Minor Pests of Bees
By: Clarence Collison
Bee Louse – The bee louse, Braula coeca Nitzch is a wingless fly that lives as a commensalist (relationship between two living organisms in which one organism benefits from the other without harming it) in western honey bee, Apis mellifera Linnaeus, colonies. Braula is presumed to be harmless to its host, though this point is debatable, and some countries recommend Braula control. Braula has an extensive global distribution, being documented in Africa, Asia, Europe, Australia (Tasmania), North America and South America (Smith and Caron, 1985).
Historically, Braula has repeatedly been introduced into the United States on importations of queen bees from foreign countries, and in many cases no effort has been made by the recipients of these queens to remove the parasites before the introduction of the queens. Usually, the parasites disappeared promptly. However, infestations were located in Carroll County, Maryland and also reported to occur in a small area in south-central Pennsylvania (Phillips, 1925).
Braula adults often are found on the heads of honey bee workers, drones and especially queens. While on the head of its host bee, Braula will feed on food from the mouth of its host as the host is fed by another bee or is feeding another bee. There is some evidence that adult Braula can induce regurgitation from bees by stroking the upper edge of a bee’s labrum until the bee extends its tongue. Then the Braula feeds on food or other secretions that the bee offers (Ellis et al., 2016).
Braula eggs are laid singly under the cappings of honey cells and the larvae excavate branched tunnels, approximately 0.75 mm in diameter, in and beneath the cappings. The tunnels are visible from the surface and spoil the appearance of comb honey (Eckert and Shaw, 1960). Female Braula can oviposit many places in the hive (empty cells, brood cappings, debris on the floor) but only eggs oviposited on honey cappings will hatch. Egg incubation periods range from two to 7.4 days, depending on the season. It is believed that Braula larvae feed on honey and pollen residues encountered while tunneling under the cell cappings. Larvae pupate within the tunnels, then emerge as adults (Ellis et al., 2016).
The bee louse is a highly specialized flattened, wingless fly that spends its entire adult life on adult honey bees. It feeds by stealing food directly from bees during social feeding (trophallaxis). The Braula fly has a preference to infest the honey bee queen. The queen is the most attended individual in the colony but despite this, the adult flies remain undetected by the workers. This is due to Braula possessing a cuticular hydrocarbon profile that mirrors that of their host honey bee colony. This chemical camouflage is most likely through odor acquisition from the honey bee host since even small colony-specific differences in the alkene isomer patterns present in the honey bees were also detected in the Braula’s profile. This finding further supports the idea that the honey bee recognition cues are contained within the alkene part of their hydrocarbon profile and Braula exploit this to remain undetected within an otherwise hostile colony (Martin and Bayfield, 2014).
Acarapis woodi (Rennie) – The honey bee tracheal mite was an extreme problem in North America in the mid- to late 80’s. Today, the honey bee tracheal mite is rarely found in beekeeping operations, so is considered to be a minor pest. “Acarapis woodi is restricted to the prothoracic tracheae of the honey bee hosts” (Delfinado-Baker and Baker, 1982).
A laboratory bioassay was used to study phenotypic differences in susceptibility of honey bees, to tracheal mites, Acarapis woodi Rennie. Significantly different infestation frequencies were found in bees from 23 colonies containing queens that were instrumentally inseminated with single drones. Queens and drones originated from a closed population composed of commercial stock from various areas of the United States. Mites were randomly distributed with respect to right and left prothoracic tracheae. Tracheae containing mites were no more or less attractive to migrating mites than non-infested tracheae. The same quantity of progeny per female was produced in tracheae containing one to three mites. Female mites apparently do not migrate a second time after egg laying begins. The degree of phenotypic variation suggests that selection of honey bees for tracheal mite resistance is feasible (Gary and Page, 1987).
The susceptibility of worker honey bees, as a function of age, to infestation by tracheal mites was investigated. Bees <24 hours old were infested most frequently, and the frequency of infestation declined precipitously thereafter. Bees more than four days old were rarely infested in colonies during active brood rearing. Only two of 255 bees more than eight days old, and one of 246 bees >16 days old, became infested. Most of the eggs found in bees more than three weeks old were apparently produced by the progeny of the original infestation (Gary et al., 1989).
An assessment was made of tracheal mite susceptibility in honey bees pupated at a low temperature. Using a laboratory bioassay, an experiment was conducted to compare the performance of newly-emerged (callow) bees raised at 30ºC (86°F) with those raised at the more normal brood temperature of 34ºC (93.2°F). The reduced temperature caused a delay of over five days in the emergence of the bees from the brood cells. The callow bees raised at 30ºC had over twice the mite prevalence level. The fecundity of the mites in the tracheae was similar for both temperature conditions. Increased susceptibility to tracheal mites resulting from reduced brood temperature may help to explain the mortality, in the temperature-stressed late Winter/early Spring period, of colonies with a moderate mite infestation in Autumn (McMullan and Brown, 2005).
