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Mating Disruption or Mass Trapping, Compared With ChemicalInsecticides, for Suppression of Chilo suppressalis (Lepidoptera:Crambidae) in Northeastern ChinaAuthor(s): Ri-Zhao Chen, Michael G. Klein, Cheng-Fa Sheng, Qi-Yun Li, Yu Li,Lan-Bing Li, and Xing HungSource: Journal of Economic Entomology, 107(5):1828-1838. 2014.Published By: Entomological Society of AmericaURL: http://www.bioone.org/doi/full/10.1603/EC14148

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FIELD AND FORAGE CROPS

Mating Disruption or Mass Trapping, Compared With ChemicalInsecticides, 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 HUNG1

J. Econ. Entomol. 107(5): 1828Ð1838 (2014); DOI: http://dx.doi.org/10.1603/EC14148

ABSTRACT Asiatic rice borer, Chilo suppressalis (Walker), larvae cause extensive crop lossesworldwide. Because chemical control is problematic, and sex pheromone applications are a valuablemanagement tactic in China, judicious timing of a minimal density of pheromone dispensers isimportant 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 perhectare 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 dispenserdensities reduced egg masses to �2.0 per 100 tillers, compared with �9.5 in the insecticide-treatedplots in 2011Ð2013. The reduced oviposition resulted in �85% reduction of larval damage, which wascomparable with the currently used insecticides, dimethoate and deltamethrin (0.35 kg/ha), whichgave no egg reduction, but �80 and 89% reduction in larval damage. The 40 and 500 densities arerecommended 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, andis grown on �4.17 � 107 ha, or 42% of the crop land(Dale 1994, Huang and Zhang 2002, Chen et al. 2010).Some 100 insect species damage rice plants through-out the world (Pathak 1967, 1968, 1977; Grist andLever 1969; Khan et al. 1991). The Asiatic rice borer,Chilo suppressalis (Walker), is distributed throughoutChina, especially in the northeast (Pathak 1968, 1977;Grist and Lever 1969; Chen et al. 2003). The Asiaticrice borer is also found in Europe, East Asia, India, andIndonesia, where it is a serious problem in rice pro-duction, and is also known as the striped stem borer orrice stem borer (Poitout and Bues 1978, Cork and Hall1998, Muralidharan and Pasalu 2006).

Asiatic rice borer has two generations per year innortheastern China. Adults occur from about mid-May to early October, with irregular population peaks(Chen et al. 2003), causing consistent damage over therice plantÕs entire growing cycle. Asiatic rice borerfemales normally ßy from 2100 to 2300 hours, and lay

two to three egg masses (each containing �70 eggs)on the leaf tips. During the tillering stage of rice, larvaesever the vascular system, causing the interior leaf ofthe tiller to wilt and thus create a dead heart. In theßowering stage, panicles are severed at their base,creating white heads with unÞlled grains (Chen andKlein 2012).

Chinese rice farmers normally suppress Asiatic riceborer with insecticides such as synthetic pyrethroidsand organophosphates, which are only effective be-tween egg hatch and plant penetration by the younglarvae (Sasmal et al. 1983, Tao et al. 2006, He et al. 2008,Huang et al. 2011, Chen and Klein 2012). This restric-tion results in serious difÞculties in timing insecticidesapplication and has resulted in excessive chemical usefor Asiatic rice borer suppression. This has resulted inserious damage to the environment and consumersÕhealth. Recently, most pyrethroids and organophos-phates, especially the commonly used Thimet, havebeen banned by The Chinese Agriculture Ministryand Insecticides (Public notice: 194,199,322).

