Transgenic Bt potato and conventional insecticides for Colorado potato beetle management: comparative efficacy and non-target impacts

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1 Entomologia Experimentalis et Applicata 100: , Kluwer Academic Publishers. Printed in the Netherlands. 89 Transgenic Bt potato and conventional insecticides for Colorado potato beetle management: comparative efficacy and non-target impacts Gary L. Reed 1, Andrew S. Jensen 1, Jennifer Riebe 2, Graham Head 3 &JianJ.Duan 3, 1 Oregon State University, Hermiston Agricultural Research & Extension Center, Hermiston, OR 97838, USA; 2 Hybritech Seed International Inc., Boise, ID 83706, USA; 3 Monsanto Company, Ecological Technology Center, 800 North Lindbergh, St. Louis, MO 63167, USA; Author for correspondence ( Jian.J.Duan@monsanto.com) Accepted: April 10, 2001 Key words: Bacillus thuringiensis, Leptinotarsa decemlineata, Cry3Aa, potato, pest management, biotechnology, risk assessment Abstract Field studies were conducted in 1992 and 1993 in Hermiston, Oregon, to evaluate the efficacy of transgenic Bt potato (Newleaf R, which expresses the insecticidal protein Cry3Aa) and conventional insecticide spray programs against the important potato pest, Leptinotarsa decemlineata (Say), Colorado potato beetle (CPB), and their relative impact on non-target arthropods in potato ecosystems. Results from the two years of field trials demonstrated that Newleaf potato plants were highly effective in suppressing populations of CPB, and provided better CPB control than weekly sprays of a microbial Bt-based formulation containing Cry3Aa, bi-weekly applications of permethrin, or early- and mid-season applications of systemic insecticides (phorate and disulfoton). When compared with conventional potato plants not treated with any insecticides, the effective control of CPB by Newleaf potato plants or weekly sprays of a Bt-based formulation did not significantly impact the abundance of beneficial predators or secondary potato pests. In contrast to Newleaf potato plants or microbial Bt formulations, however, bi-weekly applications of permethrin significantly reduced the abundance of several major generalist predators such as spiders (Araneae),big-eyedbugs (Geocorussp.), damsel bugs (Nabidsp.), and minute pirate bugs (Orius sp.), and resulted in significant increases in the abundance of green peach aphid (GPA), Myzus persicae (Sulzer) vector of viral diseases, on the treated potato plots. While systemic insecticides appeared to have reduced the abundance of some plant sap-feeding insects such as GPA, lygus bugs, and leafhoppers, early and mid-season applications of these insecticides had no significant impact on populations of the major beneficial predators. Thus, transgenic Bt potato, Bt-based microbial formulations and systemic insecticides appeared to be compatible with the development of integrated pest management (IPM) against other potato pests such as GPA because these CPB control measures have little impact on major natural enemies. In contrast, the broad-spectrum pyrethroid insecticide (permethrin) is less compatible with IPM programs against GPA and the potato leafroll viral disease. Introduction Advances in plant molecular biology and biochemistry in the past two decades have allowed the development of modern genetic engineering technology that offers the potential to improve agronomic traits of crop cultivars. Several species of crops have been modified with genetic engineering methods to express genes from various subspecies of Bacillus thuringiensis Berliner (Bt) that encode Crystalline (Cry) proteins (δ-endotoxins). These Cry proteins confer effective protection to the crop plants from damage by certain phytophagous insect pests. Currently, a number of genetically modified Bt crop cultivars are widely used by farmers as alternatives to chemical insecticides for control of economically important insect pests in both developed and developing countries such as the United

2 90 States, Canada, and China (see review in Lewellyn et al., 1994; Persley, 1996; Federici, 1998). Cry proteins have been the primary (if not sole) active components of Bt-based microbial insecticides, which have been used as foliar sprays in agricultural and forest settings for several decades. Partly because of their selectivity and short half-life, Bt Cry proteins (as well as cell bodies and spores) are generally considered to have fewer adverse impacts on the environment than many broad-spectrum and persistent chemical insecticides (see review in Schnepf et al., 1998). Although the intrinsic insecticidal activity of Bt protein toxins is not altered in the transgenic crops, the continuous expression of Bt Cry