Cristina Botías

Bee declines driven by combined stress from parasites, pesticides, and lack of flowers

Conserving pollinator services for crops If pollination fails, ecosystems are eroded and we will lose reliable sources of many critical foodstuffs. Focusing on the pollination services provided by bees, Goulson et al. review the stresses bees are experiencing from climate change, infectious diseases, and insecticides. We can mitigate some of the stress on bees by improving floral resources and adopting quarantine measures, and by surveillance of bee populations. Crucially, we need to resolve the controversy surrounding prophylactic use of pesticides. Science, this issue 10.1126/science.1255957 BACKGROUND The species richness of wild bees and other pollinators has declined over the past 50 years, with some species undergoing major declines and a few going extinct. Evidence of the causes of these losses is patchy and incomplete, owing to inadequate monitoring systems. Managed honey bee stocks have also declined in North America and many European countries, although they have increased substantially in China. During this same period, the demand for insect pollination of crops has approximately tripled, and the importance of wild pollinators in providing such services has become increasingly apparent, leading to concern that we may be nearing a “pollination crisis” in which crop yields begin to fall. This has stimulated much-needed research into the causes of bee declines. Habitat loss, which has reduced the abundance and diversity of floral resources and nesting opportunities, has undoubtedly been a major long-term driver through the 20th century and still continues today. In addition, both wild and managed bees have been exposed to a succession of emerging parasites and pathogens that have been accidentally moved around the world by human action. The intensification of agriculture and increasing reliance on pesticides means that pollinators are also chronically exposed to cocktails of agrochemicals. Predicted changes in global climate are likely to further exacerbate such problems in the future. ADVANCES It has lately become clear that stressors do not act in isolation and that their interactions may be difficult to predict; for example, some pesticides act synergistically rather than additively. Both pesticide exposure and food stress can impair immune responses, rendering bees more susceptible to parasites. It seems certain that chronic exposure to multiple interacting stressors is driving honey bee colony losses and declines of wild pollinators, but the precise combination apparently differs from place to place. Although the causes of pollinator decline may be complex and subject to disagreement, solutions need not be; taking steps to reduce or remove any of these stresses is likely to benefit pollinator health. Several techniques are available that have been demonstrated to effectively increase floral availability in farmland. Similarly, encouraging gardeners to grow appropriate bee-friendly flowers and to improve management of amenity grasslands can also reduce dietary stress. Retaining or restoring areas of seminatural habitat within farmland will improve nest site availability. A return to the principles of integrated pest management and avoidance of prophylactic use of agrochemicals could greatly decrease exposure of bees to pesticides. OUTLOOK Interactions among agrochemicals and stressors are not addressed by current regulatory procedures, which typically expose well-fed, parasite-free bees to a single pesticide for a short period of time. Devising approaches to study these interactions and incorporating them into the regulatory process poses a major challenge. In the meantime, providing support and advice for farmers in more sustainable farming methods with reduced pesticide use is likely to have broad benefits for farmland biodiversity. Enforcing effective quarantine measures on bee movements to prevent further spread of bee parasites is also vital. Finally, effective monitoring of wild pollinator populations is urgently needed to inform management strategies. Without this, we have no early warning system to tell us how close we may be to a pollination crisis. With a growing human population and rapid growth in global demand for pollination services, we cannot afford to see crop yields begin to fall, and we would be well advised to take preemptive action to ensure that we have adequate pollination services into the future. Multiple interacting stressors drive bee declines. Both wild and managed bees are subject to a number of important and interacting stressors. For example, exposure to some fungicides can greatly increase the toxicity of insecticides, whereas exposure to insecticides reduces resistance to diseases. Dietary stresses are likely to reduce the ability of bees to cope with both toxins and pathogens. Photo credit: DAVE GOULSON Bees are subject to numerous pressures in the modern world. The abundance and diversity of flowers has declined; bees are chronically exposed to cocktails of agrochemicals, and they are simultaneously exposed to novel parasites accidentally spread by humans. Climate change is likely to exacerbate these problems in the future. Stressors do not act in isolation; for example, pesticide exposure can impair both detoxification mechanisms and immune responses, rendering bees more susceptible to parasites. It seems certain that chronic exposure to multiple interacting stressors is driving honey bee colony losses and declines of wild pollinators, but such interactions are not addressed by current regulatory procedures, and studying these interactions experimentally poses a major challenge. In the meantime, taking steps to reduce stress on bees would seem prudent; incorporating flower-rich habitat into farmland, reducing pesticide use through adopting more sustainable farming methods, and enforcing effective quarantine measures on bee movements are all practical measures that should be adopted. Effective monitoring of wild pollinator populations is urgently needed to inform management strategies into the future.

