Arthropod Abundance and Diversity in Transgenic Bt Soybean Author(s): Huilin Yu, Yunhe Li, Xiangju Li and Kongming Wu Source: Environmental Entomology, 43(4):1124-1134. Published By: Entomological Society of America URL: http://www.bioone.org/doi/full/10.1603/EN13337

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.

BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.

TRANSGENIC PLANTS AND INSECTS

Arthropod Abundance and Diversity in Transgenic Bt Soybean HUILIN YU, YUNHE LI, XIANGJU LI,

AND

KONGMING WU1

State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China

Environ. Entomol. 43(4): 1124Ð1134 (2014); DOI: http://dx.doi.org/10.1603/EN13337

ABSTRACT Before the commercialization of any insect-resistant genetically modiÞed crop, it must be subjected to a rigorous premarket risk assessment. Here, possible effects of growing of transgenic Cry1Ac soybean on arthropod communities under Þeld conditions were assessed for 2 yr and quantiÞed in terms of arthropod community indices including the ShannonÐWeaver diversity index, richness index, and dominance index. Our results showed no signiÞcant differences of diversity, richness, or dominant indices for Bt soybean compared with the recipient cultivar, conventional soybean, or sprayed conventional soybean. Conventional soybean treatment with insecticide had an adverse effect on the arthropod community after spraying, but arthropod community diversity recovered quickly. Bt soybean had no negative effect on the dominant distribution of subcommunities, including sucking pests, other pests, predators, parasitoids, and others except for lepidopteran pests. The dominance distribution of lepidopteran pests decreased signiÞcantly in Bt soybean because of the signiÞcant decrease in the numbers of Spodoptera litura (F.) and Ascotis selenaria Schiffermu¨ ller et Denis compared with the recipient cultivar. Our results showed that there were no negative effects of Cry1Ac soybean on the arthropod community in soybean Þeld plots in the short term. KEY WORDS Bt soybean, Cry1Ac, diversity, arthropod community

Use of transgenic crops that express insecticidal proteins derived from Bacillus thuringiensis Berliner (Bt) has revolutionized production agriculture on a global scale since Bt maize and Bt cotton were Þrst commercially planted in the United States in 1996. They have not only provided an effective tool for pest control, but also provided many social, environmental, and economic beneÞts such as decreasing environmental pollution owing to reduced use of chemical pesticides and increased farm income (Wu et al. 2008a, Brookes and Barfoot 2013). For example, the direct global farm income beneÞt from Bt cotton in 2011 was US$6.6 billion. Within this amount, 73% of the farm income gain derived from yield gains (less pest damage), and the balance (27%) from reduced expenditure on crop protection (spraying of insecticides) (Brookes and Barfoot 2013). Bt crops (Bt cotton and Bt maize) have been consistently adopted by farmers of many countries. In 2012, total plantings of Bt crops in the world increased to 69.9 million hectares (James 2012). However, their deployment has sparked debates with regard to potential ecological effects on nontarget organisms, especially effects on their abundance and diversity in the Þeld (Torres and Ruberson 2006, Rose and Dively 2007, Dhillon and Sharma 2013). In the past two decades, a large number of laboratory and Þeld studies on the potential ecological effects of Bt crops 1

Corresponding author, e-mail: [email protected].

on nontarget organisms were reported for promoting the sustainable utilization of transgenic Bt crops. Soybeans are a primary source of vegetable oil and protein for use in food, feed, and industrial applications (Conner et al. 2004). A number of lepidopteran pests have seriously affected the agronomics and economics of soybean production, and also have affected yield and quality of grain and seed. Globally important pests on soybean include velvetbean caterpillar Anticarsia gemmatalis Hu¨ bner, corn earworm Helicoverpa zea (Boddie), soybean looper Pseudoplusia includens (Walker), and beet armyworm Spodoptera exigua (Hu¨ bner) (Boldt et al. 1975, Harish 2008). In 2006, velvetbean caterpillar and soybean looper caused 33% yield losses of soybean in Georgia (Roberts and McPherson 2008). Musser et al. (2013) showed that corn earworm was the most costly insect pest in the surveyed states of the southern United States in 2012, costing growers more than US$20 per acre in direct costs and yield loss. In China, lepidopteran pests, including common cutworm Spodoptera litura (F.), beet armyworm S. exigua, and cotton bollworm Helicoverpa armigera Hu¨ bner, cause 15% losses of soybean yield in average outbreak years, reaching ⬎50% in serious years (Xu and Liu 2003). Bt insecticidal activity is highly selective and limited to a narrow species range, such as Cry1 and Cry2 with speciÞc activity against lepidopteran pests, and Cry3 active against coleopteran pests (Malone et al. 2008). The mode of action of the Bt protein is to selectively

0046-225X/14/1124Ð1134$04.00/0 䉷 2014 Entomological Society of America

August 2014

YU ET AL.: ARTHROPOD ABUNDANCE IN BT SOYBEAN FIELD

bind to speciÞc receptors on the epithelial surface of the midgut of larvae of target insect species, leading to death of larvae through pore formation, cell burst, and subsequent septicemia (Sanahuja et al. 2011). Although most Bt soybean varieties have not been commercially planted so far, Cry1A* transgenic soybean lines have been developed (Walker et al. 2000, Miklos et al. 2007), and some Bt soybean lines have provided good resistance against lepidopteran insects (McPherson and MacRae 2009a,b). Soybean line MON87701RR2Y expressing both Cry1Ac and Cp4 EPSPS proteins conferring insect resistance and herbicide tolerance traits, respectively, was developed by Monsanto Company (St. Louis, MO). It provided a high-level control against An. gemmatalis and P. includens in laboratory and Þeld studies (Bernardi et al. 2012). MON87701RR2Y was registered for commercial use in Brazil in 2011, and in 2013 it was approved for commercial planting in Brazil (James 2012). In 2013, the soybean line was approved by the Chinese Ministry of Agriculture for import for food and feed use, and it may have the potential for commercial planting in China in the near future. The efÞciency of MON87701RR2Y for control of four major target pests that frequently occur in Chinese soybean Þelds was evaluated, and the results indicated that the transgenic soybean line exhibits high resistance to the pests besides H. armigera (Yu et al. 2013). In the current study, Þeld surveys were conducted to investigate its potential impacts on nontarget arthropods at the population level. Materials and Methods Plants. Bt soybean line MON87701RR2Y and the corresponding untransformed parental cultivar A5547 were used in the study. Besides expressing the Cry1Ac gene, the transgenic plants also express a Cp4 epsps gene derived from Agrobacterium tumefaciens conferring tolerance to glyphosate. Both types of soybean seeds were supplied by the Monsanto Far East Limited Beijing Representative OfÞce. A soybean variety of ZhongHuang13 (“ZH13”), a widely grown variety in the local region, was also included as a control because it may provide a good reference for comparison with the Monsanto soybean varieties. The seeds of ZH13 were provided by the Institute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS). Field Experiment Design. This study was conducted at the Agriculture Experiment Station of CAAS located at Langfang in Hebei province (39⬚ 08⬘ N, 116⬚ 23⬘ E) in 2010 and 2011, and where Þeld trials of Bt soybean are permitted in Hebei Province in China. The planting dates were 20 June 2010, and 5 July 2011. Four treatments were set up: 1) MON87701RR2Y (Bt soybean), 2) A5547 (recipient cultivar), 3) ZH13 (conventional soybean) without insecticide, and 4) ZH13 with insecticide application (sprayed conventional soybean), in which an emulsion of 4.5% ␭-cyhalothrin (Weihai Hanfu Biological and Chemical Medication Co. Ltd., Weihai, Shangdong, China) was sprayed at a rate of 500 ml/ha on 1 September 2010 and

