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.