Bt Research 2015, Vol.6, No.5, 1-10
6
the toxicity of the Cry proteins (T2) (
Bt
plants or
strains) and or only parasitism (T3). Indicating a
potentiating in mortality of larvae, when used both
control methods (Cry proteins and parasitoid).
A similar result was obtained by Dequech et al. (2005),
who observed that the use of
C. flavicincta
combined
with
B. thuringiensis aizawai
resulted in increased
mortality of
S. frugiperda
. Additionally, (Ahmad et al.,
1978) reported that the mortality of
Lymantria dispar
was greater in the presence of both
Bt. thuringiensis
and the parasitoid
Apanteles melanoscelus
compared
with
A. melanoscelus
alone.
The average percentage of larvae mortality in all
bioassays that were only exposed to parasitism by
C.
flavicincta
was 60%, indicating a high potential for the
control of micro-hymenopteran larvae of
S. frugiperda
. A
similar result was obtained by (Dequech et al., 2005),
who found that larvae of
S. frugiperda
that were only
exposed to parasitism by
C. flavicincta
showed a high
average mortality, of 78.4%.
In the present work, the offspring of the parasitoids
that developed in larvae treated with
Bt thuringiensis
4412 exhibited altered biological characteristics, because
these toxins affect the survival of the host, which
ranged from only 5-6 days, while the parasitoid
C.
flavicincta
requires 8-11 days to complete larval
development. These effects were largely indirect, related
to the sensitivity of lepidopteran larvae to
B. thuringiensis.
Herbivores that have consumed tissues from
Bt
crops,
when used as prey or hosts for a natural enemy,
provide a realistic exposure pathway. However,
Bt
proteins will affect
Bt
susceptible herbivores and
consequently affect their quality as a resource for
natural enemies. Such ‘host/prey-quality mediated effects’
have been observed in numerous tri-trophic feeding
studies with
Bt
crops (Flexner et al., 1986; Vinson,
1990; Sharma et al., 2008; Meissle et al., 2004; Prutz
and Dettner, 2004; Dhillon and Sharma, 2010).
The toxic action of
Bt
in
S. frugiperda
most likely
prevents the host larvae from supplying sufficient
nutrients for healthy development of the parasitoid
larvae. The
Bt
toxin is known to modify amino acids
and ions within the hemolymph composition of herbivores
such as
S. frugiperda
. Thus, the existence of direct
effects cannot be excluded, although they are quite
unlikely because the Cry proteins act by binding to
specific receptors in the insect gut epithelium, and has
shown been to be specific for Lepidoptera (Salama et
al., 1983).
Hence, the level of injury occurring in a parasitoid in
its host also depends on the biology of the parasitoid.
In contrast to
Campoletis sonorensis
, which consumes
the body of its host (Ridgway and Wilson, 1975),
other parasitoids such as
Cotesia marginiventris
feed
only a portion of the inner body. The decreased levels
of some essential amino acids may be one of the
mechanisms through which larvae of
Helicoverpa
armigera
infected with
Bt
toxins impact the parasitoid
Campoletis chlorideae
(Yazlovetzky, 2001).
Dhillon and Sharma (2010) evaluated the developmental
period of the first generation of
Campoletis chlorideae
,
and their results revealed a longer period of pupal
formation and a reduced adult emergence period in
Helicoverpa armigera
treated with
Bt
(Biolep) compared
with untreated individuals (control); however, in the
second generation, there were no significant effects in
any of the examined cases.
Dequech et al. (2005) found no significant difference
when evaluating the biology of the descendants of
Campoletis flavicincta
parasitoids that had emerged
from
Spodoptera frugiperda
that were infected or
non-infected with
Bacillus thuringiensis aizawai
.
It is likely that our results are related to the poor
quality of prey exposed to the protein Cry1B. The
proteins Cry affected survival, development times and
growth rates larvae of
S. frugiperda
and consequently
affected the development of the parasitoid
C. flavicincta.
For
S. frugiperda
, (Mendes et al., 2011) reported a
20-fold reduction in the weight of larvae fed with
Cry1Ab maize compared to those fed with the same
non-
Bt
hybrid. Studies using
Bt
-resistant lepidopteran
larvae, the hosts for parasitic wasps, support such
indirect adverse effects (Schuler et al., 2004; Chen et
al., 2008).
The preservation of natural enemies is critical because
they help control primary and secondary pests not
controlled by the
Bt
crop. Furthermore, recent modeling
work (Onstad et al., 2013) has suggested natural
enemies can also delay the evolution of resistance to
the
Bt
plants by the targeted pest. Additional important