1125

20 August 2011, mainly for lepidopteran and sucking pest control. There were four replicates (plots) of each soybean treatment, with the exception of conventional and sprayed conventional soybean with three replications in 2010. We used a randomized complete block design, with each plot of 180 m2 (15 m in length by 12 m in width). In each plot, soybeans were sown in 26 rows with line spacing of 0.40 m, and plant spacing of 0.12 m. Between the soybean plots, isolation belts planted with maize (5 m in width) were set up. During the growing period, crop management was according to common local agricultural practices. Arthropod Survey. Above-ground arthropods were surveyed every 7Ð10 d by direct visual observations. In each plot, Þve points were chosen along a diagonal, and 20 soybean plants were randomly selected at each point. The selected plants were gently turned over, and the numbers of different visible arthropods on the surface of each plant were quickly counted. Any unknown species were sampled and put into a 5-ml plastic tube individually, and were brought to the laboratory for identiÞcation under an insect anatomical lens. The experiments were conducted from 31 July to 25 September with 9 investigations in 2010, and from 10 August to 20 October with 10 investigations in 2011. Based on the observation, the arthropod community structure parameters (MenhinickÕs index, ShannonÐWeaver index, and SimpsonÕs index) were calculated. In addition, the number of arthropods, mean number of each arthropod subcommunity, the dominance distribution of arthropod subcommunities, and mean number of main lepidopteran pests were compared between Bt and non-Bt treatments. s , Data Analysis. MenhinickÕs richness index, D ⫽ 冑N where s is the number of different species represented in the total sample, and N is the total number of individuals, was calculated as a measure of species richness in arthropod community (Menhinick 1964). The ShannonÐWeaver diversity index, H ⫽ ⫺兺 Pi Ln Pi, where Pi is the proportion of a given species in the total sample, was calculated as a measure of species diversity (Shannon and Weaver 1949). The SimpsonÕs dominance index was calculated as C ⫽ 兺(Pi)2 (Simpson 1949). The dominance distribution is the percentage of each subcommunity among the total communities. The arthropods observed in soybean plots were split into pests, natural enemies, and other species. The pest subcommunity was divided into lepidopteran pests, sucking pests, and other pests. The natural enemies subcommunity was separated into parasitoids and predators. The ShannonÐWeaver diversity indices, SimpsonÕs dominance indices, MenhinickÕs richness indices, mean number of each arthropod subcommunity, the number of arthropods, dominance distribution of each subcommunity, and mean number of main lepidopteran insects from different treatments were all analyzed using one-way analysis of variance (ANOVA), followed by TukeyÕs HSD (honestly significance difference) tests. Before analysis, the data of dom-

1126 Table 1.

ENVIRONMENTAL ENTOMOLOGY The arthropods separated into four guilds were observed in soybean plots in 2010 and 2011

Subcommunity Pests Lepidoptera insects

Sucking pests Other pests Predators Parasitoids Others

Vol. 43, no. 4

Family Noctuidae (owlet moths), Pyralidae (snout moths), Sphingidae (hawk moths), Geometridae (geometer moths), Olethreutidae (tortrix moths), Plutellidae (plutellid moths), Arctiidae (tiger moths), Lymantridae (tussock moths), Limacodidae (slug moths), Lycaenidae (gossamer-winged butterßies), and Pieridae (pierid butterßies). Aphididae (aphids), Thripidae (thrips), Tetranychidae (spider mites), Pseudococcidae (mealybugs), Cicadellidae (leafhoppers), Aleyrodidae (whiteßies), Pentatomidae (stink bugs), Miridae (mirid bugs), Coreidae (coreid bugs), and Plataspidae (shield bugs) Curculionidae (snout beetles), Lariidae (bean weevils), Chrysomelidae (leaf beetles), Elateridae (click beetles), Acrididae (grasshoppers), Gryllidae (true crickets), Agromyzidae (leaf-miner ßies), Rutelidae (scarab beetles), and Melolonthidae (scarab beetles) Chrysopidae (lacewings), Coccinellidae (ladybirds), Anthocoridae (ßower bugs), Nabidae (damsel bugs), Lygaeidae (true bugs), Miridae, Vespidae (wasps), Syrphidae (hoverßies), Thomisidae (ßower crab spiders), Linyphiidae (sheet weavers), and Lycosidae (wolf spiders) Braconidae, Ichneumonidae, Aphidiidae, Aphelinidae, and Encyrtidae Calliphoridae (blow ßies), Formicidae (ants), Neriidae (long-legged ßies), Tipulidae (crane ßies), and Chironomidae (midges)

inance distribution were transformed by arcsine 冑X, while all other data were transformed by log(x ⫹ 1) for Þtting the assumption of parametric tests. The P value (⬍0.05) was used to determine signiÞcant differences. All statistical analyses were executed using SPSS, v. 13.0 (SPSS Inc., Chicago, IL). Results Abundance of Arthropods and Arthropod Subcommunities in Soybean Plots. We observed 63,158 total arthropods over 2 yr (43,059 and 20,099 in 2010 and 2011, respectively) in Bt, recipient cultivar, conventional, and sprayed conventional soybeans. In each year, the number of arthropods in Bt, recipient cultivar, conventional, and sprayed conventional soybean varieties were not signiÞcantly different (Table 2).The arthropods observed on the respective soybean plots were separated into four guilds, including pests, predators, parasitoids, and others. In total, 51 families of insects and spiders were observed on the experimental plots (Table 1). There was no signiÞcant difference of mean numbers of arthropod subcommunities (sucking pests, other pests, predators, parasitoids, and other) in Bt soybean compared with other non-Bt treatments except for lepidopteran insects. Two-year study showed that mean number of lepidopteran insects in Bt soybean was signiÞcantly less than recipient cultivar and conventional soybean (Table 2). Diversity and Species Richness. Arthropod community indices (MenhinickÕs richness index D, ShannonÐ Weaver diversity index H, and SimpsonÕs dominance index C) for the respective plots during the 2 yr are shown in Table 3. The results revealed no signiÞcant differences among Bt, recipient cultivar, conventional soybean, and sprayed conventional soybean plots. The temporal dynamics of these indices of arthropod community diversity for Bt soybean showed no signiÞcant differences compared with the recipient cultivar, conventional soybean, and sprayed conventional soybean plots in 2010 (TukeyÕs HSD test: P ⬎ 0.05, each comparison; Fig. 1) The diversity index for

