Issue:

Can Genetically Engineered Crops Cause Adverse Effects on Nontarget Organisms?

Response:

Various published studies analyzed effects of Bt maize on nontarget insects. Two well-known studies focused on monarch butterflies (1) and on black swallowtails (2). The first, a note to Nature in 1999, was a laboratory study in which monarch caterpillars were fed milkweed leaves dusted with loosely quantified amounts of pollen from a single Bt corn variety. In the second study in 2000, black swallowtail caterpillars were placed different distances from a cornfield planted with a Bt corn variety different from that used in the 1999 study; populations were studied for effects of Bt for seven days. In the first study more monarch caterpillars died when they ate leaves dusted with Bt corn pollen versus leaves dusted with conventional corn pollen. In the second study, no negative effects of Bt pollen were found on numbers of swallowtail caterpillars.

After those papers appeared, data from numerous university studies performed in the laboratory and in the field on the effects of Bt corn on monarch butterflies were published (3; for a summary of studies see References 4 and 5). After reviewing the data, the U.S. EPA concluded there was a very low probability of risk to monarch butterflies beyond 12 feet from the Bt corn field. Two varieties, Bt11 and Mon810, had no acute adverse effects, even at pollen densities greater than the highest densities observed in cornfields (6). Another variety, 176, had limited negative impacts on some nontarget insects because expression of the 3’ truncated cry1Ab was linked to a maize pollenspecific promoter (2). Rates of larval survival and weight gain in fields of 176, however, were much greater than in fields sprayed with the insecticide Warrior 1E (7). The EPA concluded from these studies that Bt corn was not a significant factor in field death of monarch larvae, particularly relative to factors such as the widespread use of pesticides and destruction of the butterfly’s winter habitats (8, 9).

To “encourage evidence-based risk analysis,” Marvier et al. (10) published a report in 2007 describing a searchable database on the effects of Bt on nontarget insects (11). In a metaanalysis of 42 field experiments, taking into account location, duration, plot sizes, and sample sizes, these authors concluded that (a) the mean abundance of all nontarget invertebrate groups, in terms of numbers, survival, and growth, was greater in Bt cotton and Bt maize fields than in non-Bt fields managed with insecticides but, (b) if Bt crop fields and insecticide-free fields were compared, certain nontarget insects were less abundant in Bt fields.

Effects of Bt on the biodiversity of nontarget soil microorganisms were studied following four years of cultivation of four maize varieties with two different Bt proteins (Cry1Ab and Cry3Bb1) versus near isogenic non-Bt varieties (12). In general, although numbers and types of microbes and enzyme activities differed from season to season and among varieties, no statistically significant differences were seen in numbers of different microbes, enzyme activities, or pH between soils with Bt and non-Bt corn. In similar studies comparing impacts on the rhizosphere of Bt cotton versus non-Bt cotton, various enzymatic activities were measured before and after harvest (13). The authors concluded that richness of the microbial communities in the rhizosphere did not differ between Bt and non-Bt cotton. No Cry2Ab protein was detected in the rhizosphere soil of field-grown Bt rice (14).

Effects on foliage-dwelling arthropods of Bt maize expressing Cry3Bb1 to protect against corn rootworm (Diabrotica sp.) were compared with those of conventional insecticide treatments (15). Bt maize had no consistent adverse impacts on abundance of any nontarget arthropods; however, insecticide treatments applied to the plant foliage significantly and consistently decreased abundance of three nontarget insects: ladybird beetles, lacewings, and damsel bugs. Thus, reducing foliar sprays with the use of Bt corn has the potential to enhance approaches using biological control agents.

Another potential effect of Bt crops on nontarget organisms is the passage of Bt from fields to nearby aquatic environments with the possibility of increasing horizontal gene flow to microbes and mortality of nontarget stream insects. To test this potential effect, soil, sediment, and water samples were analyzed after spiking sediments and surface waters with Bacillus thuringiensis kurstaki and genomicDNA from GE Bt corn (16). PCR analyses revealed that half-lives for both sources of Bt DNA were 1.7 d for clay- and sand-rich sediments and 14.3 d in surface water. Soil, sediment, and surface water from Bt maize fields were also tested for the presence of cry1Ab two weeks after pollen release, after corn harvest, and after mechanical root remixing. Sediments had more cry1Ab DNA than surface water, perhaps reflecting binding to soil particles that increased its persistence; however, Cry1Ab protein was undetectable in most samples. Without making field measurements on nontarget populations, it was suggested that release of products with Bt transgenes into the environment might adversely affect nontarget organisms; however, other researchers objected because actual measurements were not made (17, 18).

Although many studies focus on potential negative effects of Bt on nontarget organisms, potential benefits to nontarget insects have also been noted. Bt maize is more susceptible to corn leaf aphids (Rhopalosiphyum maidis), which leads to larger colony densities and increased production of the honeydew consumed by beneficials such as a parasitoid of aphids, Cotesia marginiventris (19). This observation underscores the delicate balance in nature between beneficial and detrimental side effects of insect protection strategies.

