Toxicity of cry1Ab Produced in Escherichia coli or Bt Maize to Nontarget Invertebrates and nonmammalian Vertebratesab

nontarget organism NoELc

Invertebrates

Insects

Honeybee (Apis mellifera) 20 ppm

Ladybird beetles (Hippodamia convergens) 20 ppm

Green lacewing (Chrysoperla carnea) 16 ppm

Wasp parasite (Brachymeria intermedia) 20 ppm

Springtail (Folsomia candida) 50 ng/g leaf tissue Earthworms

Earthworm (Eisenia fetida) 200 mg/kg soil Freshwater crustacead

Daphnid (Daphnia magna) 100 mg pollen/liter Vertebrates

Northern bobwhite quaile 100,000 ppm

Channel catfish > 3 ng/g maize feed

Broiler chickense > 3 ng/g maize feed a From Yu, L., Berry, R.R., and Croft, B.A., Effects of Bacillus thuringiensis toxins in transgenic cotton and potato on Folsomia candida (Collembola: Isotomidae) and Oppia nitens (Acari: Orbatidae), Ecotoxicol., 90, 113, 1997; Brake, J. and Vlachos, D., Evaluation of transgenic event 176 Bt-corn in broiler chickens, Poult. Sci., 77, 648, 1998; and Sanders, P.R. et al., Safety assessment of insect-protected corn, in Biotechnology and Safety Assessment, 2nd ed., Thomas, J.A., Ed., Taylor & Francis, Ltd, London. 1998, pp. 241-256; and "Factsheets" produced by the U. S. Environmental Protection Agency.

b Results of similar tests on other Cry proteins used in Bt-crops are similar, and can be viewed on the above website.

c Tests are conducted using a single, high level of toxin — much higher than that estimated the test organisms would likely encounter under field conditions. This is referred to as the no-observed-effect-level (NOEL). d Bt maize pollen. e Fed Bt maize grain.

amount of Cry protein in a maturing field is estimated to be about 500 g per hectare, and thus the test levels are adjusted to ensure a dose of 10 to 100 times this level. To date, no significant effects have been found on nontarget invertebrates and vertebrates evaluated in these studies.

Regardless of the whether the results obtained against nontarget organisms in laboratory studies show favorable, unfavorable, or neutral effects, these must be followed by long-term studies under field conditions. The reason is that laboratory studies are designed to only reveal any potential acute adverse effects (hazards) in a short time period by exposing nontarget organisms to excessively high levels of Bt proteins — levels that would not be encountered under field conditions. Moreover, field studies should include a more appropriate control (comparisons to the chemical insecticides currently used in agriculture). Until recently, only a few studies evaluated the effects of Bt crops on nontarget organisms under field conditions over the length of the growing season. In these initial studies carried out in the mid-1990s in the United States, the nontarget organisms studied under field conditions were all insects or spiders and the test crops were either Bt corn or Bt cotton producing Cry1 proteins. The insects consisted of a plant bug and four beneficial insects, specifically two parasites and two predators, one of which was the lacewing (Chrysoperla carnea). These studies were important because nontarget organisms and their prey were exposed to Bt Cry proteins in the form synthesized in the crop and over a continuous period at an operational level.101-103 In these season-long studies, no adverse effects were observed on any of the nontargets under field conditions (Table 3.9).

These preliminary field studies provided evidence that Bt crops would be safe for most nontarget invertebrates under operational growing conditions, thereby supporting earlier laboratory studies on Bt crop safety. However, shortly after publication of these studies several reports of detrimental effects of Bt Cry proteins and Bt crops questioned the putative safety of Bt crops. The most widely publicized of these studies was a study of the potential impact of Bt corn on larvae of the Monarch butterfly (Danaus plexippus), showing that these are sensitive to Bt corn (Cry1Ab) pollen.104 In this laboratory study, milkweed leaves were covered with Bt corn pollen and then fed to larvae. Control larvae were fed milkweed leaves covered with non-Bt pollen or untreated milkweed. The key finding of the study was that the larvae fed milkweed leaves treated with an unknown amount of Bt pollen had a lower survival rate (56%) in comparison to the controls (100%). The authors reported that their results had "potentially profound implications for the conservation of Monarch butterflies" because the central corn belt, where Bt corn adoption by farmers was likely to continue to increase (and has) is also an important breeding area for Monarch butterflies in the United States.

TABLE 3.9

Effects of Bt Crops on Nontarget Invertebrates Under Field Conditions: Short-Term Studies

TABLE 3.9

Effects of Bt Crops on Nontarget Invertebrates Under Field Conditions: Short-Term Studies

Nontarget

Cry

Adverse

(Insect Order)

Crop

Protein

Effects

Reference

Lygus lineolaris

Cotton

CrylAc

None

Hardee and Bryan, 1997100

(Heteroptera)

Coleomegilla maculata

Maize

CrylAb

None

Pilcher et al., 1997101

(Coleoptera)

Orius insidiosus

Maize

CrylAb

None

Pilcher et al., 1997101

(Heteroptera)

Chrysoperla carnea

Maize

CrylAb

None

Pilcher et al., 1997102

(Neuroptera)

Eriborus tenebrans

Maize

CrylAb

None

Orr and Landis, 1997103

(Hymenoptera)

