Mass Trapping Popillia quadriguttata Using Popillia japonica (Coleoptera: Scarabaeidae) Pheromone and Floral Lures in Northeastern China Author(s): Ri-zhao Chen, Michael G. Klein, Qi-yun Li, and Yu Li Source: Environmental Entomology, 43(3):774-781. Published By: Entomological Society of America URL: http://www.bioone.org/doi/full/10.1603/EN13319
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CHEMICAL ECOLOGY
Mass Trapping Popillia quadriguttata Using Popillia japonica (Coleoptera: Scarabaeidae) Pheromone and Floral Lures in Northeastern China RI-ZHAO CHEN,1 MICHAEL G. KLEIN,2,3,4 QI-YUN LI,5
AND
YU LI1
Environ. Entomol. 43(3): 774Ð781 (2014); DOI: http://dx.doi.org/10.1603/EN13319
ABSTRACT Popillia quadriguttata (F.) has caused extensive damage to ⬇20 families and 25 species of plants in Asia, especially in China and Korea. Adult feeding causes serious damage to soybean leaves, and larvae develop on the roots of soybean, turf, and horticultural crops. As Japanese beetle (Popillia japonica Newman) lures have been used for trapping P. quadriguttata in a previous study, mass trapping this pest with various densities of the Japanese beetle pheromone, Japonilure, and ßoral lure, alone and in combination, were carried out during 2012Ð2013 in a northeastern China soybean Þeld. Mass trapping in 2012 with Japonilure gave the best results with 72 and 75% adult and larval reduction, respectively. In 2013, mass trapping (30 traps per hectare) with Japonilure, ßoral lure, or the combination resulted in a 93, 70, and 74% reduction of adults trapped, and a 90, 77, and 93% reduction of overwintering larvae, respectively. In addition, Þeld tests showed that almost twice as many beetles approached the lure combination compared with the ßoral lure alone, and the pheromone residual was ⬇80% of the initial dosage after 30 d. Because reduction of overwintering larvae is the most critical parameter indicating treatment efÞcacy, the results here indicate that the lure or lure combinations can be recommended for use by Chinese soybean farmers. KEY WORDS Japanese beetle lure, crop damage, adult and larval control
Soybeans are one of ChinaÕs most important crops, especially in Heilongjiang and Jilin provinces, and are grown on ⬇1.0 ⫻ 107 ha, representing 10% of the total crop area. More than 20 insects cause serious damage to soybeans throughout the world (Hao and Ren 2003). Popillia quadriguttata (F.) is an important species within the complex of soybean insect pests, and is regarded as the dominant species in soybean Þelds and turfgrass in Liaoning province (Sang 1979). This scarab beetle is widely distributed throughout China, especially in the northeast region, which has been the primary Chinese soybean production region for the past 60 yr (Zhang et al. 1981, Wang et al. 1999, Hao and Ren 2003, Fang 2007). In both China and Korea, P. quadriguttata was long misidentiÞed as the Japanese beetle, Popillia japonica Newman, because of their extremely similar morphology. Consequently, 20th century references to the Japanese beetle in China and Korea (Fleming 1972) were in fact P. quadriguttata (Ping 1988, Ku et al. 1999). In addition, studies by Kim et al. (1990) and 1 College of Agronomy, Jilin Agricultural University, 2888 Xincheng Road, 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 89528. 4 Corresponding author, e-mail: [email protected]. 5 Jilin Agricultural Academy of Science, Cai Yu Rd., Changchun 130118, Jilin Province, China.
Reed et al. (1991) noted a common scarab species in Korea as Popillia uchidai Niijima and Kinoshita. That species has been reexamined (Ku et al. 1999) and determined to also be P. quadriguttata. P. quadriguttata has also been reported from Russian and Vietnam (Reed et al. 1991, Lee et al. 2007). Known as a polyphagous pest, adults of P. quadriguttata have been shown to feed on ⬇20 families and 25 species of plants in China and Korea (Sang 1979, Lee et al. 2002). Severe damage occurs to fruit trees, ßowers, ornamental, and horticultural plants as well as other important agricultural crops (Zhang et al. 1981, Luo and Zhang 1981, Tan et al. 1998, Wang 2001, CAB International [CABI] 2002). Adult feeding causes damage to soybean ßowers, buds, immature leaves, and shoots, whereas larvae feed on plant roots. This insect has resulted in ⬇1% yield losses of Chinese soybeans per year (Wang and Zheng 2006, Fang 2007). In the recent past, feeding by P. quadriguttata has caused signiÞcant crop losses, especially on turfgrass, ßower crops, soybeans, and tree fruit (Qu et al. 1993, Wang 2001, State General Administration of Quality Supervision, Inspection and Quarantine of the PeopleÕs Republic of China [AQSIQ] 2003a,b, Australian Government, Department of Agriculture, Fisheries and Forestry 2004, Fang 2007). In South Korea, this scarab is the dominant pest on golf courses, as adults feed on ornamental plants and larvae feed heavily on turfgrass roots (Reed et al. 1991, Lee et al. 2007). As with the
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Japanese beetle, turf damage is often made worse by birds and mammals digging up the turf searching for larvae to eat. Therefore, P. quadriguttata will likely cause increased destruction of turf, as golf courses and green areas are developed in China. With increases in the Chinese economy, there will likely be a greater demand for ornamental plants, turfgrass, tree fruit, and agronomic production, all of which will be negatively impacted by P. quadriguttata larva or adult feeding. Although the parasitoid Tiphia vernalis Rohwer has been reported to parasitize P. quadriguttata in Korea and China, and P. japonica in Japan and the United States (Clausen et al. 1927, 1932, 1933; Fleming 1968, 1972; Sang 1979; Ding and Fu 2000; Reding and Klein 2001), pest suppression from biological control is insufÞcient for either insect. In China, chemical insecticides, including dipterex (⫽ trichlorfon), benzene hexachloride (⫽ lindane), and Carbofuran (⫽ Furadan) remain the mainstay of P. quadriguttata control in Þeld crops (Wang 2001, Fang 2007). However, chemical applications remain problematic because of environment contamination, increasing pest resistance, and an overuse of chemicals. Because there is an increasing awareness and value of organic agricultural products in China, there is a corresponding increased emphasis on environmentally friendly pest control measures. Finally, some previously popular chemicals, such as benzene hexachloride and Carbofuran noted above, are now being prohibited in China. There is also an increasing realization that chemical sprays damage pollinating insects in crop ßowers and may negatively impact crop yields. Sex lures (pheromones) and ßoral lures (kairomones) can be used in pest management by providing early detection, mass trapping, lure and kill measures, and mating disruption of pest insects (Weinzierl et al. 2012). In addition, several scarabs have been attracted to the P. japonica sex attractant (JaponilureÑ[(R, Z)-5-(I-decenyl) dihydro-2(3H)-furanone)ÑÞrst described by Tumlinson et al. (1977)), and many respond to the ßoral lures (Ladd et al. 1981; PEGÑ phenethyl propionate, eugenol, and geraniol [3:7:3]), or the combination (Chow 1986, Donaldson et al. 1986, Klein and Edwards 1989, Reed et al. 1991, Li et al. 1995, Cherry et al. 1996, Crocker et al. 1999, Chen et al. 2001, Toth et al. 2003, Lee et al. 2007). Attraction of P. quadriguttata to the P. japonica lures (Reed et al. 1991, Li et al. 1995, Lee et al. 2007, Chen et al. 2013b) provides an opportunity to exploit commercially available lures to protect Chinese crops from P. quadriguttata. The objectives of this study were to evaluate the use of traps baited with Japonilure plus ßoral lures to evaluate the effect of trapping on P. quadriguttata by observing soybean damage and overwintering larval populations. Materials and Methods Experiments were conducted at the Jilin Agricultural University experimental farms and campus in 2012, and elsewhere in Shuangyang county in 2013, for Þeld trail at Changchun, Jilin Province, northeastern
