Apocephalus borealis is a species of North American parasitoid phorid fly that parasitizes bumblebees, honey bees and wasps (Brues 1924, Ennik 1973, Brown, 1993, Otterstatter et al. 2002). The association with honey bees has so far only been documented from California and South Dakota (Core et al. 2012); elsewhere, they are primarily associated with bumblebees (Otterstatter et al. 2002).
Female flies land on the abdomen of their host and pierce the cuticula with a sharp, swordlike ovipositor. As the larvae develop, they attack the host's brains and cause it to become disoriented, fly at night and exhibit other unusual behaviors. Whether these changes in host behavior increase parasite fitness remains to be established (Core et al. 2012). Mature larvae emerge from the junction of the head and thorax, often decapitating the host (the generic name Apocephalus refers to this grim result). A. borealis has been suggested as a possible vector promoting the spread of the pathogens responsible for colony collapse disorder in bees (Coghlan 2012, Core et al. 2012).
- Brown, B. V. 1993. Taxonomy and preliminary phylogeny of the parasitic genus Apocephalus, subgenus Mesophora (Diptera: Phoridae). Systematic Entomology 18:191-230.
- Brues, C. T. 1924. Notes on Some New England Phoridæ (Diptera). Psyche 31: 41–44. doi:10.1155/1924/42175.
- Coghlan, A. 2012. Parasitic fly could account for disappearing honeybees. New Scientist 2846 (January 3, 2012).
- Core, A., Runcke, C., Ivers, J., Quock, C., Siapno, T. DeNault, S., Brown, B. DeRisi, J., Smith, C. D., and Hafernik, j. 2012. A new threat to honey bees, the parasitic phorid fly Apocephalus borealis. PLoS ONE 7 (1): e29639. doi:10.1371/journal.pone.0029639
- Ennik, F. 1973. Apocephalus borealis Brues parasitic upon Vespula spp. (Diptera: Phoridae, Hymenoptera: Vespidae). Pan-Pacific Entomologist 49:403-404.
♀. Length, including ovipositor 2.2 mm. Pale yellow, the central portion of the abdomen with an orange tinge and the legs pale brownish yellow; first segment of abdomen brownish, with pale hind margin; second segment with a brownish blotch at the middle of the lateral margin; third and fourth each with a larger darker spot; fifth entirely fuscous; sixth with the anterior angles brown; ovipositor brownish black, paler at tip, the membrane covering its upper side pale. Wings hyaline, venation pale fuscous. Front barely as high as wide; with only eight bristles below the ocelli; lowest row consisting of two reclinate post antennal ones and a lateral one next to the eye, median pair of the row above further apart than the post-antennals, this row curved upwards at the sides with the lateral bristle rather close to the eye margin and nearer to one of the median bristles than these are to one another. Ocellar row of four. All bristles strong, subequal. Median frontal suture distinct; lower half of front with scattered minute black bristles. Postocular cilia moderate, but the upper one on each side much enlarged. Antennae pyriform, obtusely pointed, as long as the front; arista no longer than the third joint, very stout, especially at base, nearly bare. Palpi rather broad, weakly bristled; cheeks each with two downwardly directed macrochaetae. Mesonotum sub-shining, with one pair of dorsocentral marcrochaetae; scutellum with one pair of bristles, the lateral pair very minute, scarcely visible. Propleura with two slender bristles above the insertion of the coxa and two minute ones near the humeral angle; mesopleura bare. Front coxa with a noticeable stripe of minute bristles along the anterior edge; middle tibiae not distinctly setulose; hind tibiae with a line of very delicate, closely placed setulae inside the posterior edge; all tarsi slender. Abdomen broad; second segment elongated, twice as broad as long, bare laterally; third to fifth segments gradually shorter, longer at the sides than along the median line; sixth longer and narrower, almost semicircular, with a few small marginal bristles medially at apex. Ovipositor of peculiar form; in dorsal view projecting beyond the sixth segment for a distance half the length of the abdomen; consisting of two chitinous pieces united at their apices, the upper one straight, issuing from the underside of the fifth and sixth segments and bearing below near the base a number of strong bristles; lower piece curved upward to meet the upper one and connected to it at the base by a large chitinous tooth originating at the extreme base of the upper piece. Viewed from the side (Fig. 1, A) the upper piece is seen to be nearly circular in section and the lower one greatly flattened; in ventral view (Fig. 1, B) the lower piece is spatulate, with truncate tip. Wing (Fig. 1, C) unusually narrow, costa not quite attaining the middle of the wing; first section of costa twice the length of the second; third very short, the minute second vein nearly perpendicular to the costa; fourth vein very slightly and evenly curved; fifth faintly bisinuate; sixth and seventh similarly sinuate; costal cilia rather long and set moderately close together.
