Varroa mites (Varroa destructor) are serious ectoparasites of honey bees and have been implicated in the transmission of several honey bee viral diseases (Kevan et al. 2006). Three potential roles of Varroa mites in relation to viral diseases in honey bees have been proposed: 1) Varroa mites activate latent viral infections in honey bees; 2) Varroa mites vector honey bee viruses; and 3) Varroa mites suppress the immunity of honey bees, causing them to be more susceptible to viral infection. The mites transmit viruses to their hosts through their saliva when feeding. The feeding habits of the mites, sharing and repeatedly using the same wounds (Kanbar and Engels 2005), increases the incidence and severity of infection. It is also reported that the saliva of mites may contain substances that interfere with the bee’s immune system.

A putative iridovirus infection was found in Varroa mites sampled from a moribund colony of bees in Pennsylvania (Camazine and Liu 1998). This was the first time that virus particles had been associated with the mite. Kleespies et al. (2000) also found virus-like particles in Varroa mites. Examination of mites from several parasitized colonies revealed mites with characteristic internal black-colored changes of the gut and of the fat body. In symptomatic Varroa mites, myriads of spherical virus-like particles were observed primarily in the nuclei of the fat body and muscle tissues. Similar virus-like particles were also found by Liu (1991) in the body cavity of the tracheal mite Acarapis woodi Rennie.

Bowen-Walker et al. (1999) was able to show that Varroa mites are effective vectors of deformed wing virus (DWV). First, it was proven that mites feeding on deformed bees are capable of acquiring DWV from their infected hosts when all the mites tested positive for the virus. They also discovered that a bee was more likely to die or emerge deformed if the mite feeding on it had previously fed on a dead infected bee. This would not have been possible if the mites were incapable of transmitting DWV between hosts.

Varroa mites mainly feed on the bees during their pupal stage. The mites consume bee hemolymph (blood), which may cause reduced adult body weight and protein content of the host bee. In association with DWV, some of the Varroa -parasitized pupae develop into adult bees with deformed wings, and the rest of the parasitized pupae develop into normal-winged bees, regardless of the number of parasitic mites. Under Varroa -free conditions, deformed wing virus (DWV) exists at low but detectable levels within bees without causing disease symptoms (Yang and Cox-Foster 2005).

Yang and Cox-Foster (2007) looked at the impact of Varroa mites on survivorship, viral incidence and physiological traits of newly emerged worker bees. First, by using real-time PCR (polymerase chain reaction), they showed that Varroa-parasitized bees with deformed wing symptoms all carried high levels of DWV RNA (Yang and Cox-Foster 2005, 2007). They were then able to demonstrate that Varroa mites have a significant negative impact on bee survivorship, especially following a pathogen challenge to DWV-infected bees. Mite free (MF) bees exhibited a long-time survivorship curve, normal winged (NW) bees from Varroa-parasitized colonies displayed a medium survival curve and a short survival curve was seen with deformed winged (DW) bees. It is believed that the short lifespan of DW bees is related to high levels of DWV (as demonstrated in PCR) and immunosuppression (i.e. the expression of genes encoding antimicrobial peptides and immunity-related enzymes is suppressed in Varroa-parasitized bees (Yang and Cox-Foster 2005)). Furthermore, the mite parasitized NW and DW bees lived a significantly shorter time than the MF bees after all groups were challenged with live Escherichia coli. This indicated an impaired immune response of mite-parasitized bees at whole-body level. Under Varroa-free conditions, DWV exists at low but detectable levels within bees without causing disease symptoms (Yang and Cox-Foster 2005). However, when bees are parasitized by Varroa mites, combined with an exposure to microbes, DWV can replicate to a level of 10⁵-fold higher within 10 hours, which may directly cause bee death.

