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Article

Impact Assessment of Ozone Absorbed through Stomata on Photosynthetic Carbon Dioxide Uptake by Japanese Deciduous Forest Trees: Implications for Ozone Mitigation Policies

by
Yoshiyuki Kinose
1,2,
Masahiro Yamaguchi
3,4,
Hideyuki Matsumura
5 and
Takeshi Izuta
6,*
1
United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, Fuchu, Tokyo 183-8509, Japan
2
Graduate Faculty of Interdisciplinary Research, University of Yamanashi, Kofu, Yamanashi 400-8510, Japan
3
Graduate School of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Tokyo 183-8509, Japan
4
Graduate School of Fisheries and Environmental Sciences, Nagasaki University, Nagasaki, Nagasaki 852-8521, Japan
5
Environmental Science Research Laboratory, Central Research Institute of Electric Power Industry, Abiko, Chiba 270-1194, Japan
6
Institute of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Tokyo 183-8509, Japan
*
Author to whom correspondence should be addressed.
Forests 2020, 11(2), 137; https://doi.org/10.3390/f11020137
Submission received: 27 November 2019 / Revised: 8 January 2020 / Accepted: 22 January 2020 / Published: 24 January 2020
(This article belongs to the Special Issue Effects of Climate Change and Air Pollutants on Forest Tree Species)
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Abstract

:
Photosynthesis by trees is expected to contribute to preventing climate change including global warming. However, the current levels of tropospheric ozone (O3) reduce the uptake of photosynthetic carbon dioxide (CO2) by forest trees in Japan, which is a concern. Furthermore, it is unknown how much O3 should be reduced to prevent plants’ O3-induced damage. The objective of the present study was to assess the negative effects of the current levels of O3 absorbed via stomata and the impact of its mitigation on the CO2 uptake by trees in Japanese forests. Impact assessment, targeted in 2011–2015, was performed for four deciduous broad-leaved trees: Fagus crenata, Quercus serrata, Q. mongolica var. crispula, and Betula platyphylla var. japonica. The assessment was based on species-specific cumulative stomatal O3 uptake (COU) and species-specific responses of annual photosynthetic CO2 uptake to COU. Annual COU differed between the four trees; the average COU of F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica across Japan was 41.7, 26.5, 33.0, and 29.1 mmol m−2, respectively, and the reductions in CO2 uptake by the four trees were 14.0%, 10.6%, 8.6%, and 15.4%, respectively. Further analysis revealed that reducing the atmospheric O3 concentration by approximately 28%, 20%, 17%, and 49% decreased the O3-induced reductions in photosynthetic CO2 uptake to 5% in F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica, respectively. In the near future, implementing mitigation measures for the O3 damage in plants is expected to enhance the photosynthetic capacity of Japanese forest tree species.

1. Introduction

Climate change, including rising air temperatures and changes in precipitation, is recognized globally as a serious environmental problem [1]. Atmospheric carbon dioxide (CO2) is one of the major factors causing climate change [1]. The CO2 concentration has increased to approximately 400 μmol mol−1 (ppm) from 280 ppm in 1750 with the increasing consumption of fossil fuels and burning of biomass [2,3]. In general, forest trees absorb atmospheric CO2 by leaf photosynthesis, which is expected to attenuate climate change [4,5,6].
Tropospheric ozone (O3) exhibits direct radiative forcing for climate change [1]. O3 also has a potential for indirect radiative forcing, as it reduces the photosynthetic CO2 uptake because of its high phytotoxicity [7,8]. Sitch et al. [9] suggested that indirect radiative forcing, which is the O3-induced reduction in the photosynthetic CO2 fixation, could also contribute to global warming. Thus, an impact assessment of O3 on photosynthetic CO2 uptake is needed to support countermeasures, such as adaptation and mitigation, against the detrimental impact of O3.
Accumulated exposure over a threshold of 40 nmol mol−1 (AOT40) has been utilized to evaluate the effects of O3 on tree species [10,11]. Although such an exposure-based O3 index is useful for impact assessment of O3 on plants because of the ease in calculation and fewer required parameters, stomatal O3 uptake is more related to leaf O3 damage than the exposure-based O3 index [7,12]. In Europe, the impact of O3 on trees has been assessed based on cumulative stomatal O3 uptake (COU) [13]. However, the impact assessment on trees based on stomatal O3 uptake is extremely limited in Asia. The tropospheric O3 concentration in Asia is relatively high in the world [14], indicating remarkable damage of O3 on plants grown in Asia. Therefore, it is necessary to assess the impact of O3 on the photosynthetic CO2 uptake of forest tree species in Asia.
In Japan, the tropospheric O3 concentration has been increasing although the concentration of its precursors, such as nitrogen oxides (NOx) and volatile organic compounds (VOCs), has decreased [15]. The increasing trend of O3 concentration is mainly caused by the reduction in the titration effect of nitric oxide (NO) and partly increasing transboundary transportation of O3 and/or its precursors from the Asian continent [15]. Current levels of O3 are related to growth inhibition of plants and forest decline in Japan [16,17]. Thus, countermeasures may need to be implemented against O3 damage to plants. Mitigation, which refers to the reduction of the atmospheric O3 concentration here, is a fundamental and effective countermeasure against the damage of O3 to plants. To date, however, limited information is available on the effects of the mitigation of O3 on plants and on how much surface O3 concentration should be reduced.
Recently, Yamaguchi et al. [18] evaluated the species-specific responses of cumulative photosynthetic CO2 uptake to COU of the leaves in four Japanese forest tree species: F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica. Using these species-specific responses, we aimed (1) to evaluate the effects of the current levels of O3 absorbed into the leaves via stomata on the photosynthetic CO2 uptake by the four representative Japanese deciduous broad-leaved tree species and (2) to assess the impact of the mitigation of O3, i.e., reducing surface O3 concentration, on the CO2 uptake by the tree species.