The above restrictions have favored the use of sexpheromones in either mass trapping or mating disrup-tion as nonchemical Asiatic rice borer control meth-ods, and make them good choices for avoiding thenegative effects described above. This also makesthem a good Þt for IPM programs which use a com-bination of biological, mechanical, cultural, and chem-ical means to control pests while reducing pesticideresistance and limiting chemical exposure. Mass trap-

1 College of Agronomy, Jilin Agricultural University, 2888 XinchengRd., Changchun 130118, Jilin Province, China.

2 Department of Entomology, The Ohio State University, Wooster,OH 44691.

3 Present address: P.O. Box 1104 Heber, AZ 85928.4 Corresponding author, e-mail: klein.10@osu.edu.5 State Key Laboratory of Integrated Management of Pest Insects

and Rodents, Institute of Zoology, Chinese Academy of Sciences,Beijing 100101, China.

6 Jilin Agricultural Academy of Science, Cai Yu Rd., Changchun130118, Jilin Province, China.

0022-0493/14/1828Ð1838$04.00/0 � 2014 Entomological Society of America

ping and mating disruption with sex pheromones canreduce the pest population by luring males into trapsor permeating synthetic pheromones in the atmo-sphere to disrupt the mating process by decreasing theencounters between males and calling females (Casa-grande 1993, Teng et al. 1993, Carde 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 canreduce pest populations, and have had fair success inthe control of various insect pests, such as leafrollermoths, Argyrotaenia velutinana (Walker) (Novak andRoelofs 1985), the oriental fruit moth (Rice and Kirsch1990, Trimble et al. 2004), codling moth, Cydia pomo-nella L. (Mani and Schwaller 1992), tortricid moths(Stelinski et al. 2004), scolytid beetles (Byers 1999),and other invasive species (El-Sayed et al. 2006). Inaddition, the theoretical basis and modeling the mech-anism of mating disruption and mass trapping havebeen evaluated (Carde 1990; Carde and Minks 1995;Miller et al. 2006a,b; Byers 2007, 2008).

An effective attraction radius (EAR) is a primaryparameter in mass trapping and mating disruptiontests. Once an optimal EAR has been established, malemoths can be effectively inßuenced by the dispenserplume or competitively attracted to pheromone dis-pensers rather than calling females (Daterman et al.1982; Carde 1990; Mani and Schwaller 1992; Stelinskiet al. 2004; Miller et al. 2006a,b; Byers 2009).

Field trials have been conducted for both masstrapping (Beevor et al. 1990, Tatsuki 1990, Kondo andTanaka 1991, Casagrande 1993, Kondo et al. 1993, Suet al. 2003, Chen et al. 2006, Zheng 2007) and matingdisruption of Asiatic rice borer (Gaston et al. 1967,Carde and Minks 1995). In addition, mating disruptionhas been the primary choice for Asiatic rice borermanagement in Spain (Casagrande 1993, Howse1998). In Jilin Province in northeastern China, masstrapping was conducted on 90,000 ha (or �1% ofÞelds) in 2011, and on �1,000,000 ha in 2013. However,no information is available from China on the optimalEAR for mass trapping or mating disruption. There-fore, various dispenser densities were tested for masstrapping and mating disruption from 2011 to 2013 todetermine the optimal densities of dispensers.

The Asiatic rice borer sex pheromone was Þrst iden-tiÞed as a two-component blend of (Z)-11-hexadece-nal 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 stabiliz-ing agent butylated hydroxytoluene (BHT), has beenused in commercial controlled release formulations(Howse et al. 1998).

Our objective here was to compare mass trappingand mating disruption at various dispenser densitieswith traditional management relying on insecticides,on the basis of male captures, egg mass numbers, anddamage control. The hypothesis is that mass trappingor mating disruption gives similar results to chemical

insecticides. If this hypothesis is supported, this tech-nique may be recommended to farmers. Here, thedynamics of adult Asiatic rice borer was also moni-tored with pheromone traps to optimize the timing ofmass trapping and mating disruption applications byreducing the cost of dispensers and their replacement.

