Naturwissenschaften (2012) 99:153–158 DOI 10.1007/s00114-011-0881-1 ORIGINAL PAPER Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema Jeffery S. Pettis & Dennis vanEngelsdorp & Josephine Johnson & Galen Dively Received: 1 May 2011 / Revised: 25 December 2011 / Accepted: 31 December 2011 / Published online: 13 January 2012 # The Author(s) 2012. This article is published with open access at Springerlink.com Abstract Global pollinator declines have been attributed to habitat destruction, pesticide use, and climate change or some combination of these factors, and managed honey bees, Apis mellifera, are part of worldwide pollinator declines. Here we exposed honey bee colonies during three brood generations to sub-lethal doses of a widely used pesticide, imidacloprid, and then subsequently challenged newly emerged bees with the gut parasite, Nosema spp. The pesticide dosages used were below levels demonstrated to cause effects on longevity or foraging in adult honey bees. Nosema infections increased significantly in the bees from pesticide-treated hives when compared to bees from control hives demonstrating an indirect effect of pesticides on pathogen growth in honey bees. We clearly demonstrate an increase in pathogen growth within individual bees reared in colonies exposed to one of the most widely used pesticides worldwide, imidacloprid, at below levels considered harmful to bees. The finding that individual bees with undetectable levels of the target pesticide, after being reared in a sub-lethal pesticide environment within the Communicated by: Sven Thatje J. S. Pettis (*) USDA-ARS Bee Research Laboratory, Beltsville, MD, USA e-mail: jeff.pettis@ars.usda.gov D. vanEngelsdorp Department of Entomology, University of Maryland, College Park, MD, USA J. Johnson Department of Toxicology, University of Maryland Baltimore, Baltimore, MD, USA G. Dively Department of Entomology, University of Maryland, College Park, MD, USA colony, had higher Nosema is significant. Interactions be- tween pesticides and pathogens could be a major contributor to increased mortality of honey bee colonies, including colony collapse disorder, and other pollinator declines worldwide. Keywords Apis mellifera . Imidacloprid . Nosema . Sub-lethal . Pesticides . Pathogens Introduction The honey bee, Apis mellifera, is arguably the most impor- tant pollinator of agricultural crops (Klein et al. 2007). While worldwide managed honey bee populations have increased over the last 50 years, colony populations have decreased significantly in many European and North American nations (Aizen and Harder 2009) as a result of habitat destruc- tion, pesticide use, pathogens, and climate change (NRC 2007) or some combination of these factors (vanEngelsdorp and Meixner 2010). At the same time, cultivation of crops that are dependent on insects for pollination (Aizen et al. 2009) has increased. The ability to provide sufficient colonies to meet this anticipated demand is questionable, especially in light of the elevated losses experienced by US beekeepers over the winters of 2006/2007 and 2007/2008 (vanEngelsdorp et al. 2007; vanEngelsdorp et al. 2008). Colonies that die with a condition known as colony collapse disorder (CCD) make up a signifi- cant proportion of recent overwintering losses in the USA (vanEngelsdorp et al. 2008). While the cause of CCD remains unknown, affected colonies are often infected with a greater variety and higher loads of disease agents than apparently healthy colonies (Johnson et al. 2009; vanEngelsdorp et al. 2009a; Cox-Foster et al. 2007). This suggests that some factor or combination of factors may be weakening bees by making them more susceptible to infection (vanEngelsdorp et al.