2. Materials and Methods

2.1. Overview of Procedure for Simulating Impact and Mitigation Effects of O3 on Photosynthetic CO2 Uptake

In the present study, the impact and mitigation effects of O3 on the annual photosynthetic CO2 uptake per area of sunlit first-flush or early leaves of four Japanese deciduous broad-leaved trees—Fagus crenata, Quercus serrata, Quercus mongolica var. crispula, and Betula platyphylla var. japonica—were simulated in 2011–2015. First, environmental data and phenological data, such as leaf emergence date and leaf senescence date, for estimating stomatal O3 uptake were collected from the databases of Japan Meteorological Agency (https://www.data.jma.go.jp/obd/stats/etrn/index.php), National Institute for Environmental Studies (https://www.nies.go.jp/igreen/), and Moderate Resolution Imaging Spectroradiometer (MODIS) product (https://doi.org/10.5067/MODIS/MCD12Q2.006). Second, COU at the O3 monitoring stations was estimated for the four tree species using species-specific parameters of the stomatal O3 uptake model developed by Kinose et al. [19]. The meteorological and phenological data to calculate the COU were obtained from nearby meteorological stations and nearby areas where the trees were distributed, respectively. Third, COU in the tree distribution areas (Ministry of the Environment, http://www.biodic.go.jp/index.html) was estimated by interpolating the COU at the monitoring stations of O3 using ordinary kriging. Fourth, according to species-specific responses of annual CO2 uptake to COU reported by Yamaguchi et al. [18], O3-induced reductions in CO2 uptake for the four trees were calculated. Finally, the effects of O3 mitigation, i.e., impact of reducing the surface O3 concentration, on CO2 uptake were calculated for the four tree species by simulating the input O3 concentrations. A summary of information on simulation settings, required data, and data sources is provided in Table 1.

2.2. Simulating Cumulative Stomatal O3 Uptake

COU is given by
COU = ΣFst
Fst = [O3]/(Rs_O3 + Rb_O3)
Rs_O3 = 1/(0.663 × gs)
Rb_O3 = 1.3 × 150 × (Ld/u)0.5
where Fst is the stomatal O3 uptake, [O3] is the atmospheric O3 concentration, Rs_O3 and Rb_O3 are the stomatal resistance and leaf boundary layer resistance to O3, respectively, gs is the stomatal conductance to H2O, Ld is the crosswind leaf dimension, and u is the wind speed.
The gs was estimated according to the gs model provided by Kinose et al. [19], originally developed by Jarvis [21]:
gs = gmax × fphen × flight × max(fmin, ftemp × fVPD × fSWC × fO3conc)
where gmax is the maximum gs; fmin is the ratio of minimum gs to gmax; and fphen, flight, ftemp, fVPD, fSWC, and fO3conc represent responses of gs/gmax to leaf phenology, photosynthetic photon flux density (PPFD), air temperature, vapor pressure deficit, volumetric soil water content, and atmospheric O3 concentration, respectively. These parameters are species-specific and were essentially based on our previous results (see details in Kinose et al. [19]). The leaf emergence date and leaf senescence date were provided by MODIS Land Cover Dynamics Product, MCD12Q2 v. 006, in 500-m grids in the world. Seasonal changes in enhanced vegetation index (EVI) of the MCD12Q2 were substituted for the fphen. These phenological data were obtained considering tree distribution using vegetation raster data (45′′ × 30′′ mesh) of the National Survey on the Natural Environment (Ministry of the Environment), indicating the distribution of dominant species, although uncertainties exist in the dataset because the forest is not necessarily pure. In the present study, gs was considered to be unchanged according to soil water content, i.e., fSWC = 1, because the amount of precipitation was relatively high in Japan (annual mean precipitation: approximately 1700 mm).
The concentrations of photochemical oxidants are officially monitored at approximately 1200 monitoring stations across Japan (National Institute for Environmental Studies). In the present study, the concentration of photochemical oxidants was considered as the concentration of O3 [10]. The meteorological data such as air temperature and wind velocity officially monitored at approximately 1300 monitoring stations throughout Japan (Japan Meteorological Agency) were used for the calculation of COU. PPFD was estimated based on the study by Masaki et al. [22]. The vapor pressure deficit (VPD) was estimated regarding the vapor pressure during the daytime as the saturated vapor pressure at the minimum temperature on the day, as the relative air humidity is almost 100% at the minimum temperature. The distribution of monitoring stations of photochemical oxidants and meteorological factors and regional partition in Japan is shown in Figure 1.
The gaussian model was used as a semi-variogram model in the ordinary kriging to interpolate the annual COU at the O3 monitoring stations, which was clipped by the tree distribution. As in a previous study [23], we did not interpolate the input data for calculating COU, i.e., meteorological data and O3 data, because the interpolation is extremely difficult due to enormous calculation time. Kriging interpolation was performed using SAGA GIS v. 6.4.0 [24].