proteins in large portions of the plant throughout most of the growing seasons has raised some environmental concerns (see reviews in Williamson, 1992; Jepson et al., 1994). One such concern centers on the possible impact of this novel pest control technology on various groups of non-target organisms of ecological and economic value through crop plant-based food chains (Riddick & Barbosa, 1998; Riddick et al., 1998; Hilbeck et al., 1998a, b, 1999). This concern (together with others, e.g., in Williamson, 1992; Poppy, 2000) has become a contentious debate among scientists, pest control practitioners, and farmers, as well as other public interest groups. To date, however, debates over potential environmental risks associated with large scale use of transgenic Bt crops have been based largely on philosophical arguments, conjectural ecological theories, and limited laboratory studies; ecological studies with robust field data are lacking. To resolve the current debates and enable a scientifically-sound risk assessment to be conducted, data from multiple-year field studies are critically needed. In this article, we report the results of a field study conducted in Oregon, USA to evaluate the efficacy and potential non-target impacts of a transgenic Bt (Newleaf R ) potato cultivar and different insecticides against important arthropods, both targets and non-targets, dwelling on potato plants. The major arthropod pests of potatoes in Oregon include the Colorado potato beetle (CPB), Leptinotarsa decemlineata and the green peach aphid (GPA), Myzus persicae (Sulzer). GPA and CPB require specific annual control measures to prevent economic damage. In addition to CPB and GPA, there are several other groups of pests including the potato aphid (PA), Macrosiphum euphorbiae (Thomas), wireworms, Limonius sp. (Coleoptera: Elateridae), flower beetles (Coleoptera: Cetoniidae), loopers, Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae), potato leafhoppers, Empoasca sp. (Homoptera: Cicadellidae), thrips, Frankliniella occidentalis and Thrips tabaci (Thysanoptera: Thripidae), plant bugs, Lygus sp. (Hemiptera:Miridae), and the two spotted spider mite, Tetranychus urticae. Unlike the major pests, these pests require fewer specific control measures because they cause less consistent damage and are often controlled by chemical sprays used against CPB and GPA. Materials and methods The research was conducted in a 3-acre potato field in 1992 and 1993 at the Hermiston Agricultural Research and Extension Center of Oregon State University, Hermiston, Oregon, USA. Agronomic procedures such as fertilization and irrigation for growing potatoes were the same as used by local farmers except that all experimental plots were hand planted, seeded cm apart on rows spaced 86 cm apart. Control regimes. Six control regimes (treatments) were evaluated: 1. No control measures (NOC) No insecticides (or other control measures) were applied to conventional (non-transgenic) Russet Burbank potato plants. 2. Systemic insecticide treatment (SYS) Systemic insecticides, phorate (Thimet R 15G, kg ai/acre) and disulfoton (Di-Syston-8 R, 1.52 kg ai/acre), were applied in-furrow to conventional Russet Burbank potato plants in early June (at planting) and July (at cultivating), respectively. 3. Pyrethroid insecticide treatment (PYR) Permethrin (Pounce R 3.2 EC, kg ai/acre) was applied to conventional Russet Burbank potatoes as foliar sprays every 2 weeks beginning in late June, with a total of five applications. 4. Microbial Bt treatment (MBT) Microbial Bacillus thuringiensis Berliner subsp. tenebrionis pesticide (M-trak R, l/acre) was applied to conventional Russet Burbank potato plants as foliar sprays weekly beginning in late June, with a total of nine applications for CPB control. 5. Transgenic Bt potato alone (TBT) The insecticidal Cry3Aa protein trait of the transgenic Bt Russet Burbank (Newleaf R ) potato plants was used as the only means of control of CPB. The Newleaf potato contains a single Cry3Aa gene encoding

