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.

Recent major losses of managed honeybee, Apis mellifera, colonies at a global scale have resulted in a multitude of research efforts to identify the underlying mechanisms. Numerous factors acting singly and/or in combination have been identified, ranging from pathogens, over nutrition to pesticides. However, the role of apiculture in limiting natural selection has largely been ignored. This is unfortunate, because honeybees are more exposed to environmental stressors compared to other livestock and management can severely compromise bee health. Here, we briefly review apicultural factors that influence bee health and focus on those most likely interfering with natural selection, which offers a broad range of evolutionary applications for field practice. Despite intense breeding over centuries, natural selection appears to be much more relevant for the health of managed A. mellifera colonies than previously thought. We conclude that sustainable solutions for the apicultural sector can only be achieved by taking advantage of natural selection and not by attempting to limit it.

The parasitic mite Varroa destructor is a serious threat for western honey bee colonies and beekeepers are compelled to control it to keep their colonies healthy. Yet, by controlling varroa no resistance to the parasite can evolve. As a trial, honey bee colonies have been left untreated in isolated locations to allow development of resistance or tolerance to the mite. These colonies developed an ability to live without control measures against varroa, although the traits responsible for this resistance or tolerance are still unclear. Two of these resistant populations have been studied to test the involvement of specific varroa mite targeted hygienic behaviour varroa sensitive hygiene (VSH) in the acquired resistance. Individual mites were manually introduced into just capped brood cells, after which the brood combs were placed in colonies of the two resistant populations and in control colonies in which varroa had always been controlled. We followed the development of the mites, including possible removals. We found that VSH had increased strongly in one of the selections, up to 40% of the infested cells with mites and pupae were removed, but it had decreased in the other selection, compared to the control colonies. Further we could not conclude from our data that VSH only or preferentially targets reproducing mites, leaving non-reproducing mites undisturbed. The different VSH responses between the two selected resistant honey bee populations lead to conclude that more than one mechanism of resistance may evolve in response to the selection pressure by varroa mites.

High losses of honey bee colonies in recent decades are of great societal and economical concern and experienced as a sign of the vulnerability of the environment, including the service of crop pollination, and of the beekeeping sector. There is no single cause for the colony losses, but many contributing stressors may act in concert. Varroa destructor infestation is acknowledged as an important cause of these losses. The roles of infestation by Nosema ceranae or exposure to insecticides are controversial. Interactions between exposure to pesticides and V. destructor or Nosema spp. have previously been implicated. In two years of field experiments, we studied the effects of and possible interactions between the stressors V. destructor infestation, Nosema spp. infestation, and chronic sublethal exposure to a field‐realistic dose of the insecticide imidacloprid on the performance and survival of honey bee colonies. Colonies highly infested by V. destructor were 13% smaller in size and were 59.1 times more likely to die than colonies infested with low levels of V. destructor. Infestation with high levels of Nosema sp. led to 2% decrease in size and 1.4 times higher likelihood to die compared to colonies with low levels of Nosema sp. No effects of chronic sublethal exposure to imidacloprid on colony size or survival were found in this study. Exposure to V. destructor and imidacloprid led to a slightly higher fraction of bees infested with Nosema sp., but in contrast to the expectations, no resulting interactions were found for colony size or survival. Colonies as a superorganism may well be able to compensate at the colony level for sublethal negative effects of stressors on their individuals. In our experimental study under field‐realistic exposure to stressors, V. destructor was by far the most lethal one for honey bee colonies.

Established invasive species can pose a continuous threat to biodiversity and food security, thereby calling for sustainable mitigation. There is a consensus that the ubiquitous ecto-parasitic mite Varroa destructor, an invasive species from Asia, is the main biological threat to global apiculture with Apis mellifera. V. destructor has almost completely wiped out wild European honey bee (Apis mellifera) populations. The only remedy for apiculture, to date, is frequent control measures against the mite throughout the season, which prevents possible adaptations. While targeted breeding efforts have, so far, not achieved the selection of tolerant or resistant bees, natural selection approaches have succeeded at least seven times. Here, we propose to take advantage of natural selection for honey bee resistance by stopping mite treatment in managed colonies. The main principles are within population mating of the colonies’ own virgin queens and drones and selection based on survival and proliferous development of colonies. Being used for 10 years, it has shown to result in grosso modo ‘normal’ colonies with a high level of resistance to V. destructor. Here, we call for local groups of beekeepers and scientists to join a novel natural selection program that has started so far on three locations. This will eventually lead to several locally adapted V. destructor resistant honey bee populations around the world, and help global apiculture becoming more sustainable.

The 2013 EU ban of three neonicotinoids used in seed coating of pollinator attractive crops was put in place because of concern about declining wild pollinator populations and numbers of honeybee colonies. It was also concluded that there is an urgent need for good field data to fill knowledge gaps. In the meantime such data have been generated. Based on recent literature we question the existence of recent pollinator declines and their possible link with the use of neonicotinoids. Because of temporal non‐coincidence we conclude that declines of wild pollinators and of honeybees are not likely caused by neonicotinoids. Even if bee decline does occur and if there is a causal relationship with the use of neonicotinoids, we argue that it is not possible on such short term to evaluate the effects of the 2013 ban. In order to supply future debate with realistic (field) data and to discourage extrapolating the effects of studies using overdoses that are not of environmental relevance, we propose – in addition to field studies performed by the chemical industry – to use the ‘semi‐field worst case’ treated artificial diet studies approach to free flying colonies in the field. This kind of study may provide realistic estimates for risk and be useful to study realistic interactions with non‐pesticide stressors. © 2017 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.