Impact of controlled neonicotinoid exposure on bumblebees in a realistic field setting

1. Pesticide exposure has been implicated as a contributor to insect pollinator declines. In social bees, which are crucial pollination service providers, the effect of low-level chronic exposure is typically non-lethal leading researchers to consider whether exposure induces sub-lethal effects on behaviour and whether such impairment can affect colony development. 2. Studies under laboratory conditions can control levels of pesticide exposure and elucidate causative effects, but are often criticised for being unrealistic. In contrast, field studies can monitor bee responses under a more realistic pesticide exposure landscape; yet typically such findings are limited to correlative results, and can lack true controls or sufficient replication. We attempt to bridge this gap by exposing bumblebees to known amounts of pesticides when colonies are placed in the field. 3. Using 20 bumblebee colonies, we assess the consequences of exposure to the neonicotinoid clothianidin, provided in sucrose at a concentration of five parts per billion, over five weeks. We monitored foraging patterns and pollen collecting performance from 3282 bouts using either a non-invasive photographic assessment, or by extracting the pollen from returning foragers. We also conducted a full colony census at the beginning and end of the experiment. 4. In contrast to studies on other neonicotinoids, showing clear impairment to foraging behaviours, we detected only subtle changes to patterns of foraging activity and pollen foraging during the course of the experiment. However, our colony census measures showed a more pronounced effect of exposure, with fewer adult workers and sexuals in treated colonies after five weeks. 5. Synthesis and applications. Pesticide induced impairments on colony development and foraging could impact on the pollination service that bees provide. Therefore our findings, that bees show subtle changes in foraging behaviour and reductions in colony size after exposure to a common pesticide, has important implications and helps to inform the debate over whether the benefits of systemic pesticide application to flowering crops outweigh the costs. We propose that our methodology is an important advance to previous semi-field methods and should be considered when considering improvements to current ecotoxicological guidelines for pesticide risk assessment

Contamination of wild plants near neonicotinoid seed-treated crops, and implications for non-target insects

Neonicotinoid insecticides are commonly-used as seed treatments on flowering crops such as oilseed rape. Their persistence and solubility in water increase the chances of environmental contamination via surface-runoff or drainage into areas adjacent to the crops. However, their uptake and fate into non-target vegetation remains poorly understood. In this study, we analysed samples of foliage collected from neonicotinoid seed-treated oilseed rape plants and also compared the levels of neonicotinoid residues in foliage (range: 1.4 – 11 ng/g) with the levels found in pollen collected from the same plants (range: 1.4 – 22 ng/g). We then analysed residue levels in foliage from non-target plants growing in the crop field margins (range: ≤ 0.02 – 106 ng/g). Finally, in order to assess the possible risk posed by the peak levels of neonicotinoids that we detected in foliage for farmland phytophagous and predatory insects, we compared the maximum concentrations found against the LC50 values reported in the literature for a set of relevant insect species. Our results suggest that neonicotinoid seed-dressings lead to widespread contamination of the foliage of field margin plants with mixtures of neonicotinoid residues, where levels are very variable and discontinuous, but sometimes overlap with lethal concentrations reported for some insect species. Understanding the distribution of pesticides in the environment and their potential effects on biological communities is crucial to properly assess current agricultural management and schemes with biodiversity conservation aims in farmland

Bumble bee parasite strains vary in resistance to phytochemicals

Nectar and pollen contain diverse phytochemicals that can reduce disease in pollinators. However, prior studies showed variable effects of nectar chemicals on infection, which could reflect variable phytochemical resistance among parasite strains. Inter-strain variation in resistance could influence evolutionary interactions between plants, pollinators, and pollinator disease, but testing direct effects of phytochemicals on parasites requires elimination of variation between bees. Using cell cultures of the bumble bee parasite Crithidia bombi, we determined (1) growth-inhibiting effects of nine floral phytochemicals and (2) variation in phytochemical resistance among four parasite strains. C. bombi growth was unaffected by naturally occurring concentrations of the known antitrypanosomal phenolics gallic acid, caffeic acid, and chlorogenic acid. However, C. bombi growth was inhibited by anabasine, eugenol, and thymol. Strains varied >3-fold in phytochemical resistance, suggesting that selection for phytochemical resistance could drive parasite evolution. Inhibitory concentrations of thymol (4.53-22.2 ppm) were similar to concentrations in Thymus vulgaris nectar (mean 5.2 ppm). Exposure of C. bombi to naturally occurring levels of phytochemicals—either within bees or during parasite transmission via flowers—could influence infection in nature. Flowers that produce antiparasitic phytochemical, including thymol, could potentially reduce infection in Bombus populations, thereby counteracting a possible contributor to pollinator decline

Neonicotinoid Insecticides and Their Impacts on Bees: A Systematic Review of Research Approaches and Identification of Knowledge Gaps

