare mass trapping and mating disruption at various dispenser densities with traditional management relying on insecticides, on the basis of male captures, egg mass numbers, and damage control. The hypothesis is that mass trapping or mating disruption gives similar results to chemical insecticides. If this hypothesis is supported, this technique may be recommended to farmers. Here, the dynamics of adult Asiatic rice borer was also monitored with pheromone traps to optimize the timing of mass trapping and mating disruption applications by reducing the cost of dispensers and their replacement. Materials and Methods Field Trial Location and Layout Tests were conducted in ca. a 17 ha rice paddy in Jilin Province, Shuangyang County, Changchun, China. A canal, 2.5 m in width and 500 m in length, runs through the Þeld cutting it into two parts (14 ha and 3 ha), but leaving them equally exposed to Asiatic rice borer adults. The rice Þelds were bounded by corn on three sides and by a small town on the other. Those Þelds and the village restricted movement of Asiatic rice borer from other near by rice Þelds as shown in previous studies (Chen et al. 2003, 2007; Chen and Klein 2012). In 2011, the larger Þeld was divided into 24 plots (83 m in length and 30 m in width), with 12 for the four densities of mating disruption (200, 300, 400, and 500 dispensers per hectare), and the other 12 for mass trapping (20, 30, 40, and 50 dispensers per hectare). Each density was replicated three times with 30 m (a 20 m buffer plus 10 m from the pheromone dispenser to the plot edge) between treatments. A 20 m buffer will eliminate interactions between traps based on our Þeld results in The pheromonebaited traps then were set up with 5, 10, 15, 20, 25, and 30 m between traps in plots and replicated three times. The results showed that when the distance was 15 m between two traps, captures were similar (12 1.2b, 8 0.9c, a, a, a, a). This shows that if the distance is 15 m, there would be no interaction between traps. The smaller Þeld was divided into 12 plots (83 m 30 m), nine for three chemical treatments (Cygon, deltamethrin, and Cartap), and three for controls. In addition, the plots were randomized each year between 2011 and For mating disruption, dispensers were placements at 7 by 7, 5.7 by 5.7, 5 by 5, and 4.5 by 5.7 m, and were 22 by 22, 18 by 18, 16 by 16, and 14.2 by 14.2 m apart for mass trapping. Dispensers were Þxed at the top of rice plants for mating disruption and put in the traps for mass trapping on 20 May. Lures were supplemented on 20 June, 25 July, and 1 September, and the last set of traps and lures were removed on 10 October. The pheromone load is slightly increased by adding new lures at 35 d, even though lures last a maximum of 40Ð45 d in the Þeld (R.Z.C., unpublished data). The dispensers were left in the Þeld to enhance their ef- Þcacy at no additional cost. Tests in 2012 and 2013 were similar to 2011, but the lowest rates for mass trapping (of 20) and mating disruption (200) and the Cartap insecticide were deleted in the later two years based on the 2011 results. The large part of the 2011 Þeld was used in the 2012 and 2013 tests, and the small part was used as an untreated control. Pheromone applications were 3 July, 8 August, and 13 September in 2012, and 27 June, 2 August, and 9 September in

4 1830 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 107, no. 5 Fig. 1. Captures of C. suppressalis from pheromone traps in control plots, 2011Ð Assessments of traps and lures were conducted every 3 d after application. Sex Pheromone and Chemical Insecticide. The pheromone dispensers for mass trapping and monitoring were green rubber septa impregnated with 0.2 mg of the synthetic sex pheromone (Z11Ð16Ald; Z13Ð 18Ald; Z9Ð16Ald, 48:6:5) at 95% purity, with n-hexane as a solvent (Cork 2004), and with 5 mg for mating disruption. The mass trapping lures were produced and provided by the fourth author (S. C. -F.). Mating disruption lures were from Pherobio Technology Co. Ltd. (Puandian Road 206, Beijing China) and had an iron hook placed in its bottom (1.2 cm in length with an elliptical sharp end at 0.3 cm) for Þxing septa securely in the rice canopy. The bell shape of the septa provided protection from rain. Cartap, deltamethrin, and Cygon (0.35 kg/ha; 40, EC, provided by Jilin Bada Insecticide Group Co., Ltd., 9 Xixinhua Road, Gongzhuling , China), at 6 g/liter were applied on 13 July in 2011, and only the later two on 8 July 2012 and 4 July 2013 (Fig. 1), followed by two more sprays at 4-wk intervals (Chen et al. 2003, Tao et al. 2006, Chen and Klein 2012). The insecticides were applied at 230 liters/ha at 0.6 MPa with a knapsack sprayer (model: M9w , Beijing Zhongyuan ScientiÞc Company, Beijing, China), equipped with a swirl nozzle (BJ64348 Chengdu Density Swirl-nozzle ScientiÞc Company, Chengdu, China). Application Timing. Population Dynamics. An automatic water-supplemented pheromone trap (Chen and Klein 2012; Chen et al. 2012, 2013) was used to assess male moth activity as a trigger