Genetically engineered crops help support conservation biological control

Eliminating this study reduced the effect size to a non-significant 0.0633.

“Eliminating this study reduced the effect size to a non-significant 0.0633.”

This result was driven by a single study where parasitoids Cotesia plutellae were offered a choice between Bt resistant Plutella xylostella caterpillars on Bt compared with non-Bt oilseed rape in field simulators in the laboratory.

“This result was driven by a single study where parasitoids (Cotesia plutellae; Hymenoptera: Braconidae) were offered a choice between Bt resistant Plutella xylostella (Lepidoptera: Plutellidae) caterpillars on Bt compared with non-Bt oilseed rape in field simulators in the laboratory (Schuler et al., 2003).”

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The majority of bitrophic studies tested material from Bt-transgenic maize, followed by rice, potato, and cotton.

“The majority of studies tested material from Bt-transgenic maize, followed by rice, potato, and cotton.”

Meta-analysis results show that a variety of Bt plants and Cry proteins have no negative effects on a broad range of natural enemy species when non-target species were exposed in an ecologically realistic manner.

“Results mirror those found in prior meta-analyses with fewer studies (Naranjo, 2009) in showing that a variety of Bt plants and Cry proteins have no negative effects on a broad range of natural enemy species when the non-target species were exposed in an ecologically realistic manner (Fig. 4).”

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Through a literature review, 68 publications presenting results from tritrophic studies using Bt plant material as test substance were retrieved.

“Through a literature review, we have retrived 68 publications presenting the results from such tritrophic studies using Bt plant material as the test substance.”

Re-running analyses eliminating all studies that used herbivores as host or prey that did not contain Cry proteins gave similar results.

“We re-ran the analyses eliminating all studies that used herbivores as host or prey that did not contain Cry proteins (Table S1).The results were similar.”

Bitrophic studies where natural enemies were directly fed with Bt plant material have been conducted on a total of 20 species from 6 orders and 12 families.

“To our knowledge, bitrophic studies, where natural enemies were directly fed with Bt plant material, have been conducted on a total of 20 species from 6 orders and 12 families (Table 1).”

With two exceptions, exposure of natural enemies to plant-produced Cry proteins in bitrophic studies has been confirmed or can be expected given the test system and feeding mode.

“With two exceptions, exposure of the natural enemies to the plant produced Cry proteins has been confirmed or can be expected given the test system and the feeding mode of the test organism.”

With the exception of four studies, none of the bitrophic studies has reported putative adverse effects of the Bt plant on natural enemies compared with respective control plant.

“With the exception of four studies, none of the bitrophic studies has reported putative adverse effects of the Bt plant on the natural enemies when compared with the respective control plant.”

Studies with no or negligible exposure were conducted with 7 hymenopteran parasitoids from 4 families and 12 predators from 6 families in 5 orders.

“Studies with no or negligible exposure were conducted with 7 hymenopteran parasitoids from 4 families and 12 predators from 6 families in 5 orders (Table S2).”

A notable exception is the abundance of parasitoids for Bt maize.

“A notable exception is the abundance of parasitoids for Bt maize.”

As of late 2008, over 63 field studies had been conducted to assess potential impacts of Bt crops on non-target arthropods encompassing six classes, >21 orders and >185 species, with vast majority being natural enemies important to biological control services.

“As of late 2008, over 63 field studies had been conducted to assess the potential impacts of Bt crops on non-target arthropods encompassing six classes, > 21 orders and > 185 species, with the vast majority of these being natural enemies important to providing biological control services (Naranjo, 2009).”

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As part of an overall integrated pest management (IPM) strategy, Bt crops can contribute to more effective biological control of both target and non-target pests.

“As part of an overall integrated pest management (IPM) strategy, Bt crops can contribute to more effective biological control of both target and non-target pests.”

The vast majority of studies demonstrates that the insecticidal proteins deployed today cause no unintended adverse effects to natural enemies.

“Overall, the vast majority of studies demonstrates that the insecticidal proteins deployed today cause no unintended adverse effects to natural enemies.”

• AssumptionRests on an assumption: The published laboratory and field studies reviewed are representative and unbiased with respect to the non-target effects of Bt crops.

When Bt crops replace synthetic chemical insecticides for target pest control, this creates an environment supportive of the conservation of natural enemies.

“Furthermore, when Bt crops replace synthetic chemical insecticides for target pest control, this creates an environment supportive of the conservation of natural enemies.”