2.3. Impact Assessment of O3-induced Reduction in Annual Photosynthetic CO2 Uptake

The responses of annual photosynthetic CO2 uptake to COU were fitted by the Weibull function, and the O3-induced reduction in annual CO2 uptake was calculated as follows:
O3-induced reduction in annual photosynthetic CO2 uptake = 100 − 100 × exp[−(COU/ω)λ]
where ω and λ are species-specific parameters of the Weibull function. ω and λ were originally proposed by Yamaguchi et al. [18] and were modified to make the intercept 100 (Figure 2).
Since previous studies indicated that leaf morphological and physiological characteristics, such as leaf mass per area and gross photosynthetic rate, are related to the sensitivity to O3 [7,25], the leaf-level photosynthetic sensitivity to O3 might be different between seedlings and mature trees due to the differences in their leaf characteristics. However, this has not been clarified to date. In the present study, therefore, we assumed that the responses of CO2 uptake to COU obtained in the seedlings in Yamaguchi et al. [18] were the same as those in the mature trees, although this might cause estimation errors in the impact of O3 on CO2 uptake to some extent.

3. Results

Figure 3 shows the spatial distribution of 5-year mean annual COU per unit leaf area of F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica in Japan in 2011–2015. The annual COU in each year is indicated in Figure 4. The 5-year mean COU averaged across Japan differed between the tree species, being 41.7 (2011–2015 range: 37.2–46.2), 26.5 (24.1–27.9), 33.0 (29.7–34.9), and 29.1 (27.8–30.6) mmol m−2 in the leaves of F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica, respectively. COU was relatively low in the Tohoku and Hokkaido regions, and relatively high in Kanto, Chubu, Kinki, and Chugoku regions relative to the other regions.
Figure 5 shows the spatial distribution of the 5-year mean O3-induced reduction in annual CO2 uptake per unit leaf area of F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica in Japan in 2011–2015. The O3-induced reduction in annual CO2 uptake each year is shown in Figure 6. The 5-year mean O3-induced reduction in CO2 uptake averaged across Japan differed between the tree species, being 14.0% (2011–2015 range: 9.5–18.7%), 10.6% (7.3–12.1%), 8.6% (6.2–10.0%), and 15.4% (14.2–16.7%) in the leaves of F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica, respectively.
Figure 7 demonstrates the impact of O3 mitigation on the annual CO2 uptake per unit leaf area of F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica in 2011–2015. A curvilinear response of the reduction in the surface O3 concentration to the O3-induced reduction in the annual CO2 uptake was observed in the four tree species. To diminish the O3-induced reduction in the annual CO2 uptake to a value of 5%, the surface O3 concentrations should be reduced by 28% (2011–2015 range: 19–34%), 20% (11–23%), 17% (8–21%), and 49% (46–51%) for F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica, respectively.