Macrocentrus grandi

Maize

CrylAb

None

Orr and Landis, 1997103

(Hymenoptera)

(Hymenoptera)

In assessing the relevance of the findings on Monarch larvae, or other nontarget organisms for that matter, it should be kept in mind that bacterial insecticides based on Bt should be just as toxic, if not more so. This is because, as noted above, the insecticidal components of foliar Bt insecticides, i.e., several different Cry proteins, viable spores, and synergists, are greater than in Bt crops, which even now only contain one or two insecticidal Cry proteins. In other words, Monarch larvae that feed under field conditions on milkweed leaves treated with a product that contains Btk, from which the Cry1Ab protein gene in Bt corn was derived, will be equally if not more sensitive to the bacterial insecticide. Similarly, predators that feed on caterpillars intoxicated as a result of feeding on a Bt insecticide will be equally sensitive to the activated toxins in these larvae. So the issue here is not so much one of Bt crops but whether Cry proteins will impact beneficial insects regardless of the source.

Extraordinary coverage was given to the preliminary reports in the scientific and popular press on the potential negative effects of Bt pollen on Monarch populations. A benefit of this attention was that it resulted in a series of collaborative studies in 1999 and 2000 devoted to a much more rigorous assessment of these potential negative effects under field conditions throughout the U.S. corn belt and Canada.105,106 Based on these studies, it was concluded that the effects of Bt corn on Monarch populations were "negligible," especially in comparison to the effects of using chemical insecticides to control corn pests. In part, this is a result of the low Cry protein levels that occur in most currently marketed varieties of Bt corn.106 However, even in cases where high levels of Cry1Ab are produced in pollen, the overall impact on Monarch populations would likely be negligible. This is because (1) pollen is only shed during a limited period of the corn growing season; (2) use of Bt corn reduces the use of chemical insecticides; and (3) milkweed, the host plant of Monarch larvae, grows in many regions of the United States and Canada where Bt corn is not grown. In a similar study carried out under field conditions, it was also found that Bt corn pollen would not likely have any significant impact on populations of the black swallowtail (Papillio polyxenes).101

In other less-known studies on the effects of Bt proteins on nontarget invertebrates, it was reported that immature lacewings (C. carnea) fed on prey that had been fed Bt corn (Cry1Ab) suffered greater mortality than control lacewings fed prey that had eaten non-Bt corn.108 Only 37% of the C. carnea fed Bt cornfed larvae of the cotton leafroller (Spodoptera littoralis) or the European corn borer (Ostrinia nubilalis) survived, whereas 62% of the control group fed on non-Bt corn fed caterpillars survived. In a subsequent study, using an artificial liquid diet, it was determined that immature C. carnea were sensitive to the Cry1Ab toxin at a level of 100 ^g/g per milliliter of diet.108 However, the level of Cry1Ab in maize is about 4 |j.g/g fresh weight, which is considerably less than 100 ^g/ml.109 The results of this study added to the controversy surrounding the safety of Bt crops to nontarget invertebrates, especially because lacewings, as natural predators of many insect pests, are considered beneficial insects. In a more recent study, however, the original studies on C. carnea were shown to be erroneous.110 Specifically, it was found that the C. carnea mortality attributed in the original studies was actually due to nutritional differences in the diets, not to Cry protein intoxication. Interestingly, the latter study was from the laboratory that published the original studies drawing attention to the potential impacts of Bt corn on C. carnea.

As part of subsequent, much more comprehensive efforts to evaluate the effects of Bt crops on nontarget organisms, several large-scale, long-term studies of from two to six years were initiated in the United States and Australia to examine the effects of Bt cotton and Bt corn production on the complex nontarget arthropod communities present in these agro-ecosystems. The Cry proteins produced by these crops included several that are insecticidal for either lepidopteran or coleopteran insects and which generally result in virtually total reduction in target pest damage (in the case of lepidopteran pests), or marked reductions (in the case of coleopteran pests). Thirteen of these nontarget effects studies were published in 2005 in a special issue of Environmental Entomology. These studies assessed of effects of Bt cotton and Bt corn on a wide range of foliage and ground-dwelling invertebrates, of from 5 to more than 200 taxa, under various growing conditions and in a wide range of different geographical regions. The principal findings were (1) Bt crops are highly selective in their insect spectrum of activity, acting in most cases only against the target pests; and (2) the use of chemical insecticides on the same crops typically resulted in significant reductions in nontarget populations. Some "minor changes" in the abundance of a few nontarget invertebrate species were observed in some of the Bt crops when compared with untreated non-Bt crops, but "almost all of these effects were explained by expected changes in target pest populations."111 For example, if you eliminate larvae of the target pest H. virescens from a large area of Bt cotton, it is expected that the population of a parasitic wasp that depends on this pest species as a host will also be reduced significantly. In these studies, those that included a broad-spectrum chemical insecticide showed that the damaging effects these had on nontarget populations could be long-term. An overall summary of representative studies from this series, chosen on the basis of crop and nontarget diversity tested by geographical region, is presented in Table 3.10. In addition, here we summarize the highlights of several of these studies to illustrate the key findings that support the above conclusions. Each of these studies involved the collection and statistical analysis of very large data sets for numerous species that were monitored repeatedly throughout multiple growing seasons. As part of our overview, we provide graphical illustrations that present typical results of these studies, beginning with those carried out on Bt cotton.

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