Identifying Viral Pathways of Transmission – Part 2
The Three-Part Honey Bee Virus Series
By Nicole McCormick, Alberta Tech Transfer Program Technician
How are honey bee viruses transmitted?
In part one of this three-part honey bee virus series, we learned how to identify clinical signs of common honey bee virus infections and to understand their effects on colony and bee health. Now, we will explore further on how they are transmitted within and across generations. The process in which a virus is transmitted is paramount to its persistence, viability, and spread within a host population1. The social structure of honey bee colonies creates many opportunities for viral transmission, these mainly include activities that involve a high contact rate between individuals1. Bee-bee interactions, such as the removal of invaders, comb building, foraging, cleaning brood cells, rearing offspring, and attending to the queen, all provide opportunities for viral spread1. Viral transmission can be divided into two major categories: horizontal and vertical transmission. Horizontal transmission, the most common route for bee viruses’, is defined as the spread of a virus within the same generation2. Furthermore, specific routes of horizontal transmission include: or oral-fecal, topical, or bodily contact, venereal, and finally, vector-based transmission2. Vertical transmission is defined as the transmission of a virus to the following generation, primarily from queen to offspring2. Within honey bee colonies, this form of transmission can either be transovum, the transmission of a virus on the outside of an egg; or transovarial, the transmission of a virus within the egg2.
Throughout this article, I will expand on these pathways of viral transmission while also linking them to the viruses that we have focused on thus far (i.e., Deformed Wing Virus (DWV), Varroa Destructor Virus (VDV), Chronic Bee Paralysis Virus (CBPV), Black Queen Cell Virus (BQCV) and Sacbrood Virus (SBV). Knowing and understanding these pathways of viral transmission is crucial to ensuring that the proper management practices are being implemented to reduce transmission and keep our bees healthy.
Oral-Oral or Oral-Fecal Viral Transmission is when bees ingest virally contaminated food, feces, or other hive products, and become infected3. This is arguably one of the most common pathways of transmission for all five viruses, as many food and other colony by-products can test positive for viral particles, and in result have the ability to be infectious2. BQCV, DWV, VDV and SBV have been detected in pollen and honey, while CBPV has been detected in honey only 1,2. DWV and SBV have been found in glandular secretions of nurse bees, therefore a potential source of viral particle in larval food2,4. The consumption of contaminated food products can introduce viruses into the bee digestive tract and, ultimately, infect healthy bees.
Due to the many hive activities that are coordinated between various working bees’, transmission from bee to bee is highly likely and happens very frequently1. Certain activities, such as cannibalizing eggs and young larvae during periods of protein deprival, removal of diseased brood containing virus particles, and cell/hive cleaning (i.e., removal of feces and dead bees from the bottom) (Figure 1.), are all opportunities of oral-oral/oral-fecal viral transmission1,3. Furthermore, activities involving trophallaxis, the mouth-to-mouth sharing of food between colony members, can be another significant route of viral transmission2. Attending to the queen, feeding brood, packing pollen, oral communication, and nectar processing are some examples1. During periods of poor weather, these activities are done in close confinement and trophallaxis happens more often, increasing viral spread1. Feces can also build up in the hive due to the bees’ inability to leave and take cleansing flights, causing an increase in workers coming into contact with contaminated feces as they remove it from the hive2.
Viral loads in different bee tissues such as the hemolymph, ovaries, gut, and head have been found to vary in comparison to one another1. It was found that viral levels, specifically for DWV, and BQCV, were highest in the gut, suggesting that the incidence of oral-fecal transmission is significantly higher than other pathways such as venereal transmission1. Feces excreted by infected adult bees will have high viral levels, increasing the risk of fecal transmission2. In fact, BQCV, DWV, and CBPV have all been detected in honey bee feces. Furthermore, it was found that the presence of feces contaminated with CBPV can trigger an overt infection (i.e., exhibiting clear infection symptoms) in healthy adult bees after contact with infected feces2.
Topical or bodily contact transmission is caused by increased rubbing, grooming, and general body contact between infected and healthy bees2. More specifically, it is the application of viral particles on newly exposed honey bee cuticle, or in other words when a bees’ protective cuticle layer has broken, giving the virus access to the epidermal cytoplasm2,3. This pathway of transmission can become an evident problem when bees are confined during periods of time when they would normally be active3. For example, during periods of poor weather, increased robbing activity, and when there are too many colonies grouped together per area of land, reducing nectar availability3. These events cause an increase in the number of bees present in the hive for long periods of time, therefore, increasing the rate of rubbing and contact between bees within the colony5. Contact transmission requires significantly more viral particles to cause infection, when compared to vector-based, and has only been linked to CBPV6.
