Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees

Abstract

Learning and memory are crucial functions which enable insect pollinators to efficiently locate and extract floral rewards. Exposure to pesticides or infection by parasites may cause subtle but ecologically important changes in cognitive functions of pollinators. The potential interactive effects of these stressors on learning and memory have not yet been explored. Furthermore, sensitivity to stressors may differ between species, but few studies have compared responses in different species. Here, we show that chronic exposure to fieldrealistic levels of the neonicotinoid clothianidin impaired olfactory learning acquisition in honeybees, leading to potential impacts on colony fitness, but not in bumblebees. Infection by the microsporidian parasite Nosema ceranae slightly impaired learning in honeybees, but no interactive effects were observed. Nosema did not infect bumblebees (3% infection success). Nevertheless, Nosema-treated bumblebees had a slightly lower rate of learning than controls, but faster learning in combination with neonicotinoid exposure. This highlights the potential for complex interactive effects of stressors on learning. Our results underline that one cannot readily extrapolate findings from one bee species to others. This has important implications for regulatory risk assessments which generally use honeybees as a model for all bees.

The influence of sublethal doses of imidacloprid on protein content and proteolytic activity in honey bees (Apis mellifera L.)

“…One of the substances most commonly used in crop protection and registered in over 120 countries is imidacloprid (IMD) (Jeschke, Nauen, Schindler, & Elbert, 2011). It is known that IMD, is an agonist of the nicotinic acetylcholine receptor (nAChRs) on the postsynaptic membrane, and like other compounds from this group of pesticides, it affects the central nervous system (CNS) of insects (Brown, Ihara, Buckingham, Matsuda, & Sattelle, 2006;Matsuda, Shimomura, Ihara, Akamatsu, & Sattelle, 2005) and subsequently the insect's physiology and behavior (Desneux, Decourtye, & Delpuech, 2007;Piiroinen & Goulson, 2016;Teeters, Johnson, Ellis, & Mario, 2012;Van Dijk, Van Staalduinen, & Van der Sluijs, 2013). For example, it has been shown that sublethal doses of IMD have an adverse effect on the bee's sense of smell and memory (Decourtye, Devillers et al, 2004, Decourtye, Armengaud et al, 2004Kirchner, 1999;Williamson, Baker, & Wright, 2013), as well as on the insects' intensity of feeding (Schneider, Tautz, Gruenewald, & Fuchs, 2012;Yang, Chuang, Chen, & Chang, 2008), territorial disorientation (Hatjina, Papachristoforou, Charistos, Bouga, & Arnold, 2012;Henry et al, 2012), and neurophysiologic changes (Goulson, 2013;Guez, Suchail, Gauthier, Maleszka, & Belzunces, 2001a, 2001bLambin, Armengaud, Raymond, & Gauthier, 2001).…”

Detrimental interactions of neonicotinoid pesticide exposure and bumblebee immunity

“…The results demonstrated here in bumblebees are congruent with the outcomes of prior studies investigating interactions between neonicotinoid exposure and immunity in honeybees (Alaux et al., ; Di Prisco et al., ; Brandt et al., ; López et al., ). This is not a trivial extension, as honeybees and bumblebees, while both highly susceptible, have been suggested to differ in their detoxification of neonicotinoids (Cresswell, Robert, Florance, & Smirnoff, ), and neonicotinoid exposure and parasite stress has been shown to have differential effects in the two groups of bees (Piiroinen & Goulson, ). The reduction in antimicrobial activity in B. impatiens is in contrast to a recent study showing elevated AMP expression following imidacloprid exposure (Simmons & Angelli, ).…”

A mechanistic framework to explain the immunosuppressive effects of neurotoxic pesticides on bees

“…Numerous global factors are thought to contribute to this alarming phenomenon, including habitat loss and fragmentation, suboptimal diet, diseases and the detrimental effects of sublethal, chronic pesticide exposure (Goulson, Nicholls, Botías, & Rotheray, ; Vanbergen et al, ). Besides affecting pollinator navigation abilities (Fischer et al., ; Henry et al., ; Jin, Klein, Leimig, Bischoff, & Menzel, ; Stanley, Russell, Morrison, Rogers, & Raine, ), cognitive abilities (Decourtye, Devillers, Cluzeau, Charreton, & Pham‐Delègue, ; Farooqui, ; Gauthier, ; Kessler et al., ; Piiroinen & Goulson, ; Stanley, Smith, & Raine, ; Williamson, Baker, & Wright, ; Williamson, Moffat, et al., ) and reproduction (Baron, Raine, & Brown, ; Sandrock et al., ; Whitehorn, O'Connor, Wackers, & Goulson, ), the immune suppressive effect of sublethal pesticide doses and the resulting elevated susceptibility of pollinators to pathogens (Baron et al., ; Brandt, Gorenflo, Siede, Meixner, & Büchler, ; Di Prisco et al., ; Doublet, Labarussias, de Miranda, Moritz, & Paxton, ; Fauser‐Misslin, Sadd, Neumann, & Sandrock, ; Hernández López et al., ; previous studies summarized in James & Xu, ) are of particular concern (Sánchez‐Bayo et al., ).…”

“…Assessing the impact of pesticides on pollinator health by sublethal chronic exposure requires a holistic view of the problem. In recent years, research has started to uncover the side‐effects of sublethal neonicotinoid exposure on cognitive abilities, including pollinator navigation and learning (Decourtye et al., ; Farooqui, ; Fischer et al., ; Gauthier, ; Goulson et al., ; Henry et al., ; Jin et al., ; Kessler et al., ; Piiroinen & Goulson, ; Stanley et al., , ; Williamson, Baker, et al., ; Williamson, Moffat, et al., ). A similar intensity of research effort now needs to be focused on the sublethal effects of neurotoxic pesticides on insect immunity.…”