INTRODUCTION
Improvements in agricultural productivity are needed in the coming decades to achieve many sustainable development goals, including reduced hunger and increased protection of forest area and biodiversity. Among the many strategies to achieve these gains are efforts to improve air quality (
1). Although these efforts are primarily motivated by human health benefits, the potential agricultural effects are substantial. In some cases, levels of pollutants such as ozone are thought to suppress yields by as much as 30 to 40%, yet these estimates include wide uncertainties (
2,
3). A better understanding of the agricultural impacts of air pollution would help to better assess both the potential benefits of air quality improvements and how prominent a role pollution reduction should have among efforts to raise agricultural productivity.
Historically, studies of air quality and crop productivity have been limited to small-scale experimental manipulations or observational analyses that rely on sparse ground measures of pollution. While these studies have provided a clear basis for further study, they are often plagued by large uncertainties associated with the difficulty of extrapolating beyond the experimental conditions (in the case of experiments) or the challenge of limited overlap between air monitoring stations and agricultural areas (in the case of empirical studies). These latter studies have also tended to focus on the secondary pollutants (ozone and particulate matter) that are most widely monitored because of human health concerns and have been limited to regions with available ground measures (
4).
An alternative to using ambient measures of pollution has been to exploit yield variations in the vicinity of known pollution sources, such as power plants, including inspection of changes before and after the power plants are active (
4–
6). These approaches circumvent some of the drawbacks of relying on pollution monitoring stations, as they do not rely on direct pollution measures, can integrate the net effect of multiple pollutants, and can more readily assess the potential effect of removing specific pollution sources. However, approaches that rely on gradients near pollution sources can suffer from an inability to distinguish effects of different pollutants, are limited to regions that have reliable inventories of, e.g., power plant activity, and can be confounded if other sources (e.g., transportation) contribute significantly to local pollution levels.
Fortunately, recent progress in satellite observations is leading to rapid advances in global air pollution monitoring. The TROPOspheric Monitoring Instrument (TROPOMI) instrument, which was launched aboard the Sentinel-5 Precursor in late 2017, is especially novel in its ability to monitor tropospheric nitrogen dioxide (NO
2) levels at daily frequency, with monthly aggregations of these measures available at spatial resolutions as fine as 0.01° (~1 km at the equator) (
7). NO
2 is itself a good measure of overall NO
x [NO
x, nitrogen oxide (NO) plus NO
2] (
8).
Plant health is affected by NO
x via both direct and indirect pathways, some of which are illustrated in
Fig. 1. NO and NO
2 are themselves phytotoxins that can directly damage plant growth and reduce yields (
9). In addition, NO
x can operate through at least two indirect pathways. First, it is a key precursor to formation of ozone (O
3) in the troposphere, another phytotoxin known to reduce crop yields (
10). Especially in seasons and regions with high levels of volatile organic compounds (VOCs), variations in NO
2 are tightly associated with variations in O
3 levels (
11,
12). Second, NO
x is a precursor to particulate matter aerosols. In the presence of ammonia (often the case in agricultural regions from application of nitrogenous fertilizers such as urea), NO
x can result in increased concentrations of ammonium nitrate aerosols (NH
4NO
3) (
13) and can also oxidize sulfur dioxide (SO
2) and drive formation of ammonium sulfate aerosols [(NH
4)
2SO
4] (
14,
15). These particles reflect and scatter incoming sunlight, changing the radiation environment experienced by crops and reducing access to photosynthetically active radiation (
16,
17). Other pathways not depicted in
Fig. 1 include additional interactions among NO
2, nitrates, O
3, and SO
2 (
18); the effects of NO
x on secondary aerosol formation; and effects of NO
x on the deposition of atmospheric nitrogen in agricultural fields.
Despite general understanding of NO
x’s potential deleterious effects, few studies have attempted to quantify its impact on crops at scale. Several studies have examined measures of plant health or crop yield along gradients of pollution near urban areas (
19,
20) or in fumigation experiments (
21–
24). In many of these cases, NO
x was just one of several pollutants, and only the combined effects of pollutants could be assessed. In other cases, experiments attempted to isolate the effect of NO
x, although typically on natural vegetation, not crops (
21,
24). In general, these studies point to direct negative yield effects of NO
x exposure at values that are commonly found in agricultural regions. For example, the World Health Organization guidelines state a “no effect” level for vegetation of 15 to 20 μg/m
3 for annual average NO
2 [roughly 8 to 11 parts per billion (ppb)] (
25), whereas reported NO
2 levels in most regions commonly exceed these values (
4,
7,
19). While previous studies thus indicate some role for direct NO
x effects, they report substantial variability across different plant species, treatments, levels of other pollutants, and temperature and radiation conditions and are therefore of limited utility in assessing overall yield impacts in farmers’ fields. To date, the lack of concurrent measures of NO
x exposure and crop yield has precluded progress on this issue.
