Interacting effect of ozone with pesticide exposure
As expected (Hayes et al. 2012; Leisner & Ainsworth 2012; Millset al. 2013), ozone levels were negatively correlated to crop
pollination. Recent studies have estimated that global agricultural
losses due to high ozone levels totalled 79–121 million metric tons in
2000 with global economic losses ranging from $11 to $26 billion (Van
Dingenen et al. 2009; Avnery et al. 2011a) and predicted
increases of between $17 and $35 billion annually by 2030 (Van
Dingenen et al. 2009; Avnery et al. 2011a). Such effects
may be partly related to a reduction in pollen germination (Leisner &
Ainsworth 2012; Taia et al. 2013; Gillespie et al. 2015).
Our results suggest that changes in pollination by insects (due to
changes in flower visitation patterns) may also play an important role.
The fact that increasing ozone levels modified the response of crop
pollination to pesticide exposure (which turns from positive to
negative) may be related with pest control. Farmers widely use
pesticides to minimize infestations by pests and protect crops from
potential reduction of crop production, both in quality and quantity
(Damalas 2009), and hence positive effects of pesticide use on
production are expected if pests are more limiting than pollinators to
production.
It is however possible, that in more degraded environments, i.e., with a
higher level of ozone pollution, the cost/benefit ratio of pesticides on
crop production changes. In less intensive landscapes with higher
pollinator pool, the negative impact of pesticides on pollinators and
these consequences on crop pollination can be compensate by the benefit
of pest regulation by pesticide use. However, in highly intensive
landscapes, due to scarcity of pollinators which limits pollination and
crop production, the negative effects of pesticides on crop pollinators
(which are more accentuated under high ozone levels, Fig 3) may outweigh
the positive effects on pest reduction on crop production.
The negative relationship between ozone pollution and flower visitor
abundance could be due to changes in plant-pollinator communication and
flower attractiveness that may affect crop pollinator foraging
behaviour. Previous studies have showed that ozone induces changes in
availability of floral resources by modifying flowering timing and
number of flowers, some plant species being particularly sensitive
(Hayes et al. 2012; Leisner & Ainsworth 2012; Mills et
al. 2013). Ozone also alters pollinator decision‐making, modifying and
reducing the volatile floral scents (Farré‐Armengol et al. 2016;
Fuentes et al. 2016; Saunier & Blande 2019; Vanderplancket al. 2021) and damaging pollinators olfactory organs (Dötterlet al. 2016; Vanderplanck et al. 2021).
The fact that the negative effect of pesticide exposure on
non-Apis pollinators (Mancini et al. 2019; Walker & Wu
2017; Woodcock et al. 2017) was more accentuated under high ozone
concentration (Table S1) could be due to communities being less diverse
and/or abundant in regions with high ozone, but also to changes in
pollinator assemblages. In more degraded areas (high pesticide exposure,
high ozone concentration), crop pollinator communities are dominated by
a handful of very dominant widespread species that are more resilient to
intensive land use (Kleijn et al. 2015), which often have a more
generalist diet and may be more mobile (Biesmeijer et al. 2006;
Goulson et al. 2008; Connop et al. 2010). Consequently, in
such regions the negative effect of ozone on non-Apis crop
pollinators might be less detectable, only under more degraded
environment, i.e., under high level of pesticide exposure.
Although the negative impact of pesticides on honey bees is well known
(e.g. Mancini et al., 2019; Walker and Wu, 2017; Woodcock et al., 2017;
Park et al., 2015; Tosi et al., 2017), we found that pesticide exposure
was positively related to honey bee density in crops. This result is
probably due to beekeeping management strategies that are likely more
frequent in intensive agricultural areas where the demand for colony
supply to ensure efficient pollination is high (Garibaldi et al.2017; Rollin & Garibaldi 2019), masking (and even compensating) the
negative effects of pesticides. However, the positive relationship
between abundance of honey bees in crops and pesticide exposure was
lower when ozone concentration increased. This can reflect the negative
effect of pesticides on honey bees, decreasing the pollination
efficiency and survival of honey bees (Prado et al. 2019),
despite the local increase of individuals due to the import of colonies
by beekeepers in intensive farming systems.