Safety of Bt Corn to Nontarget Invertebrates

To turn to corn, one of the first studies followed up on previous studies of Bt corn carried out in Iowa. In the new studies, the effect of Cry1Ab corn on the target pest, the European corn borer (O. nubilalis), and several generalist insect predators and one parasitic wasp (a specialist on this pest) were carried out in Iowa over a two-year period (1997-1998).117 The predators included two beetle species along with the lacewing (C. carnea) and a heteropteran. The hymenopteran parasite was Macro-centrus cingulum, a braconid wasp. Over the two-year period, few differences were found in the general predator populations occurring on Cry1Ab corn versus non-Bt corn. As anticipated, use of Cry1Ab corn resulted in significant reductions in the corn borer populations throughout each season. This in turn resulted in significant decreases in the M. cingulum populations, especially during the latter part of the summer (August).

In a study carried out in Georgia (U.S.) during 2001 and 2002, where the target insect was the corn earworm (H. zea), effects of Cry1Ab corn were monitored on various nontarget populations, including those of predators and parasites.118 Key arthropods monitored included chinch bugs, flea beetles, leafhoppers, crickets, ants, stink bugs, sap beetles, predaceous cocinellids and heteropteran insects, and spiders. In general, with the exception of the target pest, there were no significant differences between the phytophagous insect populations on the Bt versus non-Bt corn. Reductions in populations of sap beetles and one phytophagous fly were noted, but this was attributed primarily to reduction in kernel damage by H. zea, which decreased the attraction of these insects to corn. The only insects other than the target pest found to have consistently lower populations on the Cry1Ab corn were Nabis spp. With the exception of the latter group, the authors concluded that Cry1Ab corn did not have adverse effects on nontarget arthropods in the Georgia corn ecosystem.

In one of the most comprehensive studies in Bt corn, Dively carried out a three-year study in Maryland from 2000 to 2002 to evaluate the effects of Bt corn on a large complex of target and nontarget invertebrates.119 The specific corn tested was a stacked variety that produces both Cry1Ab and VIP3A, a non-Cry insecticidal Bt protein produced during vegetative growth. The primary target pest was the European corn borer (O. nubilalis). The insecticide control was ^-cyhalothrin, a pyre-throid. Nontreated, non-Bt corn was compared with insecticide-treated corn and Bt corn. During the course of the three-year study, hundreds of thousands of specimens were collected and identified, with the total representing 13 orders, 112 families, and 203 taxa of nontarget invertebrates. Among these groups were numerous species of predatory coleopterans, heteropterans, lacewings, ants, spiders, and dipterans, as well as many other herbivores and scavengers. No significant effects were observed with respect to biodiversity and overall population structure between the nontreated, non-Bt corn and Bt corn. Differences were observed between these two crop types in some nontarget populations but, as observed in other studies cited above, these were attributed to the absence of the target pest in the Bt corn and the lack of feeding by corn borer larvae which, when they feed, cause the release of secondary plant compounds that attract, for example, hymenopteran parasitoids. In contrast to the Bt corn and non-insecticide-treated corn, there were significant reductions in many nontarget arthropods in the corn treated with ^-cyhalothrin.

The target insects in all of the studies cited immediately above were lepidopteran pests. In the United States, some of the most intensive use of chemical insecticides is devoted to controlling the corn rootworm (Diabrotica virgifera) (Coleoptera; Chrysomelidae) and related rootworm pest species. However, even with chemical insecticides such as chlopyrophos and imidacloprid, control of these pests can be highly variable due to the lack of good soil penetration during the growing season. Thus, a transgenic corn that can produce an insecticidal protein in corn roots offers the possibility of controlling the pest while at the same time reducing use of synthetic chemical insecticides, and the sterilizing effects these are known to have on many nontarget soil arthropods. Toward this end, Bt corn lines producing Cry3Bb, which is toxic to many species of coleopterans but has little or no toxicity to other arthropods, have been developed and released beginning several years ago.

Among the studies published in the October, 2005 issue of Environmental Entomology are three papers that examined the effects of the Cry3Bb corn over a three-year period, from 2000 to 2003, on nontarget invertebrate populations.120-122 The first two of these examined the effects on, respectively, soil-dwelling and foliage-dwelling arthropods on corn grown in Illinois, whereas the last examined the effects on populations of springtails (Collembola) in Illinois and Iowa. Insecticides used as controls on non-Bt corn were imidacloprid and the pyrethroid, tefluthrin. As in the studies of Bt corn targeted to control lepidopteran pests, a wide range of nontarget arthropods were evaluated in the first two studies, including spiders, ground beetles, rove beetles, syrphid flies, lacewings, hymenopteran parasitoids, heteropteran predators, centipedes, earthworms, and detritovores. Minor effects were observed in 2 of the 14 major taxa studied on Bt corn compared to conventional corn, whereas in the insecticide-treated plots significant reductions in 6 of the 14 major taxa were observed. In the studies of springtails, in which the insecticide controls were the same, no significant differences were observed between the conventional corn and Bt corn. However, in the insecticide-treated plots, the springtail populations increased significantly as a result of the reductions in arthropod predator populations that prey on these insects.

A particularly interesting and important finding to emerge from these long-term studies is that no effects were observed on the lacewing populations in any of the Bt crops studied in any geographical region. It will be recalled that laboratory studies of the lacewing (C. carnea), a generalist predator, are routinely cited as an example of the potential negative impact that Bt crops could have on beneficial insect populations.108,109 Although the results of these two studies by Hilbeck et al. and a subsequent study123 were later shown to be due to nutritional effects and poor prey quality, and thus erroneous,110 well-designed field studies are clearly much better for determining whether Bt crops present risks for nontarget arthropods. In the case of C. carnea, the lack of any impact determined in the numerous long-term field studies noted above is that this predator was able to exercise prey choice and likely fed mostly on aphids and other small insects not affected by Bt cotton or corn.

Studies of the Monarch butterfly provide another example of the value of field studies done in the ecological context in which Bt crops are planted commercially. The initial laboratory studies by Losey et al. suggested a significant potential risk,104 which clearly caused alarm in many quarters and was used (and continues to be used) by opponents to genetically engineered crops to halt their use. Subsequent, much more careful studies conducted in both the laboratory and field again demonstrated that the initial claims were not valid and that the effect on Monarch populations, if any, would be negligible.105,106 In essence, laboratory studies may identify hazards but potential real risks can only be assessed under actual field conditions, and preferably through long-term studies.

The two major safety concerns about Bt crops are their safety to nontarget invertebrates, especially arthropods occurring in agro-ecosystems, and vertebrates, mainly humans. Thus, the importance of these long-term field studies cannot be overestimated. These studies, along with prior short-term studies and ongoing long-term studies, show no significant impact of Bt crops on nontarget arthropods populations. Though clearly some populations are affected on a short-term basis, primarily as a result of the removal of their insect hosts which are pest-targeted by these crops, the overall arthropod community suffers much greater reductions when chemical insecticides are used. These results show clearly that Bt crops provide an agro-ecosystem that enhances natural methods of control, such as conservation of natural enemies and biological control. By 2001, for example, it was estimated that the use of Bt cotton in the United States resulted in 15 million fewer insecticide applications, which reduced the amount of insecticides applied by 2.7 million pounds.124 It could be argued that it is premature to conclude that this new technology is safe for the very long term. However, the data resulting from the studies cited above provide substantial evidence that Bt crops are one of the safest and environmentally compatible technologies developed over the past century.

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