A New Threat to Honey Bees, the Parasitic Phorid Fly Apocephalus borealis

Honey bee colonies are subject to numerous pathogens and parasites. Interaction among multiple pathogens and parasites is the proposed cause for Colony Collapse Disorder (CCD), a syndrome characterized by worker bees abandoning their hive. Here we provide the first documentation that the phorid fly Apocephalus borealis, previously known to parasitize bumble bees, also infects and eventually kills honey bees and may pose an emerging threat to North American apiculture. Parasitized honey bees show hive abandonment behavior, leaving their hives at night and dying shortly thereafter. On average, seven days later up to 13 phorid larvae emerge from each dead bee and pupate away from the bee. Using DNA barcoding, we confirmed that phorids that emerged from honey bees and bumble bees were the same species. Microarray analyses of honey bees from infected hives revealed that these bees are often infected with deformed wing virus and Nosema ceranae. Larvae and adult phorids also tested positive for these pathogens, implicating the fly as a potential vector or reservoir of these honey bee pathogens. Phorid parasitism may affect hive viability since 77% of sites sampled in the San Francisco Bay Area were infected by the fly and microarray analyses detected phorids in commercial hives in South Dakota and California's Central Valley. Understanding details of phorid infection may shed light on similar hive abandonment behaviors seen in CCD

Distribution of phorid-infected honey bees sampled in this study (red).

<p>Inset shows the San Francisco Bay Area counties where we found phorid-parasitized honey bees. The routes of commercial hives tested are indicated (arrows), where dotted lines represent states the hives crossed before viral microarray testing and solid lines represent the route of hives during the period of microarray testing. Sites where <i>A. borealis</i> was previously known <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0029639#pone.0029639-Genersch1" target="_blank">[7]</a> are indicated by black dots.</p

Images of <i>Apocephalus borealis</i> and honey bees.

<p>(A) Adult female <i>A. borealis</i>. (B) Female <i>A. borealis</i> ovipositing into the abdomen of a worker honey bee. (C) Two final instar larvae of <i>A. borealis</i> exiting a honey bee worker at the junction of the head and thorax (red arrows).</p