Assessing the Impact of Ozone on Forest Trees in An Integrative Perspective: Are Foliar Visible Symptoms Suitable Predictors for Growth Reduction? A Critical Review

Abstract

Plant growth reduction (GR) is the most widely accepted damage parameter to assess the sensitivity of trees to tropospheric ozone (O3) pollution since it integrates different physiological processes leading to loss of photosynthetic activity and distraction of metabolic resources from growth to defense, repair, and recovery pathways. Because of the intrinsic difficulty to assess the actual O3 risk assessment for forests in field conditions, foliar visible symptoms (FVS) induced by O3 have been proposed as a proxy to estimate possible GR in forest trees. The rationale for this assumption is that the onset of FVS implies a reduction of the photosynthetic capacity of plants. In this review, we show that GR and FVS can be the consequences of independent physiological pathways involving different response mechanisms that can cause both FVS without GR and GR without FVS. The onset of FVS may not lead necessarily to significant GR at plant level for several reasons, including the rise of compensatory photosynthesis, the time lag between growth processes and the accumulation of critical O3 dose, and the negligible effect of a modest amount of injured leaves. Plant GR, on the other hand, may be induced by different physiological mechanisms not necessarily related to FVS, such as stomatal closure (i.e., carbon starvation) to avoid or reduce O3 uptake, and the increase of respiratory processes for the production of metabolic defense compounds. Growth reduction and FVS can be interpreted as different strategies for the acclimation of plants to a stressful environment, and do not mean necessarily damage. Growth reduction (without FVS) seems to prevail in species adapted to limiting environmental conditions, that avoid loss and replacement of injured leaves because of the high metabolic cost of their production; conversely, FVS manifestation (without GR) and the replacement of injured leaves is more common in species adapted to environments with low-stress levels, since they can benefit from a rapid foliar turnover to compensate for the decreased rate of photosynthesis of the whole plant.

Invasive herbaceous respond more negatively to elevated ozone concentration than native species

“…That indicates in general invasive species had higher foliar injury rates under O 3 stress. Given that the degree of foliar injury is closely related with photosynthesis (Marzuoli et al, 2019; Vainonen & Kangasjärvi, 2015), the most likely explanation for the higher growth suppression of invasive species than of native species is the greater photosynthesis suppression due to higher foliar injury in invasive species.…”

“…Such injuries often appear as chlorosis, necrosis, spots and bronzing (Agathokleous et al, 2020). Some studies suggested that visible foliar injury could be associated with not only plant susceptibility (Bergmann et al, 2017; Davison & Barnes, 1998; Li et al, 2016) but also negative impacts on fitness traits (Marzuoli et al, 2019). In agricultural ecosystems, the influence of elevated O 3 on crop species has received much attention and is well understood, especially the effect on yield reduction (Ainsworth, 2017; Tai et al, 2014; Wilkinson et al, 2012).…”

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

“…While it is difficult to distinguish whether chlorosis and necrosis are induced by O 3 or normal senescence in the field, a characteristic of O 3 -induced symptoms is that they usually occur on interveinal areas of the upper leaf surface only and older leaves show the most symptoms. Species-specific visible injuries have been widely found in nature ( 10 , 35 – 37 ), although evidence for the relationship between O 3 -induced visible injuries and damage is contradictory and uncertain especially for forest trees ( 38 ). Visible injuries may be associated with negative impacts on fitness traits [e.g., the reduction of carbon (C) assimilation/allocation limits growth and seed production, making the species uncompetitive] ( 38 ).…”

“…Species-specific visible injuries have been widely found in nature ( 10 , 35 – 37 ), although evidence for the relationship between O 3 -induced visible injuries and damage is contradictory and uncertain especially for forest trees ( 38 ). Visible injuries may be associated with negative impacts on fitness traits [e.g., the reduction of carbon (C) assimilation/allocation limits growth and seed production, making the species uncompetitive] ( 38 ). Little is known, however, about the relationship between short-term phenomena such as visible foliar injury and longer-term processes affecting plant-community structure and ecosystem biodiversity ( 5 , 10 ).…”

Impacts of Ozone on Forest Plants and Ecosystems

“…Finally, the review paper by Marzuoli et al [6] analysed the relationships between visible foliar symptoms and plant growth reduction based on the available literature on forest tree species exposed to ozone in different experimental systems. The authors concluded that the appearance of visible injuries and negative growth responses are consequences of separate physiological processes such as various compensatory, detoxification and repair processes, increased respiration, defoliation and closure of stomata, leading to ozone avoidance.…”