Olfaction in the Anthropocene: NO3 negatively impacts floral scent and nocturnal pollination

There is growing concern about sensory pollutants impacting ecological communities. Anthropogenically enhanced oxidants (O3 and NO3) rapidly degrade floral scents, potentially reducing pollinator attraction to flowers. However, the physiological and behavioral impacts on pollinators and plant fitness are unknown. Using a nocturnal flower-moth system, we find that atmospheric concentrations of NO3, but not O3, eliminate flower visitation by moths, and it is the reaction of NO3 to a subset of monoterpenes that reduces the scent’s attractiveness. Global atmospheric models of floral scent oxidation reveal that pollinators in certain urban areas may have a reduced ability to perceive and navigate to flowers. These results illustrate the impact of anthropogenic pollutants on an animal’s olfactory ability and indicate that such pollutants may be critical regulators of global pollination. Methods The GEOS-Chem chemical transport model was used for simulations driven by assimilated MERRA-2 (Modern-Era Retrospective analysis for Research and Applications, Version 2) meteorological fields (33). GEOS-Chem is an open-access global atmospheric chemistry model that can simulate tropospheric and stratospheric oxidant–aerosol chemistry, aerosol microphysics, and budgets of various gases, including ozone and nitrate radicals. The model uses analyzed winds and other meteorological variables produced by Goddard Earth Observing System (GEOS) simulations of the NASA Global Modeling and Assimilation Office (GMAO) with assimilated meteorological observations and couples these measurements with the chemistry. The recent model advances and assimilation of observed meteorological fields via MERRA-2 have led to accurate simulation of ozone and nitrate radical concentrations in the models (51). In the present day simulation, we use GEOS-Chem version 12.1.0 driven by MERAA-2 meteorology at a horizontal resolution of 2° × 2.5° (lat × long) with 47 vertical levels. The simulation period was from March 2012 to June 2014, with the first year as a spin-up period to allow for the accumulation of intermediate chemical reservoir species. These years were representative of the conditions of our study period, and have detailed information on the physicochemical environment. A reference simulation was conducted based on the public version 13.2.1 of GEOS-Chem (https://wiki.seas.harvard.edu/geos-chem/index.php/GEOS-Chem_13.2.1). The HOx –NOx –VOC–O3–BrOx tropospheric chemistry chemical mechanism in the reference simulation is described in Mao et al. (52, 53) with recent updates for biogenic volatile organic compound (VOC) chemistry (54, 55). The Model of Emissions of Gasses and Aerosols from Nature v2.1 (MEGAN) (56) was used to derive biogenic emissions, and the Global Fire Emissions Database (GFED4) was used for open fire emissions. For anthropogenic emissions of various gaseous and aerosol species`, the CEDS (Community Emission Data System) inventory was the basis (57) but combined with local inventories in Asia, USA, Canada, Mexico, Europe, and Africa. More details about the simulations are described in (58). For the preindustrial GEOS-Chem model run, we used the GEOS-Chem chemical transport model version 13.2.1 (50) driven by assimilated meteorology from MERRA-2 (Modern-Era Retrospective analysis for Research and Applications, Version 2) from the year 2013 at a horizontal resolution of 4°x 5° and 72 vertical levels up to 0.01 hPa. GEOS-Chem contains detailed HOx-NOx-VOC-ozone-halogen-aerosol chemistry (59) including isoprene chemistry from (60) and reactive uptake of NO2, NO3, and N2O5 by aerosols from (61, 62). Global anthropogenic emissions of pollutants including VOCs, NO3, and various aerosol species are from the Community Emissions Data System (CEDS) v2 inventory from (63). Biogenic VOC emissions are from the Model of Emissions of Gasses and Aerosols from Nature v2.1 (MEGAN) (56, 64) and biogenic soil NOx emissions are from (65). Open fire emissions are from Global Fire Emissions Database (GFED4.1)(66). Dry deposition for aerosols and gasses is based on a resistance-in-series scheme described in in (67). The wet deposition scheme is described in (68) for water-soluble aerosols, and (69) for gases. To simulate a preindustrial atmosphere, all anthropogenic emissions are turned off (sensu (70)), and this was run alongside the 2013 and 2021 simulations with all emissions turned on. The preindustrial simulation had 12 months of spin-up to equilibrate the model to preindustrial conditions. More details about the simulation are described in Jongebloed et al. (2023) (70). The O3 and NO3 emissions and meteorology were averaged monthly