Bt or not Bt: is that the question?

R public concerns over the transgenic (genetically modified) plants and nontarget impacts such as those from Bttoxin expressing corn pollen on the monarch butterfly populations have escalated, despite good pest management intentions and good science (1–9). Plant resistance to insect pests has evolved naturally over many millions of years and involves (i) both constitutive and inducible phytochemical and morphological mechanisms in plants, (ii) counteradaptations to plant defenses by the herbivores, and (iii) biotic interactions of the multitrophic level communities of insect pathogens, parasites, and predators (10– 13). The outcomes of such complex biotic interactions are sometimes determined by local mosaics of abiotic environmental conditions or regional climate changes that directly influence the component participants and their behavioral, physiological, and genetic adaptations (14–16). The intentional selection and breeding of insect andyor pathogen-resistant plant genotypes such as corn (Zea mays) has resulted in slow, but steady, progress against stalk-boring larvae such as the European corn borer and other such species, and host plant resistance in general has significantly reduced the need for broad-spectrum insecticides across agroecosystems and forests (17, 18). The use of fairly specific natural microbial insecticides such as the Cry1Ab or Cry 1Ac endotoxins from Bacillus thuringiensis var. kurstaki (Btk) have been hailed as a new jump-shift in targeted pest control methods, with putatively minimal impacts on nontarget organisms in millions of acres of forests for gypsy moth control and cornfields for stalk-boring Lepidoptera control (19, 20). The specificity of Btk (for Lepidoptera) and Bti (for Diptera) has not always been accepted in the public mind. For example, in the 1980s mosquito control sprays with Bti were suspected to be killing nontarget Lepidoptera (including the endangered Schaus swallowtail butterfly) in Munroe County of the Florida Keys (P. Eliazar, personal communication) potentially caused by bacterial spore or other microbial contamination of the formulation. Contamination of Btk during production with other microbes and different types of Bt toxins that could poison other animals and humans has reportedly been reduced since 1989 (21). It has recently been possible to genetically engineer plants, such as Z. mays, to avoid problems with insecticidal spray drift and more efficiently express toxins in particular plant tissues against lepidopterous pests. Such efficient, effective, and relatively safe tools for pest management have eluded classical plant breeders and integrated pest management practitioners for many decades (20). However, even though safe for most other taxonomic groups of insects other than Lepidoptera, the nontarget impacts of Btk require careful and thorough evaluation combined with extensive publicizing. If not done, the real risks, which may be minimal, can be significantly amplified in the public minds by perceived risks and distrust of biotech corporations and the regulatory federal agencies and similar goal-affiliated agricultural research institutions and universities (22, 23). Additional risks for crop pest management such as the rapid development of insect resistance to the Bt insecticides also need serious attention and consideration in long-term agroecosystem design as well (24, 25). The use of aerial applications of Btk toxins (and live spores) across millions of acres of forests and urban areas against the gypsy moth, Lymantria dispar, resulted in heated debates across the United States as the moth defoliation damage steadily spread. This largely emotional public reaction to gypsy moth damage and the pesticides sprayed for control illustrates the importance of careful studies of nontarget impacts and open disclosure of these potential impacts to the public (21). Despite the assurances about short duration field toxicity of Btk, it turned out that the purported window of ‘‘vulnerability’’ for hundreds of nontarget Lepidoptera species was not simply 2–4 days postspray as reported for the gypsy moth larvae, but instead could extend for 4–6 weeks or more, even under natural field conditions with several heavy rains, direct sunlight (and UV radiation), and opportunities for microbial degradation (26, 27). The mechanisms permitting this extended toxicity of aerially applied Btk sprays to nontarget lepidopteran species so exposed under natural conditions are still not clearly identified, but may include naturally lower toxic dosages than for gypsy moths (28, 29), differential interactions with natural phytochemicals (such as tannins and phenolics) in different plant species (30), vegetative growth of the live spores and subsequent protein crystallization and concentration on the nutrientrich leaf phylloplanes (21, 31), andyor other leaf phylloplane microbial synergisms of Btk toxicity inside the insect gut (32, 33). With these concerns publicized, and the potential of ecosystem-wide effects (21, 26, 27) there was eventually a need recognized (federally) to officially investigate nontarget effects of Btk sprays for gypsy moths, which resulted in large funding through the Forest Service to a single state. A similar political need to assess the extent of nontarget risks of Bt corn pollen surfaced shortly after the 1999 Nature publication on monarch butterflies (1, 7). It seems clear, for various reasons described in the six articles that recently appeared in PNAS (1–6), that the risks to nontarget lepidopterans of Bt toxins in corn pollen are significantly less than those involved with aerial application of Bt sprays for gypsy moths. It may be that much of the concern about Btk corn pollen deals more with perceived risks than with realized and potential risks (34). However, even with studies by federal research and enforcement agencies (19, 21), the public and some of the scientific community remain understandably cautious about accepting the stated ‘‘safety’’ assurances associated with new technologies (22, 23). The potential dangers of movement of transgenic pollen from the corn plant into the agroecosystem and adjacent hedge-rows and forest edges has been demonstrated to be of minor and rather localized concern (4, 6). However, escape of crop transgenes into wild relatives via hybridization (22) or virusinfected transgenic plants producing more virulent (pathogenic) genotypes with recombined mRNA of the transgene should not be lightly dismissed (35). These articles addressing Bt-corn pollen impacts on the migratory ‘‘conservation flagship species’’ of monarch butterfly (1–5) and one swallowtail butterfly (6) strongly suggest that the