Effects of the cultivation of genetically modified Bt crops on nontarget soil organisms - Microbial Ecology in Sustainable Agroecosystems - page 202

Wolfenbarger et al., 2008; Lovei et al., 2009; Lundgren et al., 2009; Lang and Otto, 2010;
Gatehouse et al., 2011).
Many of the studies evaluating the effects of the cultivation of Bt crops on nontarget
insects have been conducted on Lepidoptera, primarily the larvae of monarch ( Danaus
plexippus ) and swallowtail ( Papilio sp.) butterflies. Larvae of the monarch butterfly, for
example, do not feed on Bt crop plants, but their primary food source (milkweed) often
grows in or near agricultural fields where Bt pollen deposition on milkweed leaves could
occur (Lang et al., 2004). Losey et al. (1999) reported that monarch caterpillars fed pollen
from Bt maize (N4640, Cry1Ab) in laboratory studies ate less, grew more slowly, and had
higher mortality than larvae fed non- Bt maize pollen and cautioned that Bt crop cultivation
may have serious unintended consequences to nontarget Lepidoptera in the environment.
However, critics pointed out that the authors neglected to record the amount of Bt corn pol-
len deposited on the milkweed leaves fed to the monarch caterpillars and argued that the
results reported in laboratory studies were unlikely to be observed under field conditions
(reviewed and discussed in Shelton and Sears, 2001). Since then, additional studies have
evaluated the effects of Bt pollen on nontarget Lepidoptera under both laboratory and field
conditions (e.g., Jesse and Obrycki, 2000; Wraight et al., 2000; Hellmich et al., 2001; Sears
et al., 2001; Stanley-Horn et al., 2001; Tschenn et al., 2001; Zangerl et al., 2001; reviewed in
Gatehouse et al., 2002; Anderson et al., 2004, 2005; Candolfi et al., 2004; Dively et al., 2004;
Gathmann et al., 2006; Lang and Vojtech, 2006; Prasifka et al., 2007) and reviewed by others
(Sears et al., 2001; Shelton and Sears, 2001; Sears, 2004; Lang and Otto, 2010).
Wind-pollinated crops, such as Bt maize, have a greater potential for nontarget effects
of pollen deposition on Lepidopteran larvae (and other insects) than non-wind-pollinated
GM crops such as Bt potato, Bt cotton, or Bt canola and thus have been the focus of many
risk assessment studies. In an analysis of 20 peer-reviewed publications (16 laboratory
feeding studies with purified Bt toxin, Bt maize pollen, or Bt maize anthers in an artifi-
cial diet or on leaf disks, whole leaves, or whole plants and 7 field-based studies using
unfenced host plants, field cages, or natural conditions), Lang and Otto (2010) found
adverse effects of Bt maize or Bt protein on nontarget Lepidopteran larvae ( Danaus plex-
ippus, Papilio polyxenes, Papilio machaon, Pieris rapae, Pieris brassicae, Pseudozizeeria maha,
Inachis io, Euchaetes pernyi, Plutella xylostella, or Galleria mellonella ) in 52% of laboratory-
based and in 21% of field-based studies. The majority of these studies were based in the
United States and focused on nontarget effects of Bt maize pollen (primarily from Events
MON810, Bt 176, Bt 11) on monarch butterfly larvae. The effects most often studied in
these experiments were on larval body mass, survival, and developmental time, whereas
effects on adult Lepidoptera were rarely examined (Lang and Otto, 2010). The results of
each study appeared to depend primarily on the methodology used, the Bt cultivar, and
the amount of Cry protein expressed in the pollen of each Bt cultivar. Although several
field-based studies found no effect of Bt crop cultivation on nontarget Lepidoptera (black
swallowtail and monarch) (e.g., Wraight et al., 2000; reviewed in Sears et al., 2001; Tschenn
et al., 2001; Anderson et al., 2004), the results of Losey et al. (1999) were supported by
those of other studies that demonstrated significant adverse effects on swallowtail or
monarch caterpillars in the presence of Bt pollen in the field (e.g., Jesse and Obrycki,
2000; Stanley-Horn et al., 2001; Zangerl et al., 2001; Dively et al., 2004) and in laboratory
feeding studies (e.g., Hellmich et al., 2001; Anderson et al., 2004, 2005; Lang and Vojtech,
2006; Prasifka et al., 2007). Most studies have shown that pollen from Bt maize Event
176 had the most lethal and sublethal effects (e.g., mortality, growth rate, body weight,
development time) on larvae of swallowtail and monarch butterflies, whereas Bt maize
Events Bt 11 and MON810 had negligible effects on the larvae. Bt maize Event 176 was