XXII CNIE - Accademia nazionale italiana di Entomologia

of CCD (Cox-Foster et al. 2007) has suggested that, at least in North America, N.
ceranae is not the definitive causative agent of CCD.
Pesticides?
Agricultural pesticides in CCD have also been suspected of playing a role in CCD. In
particular, the absence of dead bees near CCD colonies was thought by many to
implicate toxins that cause sublethal alterations in behavior that interfere with orientation
and navigation in foraging bees. Such behavioral effects have been documented to result
from exposure to neonicotinoid pesticides in laboratory studies (Decourtye et al. 2004)
and concerns over sublethal behavioral effects led to a ban on the use of imidacloprid
and other neonicotinoids in France beginning in 2004. However, neonicotinoids in the
U.S. have been in widespread use for over a decade and no recent changes in usage
patterns are consistent with the sudden appearance of CCD. Moreover, the fact that
certain states associated with widespread usage of neonicotinoids, such as Illinois, where
neonicotinoids are routinely used as seed treatments for soybeans and corn, did not
experience CCD argues against neonicotinoids as a primary cause of CCD.
Use of combinations of in-hive pesticides for control of honey bee parasites has also
been suspected of contributing to bee mortality that may be associated with CCD
(Johnson et al., 2009). Although the varroa mite (Varroa destructor), a devastating
parasite of honey bees (Apis mellifera ), was initially well controlled with the pyrethroid
tau-fluvalinate (Apistan®) (Atkins 1992), widespread resistance in mite populations
worldwide compromised its efficacy (Lodesani et al. 1995, Elzen et al. 1998). In 1998,
the organophosphate pesticide coumaphos (Checkmite+®), with a mode of action
different from that of fluvalinate, was approved in the US as a miticide for resistant
populations and as a treatment for a new pest, the recently introduced small hive beetle
(Aethina tumida; Federal Register 2000) (Elzen et al. 2000). However, resistance to
coumaphos developed in mite populations soon after its introduction (Elzen and
Westervelt 2002).
Both coumaphos and tau-fluvalinate are lipophilic compounds that are absorbed by the
wax component of the hive, where they are stable and have the potential to build up over
repeated treatments. In a recent survey of in-hive chemical residues conducted in the
wake of colony collapse disorder, both compounds were found in 100% of wax samples
from both healthy and collapsed colonies (Frazier et al. 2008). Johnson et al. (2009)
demonstrated in a laboratory study that these two pesticides synergize each other; the
toxicity of each is enhanced in the presence of the other. The widespread presence of
residues of both in-hive miticides in foundation raises the possibility that the
detoxification capacity of U.S.honey bees may be compromised on a wide scale. Honey
bee mortality may occur with the application of otherwise sublethal doses of miticide
when tau-fluvalinate and coumaphos are simultaneously present in the hive. Beekeepers
often move potentially miticide-contaminated frames within and between hives.
Additionally, both coumaphos and tau-fluvalinate survive and are concentrated by the
wax recycling process used to make new foundation such that these compounds can be
detected in colonies that have never been treated with either miticide (Bogdanov et al.
1998, Martel et al. 2007).
To manage varroa resistance to both tau-fluvalinate and coumaphos, beekeepers have
been encouraged to adopt a rotation program alternating between Apistan® and
Checkmite+® (Elzen et al. 2001). In light of the potential for synergistic interactions
between tau-fluvalinate and coumaphos, other miticides with no known potential for
P450 interactions, such as the organic acids (Underwood and Currie 2004), should be
considered for management of varroa. The flagging effectiveness of the miticides taufluvalinate
and coumaphos, combined with their propensity to accumulate in wax and
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