The Neonicotinoid Insecticide Imidacloprid Repels Pollinating Flies and Beetles at Field-Realistic Concentrations

Goulson D (2013) The Neonicotinoid Insecticide Imidacloprid Repels Pollinating Flies and Beetles at Field-Realistic Concentrations. PLoS ONE 8(1): e54819. doi:10.1371/journal.pone.0054819 The Neonicotinoid Insecticide Imidacloprid Repels Pollinating Flies and Beetles at Field-Realistic Concentrations Amy H. Easton 0 Dave Goulson 0 Guy Smagghe, Ghent University, Belgium 0 Biological and Environmental Sciences, School of Natural Sciences, University of Stirling, Stirling , Scotland Neonicotinoids are widely used systemic insecticides which, when applied to flowering crops, are translocated to the nectar and pollen where they may impact upon pollinators. Given global concerns over pollinator declines, this potential impact has recently received much attention. Field exposure of pollinators to neonicotinoids depends on the concentrations present in flowering crops and the degree to which pollinators choose to feed upon them. Here we describe a simple experiment using paired yellow pan traps with or without insecticide to assess whether the commonly used neonicotinoid imidacloprid repels or attracts flying insects. Both Diptera and Coleoptera exhibited marked avoidance of traps containing imidacloprid at a field-realistic dose of 1 mg L21, with Diptera avoiding concentrations as low as 0.01 mg L21. This is to our knowledge the first evidence for any biological activity at such low concentrations, which are below the limits of laboratory detection using most commonly available techniques. Catch of spiders in pan traps was also slightly reduced by the highest concentrations of imidacloprid used (1 mg L21), but catch was increased by lower concentrations. It remains to be seen if the repellent effect on insects occurs when neonicotinoids are present in real flowers, but if so then this could have implications for exposure of pollinators to neonicotinoids and for crop pollination. - Declines in pollinator abundance have led to fears of a pollination crisis which threatens both agricultural productivity and biodiversity [1,2]. Worldwide, ,1,500 crops require insect pollination, and ,35% of human food depends directly or indirectly on pollinators, primarily insects, with the pollination services they provide contributing an estimated $14.6 billion to the economy of the USA and 440 million/yr to the UK [35]. Most crops are treated with one or more insecticide, leading to a potential conflict between the need to manage insect pests and the risks of harming pollinator populations. One group of insecticides in particular, the neonicotinoids, have been suspected of contributing to declines in bees [69]. These chemicals are among the most widely used pesticides globally, and are routinely used as seed dressings for crops such as oilseed rape and sunflower. Imidacloprid alone is registered for use on over 140 crops in over 120 countries [10]. In the UK, use of neonicotinoids has increased year on year since 1994, with ,80,000 kg applied to .1.2 million hectares of crops in 2010 [11]. Neonicotinoids bind to the postsynaptic nicotinic acetylcholine receptor (nAChRs) in insects, causing over stimulation of the central nervous system leading to paralysis and death [12].They are systemic, rendering the growing plant toxic to insect herbivores and thus reducing or removing the need to apply aerial sprays of insecticides. However, the compounds occur at low levels (0.7 51 mg L21) in both the nectar and pollen of the crop when it flowers, so they are likely to be consumed by pollinators. A recent meta-analysis based on 13 studies of the impacts of imidacloprid on honeybees found that field-realistic doses under laboratory and semi-field conditions had no lethal effects but reduced colony performance by 6 to 20% [13]. It is now becoming clear that subtle sublethal effects of pesticides as described by Desneux et al. [6] can have profound implications at the colony level. For example Henry et al. [9] showed that honeybees, after being fed with sublethal doses of thiomethoxam, had a lower chance of finding their home colony than control bees. Whitehorn et al. [8] simulated exposure of bumblebee colonies to a crop of flowering oilseed rape treated with imidacloprid and describe reduced nest growth and an 85% drop in queen production compared to control colonies. Gill et al. [14] found that bumblebees exposed to imidacloprid exhibited a reduced foraging efficiency under field conditions, particularly when collecting pollen, while Schneider et al. [15] describe reduced foraging activity following exposure of honeybee foragers to low levels of either imidacloprid or clothianidin. These studies suggest that neonicotinoids may indeed be having significant impacts on bees, although how this translates into population-level effects is not clear [16]. However, studies to date have largely used experimentally dosed bees where the bees were unable to avoid feeding on the insecticide. If pollinators are attracted to or repelled by treated crops (compared to controls), then their level of exposure to neonicotinoids could be higher or lower than expected. Previous studies suggest that honeybees avoid imidacloprid in nectar, but the doses used were higher than Figure 1. Mean numbers of arthropods (6 SE) caught per trap per 14 day sampling period (n = 25). A) Diptera; B) Coleoptera; C) Araneae. doi:10.1371/journal.pone.0054819.g001 naturally encountered in nectar of treated crops [17]. Here we describe a simple experiment to assess whether the neonicotinoid insecticide imidacloprid increases or decreases attraction of flying insects to coloured pan traps. Materials and Methods A total of 50 bright yellow rectangular pan traps (1761164 cm) were randomly distributed as 25 pairs in a ,4 ha area of unmanaged neutral grassland at the University of Stirling, Scotland (56u 089 390 N, 3u 549 450 W). The area has not been managed other than by occasional mowing for in excess of 10 years, and contains a diversity of flowers including, for example, Cirsium arvense, Taraxacum officinale, Potentilla reptans, Lathyrus pratensis and Hypochaeris radicata, Pan traps are a standard technique for sampling flower-visiting insects, and yellow is generally the most effective colour to attract large numbers [18]. However, pan traps attract also catch many other flying insects, and they do not contain sugar or floral scents found in flowers, so caution is needed in interpreting patterns of capture as reflecting insect behaviour on real flowers. Trap pairs were situated 1 m apart, and were placed on the ground. All traps were filled with ,250 ml of water plus two drops of detergent (which breaks the surface tension and so improves the catch). In addition, a low concentration of imidacloprid (analytical grade, Sigma-Aldrich, USA) was added to one of each pair at random. Traps were emptied and refilled every 48 h, since imidacloprid can be rapidly degraded by sunlight. All arthropods were preserved in 60% ethanol until they could (...truncated)