4. Discussion

The present study firstly evaluated the impact of the current levels of O3 absorbed via stomata on the annual cumulative photosynthetic CO2 uptake per unit leaf area of four Japanese forest tree species. The O3-induced reduction in annual CO2 uptake averaged across Japan was 14.0%, 10.6%, 8.6%, and 15.4% in F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica, respectively (Figure 5 and Figure 6). This result indicated that the current atmospheric O3 concentrations have the potential to reduce the capacity of CO2 uptake by Japanese forest tree species.
Kinose et al. [19] indicated that when the four tree species were grown in the same environmental conditions, the COU was ranked as follows: B. platyphylla var. japonica > F. crenata > Q. mongolica var. crispula > Q. serrata. However, the tree distributions and environmental growth conditions greatly differ between the four tree species. Betula platyphylla var. japonica is mainly distributed in the Hokkaido region, where the stomatal O3 uptake was relatively low (Figure 3). As a result, the COU of B. platyphylla var. japonica averaged across Japan was lower than that of F. crenata and Q. mongolica var. crispula (Figure 3 and Figure 4). Nevertheless, the impact of O3 on the CO2 uptake of B. platyphylla var. japonica was more remarkable than that of the other tree species (Figure 5 and Figure 6). This is due to the relatively higher sensitivity of photosynthetic CO2 uptake to COU in B. platyphylla var. japonica (Figure 2).
Several studies have assessed the effects of O3 absorbed via stomata on gross or net primary production (GPP or NPP, respectively) in forest ecosystems [9,26]. Lombardozzi et al. [26] estimated the O3-induced reduction in GPP targeted at global forest based on the relationships between COU and maximum carboxylation rate and between COU and stomatal conductance derived in a specific tree species, the tulip poplar. Sitch et al. [9] evaluated the impact of O3 on the GPP of five plant functional types, namely broad-leaved trees, conifers, C3 grasses, C4 grasses, and shrubs, considering different sensitivities of the net photosynthetic rate to O3 among the plant functional types. However, the sensitivity of the photosynthetic capacity to O3 is extremely different between tree species possibly because of the differences in the defensive ability to O3 [18]. The advantage of our impact assessment is that we considered the species-specific responses of photosynthetic CO2 uptake to COU, even though there was uncertainty in the evaluation of O3-induced reduction rates by 3.1%, 3.6%, 3.8%, and 6.2% in F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica, respectively (Figure 2).
In the present study, COU and O3-induced reduction rates of CO2 uptake were relatively high in Kanto, Chubu, Kinki, and Chugoku regions (Figure 3, Figure 4, Figure 5 and Figure 6). Akimoto et al. [15] reported that the contribution of the transboundary transport of O3 from the Asian continent to its concentration in Japan seemed to be relatively small except for that in the Kyushu region. According to Nagashima et al. [27], the contribution to the O3 concentrations in Japan from China and the Korean Peninsula were estimated to be approximately 10% and 4%, respectively, although the domestic contribution was approximately 42% in the Japanese summer. Furthermore, O3 is recognized as a short-lived climate pollutant (SLCP). These results indicate the necessity and effectiveness of domestic countermeasures against O3 formulation for avoiding the O3-induced reduction in CO2 uptake by Japanese forest tree species.
The concept of critical level of O3 has been discussed in Europe to prevent its damage to plants. The critical levels of O3 for European beech and European birch were defined as 5 ppm h of daylight AOT40 to diminish the growth reduction to a value of 5% [28]. In Japan, a provisional critical level based on AOT40 is suggested for the tree species sensitive to O3, namely 8–15 ppm h (6 months) corresponding to a 10% growth reduction [29]. However, the critical level based on stomatal O3 uptake has been developed because the O3 absorbed through stomata is more physiologically related to the O3 damage to tree growth [30]. Critical levels of the two European trees were set at 5.2 mmol m−2 of POD1 (phytotoxic O3 dose above the threshold of 1 nmol m−2 s−1) corresponding to a 4% growth reduction [28]. Although this concept of the critical level of O3 is more scientifically plausible, how much O3 should be reduced is unclear. While the stomatal O3 uptake concept is significantly useful to assess the impact of O3 on plants, to create and implement mitigation measures against O3 damage to plants, determining the atmospheric O3 concentration is needed. To the best of our knowledge, the present study is the first to evaluate the impact of the mitigation of O3 absorbed via stomata on the annual photosynthetic CO2 uptake. As a result, we clarified that O3 concentrations should be reduced by 28% (2011–2015 range: 19–34%), 20% (11–23%), 17% (8–21%), and 49% (46–51%) for F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica, respectively, to diminish the O3-induced reduction to a value of 5% (Figure 7). Because the domestic contribution of O3 formation is 42% in the Japanese summer [27], it would be impossible to prevent the O3 damage by 5% for B. platyphylla var. japonica by domestic control of the emission of O3 precursors. In contrast, such a mitigation measure may be effective for the other tree species: F. crenata, Q. serrata, and Q. mongolica var. crispula. We provisionally propose that the O3 concentration should be reduced by approximately 30% to decrease its damage on CO2 uptake below 5% in some Japanese forest tree species. We hope our results will contribute to creating and implementing mitigation measures against the detrimental impact of O3 on forest tree species in Japan and to enhancing their photosynthetic CO2 uptake.
There are some uncertainties and future issues in the assessment on the impact of O3 on the photosynthetic CO2 uptake by forest tree species, including estimation accuracies of the stomatal conductance and errors of COU induced by the interpolation or extrapolation by kriging. One of the major issues is whether the parameterization results of the stomatal conductance model and the responses of CO2 uptake to COU obtained in the particular environment of the experimental studies by Kinose et al. [19] and Yamaguchi et al. [18] could be applicable to the whole Japan in 2011–2015. Alonso et al. [31] reported different parameter values of the stomatal conductance model of Quercus ilex between marine-influenced sites and continental sites, indicating that the values of the model parameters depend on the environmental growth conditions of the trees. Actually, the optimum air temperature for stomatal opening depends on the growth conditions of F. crenata seedlings in Japan possibly because of an acclimation to the air temperature [32]. Therefore, the application of the stomatal conductance model of Kinose et al. [19] to the whole Japan may cause estimation errors of COU. Furthermore, Kinose et al. [7] indicated a higher sensitivity in the high-fertilized F. crenata seedlings due to the higher COU. In a forest area with a higher soil nutrient status, stomatal conductance may be higher via photosynthetic enhancement and be limited to some extent with shorter leaf longevity [33], indicating nutrient-dependent gmax and fphen. In the present study, nutrient-dependent fphen may be partly considered because fphen was determined from the seasonal changes in EVI provided by satellite data. However, gmax was regarded as a constant in the present study, which could cause estimation errors of COU. The nutrient-induced modification of gmax in the calculation of COU is an issue to be considered in the future. On the other hand, the responses of CO2 uptake to COU can differ depending on the growth conditions because the environmental conditions, such as atmospheric CO2 concentration and soil drought, affect the leaf detoxification capacity to O3 [34,35]. However, information on the effects of tree growth environment on the responses of CO2 uptake to COU is insufficient to date. In order to perform a more accurate evaluation of the impact of O3 on the photosynthetic CO2 uptake by forest tree species, the effects of environmental growth conditions on COU and responses of CO2 uptake to COU should be considered.

