If your bees have Varroa, your bees have viruses.
Authors: Philip A. Moore, Michael E. Wilson, and John A. Skinner
Department of Entomology and Plant Pathology, the University of Tennessee, Knoxville TN
Date: August 21, 2014
Varroa mites (Varroa spp.) are a ubiquitous parasite of honey bee (Apis spp.) colonies. They are common nearly everywhere honey bees are found, and every beekeeper should assume they have a Varroa infestation, if they are in a geographic area that has Varroa (Varroa mites are not established in Australia as of spring 2014). Varroa mites were first introduced to the western honey bee (Apis mellifera) about 70 years ago after bringing A. mellifera to the native range of the eastern honey bee (Apis cerana). Varroa mites (Varroa jacobsoni) in eastern honey bee colonies cause little damage. But after switching hosts and being dispersed across the world through natural and commercial transportation of honey bee colonies, Varroa has became a major western honey bee pest since the 1980’s. Varroa mites (Varroa destructor) are now the most serious pest of western honey bee colonies and one of the primary causes of honey bee decline (Dietemann et al. 2012). A western honey bee colony with Varroa, that is not treated to kill the pest, will likely die within one to three years (Korpela et al. 1993; Fries et al. 2006).
Varroa mites attack honey bee colonies as an external parasite of adult and developing bees, by feeding on hemolymph (fluid of the circulatory system similar to blood), spreading disease, and reducing their lifespan. Evidence suggests that Varroa and their vectored viruses affect the immune response of honey bees, making them more susceptible to disease agents (Yang and Cox-Foster 2005). For more information on this topic see here. Mature female Varroa mites survive on immature and adult honey bees (worker, drone, and rarely queen), are reddish brown, and about the size of a pin head. Male mites are a smaller size and tan color, do not feed on bees, and are only found inside brood cells (Rosenkranz et al. 2010).
Varroa have two life stages, phoretic and reproductive. The phoretic stage is when a mature Varroa mite is attached to an adult bee and survives on the bee’s hemolymph. During this stage the mite may change hosts often transmitting viruses by picking up the virus on one individual and injecting it to another during feeding. Phoretic mites may fall off the host, sometimes being bitten when bees groom each other, or it may die of old age. Mites found on the bottom board of the hive or that fall though a screen bottom board are called the “natural mite drop”. But these mites that fall off of bees represent a small portion of the total mite population because the reproductive mites are hidden under cell cappings.
The reproductive life stage of Varroa begins when an adult female mite is ready to lay eggs and moves from an adult bee into the cell of a developing larval bee. After the brood cell is capped and the larva begins pupating, the mite begins to feed. After about three days from capping, the mite lays its eggs, one unfertilized egg (male) and four to six fertilized (female) eggs (Rosenkranz et al. 2010). After the eggs hatch, the female mites feed on the pupa, mate with the male mite and the surviving sexually mature female mites stay attached to the host bee when it emerges as an adult. It takes six to seven days for a female mite to mature from egg to adult and it can live two to three months in the summer and five to eight months in the fall. Only mature female mites can survive outside of a brood cell (the phoretic stage), and on average a mite will produce 1.2 viable mature female offspring per worker cell invaded (Schulz 1984; Fuchs & Langenbach 1989). However, since the development time is longer for drone brood, the average viable offspring for a mite in a drone cell increases to 2.2 per cell invaded (Schulz 1984; Fuchs & Langenbach 1989). For more on Varroa life history see here.
One of the serious problems caused by Varroa is the transmission of viruses to honey bees which cause deadly diseases. Viruses found in honey bees have been known to scientists for 50 years and were generally considered harmless until the 1980’s when Varroa became a widespread problem. Since then, nearly twenty honey bee viruses have been discovered and the majority of them have an association with Varroa mites, which act as a physical and or biological vector (Kevan et al. 2006). Therefore controlling Varroa populations in a hive will often control the associated viruses and finding symptoms of the viral diseases is indicative of a Varroa epidemic in the colony. Viruses are however, the least understood of honey bee diseases. Emerging information of honey bee viruses continue to alter our understanding of the role viruses play in honey bee colonies (Genersch and Aubert 2010).
