Traditionally, measurement of the acute toxicity of pesticides to beneficial arthropods has relied largely on the determination of an acute median lethal dose or concentration. However, the estimated lethal dose during acute toxicity tests may only be a partial measure of the deleterious effects. In addition to direct mortality induced by pesticides, their sublethal effects on arthropod physiology and behavior must be considered for a complete analysis of their impact. An increasing number of studies and methods related to the identification and characterization of these effects have been published in the past 15 years. Review of sublethal effects reported in published literature, taking into account recent data, has revealed new insights into the sublethal effects of pesticides including effects on learning performance, behavior, and neurophysiology. We characterize the different types of sublethal effects on beneficial arthropods, focusing mainly on honey bees and natural enemies, and we describe the methods used in these studies. Finally, we discuss the potential for developing experimental approaches that take into account these sublethal effects in integrated pest management and the possibility of integrating their evaluation in pesticide registration procedures.

The Sublethal Effects of Pesticides on Beneficial Arthropods

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.

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

We assessed the state of knowledge regarding the effects of large-scale pollution with neonicotinoid insecticides and fipronil on non-target invertebrate species of terrestrial, freshwater and marine environments. A large section of the assessment is dedicated to the state of knowledge on sublethal effects on honeybees (Apis mellifera) because this important pollinator is the most studied non-target invertebrate species. Lepidoptera (butterflies and moths), Lumbricidae (earthworms), Apoidae sensu lato (bumblebees, solitary bees) and the section “other invertebrates” review available studies on the other terrestrial species. The sections on freshwater and marine species are rather short as little is known so far about the impact of neonicotinoid insecticides and fipronil on the diverse invertebrate fauna of these widely exposed habitats. For terrestrial and aquatic invertebrate species, the known effects of neonicotinoid pesticides and fipronil are described ranging from organismal toxicology and behavioural effects to population-level effects. For earthworms, freshwater and marine species, the relation of findings to regulatory risk assessment is described. Neonicotinoid insecticides exhibit very high toxicity to a wide range of invertebrates, particularly insects, and field-realistic exposure is likely to result in both lethal and a broad range of important sublethal impacts. There is a major knowledge gap regarding impacts on the grand majority of invertebrates, many of which perform essential roles enabling healthy ecosystem functioning. The data on the few non-target species on which field tests have been performed are limited by major flaws in the outdated test protocols. Despite large knowledge gaps and uncertainties, enough knowledge exists to conclude that existing levels of pollution with neonicotinoids and fipronil resulting from presently authorized uses frequently exceed the lowest observed adverse effect concentrations and are thus likely to have large-scale and wide ranging negative biological and ecological impacts on a wide range of non-target invertebrates in terrestrial, aquatic, marine and benthic habitats.

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Effects of neonicotinoids and fipronil on non-target invertebrates

Until 1985 discussions of pesticides and honey bee toxicity in the USA were focused on pesticides applied to crops and the unintentional exposure of foraging bees to them. The recent introduction of arthropod pests of honey bees, Acarapis woodi (1984), Varroa destructor (1987), and Aethina tumida (1997), to the USA have resulted in the intentional introduction of pesticides into beehives to suppress these pests. Both the unintentional and the intentional exposure of honey bees to pesticides have resulted in residues in hive products, especially beeswax. This review examines pesticides applied to crops, pesticides used in apiculture and pesticide residues in hive products. We discuss the role that pesticides and their residues in hive products may play in colony collapse disorder and other colony problems. Although no single pesticide has been shown to cause colony collapse disorder, the additive and synergistic effects of multiple pesticide exposures may contribute to declining honey bee health.

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Pesticides and honey bee toxicity – USA

https://www.boerenlandvogels.nl/sites/default/files/VanderSluijs_ea_2013_neonicotinoids_bee_disorders_0.pdf

Neonicotinoids, bee disorders and the sustainability of pollinator services

Using a conditioned proboscis extension response (PER) assay, honeybees (Apis mellifera L.) can be trained to associate an odor stimulus with a sucrose reward. Previous studies have shown that observations of conditioned PER were of interest for assessing the behavioral effects of pesticides on the honeybee. In the present study, the effects of sublethal concentrations of nine pesticides on learning performances of worker bees subjected to the PER assay were estimated and compared. Pesticides were tested at three concentrations. The highest concentration of each pesticide corresponded to the median lethal dose value (48-h oral LD50), received per bee and per day, divided by 20. Reduced learning performances were observed for bees surviving treatment with fipronil, deltamethrin, endosulfan, and prochloraz. A lack of behavioral effects after treatment with lambda-cyalothrin, cypermethrin, tau-fluvalinate, triazamate, and dimethoate was recorded. No-observed-effect concentrations (NOECs) for the conditioned PER were derived for the studied pesticides. Our study shows that the PER assay can be used for estimating sublethal effects of pesticides on bees. Furthermore, comparisons of sensitivity as well as the estimation of NOECs, useful for regulatory purposes, are possible.

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A. Decourtye

Papers

Comparative Sublethal Toxicity of Nine Pesticides on Olfactory Learning Performances of the Honeybee Apis mellifera

The proboscis extension response: assessing the sublethal effects of pesticides on the honey bee.