3 91 full-length Cry3Aa protein, which is effective in controlling larvae and adults of CPB. 6. Transgenic Bt potato treated with systemic insecticides (TBTSYS) Plots of transgenic Bt (Newleaf) potato plants were treated with infurrow applications of the systemic insecticides, phorate (Thimet 15 G, kg ai/acre) and disulfoton (Di-Syston-8, 1.52 kg ai/acre). The rate and timing of phorate and disulfoton application were the same as the systemic insecticide treatment for conventional potato plants. General information on the active ingredient, insecticidal properties (selectivity) and mode of delivery of these pesticides is summarized in Table 1. Experimental plot design. The 3-acre experimental field was divided into 36 experimental plots (each 337 m 2 ), and 6 6 Latin square designs were used to compare effects of the six insect control regimes. Each experimental plot (i.e., experimental unit) consisted of the treatment area (16 16 m 2 in 1992 and m 2 in 1993) of potato plants, which was bordered on all sides by an outer walkway and by untreated conventional Russet Burbank potato plants. An entire experimental plot including walkways and conventional Russet Burbank potato plants was m 2 for both 1992 and Inside each treatment plot, the inner 5 5m 2 was restricted from entry during the season to prevent operational effects on yields. The 5 5m 2 yield plot was surrounded by an inner walkway consisting of an unplanted row on the sides and 1 m of unplanted row at the ends of each 5-m row to allow for arthropod sampling. Arthropod sampling. Visual counts and beat cloths were used to estimate the abundance of major arthropods on potato plants. Arthropod samples were taken twice each week with each of the two sampling methods from mid June until late August when potato tubers were fully grown and ready for harvest. Visual counts were used only for estimating the abundance of CPB adults, egg masses and larvae in each treatment plot. This method involved counting the number of CPB adults, egg masses, and larvae on one side of two rows (16 plants per row) at each sampling time without disturbing the plant vegetation. In addition, defoliation of potato plants by CPB larvae and adults was scored. Sampling with beating cloths involved inserting a square cloth (71 71 cm 2 ) under one side of two plants, gently folding the plants over the cloth, and then striking the plants eight times with a beating stick. All arthropods falling on the cloth were counted. Arthropods sampled by the beating-cloth method included active stages (adults and/or larvae or nymphs) of various groups of phytophagous insect pests such as flower beetles, loopers, aphids, leafhoppers, thrips, and plant bugs, and predators such as big-eyed bugs, damsel bugs, minute pirate bugs, ladybird beetles, lacewings, and spiders. At each time (once every 2 weeks), two potato plants were sampled from each treatment plot. In cases where the taxonomic identity of the arthropod species or groups could not be confirmed in the field, voucher specimens were collected and identified later by expert taxonomists. Data analysis. We focused primarily on the effects of different insect pest control regimes on the total abundance of each arthropod species or group sampled during the entire growing season. Total counts of each arthropod species or group sampled during the entire sampling season were analyzed by ANOVA (with Latin square design). Logarithmic transformations were used to stabilize the variation among treatments for the ANOVA. Transformed means of the total abundance for each arthropod species and/or group were compared statistically using Tukey Kramer multiple mean comparison procedures; untransformed means are presented. All statistical calculations were performed using JMP Statistical Discovery software (SAS, 1995). In addition, patterns of population change during the season in the major non-target potato pest M. persicae and the most abundant predators were also examined graphically by plotting the number of individual insects observed on beat cloths at each sampling time. Results Effects on CPB. Data from visual counts (Figure 1) showed that the seasonal abundance of CPB varied significantly among insect control regimes in both 1992 (for adults: F = 20.27, df = 5/20, P < ; for eggs F = 20.12, df = 2/20, P < ; for larvae: F = 68.57, df = 5/20, P < ) and 1993 (for adults: F = 27.68, df = 5/20, P < ; for eggs: F = 5.70, df = 5/20, P = ; for larvae: F = , df = 5/20, P < ). In contrast to conventional potato plots not treated with any insecticides, all active control measures significantly reduced the abundance of CPB larvae and egg masses

4 92 Figure 1. Total seasonal abundance of different stages of Colorado potato beetles in potato plots treated with different control regimes, Hermiston, Oregon, 1992 and Bars followed by the same letter indicate no significant differences in the mean number of CPB (per 32 plants over the entire seasons) at the 0.05 level according to ANOVA (Latin square design) and Tukey Kramer multiple mean comparison procedures. Treatment description: NOC = conventional potato with no control measures; SYS = conventional potato with systemic insecticide treatments; PYR = conventional potato with pyrethroid treatments; MBT = conventional potato with microbial Bt sprays; TBT = transgenic Bt potato alone; TBTSYS = transgenic Bt potato with systemic insecticide treatments.

