The Trojan hives: pollinator pathogens, imported and distributed in bumblebee colonies

Abstract

Summary Over a million commercially produced bumblebee colonies are imported annually on a global scale for the pollination of greenhouse crops. After importation, they interact with other pollinators, with an associated risk of any parasites they carry infecting and harming native bees. National and supranational regulations are designed to prevent this, and commercially produced bumblebee colonies are accordingly now often sold and imported as being parasite‐free. Here, we used molecular methods to examine the occurrence of parasites in bumblebee colonies that were commercially produced in 2011 and 2012 by three producers. We then used controlled experiments to determine whether any parasites present were infectious. We found that 77% of the commercially produced bumblebee colonies from the three producers, which were imported on the basis of being free of parasites, in fact carried microbial parasites, with five different parasites being detected across the total sample of bumblebees and a further three in the pollen supplied with the colonies as food. Our controlled experiments demonstrated that at least three of these parasites were infectious to bumblebees with significant negative effects on their health. Furthermore, we also found that at least four of the parasites carried by commercially produced bumblebees were infectious to honeybees, indicating that they pose a risk to other pollinators as well. Synthesis and applications. The results demonstrate that commercially produced bumblebee colonies carry multiple, infectious parasites that pose a significant risk to other native and managed pollinators. More effective disease detection and management strategies are urgently needed to reduce the pathogen spillover threat from commercially produced bumblebees.

Parasites in bloom: flowers aid dispersal and transmission of pollinator parasites within and between bee species

“…Nosema ceranae is traditionally thought of as being a honeybee parasite and has been implicated in colony losses in some areas [31][32][33]. However, N. ceranae has more recently been identified as an emerging pathogen in several bumblebee species, causing both lethal and sublethal effects [22,37,39,40]. The results here highlight the potential role of shared flower use as a mode of transmission, which will facilitate the spillover of harmful parasites between different pollinators and populations.…”

“…There is currently great interest in the stress factors affecting pollinators, many of which are showing substantial population declines with knock-on effects on the plants that rely on them for pollination [17][18][19]. Parasites are well established as being an important factor in at least some of these declines, with several bumblebee species showing population declines that correlate with pathogen spillover from commercially produced bumblebees [20][21][22][23][24][25][26][27][28], and honeybee colony losses in many countries being associated with emerging parasites such as the Varroa mite and the microsporidian Nosema ceranae [29][30][31][32][33][34]. Importantly, there is increasing evidence of parasite transmission between pollinator taxa being more significant than has generally been appreciated.…”

“…Importantly, there is increasing evidence of parasite transmission between pollinator taxa being more significant than has generally been appreciated. Several honeybee viruses and the N. ceranae microsporidian parasite of honeybees have been detected infecting bumblebees [22,[35][36][37][38][39][40][41][42], and the Apicystis bombi neogregarine parasite of bumblebees has been shown experimentally to infect honeybees [22,43].…”

Test of the invasive pathogen hypothesis of bumble bee decline in North America

“…Such low diversity outside of Asia could have arisen through multiple mechanisms, including the natural spread of a Holarctic Nosema lineage before Bombus domestication, or more recently as a result of intensive Bombus domestication in Europe and North America, which has not occurred in China (27). Given the high parasite levels found today in European commercial bumble bees (28), together with the knowledge that commercial foraging bees come and go from "leaky" greenhouses (18,21) and have been used in open-field pollination, a sweep of a common N. bombi strain is possible. In this scenario, the N. bombi strain resulting in increasing North American prevalence could conceivably reflect a secondary introduction from Europe.…”

Evidence of Varroa-mediated deformed wing virus spillover in Hawaii

“…Re-emerging viral diseases such as DWV represent one of the major threats to honey bee health, and the "spillover" of pathogens to wild bees and other insects may also contribute to the current global pollinator decline (Fürst et al, 2014;Genersch et al, 2006;Graystock et al, 2013a;Graystock et al, 2013b;Manley et al, 2015;Tehel et al, 2016). Here we carry out a preliminary comparison of the incidence of DWV on non-Apis insects in areas with and without V. destructor.…”