Bt crops have been shown to promote biological pest control in the system, if foliar insecticides are reduced.

“In addition, they have been shown to promote biological pest control in the system, if foliar insecticides are reduced (Lu et al., 2012;Zhang et al., 2018).”

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Toxicity of the insecticidal protein to natural enemies is typically evaluated in a tiered risk assessment approach conceptually similar to that used for pesticides.

“Toxicity of the insecticidal protein to natural enemies is typically evaluated in a tiered risk assessment approach that is conceptually similar to that used for pesticides.”

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• cites Romeis et al., 2008aNot checked yet

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Modern Bt maize varieties based on transformation events other than event 176, such as MON810 and Bt11, express very low levels of Cry1Ab in the pollen.

“Modern Bt maize varieties based on other transformation events (e.g., MON810, Bt11) express very low levels of Cry1Ab in the pollen (Perry et al., 2010;Shelton and Sears, 2001).”

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• cites Shelton and Sears, 2001Not checked yet

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Assessing potential risk of HT technology compared to conventional cropping systems is difficult.

“Because of this complexity, assessing potential risk of HT technology compared to conventional cropping systems is difficult.”

Only trace amounts of Cry proteins were detected in the honeydew produced by the brown planthopper on different Bt rice lines.

“Only trace amounts of Cry proteins were detected in the honeydew produced by the brown planthopper (Nilaparvata lugens; Hemiptera: Delphacidae) on different Bt rice lines (Bernal et al., 2002;Tian et al., 2018a).”

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• cites Tian et al., 2018aNot checked yet

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Bt plant material entering the decomposition process in the soil is degraded rapidly.

“Bt plant material entering the decomposition process in the soil is degraded rapidly.”

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• cites Nguyen and Jehle, 2007Not checked yet

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The body of literature from more realistic laboratory and field experiments does not provide any evidence for accumulation of Bt proteins in ladybirds.

“However, the body of literature from more realistic laboratory and field experiments does not provide any evidence for such an accumulation (Meissle and Romeis, 2012).”

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Arthropods living in field margins or other elements of the surrounding landscape may encounter Bt proteins from fields where Bt plants are grown.

“However, arthropods living in the field margins or other elements of the surrounding landscape may also encounter Bt proteins from fields where Bt plants are grown.”

During harvest, plant debris might drift to neighboring habitats and expose decomposers and their natural enemies.

“During harvest, in particular when only cobs are harvested and the remaining plant material is shredded and left on the field, parts of the plant debris might drift to neighboring habitats and expose decomposers and their natural enemies (Fig. 2, route 6).”

Natural enemies consuming mainly aphids are generally not exposed to significant concentrations of Bt protein.

“Natural enemies consuming mainly aphids are thus generally not exposed to significant concentrations of Bt protein.”

The process of genetic engineering generally has fewer effects on crop composition compared with traditional breeding methods.

“There is increasing evidence that the process of genetic engineering generally has fewer effects on crop composition compared with traditional breeding methods (Herman and Price, 2013).”

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Insecticidal GE crops work synergistically with other tactics such as conservation biological control to achieve more sustainable pest control.

“They work synergistically with other tactics such as conservation biological control to achieve more sustainable pest control.”

The effects caused by a shift from a conventional weed management scheme to a HT crop system on arthropods and biological control are difficult to predict.

“Overall, the experience available to date shows that the effects caused by a shift from a conventional weed management scheme to a HT crop system on arthropods and biological control are difficult to predict.”

Exposure to plant-produced Bt proteins is longer than it would be with most insecticides because Bt proteins are present constantly.

“Exposure to the pest and non-target organisms is therefore longer than it would be with most insecticides.”

The amount of Bt protein ingested by natural enemies is highly variable and depends on the concentration of the Bt protein in the plant, the stability of the Bt protein, the time of the last meal, the mode of feeding of the herbivore and the natural enemy, and behavior.

“But the amount of Bt protein ingested by natural enemies is highly variable and depends on the concentration of the Bt protein in the plant, the stability of the Bt protein, the time of the last meal, the mode of feeding of the herbivore and the natural enemy, and behavior (Dutton et al., 2003;Romeis et al., 2009).”

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• cites Romeis et al., 2009Not checked yet

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When consuming prey or hosts, bioactive Bt protein is transferred from herbivores to natural enemies.

“When consuming prey or hosts, bioactive Bt protein is thus transferred from herbivores to natural enemies.”

Bt proteins in current crops can be found in the whole plant including roots, stems, leaves, pollen, and fruits.