In the current study, we combine the recent TROPOMI measures of NO
2 for 2018–2020 with satellite measures of crop greenness to elucidate the role of NO
2 in crop productivity. One benefit of focusing on NO
2 is that it is measured with more precision than most pollutants because of its unique spectral signature (
8). Another substantial benefit is that NO
2 is a primary pollutant (i.e., directly emitted from pollution sources) rather than a secondary pollutant formed in the atmosphere (e.g., O
3 and NH
4NO
3), which makes it more straightforward to translate estimated impacts, even if they occur through multiple pathways, to the underlying emissions and possible control measures. This approach is less convoluted, for example, than calculating yield gains associated with a reduction in O
3 and then separately estimating the necessary NO
x reductions needed to achieve the O
3 reductions.
The use of satellite measures of greenness enables us to examine crop conditions at a resolution commensurate with the NO
2 measures, which would not be possible using administrative records of crop yields. Our preferred greenness measure, near-infrared reflectance of vegetation (NIRv) (see Materials and Methods), has been shown in many recent studies to be linearly and strongly correlated with crop growth and yield (
26–
28). Satellite data thus offer a practical and robust way to measure both pollution exposure and crop growth, enabling us to examine the effects of NO
2 in multiple regions and years.
Here, we address three fundamental questions related to NOx impacts for five major growing regions around the world. First, is there a clear negative association between NO2 and crop productivity throughout different regions, consistent with the idea that NOx is an important factor in crop growth? Second, how much does the effect of NO2 differ by season and region, and what do these differences indicate about the direct versus indirect effects of NOx? Third, what is the potential gain in crop productivity that could reasonably be expected if NOx levels were reduced in each region?
RESULTS
We observed a wide range of crop exposure to NO
2 across major growing regions and seasons (
Fig. 2). NO
2 levels were generally highest in the winter season, which leads to exposure of wheat and other winter crops to higher NO
2 levels than summer crops. Exposure was generally highest for crop locations in China, although not all areas in China experienced high levels. After China, exposure was highest in India and Western Europe, with both having many locations with exposures in terms of tropospheric vertical column density (TVCD) above 25 μmol m
−2. North and South America generally had the lowest exposures. All five regions exhibited a considerable range of exposures, even when examining variation within 1° × 1° or 0.5° × 0.5° areas within each region (fig. S1).
These local gradients of NO
2 (i.e., within roughly 50 km × 50 km) form the basis of our estimates of the impacts of NO
2, which rely on the degree to which the local de-meaned NO
2 variations are correlated with spatial variations in de-meaned peak greenness, as measured by the NIRv vegetation index (VI) (
Fig. 3). This identification strategy relies only on local (~50 km) variation to estimate impacts because, while larger-scale spatial variations in both pollution and crop yields (e.g., northern versus southern China) can provide meaningful information, they also greatly increase the risk of confounding from omitted variables (
29). We find that, in all five regions, there is a highly significant negative association between the two (
Fig. 4).
Robustness checks indicate that these relationships are unlikely to arise because of artifacts in the NO
2 retrieval algorithms, specifically the reliance on surface albedo, which is itself influenced by vegetation (table S1). Similarly, results are unlikely to result from the spatial correlation of NO
2 with overall aerosols (of which nitrate aerosols are typically a small fraction) (
30), given that results are robust to including controls for aerosol optical depth (fig. S2). Results are also robust to removing grid cells with a large fraction of noncropland, which could potentially affect both NO
2 and greenness measures (fig. S3), using alternate sources of crop masks (fig. S4) and using alternate measures of crop greenness (fig. S4). These tests and the fact that estimated NO
2 effects were consistently negative across all study years (fig. S4) indicate that these estimates are very likely to reflect a true causal relationship between NO
2 and crop growth. However, these estimates alone cannot indicate the likely mechanism of impact.