Viruses are microscopic organisms that consist of genetic material (RNA or DNA) contained in a protein coat. Viruses do not acquire their own nutrients or live independently, and can only multiply within living cells of a host. An individual virus unit is called a virus particle or virion and the abundance of these particles in a host is called the virus titer. A virus particle injects itself in to a host cell and uses the cells’ organelles to make copies of itself. This process will continue without obvious change to the cell, until the host cell becomes damaged or dies, releasing large amounts of infective virus particles. All forms of life are attacked by viruses and most are host specific.
Viruses of the honey bee typically infect the larval or pupa stage, but the symptoms are often most obvious in adult bees. Many of these viruses are consumed in pollen or the jelly produced by nurse bees that are fed to developing bees. Many viruses are also transmitted by Varroa. Varroa, when feeding on the hemolymph transfer the viruses directly into the open circulatory system, which reaches every cell in the insect body.
Honey bee viruses are not limited to honey bees. Honey bee viruses have been found in other non-Apis bee species, other colony inhabitants like small hive beetle, and in pollen and nectar (Andersen 1991; Bailey and Gibbs 1964; Genersch et al. 2006; Singh et al 2010). For more on honey bee pathogens found in native bees see here. Transfer of honey bee viruses from infected colonies to non-infected individuals or colonies can occur during foraging on common flowers or through robbing of weak or collapsed colonies (Singh et al 2010).
Identification of a virus is difficult due to the small size of particles. Expensive and often uncommon laboratory equipment is required for accurate diagnosis. However, symptoms of some viral diseases are more visible, especially with overt infection. A lack of symptoms does not rule out the presence of a virus. Viruses can remain in a latent form within the host, acting as a reservoir of infection, complicating diagnosis and control, and only becoming an outbreak when conditions are right.
The USDA-APHIS National Honey Bee Pests and Diseases Survey has taken samples from honey bee colonies in over 27 states since the year 2009. Data from these surveys and other data are complied into a database with the Bee Informed Partnership and used to determine baseline disease level, determine the absence of exotic honey bee pests that have not yet been found in America, and to gauge the overall health of U.S. honey bee colonies. Results of virus presence from the 2013 survey are below (Figure 1). Deformed wing virus (DWV) and Black queen cell virus (BQCV) were present in over 80% of sampled colonies. Other viruses were much less common, but still present in 10-20 percent of colonies sampled. Of the viruses tested for presence, only slow bee paralysis virus (SBPV) was not found in the U.S
Sacbrood, a disease cause by a virus, was the first honey bee virus to be discovered in the early 20th century and now has a recognized widespread distribution. It is perhaps the most common honey bee virus (Shen et al. 2005). This disease has been found in adult, queen, egg, and larval bees, in all forms of food, and in Varroa mites, suggesting a wide range of transmission routes. Although it is commonly found without serious outbreak, sacbrood is more likely to cause disease when the division of labor is less defined, in the early parts of the year before the nectar flow, or during prolong dearth (Bailey 1981). It often goes unnoticed since it usually infects only a small portion of brood, and adult bees will usually detect and remove infected larvae.
The disease causes larvae to fail to shed their final skin prior to pupation, after the larva has spun its cocoon. Infected larvae remain on their back with their head towards the cell capping. Fluid accumulates in the body and the color will change from pearly white to pale yellow, with the head changing color first. Then, after the larva dies, it becomes dark brown with the head black (Image 2). Larvae that have ingested sufficient quantities of sacbrood in their food die after being sealed in their comb.
