Research ArticleECOLOGY

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

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Science Advances  12 Aug 2020:
Vol. 6, no. 33, eabc1176
DOI: 10.1126/sciadv.abc1176
  • 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).

  • Table 1 Evidence that the susceptibility of plants to O3 is conserved at relatively high taxonomic levels.

    Evidence that the susceptibility of plants to O3 is conserved at relatively high taxonomic levels.. The reader may refer to the references for further details.

    SusceptibilityReference
    Angiosperms > gymnosperms(204)
    Pioneer species > climax species(205)
    Temperate species > subtropical
    species
    (12)
    Therophytes > other Raunkiaer life
    forms (chamaephytes and
    hemicryptophytes)
    (14, 43)
    Deciduous trees > evergreen
    conifers
    (5)
    Deciduous broadleaf species >
    evergreen broadleaf and
    needle-leaf species
    (12)
    Fabaceae (legumes), Poaceae, and
    Asteraceae > Brassicaeae
    (5, 43)
    Fabaceae > Asteraceae,
    Caryophyllaceae, and Poaceae
    (43)
    Myrtaceae and Salicaceae >
    Boraginaceae and Brassicaceae
    (5)
    Legumes > other forbs and grasses(14)
    Species grown under favorable
    growth conditions or productive
    habitats > species grown in less
    productive habitats
    (14)
    Light-loving plants > Plants that
    normally occur in the shade
    (43)
    Plants grown at dry sites > plants
    grown in moister soils
    (43)
    Plants tolerant to moderate salinity
    > plants of no saline habitats
    (43)
  • Table 2 Land areas for three ranges of the endemic richness of vascular plants exposed to high O3 exposures (AOT40, >5 ppm·hour) by 2100 estimated using three RCPs.

    Land area exposed to AOT40 > 5 ppm·hour (%)
    HistoricalRCP2.6RCP4.5RCP8.5
    Area with 20–50 species per
    10,000 km2 (15.1% of total
    land area)
    41.723.929.941.7
    Area with >50 species per
    10.000 km2 (11.4% of total
    land area)
    37.723.223.251.3
    Area with >200 species per
    10,000 km2 (1.8% of total
    land area)
    0.00.00.04.4

Supplementary Materials

  • Supplementary Materials

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

    Evgenios Agathokleous, Zhaozhong Feng, Elina Oksanen, Pierre Sicard, Qi Wang, Costas J. Saitanis, Valda Araminiene, James D. Blande, Felicity Hayes, Vicent Calatayud, Marisa Domingos, Stavros D. Veresoglou, Josep Peñuelas, David A. Wardle, Alessandra De Marco, Zhengzhen Li, Harry Harmens, Xiangyang Yuan, Marcello Vitale, Elena Paoletti

    Download Supplement

    This PDF file includes:

    • Ozone in the atmosphere
    • Ozone effects on plant communities
    • Global maps of AOT40 and endemism richness
    • Table S1
    • References

    Files in this Data Supplement:

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