Threats to Honey Bees by phorid flies (Insecta: Diptera: Phoridae)

by Brian V. Brown, last updated April 17, 2016

Highly productive agriculture relies on fruits and vegetables pollinated largely by the Western Honey Bee, Apis mellifera (hereafter referred to as “honey bees”). This insect was introduced into North America from its original range in Europe and Western Asia shortly after Europeans began to settle here. Although there is a diverse native bee fauna in North America, there is no species that has the horticulturally desireable characteristics of honey bees, namely that they 1) live in large colonies usually found in tree cavities, but happily accept a man-made version (commercial hives, or “supers”), 2) are relatively docile and allow manipulation of their colonies, 3) are generalist pollinators that will forage amongst nearly any crop in which they are stationed. Because of these factors, honeybees can be cultured in large numbers, transported to the crops needing pollination and “applied” in numbers suitable to ensure the required level of flower visitation. The use of honey bees markedly and predictably increases the yield of crops, thus greatly increasing the efficiency of US agriculture.

A list of plants that require honey bee pollination is massive, comprising over 100 food crops. In addition to pollination services, honey bees also provide other commercial benefits, such as the production of honey, beeswax, royal jelly, and bee pollen.

Because of their undeniably vital nature to US farmers, honey bees are among the most agriculturally important insects. Recent reductions in colonies because of the mysterious colony collapse disorder (CCD) have raised concern about the security of our food supply. Further stresses on colonies caused by predators, parasites, and diseases could seriously compromise our ability to mass culture honey bees and to export honey bees elsewhere.

Most insects are attacked by predators and parasitoids, the difference being that predators attack multiple hosts, while parasitoids attack and kill a single host (usually by the feeding of their immature stages). In their homeland of Europe, honey bees are attacked by many predators, as well as parasitoid conopid flies. When introduced to the New World, however, they became exposed to a whole range of new parasitoids of the family Phoridae, whose original hosts are the diverse native bumblebees and, in South and Central America, stingless bees.

Phorid flies (Diptera: Phoridae) are found throughout the world, and are among the most biologically diverse families of insects. An approximate 200 species are known to be associated with native bees of the family Apidae, and a few others with family Halictidae. Relationships of the flies to the bees range from scavengers and kleptoparasites in the nest to parasitoids of adult workers. The effects of these flies upon their hosts and upon host colonies are largely unknown, especially in the New World tropics. Observations made by me and coworkers indicate that many tropical parasitoid species will attempt to oviposit (lay eggs) in foraging honey bees in the field. Various species of these flies live at low to high elevations, such that survival in at least southern North America is unfortunately possible if the correct species were introduced.

The importance of phorid flies to apiculture was until recently considered minimal, but the apparent recent host switch of Apocephalus borealis from bumble bees to honey bees has raised concerns (Core et al. 2012) that an overall decline in honey bee colony viability (via CCD), could be exacerbated by attack from these new parasitoids. Additionally, a colony of Central American stingless bees has become established in Palo Alto, California, supporting the possibility that associated tropical phorid parasitoids could also become established here.

Honey bees are attacked by many phorid flies whose native hosts are mostly other apid bees. There are two main categories of honey bee associates within the Phoridae: those that attack the brood in the nest, and those that attack workers foraging outside the colony.

Brood predators

Pseudohypocera. The most serious threat to honey bees from the Phoridae are brood predators of the species Pseudohypocera kerteszi. This fly is found throughout the New World tropics, where it is especially damaging to attempts to culture stingless bees, but also has been found in colonies of honey bees (Robinson 1981, Reyes 1983, Hernández and Gutiérrez 2001). Weakened colonies are especially vulnerable to attack, which can lead to destruction of entire colonies.

Megaselia. Megaselia scalaris in warmer climates and Megaselia rufipes in cooler climates are often found in declining honey bee colonies, and can be facultative predators on injured or diseased bee larvae (Disney 1994, 2008). In particular, Megaselia scalaris are found in colonies that have already been damaged by Pseudohypocera (B.Brown, personal observation). The effects of these flies on bee colony health is unknown.

Parasitoids

Apocephalus. Several species of this genus are known to be parasitoids of stingless bees in South and Central America (Brown 1993, 1996a, b, 1997), all belonging to the A. wheeleri subgroup (formally known as subgenus Mesophora). An additional species of the A. wheeleri subgroup, Apocephalus borealis, was known to parasitize bumblebees, vespid wasps, and black widow spiders (Brown 1993), but has been shown more recently also to attack honey bees (Core et al. 2012). Heavily parasitized colonies were abandoned by bees, and a pattern reminiscent of some CCD afflicted colonies. Parasitized bees seem to have altered behavior, and have been dubbed “zombees”. The original report emphasized attraction of parasitized bees to lights at night, but later instances of light attracted bees had no associated parasitism. Thus, the role of the flies in altering bee behavior is unknown.

Numerous described species of the Apocephalus wheeleri subgroup are known from middle elevation Central America, most with unknown hosts. Some species closely resemble A. borealis and may have similar habits.