Materials and Methods

Field Trial Location and Layout 2011–2013. Testswere conducted in ca. a 17 ha rice paddy in JilinProvince, Shuangyang County, Changchun, China. Acanal, �2.5 m in width and 500 m in length, runsthrough the Þeld cutting it into two parts (14 ha and3 ha), but leaving them equally exposed to Asiatic riceborer adults. The rice Þelds were bounded by corn onthree sides and by a small town on the other. ThoseÞelds and the village restricted movement of Asiaticrice borer from other near by rice Þelds as shown inprevious studies (Chen et al. 2003, 2007; Chen andKlein 2012). In 2011, the larger Þeld was divided into24 plots (83 m in length and 30 m in width), with 12for the four densities of mating disruption (200, 300,400, and 500 dispensers per hectare), and the other 12for mass trapping (20, 30, 40, and 50 dispensers perhectare). Each density was replicated three times with�30 m (a 20 m buffer plus 10 m from the pheromonedispenser to the plot edge) between treatments. A20 m buffer will eliminate interactions between trapsbased on our Þeld results in 2010. The pheromone-baited traps then were set up with 5, 10, 15, 20, 25, and30 m between traps in plots and replicated three times.The results showed that when the distance was �15 mbetween two traps, captures were similar (12 � 1.2b,8 � 0.9c, 14 � 2.3a, 15 � 3.2a, 15 � 2.9a, 15 � 4.1a).This shows that if the distance is ��15 m, there wouldbe no interaction between traps. The smaller Þeld wasdivided into 12 plots (83 m � 30 m), nine for threechemical treatments (Cygon, deltamethrin, and Car-tap), and three for controls. In addition, the plots wererandomized each year between 2011 and 2013.

For mating disruption, dispensers were placementsat 7 by 7, 5.7 by 5.7, 5 by 5, and 4.5 by 5.7 m, and were22 by 22, 18 by 18, 16 by 16, and 14.2 by 14.2 m apartfor mass trapping. Dispensers were Þxed at the top ofrice plants for mating disruption and put in the trapsfor mass trapping on 20 May. Lures were supple-mented on 20 June, 25 July, and 1 September, and thelast set of traps and lures were removed on 10 October.The pheromone load is slightly increased by addingnew lures at �35 d, even though lures last a maximumof 40Ð45 d in the Þeld (R.Z.C., unpublished data). Thedispensers were left in the Þeld to enhance their ef-Þcacy at no additional cost. Tests in 2012 and 2013were similar to 2011, but the lowest rates for masstrapping (of 20) and mating disruption (200) and theCartap insecticide were deleted in the later two yearsbased on the 2011 results. The large part of the 2011Þeld was used in the 2012 and 2013 tests, and the smallpart was used as an untreated control. Pheromoneapplications were 3 July, 8 August, and 13 Septemberin 2012, and 27 June, 2 August, and 9 September in

October 2014 CHEN ET AL.: PHEROMONE SUPPRESSION OF ASIATIC RICE BORER 1829

2013. Assessments of traps and lures were conductedevery 3 d after application.Sex Pheromone and Chemical Insecticide. The

pheromone dispensers for mass trapping and moni-toring were green rubber septa impregnated with 0.2mg of the synthetic sex pheromone (Z11Ð16Ald; Z13Ð18Ald; Z9Ð16Ald, 48:6:5) at 95% purity, with n-hexaneas a solvent (Cork 2004), and with 5 mg for matingdisruption. The mass trapping lures were producedand provided by the fourth author (S. C. -F.). Matingdisruption lures were from Pherobio Technology Co.Ltd. (Puandian Road 206, Beijing China) and had aniron hook placed in its bottom (1.2 cm in length withan elliptical sharp end at 0.3 cm) for Þxing septasecurely in the rice canopy. The bell shape of the septaprovided 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 136100, China), at6 g/liter were applied on 13 July in 2011, and only thelater two on 8 July 2012 and 4 July 2013 (Fig. 1),followed by two more sprays at 4-wk intervals (Chenet al. 2003, Tao et al. 2006, Chen and Klein 2012). Theinsecticides were applied at �230 liters/ha at 0.6 MPawith a knapsack sprayer (model: M9w-315207, BeijingZhongyuan ScientiÞc Company, Beijing, China),equippedwitha swirlnozzle(BJ64348ChengduDensitySwirl-nozzle ScientiÞc Company, Chengdu, China).Application Timing. Population Dynamics. An au-