“Consequently, Bt proteins in current crops can be found in the whole plant including roots, stems, leaves, pollen, and fruits.”

Depending on the crop, the arthropod taxa and the actual changes in crop management, effects of HT crop systems on arthropods and biological control can be positive or negative.

“Depending on the crop, the arthropod taxa and the actual changes in crop management (types of herbicides, application timing, tillage practice, etc.) effects can be positive or negative.”

Bt plants have turned what was once a minor foliar insecticide into a major control strategy.

“Thus, Bt plants have turned what was once a minor foliar insecticide into a major control strategy (Shelton et al., 2008)”

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Concentrations of Bt proteins can vary considerably in different plant tissues, across developmental stages, and among different Bt proteins and transformation events.

“However, concentrations can vary considerably in different plant tissues, across different developmental stages, and among different Bt proteins and transformation events (Eisenring et al., 2017;Knight et al., 2013;Nguyen andJehle 2007, 2009;Obrist et al., 2006a;Svobodová et al., 2017).”

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• cites Knight et al., 2013 sourceNot checked yet

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• cites Nguyen andJehle 2007, 2009Not checked yet

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Excretion and digestion at each trophic level leads to a dilution effect when Bt proteins move along the food chain.

“Furthermore, excretion and digestion at each trophic level leads to a dilution effect when Bt proteins move along the food chain.”

Bt proteins do not seem to enter the phloem sap, which is the food for aphids.

“Bt proteins, however, do not seem to enter the phloem sap, which is the food for aphids (Raps et al., 2001).”

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Bt proteins are generally transferred from plants to herbivores to natural enemies.

“In conclusion, Bt proteins are generally transferred from plants to herbivores to natural enemies.”

The more common route of exposure to Bt proteins for natural enemies is through consumption of prey or hosts.

“While exposure through direct plant feeding might be a significant route of exposure for some natural enemy species or in particular situations (e.g. when no prey is available), the more common route of exposure to Bt proteins is through consumption of prey or hosts (Fig. 2, route 2).”

Aphid honeydew is a negligible route of exposure to plant-produced Bt proteins.

“Consequently, aphid honeydew, which is an important source of energy for both predators and parasitoids (Wäckers, 2005), is a negligible route of exposure to plant-produced Bt proteins (Fig. 2, route 3).”

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The most prominent example of off-crop exposure is pollen from Bt maize deposited on food plants of butterflies in field margins.

“The most prominent example is pollen from Bt maize that is deposited on food plants of butterflies in the field margins (Fig. 2, route 5).”

As a highly effective form of host plant resistance, insecticidal GE crops are a foundational tactic in IPM.

“As a highly effective form of host plant resistance, insecticidal GE crops are a foundational tactic in IPM.”

During pollen shed, butterfly larvae are likely to ingest certain amounts of pollen grains together with their food plant.

“During the period of pollen shed, butterfly larvae are likely to ingest certain amounts of pollen grains together with their food plant (Perry et al., 2010;Schuppener et al., 2012;Shelton and Sears, 2001).”

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• cites Schuppener et al., 2012 sourceNot checked yet

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• cites Shelton and Sears, 2001Not checked yet

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The honeydew route of exposure could be important for insecticidal non-Bt plants.

“Consequently, this route of exposure could be important for insecticidal non-Bt plants.”

It is likely that those unexpected results are artifacts, probably resulting from problems in study design.

“It is thus likely that those results are artifacts, probably resulting from problems in study design (EFSA, 2009;Rauschen, 2010;Ricroch et al., 2010;Romeis et al., 2013aRomeis et al., , 2014b)).”

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Ignorance of prey/host-quality effects has led to erroneous claims that lepidopteran-active Cry proteins cause direct toxic effects on natural enemies.

“Ignorance of prey/host-quality effects has led to erroneous claims that lepidopteran-active Cry proteins cause direct toxic effects on natural enemies (see Shelton et al., 2009 for detailed discussion).”

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Studies with Bt maize pollen from events MON810 and Bt11 lacked exposure given very low concentrations of Cry proteins in pollen of this event.

“Studies conducted with Bt maize pollen from events MON810 and Bt11 (Meissle et al., 2014;Obrist et al., 2006c) also lacked exposure given the very low concentrations of Cry proteins in the pollen of this event (Dutton et al., 2003;Nguyen and Jehle, 2007).”