5 93 Table 1. Active ingredients, insecticidal spectrum and mode of delivery of the CPB control agents evaluated in the present study Trade name Active Ingredients Insecticidal spectrum Mode of delivery Pounce R Permethrin Broad-spectrum effective against insects foliar spray and other arthropods exposed to treated habitats Thimet R Phorate Broad-spectrum effective against Furrow application, phytophagous insects and spider mites systemic feeding on treated plants Di-Syston-8 R Disulfoton Broad-spectrum effective against Furrow application, phytophagous insects and spider mites systemic feeding on treated plants M-trak R Cry3Aa Highly selective effective against Foliar spray chrysomelid beetles feeding on treated plants Newleaf R Cry3Aa Highly selective effective against Within-plant chrysomelid beetles feeding on potato plants in In 1993, there was a significant reduction in CPB larval abundance in conventional potato plots treated with systemic insecticides, as well as in plots of Bt potatoes with or without systemic insecticide treatment. However, treatment with permethrin or microbial Bt insecticides failed to significantly reduce populations of CPB. In both 1992 and 1993, transgenic Bt potato plants treated with or without insecticides resulted in a significantly greater reduction of CPB populations than applications of systemic insecticides, permethrin, or microbial Bt insecticides. Defoliation surveys also indicated that nearly 100% of conventional (non-transgenic) potato plants not protected by any insecticides were defoliated by CPB larvae and adults in mid to late July in both 1992 and 1993, whereas no Bt potato plants (with or without insecticide treatments), and less than 5% of non-bt potato plants protected with conventional insecticides, were defoliated during this period. Effects on other potato insect pests. The seasonal abundance of other insects feeding on potato plants are presented in Table 2. In both 1992 and 1993, GPA was the most abundant species among the non-target potato pests, and its seasonal abundance was significantly higher on conventional Russet Burbank potato plants treated biweekly with permethrin than with any other insect control regime, including no action control. In both years, populations of GPA increased sharply in permethrin-treated plots from mid July onward and reached an outbreak level in August. In other treatment plots, GPA populations were very low throughout the season and appeared never to reach an outbreak level (Figures 2A and 3A). Besides aphids, other common potato pests sampled with beat cloths included thrips, lygus bugs, leafhoppers, loopers, and flower beetles. In both 1992 and 1993, aphids, thrips, and lygus bugs were much more abundant than leafhoppers, loopers, and flower beetles. While none of these potato pests appeared to reach economic injury levels in either 1992 or 1993 in any of the experimental plots, the abundance of some of these species or groups varied significantly among different insect control regimes. Weekly sprays of permethrin significantly reduced the abundance of lygus bugs (in both 1992 and 1993), leafhoppers (in 1992), and loopers (in both 1992 and 1993), but had little impact on the abundance of thrips and flower beetles. In contrast, early and mid-season applications of systemic insecticides significantly reduced plant-sap feeding insects such as lygus bugs and leafhoppers, but had little impact on the abundance of loopers or flower beetles. As expected, Newleaf potato plants or weekly sprays of a Bt-based microbial formulation did not reduce the abundance of any of the non-target (non-cpb) potato pests. Effects on predators. In both 1992 and 1993, the most abundant groups of generalist predators across all treatments were big-eyed bugs (Geocoris sp.), damsel

6 94 Figure 2. Population dynamics of green peach aphids and major predators in different treatment plots sampled with beating cloths in 1992 field trial. Treatment description: NOC = conventional potato with no control measures; SYS = conventional potato with systemic insecticide treatments; PYR = conventional potato with pyrethroid treatments; MBT = conventional potato with microbial Bt sprays; TBT = transgenic Bt potato alone; TBTSYS = transgenic Bt potato with systemic insecticide treatments.

