Honey Bee Viruses

Yan Ping Chen1,*; Reinhold Siede †,‡judy.chen@ars.usda.gov    * USDA‐ARS, Bee Research Laboratory, Beltsville, Maryland 20705
† Landesbetrieb Landwirtschaft Hessen, Bieneninstitut Kirchhain, 35274 Kirchhain, Germany
‡ Institute of Virology, Justus Liebig University, 35392 Giessen, Germany
1 To whom correspondence should be addressed.

I Introduction

The honey bee, Apis mellifera L. (Hymenoptera: Apidae), is found all over the world and plays an important role in the global economy by assisting in the pollination of a wide variety of food crops and by producing honey, beeswax, pollen, propolis, royal jelly, and other hive products. To ensure an adequate supply of bees for the pollination of agricultural crops and the production of hive products, a healthy and vigorous population of honey bees will be essential. However, like other animals, honey bees are inevitably subject to infection by a wide variety of pathogens that are responsible for significant colony losses. Among honey bee pathogens, viruses pose one of the major threats to the health and well‐being of honey bees and have caused serious concerns for researchers and beekeepers.

Viruses were first identified as a new class of pathogens infecting honey bees when a US scientist, Dr. White, discovered that a filterable agent from diseased bee larvae could cause sacbrood disease in the honey bee (White, 1913). Since then, at least 18 viruses have been reported to infect honey bees worldwide (Allen and Ball, 1996; Ellis and Munn, 2005). Although knowledge of honey bee viruses is still limited compared to that of other well‐studied insect viruses, such as baculoviruses, understanding of virus infections in honey bees has grown considerably over the last three decades and a body of literature dealing with bee virus identification, physiochemical properties, natural history, transmission, incidence, and pathology has been accumulated. In this chapter, we describe recent progress in understanding morphology, genome organization, transmission, epidemiology, and pathogenesis of honey bee viruses as well as their interactions with their honey bee host. Infections of viruses in honey bees have been reviewed previously. The main goal of this chapter is to update previous findings with more recent work relating to the molecular biology of the honey bee viruses, however, some main features of earlier reviews: Bailey, 1976, 1981, 1982a; Bailey and Ball, 1991; Ball, 1996; Ball and Bailey, 1991, 1997.

II Common Honey Bee Viruses

Viruses could attack at different developing stages and castes of the honey bees, including eggs, larvae, pupae, adult worker bees, adult drones, and queen of the colonies. Although bee viruses usually persist as inapparent infections and cause no overt signs of disease, they can dramatically affect honey bee health and shorten the lives of infected bees under certain conditions (Ball and Allen, 1988; Martin, 2001). Of 18 viruses identified to attack honey bees, six viruses, namely, Deformed wing virus (DWV), Black queen cell virus (BQCV), Sacbrood virus (SBV), Kashmir bee virus (KBV), Acute bee paralysis virus (ABPV), and Chronic bee paralysis virus (CBPV) are the most common infections and have been objects of active research currently.

A Deformed wing virus

DWV was first isolated from diseased adult bees in Japan (Bailey and Ball, 1991). The occurrence and distribution of DWV has since been worldwide. Except for Oceania, the infection of DWV so far has been reported in Europe, North America, South America, Africa, Asia, and the Middle East (Allen and Ball, 1996; Antúnez et al., 2006; Ellis and Munn, 2005). The infection of DWV has also been identified in A. cerana in China (Bailey and Ball, 1991).

DWV is one of a few bee viruses that cause well‐defined disease symptoms in infected bees. Typical disease symptoms of DWV infection include shrunken, crumpled wings, decreased body size, and discoloration in adult bees. However, the mechanism by which the DWV causes the morphological deformities of the infected hosts is unclear. Aside from the adult stage, DWV infection is also detected in other stages of bee development, including egg, larvae, and pupae. When pupae at the normally multiplies slowly and rarely kills the pupae, instead mostly causing deformity and early death in newly emerged adult bees. Adult honey bees infected with DWV usually appear normal but are believed to have a reduction in life span (Bailey and Ball, 1991; Ball and Bailey, 1997; Kovac and Crailsheim, 1988).

DWV appears to be the most prevalent infection in A. mellifera in recent years. Our 5‐year field survey carried out in Beltsville, MD showed that DWV infection occurred in 100% of the apiaries investigated (Y. P. C., unpublished observation). Similar results were reported previously by Tentcheva et al. (2004b) who observed that DWV was detected in over 97% of French apiaries when the adult bee population was examined. A study on the prevalence and distribution pattern of viruses in Austria demonstrated that DWV was present in 91% of tested bee samples (Berényi et al., 2006). Although high prevalence of DWV is not geographically related, some seasonal variation in virus incidence was observed and the frequency of DWV infection in both adult bees and pupae increased considerably from summer to autumn during the year (Tentcheva et al., 2004a,b). The striking high incidence of DWV infection in honey bees obtained from these studies indicate that DWV is prevalent over a wide range of geographic locations and is likely to become an important cause of mortality in honey bee colonies whenever a viral disease outbreak occurs, and warrants further investigation in the epidemiology and pathogenesis of this pathogen.

Bee colonies infected with DWV are often found to be associated with the infestation of a parasitic mite, Varroa destructor (Anderson and Trueman, 2000). Both laboratory and field studies showed that the varroa mite is an effective vector of the DWV (Ball and Allen, 1988; Bowen‐Walker et al., 1999; Martin et al., 1998; Nordström, 2003; Nordström et al., 1999; Shen et al., 2005b). Varroa mites acquire the virus from infected bees and transmit it to uninfected bees, which either develop morphological deformities or die after the mites feed on them for a period of time. Studies of virus status in varroa mites showed that DWV was present in 100% of varroa mites collected from Thailand (Chantawannakul et al., 2006) and that varroa mites appeared to be DWV positive in 100% of French apiaries (Tentcheva et al., 2004b). Evaluation of DWV infection in individual bees showed that DWV was detected in 69% of bees collected from mite‐infested colonies in Poland (Topolska et al., 1995), and in over 90% of bees from mite‐infested colonies in England (Ball, 2001). The high frequency of DWV in mites and mite‐infested bee colonies suggests that the significant increase in prevalence of DWV infection in recent years is likely associated with the worldwide infestation of varroa mites in honey bees. It also suggests that the varroa mite may play a major role in colony collapse due to the outbreak of viral disease.

B Sacbrood virus

SBV is the most widely distributed of all honey bee viruses. Since its first identification in the United States in 1913 (White, 1913), infection of SBV has been found on every continent where A. mellifera honey bees are present (Allen and Ball, 1996; Bradbear, 1988; Ellis and Munn, 2005).

SBV attacks both brood and adult stages of bees, but larvae about 2‐day old are most susceptible to SBV infections (Ball and Bailey, 1997). SBV affects adult bees without causing obvious signs of disease, but the infected adult bees may have a decreased life span (Bailey, 1969; Bailey and Fernando, 1972). The initial spread of SBV within a colony occurs when nurse bees become infected while removing larvae killed by SBV. Virus particles accumulate in the hypopharyngeal...