for mass trapping and mating disruption in the three years, to compare moth populations between 2011, 2012, and 2013, and to evaluate the possible carry-over effect of 2011 applications. Nine traps were divided into three groups and placed diagonally in the control plots from 1 May to 30 October during the three years. All plots had the same rice variety (Jinongda 19), as well as weather, water, and soil conditions, and had been planted with the same rice cultivar for 20 yr. Both the overwintering and Þrst-generation Asiatic rice borer commonly emerged in these Þelds. Traps were mounted on 1.2-m bamboo sticks with the trap bottom 60Ð100 cm above ground (at least 10 cm above the rice canopy), and placed 20 m apart to give 7.5 mg of pheromone per hectare based on previous work (Sheng et al. 2002, 2003a,b; Chen et al. 2003, 2007, 2013). Traps were examined and moths removed and counted every 48 h, and lures were replaced every 5 wk. Correlation Between Captures and Damage Rate. Based on previous studies, three factors determined application timing: 1) when accumulated captures reached 16% of the total captures of the overwintering Asiatic rice borer moth emergence. This was 2100 per trap in previous studies (2009), and determined to be a reliable standard (Sheng et al. 2003a; Jiao et al. 2004, 2006; Chen et al. 2003, 2007; Chen and Klein 2012); 2) when the linear correlation between cumulative captures and dead shell plants is 2% (larvae bore into the stem, causing the inner leaf to turn brownish and wilt, thus creating a dead shell plant; Chen and Klein 2012); and 3) when daily captures equal those from the past six days. The simultaneous occurrence of these three factors triggers the Þrst application. To help establish the linear correlation above, a paddy ( 0.5 ha) located at the 2011Ð2013 Þeld site was selected in 2009, and three traps were set out. Asiatic rice borer adults were counted and removed daily from 1 May to 1 October. When the cumulative captures per trap exceeded 200 moths, the egg masses and dead shell rates were investigated 5 and 15 d later for establishing a correlation between cumulative captures and % dead shells. Evaluation of Treatment Efficacy. Treatment ef- Þcacy of both mating disruption and mass trapping was determined by counts of egg masses, captures of male moths in pheromone-baited assessment traps, larval sampling, and crop damage. Although the absence of egg masses and trap catches are good indications a technique is effective, the percent of dead hearts and dead heads found in each treatment provides the best assessment (Howse et al. 1998, Sheng et al. 2003a, Chen et al. 2007, Chen and Klein 2012).

5 October 2014 CHEN ET AL.: PHEROMONE SUPPRESSION OF ASIATIC RICE BORER 1831 Fig. 2. Linear relationship between cumulative captures of C. suppressalis and % dead shell of rice Egg Masses. Four 10-m 2 areas were randomly selected from treated and control plots, and Asiatic rice borer egg masses were counted on 400 tillers diagonally across each area. Sampling was done on 1, 10, 20, and 30 July. The average number of egg masses per 100 tillers was calculated and pooled over the season for analyses Pheromone Trap Captures. Three pheromone traps per plot were placed diagonally across the treatments resulting in 24 traps in both mating disruption and mass trapping plots in 2011and 18 traps in 2012, plus 12 traps in both chemical and control plots in 2011 and 9 traps in 2012Ð2013. Captures in treatment and control plots were compared to assess the treatment efþcacy. Reductions of moth catches in mass trapping and mating disruption treatments, compared with captures from insecticide-treated plots also indicated efþcacy. Mass trapping efþcacy was established as follows: % Control (average catches per treatment trap minus average catches per control trap, controls are the nontreated plots as opposed to insecticide-treated plots) divided by average catches per control trap 100. Crop Damage Assessment. Evaluating damage to rice gives the best parameter for treatment efþcacy. From a 20 yr Indian dataset, 1% dead hearts caused 2.5% yield loss, 1% white heads caused 4.0% loss, and 1% dead hearts or dead heads resulted in 6.4% loss (Liu 1990, Bandong and Litsinger 2005). These damages are also the main cause for the rice productions losses in China and the best measure available (Sheng et al. 2003a, Chen et al. 2007, Chen and Klein 2012). Here, plant damage was evaluated in late September 2011, by selecting 800 tillered rice plants at random from a pile of harvested plants from each trial plot (Chen and Klein 2012). Damage was established from white heads and dead heads, and the quantity and location of Asiatic rice borer larvae. Data Analysis. Egg mass counts, larval samples, and trap capture data were transformed by sq root (x) and crop damage by log (x 1), to normalize the data. After transformation, data were analyzed by RMANOVA using SAS software (version ), followed by TukeyÕs test to establish statistical differences. Captures, plant damage, egg masses, larval