7 95 Table 2. Seasonal abundance of non-target phytophagous insect pests in potato plots treated with different CPB control regimes (sampled with beating cloth) Insect group Taxonomic status Year Number of individuals observed on beating-cloths during the entire season (mean ± S.E.) a NOC SYS PYR MBT TBTP TBTSYS Aphids Homoptera: Aphididae ± 27.3c 149 ± 16.3c ± a ± 41.9b ± 28.5bc ± 29.5bc ± 71.9bc ± 21.3c ± 438.5a ± 24.5bc ± 24.6b ± 67.7bc Thrips Thysanoptera: Thripidae ± 3.5b 40.3 ± 6.8ab 58.0 ± 7.4a 50.3 ± 9.3a 52.5 ± 5.6a 35.0 ± 5.2ab ± 45.0a ± 35.2a ± 34.0a ± 31.6a ± 63.7a ± 57.6a Lygus bugs Hemiptera: Miridae ± 5.1ab 46.5 ± 7.9ab 21.2 ± 2.9b 63.8 ± 9.9a 55.2 ± 6.7ab 27.5 ± 6.7ab ± 40.7a 73.2 ± 6.4b ± 15.4b ± 19.2a ± 20.7a ± 11.9b Leafhoppers Homoptera: Cicadellidae ± 0.2b 0.2 ± 0.2b 1.2 ± 0.8b 1.5 ± 0.4b 5.8 ± 1.8a 0.5 ± 0.2b ± 2.08a 3.5 ± 0.3b 10.2 ± 1.9ab 12.0 ± 2.2a 15.5 ± 2.2a 5.0 ± 1.5ab Loopers Lepidoptera: Noctuidae ± 1.2a 14.3 ± 1.5a 1.5 ± 0.6b 8.5 ± 2.1a 9.0 ± 2.0a 11.7 ± 1.9a ± 1.5ab 10.8 ± 0.8a 3.3 ± 0.8b 8.0 ± 0.9ab 6.5 ± 1.5ab 14.7 ± 4.6a Brown flower beetles Coleoptera: Cetoniidae ± 1.3a 3.0 ± 0.9a 6.3 ± 1.2a 5.3 ± 1.0a 2.8 ± 0.7a 3.8 ± 1.0a Striped flower beetles Coleoptera: Cetoniidae ± 0.5a 1.0 ± 0.4a 2.3 ± 0.9a 2.8 ± 1.5a 5.0 ± 2.1a 3.1 ± 0.7a a Values in each row followed by the same letter are not significantly different at the 0.05 level according to ANOVA (Latin square design) and Tukey Kramer multiple mean comparison procedures. NOC = conventional potato with no control measures; SYS = conventional potato with systemic insecticide treatments; PYR = conventional potato with pyrethroid treatments; MBT = conventional potato with microbial Bt sprays; TBT = transgenic Bt potato alone; TBTSYS = transgenic Bt potato with systemic insecticide treatments.

8 96 bugs (Nabid sp.), minute pirate bugs (Orius sp.), and spiders (Table 3). Together, these major predators accounted for over 95% of all of the predators observed on beat cloths. In both years, ladybird beetles accounted for about 3% of the total predators observed on beat cloths, while brown lacewings, syrphid flies and assassin bugs were the least abundant predators, accounting for less than 2% of all predators observed. For the major predators, the total seasonal abundance varied significantly among different CPB control regimes, as well as between taxonomic groups in different years (Table 3). In both 1992 and 1993, the abundance of all major groups of generalist predators observed on transgenic Bt potato plants not treated with any insecticides was either comparable to or significantly higher than in any other treatment (including conventional potato plots with no insect control treatments). Biweekly application of permethrin sprays significantly reduced the abundance of spiders in both years, and also the abundance of big-eyed bugs and damsel bugs in In both 1992 and 1993, there was no significant difference among treatment plots in the abundance of brown lacewings, syrphid flies or assassin bugs. However, the abundance of ladybird beetles (larvae and nymphs) was significantly higher in 1993 in the conventional potato plots treated with permethrin than in the conventional plots treated with systemic insecticides, probably reflecting numeric responses to the significantly higher aphid populations (Table 2 and Figures 2A and 3A) in the permethrin-treated plots. Graphical examination of the population dynamics of major predators (Figures 2B E and 3B E) indicated that the patterns of population change during the season varied between years, and among taxonomic groups and CPB control regimes. In 1992, populations of big-eyed bugs, damsel bugs, minute pirate bugs and spiders were consistently higher throughout most of the season (from early July to mid or late August) in plots of transgenic Bt potato with or without systemic insecticides, and conventional potato plots treated with microbial Bt foliar sprays or applications of systemic insecticides than in conventional potato plots treated with permethrin. However, fewer differences were apparent in numbers of minute pirate bugs among treatments. In 1992, populations of these major predators in the conventional potato plots not treated with any insecticides were about the same as in the transgenic Bt potato plots and those plots treated with microbial Bt foliar sprays or systemic insecticides before mid to late July, but decreased sharply thereafter