XXII CNIE - Accademia nazionale italiana di Entomologia

Scientists converged on a subset deemed most consistent with the epidemiological
evidence, which included the introduction of a new parasite or pathogen, exposure to
pesticides, problems with nutrition, and/or exposure to stresses of contemporary
beekeeping practices. A working group was constituted and an extraordinary collective
effort involving a large number of institutions was launched to investigate the
phenomenon and identify its cause (Cox-Foster and van Engelsdorp 2009). This effort is
still ongoing but even in this relatively short period of time a considerable amount of
information has been obtained that can be applied to improve the general health and
well-being of U.S. honey bees. In fact, as Kim Flottum, longtime editor of Bee Culture
magazine, was moved to note, “beekeeping has changed more in the last two years than
in the last 20” (http://www.thedailygreen.com/environmental-news/blogs/bees/colonycollapse-disorder-88012901).
Publication in 2006 of the honey bee genome sequence (Weinstock et al. 2006) provided
new insights into potential vulnerabilities of Apis mellifera as well as powerful new
tools to use in investigating possible causes of CCD. An evaluation of the honey bee
revealed that suites of genes associated with immune responses (Evans et al. 2006) and
detoxification (Claudianos et al. 2006) are reduced in number relative to other insect
species and may account for relatively greater vulnerability of honey bees to disease and
to pesticide poisoning. Thus, novel pathogens or novel pesticides were considered
likely possibilities as causing or contributing to CCD.
Pathogens?
The rapid spread of CCD throughout the country, as well as unusual autopsy findings,
suggested that a new pathogen may be the cause of bee die-offs. Using an unbiased
metagenomic approach, Cox-Foster et al. (2007) evaluated the microbial flora of honey
bees in hives diagnosed with CCD, ostensibly healthy hives, and imported royal jelly.
Candidate pathogens were analyzed to estimate the degree of association with a
diagnosis of CCD. Bees afflicted with CCD were found to contain a variety of
pathogens, the most predictive of which was the Israeli acute paralysis virus (IAPV), a
dicistrovirus not previously reported in the U.S. However, assigning a causative role to
IAPV has been problematic as differences in symptomology argued against IAPV as the
sole agent, and a later study found that IAPV had been present in the US bee population
prior to the appearance of CCD (Chen et al. 2007). The metagenomic analysis identified
other pathogens associated with CCD bees, including Kashmir bee virus (KBV),
deformed wing virus (DWV) and two species in the microsporidian genus Nosema.
Indeed, the presence of multiple pathogens was a better predictor of CCD than presence
of IAPV alone. The high prevalence of multiple pathogens in CCD bees was consistent
with the suggestion that a change in immune function may be integral to development of
CCD.
Another candidate pathogen suspected early on to play a role in CCD is the
microsporidian pathogen Nosema ceranae. N. ceranae is a coevolved parasite of the
Asian honey bee Apis cerana and there is considerable evidence that it has recently
colonized A. mellifera in the U.S. and Europe, which, as a novel host, has little
resistance. Although N. ceranae is very similar to Nosema apis, a longtime pathogen of
Apis mellifera, in many ways, it causes a suite of symptoms that differ from N. apis
infection, most notably in the swiftness of onset and absence of diarrhea-like
gastrointestinal problems. Although studies in Europe documented that N. ceranae
infections can lead to seemingly sudden collapses in the presence of ample brood, pollen
and honey due to a long asymptomatic incubation period (Higes et al. 2008), the
presence of N. ceranae in a high proportion of colonies in the U.S. considered to be free
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