Field Trapping of Predaceous Insects With Synthetic Herbivore-Induced Plant Volatiles in Cotton Fields

Field Trapping of Predaceous Insects With Synthetic Herbivore-Induced Plant Volatiles in Cotton... Abstract Nine herbivore-induced plant volatiles (HIPVs) and one methyl jasmonate were field-tested for their attractiveness to the main predators in cotton fields of North China in 2 yr. The main predators including ladybird beetles (Propylaea japonica (Thunberg), Harmonia axyridis (Pallas)), green lacewings (Chrysoplera sinica (Tjeder), Chrysopa spp.), predatory bugs (Geocoris pallidipennis (Costa), Orius spp., Nabis spp.) and spiders (Misumenops tricuspidatus (Fabricius), Erigonidium graminicolum (Sundevall)) were investigated. Two-way ANOVA indicated that the volatile compound, year, and the volatile compound × year interaction affected the behavioral responses of predators. It was found that indole significantly attracted the ladybird beetle P. japonica, H. axyridis. Linalool could attract P. japonica. Green lacewing C. sinica was significantly attracted by α-pinene and β-pinene, whereas indole significantly attracted Chrysopa spp. Methyl jasmonate and α-pinene showed significant attraction to small-flower bug Orius spp. In addition, the attraction of α-humulene to C. sinica, attractiveness of β-pinene to Orius spp. and Chrysopa spp., were observed only in one of the two years. However, the big-eyed bug G. pallidipennis, damsel bug Nabis spp., spiders M. tricuspiata and E. graminicolum did not respond to any of the tested HIPVs. These results are discussed with respect to possible applications of a synthetic attractant for main predators in cotton fields. Over the past three decades, numerous studies demonstrated that herbivore-induced plant volatiles (HIPVs) are attractive to natural enemies of pests. And these HIPVs are released from plant species such as soybean, tomato, potato, maize, and green pepper (Turlings et al. 1991, Arab et al. 2007, Michereff et al. 2011, Cho et al. 2014, Tan and Liu 2014, Xu et al. 2015). Many field assays showed that lures of synthetic volatile chemicals could increase the abundance of natural enemies. Methyl salicylate (MeSA) attracts the green lacewing Chrysopa nigricornis Burmeister, the minute pirate bug Orius tristicolor (White) and the big-eyed bug Geocoris pallens Stal. in the hop yard and increases the abundance of the diamondback moth parasitoid Diadegma semiclausum Hellén in turnip fields (James 2003a, 2005; Orre et al. 2010). The 2-methyl butyral doxime and (Z)-3-hexenol, which were emitted from herbivore-damaged black poplar foliage, could significantly attract braconid parasitoids in the field (McCormick et al. 2014). Thus, the volatiles are expected to be ideal tools for biological control to increase natural enemy abundance and inhibit insect pests (Khan et al. 2008, Kaplan 2012). So far, synthetic HIPVs have been employed in a range of agricultural systems, including plots of cotton, hops, grape, cranberry, soybean, turnip, strawberry, and broccoli (James 2003b, James and Price 2004, Williams et al. 2008, Lee 2010, Orre et al. 2010, Mallinger et al. 2011, Rodriguez-Saona et al. 2011, Simpson et al. 2011). Recently, volatile compounds combined with traps were used to monitor the biodiversity of natural enemies in orchard ecosystems (Jones et al. 2011, 2016; Mills et al. 2016). The selection of compound or compounds is crucial in biological control strategy, which affects the attracted insect species and intensity (Kaplan 2012). In initial studies, researchers focused on the effects of commonly emitted volatiles such as MeSA, indole, cis-3-hexen-1-ol, and cis-3-hexenyl acetate, on natural enemy recruitment (James 2003a,b, 2005). A recent meta-analysis suggested that MeSA could be as a broad-spectrum attractant to lure the key natural enemy species from Anthocoridae, Coccinellidae, Syrphidae, Parasitic Hymenoptera, predaceous Heteroptera, and lacewings (Rodriguez-Saona et al. 2011). MeSA is also an active ingredient in the commercially available carnivore attractant, PredaLure (MSTRS Technologies, Ames, IA) (Kaplan 2012). There were more than 2,000 volatile compounds identified from 900 plant families (War et al. 2011), however, the roles of numerous candidate volatile compounds remain unclear. Cotton bollworm Helicoverpa armigera Hübner, cotton aphid Aphis gossypii Glover and sweetpotato whitefly Bemisia tabaci (Gennadius) are the major pests of cotton in North China (Luo et al. 2014). And pest suppression mainly depended on chemical control before the 1970s. However, the over-reliance on chemical pesticides caused a series of problems such as environmental pollution, pest resurgence and pest resistance. Since then, integrated pest management (IPM) containing biological control was adopted in China. Predators, an important component of biological control in cotton field, are a large group including spider families, predaceous insects such as ladybird beetles, green lacewing, predatory bugs (Guo 1998, Wu et al. 2005, Luo et al. 2014). The employment of synthetic HIPVs to enhance the recruitment of predator groups in cotton fields could be an effectively strategy in biological control. HIPVs such as α-pinene, α-humulene, α-farnesene, β-pinene, linalool, indole, β-ocimene, and (Z)-3-hexenyl butyrate were identified from cotton plants (McCall et al. 1994; Paré and Tumlinson 1997; Yu et al. 2006, 2007; Morawo and Fadamiro 2016). The attractiveness of these HIPVs to natural enemies was evaluated in hop yard, vineyard and alfalfa field (James 2005, Zhu et al. 2005). However, there was rare investigation on employment of the above mentioned compounds in cotton fields (Flint et al. 1979, Yu et al. 2008, 2010). In the present study, the potential attraction of nine cotton volatile compounds (α-humulene, α-pinene, α-farnesene, β-pinene, ocimene, linalool, indole, (Z)-3-hexenyl butyrate, and benzoic acid ethyl ester) and one methyl jasmonate (MeJA) to predators was investigated in cotton field. We aimed to better understand whether the application of synthetic compounds could be used as attractants in cotton fields in northern China. Materials and Methods Field experiments were conducted in a 1.5-ha cotton field at the Langfang Experimental Station of the Chinese Academy of Agriculture Sciences (CAAS), Hebei province (39°08′ N,116°23′ E) in the years of 2013 and 2014. During the growing season, the crop management without pesticides was performed identically to those of local typical operation. Experiments were performed separately from 11 June to 10 September in 2013 and from 14 July to 19 September in 2014. White sticky cards (36 × 25 cm, Pherobio Technology Co., Ltd, Beijing, China) were stapled to 50 × 25-cm plastic cards and attached by wire to bamboo sticks at a height of 2 m above the ground. Cards were baited with 1 ml (10 mg/ml diluted in lanolin (Sigma-Aldrich, St. Louis, MO) of the candidate HIPV solutions in 2-ml glass vials. Control treatments were baited only with 1 ml lanolin. In 2013, nine tested HIPVs were α-humulene, α-pinene, β-pinene, α-farnesene, indole, (Z)-3-hexenyl butyrate, MeJA, linalool, and benzoic acid ethyl ester, and in 