5. Conclusions

We evaluated the O3-induced reduction in annual CO2 uptake per unit leaf area of Fagus crenata, Quercus serrata, Quercus mongolica var. crispula, and Betula platyphylla var. japonica in 2011–2015 based on the COU per unit leaf area and species-specific responses of the annual CO2 uptake to COU. The current levels of ambient O3 reduced the annual CO2 uptake of F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica by 14.0%, 10.6%, 8.6%, and 15.4%, respectively. Further analysis revealed that, to diminish the O3 damage to a value of 5%, O3 concentrations should be reduced by 28%, 20%, 17%, and 49% for F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica, respectively. We hope that implementing mitigation measures against O3 damage will help increase the photosynthetic CO2 uptake by Japanese forest tree species.

Author Contributions

Conceptualization, T.I. and H.M.; Investigation, Y.K.; Data Curation, Y.K.; Resources, H.M. and M.Y.; Writing—Original Draft Preparation, Y.K.; Writing—Review & Editing, T.I., H.M., and Y.M.; Visualization, Y.K.; Supervision, T.I.; Funding acquisition, T.I. All authors have read and agreed to the published version of the manuscript.

Funding

The present study was funded by the Ministry of the Environment, Japan, through the Program of the Environment Research and Technology Development Fund (5B-1105, to T.I.).

Acknowledgments

The authors would like to thank Takayoshi Koike (Hokkaido University) and Mitsutoshi Kitao (Forestry and Forest Products Research Institute) for their valuable suggestions and technical support. The authors are greatly indebted to Makoto Watanabe (Tokyo University of Agriculture and Technology) for his technical support.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