sprayed conventional soybean was signiÞcantly lower than those of other treatments on 1 September 2010 (F ⫽ 53.27; df ⫽ 3,13; P ⬍ 0.0001). In 2011, there were no signiÞcant differences for diversity indices for Bt soybean compared with recipient cultivar and conventional soybean plots (TukeyÕs HSD tests: P ⬎ 0.05, each comparison), except that on 21 September the diversity for Bt soybean was signiÞcantly lower than that for conventional soybean (F ⫽ 3.62; df ⫽ 3,15; P ⫽ 0.046). Sprayed conventional soybean had signiÞcantly lower diversity indices on 22 and 31 August than those for conventional soybean, recipient cultivar, and Bt soybean after spraying insecticides (22 August: F ⫽ 7.25; df ⫽ 3,15; P ⫽ 0.005; 31 August: F ⫽ 9.01; df ⫽ 3,15; P ⫽ 0.002; Fig. 1). The temporal dynamics of dominance indices of Bt soybean did not differ signiÞcantly among soybean lines in 2010 (P ⬎ 0.05, each comparison), with the one exception of 1 September 2010 (Fig. 2). Bt soybean, recipient cultivar, and conventional soybean plots on 1 September 2010 had signiÞcantly lower dominance indices in comparison with sprayed conventional soybean (F ⫽ 12.19; df ⫽ 3,13; P ⫽ 0.001). In 2011, there were no signiÞcant differences for dominance indices between Bt soybean and recipient cultivar through the whole growing season. However, sprayed conventional soybean on 22 and 31 August 2011 had signiÞcantly higher dominance indices than other soybean treatments (22 August: F ⫽ 7.31; df ⫽ 3,15; P ⫽ 0.005; 31 August: F ⫽ 12.67; df ⫽ 3,15; P ⬍ 0.0001). On 21 September 2011, Bt soybean had a signiÞcantly higher dominance index than conventional soybean (F ⫽ 6.34; df ⫽ 3,15; P ⫽ 0.008), and its dominance index was not higher than those of recipient cultivar and sprayed conventional soybean. On 27 September 2011, the dominance indices for Bt soybean and recipient cultivar were signiÞcantly higher than that for sprayed conventional soybean (F ⫽ 9.27; df ⫽ 3,15; P ⫽ 0.002), while there were no signiÞcant differences between conventional soybean and sprayed conventional soybean (Fig. 2). The temporal dynamics of richness indices for Bt soybean were showed in Fig. 3. There were no sig-

Data are shown as mean ⫾ SE with the different lowercase letters in same column representing signiÞcant differences (P ⬍ 0.05). Prior to analysis, the data were transformed by log (x⫹1). A one-way ANOVA was conducted, followed by TukeyÕs HSD tests.

2.125 ⫾ 0.610a 3.450 ⫾ 1.574a 2.800 ⫾ 1.030a 1.100 ⫾ 0.277a F ⫽ 0.92; df ⫽ 3,39; P ⫽ 0.45 10.250 ⫾ 3.001a 11.65 ⫾ 3.299a 8.125 ⫾ 2.526a 9.025 ⫾ 4.828a F ⫽ 0.99; df ⫽ 3,39; P ⫽ 0.41 54.075 ⫾ 6.647a 61.550 ⫾ 11.082a 41.250 ⫾ 4.301a 40.150 ⫾ 9.033a F ⫽ 2.08; df ⫽ 3,39; P ⫽ 0.12 421.900 ⫾ 76.496a 494.850 ⫾ 87.229a 398.125 ⫾ 64.793a 359.650 ⫾ 57.359a F ⫽ 1.27; df ⫽ 3,39; P ⫽ 0.30

2011 Bt Recipient Conventional Sprayed Conventional

496.050 ⫾ 81.161a 611.775 ⫾ 92.429a 480.800 ⫾ 64.045a 421.25.⫾64.191a F ⫽ 0.77; df ⫽ 3,39; P ⫽ 0.52

6.975 ⫾ 3.092b 39.150 ⫾ 14.148a 28.300 ⫾ 9.118a 8.175 ⫾ 1.490b F ⫽ 6.05; df ⫽ 3,39; P ⫽ 0.002

0.725 ⫾ 0.383a 1.125 ⫾ 0.475a 2.200 ⫾ 1.872a 3.150 ⫾ 2.101a F ⫽ 0.36; df ⫽ 3,39; P ⫽ 0.78

18.417 ⫾ 1.871a 23.361 ⫾ 5.047a 32.444 ⫾ 4.825a 22.232 ⫾ 6.263a F3,35 ⫽ 1.51; df ⫽ 3,35; P ⫽ 0.23 4.324 ⫾ 2.088a 4.361 ⫾ 1.466a 2.426 ⫾ 0.923a 3.370 ⫾ 1.386a F ⫽ 0.34; df ⫽ 3,35; P ⫽ 0.80 94.179 ⫾ 17.472a 97.565 ⫾ 14.712a 109.482 ⫾ 11.607a 100.083 ⫾ 10.826a F ⫽ 0.55; df ⫽ 3,35; P ⫽ 0.65 843.370 ⫾ 234.255a 863.074 ⫾ 232.567a 1394.296 ⫾ 270.635a 935.639 ⫾ 127.685a F ⫽ 1.90; df ⫽ 3,35; P ⫽ 0.15 2010 Bt Recipient Conventional Sprayed Conventional

972.167 ⫾ 236.066a 1023.389 ⫾ 233.988a 1668.870 ⫾ 274.039a 1119.917 ⫾ 141.178a F ⫽ 2.30; df ⫽ 3,35; P ⫽ 0.10

10.833 ⫾ 1.821c 32.583 ⫾ 4.443b 128.630 ⫾ 11.864a 56.889 ⫾ 24.963b F ⫽ 16.70; df ⫽ 3,35; P ⬍ 0.0001

0.759 ⫾ 0.273a 2.444 ⫾ 1.374a 1.370 ⫾ 0.528a 1.704 ⫾ 1.419a F ⫽ 0.81; df ⫽ 3,35; P ⫽ 0.50

Predators Other pests Sucking pests

Mean no. of each arthropod subcommunity

Parasitoids

Others

YU ET AL.: ARTHROPOD ABUNDANCE IN BT SOYBEAN FIELD

Lepidopteran pests

Pests The no. of arthropods Line

Table 2. The number of arthropods and the mean number of each arthropod subcommunity per 100 plants for each sampling date in Bt, recipient cultivar, conventional, and sprayed conventional soybean plots in 2010 and 2011