2014, ocimene was also tested. All the chemical compounds (purity levels of ≥ 90%) were obtained from Sigma-Aldrich. Every card with a glass vial containing the tested compound or the control was suspended by wire at a height of 2 cm above the center of each card. The distance between two traps was 6 m and traps were distributed using a randomized block design. At the same time every week, there were 12 replicates for each treatment in 2013 (12 × 10 treatments) and six replicates were sampled in 2014 (6 × 11 treatments). Sticky cards were collected and replaced weekly for 12 wk (12 × 12 × 10 samples) in 2013 and for 10 wk (10 × 6 × 11 samples) in 2014. Counts were conducted for the predators captured including ladybird beetles, green lacewings, predatory bugs, and spiders. Trapped beneficial insects species or genera were identified in laboratory under a stereomicroscope, and then evaluated the attraction of HIPVs. Statistical Analysis The numbers of predators on sticky cards containing different volatile compounds (except for ocimene) were analyzed using two-way ANOVA (volatile compound and year as main factors), followed by Tukey’s HSD tests. Student’s t-test was used to compare the numbers of predators on sticky cards containing ocimene with those of control sticky cards. Prior to analysis, all data were transformed by log(x + 1) for fitting the assumption of parametric tests. All statistical analyses were executed using SPSS 19.0. Results Total 8,740 predators from 1,440 sticky traps in 2013, and 6,012 predators from 660 sticky traps in 2014 were captured. The major predators from the sticky traps were collected and analyzed in this trial over 2 yr. The predatory beetles included Propylaea japonica (Thunberg) and multicolored Asian ladybeetle Harmonia axyridis (Pallas). Green lacewings included Chrysopa spp. and Chrysoperla sinica (Tjeder). Predatory bugs included the flower bugs Orius spp., the big-eyed bug Geocoris pallidipennis (Costa), and damsel bugs Nabis spp. Spiders included Misumenops tricuspidatus (Fabricius) and Erigonidium graminicolum (Sundevall). The numbers of ladybird beetles P. japonica on sticky cards showed no difference in the interaction between the volatile compound and year (two-way ANOVAs, F9,219 = 1.20, P = 0.30), but were significant differences among volatile compounds (F9,219 = 6.50, P < 0.001). Linalool and indole obviously attracted P. japonica in the 2 yr compared with the controls (all P < 0.05), however, there was no significant difference between these two compounds (both P > 0.05). Similar results were also found in H. axyridis assays (volatile compound × year interaction: F9,219 = 0.82, P = 0.60; volatile compound: F9,219 = 3.10, P = 0.002). Indole was significantly attractive to H. axyridis in the 2 yr (both P < 0.05) (Table 1). The number of green lacewings C. sinica on sticky cards was significantly different among volatile compounds (F9,219 = 4.30, P < 0.001), but was not affected by the volatile compound × year interaction (F9,219 = 0.72, P = 0.69). The α-humulene, α-pinene and β-pinene significantly attracted green lacewings C. sinica in 2013 (all P < 0.05), whereas in 2014, C. sinica only showed significant attraction to α-pinene and β-pinene (both P < 0.05). The number of green lacewings Chrysopa spp. was affected by the volatile compound (F9,219 = 7.32, P < 0.001) and the volatile compound × year interaction (F9,219 = 2.58, P = 0.008). Chrysopa spp. was significantly attracted by indole in the 2 yr (both P < 0.05), whereas β-pinene remarkably attracted Chrysopa spp. only in 2014 (P < 0.001) (Table 1). The number of small flower bugs Orius spp. was significantly affected by the volatile compound (F9,219 = 5.44, P < 0.001) and the volatile compound × year interaction (F9,219 = 2.69, P = 0.006). Compared with the controls, the Orius spp. was significantly attracted by α-pinene and MeJA in 2 yr (all P < 0.05). Moreover, in 2013, β-pinene was significantly attractive to Orius spp. (P < 0.001) (Table 1). Table 1. Mean (±SE) number of the predators attracted by the tested volatile compounds in the years of 2013 and 2014 Predator  Year  Volatile Compounds  Benzoic acid ethyl ester  α-Farnesene  (Z)-3-Hexenyl butyrate  α-Humulene  Indole  Linalool  MeJA  α-Pinene  β-Pinene  Control  Ocimene #  Propylaea japonica  2013  0.96 ± 0.31b A  1.74 ± 0.55ab A  1.08 ± 0.30b A  0.76 ± 0.47b A  2.53 ± 0.64a A  2.72 ± 0.89a A  0.81 ± 0.28b A  1.37 ± 0.56ab A  0.99 ± 0.28b A  0.80 ± 0.20b A    2014  1.27 ± 0.42ab A  1.50 ± 0.70ab A  1.35 ± 0.46ab A  1.13 ± 0.51ab A  1.80 ± 0.75a A  2.33 ± 0.74a A  1.32 ± 0.58ab A  1.53 ± 0.70ab A  1.10 ± 0.53ab A  0.52 ± 0.36b A  1.28 ± 0.50  Harmonia axyridis  2013  0.43 ± 0.15b A  0.41 ± 0.14b A  0.51 ± 0.17b A  0.37 ± 0.13b A  1.29 ± 0.48a A  0.64 ± 0.28ab A  0.51 ± 0.14b A  0.67 ± 0.17ab A  0.43 ± 0.15b A  0.38 ± 0.14b A    2014  0.37 ± 0.19b A  0.62 ± 0.18b A  0.40 ± 0.11b A  0.67 ± 0.29ab A  1.00 ± 0.21a A  0.35 ± 0.18b A  0.55 ± 0.30ab A  0.67 ± 0.20ab A  0.72 ± 0.33ab A  0.30 ± 0.15b A  0.38 ± 0.08  Chrysoplera sinica  2013  0.26 ± 0.06c B  0.30 ± 0.09c B  0.25 ± 0.05c B  0.57 ± 0.18ab B  0.41 ± 0.29abc B  0.26 ± 0.18bc B  0.20 ± 0.04c B  0.67 ± 0.17a B  0.60 ± 0.19ab B  0.16 ± 0.04c B    2014  1.22 ± 0.33ab A  1.42 ± 0.33ab A  1.28 ± 0.24ab A  1.48 ± 0.39ab A  1.83 ± 0.62ab A  1.43 ± 0.32ab A  1.48 ± 0.38ab A  2.47 ± 0.42a A  2.13 ± 0.41a A  0.62 ± 0.56b A  1.15 ± 0.28  Chrysopa spp.  2013  0.09 ± 0.04b A  0.15 ± 0.09b A  0.13 ± 0.06b A  0.28 ± 0.19ab A  0.66 ± 0.21a A  0.36 ± 0.26ab A  0.17 ± 0.06b A  0.17 ± 0.06b A  0.26 ± 0.13b A  0.10 ± 0.08b A    2014  0.03 ± 0.03b A  0.02 ± 0.02b A  0.07 ± 0.05b A  0.02 ± 0.02b A  1.18 ± 0.46a A  0.03 ± 0.03b A  0.17 ± 0.12b A  0.18 ± 0.15ab A  0.87 ± 0.31a A  0.02 ± 0.02b A  0.02 ± 0.02  Orius spp.  2013  0.24 ± 0.04c B  0.27 ± 0.07c B  0.28 ± 0.03c B  0.32 ± 0.13c B  0.37 ± 0.15c B  0.76 ± 0.19b B  1.57 ± 0.38a B  0.91 ± 0.30ab B  1.12 ± 0.38ab B  0.23 ± 0.08c B    2014  1.78 ± 0.45bc A  1.85 ± 0.41bc A  2.33 ± 0.75bc A  2.10 ± 0.45bc A  2.13 ± 0.60bc A  1.73 ± 0.38bc A  2.78 ± 0.61b A  4.82 ± 1.12a A  2.05 ± 0.97bc A  1.17 ± 0.42c A  2.38 ± 0.72  Predator  Year  Volatile Compounds  Benzoic acid ethyl ester  α-Farnesene  (Z)-3-Hexenyl butyrate  α-Humulene  Indole  Linalool  MeJA  α-Pinene  β-Pinene  Control  Ocimene #  Propylaea japonica  2013  0.96 ± 0.31b A  1.74 ± 0.55ab A  1.08 ± 0.30b A  0.76 ± 0.47b A  2.53 ± 0.64a A  2.72 ± 0.89a A  0.81 ± 0.28b A  1.37 ± 0.56ab A  0.99 ± 0.28b A  0.80 ± 0.20b A    2014  1.27 ± 0.42ab A  1.50 ± 0.70ab A  1.35 ± 0.46ab A  1.13 ± 0.51ab A  1.80 ± 0.75a A  2.33 ± 0.74a A  1.32 ± 0.58ab A  1.53 ± 0.70ab A  1.10 ± 0.53ab A  0.52 ± 0.36b A  1.28 ± 0.50  Harmonia axyridis  2013  0.43 ± 0.15b A  0.41 ± 0.14b A  0.51 ± 0.17b A  0.37 ± 0.13b A  1.29 ± 0.48a A  0.64 ± 0.28ab A  0.51 ± 0.14b A  0.67 ± 0.17ab A  0.43 ± 0.15b A  0.38 ± 0.14b A    2014  0.37 ± 0.19b A  0.62 ± 0.18b A  0.40 ± 0.11b A  0.67 ± 0.29ab A  1.00 ± 0.21a A  0.35 ± 0.18b A  0.55 ± 0.30ab A  0.67 ± 0.20ab A  0.72 ± 0.33ab A  0.30 ± 0.15b A  0.38 ± 0.08  Chrysoplera sinica  2013  0.26 ± 0.06c B  0.30 ± 0.09c B  0.25 ± 0.05c B  0.57 ± 0.18ab B  0.41 ± 0.29abc B  0.26 ± 0.18bc B  0.20 ± 0.04c B  0.67 ± 0.17a B  0.60 ± 0.19ab B  0.16 ± 0.04c B    2014  1.22 ± 0.33ab A  1.42 ± 0.33ab A  1.28 ± 0.24ab A  1.48 ± 0.39ab A  1.83 ± 0.62ab A  1.43 ± 0.32ab A  1.48 ± 0.38ab A  2.47 ± 0.42a A  2.13 ± 0.41a A  0.62 ± 0.56b A  1.15 ± 0.28  Chrysopa spp.  2013  0.09 ± 0.04b A  0.15 ± 0.09b A  0.13 ± 0.06b A  0.28 ± 0.19ab A  0.66 ± 0.21a A  0.36 ± 0.26ab A  0.17 ± 0.06b A  0.17 ± 0.06b A  0.26 ± 0.13b A  0.10 ± 0.08b A    2014  0.03 ± 0.03b A  0.02 ± 0.02b A  0.07 ± 0.05b A  0.02 ± 0.02b A  1.18 ± 0.46a A  0.03 ± 0.03b A  0.17 ± 0.12b A  0.18 ± 0.15ab A  0.87 ± 0.31a A  0.02 ± 0.02b A  0.02 ± 0.02  Orius spp.  2013  0.24 ± 0.04c B  0.27 ± 0.07c B  0.28 ± 0.03c B  0.32 ± 0.13c B  0.37 ± 0.15c B  0.76 ± 0.19b B  1.57 ± 0.38a B  0.91 ± 0.30ab B  1.12 ± 0.38ab B  0.23 ± 0.08c B    2014  1.78 ± 0.45bc A  1.85 ± 0.41bc A  2.33 ± 0.75bc A  2.10 ± 0.45bc A  2.13 ± 0.60bc A  1.73 ± 0.38bc A  2.78 ± 0.61b A  4.82 ± 1.12a A  2.05 ± 0.97bc A  1.17 ± 0.42c A  2.38 ± 0.72  Means for each predator with the same lowercase letters in the rows and with the same uppercase letters in the same column are not significantly different (P > 0.05). Prior to analysis, all data were transformed by log(χ +1) for fitting the assumption of parametric tests. Data of each predator on sticky cards baited with different volatile compounds (except for ocimene) were analyzed using two-way ANOVA (volatile compound and year as main factors), followed by Tukey’s HSD tests. # Data of each predator was analyzed using the Student’s t-test compared with that of control in 2014. View Large The numbers of big-eyed bugs G. pallidipennis, damsel bugs Nabis spp., spiders E. graminicolum and M. tricuspiata were not affected by volatiles or volatile by year interaction [two-way ANOVAs, volatile compound (F9,219 = 0.20~0.63, all P > 0.05), the volatile compound × year interaction (F9,219 = 0.25~0.91, all P > 0.05)] (Table 2). Compared with the controls, predatory beetles (P. japonica, H. axyridis), green lacewings (C. sinica, Chrysopa spp.), predatory bugs (Orius spp., G. pallidipennis, Nabis spp.), and spiders (E. graminicolum, M. tricuspiata) were not significantly attracted by ocimene in 2014 (t18 = 0.00~1.73, all P > 0.05) (Tables 1 and 2). Table 2. Mean (±SE) number of the predators not attracted by the tested volatile compounds in the years of 2013 and 2014 Predator  Year  Volatile compounds  Benzoic acid ethyl ester  α-Farnesene  (Z)-3-Hexenyl butyrate  α-Humulene  Indole  Linalool  MeJA  α-Pinene  β-Pinene  Control  Ocimene #  Geocoris pallidipennis  2013  0.15 ± 0.15a A  0.06 ± 0.05a A  0.28 ± 0.23a A  0.03 ± 0.03a A  0.04 ± 0.02a A  0.01 ± 0.01a A  0.19 ± 0.16a A  0.05 ± 0.03a A  0.03 ± 0.02a A  0.03 ± 0.03a A    2014  0.02 ± 0.02a A  0.07 ± 0.04a A  0.03 ± 0.03a A  0.12 ± 0.04a A  0.07 ± 0.04a A  0.03 ± 0.03a A  0.08 ± 0.04a A  0.05 ± 0.04a A  0.13 ± 0.03a A  0.07 ± 0.04a A  0.03 ± 0.02  Nabis spp.  2013  0.53 ± 0.17a B  0.44 ± 0.18a B  0.47 ± 0.19a B  0.42 ± 0.16a B  0.49 ± 0.20a B  0.50 ± 0.24a B  0.33 ± 0.13a B  0.56 ± 0.21a B  0.43 ± 0.18a B  0.54 ± 0.21a B    2014  0.60 ± 0.18a A  0.65 ± 0.21a A  0.90 ± 0.46a A  0.63 ± 0.17a A  1.02 ± 0.36a A  0.77 ± 0.24a A  1.22 ± 0.49a A  0.72 ± 0.20a A  1.27 ± 0.72a A  0.52 ± 0.16a A  0.28 ± 0.15  Erigonidium graminicolum    0.19 ± 0.03a B  0.17 ± 0.03a B  0.23 ± 0.05a B  0.21 ± 0.04a B  0.18 ± 0.05a B  0.23 ± 0.05a B  0.22 ± 0.03a B  0.18 ± 0.03a B  0.29 ± 0.03a B  0.12 ± 0.03a B    2014  1.13 ± 0.26a A  1.47 ± 0.24a A  1.07 ± 0.21a A  1.32 ± 0.28a A  1.32 ± 0.24a A  1.28 ± 0.35a A  1.33 ± 0.31a A  1.22 ± 0.25a A  1.22 ± 0.17a A  1.48 ± 0.34a A  1.00 ± 0.20  Misumenops tricuspidatus  2013  0.16 ± 0.10a B  0.14 ± 0.08a B  0.14 ± 0.07a B  0.07 ± 0.03a B  0.08 ± 0.06a B  0.11 ± 0.07a B  0.10 ± 0.04a B  0.10 ± 0.06a B  0.07 ± 0.04a B  0.11 ± 0.06a B    2014  0.37 ± 0.11a A  0.25 ± 0.10a A  0.38 ± 0.16a A  0.22 ± 0.08a A  0.18 ± 0.09a A  0.27 ± 0.10a A  0.30 ± 0.08a A  0.18 ± 0.05a A  0.27 ± 0.09a A  0.18 ± 0.09a A  0.18 ± 0.08  Predator  Year  Volatile compounds  Benzoic acid ethyl ester  α-Farnesene  (Z)-3-Hexenyl butyrate  α-Humulene  Indole  Linalool  MeJA  α-Pinene  β-Pinene  Control  Ocimene #  Geocoris pallidipennis  2013  0.15 ± 0.15a A  0.06 ± 0.05a A  0.28 ± 0.23a A  0.03 ± 0.03a A  0.04 ± 0.02a A  0.01 ± 0.01a A  0.19 ± 0.16a A  0.05 ± 0.03a A  0.03 ± 0.02a A  0.03 ± 0.03a A    2014  0.02 ± 0.02a A  0.07 ± 0.04a A  0.03 ± 0.03a A  0.12 ± 0.04a A  0.07 ± 0.04a A  0.03 ± 0.03a A  0.08 ± 0.04a A  0.05 ± 0.04a A  0.13 ± 0.03a A  0.07 ± 0.04a A  0.03 ± 0.02  Nabis spp.  2013  0.53 ± 0.17a B  0.44 ± 0.18a B  0.47 ± 0.19a B  0.42 ± 0.16a B  0.49 ± 0.20a B  0.50 ± 0.24a B  0.33 ± 0.13a B  0.56 ± 0.21a B  0.43 ± 0.18a B  0.54 ± 0.21a B    2014  0.60 ± 0.18a A  0.65 ± 0.21a A  0.90 ± 0.46a A  0.63 ± 0.17a A  1.02 ± 0.36a A  0.77 ± 0.24a A  1.22 ± 0.49a A  0.72 ± 0.20a A  1.27 ± 0.72a A  0.52 ± 0.16a A  0.28 ± 0.15  Erigonidium graminicolum    0.19 ± 0.03a B  0.17 ± 0.03a B  0.23 ± 0.05a B  0.21 ± 0.04a B  0.18 ± 0.05a B  0.23 ± 0.05a B  0.22 ± 0.03a B  0.18 ± 0.03a B  0.29 ± 0.03a B  0.12 ± 0.03a B    2014  1.13 ± 0.26a A  1.47 ± 0.24a A  1.07 ± 0.21a A  1.32 ± 0.28a A  1.32 ± 0.24a A  1.28 ± 0.35a A  1.33 ± 0.31a A  1.22 ± 0.25a A  1.22 ± 0.17a A  1.48 ± 0.34a A  1.00 ± 0.20  Misumenops tricuspidatus  2013  0.16 ± 0.10a B  0.14 ± 0.08a B  0.14 ± 0.07a B  0.07 ± 0.03a B  0.08 ± 0.06a B  0.11 ± 0.07a B  0.10 ± 0.04a B  0.10 ± 0.06a B  0.07 ± 0.04a B  0.11 ± 0.06a B    2014  0.37 ± 0.11a A  0.25 ± 0.10a A  0.38 ± 0.16a A  0.22 ± 0.08a A  0.18 ± 0.09a A  0.27 ± 0.10a A  0.30 ± 0.08a A  0.18 ± 0.05a A  0.27 ± 0.09a A  0.18 ± 0.09a A  0.18 ± 0.08  Means for each predator with the same lowercase letters in the rows and with the same uppercase letters in the same column are not significantly different (P > 0.05). Prior to analysis, all data were transformed by log(χ +1) for fitting the assumption of parametric tests. Data of each predator on sticky cards baited with different volatile compounds (except for ocimene) were analyzed using two-way ANOVA (volatile compound and year as main factors), followed by Tukey’s HSD tests. # Data of each predator was analyzed using the Student’s t-test compared with that of control in 2014. View Large Discussion Several field experiments have been conducted to evaluate the attraction of plant volatiles to predators in cotton fields (Flint et al. 1979, Yu et al. 2008). In this work, nine HIPVs and one MeJA were field-tested for their attractiveness to the main predators. Positive results revealed that some of the selected synthetic compounds significantly attracted ladybird beetles (P. japonica, H. axyridis), green lacewings (C. sinica and Chrysopa spp.), and small flower bugs Orius spp. P. japonica and H. axyridis are the two most abundant species of predatory beetles in cotton in North China (Liu et al. 2000, Wu et al. 2005). Moreover, P. japonica accounts for 60–90% of all natural enemies in cotton fields during certain years (Cui 1996). Field trials showed that the population density of P. japonica is higher than that of H. axyridis during the early and middle cotton growth stages, and decreased in the later cotton growth stages (Wang et al. 2013). In