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• cites Obrist et al., 2006cNot checked yet

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• cites Dutton et al., 2003 sourceNot checked yet

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Recent studies have demonstrated that the lack of unexpected effects is also true for a combination of Cry proteins and dsRNA.

“Recent studies have demonstrated that this is also true for a combination of Cry proteins and dsRNA (Khajuria et al., 2018;Levine et al., 2015;Ni et al., 2017).”

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In general, studies with purified Bt proteins have not indicated any adverse effects on the tested non-target organisms.

“In general, studies with purified Bt proteins have not indicated any adverse effects on the tested non-target organisms.”

The same unsuitability holds for studies that offered eggs to natural enemies from herbivores that developed on Bt-transgenic plants.

“The same holds true for studies that have offered eggs to natural enemies from herbivores that developed on Bt-transgenic plants.”

Differences in composition of plant tissues exist even between a GE line and the respective near-isoline because several breeding steps are necessary to generate a stable GE line from the parental line.

“Because several breeding steps are necessary to generate a stable GE line from the parental line, differences in the composition of plant tissues exist even between a GE line and the respective near-isoline (see Section 3).”

Bt protein concentrations in aquatic systems are expected to be very low due to a huge dilution effect of running water.

“Bt protein concentrations in aquatic systems, however, are expected to be very low due to a huge dilution effect of the running water (Carstens et al., 2012;Tank et al., 2010).”

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The unexpected effects observed in the four bitrophic studies were not caused by the expressed Cry protein but by some unidentified plant-related characteristics.

“In summary, it is apparent, that the unexpected effects observed in these four studies were not caused by the expressed Cry protein but by some unidentified plant-related characteristics.”

These differences are likely to increase when the transgenic event is conventionally crossed into a range of different genetic backgrounds to generate commercial varieties.

“These differences are likely to increase when the transgenic event is conventionally crossed into a range of different genetic backgrounds to generate commercial varieties.”

This lack of direct adverse effects also holds true for Bt plants that produce two or more different insecticidal proteins.

“This also holds true for Bt plants that produce two or more different insecticidal proteins.”

While a few studies claim unexpected non-target effects, none of those claims has been verified in follow-up studies by other research groups.

“While a few studies claim to have revealed unexpected non-target effects, none of those claims has been verified, i.e., confirmed in followup studies conducted by other research groups.”

Valid conclusions about Cry1Ab toxicity are not possible from those studies.

“Thus, valid conclusions about Cry1Ab toxicity are not possible from those studies.”

One challenge with tritrophic studies is that they can lead to erroneous results when sublethally affected Cry-sensitive herbivores are used as prey or hosts.

“One challenge with tritrophic studies is that they can lead to erroneous results when sublethally affected Cry-sensitive herbivores are used as prey or hosts.”

There is increasing evidence in the literature that phloem feeders have extremely low or non-existent titers of Cry proteins in their bodies after feeding on Bt plants.

“This list includes phloem feeding insects like aphids, but there is increasing evidence in the literature that phloem feeders have extremely low or non-existent titers of Cry proteins in their bodies after feeding on Bt plants (Romeis and Meissle, 2011).”

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This can lead to adverse effects on the natural enemy that are related to reduced quality of the prey/host rather than to the insecticidal protein itself.

“This can lead to adverse effects on the natural enemy that are related to the reduced quality of the prey/host rather than to the insecticidal protein itself (Fig. 3) (Naranjo, 2009;Romeis et al., 2006).”

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The importance of prey/host-quality effects has been demonstrated experimentally for parasitoids Diadegma insulare and Macrocentrus cingulum and predators C. carnea and C. maculata.

“The importance of such prey/host-quality effects has been demonstrated experimentally for the parasitoids Diadegma insulare (Hymenoptera: Ichneumonidae) (Chen et al., 2008) and Macrocentrus cingulum (Hymenoptera: Braconidae) (Wang et al., 2017) and for the predators C. carnea (Lawo et al., 2010) and C. maculata (Li et al., 2011).”

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• cites Lawo et al., 2010 sourceNot checked yet

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The available body of literature provides evidence that insecticidal proteins used in commercialized Bt crops cause no direct, adverse effects on non-target species outside the order or family of the target pest(s).

“In summary, the available body of literature provides evidence that insecticidal proteins used in commercialized Bt crops cause no direct, adverse effects on non-target species outside the order (i.e., Lepidoptera for Cry1 and Cry2 proteins) or the family (i.e.Coleoptera, Chrysomelidae for Cry3 proteins) of the target pest(s).”

