Resistance of Lepidopteran Egg Parasitoids, Trichogramma japonicum and Trichogramma chilonis, to Insecticides Used for Control of Rice Planthoppers.

Trichogramma wasps are commonly used as biocontrol agents to manage lepidopteran rice pests in rice fields. However, lepidopteran pests synergistically occur with rice planthoppers which are not targeted by Trichogramma. The use of Trichogramma parasitoids in field-based pest control efforts is greatly affected by the application of insecticides targeting planthoppers. As such, insecticide-resistant strains of Trichogramma are urgently needed for the incorporation of these beneficial natural enemies into integrated pest management programs in rice agroecosystems. In the present study, Trichogramma japonicum Ahmead (Hymenoptera: Trichogrammitidae) and Trichogramma chilonis Ishii (Hymenoptera: Trichogrammitidae) were treated with sublethal doses of four insecticides which target rice planthoppers, to generate tolerant strains in the laboratory. The resistance rate of T. japonicum to imidacloprid was the highest (17.8-folds) after 10 successive treatments and experienced 2.5, 4.72, and 7.41-fold increases in tolerance to thiamethoxam, buprofezin, and nitenpyram, respectively. Tolerance of T. chilonis to imidacloprid, thiamethoxam, buprofezin, and nitenpyram were 8.8, 6.9, 4.43, and 5.67-fold greater, respectively. The emergence and deformity (without spreading wings or short wings) rates of T. japonicum and T. chilonis gradually recovered with an increased exposure time of treatments. The fecundity of T. japonicum treated with thiamethoxam was significantly higher than that of the control and T. chilonis treated with thiamethoxam and nitenpyra. Our results demonstrate that screening for insecticide-tolerant/resistant Trichogramma strains was feasible, especially in the pairing of T. japonicum and imidacloprid, which could provide a valuable biological control tool that can be combined with traditional chemical control strategies for use in IPM of rice agroecosystems.

Screening Sugars Can Benefit the Parasitoid Cotesia chilonis (Hymenoptera: Braconidae) Without Benefiting Its Host, Chilo suppressalis (Lepidoptera: Crambidae).

Most adult parasitoids depend on carbohydrate-rich food as an energy source for longevity, fecundity, and mobility. Thus, providing sugars has been proposed as a technique to maximize the biological control efficacy of parasitoids. However, the sugars provided for parasitoids need to be carefully selected because herbivore hosts might also benefit. Here we explore the effects of 12 naturally occurring sugars on the longevity and fecundity of the rice pest, Chilo suppressalis, and the longevity of its parasitoid, Cotesia chilonis, as well as the effect of sugars on sugar consumption of C. chilonis. Results showed that none of the tested sugars significantly impacted the longevity of C. suppressalis, but fructose, glucose, maltose, and sucrose significantly increased its fecundity. The longevity of C. chilonis was significantly increased when fed fructose, glucose, sucrose, maltose, trehalose, and melezitose. Our data suggest that C. chilonis consumed larger quantities of glucose, fructose, and sucrose followed by maltose, melezitose, and trehalose and the longevity of C. chilonis was positively correlated to sugar consumption. Our data also suggest that the herbivore C. suppressalis and its parasitoid C. chilonis responded differently to trehalose and melezitose. Although additional studies are needed, our data suggest that these sugars could be considered as candidate components for sugar sprays to enhance the activity and efficacy of C. chilonis, but without benefiting its pest host.

The rice planthopper parasitoid Anagrus nilaparvatae is not at risk when feeding on honeydew derived from Bacillus thuringiensis (Bt) rice.

