THE ROLE OF DEFORMED WING VIRUS IN THE MORTALITY OF VARROA INFESTED HONEYBEE COLONIES
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1 THE ROLE OF DEFORMED WING VIRUS IN THE MORTALITY OF VARROA INFESTED HONEYBEE COLONIES Stephen Martin, Brenda Ball l, Norman Carreck'' ILaboratory of Apiculture and Social Insects, Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S 10 2TN, UK. 2Plant and Invertebrate Ecology Division, Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK. ABSTRACT The parasitic mite Varroa destructor has become the most economically important pest of the western honey bee, Apis mellifera. Long term studies undertaken in the UK have revealed that deformed wing virus (DWV), a naturally occurring bee virus, in association with the mite is now the cause of the majority of honey bee colony deaths ascribed to V. destructor. Many of the symptoms previously associated with the mite such as deformed wings, patchy brood patterns and reduced honey bee longevity, can now be explained by the natural history of DWV. The role of V. destructor is primarily as a virus vector. Once DWV is introduced into the haemolymph of parasitised individuals via the feeding activities of the mites, it multiplies rapidly, producing an overtly infected bee. This causes reduced brood survival and wing deformity in some, but not ali infected newly emerging individuals. Those that do survive have a significantly reduced longevity. Adult bees which become infected after they have emerged appear do not show such a marked reduction in longevity and act as reservoirs of DWV infection allowing mites an opportunity to reacquire and transmit the virus to other adult bees and brood The prevalence and persistence of DWV in colonies which were either treated with acarcide or allowed to die was also determined. This revealed that the number of overtly infected adult bees was greater than the number of mite infested bees, whilst the converse was found in the sealed brood. To ensure colony survival in temperate regions, mites must be removed prior to the production of the over-wintering bee population to minimise overt DWV infection in the newly emerging bees. Keywords: varroa, deformed wing virus, colony death, virus vector, virus persistence INTRODUCTION Although the parasitic honey bee mite Varroa destructor has been the subject of intensive study during the past 50 years, the true role of the mite in the death of millions of honey bee (Apis mellifera) colonies is only just being revealed. A central problem has been the lack of a clear relationship between the size of the mite population and when or if the infested colony dies. Honey bee colonies have often appeared healthy despite hosting large (1000's) mite populations, especially during the initial phase of spread into a region. For example, in South Africa mite populations in both A. m. scutellata and A. m. capensis 1
2 colonies were regularly reported to exceed in apparently healthy colonies (Allsopp, 1998; Allsopp, 2000). This is a paradox since it has been estimated that only mites are needed to either kill or cause severe economic damage to a colony of A. mellifera (Martin, 1999; Hood and Delaplane, 2001). A solution to this paradox could be provided by the involvement of an unknown third party. A prime candidate may be one or more of the many honey bee pathogens (e.g. viruses, bacteria, fungi etc.) which are known to occur naturally in honey bee populations (Bailey and Ball, 1991). Batuev (1979) found that dead bees from colonies severely infested with V. destructor contained large amounts of a naturally occurring bee pathogen called acute paralysis virus (APV) and that mites were able to vector APV between adult bees. Normally APV resides as an inapparent infection in the bee, and only extremely rarely multiplies sufficiently to kill (Bailey et al., 1981). Studies in Germany (Ball and Allen, 1988) and the USA (Hung et al., 1995) also found large amounts of APV in dead bees and brood from infested colonies. Further studies (Ball, 1997; Hung, et al., 1995; Martin et al., 1998; Nordstrom, 2000) revealed three more honey bee viruses which appeared to be associated with colonies infested by V. destructor. These were: deformed wing virus (DVW), Kashmir bee virus (KEV) and slow paralysis virus (SPV). It is known that DWV can cause wing deformity if injected into developing bee pupae (Bailey and Ball, 1991) and wing deformity has long been associated world-wide with colonies infested by V. destructor (Smimov, 1978; De long et al., 1982; Koch and Ritter, 1991), although such malformation has normally been attributed to the direct effects of mite feeding. Furthermore, DWV has been shown to be vectored by V. destructor (Ball, 1989; Bowen-Walker