tomatic water-supplemented pheromone trap (Chenand Klein 2012; Chen et al. 2012, 2013) was used toassess male moth activity as a trigger for mass trappingand mating disruption in the three years, to comparemoth populations between 2011, 2012, and 2013, andto evaluate the possible carry-over effect of 2011 ap-plications. Nine traps were divided into three groupsand placed diagonally in the control plots from 1 Mayto 30 October during the three years. All plots had thesame rice variety (Jinongda 19), as well as weather,water, and soil conditions, and had been planted withthe same rice cultivar for �20 yr. Both the overwin-tering and Þrst-generation Asiatic rice borer com-

monly emerged in these Þelds. Traps were mountedon 1.2-m bamboo sticks with the trap bottom 60Ð100cm above ground (at least 10 cm above the rice can-opy), and placed 20 m apart to give �7.5 mg of pher-omone per hectare based on previous work (Sheng etal. 2002, 2003a,b; Chen et al. 2003, 2007, 2013). Trapswere examined and moths removed and counted ev-ery 48 h, and lures were replaced every 5 wk.Correlation Between Captures and Damage Rate.

Based on previous studies, three factors determinedapplication timing: 1) when accumulated capturesreached �16% of the total captures of the overwin-tering Asiatic rice borer moth emergence. This was�2100 per trap in previous studies (2009), and deter-mined tobea reliable standard(Shenget al. 2003a; Jiaoet al. 2004, 2006; Chen et al. 2003, 2007; Chen and Klein2012); 2) when the linear correlation between cumu-lative captures and dead shell plants is �2% (larvae boreinto thestem,causingthe inner leaf to turnbrownishandwilt, thus creating a dead shell plant; Chen and Klein2012); and 3) when daily captures equal those from thepastsixdays.Thesimultaneousoccurrenceofthesethreefactors triggers the Þrst application.

To help establish the linear correlation above, apaddy (�0.5 ha) located at the 2011Ð2013 Þeld site wasselected in 2009, and three traps were set out. Asiaticrice borer adults were counted and removed dailyfrom 1 May to 1 October. When the cumulative cap-tures per trap exceeded 200 moths, the egg masses anddead shell rates were investigated 5 and 15 d later forestablishing a correlation between cumulative cap-tures and % dead shells.Evaluation of Treatment Efficacy. Treatment ef-

Þcacy of both mating disruption and mass trapping wasdetermined by counts of egg masses, captures of malemoths in pheromone-baited assessment traps, larvalsampling, and crop damage. Although the absence ofegg masses and trap catches are good indications atechnique is effective, the percent of dead hearts anddead heads found in each treatment provides the bestassessment (Howse et al. 1998, Sheng et al. 2003a,Chen et al. 2007, Chen and Klein 2012).

Fig. 1. Captures of C. suppressalis from pheromone traps in control plots, 2011Ð2012.

1830 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 107, no. 5

Egg Masses. Four 10-m2 areas were randomly se-lected from treated and control plots, and Asiatic riceborer egg masses were counted on 400 tillers diago-nally across each area. Sampling was done on 1, 10, 20,and 30 July. The average number of egg masses per 100tillers was calculated and pooled over the season foranalysesPheromone Trap Captures. Three pheromone traps

per plot were placed diagonally across the treatmentsresulting in 24 traps in both mating disruption andmass trapping plots in 2011and 18 traps in 2012, plus 12traps in both chemical and control plots in 2011 and 9traps in 2012Ð2013. Captures in treatment and controlplots were compared to assess the treatment efÞcacy.Reductions of moth catches in mass trapping and mat-ing disruption treatments, compared with capturesfrom insecticide-treated plots also indicated efÞcacy.Mass trapping efÞcacy was established as follows: %Control � (average catches per treatment trap minusaverage catches per control trap, controls are the non-treated 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 caused2.5% yield loss, 1% white heads caused 4.0% loss, and1% dead hearts or dead heads resulted in 6.4% loss (Liu1990, Bandong and Litsinger 2005). These damages arealso the main cause for the rice productions losses inChina and the best measure available (Sheng et al.2003a, Chen et al. 2007, Chen and Klein 2012). Here,plantdamagewasevaluated in lateSeptember2011,byselecting �800 tillered rice plants at random from apile of harvested plants from each trial plot (Chen andKlein 2012). Damage was established from whiteheads and dead heads, and the quantity and locationof 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 thedata. After transformation, data were analyzed byRMANOVA using SAS software (version 9.1 2003),followed by TukeyÕs test to establish statistical differ-ences. Captures, plant damage, egg masses, larval sam-