The exceptions are studies with adult egg parasitoids of genus Trichogramma, which cannot feed on maize pollen grains due to their minute size.

“The exceptions are studies conducted with adult egg parasitoids belonging to the genus Trichogramma (Hymenoptera: Trichogrammatidae) which, due to their minute size, are not able to feed on maize pollen grains (Romeis et al., 2005).”

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Extensive experimental work documented the role of natural enemies generally and their conservation specifically in the suppression and economic management of B. tabaci.

“Extensive experimental work documented the role of natural enemies generally and their conservation specifically in the suppression and economic management of B. tabaci (Asiimwe et al., 2016;Naranjo andEllsworth, 2005, 2009b;Vandervoet et al., 2018).”

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• cites Naranjo andEllsworth, 2005Not checked yet

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• cites Vandervoet et al., 2018 sourceNot checked yet

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Without this capstone event, it is unlikely this success would have been possible.

“Without this capstone event, it is unlikely this success would have been possible.”

The use of insecticides for Bt targeted pests in non-Bt crops can significantly reduce biological control function.

“In contrast, the use of insecticides for Bt targeted pests in non-Bt crops can significantly reduce biological control function (Musser and Shelton, 2003;Rose, 2005).”

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This together with bitrophic results confirms that transformation-related, unintended effects do not appear to impair natural enemy performance.

“This together with the results from the bitrophic studies (Section 5.2) also confirms that transformation-related, unintended effects do not appear to impair natural enemy performance.”

In the first comparison study, adult parasitoids only emerged from Cry1C-resistant diamondback moth larvae.

“Adult parasitoids only emerged from the Cry1C-resistant larvae.”

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The impact of Bt crops on biological control services supplied by generalist arthropod predators has been uniformly neutral in Bt maize and Bt cotton.

“The impact of Bt crops on the biological control services supplied by generalist arthropod predators have been uniformly neutral in Bt maize (Ahmad et al., 2006) and Bt cotton (Head et al., 2005;Naranjo, 2005b;Olson and Ruberson, 2012;Sisterson et al., 2004).”

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• cites Naranjo, 2005bNot checked yet

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Reductions in target host abundance do not always lead to reductions in biological control function.

“However, reductions in target host abundance do not always lead to reductions in biological control function (Dhillon and Sharma, 2013;Fernandes et al., 2007;Lumbierres et al., 2011;Orr and Landis, 1997;Rose, 2005;Thomazoni et al., 2010).”

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• cites Lumbierres et al., 2011 sourceNot checked yet

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Overall, field studies have collectively concluded that nontarget effects of Bt crops are minimal or negligible, especially in comparison to negative effects of insecticide use for control of Bt targeted pest.

“Overall, these studies have collectively concluded that nontarget effects of Bt crops are minimal or negligible, especially in comparison to the negative effects of the use of insecticides for control of the Bt targeted pest (Fig. 5).”

Only one study observed small reductions in several arthropod predator taxa in Bt cotton in long-term field studies in Arizona that were likely associated with reductions in caterpillar prey.

“Only one study observed small reductions in several arthropod predator taxa in Bt cotton in long term field studies in Arizona that were likely associated with reductions in caterpillar prey (Naranjo, 2005a).”

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Bt cotton was a keystone technology that eliminated the early season use of broad-spectrum insecticides for pink bollworm.

“While many components contributed to this transformative change that allowed conservation biological control to function at a high capacity in Arizona cotton production, Bt cotton was a keystone technology that eliminated the early season use of broad-spectrum insecticides for pink bollworm.”

Considerable laboratory research has demonstrated the safety of Bt proteins to a suite of important natural enemies.

“As noted, there has been considerable laboratory research demonstrating the safety of Bt proteins to a suite of important natural enemies.”

The compatibility of Bt crops and biological control has been well documented with Bt cotton in Arizona as part of their overall IPM program.

“The compatibility of Bt crops and biological control has been well documented with Bt cotton in Arizona as part of their overall IPM program.”

The analyses of tritrophic studies provide further substantiation of the lack of effects of Bt plants and different Cry proteins on the biology or function of natural enemies.

“The analyses of the tritrophic studies provide further substantiation of the lack of effects of Bt plants and different Cry proteins on the biology or function of natural enemies.”

Changes in the target herbivore community are not unique to Bt crops, but would arise from deployment of any effective pest management tactic or overall IPM strategy.