BACKGROUND: Honeydew is a sugar-rich excretion produced by sap-feeding Sternorrhyncha and is an important source of carbohydrates for natural enemies, especially for parasitoids. Honeydew derived from genetically modified (GM) crops can contain amounts of the transgene product. Thus, it is a possible route of exposure for natural enemies feeding on honeydew. In the present study, the potential effects of Nilaparvata lugens honeydew derived from Cry1C and Cry2A rice on different life-table parameters and parasitism dynamics of the egg parasitoid Anagrus nilaparvatae were evaluated under laboratory and field conditions. Furthermore, the Bacillus thuringiensis (Bt) levels and the sugar and amino acid composition of honeydew were analyzed. RESULTS: Results indicated that A. nilaparvatae was exposed to Bt proteins by feeding on N. lugens honeydew produced from Bt rice. However, honeydew derived from the tested Cry1C and Cry2A rice lines did not affect the development, longevity, emergence rate and fecundity of A. nilaparvatae. Also, the parasitism dynamics in the field remained unaffected. In addition, the sugar and amino acid composition of N. lugens honeydew was not significantly altered for the tested Bt rice lines compared with the parental non-Bt plant. CONCLUSION: The quality of honeydew derived from the tested Bt rice lines as a food resource for natural enemies was maintained. © 2018 Society of Chemical Industry.

Bt cotton producing Cry1Ac and Cry2Ab does not harm two parasitoids, Cotesia marginiventris and Copidosoma floridanum.

Cabbage looper, Trichoplusia ni (Hübner) is an important lepidopteran pest on many vegetable and greenhouse crops, and some field crops. Although there are no commercial transgenic Bt vegetable or greenhouse crops, T. ni is a target of Bollgard II cotton, which produces Cry1Ac and Cry2Ab. We expand on previous work that examined the effect of Bt crops on parasitoids using Bt-resistant lepidopteran populations as hosts. Cry1Ac/Cry2Ab-resistant T. ni larvae were used to eliminate host quality effects and to evaluate the direct effects of Bt cotton on the parasitoids Copidosoma floridanum (Ashmead) and Cotesia marginiventris (Cresson). These tri-trophic studies confirm that Bt cotton had no significant impact on development, success of parasitism, survival and adult longevity of C. marginiventris when using Bt-resistant T. ni fed on Bt cotton. Similarly, this Bt cotton had no significant impact on the development, mummy weight and the number of progeny produced by C. floridanum. Our studies verified that lyophilized Bt crop tissue maintained its insecticidal bioactivity when incorporated into an artificial diet, demonstrating that hosts and parasitoids were exposed to active Cry proteins. The egg-larval parasitoid C. floridanum, or similar species that consume their entire host, should be considered useful surrogates in risk assessment of Bt crops to non-target arthropods.

Assessing the effects of Cry1C rice and Cry2A rice to Pseudogonatopus flavifemur, a parasitoid of rice planthoppers.

Transgenic rice producing insecticidal proteins from Bacillus thuringiensis (Bt) could help protect the plants from damage by lepidopteran pests. However, one concern is the potential of Bt rice to harm non-target natural enemies, which play a vital role in pest control. In the present study, the potential effects of Cry1C rice and Cry2A rice on different life-table parameters and population dynamics of Pseudogonatopus flavifemur, a parasitoid of rice planthoppers, were evaluated under laboratory and field condition. The exposure of P. flavifemur to plant-produced Bt proteins was also analyzed. Results indicated that direct feeding on rice plants was the main exposure pathway of P. flavifemur to the Cry1C and Cry2A proteins. No significant difference on the development, survival, longevity, fecundity, and prey consumption of P. flavifemur was detected over two generations between the Bt and non-Bt rice treatments. Furthermore, the population dynamics of P. flavifemur were not affected by Cry1C rice and Cry2A rice. In conclusion, the tested Cry1C rice and Cry2A rice do not appear to harm the parasitoid P. flavifemur.

The Effects of Temperature and Host Age on the Fecundity of Four Trichogramma Species, Egg Parasitoids of the Cnaphalocrocis medinalis (Lepidoptera: Pyralidae).

The Cnaphalocrocis medinalis (Guenée) is one of the most important rice pests in Asia and is difficult to control by chemical insecticides due to its rapid development of resistance. To screen potential species for biological control of C. medinalis, we investigated the effects of temperature (20, 24, 28, 32, and 36 °C) and host age (1-, 2-, 3-, and 4-d-old) on the fecundity of four Trichogramma spp. on C. medinalis eggs. Our results indicated that C. medinalis eggs were acceptable to T. japonicum, T. chilonis, T. dendrolimi, and T. ostriniae, though no eggs were parasitized at 36 °C. There were no significant differences in parasitism among the four Trichogramma species under the tested temperature regions, except at 20 °C where parasitism by T. japonicum was significantly higher than that by T. chilonis and T. ostriniae. However, T. japonicum had significantly more progeny than the other three Trichogramma species at 32 °C. All four Trichogramma species performed well on 1-, 2-, and 3-d-old C. medinalis eggs, but parasitism on 4-d-old eggs was significantly reduced. Trichogramma japonicum parasitized the highest number of C. medinalis eggs on different aged hosts and had more progeny than the other Trichogramma species, especially on 3-d-old hosts. In conclusion, T. japonicum exhibited better performance on C. medinalis eggs than the other three Trichogramma species and could be considered as our most suitable Trichogramma candidate for control of C. medinalis.