Sacbrood multiplies in several body tissues of young larvae but these larvae appear normal until cell capping. Each larva that dies from sacbrood contains enough virus particles to infect every larva in 1000 colonies (Bailey 1981). But in most instances, diseased larvae are quickly removed in the early stages of the disease by nurse bees. The cell cappings are first punctured to detect the disease, which a good sign of infection for the beekeeper look for (Image 6). Then, young worker bees remove the diseased larvae from the colony. Adult bees, although not susceptible to infection, become a harbor as the virus collects in the bee’s hypopharyngeal glands, which are used to produce larval jelly (Bailey 1981). These infected adult bees, however, cease to eat pollen and soon stop tending larvae. They will become foragers more quickly in life than usual and tend to collect nectar instead of pollen (Bailey 1981). Nectar that contains the virus becomes diluted in the colony when mixed with nectar from other foragers. Whereas pollen, is collected and compacted into the “pollen basket” and deposited intact into a cell. Dilute virus containing nectar is less likely to cause infection than when the virus is concentrated in a pollen pellet. Therefore use caution when transferring frames with pollen among colonies. Little is known of the other transmission routes: through Varroa mites, between workers, from bee feces or through transovarial transmission (from queen to egg). Sacbrood usually subsides in late spring when the honey flow begins, but if symptoms persist, requeening with hygienic stock is recommended (Frazier et al. 2011).
Deformed wing virus is common, widely distributed, and closely associated with Varroa mites. Both the virus titers and prevalence of the virus in colonies are directly linked to Varroa infestations (Bowens-Walker et al. 1999). In heavily Varroa infested colonies, nearly 100 percent of adult workers may be infected with DWV and have high virus titers even without showing symptoms (de Miranda et al. 2012). DWV is strongly associated with winter colony mortality (Highfield et al 2009; Genersch et al 2010). Control of DWV is usually achieved by treatment against Varroa, After treatment a gradual decrease in virus titers occurs as infected bees are replaced by healthy ones (Martin et al 2010). DWV can be found in all castes and life stages of honey bees and will persist in adults without obvious symptoms. DWV is also transmitted through food, feces, from queen to egg, and from drone to queen (de Miranda et al. 2012).
Acute infections of DWV are typically linked to high Varroa infestation levels (Martin et al 2010). Covert infections (a detectable level of virus without damaging symptoms) can occur through transovarial transmission (Chen et al. 2004), and through larval food (Chen et al. 2006). Symptoms noted in acute infections include early death of pupae, deformed wings, shortened abdomen, and cuticle discoloration in adult bees, which die within 3 days causing the colony to eventually collapse. Not all mite infested pupae develop these symptoms, but all adult honey bees with symptoms develop from parasitized pupae. Bees infected as adults can have high virus titers but do not develop symptoms. DWV may also affect aggression (Fujiyuki et al. 2004) and learning behaviors of adult bees (Iqbal and Muller 2007). DWV appears to replicate in Varroa, making it a biological as well as physical vector. Infection of pupae may be dependent on DWV replication in Varroa prior to transmission. Winter colony mortality is strongly associated with DWV presence, irrespective of Varroa infestation. This suggests that Varroa infection should be reduced in a colony far in advance of producing overwintering bees, to ensure reduction in DWV titers. DWV is closely related to Kakugo Virus and Varroa destructor Virus 1, which together form the Deformed Wing Virus Complex (de Miranda et al. 2012).
Black queen cell virus is a widespread and common virus that persists as asymptomatic infections of worker bees and brood. Although generally understood as being asymptomatic in adult bees, Shutler et al. (2014) found BQCV to be associated with the symptom K-wing, where the wing pair is disjointed and more perpendicular to one another. Queen pupae with symptoms display a pale yellow sac-like skin similar to sacbrood. The pupae rapidly darken after death and turn the wall of the queen cell dark brown to black. Symptomatic drone pupae have also been observed. Unlike other viruses that are associated with Varroa, BQCV is strongly associated with Nosema apis and little evidence supports its co-occurrence with Varroa, although, BQCV has been isolated from Varroa (Ribière et al. 2008). Nosema disease affects a bee’s mid gut, increasing susceptibility of the alimentary tract to infection by BQCV. BQCV can be orally transmitted to adults only when Nosema has co-infected (Ribière et al. 2008). It can also be transmitted by injection to pupae. BQCV has a seasonal relationship similar to Nosema, with a strong peak in spring. Because of the seasonal occurrence with Nosema, queen rearing operations who produce queens in the spring are susceptible to BQCV (Ribière et al. 2008).