samples, and controls were the variables, and accumulated captures and the dead shells were the interactions tested in the TukeyÕs test. To test the correlation between captures and damage rate, data of the captures and the dead shell from the season were each pooled, giving 10 pairs of data for the correlation formulation. R 2 was determined and the P value was obtained by TukeyÕs test. For mean egg mass reductions, plant damage control, larval control, and capture reductions, data from 2011 to 2013 were pooled and transformed by arcsine (x) for analyzing with RMANOVA, followed by TukeyÕs test. Results Application Timing. Capture Data. The Þrst overwintering moths were captured in late May, and the captures steadily rose for 3 wk to a peak, and then dropped (Fig. 1). Following an increase to 50Ð60 moths per day ca. 30 July, captures quickly dropped to single digits. Between mid-august and mid-september, a new, but smaller, Asiatic rice borer generation was captured. On 20 June, 3 July, and 27 June, 2011Ð13, captures averaged , , and per day, respectively. In these three years, this was ca. 3 the previous six days captures and indicated a trigger for treatments had been met. Correlation Between Captures and % Dead Shell. The mean captures of Þrst-generation Asiatic rice borer were 2,038 per trap (CV 0.14) over that ßight period in Similar numbers of moths (1,969, 2,000, and 2,096) were captured during this study in 2011, 2012, and Between 1 May and 30 October, a signiþcant correlation between cumulative captures and dead shell rate showed when captures reached ca. 971 the % dead shell reached 2% (Fig. 2). On 20 June, 3 July, and 27 June, 2011Ð2013, captures reached 968, 998, and 972, respectively, and the damage thresholds were reached. By 11, 18, and 15 June, 2011Ð2013, 16% (315, 320, and 331 moths) of the Þrst generation were captured. Taking into consideration the damage thresholds in 2011Ð2013, plus the other two factors, applications were made at the critical moth emer-

6 1832 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 107, no. 5 Fig. 3. Egg mass reduction of C. suppressalis 2011Ð2013. gence point of the Þrst generation on 20 June, 3 July, and 27 June in these three years. Evaluation of Treatment Efficacy. Egg Masses. Most egg masses (AV: 9.8) were observed in insecticide-treated plots in 2011Ð2013 (Fig. 3), the 200 dispensers per hectare mating disruption plots (AV: 8.6), compared with the 300, 400, and 500 dispensers per hectare mating disruption (AV: 1.9, 1.7, 1.3), and 30, 40 and 50 dispensers per hectare mass trapping treated plots (AV: 1.7, 1.6, 1.6) in 2011Ð2013. Egg masses were reduced by the other pheromone treatments, signiþcantly so in the 500 dispensers per hectare mating disruption, and 50 and 40 dispensers per hectare mass trapping treatments from the insecticide and other pheromone-treated plots. Slightly reduced numbers of egg masses were found with the middle densities, but they were not signiþcantly lower than the control (Fig. 3). Trap Captures. During the Þrst generation in 2011, assessment traps captured many moths in the chemical treatments, and even more in the controls, but the differences were not signiþcant (Table 1). During the whole growing season, average catches were reduced with all the mass trapping and mating disruption densities. Average catches from both generations in the two higher mass trapping and mating disruption plots Table 1. Captures of male rice stem borer Captures per trapñ% reduction Plots First generation Second generation % reduction % reduction Average Average Mass trap a 20/ha d d d c 30/ha b b b b c b b b 40/ha a a a a a a a a 50/ha a ab a ab a a a a Mating dis b 200/ha d c d c 300/ha c b b b b b b 400/ha b b ab b ab a a ab 500/ha b ab ab ab bc a a a Insecticide Cygon e c c d e c c d Deltamethrin e d c e e c de Cartap e f e Means SD. Reduction (moth per trap in ck moth per trap in treatment/moth per trap in ck) differed signiþcantly among treatments, the Þrst generation (2011: F 10, , P ; 2012: F 7, , P ; 2013: F 7, , P ; average: F 10, , P ) and the second generation (2011: F 10, , P ; 2012: F 7, , P ; 2013: F 7, , P ; average: F 10, , P ). Numbers in a column followed by the same letter are not signiþcantly different (0.01%). a Mass trapping. b Mating disruption.