Braula coeca
Colonies of honey bees infested with Acarapis woodi (Rennie) were studied during the four Winters of 1985-1989 in New York state. Samples of bees were obtained from colonies on several dates from Fall to Spring to determine mite prevalence and mite load scores. Mite infestations were much heavier than those reported elsewhere in North America. Over the two Winters for which adequate data were available (1987-1988 and 1988-1989), colonies with heavy mite infestations had significantly greater mortality. Spring brood areas were negatively correlated with mite prevalence and mite load scores. However, the strength of these correlations varied depending on the month and the year. These results indicate that tracheal mites have a substantial negative effect on colonies of honey bees in New York (Otis and Scott-Dupree, 1992).
Acarapis woodi
Acarapis dorsalis and Acarapis externus – Both mite species are external parasites found on the western honey bee (Apis mellifera). “Acarapis dorsalis Morgenthaler is found living in the dorsal groove of the scutellum on the thorax. Acarapis externus Morgenthaler is found on the ventral side of the neck and in the posterior tentorial pits” (Delfinado-Baker and Baker, 1982). These parasites have been the United States since the 1930s. In the late 1980s to early 2000s, these two Acarapis species were frequently detected with A. externus being found at higher levels than A. dorsalis. The abundance of A. externus over A. dorsalis may be due to the lack of host age preference by A. externus as their prevalence and intensity remained high on bees up to 35 days old. In contrast, infestation rate and mite load of A. dorsalis decreased as bees became older. By examining 16,515 worker bees from 2007 to 2019, A. dorsalis was detected yearly while A. externus infestation was sporadic. The higher frequency of detecting A. dorsalis over A. externus may be due to their differences in colonization ability. A. dorsalis was faster in establishing their population in mite-free colonies than A. externus and was also successful in invading A. externus-infested colonies. The introduction of 50 A. dorsalis in mite-free colonies was sufficient to found a population, while 500 A. externus may be too small to establish a population. Variation in responses to parasitic mites by different honey bee stocks also influenced Acarapis populations. A. dorsalis was most prevalent in the Hastings stock while the levels of A. externus were higher on the ARS-Y-C-1, Hastings x ARS-Y-C-1 hybrid and Louisiana stocks. The Russian honey bees also had higher levels of A. dorsalis than the Italian honey bees. However, both stocks’ responses to A. externus were inconsistent. Nonetheless, both ARS-Y-C-1 and Russian honey bees are known to be resistant to another Acarapis species, A. woodi, which is known to be a more serious parasite of honey bees than these two external Acarapis. The potential role of external Acarapis in virus transmission especially in Varroa-infested colonies needs to be studied (De Guzman et al., 2019).
The biology of the two external Acarapis mites of honey bees, Acarapis dorsalis and Acarapis externus was studied. It was observed that both Acarapis species have a similar developmental period (eight to nine days) with males emerging earlier than females. Mite load and infestation rate of A. dorsalis decreased as bees become older. A. externus remained high on bees up to 35 days old. This observation may indicate that A. dorsalis prefers younger bees while A. externus seems to maintain its population on older bees. In nucleus colonies deliberately exposed to known populations of both external Acarapis species, infestation by A. dorsalis appears to be more rapid than A. externus. The introduction of 500 A. dorsalis established the highest rate of infestation (17.10%) in a relatively short period of time, i.e., nine to 12 weeks. The highest infestations of A. dorsalis were during the Spring months (March to June) and in mid-late Summer (August and September) with the lowest infestation rates in January and July. For A. externus, mite population was highest in the Fall (October and November). The lowest infestation was recorded in July. The average female:male ratios observed were 1.9:1 for A. dorsalis and 2.07:1 for A. externus. No relationship between nectar flow and percent mite infestation was established (Ibay, 1989).
Ants – Ants are ubiquitous within apiaries and are common pests of managed honey bees. Payne et al. (2020) conducted a study in Texas to: 1) survey ants found within or near managed honey bee colonies, 2) document what interactions are occurring between ant pests and managed honey bees and 3) determine if any of six commonly occurring honey bee-associated viruses were present in ants collected from within or far from apiaries. Ants belonging to 14 genera were observed interacting with managed colonies in multiple ways, most commonly by robbing sugar resources from within hives. At least one virus was detected in 89% of the ant samples collected from apiary sites and in 15% of ant samples collected at non-apiary sites. They found that none of these ant samples tested positive for the replication of Deformed wing virus, Black queen cell virus or Israeli acute paralysis virus, however. Future studies looking at possible virus transmission between ants and bees could determine whether ants can be considered mechanical vectors of honey bee-associated viruses, making them a potential threat to pollinator health.
