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Bug of the Week is written by "The Bug Guy," Michael J. Raupp, Professor of Entomology at the University of Maryland.

Zombie bees, Apis mellifera, and their tormentor the humpbacked fly, Apocephalus borealis

 

The honey bee is one of the most important pollinators we have, responsible for about one out of every 3 bites of food we eat. 

 

This week we return from the tropical paradise of the Belizean rainforest where we met tarantulas and lanternflies to frigid North America, where reports of zombie honey bees made headlines over the past few weeks. In recent years zombies have been all the rage on television and the silver screen, but when it comes to honey bees, becoming a zombie is a serious and disturbing matter.

This saga began in 2008 when Professor John Hafernik of San Francisco State University discovered honey bees behaving in aberrant ways. Normally honey bees are one of the most orderly species of insects, displaying distinct patterns of foraging behavior and brood care. The ability of worker bees to communicate information such as the location and quality of food sources is one of the paradigms on animal behavior. However, while observing honey bees in California, Professor Hafernik noticed bees behaving abnormally, becoming disoriented, demonstrating uncoordinated movement, and flying at night, all behaviors very un-beelike. Upon closer examination, these zombie bees were found to be infested with larvae of a small parasitic fly, Apocephalus borealis, known as a humpbacked fly.

Phorid flies like this one share the humpbacked appearance found in Apocephalus.

Humpbacked flies are some of the most curious flies in the insect world. One species, the coffin fly, breeds in carrion and these flies can burrow more than a meter into the earth and enter leaky coffins in search of cadavers that serve as food for their larvae. Other humpbacked flies attack and parasitize ants. Upon hatching within the ant, larvae migrate to the ant’s head and consume the victim’s brains. The ultimate outcome of this outrageous act is the decapitation of the ant, and the final development of the fly takes place in the ant’s head on the ground. Yikes! Prior to last autumn, honey bees under siege by Apocephalus borealis were known to occur only in California, Washington, Oregon, and South Dakota, but in the autumn of 2013, the zombie-producing fly was discovered attacking honey bees in Vermont.

The act of zombiefication begins when the female Apocephalus fly lands on the worker bee and injects her eggs into its body cavity. Eggs hatch into maggots that consume tissues within the bee. The presence of the maggots causes the unusual behaviors and ultimately results in the honey bee abandoning its hive during the night. The loss of worker bees is particularly disturbing given the array of factors threatening honey bees. Over the past decade honey bees have been beset by a variety of ills collectively known as Colony Collapse Disorder or CCD. Soon after CCD was discovered, national surveys of beekeepers were conducted to determine the magnitude of the problem. Between September 2006 and March 2007, beekeepers lost approximately 32% of their hives. During a similar period in 2007 and 2008, beekeepers lost about 36% of their colonies.

 

How serious is the threat of zombie-making phorid flies to our honey bees?

The cause of CCD is not fully understood, but researchers have made great progress identifying some of the culprits in this mystery. The introduction of Varroa mites in the late 1980’s decimated the bee industry in the United States. Varroa mites infest honey bees and suck blood from larvae, pupae, and adults, particularly male bees. Not surprisingly, this weakens bees and predisposes them to more serious diseases. Varroa mites have also been implicated in transferring viruses that attack or cripple bees, such as acute bee paralysis virus and deformed wing virus. It appears that several primary stress agents including Varroa mites, pesticides, and less than optimal sources of pollen impose physiological stress on colonies of bees. Pesticides are regularly used to manage pests of crops and honey bees may encounter residues in nectar and pollen. A recent publication implicates fungicides as an important contributor to declines in honey bee health. Even pesticides used to combat Varroa mites may accumulate in beeswax in the hive. As bees return with nectar and pollen, pesticides can accumulate in comb and other products, including honey. Pesticides are thought to further stress bees and weaken their immune systems, predisposing them to diseases. In addition to the viral diseases mentioned previously, honey bees are susceptible to a nasty single celled gut parasite called Nosema.  Nosema hits worker bees the hardest with symptoms of dysentery and a reduced ability to conduct their important job of tending brood and the queen. Queens infected with Nosema have shortened lives and lay fewer eggs.

While the incidence of CCD has declined somewhat in recent years, hive losses by commercial beekeepers still exceeded 30% in many parts of the country. Scientists and beekeepers are concerned that this long, exceptionally cold winter will not prove to be a good one for our honey bees. The bad news for honey bees is that one more debilitating parasite has been added to the list of miscreants attacking this beloved pollinator. Unfortunately, Apocephalus borealis is native to the United States and known to exist from coast to coast and border to border, where it parasitizes native bumble bees and paper wasps. Will it pop up attacking honey bees in more states? Time will tell.

 

In addition to crops, honey bees are important pollinators of native plants like these bluebonnets.

References

Bug of the Week consulted the following publications in preparation of this episode. Core A, Runckel C, Ivers J, Quock C, Siapno T, et al. (2012) A New Threat to Honey Bees, the Parasitic Phorid Fly Apocephalus borealis. PLoS ONE 7(1): e29639. doi:10.1371/journal.pone.0029639; and Pettis JS, Lichtenberg EM, Andree M, Stitzinger J, Rose R, et al. (2013) Crop Pollination Exposes Honey Bees to Pesticides Which Alters Their Susceptibility to the Gut Pathogen Nosema ceranae. PLoS ONE 8(7): e70182. doi:10.1371/journal.pone.0070182.

To learn more about honey bees and the latest on CCD, please visit the following web site:

http://www.ars.usda.gov/news/docs.htm?docid=15572