et al., 1999; Nordstrom, 2000), making it the prime candidate for further investigation. MA TERIALS AND METHODS VIRUS ASSAY DWV was detected in all individual bees, brood and mites using an indirect ELISA (AlIen et al., 1986) which has a detection limit of around 107 viral particles per ml., so only overt, and not inapparant DWV infections could be detected. PRELIMINARY SMALL CAGE STUDIES Two preliminary studies were conducted using small cages (Bailey and Ball, 1991; Fig. 34b) into which c. 30 adult bees from non-infested or acaricide treated colonies i.e. suspected of being free from DWV, were introduced. Then, either mites or marked worker honey bees from severely infested colonies were introduced into some of the cages containing bees. The cages were supplied with sugar syrup, water, poljen, and maintained at 30 C in a dark incubator. Cages were checked daily, and any dead bees or dead mites removed for virus analysis. RESULTS SMALL CAGE STUDY 1 Two groups of five marked bees from a severely infested colony were introduced into cages containing either 25 or 19 adult bees from a non-infested colony. After ten days none of the 44 bees from the non-infested colony had DWV that was detectable by ELlS A, despite having been in close contact with the ten marked bees, all of which contained large amounts of DWV. This was the first preliminary indication that bee to bee transmission of 2
3 overt DWV may not be occurring over a short time period. In addition, there was no significant difference between the mortality (p < 0.2, unpaired t-test) of DWV infected and non-infected honey bees over the ten day period, nor the non-infested honey bees caged separately at the same time. SMALL CAGE STUDY 2 In the control cage no mites were introduced, and DWV was detected in seven of the 31 (22%) bees, reflecting the background level of overt DWV infection in adult bees from the source colony. In the other cage 25 mites were introduced, of which 21 were subsequently determined to be carrying DWV. The percentage of honey bees with overt DWV infection then increased to 65% (13 out of 20), as expected. However, although the number of adult bees in which DWV was detected increased in one group their survival remained similar to the control group over the 29 day study period (Fig. 1). Figure 1. Survival curves of bees maintained in small cages which either had a small (22%) (solid line) or a large (65%) (dashed line) percentage of worker bees overtly infected with DWV. 100'-~.g 30 <C o Time (days) DISCUSSIO These two preliminary tests support previous findings (Ball, 1989; Bowen-Walker et al., 1999; Nordstrom, 2000) that adult female V. destructor mites transfer DWV between adult bees much more efficiently than do adult bees. This is primarily due to the mode of transmission and route of infection. For example, Bailey and Gibbs (1964) showed that only 102 particles of APV injected directly into the bee's haemolymph causes an overt infection but 1011 particles are needed to cause infection by feeding. Some other bee viruses, such as cloudy wing virus (CWV) do not multiply by injection into the haemolymph of adult bees (Bailey et al., 1981) and are therefore, unlikely to be transmitted by V. destructor (Nordstrom et al., 1999; Carreck et al., 2001) in the same 3
4 manner as APV and DWV. Therefore, it is important to realise that although many honey bee viruses are similar in physical size and shape they each have a very different and distinct natural history, so generalisations are difficult to make. Another major difference between overt APV and DWV infections is their effect on the longevity of honey bees. In the cage studies, during the short period of observation, there was no detectable difference in the survival of DWV infected and non-infected adult bees. However, the ability of DWV infected adult bees to act as fully functional members of the colony remains undetermined. By contrast, young adult bees injected with APV die within three to five days (Ball, 1985). Nevertheless, systemically infected adult bees can act as reservoirs of virus for mites to acquire and transmit, increasing the chances of a virus epidemic being established within the colony. Adult bees infected with APV will be rapidly lost from the population, whereas bees infected with DWV will survive and persist within the colony for some time. As a consequence, fewer mites will be needed to sustain overt DWV infection within the bee population (Martin, 2001). Using a series of differential equations the dynamics of an APV and a DWV virus epidemic in a honey bee colony infested with V. destructor, has been studied (Sumpter and Martin, 2003). This revealed that during the summer months a minimum of c mites vectoring DWV