Can you summarize and explain the findings of this research in simpler words. What were the main conclusions about the role of nitrogen oxides and sulfur dioxide ?
In this study we combine tree ring-derived carbon isotope signatures with contemporary leaf physiological measurements to identify the trends and drivers of canopy-integrated iWUE of two mature broadleaf deciduous tree species since 1940 in the central Appalachian Mountains. We show moderate increases in iWUE of mature Quru and Litu over the past ca. 55 years, which is consistent with other studies examining the response of tree iWUE in the eastern United States (Belmecheri et al., 2021; Levesque et al., 2017; Mathias & Thomas, 2018; Maxwell et al., 2019; Thomas et al., 2013), as well as in other tree species globally (Adams et al., 2020; Frank et al., 2015; Guerrieri et al., 2019; Leonelli et al., 2012; Mathias & Thomas, 2021; Peñuelas et al., 2011). Importantly, we identify a ca. 43%–50% stimulation in Anet as the dominant mechanism driving increases in iWUE of both species across ca. 79%–86% of the 76-year chronology, particularly beyond ca. 1970 (Figure 4; Figure S3), adding to the evidence that gs may not always significantly decline as expected under iCO2 (Guerrieri et al., 2019; Mathias & Thomas, 2021). Moreover, we document differences in interspecific leaf gas exchange characteristics that likely resulted in a saturation in Quru iWUE, but a sustained increase in Litu iWUE in recent years (Figure 3). Finally, we highlight the relatively greater impact of air pollution (iCO2, NOx, and SO2) than climate in explaining changes in tree iWUE at our study locations in the mid-Atlantic region (Figure 6).
We found iCO2 was one of the most important factors in explaining increases in tree iWUE of Quru and Litu over the last seven decades (Figure 6), supporting previous studies using tree-ring chronologies (Belmecheri et al., 2021; Frank et al., 2015; Keller et al., 2017; Mathias & Thomas, 2021; Peñuelas et al., 2011; Saurer et al., 2004; Thomas et al., 2013) and consistent with leaf physiology theory (Frank et al., 2015; Lavergne et al., 2019). However, we found several environmental factors interacted with iCO2 to moderate the integrated response of iWUE in the two study species. For both Quru and Litu, we found increasing NOx stimulated iWUE, but to a greater extent at low [CO2] (Figure S4), likely through increased N deposition resulting in higher plant available N stimulating Anet (Gharun et al., 2021; Jennings et al., 2016; Leonardi et al., 2012). We additionally found iCO2 stimulated Quru iWUE less when it was warm (Figure S4; Table S5), pointing to the interactive effects between atmospheric pollutants and climate on tree physiology (Zuidema et al., 2020), but also suggesting leaf respiration may increase proportionally more than photosynthesis. This may lead to Quru trees at relatively cooler, higher latitudes experiencing larger increases in future iWUE as CO2 continues to rise. We highlight positive interactions between VPD and SO2 and NOx, in turn, on Quru and Litu iWUE. While increasing VPD led to increasing iWUE in both species, likely through reductions in gs (Grossiord et al., 2020; Novick et al., 2016), this effect is likely compounded by SO2 on Quru (Choi et al., 2014; Mathias & Thomas, 2018; Ooi et al., 2018), whereas NOx likely stimulated Anet in Litu (Jennings et al., 2016; Leonardi et al., 2012; Mathias & Thomas, 2018). While we found growing season precipitation to have no impact on the interannual variability of iWUE for either species at our study locations, mean growing season precipitation increased by ca. 6% in the 45 years following 1970 relative to the previous 31 years and may help to explain the saturation of Quru iWUE. Indeed, this physiological response has been recently observed in eastern hemlock (Tsuga canadensis, Tsca) trees in the northeastern United States (Belmecheri et al., 2021), and at broader scales globally (Guerrieri et al., 2019; Levesque et al., 2017; Mathias & Thomas, 2021). Thus, while our study shows increasing CO2 is a strong driver of increased water use efficiency in trees, it is clear this is context dependent, and modulated by other environmental factors.
Evidence for a spectrum of physiological behavior and responses at the leaf and tree level have been observed across a range of environmental drivers (Ainsworth & Rogers, 2007; Belmecheri et al., 2021; Brzostek et al., 2014; Horn et al., 2018; Lin et al., 2015; Mathias & Thomas, 2021; Saurer et al., 2004; Thomas et al., 2010). Our results here indicate divergent leaf gas exchange strategies in Quru and Litu beginning near the mid-to-late-20th century, despite both species showing strong, active stomatal closure (i.e., constant Ci) during the initial study period (Figure 3). While Quru trees exhibited patterns consistent with a more passive stomatal response (i.e., more anisohydric, constant Ca-Ci) beyond 1970, Litu trees exhibited patterns consistent with moderate stomatal closure (i.e., more isohydric, constant Ci:Ca) during the majority of the examined chronology beyond 1957 (Figure 3). The remarkable similarity in iWUE between Quru trees in the central Appalachian Mountains documented here and Tsca trees in the northeastern United States presented in Belmecheri et al. (2021) (Pearson’s R = .86, p < .001 for 1940–2012) provides evidence for a broader physiological phenomenon across unique plant functional types, but also lends support for a range physiological control under in tree species experiencing similar environmental conditions (Bryant et al., 2022; Brzostek et al., 2014; Roman et al., 2015), indicating the importance of species-level responses to environmental change.
