A new threat to honey bees, the parasitic phorid fly Apocephalus borealis

Abstract

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.

Figure 1. Distribution of phorid-infected honey bees sampled in this study (red).

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 A. borealis was previously known are indicated by black dots.

Figure 2. Images of Apocephalus borealis and honey bees.

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

Figure 3. Rates of phorid parasitism in honey bees.

(A) Rates of parasitism for bees sampled from April 2009 through November 2010. Black solid line shows rates in stranded bees from under lights on the San Francisco State University campus, while the pink dashed line shows rates in foraging bees. Stranded bees found under lights were sampled at irregular intervals during 2009 and sampled every two days in 2010. Foragers were sampled monthly from our main study hive. A rate of zero indicates that samples from that period contained no parasitized bees. We compared rates of parasitism in stranded and active foraging bees collected at San Francisco State University from October 2009 through January 2010 and from July 2010 to December 2010 (when parasitism rates peaked). 2009–2010 peak rates of parasitism in samples of stranded bees (Mean = 60%, n = 276) were significantly higher than peak rates of parasitism in active foragers from our main study hive (Mean = 6%, n = 164) (χ² = 126.7, d.f. 1, p<0.0001). This pattern repeated in 2010 when peak rates of parasitism in samples of stranded bees (Mean = 50%, n = 860) were again significantly higher than rates of parasitism in active foragers (Mean = 4%, n = 422) (χ² = 255.3, d.f. 1, p<0.0001). (B) Proportion of honey bees parasitized by phorids in samples from stranded bees collected from the Hensill Hall landing under lights (dotted line) and from samples of bees collected from overnight hive enclosures on adjacent nights (solid line). Parasitism rates of bees trapped in the enclosures closely track rates in stranded bees found under lights during the same period and the number of bees found under lights significantly declined when the enclosure was in place (Welch's t-test p<0.0001) indicating that stranded bees came from our main study hive and were parasitized prior to abandoning the hive.