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China (GPS coordinates: 125⬚ 26⬘, 43⬚ 23⬘), during July and August of both years. During this time, Tre´ ce´ Japanese beetle traps and lures were used (Tre´ ce´ , Inc., Adair, OK). The Tre´ ce´ Japanese beetle trap is made of two perpendicular, yellow, high-impact styrene vanes and a plastic bag that forms a funnel and beetle receptacle (Chen et al. 2013b). The ßoral lure was contained in a felt pad in 2012 (Chen et al. 2013b) and a high void polyethylene disk in 2013 (Klein and Edwards 1989), either held in a solvent-resistant plastic pack. The sex pheromone (1 mg) was placed in a rubber septum held in its own compartment in the same pack, and attached to adjoining trap vanes (Chen et al. 2013b). Control Efficiency. Trial and Trap Layout. In 2012, tests were conducted in a 3-ha soybean Þeld bounded by corn on all sides. The tall corn reduced the movement of P. quadriguttata from other local soybean Þelds. The Þeld was divided into 12 plots for trapping at ⬇10 traps per hectare for each of three lure treatments (ßoral lure and Japonilure, ßoral lure or Japonilure alone, and an unbaited control). In 2013, tests were conducted in ⬇5.5-ha soybean Þeld, divided into 30 plots (⬇0.17Ð 0.2 ha) for the three densities of mass trapping (10, 20, or 30 traps per hectare) baited with the same combinations as 2012. In both years, the trial Þeld had never been previously trapped. Each lure treatment was replicated three times with lure-baited traps placed in a randomized complete block design. There were ⬇25 m between plots as buffer to minimize the interaction between baited traps. However, because traps were placed inside the plot lines, the real distance from a trap in one replication to a trap in adjoining plots was ⬍40 m. In addition, the corn in the buffer and surrounding Þelds reduced the movement of adults and attractant components between plots. Also, at several random points in the buffer, no lure components were detected on pieces of absorbent foam placed 48 h earlier to check for chemicals in the atmosphere. Traps were secured to wooden poles so the upper edge of the funnel was ⬇75 cm above the ground. In both years, the investigations were conducted from 1 July to 30 August, and the lures were replaced on ⬇1 August. Evaluation of Treatment Efficacy. Lure-trap efÞcacy was compared with the untreated control plots for: 1) crop damage, 2) number of adults remaining on soybean leaves, and 3) overwintering larval populations. The Þrst two indices can be a good indication that the trapping was effective, but the overwintering larval assessment provides the conclusive proof. Crop Damage Assessment. Soybean leaf damage in the Þeld from P. quadriguttata was assessed on ⬇29 August in both years by randomly selecting 10 soybean plants in each lure treatment plot. Leaves from each plant were returned to the laboratory, scanned (HP Scanjet 200, Hewlett-Packard Co., Palo Alto, CA), and damage accessed with Photoshop software (version 7.0, Adobe Inc., San Jose, CA). Damage values were: 0 (no damage), 1 (up to 1% leaf eaten), 2 (2Ð4% leaf eaten), and 3 (4Ð6% leaf eaten). Generally, when damage reaches ⬇4%, soybean yield will be reduced by ⬎3%.
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Table 1. Control of P. quadriguttata in soybean fields treated either with 10 baited traps per hectare or in an untreated control in Changchun, Jilin Province, China in 2012 Mean ⫾ SE per plot Type of lure
Beetles captured (male/female) Treated
Adults on foliage (male/female)
Control
Treated
% reduction
Control
Larval mean
Adult (male/female)
Larvae
71.9a/0.8b 33.1b/28.8a 25.7b/26.3a
75.3a 49.0b 42.5b
97.4 ⬍ 0.001
67.5 ⬍ 0.001
Japonilure 185 ⫾ 21a/13 ⫾ 2c 83 ⫾ 6c/353 ⫾ 33a 401 ⫾ 10c Floral lure 56 ⫾ 12b/65 ⫾ 7a 198 ⫾ 13b/255 ⫾ 24b 830 ⫾ 64b a Combination 46 ⫾ 9b/42 ⫾ 8b 220 ⫾ 21b/264 ⫾ 17b 937 ⫾ 26b Control 3.4 ⫾ 1/2.3 ⫾ 0.2 296 ⫾ 25/358 ⫾ 36 1630 ⫾ 31a F (4, 10)/P.value 112.3 ⬍ 0.001 92.3 ⬍ 0.001 156.4 ⬍ 0.001
Numbers in a column followed by the same letter are not signiÞcantly different, LSD test (0.001). a Combination of Japonilure and ßoral lure.
Protection values were based on the damage value in the control minus the damage value in the treatments. Adults on Foliage and Overwintering Larvae. Adults attracted to plants, but not into traps in each lure treatment, were counted and recorded from 10 random soybean plants every 5 d from 2 July to 12 August in both years. Because overwintering larvae are commonly found ⬇30 cm deep under the ground in October, larvae were counted and recorded ⬇10 October by digging 1.5-m2 holes to a depth of ⬇30 cm in 10 randomly selected areas in trapped and untrapped soybean plots. Scarab Response to Lures. These observations were inspired by the research of Stelinski et al. (2013). Scarab beetle approaches to randomized dispensers during JulyÐAugust 2013 were recorded in each treatment. Each treatment was simultaneously observed for 60 min by nine people. The number of P. quadriguttata orienting to a dispenser, duration of visit near the dispenser(s), and closest approach of adults relative to the dispenser(s) were recorded. Observations were conducted on three different sunny- and low-wind days. Wind speeds were estimated every 5 min by a wind velocity indicator (HHF2005HW, 1698 Yi Shan Road, Unit 102, Min Hang District, Shanghai 201103, China). It was considered a valid observation period if wind speeds were ⬍0.03 m/s during the 60 min. The sex of beetles was not determined because of the nature of observations.
Lure Release Rates. In 2013, the amount of the Tre´ ce´ pheromone and Floral Lure components (phenethyl propionate, eugenol, and geraniol [3:7:3]) present after 5-d intervals in the Þeld was monitored. This was accomplished by putting 18 dispensers of each type of lure and then removing 3 of them for residue assessment every 5 d from the Þfth to thirtieth day after the exposure. The details on identiÞcation of components were similar to those by Chen et al. (2013a). The exceptions were that dispensers were stored at ⫺22⬚C, and ethyl phenethyl was used as the internal standard for phenethyl propionate, acetone for (R, Z)-5- (I-decenyl) dihydro-2(3H)-furanone, phenol for eugenol, and butyl acetate for geraniol. Data Analysis. During the 2-mo investigations, all beetles were taken to the Agricultural Insects Research Laboratory at the Jilin Agricultural University, Changchun, where they were identiÞed and counted. The number of adults on each soybean plant was recorded at eight different times and pooled. Adult captures (male or female), the number of adults in scarab response observation, overwintering larvae, and crop damage data were transformed by log (x ⫹ 1) to normalize the data. After transformation, data were analyzed by one-way analysis of variance, followed by a least signiÞcant difference (LSD) test to establish statistical differences.
100 adult reduction n
Mean value
80 60
a
a
overwintering larva reduction ductio in
a
a
a a
a
b
b
b c
b
b
c
b
b
b
40
b 20 0 J- J+F- F2012 2012 2012
J- J+F- F2013 2013 2013
J- J+F- F2012 2012 2012
J- J+F- F2013 2013 2013
J- J+F- F2012 2012 2012
J- J+F- F2013 2013 2013
Treatments
Fig. 1. P. quadriguttata. Percentage reduction of soybean plant leaf damage, adult captures, and overwintering larvae in 2012Ð2013 in Changchun, Jilin Province, China. Data of different density trap treatments of each type of lure were respectively pooled: J, Tre´ ce´ sex attractant (SA); F, Tre´ ce´ ßoral lure (FL); J⫹F, combination SA and FL.
78.1 ⬍ 0.01 66.3 ⬍ 0.01
60.1c/5.3d 92.6a/14.6d 92.6a/14.6d 35.3d/46.7bc 57.6c/53.6b 69.6b/63.7a 28.3d/42.3c 44.2d/49.4bc 74.2b/56.8a
437 ⫾ 26c 253 ⫾ 36d 176 ⫾ 27d 580 ⫾ 54b 460 ⫾ 57c 366 ⫾ 53d 760 ⫾ 48b 223 ⫾ 75d 110 ⫾ 17d 1609 ⫾ 197a 56.4 ⬍ 0.01 76.4 ⬍ 0.01 Control F (9, 20)/p.value
Comba
Floral Lure
10 20 30 10 20 30 10 20 30 Japonilure
Numbers in a column followed by the same letter are not signiÞcantly different (0.001). a Combination of Japonilure and ßoral lure. * Numbers in each treated-control group are signiÞcantly different, LSD test(0.001).
