Ellen L. Rotheray

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.

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.

Floral abundance and resource quality influence pollinator choice

Pollinator declines caused by forage habitat loss threaten insect pollination services. Pollinating insects depend on adequate floral resources, and their ability to track these resources. Variability of these resources and the effect on insect foraging choice is poorly understood. We record patterns of visitation to six wildflower species and test the hypotheses that: pollinators preferentially visit the most rewarding flowers; nectar diurnal variations affect foraging preferences; pollinators respond most strongly to nectar rewards. Nectar volume and sugar concentration were negatively correlated within plant species over time of day where greater concentration and lower volume was evident in the afternoon, but this did not correspond to pollinator visitation. Both floral abundance and nectar quality (total sugar per inflorescence) positively affect insect visitation. For some foragers, the positive effects of high‐quality rewards were only evident when floral abundance was high (>50 inflorescences per patch), perhaps reflecting the low probability of pollinators detecting scarce rewards. Pollen quality (total protein per inflorescence) was negatively related to visitation of Apis mellifera and Bombus pascuorum. Fewer pollinators visiting flowers of higher pollen quality could reflect plant allocation trade‐offs or the presence of secondary metabolites in pollen, meaning pollen foraging is likely affected by factors other than protein concentration. Nectar rather than pollen appeared to be the main driver of floral choice by insects in this system. Conservation schemes for bees in farmland or gardens might benefit from ensuring that rewarding plant species are present at high density and/or are aggregated in space.

Bumblebee Pupae Contain High Levels of Aluminium

The causes of declines in bees and other pollinators remains an on-going debate. While recent attention has focussed upon pesticides, other environmental pollutants have largely been ignored. Aluminium is the most significant environmental contaminant of recent times and we speculated that it could be a factor in pollinator decline. Herein we have measured the content of aluminium in bumblebee pupae taken from naturally foraging colonies in the UK. Individual pupae were acid-digested in a microwave oven and their aluminium content determined using transversely heated graphite furnace atomic absorption spectrometry. Pupae were heavily contaminated with aluminium giving values between 13.4 and 193.4 μg/g dry wt. and a mean (SD) value of 51.0 (33.0) μg/g dry wt. for the 72 pupae tested. Mean aluminium content was shown to be a significant negative predictor of average pupal weight in colonies. While no other statistically significant relationships were found relating aluminium to bee or colony health, the actual content of aluminium in pupae are extremely high and demonstrate significant exposure to aluminium. Bees rely heavily on cognitive function and aluminium is a known neurotoxin with links, for example, to Alzheimer’s disease in humans. The significant contamination of bumblebee pupae by aluminium raises the intriguing spectre of cognitive dysfunction playing a role in their population decline.

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

Differences in ecomorphology and microhabitat use of four saproxylic larvae (Diptera, Syrphidae) in Scots pine stump rot holes

Co‐existence and microhabitat partitioning was explored in larvae of four species of hoverfly which occupy rot holes in Scots Pine Pinus sylvestris L. in Scotland, U.K. including the endangered pine hoverfly Blera fallax (Linnaeus), and three more common species, Callicera rufa (Schummel), Myathropa florea (Linnaeus), and Sphegina clunipes (Fallén) (Diptera, Syrphidae). The primary aim of the study was to investigate competitive exclusion risks to B. fallax, a species that now remains at just one site in the U.K. Morphological differences were examined between species and these were compared with microhabitat use in an artificial rot hole. In addition, larval growth was measured for three of the species in different volumes of pinewood substrate to investigate differences in development in response to varying substrate levels. Field surveys confirmed that B. fallax, C. rufa, and M. florea frequently co‐occur in pine rot holes. Species differed in their growth rates and responses to variation in substrate level. Blera fallax developed quickly before winter, and decreasing substrate volume significantly inhibited growth, whereas C. rufa and M. florea took 6 months longer to achieve a critical size for eclosion. Each species inhabited a distinct depth in the rot hole and exhibited correspondingly different behaviours associated with respiration and the length of their posterior breathing tubes. The microhabitat partitioning observed in this study may facilitate the coexistence of these four species, and suggests that competitive exclusion will not hamper conservation management efforts for B. fallax.

