The neonicotinoid insecticide Imidacloprid repels pollinating flies and beetles at field-realistic concentrations

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 μg L-1, with Diptera avoiding concentrations as low as 0.01 μg L-1. 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 μg L-1), 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. © 2013 Easton, Goulson

The Effects of Aphid Traits on Parasitoid Host Use and Specialist Advantage

Specialization is a central concept in ecology and one of the fundamental properties of parasitoids. Highly specialized parasitoids tend to be more efficient in host-use compared to generalized parasitoids, presumably owing to the trade-off between host range and hostuse efficiency. However, it remains unknown how parasitoid host specificity and host-use depends on host traits related to susceptibility to parasitoid attack. To address this question, we used data from a 13-year survey of interactions among 142 aphid and 75 parasitoid species in nine European countries. We found that only aphid traits related to local resource characteristics seem to influence the trade-off between host-range and efficiency: more specialized parasitoids had an apparent advantage (higher abundance on shared hosts) on aphids with sparse colonies, ant-attendance and without concealment, and this was more evident when host relatedness was included in calculation of parasitoid specificity. More traits influenced average assemblage specialization, which was highest in aphids that are monophagous, monoecious, large, highly mobile (easily drop from a plant), without myrmecophily, habitat specialists, inhabit non-agricultural habitats and have sparse colonies. Differences in aphid wax production did not influence parasitoid host specificity and host-use. Our study is the first step in identifying host traits important for aphid parasitoid host specificity and host-use and improves our understanding of bottom-up effects of aphid traits on aphid-parasitoid food web structure

Use of an innovative T-tube maze assay and the proboscis extension response assay to assess sublethal effects of GM products and pesticides on learning capacity of the honey bee Apis mellifera L.

Transgenic Cry1Ac+CpTI cotton (CCRI41) is a promising cotton cultivar throughout China but side effects and especially sublethal effects of this transgenic cultivar on beneficial insects remain poorly studied. More specifically potential sublethal effects on behavioural traits of the honey bee Apis mellifera L. have not been formally assessed despite the importance of honey bees for pollination. The goal of our study was to assess potential effects of CCRI41 cotton pollen on visual and olfactory learning by honey bees. After a 7-day oral chronic exposure to honey mixed with either CCRI41 pollen, imidacloprid-treated conventional pollen (used as positive sublethal control) or conventional pollen (control), learning performance was evaluated by the classical proboscis extension reflex (PER) procedure as well as a T-tube maze test. The latter assay was designed as a new device to assess potential side effects of pesticides on visual associative learning of honey bees. These two procedures were complementary because the former focused on olfactory learning while the latter was involved in visual learning based on visual orientation ability. Oral exposure to CCRI41 pollen did not affect learning capacities of honey bees in both the T-tube maze and PER tests. However, exposure to imidacloprid resulted in reduced visual learning capacities in T-tube maze evaluation and decreased olfactory learning performances measured with PER. The implications of these results are discussed in terms of risks of transgenic CCRI41 cotton crops for honey bees

Quantification of toxins in a Cry1Ac + CpTI cotton cultivar and its potential effects on the honey bee Apis mellifera L.

Transgenic Cry1Ac + CpTI cotton (CCRI41) is increasingly planted throughout China. However, negative effects of this cultivar on the honey bee Apis mellifera L., the most important pollinator for cultivated ecosystem, remained poorly investigated. The objective of our study was to evaluate the potential side effects of transgenic Cry1Ac + CpTI pollen from cotton on young adult honey bees A. mellifera L. Two points emphasized the significance of our study: (1) A higher expression level of insecticidal protein Cry1Ac in pollen tissues was detected (when compared with previous reports). In particular, Cry1Ac protein was detected at 300 ± 4.52 ng g−1 [part per billion (ppb)] in pollen collected in July, (2) Effects on chronic mortality and feeding behaviour in honey bees were evaluated using a no-choice dietary feeding protocol with treated pollen, which guarantee the highest exposure level to bees potentially occurring in natural conditions (worst case scenario). Tests were also conducted using imidacloprid-treated pollen at a concentration of 48 ppb as positive control for sublethal effect on feeding behaviour. Our results suggested that Cry1Ac + CpTI pollen carried no lethal risk for honey bees. However, during a 7-day oral exposure to the various treatments (transgenic, imidacloprid-treated and control), honey bee feeding behaviour was disturbed and bees consumed significantly less CCRI41 cotton pollen than in the control group in which bees were exposed to conventional cotton pollen. It may indicate an antifeedant effect of CCRI41 pollen on honey bees and thus bees may be at risk because of large areas are planted with transgenic Bt cotton in China. This is the first report suggesting a potential sublethal effect of CCRI41 cotton pollen on honey bees. The implications of the results are discussed in terms of risk assessment for bees as well as for directions of future work involving risk assessment of CCRI41 cotton

Choosing Organic Pesticides over Synthetic Pesticides May Not Effectively Mitigate Environmental Risk in Soybeans