7 October 2014 CHEN ET AL.: PHEROMONE SUPPRESSION OF ASIATIC RICE BORER 1833 Fig. 4. Mean plant damage, larval control, and capture reduction in various treatments 2011Ð2013. were signiþcantly less than the other pheromone treatments (Table 1). This correlates with control obtained where 50 dispensers per hectare mass trapping and 400 and 500 dispensers per hectare mating disruption provided 85% control, followed by 40 dispensers per hectare mass trapping and 300 dispensers per hectare mating disruption ( 80%) and 30 dispensers per hectare mass trapping ( 79%) in both generations 2011Ð2013 (Table 1). Both 40 and 50 dispensers per hectare for mass trapping, and 400 and 500 dispensers per hectare for mating disruption provided signiþcant reductions in moths captured when compared with other treatments in 2011Ð2013 (Fig. 4). Crop Damage. SigniÞcantly less damage was found with mass trapping at 40 and 50 dispensers per hectare, mating disruption at 400 and 500 dispensers per hectare, and the insecticide treatments with Cygon and Deltamethrin in 2011 (0.83, 0.80, 0.90, 0.88, 1.11, and 1.15, respectively) than mass trapping at 20 and 30 dispensers per hectare, or mating disruption at 200 and 300 dispensers per hectare (1.96, 1.7, 2.55, 2.29, respectively), with no signiþcant difference between these latter treatments (Table 2). Mass trapping at lower rates had more damage in these three years. The lowest rate of mating disruption and the control had the highest damage. SigniÞcant differences in damage were observed between the three treatment groups when treatment types were pooled for analyses, but there were no signiþcant differences within the groups. Overall, 40 and 50 dispensers per hectare mass trapping, 400 and 500 dispensers per hectare mating disruption, and the insecticide provided ca. 80Ð89% damage reduction in 2011Ð2013 (Fig. 4). Comparison Between 2011, 2012, and 2013 Population Dynamic Pattern. High captures of Asiatic rice borer were recorded in the control area from 15 May to 8 August, 2011 (Fig. 1), but trap catches per plot were relatively lower in 2012 and 2013 during the same time (Fig. 1). In 2011, average captures per assessment trap that represent the average moth population in the control were in the Þrst generation and in the second, while in 2012 and 2013 captures in the same plots were and and and 8 1.2, respectively. The population patterns for the two years closely match from mid-august to 7 October, suggesting that a negative population effect from any source had dissipated by the second generation of Asiatic rice borer, whereas the Þrst generation population was apparently affected by some factor, possibly the previous pheromone use. Discussion Asiatic rice borer is distributed over most of China, and damage sometimes reaches 30% despite the use of insecticides (Gao et al. 1987, Qin et al. 1991, Directorate of Rice Research [DRR] 2004, Chi et al. 2005, Litsinger 2009). There have been previous studies on using sex pheromone as mating disruption techniques for Asiatic rice borer control, especially in Europe by Casagrande (1993), Howse (1998), and Alfaro et al. (2009), which encouraged us to try to gain similar control in China, but with less pheromone and more convenient dispensers. This work was also stimulated by studies against other Lepidoptera pests. For example, Witzgall et al. (2008) and Stelinski et al. (2008, 2013) successfully used red rubber septa as sex pheromone dispensers at densities of 35, 215, and 1100 dispensers per hectare, with 1.5 g (AI)/ha to control pests such as the citrus leafminer, Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae). In addition, Su et al. (2003) also used rubber septa in successful mass

8 1834 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 107, no. 5 Table 2. Control of rice stem borer and % damage to plants following application of various treatments Mean per plot Treatment Dead heart White head Variable testedñ% damage % control Larvae per plants Larvae per plants % larval % damage plant Larval per damage Mass trap a 20/ha 35 2b/12 2b 25 5c/9 1c 5.6 1,2bc bc 68 7d/59 7e 30/ha 33 2b/11 3b 38 3c/12 1bc 54 4c/19 3b 23 4c/8 2c 25 3d/7 1c 67 9b/11 2b c cd b c c b 72 8c/65 8d 65 5b/71 7c 72 8c/75 6c 40/ha 14 3c/4 1c 16 2d/5 2c 33 2e/8 2c 13 3d/5 1c 14 3e/6 1cd 25 3d/6 1de c d c d cd c 86 8a/83 14a 85 11a/83 9b 82 9b/87 8ab 50/ha 16 1c/3 1c 18 3d/6 1c 21 6e/7 2c 14 3d/6 1c 13 3e/5 1cd 19 3d/7 1c c d d d 1.0 cd c 86 8a/84 16a 87 12a/83 15b 88 9a/87 7ab Mating dis b 200/ha 53 6b/17 4b 51 8b/14 2b b b 51 5g/48 5g 300/ha 43 7b/16 1b 46 6c/18 1b 78 8b/22 4b 33 7c/10 2bc 35 6c/12 2b 42 6c/15 1b bc c b b b b 62 6f/53 5f 59 9b/53 11d 72 9c/73 7c 400/ha 19 4c/6 1c 17 2d/5 1c 29 3e/9 2c 15 3d/4 1c 16 2e/5 1c 19 3d/7 1c c d cd d cd c 83 11ab/82 7a 82 12a/83 14b 86 9a/85 5b 500/ha 20 3c/5 2c 18 3d/3 1c 20 4e/6 1c 6 1d/4 1c 11 2e/3 1d 18 2d/4 1e c d d d d d 84 13a/83 9a 86 9a/91 12a 90 8a/91 12a Insecticide Cygon 22 3c/8 2c 25 6d/7 2c 41 6d/12 2c 13 3d/5 1c 14 2e/6 1cd 21 3d/6d 1e c d c d cd c 82 12b/77 9b a/83 11b 82 11b/84 13b Delta c 27 4c/12 1b 19 5d/5 2c 27 4e/8 1c 13 4d/7 1c 13 3e/5 1cd 14 2e/5d 1e c d d d cd c 83 ab/76 bc 82 a/83 b 89 a/89 a Cartap 22 4c/14 1b 11 2d/6 1c c d 86 a/71 c Control 82 9a/33 4a 85 8a/36 6a a/69 9a 135 9a/27 2a 113 9a/28 4a 141 9a/32 3a a a a a a a Control efþcacy (% damage in ck % damage in treatment/% damage in ck) differed signiþcantly among treatments (2011: F 9, , P ; 2012: F 8, , P ; 2013: F 7, , P ), and plant damaged rate differed signiþcantly among treatments (2011: F 10, , P ; 2012: F 9, , P ; F 8, , P ) and larvae per plant (2011: F 9, , P ; 2012: F 8, , P ; 2013: F 7, , P ). Numbers in a column followed by the same letter are not signiþcantly different (0.01%). a Mass trapping. b Mating disruption. c Deltapmethrin.