Neonicotinoid Residues in Wildflowers, a Potential Route of Chronic Exposure for Bees

In recent years, an intense debate about the environmental risks posed by neonicotinoids, a group of widely used, neurotoxic insecticides, has been joined. When these systemic compounds are applied to seeds, low concentrations are subsequently found in the nectar and pollen of the crop, which are then collected and consumed by bees. Here we demonstrate that the current focus on exposure to pesticides via the crop overlooks an important factor: throughout spring and summer, mixtures of neonicotinoids are also found in the pollen and nectar of wildflowers growing in arable field margins, at concentrations that are sometimes even higher than those found in the crop. Indeed, the large majority (97%) of neonicotinoids brought back in pollen to honey bee hives in arable landscapes was from wildflowers, not crops. Both previous and ongoing field studies have been based on the premise that exposure to neonicotinoids would occur only during the blooming period of flowering crops and that it may be diluted by bees also foraging on untreated wildflowers. Here, we show that exposure is likely to be higher and more prolonged than currently recognized because of widespread contamination of wild plants growing near treated crops.

Widespread contamination of wildflower and bee-collected pollen with complex mixtures of neonicotinoids and fungicides commonly applied to crops

There is considerable and ongoing debate as to the harm inflicted on bees by exposure to agricultural pesticides. In part, the lack of consensus reflects a shortage of information on field-realistic levels of exposure. Here, we quantify concentrations of neonicotinoid insecticides and fungicides in the pollen of oilseed rape, and in pollen of wildflowers growing near arable fields. We then compare this to concentrations of these pesticides found in pollen collected by honey bees and in pollen and adult bees sampled from bumble bee colonies placed on arable farms. We also compared this with levels found in bumble bee colonies placed in urban areas. Pollen of oilseed rape was heavily contaminated with a broad range of pesticides, as was the pollen of wildflowers growing nearby. Consequently, pollen collected by both bee species also contained a wide range of pesticides, notably including the fungicides carbendazim, boscalid, flusilazole, metconazole, tebuconazole and trifloxystrobin and the neonicotinoids thiamethoxam, thiacloprid and imidacloprid. In bumble bees, the fungicides carbendazim, boscalid, tebuconazole, flusilazole and metconazole were present at concentrations up to 73nanogram/gram (ng/g). It is notable that pollen collected by bumble bees in rural areas contained high levels of the neonicotinoids thiamethoxam (mean 18ng/g) and thiacloprid (mean 2.9ng/g), along with a range of fungicides, some of which are known to act synergistically with neonicotinoids. Pesticide exposure of bumble bee colonies in urban areas was much lower than in rural areas. Understanding the effects of simultaneous exposure of bees to complex mixtures of pesticides remains a major challenge.

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: 1.4-11ng/g) with the levels found in pollen collected from the same plants (range: 1.4-22ng/g). We then analysed residue levels in foliage from non-target plants growing in the crop field margins (range: ≤0.02-106ng/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.

Preliminary data on carrion insects in urban (indoor and outdoor) and periurban environments in central Spain

Although most cases involving entomological evidence occur in urban environments and under indoor conditions, there is a lack of studies determining the insect fauna of forensic importance in those environments. In the current paper we provide the first data on the composition of the forensically important insect species occurring in periurban and both indoor and outdoor urban environments in central Spain. Insects were collected fortnightly by means of carrion-baited traps, uninterruptedly during one year. Most species and individuals were collected in the periurban site, whereas the indoor urban site showed the lowest number of species and captures. Moreover, the composition of species differed among environments and seasons. A few species occurred under both indoor and outdoor conditions, including the blowfly Calliphora vicina and some Sarcophagidae species. These preliminary results suggest interesting differences in the insect composition between environments and conditions which may be of forensic importance, and represent a first step to further research into the application of insects to forensic investigations in urban environments of central Spain.