Quantifying the food requirements and effects of food stress on bumble bee colony development

Agricultural intensification has led to a reduction in semi-natural areas and in the abundance of wild flowering plants, reducing the availability of floral resources upon which pollinating insects depend. This is widely accepted as one of the major drivers of pollinator declines, but few studies have directly addressed the effects of dietary restrictions on pollinator fitness. Here, we investigated the effects of restricting pollen and nectar supply on bumble bee (Bombus terrestris) colony growth, adult size and number. Colonies required up to 6 g pollen/1 g protein and 50 g sugar to establish a colony of 5 workers, and consumed in excess of 176 g pollen/31 g protein and 1,186 g sugar in their lifetime. Regardless of restrictions on pollen or nectar availability, colonies consumed a ratio of 1 g protein to ~43 g sugar, though free-flying colonies require proportionally more sugar to fuel foraging. Food-limited colonies from an early stage grew little with anything less than ad-lib nectar, while more-established colonies increased in weight even with low levels of nectar suggesting a shortage of resources in early spring may be most damaging to bumble bee colonies. Dietary restriction reduced the number of reproductives produced, but had variable effects on the size of workers and males. Nosema ceranae infection was included as a covariate in analyses and had a significant negative effect on colony growth. This study provides a base line for the developmental requirements of bumble bee colonies, and indicates the effects a resource deficit may have on their development and reproduction.

Growth, development, and life‐history strategies in an unpredictable environment: case study of a rare hoverfly Blera fallax (Diptera, Syrphidae)

1. Development in organisms can vary in response to fluctuating environments. In holometabolous insects, variation in adult phenotypic traits is strongly influenced by growth conditions experienced by larvae. The main aim of this study was to assess how much environmental insight can be gained from analysis of the phenotypic changes in an insects life history parameters in response to realistic food limitations.

Bumble-BEEHAVE: a systems model for exploring multifactorial causes of bumblebee decline at individual, colony, population and community level.

Abstract World‐wide declines in pollinators, including bumblebees, are attributed to a multitude of stressors such as habitat loss, resource availability, emerging viruses and parasites, exposure to pesticides, and climate change, operating at various spatial and temporal scales. Disentangling individual and interacting effects of these stressors, and understanding their impact at the individual, colony and population level are a challenge for systems ecology. Empirical testing of all combinations and contexts is not feasible. A mechanistic multilevel systems model (individual‐colony‐population‐community) is required to explore resilience mechanisms of populations and communities under stress. We present a model which can simulate the growth, behaviour and survival of six UK bumblebee species living in any mapped landscape. Bumble‐BEEHAVE simulates, in an agent‐based approach, the colony development of bumblebees in a realistic landscape to study how multiple stressors affect bee numbers and population dynamics. We provide extensive documentation, including sensitivity analysis and validation, based on data from literature. The model is freely available, has flexible settings and includes a user manual to ensure it can be used by researchers, farmers, policy‐makers, NGOs or other interested parties. Model outcomes compare well with empirical data for individual foraging behaviour, colony growth and reproduction, and estimated nest densities. Simulating the impact of reproductive depression caused by pesticide exposure shows that the complex feedback mechanisms captured in this model predict higher colony resilience to stress than suggested by a previous, simpler model. Synthesis and applications. The Bumble‐BEEHAVE model represents a significant step towards predicting bumblebee population dynamics in a spatially explicit way. It enables researchers to understand the individual and interacting effects of the multiple stressors affecting bumblebee survival and the feedback mechanisms that may buffer a colony against environmental stress, or indeed lead to spiralling colony collapse. The model can be used to aid the design of field experiments, for risk assessments, to inform conservation and farming decisions and for assigning bespoke management recommendations at a landscape scale.