“Overall, such changes in the target herbivore community are not unique to Bt crops, but would arise from the deployment of any effective pest management tactic or overall IPM strategy.”

The data available do not support the proposal that in-planta studies are needed to fully assess Bt-plant effects on natural enemies.

“Thus, the data available do not support the proposal by some scientists (Arpaia et al., 2017) and the European Food Safety Authority (EFSA) (EFSA, 2010) that in-planta studies are needed to fully assess the Bt-plant effects on natural enemies (see Devos et al., 2016 for detailed discussion).”

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These progressive reductions in insecticide use provided an environment that allowed biological control by a diverse community of native natural enemies to flourish.

“These progressive reductions in insecticide use provided an environment that allowed biological control by a diverse community of native natural enemies to flourish.”

Using predator:prey ratios, sentinel prey and life tables of natural populations of Bemisia tabaci, it was shown that these small reductions in predator abundance were not associated with any change in overall biological control services provided by the natural enemy community.

“However, using predator:prey ratios, sentinel prey and life tables of natural populations of Bemisia tabaci (Hemiptera: Aleyrodidae), it was shown that these small reductions in predator abundance were not associated with any change in the overall biological control services provided by the natural enemy community (Naranjo, 2005b).”

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In Arizona, Bt cotton led to dramatic reductions in the use of foliar insecticides for the target pest, all of them broad-spectrum in nature.

“In Arizona, Bt cotton led to dramatic reductions in the use of foliar insecticides for the target pest, all of them broad-spectrum in nature (Henneberry and Naranjo, 1998).”

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These effects were not only observed in the Bt crop itself but also in other (non-GE) crops within the region.

“More importantly, these effects were not only observed in the Bt crop itself but also in other (non-GE) crops within the region.”

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Biological control may play a significant role in limiting the number of cases of resistance to Bt plants to date, especially compared to the ever-increasing cases of resistance to broad-spectrum insecticides.

“These findings suggest that biological control, in addition to other factors including refuges and gene expression (Tabashnik et al., 2013), may play a significant role in limiting the number of cases of resistance to Bt plants to date, especially compared to the ever-increasing cases of resistance to broad-spectrum insecticides (Sparks and Nauen, 2015).”

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• cites Sparks and Nauen, 2015Not checked yet

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Bt sweet corn provides better control of lepidopteran pests than lambda cyhalothrin and indoxacarb.

“Furthermore, this study demonstrated that Bt sweet corn provided better control of lepidopteran pests, and did not negatively affect the predation rates of sentinel egg masses of the European corn borer, as did lambda cyhalothrin and indoxacarb.”

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Targeted pests are evolving resistance to Bt proteins expressed in plants.

“With the threat of targeted pests evolving resistance to Bt proteins expressed in plants (Tabashnik and Carrière, 2017), investigations have been undertaken to determine whether natural enemies may help delay resistance to Bt proteins in the targeted pest.”

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In China, dozens of rice lines with resistance to various lepidopteran pests have been developed that are highly resistant to stem borers such as Chilo suppressalis.

“For example, in China dozens of rice lines with resistance to various lepidopteran pests have already been developed that are highly resistant to stem borers such as Chilo suppressalis (Crambidae) (Li et al., 2016;Liu et al. 2016a).”

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• cites Liu et al. 2016aNot checked yet

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Seed treatments in maize have the potential to erase some of the positive gains in foliar insecticide reduction in maize.

“Thus, such treatments have the potential to erase some of the very positive gains in foliar insecticide reduction in maize.”

Modified Cry51Aa2 protein (Cry51Aa2.834_16) protects cotton against feeding damage caused by hemipteran and thysanopteran pests.

“An example is modified Cry51Aa2 protein (Cry51Aa2.834_16)that protects cotton against feeding damage caused by hemipteran and thysanopteran pests (Baum et al., 2012;Gowda et al., 2016;Bachman et al., 2017).”

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• cites Gowda et al., 2016 sourceNot checked yet

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• cites Bachman et al., 2017 sourceNot checked yet

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The finding on the importance of conserving biological control agents was instrumental in the development of the Integrated Control Concept.

“This key finding on the importance of conserving biological control agents was instrumental in the development of the Integrated Control Concept (Smith and Hagen, 1959;Stern and van den Bosch, 1959;Stern et al., 1959), the precursor of the IPM concept.”

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In the northeastern US, Bt sweet corn is far less toxic to the major predators C. maculata, H. axyridis, and Orius insidiosus than the commonly used pyrethroid lambda cyhalothrin, spinosad, and indoxacarb.