98.3 ⬍ 0.01
283 ⫾ 36*/336 ⫾ 67* 283 ⫾ 36*/336 ⫾ 67* 283 ⫾ 36*/336 ⫾ 67* 283 ⫾ 36*/336 ⫾ 67* 283 ⫾ 36*/336 ⫾ 67* 283 ⫾ 36*/336 ⫾ 67* 283 ⫾ 36*/336 ⫾ 67* 283 ⫾ 36*/336 ⫾ 67* 283 ⫾ 36*/336 ⫾ 67* 283 ⫾ 36/336 ⫾ 67 4 ⫾ 0.6*/3 ⫾ 0.4* 4 ⫾ 0.6*/3 ⫾ 0.4* 4 ⫾ 0.6*/3 ⫾ 0.4* 4 ⫾ 0.6*/3 ⫾ 0.4* 4 ⫾ 0.6*/3 ⫾ 0.4* 4 ⫾ 0.6*/3 ⫾ 0.4* 4 ⫾ 0.6*/3 ⫾ 0.4* 4 ⫾ 0.6*/3 ⫾ 0.4* 4 ⫾ 0.6*/3 ⫾ 0.4* 4 ⫾ 0.6/3 ⫾ 0.4 195 ⫾ 32ab/5 ⫾ 1c 238 ⫾ 37a/12 ⫾ 4c 255 ⫾ 42a/6 ⫾ 4c 85 ⫾ 18c/96 ⫾ 21bc 136 ⫾ 32b/121 ⫾ 23b 122 ⫾ 45b/105 ⫾ 19a 65 ⫾ 13c/72 ⫾ 17c 106 ⫾ 27b/98 ⫾ 21bc 125 ⫾ 31b/154 ⫾ 35a
113 ⫾ 17c/318 ⫾ 77a 21 ⫾ 4d/287 ⫾ 64a 17 ⫾ 3d/302 ⫾ 27a 183 ⫾ 18ab/179 ⫾ 35b 120 ⫾ 22c/156 ⫾ 43bc 86 ⫾ 7d/122 ⫾ 16c 203 ⫾ 38a/197 ⫾ 21b 158 ⫾ 21b/170 ⫾ 18b 73 ⫾ 12d/145 ⫾ 15c
Larvae % reduction
Adult (male/female) Larval mean Control Treated
777
Control
Mean ⫾ SE per plot
Adults on foliage (male/female) Beetles captured (male/female)
Density traps per hectare Type of lure
Table 2.
Control of P. quadriguttata in soybean fields either treated with at one of densities of baited traps per hectare or in untreated control in Changchun, Jilin Province, China in 2013
Results Control Efficacy. In 2012, signiÞcant differences (F ⫽ 112.3,92.3; df ⫽ 4, 10; P ⬍ 0.01) were found in the numbers of adults on leaves and of overwinter larva in soybean Þelds with different Tre´ ce´ lure treatments (Table 1). In addition, beetle trap captures and leaf damage also differed signiÞcantly between those treatments (Fig. 1). With all the lures, reductions of beetles on soybean leaves, and the decrease in overwintering larval populations compared with the unbaited control were highly signiÞcant. The traps baited with Japonilure alone were superior with 71.9% reduction of adults on leaves and 75.3% reduction of overwintering larvae compared with the unbaited control (Table 1; Fig. 1). In comparison to the control, trapping with Japoniture alone, the combination of Japonilure and ßoral lure, and the ßoral lure alone also resulted in very low plant damage (0.62 ⫹ 0.46, 1.38 ⫹ 0.36, and 1.63 ⫹ 0.32; Chen and Klein, unpublished data) and provided 52.18, 47.34, and 39.16% damage reduction, respectively. The plant damage had a generally positive correlation (not statistically determined) with both beetles on leaves and overwintering larval populations (Tables 1 and 2). In 2013, similar to 2012, signiÞcant differences (F ⫽ 98.3,56.4,76.4; df ⫽ 9, 20; P ⬍ 0.01) were found in the numbers of adults on leaves, overwinter larva in soybean Þelds, beetle trap captures, and leaf damage (F ⫽ 167.7; df ⫽ 9, 90; P ⬍ 0.01) with different lures treatment (Table 2; Fig. 1). SigniÞcantly more male beetles were captured with Japonilure at 20 or 30 baited traps per hectare than with 10 baited traps per hectare, whereas the combination of ßoral lure and Japonilure captured signiÞcantly more female beetles at 30 baited traps per hectare (Table 2). Traps baited with Japonilure caught signiÞcantly more total adults, mainly males, followed by the combination of lures and the ßoral lure alone (Fig. 1; Table 2). This resulted in the largest reduction of adult damage and overwintering larvae by Japonilure (Fig. 1), especially male reductions of 92.6% with either 30 or 20 dispensers per hectare (Table 2). Scarab Response to Lures. During the highest period of P. quadriguttata ßight activity (15 July to 5 AugustÑChen and Klein, unpublished data), the number of beetles captured per trap ranged from 8 to 22. SigniÞcantly more beetles (F ⫽ 107.3; df ⫽ 3, 24; P ⬍ 0.01) reached traps with the combination of lures than with Japonilure alone, which exceeded the ßoral lure alone. Almost twice as many beetles approached the lure combination compared with the ßoral lure alone (Fig. 2). The average duration of beetle visits to the traps ranged between 13 and 15 s, and there were no signiÞcant differences in duration of visits between treatments (Fig. 2). The average closest approach ranged between 13 and 15 cm from dispensers and the relative differences were signiÞcant (F ⫽ 121.2; df ⫽ 3, 24; P ⬍ 0.01) between treatments (Fig. 2). The sex of beetles was not obtained because of the inability to identify characteristic sex differences between adults ßying in the Þeld.
72.8c 84.3b 89.6ab 63.9d 71.4c 77.3c 52.8e 86.1b 93.2a
CHEN ET AL.: MASS TAPPING P. quadriguttata IN NORTHEASTERN CHINA
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Fig. 2. Mean total number, approach distance (cm), and visitation time duration (sec) of P. quadriguttata to dispensers in 2013 in Changchun, Jilin Province, China. Data of different density trap treatments of each type of lure were respectively pooled: J, Tre´ ce´ sex attractant (SA); F, Tre´ ce´ ßoral lure (FL); J⫹F, combination SA and FL.
Lure Release Rates. The laboratory bioassay of the lures (Fig. 3) showed that the pheromone was released very slowly from the dispenser. After l5 d., ⬎90% of Japonilure and ⬎89% ßoral lure remained, and both lure residual was ⬇80% of the initial dosage after 30 d. This is consistent with the label description of a 40-d Þeld life. Discussion P. quadriguttata is a serious insect pest in Asia that has caused soybean yields decreases by ⬇5Ð 8% when ßowers are seriously damaged by the beetleÕs feeding (Qu et al. 1993). There are no reports about efÞcient ways to change planting and subsequent ßower dates to avoid economic damage to ßowers from this beetle. Furthermore, the recent increase in Chinese golf
course turf, and ornamental grass, provides an ideal habitat where adults can lay eggs and the larvae can overwinter without disruption by natural enemies or agricultural practices such as tilling. In addition, the grass roots provide P. quadriguttata larvae a highly favorable and sustainable food resource each summer. There are ⬎20 insect species that damage soybean leaves, and several white grub species feed on the soybean roots (Hao and Ren 2003, Xu and Liu 2011). A reduction in soybean plant damage levels can be a good indication that a suppression technique is effective, but reductions of overwintering larvae provide the best proof of control. P. quadriguttata adult damage to leaves causes elliptical holes with the leaf veins, which looks very different from the damage caused by Lepidoptera larvae. Therefore, damage caused by these beetles can be easily assessed and evaluated.