because of the severe defoliation of potato plants by the uncontrolled CPB populations. In 1993, the population dynamics of major predators appeared to be different from those in Fewer differences were apparent in populations of big-eyed bugs and damsel bugs among treatments, but populations of minute pirate bugs and spiders were lower throughout most of the season (from early July to mid August) in permethrin-treated plots than in any other treatment plots. Discussion Results from the 2 years of field trials indicated that transgenic Newleaf potatoes were highly effective in reducing the abundance of CPB populations and provided levels of CPB control better than weekly sprays of Bt-based microbial insecticides, bi-weekly applications of permethrin, or early and mid-season applications of systemic insecticides (phorate and disulfoton). In contrast to the insecticide treatments, however, effective control of CPB by Newleaf potatoes or by weekly sprays of Bt-based formulations did not appear to have significantly impacted the abundance of major beneficial predators or secondary potato pests. These findings are not surprising because the Cry3Aa protein is highly selective in its activity, affecting only Coleoptera (such as CPB) in the family Chrysomelidae (Hernstadt et al., 1986; MacIntosh et al., 1990; Eckberg & Cranshaw, 1994; see review in Keller & Langenbruch, 1993). In contrast to Newleaf potatoes and microbial Bt formulations, however, the broad-spectrum insecticide, permethrin, had much broader and more severe unintended impacts on non-target arthropods. Applications of permethrin significantly reduced the abundance of several major generalist predators such as spiders, big-eyed bugs, damsel bugs, and minute pirate bugs, and apparently resulted in significant increases in the abundance of GPA on treated plants. While systemic insecticides appeared to have reduced the abundance of some plant-sap feeding insects such as GPA, lygus bugs, and leafhoppers, they had no significant impact on populations of the major predators such as spiders, big-eyed bugs, damsel bugs, and minute pirate bugs. Although many studies have shown that permethrin and the systemic insecticides, phorate and disulfoton, have broad toxicity against many groups of arthropod natural enemies such as spiders, preda-

9 97 Table 3. Seasonal abundance of plant-dwelling arthropod predators in potato plots with different CPB control treatments (sampled with beating cloth) Insect group Taxonomic status Year Number of individuals observed on beating-cloths during the entire season (mean ± S.E.) a NOC SYS PYR MBT TBT TBTSYS Big-eyed bug Hemiptera: Lygaedae ± 6.8b 51.3 ± 3.4bc 34.1 ± 4.6c ± 12.5a ± 9.1a 52.8 ± 3.2bc ± 6.4a 33.3 ± 2.4a 39.2 ± 2.7a 44.0 ± 5.6a 44.3 ± 5.2a 36.3 ± 3.0a Damsel bug Hemiptera: Nabidae ± 2.7b 33.5 ± 5.0ab 9.5 ± 1.5c 48.2 ± 4.5a 50.2 ± 6.1a 40.2 ± 4.9a ± 1.9a 31.5 ± 2.8a 33.5 ± 3.7a 28.5 ± 2.2a 36.5 ± 6.0a 28.7 ± 4.7a Pirate bug Hemiptera: Anthocoridae ± 1.0ab 10.8 ± 1.7b 13.2 ± 1.6ab 19.7 ± 2.9a 14.7 ± 2.3ab 9.8 ± 0.9b ± 5.0ab 47.8 ± 4.2b 64.8 ± 8.8ab 83.0 ± 11.9ab 93.8 ± 9.8a 76.3 ± 5.0ab Ladybird beetle Coleoptera: Coccinellidae ± 0.9a 2.3 ± 0.8a 3.8 ± 1.2a 3.7 ± 1.0a 4.7 ± 1.0a 3.3 ± 1.0a ± 1.7ab 3.3 ± 0.7b 15.0 ± 4.4a 7.8 ± 2.0ab 9.0 ± 1.9ab 5.2 ± 1.3ab Brown lacewing Neuroptera: Hemerobiidae ± 0.4a 1.2 ± 0.5a 1.5 ± 0.7a 1.5 ± 0.7a 2.8 ± 1.1a 1.0 ± 0.3a ± 0.7a 2.0 ± 0.6a 3.5 ± 1.0a 3.2 ± 1.1a 2.8 ± 0.5a 4.7 ± 1.2a Syrphid fly Diptera: Syrphidae ± 0.0a 1.0 ± 0.5a 0.0 ± 0.0a 1.5 ± 1.1a 0.3 ± 0.2a 0.3 ± 0.3a ± 0.2a 0.0 ± 0.0a 0.0 ± 0.0a 0.2 ± 0.2a 0.3 ± 0.3a 0.2 ± 0.2a Assassin bug Hemiptera: Reduviidae ± 0.2a 0.2 ± 0.2a 0.0 ± 0.0a 0.3 ± 0.2a 0.5 ± 0.2a 0.2 ± 0.2a ± 0.0a 0.0 ± 0.0a 0.0 ± 0.0a 0.0 ± 0.0a 0.0 ± 0.0a 0.0 ± 0.0a Spider Araneae ± 2.5b 64.3 ± 5.8ab 14.7 ± 3.1c 72.0 ± 6.8ab 83.5 ± 4.3a 79.3 ± 8.4ab ± 5.9a 53.2 ± 7.6a 28.2 ± 4.2b 59.3 ± 5.0a 65.3 ± 5.3a 65.3 ± 8.0a a Values in each row followed by the same letter are not significantly different at the 0.05 level according to ANOVA (Latin square design) and Tukey Kramer multiple mean comparison procedures. NOC = conventional potato with no control measures; SYS = conventional potato with systemic insecticide treatments; PYR = conventional potato with pyrethroid treatments; MBT = conventional potato with microbial Bt sprays; TBT = transgenic Bt potato alone; TBTSYS = transgenic Bt potato with systemic insecticide treatments.