allowing a conservative estimate of NO3 and O3 levels. Although these reactive compounds vary over the 24 h period, calculating the monthly average provides a conservative estimate for modeling the effects on the floral volatiles and flower recognition distances. Changes to the GEOS-Chem chemical mechanism and model physics between version 12.1.0 and version 13.2.1 preclude direct comparison of model output from the two different versions. We use the version 12.1.0 present-day simulation as the primary representation of present-day NO3 and O3 because this simulation was run at higher resolution (2° × 2.5°) compared to the preindustrial simulation run with 13.2.1 (4° × 5°). To avoid influence from model updates when comparing version 13.2.1 preindustrial simulation to the version 12.1.0 present-day simulation, a factor map was created by dividing the preindustrial simulation by the 2013 simulation with all emissions turned on. This factor map was then applied to the 2013 map from GEOS-Chem version 12.1.0 for preindustrial comparisons. To examine the 2013 ozone and NO3 emissions to current levels, we compared model runs of O3 and NO3 for 2019 and 2021, relative to 2013. We find that the increase in O3 and NO3 from the preindustrial to present day are orders of magnitude larger than the interannual variability between 2013, 2019, and 2021, especially in regions within or near high anthropogenic pollutant emissions, such as urban areas. Global trends across years showed similar O3 and NO3 levels, with the secular increase in anthropogenic NOx leading to little variability in NO3 over the last ten years across large portions of North and South America, Europe, and megacity regions, especially compared to pre-industrial conditions. These results reflect prior work in troposphere O3 (71, 72), and NO3 (30, 73). However, natural NOx sources in the form of biomass burning caused year-to-year temporal and spatial variability in the importance of NO3 regions distant from anthropogenic urban sources (Canada, areas in N. Eurasia)(30). To further examine the relationship between the population size around large urban areas and preindustrial impacts and pollinator detection distances, we performed regression models between these variables and the population of the top 98 megacities (Table S13). Regression models were compared based on their adjusted-R2 and Akaike information criterion (AIC). Based on the R2 and AIC scores, only second or third-degree quadratic regressions were used to prevent data over-fitting. GEOS-Chem code availability: GEOS-Chem version 12.1.0 code is publicly available at http://wiki.geos-chem.org/GEOS-Chem_12#12.1.0 (https://doi.org/10.5281/zenodo.1553349, International GEOS-Chem User Community, 2018). GEOS-Chem version 13.2.1 code is publicly available at https://doi.org/10.5281/zenodo.5500717. 2019 GEOS-Chem 13.2.1 benchmark output was used for creating NO3 comparison maps to determine the interannual variation in NO3 concentrations. 2021/2013, 2019/2013, and 2021/2019 comparison maps were made by dividing the July NO3 maps from the GEOS-Chem 13.2.1 simulations. The bottom vertical layers of the model output were used in computing the pollinator impacts maps. The data was processed, and the maps were plotted using MATLAB R2020b. Data from January 2013 was used to investigate the pollinator impacts in the summer in the southern hemisphere, and data from July 2013 was used to investigate the pollinator impacts in the summer in the northern hemisphere. For the pre-industrial comparisons map, values over the oceans were masked by creating a mask using a modified version of the global-land-mask 1.0.0 package by toddkarin in Python, using the ‘Natural Earth’ map database. The land/water values in each grid cell were summed, and if there were any land values in the grid cell, the grid cell was classified as a land grid cell. Antarctica was also excluded from consideration by masking all grid cells below -56° in latitude. Mean O3 and NO3 values over the northern latitudes were calculated by averaging all values over land between 10° and 50° latitude in the July 2013 GEOS-Chem model simulation. A plot of reaction rate ratios of various monoterpenes, sesquiterpenes, and green leaf volatiles (74)(Table S12, Fig. S8B) at the mean northern latitude concentrations of NO3 (2.6 ppt) and O3 (37 ppb) was generated. The O3 reactivity ratio was obtained by dividing the O3 reaction rate by the NO3 reaction rate. The NO3 reactivity ratio was obtained by dividing the NO3 reaction rate by the O3 reaction rate. The monoterpenes used in the model are commonly emitted from flowers in many regions of the world, including North America, Europe, Central Asia, the Middle East, and southern Africa (7, 11, 35-37).