Air pollution disproportionately impairs beneficial invertebrates: a meta-analysis

Abstract

Air pollution has the potential to disrupt ecologically- and economically-beneficial services provided by invertebrates, including pollination and natural pest regulation. To effectively predict and mitigate this disruption requires an understanding of how the impacts of air pollution vary between invertebrate groups. Here we conduct a global meta-analysis of 120 publications comparing the performance of different invertebrate functional groups in unpolluted and polluted atmospheres. We focus on the pollutants ozone, nitrogen oxides, sulfur dioxide and particulate matter. We show that beneficial invertebrate performance is reduced by air pollution, whereas the performance of plant pest invertebrates is not significantly affected. Ozone pollution has the most detrimental impacts, and these occur at concentrations below national and international air quality standards. Changes in invertebrate performance are not dependent on air pollutant concentrations, indicating that even low levels of pollution are damaging. Predicted increases in tropospheric ozone could result in unintended consequences to global invertebrate populations and their valuable ecological services.

Fig. 1. Geographical distribution of studies included in the meta-analysis.

For each included country (highlighted green), the total number of publications (circled) is shown. Map and centroids (points) for each country used the Natural Earth data set with the R package ‘maps’. The treemaps (produced by the R package ‘treemap’) shown for each country are scaled by the total number of effect sizes and indicate the proportion of effect sizes per pollutant.

Fig. 2. The effects of air pollution on pest and beneficial invertebrate performance.

Orchard plots of meta-analytic mean effect sizes (ln RR; log response ratio) for each of three levels of invertebrate pest status. White points represent meta-analytic means and black rectangles represent the 95% confidence intervals from a model across all pollutants (A) or individual pollutants (B–E; ozone (O₃), nitrogen oxides (NO_x), sulfur dioxide (SO₂) and particulate matter (PM), respectively). Points to the left of zero indicate negative impacts and points to the right indicate positive impacts. 95% confidence intervals overlapping the zero line indicate the mean estimate is not significantly different from zero (P < 0.05). Significant effects of O₃, NO_x, and SO₂ are indicated by ***P < 0.0001, **P = 0.004 and *P = 0.046, respectively. Number of effect sizes for significant pests, other herbivores, and beneficial invertebrates (top to bottom): All (415, 282, 166), O₃ (302, 95, 74), NO_x (26, 36, 27), SO₂ (80, 111, 54), PM (7, 40, 11). Source data are provided as a Source Data file.

Fig. 3. The effects of air pollution on the performance of invertebrates from different feeding guilds.

Orchard plots of meta-analytic mean effect sizes (lnRR; log response ratio) for up to seven invertebrate feeding guilds. Model estimates for each feeding guild calculated from less than three studies were not included. White points represent meta-analytic means and black rectangles represent the 95% confidence intervals from a model across all pollutants (A) or individual pollutants (B–E; ozone (O₃), nitrogen oxides (NO_x), sulfur dioxide (SO₂) and particulate matter (PM), respectively). Points to the left of zero indicate negative impacts and points to the right indicate positive impacts. 95% confidence intervals overlapping the zero line indicate the mean estimate is not significantly different from zero (P < 0.05). Number of effect sizes from top to bottom: All (10, 47, 80, 24, 428, 210, 22), O₃ (5, 18, 34, 7, 263, 111, 15), NO_x (12, 14, 12, 31), SO₂ (4, 17, 25, 108, 68), PM (7, 45). Source data are provided as a Source Data file.

Fig. 4. The relationship between air pollutant concentration and changes in invertebrate performance.

Panel A line shows the relationship between the change in invertebrate performance in control and elevated treatments (log response ratio, ln RR) and the scaled concentration of pollution in the elevated treatment (z-transformed within each pollutant type) from meta-regression model. Shaded area shows a 95% confidence interval and P-value is for the slope. B–E Scatter plots showing the relationship between ln RR and the (unscaled) concentration of elevated pollutant treatment for each pollutant. NO_x panel combines NO, NO₂, and NO_x. Dashed vertical lines illustrate the highest National Ambient Air Quality Standards (NAAQS) per pollutant set by the United States Environmental Protection Agency. Levels for NO_x (NO + NO₂) are not stipulated, but the NAAQS hourly daily maximum concentrations for NO₂ is 100 ppb. Source data are provided as a Source Data file.