Effects of exposure to event 176 Bacillus thuringiensis corn pollen on monarch and black swallowtail caterpillars under field conditions

Abstract

The widespread planting of corn genetically modified to produce Bacillus thuringiensis endotoxin has led to speculation that pollen from these fields might adversely affect nearby nontarget lepidopterans. A previous study of Bt corn engineered with Monsanto event 810 failed to detect an effect of pollen exposure on the black swallowtail, Papilio polyxenes, in either the field or the laboratory. Here, we report results of a field study investigating the impact of exposure to pollen from a Bt corn hybrid containing Novartis event 176 on two species of Lepidoptera, black swallowtails and monarch butterflies, Danaus plexippus. Nearly half of the 600 monarch larvae died within the first 24 h; this and subsequent mortality was not associated with proximity to Bt corn and may have been due in part to predation. Survivorship of black swallowtails was much higher than that of the monarchs and was also independent of proximity to the transgenic corn. However, despite five rainfall events that removed much of the pollen from the leaves of their host plants during the experiment, we observed a significant reduction in growth rates of black swallowtail larvae that was likely caused by pollen exposure. These results suggest that Bt corn incorporating event 176 can have adverse sublethal effects on black swallowtails in the field and underscore the importance of event selection in reducing environmental impacts of transgenic plants.

Figure 1

Pollen densities on foliage of milkweeds (A. syriaca) and wild parsnips (P. sativa) as a function of time and distance from a stand of event 176 Bt corn. In each case, larvae were placed on the plants on the earliest date indicated. Rainfalls of 0.20, 0.43, 0.10, and 0.10 cm occurred on July 28, 29, 30, and 31, respectively. An additional rainfall of 1.56 cm occurred on August 2 after the last pollen sampling and the day before the final larval census.

Figure 2

Survivorship of monarch (D. plexippus) and black swallowtail (P. polyxenes) larvae as a function of distance from a field of event 176 Bt corn.

Figure 3

Larval masses of the black swallowtail (P. polyxenes) at different distances from a field of event 176 Bt corn. The white lines within the boxes are the means. The boundaries of the boxes represent the 25th and 75th percentiles, and the boundaries of the whiskers represent the 10th and 90th percentiles. ●, outliers (one outlier value of 51.8 in the 7 m position is not shown). Larval masses differed significantly among distance treatments (Kruskal–Wallace χ² = 60.5, P < 0.001). The regression of mean larval mass against distance was also significant (P = 0.012, y = 1.36x + 5.23). Sample sizes for distances from 0.5 to 7 m were 39, 26, 25, 36, and 46, respectively.

Figure 4

Daily and cumulative totals of arthropods found and removed from milkweeds and wild parsnips during the experiment. Dates with asterisks indicate significantly higher numbers of predaceous arthropods on milkweeds (χ² values = 11.26 and 8 for July 28 and 29, respectively; both values have probabilities less than 0.05).

Figure 5

Frequency of taxonomic groups found and removed from both milkweeds and wild parsnips during the experiment. Asterisks denote groups known to be generalist consumers of lepidopteran larvae.

Figure 6

Survivorship of first instar black swallowtails administered different doses of event 176 pollen in the laboratory. The only survivorship curve that does not differ from control is the 10 grains/cm² (log rank test P = 0.263). Pollen was suspended in acetone and applied to leaf material. The control consisted of addition of acetone only. For details of the bioassay method, see Wraight et al. (7).