Introduction
Human activity is changing environmental conditions worldwide (Rockströmet al. 2009), affecting global biogeochemical flows (e.g.
nitrogen, ozone; Fowler et al. 2013; Mills et al. 2013;
Lefohn et al. 2018; Smil 2000) and, consequently, air, water and
soil quality. In addition to habitat loss and climate change (with
increased greenhouse-gas contributors), environmental pollution,
including nitrogen deposition, is considered a major driver of
biodiversity loss (Sala et al. 2000; Mazor et al. 2018)
and can negatively impact ecosystem functioning and associated ecosystem
services such as crop pollination (González-Varo et al. 2013).
Nitrogen deposition (estimated to be 413 Tg N yr-1 in
2010) has more than doubled over the last century (Fowler et al.2013) due to emissions of ammonia (NH3, from pecuary and
agriculture) and nitrogen oxides (NOx produced in the combustion of
fossil fuels). Such increases have affected plant communities (Tilmanet al. 2002; Carvalheiro et al. 2020), with associated
bottom-up impacts on higher trophic levels including pollinators (Pöyryet al. 2017; Ramos et al. 2018; David et al. 2019;
Wang & Tang 2019; Carvalheiro et al. 2020; Johnson et al.2020). While scarcity of nitrogen can constrain the positive effect of
pollinators on crop production (e.g. sunflower; Tamburini et al., 2016;
oilseed rape; Garratt et al. 2018), negative effects of excess
nitrogen on pollination have also been reported (Marini et al.2015; Tamburini et al. 2017; Ramos et al. 2018). Such
responses are likely mediated by changes in floral resources quality and
quantity, which in turn can be moderated by changes in climatic
conditions (Flores-Moreno et al. 2016).
Another important air pollutant is tropospheric ozone, a major
greenhouse-gas which is also phytotoxic (Mills et al. 2013;
Lefohn et al. 2018; Ilić & Maksimović 2021). Ozone levels have
increased since the beginning of the industrial period (estimated to up
of 35%; Mills et al., 2013; Guerreiro et al., 2014; IPCC, 2014). While
there are other sources of ozone (e.g. volatile organic compounds,
carbon monoxide and methane), oxidized nitrogen (NOx) is
one of the two major ozone precursors (Mills et al. 2013; Lefohnet al. 2018). Increased concentrations of ozone can reduce
photosynthesis and plant growth (Tjoelker & Luxmoore 1991; Blacket al. 2007) and negatively affect the timing of flowering and
number of flowers (Feder & Sullivan 1969; Hayes et al. 2012;
Leisner & Ainsworth 2012) (Fig. 1). Increased ozone concentration in
the air (e.g. 80-120 ppb, frequently found near urban areas; Paoletti et
al., 2014) can also change the concentration and emission distance of
floral volatile organic compounds (Heiden et al. 1999;
McFrederick et al. 2008; Farré‐Armengol et al. 2016;
Fuentes et al. 2016; Jürgens & Bischoff 2017) and, consequently,
affect pollinator olfaction and foraging behaviour (Farré‐Armengolet al. 2016; Fuentes et al. 2016; Vanderplanck et
al. 2021) (see Fig. 1). These effects on plant pollinator interactions
may partly explain the reported negative effects of ozone on seed and
fruit production detected in previous studies (Mills et al. 2013;
Farré‐Armengol et al. 2016; Fuhrer et al. 2016). Yet, few
studies have explored the effects of air pollution (e.g., nitrogen
oxides and ozone) on pollinator foraging patterns and efficiency, and if
the strength and direction of such effects depends on other important
environment drivers, such as pesticide use (Walker & Wu 2017) or land
use (Mazor et al., 2018; Sala et al., 2000).
Taking into account potential interactive effects with landscape quality
for pollinators (i.e., natural and semi-natural vegetation composition)
and pesticide exposure, we investigated how air pollution by ozone and
different sources of nitrogen compromise pollinator visitation rates and
their contribution to crop production (apple, blueberry, fava bean,
oilseed rape). Given the negative effects on flower abundance and odours
described above, and the fact that previous studies detected greater
benefit from pollination under lower N availability (Marini et
al. 2015; Ramos et al. 2018), we expect that increased ozone and
nitrogen will lead to declines in crop pollinator visitation rates and
pollination service delivery. However, availability of non-crop habitats
is an important determinant of pollinator abundance, richness and
pollination services (Kennedy et al. 2013; Dainese et al.2019). We also expect that the effect of ozone and nitrogen on
pollinators and pollination will be weaker in structurally more simple
landscapes (less semi-natural habitat and greater risk of exposure to
pesticides), where the only potential pollinators would be species with
greater resilience to land use intensification (Williams et al.2010; Bartomeus et al. 2013; Kremen & M’Gonigle 2015; Kleijnet al. 2015).
The results of this study contribute to our understanding of interactive
effects among atmospheric pollution, land-use management and
eutrophication on crop pollinators and pollination and as such help
inform the development of new practices and policies to safeguard
pollinators and crop pollination.