9 October 2014 CHEN ET AL.: PHEROMONE SUPPRESSION OF ASIATIC RICE BORER 1835 trapping in China, and Yang et al. (2001) and Wang et al. (2011) controlled Asiatic rice borer with mating disruption, but they did not use rubber septa for pheromone release. In this study, three applications of pheromones for mating disruption with 400 and 500 dispensers per hectare provided comparable control to chemical and used only 7.5 and 6.0 g of pheromone per hectare during the entire growing season (2.5 g/ha per application with three applications). These doses are probably less than that used by Casagrande (1993) and similar to that used by Alfaro et al. (2009; 6.4 g/ha) for Asiatic rice borer control in Spain. With all of the interacting factors in such Þeld tests, it is possible that lack of signiþcant differences between treatments may be due to a lower power in the evaluations, which may make selected results somewhat equivocal. However, it does not change the basic Þndings of successful suppression of Þeld populations at the higher rates tested. We used a lower dose in the Þeld, and gained comparable control to that of Casagrande and Alfaro et al. for the following possible reasons: First, rice only grows in northeastern China from early June to early October and the long cold winter results in less than two full Asiatic rice borer generations a year. In addition the second generation in China is considerably smaller than the Þrst (Fig. 1), resulting in much reduced second generation pressure and damage (Chen et al. 2003, 2007; Sheng et al. 2003a; Chen and Klein 2012). Second, we used rubber septa dispensers that probably released pheromone over a longer Þeld life, and were supplemented with new dispensers. Previous studies (Su et al. 2001, Sheng et al. 2002, Jiao et al. 2003) showed rubber septa still had 37% of their initial pheromone activity after a yearõs storage at 20 C and its Þeld life can be six weeks to two months. Additional low-load septa were added twice during the tests, rather than removing septa from the traps. Based on the above observations, the older septa would have provided additional pheromone to the newer septa for mating disruption action. More importantly, pheromone trapping probably works well in temperate climates like northeastern China where only one rice crop per year is grown moth ßights are synchronized by generation. In tropical areas, moths are ßying at various times and distinct generations are difþcult to deduce from trapping data or damage counts. In the tropical areas, Asiatic rice borer is the most highly adapted stem borer worth those climates (Reissig et al. 1986, Litsinger et al. 2006). Special dispensers with high pheromone doses have been used in mating disruption studies in some countries. However, mating disruption in northeastern China with 750 septa per hectare resulted in 84.9% Asiatic rice borer control (Yang et al. 2001). This investigation found similar control with a lower dose per dispenser and reduced dispenser densities. In addition, there is little wind during the rice growing season in northeastern China, and this prolongs the septaõs Þeld life and enhances the effect of the mating disruption (Sheng et al. 2002, 2003b; Jiao et al. 2003). Mass trapping with pheromones at 45 dispensers per hectare in Heilongjiang Province (the northernmost province in northeastern China) in 2013 provided 80% control (Liu et al. 2013). That density is similar to what was used in this trial. In addition, Wang et al. (2011) used 30 dispensers per hectare in Liaoning Province (southernmost province in northeastern China). Because this study on mass trapping trial in Jilin Province evaluated 20Ð50 dispensers per hectare, the results indicate 40 dispensers per hectare can be recommended to farmers for mass trapping of Asiatic rice borer in northeastern China. Crop damage assessment is the best way for showing the efþcacy of mating disruption (Karg and Sauer 1995, Howse 1998) or mass trapping (Sheng et al. 2002, 2003a; Chen et al. 2007). Here, and in previous studies, a correlation between cumulative captures and rice damage was established to obtain an optimal application time for the important overwintering generation of Asiatic rice borer. Jiao et al. (2004, 2006) reported that when the cumulative captures reached 870, there will be 2% damaged tillers. That coincides nicely with what was found here, showing our correlation equation is accurate and valid, and can be used in northeastern China. Furthermore, combining the three factors, i.e., the sharp increase in captures, initial peak date, and the correlation equation, is a novel method to accurately establish application timing. Moth capture patterns from 2010 and 2011 were shown and discussed by Chen and Klein (2012, Fig. 2). The captures for all three years were