Fig. 3. Percentage residual (a) Japonilure Ð (sex attractant): (R, Z)-5-(I-decenyl) dihydro-2(3H)-furanone and (b) ßoral lure; (PEG) in dispensers after a given number of days in the Þeld in 2013 in Changchun, Jilin Province, China.
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Soybean yield losses have been caused by several pest species including P. quadriguttata, and the soybean pod borer Leguminivora glycinivorella Matsumura (Lepidoptera : Olethreutidae) (Hao and Ren 2003). However, yield loss does not always correlate with pest density. However, the damage this year, and moreover for next year, will correlate with the overwintering larvae density. Therefore, overwintering larvae were used as the best indication for the effectiveness of mass trapping P. quadriguttata. This is the Þrst report of using attractants to mass trap the economically important P. quadriguttata in Asia. These beetles congregate diurnally and feed on ßowers and young leaves, resulting in 5Ð10% soybean yield losses annually, and larval feeding causes mortality to newly planted trees by feeding on developing roots (Wang 2001, Wang and Zheng 2006, Yang and Wang 2008). Therefore, there is need to develop an effective means to reduce the density and damage from these beetles. Using the commercial Tre´ ce´ Japanese beetle traps and lures to capture P. quadriguttata provides an adoptable control tactic that could be implemented by Asian growers. Interestingly, although P. japonica and P. quadriguttata feed on many of the same plants, the latter scarab is not a pest of rose (Sang 1979, Lee et al. 2002), which is one of the highly favored plants of the former (Fleming 1972). If the rose-derived attractant is not important for P. quadriguttata, elimination of the geraniol could make the ßoral lure cheaper. In any event, here in China, mass trapping provided ⬇80% reduction of overwintering larvae. This means the following year pest population will be signiÞcantly decreased, which may lead to lower crop damage without additional treatments. Overall, mass trapping with the Tre´ce´ system can provide a powerful means of early detection, forecasting, and control of P. quadriguttata in northeastern China Þelds. Sex pheromones are an ideal component of integrated pest management programs (Liu and Zhang 2006, Chen and Li 2011, Chen and Klein 2012, Chen et al. 2013a), and are a suggested tactic for moth mating disruption when the proper number of dispensers are placed in Þelds (Stelinski et al. 2008, Witzgall et al. 2008). Information here correlates positively with previous research. In addition, studies have shown an increase in efÞcacy of pheromones by coreleasing pheromones with kairomones (Ladd et al. 1981, Knight et al. 2012, Stelinski et al. 2013). This is often based on food and ßoral lures being attractive to both sexes (Hulcr et al. 2011). Here, traps with Japonilure alone caught more beetles than the combination of sex attractant and ßoral lure, which is in agreement with our previous report (Chen et al. 2013b). The highest reductions of overwintering larvae in both years were found in the plots treated with Japonilure. This may indicate that reduction of males from mass trapping, or confusion of males due to the presence of the sex attractant, resulted in females in those plots not being mated. P. japonica females are normally highly mobile, and could be expected to move between plots and mated. These results indicate that P. quadriguttata females may not be as mobile at these population
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levels. Almost as many females were found on the foliage in the Japonilure plots as in the controls, but the larval population was greatly reduced in the Japonilure treatments. In any event, Japonilure at 30 dispensers per hectare provided greater larval reduction (93.2%) than any other treatments in 2013 (Table 2). This correlates positively with the number of beetles approaching the lures. The movement of female beetles, effects of lures without geraniol, effects of lures on high populations, and the necessity of pure Japonilure need to be investigated further.
Acknowledgments We sincerely thank Tre´ ce´ Inc. for providing the traps and lures used in these studies. KleinÕs trip and the expenses for the Þeld trials were sponsored by the International Cooperation Project between Jilin Agricultural University and The Ohio State University funded by the Bureau of Foreign Experts Affairs (BFEA) of Jilin Province (Fundament number: L20122200014-2012; L20132200019-2013).
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Chen, R.-Z., M. G. Klein, C.-F. Sheng, Y. Li, D.-X. Shao, and Q.-Y. Li. 2013b. Male and female Popillia quadriguttata (Fabricius) and Protaetia brevitarsis (Lewis) (Coleoptera: Scarabaeidae) response to Japanese beetle ßoral and pheromone lures. J. Asia-PaciÞc Entomol. 16: 479Ð484. Cherry, R. H., M. G. Klein, and W. S. Leal. 1996. Attraction of adult Anomala marginata (Coleoptera: Scarabaeidae) to anethole. J. Agric. Entomol. 13: 359 Ð364. Chow, Y. S. 1986. Attractants for two ßower Popillia beetles in Taiwan. Plant Prot. Bull. 28: 133Ð137. Clausen, C. P., J. L. King, and C. Teranishi. 1927. The parasites of Popillia japonica in Japan and Korea and their introduction into the United States, p.56. U.S. Department of Agriculture Bulletin 1429, Washington, DC. Clausen, C. P., T. R. Gardner, and K. Sato. 1932. Biology of some Japanese and Chosenese grub parasites (Scoliidae), p. 27. U.S. Department of Agriculture Technical Bulletin 308, Beltsville, MD. Clausen, C. P., H. A. Jaynes, and T. R. Gardner. 1933. Further investigations of the parasites of Popillia japonica in the Far East, p. 57. U.S. Department of Agriculture Technical Bulletin 366, Beltsville, MD. Crocker, R. L., M. G. Klein, W. Xu, and W. T. Jailon. 1999. Attraction of Phyllophaga congrua, P. crassissima, P. crinite, and Cyclocephala lurida (Coleoptera: Scarabaeidae) adults to selected volatile compounds. Southwest. Entomol. 24: 315Ð319. Ding, J.-Q., and W.-D. Fu. 2000. Insects associated with mile-a-minute weed (Polygonum perfoliatum L.) in China: a three-year-survey report, pp. 225Ð231. In R. S. Neal (ed.), Proceedings of the X International Symposium on Biological Control of Weeds, 4 Ð14 July 1999, Montana State University, Bozeman, MT. Donaldson, J.M.I., T. P. McGovern, and T. L. Ladd. 1986. Trapping techniques and attractants for Cetoniinae and Rutelinae (Coleoptera: Scarabaeidae). J. Econ. Entomol. 79: 374 Ð377. Fang, J.-J. 2007. The damage of Popillia quadriguttata Fabricius on turf and corresponding control practices. For. Shanxi 2: 31Ð32. Fleming, W. E. 1968. Biological control of the Japanese beetle, p. 78. U.S. Department of Agriculture Technical Bulletin 1383, USDA, Washington, DC. Fleming, W. E. 1972. Biology of the Japanese beetle, p. 129. U.S. Department of Agriculture Technical Bulletin 1449, USDA, Washington, DC. Hao, X.-L., and B.-Z. Ren. 2003. The species and distribution of the soybean pests in Jilin Province. J. Jilin Normal Univ. 4: 33Ð36. Hulcr, J., R. S. Mann, and L. L. Stelinski. 2011. The scent of a partner: ambrosia beetles are attracted to volatiles from their fungal symbionts. J. Chem. Ecol. 37: 1374 Ð1377. Kim, S. H., M. H. Lee, J. H. Kim, and M. S. Kim. 1990. Species and seasonal ßuctuation of chafers in pasture. Res. Report RDA (C.P) 32: 64 Ð 69. Klein, M. G., and D. C. Edwards. 1989. Captures of Popillia lewisi (Coleoptera: Scarabaeidae) and other scarabs on Okinawa with Japanese beetle lures. J. Econ. Entomol. 82: 101Ð 103. Knight, A. L., L. L. Stelinski, V. Hebert, L. Gut, D. Light, and J. Brunner. 2012. Evaluation of novel semiochemical dispensers simultaneously releasing pear ester and sex pheromone for mating disruption of codling moth (Lepidoptera: Tortricidae). J. Appl. Entomol. 136: 79 Ð 86. Ku, D.-S., S.-B. Ahn, K.-J. Hong, S.-H. Lee, and J.-I. Kim. 1999. Does the Japanese beetle (Popillia japonica Newman) distribute in Korea or not? Korean J. Appl. Entomol. 38: 171Ð176.