ples, and controls were the variables, and accumulatedcaptures and the dead shells were the interactionstested in the TukeyÕs test.

To test the correlation between captures and dam-age rate, data of the captures and the dead shell fromthe season were each pooled, giving 10 pairs of datafor the correlation formulation. R2 was determinedand thePvaluewasobtainedbyTukeyÕs test.Formeanegg mass reductions, plant damage control, larval con-trol, and capture reductions, data from 2011 to 2013were pooled and transformed by arcsine (x) for an-alyzing with RMANOVA, followed by TukeyÕs test.

Results

Application Timing. Capture Data. The Þrst over-wintering moths were captured in late May, and thecaptures steadily rose for �3 wk to a peak, and thendropped (Fig. 1). Following an increase to 50Ð60moths per day ca. 30 July, captures quickly dropped tosingle digits. Between mid-August and mid-Septem-ber, a new, but smaller, Asiatic rice borer generationwas captured.

On 20 June, 3 July, and 27 June, 2011Ð13, capturesaveraged 56 � 3.3, 46 � 5.4, and 49 � 3.8 per day,respectively. In these three years, this was ca. 3� theprevious six days captures and indicated a trigger fortreatments had been met.Correlation Between Captures and % Dead Shell.

The mean captures of Þrst-generation Asiatic riceborer were 2,038 per trap (CV � 0.14) over that ßightperiod in 2009. Similar numbers of moths (1,969, 2,000,and 2,096) were captured during this study in 2011,2012, and 2013. Between 1 May and 30 October, asigniÞcant correlation between cumulative capturesand 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 thresholdswere reached. By 11, 18, and 15 June, 2011Ð2013, 16%(315, 320, and 331 moths) of the Þrst generation werecaptured. Taking into consideration the damagethresholds in 2011Ð2013, plus the other two factors,applications were made at the critical moth emer-

Fig. 2. Linear relationship between cumulative captures of C. suppressalis and % dead shell of rice 2011.

October 2014 CHEN ET AL.: PHEROMONE SUPPRESSION OF ASIATIC RICE BORER 1831

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 insecti-cide-treated plots in 2011Ð2013 (Fig. 3), the 200 dis-pensers per hectare mating disruption plots (AV: 8.6),compared with the 300, 400, and 500 dispensers perhectare mating disruption (AV: 1.9, 1.7, 1.3), and 30, 40and 50 dispensers per hectare mass trapping treatedplots (AV: 1.7, 1.6, 1.6) in 2011Ð2013. Egg masses werereduced by the other pheromone treatments, signiÞ-cantly so in the 500 dispensers per hectare matingdisruption, and 50 and 40 dispensers per hectare mass

trapping treatments from the insecticide and otherpheromone-treated plots. Slightly reduced numbersof 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 trapscapturedmanymoths in thechemicaltreatments, and even more in the controls, but thedifferences were not signiÞcant (Table 1). During thewhole growing season, average catches were reducedwith all the mass trapping and mating disruption den-sities. Average catches from both generations in thetwo higher mass trapping and mating disruption plots

Fig. 3. Egg mass reduction of C. suppressalis 2011Ð2013.