[A banker plant system of 'Leesia sayanuka-Nlilaparvata muiri-Tytthus chinensis' to control rice planthoppers]. / "秕谷草-伪褐飞虱-ä¸­åŽæ·¡ç¿ ç›²è½"载体植物系统的可行性.

In order to clarify the feasibility of the banker plant system "Leesia sayanuka-Nlilaparvata muiri-Tytthus chinensis" to control rice planthooper, the effects of the combination of rice, L. sa-yanuka, N. lugen and N. muiri on the adult morphology, population growth, oviposition and feeding selectivity of T. chinensis were carried out in the present study. The results showed that the body size of male and female adults of T. chinensis rice population (feeding on N. lugens eggs) were significantly larger than those of T. chinensis population (feeding on N. muiri eggs). Population growth parameters including fecundity, net productive rate, innate capacity for increase, finite rate of increase of L. sayanuka feeding on N. lugens eggs were significantly higher than those of L. sayanuka feeding on N. muiri eggs. However, the population growth ability of L. sayanuka feeding on N. muiri was still high enough to expand the population. For the oviposition selection, both rice population and L. sayanuka population preferred laying eggs on rice than on L. sayanuka. Meanwhile, there was no significant difference in the predation of females, males and nymphs to N. lugens eggs or N. muiri eggs between rice population and L. sayanuka population. At last, based on our results, we discussed the feasibility of establishing the banker plant system "L. sayanuka-N. muiri-T. chinensis" in rice fields.

Different Performance of Two Trichogramma (Hymenoptera: Trichogrammatidae) Species Feeding on Sugars.

Most parasitoids depend on carbohydrate-rich foods to maximize their longevity and reproduction potential. These food resources are commonly from floral nectar, extra-floral nectar, and honeydew, which contain monosaccharides, disaccharides, and oligosaccharides. Here, we report an experiment to explore the effects of 12 naturally occurring sugars on the gustatory response, longevity, and fecundity of Trichogramma japonicum and Trichogramma chilonis These two parasitoid species differed in their responses to the tested sugars. Trichogramma japonicum showed a high gustatory response to eight sugars, but T. chilonis to only six. However, only fructose, glucose, and sucrose increased the longevity of T. japonicum, and only glucose enhanced the fecundity. For T. chilonis, fructose, galactose, gluctose, maltose, melibiose, sucrose, and melezitose prolonged the longevity and increased fecundity. Furthermore, female T. japonicum benefitted much less from the ingestion of sugars when compared with female T. chilonis For T. japonicum, feeding on suitable sugars, longevity was increased by a factor of 1.8-2.0, and fecundity by a factor of 1.5. In T. chilonis, longevity increased by a factor of 2.9-5.2 and fecundity by 2.7-4.0. Thus, providing the right sugars to the parasitoids will help to enhance the biological control efficacy of Trichogramma, and T. chilonis in particular.

The interaction of two-spotted spider mites, Tetranychus urticae Koch, with Cry protein production and predation by Amblyseius andersoni (Chant) in Cry1Ac/Cry2Ab cotton and Cry1F maize.