August 2014

1127

niÞcant differences of richness indices among different soybean treatments in the 2-yr investigations (P ⬎ 0.05, each comparison), except on 1 September 2010 and 22 and 31 August 2011. SigniÞcantly lower richness indices in sprayed conventional soybean were found in comparison with that of other soybean treatments on 1 September 2010 (F ⫽ 12.22; df ⫽ 3,13; P ⫽ 0.001) and 22 and 31 August 2011 (22 August: F ⫽ 19.38; df ⫽ 3,15; P ⬍ 0.0001; 31 August: F ⫽ 3.71; df ⫽ 3,15; P ⫽ 0.042; respectively). Dominance Distribution. The sucking pests were the uppermost dominant pests in pest subcommunity in a 2-yr study. There were no signiÞcant differences for dominance of sucking pests and other pests among soybean lines and treatments. Predators displayed the second-highest level of dominance among the guilds. The dominance of predators in Bt soybean plots was not remarkably higher than those on recipient cultivar, conventional soybean, and sprayed conventional soybean plots in 2010 and 2011. There was no significant difference of dominance of parasitoids and other arthropods among different soybean treatments (Table 4). The dominance distribution of lepidopteran pests in Bt soybean plots was signiÞcantly lower than on recipient cultivar plots in 2010 and 2011, and sprayed conventional soybean had signiÞcantly lower dominance of lepidopteran pests compared with conventional soybean in the 2-yr study (Table 4). Abundance of Main Lepidopteran Pests in Soybean Plots. Ten species of lepidopteran pests were shown in Table 5 and the densities of Ascotis selenaria Schiffermuller et Denis and S. litura occurring in Bt soybean or sprayed conventional soybean plots were signiÞcantly less than in recipient cultivar and conventional soybean plots. In addition, the densities of Pieris rapae (L.) in Bt soybean and sprayed conventional soybean plots were lower than in recipient cultivar and conventional soybean plots in 2011, while there were no signiÞcant difference for other lepidopteran pests in Bt soybean than in recipient cultivar, conventional soybean, and sprayed conventional soybean plots (Table 5). Discussion To date, studies of the inßuence of Bt crops on community structure and diversity of arthropods mostly have focused on Bt cotton, Bt maize, and Bt rice. There is no report on the effects of Bt soybean on arthropod communities because Bt soybean varieties have been developed recently. We studied the effects of Bt soybean on arthropod communities, and quantiÞed community structure by MenhinickÕs richness indices, ShannonÐWeaver diversity, and SimpsonÕs dominance indices. We found that abundance, species richness, diversity of arthropods, and dominance distribution of nontarget arthropods in plots of Bt soybean did not differ signiÞcantly from those with the recipient cultivar and conventional soybean. Therefore, we conclude that there were no marked negative effects of Bt soybean on the arthropod community. Our overall result was in agreement with those of

1128

ENVIRONMENTAL ENTOMOLOGY

Vol. 43, no. 4

Table 3. Diversity indices for arthropod communities in Bt-transgenic, recipient cultivar, conventional, and sprayed conventional soybeans in 2010 and 2011 Year

Line

D

H

C

2010

Bt Recipient Conventional Sprayed conventional

2011

Bt Recipient Conventional Sprayed conventional

0.608 ⫾ 0.075a 0.611 ⫾ 0.077a 0.486 ⫾ 0.058a 0.466 ⫾ 0.074a F ⫽ 1.00; df ⫽ 3,35; P ⫽ 0.40 0.759 ⫾ 0.056a 0.744 ⫾ 0.049a 0.834 ⫾ 0.078a 0.707 ⫾ 0.091a F ⫽ 0.62; df ⫽ 3,39; P ⫽ 0.61

1.117 ⫾ 0.112a 1.228 ⫾ 0.121a 1.216 ⫾ 0.109a 1.190 ⫾ 0.114a F ⫽ 0.18; df ⫽ 3,35; P ⫽ 0.91 1.362 ⫾ 0.091a 1.433 ⫾ 0.080a 1.575 ⫾ 0.075a 1.397 ⫾ 0.094a F ⫽ 1.21; df ⫽ 3,39; P ⫽ 0.32

0.485 ⫾ 0.046a 0.495 ⫾ 0.053a 0.497 ⫾ 0.061a 0.499 ⫾ 0.060a F ⫽ 0.01; df ⫽ 3,35; P ⫽ 1.00 0.405 ⫾ 0.043a 0.390 ⫾ 0.040a 0.308 ⫾ 0.027a 0.366 ⫾ 0.031a F ⫽ 1.40; df ⫽ 3,39; P ⫽ 0.30

D is the MenhinickÕs richness index, H is the ShannonÐWeaver diversity index, and C is the Simpson dominance index. Data are shown as mean ⫾ SE, with different lowercase letters in same column representing signiÞcant differences (P ⬍ 0.05). Prior to analysis, the data were transformed by log(x ⫹ 1). A one-way ANOVA was conducted, followed by TukeyÕs HSD tests.

Fig. 1. Temporal dynamics of ShannonÐWeaver diversity indices, H, for arthropod community diversity in plots containing different lines of soybean and treatments at Langfang, Hebei Province, China, in 2010 and 2011. Data are shown as mean ⫾ SE with different lowercase letters for the same date for the same year representing signiÞcant differences (P ⬍ 0.05). Before analysis, the data were transformed by log(x ⫹ 1). A one-way ANOVA was conducted, followed by TukeyÕs HSD tests.

August 2014

YU ET AL.: ARTHROPOD ABUNDANCE IN BT SOYBEAN FIELD

1129

Fig. 2. Temporal dynamics of SimpsonÕs dominance indices, C, for arthropod community diversity in plots containing different lines of soybean and treatments at Langfang, Hebei Province, China, in 2010 and 2011. Data are shown as mean ⫾ SE with different lowercase letters for the same date for the same year representing signiÞcant differences (P ⬍ 0.05). Before analysis, the data were transformed by log(x ⫹ 1). A one-way ANOVA was conducted, followed by TukeyÕs HSD tests.

previous Þeld studies showing that there was little or no change in the arthropod community on Bt crops compared with controls in terms of population abundance, density, species richness, and diversity of nontarget arthropods (Lopez et al. 2005, Li et al. 2007, Balog et al. 2010, Mann et al. 2010). Although the population of lepidopteran insects on Bt soybean was signiÞcantly different than that of the recipient cultivar, results of this 2-yr study showed that numbers of lepidopteran pests on Bt soybean were lower than those on the recipient cultivar, which is in agreement with results showing that transgenic Bt crops effectively resist lepidopteran pests (Wu et al. 2008a). Our results showed that Bt soybean exhibited decreased population numbers of S. litura and A. selenaria. S. litura is a major lepidopteran pest on soybean in China (Xu and Liu 2003). In general, transgenic Bt cotton expressing Cry1Ac proved not to be effective

against Spodoptera spp. (Lalitha et al. 2012, Selvi et al. 2012). Wan et al. (2008) showed that there was no signiÞcant difference in S. litura larval population densities on Bt cotton lines GK19 and BG1560 expressing the Cry1Ac protein in comparison with a non-Bt cotton Þeld. Results of our study were not consistent with those of Wan et al. (2008). Transgenic Cry1Ac soybean (MON87701RR2Y) exhibited limited resistance to S. litura neonates in a laboratory experiment (Yu et al. 2013). The decrease of S. litura population numbers in Bt soybean Þeld plots maybe due to suppression of neonates by Bt protein. Moreover, we found that the numbers of A. selenaria on Bt soybean decreased in comparison with the recipient cultivar, although there was no report that Cry1Ac is toxic to A. selenaria; we need more experiments to study this possible effect. As expected, because of the use of chemical insecticide, the occurrence of lepidopteran insects in

