Effects of the cultivation of genetically modified Bt crops on nontarget soil organisms - Microbial Ecology in Sustainable Agroecosystems - page 193

and there were no deleterious effects on survival and reproduction of E. fetida fed leaves of
Bt maize expressing Cry1Ab (Clark and Coats, 2006). Similarly, Saxena and Stotzky (2001a)
found no significant difference in mortality and weight of Lumbricus terrestris grown for 40
days in soil cultivated with Bt maize (Cry1Ab) or non- Bt maize and no effect on mortality
and weight of L. terrestris grown in soil amended with ground, dried Bt maize biomass
for 45 days. No lethal effects of Bt maize (Cry1Ab) residues on adult or immature earth-
worms were found in field studies (Zwahlen, Hilbeck, Howald, et al., 2003; Lang et al., 2006;
Zwahlen et al., 2007). However, adult L. terrestris had a significant loss in weight in a labora-
tory experiment when worms were grown in soil amended with Bt (Cry1Ab) versus non- Bt
maize biomass for 200 days (Zwahlen, Hilbeck, Howald, et al., 2003).
Laboratory studies with Aporrectodea caliginosa reported no negative effect on survival,
growth, development, or reproduction of individuals grown in soil amended with leaves
of Bt maize (Cry1Ab) or grown in pots cultivated with Bt maize (Vercesi et al., 2006), and
there was no effect on survival and reproduction of Enchytraeus albidus that were fed diets
with Bt maize (Cry3Bb1) versus non- Bt maize leaf biomass (Honemann and Nentwig, 2009).
However, E. albidus fed Bt leaves (Cry1Ab) had a lower reproduction rate but a higher sur-
vival rate when compared with worms fed leaves of the non- Bt maize isoline (Honemann
and Nentwig, 2009). When litterbags containing biomass of nine different Bt maize (Cry1Ab
and Cry3Bb1) and non- Bt maize cultivars were buried in the field, there was no difference
in the numbers of Enchytraeidae or Lumbricidae found in litterbags after 9 months or a
difference in the degradation rate between the different maize varieties (Honemann et al.,
2008). Interestingly, when maize residues were added to soil microcosms, consumption of
Bt plant material by L. terrestris and A. caliginosa lowered the concentration of immunore-
active Cry1Ab protein in soil to less than 10% of the original concentration after 5 weeks
without causing any detectable harm on the earthworms (Schrader et al., 2008). E. fetida fed
Bt cotton leaves expressing Cry1Ac in the laboratory also displayed no toxic effects and
even resulted in slight increases in growth and reproduction compared with earthworms
fed non- Bt cotton leaves, although this difference was not statistically significant (Liu, Cui,
et al., 2009; Liu, Wang, et al., 2009).
In other studies, there have been no negative effects reported of the cultivation of Bt
maize expressing Cry3Bb1 on the abundance of Oligochaeta in the field (Bhatti et al., 2005)
or soil planted with or amended with Bt maize (Cry3Bb1) on weight and mortality of L. ter-
restris in the greenhouse (Ahmad et al., 2006). There was also no difference in the biomass
of juveniles or adults of A. caliginosa, Aporrectodea trapezoides, Aporrectodea tuberculata, and
L. terrestris in soil cultivated with Bt maize expressing Cry1Ab and Cry3Bb1 compared to
soil cultivated with non- Bt maize over a 4-year field study (Zeilinger et al., 2010). When
effects of the cultivation of Bt maize (Cry1Ab) and HT maize were tested on natural popu-
lations of earthworms (including A. caliginosa, Aporrectodea longa, Aporrectodea rosea, L. ter-
restris, Allolobophora chlorotica, Prosellodrilus amplisetosus, and Allolobophora cupulifera ) over
two consecutive growing seasons at two different field sites, earthworm populations were
reduced only in the plots with the HT crop, likely due to reduced tillage (RT) practices
associated with HT crops (Krogh et al., 2007). Plots with the HT maize allowed the practice
of RT; plants can be sprayed with herbicides for weed control rather than using tillage mea-
sures. In the HT, RT plots, earthworm populations were significantly reduced to about half
of earthworm populations in the HT plots that received the conventional tillage treatment.
The authors speculated that the reduction in earthworm populations in the HT plots was
likely because of exposure to the herbicide Basta ® , as the HT maize plants were the same
across treatments (Krogh et al., 2007).