Crops producing insecticidal crystal (Cry) proteins from the bacterium, Bacillus thuringiensis (Bt), are an important tool for managing lepidopteran pests on cotton and maize. However, the effects of these Bt crops on non-target organisms, especially natural enemies that provide biological control services, are required to be addressed in an environmental risk assessment. Amblyseius andersoni (Acari: Phytoseiidae) is a cosmopolitan predator of the two-spotted spider mite, Tetranychus urticae (Acari: Tetranychidae), a significant pest of cotton and maize. Tri-trophic studies were conducted to assess the potential effects of Cry1Ac/Cry2Ab cotton and Cry1F maize on life history parameters (survival rate, development time, fecundity and egg hatching rate) of A. andersoni. We confirmed that these Bt crops have no effects on the biology of T. urticae and, in turn, that there were no differences in any of the life history parameters of A. andersoni when it fed on T. urticae feeding on Cry1Ac/Cry2Ab or non-Bt cotton and Cry1F or non-Bt maize. Use of a susceptible insect assay demonstrated that T. urticae contained biologically active Cry proteins. Cry proteins concentrations declined greatly as they moved from plants to herbivores to predators and protein concentration did not appear to be related to mite density. Free-choice experiments revealed that A. andersoni had no preference for Cry1Ac/Cry2Ab cotton or Cry1F maize-reared T. urticae compared with those reared on non-Bt cotton or maize. Collectively these results provide strong evidence that these crops can complement other integrated pest management tactics including biological control.

Bt crops benefit natural enemies to control non-target pests.

Crops producing insecticidal crystal (Cry) proteins from Bacillus thuringiensis (Bt) control important lepidopteran pests. However, pests such as aphids not susceptible to Cry proteins may require other integrated pest management (IPM) tactics, including biological control. We fed aphids on Bt and non-Bt plants and analyzed the Bt protein residue in aphids and compared the effects of Bt plants and a pyrethroid, lambda-cyhalothrin, on the performance of three natural enemies (predators: Coleomegilla maculata and Eupeodes americanus; parasitoid Aphidius colemani) of the green peach aphid, Myzus persicae. No Bt protein residues in aphids were detected and no significant differences were recorded in the performance of pyrethroid-resistant aphids that fed on Bt broccoli expressing Cry1Ab or Cry1C, or on non-Bt broccoli plants treated or not treated with the pyrethroid. This indicated the aphids were not affected by the Cry proteins or the pyrethroid, thus removing any effect of prey quality. Tri-trophic experiments demonstrated that no C. maculata and E. americanus survived consumption of pyrethroid-treated aphids and that ovipositional behavior of A. colemani was impaired when provided with pyrethroid-treated aphids. In contrast, natural enemies were not affected when fed aphids reared on Bt broccoli, thus demonstrating the safety of these Bt plants for IPM.

Transgenic cry1C or cry2A rice has no adverse impacts on the life-table parameters and population dynamics of the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae).

BACKGROUND: Transgenic rice producing the insecticidal protein from Bacillus thuringiensis Berliner (Bt) is protected from damage by lepidopteran insect pests. However, one of the main concerns about Bt rice is the potential impact on non-target herbivores. In the present study, the ecological impacts of two Bt rice lines, T1C-19 expressing Cry1C protein and T2A-1 expressing Cry2A protein, on the non-target herbivore brown planthopper (BPH), Nilaparvata lugens (Stål), were evaluated under laboratory and field conditions. The purpose was to verify whether these Bt rice lines could affect the performance of BPH at individual and population scales. RESULTS: Laboratory results showed that most of the fitness parameters (development duration, survival rate, fecundity, fertility, amount of honeydew excreted) of BPH were not significantly affected by the two tested Bt rice lines, although the development duration of fourth-instar nymphs fed on T1C-19 was distinctly longer compared with that on T2A-1 and non-Bt rice plants. Five life-table parameters did not significantly differ among rice types. Two-year field trials also revealed no significant difference in population dynamics of BPH among rice types. CONCLUSION: It is inferred that the tested Bt rice lines are unlikely to affect the population growth of BPH.

[Effects of plant viruses on vector and non-vector herbivorous arthropods and their natural enemies: a mini review].

Plant viruses transmitted by arthropods, as an important biotic factor, may not only directly affect the yield and quality of host plants, and development, physiological characteristics and ecological performances of their vector arthropods, but also directly or indirectly affect the non-vector herbivorous arthropods and their natural enemies in the same ecosystem, thereby causing influences to the whole agro-ecosystem. This paper reviewed the progress on the effects of plant viruses on herbivorous arthropods, including vector and non-vector, and their natural enemies, and on their ecological mechanisms to provide a reference for optimizing the management of vector and non-vector arthropod populations and sustainable control of plant viruses in agro-ecosystem.