the current work, we found that these two species of ladybird beetles were abundant from the middle of June to the middle of September. The attractiveness of linalool and indole to P. japonica and H. axyridis were only evaluated using electroantennogram (EAG) and behavior (olfactometer) techniques under laboratory conditions (Han and Chen 2002, Qi et al. 2008). Our data indicated that linalool attracted P. japonica and indole significantly attracted P. japonica, H. axyridis in cotton fields over 2 yr. Moreover, we found that indole attracted more P. japonica than H. axyridis during the early and middle cotton growing stages, whereas more H. axyridis than P. japonica were attracted by indole in the later cotton growing season (unpublished data). Chrysopa spp. (Chrysopa septempunctata Wesmael, Chrysopa shansiensis Kuwayama, Chrysopa phyllochroma Wesmael and Chrysopa formosa Brauer) and C. sinica are predominant chrysopids observed in the field of North China (Guo 1998, Liu et al. 2000). It was reported that Chrysopa spp. and Chrysoperla spp. were attracted by plant volatiles, the combination of plant volatile (MeSA) and lacewing pheromone (iridodial) (Flint et al. 1979; James 2003a, 2006; James and Price 2004; Zhu et al. 2005; Zhang et al. 2006; Tóth et al. 2009; Lee 2010; Jones et al. 2011, 2016). Moreover, plant volatiles could significantly enhance female C. phyllochroma oviposition to retain individuals and establish populations (Xu et al. 2015). Laboratory data showed that indole could elicit strong electrophysiological and behavioral responses of C. septempunctata (Han and Chen 2002). Field trapping tests demonstrated that 100 mg of indole could significantly attract adult Chrysopa oculata L., but did not attract adult Chrysoperla carnea (Say) in the alfalfa filed (Zhu et al. 2005). Similarly, our data showed that indole significantly attracted Chrysopa spp., but did not attract C. sinica. A possible explanation for this phenomenon is that the former is a carnivore as an adult, whereas the latter is carnivorous only as a larva (Aldrich and Zhang 2016). Adult C. sinica typically feeds on pollen, honeydew and nectar. Thus, indole might mainly be used as a signal by lacewings for locating prey. Attraction of α-pinene and β-pinene to C. sinica in our tests were consistent with the results reported by Zhang et al (2012b), who suggested that α-pinene and β-pinene were two novel compounds released from the damaged persimmon leaves with high emission amounts and they were considered to be important compounds for recruiting C. sinica. Although pinene was previously reported to be unattractive to C. carnea adults in cotton (Flint et al. 1979), α-pinene could attract C. sinica adults in this study. MeSA and iridodial are considered as two strong attractants for green lacewings (Neuroptera: Chrysopidae) (Jones et al. 2011, 2016). So, we speculated that indole, α-pinene and β-pinene could be combined with MeSA and/or iridodial to exert better biological control of this predatory group. Due to their long occurrence time, high population density, diverse spectrum of prey species, and high predation rate, Orius bugs are considered as a promising agent for controlling pests (Zhou and Lei 2002, Ahmadi et al. 2009, Zhang et al. 2012a). Field trapping tests showed that Orius spp. were attracted to a variety of plant volatiles including benzaldehyde, MeSA, nonanal, octylaldehyde, (Z)-3-hexen-1-ol, (Z)-3-hexenyl acetate, 3,7-dimethyl,1,3,6-octatriene, and nonanal+(Z)-3-hexen-1-ol in the hops, cotton and strawberry field (James 2003a, 2005; Yu et al. 2008; Lee 2010). Our results revealed that sticky traps baited with α-pinene or MeJA captured more Orius spp. than that of the control traps. These findings were in agreement with the previous studies that Orius spp. significantly preferred α-pinene and MeJA in olfactometer or pot assays (Arab et al. 2007, Stepanycheva et al. 2014, Gebreziher and Nakamutan 2016b). In the current study, Nabis spp. and G. pallidipennis were not attracted by any tested HIPVs. Thus, it will be worthwhile to select effective volatiles to be used as attractants for the genus Orius spp. Some tested HIPVs attracted the predators only in one of the 2 yr, such as β-pinene attracting Orius bugs and Chrysopa spp., as well as α-humulene attracting C. sinica. Kaplan (2012) pointed out that spatiotemporal heterogeneity in the sex ratios, mating status, and age structures of field populations is likely correlated with the strength of responses to plant volatiles. Other exogenous factors such as the climate, geographical situation, plant species, and HIPV application technique also affect the responses of insects (Zhu et al. 2005, Schröder and Hilker 2008, Kaplan 2012). In this work, weather might be one of the main factors influencing on our results. Actually, weather factors manipulated the occurrence of insects and the infestation levels of pests in fields that eventually affected attractiveness of specific compounds during the seasons. Recently, mirid bugs have become the key pests in China due to the wide adoption of Bt cotton and decrease of insecticides in cotton fields (Lu et al. 2010). And considerable study is now focused on how to control this pest through biological control (Lu and Wu 2008, Luo et al. 2011). The predaceous insects of mirid bugs included small flower bugs (Orius similis Zheng, Orius minutes (L.)), big-eyed bug G. pallidipennis, damsel bugs Nabis sinoferus Hsiao, Nabis stenoferus Hsiao, and green lacewings C. sinica, C. formosa, C. septempunctata (Luo et al. 2014). Thus, the application of HIPVs to increase abundance of predators and attract/repel mirid bugs, may contribute to biological control of this pest in the future. Geng (2012) showed that propanoic acid butyl ester and 1-ethyl-4-(2-methylpropyl)-benzene from mungbean plants could effectively trap plant bugs Apolygus lucorum (Meyer-Dür) in cotton fields. How to deploy the HIPVs to control mirid bugs at certain temporal/phenological stages of the cotton would be explored in next work. As a strategy of IPM, the control effects of HIPVs must be reliable and stable. Therefore, more trials need to be conducted to verify the effectiveness of HIPVs over multiple years, and mixtures of volatiles should be tested if a single HIPV is not sufficiently attractive (Maeda et al. 2015; Gebreziher and Nakamuta 2016a,b). In addition, due to the limited experiment fields there was relatively close trap spacing (6 m) in our study. The spatial range of particular volatiles detected by natural enemy may depend on natural enemy species, cotton cultivars, and release rate of volatile compounds, etc. The effects of the perceived volatile ‘blend’ by predators on attractiveness of each of the single compounds will be investigated within this set-up. And the impact of some highly-attractive compounds on attraction of other chemicals deployed in the same field plot should be also evaluated. Furthermore, the exact densities of HIPV lures in field at specific cotton stages should be made clear to develop practical semiochemical formulations and its application in IPM. 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Field Trapping of Predaceous Insects With Synthetic Herbivore-Induced Plant Volatiles in Cotton Fields