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Ladd, T., M. G. Klein, and J. H. Tumlinson. 1981. Phenethyl propionate: eugenol: geraniol (3:7:3) and Japonilure: a highly effective joint lure for Japanese beetles. J. Econ. Entomol. 74: 665Ð 667. Lee D. W., H. Y. Choo, J. M. Chung, S. M. Lee, and Y.-B. Sagong. 2002. Host plants of Popillia quadriguttata (Coleoptera: Scarabaeidae). Korean J. Appl. Entomol. 41: 15Ð19. Lee D. W., H. Y. Choo, D. R. Smitley, S. M. Lee, H. K. Shin, H. K. Kaya, G. G. Park, and J. K. Park. 2007. Distribution and adult activity of Popillia quadriguttata (Coleoptera: Scarabaeidae) on golf courses in Korea. J. Econ. Entomol. 100: 103Ð109. Li, Z. X., C. Q. Liu, Q. L. Wang, and J. Y. Cui. 1995. Effect of attractants on scarabee. Acta Agric. Boreali-Sinica 10: 153Ð156. Liu, T.-L., and Z.-M. Zhang. 2006. Control efÞcacy of various insecticides and sex pheromone on Asia corn borer, Ostrinia furnacalis Guenee, Lepidoptera: Pyralidae. Shanghai Veg. 3: 71Ð72. Luo, C., and Z.-L. Zhang. 1981. The species and damage of white grubs in the lawn, pp. 312Ð314. In The Fifth International Conference on Biodiversity Conservation and Utilization, July 1981, Beijing, China. Ping, L. 1988. The Popillia of China. Tianze Elldonejo 1Ð71. Qu, Y.-X., X.-H. Gao, Z.-Q. Ma, and X.-Y. Zou. 1993. Studies on the injury equivalency system and mixed act on threshold of main soybean leaf feeding insect pest. Acta Phytophysiol. Sin. 20: 42Ð 48. Reding, M. E., and M. G. Klein. 2001. Tiphia vernalis parasitizing oriental beetle, Anomala orientalis in a nursery. Great Lakes Entomol. 34: 67Ð 68. Reed, D. K., M. H. Lee, S. H. Kim, and M. G. Klein. 1991. Attraction of scarab beetle populations (Coleoptera: Scarabaeidae) to Japanese beetle lures in the Republic of Korea. Agric. Ecosyst. Environ. 36: 163Ð174. Sang, X.-H. 1979. Study on the bionomics and control of Popillia quadriguttata Fabricius. Acta Entomol. Sin. 4: 478 Ð 480. Stelinski, L. L., J. R. Miller, and M. E. Rogers. 2008. 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. 2013. An Attempt to increase efÞcacy of moth mating disruption by coreleasing pheromones with kairomones and to understand possible underlying mechanisms of this technique. Environ. Entomol. 42: 158 Ð166. Tan, S. D., J.-D. Wei, and R.-X. Lan. 1998. Analysis on the similarity of the structure of the litchi and longan pest communities. Guangxi Sci. Tech. Trop. Crops 69: 4 Ð10. Toth, M., M. G. Klein, and Z. Imrei. 2003. Field screening for attractants of scarab pests in Hungary (Coleoptera: Scarabaeidae). Acta Phytopathol. Entomol. Hung. 38: 323Ð331. Tumlinson, J. H., M. G. Klein, R. E. Doolittle, T. L. Ladd, and A. T. Proveaux. 1977. IdentiÞcation of the female Japanese beetle sex pheromone: inhibition of male response by an enantiomer. Science 197: 789 Ð792. Wang, H.-L. 2001. Control of Popillia quadriguttata Fabricius on grape. Agric. Tech. Ext. China 6: 12Ð14. Wang, W., and W.-L. Zheng. 2006. Comparison among four chemical insecticides protecting plums. Hort. N. China 6: 167Ð168. Wang W., J.-Z. Wang, and H.-H. Lin. 1999. A preliminary list of Scarabs (Coleoptera: Scarabaeoidea) from Beijing. J. Beijing Agric. Coll. 3: 15Ð18. Weinzierl, R., T. Henn, P. G. Koehler, and C. L. Tucker. 2012. Insect attractants and traps. University of Florida
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IFAS Extension. Publication ENY277. (http://edis.ifas.uß. edu/pdfÞles/IN/IN08000.pdf) (accessed 17 February 2014). Witzgall, P., L. L. Stelinski, L. Gut, and D. Thomson. 2008. Codling moth management and chemical ecology. Annu. Rev. Entomol. 53: 503Ð522. Xu, S.-M., and X.-R. Liu. 2011. Survey of soybean pests. J. Beihua Agric. Univ. 32: 272Ð275.
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CHEMICAL ECOLOGY
Mass Trapping Popillia quadriguttata Using Popillia japonica (Coleoptera: Scarabaeidae) Pheromone and Floral Lures in Northeastern China RI-ZHAO CHEN,1 MICHAEL G. KLEIN,2,3,4 QI-YUN LI,5
AND
YU LI1
Environ. Entomol. 43(3): 774Ð781 (2014); DOI: http://dx.doi.org/10.1603/EN13319
ABSTRACT Popillia quadriguttata (F.) has caused extensive damage to ⬇20 families and 25 species of plants in Asia, especially in China and Korea. Adult feeding causes serious damage to soybean leaves, and larvae develop on the roots of soybean, turf, and horticultural crops. As Japanese beetle (Popillia japonica Newman) lures have been used for trapping P. quadriguttata in a previous study, mass trapping this pest with various densities of the Japanese beetle pheromone, Japonilure, and ßoral lure, alone and in combination, were carried out during 2012Ð2013 in a northeastern China soybean Þeld. Mass trapping in 2012 with Japonilure gave the best results with 72 and 75% adult and larval reduction, respectively. In 2013, mass trapping (30 traps per hectare) with Japonilure, ßoral lure, or the combination resulted in a 93, 70, and 74% reduction of adults trapped, and a 90, 77, and 93% reduction of overwintering larvae, respectively. In addition, Þeld tests showed that almost twice as many beetles approached the lure combination compared with the ßoral lure alone, and the pheromone residual was ⬇80% of the initial dosage after 30 d. Because reduction of overwintering larvae is the most critical parameter indicating treatment efÞcacy, the results here indicate that the lure or lure combinations can be recommended for use by Chinese soybean farmers. KEY WORDS Japanese beetle lure, crop damage, adult and larval control
Soybeans are one of ChinaÕs most important crops, especially in Heilongjiang and Jilin provinces, and are grown on ⬇1.0 ⫻ 107 ha, representing 10% of the total crop area. More than 20 insects cause serious damage to soybeans throughout the world (Hao and Ren 2003). Popillia quadriguttata (F.) is an important species within the complex of soybean insect pests, and is regarded as the dominant species in soybean Þelds and turfgrass in Liaoning province (Sang 1979). This scarab beetle is widely distributed throughout China, especially in the northeast region, which has been the primary Chinese soybean production region for the past 60 yr (Zhang et al. 1981, Wang et al. 1999, Hao and Ren 2003, Fang 2007). In both China and Korea, P. quadriguttata was long misidentiÞed as the Japanese beetle, Popillia japonica Newman, because of their extremely similar morphology. Consequently, 20th century references to the Japanese beetle in China and Korea (Fleming 1972) were in fact P. quadriguttata (Ping 1988, Ku et al. 1999). In addition, studies by Kim et al. (1990) and 1 College of Agronomy, Jilin Agricultural University, 2888 Xincheng Road, 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 89528. 4 Corresponding author, e-mail: [email protected]. 5 Jilin Agricultural Academy of Science, Cai Yu Rd., Changchun 130118, Jilin Province, China.