Effects of Bt cotton on Thrips tabaci (Thysanoptera: Thripidae) and its predator, Orius insidiosus (Hemiptera: Anthocoridae).

Laboratory studies were conducted to investigate tritrophic transfer of insecticidal Cry proteins from transgenic cotton to an herbivore and its predator, and to examine effects of these proteins on the predator's development, survival, and reproduction. Cry1Ac and Cry2Ab proteins from the bacterium Bacillus thuringiensis (Bt) produced in Bollgard-II (BG-II, Event 15985) cotton plants were acquired by Thrips tabaci Lindeman (Thysanoptera: Thripidae), an important sucking pest of cotton, and its generalist predator, Orius insidiosus (Say) (Hemiptera: Anthocoridae). The average protein titers in BG-II cotton leaves were 1,256 and 43,637 ng Cry1Ac and Cry2Ab per gram fresh leaf tissue, respectively. At the second trophic level, larvae of T. tabaci reared on BG-II cotton for 48-96 h had 22.1 and 2.1% of the Cry1Ac and Cry2Ab levels expressed in leaves, respectively. At the third trophic level, O. insidiosus that fed on T. tabaci larvae had 4.4 and 0.3% of the Cry1Ac and Cry2Ab protein levels, respectively, expressed in BG-II plants. O. insidiosus survivorship, time of nymphal development, adult weight, preoviposition and postoviposition periods, fecundity, and adult longevity were not adversely affected owing to consumption of T. tabaci larvae that had fed on BG-II cotton compared with non-Bt cotton. Our results indicate that O. insidiosus, a common predator of T. tabaci, is not harmed by BG-II cotton when exposed to Bt proteins through its prey. Thus, O. insidiosus can continue to provide important biological control services in the cotton ecosystem when BG-II cotton is used to control primary lepidopteran pests.

Tri-trophic studies using Cry1Ac-resistant Plutella xylostella demonstrate no adverse effects of Cry1Ac on the entomopathogenic nematode, Heterorhabditis bacteriophora.

The potential impacts on natural enemies of crops that produce insecticidal Cry proteins from Bacillus thuringiensis (Bt) are an important part of an environmental risk assessment. Entomopathogenic nematodes are important natural enemies of lepidopteran pests, and the effects of Bt crops on these nontarget organisms should be investigated to avoid disruption of their biological control function. The objective of this study was to investigate the effects of Cry1Ac-expressing transgenic Bt broccoli on the entomopathogenic nematode, Heterorhabditis bacteriophora Poinar (Rhabditida: Heterorhabditidae), under tri-trophic conditions. Using CrylAc-resistant Plutella xylostella L. (Lepidoptera: Plutellidae) larvae as hosts, we evaluated the potential impact of Cry1Ac-expressing Bt broccoli on several fitness parameters of H. bacteriophora. Virulence, reproductive potential, time of emergence, and preference of H. bacteriophora for the host (P. xylostella) were not significantly affected when CrylAc-resistant P. xylostella larvae were reared on leaves of Cry1Ac or non-Bt broccoli. Also the aforementioned parameters of the subsequent generation of H. bacteriophora did not differ between nematodes obtained from P. xylostella reared on CrylAc broccoli compared with those obtained from P. xylostella reared on non-Bt broccoli. To the best of our knowledge, the current study provides the first clear evidence that Cry1Ac does not affect important fitness parameters of H. bacteriophora.

Using resistant prey demonstrates that Bt plants producing Cry1Ac, Cry2Ab, and Cry1F have no negative effects on Geocoris punctipes and Orius insidiosus.