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Abstract

Abstract Nine herbivore-induced plant volatiles (HIPVs) and one methyl jasmonate were field-tested for their attractiveness to the main predators in cotton fields of North China in 2 yr. The main predators including ladybird beetles (Propylaea japonica (Thunberg), Harmonia axyridis (Pallas)), green lacewings (Chrysoplera sinica (Tjeder), Chrysopa spp.), predatory bugs (Geocoris pallidipennis (Costa), Orius spp., Nabis spp.) and spiders (Misumenops tricuspidatus (Fabricius), Erigonidium graminicolum (Sundevall)) were investigated. Two-way ANOVA indicated that the volatile compound, year, and the volatile compound × year interaction affected the behavioral responses of predators. It was found that indole significantly attracted the ladybird beetle P. japonica, H. axyridis. Linalool could attract P. japonica. Green lacewing C. sinica was significantly attracted by α-pinene and β-pinene, whereas indole significantly attracted Chrysopa spp. Methyl jasmonate and α-pinene showed significant attraction to small-flower bug Orius spp. In addition, the attraction of α-humulene to C. sinica, attractiveness of β-pinene to Orius spp. and Chrysopa spp., were observed only in one of the two years. However, the big-eyed bug G. pallidipennis, damsel bug Nabis spp., spiders M. tricuspiata and E. graminicolum did not respond to any of the tested HIPVs. These results are discussed with respect to possible applications of a synthetic attractant for main predators in cotton fields. Over the past three decades, numerous studies demonstrated that herbivore-induced plant volatiles (HIPVs) are attractive to natural enemies of pests. And these HIPVs are released from plant species such as soybean, tomato, potato, maize, and green pepper (Turlings et al. 1991, Arab et al. 2007, Michereff et al. 2011, Cho et al. 2014, Tan and Liu 2014, Xu et al. 2015). Many field assays showed that lures of synthetic volatile chemicals could increase the abundance of natural enemies. Methyl salicylate (MeSA) attracts the green lacewing Chrysopa nigricornis Burmeister, the minute pirate bug Orius tristicolor (White) and the big-eyed bug Geocoris pallens Stal. in the hop yard and increases the abundance of the diamondback moth parasitoid Diadegma semiclausum Hellén in turnip fields (James 2003a, 2005; Orre et al. 2010). The 2-methyl butyral doxime and (Z)-3-hexenol, which were emitted from herbivore-damaged black poplar foliage, could significantly attract braconid parasitoids in the field (McCormick et al. 2014). Thus, the volatiles are expected to be ideal tools for biological control to increase natural enemy abundance and inhibit insect pests (Khan et al. 2008, Kaplan 2012). So far, synthetic HIPVs have been employed in a range of agricultural systems, including plots of cotton, hops, grape, cranberry, soybean, turnip, strawberry, and broccoli (James 2003b, James and Price 2004, Williams et al. 2008, Lee 2010, Orre et al. 2010, Mallinger et al. 2011, Rodriguez-Saona et al. 2011, Simpson et al. 2011). Recently, volatile compounds combined with traps were used to monitor the biodiversity of natural enemies in orchard ecosystems (Jones et al. 2011, 2016; Mills et al. 2016). The selection of compound or compounds is crucial in biological control strategy, which affects the attracted insect species and intensity (Kaplan 2012). In initial studies, researchers focused on the effects of commonly emitted volatiles such as MeSA, indole, cis-3-hexen-1-ol, and cis-3-hexenyl acetate, on natural enemy recruitment (James 2003a,b, 2005). A recent meta-analysis suggested that MeSA could be as a broad-spectrum attractant to lure the key natural enemy species from Anthocoridae, Coccinellidae, Syrphidae, Parasitic Hymenoptera, predaceous Heteroptera, and lacewings (Rodriguez-Saona et al. 2011). MeSA is also an active ingredient in the commercially available carnivore attractant, PredaLure (MSTRS Technologies, Ames, IA) (Kaplan 2012). There were more than 2,000 volatile compounds identified from 900 plant families (War et al. 2011), however, the roles of numerous candidate volatile compounds remain unclear. Cotton bollworm Helicoverpa armigera Hübner, cotton aphid Aphis gossypii Glover and sweetpotato whitefly Bemisia tabaci (Gennadius) are the major pests of cotton in North China (Luo et al. 2014). And pest suppression mainly depended on chemical control before the 1970s. However, the over-reliance on chemical pesticides caused a series of problems such as environmental pollution, pest resurgence and pest resistance. Since then, integrated pest management (IPM) containing biological control was adopted in China. Predators, an important component of biological control in cotton field, are a large group including spider families, predaceous insects such as ladybird beetles, green lacewing, predatory bugs (Guo 1998, Wu et al. 2005, Luo et al. 2014). The employment of synthetic HIPVs to enhance the recruitment of predator groups in cotton fields could be an effectively strategy in biological control. HIPVs such as α-pinene, α-humulene, α-farnesene, β-pinene, linalool, indole, β-ocimene, and (Z)-3-hexenyl butyrate were identified from cotton plants (McCall et al. 1994; Paré and Tumlinson 1997; Yu et al. 2006, 2007; Morawo and Fadamiro 2016). The attractiveness of these HIPVs to natural enemies was evaluated in hop yard, vineyard and alfalfa field (James 2005, Zhu et al. 2005). However, there was rare investigation on employment of the above mentioned compounds in cotton fields (Flint et al. 1979, Yu et al. 2008, 2010). In the present study, the potential attraction of nine cotton volatile compounds (α-humulene, α-pinene, α-farnesene, β-pinene, ocimene, linalool, indole, (Z)-3-hexenyl butyrate, and benzoic acid ethyl ester) and one methyl jasmonate (MeJA) to predators was investigated in cotton field. We aimed to better understand whether the application of synthetic compounds could be used as attractants in cotton fields in northern China. Materials and Methods Field experiments were conducted in a 1.5-ha cotton field at the Langfang Experimental Station of the Chinese Academy of Agriculture Sciences (CAAS), Hebei province (39°08′ N,116°23′ E) in the years of 2013 and 2014. During the growing season, the crop management without pesticides was performed identically to those of local typical operation. Experiments were performed separately from 11 June to 10 September in 2013 and from 14 July to 19 September in 2014. White sticky cards (36 × 25 cm, Pherobio Technology Co., Ltd, Beijing, China) were stapled to 50 × 25-cm plastic cards and attached by wire to bamboo sticks at a height of 2 m above the ground. Cards were baited with 1 ml (10 mg/ml diluted in lanolin (Sigma-Aldrich, St. Louis, MO) of the candidate HIPV solutions in 2-ml glass vials. Control treatments were baited only with 1 ml lanolin. In 2013, nine tested HIPVs were α-humulene, α-pinene, β-pinene, α-farnesene, indole, (Z)-3-hexenyl butyrate, MeJA, linalool, and benzoic acid ethyl ester, and in 2014, ocimene was also tested. All the chemical compounds (purity levels of ≥ 90%) were obtained from Sigma-Aldrich. Every card with a glass vial containing the tested compound or the control was suspended by wire at a height of 2 cm above the center of each card. The distance between two traps was 6 m and traps were distributed using a randomized block design. At the same time every week, there were 12 replicates for each treatment in 2013 (12 × 10 treatments) and six replicates were sampled in 2014 (6 × 11 treatments). Sticky cards were collected and replaced weekly for 12 wk (12 × 12 × 10 samples) in 2013 and for 10 wk (10 × 6 × 11 samples) in 2014. Counts were conducted for the predators captured including ladybird beetles, green lacewings, predatory bugs, and spiders. Trapped beneficial insects species or genera were identified in laboratory under a stereomicroscope, and then evaluated the attraction of HIPVs. Statistical Analysis The numbers of predators on sticky cards containing different volatile compounds (except for ocimene) were analyzed using two-way ANOVA (volatile compound and year as main factors), followed by Tukey’s HSD tests. Student’s t-test was used to compare the numbers of predators on sticky cards containing ocimene with those of control sticky cards. Prior to analysis, all data were transformed by log(x + 1) for fitting the assumption of parametric tests. All statistical analyses were executed using SPSS 19.0. Results Total 8,740 predators from 1,440 sticky traps in 2013, and 6,012 predators from 660 sticky traps in 2014 were captured. The major predators from the sticky traps were collected and analyzed in this trial over 2 yr. The predatory beetles included Propylaea japonica (Thunberg) and multicolored Asian ladybeetle Harmonia axyridis (Pallas). Green lacewings included Chrysopa spp. and Chrysoperla sinica (Tjeder). Predatory bugs included the flower bugs Orius spp., the big-eyed bug Geocoris pallidipennis (Costa), and damsel bugs Nabis spp. Spiders included Misumenops tricuspidatus (Fabricius) and Erigonidium graminicolum (Sundevall). The numbers of ladybird beetles P. japonica on sticky cards showed no difference in the interaction between the volatile compound and year (two-way ANOVAs, F9,219 = 1.20, P = 0.30), but were significant differences among volatile compounds (F9,219 = 6.50, P < 0.001). Linalool and indole obviously attracted P. japonica in the 2 yr compared with the controls (all P < 0.05), however, there was no significant difference between these two compounds (both P > 0.05). Similar results were also found in H. axyridis assays (volatile compound × year interaction: F9,219 = 0.82, P = 0.60; volatile compound: F9,219 = 3.10, P = 0.002). Indole was significantly attractive to H. axyridis in the 2 yr (both P < 0.05) (Table 1). The number of green lacewings C. sinica on sticky cards was significantly different among volatile compounds (F9,219 = 4.30, P < 0.001), but was not affected by the volatile compound × year interaction (F9,219 = 0.72, P = 0.69). The α-humulene, α-pinene and β-pinene significantly attracted green lacewings C. sinica in 2013 (all P < 0.05), whereas in 2014, C. sinica only showed significant attraction to α-pinene and β-pinene (both P < 0.05). The number of green lacewings Chrysopa spp. was affected by the volatile compound (F9,219 = 7.32, P < 0.001) and the volatile compound × year interaction (F9,219 = 2.58, P = 0.008). Chrysopa spp. was significantly attracted by indole in the 2 yr (both P < 0.05), whereas β-pinene remarkably attracted Chrysopa spp. only in 2014 (P < 0.001) (Table 1). The number of small flower bugs Orius spp. was significantly affected by the volatile compound (F9,219 = 5.44, P < 0.001) and the volatile compound × year interaction (F9,219 = 2.69, P = 0.006). Compared with the controls, the Orius spp. was significantly attracted by α-pinene and MeJA in 2 yr (all P < 0.05). Moreover, in 2013, β-pinene was significantly attractive to Orius spp. (P < 0.001) (Table 1). Table 1. Mean (±SE) number of the predators attracted by the tested volatile compounds in the years of 2013 and 2014 Predator  Year  Volatile Compounds  Benzoic acid ethyl ester  α-Farnesene  (Z)-3-Hexenyl butyrate  α-Humulene  Indole  Linalool  MeJA  α-Pinene  β-Pinene  Control  Ocimene #  Propylaea japonica  2013  0.96 ± 0.31b A  1.74 ± 0.55ab A  1.08 ± 0.30b A  0.76 ± 0.47b A  2.53 ± 0.64a A  2.72 ± 0.89a A  0.81 ± 0.28b A  1.37 ± 0.56ab A  0.99 ± 0.28b A  0.80 ± 0.20b A    2014  1.27 ± 0.42ab A  1.50 ± 0.70ab A  1.35 ± 0.46ab A  1.13 ± 0.51ab A  1.80 ± 0.75a A  2.33 ± 0.74a A  1.32 ± 0.58ab A  1.53 ± 0.70ab A  1.10 ± 0.53ab A  0.52 ± 0.36b A  1.28 ± 0.50  Harmonia axyridis  2013  0.43 ± 0.15b A  0.41 ± 0.14b A  0.51 ± 0.17b A  0.37 ± 0.13b A  1.29 ± 0.48a A  0.64 ± 0.28ab A  0.51 ± 0.14b A  0.67 ± 0.17ab A  0.43 ± 0.15b A  0.38 ± 0.14b A    2014  0.37 ± 0.19b A  0.62 ± 0.18b A  0.40 ± 0.11b A  0.67 ± 0.29ab A  1.00 ± 0.21a A  0.35 ± 0.18b A  0.55 ± 0.30ab A  0.67 ± 0.20ab A  0.72 ± 0.33ab A  0.30 ± 0.15b A  0.38 ± 0.08  Chrysoplera sinica  2013  0.26 ± 0.06c B  0.30 ± 0.09c B  0.25 ± 0.05c B  0.57 ± 0.18ab B  0.41 ± 0.29abc B  0.26 ± 0.18bc B  0.20 ± 0.04c B  0.67 ± 0.17a B  0.60 ± 0.19ab B  0.16 ± 0.04c B    2014  1.22 ± 0.33ab A  1.42 ± 0.33ab A  1.28 ± 0.24ab A  1.48 ± 0.39ab A  1.83 ± 0.62ab A  1.43 ± 0.32ab A  1.48 ± 0.38ab A  2.47 ± 0.42a A  2.13 ± 0.41a A  0.62 ± 0.56b A  1.15 ± 0.28  Chrysopa spp.  2013  0.09 ± 0.04b A  0.15 ± 0.09b A  0.13 ± 0.06b A  0.28 ± 0.19ab A  0.66 ± 0.21a A  0.36 ± 0.26ab A  0.17 ± 0.06b A  0.17 ± 0.06b A  0.26 ± 0.13b A  0.10 ± 0.08b A    2014  0.03 ± 0.03b A  0.02 ± 0.02b A  0.07 ± 0.05b A  0.02 ± 0.02b A  1.18 ± 0.46a A  0.03 ± 0.03b A  0.17 ± 0.12b A  0.18 ± 0.15ab A  0.87 ± 0.31a A  0.02 ± 0.02b A  0.02 ± 0.02  Orius spp.  2013  0.24 ± 0.04c B  0.27 ± 0.07c B  0.28 ± 0.03c B  0.32 ± 0.13c B  0.37 ± 0.15c B  0.76 ± 0.19b B  1.57 ± 0.38a B  0.91 ± 0.30ab B  1.12 ± 0.38ab B  0.23 ± 0.08c B    2014  1.78 ± 0.45bc A  1.85 ± 0.41bc A  2.33 ± 0.75bc A  2.10 ± 0.45bc A  2.13 ± 0.60bc A  1.73 ± 0.38bc A  2.78 ± 0.61b A  4.82 ± 1.12a A  2.05 ± 0.97bc A  1.17 ± 0.42c A  2.38 ± 0.72  Predator  Year  Volatile Compounds  Benzoic acid ethyl ester  α-Farnesene  (Z)-3-Hexenyl butyrate  α-Humulene  Indole  Linalool  MeJA  α-Pinene  β-Pinene  Control  Ocimene #  Propylaea japonica  2013  0.96 ± 0.31b A  1.74 ± 0.55ab A  1.08 ± 0.30b A  0.76 ± 0.47b A  2.53 ± 0.64a A  2.72 ± 0.89a A  0.81 ± 0.28b A  1.37 ± 0.56ab A  0.99 ± 0.28b A  0.80 ± 0.20b A    2014  1.27 ± 0.42ab A  1.50 ± 0.70ab A  1.35 ± 0.46ab A  1.13 ± 0.51ab A  1.80 ± 0.75a A  2.33 ± 0.74a A  1.32 ± 0.58ab A  1.53 ± 0.70ab A  1.10 ± 0.53ab A  0.52 ± 0.36b A  1.28 ± 0.50  Harmonia axyridis  2013  0.43 ± 0.15b A  0.41 ± 0.14b A  0.51 ± 0.17b A  0.37 ± 0.13b A  1.29 ± 0.48a A  0.64 ± 0.28ab A  0.51 ± 0.14b A  0.67 ± 0.17ab A  0.43 ± 0.15b A  0.38 ± 0.14b A    2014  0.37 ± 0.19b A  0.62 ± 0.18b A  0.40 ± 0.11b A  0.67 ± 0.29ab A  1.00 ± 0.21a A  0.35 ± 0.18b A  0.55 ± 0.30ab A  0.67 ± 0.20ab A  0.72 ± 0.33ab A  0.30 ± 0.15b A  0.38 ± 0.08  Chrysoplera sinica  2013  0.26 ± 0.06c B  0.30 ± 0.09c B  0.25 ± 0.05c B  0.57 ± 0.18ab B  0.41 ± 0.29abc B  0.26 ± 0.18bc B  0.20 ± 0.04c B  0.67 ± 0.17a B  0.60 ± 0.19ab B  0.16 ± 0.04c