Original article
Effect of the elevated ozone on greening tree species of urban: Alterations in C-N-P stoichiometry and nutrient stock allocation to leaves and fine roots

https://doi.org/10.1016/j.ufug.2022.127735Get rights and content

Highlights

  • E-O3 reduced leaf C concentration, but increased fine roots N concentration.

  • E-O3 significantly reduced leaf C and N stocks and had no effect on fine roots.

  • O3-induced increases in leaf P concentration was in deciduous species rather than in evergreen species.

  • Significant differences in the response of evergreen and deciduous broadleaf species to O3.

Abstract

Anthropogenic ground-level ozone (O3) pollution can alter the phosphorus (P), carbon (C), and nitrogen (N) of terrestrial plants’ ecological stoichiometry, which in turn affects forest productivity, nutrient utilization, and carbon sink capacity. However, there is still quite a lot of uncertainty regarding the impact of high O3 levels on C-N-P stoichiometry in organs with a rapid turnover (i.e., fine roots and leaves) across varied functional types. This study investigated the effects of O3 on the stoichiometry of C-N-P nutrient allocation of stocks to various plant organs, with a special focus on tree species frequently employed for urban greening. The impact of O3 on C-N-P stoichiometry among different functional tree types was subsequently evaluated by reviewing the published literature. Under a pooling of all species, elevated O3 decreased and leaf C and P concentrations increased, thereby decreasing the leaf C: P ratio. Elevated O3 increased the N concentration in fine roots, thereby decreasing the C: N ratio, although no significant impact was observed in leaves. Elevated O3 significantly reduced the leaf stocks of C (CSleaf) and N (NSleaf), however, there was no observed variation in these stocks in fine roots. The content of P, C, and N in fine roots and leaves in evergreen broadleaf species exceeded those in deciduous species. Elevated O3 significantly reduced CSleaf, NSleaf, and PSleaf in deciduous broadleaf species, whereas there was a significant reduction for the same in evergreen species. The literature analysis further demonstrated a larger O3-induced increment in leaf P concentration in deciduous species as compared to evergreen species. Elevated O3 significantly increased the difference in C and N stocks between fine roots and leaves in deciduous broadleaf species, whereas this difference was observed to decrease in evergreen species. The results of this study can facilitate an improved understanding of ecological stoichiometric responses of urban greening tree species under O3 stress and the resulting nutrient use strategies.

Introduction

Ozone (O3) at ground level is a strong phytotoxic atmospheric pollutant, and the current levels of ground-level O3 are harming global natural and artificial forests (Mills et al., 2018, Feng et al., 2019, Agathokleous et al., 2020). Volatile organic compounds and nitrogen oxides are the two primary O3 precursors, and anthropogenic activities have greatly increased their emissions. This has led to an increase in O3 (Cooper et al., 2014). Ozone levels have been rising in China at a rate of 1–2 ppb each year (Zeng et al., 2019), and during the last 5–9 months, they have exceeded 100 ppb in the megacities of northern China (Feng et al., 2019). Particularly in urban forests, these elevated O3 concentrations are likely to change the structure and functioning of the forest ecosystem (Li et al., 2016). However, as tree species utilized for urban greening play a significant role in the vulnerable ecology of urban ecosystems, current research primarily focuses on the photosynthesis of afforestation tree species (Yang et al., 2016). The effects of O3 pollution on the ecological stoichiometry of different tree species employed for urban greening have not been widely explored, thus preventing the authorities from making informed choices regarding the plantation of green tree species in cities with severe O3 pollution.

Urban green trees play an indispensable role in maintaining the ecological balance of cities and reducing urban ecological problems (Manes et al., 2012). Elevated O3 can result in a series of adverse physiological and metabolic responses in terrestrial plants, altering the pattern of biomass distribution and the resilience of urban trees to environmental stress, thereby reducing the potential of carbon sequestration and nutrient uptake in the urban forest ecosystem (Agathokleous et al., 2020). These responses often begin in the leaves, following which they affect underground plant processes, such as root dynamics (Li et al., 2020, Pregitzer et al., 2008), the soil microbial community composition (Li et al., 2022b), and uptake and distribution of nutrients in the plant, including P and N (Shang et al., 2018). Plant responses to O3 illustrate intra- (Shang et al., 2017), inter- (de Vries et al., 2014, Li et al., 2016) and organ-specific sensitivity (Li et al., 2022a). For example, the sensitivity of deciduous broadleaved species to O3 tends to exceed that of evergreen species. This can mainly be attributed to the small per-unit-area mass of leaves and small leaf area of deciduous broadleaved species (Feng et al., 2018, Li et al., 2017). Leaves and fine roots are the major factors contributing to biogeochemical turnover due to their shorter lifespans and faster turnover rate (Li et al., 2022a). Recent research has demonstrated that fine roots are more sensitive to O3 than to leaves in terms of response time and biomass loss (Li et al., 2022a, Li et al., 2019). The uptake and distribution of N and P, as well as the assimilation and sequestration of carbon (C), are all impacted by O3-induced damage to the physiological processes in leaves and fine roots (Li et al., 2022a). Therefore, monitoring the nutrient ratios in plants can make it easier to research interspecies differences in organ sensitivity and O3 impacts. The knowledge gained can assist in predicting the plant productivity and C sink potential under future O3 pollution scenarios (Agathokleous et al., 2020, Ainsworth et al., 2012).