Geocoris punctipes (Say) and Orius insidiosus (Say) are generalist predators found in a wide range of crops, including cotton (Gossypium hirsutum L.) and maize (Zea mays L.), where they provide important biological control services by feeding on an array of pests, including eggs and small larvae of caterpillars. A high percentage of cotton and maize in the United States and several other countries are transgenic cultivars that produce one or more of the insecticidal Cry proteins of Bacillus thuringiensis Berliner (Bt). Here we quantify effects of three Cry proteins on the life history of these predators over two generations when they are exposed to these Cry proteins indirectly through their prey. To eliminate the confounding prey quality effects that can be introduced by Bt-susceptible prey, we used Cry1Ac/Cry2Ab-resistant Trichoplusia ni (Hübner) and Cry1 F-resistant Spodoptera frugiperda (J.E. Smith) in a series of tri-trophic studies. Survival, development, adult mass, fecundity, and fertility were similar when predators consumed larvae feeding on Cry1Ac/Cry2Ab cotton or Cry1 F maize compared with prey feeding on isogenic or near-isogenic cotton or maize. Repeated exposure of the same initial cohort over a second generation also resulted in no differences in life-history traits when feeding on non-Bt- or Bt-fed prey. Enzyme-linked immunosorbent assay showed that predators were exposed to Bt Cry proteins from their prey and that these proteins became increasingly diluted as they moved up the food chain. Results show a clear lack of effect of three common and widespread Cry proteins on these two important predator species. The use of resistant insects to eliminate prey quality effects provides a robust and meaningful assessment of exposure and hazard.

Eliminating host-mediated effects demonstrates Bt maize producing Cry1F has no adverse effects on the parasitoid Cotesia marginiventris.

The fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), is an important pest of maize in the United States and many tropical areas in the western hemisphere. In 2001, Herculex I(®) (Cry1F) maize was commercially planted in the United States to control Lepidoptera, including S. frugiperda. In 2006, a population of S. frugiperda was discovered in Puerto Rico that had evolved resistance to Cry1F maize in the field, making it the first well-documented case of an insect with field resistance to a plant producing protein from Bacillus thuringiensis (Bt). Using this resistant population, we conducted tri-trophic studies with a natural enemy of S. frugiperda. By using resistant S. frugiperda, we were able to overcome possible prey-mediated effects and avoid concerns about potential differences in laboratory- or field-derived Bt resistance. We used the Cry1F-resistant S. frugiperda to evaluate effects of Cry1F on Cotesia marginiventris (Cresson) (Hymenoptera: Braconidae), a larval endoparasitoid of S. frugiperda, over five generations. Our results clearly demonstrate that Cry1F maize does not affect development, parasitism, survivorship, sex ratio, longevity or fecundity of C. marginiventris when they parasitize Cry1F maize-fed S. frugiperda. Furthermore, the level of Cry1F protein in the leaves was strongly diluted when transferred from Bt maize to S. frugiperda and was not detected in larvae, cocoons or adults of C. marginiventris. Our results refute previous reports of C. marginiventris being harmed by Bt proteins and suggest that such results were caused by prey-mediated effects due to using Bt-susceptible lepidopteran hosts.

[Ecological responses of brown planthopper, Nilaparvata lugens, to triazophos and deltamethrin on transgenic Bt rice lines and their non-Bt parental rice].

In this study, the brown planthopper (BPH), Nilaparvata lugens (Hemiptera: Delphacidae), cultured on Bt rice lines (T1C-19 with cry1C gene and T2A-1 with cry2A gene) and their parental rice MH63, were treated with a series of concentrations of triazophos and deltamethrin when they developed up to the third instar for the evaluation of the effects of Bt rice on BPH resurgence induced by pesticides. The results indicated that BPH nymphal duration decreased with the increasing concentration of deltamethrin, while no significant differences of BPH nymphal duration were observed on the same rice variety treated with the different concentrations of triazophos. Furthermore, the survival rate of BPH significantly declined and their fecundity significantly increased with the increasing concentration of insecticides. However, ecological fitness parameters of BPH including nymphal duration, survival rate, female adult mass, fecundity and egg hatchability were not significantly different among Bt and non-Bt rice varieties when they treated with the same concentration of insecticide. These results implied that no significant difference in the BPH resurgence induced by pesticides was observed among the two tested Bt rice varieties and their non-Bt parental rice variety.

Bt crops producing Cry1Ac, Cry2Ab and Cry1F do not harm the green lacewing, Chrysoperla rufilabris.

