Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema
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 colony, had higher Nosema is significant. Interactions between pesticides and pathogens could be a major contributor to increased mortality of honey bee colonies, including colony collapse disorder, and other pollinator declines worldwide.
Pettis JS, vanEngelsdorp D, Johnson J, Dively G. Naturwissenschaften. 2012 Feb;99(2):153-8. doi: 10.1007/s00114-011-0881-1. Epub 2012 Jan 13.
A nicotinic acetylcholine receptor agonist affects honey bee sucrose responsiveness and decreases waggle dancing.
A nicotinic acetylcholine receptor agonist, imidacloprid, impairs memory formation in honey bees and has general effects on foraging. However, little is known about how this agonist affects two specific aspects of foraging: sucrose responsiveness (SR) and waggle dancing (which recruits nestmates). Using lab and field experiments, we tested the effect of sublethal doses of imidacloprid on (1) bee SR with the proboscis extension response assay, and (2) free-flying foragers visiting and dancing for a sucrose feeder. Bees that ingested imidacloprid (0.21 or 2.16 ng bee(-1)) had higher sucrose response thresholds 1 h after treatment. Foragers that ingested imidacloprid also produced significantly fewer waggle dance circuits (10.5- and 4.5-fold fewer for 50% and 30% sucrose solutions, respectively) 24 h after treatment as compared with controls. However, there was no significant effect of imidacloprid on the sucrose concentrations that foragers collected at a feeder 24 h after treatment. Thus, imidacloprid temporarily increased the minimum sucrose concentration that foragers would accept (short time scale, 1 h after treatment) and reduced waggle dancing (longer time scale, 24 h after treatment). The effect of time suggests different neurological effects of imidacloprid resulting from the parent compound and its metabolites. Waggle dancing can significantly increase colony food intake, and thus a sublethal dose (0.21 ng bee(-1), 24 p.p.b.) of this commonly used pesticide may impair colony fitness.
Eiri DM, Nieh JC. J Exp Biol. 2012 Jun 15;215(Pt 12):2022-9. doi: 10.1242/jeb.068718.
Neonicotinoid pesticide reduces bumble bee colony growth and queen production
Growing evidence for declines in bee populations has caused great concern because of the valuable ecosystem services they provide. Neonicotinoid insecticides have been implicated in these declines because they occur at trace levels in the nectar and pollen of crop plants. We exposed colonies of the bumble bee Bombus terrestris in the laboratory to field-realistic levels of the neonicotinoid imidacloprid, then allowed them to develop naturally under field conditions. Treated colonies had a significantly reduced growth rate and suffered an 85% reduction in production of new queens compared with control colonies. Given the scale of use of neonicotinoids, we suggest that they may be having a considerable negative impact on wild bumble bee populations across the developed world.
Whitehorn PR, O'Connor S, Wackers FL, Goulson D. Science. 2012 Apr 20;336(6079):351-2. doi: 10.1126/science.1215025. Epub 2012 Mar 29.
RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera.
The development of insecticides requires valid risk assessment procedures to avoid causing harm to beneficial insects and especially to pollinators such as the honeybee Apis mellifera. In addition to testing according to current guidelines designed to detect bee mortality, tests are needed to determine possible sublethal effects interfering with the animal's vitality and behavioral performance. Several methods have been used to detect sublethal effects of different insecticides under laboratory conditions using olfactory conditioning. Furthermore, studies have been conducted on the influence insecticides have on foraging activity and homing ability which require time-consuming visual observation. We tested an experimental design using the radiofrequency identification (RFID) method to monitor the influence of sublethal doses of insecticides on individual honeybee foragers on an automated basis. With electronic readers positioned at the hive entrance and at an artificial food source, we obtained quantifiable data on honeybee foraging behavior. This enabled us to efficiently retrieve detailed information on flight parameters. We compared several groups of bees, fed simultaneously with different dosages of a tested substance. With this experimental approach we monitored the acute effects of sublethal doses of the neonicotinoids imidacloprid (0.15-6 ng/bee) and clothianidin (0.05-2 ng/bee) under field-like circumstances. At field-relevant doses for nectar and pollen no adverse effects were observed for either substance. Both substances led to a significant reduction of foraging activity and to longer foraging flights at doses of ≥0.5 ng/bee (clothianidin) and ≥1.5 ng/bee (imidacloprid) during the first three hours after treatment. This study demonstrates that the RFID-method is an effective way to record short-term alterations in foraging activity after insecticides have been administered once, orally, to individual bees. We contribute further information on the understanding of how honeybees are affected by sublethal doses of insecticides.
A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees
Honey bees provide important pollination services to crops and wild plants. The agricultural use of systemic insecticides, such as neonicotinoids, may harm bees through their presence in pollen and nectar, which bees consume. Many studies have tested the effects on honey bees of imidacloprid, a neonicotinoid, but a clear picture of the risk it poses to bees has not previously emerged, because investigations are methodologically varied and inconsistent in outcome. In a meta-analysis of fourteen published studies of the effects of imidacloprid on honey bees under laboratory and semi-field conditions that comprised measurements on 7073 adult individuals and 36 colonies, fitted dose-response relationships estimate that trace dietary imidacloprid at field-realistic levels in nectar will have no lethal effects, but will reduce expected performance in honey bees by between 6 and 20%. Statistical power analysis showed that published field trials that have reported no effects on honey bees from neonicotinoids were incapable of detecting these predicted sublethal effects with conventionally accepted levels of certainty. These findings raise renewed concern about the impact on honey bees of dietary imidacloprid, but because questions remain over the environmental relevance of predominantly laboratory-based results, I identify targets for research and provide procedural recommendations for future studies.