Elemental stoichiometry, particularly for N, P, and K, is used to determine how ecological processes and nutrient limitations are affected by environmental change at all scales; from the molecule to the biosphere (Elser et al., 2010). More than half of a plant's dry mass is made up of carbon, which also serves as an energy source and a building block for the skeleton of the plant (Agren, 2008). The Rubisco enzyme, which maximizes photosynthetic effectiveness (Kerkhoff et al., 2005), is primarily composed of nitrogen. In addition to regulating metabolism and protein synthesis, phosphorus is necessary for the synthesis of nucleotides and phospholipids (Paz-Ares et al., 2022). Plant components and growth, which are intimately tied to the C-N-P stoichiometry (Shang et al., 2018, Sterner and Elser, 2002), may be affected by elevated O3. Understanding the C-N-P stoichiometric responses to O3 content is essential for predicting how biogeochemical cycles would evolve in future habitats that will undergo environmental change (Elser et al., 2010, Yan et al., 2017). Recent research has concentrated on the impact of climatic change on the urban forest ecosystem's C-N-P stoichiometry, including the effects of high CO2 concentration (Du et al., 2019), N deposition (Han et al., 2019), warming (Yuan and Chen, 2015), and drought (Yuan and Chen, 2015), in higher plants as well as in soil and microorganisms (Tian et al., 2019, Yuan and Chen, 2015, Zechmeister-Boltenstern et al., 2015). Several studies have shown the impact of high O3 on N, C, and P stoichiometry of the ecosystem (Agathokleous et al., 2018, Cao et al., 2016, Shang et al., 2018, Shi et al., 2021). However, no consistent and clear pattern has yet emerged. For instance, the findings of Shang et al. (2018) revealed that elevated O3 levels increased P but the ratio C: P is decreased for species in the clones of Populus, whereas Cao et al. (2016) identified no changing trend for species belonging to the Phoebe genus. The inconsistency in the study findings may help to explain why interspecies differences in susceptibility to O3 remain uncertain. The ecological stoichiometry of C-N-P and its physiological and biochemical changes throughout tree growth has a significant impact on the ecological advantages of plants selected for urban greening and atmospheric equilibrium as O3 concentrations in the cities continue to rise (Agathokleous et al., 2020, Shang et al., 2018).

The objectives of this study include (1) determination of P, N, and C concentrations and ecological stoichiometric ratios i.e. N:P, C: N, and C:P of the different plant organs under elevated O3 levels in species employed for urban greening; (2) comparing the response variation of C-N-P ecological stoichiometry to O3 among different plant functional types, and (3) determination of the impact of O3 on N, C, and P stocks and distribution within different organs. The results of the present study could facilitate an improved selection and management of plant species for greening of urban areas with high levels of O3.

Section snippets

Experimental location/ site

The experimental site selected for this study was located at the base of the research and experiment of Yanqing (116.34°E, 40.47°N), located in a warm temperate region northwest of Beijing, China, that exhibits a semi-humid and semi-arid continental monsoon climate. This site has an average annual precipitation of 500–600 mm, an average annual temperature of 11–13 °C, an average summer temperature of 22–25 °C, average annual sunshine hours of 2100–2700 h, and an average annual frost-free period

N, C, and P stoichiometric ratios and concentrations among different plant organs

Table 2 and Fig. 1 show the variation impact of high O3 on the concentration of N, C, and P among different plant species and organs. An analysis of the data for all species indicated that relative to the CF, high O3 significantly decreased and increased the leaf concentrations of C and P by 0.5% (Figs. 1a) and 11.4% (Fig. 1e) respectively. Elevated O3 significantly elevated N concentrations of fine roots by 10.7% (Fig. 1d). More specifically, elevated O3 significantly elevated the N, C, and P

Leaf and fine root responses to ozone

The current study is the first to evaluate the impact of O3 pollution levels on the stoichiometry of leaves and fine roots in a variety of urban trees and serves as a guide for choosing urban greening tree species for cities with severe O3 pollution. The accumulation and distribution of components in a tree are strongly related to damage to urban trees in high O3 conditions (Shang et al., 2018). Given the considerable risk that is posed by high O3 concentrations in urban forests, the findings

Conclusions

The present study revealed that the impact of O3 on N, C, and P stoichiometry in fine roots and leaves varied considerably among different tree species. In general, elevated O3 respectively decreased and increased leaf C and leaf P concentrations, thereby decreasing the leaf C: P ratio. The elevated O3 increased the concentrations of N while decreasing the C: N ratio in fine roots, whereas no significant impact was observed in leaves. Ozone had significant negative impacts on stocks of leaf C

CRediT authorship contribution statement

Pin Li designed the research. Xiaofan Hou, Xianjie Wu, Chenhan Ma and Pin Li conducted field experiments and analyzed data. Xiaofan Hou wrote the manuscript, Pin Li, Di Tian and Zhengbing Yan revised the manuscript and comments.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This study was supported by the Fundamental Research Funds for the Central Universities (2021ZY07), and the National Natural Science Foundation of China (31870458). We thank Shuangjiang Li for support with the experimental management. We also thank all the reviewers who participated in the review and MJEditor (www.mjeditor.com) for its linguistic assistance during the preparation of this manuscript.

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