Reed et al. (1991) noted a common scarab species in Korea as Popillia uchidai Niijima and Kinoshita. That species has been reexamined (Ku et al. 1999) and determined to also be P. quadriguttata. P. quadriguttata has also been reported from Russian and Vietnam (Reed et al. 1991, Lee et al. 2007). Known as a polyphagous pest, adults of P. quadriguttata have been shown to feed on ⬇20 families and 25 species of plants in China and Korea (Sang 1979, Lee et al. 2002). Severe damage occurs to fruit trees, ßowers, ornamental, and horticultural plants as well as other important agricultural crops (Zhang et al. 1981, Luo and Zhang 1981, Tan et al. 1998, Wang 2001, CAB International [CABI] 2002). Adult feeding causes damage to soybean ßowers, buds, immature leaves, and shoots, whereas larvae feed on plant roots. This insect has resulted in ⬇1% yield losses of Chinese soybeans per year (Wang and Zheng 2006, Fang 2007). In the recent past, feeding by P. quadriguttata has caused signiÞcant crop losses, especially on turfgrass, ßower crops, soybeans, and tree fruit (Qu et al. 1993, Wang 2001, State General Administration of Quality Supervision, Inspection and Quarantine of the PeopleÕs Republic of China [AQSIQ] 2003a,b, Australian Government, Department of Agriculture, Fisheries and Forestry 2004, Fang 2007). In South Korea, this scarab is the dominant pest on golf courses, as adults feed on ornamental plants and larvae feed heavily on turfgrass roots (Reed et al. 1991, Lee et al. 2007). As with the
0046-225X/14/0774Ð0781$04.00/0 䉷 2014 Entomological Society of America
June 2014
CHEN ET AL.: MASS TAPPING P. quadriguttata IN NORTHEASTERN CHINA
Japanese beetle, turf damage is often made worse by birds and mammals digging up the turf searching for larvae to eat. Therefore, P. quadriguttata will likely cause increased destruction of turf, as golf courses and green areas are developed in China. With increases in the Chinese economy, there will likely be a greater demand for ornamental plants, turfgrass, tree fruit, and agronomic production, all of which will be negatively impacted by P. quadriguttata larva or adult feeding. Although the parasitoid Tiphia vernalis Rohwer has been reported to parasitize P. quadriguttata in Korea and China, and P. japonica in Japan and the United States (Clausen et al. 1927, 1932, 1933; Fleming 1968, 1972; Sang 1979; Ding and Fu 2000; Reding and Klein 2001), pest suppression from biological control is insufÞcient for either insect. In China, chemical insecticides, including dipterex (⫽ trichlorfon), benzene hexachloride (⫽ lindane), and Carbofuran (⫽ Furadan) remain the mainstay of P. quadriguttata control in Þeld crops (Wang 2001, Fang 2007). However, chemical applications remain problematic because of environment contamination, increasing pest resistance, and an overuse of chemicals. Because there is an increasing awareness and value of organic agricultural products in China, there is a corresponding increased emphasis on environmentally friendly pest control measures. Finally, some previously popular chemicals, such as benzene hexachloride and Carbofuran noted above, are now being prohibited in China. There is also an increasing realization that chemical sprays damage pollinating insects in crop ßowers and may negatively impact crop yields. Sex lures (pheromones) and ßoral lures (kairomones) can be used in pest management by providing early detection, mass trapping, lure and kill measures, and mating disruption of pest insects (Weinzierl et al. 2012). In addition, several scarabs have been attracted to the P. japonica sex attractant (JaponilureÑ[(R, Z)-5-(I-decenyl) dihydro-2(3H)-furanone)ÑÞrst described by Tumlinson et al. (1977)), and many respond to the ßoral lures (Ladd et al. 1981; PEGÑ phenethyl propionate, eugenol, and geraniol [3:7:3]), or the combination (Chow 1986, Donaldson et al. 1986, Klein and Edwards 1989, Reed et al. 1991, Li et al. 1995, Cherry et al. 1996, Crocker et al. 1999, Chen et al. 2001, Toth et al. 2003, Lee et al. 2007). Attraction of P. quadriguttata to the P. japonica lures (Reed et al. 1991, Li et al. 1995, Lee et al. 2007, Chen et al. 2013b) provides an opportunity to exploit commercially available lures to protect Chinese crops from P. quadriguttata. The objectives of this study were to evaluate the use of traps baited with Japonilure plus ßoral lures to evaluate the effect of trapping on P. quadriguttata by observing soybean damage and overwintering larval populations. Materials and Methods Experiments were conducted at the Jilin Agricultural University experimental farms and campus in 2012, and elsewhere in Shuangyang county in 2013, for Þeld trail at Changchun, Jilin Province, northeastern
775
China (GPS coordinates: 125⬚ 26⬘, 43⬚ 23⬘), during July and August of both years. During this time, Tre´ ce´ Japanese beetle traps and lures were used (Tre´ ce´ , Inc., Adair, OK). The Tre´ ce´ Japanese beetle trap is made of two perpendicular, yellow, high-impact styrene vanes and a plastic bag that forms a funnel and beetle receptacle (Chen et al. 2013b). The ßoral lure was contained in a felt pad in 2012 (Chen et al. 2013b) and a high void polyethylene disk in 2013 (Klein and Edwards 1989), either held in a solvent-resistant plastic pack. The sex pheromone (1 mg) was placed in a rubber septum held in its own compartment in the same pack, and attached to adjoining trap vanes (Chen et al. 2013b). Control Efficiency. Trial and Trap Layout. In 2012, tests were conducted in a 3-ha soybean Þeld bounded by corn on all sides. The tall corn reduced the movement of P. quadriguttata from other local soybean Þelds. The Þeld was divided into 12 plots for trapping at ⬇10 traps per hectare for each of three lure treatments (ßoral lure and Japonilure, ßoral lure or Japonilure alone, and an unbaited control). In 2013, tests were conducted in ⬇5.5-ha soybean Þeld, divided into 30 plots (⬇0.17Ð 0.2 ha) for the three densities of mass trapping (10, 20, or 30 traps per hectare) baited with the same combinations as 2012. In both years, the trial Þeld had never been previously trapped. Each lure treatment was replicated three times with lure-baited traps placed in a randomized complete block design. There were ⬇25 m between plots as buffer to minimize the interaction between baited traps. However, because traps were placed inside the plot lines, the real distance from a trap in one replication to a trap in adjoining plots was ⬍40 m. In addition, the corn in the buffer and surrounding Þelds reduced the movement of adults and attractant components between plots. Also, at several random points in the buffer, no lure components were detected on pieces of absorbent foam placed 48 h earlier to check for chemicals in the atmosphere. Traps were secured to wooden poles so the upper edge of the funnel was ⬇75 cm above the ground. In both years, the investigations were conducted from 1 July to 30 August, and the lures were replaced on ⬇1 August. Evaluation of Treatment Efficacy. Lure-trap efÞcacy was compared with the untreated control plots for: 1) crop damage, 2) number of adults remaining on soybean leaves, and 3) overwintering larval populations. The Þrst two indices can be a good indication that the trapping was effective, but the overwintering larval assessment provides the conclusive proof. Crop Damage Assessment. Soybean leaf damage in the Þeld from P. quadriguttata was assessed on ⬇29 August in both years by randomly selecting 10 soybean plants in each lure treatment plot. Leaves from each plant were returned to the laboratory, scanned (HP Scanjet 200, Hewlett-Packard Co., Palo Alto, CA), and damage accessed with Photoshop software (version 7.0, Adobe Inc., San Jose, CA). Damage values were: 0 (no damage), 1 (up to 1% leaf eaten), 2 (2Ð4% leaf eaten), and 3 (4Ð6% leaf eaten). Generally, when damage reaches ⬇4%, soybean yield will be reduced by ⬎3%.
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Table 1. Control of P. quadriguttata in soybean fields treated either with 10 baited traps per hectare or in an untreated control in Changchun, Jilin Province, China in 2012 Mean ⫾ SE per plot Type of lure
Beetles captured (male/female) Treated
Adults on foliage (male/female)
Control
Treated
% reduction
Control
Larval mean
Adult (male/female)
Larvae
71.9a/0.8b 33.1b/28.8a 25.7b/26.3a
75.3a 49.0b 42.5b
97.4 ⬍ 0.001
67.5 ⬍ 0.001
Japonilure 185 ⫾ 21a/13 ⫾ 2c 83 ⫾ 6c/353 ⫾ 33a 401 ⫾ 10c Floral lure 56 ⫾ 12b/65 ⫾ 7a 198 ⫾ 13b/255 ⫾ 24b 830 ⫾ 64b a Combination 46 ⫾ 9b/42 ⫾ 8b 220 ⫾ 21b/264 ⫾ 17b 937 ⫾ 26b Control 3.4 ⫾ 1/2.3 ⫾ 0.2 296 ⫾ 25/358 ⫾ 36 1630 ⫾ 31a F (4, 10)/P.value 112.3 ⬍ 0.001 92.3 ⬍ 0.001 156.4 ⬍ 0.001
Numbers in a column followed by the same letter are not signiÞcantly different, LSD test (0.001). a Combination of Japonilure and ßoral lure.
