Elizabeth Nicholls

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.

Bees associate colour cues with differences in pollen rewards

In contrast to the wealth of knowledge concerning sucrose-rewarded learning, the question of whether bees learn when they collect pollen from flowers has been little addressed. The nutritional value of pollen varies considerably between species, and it may be that bees learn the features of flowers that produce pollen best suited to the dietary requirements of their larvae. It is still unknown, however, whether a non-ingestive reward pathway for pollen learning exists, and how foraging bees sense differences between pollen types. Here we adopt a novel experimental approach testing the learning ability of bees with pollen rewards. Bumblebees were reared under controlled laboratory conditions. To establish which pollen rewards are distinguishable, individual bees were given the choice of collecting two types of pollen, diluted to varying degrees with indigestible α-cellulose. Bees preferentially collected a particular pollen type, but this was not always the most concentrated sample. Preferences were influenced by the degree of similarity between samples and also by the period of exposure, with bees more readily collecting samples of lower pollen concentration after five trials. When trained differentially, bees were able to associate an initially less-preferred contextual colour with the more concentrated sample, whilst their pollen preferences did not change. Successful learning of contextual cues seems to maintain pollen foraging preferences over repeated exposures, suggesting that fast learning of floral cues may preclude continuous sampling and evaluation of alternative reward sources, leading to constancy in pollen foraging.

Assessment of pollen rewards by foraging bees

Summary The removal of pollen by flower-visiting insects is costly to plants, not only in terms of production, but also via lost reproductive potential. Modern angiosperms have evolved various reward strategies to limit these costs, yet many plant species still offer pollen as a sole or major reward for pollinating insects. The benefits plants gain by offering pollen as a reward for pollinating are defined by the behaviour of their pollinators, some of which feed on the pollen at the flower, while others collect pollen to provision offspring. We explore how pollen impacts on the behaviour and foraging decisions of pollen-collecting bees, drawing comparisons with what is known for nectar rewards. This question is of particular interest since foraging bees typically do not eat pollen during collection, meaning the sensory pathways involved in evaluating this resource are not immediately obvious. Previous research has focussed on whether foraging bees can determine the quality of pollen sources offered by different plant species, and attempted to infer the mechanisms underpinning such evaluations, mainly through observations of collection preferences in the field More recently experimental research has started to ask whether pollen itself can mediate the detection of, and learning about, pollen sources and associated floral cues. We review advancements in the understanding of how bees forage for pollen and respond to variation in pollen quality, and discuss future directions for studying how this ancestral floral food reward shapes the behaviour of pollinating insects. A lay summary is available for this article.

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.

Optimal search patterns in honeybee orientation flights are robust against emerging infectious diseases

Lévy flights are scale-free (fractal) search patterns found in a wide range of animals. They can be an advantageous strategy promoting high encounter rates with rare cues that may indicate prey items, mating partners or navigational landmarks. The robustness of this behavioural strategy to ubiquitous threats to animal performance, such as pathogens, remains poorly understood. Using honeybees radar-tracked during their orientation flights in a novel landscape, we assess for the first time how two emerging infectious diseases (Nosema sp. and the Varroa-associated Deformed wing virus (DWV)) affect bees’ behavioural performance and search strategy. Nosema infection, unlike DWV, affected the spatial scale of orientation flights, causing significantly shorter and more compact flights. However, in stark contrast to disease-dependent temporal fractals, we find the same prevalence of optimal Lévy flight characteristics (μ ≈ 2) in both healthy and infected bees. We discuss the ecological and evolutionary implications of these surprising insights, arguing that Lévy search patterns are an emergent property of fundamental characteristics of neuronal and sensory components of the decision-making process, making them robust against diverse physiological effects of pathogen infection and possibly other stressors.

Pollen Elicits Proboscis Extension but Does not Reinforce PER Learning in Honeybees

The function of pollen as a reward for foraging bees is little understood, though there is evidence to suggest that it can reinforce associations with visual and olfactory floral cues. Foraging bees do not feed on pollen, thus one could argue that it cannot serve as an appetitive reinforcer in the same way as sucrose. However, ingestion is not a critical parameter for sucrose reinforcement, since olfactory proboscis extension (PER) learning can be conditioned through antennal stimulation only. During pollen collection, the antennae and mouthparts come into contact with pollen, thus it is possible that pollen reinforces associative learning through similar gustatory pathways as sucrose. Here pollen was presented as the unconditioned stimulus (US), either in its natural state or in a 30% pollen-water solution, and was found to elicit proboscis extension following antennal stimulation. Control groups were exposed to either sucrose or a clean sponge as the US, or an unpaired presentation of the conditioned stimulus (CS) and pollen US. Despite steady levels of responding to the US, bees did not learn to associate a neutral odour with the delivery of a pollen reward, thus whilst pollen has a proboscis extension releasing function, it does not reinforce olfactory PER learning.

Larval exposure to field-realistic concentrations of clothianidin has no effect on development rate, over-winter survival or adult metabolic rate in a solitary bee, Osmia bicornis

There is widespread concern regarding the effects of agro-chemical exposure on bee health, of which neonicotinoids, systemic insecticides detected in the pollen and nectar of both crops and wildflowers, have been the most strongly debated. The majority of studies examining the effect of neonicotinoids on bees have focussed on social species, namely honey bees and bumble bees. However, most bee species are solitary, their life histories differing considerably from these social species, and thus it is possible that their susceptibility to pesticides may be quite different. Studies that have included solitary bees have produced mixed results regarding the impact of neonicotinoid exposure on survival and reproductive success. While the majority of studies have focused on the effects of adult exposure, bees are also likely to be exposed as larvae via the consumption of contaminated pollen. Here we examined the effect of exposure of Osmia bicornis larvae to a range of field-realistic concentrations (0–10 ppb) of the neonicotinoid clothianidin, observing no effect on larval development time, overwintering survival or adult weight. Flow-through respirometry was used to test for latent effects of larval exposure on adult physiological function. We observed differences between male and female bees in the propensity to engage in discontinuous gas exchange; however, no effect of larval clothianidin exposure was observed. Our results suggest that previously reported adverse effects of neonicotinoids on O. bicornis are most likely mediated by impacts on adults.

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