The distribution, infestation levels and effects of honeybee parasites and pathogens on colony performance in two agro-ecological zones of Uganda

In Uganda, the honeybee, Apis mellifera is kept mainly for honey, other beehive products and for the provision of vital pollination services. Although the beekeeping sector is growing and providing a source of income, food and medicine to many rural households, the potential threat from honeybee parasites and pathogens poses challenges to the sector. Indeed, some of the parasites like Varroa mites which have devastated the beekeeping industry in Europe, Asia and North America have already been registered in Uganda. Although, such parasites and their impacts on European honeybee races are fairly known; their distribution, infestation levels and impacts on African honeybee races are poorly understood. In order to contribute to bridge this information gap, apiaries and feral colonies in the eastern and western highland agro-ecological zones of Uganda each with an altitudinal gradient and varying land uses were sampled during the dry and wet seasons between December 2014 and September 2015. The samples were screened for 11 common RNA viruses, Paenibacillus larvae, Mellisococcus plutonius, Ascosphaera apis, Nosema spp. and Varroa mites using standard techniques with the aim of establishing their infestation levels and their effects on colony performance in the two highland agro-ecological zones of Uganda. Five RNA viruses, P. larvae, three Nosema spp. and Varroa mites were detected. The infection rates of viruses varied: Deformed wing virus (51.9%), Black queen cell virus (20%), Acute bee paralysis virus (9.5%), Lake Sinai virus (2.5%) and Sacbrood virus (2.5%) in sampled colonies. Furthermore, one asymptomatic colony in a protected area of the western highlands was found positive for P. larvae ERIC I strain whose virulence was at least equally high as the reference strain on carniolan bees. A new microsporidian that is smaller than the known honeybee microsporidian parasites; Nosema ceranae and Nosema apis was detected in Ugandan honeybees. The new microsporidian has fewer polar filament coils (10 - 12), compared to 20 - 23 for N. ceranae and more than 30 often seen in N. apis. This new microsporidian was found at higher infestation rates compared to the other two known microsporidian parasites of honeybees. Varroa mite infestation levels in the eastern zone was significantly higher than that in the western during the dry season (P = 0.02). Varroa mites were spreading from lower to higher elevations. Feral colonies were also infested with parasites and pathogens similar to those in managed colonies. Landscape factors like altitude and land use influenced honeybee parasite/pathogen distribution and infestation levels. Increase in viral diversity in Ugandan honeybee colonies and high Nosema spore loads reduced colony performance while Varroa mite infestation alone did not affect colony strength and productivity. The detection of these pathogens and parasites highlight the need for vigilance and development of a national honeybee health strategy to manage them in the country. Detailed studies on the new Nosema species and generally African honeybee health should be carried out in order to: 1) understand distribution, transmission, development, 2) identify associated effects on honeybees at individual and colony levels and 3) to reach a better understanding of the poorly known African honeybee pathogen complex especially in terms of the identities of pathogens present and survival mechanisms.

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