very similar and identiþed the important Þrst generation peak as mid- June, indicating the best time for treatments. Historically in northeastern China, the Asiatic rice borer Þrst appears in mid-may, and pheromone applications were started ca. 25Ð30 May (Sheng et al. 2003a; Chen et al. 2007, 2010). Results here showed that pheromone application could be applied before peak ßight, ca. 20Ð30 June, when the damage threshold is reached, therefore saving one entire application of lures. This saves signiþcant lure and application costs, especially in mating disruption treatments, while still obtaining acceptable control with lower pheromone costs. Compared with chemical insecticides, pheromones provide obvious advantages. Application of pheromones for managing stem borers provides farmers with crop protection that is user and environmentally friendly. In addition, pest reductions may last more than one season which is consistent with previous work by Jiao et al. (2003) and Sheng et al. (2003a). Furthermore, chemical treatments require a period of 20 d between the last application and harvest. This prevents the need for treating the second-generation moths in northeastern China. Acknowledgments We thank the Changchun Government and Jilin Government Fund on sex pheromone Asiatic rice borer Control, 13NK19, XH, with special thanks to the Bureau of Foreign Experts Affairs (BFEA) of Jilin Province for Asiatic rice borer control. KleinÕs trips to China were supported by

10 1836 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 107, no. 5 Fundament Numbers: L and L We also thank the JEE reviewer and editor for their constructive suggestions. References Cited Alfaro, C., V. Navarro-Llopis, and J. Primo Optimization of pheromone dispenser density for managing the rice striped stem borer, Chilo suppressalis (Walker), by mating disruption. Crop Prot. 28: 567Ð572. Bandong, J. P., and J. A. Litsinger Rice crop stage susceptibility to the rice yellow stem borer Scirpophaga incertulas (Walker). Int. J. Pest Manag. 51: 37Ð43. Beevor, P. S., H. David, and O. T. Jones Female sex pheromones of Chilo spp. (Lepidoptera: Pyralidae) and their development in pest control applications. Insect Sci. Appl. 11: 787Ð794. Byers, J. A Effects of attraction radius and ßight paths on catch of scolytid beetles dispersing outward through rings of pheromone traps. J. Chem. Ecol. 25: 985Ð1005. Byers, J. A Simulation of mating disruption and mass trapping with competitive attraction and camoußage. Environ. Entomol. 36: 1328Ð1338. Byers, J. A Active space of pheromone plume and its relationship to effective attraction radius in applied models. J. Chem. Ecol. 34: 1134Ð1145. Byers, J. A Modeling distributions of ßying insects: effective attraction radius of pheromone in two and three dimensions. J. Theor. Biol. 256: 81Ð89. Cardé, R. T Principles of mating disruption, pp. 47Ð71. In R. L. Ridgway and R. M. Silverstein (eds.), Behavior modifying chemicals for pest management: applications of pheromones and other attractants. Marcel Dekker, New York, NY. Cardé, R. T., and A. K. Minks Control of moth pests by mating disruption: successes and constraints. Annu. Rev. Entomol. 40: 559Ð585. Casagrande, E The commercial implementation of mating disruption for the control of the rice stem borer, Chilo suppressalis, in rice in Spain. IOBC WPRS Bull. 16: 82Ð89. Chen, J., J. Huang, and J. Hua Mapping rice planting areas in southern China using the China Environment Satellite Data. Math Comput. Model. 54: 1037Ð1043. (doi: /j.mcm ). Chen, R.-Z., and M. G. Klein EfÞcacy of insecticides against the rice stem-borer, Chilo suppressalis (Walker) (Lepidoptera: Crambidae), and use of sex pheromones to more accurately time the yearly application. Int. J. Pest Manag. 58: 354Ð360. Chen, R.-Z., and Y. Li A novel plant volatile attractant scheme to protect corn in China from the white-spotted ßower chafer (Coleoptera: Scarabaeidae: Cetoniinae). J. Pest Sci. 84: 327Ð335. Chen, R.-Z., L.-S. Zang, Y. Mu, M. Liu, G.-Z. Sun, and Z.-M. Wang Preliminary study on generation and chemical prevention and control of Chilo suppressalis in Jilin Province. J. Jilin Agric. Univ. 25: 250Ð252, 256. Chen, R.-Z., X.-Y. Li, M. Liu, B.-R. Yi, C.-F. Sheng, and J.-Y. Ma Preliminary study on generation of Chilo suppressalis (Walker) in Changchun City using sex technique. J. Jilin Agric. Sci. 32: 37Ð39. Chen, R.-Z., Z.-F. Wang, and Y.-F. Yang A patent of utility model: an automatically water supplied trap. Patent no Chen, R.-Z., M. G. Klein, C.-F. Sheng, Y. Li, D.-X. Shao, and Q.-Y. Li Use of pheromone timed insecticide applications integrated with mating disruption or mass trapping against Ostrinia furnacalis (Génuéé) (Lepidoptera: Pyralidae) in sweet corn. Environ. Entomol. 42: 1390Ð Chen, X., L.