B    2014  1.22 ± 0.33ab A  1.42 ± 0.33ab A  1.28 ± 0.24ab A  1.48 ± 0.39ab A  1.83 ± 0.62ab A  1.43 ± 0.32ab A  1.48 ± 0.38ab A  2.47 ± 0.42a A  2.13 ± 0.41a A  0.62 ± 0.56b A  1.15 ± 0.28  Chrysopa spp.  2013  0.09 ± 0.04b A  0.15 ± 0.09b A  0.13 ± 0.06b A  0.28 ± 0.19ab A  0.66 ± 0.21a A  0.36 ± 0.26ab A  0.17 ± 0.06b A  0.17 ± 0.06b A  0.26 ± 0.13b A  0.10 ± 0.08b A    2014  0.03 ± 0.03b A  0.02 ± 0.02b A  0.07 ± 0.05b A  0.02 ± 0.02b A  1.18 ± 0.46a A  0.03 ± 0.03b A  0.17 ± 0.12b A  0.18 ± 0.15ab A  0.87 ± 0.31a A  0.02 ± 0.02b A  0.02 ± 0.02  Orius spp.  2013  0.24 ± 0.04c B  0.27 ± 0.07c B  0.28 ± 0.03c B  0.32 ± 0.13c B  0.37 ± 0.15c B  0.76 ± 0.19b B  1.57 ± 0.38a B  0.91 ± 0.30ab B  1.12 ± 0.38ab B  0.23 ± 0.08c B    2014  1.78 ± 0.45bc A  1.85 ± 0.41bc A  2.33 ± 0.75bc A  2.10 ± 0.45bc A  2.13 ± 0.60bc A  1.73 ± 0.38bc A  2.78 ± 0.61b A  4.82 ± 1.12a A  2.05 ± 0.97bc A  1.17 ± 0.42c A  2.38 ± 0.72  Means for each predator with the same lowercase letters in the rows and with the same uppercase letters in the same column are not significantly different (P > 0.05). Prior to analysis, all data were transformed by log(χ +1) for fitting the assumption of parametric tests. Data of each predator on sticky cards baited with different volatile compounds (except for ocimene) were analyzed using two-way ANOVA (volatile compound and year as main factors), followed by Tukey’s HSD tests. # Data of each predator was analyzed using the Student’s t-test compared with that of control in 2014. View Large The numbers of big-eyed bugs G. pallidipennis, damsel bugs Nabis spp., spiders E. graminicolum and M. tricuspiata were not affected by volatiles or volatile by year interaction [two-way ANOVAs, volatile compound (F9,219 = 0.20~0.63, all P > 0.05), the volatile compound × year interaction (F9,219 = 0.25~0.91, all P > 0.05)] (Table 2). Compared with the controls, predatory beetles (P. japonica, H. axyridis), green lacewings (C. sinica, Chrysopa spp.), predatory bugs (Orius spp., G. pallidipennis, Nabis spp.), and spiders (E. graminicolum, M. tricuspiata) were not significantly attracted by ocimene in 2014 (t18 = 0.00~1.73, all P > 0.05) (Tables 1 and 2). Table 2. Mean (±SE) number of the predators not attracted by the tested volatile compounds in the years of 2013 and 2014 Predator  Year  Volatile compounds  Benzoic acid ethyl ester  α-Farnesene  (Z)-3-Hexenyl butyrate  α-Humulene  Indole  Linalool  MeJA  α-Pinene  β-Pinene  Control  Ocimene #  Geocoris pallidipennis  2013  0.15 ± 0.15a A  0.06 ± 0.05a A  0.28 ± 0.23a A  0.03 ± 0.03a A  0.04 ± 0.02a A  0.01 ± 0.01a A  0.19 ± 0.16a A  0.05 ± 0.03a A  0.03 ± 0.02a A  0.03 ± 0.03a A    2014  0.02 ± 0.02a A  0.07 ± 0.04a A  0.03 ± 0.03a A  0.12 ± 0.04a A  0.07 ± 0.04a A  0.03 ± 0.03a A  0.08 ± 0.04a A  0.05 ± 0.04a A  0.13 ± 0.03a A  0.07 ± 0.04a A  0.03 ± 0.02  Nabis spp.  2013  0.53 ± 0.17a B  0.44 ± 0.18a B  0.47 ± 0.19a B  0.42 ± 0.16a B  0.49 ± 0.20a B  0.50 ± 0.24a B  0.33 ± 0.13a B  0.56 ± 0.21a B  0.43 ± 0.18a B  0.54 ± 0.21a B    2014  0.60 ± 0.18a A  0.65 ± 0.21a A  0.90 ± 0.46a A  0.63 ± 0.17a A  1.02 ± 0.36a A  0.77 ± 0.24a A  1.22 ± 0.49a A  0.72 ± 0.20a A  1.27 ± 0.72a A  0.52 ± 0.16a A  0.28 ± 0.15  Erigonidium graminicolum    0.19 ± 0.03a B  0.17 ± 0.03a B  0.23 ± 0.05a B  0.21 ± 0.04a B  0.18 ± 0.05a B  0.23 ± 0.05a B  0.22 ± 0.03a B  0.18 ± 0.03a B  0.29 ± 0.03a B  0.12 ± 0.03a B    2014  1.13 ± 0.26a A  1.47 ± 0.24a A  1.07 ± 0.21a A  1.32 ± 0.28a A  1.32 ± 0.24a A  1.28 ± 0.35a A  1.33 ± 0.31a A  1.22 ± 0.25a A  1.22 ± 0.17a A  1.48 ± 0.34a A  1.00 ± 0.20  Misumenops tricuspidatus  2013  0.16 ± 0.10a B  0.14 ± 0.08a B  0.14 ± 0.07a B  0.07 ± 0.03a B  0.08 ± 0.06a B  0.11 ± 0.07a B  0.10 ± 0.04a B  0.10 ± 0.06a B  0.07 ± 0.04a B  0.11 ± 0.06a B    2014  0.37 ± 0.11a A  0.25 ± 0.10a A  0.38 ± 0.16a A  0.22 ± 0.08a A  0.18 ± 0.09a A  0.27 ± 0.10a A  0.30 ± 0.08a A  0.18 ± 0.05a A  0.27 ± 0.09a A  0.18 ± 0.09a A  0.18 ± 0.08  Predator  Year  Volatile compounds  Benzoic acid ethyl ester  α-Farnesene  (Z)-3-Hexenyl butyrate  α-Humulene  Indole  Linalool  MeJA  α-Pinene  β-Pinene  Control  Ocimene #  Geocoris pallidipennis  2013  0.15 ± 0.15a A  0.06 ± 0.05a A  0.28 ± 0.23a A  0.03 ± 0.03a A  0.04 ± 0.02a A  0.01 ± 0.01a A  0.19 ± 0.16a A  0.05 ± 0.03a A  0.03 ± 0.02a A  0.03 ± 0.03a A    2014  0.02 ± 0.02a A  0.07 ± 0.04a A  0.03 ± 0.03a A  0.12 ± 0.04a A  0.07 ± 0.04a A  0.03 ± 0.03a A  0.08 ± 0.04a A  0.05 ± 0.04a A  0.13 ± 0.03a A  0.07 ± 0.04a A  0.03 ± 0.02  Nabis spp.  2013  0.53 ± 0.17a B  0.44 ± 0.18a B  0.47 ± 0.19a B  0.42 ± 0.16a B  0.49 ± 0.20a B  0.50 ± 0.24a B  0.33 ± 0.13a B  0.56 ± 0.21a B  0.43 ± 0.18a B  0.54 ± 0.21a B    2014  0.60 ± 0.18a A  0.65 ± 0.21a A  0.90 ± 0.46a A  0.63 ± 0.17a A  1.02 ± 0.36a A  0.77 ± 0.24a A  1.22 ± 0.49a A  0.72 ± 0.20a A  1.27 ± 0.72a A  0.52 ± 0.16a A  0.28 ± 0.15  Erigonidium graminicolum    0.19 ± 0.03a B  0.17 ± 0.03a B  0.23 ± 0.05a B  0.21 ± 0.04a B  0.18 ± 0.05a B  0.23 ± 0.05a B  0.22 ± 0.03a B  0.18 ± 0.03a B  0.29 ± 0.03a B  0.12 ± 0.03a B    2014  1.13 ± 0.26a A  1.47 ± 0.24a A  1.07 ± 0.21a A  1.32 ± 0.28a A  1.32 ± 0.24a A  1.28 ± 0.35a A  1.33 ± 0.31a A  1.22 ± 0.25a A  1.22 ± 0.17a A  1.48 ± 0.34a A  1.00 ± 0.20  Misumenops tricuspidatus  2013  0.16 ± 0.10a B  0.14 ± 0.08a B  0.14 ± 0.07a B  0.07 ± 0.03a B  0.08 ± 0.06a B  0.11 ± 0.07a B  0.10 ± 0.04a B  0.10 ± 0.06a B  0.07 ± 0.04a B  0.11 ± 0.06a B    2014  0.37 ± 0.11a A  0.25 ± 0.10a A  0.38 ± 0.16a A  0.22 ± 0.08a A  0.18 ± 0.09a A  0.27 ± 0.10a A  0.30 ± 0.08a A  0.18 ± 0.05a A  0.27 ± 0.09a A  0.18 ± 0.09a A  0.18 ± 0.08  Means for each predator with the same lowercase letters in the rows and with the same uppercase letters in the same column are not significantly different (P > 0.05). Prior to analysis, all data were transformed by log(χ +1) for fitting the assumption of parametric tests. Data of each predator on sticky cards baited with different volatile compounds (except for ocimene) were analyzed using two-way ANOVA (volatile compound and year as main factors), followed by Tukey’s HSD tests. # Data of each predator was analyzed using the Student’s t-test compared with that of control in 2014. View Large Discussion Several field experiments have been conducted to evaluate the attraction of plant volatiles to predators in cotton fields (Flint et al. 1979, Yu et al. 2008). In this work, nine HIPVs and one MeJA were field-tested for their attractiveness to the main predators. Positive results revealed that some of the selected synthetic compounds significantly attracted ladybird beetles (P. japonica, H. axyridis), green lacewings (C. sinica and Chrysopa spp.), and small flower bugs Orius spp. P. japonica and H. axyridis are the two most abundant species of predatory beetles in cotton in North China (Liu et al. 2000, Wu et al. 2005). Moreover, P. japonica accounts for 60–90% of all natural enemies in cotton fields during certain years (Cui 1996). Field trials showed that the population density of P. japonica is higher than that of H. axyridis during the early and middle cotton growth stages, and decreased in the later cotton growth stages (Wang et al. 2013). In the current work, we found that these two species of