Background: Selection of pesticides with small ecological footprints is a key factor in developing sustainable agricultural systems. Policy guiding the selection of pesticides often emphasizes natural products and organic-certified pesticides to increase sustainability, because of the prevailing public opinion that natural products are uniformly safer, and thus more environmentally friendly, than synthetic chemicals. Methodology/Principal Findings: We report the results of a study examining the environmental impact of several new synthetic and certified organic insecticides under consideration as reduced-risk insecticides for soybean aphid (Aphis glycines) control, using established and novel methodologies to directly quantify pesticide impact in terms of biocontrol services. We found that in addition to reduced efficacy against aphids compared to novel synthetic insecticides, organic approved insecticides had a similar or even greater negative impact on several natural enemy species in lab studies, were more detrimental to biological control organisms in field experiments, and had higher Environmental Impact Quotients at field use rates. Conclusions/Significance: These data bring into caution the widely held assumption that organic pesticides are more environmentally benign than synthetic ones. All pesticides must be evaluated using an empirically-based risk assessment

Multiple Routes of Pesticide Exposure for Honey Bees Living Near Agricultural Fields

Populations of honey bees and other pollinators have declined worldwide in recent years. A variety of stressors have been implicated as potential causes, including agricultural pesticides. Neonicotinoid insecticides, which are widely used and highly toxic to honey bees, have been found in previous analyses of honey bee pollen and comb material. However, the routes of exposure have remained largely undefined. We used LC/MS-MS to analyze samples of honey bees, pollen stored in the hive and several potential exposure routes associated with plantings of neonicotinoid treated maize. Our results demonstrate that bees are exposed to these compounds and several other agricultural pesticides in several ways throughout the foraging period. During spring, extremely high levels of clothianidin and thiamethoxam were found in planter exhaust material produced during the planting of treated maize seed. We also found neonicotinoids in the soil of each field we sampled, including unplanted fields. Plants visited by foraging bees (dandelions) growing near these fields were found to contain neonicotinoids as well. This indicates deposition of neonicotinoids on the flowers, uptake by the root system, or both. Dead bees collected near hive entrances during the spring sampling period were found to contain clothianidin as well, although whether exposure was oral (consuming pollen) or by contact (soil/planter dust) is unclear. We also detected the insecticide clothianidin in pollen collected by bees and stored in the hive. When maize plants in our field reached anthesis, maize pollen from treated seed was found to contain clothianidin and other pesticides; and honey bees in our study readily collected maize pollen. These findings clarify some of the mechanisms by which honey bees may be exposed to agricultural pesticides throughout the growing season. These results have implications for a wide range of large-scale annual cropping systems that utilize neonicotinoid seed treatments

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

Field realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency

Bumblebees and other pollinators provide a vital ecosystem service for the agricultural sector. Recent studies however have suggested that exposure to systemic neonicotinoid insecticides in flowering crops has sub-lethal effects on the bumblebee workforce, and hence in reducing queen production. The mechanism behind reduced nest performance, however, remains unclear. Here we use Radio Frequency Identification (RFID) technology to test whether exposure to a low, field realistic dose (0.7 ppb in sugar water and 6 ppb in pollen) of the neonicotinoid imidacloprid, reduces worker foraging efficiency. Whilst the nectar foraging efficiency of bees treated with imidacloprid was not significantly different than that of control bees, treated bees brought back pollen less often than control bees (40 % of trips vs 63 % trips, respectively) and, where pollen was collected, treated bees brought back 31 % less pollen per hour than controls. This study demonstrates that field-realistic doses of these pesticides substantially impacts on foraging ability of bumblebee workers when collecting pollen, and we suggest that this provides a causal mechanism behind reduced queen production in imidacloprid exposed colonies

Combined pesticide exposure severely affects individual- and colony-level traits in bees

Reported widespread declines of wild and managed insect pollinators have serious consequences for global ecosystem services and agricultural production [1–3]. Bees contribute approximately 80% of insect pollination, so it is important to understand and mitigate the causes of current declines in bee populations [4–6]. Recent studies have implicated the role of pesticides in these declines, as exposure to these chemicals has been associated with changes in bee behaviour [7–11] and reductions in colony queen production [12]. However, the key link between changes in individual behaviour and the consequent impact at the colony level has not been shown. Social bee colonies depend on the collective performance of many individual workers. Thus, although field-level pesticide concentrations can have subtle or sublethal effects at the individual level [8], it is not known whether bee societies can buffer such effects or whether it results in a severe cumulative effect at the colony level. Furthermore, widespread agricultural intensification means that bees are exposed to numerous pesticides when foraging [13–15], yet the possible combinatorial effects of pesticide exposure have rarely been investigated [16,17]. Here we show that chronic exposure of bumblebees to two pesticides (neonicotinoid and pyrethroid) at concentrations that could approximate field-level exposure impairs natural foraging behaviour and increases worker mortality leading to significant reductions in brood development and colony success. We found that worker foraging performance, particularly pollen collecting efficiency, was significantly reduced with observed knock-on effects for forager recruitment, worker losses and overall worker productivity. Moreover, we provide evidence that combinatorial exposure to pesticides increases the propensity of colonies to fail