-R. Wang, and L. Chen Studies on the action threshold of Chilo suppressalis on rice in Shengyang District. Liaoning Agric. Sci. 6: 40Ð41. Chi, S.-Y., Y. Peng, Y. C. Wang, Z.-J. Han, and C.-K. Chen Advances in the research of insecticide resistance of Chilo suppressalis. Plant Prot. 31: 3Ð6. Cork, A Pheromone Manual, chapter 4. Natural Resources Institute, Chatham Maritime, United Kingdom. Cork, A., and D. R. Hall Application of pheromones for crop pest management in the Indian Sub-Continent. J. Asia-PaciÞc Entomol. 1: 35Ð49. Dale, D Insect pests of rice plants their biology and ecology. In Heinrichs E. A. (ed.). Biology and Management of Rice Insects. IRRI, Los-Banos, The Philippines. pp. 363Ð485. Daterman, G. E., L. L. Sower, and C. Sartwell Challenges in the use of pheromones for managing western forest Lepidoptera, pp. 243Ð254. In B. Leonhardt and M. Beroza (eds.), Insect pheromone technology: chemistry and applications. American Chemical Society, Washington, DC. (DRR) Directorate of Rice Research Production oriented survey. Annual Reports 1965Ð2003. All-India Coordinated Rice Improvement Project (AI-CRIP), Hyderabad, India. El-Sayed, A. M., D. M. Suckling, C. H. Wearing, and J. A. Byers Potential of mass trapping for long-term pest management and eradication of invasive species. J. Econ. Entomol. 99: 1550Ð1564. Gao, J.-S., W.-M. Li, and G.-R. Jing Discussion on the economic threshold of the striped rice-stem borer (Chilo suppressalis Walker). Acta Phytophyl. Acica Sin. 14: 107Ð 113. Gaston, L. K., H. H. Shorey, and C. A. Saario Insect population control by use of sex pheromones to inhibit orientation between sexes. Nature 213: Grist, D. H., and R.J.A.W. Lever Pests of rice. Longmans, Green and Co., Ltd., London, United Kingdom. He, Y.-P., Z.-R. Shao, W.-M. Chen, G.-M. Liang, and Y.-P. Li Laboratory screening of alternative insecticides for highly toxic insecticides against the striped stem borer (Chilo suppressalis) on rice. Chinese J. Rice Sci. 3: 313Ð 320. Howse, P. E Pheromones and behaviour, pp. 1Ð130. In P. E. Howse, I. Stevens, and O. T. Jones (eds.), Insect pheromones and their use in pest management. Chapman & Hall, London, United Kingdom. Howse, P., I. Stevens, and O. T. Jones Insect pests of rice, pp. 325Ð330. In P. E. Howse, I. Stevens, and O. T. Jones (eds.), Insect pheromones and their use in pest management. Chapman & Hall, London, United Kingdom. Huang, Z.-G., and W.-Q. Zhang The origin and expansion of cultivated rice in ancient China. Trop. Geogr. 22: 76Ð79. Huang, J., S.-F. Wu, and G.-Y. Ye Evaluation of lethal effects of chlorantraniliprole on Chilo suppressalis and its larval parasitoid, Cotesia chilonis. Agric. Sci. China 10: 1134Ð1138. Jiao, X.-G., W.-J. Xuang, H.-T. Wang, and C.-F. Sheng Effect of storage temperature and duration of sex pheromone septa on capturing male Chilo suppressalis (Walk). J. Jilin Agric. Univ. 25: 367Ð370. Jiao, X.-G., W.-J. Xuang, H.-T. Wang, and C.-F. Sheng Correlation analysis between the Chilo suppressalis male

11 October 2014 CHEN ET AL.: PHEROMONE SUPPRESSION OF ASIATIC RICE BORER 1837 moths caught by pheromone traps and the forecasting indexes. J. Jilin Agric. Univ. 26: 256Ð259. Jiao, X.-G., W.-J. Xuang, and C.-F. Sheng Establishment of forecasting model for the occurring periods of Chilo suppressalis in Liuhe County of Jilin Province. J. Jilin Agric. Univ. 28: 365Ð368. Karg, G., and A. E. Sauer Spatial-distribution of pheromone in vineyards treated for mating disruption of the grape vine moth Lobesia botrana measured with electroantennograms. J. Chem. Ecol. 21: 1299Ð1314. Khan, Z. R., J. A. Litsinger, A. T. Barrion, and F.F.D. Villanueva World bibliography of rice stem borers 1794Ð1990. International Rice Research Institute, Makati, Philippines. Kondo, A., and F. Tanaka Pheromone trap catches of the rice stem borer moth, Chilo suppressalis (Walker) (Lepidoptera, Pyralidae) and related trap variables in the Þeld. Appl. Entomol. Zool. 26: 167Ð172. Kondo, A., F. Tanaka, H. Sugie, and N. Hokyo Analysis of some biological factors affecting differential pheromone trap efþcacy between generations in the rice stem borer moth, Chilo suppressalis (Walker) (Lepidoptera, Pyralidae). Appl. Entomol. Zool. 28: 503Ð511. Litsinger, J. A When is a rice insect a pest: yield loss and the green revolution, pp. 391Ð498. In: R. Peshin and A. K. Dhawan (eds.), Integrated pest management: innovationdevelopment process, vol. 1. Springer Science Media B.V., Berlin, Germany. Litsinger, J. A., J. P. Bandong, B. L. Canapi, C. G. dela Cruz, P. C. Pantua, A. L. Alviola, III, and E. Batay-an Evaluation of action thresholds against chronic insect pests of rice in the Philippines: IV. Stemborers. Int. J. Pest Manag. 52: 194Ð207. Liu, T. S A survey on the occurrence of rice stem borers and their damage in Taichung Area. Bull. Taichung Plant Prot. Manual. 