1130

ENVIRONMENTAL ENTOMOLOGY

Vol. 43, no. 4

Fig. 3. Temporal dynamics of MenhinickÕs richness indices, D, for arthropod community diversity in plots containing different lines of soybean and treatments at Langfang, Hebei Province, China, in 2010 and 2011. Data are shown as mean ⫾ SE with different lowercase letters for the same date for the same year representing signiÞcant differences (P ⬍ 0.05). Before analysis, the data were transformed by log(x ⫹ 1). A one-way ANOVA was conducted, followed by TukeyÕs HSD tests.

sprayed conventional soybean plots was signiÞcantly decreased in comparison with unsprayed conventional soybean. The sucking pests such as aphid, leafhopper, whiteßy, and mirid bug are dominant species in soybean Þelds. Our data showed no signiÞcant difference in their abundances in Bt soybean plots compared with those in the recipient cultivar. Our results were consistent with previous data showing that the population densities of aphids and thrips did not differ between Bt and non-Bt maize Þelds by 6-yr survey in Germany (Schorling and Freier 2006). Likewise, no signiÞcant difference was detected between Bt and non-Bt rice Þelds in population densities of six sucking pest species including planthoppers, Sogatella furcifera (Horva´th), Nilaparvata lugens (Stål), and Laodelphax striatellus (Falle´ n), and three species of leafhoppers, Nephotettix cincticeps (Uhler), Thaia subrufa (Motschulsky), and Recilia dorsalis (Motschulsky) (Chen at al. 2006, 2012). However, a long-term survey indicated that the

population of mirid bug have gradually increased and evolved into key pests with wide adoption of Bt cotton in China (Lu et al. 2010), while it seems that it is caused by decline of insecticide use against target lepidoptera pests, but not directly by Bt cotton. A treatment of insecticide spraying soybean was included in the current study, and a short-term effect was detected on population densities of the sucking pests just after spraying. Subsequently, the populations of the sucking pests quickly recovered and it may be because of the fact that the experimental plots were relatively small. This may demonstrate larger scale plots are useful for such studies. Bt soybean did not affect abundance of predator and parasitoid, which was in accord with those of previous reports (Pilcher et al. 2005, Torres and Ruberson 2005, reviewed by Yu et al. 2011, Devos et al. 2012). In Bt maize varieties derived from the event MON810 in Spain, the abundance of plant-dwelling predators and the activity and density of soil-dwelling

Pests Other pests

Predators

Parasitoids

0.015 ⫾ 0.009b 0.089 ⫾ 0.037a 0.066 ⫾ 0.023a 0.021 ⫾ 0.004b F ⫽ 3.18; df ⫽ 3,39; P ⫽ 0.04

冑X. A one-way ANOVA

0.831 ⫾ 0.017a 0.001 ⫾ 0.001a 0.127 ⫾ 0.051a 0.020 ⫾ 0.003a 0.004 ⫾ 0.001a 0.780 ⫾ 0.034a 0.002 ⫾ 0.001a 0.106 ⫾ 0.040a 0.018 ⫾ 0.003a 0.005 ⫾ 0.002a 0.813 ⫾ 0.024a 0.004 ⫾ 0.003a 0.096 ⫾ 0.010a 0.016 ⫾ 0.003a 0.006 ⫾ 0.002a 0.848 ⫾ 0.022a 0.005 ⫾ 0.003a 0.107 ⫾ 0.020a 0.017 ⫾ 0.006a 0.003 ⫾ 0.001a F ⫽ 1.27; df ⫽ 3,39; P ⫽ 0.30 F ⫽ 0.68; df ⫽ 3,39; P ⫽ 0.57 F ⫽ 0.74; df ⫽ 3,39; P ⫽ 0.54 F ⫽ 0.51; df ⫽ 3,39; P ⫽ 0.68 F ⫽ 0.49; df ⫽ 3,39; P ⫽ 0.69

F ⫽ 0.39; df ⫽ 3,35; P ⫽ 0.76

0.000 ⫾ 0.000a 0.194 ⫾ 0.116a

0.222 ⫾ 0.184a 0.037 ⫾ 0.037a

0.000 ⫾ 0.000a 0.037 ⫾ 0.037a

F ⫽ 1.26; df ⫽ 3,35; P ⫽ 0.31 F ⫽ 1.93; df ⫽ 3,35; P ⫽ 0.44

1.111 ⫾ 0.868a

F ⫽ 2.36; df ⫽ 3,35; P ⫽ 0.09 F ⫽ 1.65; df ⫽ 3,35; P ⫽ 0.20

0.056 ⫾ 0.056a 0.167 ⫾ 0.110a

3.037 ⫾ 2.667a

2.000 ⫾ 1.074a 0.296 ⫾ 0.130a

Spayed conventional

F ⫽ 9.04; df ⫽ 3,35; P ⬍ 0.0001 F ⫽ 1.695; df ⫽ 3,35; P ⫽ 0.19 F ⫽ 10.88; df ⫽ 3,35; P ⬍ 0.0001 F ⫽ 2.75; df ⫽ 3,35; P ⫽ 0.06 F ⫽ 0.62; df ⫽ 3,35; P ⫽ 0.61

0.806 ⫾ 0.625a

0.333 ⫾ 0.167a

2.185 ⫾ 0.547a 1.111 ⫾ 0.596a

2010

0.306 ⫾ 0.108b 6.148 ⫾ 1.944a 5.000 ⫾ 1.118a 2.185 ⫾ 1.032a 3.361 ⫾ 0.658a 6.390 ⫾ 1.610a 3.963 ⫾ 1.163a 2.926 ⫾ 0.635a 4.083 ⫾ 0.466c 12.806 ⫾ 2.101b 108.259 ⫾ 21.490a 46.519 ⫾ 29.901b 1.167 ⫾ 0.333a 1.778 ⫾ 0.445a 3.297 ⫾ 0.759a 1.074 ⫾ 0.328a 1.056 ⫾ 0.901a 0.722 ⫾ 0.271a 1.407 ⫾ 0.680a 0.556 ⫾ 0.478a

1.926 ⫾ 0.487a 0.444 ⫾ 0.249a

0.556 ⫾ 0.273a 0.083 ⫾ 0.059a

Conventional

0.175 ⫾ 0.106a

0.175 ⫾ 0.075a 0.150 ⫾ 0.085a

Recipient

2011

0.125 ⫾ 0.085b 0.125 ⫾ 0.067a

3.000 ⫾ 1.801a 0.125 ⫾ 0.100a

Spayed conventional

F ⫽ 4.20; df ⫽ 3,39; P ⫽ 0.01 F ⫽ 1.22; df ⫽ 3,39; P ⫽ 0.32 F ⫽ 2.89; df ⫽ 3,39; P ⫽ 0.049 F ⫽ 2.20; df ⫽ 3,39; P ⫽ 0.11 F ⫽ 1.30; df ⫽ 3,39; P ⫽ 0.29 5.250 ⫾ 3.243a 0.100 ⫾ 0.100b F ⫽ 6.69; df ⫽ 3,39; P ⫽ 0.001 0.650 ⫾ 0.340a 0.425 ⫾ 0.303a F ⫽ 1.03; df ⫽ 3,39; P ⫽ 0.39