The biological control function provided by natural enemies is regarded as a protection goal that should not be harmed by the application of any new pest management tool. Plants producing Cry proteins from the bacterium, Bacillus thuringiensis (Bt), have become a major tactic for controlling pest Lepidoptera on cotton and maize and risk assessment studies are needed to ensure they do not harm important natural enemies. However, using Cry protein susceptible hosts as prey often compromises such studies. To avoid this problem we utilized pest Lepidoptera, cabbage looper (Trichoplusia ni) and fall armyworm (Spodoptera frugiperda), that were resistant to Cry1Ac produced in Bt broccoli (T. ni), Cry1Ac/Cry2Ab produced in Bt cotton (T. ni), and Cry1F produced in Bt maize (S. frugiperda). Larvae of these species were fed Bt plants or non-Bt plants and then exposed to predaceous larvae of the green lacewing Chrysoperla rufilabris. Fitness parameters (larval survival, development time, fecundity and egg hatch) of C. rufilabris were assessed over two generations. There were no differences in any of the fitness parameters regardless if C. rufilabris consumed prey (T. ni or S. frugiperda) that had consumed Bt or non-Bt plants. Additional studies confirmed that the prey contained bioactive Cry proteins when they were consumed by the predator. These studies confirm that Cry1Ac, Cry2Ab and Cry1F do not pose a hazard to the important predator C. rufilabris. This study also demonstrates the power of using resistant hosts when assessing the risk of genetically modified plants on non-target organisms.

Transgenic Cry1Ab rice does not impact ecological fitness and predation of a generalist spider.

BACKGROUND: The commercial release of rice genetically engineered to express a Cry1Ab protein from Bacillus thuringiensis (Bt) for control of Lepidoptera in China is a subject of debate. One major point of the debate has focused on the ecological safety of Bt rice on nontarget organisms, especially predators and parasitoids that help control populations of insect pests. METHODOLOGY/PRINCIPAL FINDINGS: A tritrophic bioassay was conducted to evaluate the potential impact of Cry1Ab-expressing rice on fitness parameters of a predaceous ground spider (Pardosa pseudoannulata (Bösenberg et Strand)) that had fed on Bt rice-fed brown planthopper (Nilaparvata lugens (Stål)) nymphs. Survival, development time and fecundity of this spider were not different when they were fed with Bt rice-fed or non-Bt rice-fed prey. Furthermore, ELISA and PCR gut assays, as well as a functional response trial, indicated that predation by P. pseudoannulata was not significantly different in Bt rice or non-Bt rice fields. CONCLUSIONS/SIGNIFICANCE: The transgenic Cry1Ab rice lines tested in this study had no adverse effects on the survival, developmental time and fecundity of P. pseudoannulata in the laboratory or on predation under field conditions. This suggests that this important predator would not be harmed if transgenic Cry1Ab rice were commercialized.

Using field-evolved resistance to Cry1F maize in a lepidopteran pest to demonstrate no adverse effects of Cry1F on one of its major predators.

Spodoptera frugiperda (JE Smith) represents the first documented case of field-evolved resistance to a genetically engineered crop expressing an insecticidal protein from Bacillus thuringiensis (Bt). In this case it was Cry1F-expressing maize (Mycogen 2A517). The ladybird beetle, Coleomegilla maculata, is a common and abundant predator that suppresses pest populations in maize and many other cropping systems. Its larvae and adults are polyphagous, feeding on aphids, thrips, lepidopteran eggs and larvae, as well as plant tissues. Thus, C. maculata may be exposed to Bt proteins expressed in genetically engineered crops by several pathways. Using Cry1F-resistant S. frugiperda larvae as prey, we evaluated the potential impact of Cry1F-expressing maize on several fitness parameters of C. maculata over two generations. Using Cry1F resistant prey removed any potential prey-mediated effects. Duration of larval and pupal stages, adult weight and female fecundity of C. maculata were not different when they were fed resistant S. frugiperda larvae reared on either Bt or control maize leaves during both generations. ELISA and insect-sensitive bioassays showed C. maculata were exposed to bioactive Cry1F protein. The insecticidal protein had no effect on C. maculata larvae, even though larvae contained 20-32 ng of Cry1F/g by fresh weight. Over all, our results demonstrated that the Cry1F protein did not affect important fitness parameters of one of S. frugiperda's major predators and that Cry1F protein did not accumulate but was strongly diluted when transferred during trophic interactions.