To further distinguish between plausible pathways of impact, we partitioned each region into two subsets of observations. In the first subset, we identified points with a ratio of HCHO:NO
2 above 2, which represents situations where O
3 formation is generally NO
x limited (
11) and, therefore, where an increase in NO
x would be expected to lead to an increase in O
3. The second subset included all points with a ratio below 2, where O
3 is expected to be less responsive to variations in NO
x. For our study regions and seasons, only the winter season in China and Western Europe had a considerable fraction of points in both regimes, whereas in other cases, the cropped areas typically experience only the NO
x limited regime, with a ratio above 2 (
Fig. 5, A and B).
When examining the NO
2 sensitivity separately by O
3 regime, we found that (i) NO
2 sensitivity was considerably higher for locations where O
3 formation was likely to be NO
x limited and (ii) NO
2 sensitivity was still significantly negative in regimes where O
3 formation was not NO
x limited (
Fig. 5, C and D). In both China and Europe, the sensitivity for NO
x-limited conditions was roughly double that for nonlimited conditions. These results suggest that O
3 is an important pathway for the impact of NO
2 but that other mechanisms including direct damage from NO
2 likely play an important role in suppressing crop growth, contributing perhaps as much as half of the total damage in some regions.
Table 1 presents an estimate of the total change in crop greenness (NIRv) that would be expected if all locations within a region were to achieve NO
2 levels equal to the fifth percentile of observed levels over the study period. This represents a simplistic scenario of aggressive actions to curb NO
2 and is not meant to substitute for a more detailed analysis of specific control measures but rather to bracket the total possible gain from reducing NO
2. A more extreme scenario, whereby all locations are reduced to zero, was not considered since this would extrapolate beyond the support of the data used to estimate the regressions.
Table 1 and
Fig. 6 also estimate the total yield gain that would be associated with this increase in NIRv. To translate NIRv to yield gain, we rely on the fact that crop photosynthetic activity has been shown to be linearly related to NIRv (
26) (see Materials and Methods). We estimate that reduction of NO
2 could contribute significantly toward yield gains in many cases, with the largest gains estimated for China: 28% in winter and 16% in summer. Western Europe would also experience substantial gains of nearly 10% for both winter and summer crops, with gains in India of roughly 8% in summer and 6% in winter.
DISCUSSION
The effects of NO2 estimated in this study represent the net impact of myriad complex processes that govern both atmospheric chemistry (e.g., the conversion of NO2 to other pollutants) and plant biology (e.g., the ability of plants to recover from exposure to high levels of NO2 or O3). This integration over many processes is both a strength and weakness of our study. By directly relating NO2 to crop productivity, we capture the net effects of many pathways of impact and recovery in actual farmers’ fields, which encompass a diversity of conditions that would be impossible to recreate in controlled experiments. At the same time, the inability to fully disentangle mechanisms can limit the understanding of how effective different potential interventions would be at lowering impacts and can complicate comparisons with prior studies.
For example, comparison with the many prior studies that have considered the effects of O3 on crop growth are difficult because (i) we are capturing effects of multiple pathways by which NOx can affect yields, with O3 being just one of these pathways, (ii) we likely fail to fully capture O3 effects because the longer residence time of O3 means that O3 concentrations are imperfectly correlated with NO2, and (iii) other studies may inadvertently capture some (but not all) NOx effects in their estimates of O3 damages since NOx is correlated with O3 and empirical studies that do not measure NOx will misattribute some direct NOx effects to O3.
Despite these caveats, comparison of our results with prior O
3 studies reveals several similarities. First, we find that the biggest estimated impacts among all locations and seasons are for winter crops in China. This result is similar to Mills
et al. (
31), who identified China as having the largest estimated wheat yield loss out of all wheat-producing countries on the basis of an analysis of exposure to O
3 above 40 ppb.
Second, similar to studies with O
3 (
1,
2), our results indicate that reducing pollution would result in substantial yield gains. Here, we considered reducing NO
2 levels to the fifth percentile observed in the region. This scenario may be more conservative than studies that consider theoretically reducing O
3 exposure to zero, although, since O
3 exposure is often measured above some threshold (e.g., 60 ppb), reducing NO
2 by 50% could lead to far great than 50% reduction in these O
3 metrics. In addition, reducing NO
2 levels to zero is unrealistic, given that lightning contributes a small but nontrivial fraction of global tropospheric NO
x (
32).
