Review
Why Bees Are So Vulnerable to Environmental Stressors

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Bee populations are declining in the industrialized world, raising concerns for the sustainable pollination of crops. Pesticides, pollutants, parasites, diseases, and malnutrition have all been linked to this problem. We consider here neurobiological, ecological, and evolutionary reasons why bees are particularly vulnerable to these environmental stressors. Central-place foraging on flowers demands advanced capacities of learning, memory, and navigation. However, even at low intensity levels, many stressors damage the bee brain, disrupting key cognitive functions needed for effective foraging, with dramatic consequences for brood development and colony survival. We discuss how understanding the relationships between the actions of stressors on the nervous system, individual cognitive impairments, and colony decline can inform constructive interventions to sustain bee populations.

Section snippets

Bees Are Exposed to Multiple Environmental Stressors

Bees are ecologically and economically vital pollinators for both wild and cultivated flowers. Presently many populations are in decline 1, 2, 3, 4, while demand for pollination-dependent crops continues to rise, generating understandable alarm and debate about the possibility of an emerging ‘pollination crisis’ [5]. Many causal factors have been identified, including a range of pathogens and parasites 6, 7, human-induced stressors such as pesticides 8, 9, 10, and other forms of environmental

Central-Place Foraging on Flowers Imposes Significant Cognitive Challenges

Bees must gather large volumes of highly dispersed pollen and nectar, and return with them to the nest to feed their brood [12]. Accordingly, these insects have evolved excellent memory and navigation skills enabling them to exploit complex and variable foraging environments, and more than a century of research has identified the underlying neural circuits 13, 14. Although most studies have focused on a few economically important social species, such as honey bees and bumblebees, solitary bees

Stressors Affect Brain Functions, Cognition, and Behavior

Successful foraging is based on the precise integration of information processed across the major brain networks, as well as dynamic structural modifications of such networks. Therefore even subtle disturbances of neural function could have dramatic consequences on individual cognitive abilities and hence foraging performance. From this perspective it is a major concern that most of the stressors presently impacting on bees target the brain. The range of stressors has been well reviewed

From Reduced Foraging Performance to Colony Collapse

Few of the stressors we have considered would kill bees outright at ecological levels. Nonetheless, impairment of the cognitive abilities and food collection performance by low stresses can have extremely severe consequences on bee functions and survival, and crucially on their capacity to successfully rear brood and maintain colonies. Hence these stresses can have very significant impacts on populations.

Comparative research on bee declines suggests that the resilience of bees to stressors

Concluding Remarks and Future Prospects

Central-place foraging bees are particularly vulnerable to many current environmental stressors. These insects have evolved refined cognitive abilities enabling them to effectively exploit complex and changing foraging environments to provision their nest. Such capacities demand the optimal function and coordination of major systems in the small bee brain. Many stressors disrupt brain function, with the consequence of reduced foraging performance, ultimately compromising the brood or whole

Acknowledgments

This work was funded by the CNRS. The research was also supported by PhD fellowships of the French Ministry of Research to S.K. and A.C., an Agence Nationale de la Recherche (ANR) grant (ANR-13-ADAP-0002) to J.M.D., an Australian Research Council (ARC) Future Fellowship to A.B.B., and ANR (ANR-16-CE02-0002-01), IDEX, and Fyssen grants to M.L.

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