Chronic bee paralysis virus was one of the first honey bee viruses to be isolated. It is unique among honey bee viruses in that it has a distinct particle size and genome composition. It is also the only common honey bee virus to have both visual behavior and physiological modifications resulting from infection. Symptoms of the disease are observed in adult bees displaying one of two sets of symptoms called syndromes (Genersch & Aubert 2010). Type 1 symptoms include trembling motion of the wings and bodies of adult bees, who are unable to fly, and crawl along the ground or up plant stems, often clustering together. The bees may also have a bloated abdomen, causing dysentery and will die within a few days after displaying symptoms.
Type 2 symptoms are greasy, hairless, black adult bees that can fly, but within a few days, become flightless, trembling, and soon die (Image 5). Both of these syndromes can occur within the same colony. Severely affected colonies, often the strongest in an apiary (Ribiere at al. 2010), quickly lose adult workers, causing collapse and often leaving few adult bees with the queen on unattended comb (Bailey & Ball 1991). These symptoms, however, are similar and often confused with other honey bee maladies including Nosema apis, colony collapse disorder (CCD), tracheal mites, chemical toxicity, and other viruses.
Transmission of the virus primarily occurs through direct body contact, although oral transmission also occurs but is much less virulent. Direct body transmission happens when bees are either crowded or confined within the hive for a long period of time (due to poor weather or during long-distance transportation) or when too many colonies are foraging within a limited area, such as a monoculture of sunflower with high honey bee colony density (Genersch & Aubert 2010). In both instances, small cuts from broken hairs on an adult bee’s cuticle and direct contact with infected adult bees spreads the virus through their exposed pores; if this occurs rapidly and enough adult bees are infected, an outbreak with colony mortality will occur. Feces from infected bees within a colony can also spread the disease, and other transmission routes are still being investigated, including possible Varroa transmission. The virus is widespread and an outbreak can occur at any time of year. Spring and summer are the most common seasons for mortality from the virus, but it will persist in a colony year-round without displaying any overt symptoms (de Miranda et al. 2012).
Two new viruses related to CBPV with no yet described symptoms are Lake Sinai virus 1 (LSV1) and Lake Sinai virus 2 (LSV2) (Runckel et al. 2011). New molecular tools have allowed researchers to identify the presence of these and other new viruses and their seasonality in test colonies. Little else is know of the Lake Sinai viruses, including its pathogenic or epidemiological significance. Other described honey bee viruses that were discovered before the advent of molecular techniques have no genomic data to reference; therefore newly discovered viruses may in fact be the already discovered viruses of the past such as Bee virus X and Y, Arkansas Bee Virus or Berkeley Bee Virus (Runckel et al. 2011).
Acute bee paralysis virus (ABPV), Kashmir bee virus (KBV), and Israel acute paralysis virus (IAPV) are a complex of associated viruses with similar transmission routes and affect similar life stages. These viruses are widespread at low titers and can quickly develop high titers due to extremely virulent pathology. Frequently associated with colony loss, this virus complex is especially deadly when colonies are heavily infested with Varroa mites. (Ball 1989; Genersch 2010, Genersh et al. 2010). These viruses have not been shown to cause symptoms in larval life stages, but show quick mortality in pupae and adult bees.
Acute bee paralysis virus was accidentally discovered when CBPV was first isolated. ABPV displays similar symptoms as CBPV however the acute adjective describes a bees’ more rapid mortality compared to CBPV. Unlike CBPV, ABPV virulence is directly related to Varroa infestation. APBV is transmitted in larval jelly from asymptomatic infected adult bees to developing larva or when vectored by Varroa mites to larvae and pupae. ABPV is common and typically cause covert infections (no obvious symptoms) when transmitted orally from adult to developing bee. It takes about one billion viral particles to cause death via ingestion, but when vectored by Varroa and directly injected into the developing bee’s hemolymph, only 100 virus particles will cause death (Genersch & Aubert 2010). When the virus is picked up by Varroa, the transmission rate to pupae is between 50 and 90 percent. The longer the feeding period of Varroa, the greater the transmission rate will become. (Genersch & Aubert 2010). Pupae infected with ABPV die before emerging, making the appearance of paralysis symptoms less obvious. The decline in emerging bees causes a colony to dwindle towards collapse. A colony infected with an ABPV epidemic will die within one season (Sumpter and Martin 2004).
