Effects of the cultivation of genetically modified Bt crops on nontarget soil organisms - Microbial Ecology in Sustainable Agroecosystems - page 185

nematodes are another group of soil organisms that may be impacted by cultivation of
transgenic Bt crops.
Few studies have evaluated the impact of Bt plants on protozoa, and the results to
date are inconsistent ( Table 8.5 ) . Some studies have reported no effect on protozoa in soil
amended with purified Cry1Ab or Cry1Ac protein (Donegan et al., 1995) or with Bt maize
biomass expressing Cry1Ab (Saxena and Stotzky, 2001a), whereas others have reported
both higher (Griffiths et al., 2006; Griffiths, Caul, et al., 2007) and lower (Griffiths et al.,
2005) numbers of protozoa in soil cultivated with Bt maize (expressing Cry1Ab) in the
greenhouse and in the field (reviewed in Birch et al., 2007). There was no significant dif-
ference in protozoa numbers between soil cultivated with Bt maize (Cry1Ab) and non- Bt
maize in a plant growth room (Saxena and Stotzky, 2001a) or in soil cultivated with Bt
(Cry1Ab and Cry3Bb1) and non- Bt maize in the field (Icoz et al., 2008). This variation in
results, even in studies conducted by the same researchers, could be the result of differ-
ences in experimental or environmental factors, such as sampling time or different ecolog-
ical conditions in the greenhouse and the field (e.g., Griffiths, Caul, et al., 2007). Moreover,
because amoebae and flagellates tend to be more sensitive to their environmental condi-
tions (e.g., soil compaction, tillage, anoxic conditions) than ciliates, for example, it is impor-
tant to evaluate each class of protozoa separately as each might have a different response
to changes in agricultural practices resulting from the cultivation of transgenic crops or
differences in Bt root exudates or Bt plant biomass.
Research on the nontarget impact of Bt crops on nematodes indicates that negative
effects on this group of soil organisms may indeed be Bt protein specific ( Table 8.6 ) . Some
Bt proteins (Cry5, Cry6, Cry12, Cry13, Cry14, Cry21) have been shown to have a direct tox-
icity to nematodes (e.g., Meadows et al., 1989a, 1989b, 1990; Marroquin et al., 2000; Kotze et
al., 2005; Hu et al., 2010; Hoess et al., 2011), and some are used as biological control agents
(i.e., Cry5, Cry6) to protect plants from root-feeding nematodes (reviewed in Bravo et al.,
2007; Li, Tan, et al., 2007; Li, Wei, et al., 2007; Li et al., 2008; Khan et al., 2010). Caenorhabditis
elegans, a common model nematode that is found in a variety of natural and agroecosys-
tems, appears to be negatively impacted by some Bt proteins, including Cry1Ab, Cry3Bb1,
Cry5A, and Cry5B. In field studies, a lower abundance of C. elegans was detected in soils
cultivated with Bt maize expressing Cry1Ab than in soils with non- Bt maize (Manachini
and Lozzia, 2003), and there was a negative effect of the Cry1Ab protein from Bt maize
on nematode growth, number of eggs, and reproduction of C. elegans (Lang et al., 2006;
Hoess et al., 2008). When C. elegans was fed purified Cry5A and Cry5B proteins, individu-
als showed substantial gut damage, decreased fertility, and increased mortality, consis-
tent with what would be expected in target insect populations (Marroquin et al., 2000).
Hoess et al. (2011) found a dose-dependent negative response on the growth and repro-
duction of C. elegans to purified Cry3Bb1 using a bioassay, and gene expression analysis
demonstrated that Cry-protein-specific defense genes were upregulated in the presence
of Cry1Ab or Cry3Bb1 protein. However, in field studies with Bt maize that expressed
Cry3Bb1, there was no negative effect on C. elegans (Al-Deeb et al., 2003; Hoess et al., 2011),
probably because of the low level of Cry3Bb1 protein in the rhizosphere (Hoess et al.,
2011). Nematode abundance and diversity were also not different in the rhizospheres of
Bt and non- Bt maize; however, a shift in nematode genus composition occurred in two
of the three Bt maize plots at the end of the field season, but it did not affect functional
diversity (Hoess et al., 2011).
The toxic effects of Cry1Ab observed in C. elegans have not been detected in other
nematode species, but in some cases, nematode communities have been affected by
the cultivation of Bt maize. Greenhouse experiments demonstrated that populations of