No. 1 Article 4/March 24, 2006

Bt Corn and Neonicotinoid Seed Treatments: Are Nontarget Effects and Potential Insecticide Resistance Justified Concerns?

The use of transgenic corn hybrids (Bt corn) continues to increase in popularity for a variety of lepidopteran pests (European corn borer, black cutworm, western bean cutworm), as well as tor the corn rootworm complex (western and northern corn rootworms). The increased use of Bt corn has been accompanied by an escalation in the use of neonicotinoids, which are used to treat transgenic corn seed, as well as seed of many nontransgenic corn hybrids. The two neonicotinoids most commonly used in corn production are clothianidin (Poncho) and thiamethoxam (Cruiser). Corn seed may be treated at 1.125 mg of active ingredient (AI) per kernel with thiamethoxam and 1.25 mg of AI per kernel with clothianidin for corn rootworm control. Lower rates of each product (thiamethoxam--0.125 mg of AI per kernel; clothianidin--0.25 mg of AI per kernel) are labeled for use as seed treatments against secondary soil insects. Does the prophylactic use of these neonicotinoid seed treatments fit within the conventional IPM paradigm? How concerned should we be regarding the potential for resistance development to these systemic insecticides in the corn and soybean agroecosystem? Why are producers mandated to deploy a refuge strategy for Bt hybrids but not for neonicotinoids? What impact, if any, do the neonicotinoids and Bt hybrids have on nontarget populations of insects? These and many other questions will continue to be asked in the coming years as the use of transgenic hybrids becomes routine.

Ground beetle larva.

Ground beetle adult.

Ground beetle adult.

The National Agricultural Statistics Service (NASS, USDA) estimated (June 30, 2005) that 81.6 million acres of corn were planted in the United States in 2005, an increase of 1% from 2004 and 4% from 2003. The use of Bt hybrids on 28.6 million acres accounted for 35% of the 2005 U.S. corn acreage. NASS estimated that 12.1 million acres of corn were planted in Illinois in 2005, of which 30% (3.63 million acres) were Bt hybrids. Five percent of the Bt hybrids planted in Illinois were the "stacked" gene hybrids that include biotech traits for herbicide and insect resistance. The use of Bt hybrids in western Corn Belt states was greater than in the eastern Corn Belt states in 2005: Indiana (15%), Iowa (46%), Kansas (33%), Michigan (20%), Minnesota (44%), Missouri (43%), Nebraska (51%), Ohio (11%), South Dakota (52%), and Wisconsin (28%). Greater use of Bt hybrids in western states can be explained by more continuous (nonrotated) corn, more livestock production, and fewer concerns about the overseas export market (particularly Europe) regarding transgenic grain. The use of all transgenic corn (Bt and herbicide-resistant) hybrids in 2005 exceeded 50% of planted acres in many Corn Belt states: Illinois (36%), Indiana (26%), Iowa (60%), Kansas (63%), Michigan (40%), Minnesota (66%), Missouri (55%), Nebraska (69%), Ohio (18%), South Dakota (83%), and Wisconsin (46%). In 2005, an estimated 52% of the corn acres in the United States were planted to transgenic hybrids. Within a 10-year span, the manner in which producers manage two very important insect pests of corn (European corn borer and corn rootworms) has fundamentally changed. This transformation has caused scientists engaged in integrated pest management (IPM) research and extensions within land grant institutions to reexamine their definitions of IPM and to question some previously held convictions about IPM, which had its formal roots in the late 1950s.

Some research on the potential effects of Bt corn hybrids on nontarget insects has been published. Of particular interest is the potential effect of the Cry3Bb1 protein against beneficial soil insects such as ground beetles (carabids) and other nontarget soil organisms. The Cry3Bb1 protein is expressed in YieldGard Rootworm hybrids for control of corn rootworms. Research conducted by Kansas State University entomologists and published in 2003 and 2005 led scientists to offer these concluding remarks:

"In general, the results of this study demonstrated that Bt corn expressing the Cry3Bb1 protein for corn rootworm control does not have deleterious effects on the nontarget microarthropods and nematodes sampled. Further studies on soil after repeated growing of Bt corn in the same field for several years are needed." (Al-Deeb, M.A., G.E. Wilde, J.M. Blair, and T.C. Todd. 2003. Effect of Bt corn for corn rootworm control on nontarget soil microarthropods and nematodes. Environmental Entomology 32: 859-865.)