Kashmir bee virus has widespread distribution and is considered the most virulent of honey bee viruses under laboratory condition (Allen and Ball 1996). When KBV is injected in to adult bee hemolymph, death occurs in just 3 days (de Miranda et al. 2012). KBV does not cause infection when fed to developing bees, but does persist in adult and developing bees without any obvious symptoms. When Varroa mites transmit the virus, it becomes deadly to all forms of the bee lifecycle but displays no clearly defined symptoms. Even with moderate levels of mite infestation, KBV, like ABPV, can kill colonies (Todd et al. 2007). Control of Varroa mites is necessary to prevent colony losses from KBV.
Symptoms of IAPV are similar to ABPV and CBPV including: shivering wings, darkened hairless abdomens and thoraxes, progressing into paralysis and death. IAPV is found in all life stages and castes of bees. IAPV and other viruses were found to be strongly associated with colony collapse disorder (CCD) in the United States, but no direct relationship between the viruses and CCD has yet been shown (Cox-Foster et al. 2007). IAPV is extremely virulent at high titers, as when vectored by Varroa and is covert at low titers.
In contrast to ABPV, which produces symptoms in a few days after infection, SBPV induces paralysis after 12 days, and only on the two fore (anterior) legs. SBPV persists as a covert infection and is transmitted by Varroa to adults and pupae. The disease will kill adult bees and eventually the entire colony (de Miranda et al. 2012). Prevalence of the virus is limited. It has not been found in the U.S., but has been found in England, Switzerland, Fiji and Western Samoa and only in Britain has SBPV been associated with colony deaths (Carreck et al. 2010).
Most pathogens invade the digestive system through oral ingestion of inoculated food. These pathogens infect the mid gut epithelial cells, which are constantly being replaced and are protected by membranes and filters which confine the pathogen to gut tissues. Parasites that infect gut tissue like Nosema apis and Nosema cerana can create lesions in the epithelium that allow a virus like BQCV to pass into the hemolymph and infect other cells in the body. In contrast the external parasite Varroa destructor feeds directly on bee hemolymph providing an opening in the cuticle for viruses to enter. Most virus infections rarely cause infection when ingested orally, but only a few virus particles are necessary to cause infection when injected directly into the hemolymph. Many viruses can be directly transmitted by Varroa mites, such as: DWV, those in the acute bee paralysis virus complex, and slow bee paralysis virus. Other viruses, like sacbrood, have been detected in Varroa mites but Varroa has not been shown to directly transmit the virus. Some viruses, like DWV, have been shown to directly multiply in Varroa mites, however in most cases we don’t know the exact relationship of Varroa mites to viruses or enough about how transmission occurs from mites to bees. Knowledge about the presence, role, and transmitting routes of these viruses in native bees, and other potential non-Varroa transmission routes is also lacking in detail, complicating recommendations for control. Research does show viruses clearly affect honey bee health and warrant attention from the beekeeper and researcher alike.
Viruses persist in normal, healthy colonies, only to explode during times of stress. Many viruses are only damaging when in combination with another stressor like Varroa or Nosema. Active, integrated management of Varroa and other stressors is essential to minimizing virus titers. To learn more about reducing stressors with best management practices see here.
Routinely inspect your colonies for possible disease. Have a thorough knowledge of symptoms and identify when colonies are slow to build up or have sporadic brood patterns, indicating brood has been pulled out and removed (Image 6). If you suspect you have a disease, take a sample and send it to be identified. For more information on submitting a sample for diagnosis see here.
Other future avenues of control include breeding hygienic bee strains that detect brood diseases and remove infected individuals from colonies or breeding of resistance to Varroa infestation. Specific resistance to viruses are not yet considered in most breeding programs. There is evidence of specific viral resistance in honey bees, and there has been at least some attempt to breed resistance to IAPV. For more on this topic see here.
Another promising research area for controlling honey bee viruses in the use of gene silencing called RNAi. The private bee research company Beeologics, as well as public and private university researchers are developing this method and a consumer product may be available in the near future as RNAi technology continues to become more efficient and inexpensive. For more on this topic see here.
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