Current ambient and elevated ozone effects on poplar: A global meta-analysis and response relationships
Graphical abstract
Introduction
Poplars are one of the most economically important trees in temperate areas of the world (Weisgerber and Han, 2000). They provide raw material supplies for industrial processing (e.g., pulp, paper, engineered wood products, pallets, furniture and increasingly bioenergy) and valuable non-wood products (e.g. livestock fodder or medicinal extracts). Furthermore, as fast-growing species, poplars sequester carbon faster than many other woody plants, thus contributing to the mitigation of climate change effects (Liang et al., 2006). Natural forests and woodlands host 91% of the poplar resources, while plantations represent a 6% and agroforestry systems a 3% (Balatinecz et al., 2014). The total area of poplars in the world is 79.1 million ha and the total area of poplar plantations is 5.3 million ha (FAO, 2009).
Despite significantly control efforts and legislation to reduce its precursor emissions, tropospheric ozone (O3) is the most important air pollutant in terms of adverse effects on natural vegetation and cultivated crops (Feng and Kobayashi, 2009; Li et al., 2017; The Royal Society, 2008), and it is also of primary interest due to its strictly relation with climate change (Ochoa Hueso et al., 2017; Lefohn et al., 2018). A recent analysis based on measured data from air quality stations has shown that the increasing trend in [O3] observed since the 19th century has stopped in Europe and other parts of the world (Cooper et al., 2014) but, on the contrary, [O3] are still increasing in Asia due to rising NO2 emissions (Cooper et al., 2014; Feng et al., 2015). Compared to 2000, the relative changes in the mean tropospheric O3, estimated using an ensemble of 15 models, will be −4%, 2%, 1% and 7% in 2030, and −16%, −7%, −9% and 18% in 2100, for IPCC scenarios RCP2.6, RCP4.5, RCP6.0 and RCP8.5, respectively (Young et al., 2013).
The effects of O3 on poplar have been documented in many studies, and poplars are considered to be rather O3 sensitive plants with a variable sensitivity among clones (Berrang et al., 1991; Dumont et al., 2014; Hu et al., 2015; Karnosky et al., 1996; Shang et al., 2017). Common effects of this pollutant on poplar were an onset of visible leaf injuries (Marzuoli et al., 2009; Novak et al., 2003), an impairment of photosynthetic processes (e.g., Shang et al., 2017; Yun and Laurence, 1999), a decrease in growth (e.g., Mäenpää et al., 2011; Volin et al., 1998) and biomass production (e.g., Hu et al., 2015; Nikula et al., 2009), but also reductions in isoprene emission (e.g., Calfapietra et al., 2008; Yuan et al., 2017) and changes in the chemical composition of leaves and wood (e.g., Häikiö et al., 2009; Seija et al., 2010). However, despite the high economic relevancy of this widely distributed tree, and its well-recognized O3 sensitivity, at present there is no review including globally published results summarizing and quantifying the impact of current and elevated [O3] (e[O3]).
On the other hand, several modeling studies have considered the impact of current and future e[O3] on the productivity of the plants and on the CO2 land‑carbon sink, highlighting the importance of changes in atmospheric chemistry as a driver of twenty-first-century climate change (e.g., Sitch et al., 2007). For modeling approaches, the availability of robust response relationships between relevant variables such as light-saturated CO2 assimilation rate (Asat), chlorophyll content (Chl) or biomass and [O3] is essential for estimating the impacts of this pollutant on different plant receptors. Response relationships, especially of biomass in the case of trees, are also central for risk assessment of the O3 effects (LRTAP, 2017). At present, both exposure- and flux-based response relationships have been proposed for several species (e.g. birch and beech, Norway spruce) and plant functional types (Büker et al., 2015; Mills et al., 2007, Mills et al., 2011), including five poplar clones (Hu et al., 2015; Shang et al., 2017). However, response functions based on multiple studies with the potential of being used worldwide are not available yet for poplar.
Therefore, the main two objectives of the present paper are to provide a synthesis of the O3 effects on poplar by means of a meta-analytic review and also to develop O3 exposure-response relationships for key response variables. The following questions are specifically addressed: 1) to what extent current and future e[O3] affect response variables such as gas exchange, growth, biomass, or nutrient content of leaves in comparison with low O3 levels? 2)Do the O3 effects differ for different poplar genotypes, for different O3 exposures (i.e., AOT40, the accumulated O3 exposure over a threshold of 40 ppb during daylight hours)?; 3) Can robust exposure-response relationships (AOT40) for selected tree responses indicators (Asat, Chl and biomass) be established when different poplar species and clones are taken into account?
Section snippets
Database
The database for this meta-analysis was built based on peer-reviewed journal articles searched in the Web of Science (Thompson-ISI, Philadelphia, PA, USA, http://apps.webofknowledge.com). A search was done using the key words ‘ozone’ and ‘poplar’ between years 1980 and 2017. To avoid missing relevant references, the reference lists of any article identified by the key-word search were cross-checked. Articles and their measurements were excluded if (1) O3 fumigation was shorter than thirty days
Effects of ambient [O3] relative to CF
Current ambient O3 concentrations (means of 40–50 ppb) induced significant effects in several variables in comparison with CF (means of 7–27 ppb) (Fig. 1). Compared with CF, current [O3] significantly impaired photosynthesis, as indicated by the reduction in CO2 assimilation rate (Pn) by 33%, Chl by 13% and the maximum quantum yield of PSII photochemistry (Fv/Fm) by 2%. The stomatal conductance (gs) was also significantly reduced by 25%. Significant effects were also observed in growth and in
Effects of ambient [O3] relative to CF
In meta-analytic reviews addressing O3 effects, CF is considered as a representative of [O3] in preindustrial times (e.g., Feng et al., 2008; Wittig et al., 2007, Wittig et al., 2009), when average [O3] was around 15 ppb (Marenco et al., 1994; Volz and Kley, 1988). Certainly, the [O3] in CF treatment exceed this value at preindustrial times due to air filtration technical limitations and high ambient O3 concentration; hence the estimation of the effects may be conservative in these cases. Our
Conclusions and implication
The results of the present study suggest that current [O3] have produced negative effects on poplar, significantly increasing leaf senescence, and reducing the carbon-sink capacity and productivity of natural and planted poplar stands. Future increases of [O3] in some parts of the world (e.g. Asia) are expected to further enhance the decline in total biomass and to compromise growth. The magnitude of the effects in comparison with other tree species confirms that poplar is among the most
Acknowledgements
This study was funded by the Key Research Program of Frontier Sciences, CAS (QYZDB-SSW-DQC019), National Natural Science Foundation of China (No. 31500396 & 41771034), Chinese Academy of Sciences President's International Fellowship Initiative (PIFI) for Senior Scientists (2013T2Z0009). VC also thanks GEISpain project (CGL2014-52838-C2-2-R).
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