0.950 ⫾ 0.333a 0.475 ⫾ 0.340a 1.600 ⫾ 1.328b 2.075 ⫾ 0.500a 0.025 ⫾ 0.025a

0.075 ⫾ 0.053a 0.275 ⫾ 0.195a F ⫽ 0.59; df ⫽ 3,39; P ⫽ 0.63

0.700 ⫾ 0.542a 0.225 ⫾ 0.108a F ⫽ 1.15; df ⫽ 3,39; P ⫽ 0.34 0.175 ⫾ 0.106a 0.200 ⫾ 0.104a F ⫽ 0.84; df ⫽ 3,39; P ⫽ 0.48

Conventional

0.050 ⫾ 0.033b 1.600 ⫾ 0.569a 1.175 ⫾ 0.382a 0.200 ⫾ 0.082a 3.675 ⫾ 2.943a 1.400 ⫾ 1.104a 5.075 ⫾ 4.991b 27.350 ⫾ 12.927a 14.125 ⫾ 7.957a 0.850 ⫾ 0.340a 0.975 ⫾ 0.259a 2.675 ⫾ 0.957a 0.050 ⫾ 0.033a 0.000 ⫾ 0.000a 0.075 ⫾ 0.038a

0.075 ⫾ 0.038a

0.025 ⫾ 0.025a 0.025 ⫾ 0.025a

Bt

YU ET AL.: ARTHROPOD ABUNDANCE IN BT SOYBEAN FIELD

Data are shown as mean ⫾ SE with the different lowercases letters in the same horizontal line representing signiÞcant differences (P ⬍ 0.05). Prior to analysis, the data were transformed by log(x ⫹ 1). A one-way ANOVA was conducted, followed by TukeyÕs HSD tests.

Lamprosema indicate F. Matsumuraeses Phaseoli Matsumura Clanis bilineata tsingtauica Mell A. selenaria H. armigera S. litura S. exigua Etiella zinckenella Treitschke P. rapae Argyrogramma agnata Staudinger

Recipient

Bt

The number of main lepidopteran pests per 100 soybean plants in Bt, recipient cultivar, conventional, and sprayed conventional soybean plots in 2010 and 2011

Species

Table 5.

Others

0.016 ⫾ 0.004c 0.813 ⫾ 0.037a 0.001 ⫾ 0.000a 0.133 ⫾ 0.027a 0.007 ⫾ 0.004a 0.031 ⫾ 0.008a 0.044 ⫾ 0.010b 0.784 ⫾ 0.037a 0.003 ⫾ 0.001a 0.128 ⫾ 0.026a 0.008 ⫾ 0.005a 0.034 ⫾ 0.011a 0.096 ⫾ 0.016a 0.801 ⫾ 0.031a 0.001 ⫾ 0.000a 0.080 ⫾ 0.015a 0.002 ⫾ 0.001a 0.023 ⫾ 0.005a 0.045 ⫾ 0.015b 0.827 ⫾ 0.018a 0.002 ⫾ 0.001a 0.098 ⫾ 0.013a 0.004 ⫾ 0.002a 0.024 ⫾ 0.008a F ⫽ 8.12; df ⫽ 3,35; P ⬍ 0.0001 F ⫽ 0.23; df ⫽ 3,35; P ⫽ 0.88 F ⫽ 0.83; df ⫽ 3,35; P ⫽ 0.49 F ⫽ 1.20; df ⫽ 3,35; P ⫽ 0.33 F ⫽ 0.76; df ⫽ 3,35; P ⫽ 0.53 F ⫽ 0.48; df ⫽ 3,35; P ⫽ 0.70

Sucking pests

Data are shown as mean ⫾ SE with the different lowercase letters in same column representing signiÞcant differences (P ⬍ 0.05). Prior to analysis, the data were transformed by arcsin was conducted, followed by TukeyÕs HSD tests.

2011 Bt Recipient Conventional Sprayed Conventional

2010 Bt Recipient Conventional Sprayed Conventional

Lepidopteran pests

Dominance distribution of arthropod subcommunities in Bt, recipient cultivar, conventional, and sprayed conventional soybean plots in 2010 and 2011

Line

Table 4.

August 2014 1131

1132

ENVIRONMENTAL ENTOMOLOGY

predators did not differ from those of non-Bt isogenic varieties (Albajes et al. 2012). Moreover, Bt crops could signiÞcantly increase in populations of beneÞcial insects and enhance their biocontrol services because of the decreased use of insecticide (Wu and Guo 2005, Lu et al. 2012). Lu et al. (2012) showed that the abundance of three types of generalist arthropod predators (ladybirds, lacewings, and spiders) markedly increased in Bt cotton Þelds on the basis of data from 1990 to 2010 at 36 sites in six provinces of northern China. Minor changes in abundance of a few natural enemies in Bt maize and cotton were explained by the change in target lepidopteran pest populations (Naranjo et al. 2005). Generalist predators such as green lacewings and lady beetles that preferentially feed on aphids are unlikely to be affected in Bt Þelds (Romeis et al. 2006). Only the population densities of specialized predators and parasitoid wasps decreased owing to poor quality and lower density of lepidopteran pests in Bt crop Þelds (Wu and Guo 2005), while there were no uniform effects of Bt cotton, maize, and potato on the functional guilds of nontarget arthropods, and insecticide effects were much larger than those of Bt crops (Wolfenbarger et al. 2008). Chemical insecticides not only control pests, but also kill other nontarget arthropods, with an especially large negative impact on natural enemies that provide biological control of pests. Thus, arthropod biodiversity is threatened by frequent use of chemical insecticides (Liu et al. 2008, Amalin et al. 2009, Park and Lee 2009, Isenring 2010). The different types of insecticides sprayed inßuenced the magnitude of differences of arthropod communities (Shi et al. 2012). Our results indicated that insecticide had negative effects on arthropod community diversity and dominance immediately after spraying, but arthropod community in sprayed conventional soybean could recover quickly, outcomes that were not consistent with Shi et al.Õs (2012) conclusion that the arthropod communities in soybean treated with insecticides recovered slowly or failed to recover. The major explanation may be because of the characteristics of ␭-cyhalothrin. Although it is a broad-spectrum insecticide effective at low rates of application, its half-life on plant surfaces is 5 d, on soil ⬇9 d, and it can be broken down by sunlight (National Pesticide Information Center [NPIC] 2001). Moreover, it is safe for some arthropods, like the parasitoid Trichogramma japonicum Ashmead (Zhao et al. 2012). Besides contact and stomach action, it has a repellent property. With spraying, some arthropodsÑsuch as whiteßy, planthopper, and leafhopperÑ could easily escape to other soybean Þelds nearby. Moreover, the plot sizes we used were relatively small. After rapid degradation of ␭-cyhalothrin, the arthropods could easy to move back gradually. However, rainfall was the other explanation for differing results. At 10:00 p.m. on 1 September 2010, there was a 14-mm rainfall, and from 1 to 20 September, there was 73 mm of rainfall (data from our experiment station). It rained immediately after conventional soybean was sprayed with insecticide, which inßuenced

