Ozone affects plant, insect, and soil microbial communities: A threat to terrestrial ecosystems and biodiversity

Abstract

Elevated tropospheric ozone concentrations induce adverse effects in plants. We reviewed how ozone affects (i) the composition and diversity of plant communities by affecting key physiological traits; (ii) foliar chemistry and the emission of volatiles, thereby affecting plant-plant competition, plant-insect interactions, and the composition of insect communities; and (iii) plant-soil-microbe interactions and the composition of soil communities by disrupting plant litterfall and altering root exudation, soil enzymatic activities, decomposition, and nutrient cycling. The community composition of soil microbes is consequently changed, and alpha diversity is often reduced. The effects depend on the environment and vary across space and time. We suggest that Atlantic islands in the Northern Hemisphere, the Mediterranean Basin, equatorial Africa, Ethiopia, the Indian coastline, the Himalayan region, southern Asia, and Japan have high endemic richness at high ozone risk by 2100.

Fig. 1. Effects of elevated ozone (O₃) on aboveground ecosystem processes.

Ecological processes occurring at the ecosystem and foliar levels in a natural (not polluted) ecosystem (A) versus an ecosystem disturbed by increased levels of O₃ (B). Gray icons represent the loss of insect or plant diversity but not for particular species. O₃ reduces the growth rate and biomass of plants (including forest trees) (I). Deciduous broadleaf species are usually more susceptible than evergreen broadleaf and needle-leaf species (I). O₃ can also reduce plant species richness and alter community composition (II). O₃ reduces the abundance of insect species but not species richness in forest ecosystems (III). O₃ and OH degrade biogenic VOC (BVOCs), thereby impeding plant-pollinator communication (IV). O₃-plant-insect interactions may be quite complex and species specific. O₃ inhibits isoprene emissions, increases monoterpene emissions in tolerant and evergreen species, reduces foliar size, induces foliage prematurity (V and I), and increases plant susceptibility to insects and pathogens (I and VI). In other cases, O₃ induces the accumulation of phenolic compounds in leaves, discouraging herbivory by insects (thus reducing insect abundance), increases insect mortality, and inhibits the growth of insect body mass (VII). O₃ also alters foliar phytochemistry, thereby impeding insect oviposition (VIII).

Fig. 2. PSFs under elevated ozone (O₃).

A healthy holobiont in a clean atmosphere (with natural background O₃ levels), where mutually beneficial PSFs occur (A), versus a suppressed holobiont and disturbed PSFs due to O₃ (B). Gray icons represent the loss of microbial biomass but not for particular species. O₃ decreases root biomass, reduces the quantity, and affects the quality of foliar and root litter, potentially affecting litter-feeding soil macrofauna, decomposition, and cycling of nutrients. O₃ may influence the chemical composition of roots and soluble root exudates, including reduced exudation of some extracellular enzymes (e.g., β-glucosidase). The rate of decomposition can be increased or decreased species-specifically. Soil microbial biomass also decreases. O₃ alters the composition and structure of soil microbial communities, with fungi being likely more susceptible to O₃ than bacteria. Some N-fixing bacteria are promoted by O₃, but N fixation is reduced by O₃ in other studies. Some denitrifying bacteria are likewise promoted by O₃, and the abundance of some nitrifying bacteria can be either reduced or increased by O₃. The decrease in microbial biomass disturbs the rates of N and C cycling as feedback, potentially reducing N₂O and storing less C in the rhizosphere. The changes in C and N cycling in PSFs may occur in tandem with changes in the cycling of other nutrients due to poor leaf and root litter as well as affected decomposition processes.

Fig. 3. Ozone exposure levels and global plant endemic richness.

Surface mean AOT40 [parts per million (ppm)·hour] for 2000–2003 (A) and for RCP2.6 (B), RCP4.5 (C), and RCP8.5 (D) by 2100, overlapping the global patterns of the endemic richness of vascular plants (number of species of vascular plants per 10,000 km²) across biogeographic regions worldwide (except Antarctica). RCP represents a representative concentration pathway, and AOT40 represents accumulated ozone exposure above a threshold of 40 parts per billion (ppb). Data sources: (9) and (197). The ozone maps are from (9).