Insect pollinators of crops and wild plants are under threat globally and their decline or loss could have profound economic and environmental consequences. Here, we argue that multiple anthropogenic pressures – including land‐use intensification, climate change, and the spread of alien species and diseases – are primarily responsible for insect‐pollinator declines. We show that a complex interplay between pressures (eg lack of food sources, diseases, and pesticides) and biological processes (eg species dispersal and interactions) at a range of scales (from genes to ecosystems) underpins the general decline in insect‐pollinator populations. Interdisciplinary research on the nature and impacts of these interactions will be needed if human food security and ecosystem function are to be preserved. We highlight key areas that require research focus and outline some practical steps to alleviate the pressures on pollinators and the pollination services they deliver to wild and crop plants.

Chronic exposure of bumblebees to two pesticides (a neonicotinoid and a pyrethroid) independently and in combination, at concentrations approximating field-level exposure, impairs natural foraging behaviour and increases worker mortality, with knock-on effects for brood development and colony success. Exposure to neonicotinoid pesticides is known to influence bee behaviour, and could be a key factor in current bee declines. It has not been possible to establish a mechanistic link between individual and colony effects, but this study demonstrates a direct link between detrimental behavioural effects and field-level pesticide exposure — to neonicotinoid and pyrethroid — in individual worker bumblebees, and consequent impacts on colony development and survival. The pesticides reduce the effectiveness of foraging behaviour, with knock-on effects on brood care and colony productivity. Reported widespread declines of wild and managed insect pollinators have serious consequences for global ecosystem services and agricultural production1,2,3. Bees contribute approximately 80% of insect pollination, so it is important to understand and mitigate the causes of current declines in bee populations 4,5,6. Recent studies have implicated the role of pesticides in these declines, as exposure to these chemicals has been associated with changes in bee behaviour7,8,9,10,11 and reductions in colony queen production12. However, the key link between changes in individual behaviour and the consequent impact at the colony level has not been shown. Social bee colonies depend on the collective performance of many individual workers. Thus, although field-level pesticide concentrations can have subtle or sublethal effects at the individual level8, it is not known whether bee societies can buffer such effects or whether it results in a severe cumulative effect at the colony level. Furthermore, widespread agricultural intensification means that bees are exposed to numerous pesticides when foraging13,14,15, yet the possible combinatorial effects of pesticide exposure have rarely been investigated16,17. Here we show that chronic exposure of bumblebees to two pesticides (neonicotinoid and pyrethroid) at concentrations that could approximate field-level exposure impairs natural foraging behaviour and increases worker mortality leading to significant reductions in brood development and colony success. We found that worker foraging performance, particularly pollen collecting efficiency, was significantly reduced with observed knock-on effects for forager recruitment, worker losses and overall worker productivity. Moreover, we provide evidence that combinatorial exposure to pesticides increases the propensity of colonies to fail.

Despite substantial evidence that neonicotinoid pesticides can have negative effects on bees, there have been no reports that this leads to problems with pollination; here bumblebee colonies exposed to a neonicotinoid are shown to provide reduced pollination services to apple trees, leading to a reduction in seed number. There is now substantial evidence that neonicotinoid pesticides can have negative effects on bees. However, it has not been shown that this leads to problems with the ecosystem service that bees provide, pollination. These authors show, in field tests involving 100 apple trees, that bumblebees exposed to a neonicotinoid provide less efficient pollination, leading to a reduction in seed number. Recent concern over global pollinator declines has led to considerable research on the effects of pesticides on bees1,2,3,4,5. Although pesticides are typically not encountered at lethal levels in the field, there is growing evidence indicating that exposure to field-realistic levels can have sublethal effects on bees, affecting their foraging behaviour1,6,7, homing ability8,9 and reproductive success2,5. Bees are essential for the pollination of a wide variety of crops and the majority of wild flowering plants10,11,12, but until now research on pesticide effects has been limited to direct effects on bees themselves and not on the pollination services they provide. Here we show the first evidence to our knowledge that pesticide exposure can reduce the pollination services bumblebees deliver to apples, a crop of global economic importance. Bumblebee colonies exposed to a neonicotinoid pesticide provided lower visitation rates to apple trees and collected pollen less often. Most importantly, these pesticide-exposed colonies produced apples containing fewer seeds, demonstrating a reduced delivery of pollination services. Our results also indicate that reduced pollination service delivery is not due to pesticide-induced changes in individual bee behaviour, but most likely due to effects at the colony level. These findings show that pesticide exposure can impair the ability of bees to provide pollination services, with important implications for both the sustained delivery of stable crop yields and the functioning of natural ecosystems.

Despite the widespread assumption that the learning abilities of animals are adapted to the particular environments in which they operate, the quantitative effects of learning performance on fitness remain virtually unknown. Here, we evaluate the learning performance of bumble-bees (Bombus terrestris) from multiple colonies in an ecologically relevant associative learning task under laboratory conditions, before testing the foraging performance of the same colonies under the field conditions. We demonstrate that variation in learning speed among bumble-bee colonies is directly correlated with the foraging performance, a robust fitness measure, under natural conditions. Colonies vary in learning speed by a factor of nearly five, with the slowest learning colonies collecting 40% less nectar than the fastest learning colonies. Such a steep fitness function is suggestive of strong selection for higher learning speed. Partial correlation analysis reveals that other factors such as forager body size or colour preference appear to be negligible in our study. Although our study does not directly prove causality of learning on foraging success, our approach of correlating natural within-species variation in these two factors represents a major advance over traditional between-species correlative analyses where comparability can be compromised by the fact that species vary along multiple dimensions.