Type from Salisbury Cove, Maine, July 17, 1913 (C. W. Johnson). It is deposited in the collection of the Boston Society of Natural History.
Apocephalus borealis is a species of North American parasitoid phorid fly that parasitizes bumblebees, honey bees and paper wasps. These flies are colloquially known as zombie flies and the bees they infect are colloquially known as zombees. The association with honey bees has so far only been documented from California, South Dakota, Oregon, and Washington; elsewhere, they are primarily associated with bumblebees and paper wasps, but most recently this species has changed host and has begun to attack the European honey bee.
The infection of European honey bees in North America by Apocephalus borealis was first discovered by Dr. John Hafernik, who noticed disoriented honey bees at a light at night on San Francisco State University's campus. He picked some up in a vial, forgot about them, and about a week later noticed that fly larvae had emerged from the dead bees. There is insufficient information as to why the parasitic fly jumped to its new host, but there is concern that this new host provides an opportunity for the fly to thrive and further threaten the decreasing honey bee population. A. borealis has been suggested as a possible vector promoting the spread of the pathogens responsible for colony collapse disorder.
Female flies lay their eggs in the bees, and as the larvae develop, they attack the bees' brains and cause them to become disoriented. Infected bees can be found walking in circles as well as losing the ability to stand. The honey bees will also remain inactive during the daytime until death occurs. The infected bees are also known to fly at night and exhibit other unusual behaviors such as hive abandonment in unusual weather conditions such as cold rainy nights when most insects remain inactive. These behaviors eventually result in the death of the bees, but increase the survival and spread of the phorid flies. Laboratory results show that female phorid flies immediately attack honey bees when put together. Females attack and pursue host honey bees until they land on their abdomens and insert the ovipositor for about two to four seconds, injecting eggs. Development of larvae take about an average of a week; the larvae feed on the honey bees' muscles and nervous system. Mature fly larvae typically emerge from the host between the head and thorax (but rarely result in decapitation), and pupate outside the host body. It usually takes about 28 days for the entire life cycle to take place.
Two final instar larvae of A. borealis exiting a honey bee worker at the junction of the head and thorax
Adult female A. borealis
Head of an A. borealis
There is now a citizen project, "Zombee Watch" which uses a social media framework for people to report sightings of potentially parasitized bees. The stated goals of the project are to determine where in North America the Zombie Fly is parasitizing honey bees, how often honey bees leave their hives at night (even if they are not parasitized by the Zombie Fly), and to engage citizen scientists in making a significant contribution to knowledge about honey bees and to become better observers of nature.
- Brues, C. T. (1924). "Notes on Some New England Phoridæ (Diptera)". Psyche: A Journal of Entomology 31: 41–44. doi:10.1155/1924/42175.
- Kayla Figard (August 2, 2012). "Seeking Zombee Hunters". The San Francisco Examiner. p. 12.
- Sandi Doughton (September 26, 2012). "Start's first case of 'zombie bees' found in Kent". The Seattle Times.
- Ben Gittleson (January 30, 2014). "'Zombie' Bees Surface in the Northeast". ABC News.
- TedTalk (October 31, 2012). "Flight of the Living Dead: Dr. John Hafernik". TedTalk.
- Anton Preston Arce, Rojelio Pedraza (2012). "Evaluation of Phorid Fly (Apocephalus borealis) Parasitism of Feral Honey Bee (Apis mellifera) Colonies in South Orange County.". KSBR and the Department of Biological Sciences,Saddleback College.
- Core, Andrew; Runcke, Charles; Ivers, Jonathan; Quock, Christopher; Siapno, Travis; DeNault, Seraphina; Brown, Brian; DeRisi, Joseph; Smith, Christopher D.; Hafernik, John. "A new threat to honey bees, the parasitic phorid fly Apocephalus borealis". PLoS ONE 7 (1): e29639. doi:10.1371/journal.pone.0029639. PMC 3250467. PMID 22235317.
- Andy Coghlan (January 3, 2012). "Parasitic fly could account for disappearing honeybees". New Scientist.
- Castro, Joseph. "Fly Parasite Turns Honeybees Into Zombies | LiveScience".
- "Zombee Watch". Zombee Watch.
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