Our analysis of changes in modeled Anet and gs reveals that enhanced Anet overwhelmed reductions in gs in driving Quru and Litu iWUE throughout the majority of the last seven decades (Figures 4 and 5; Figure S3; Table S4). In fact, cases where reduced gs contributed to increasing iWUE occurred almost exclusively before ca 1970 (Figure S3) when mean precipitation was lower (Figure S5). Importantly, our findings are robust against changes in the nature the leaf A-Ci response to iCO2 (Figure S6). While iCO2 independently increases Anet and decreases gs, thereby stimulating iWUE (Ainsworth & Long, 2004; Ainsworth & Rogers, 2007), local site conditions are known to modify this response (Belmecheri et al., 2021; Fernández-de-Uña et al., 2016). Indeed, observations of increasing water availability have been linked to similar patterns in gs in trees throughout North America despite simultaneous increases in iWUE (Guerrieri et al., 2019; Levesque et al., 2017), again underscoring the importance of relatively greater increases in stimulated Anet. The lack of a strong reduction in gs over time for Quru and Litu trees in our study is in agreement with recent analyses using a dual carbon–oxygen stable isotope technique from trees around the globe (Guerrieri et al., 2019; Mathias & Thomas, 2021), despite suggested caveats using the dual isotope method (Guerrieri et al., 2022; Lin et al., 2022), and is likely a product of generally mesic conditions at our study locations. Finally, our findings of increasing Anet stimulating iWUE are consistent with observations of increasing carbon uptake globally (Campbell et al., 2017; Cernusak et al., 2019; Haverd et al., 2020), and highlight the nuanced, context-dependent response of leaf physiology to environmental change.
A careful consideration of the complexity behind annual tree growth and physiology is required to attribute the role of any given environmental factor on long-term trends in tree iWUE. While we highlight some of the environmental drivers and their interactions that affect iWUE in this study, there are factors such as competition (González de Andrés et al., 2018), potential legacy effects of SO2 and NOx (Likens et al., 1996), and light environment (Vadeboncoeur et al., 2020) that we are unable to consider and may contribute some uncertainty to our analysis. Moreover, while iWUE increases with tree height (McDowell et al., 2011), light environment can exert stronger controls over iWUE (Vadeboncoeur et al., 2020), complicating this response. Nevertheless, our study using mature, canopy-dominant trees contextualizes the response of Quru and Litu tree iWUE to changes in multiple environmental factors and is in direct agreement with assessments from regional (Mathias & Thomas, 2018) and global analyses (Belmecheri et al., 2021; Frank et al., 2015; Guerrieri et al., 2019; Mathias & Thomas, 2021).
The extent to which tree iWUE will continue to increase remains an open question. Our study clearly highlights the importance of local environmental factors beyond climate, many of which interact (Figure S4; Table S5), that have large influences over iWUE (Figure 6). Indeed, there is growing evidence for stimulated Anet persisting under iCO2 (Ainsworth & Long, 2004; Ainsworth & Rogers, 2007; Gardner et al., 2021; Springer et al., 2005) which would be reflected in iWUE, so long as nutrient demand is met (Luo et al., 2004) and temperature increases are moderate (Zuidema et al., 2020). However, our data from Quru and Litu trees in the eastern United States also pinpoint the impact of acidic air pollution (i.e., SO2) on leaf physiology. For example, it is likely the increase in gs observed at some sites in recent years (Figure 4; Figure S3) is linked to reductions in SO2 emissions (Borer et al., 2005; Ooi et al., 2018), which reinforces the importance of air quality on forest function (Engel et al., 2016; Mathias & Thomas, 2018). Future work will need to continue to directly assess the underlying mechanisms impacted by air pollution outlined here. Last, although we did not find precipitation to impact interannual variability of iWUE in our study, it is clear changes in water availability impacts tree iWUE—potentially saturating Quru iWUE—and should not be overlooked (Belmecheri et al., 2021; Levesque et al., 2017).
Accurately resolving the contribution of concurrently changing environmental factors on tree physiology is not trivial. While in this study we document moderate increases in the iWUE of Quercus rubra and Liriodendron tulipifera trees located in the central Appalachian Mountains, how other forest ecosystems will respond to future climate change still requires attention. Indeed, we found iCO2 to be an important factor in the proximate increases in iWUE for both species, but there is evidence for an attenuation of this response (Adams et al., 2020). Moreover, it has become clear considering the impact of air pollutants (i.e., NOx, SO2) is important in the interpretation of tree iWUE, especially over decadal to century time scales (Gharun et al., 2021; Jennings et al., 2016; Leonardi et al., 2012; Mathias & Thomas, 2018), and must be taken into account moving forward, particularly in highly industrialized areas. The interactions among environmental factors on leaf physiology uncovered here reinforce previous work at larger scales across a range of tree species and site environmental conditions (Fernández-Martínez et al., 2017). While it is clear the water cost of carbon uptake has declined over the last few decades, and in our study locations primarily due to increasing Anet, the extent to which these findings are observed more broadly is critical to resolve as changes in climate and atmospheric composition continue to accelerate.