Vol. 43, no. 4

its efÞciency for controlling pests and also caused the prompt recovery of the arthropod community. The number of arthropod species found in our study was clearly lower than that of herbicide-tolerant soybeans reported for the Langfang experiment station (Wu et al. 2008b). While part of the explanation may be the differing transgenes, another may be the difference of sampling strategies. We performed our study only by visual observation. Some kinds of small arthropods such as Ichneumonid insects ßy well, and some such as spiders escape easily; these were difÞcult to distinguish without a microscope, and hence difÞcult to record. The effects of Bt soybean on abundance and diversity of the nontarget arthropods require more study. Acknowledgments We thank Yiping Li (Northwest A&F University, Shaanxi Province, China) and Wenliang Li (China Agricultural University, Beijing, China) for identifying species of arthropods; Hongbo Niu and Xinhao Yang (Institute of Plant Protection, CAAS, China) for helping to count the arthropods. We also thank Monsanto Company for providing us with soybean seeds. We thank Eric Hallerman (Virginia Polytechnic Institute and State University, Blacksburg, VA) for critical comments on the draft manuscript. This research was supported by the National Natural Science Funds (31321004) and the Key Project for Breeding Genetic ModiÞed Organisms (2011ZX08012-004)

References Cited Albajes, R., G. P. Farino´ s, M. Perez-Hedo, M. de la Poza, B. Lumbierres, F. Ortego, X. Pons, and P. Castanˇ a. 2012. Post-market environmental monitoring of Bt maize in Spain: Non-target effects of varieties derived from the event MON810 on predatory fauna. Span. J. Agric. Res. 10: 977Ð985. Amalin, D. M., J. E. Pen˜ a, R. Duncan, J. Leavengood, and S. Koptur. 2009. Effects of pesticides on the arthropod community in the agricultural area near the Everglades National Park. Proc. Fla. State Hort. Soc. 122: 429 Ð 437. Balog, A., J. Kiss, D. Szekeres, A´ . Sze´na´ si, and V. Marko´ d. 2010. Rove beetle (Coleoptera: Staphylinidae) communities in transgenic Bt (MON810) and near isogenic maize. Crop Prot. 29: 567Ð571. Bernardi, O., G. S. Malvestiti, P. M. Dourado, W. S. Oliveira, S. Martinelli, G. U. Berger, G. P. Head, and C. Omoto. 2012. Assessment of the high-dose concept and level of control provided by MON87701⫻MON89788 soybean against Anticarsia gemmatalis and Pseudoplusia includes (Lepidoptera: Noctuidae) in Brazil. Pest Manage. Sci. 68: 1083Ð1091. Boldt, P. E., K. D. Biever, and C. M. Ignoffo. 1975. Lepidopteran pests of soybeans: consumption of soybean foliage and pods and development time. J. Econ. Entomol. 68: 480 Ð 482. Brookes, G., and P. Barfoot. 2013. GM crops: Global socioeconomic and environmental impacts 1996Ð2011. PG Economics Ltd, United Kingdom. (http://www.europabio.org/ sites/default/. . . /2013globalimpactstudyÞnalreport.pdf). Chen, M., G. Y. Ye, H. W. Yao, X. X. Chen, S. Z. Shen, C. Hu, and S. K. Datta. 2006. Field assessment of the effects of transgenic rice expressing a fused gene of cry1Ab and cry1Ac from Bacillus thuringiensis Berliner on nontarget

August 2014

YU ET AL.: ARTHROPOD ABUNDANCE IN BT SOYBEAN FIELD

planthopper and leafhopper populations. Environ. Entomol. 35: 127Ð134. Chen, Y., J. C. Tian, W. Wang, Q. Fang, Z. R. Akhtar, Y. F. Peng, C. Hu, Y. Y. Guo, Q. S. Song, and G. Y. Ye. 2012. Bt rice expressing Cry1Ab does not stimulate an outbreak of its non-target herbivore, Nilaparvata lugens. Transgenic Res. 21: 279 Ð291. Conner, T., E. H. Paschal, A. Barbero, and E. Johnson. 2004. The challenges and potential for future agronomic traits in soybeans. AgBioForum 7: 47Ð50. Devos, Y., A. D. Schrijver, P. D. Clercq, J. Kiss, and J. Romeis. 2012. Bt-maize event MON88017 expressing Cry3Bb1 does not cause harm to non-target organism. Transgenic Res. 21: 1191Ð1214. Dhillon, M. K., and H. C. Sharma. 2013. Comparative studies on the effects of Bt-transgenic and non-transgenic cotton on arthropod diversity, seed cotton yield and bollworm control. J. Environ. Biol. 34: 67Ð73. Harish, G. 2008. Studies on incidence and management of defoliator pests of soybean. M.S. thesis, University of Agricultural Sciences, Dharwad, India. Isenring, R. 2010. Pesticides reduce biodiversity. Pesticides New 88. June 2010. (http://www.pan-uk.org/pestnews/ Issue/pn88/PN88_p4-7.pdf) (26 March 2013). James, C. 2012. Global Status of Commercialized Biotech/GM Crops in 2012. International Service for the Acquisition of Agri-Biotech Applications, Ithaca, New York, NY. Lalitha, C., T. Muralikrishna, S. Sravani, and K. Devaki. 2012. In vitro evaluation of native Bacillus thuringiensis isolates against II instar Spodoptera litura (Fabricius). Ann. Plant Protect. Sci. 20: 88 Ð90. Li, F. F., G. Y. Ye, Q. Wu, Y. F. Peng, and X. X. Chen. 2007. Arthropod abundance and diversity in Bt and non-Bt rice Þelds. Environ. Entomol. 36: 646 Ð 654. Liu, C. Z., G. Wang, and L. Yan. 2008. Effects of imidacloprid on arthropod community structure and its dynamics in alfalfa Þeld. Chin. J Appl. Ecol. 18: 2379 Ð2383. Lopez, M. D., J. R. Prasifka, D. J. Bruck, and L. C. Lewis. 2005. Utility of ground beetle species in Þeld tests of potential nontarget effects of Bt crops. Environ. Entomol. 34: 1317Ð1324. Lu, Y. H., K. M. Wu, Y. Y. Jiang, B. Xia, P. Li, H. Q. Feng, K.A.G. Wychhuys, and Y. Y. Guo. 2010. Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science 328: 1151Ð1154. Lu, Y. H., K. M. Wu, Y. Y. Jiang, Y. Y. Guo, and N. Desneux. 2012. Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487: 362Ð 365. Malone, L. A., A.M.R. Gatehouse, and B.I.P. Barratt. 2008. Beyond Bt: alternative strategies for insect-resistant genetically modiÞed crops, pp. 357Ð 417. In J. Romeis, A. M. Shelton, and G. G. Kennedy (eds.), Integration of insectresistant genetically modiÞed crops with IPM programs. Springer, Berlin, Germany. Mann, R. S., R. S. Gill, A. K. Dhawan, and P. S. Shera. 2010. Relative abundance and damage by target and non-target insects on Bollgard and Bollgard II cotton cultivars. Crop Prot. 29: 793Ð 801. McPherson, R. M., and T. C. MacRae. 2009a. Assessing Lepidopteran abundance and crop injury in soybean lines exhibiting a synthetic Bacillus thuringiensis Cry1A gene. J. Entomol. Sci. 44: 120 Ð131. McPherson, R. M., and T. C. MacRae. 2009b. Evaluation of transgenic soybean exhibiting high expression of a synthetic Bacillus thuringiensis Cry1A transgene for suppress-