No effect of low-level chronic neonicotinoid exposure on bumblebee learning and fecundity

In recent years, many pollinators have declined in abundance and diversity worldwide, presenting a potential threat to agricultural productivity, biodiversity and the functioning of natural ecosystems. One of the most debated factors proposed to be contributing to pollinator declines is exposure to pesticides, particularly neonicotinoids, a widely used class of systemic insecticide. Also, newly emerging parasites and diseases, thought to be spread via contact with managed honeybees, may pose threats to other pollinators such as bumblebees. Compared to honeybees, bumblebees could be particularly vulnerable to the effects of stressors due to their smaller and more short-lived colonies. Here, we studied the effect of field-realistic, chronic clothianidin exposure and inoculation with the parasite Nosema ceranae on survival, fecundity, sugar water collection and learning using queenless Bombus terrestris audax microcolonies in the laboratory. Chronic exposure to 1 ppb clothianidin had no significant effects on the traits studied. Interestingly, pesticide exposure in combination with additional stress caused by harnessing bees for Proboscis Extension Response (PER) learning assays, led to an increase in mortality. In contrast to previous findings, the bees did not become infected by N. ceranae after experimental inoculation with the parasite spores, suggesting variability in host resistance or parasite virulence. However, this treatment induced a slight, short-term reduction in sugar water collection, potentially through stimulation of the immune system of the bees. Our results suggest that chronic exposure to 1 ppb clothianidin does not have adverse effects on bumblebee fecundity or learning ability.

The combined effects of a monotonous diet and exposure to thiamethoxam on the performance of bumblebee micro-colonies

There is a pressing need to better understand the factors contributing to declines of wild pollinators such as bumblebees. Many different contributors have been postulated including: loss of flower-rich habitats and nesting sites; monotonous diets; impacts of invasive pathogens; exposure to pesticides such as neonicotinoids. Past research has tended to investigate the impacts of these stressors in isolation, despite the increasing recognition that bees are simultaneously exposed to a combination of stressors, with potentially additive or synergistic effects. No studies to date have investigated the combined effects of a monotonous diet and exposure to pesticides. Using queenless micro-colonies of Bombus terrestris audax, we examined this interaction by providing bees with monofloral or polyfloral pollen that was either contaminated with field-realistic levels of thiamethoxam, a commonly used neonicotinoid, or not contaminated. Both treatments were found to have a significant effect on various parameters relating to micro-colony performance. Specifically, both pesticide-treated micro-colonies and those fed monofloral pollen grew more slowly than those given polyfloral pollen or pollen without pesticides. The two factors appeared to act additively. Micro-colonies given monofloral pollens also exhibited lower reproductive efforts and produced smaller drones. Although further research is needed to examine whether similar effects are found in whole colonies, these findings increase our understanding of the likely effects of multiple stressors associated with agricultural intensification on bee declines.

Qualifying pollinator decline evidence—response.

Ghazoul is accurate in pointing out that we have no population data on the majority of pollinators, that the data we do have are biased toward a small number of taxa (bumblebees, honey bees, and butterflies), and that data are far better for Europe and North America than for elsewhere. These points

Response to Comment on “Neonicotinoid Residues in Wildflowers, A Potential Route of Chronic Exposure for Bees”

Many previous studies report nectar residues being consistently lower than pollen residues in the same plant species. This is also evident in our samples from the oilseed rape (OSR) crop, where 100% of pollen samples contained thiamethoxam, whereas only 53.9% of the nectar samples had detectable levels of this compound. However, as clearly explained in our manuscript, our wildflower nectar and pollen samples were hand collected from different subsets of plant species−because some species produce plentiful pollen but little nectar, and others vice versa. Since the samples are from different species and were sometimes pooled, it is not surprising that they differ in levels of contamination. However, it should be mentioned that frequency of detections for thiamethoxam in pollen and nectar collected from wildflowers growing in OSR margins were 58.1 and 20.8% respectively, showing a similar relative proportion to what was found for OSR pollen and nectar (see above).