Table 1. Captures of male rice stem borer 2011–2012

Plots

Captures per trapÑ% reduction

First generation Second generation

% reduction % reduction

2011 2012 2013 Average 2011 2012 2013 Average

Mass trapa

20/ha 65.5 � 4.3d 65.5 � 4.3d 67.4 � 8.8d 67.4 � 8.8c30/ha 84.3 � 3.2b 80.2 � 8.7b 84.5 � 7.9b 83.0 � 5.7b 78.0 � 5.9c 80.2 � 9.9b 81.3 � 8.6b 79.8 � 6.9b40/ha 90.3 � 5.5a 88.4 � 6.9a 89.8 � 8.5a 89.5 � 9.4a 87.5 � 7.3a 85.4 � 6.8a 86.9 � 7.4a 86.6 � 8.7a50/ha 89.4 � 4.8a 87.5 � 7.5ab 90.3 � 9.6a 89.1 � 7.3ab 86.9 � 5.5a 85.4 � 10.8a 88.7 � 4.9a 87.0 � 5.9a

Mating disb

200/ha 61.9 � 11.3d 61.9 � 11.3c 65.5 � 4.1d 65.5 � 4.1c300/ha 72.9 � 9.8c 80.5 � 8.5b 84.3 � 11.3b 80.9 � 6.3b 76.6 � 5.8 80.0 � 9.3b 81.3 � 7.6b 79.3 � 7.9b400/ha 80.8 � 6.6b 84.3 � 7.3b 87.6 � 7.3ab 84.2 � 7.1b 84.5 � 8.2ab 85.8 � 8.7a 86.4 � 9.8a 85.6 � 4.3ab500/ha 84.1 � 5.9b 85.2 � 11.4ab 89.9 � 4.9ab 86.4 � 6.4ab 81.1 � 5.7bc 87.9 � 9.2a 88.9 � 9.2a 86.3 � 7.6a

InsecticideCygon 8.9 � 1.3e 21.6 � 8.2c 10.3 � 2.7c 13.6 � 3.7d 19.5 � 3.4e 9.0 � 2.3c 9.5 � 1.3c 12.6 � 2.5dDeltamethrin 7.6 � 2.1e 9.2 � 1.9d 5.5 � 02c 7.4 � 1.7e 15.6 � 2.2e 7.6 � 1.5c 6.4 � 1.8 6.5 � 1.3deCartap 2.2 � 0.3e 2.2 � 0.3f 3.3 � 0.6e

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: F10,22 � 36.44, P � 0.0001; 2012: F7,16 � 107.9, P � 0.0001; 2013: F7,16 � 99.6, P � 0.0001; average: F10,22 � 49.3, P �0.0001) and the second generation (2011: F10,22 � 124.5, P� 0.0001; 2012: F7,16 � 19.22, P� 0.0001; 2013: F7,16 � 36.9, P� 0.0001; average: F10,22 �101.8, P � 0.0001). Numbers in a column followed by the same letter are not signiÞcantly different (0.01%).aMass trapping.bMating disruption.

1832 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 107, no. 5

were signiÞcantly less than the other pheromonetreatments (Table 1). This correlates with controlobtained where 50 dispensers per hectare mass trap-ping and 400 and 500 dispensers per hectare matingdisruption provided �85% control, followed by 40dispensers per hectare mass trapping and 300 dispens-ers per hectare mating disruption (�80%) and 30dispensers per hectare mass trapping (�79%) in bothgenerations 2011Ð2013 (Table 1). Both 40 and 50 dis-pensers per hectare for mass trapping, and 400 and 500dispensers per hectare for mating disruption providedsigniÞcant reductions in moths captured when com-pared 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 hect-are, and the insecticide treatments with Cygon andDeltamethrin in 2011 (0.83, 0.80, 0.90, 0.88, 1.11, and1.15, respectively) than mass trapping at 20 and 30dispensers per hectare, or mating disruption at 200 and300 dispensers per hectare (1.96, 1.7, 2.55, 2.29, re-spectively), with no signiÞcant difference betweenthese latter treatments (Table 2). Mass trapping atlower rates had more damage in these three years. Thelowest rate of mating disruption and the control hadthe highest damage. SigniÞcant differences in damagewere observed between the three treatment groupswhen treatment types were pooled for analyses, butthere were no signiÞcant differences within thegroups. Overall, 40 and 50 dispensers per hectare masstrapping, 400 and 500 dispensers per hectare matingdisruption, and the insecticide provided ca. 80Ð89%damage reduction in 2011Ð2013 (Fig. 4).Comparison Between 2011, 2012, and 2013 Popula-tion Dynamic Pattern. High captures of Asiatic riceborer were recorded in the control area from 15 May