Interestingly, a study on the effects of pollen traps on CBPV relapse, found that the use of pollen traps in commercial beekeeping can aid in the transmission of CBPV in colonies that were previously infected with this virus5. This increased relapse rate was attributed to infected foragers transferring the virus on to the pollen trap, which in turn would infect healthy forager as they entered and exited the colony5. It was also found that pollen traps reduced the colony’s ability to dispose of dead or infected bees, increasing the chances of healthy bees within the colony coming into contact with dead CBPV-infected bees5. It’s important to note, in this example, that pollen traps do not cause CBPV to enter the colony, but they can make the onset of the infection worse.
Venereal transmission is the spread of a virus between two sexes during mating1. More clearly, it’s the transmission of a virus from drone to queen exclusively during mating flights2. This type of transmission is considered to be one-directional, as the drone soon dies after mating while the queen will go on to lay eggs that are potentially infected3. Venereal transmission is a form of horizontal transmission, as it occurs within the same generation2. However, it’s also a precursor for vertical transmission as once a queen is infected, the virus could potentially be passed on to the following generations2. Drone seminal fluid tends to contain high levels of multiple viruses, therefore, making the spread of these viruses possible3. This could potentially be because varroa mites favour drones as they are larger and have more fat to feed on (Figure 2.), which in turn increases the rate of varroa-mediated viral transmission7. In an experimental setting using artificially inseminated queens, researchers detected BQCV, SBV, VDV and DWV in the queen spermatheca (internal organ responsible for storing semen) following insemination, suggesting that these viruses can be spread via seminal fluid2,3. Venereal transmission has also been observed in the natural mating of honey bees2. This form of viral spread is thought to be very efficient as queen mating happens over a 3. During mating flights queens will visit multiple drone congregation areas and mating happens with drones from far away locations, allowing for viruses to spread not only within a colony or an apiary, but between different regions of land.
Vector-based transmission is a form of indirect transmission as viruses are harboured within a living parasitic vector, such as Varroa destructor, and are then passed on to a healthy host during parasitic behaviours1. A high Varroa mite infestation is one of the main causes of increased viral levels within honey bee populations, and their prevalence throughout North America has continually been increasing3.
Varroa mites can act as both mechanical and biological vectors2. A mechanical vector passes along the virus without becoming infected itself, while a biological vector allows for viral replication before passing it along to a host2. Depending on the virus, the varroa mite can act as both types of vectors. For instance, it has been found that DWV and VDV can replicate within the mite before spreading to honey bees, increasing the quantity of virus particles transmitted2. Chronic Bee Paralysis Virus has also been detected within varroa mites, indicating that mites can act as a mechanical vector for this virus2. Conversely, there has been no definitive evidence that varroa mites can act as a vector for SBV or BQCV, however in the field these viruses are frequently associated with high varroa levels1.
Traynor et al. (2020) outlined three major parts of varroa-mediated viral transmission8. The first being acquisition of the viral pathogens, where varroa mites will feed on the hemolymph of infected bees and acquire any pathogens that are present in the bee tissue. The second part is mobility; the mites frequently move around a colony between brood and adult bees as this is part of their reproductive cycle1. Finally, the last part is transmission. After acquiring the virus and moving to a new potentially uninfected host, the mite facilitates the direct injection of viral particles into the host, therefore causing infection. If the mite infestation within a colony is high, this cycle can persist on a larger scale, making this method of transmission the most efficient and lethal within honeybee colonies1.
Vertical transmission is the transmission of a virus between generations from queen to offspring2. This route of transmission is not as common as horizontal transmission and tends to have less detrimental effects as it allows the virus to persist at low levels without causing harm1. The detection of CBPV, SBV, DWV, VDV and BQCV in queen ovaries and/or in eggs has indicated that there is potential for transmission of these viruses vertically2. It has been commonly found that queens that have tested positive for viruses will produce offspring that test positive for the same viruses7. The positive detection of viruses within queen ovaries can indicate transovarial transmission, where viruses in infected ovarian tissue spread into developing eggs before being released1. This was further proven when eggs that had been surface sterilized continued to test positive for viral particles, showing that transovarial transmission exists1. The potential of a venereal-vertical transmission has been proven with the transmission of DWV, as the virus was traced from infected drones all the way to infected offspring2. Due to the detection of other viruses within the queen ovaries and eggs, it’s possible that this horizontal to vertical pathway also happens for CBPV, SBV, VDV, and BQCV2.
