In recent years several bumblebee species as well as other pollinators have suffered range declines in parts of Europe, the Americas and Asia (Biesmeijer et al., 2006; Cameron et al., 2011; Goulson, Lye & Darvill, 2008; Potts et al., 2010). Changes in anthropogenic land-use is a major contributing factor to these declines, with agricultural intensification reducing floral diversity and nesting habitats from many pollinators (Goulson et al., 2005; Ricketts et al., 2008; Vanbergen et al., 2013). This has left some bumblebee species fragmented, in small populations with low genetic diversity, something which may make bees more vulnerable to stresses such as parasites (Darvill et al., 2006; Ellis et al., 2006; Evison et al., 2013; Oldroyd, 2007; Whitehorn et al., 2011).
In addition to the stresses of habit loss, pesticide exposure and natural parasites, (Goulson, 2003), the use of managed bees may place additional stresses on bumblebee populations. Honey bees have been managed commercially for crop pollination and honey production for centuries, and are often kept in commercial apiaries with tens to thousands of colonies, substantially increasing the density of bees in an area. Bumblebees are also now commercially produced and used mainly in greenhouses, but also sometimes in polytunnels and open crops, in Europe, North America, South America, New Zealand and Asia to enhance the yields of soft fruit crops (Velthuis & van Doorn, 2006). Although the greenhouses in which commercially produced bumblebees are most commonly used are meant to be closed, the commercially produced bumblebees are frequently found foraging outside the greenhouses, and wild bees have been found foraging inside them (Kraus et al., 2011; Morandin et al., 2001; Murray et al., 2013; Whittington et al., 2004). By freely mixing with wild bumblebees, the deployment of commercially produced bumblebees effectively increases the local density of bumblebees. Bumblebee parasites can be dispersed between bumblebees following shared flower usage (Durrer & Schmid-Hempel, 1994), and, as a result, the rate of parasite transmission between bees will predictably rise with increased pollinator density (Arneberg et al., 1998). In areas utilising commercially produced bumblebees, higher parasite prevalence may be expected to be the result, due to either the spillover of parasites from the commercially produced bumblebees, parasite spillback from wild bumblebees, or stress related to the high pollinator density (Kelly et al., 2009; Power & Mitchell, 2004; Schmid-Hempel, 2011).
The spillover of parasites from one host to another, either intraspecifically or interspecifically, is well known for many organisms (Power & Mitchell, 2004). There is now good evidence that the honey bee parasites Nosema ceranae and deformed wing virus have spilled over to bumblebees, with both being virulent and now widespread in their new bumblebee host (Evison et al., 2012; Furst et al., 2014; Genersch et al., 2006; Graystock et al., 2013a; Plischuk et al., 2009). In addition, parasites may also spill over to wild bumblebees from the commercially reared bumblebees used in greenhouses. Colonies of commercially produced bumblebees have been shown in many studies to carry parasites (Colla et al., 2006; Gegear, Otterstatter & Thomson, 2005; Manson, Otterstatter & Thomson, 2010; Meeus et al., 2011; Murray et al., 2013; Otterstatter & Thomson, 2007; Singh et al., 2010; Whittington & Winston, 2003), with the most recent study using sensitive molecular methods finding that three-quarters of the colonies investigated were infected by at least one parasite and confirming that these parasites were in many cases infectious (Graystock et al., 2013b). The introduction of commercially produced bumblebees has been associated with the introduction of foreign parasites and correlated declines in native bumblebee species in Japan, South America and North America, suggesting that the spillover of parasites has occurred on multiple occasions (Arbetman et al., 2012; Colla et al., 2006; Goka et al., 2001; Meeus et al., 2011; Otterstatter & Thomson, 2008; Szabo et al., 2012).
Although attention has focussed on parasite spillover, it is also possible that the use of managed honey bees and commercially produced bumblebees may increase the prevalence of parasites in wild bumblebees via parasite spillback or heightened stress from increased competition when foraging. Managed honey bees or commercially produced bumblebees may become infected with parasites carried by the wild bees, and their unnaturally high density in apiaries or greenhouses may then result in them acting as a reservoir in which the prevalence of parasites becomes high, from which the parasites can then spillback into wild bees (Kelly et al., 2009). The increased competition for resources caused by the introduction of high densities of managed honey bees or commercially produced bumblebees may also stress wild bees due to the increased competition when foraging, which can have negative effects on various fitness components including resistance to parasites (Brown, Loosli & Schmid-Hempel, 2000; Elbgami et al., 2014; Foley et al., 2012; Goulson & Sparrow, 2009; Lafferty & Gerber, 2002; Mallon, Brockmann & Schmid-Hempel, 2003).
The prevalence of parasites in wild bumblebees appears to be greater when the bees are in proximity to greenhouses using commercially produced bumblebee colonies (Colla et al., 2006; Murray et al., 2013; Otterstatter & Thomson, 2008). However, whether this is due to parasite spillover, parasite spillback, or stress, is not always clear. Here we investigate the relationships between commercially reared bumblebees or managed honey bees and the prevalence of a range of parasites in bumblebees. We first examine the relationship between the prevalence of parasites in wild bumblebees and proximity to three farms in which commercially reared bumblebees being used and two greenhouse farms in which they were not being used. In addition, we examine the effect of proximity to honey bees on bumblebee parasite prevalence, using bumblebee colonies located at two sites, either near or far from an apiary.