  1. Pachauri, R.K.; Meyer, L.A. (Eds.) IPCC Climate Change 2014: Synthesis Report; IPCC: Geneva, Switzerland, 2014; 151p, ISBN 978-92-9169-143-2. [Google Scholar]
  2. Joos, F.; Spahni, R. Rates of change in natural and anthropogenic radiative forcing over the past 20,000 years. Proc. Natl. Acad. Sci. USA 2008, 105, 1425–1430. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Dlugokencky, E.; Tans, P. NOAA/ESRL. 2019. Available online: https://www.esrl.noaa.gov/gmd/ccgg/trends/ (accessed on 24 November 2019).
  4. Bonan, G.B. Forests and Climate Change: Forcings, Feedbacks, and the Climate Benefits of Forests. Science 2008, 320, 1444–1449. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  5. Pan, Y.; Birdsey, R.A.; Fang, J.; Houghton, R.; Kauppi, P.E.; Kurz, W.A.; Phillips, O.L.; Shvidenko, A.; Lewis, S.L.; Canadell, J.G.; et al. A Large and Persistent Carbon Sink in the World’s Forests. Science 2011, 333, 988–993. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  6. Keenan, T.F.; Prentice, I.C.; Canadell, J.G.; Williams, C.A.; Wang, H.; Raupach, M.; Collatz, G.J. Recent pause in the growth rate of atmospheric CO2 due to enhanced terrestrial carbon uptake. Nat. Commun. 2016, 7, 13428. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  7. Kinose, Y.; Fukamachi, Y.; Okabe, S.; Hiroshima, H.; Watanabe, M.; Izuta, T. Photosynthetic responses to ozone of upper and lower canopy leaves of Fagus crenata Blume seedlings grown under different soil nutrient conditions. Environ. Pollut. 2017, 223, 213–222. [Google Scholar] [CrossRef] [PubMed]
  8. Kinose, Y.; Fukamachi, Y.; Okabe, S.; Hiroshima, H.; Watanabe, M.; Izuta, T. Nutrient supply to soil offsets the ozone-induced growth reduction in Fagus crenata seedlings. Trees 2017, 31, 259–272. [Google Scholar] [CrossRef]
  9. Sitch, S.; Cox, P.M.; Collins, W.J.; Huntingford, C. Indirect radiative forcing of climate change through ozone effects on the land-carbon sink. Nature 2007, 448, 791–794. [Google Scholar] [CrossRef]
  10. Watanabe, M.; Matsuo, N.; Yamaguchi, M.; Matsumura, H.; Kohno, Y.; Izuta, T. Risk assessment of ozone impact on the carbon absorption of Japanese representative conifers. Eur. J. For. Res. 2010, 129, 421–430. [Google Scholar] [CrossRef] [Green Version]
  11. Watanabe, M.; Yamaguchi, M.; Matsumura, H.; Kohno, Y.; Izuta, T. Risk assessment of ozone impact on Fagus crenata in Japan: Consideration of atmospheric nitrogen deposition. Eur. J. For. Res. 2011, 131, 475–484. [Google Scholar] [CrossRef]
  12. Reich, P.B. Quantifying plant response to ozone: A unifying theory. Tree Physiol. 1987, 3, 63–91. [Google Scholar] [CrossRef]
  13. Oliver, R.J.; Mercado, L.M.; Sitch, S.; Simpson, D.; Medlyn, B.E.; Lin, Y.-S.; Folberth, G.A. Large but decreasing effect of ozone on the European carbon sink. Biogeosciences 2018, 15, 4245–4269. [Google Scholar] [CrossRef] [Green Version]
  14. Royal Society Ground-Level Ozone in the 21st Century: Future Trends, Impacts and Policy Implications; The Royal Society: London, UK, 2008; 132p, ISBN 978-0-85403-713-1.
  15. Akimoto, H.; Mori, Y.; Sasaki, K.; Nakanishi, H.; Ohizumi, T.; Itano, Y. Analysis of monitoring data of ground-level ozone in Japan for long-term trend during 1990–2010: Causes of temporal and spatial variation. Atmos. Environ. 2015, 102, 302–310. [Google Scholar] [CrossRef]
  16. Kume, A.; Numata, S.; Watanabe, K.; Honoki, H.; Nakajima, H.; Ishida, M. Influence of air pollution on the mountain forests along the Tateyama–Kurobe Alpine route. Ecol. Res. 2009, 24, 821–830. [Google Scholar] [CrossRef]
  17. Takeda, M.; Komatsu, H. Development of a comprehensive monitoring method for assessing the vegetation decline in the beech forests. Bull. Kanagawa Environ. Res. Cent. 2012, 45, 45–51. (In Japanese) [Google Scholar]
  18. Yamaguchi, M.; Kinose, Y.; Matsumura, H.; Izuta, T. Evaluation of O3 effects on cumulative photosynthetic CO2 uptake in seedlings of four Japanese deciduous broad-leaved forest tree species based on stomatal O3 uptake. Forests 2019, 10, 556. [Google Scholar] [CrossRef] [Green Version]
  19. Kinose, Y.; Azuchi, F.; Uehara, Y.; Kanomata, T.; Kobayashi, A.; Yamaguchi, M.; Izuta, T. Modeling of stomatal conductance to estimate stomatal ozone uptake by Fagus crenata, Quercus serrata, Quercus mongolica var. crispula and Betula platyphylla. Environ. Pollut. 2014, 194, 235–245. [Google Scholar] [CrossRef] [PubMed]
  20. Friedl, M.; Gray, J.; Sulla-Menashe, D. MCD12Q2 MODIS/Terra+Aqua Land Cover Dynamics Yearly L3 Global 500m SIN Grid V006. NASA EOSDIS Land Processes DAAC. 2019. Available online: https://doi.org/10.5067/MODIS/MCD12Q2.006 (accessed on 24 November 2019).
  21. Jarvis, P.G.; Monteith, J.L.; Weatherley, P.E. The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1976, 273, 593–610. [Google Scholar] [CrossRef]
  22. Masaki, Y.; Kuwagata, T.; Ishigooka, Y. Precise estimation of hourly global solar radiation for micrometeorological analysis by using data classification and hourly sunshine. Theor. Appl. Climatol. 2010, 100, 283–297. [Google Scholar] [CrossRef]