It has been suggested that the widespread use of neonicotinoid insecticides threatens bees, but research on this topic has been surrounded by controversy. In order to synthesize which research approaches have been used to examine the effect of neonicotinoids on bees and to identify knowledge gaps, we systematically reviewed research on this subject that was available on the Web of Science and PubMed in June 2015. Most of the 216 primary research studies were conducted in Europe or North America (82%), involved the neonicotinoid imidacloprid (78%), and concerned the western honey bee Apis mellifera (75%). Thus, little seems to be known about neonicotinoids and bees in areas outside Europe and North America. Furthermore, because there is considerable variation in ecological traits among bee taxa, studies on honey bees are not likely to fully predict impacts of neonicotinoids on other species. Studies on crops were dominated by seed-treated maize, oilseed rape (canola) and sunflower, whereas less is known about potential side effects on bees from the use of other application methods on insect pollinated fruit and vegetable crops, or on lawns and ornamental plants. Laboratory approaches were most common, and we suggest that their capability to infer real-world consequences are improved when combined with information from field studies about realistic exposures to neonicotinoids. Studies using field approaches often examined only bee exposure to neonicotinoids and more field studies are needed that measure impacts of exposure. Most studies measured effects on individual bees. We suggest that effects on the individual bee should be linked to both mechanisms at the sub-individual level and also to the consequences for the colony and wider bee populations. As bees are increasingly facing multiple interacting pressures future research needs to clarify the role of neonicotinoids in relative to other drivers of bee declines

Neonicotinoids override a parasite exposure impact on hibernation success of a key bumblebee pollinator

1. The persistence of both geographical and reproductive boundaries between related species poses a fundamental puzzle in biology. Reproductive interactions between species can have a substantial impact on the maintenance of a boundary, potentially contributing to its collapse (e.g. via hybridisation) or facilitating reproductive isolation (e.g. via reinforcement). 2. The degree to which two parapatric insect species in the genus Phymata are reproductively isolated was evaluated and several mechanisms that could contribute to the maintenance of species boundaries were assessed. 3. Behavioural assays showed no indication of species-assortative mating, nor any fecundity costs associated with heterospecific mating. Thus, there was no evidence of prezygotic mechanisms of reproductive isolation between the two species. 4.In laboratory crosses, it was found that the two species were indeed capable of producing viable F1 hybrids. Morphologically, these hybrids were phenotypically intermediate to the two parental species, and similar to the phenotypes seen in natural populations thought to occur in a hybrid zone. F1 hybrids did not show reduced viability, although there was some suggestion of ‘hybrid breakdown’, evident from the lower viability observed for progeny of ‘natural hybrids’. 5. Collectively, we show that despite genetically based morphological differences between species, P. americana and pennsylvanica can, and probably do hybridise. More studies are needed to understand the mechanisms that maintain the distinct phenotypes and geographical ranges of these species, despite the considerable potential for introgression

Impact of Chronic Neonicotinoid Exposure on Honeybee Colony Performance and Queen Supersedure

Background Honeybees provide economically and ecologically vital pollination services to crops and wild plants. During the last decade elevated colony losses have been documented in Europe and North America. Despite growing consensus on the involvement of multiple causal factors, the underlying interactions impacting on honeybee health and colony failure are not fully resolved. Parasites and pathogens are among the main candidates, but sublethal exposure to widespread agricultural pesticides may also affect bees. Methodology/Principal Findings To investigate effects of sublethal dietary neonicotinoid exposure on honeybee colony performance, a fully crossed experimental design was implemented using 24 colonies, including sister-queens from two different strains, and experimental in-hive pollen feeding with or without environmentally relevant concentrations of thiamethoxam and clothianidin. Honeybee colonies chronically exposed to both neonicotinoids over two brood cycles exhibited decreased performance in the short-term resulting in declining numbers of adult bees (−28%) and brood (−13%), as well as a reduction in honey production (−29%) and pollen collections (−19%), but colonies recovered in the medium-term and overwintered successfully. However, significantly decelerated growth of neonicotinoid-exposed colonies during the following spring was associated with queen failure, revealing previously undocumented long-term impacts of neonicotinoids: queen supersedure was observed for 60% of the neonicotinoid-exposed colonies within a one year period, but not for control colonies. Linked to this, neonicotinoid exposure was significantly associated with a reduced propensity to swarm during the next spring. Both short-term and long-term effects of neonicotinoids on colony performance were significantly influenced by the honeybees’ genetic background. Conclusions/Significance Sublethal neonicotinoid exposure did not provoke increased winter losses. Yet, significant detrimental short and long-term impacts on colony performance and queen fate suggest that neonicotinoids may contribute to colony weakening in a complex manner. Further, we highlight the importance of the genetic basis of neonicotinoid susceptibility in honeybees which can vary substantially

Model-based estimates of contrasts and corresponding significance levels of the treatment effect (neonicotinoid <i>versus</i> control) and honeybee genetics (strain A <i>vs.</i> strain B).

<p>Results are shown in the transformed scale for the three response variables adult bees, eggs and larvae and pupae assessed directly after the 1.5 months of treatment (Summer 2011), 3.5 months later (Autumn 2011) and 1 year later (Spring 2012). For adult bees and eggs and larvae (the models that included a significant threefold interaction between treatment, honeybee strain and assessment date) contrasts for treatment effects were also computed within individual honeybee strains at each assessment date. <i>P</i> values are adjusted for multiple testing. ***<i>P</i><0.001; **<i>P</i><0.01; *<i>P</i><0.05; <b>·</b> 0.05<<i>P</i><0.1.</p

Pollen collections.

<p>Mean (±SD) fresh weights of pollen collections for control (black) and neonicotinoid-exposed (white) colonies over the course of the treatment period (pollen-trap contents were weighed in 2-2–3 days intervals throughout the study).</p