“In the northeastern US where a considerable amount of sweet corn is grown, studies have shown that Bt sweet corn is far less toxic to the major predators in the system (ladybeetles C. maculata and H. axyridis and the minute pirate bug, Orius insidiosus [Hemiptera: Anthocoridae]), than the commonly used pyrethroid lambda cyhalothrin, spinosad, and indoxacarb (Musser and Shelton, 2003).”

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Cowpea contains Cry1Ab to protect the plant from damage by Maruca testulalis.

“Another example is that of cowpea (Vigna unguiculata ssp.unguiculata) that contains Cry1Ab to protect the plant from damage by Maruca testulalis (Lepidoptera: Crambidae) (Ba et al., 2018;Huesing et al., 2011;Mohammed et al., 2014).”

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• cites Mohammed et al., 2014 sourceNot checked yet

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In sweet corn, conservation of natural enemies with Bt plants results in enhanced biological control.

“Studies in sweet corn, which is routinely treated with foliar insecticides far more than field corn, have been able to document that the conservation of natural enemies with Bt plants results in enhanced biological control.”

Cry1Ac causes no harm to D. insulare compared to other commonly used insecticides for control of P. xylostella.

“This latter finding agrees with previous studies using this experimental system that demonstrated the lack of harm to the parasitoid by Cry1Ac, compared to other commonly using insecticides for control of P. xylostella (Chen et al., 2008).”

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Use of selective insecticides can control the spotted alfalfa aphid without disrupting an important parasitoid that helped keep it in check.

“Work by Stern and colleagues in California in the 1950 s demonstrated that use of selective insecticides could be used to control the spotted alfalfa aphid without disrupting an important parasitoid that helped keep it in check (Smith and Hagen, 1959;Stern and van den Bosch, 1959;Stern et al., 1959).”

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• cites Stern and van den Bosch, 1959Not checked yet

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Studies have shown that using Bt maize (field corn) has resulted in large global reductions in the use of foliar insecticides for control of Lepidoptera.

“As for cotton, studies have shown that using Bt maize (field corn) has resulted in large global reductions in the use of foliar insecticides for control of Lepidoptera (Klümper and Qaim, 2014;Brookes and Barfoot, 2018).”

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Bt cowpea has the potential to significantly reduce yield loss caused by M. testulalis in sub-Saharan Africa.

“While the plant has not yet been approved, it has the potential to significantly reduce the yield loss caused by this major pest in sub-Saharan Africa, where cowpea is the most important grain legume (Murdock et al., 2008).”

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RNAi effects caused by ingested dsRNA have been shown in various insect orders but with highly variable success rates in down regulation of target genes.

“RNAi effects caused by ingested dsRNA have been shown in various insect orders but with highly variable success rates in the down regulation of the target genes (Baum and Roberts, 2014;Huvenne and Smagghe, 2010).”

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Combining Bt Cry proteins with RNAi has great potential to delay resistance development.

“Combing Bt Cry proteins with RNAi has great potential to delay resistance development (Khajuria et al., 2018;Ni et al., 2017).”

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The wound-inducible AoPR1 promotor isolated from Asparagus officinalis has been successfully used in cotton and potato.

“Another example is the successful use of the wound-inducible AoPR1 promotor isolated from Asparagus officinalis in cotton and potato (Ahmed et al., 2017;Anayol et al., 2016).”

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• AssumptionRests on an assumption: In today's Bt-transgenic plants, expression of insecticidal genes is driven by constitutive promotors (e.g., CaMV 35s) and the proteins are constantly produced in most plant tissues.

Plants can be developed to produce dsRNA that silences an essential gene in the target species after ingestion.

“Another promising new development is the use of RNA interference (RNAi) to control arthropod pests by developing plants to produce double-stranded RNA (dsRNA) that silences an essential gene in the target species after ingestion (Burand and Hunter, 2013;Zhang et al., 2017).”

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Studies on numerous non-target species using the dsRNA targeting Snf7 in D. v. virgifera have demonstrated this specificity.

“Studies on numerous non-target species using the dsRNA targeting Snf7 in D. v. virgifera have demonstrated this specificity (Bachmann et al., 2016).”

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Zhang et al. (2015) reported control of the Colorado potato beetle by expressing dsRNA in chloroplasts of potato.

“Later, Zhang et al. (2015) reported control of the Colorado potato beetle Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) by expressing dsRNA in chloroplasts of potato.”