In China, we estimate a 28% yield gain for winter crops from reducing NO
2 to background levels (i.e., fifth percentile). For wheat, the main winter crop, an empirical study (
33) estimated that each 10% reduction in O
3 would lead to a 2.5% increase in wheat yields, implying a total of 25% gain from removing O
3. Studies that use dose-response functions from experimental studies and then apply these to observed O
3 levels result in fairly wide ranges, given the uncertainty in both O
3 exposures and response functions. For example, Mills
et al. (
31) estimated between 12 and 25% yield loss for wheat in China depending on the ozone metric used. A recent analysis focused on China estimated potential gains from eliminating O
3 of 21 to 39% for winter wheat, 3.9 to 14% for rice, and 2.2 to 5.5% for maize (
34). Thus, our estimate of ~28% gains possible from reduced air pollution is consistent with prior work focused on O
3. In addition, similar to other studies, we find that gains for summer crops would be roughly half as large as for winter, given that NO
2 levels are generally lower in summer.
In India, we estimate gains from NO
2 reductions that are ~6 to 8% for both winter and summer seasons (
Fig. 6). A recent review of O
3 studies for India wheat estimates 21% yield gains for elimination of O
3 (
35), roughly double our estimate for NO
2. One source of this disparity is likely the fact that the fifth percentile of NO
2 in India is roughly half the mean value, so our reduction scenario would likely leave a considerable amount of O
3 exposure.
In general, our estimated sensitivities to NO
2 are higher for summer than winter seasons (
Fig. 4). Although there are many differences between the two seasons that could plausibly explain this pattern, it is likely that the indirect effects via O
3 are stronger in the summer, both because overall O
3 concentrations are typically higher in summer and the O
3 regime is more NO
x limited in the summer (
Fig. 5). Similarly, the indirect pathway via NH
4NO
3- or NO
2-driven formation of sulfate aerosols is plausibly higher when more NH3 is present, although this relationship is complicated by meteorological factors and the presence of other aerosol precursors in the environment (e.g., SO
2) and likely varies by region. We thus do not attempt to isolate the role of the aerosol pathway, which would require assumptions about the proportion of NH
4NO
3 to overall aerosols and the direct effect of each aerosol type on the greenness measures. However, the fact that NH
3 levels are generally higher in summer (fig. S5) is consistent with enhanced aerosol formation in general. Temperature and radiation regimes also likely play some role, although previous work suggested that damage from NO
2 was smaller, not larger, under high radiation regimes (
21).
Overall, we find a remarkably consistent negative association between NO
2 and crop growth in major cropping regions. The persistence of these negative effects across many conditions, including when NO
x is not limiting O
3 formation, indicates a significant role for direct phytotoxicity of NO
2. At the same time, effects appear most negative in seasons and locations where NO
x likely drives O
3 formation, indicating that indirect pathways are also important. These results indicate that reduction of NO
x emissions could have important benefits for crop production, sometimes exceeding 30% of current yields. The magnitude of these effects have the potential both to alter overall yield growth rates (which are typically ~1% per year) and substantially change cost-benefit analysis for pollution mitigation measures (
36,
37).
Maps of the spatial pattern of impacts (fig. S6) indicate that yield gradients from ambient NO
2 can be substantial within a region, with impacts differing by up to 50%. At first glance, the strong negative yield impacts in China and India may appear at odds with recent reports of substantial greening of vegetation in these countries, with much of that greening associated with croplands (
38). However, trends in greenness should respond to trends in NO
2 rather than average levels, and the trends in greenness in China are highest in the same areas (around the North China plain) that have experienced significant declines in NO
2 since 2005 (
39). Similarly, greenness trends in India were strongest in the northwest, which has experienced much smaller increases in NO
2 than the rest of the country (
39). Thus, while detailed trend analysis is not possible with the short TROPOMI record, the estimated importance of NO
2 reported here is consistent with prior independent analyses of global greenness trends and NO
2 trends.
We anticipate several fruitful directions for future work. Incorporation of other spaceborne measures of crop activity, including measures of photosynthetic activity from solar-induced fluorescence (SIF) (
40,
41), could help to probe the mechanisms of NO
2 effects and the differential sensitivity of crops throughout the growing season. More detailed examination of other pollutants, such as SO
2 and NH
3, and meteorological variables could help to understand variation in NO
2 sensitivity across different regions, years, and seasons. Notwithstanding these remaining research gaps, the consistent negative impact of NO
2 crops across diverse conditions reported here is an important advancement in our understanding of the widespread role that air pollution plays in crop production.