Abstract
For effective foraging, many insect pollinators rely on the ability to learn and recall floral odours, behaviours that are associated with a complex suite of cellular processes. Here, we investigated how acute exposure to a high-dose of diesel exhaust (containing 19.8 and 17.5 ppm of NO and NO2, respectively) affected associative learning behaviour of honey bees (Apis mellifera) and expression of a ubiquitous heat shock protein, HSP70, in their central nervous system (CNS). To determine whether exposure to diesel exhaust would alter their tolerance to a subsequent abiotic stress, we further subjected individuals to heat stress. Diesel exhaust exposure decreased honey bees’ ability to learn and recall a conditioned odour stimulus. Whilst there was no significant difference in CNS HSP70 expression between honey bees exposed to either diesel exhaust or clean air across the entire duration of the experiment (3.5 h), there was a significant effect of time and a significant interaction between exposure treatment and time. This interaction was investigated using correlation analyses, which demonstrated that only in the diesel exhaust exposed honey bees was there a significant positive correlation between HSP70 expression and time. Furthermore, there was a 44% reduction in honey bee individuals that were able to recall the odour 72 h after diesel exposure compared with clean air control individuals. Moreover, diesel exhaust affected A. mellifera in a way that reduced their ability to survive a second subsequent stressor. Such negative effects of air pollution on learning, recall, and stress tolerance has potential to reduce foraging efficiency and pollination success of individual honey bees.
Highlights
Pollination services are critical for production of many crops with, for example, 84% of crop species cultivated in Europe benefitting from insect pollination[1,2]
All honey bees used in learning and memory retrieval experiments were initially exposed to either a diesel exhaust or a clean air treatment and assessed to ensure they could extend their proboscis in response to sucrose solution, with only responsive animals used in subsequent tests
Diesel exhaust exposure significantly decreased the ability of A. mellifera to learn the conditioned stimulus and reduced their ability to remember and respond to that odour over a 72-hour period compared with individuals that were not exposed to diesel exhaust
Summary
Pollination services are critical for production of many crops with, for example, 84% of crop species cultivated in Europe benefitting from insect pollination[1,2]. Nitrogen oxide (NOx) gases released in diesel exhaust, for example, can alter the chemical composition of floral volatiles, which, in turn, affects honey bees’ (Apis mellifera) ability to recognise an altered odour[7,8]. This species is the most widespread managed pollinator and despite a global increase in numbers of managed colonies Effective foraging is the basis of pollinator success, requiring complex cognitive abilities associated with decision making, learning, memory, and communication[18] Any degradation of these abilities is likely to have negative impacts upon pollinator foraging and success. The complex social, navigational, and communication behaviours of honey bees and relative simplicity of their well-studied CNS make them excellent models for testing learning and memory function in response to atmospheric changes[19,20]
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