"In conclusion, our studies indicated that transgenic Bt corn expressing Cry3Bb1 was not detrimental to surface or below-ground arthropod communities. None of the Cry3Bb1 protein or only a trace amount was detected from soil near the base of the plants. Furthermore, there was no indication of protein accumulation over a 3-year period." (Ahmad, A., G. Wilde, and K.Y. Zhu. 2005. Detectability of coleopteran-specific Cry3Bb1 protein in soil and its effect on nontarget surface and below-ground arthropods. Environmental Entomology 34: 385-394.)

In 2006, a few researchers with Monsanto Company, in cooperation with scientists formerly with the Illinois Natural History Survey, published a paper that specifically focused on a dietary exposure bioassay with Cry3Bb1 targeted at larvae of one species of ground beetle, Poecilus chalcites (Say). They offered the following comments in their discussion:

"Results from this study show that the Cry3Bb1 protein at 10 times the maximum concentration expressed in MON 863 corn tissues (930 µg/g of diet) had no apparent adverse effects on the survival, growth, and development of larvae of P. chalcites, and thus is expected to pose no risk to this nontarget beneficial insect." (Duan, J.J., M.S. Paradise, J.G. Lundgren, J.T. Bookout, C. Jiang, and R.N. Wiedenmann. 2006. Assessing nontarget impacts of Bt corn resistant to corn rootworms: tier-1 testing with larvae of Poecilus chalcites (Coleoptera: Carabidae). Environmental Entomology 35: 135-142.)

Are we ready to conclude that Bt corn rootworm hybrids have minimal impact, if any, on nontarget populations of soil arthropods? Not yet. A recently published paper has shed some light on the potential negative impact of neonicotinoid systemic insecticides that are used as seed treatments on transgenic corn hybrids:

"A series of laboratory-feeding and defined-dose bioassays effectively delivered or exposed representative carabid species collected from these field plots to Cry toxins and seed treatments. We found that the neonicotinoid/fungicide seed treatments, and not Cry3Bb1, were a major mortality factor for the 16 ground beetle species tested." (Mullin, C.A., M.C. Saunders II, T.W. Leslie, D.J. Biddinger, and S.J. Fleischer. 2005. Toxic and behavioral effects to Carabidae of seed treatments used on Cry3Bb1- and Cry1Ab/c-protected corn. Environmental Entomology 34: 1626-1636.)

The researchers further commented on the importance of conducting future field studies: "Field studies are needed to determine population and community level effects on Carabidae when these transgenic and seed-treatment technologies are combined." The potential threat of neonicotinoids to nontarget insects can be expanded to include soybean seed treated with neonicotinoids (thiamethoxam and imidacloprid [Gaucho]).

With respect to potential development of insecticide resistance to neonicotinoids, how concerned should we be? Western corn rootworms have developed resistance to chlorinated hydrocarbons, organophosphates, and carbamates, and even crop rotation has lost its usefulness as a pest management tactic against western corn rootworms throughout much of Illinois. The western corn rootworm is quite capable of adapting when "squeezed" too hard. Resistance to neonicotinoids has occurred with other beetles in the same family (Chrysomelidae) as corn rootworms. Resistance to imidacloprid was documented for the Colorado potato beetle in the following paper:

"Colorado potato beetle, Leptinotarsa decemlineata (Say), adults and larvae collected from Long Island, NY, were 100.8 and 13.2 times more resistant to imidacloprid, respectively, compared with a susceptible strain. This high level of resistance appeared in only the third field season of imidacloprid use." (Zhao, J.-Z., B.A. Bishop, and E.J. Grafius. 2000. Inheritance and synergism of resistance to imidacloprid in the Colorado potato beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology 93: 1508-1514.)

The authors of this 2000 paper offered additional comments regarding the potential management of imidacloprid resistance:

"Our results indicate that autosomal, incompletely recessive factors are involved in imidacloprid resistance. Thus, resistance management practices such as refugia and high doses, which rely on recessive resistance traits, may be more successful for managing resistance to imidacloprid than was the case for other insecticides."

Based on the findings presented in this paper, the use of a refuge as part of an overall resistance management plan for neonicotinoid use within the corn and soybean production system warrants discussion. In addition, because we are using the lower rates of neonicotinoids on Bt corn, are we additionally increasing the potential threat of development of resistance? We look forward to our readers' responses to these questions.--Mike Gray and Kevin Steffey

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