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

Abstract

Emergent fungal diseases are critical factors in global biodiversity declines. The fungal pathogen Nosema bombi was recently found to be widespread in declining species of North American bumble bees (Bombus), with circumstantial evidence suggesting an exotic introduction from Europe. This interpretation has been hampered by a lack of knowledge of global genetic variation, geographic origin, and changing prevalence patterns of N. bombi in declining North American populations. Thus, the temporal and spatial emergence of N. bombi and its potential role in bumble bee decline remain speculative. We analyze Nosema prevalence and genetic variation in the United States and Europe from 1980, before an alleged introduction in the early 1990s, to 2011, extracting Nosema DNA from Bombus natural history collection specimens from across this time period. Nosema bombi prevalence increased significantly from low detectable frequency in the 1980s to significantly higher frequency in the mid- to late-1990s, corresponding to a period of reported massive infectious outbreak of N. bombi in commercial bumble bee rearing stocks in North America. Despite the increased frequency, we find no conclusive evidence of an exotic N. bombi origin based on genetic analysis of global Nosema populations; the widespread Nosema strain found currently in declining United States bumble bees was present in the United States before commercial colony trade. Notably, the US N. bombi is not detectably different from that found predominantly throughout Western Europe, with both regions characterized by low genetic diversity compared with high levels of diversity found in Asia, where commercial bee breeding activities are low or nonexistent.

Incorporating citizen science, museum specimens, and field work into the assessment of extinction risk of the American Bumble bee (Bombus pensylvanicus De Geer 1773) in Canada

“…Additional threats to Bumble bees like B. pensylvanicus may include parasites and pathogens, such as the fungal pathogen Nosema bombi, including those spread from managed commercial Bumble bee and honeybee colonies (Colla et al 2006;Hoffmann et al 2008;Otterstatter and Thomson 2008;Gillespie 2010;Cameron et al 2011aCameron et al , 2016Szabo et al 2012;Graystock et al 2016). Pesticides have been and still are a threat to bees, from past use of organophosphorus and carbamate compounds (Kevan 1975;Kevan et al 1984Kevan et al , 1997 to the current widespread use of systemic neonicotinoid insecticides and fungicides; neonicotinoids have been used increasingly since the 1990 s with mounting evidence showing negative impacts on Bumble bees, particularly sub-lethal effects (Gill et al 2012;Szabo et al 2012;Whitehorn et al 2012;Godfray et al 2014Godfray et al , 2015Goulson 2015;Lundin et al 2015;Wood and Goulson 2017).…”

Massively Introduced Managed Species and Their Consequences for Plant–Pollinator Interactions

“…Bumblebees, particularly B. terrestris, are infected by several other pathogens such as Apicystis bombi (protozoan), Crithidia bombi (protozoan), Nosema bombi (Microsporidia), Locustacarus buchneri (Acari) (Cameron et al, 2016;Colla et al, 2006;Graystock et al, 2014Graystock et al, , 2015Graystock et al, , 2016Otterstater and Thompson, 2008;Stout and Morales, 2009). There is now clear evidence of a high prevalence of parasites in commercially reared bumblebees (Colla et al, 2006;Graystock et al, 2013aGraystock et al, , 2015Graystock et al, , 2016.…”

Effects of parasites and pathogens on bee cognition

“…colonies are usually infected with parasites and pathogens (e.g. 77% of colonies with up to five different parasites; Graystock et al, 2014) and their use in crop pollination has increased the spillover of parasites, such as C. bombi and N. bombi, into wild conspecifics and heterospecifics that forage close to the greenhouses where commercial colonies are used (Murray et al, 2013;Cameron et al, 2016). This is because commercial workers very often escape from greenhouses and forage outside, where they come into contact with wild flowers and pollinators (Whittington & Winston, 2004).…”