Developmental exposure to pesticide contaminated food impedes bumblebee brain growth predisposing adults to become poorer learners

Abstract

11Understanding the risk to biodiversity from pesticide exposure is a global priority. For bees, an 12 understudied step in evaluating pesticide risk is understanding how pesticide contaminated foraged food 13 brought back to the colony can affect developing individuals. Provisioning bumblebee colonies with 14 pesticide (neonicotinoid) treated food, we investigated how exposure during two key developmental 15 phases (brood and/or early-adult), impacted brain growth and assessed the consequent effects on adult 16 learning behaviour. Using micro-computed tomography (µCT) scanning and 3D image analysis, we 17 compared brain development for multiple neuropils in workers 3 and 12-days post-emergence. 18Mushroom body calyces were the neuropils most affected by exposure during either of the developmental 19 phases, with both age cohorts showing smaller structural volumes. Critically, reduced calyces' growth in 20 pesticide exposed workers was associated with lower responsiveness to a sucrose reward and impaired 21 learning performance. Furthermore, the impact from brood exposure appeared irrecoverable despite no 22 exposure during adulthood. 23 2 24 1998; Jones et al., 2013;Maleszka et al., 2009;Riveros and Gronenberg, 2010). To distinguish the effects 65 of pesticide exposure from variation caused by other interacting factors, we therefore: i) attempted to 66 standardise experience and sensory input across tested workers, ii) tested workers of controlled age, and 67iii) compared between young and old age cohorts. Furthermore, by studying two main developmental 68 stages, such as brood (larval & pupal) and early adulthood, here we reveal which development phase is 69 more vulnerable to pesticide exposure, and whether developmental plasticity in bee brains (Farris et al., 70 Learning 132 Lobulas n=71l mer -medul l a s ~ trea tment + a ge + s i ze + (1|col ony) Central Body n=88l mer -centra l Body ~ trea tment + a ge + s i ze + (1|col ony) Medullas n=71l mer -l obul a s ~ trea tment + a ge + s i ze + (1|col ony) Antennal Lobes n=89l mer -a ntenna l l obes ~ trea tment + a ge + s i ze + (1|col ony)