Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment

Abstract

Neonicotinoid insecticides are successfully applied to control pests in a variety of agricultural crops; however, they may not only affect pest insects but also non-target organisms such as pollinators. This review summarizes, for the first time, 15 years of research on the hazards of neonicotinoids to bees including honey bees, bumble bees and solitary bees. The focus of the paper is on three different key aspects determining the risks of neonicotinoid field concentrations for bee populations: (1) the environmental neonicotinoid residue levels in plants, bees and bee products in relation to pesticide application, (2) the reported side-effects with special attention for sublethal effects, and (3) the usefulness for the evaluation of neonicotinoids of an already existing risk assessment scheme for systemic compounds. Although environmental residue levels of neonicotinoids were found to be lower than acute/chronic toxicity levels, there is still a lack of reliable data as most analyses were conducted near the detection limit and for only few crops. Many laboratory studies described lethal and sublethal effects of neonicotinoids on the foraging behavior, and learning and memory abilities of bees, while no effects were observed in field studies at field-realistic dosages. The proposed risk assessment scheme for systemic compounds was shown to be applicable to assess the risk for side-effects of neonicotinoids as it considers the effect on different life stages and different levels of biological organization (organism versus colony). Future research studies should be conducted with field-realistic concentrations, relevant exposure and evaluation durations. Molecular markers may be used to improve risk assessment by a better understanding of the mode of action (interaction with receptors) of neonicotinoids in bees leading to the identification of environmentally safer compounds.

Interaction betweenVarroa destructorand imidacloprid reduces flight capacity of honeybees

“…Also, we assessed chronic oral toxicity on the colony level, in contrast to measuring the direct acute toxicity on the individual level. Acute toxicity may induce more stress to honeybees, as reduced mobility and a phase of motionlessness was observed after exposure to a high LD 50 dose of imidacloprid [7,8,14,37]. Chronic sub-lethal oral exposure on the colony level may show less acute toxicity, but may reduce performance and thereby reduce colony survival.…”

“…Exposure to the parasitic mite Varroa destructor, and related diseases, is generally seen as one of the important stressors in honeybee colonies. The role of insecticides in causing high colony losses remains highly debated [7][8][9]. Recent studies show it is unlikely that fieldrealistic, sub-lethal doses of neonicotinoid insecticides are the sole cause of colony declines [10,11].…”

Resistance of developing honeybee larvae during chronic exposure to dietary nicotine

“…Compared to adult bees, relatively little work has examined the effects of pesticides on bee larvae; see review for neonicotinoids by Blacquière et al (2012). However, high levels of agrochemical and miticide residues, including neonicotinoids, have been measured in pollen loads, bee bread, honey and propolis, as well as in the wax cells in which larvae develop and pollen is stored (Chauzat and Faucon, 2007;Chauzat et al, 2006;Mullin et al, 2010;Pettis et al, 2013;Wu et al, 2011).…”

“…The systemic neonicotinoids, which have been detected as residues in nectar and pollen, have been blamed for colony losses and shown to affect bees negatively at both individual and colony levels (Blacquière et al, 2012;Decourtye and Devilliers, 2009). Until the development of this class of synthetic insecticides, the chemically related alkaloid nicotine was widely used as an insecticide, and still plays a role in organic farming (Casanova et al, 2002).…”

Honey Bee Diversity is Swayed by Migratory Beekeeping and Trade Despite Conservation Practices: Genetic Evidences for the Impact of Anthropogenic Factors on Population Structure

“…Among them, destruction and fragmentation of natural habitats, toxicity caused by pollution and pesticides -like widely used neonicotinoids-, diseases and their spread getting easier, invasive species are leading the way (Meffe 1998;Brown & Paxton 2009;Van Engelsdorp & Meixner 2010;Blacquiere et al 2012). Honey bees also, especially wild populations that are not managed by beekeepers (including the feral populations), take their share from the situation (Oldroyd 2007;Dietemann et al 2009;Van Engelsdorp et al 2009;Genersch 2010;Evans & Schwarz 2011).…”