to 8 August, 2011 (Fig. 1), but trap catches per plotwere relatively lower in 2012 and 2013 during the sametime (Fig. 1). In 2011, average captures per assessmenttrap that represent the average moth population in thecontrol were 17 � 1.3 in the Þrst generation and 10 �2.1 in the second, while in 2012 and 2013 captures inthe same plots were 13.9 � 3.2 and 12 � 2.8 and 12 �1.9 and 8 � 1.2, respectively. The population patternsfor the two years closely match from mid-August to 7October, suggesting that a negative population effectfrom any source had dissipated by the second gener-ation of Asiatic rice borer, whereas the Þrst generationpopulation 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 ofinsecticides (Gao et al. 1987, Qin et al. 1991, Direc-torate of Rice Research [DRR] 2004, Chi et al. 2005,Litsinger 2009). There have been previous studies onusing sex pheromone as mating disruption techniquesfor Asiatic rice borer control, especially in Europe byCasagrande (1993), Howse (1998), and Alfaro et al.(2009), which encouraged us to try to gain similarcontrol in China, but with less pheromone and moreconvenient dispensers. This work was also stimulatedby studies against other Lepidoptera pests. For exam-ple, Witzgall et al. (2008) and Stelinski et al. (2008,2013) successfully used red rubber septa as sex pher-omone dispensers at densities of 35, 215, and 1100dispensers per hectare, with �1.5 g (AI)/ha to controlpests such as the citrus leafminer, Phyllocnistis citrellaStainton (Lepidoptera: Gracillariidae). In addition, Suet al. (2003) also used rubber septa in successful mass

Fig. 4. Mean plant damage, larval control, and capture reduction in various treatments 2011Ð2013.

October 2014 CHEN ET AL.: PHEROMONE SUPPRESSION OF ASIATIC RICE BORER 1833

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1834 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 107, no. 5

trapping in China, and Yang et al. (2001) and Wang etal. (2011) controlled Asiatic rice borer with matingdisruption, but they did not use rubber septa for pher-omone release.

In this study, three applications of pheromones formating disruption with 400 and 500 dispensers perhectare provided comparable control to chemical andused only 7.5 and 6.0 g of pheromone per hectareduring the entire growing season (2.5 g/ha per appli-cation with three applications). These doses are prob-ably less than that used by Casagrande (1993) andsimilar to that used by Alfaro et al. (2009; �6.4 g/ha)for Asiatic rice borer control in Spain. With all of theinteracting factors in such Þeld tests, it is possible thatlack of signiÞcant differences between treatmentsmay be due to a lower power in the evaluations, whichmay make selected results somewhat equivocal. How-ever, it does not change the basic Þndings of successfulsuppression of Þeld populations at the higher ratestested.