are required to sustain an overt DWV infection within a colony, whereas during the autumn period this number falls to c.700 (Sumpter and Martin, 2003). By comparison c.12300, mites vectoring APV are required to sustain an overt infection within a colony in the summer, which falls to c mites during the autumn (Sumpter and Martin, 2003). However, the ultimate fate of a colony in which either APV or DWV becomes an established infection will also depend on other factors such as colony size, time of year etc. (Martin, 2001). The predicted large mite populations needed to sustain a mite-vectored APV epidemic combined with the very low incidence of overt infections of APV (Bailey et ai., 1981) may explain why so few occurrences of APV in V. destructor infested colonies have been reported. Also, the relatively small number of mites needed to sustain a DWV epidemic and the large number of live adult bees which act as a persistent virus reservoir within colonies, help to explain the increased prevalence of DWV since the arrival of Varroa in the UK (Carreck, et ai., 2001). ACKNOWLEDGEMENTS This work was funded by the Department for Environment, Food and Rural Affairs. Rothamsted Research receives grant aided support from the Biotechnology and Biological Sciences Research Council. REFRE CES Allen M.F., Ball B.V., White R.F., Antoniw J.F. (1986) The detection of acute paralysis virus in Varroajacobsoni by the use of a simple indirect ELISA. J. Apic. Res. 25, Allsopp M.H. (1998) Survey for Varroa jacobsoni in South Africa. S. Afr. Bee J. 70, Allsopp M. H. (2000) A Varroa update. South African Bee J. 72,
5 Bailey L., Gibbs A.J. (1964) Acute infection of bees with paralysis virus. J. Insect Path. 6, Bailey L., Ball B.Y. (1991) Honey bee pathology. Academic Press, London. Bailey L., Ball B.Y., Perry, J.N. (1981) The prevalence of viruses of honey bees in Britain. Ann. Appl.Biol. 97, Ball B.V. (1985) Acute paralysis virus isolates from honey bee colonies infested with Varroajacobsoni. J. Api. Res. 24, Ball B.V. (1989) Varroa jacobsoni as a virus vector. In Present status of varroatosis in Europe andprogress in the Varroa mite control (ed. Cavalloro, R.), pp E.E.C., Luxembourg. Ball B.V. (1997) Varroa and viruses. In Varroa! Fight the Mite (ed. Munn, P. and Jones, R.)mRA, UK. Ball B.V., Alien, M. (1988) The prevalence of pathogens in honey bee (Apis mellifera) colonies infested with the parasitic mite Varroa jacobsoni. Annals Appl. Biol, 113, Batuev Y.M. (1979) [New information about virus paralysis in Russia.] Pchelovodstvo 7, Bowen-Walker P.L., Martin SJ., Gunn A. (1999) The transmission of deformed wing virus between honeybees (Apis mellifera) by the ecto-parasitic mite Varroa jacobsoni Oud. J. Invert. Path. 73, Carreck N.L., Ball B.V., Wilson J.K (2001) Virus succession in honey bee colonies infested with Varroa destructor. Proc. 37th Int. Apic. Congr., 28 Oct - 1 Nov 2001, Durban, South Africa. De Jong D., De Jong P.H., Goncalves L.S. (1982) Weight loss and other damage to developing worker honey bees (Apis mellifera) due to infestation with Varroa jacobsoni. J. Apic. Res. 21, Hood M.W., Delaplane KS. (2001) Treatment thresholds for Varroa mites. In Mites of the honey bee (eds.webster, T. C. and Delaplane, K S.), pp Dadant publication, USA. Hung A.C.F., Adams J.R., Shimanuki H. (1995). Bee parasitic mite syndrome (ll): The role of Varroa mite and viruses. Am. Bee J. 135, Koch W., Ritter W. (1991) Experimental examinations concerning the problem of deformed emerging bees after infestation with Varroa jacobsoni. J. Vet. Med. B 38,
6 Martin SJ. (1999) Population modelling and the production of a monitoring tool for Varroajacobsoni an ectoparasitic mite of honey bees. Aspects AppI. BioI. 53, Martin SJ. (2001) The role of Varroa and viral pathogens in the collapse of honey bee colonies: a modelling approach. J. AppI. EcoI. 38, Martin S.J., Hogarth A., Van breda J., Perrett J. (1998) A scientific note on Varroa jacobsoni and the collapse of Apis mellifera colonies in the United Kingdom. Apidologie 29, Nordstrom S. (2000) Virus infections and Varroa infestations in honey bee colonies. Ph.D. thesis, Swedish Univ. of Agricultural Sciences, Dept. of Entomology, S Uppsala, Sweden. Nordstrom S., Fries 1., Aarhus A., Hansen H., Korpela S. (1999) Virus infections in Nordic honey bee colonies with no, low or severe Varroa jacobsoni infestations. Apidologie 30, Smirnov A.M. (1978) Research results obtained in USSR concerning aetiology, pathogenesis, epizootiology, diagnosis and control of Varroa disease in bees. Apiacta 13, Sumpter D., Martin SJ. (2003) The dynamics of virus epidemics in Varroa infested honey bee colonies. J. AppI. Ecol. (in press).
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