Responses of stream macroinvertebrates to Bt maize leaf detritus

Abstract

In the midwestern United States, maize detritus enters streams draining agricultural land. Genetically modified Bt maize is commonly planted along streams and can possibly affect benthic macroinvertebrates, specifically members of the order Trichoptera, which are closely related to target species of some Bt toxins and are important detritivores in streams. The significance of inputs of Bt maize to aquatic systems has only recently been recognized, and assessments of potential nontarget impacts on aquatic organisms are lacking. We conducted laboratory feeding trials and found that the leaf-shredding trichopteran, Lepidostoma liba, grew significantly slower when fed Bt maize compared to non-Bt maize, while other invertebrate taxa that we examined showed no negative effects. We also used field studies to assess the influence of Bt maize detritus on benthic macroinvertebrate abundance, diversity, biomass, and functional structure in situ in 12 streams adjacent to Bt maize or non-Bt maize fields. We found no significant differences in total abundance or biomass between Bt and non-Bt streams, and trichopterans comprised only a small percentage of invertebrate biomass at all sites (0-15%). Shannon diversity did not differ among Bt and non-Bt streams and was always low (H' range = 0.9-1.9). Highly tolerant taxa, such as oligochaetes and chironomids, were dominant in both Bt and non-Bt streams, and macroinvertebrate community composition was relatively constant across seasons. We used litterbags to examine macroinvertebrate colonization of Bt and non-Bt maize detritus and found no significant differences among litter or stream types. Our in situ findings did not support our laboratory results; this is likely because the streams we studied in this region are highly degraded and subject to multiple, persistent anthropogenic stressors (e.g., channelization, altered flow, nutrient and pesticide inputs). Invertebrate communities in these streams are a product of these degraded conditions, and thus the impact of a single stressor, such as Bt toxins, may not be readily discernable. Our results add to growing evidence that Bt toxins can have sublethal effects on nontarget aquatic taxa, but this evidence should be considered in the context of other anthropogenic impacts and alternative methods of pest control influencing streams draining agricultural regions.

Occurrence of maize detritus and a transgenic insecticidal protein (Cry1Ab) within the stream network of an agricultural landscape

“…Therefore, the material that we found during our synoptic survey had entered these streams relatively recently. Maize detritus is rapidly colonized by stream-dwelling invertebrates, and growth rates of invertebrates feeding on nontransgenic decomposing maize are comparable to those feeding on the deciduous leaf litter commonly found in forested streams (8).…”

“…Once maize detritus enters stream channels, this carbon source degrades rapidly via a combination of microbial decomposition, physical breakdown, and invertebrate consumption (6,8,20), and that energy may fuel stream food webs. Maize detritus in agricultural streams decomposes in ∼66 d (k = −0.015 d −1 ) (6).…”

“…Cry1Ab protein is expressed throughout the tissues of Bt maize (2,3), and after maize is harvested, the protein is detectable in terrestrial detritus left on agricultural fields for at least 7 mo (4,5). Recent work established that maize detritus enters, is processed, and can be transported within streams (6,7), and laboratory trials suggested that consumption of Bt maize detritus may affect stream-dwelling invertebrates (7,8) but some studies have shown little or no effect if detritus is leached prior to consumption (9). However, the fate of Cry1Ab protein in senescent and decaying maize detritus in aquatic environments is largely unknown.…”

“…For example, using stable isotope analysis, Dalzell et al (18) found that the contribution of C4 carbon (attributed to maize) to the transported particulate organic carbon pool in west-central Indiana streams was 17% at base flow and increased to 22% during flood conditions. Although these simplified channels contain few natural retention structures, maize detritus is retained within the channels when discharge is low (7), and this material is rapidly decomposed by microorganisms (6) and may be consumed by aquatic invertebrates (6,8,20). Given the widespread planting of Bt maize, some portion of the maize detritus within stream channels may contain the Cry1Ab protein, and fluvial networks could distribute this material away from fields and across the larger landscape.…”

Chronic Responses ofDaphnia magnaUnder Dietary Exposure to Leaves of a Transgenic (Event MON810) Bt–Maize Hybrid and its Conventional Near-Isoline

“…In contrast, negative nontarget effects of Bt-maize were found in certain cases, particularly for aquatic organisms, such as Trichoptera larvae fed Bt-maize leaves (Rosi-Marshall et al, 2007;Chambers et al, 2010), and Daphnia magna fed ground Bt-maize kernels (Bøhn et al, 2008(Bøhn et al, , 2010. Significant effects of MON810 maize were recently noted in salmon (Salmo salar) (Gu et al 2013(Gu et al , 2014, but were considered to be of minor biological significance because the overall development and health of the animals was not affected.…”