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. 2021 Apr 21;10(5):636.
doi: 10.3390/antiox10050636.

Ozone Pollution Alters Olfaction and Behavior of Pollinators

Maryse Vanderplanck  1   2 , Benoît Lapeyre  3 , Margot Brondani  3 , Manon Opsommer  3 , Mathilde Dufay  3 , Martine Hossaert-McKey  3   4 , Magali Proffit  3
Affiliations

Ozone Pollution Alters Olfaction and Behavior of Pollinators

Maryse Vanderplanck et al. Antioxidants (Basel). .

Abstract

Concentration of air pollutants, particularly ozone (O3), has dramatically increased since pre-industrial times in the troposphere. Due to the strong oxidative potential of O3, negative effects on both emission and lifetime in the atmosphere of plant volatile organic compounds (VOCs) have already been highlighted. VOCs alteration by O3 may potentially affect the attraction of pollinators that rely on these chemical signals. Surprisingly, direct effects of O3 on the olfaction and the behavioral response of pollinators have not been investigated so far. We developed a comprehensive experiment under controlled conditions to assess O3 physiological and behavioral effects on two pollinator species, differing in their ecological traits. Using several realistic concentrations of O3 and various exposure times, we investigated the odor antennal detection and the attraction to VOCs present in the floral scents of their associated plants. Our results showed, in both species, a clear effect of exposure to high O3 concentrations on the ability to detect and react to the floral VOCs. These effects depend on the VOC tested and its concentration, and the O3 exposure (concentration and duration) on the pollinator species. Pollination systems may, therefore, be impaired in different ways by increased levels of O3, the effects of which will likely depend on whether the exposure is chronic or, as in this study, punctual, likely causing some pollination systems to be more vulnerable than others. While several studies have already shown the negative impact of O3 on VOCs emission and lifetime in the atmosphere, this study reveals, for the first time, that this impact alters the pollinator detection and behavior. These findings highlight the urgent need to consider air pollution when evaluating threats to pollinators.

Keywords: atmospheric pollution; behavioral response; ozone; plant VOC perception; plant-pollinator interactions; pollinators.

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Conflict of interest statement

The authors declare no conflict of interest. The funders had no role in the design of the study, in the collection, analyses, or interpretation of data, in the writing of the manuscript, or in the decision to publish the results.

Figures

Figure 1
Figure 1
The effect of O3 exposure on the electroantennographic (EAG) responses (mean ± SE) of fig wasps to different doses of four synthetic volatile compounds (n, number of specimens tested). Prior to the EAG recording, wasps were exposed to different O3 concentrations for 60-min or 180-min. Different letters (n.s. p > 0.05) or asterisks (* p < 0.05) indicate significant differences in the EAG response to one compound at a given dose between O3 treatments based on contrasts.
Figure 1
Figure 1
The effect of O3 exposure on the electroantennographic (EAG) responses (mean ± SE) of fig wasps to different doses of four synthetic volatile compounds (n, number of specimens tested). Prior to the EAG recording, wasps were exposed to different O3 concentrations for 60-min or 180-min. Different letters (n.s. p > 0.05) or asterisks (* p < 0.05) indicate significant differences in the EAG response to one compound at a given dose between O3 treatments based on contrasts.
Figure 2
Figure 2
Effect of O3 exposure on the electroantennographic (EAG) responses (mean ± SE) of bumblebee foragers to different doses of three synthetic compounds (n, number of specimens tested). Prior to the EAG recording, bumblebees were exposed to different O3 concentrations for 60-min or 180-min. Different letters (a and b) indicate significant differences (p < 0.05) in the EAG response to one compound at a given dose between O3 concentrations based on contrast analysis.
Figure 3
Figure 3
Effect of O3 exposure on the attraction of fig wasps to the VOC mix mimicking fig odor or clean air in Y-tube olfactometers (n, number of specimens tested). Prior to the behavioral test, wasps were exposed to different O3 concentrations for 60-min or 180-min. Asterisks indicate a significant preference based on two-sided binomial tests (* p < 0.05).
Figure 4
Figure 4
Effect of 60-min O3 exposure on the attraction (mean ± SE based on the percentage of bouts) of bumblebee foragers to benzaldehyde or clean air in Y-tube olfactometers (n, number of specimens tested). Asterisks indicate a preference, according to the paired Wilcoxon signed-rank tests (** p < 0.01), and different letters indicate a significant difference in choice among O3 treatments, according to the multiple pairwise comparisons based on the binomial model (p < 0.05).
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