Table 1. Summary of all current information regarding transmission pathways for Deformed Wing Virus (DWV), Varroa Destructor Virus (VDV), Chronic Bee Paralysis Virus (CBPV), Black Queen Cell Virus (BQCV), and Sacbrood Virus (SBV). (+), transmission route confirmed; (-), no transmission pathway; (B), biological vector; (M), mechanical vector; Ve.S., suggested venereal transmission due to presence of viral particles in semen/spermatheca.
Note. Adapted from “Bee viruses: Routes of infection in Hymenoptera”, by Yañez, O., Piot, N., Dalmon, A., De Miranda, J. R., Chantawannakul, P., Panziera, D., Amiri, E., Smagghe, G., Schroeder, D., & Chejanovsky, N. (2020). Frontiers in Microbiology, 11, 943. And “Honey bee viruses and their effect on bee and colony health”, by de Miranda, J. R., Gauthier, L., Ribière, M., & Chen, Y. P. (2011). In D. Sammataro & J. A. Yoder (Eds.), Honey Bee Colony Health (pp. 71-102). CRC press.
As highlighted above (Table 1.), honeybee viruses can use multiple pathways of transmission in order to spread through a colony and cause major bee health issues. As viruses become a bigger threat to the beekeeping industry, it is crucial that beekeepers work towards understanding how these viruses are spread throughout a colony in order to control and manage them. To learn more about what to do next, follow along with the Three-Part Honeybee Virus Series. Next month’s edition of the Bee News will have “Part 3: Outlining Good Management Practices to Reduce and Mitigate Viral Infection”, where we will look into management strategies to help beekeepers control viral levels and maintain healthy bees.
Chen, Y., Evans, J., & Feldlaufer, M. (2006). Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. Journal of Invertebrate Pathology, 92(3), 152-159. https://doi.org/10.1016/j.jip.2006.03.010
Yañez, O., Piot, N., Dalmon, A., De Miranda, J. R., Chantawannakul, P., Panziera, D., Amiri, E., Smagghe, G., Schroeder, D., & Chejanovsky, N. (2020). Bee viruses: Routes of infection in Hymenoptera. Frontiers in Microbiology, 11, 943. https://doi.org/10.3389/fmicb.2020.00943
de Miranda, J. R., Gauthier, L., Ribière, M., & Chen, Y. P. (2011). Honey bee viruses and their effect on bee and colony health. In D. Sammataro & J. A. Yoder (Eds.), Honey Bee Colony Health (pp. 71-102). CRC press. https://doi.org/10.1201/b11318
Wei, R., Cao, L., Feng, Y., Chen, Y., Chen, G., & Zheng, H. (2022). Sacbrood Virus: A Growing Threat to Honeybees and Wild Pollinators. Viruses, 14(9), 1871. https://doi.org/10.3390/v14091871
Dubois, E., Reis, C., Schurr, F., Cougoule, N., & Ribière-Chabert, M. (2018). Effect of pollen traps on the relapse of chronic bee paralysis virus in honeybee (Apis mellifera) colonies. Apidologie, 49(2), 235-242. https://doi.org/10.1007/s13592-017-0547-x
Ribière, M., Olivier, V., & Blanchard, P. (2010). Chronic bee paralysis: a disease and a virus like no other?. Journal of Invertebrate Pathology, 103, S120-S131. https://doi.org/10.1016/j.jip.2009.06.013
Amiri, E., Strand, M. K., Tarpy, D. R., & Rueppell, O. (2020). Honey bee queens and virus infections. Viruses, 12(3), 322. https://doi.org/10.3390/v12030322
Traynor, K. S., Mondet, F., de Miranda, J. R., Techer, M., Kowallik, V., Oddie, M. A., Chantawannakul, P., & McAfee, A. (2020). Varroa destructor: A complex parasite, crippling honey bees worldwide. Trends in Parasitology, 36(7), 592-606. https://doi.org/10.1016/j.pt.2020.04.004