10 98 Figure 3. Population dynamics of green peach aphids and major predators in different treatment plots sampled with beating cloths in 1993 field trial. Treatment description: NOC = conventional potato with no control measures; SYS = conventional potato with systemic insecticide treatments; PYR = conventional potato with pyrethroid treatments; MBT = conventional potato with microbial Bt sprays; TBT = transgenic Bt potato alone; TBTSYS = transgenic Bt potato with systemic insecticide treatments.

11 99 ceous hemipterans, ladybird beetles and lacewings (e.g., Cherry & Pless, 1971; Croft, 1994; Castane et al., 1996; Boyd & Boethel, 1998), differences in the modes of delivery of these two types of insecticides to the potatoes played a major role in limiting potential negative impacts on non-target species. Unlike permethrin, phorate and disulfoton are taken up into plant tissues through the roots following in-furrow application, and thus their exposure is mainly limited to insects feeding on treated potatoes. In this regard, transgenic Bt plants may have an advantage over foliar sprays of microbial Bt. Potential non-target impacts of insect pest control measures often result from either (1) lethal (or toxic) effects on the exposed non-target species and/or (2) trophic effects of the reduction of the target pest population on the immediate upper trophic level of non-target species (such as predators and/or parasitoids). While the lethal effects depend on the selectivity of the pest control measure against different species or groups of non-target species, trophic effects on the non-target species will occur with any active pest control measure that effectively reduces target pest populations. However, the trophic nontarget effects of a pest control measure will be limited primarily to host- or prey-specific predators and/or parasitoids that rely on the targeted pests as their only food sources. In Oregon, there are few prey-specific predators or parasitoids that attack CPB. Major natural enemies attacking CPB in Oregon are the generalist predators such as spiders, big-eyed bugs, damsel bugs, minute pirate bugs and ladybird beetles. These generalist predators also frequently feed upon other groups of insect prey such as aphids, thrips, and leafhoppers. Thus, control measures such as Newleaf potatoes and Bt sprays that specifically target CPB are likely to have minimal negative impact on these generalist predators, and thus promote the role of these predators in suppressing other (non-target) potato pests such as aphids. Like other agricultural practices, all pest control measures have ecological consequences. From the perspective of integrated pest management (IPM), control measures against a specific pest should be chosen to be compatible with the management of other species or groups of pests. In this regard, the use of broadspectrum insecticides for CPB control appears not to be compatible with the control of GPA and the GPAtransmitted leaf-roll disease. In Oregon and many other potato growing regions, GPA is an effective vector of potato leaf-roll virus. Thus, any CPB control measures that have severe adverse impacts on the major predators of aphids should not be recommended for use in potato IPM programs. In contrast, Newleaf potatoes, application of Bt-based formulation, and systemic insecticides appear to have an advantage over broad-spectrum foliar applied insecticides in promoting the role of natural enemies. Currently, some novel insecticides such as imidacloprid with long residual and systemic activity are also registered as an at-planting soil treatment for insect control and have become widely used in the US to target both CPB and GPA (Dively et al., 1998). Future studies should be conducted to compare the relative compatibility of these novel insecticides (e.g., Admire R ) with transgenic Bt and non-transgenic (conventional) insecticide-based IPM programs. Acknowledgements We thank Paul Jepson (Oregon State University), Elizabeth Owens, Tom Nickson, Mike McKee and Mark Holland (Monsanto Company) for helpful comments on the manuscript. References Boyd, M. L. & D. J. Boethel, Susceptibility of predaceous hemipteran species to selected insecticides on soybean in Louisiana. 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