29: 39Ð47. Liu, X.-L., S.-M. Sheng, R.-Z. Chen, H.-R. Gao, Y.-J. Li, C.-L. Liu, K.-Q. Wang, and C.-F. Sheng A preliminary study of pheromone trap density for the rice stem borer in northeastern area in China. J. Jilin Agric. Sci. 1: 63Ð67. Mani, E., and R. Schwaller Results of 12 years experience to control codling moth, Cydia pomonella L., by mating disruption. IOBC/WPRS Bull. 15: 76Ð80. Miller, J. R., L. J. Gut, F. M. de Lame, and L. L. Stelinski. 2006a. Differentiation of competitive vs. non-competitive mechanisms mediating disruption of moth sexual communication by point sources of sex pheromone (part1). Theory J. Chem. Ecol. 32: 2089Ð2114. Miller, J. R., L. J. Gut, F. M. de Lame, and L. L. Stelinski. 2006b. Differentiation of competitive vs. non-competitive mechanisms mediating disruption of moth sexual communication by point sources of sex pheromone (part2): case studies. J. Chem. Ecol. 32: 2115Ð2143. Muralidharan, K., and I. C. Pasalu Assessments of crop losses in rice ecosystem due to stem borer damage. Crop Prot. 25: 409Ð417. Nesbitt, B. F., P. S. Beevor, D. R. Hall, R. Lester, V. A. Dyck IdentiÞcation of female sex pheromones of moth, Chilo suppressalis. J. Insect Physiol. 21: 1883Ð1886. Novak, M. A., and W. L. Roelofs Behavior of male redbanded leafroller moths, Argyrotaenia velutinana (Lepidoptera: Tortricidae), in small disruption plots. Environ. Entomol. 14: 12Ð16. Ohta, K., S. Tatsuki, K. Uchiumi, M. Kurihara, and J. Fukami Sex-pheromone of rice stem borer puriþcation and chemical properties. Agric. Biol. Chem. 39: 2437Ð2438. Ohta, K., S. Tatsuki, K. Uchiumi, M. Kurihara, and J. Fukami Structures of sex pheromones of rice stem borer. Agric. Biol. Chem. 40: 1897Ð1899. Pathak, M. D Recent developments and future prospects for the chemical control of rice stem borer at IRRI, pp. 335Ð349. In Proceedings of the Symposium on Major Insect Pests of Rice Plants at the International Rice Research Institute, The Philippines. The Johns Hopkins Press, Baltimore, MD. Pathak, M. D Ecology of common insect pests of rice. Annu. Rev. Entomol. 13: 257Ð294. Pathak, M. D Defense of the rice crop against pests. The genetic basis of epidemics in agriculture. Ann. N. Y. Acad. Sci. 287: 287Ð295. Pingali, P. L., and P. A. Roger Impact of pesticides on farmer health and the rice eco-system. Kluwer Academic Publishers, Boston, MA. Poitout, S., and R. Bues Life-cycle of rice stem borer Chilo suppressalis (Walker) in Rhone delta (Camargue) use of sex trap. Ann. Zool. Ecol. Anim. 10: 245Ð265. Qin, H.-G., S.-X Hu, and R. Fang Studies on the action threshold of rice striped borer on hybrid rice. Acta Phytophyl. Acica Sin. 18: 193Ð198. Reissig, W. H., E. A. Heinrichs, J. A. Litsinger, K. Moody, L. Fiedler, T. W. Mew, and A. T. Barrion Illustrated guide to integrated pest management in rice in tropical Asia, p IRRI, Laguna, Philippines. Rice, R. E., and P. Kirsch Mating disruption of oriental fruit moth in the United States, pp. 193Ð211. In R. L. Ridgeway, R. M. Silverstein, and M. N. Inscoe (eds.), Behavior-modifying chemicals for insect management. Marcel Dekker, New York, NY. Sasmal, S., J. P. Kulshrestha, and S. Rajamani Chlorpyriphos spraying is economical in controlling stem borer in Rabi rice. Int. Rice Res. Newsl. 4: 3. Sheng, C.-F., Z.-X. Kang, R.-Z. Chen, H.-T. Wang, and W.-J. Xuan Effect of storage duration of sex pheromone septa on male catches of rice stem borer, Chilo suppressalis (Walker). Plant Prot. 28: 9Ð11. Sheng, C.-F., W.-J. Xuan, B.-R. Yi, R.-Z. Chen, and X.-N. Qi. 2003a. Monitoring seasonal dynamics and generations of the rice stem borer male moths with sex pheromone in Jilin Province in China. Chin. J. Ecol. 22: 79Ð81. Sheng, C.-F., H.-T. Wang, S.-Y. Sheng, L.-D. Gao, and W.-J. Xuang. 2003b. Pest status and loss assessment of crop damage caused by the rice stem borers, Chilo suppressalis and Tryporyza incertulas in China. Entomol. Knowl. 40: 289Ð294. Stelinski, L. L., L. J. Gut, A. V. Pierzchala, and J. R. Miller Field observations quantifying attraction of four tortricid moths to high-dosage pheromone dispensers in untreated and pheromone-treated orchards. Entomol. Exp. Appl. 113: 187Ð196. Stelinski, L. L., J. R. Miller, and M. E. Rogers Mating disruption of citrus leafminer mediated by a noncompetitive mechanism at a remarkably low pheromone release rate. J. Chem. Ecol. 34: 1107Ð1113. Stelinski, L. L., L. Gut, and J. R. Miller An attempt to increase efþcacy of moth mating disruption by co-releasing pheromones with kairomones and to understand possible underlying mechanisms of this technique. Environ. Entomol. 42: 158Ð166. Su, J.-W., G.-F. Zhang, W.-M. Fan, W.-J. Xuan, and C.-F. Sheng The sex pheromone of the rice stem borer, Chilo suppressalis in paddy Þelds, sticky trap and lure storage time and lure dosage. Chin. J. Rice Sci. 15: 197Ð 200.