1133

ing Lepidopteran population densities and crop injury. J. Econ. Entomol. 102: 1640 Ð1648. Menhinick, E. P. 1964. A comparison of some species-individuals diversity indices applied to samples of Þeld insects. Ecology 45: 859 Ð 861. Miklos, J. A., M. F. Alibhai, S. A. Bledig, D. C. Connor-Ward, A. G. Gao, B. A. Holmes, K. H. Kolacz, V. T. Kabuye, T. C. MacRae, M. S. Paradise, et al. 2007. Characterization of soybean exhibiting high expression of a synthetic Bacillus thuringiensis Cry1A transgene that confers a high degree of resistance to lepidopteran pests. Crop Sci. 47: 148 Ð157. Musser, F. R., A. L. Catchot, Jr., J. A. Davis, D. A. Herbert, Jr., G. M. Lorenz, T. Reed, D. D. Reisig, and S. D. Stewart. 2013. 2012 soybean insect losses in the Southern US. Midsouth Entomol. 6: 12Ð24. Naranjo, S. E., G. Head, and G. Dively. 2005. Field studies assessing arthropod non-target effects in Bt transgenic crops: Introduction. Environ. Entomol. 34: 1178 Ð1180. (NPIC) National Pesticide Information Center. 2001. Lambda-cyhaothrin. Oregon State University, 310 Weniger Hall, Corvallis, Oregon 97331. (http://npic.orst.edu/ ingred/aifact.html). Park, H. H., and J. H. Lee. 2009. Impact of pesticide treatment on an arthropod community in the Korean rice ecosystem. J. Ecol. Field Biol. 32: 19 Ð25. Pilcher, C. D., M. E. Rice, and J. J. Obrycki. 2005. Impact of transgenic Bacillus thuringiensis corn and crop phenology on Þve nontarget arthropods. Environ. Entomol. 34: 1302Ð 1316. Roberts, P. M., and R. M. McPherson. 2008. Soybean insects, pp. 33Ð35. In P. Guillebeau, N. Hinkle, and P. Roberts (eds.), Summary of losses from insect damage and costs of control in Georgia 2006, vol. 106. University of Georgia College of Agriculture and Environmental Science Miscellaneous Publication, Georgia. Romeis, J., M. Meissle, and F. Bigler. 2006. Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat. Biotechnol. 24: 63Ð71. Rose, R., and G. P. Dively. 2007. Effects of insecticidetreated and lepidopteran-active Bt transgenic sweet corn on the abundance and diversity of arthropods. Environ. Entomol. 36: 1254 Ð1268. Sanahuja, G., R. Banakar, R. M. Twyman, T. Capell, and P. Christou. 2011. Bacillus thuringiensis: a century of research, development and commercial applications. Plant Biotechnol. J. 9: 283Ð300. Schorling, M., and B. Freier. 2006. Six-year monitoring of non-target arthropods in Bt maize (Cry 1Ab) in the European corn borer (Ostrinia nubilalis) infestation area Oderbruch (Germany). J. Verbr. Lebensm. 1: 106 Ð108. Selvi, C., S. V. Krishnamoorty, and P. Sivasubramanian. 2012. BioefÞcacy of Bt cotton hybrids containing the fusion gene Cry1Ac-1Ab against Spodoptera litura. Indian J. Plant Protect. 40: 22Ð25. Shannon, C. E, and W. Weaver. 1949. The mathematical theory of communication. University of Illinois Press, Chicago, IL. Shi, S. S., Y. B. Gao, L. S. Zang, W. Yang, and J. W. Gao. 2012. Effects of several insecticides on the arthropod community in soybean Þelds. Chin J. Appl. Entomol. 49: 1249 Ð 1254. Simpson, E. H. 1949. Measurement of diversity. Nature 163: 688. Torres, J. B., and J. R. Ruberson. 2005. Canopy- and grounddwelling predatory arthropods in commercial Bt and non-Bt cotton Þelds: patterns and mechanisms. Environ. Entomol. 34: 1242Ð1256.

1134

ENVIRONMENTAL ENTOMOLOGY

Torres, J. B., and J. R. Ruberson. 2006. Abundance and diversity of ground-dwelling arthropods of pest management importance in commercial Bt and non-Bt cotton Þelds. Ann. Appl. Biol. 150: 27Ð39. Walker, D. R., J. N. All, R. M. McPherson, H. R. Boerma, and W. A. Parrott. 2000. Field evaluation of soybean engineered with a synthetic cry1Ac transgene for resistance to corn earworm, soybean looper, velvetbean caterpillar (Lepidoptera: Noctuidae), and lesser cornstalk borer (Lepidoptera: Pyralidae). J. Econ. Entomol. 93: 613Ð 622. Wan, P., K. M. Wu, M. S. Huang, D. Yu, and J. P. Wu. 2008. Population dynamics of Spodptera litura (Lepidoptera: Noctuidae) on Bt cotton in the Yangtze River Valley of China. Environ. Entomol. 37: 1043Ð1048. Wolfenbarger, L. L., S. E. Naranjo, J. G. Lundgren, R. J. Bitzer, and L. S. Watrud. 2008. Bt crop effects on functional guilds of non-target arthropods: A meta-analysis. PLoS ONE 3: 1Ð11. Wu, K. M., and Y. Y. Guo. 2005. The evolution of cotton pest management practices in China. Annu. Rev. Entomol. 50: 31Ð52. Wu, K. M., Y. H. Lu, H. Q. Feng, Y. Y. Jiang, and J. Z. Zhao. 2008a. Suppression of cotton bollworm in multiple crops

Vol. 43, no. 4

in China in areas with Bt toxin-containing cotton. Science 5896: 1676 Ð1678. Wu, Q., D. L. Peng, and Y. F. Peng. 2008b. Effects of herbicide tolerant soybean on biodiversity of non-target arthropods communities. Acta Ecol. Sin. 28: 2622Ð2628. Xu, S. M., and X. R. Liu. 2003. Survey of soybean pests. J. Beihua Univ. 4: 478 Ð 483. Yu, H. L., Y. H. Li, and K. M. Wu. 2011. Risk assessment and ecological effects of transgenic Bacillus thuringiensis crops on non-target organisms. J. Integr. Plant Biol. 53: 520 Ð538. Yu, H. L., Y. H. Li, X. J. Li, J. Romeis, and K. M. Wu. 2013. Expression of Cry1Ac in transgenic Bt soybean lines and their efÞciency in controlling lepidopteran pests. Pest Manage. Sci. 69: 1326 Ð1333. Zhao, X. P., C. X. Wu, Y. H. Wang, T. Chang, L. P. Chen, R. X. Yu, and Q. Wang. 2012. Assessment of toxicity risk of insecticides used in rice ecosystem on Trichogramma japonicum, an egg parasitoid of rice lepidopterans. J. Econ. Entomol. 105: 92Ð101. Received 6 December 2013; accepted 19 April 2014.