Abstract
BackgroundIn 2010 Colony Collapse Disorder (CCD), again devastated honey bee colonies in the USA, indicating that the problem is neither diminishing nor has it been resolved. Many CCD investigations, using sensitive genome-based methods, have found small RNA bee viruses and the microsporidia, Nosema apis and N. ceranae in healthy and collapsing colonies alike with no single pathogen firmly linked to honey bee losses.Methodology/Principal FindingsWe used Mass spectrometry-based proteomics (MSP) to identify and quantify thousands of proteins from healthy and collapsing bee colonies. MSP revealed two unreported RNA viruses in North American honey bees, Varroa destructor-1 virus and Kakugo virus, and identified an invertebrate iridescent virus (IIV) (Iridoviridae) associated with CCD colonies. Prevalence of IIV significantly discriminated among strong, failing, and collapsed colonies. In addition, bees in failing colonies contained not only IIV, but also Nosema. Co-occurrence of these microbes consistently marked CCD in (1) bees from commercial apiaries sampled across the U.S. in 2006–2007, (2) bees sequentially sampled as the disorder progressed in an observation hive colony in 2008, and (3) bees from a recurrence of CCD in Florida in 2009. The pathogen pairing was not observed in samples from colonies with no history of CCD, namely bees from Australia and a large, non-migratory beekeeping business in Montana. Laboratory cage trials with a strain of IIV type 6 and Nosema ceranae confirmed that co-infection with these two pathogens was more lethal to bees than either pathogen alone.Conclusions/SignificanceThese findings implicate co-infection by IIV and Nosema with honey bee colony decline, giving credence to older research pointing to IIV, interacting with Nosema and mites, as probable cause of bee losses in the USA, Europe, and Asia. We next need to characterize the IIV and Nosema that we detected and develop management practices to reduce honey bee losses.
Highlights
Honey Bee Colony Health in the USA Colony Collapse Disorder (CCD) continues to impact bee colonies in the USA in 2010 at levels seemingly equal to, or exceeding that of 2007, when this unusual syndrome first received worldwide press coverage [1,2]
Proteomics analysis of other samples of bees from CCD colonies, conducted by the U.S Army, yielded one of the earliest reports of Nosema ceranae and of Varroa destructor virus-1 (VDV-1) [6], as well as an RNA virus that was later identified as Israeli acute paralysis virus (IAPV) [7], in North American bees
A recent study failed to confirm a link between CCD and IAPV [9], and while IAPV can contribute to honey bee mortality, the signs are not consistent with CCD [10]
Summary
Honey Bee Colony Health in the USA Colony Collapse Disorder (CCD) continues to impact bee colonies in the USA in 2010 at levels seemingly equal to, or exceeding that of 2007, when this unusual syndrome first received worldwide press coverage [1,2]. The disorder is characterized by sudden losses of bees This results in nearly empty beehives that, at best, may harbor a queen and a small worker bee population. Metagenomics initially identified Israeli acute paralysis virus (IAPV) as a potential marker or cause of CCD [4], yet a subsequent study demonstrated that IAPV was in the USA long before the recent CCD outbreaks [5]. A recent study failed to confirm a link between CCD and IAPV [9], and while IAPV can contribute to honey bee mortality, the signs are not consistent with CCD [10]. Many CCD investigations, using sensitive genome-based methods, have found small RNA bee viruses and the microsporidia, Nosema apis and N. ceranae in healthy and collapsing colonies alike with no single pathogen firmly linked to honey bee losses
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