ladybird beetles were abundant from the middle of June to the middle of September. The attractiveness of linalool and indole to P. japonica and H. axyridis were only evaluated using electroantennogram (EAG) and behavior (olfactometer) techniques under laboratory conditions (Han and Chen 2002, Qi et al. 2008). Our data indicated that linalool attracted P. japonica and indole significantly attracted P. japonica, H. axyridis in cotton fields over 2 yr. Moreover, we found that indole attracted more P. japonica than H. axyridis during the early and middle cotton growing stages, whereas more H. axyridis than P. japonica were attracted by indole in the later cotton growing season (unpublished data). Chrysopa spp. (Chrysopa septempunctata Wesmael, Chrysopa shansiensis Kuwayama, Chrysopa phyllochroma Wesmael and Chrysopa formosa Brauer) and C. sinica are predominant chrysopids observed in the field of North China (Guo 1998, Liu et al. 2000). It was reported that Chrysopa spp. and Chrysoperla spp. were attracted by plant volatiles, the combination of plant volatile (MeSA) and lacewing pheromone (iridodial) (Flint et al. 1979; James 2003a, 2006; James and Price 2004; Zhu et al. 2005; Zhang et al. 2006; Tóth et al. 2009; Lee 2010; Jones et al. 2011, 2016). Moreover, plant volatiles could significantly enhance female C. phyllochroma oviposition to retain individuals and establish populations (Xu et al. 2015). Laboratory data showed that indole could elicit strong electrophysiological and behavioral responses of C. septempunctata (Han and Chen 2002). Field trapping tests demonstrated that 100 mg of indole could significantly attract adult Chrysopa oculata L., but did not attract adult Chrysoperla carnea (Say) in the alfalfa filed (Zhu et al. 2005). Similarly, our data showed that indole significantly attracted Chrysopa spp., but did not attract C. sinica. A possible explanation for this phenomenon is that the former is a carnivore as an adult, whereas the latter is carnivorous only as a larva (Aldrich and Zhang 2016). Adult C. sinica typically feeds on pollen, honeydew and nectar. Thus, indole might mainly be used as a signal by lacewings for locating prey. Attraction of α-pinene and β-pinene to C. sinica in our tests were consistent with the results reported by Zhang et al (2012b), who suggested that α-pinene and β-pinene were two novel compounds released from the damaged persimmon leaves with high emission amounts and they were considered to be important compounds for recruiting C. sinica. Although pinene was previously reported to be unattractive to C. carnea adults in cotton (Flint et al. 1979), α-pinene could attract C. sinica adults in this study. MeSA and iridodial are considered as two strong attractants for green lacewings (Neuroptera: Chrysopidae) (Jones et al. 2011, 2016). So, we speculated that indole, α-pinene and β-pinene could be combined with MeSA and/or iridodial to exert better biological control of this predatory group. Due to their long occurrence time, high population density, diverse spectrum of prey species, and high predation rate, Orius bugs are considered as a promising agent for controlling pests (Zhou and Lei 2002, Ahmadi et al. 2009, Zhang et al. 2012a). Field trapping tests showed that Orius spp. were attracted to a variety of plant volatiles including benzaldehyde, MeSA, nonanal, octylaldehyde, (Z)-3-hexen-1-ol, (Z)-3-hexenyl acetate, 3,7-dimethyl,1,3,6-octatriene, and nonanal+(Z)-3-hexen-1-ol in the hops, cotton and strawberry field (James 2003a, 2005; Yu et al. 2008; Lee 2010). Our results revealed that sticky traps baited with α-pinene or MeJA captured more Orius spp. than that of the control traps. These findings were in agreement with the previous studies that Orius spp. significantly preferred α-pinene and MeJA in olfactometer or pot assays (Arab et al. 2007, Stepanycheva et al. 2014, Gebreziher and Nakamutan 2016b). In the current study, Nabis spp. and G. pallidipennis were not attracted by any tested HIPVs. Thus, it will be worthwhile to select effective volatiles to be used as attractants for the genus Orius spp. Some tested HIPVs attracted the predators only in one of the 2 yr, such as β-pinene attracting Orius bugs and Chrysopa spp., as well as α-humulene attracting C. sinica. Kaplan (2012) pointed out that spatiotemporal heterogeneity in the sex ratios, mating status, and age structures of field populations is likely correlated with the strength of responses to plant volatiles. Other exogenous factors such as the climate, geographical situation, plant species, and HIPV application technique also affect the responses of insects (Zhu et al. 2005, Schröder and Hilker 2008, Kaplan 2012). In this work, weather might be one of the main factors influencing on our results. Actually, weather factors manipulated the occurrence of insects and the infestation levels of pests in fields that eventually affected attractiveness of specific compounds during the seasons. Recently, mirid bugs have become the key pests in China due to the wide adoption of Bt cotton and decrease of insecticides in cotton fields (Lu et al. 2010). And considerable study is now focused on how to control this pest through biological control (Lu and Wu 2008, Luo et al. 2011). The predaceous insects of mirid bugs included small flower bugs (Orius similis Zheng, Orius minutes (L.)), big-eyed bug G. pallidipennis, damsel bugs Nabis sinoferus Hsiao, Nabis stenoferus Hsiao, and green lacewings C. sinica, C. formosa, C. septempunctata (Luo et al. 2014). Thus, the application of HIPVs to increase abundance of predators and attract/repel mirid bugs, may contribute to biological control of this pest in the future. Geng (2012) showed that propanoic acid butyl ester and 1-ethyl-4-(2-methylpropyl)-benzene from mungbean plants could effectively trap plant bugs Apolygus lucorum (Meyer-Dür) in cotton fields. How to deploy the HIPVs to control mirid bugs at certain temporal/phenological stages of the cotton would be explored in next work. As a strategy of IPM, the control effects of HIPVs must be reliable and stable. Therefore, more trials need to be conducted to verify the effectiveness of HIPVs over multiple years, and mixtures of volatiles should be tested if a single HIPV is not sufficiently attractive (Maeda et al. 2015; Gebreziher and Nakamuta 2016a,b). In addition, due to the limited experiment fields there was relatively close trap spacing (6 m) in our study. The spatial range of particular volatiles detected by natural enemy may depend on natural enemy species, cotton cultivars, and release rate of volatile compounds, etc. The effects of the perceived volatile ‘blend’ by predators on attractiveness of each of the single compounds will be investigated within this set-up. And the impact of some highly-attractive compounds on attraction of other chemicals deployed in the same field plot should be also evaluated. Furthermore, the exact densities of HIPV lures in field at specific cotton stages should be made clear to develop practical semiochemical formulations and its application in IPM. 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Published: Feb 1, 2018

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