Protection values were based on the damage value in the control minus the damage value in the treatments. Adults on Foliage and Overwintering Larvae. Adults attracted to plants, but not into traps in each lure treatment, were counted and recorded from 10 random soybean plants every 5 d from 2 July to 12 August in both years. Because overwintering larvae are commonly found ⬇30 cm deep under the ground in October, larvae were counted and recorded ⬇10 October by digging 1.5-m2 holes to a depth of ⬇30 cm in 10 randomly selected areas in trapped and untrapped soybean plots. Scarab Response to Lures. These observations were inspired by the research of Stelinski et al. (2013). Scarab beetle approaches to randomized dispensers during JulyÐAugust 2013 were recorded in each treatment. Each treatment was simultaneously observed for 60 min by nine people. The number of P. quadriguttata orienting to a dispenser, duration of visit near the dispenser(s), and closest approach of adults relative to the dispenser(s) were recorded. Observations were conducted on three different sunny- and low-wind days. Wind speeds were estimated every 5 min by a wind velocity indicator (HHF2005HW, 1698 Yi Shan Road, Unit 102, Min Hang District, Shanghai 201103, China). It was considered a valid observation period if wind speeds were ⬍0.03 m/s during the 60 min. The sex of beetles was not determined because of the nature of observations.
Lure Release Rates. In 2013, the amount of the Tre´ ce´ pheromone and Floral Lure components (phenethyl propionate, eugenol, and geraniol [3:7:3]) present after 5-d intervals in the Þeld was monitored. This was accomplished by putting 18 dispensers of each type of lure and then removing 3 of them for residue assessment every 5 d from the Þfth to thirtieth day after the exposure. The details on identiÞcation of components were similar to those by Chen et al. (2013a). The exceptions were that dispensers were stored at ⫺22⬚C, and ethyl phenethyl was used as the internal standard for phenethyl propionate, acetone for (R, Z)-5- (I-decenyl) dihydro-2(3H)-furanone, phenol for eugenol, and butyl acetate for geraniol. Data Analysis. During the 2-mo investigations, all beetles were taken to the Agricultural Insects Research Laboratory at the Jilin Agricultural University, Changchun, where they were identiÞed and counted. The number of adults on each soybean plant was recorded at eight different times and pooled. Adult captures (male or female), the number of adults in scarab response observation, overwintering larvae, and crop damage data were transformed by log (x ⫹ 1) to normalize the data. After transformation, data were analyzed by one-way analysis of variance, followed by a least signiÞcant difference (LSD) test to establish statistical differences.
100 adult reduction n
Mean value
80 60
a
a
overwintering larva reduction ductio in
a
a
a a
a
b
b
b c
b
b
c
b
b
b
40
b 20 0 J- J+F- F2012 2012 2012
J- J+F- F2013 2013 2013
J- J+F- F2012 2012 2012
J- J+F- F2013 2013 2013
J- J+F- F2012 2012 2012
J- J+F- F2013 2013 2013
Treatments
Fig. 1. P. quadriguttata. Percentage reduction of soybean plant leaf damage, adult captures, and overwintering larvae in 2012Ð2013 in Changchun, Jilin Province, China. Data of different density trap treatments of each type of lure were respectively pooled: J, Tre´ ce´ sex attractant (SA); F, Tre´ ce´ ßoral lure (FL); J⫹F, combination SA and FL.
78.1 ⬍ 0.01 66.3 ⬍ 0.01
60.1c/5.3d 92.6a/14.6d 92.6a/14.6d 35.3d/46.7bc 57.6c/53.6b 69.6b/63.7a 28.3d/42.3c 44.2d/49.4bc 74.2b/56.8a
437 ⫾ 26c 253 ⫾ 36d 176 ⫾ 27d 580 ⫾ 54b 460 ⫾ 57c 366 ⫾ 53d 760 ⫾ 48b 223 ⫾ 75d 110 ⫾ 17d 1609 ⫾ 197a 56.4 ⬍ 0.01 76.4 ⬍ 0.01 Control F (9, 20)/p.value
Comba
Floral Lure
10 20 30 10 20 30 10 20 30 Japonilure
Numbers in a column followed by the same letter are not signiÞcantly different (0.001). a Combination of Japonilure and ßoral lure. * Numbers in each treated-control group are signiÞcantly different, LSD test(0.001).
98.3 ⬍ 0.01
283 ⫾ 36*/336 ⫾ 67* 283 ⫾ 36*/336 ⫾ 67* 283 ⫾ 36*/336 ⫾ 67* 283 ⫾ 36*/336 ⫾ 67* 283 ⫾ 36*/336 ⫾ 67* 283 ⫾ 36*/336 ⫾ 67* 283 ⫾ 36*/336 ⫾ 67* 283 ⫾ 36*/336 ⫾ 67* 283 ⫾ 36*/336 ⫾ 67* 283 ⫾ 36/336 ⫾ 67 4 ⫾ 0.6*/3 ⫾ 0.4* 4 ⫾ 0.6*/3 ⫾ 0.4* 4 ⫾ 0.6*/3 ⫾ 0.4* 4 ⫾ 0.6*/3 ⫾ 0.4* 4 ⫾ 0.6*/3 ⫾ 0.4* 4 ⫾ 0.6*/3 ⫾ 0.4* 4 ⫾ 0.6*/3 ⫾ 0.4* 4 ⫾ 0.6*/3 ⫾ 0.4* 4 ⫾ 0.6*/3 ⫾ 0.4* 4 ⫾ 0.6/3 ⫾ 0.4 195 ⫾ 32ab/5 ⫾ 1c 238 ⫾ 37a/12 ⫾ 4c 255 ⫾ 42a/6 ⫾ 4c 85 ⫾ 18c/96 ⫾ 21bc 136 ⫾ 32b/121 ⫾ 23b 122 ⫾ 45b/105 ⫾ 19a 65 ⫾ 13c/72 ⫾ 17c 106 ⫾ 27b/98 ⫾ 21bc 125 ⫾ 31b/154 ⫾ 35a
113 ⫾ 17c/318 ⫾ 77a 21 ⫾ 4d/287 ⫾ 64a 17 ⫾ 3d/302 ⫾ 27a 183 ⫾ 18ab/179 ⫾ 35b 120 ⫾ 22c/156 ⫾ 43bc 86 ⫾ 7d/122 ⫾ 16c 203 ⫾ 38a/197 ⫾ 21b 158 ⫾ 21b/170 ⫾ 18b 73 ⫾ 12d/145 ⫾ 15c
Larvae % reduction
Adult (male/female) Larval mean Control Treated
777
Control
Mean ⫾ SE per plot
Adults on foliage (male/female) Beetles captured (male/female)
Density traps per hectare Type of lure
Table 2.