Deformed-wing, mite-parasitized bees died within an average of one day, even without an E. coli challenge. This was explained by the absence of an important enzyme activity in insect immune response –phenol oxidase – which was lacking even in those bees challenged with immuno-eliciting bacteria. The lack of inducible phenol oxidase activity indicated that the DW bee’s immune system is not fully competent upon adult emergence. The gene encoding phenol oxidase in cellar immune functions is normally expressed in newly-emerged worker bees; however, the expression of this gene is suppressed at transcriptional level in the Varroa-parasitised bees (Yang and Cox-Foster 2005). Varroa parasitism also significantly reduced body weight of the parasitized bees, but body weight was not significantly correlated with the survivorship of mite-parasitized bees. In summary, the research elucidated that the combination of mite parasitization, the interaction of DWV and microbes, and a developmental immune incompetency attribute to decreased worker survivorship and have a negative impact on colony fitness.

Deformed wing virus can be transmitted horizontally during trophallaxis between colony members (Yue and Genersch 2005) or when Varroa mites feed on bee hemolymph (Bowen-Walker et al. 1999) and vertically through infected eggs and semen (Chen et al. 2006, Yue et al. 2007). Under field conditions, Varroa mites were shown to be highly effective vectors of deformed wing virus (DWV) between bees (Bowen-Walker et al. 1999). Varroa mites can also activate DWV virus replication (Shen et al. 2005). Adult female mites obtained from honey bee pupae naturally infected with DWV contained virus titers many times in excess of those found in their hosts.

To determine the roles of Varroa mites in activating or vectoring viral infections (Shen et al. 2005) performed quantitative comparison of viral infections between bees with and without mites. Under natural and artificial mite infestations, bee pupae contained significantly higher levels of Kashmir bee virus (KBV) and deformed wing virus (DWV) RNAs and KBV structural proteins than mite-free pupae. Also, DWV had amplified to extremely high titers in mite infested bee pupae. A positive correlation between the number of mites introduced and the levels of viral RNAs was found. The detection of viral RNAs in the nymph and adult mites underline the possible role of Varroa in virus transmission. However, most groups of virus-free adult mites were associated with bee pupae heavily infected by viruses, suggesting that the elevated viral titers in mite infested pupae more likely resulted from activated viral replication. Based on these observations, in addition to research demonstrating suppressed immune responses in bees infested with mites, they concluded that parasitization by varroa suppresses the immunity of honey bees, leading to activation of persistent, latent viral infection.

Recent research has shown that small hive beetles (SHB) may also be a potential biological vector of honey bee viruses. Eyer et al. (2009) studied the interaction of the beetle with the deformed wing virus (DWV). There are several different potential contamination pathways for oral uptake of honey bee viruses by the beetle. One example is that the beetles can exploit trophallaxis feeding (food/pheromone transmission between bees) within the host colonies (Ellis et al. 2002b). As a defense strategy against the SHB, honey bees construct cells of propolis into which they drive the beetles and imprison them (Neumann et al. 2001). Through behavioral mimicry, SHB can induce trophallaxis feeding from the honey bees (Ellis et al. 2002a), which is the only way for SHB to obtain food in such prisons except in rare cases of cannibalism (Neumann et al. 2001). Other potential infection avenues include: adult beetles become infected with the virus by feeding on dead adult bees with clinical symptoms, feeding on infected honey bee brood, feeding on virus contaminated pollen, and by being associated with contaminated beeswax. Viruses, once ingested by the beetles, may replicate in the SHB, similarly as they do in Varroa mites (Yue and Genersch 2005).

An illustration of DWV transmission in SHB was given in Eyer et al. 2009. Deformed wing virus was detected in adult small hive beetles that were fed dead worker bees with deformed wings (97% of the beetles), DWV-positive brood (100% of the beetles) and were associated with DWV-contaminated wax (91% of the beetles). No virus was detected in SHBs that were supplied with DWV-infected pollen and sugar water (negative control). DWV was also detected in 41% of the adult SHB after trophallaxis with infected workers. This study provides the first evidence of honey bee viruses in small hive beetles. Furthermore, SHB identified as DWV-positive, 40% of beetles carried negative stranded RNA of DWV, indicting virus replication (Eyer et al. 2009). These results suggest that small hive beetles can be infected by honey bee viruses via trophallactic transmission and have the potential of being a biological vector of honey bee viruses. The occasional incidence of adult SHB with deformed wings within honey bee colonies, suggests that natural symptomatic infections occur in the field.