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The feasibility of using wound-inducible promoters to drive cry genes has been documented in glasshouse and field for rice where cry genes were driven by the wound-inducible mpi promotor from maize.

“The feasibility of this approach has been documented in the glasshouse and in the field for rice where cry genes were driven by the woundinducible mpi promotor from maize (Breitler et al., 2001(Breitler et al., , 2004).”

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• AssumptionRests on an assumption: In today's Bt-transgenic plants, expression of insecticidal genes is driven by constitutive promotors (e.g., CaMV 35s) and the proteins are constantly produced in most plant tissues.

Planting of Bt crops has tended to result in higher insect biodiversity on farms than planting similar varieties without the Bt trait that were treated with synthetic insecticides.

“On the basis of the available data, the committee found that planting of Bt crops has tended to result in higher insect biodiversity on farms than planting similar varieties without the Bt trait that were treated with synthetic insecticides.”

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Because the RNAi effect is sequence specific, dsRNA can be designed to specifically target the gene in the target pest insect.

“Because the RNAi effect is sequence specific, the dsRNA can be designed to specifically target the gene in the target pest insect.”

The alpha-amylases of hymenopteran parasitoids of bruchids are susceptible to αAI-1.

“Despite the fact that the alphaamylases of hymenopteran parasitoids of bruchids are also susceptible to this particular inhibitor (Álvarez-Alfagemen et al., 2012), tritrophic studies have shown that the αAI-1 containing GE seeds cause no harm to their parasitoids (Lüthi et al., 2013b(Lüthi et al., , 2018)).”

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RNAi can target hemipteran pests, including phloem-feeders, that have not yet been targeted by Bt proteins.

“What makes the technology interesting is the fact that one can also target hemipteran pests (including phloem-feeders) that have not yet been targeted by Bt proteins (Baum and Roberts, 2014;Ibrahim et al., 2017).”

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Insects can develop resistance to dsRNA.

“A recent study demonstrated that insects can develop resistance to dsRNA (Khajuria et al., 2018).”

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Suppression of serotonin biosynthesis resulted in enhanced insect resistance.

“The suppression of the serotonin biosynthesis resulted in enhanced insect resistance.”

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• AssumptionRests on an assumption: The CYP71A1 gene encodes an enzyme that catalyzes the conversion of tryptamine to serotonin.

By knocking out the cytochrome P450 gene CYP71A1, rice plants became resistant against rice brown planthopper and striped stem borer.

“By knocking out the cytochrome P450 gene CYP71A1, rice plants became resistant against rice brown planthopper (N.lugens) and striped stem borer (C.suppressalis) (Lu et al., 2018).”

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αAI-1 containing GE seeds cause no harm to their parasitoids in tritrophic studies.

“Despite the fact that the alphaamylases of hymenopteran parasitoids of bruchids are also susceptible to this particular inhibitor (Álvarez-Alfagemen et al., 2012), tritrophic studies have shown that the αAI-1 containing GE seeds cause no harm to their parasitoids (Lüthi et al., 2013b(Lüthi et al., , 2018)).”

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In the USA, and possibly other parts of the world, the benefit of Bt crops is to some extent counteracted by the increasing application of insecticidal seed treatments to both Bt and non-Bt crops for management of early season pests and as insurance against sporadic pests.

“However, in the USA, and possibly other parts of the world, this benefit is to some extent counteracted by the increasing application of insecticidal seed treatments (to both Bt and non-Bt crops) for the management of early season pests and as insurance against sporadic pests (Allen et al., 2018;Sappington et al., 2018).”

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The use of Bt crops typically replaces chemical broad-spectrum insecticides, including foliar sprays and soil insecticides.

“The use of Bt crops typically replaces chemical broad-spectrum insecticides (foliar sprays and soil insecticides).”

The GE maize event MON87411 produces a dsRNA targeting the Snf7 protein in D. v. virgifera, which is crucial for the transport of transmembrane proteins.

“This GE maize event (MON87411) produces a dsRNA targeting the Snf7 protein in D. v. virgifera, which is crucial for the transport of transmembrane proteins (Bachman et al., 2013;Bolognesi et al., 2012).”

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Large-scale adoption of Bt crops in some parts of the world has led to area-wide suppressions of target pest populations benefitting both farmers that adopted the technology and those that did not.

“Furthermore, the large-scale adoption of Bt crops in some parts of the world has led to area-wide suppressions of target pest populations benefitting both farmers that adopted the technology and those that did not.”