Trends in Ecology & Evolution
ReviewWhy Bees Are So Vulnerable to Environmental Stressors
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.
References (100)
Global pollinator declines: trends, impacts and drivers
Trends Ecol. Evol.
(2010)Neonicotinoids, bee disorders and the sustainability of pollinator services
Curr. Opin. Environ. Sustain.
(2013)Cognition with few neurons: higher-order learning in insects
Trends Neurosci.
(2013)Insect societies and the social brain
Curr. Opin. Insect Sci.
(2016)Bee reverse-learning behavior and intra-colony differences: Simulations based on behavioral experiments reveal benefits of diversity
Ecol. Modell.
(2014)Learning by observation emerges from simple associations in an insect model
Curr. Biol.
(2013)- et al.
Neural mechanisms of insect navigation
Curr. Opin. Insect Sci.
(2016) Spatial memory in insect navigation
Curr. Biol.
(2013)Exploratory behaviour of honeybees during orientation flights
Anim. Behav.
(2015)Effect of fipronil on side-specific antennal tactile learning in the honeybee
J. Insect Physiol.
(2009)
Acute exposure to selenium disrupts associative conditioning and long-term memory recall in honey bees (Apis mellifera)
Ecotoxicol. Environ. Saf.
Single amino acids in sucrose rewards modulate feeding and associative learning in the honeybee
J. Insect Physiol.
Bee nutrition and floral resource restoration
Curr. Opin. Insect Sci.
Automated monitoring reveals extreme interindividual variation and plasticity in honeybee foraging activity levels
Anim. Behav.
Seed coating with a neonicotinoid insecticide negatively affects wild bees
Nature
Extinctions of aculeate pollinators in Britain and the role of large-scale agricultural changes
Science
Impacts of neonicotinoid use on longterm population changes in wild bees in England
Nat. Commun.
Report warns of looming pollination crisis in North America
Science
Pathogen webs in collapsing honey bee colonies
PLoS One
Varroa–virus interaction in collapsing honey bee colonies
PLoS One
A common pesticide decreases foraging success and survival in honey bees
Science
Combined pesticide exposure severely affects individual- and colony-level traits in bees
Nature
Bee declines driven by combined stress from parasites, pesticides, and lack of flowers
Science
The Bees of the World
The honeybee as a model for understanding the basis of cognition
Nat. Rev. Neurosci.
Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees
Nat. Commun.
Sublethal dosage of imidacloprid reduces the microglomerular density of honey bee mushroom bodies
Sci. Rep.
Omega-3 deficiency impairs honey bee learning
Proc. Natl. Acad. Sci. USA
Virus infection causes specific learning deficits in honeybee foragers
Proc. R. Soc. B.
The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies
Chronic sublethal stress causes bee colony failure
Ecol. Lett.
Rapid behavioral maturation accelerates failure of stressed honey bee colonies
Proc. Natl. Acad. Sci. USA
A quantitative model of honey bee colony population dynamics
PLoS One
The neonicotinoid clothianidin interferes with navigation of the solitary bee Osmia cornuta in a laboratory test
J. Exp. Biol.
Colour processing in complex environments: insights from the visual system of bees
Proc. R. Soc. B.
Behavioral and neurophysiological study of olfactory perception and learning in honeybees
Front. Syst. Neurosci.
The Dancing Bees: An Account of the Life and Senses of the Honey Bee
Flower constancy, insect psychology, and plant evolution
Naturwissenschaften
No trade-off between learning speed and associative flexibility in bumblebees: a reversal learning test with multiple colonies
PLoS One
Invertebrate learning and memory: fifty years of olfactory conditioning of the proboscis extension response in honeybees
Learn. Mem.
Neural substrate for higher-order learning in an insect: Mushroom bodies are necessary for configural discriminations
Proc. Natl. Acad. Sci. USA
Memory dynamics in the honeybee
J. Comp. Physiol. A
Honeybee navigation: nature and calibration of the ‘odometer’
Science
Integration of polarization and chromatic cues in the insect sky compass
J. Comp. Physiol. A
The depth of the honeybee’s backup sun-compass systems
J. Exp. Biol.
Transmedulla neurons in the sky compass network of the honeybee (Apis mellifera) are a possible site of circadian input
PLoS One
Magnetoreception in eusocial insects: an update
J. R. Soc. Interface
Memory use in insect visual navigation
Nat. Rev. Neurosci.
Bumblebee calligraphy: the design and control of flight motifs in the learning and return flights of Bombus terrestris
J. Exp. Biol.
Goal seeking in honeybees: matching of optic flow snapshots?
J. Exp. Biol.
Cited by (163)
Floral nectar: Fifty years of new ecological perspectives beyond pollinator reward
2024, Perspectives in Plant Ecology, Evolution and SystematicsMicroplastics reach the brain and interfere with honey bee cognition
2024, Science of the Total EnvironmentThe impact of heavy metal pollution on wild bee communities in smallholder farmlands
2023, Environmental ResearchMineral composition of bee pollen and its relationship with botanical origin and harvesting period
2023, Journal of Food Composition and Analysis
- 3
These authors contributed equally to this work.