Honey bee-associated viruses are found in various arthropod species including invasive ants. The globally invasive Argentine ant (Linepithema humile), which can reach high densities and infest beehives, is associated with pathogen dynamics in honey bees was examined. Viral loads of deformed wing virus (DWV), which has been linked to millions of beehive deaths around the globe, and black queen cell virus significantly increased in bees when invasive ants were present. Microsporidian and trypanosomatid infections, which are more bee-specific, were not affected by ant invasion. The bee virome in Autumn revealed that DWV was the predominant virus with the highest infection levels and that no ant-associated viruses were infecting bees. Viral spillback from ants could increase infections in bees. In addition, ant attacks could pose a significant stressor to bee colonies that may affect virus susceptibility. These viral dynamics are a hidden effect of ant pests, which could have a significant impact on disease emergence in this economically important pollinator (Dobelmann et al., 2023).
Emerging infectious diseases are often the products of host shifts, where a pathogen jumps from its original host to a novel species. Viruses in particular cross species barriers frequently. Acute bee paralysis virus (ABPV) and deformed wing virus (DWV) are viruses described in honey bees (Apis mellifera) with broad host ranges. Ants scavenging on dead honey bees may get infected with these viruses via foodborne transmission. However, the role of black garden ants, Lasius niger and Lasius platythorax, as alternative hosts of ABPV and DWV is not known and potential impacts of these viruses have not been addressed yet. In a laboratory feeding experiment, we show that L. niger can carry DWV and ABPV. However, negative-sense strand RNA, a token of virus replication, was only detected for ABPV. Therefore, additional L. niger colonies were tested for clinical symptoms of ABPV infections. Symptoms were detected at colony (fewer emerging workers) and individual levels (impaired locomotion and movement speed). In a field survey, all L. platythorax samples carried ABPV, DWV-A and -B, as well as the negative-sense strand RNA of ABPV. These results show that L. niger and L. platythorax are alternative hosts of ABPV, possibly acting as a biological vector of ABPV and as a mechanical one for DWV. This is the first study showing the impact of honey bee viruses on ants. The common virus infections of ants in the field support possible negative consequences for ecosystem functioning due to host shifts (Schläppi et al., 2020).
The free-foraging honey bee visitation rate and visitation duration to aloe flowers with and without Argentine ants (Linepithema humile (Mayr)) in a drought-stressed environment study found that bees actively avoided foraging on the ant-occupied flowers. To determine the mechanisms of avoidance, their subsequent experiments assessed visitation in the absence of ants and compared visitation in the absence of ants and compared aloe flowers treated with ant pheromone to unmanipulated flowers lacking ant pheromone. Bees approached all flowers equally, but accepted flowers without ants at a higher rate than flowers with ants. Visitation duration also increased twofold on ant-excluded flowers, which suggest that Argentine ants may limit resource acquisition by bees. Honey bees similarly avoided flowers with Argentine ant pheromone and preferentially visited unmanipulated flowers at threefold higher rate. This study demonstrates that honey bees avoid foraging on floral-resources with invasive Argentine ants and that bees use ant odors to avoid ant-occupied flowers (Sidhu and Rankin, 2016).
References
De Guzman, L.I., T.E. Rinderer, D.M. Burgett, and A.M. Frake 2019. Understanding the trends in prevalence and abundance of Acarapis dorsalis and Acarapis externus in Apis mellifera colonies. Trends Entomol. 15: 85-98.
Delfinado-Baker, M. and E.W. Baker 1982. Notes on honey bee mites of the genus Acarapis hirst (Acari: Tarsonemidae). Int. J. Acarol. 8: 211-226.
Dobelmann, J., A. Felden and P.J. Lester 2023. An invasive ant increases deformed wing virus loads in honey bees. Biol. Lett. 19: 20220416
Eckert, J.E. and F.R. Shaw 1960. Beekeeping. Macmillan Co., New York, 536 pp.
Ellis, J.D., A.N. Mortensen and C.M. Zettle Nalen 2016. Bee louse, bee fly, Braulid, Braula coeca Nitzch (Insecta: Diptera: Braulidae). EENY472.
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Ibay, L.I. 1989. Biology of the two external Acarapis species of honey bees: Acarapis dorsalis Morgenthaler and Acarapis externus Morgenthaler (Acari: Tarsonemidae). Master Of Science Thesis, Oregon State University, 48 pp.
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Sidhu, C.S. and E.E.W. Rankin 2016. Honey bees avoiding ant harassment at flowers using scent cues. Environ. Entomol. 45: 420-426.
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Clarence Collison is an Emeritus Professor of Entomology and Department Head Emeritus of Entomology and Plant Pathology at Mississippi State University, Mississippi State, MS.