  23. Feng, Z.; Kobayashi, K.; Li, P.; Xu, Y.; Tang, H.; Guo, A.; Paoletti, E.; Calatayud, V. Impacts of current ozone pollution on wheat yield in China as estimated with observed ozone, meteorology and day of flowering. Atmos. Environ. 2019, 217, 116945. [Google Scholar] [CrossRef]
  24. Conrad, O.; Bechtel, B.; Bock, M.; Dietrich, H.; Fischer, E.; Gerlitz, L.; Wehberg, J.; Wichmann, V.; Böhner, J. System for Automated Geoscientific Analyses (SAGA) v. 2.1.4. Geosci. Model Dev. 2015, 8, 1991–2007. [Google Scholar] [CrossRef] [Green Version]
  25. Li, P.; Calatayud, V.; Gao, F.; Uddling, J.; Feng, Z. Differences in ozone sensitivity among woody species are related to leaf morphology and antioxidant levels. Tree Physiol. 2016, 36, 1105–1116. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  26. Lombardozzi, D.; Levis, S.; Bonan, G.; Sparks, J.P. Predicting photosynthesis and transpiration responses to ozone: Decoupling modeled photosynthesis and stomatal conductance. Biogeosciences 2012, 9, 3113–3130. [Google Scholar] [CrossRef] [Green Version]
  27. Nagashima, T.; Ohara, T.; Sudo, K.; Akimoto, H. The relative importance of various source regions on East Asian surface ozone. Atmospheric Chem. Phys. 2010, 10, 11305–11322. [Google Scholar] [CrossRef] [Green Version]
  28. CLRTAP Mapping Critical Levels for Vegetation. Chapter III of Manual on Methodologies and Criteria for Modelling and Mapping Critical Loads and Levels and Air Pollution Effects, Risks and Trends. UNECE Convention on Long-Range Transboundary Air Pollution, 2017. Available online: https://www.icpmapping.org (accessed on 24 November 2019).
  29. Kohno, Y.; Matsumura, H.; Ishii, T.; Izuta, T. Establishing critical levels of air pollutants for protecting East Asian vegetation—A challenge. In Plant Responses to Air Pollution and Global Change; Omasa, K., Nouchi, I., De Kok, L.J., Eds.; Springer Japan: Tokyo, Japan, 2005; pp. 243–250. ISBN 978-4-431-31013-6. [Google Scholar]
  30. Karlsson, P.E.; Braun, S.; Broadmeadow, M.; Elvira, S.; Emberson, L.; Gimeno, B.S.; Le Thiec, D.; Novak, K.; Oksanen, E.; Schaub, M.; et al. Risk assessments for forest trees: The performance of the ozone flux versus the AOT concepts. Environ. Pollut. 2007, 146, 608–616. [Google Scholar] [CrossRef]
  31. Alonso, R.; Elvira, S.; Sanz, M.J.; Gerosa, G.; Emberson, L.D.; Bermejo, V.; Gimeno, B.S. Sensitivity analysis of a parameterization of the stomatal component of the DO3SE model for Quercus ilex to estimate ozone fluxes. Environ. Pollut. 2006, 155, 473–480. [Google Scholar] [CrossRef] [PubMed]
  32. Azuchi, F.; Kinose, Y.; Matsumura, T.; Kanomata, T.; Uehara, Y.; Kobayashi, A.; Yamaguchi, M.; Izuta, T. Modeling stomatal conductance and ozone uptake of Fagus crenata grown under different nitrogen loads. Environ. Pollut. 2014, 184, 481–487. [Google Scholar] [CrossRef] [PubMed]
  33. Kikuzawa, K.; Lechowicz, M.J. Ecology of Leaf Longevity; Springer: Tokyo, Japan, 2011; ISBN 978-4-431-53917-9. [Google Scholar]
  34. Alonso, R.; Elvira, S.; Castillo, F.J.; Gimeno, B.S. Interactive effects of ozone and drought stress on pigments and activities of antioxidative enzymes in Pinus halepensis. Plant Cell Environ. 2001, 24, 905–916. [Google Scholar] [CrossRef]
  35. Booker, F.L.; Fiscus, E.L. The role of ozone flux and antioxidants in the suppression of ozone injury by elevated CO2 in soybean. J. Exp. Bot. 2005, 56, 2139–2151. [Google Scholar] [CrossRef] [Green Version]
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Figure 1. Distribution of monitoring stations of photochemical oxidants (red circle) and meteorological factors (green circle) and regional division in Japan.
Figure 1. Distribution of monitoring stations of photochemical oxidants (red circle) and meteorological factors (green circle) and regional division in Japan.
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Figure 2. Responses of annual CO2 uptake per unit leaf area to cumulative stomatal O3 uptake (COU) of F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica seedlings. These responses were obtained from the study by Yamaguchi et al. [18] with slight modifications. The Y-intercept was modified to 100 in the present study. Plots indicate the first-flush or early leaves (○) or second-flush or late leaves (×). The Weibull function was fitted to the response, and its parameters, ω and λ, and the mean absolute error (MAE, %) are indicated in each figure.
Figure 2. Responses of annual CO2 uptake per unit leaf area to cumulative stomatal O3 uptake (COU) of F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica seedlings. These responses were obtained from the study by Yamaguchi et al. [18] with slight modifications. The Y-intercept was modified to 100 in the present study. Plots indicate the first-flush or early leaves (○) or second-flush or late leaves (×). The Weibull function was fitted to the response, and its parameters, ω and λ, and the mean absolute error (MAE, %) are indicated in each figure.