Control of P. quadriguttata in soybean fields either treated with at one of densities of baited traps per hectare or in untreated control in Changchun, Jilin Province, China in 2013
Results Control Efficacy. In 2012, signiÞcant differences (F ⫽ 112.3,92.3; df ⫽ 4, 10; P ⬍ 0.01) were found in the numbers of adults on leaves and of overwinter larva in soybean Þelds with different Tre´ ce´ lure treatments (Table 1). In addition, beetle trap captures and leaf damage also differed signiÞcantly between those treatments (Fig. 1). With all the lures, reductions of beetles on soybean leaves, and the decrease in overwintering larval populations compared with the unbaited control were highly signiÞcant. The traps baited with Japonilure alone were superior with 71.9% reduction of adults on leaves and 75.3% reduction of overwintering larvae compared with the unbaited control (Table 1; Fig. 1). In comparison to the control, trapping with Japoniture alone, the combination of Japonilure and ßoral lure, and the ßoral lure alone also resulted in very low plant damage (0.62 ⫹ 0.46, 1.38 ⫹ 0.36, and 1.63 ⫹ 0.32; Chen and Klein, unpublished data) and provided 52.18, 47.34, and 39.16% damage reduction, respectively. The plant damage had a generally positive correlation (not statistically determined) with both beetles on leaves and overwintering larval populations (Tables 1 and 2). In 2013, similar to 2012, signiÞcant differences (F ⫽ 98.3,56.4,76.4; df ⫽ 9, 20; P ⬍ 0.01) were found in the numbers of adults on leaves, overwinter larva in soybean Þelds, beetle trap captures, and leaf damage (F ⫽ 167.7; df ⫽ 9, 90; P ⬍ 0.01) with different lures treatment (Table 2; Fig. 1). SigniÞcantly more male beetles were captured with Japonilure at 20 or 30 baited traps per hectare than with 10 baited traps per hectare, whereas the combination of ßoral lure and Japonilure captured signiÞcantly more female beetles at 30 baited traps per hectare (Table 2). Traps baited with Japonilure caught signiÞcantly more total adults, mainly males, followed by the combination of lures and the ßoral lure alone (Fig. 1; Table 2). This resulted in the largest reduction of adult damage and overwintering larvae by Japonilure (Fig. 1), especially male reductions of 92.6% with either 30 or 20 dispensers per hectare (Table 2). Scarab Response to Lures. During the highest period of P. quadriguttata ßight activity (15 July to 5 AugustÑChen and Klein, unpublished data), the number of beetles captured per trap ranged from 8 to 22. SigniÞcantly more beetles (F ⫽ 107.3; df ⫽ 3, 24; P ⬍ 0.01) reached traps with the combination of lures than with Japonilure alone, which exceeded the ßoral lure alone. Almost twice as many beetles approached the lure combination compared with the ßoral lure alone (Fig. 2). The average duration of beetle visits to the traps ranged between 13 and 15 s, and there were no signiÞcant differences in duration of visits between treatments (Fig. 2). The average closest approach ranged between 13 and 15 cm from dispensers and the relative differences were signiÞcant (F ⫽ 121.2; df ⫽ 3, 24; P ⬍ 0.01) between treatments (Fig. 2). The sex of beetles was not obtained because of the inability to identify characteristic sex differences between adults ßying in the Þeld.
72.8c 84.3b 89.6ab 63.9d 71.4c 77.3c 52.8e 86.1b 93.2a
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Fig. 2. Mean total number, approach distance (cm), and visitation time duration (sec) of P. quadriguttata to dispensers in 2013 in Changchun, Jilin Province, China. Data of different density trap treatments of each type of lure were respectively pooled: J, Tre´ ce´ sex attractant (SA); F, Tre´ ce´ ßoral lure (FL); J⫹F, combination SA and FL.
Lure Release Rates. The laboratory bioassay of the lures (Fig. 3) showed that the pheromone was released very slowly from the dispenser. After l5 d., ⬎90% of Japonilure and ⬎89% ßoral lure remained, and both lure residual was ⬇80% of the initial dosage after 30 d. This is consistent with the label description of a 40-d Þeld life. Discussion P. quadriguttata is a serious insect pest in Asia that has caused soybean yields decreases by ⬇5Ð 8% when ßowers are seriously damaged by the beetleÕs feeding (Qu et al. 1993). There are no reports about efÞcient ways to change planting and subsequent ßower dates to avoid economic damage to ßowers from this beetle. Furthermore, the recent increase in Chinese golf
course turf, and ornamental grass, provides an ideal habitat where adults can lay eggs and the larvae can overwinter without disruption by natural enemies or agricultural practices such as tilling. In addition, the grass roots provide P. quadriguttata larvae a highly favorable and sustainable food resource each summer. There are ⬎20 insect species that damage soybean leaves, and several white grub species feed on the soybean roots (Hao and Ren 2003, Xu and Liu 2011). A reduction in soybean plant damage levels can be a good indication that a suppression technique is effective, but reductions of overwintering larvae provide the best proof of control. P. quadriguttata adult damage to leaves causes elliptical holes with the leaf veins, which looks very different from the damage caused by Lepidoptera larvae. Therefore, damage caused by these beetles can be easily assessed and evaluated.
Fig. 3. Percentage residual (a) Japonilure Ð (sex attractant): (R, Z)-5-(I-decenyl) dihydro-2(3H)-furanone and (b) ßoral lure; (PEG) in dispensers after a given number of days in the Þeld in 2013 in Changchun, Jilin Province, China.
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CHEN ET AL.: MASS TAPPING P. quadriguttata IN NORTHEASTERN CHINA
Soybean yield losses have been caused by several pest species including P. quadriguttata, and the soybean pod borer Leguminivora glycinivorella Matsumura (Lepidoptera : Olethreutidae) (Hao and Ren 2003). However, yield loss does not always correlate with pest density. However, the damage this year, and moreover for next year, will correlate with the overwintering larvae density. Therefore, overwintering larvae were used as the best indication for the effectiveness of mass trapping P. quadriguttata. This is the Þrst report of using attractants to mass trap the economically important P. quadriguttata in Asia. These beetles congregate diurnally and feed on ßowers and young leaves, resulting in 5Ð10% soybean yield losses annually, and larval feeding causes mortality to newly planted trees by feeding on developing roots (Wang 2001, Wang and Zheng 2006, Yang and Wang 2008). Therefore, there is need to develop an effective means to reduce the density and damage from these beetles. Using the commercial Tre´ ce´ Japanese beetle traps and lures to capture P. quadriguttata provides an adoptable control tactic that could be implemented by Asian growers. Interestingly, although P. japonica and P. quadriguttata feed on many of the same plants, the latter scarab is not a pest of rose (Sang 1979, Lee et al. 2002), which is one of the highly favored plants of the former (Fleming 1972). If the rose-derived attractant is not important for P. quadriguttata, elimination of the geraniol could make the ßoral lure cheaper. In any event, here in China, mass trapping provided ⬇80% reduction of overwintering larvae. This means the following year pest population will be signiÞcantly decreased, which may lead to lower crop damage without additional treatments. Overall, mass trapping with the Tre´ce´ system can provide a powerful means of early detection, forecasting, and control of P. quadriguttata in northeastern China Þelds. Sex pheromones are an ideal component of integrated pest management programs (Liu and Zhang 2006, Chen and Li 2011, Chen and Klein 2012, Chen et al. 2013a), and are a suggested tactic for moth mating disruption when the proper number of dispensers are placed in Þelds (Stelinski et al. 2008, Witzgall et al. 2008). Information here correlates positively with previous research. In addition, studies have shown an increase in efÞcacy of pheromones by coreleasing pheromones with kairomones (Ladd et al. 1981, Knight et al. 2012, Stelinski et al. 2013). This is often based on food and ßoral lures being attractive to both sexes (Hulcr et al. 2011). Here, traps with Japonilure alone caught more beetles than the combination of sex attractant and ßoral lure, which is in agreement with our previous report (Chen et al. 2013b). The highest reductions of overwintering larvae in both years were found in the plots treated with Japonilure. This may indicate that reduction of males from mass trapping, or confusion of males due to the presence of the sex attractant, resulted in females in those plots not being mated. P. japonica females are normally highly mobile, and could be expected to move between plots and mated. These results indicate that P. quadriguttata females may not be as mobile at these population
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levels. Almost as many females were found on the foliage in the Japonilure plots as in the controls, but the larval population was greatly reduced in the Japonilure treatments. In any event, Japonilure at 30 dispensers per hectare provided greater larval reduction (93.2%) than any other treatments in 2013 (Table 2). This correlates positively with the number of beetles approaching the lures. The movement of female beetles, effects of lures without geraniol, effects of lures on high populations, and the necessity of pure Japonilure need to be investigated further.
Acknowledgments We sincerely thank Tre´ ce´ Inc. for providing the traps and lures used in these studies. KleinÕs trip and the expenses for the Þeld trials were sponsored by the International Cooperation Project between Jilin Agricultural University and The Ohio State University funded by the Bureau of Foreign Experts Affairs (BFEA) of Jilin Province (Fundament number: L20122200014-2012; L20132200019-2013).
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