References:

1. Losey JE, Rayor LS, Carter ME. 1999. Transgenic pollen harms monarch larvae. Nature 399:214

2. Wraight CL, Zangerl AR, Carroll MJ, Berenbaum MR. 2000. Absence of toxicity of Bacillus thuringiensis pollen to black swallowtails under field conditions. Proc. Natl. Acad. Sci. USA 97:7700–3

3. Carpenter JE, Gianessi LP. 2001. Agricultural Biotechnology: Updated Benefit Estimates, pp. 1–46. Washington, DC: Natl. Cent. Food Agric. Policy. http://www.ncfap.org/documents/updatedbenefits.pdf. Last accessed 2011-12-9. PDF

4. Environ. Prot. Agency (EPA). 2000. Bt plant-pesticides biopesticides registration action document. http://www.epa.gov/oscpmont/sap/meetings/2000/october/brad3_enviroassessment.pdf. Last accessed 2011-12-9. PDF

5. Sears MK, Hellmich RL, Stanley-Horn DE, Oberhauser KS, Pleasants JM, et al. 2001. Impact of Bt corn pollen on monarch butterfly populations: A risk assessment. Proc. Natl. Acad. Sci. USA 98:12326–30
Describes five independent field studies—commissioned to investigate findings reported by Losey et al. (1999)—to determine impact of Bt corn pollen on the survival of nontarget monarch butterfly larvae.

6. Pleasants JM, Hellmich RL, Dively GP, Sears MK, Stanley-Horn DE, et al. 2001. Corn pollen deposition on milkweeds in and near cornfields. Proc. Natl. Acad. Sci. USA 98:11919–24

7. Stanley-Horn DE, Dively GP, Hellmich RL, Mattila HR, Sears MK, et al. 2001. Assessing the impact of Cry1Ab-expressing corn pollen on monarch butterfly larvae in field studies. Proc. Natl. Acad. Sci. USA 98:11931–36

8. MonarchWatch. 2007. MonarchWatch Email Updates. http://www.monarchwatch.org/update/index.html. Last accessed 2011-12-9. PDF

9. Pimentel DS, Raven PH. 2000. Bt corn pollen impacts on nontarget Lepidoptera: Assessment of effects in nature. Proc. Natl. Acad. Sci. USA 97:8109–99

10. Marvier M, McCreedy C, Regetz J, Kareiva J. 2007. A Meta-analysis of effects of Bt cotton and maize on nontarget invertebrates. Science 316:1475–77
Creates a searchable database for nontarget effects of Bt crops plus results of meta-analysis of 42 field experiments on nontarget invertebrates.

11. Natl. Cent. Ecol. Anal. Synth. 2008. Nontarget effects of Bt crops. http://delphi.nceas.ucsb.edu/btcrops. Last accessed 2011-12-9. PDF

12. Icoz I, Saxena D, Andow DA, Zwahlen C, Stotzky G. 2008. Microbial populations and enzyme activities in soil in situ under transgenic corn expressing cry proteins from Bacillus thuringiensis. J. Environ. Qual. 37:647–62

13. Shen RF, Cai H, Gong WH. 2006. Transgenic Bt cotton has no apparent effect on enzymatic activities or functional diversity of microbial communities in rhizosphere soil. Plant Soil 285:149–59

14. Wang H, Ye Q, Wang W,Wu L,Wu W. 2006. Cry1Ab protein from Bt transgenic rice does not residue in rhizosphere soil. Environ. Pollut. 143:449–55

15. Bhatti MA, Duan J, Head G, Jiang C, McKee MJ, et al. 2005. Field evaluation of the impact of corn rootworm (Coleoptera: Chrysomelidae)-protected Bt corn on Foliage-dwelling arthropods. Environ. Entomol. 34:1336–45

16. Douville M, Gagné F, Blaise C, André C. 2007. Occurrence and persistence of Bacillus thuringiensis (Bt) and transgenic Bt corn cry1Ab gene from an aquatic environment. Ecotoxicol. Environ. Saf. 66:195–203

17. Beachy RN, Fedoroff NV, Goldberg RB, McHughen A. 2008. The burden of proof: A response to Rosi-Marshall et al. Proc. Natl. Acad. Sci. USA 105:E9

18. Parrott W. 2008. Study of Bt impact on caddisflies overstates its conclusions: Response to Rosi-Marshall et al. Proc. Natl. Acad. Sci. USA 105:E10

19. Faria CA, Wäckers FL, Pritchard J, Barrett DA, Turlings TCJ. 2007. High susceptibility of Bt maize to aphids enhances the performance of parasitoids of lepidopteran pests. PLoS ONE 2:e600

 

Updated 2/16/12