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Figure 3. Spatial distribution of 5-year mean annual cumulative stomatal O3 uptake (COU) per unit leaf area (mmol m−2) of F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica in 2011–2015.
Figure 3. Spatial distribution of 5-year mean annual cumulative stomatal O3 uptake (COU) per unit leaf area (mmol m−2) of F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica in 2011–2015.
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Figure 4. Annual cumulative stomatal O3 uptake (COU) per unit leaf area (mmol m−2) of F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica in 2011–2015. Horizontal solid lines show the median, boxes show the first through third interquartile ranges, and whiskers show the minimum and maximum COU.
Figure 4. Annual cumulative stomatal O3 uptake (COU) per unit leaf area (mmol m−2) of F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica in 2011–2015. Horizontal solid lines show the median, boxes show the first through third interquartile ranges, and whiskers show the minimum and maximum COU.
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Figure 5. Spatial distribution of 5-year mean O3-induced reduction in annual CO2 uptake per unit leaf area (%) of F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica in 2011–2015.
Figure 5. Spatial distribution of 5-year mean O3-induced reduction in annual CO2 uptake per unit leaf area (%) of F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica in 2011–2015.
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Figure 6. Ozone-induced reduction in annual CO2 uptake per unit leaf area (%) of F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica in 2011–2015. Horizontal solid lines show the median, boxes show the first through third interquartile ranges, and whiskers show the minimum and maximum reductions in CO2 uptake.
Figure 6. Ozone-induced reduction in annual CO2 uptake per unit leaf area (%) of F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica in 2011–2015. Horizontal solid lines show the median, boxes show the first through third interquartile ranges, and whiskers show the minimum and maximum reductions in CO2 uptake.
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Figure 7. Effects of O3 mitigation for the O3-induced reduction in annual CO2 uptake per unit leaf area (%) of F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica in Japan in 2011–2015. The range of the O3-induced reduction in annual CO2 uptake in 2011–2015 is represented in gray, and the means are indicated by the solid black lines.
Figure 7. Effects of O3 mitigation for the O3-induced reduction in annual CO2 uptake per unit leaf area (%) of F. crenata, Q. serrata, Q. mongolica var. crispula, and B. platyphylla var. japonica in Japan in 2011–2015. The range of the O3-induced reduction in annual CO2 uptake in 2011–2015 is represented in gray, and the means are indicated by the solid black lines.
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Table
Table 1. Simulation setting and data sources for the impact assessment of O3 on annual CO2 uptake.
Table 1. Simulation setting and data sources for the impact assessment of O3 on annual CO2 uptake.
ParameterValue or Source
Targeted year2011–2015
Targeted leavesSunlit leaves
Calculation time step1 h
LatitudeFrom 24° to 46°
LongitudeFrom 122° to 154°
Meteorological factorsJapan Meteorological Agency (https://www.data.jma.go.jp/obd/stats/etrn/index.php)
Ozone concentrationNational Institute for Environmental Studies (https://www.nies.go.jp/igreen/)
Tree distribution (45′′ × 30′′ mesh)Ministry of the Environment (http://www.biodic.go.jp/index.html)
Parameters of stomatal conductance modelKinose et al. [19]
Phenology (leaf emergence date, leaf senescence date, and fphen)Friedl et al. [20] (https://doi.org/10.5067/MODIS/MCD12Q2.006)
Response of annual photosynthetic CO2 uptake to COU Yamaguchi et al. [18]

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Kinose, Y.; Yamaguchi, M.; Matsumura, H.; Izuta, T. Impact Assessment of Ozone Absorbed through Stomata on Photosynthetic Carbon Dioxide Uptake by Japanese Deciduous Forest Trees: Implications for Ozone Mitigation Policies. Forests 2020, 11, 137. https://doi.org/10.3390/f11020137

AMA Style

Kinose Y, Yamaguchi M, Matsumura H, Izuta T. Impact Assessment of Ozone Absorbed through Stomata on Photosynthetic Carbon Dioxide Uptake by Japanese Deciduous Forest Trees: Implications for Ozone Mitigation Policies. Forests. 2020; 11(2):137. https://doi.org/10.3390/f11020137

Chicago/Turabian Style

Kinose, Yoshiyuki, Masahiro Yamaguchi, Hideyuki Matsumura, and Takeshi Izuta. 2020. "Impact Assessment of Ozone Absorbed through Stomata on Photosynthetic Carbon Dioxide Uptake by Japanese Deciduous Forest Trees: Implications for Ozone Mitigation Policies" Forests 11, no. 2: 137. https://doi.org/10.3390/f11020137

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