Melaloncha. Nearly 200 species of this genus are known from South and Central America (Brown 2004a, b, Gonzalez and Brown 2004, Brown 2005, 2006, Brown and Kung 2006, Kung 2008, Smith and Brown 2008, Brown and Smith 2010). All are parasitoids of apid bees, mostly of tribe Meliponini (stingless bees), although some are also known to attack orchid bees and bumble bees. In mixed foraging situations, especially on the flowers of palm trees, we observed many oviposition attempts by these flies on honey bees. In fact,the first parasitoid described from Apis mellifera was a phorid fly from Brazil, Melaloncha ronnai. This is the only species of Melaloncha that has been recorded breeding in honey bees, but in the field we have observed numerous other species of Melaloncha attempting to lay eggs in these bees, and it is a virtual certainty that some have been successful.

Styletta. Only one species of this genus is known, the minute Styletta crocea of South and Central America. Although it usually attacks small stingless bees, we have observed attempted oviposition in honey bees as well.

Other possible parasitoids. The bee associated phorid fly fauna of the Old World tropics has never been studied, a particularly unfortunate omission since the genus Apis is most diverse in Southeast Asia. Some species of the phorid genus Phalacrotophora from the Philippines are remarkably similar in body structure to the New World genus Melaloncha, and may have similar lifestyles.

References

Brown, B. V. 1993. Taxonomy and preliminary phylogeny of the parasitic genus Apocephalus, subgenus Mesophora (Diptera: Phoridae). Systematic Entomology 18: 191-230.

Brown, B. V. 1996a. Preliminary analysis of a host shift: revision of the Neotropical species of Apocephalus, subgenus Mesophora (Diptera: Phoridae). Contributions in Science 462: 1-36.

Brown, B. V. 1996b. A further species of Apocephalus, subgenus Mesophora (Diptera: Phoridae) parasitic on stingless bees (Hymenoptera: Apidae: Meliponinae). Studia dipterologica 3: 231-235.

Brown, B. V. 1997. Parasitic phorid flies: a previously unrecognized cost to aggregation behavior of male stingless bees. Biotropica 29: 370-372.

Brown, B. V. 2004a. Revision of the subgenus Udamochiras of Melaloncha bee-killing flies (Diptera: Phoridae). Zoological Journal of the Linnean Society 140: 1-42.

Brown, B. V. 2004b. Revision of the Melaloncha cingulata-group of bee-killing flies (Diptera: Phoridae). Annals of the Entomological Society of America 97: 386-392.

Brown, B. V. 2005. Revision of the Melaloncha (M.) furcata-group of bee-killing flies (Diptera: Phoridae). Insect Systematics and Evolution 36: 241-258.

Brown, B. V. 2006. Revision of the untreated taxa of Melaloncha s. s. bee-killing flies (Diptera: Phoridae). Zootaxa 1280: 1-68.

Brown, B. V., and G. Kung. 2006. Revision of the Melaloncha ungulata-group of bee-killing flies (Diptera: Phoridae). Contributions in Science 507: 1-31.

Brown, B. V., and P. T. Smith. 2010. The bee-killing flies, genus Melaloncha Brues (Diptera: Phoridae): a combined molecular and morphological phylogeny. Systematic Entomology 35: 649-657.

Core, A., C. Runckel, J. Ivers, C. Quock, T. Siapno, S. DeNault, B. V. Brown, J. DeRisi, C. D. Smith, and J. Hafernik. 2012. A new threat to honey bees, the parasitic phorid fly Apocephalus borealis. PLoS One 7: e29639.

Disney, R. H. L. 1994. Scuttle flies: the Phoridae. Chapman and Hall, London.

Disney, R. H. L. 2008. Natural history of the scuttle fly, Megaselia scalaris. Annual Review of Entomology 53: 39-60.

Gonzalez, L., and B. V. Brown. 2004. New species and records of Melaloncha (Udamochiras) bee-killing flies (Diptera: Phoridae). Zootaxa 730: 1-14.

Hernández, F. O., and A. A. Gutiérrez. 2001. Avoiding Pseudohypocera attacks (Diptera: Phoridae) during the artificial propagation of Melipona beecheii colonies (Hymenoptera: Apidae: Meliponini). Folia Entomologica Mexicana 40: 373-379.

Kung, G. 2008. Two new species of the Melaloncha ungulata group of bee-killing flies (Diptera: Phoridae). Sociobiology 51: 491-496.

Reyes, F. 1983. A new record of Pseudohypocera kerteszi, a pest of honey bees in Mexico. American Bee Journal (1983): 119-120.

Robinson, G. E. 1981. Pseudohypocera kerteszi (Enderlein) (Diptera: Phoridae), a pest of the honey bee. Florida Entomologist 64: 456-457.

Smith, P. T., and B. V. Brown. 2008. Utility of DNA sequences for inferring phylogenetic relationships and associating morphologically dissimilar males and females of the bee-killing flies, genus {IMelaloncha} (Diptera: Phoridae). Annals of the Entomological Society of America 101: 713-721.