We used a lower dose in the Þeld, and gained com-parable control to that of Casagrande and Alfaro et al.for the following possible reasons: First, rice onlygrows in northeastern China from early June to earlyOctober and the long cold winter results in less thantwo full Asiatic rice borer generations a year. In ad-dition the second generation in China is considerablysmaller than the Þrst (Fig. 1), resulting in much re-duced second generation pressure and damage (Chenet al. 2003, 2007; Sheng et al. 2003a; Chen and Klein2012). Second, we used rubber septa dispensers thatprobably released pheromone over a longer Þeld life,and were supplemented with new dispensers. Previ-ous studies (Su et al. 2001, Sheng et al. 2002, Jiao et al.2003) showed rubber septa still had �37% of theirinitial pheromone activity after a yearÕs storage at 20Cand its Þeld life can be six weeks to two months.Additional low-load septa were added twice duringthe tests, rather than removing septa from the traps.Based on the above observations, the older septawould have provided additional pheromone to thenewer septa for mating disruption action. More im-portantly, pheromone trapping probably works well intemperate climates like northeastern China whereonly one rice crop per year is grown moth ßights aresynchronized by generation. In tropical areas, mothsare ßying at various times and distinct generations aredifÞcult to deduce from trapping data or damagecounts. In the tropical areas, Asiatic rice borer is themost highly adapted stem borer worth those climates(Reissig et al. 1986, Litsinger et al. 2006). Special dis-pensers with high pheromone doses have been used inmating disruption studies in some countries. However,mating disruption in northeastern China with 750septa per hectare resulted in 84.9% Asiatic rice borercontrol (Yang et al. 2001). This investigation foundsimilar control with a lower dose per dispenser andreduced dispenser densities. In addition, there is littlewind during the rice growing season in northeasternChina, and this prolongs the septaÕs Þeld life and en-hances the effect of the mating disruption (Sheng etal. 2002, 2003b; Jiao et al. 2003).

Mass trapping with pheromones at 45 dispensers perhectare in Heilongjiang Province (the northernmostprovince in northeastern China) in 2013 provided�80% control (Liu et al. 2013). That density is similarto what was used in this trial. In addition, Wang et al.(2011) used 30 dispensers per hectare in LiaoningProvince (southernmost province in northeasternChina). Because this study on mass trapping trial inJilin Province evaluated 20Ð50 dispensers per hectare,the results indicate 40 dispensers per hectare can berecommended to farmers for mass trapping of Asiaticrice borer in northeastern China.

Crop damage assessment is the best way for showingthe efÞcacy of mating disruption (Karg and Sauer1995, 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 ricedamage was established to obtain an optimal applica-tion time for the important overwintering generationof Asiatic rice borer. Jiao et al. (2004, 2006) reportedthat when the cumulative captures reached 870, therewill be �2% damaged tillers. That coincides nicelywith what was found here, showing our correlationequation is accurate and valid, and can be used innortheastern China. Furthermore, combining thethree factors, i.e., the sharp increase in captures, initialpeak date, and the correlation equation, is a novelmethod to accurately establish application timing.

Moth capture patterns from 2010 and 2011 wereshown and discussed by Chen and Klein (2012, Fig. 2).The captures for all three years were very similar andidentiÞed the important Þrst generation peak as mid-June, indicating the best time for treatments. Histor-ically in northeastern China, the Asiatic rice borer Þrstappears in mid-May, and pheromone applicationswere started ca. 25Ð30 May (Sheng et al. 2003a; Chenet al. 2007, 2010). Results here showed that phero-mone application could be applied before peak ßight,ca. 20Ð30 June, when the damage threshold is reached,therefore saving one entire application of lures. Thissaves signiÞcant lure and application costs, especiallyin mating disruption treatments, while still obtainingacceptable control with lower pheromone costs.

Compared with chemical insecticides, pheromonesprovide obvious advantages. Application of phero-mones for managing stem borers provides farmerswith crop protection that is user and environmentallyfriendly. In addition, pest reductions may last morethan one season which is consistent with previouswork 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. Thisprevents the need for treating the second-generationmoths in northeastern China.

Acknowledgments

We thank the Changchun Government and Jilin Govern-ment Fund on sex pheromone Asiatic rice borer Control,13NK19, 20130411005XH, with special thanks to the Bureauof Foreign Experts Affairs (BFEA) of Jilin Province for Asiaticrice borer control. KleinÕs trips to China were supported by

October 2014 CHEN ET AL.: PHEROMONE SUPPRESSION OF ASIATIC RICE BORER 1835

Fundament Numbers: L20122200014-2012 and L20132200019-2013. We also thank the JEE reviewer and editor for theirconstructive suggestions.

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Received 7 April 2014; accepted 5 August 2014.

1838 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 107, no. 5