TY - JOUR
AU - Li,, Xiaoqin
AB - Abstract Tree-ring δ13C and δ18O of dominant Dahurian larch and Mongolia pine in the permafrost region of the northern Great Higgnan Mountains, China were used to elucidate species-specific ecophysiological responses to warming temperatures and increasing CO2 over the past century. Larch and pine stable carbon discrimination (Δ13C) 13C and δ18O in tree rings both showed synchronous changes during the investigated period (1901–2010), but with species-specific isotopic responses to atmospheric enriched CO2 and warming. Tree-ring Δ13C and δ18O were controlled by both maximum temperature and moisture conditions (precipitation, relative humidity and vapor pressure deficit), but with different growth periods (Δ13C in June–July and δ18O in July–August, respectively). In addition, stable isotopes of larch showed relatively greater sensitivity to moisture deficits than pine. Climatic conditions from 1920 to 1960 strongly and coherently regulated tree-ring Δ13C and δ18O through stomatal conductance. However, climatic-sensitivities of tree-ring Δ13C and δ18O recently diverged, implying substantial adjustments of stomatal conductance, photosynthetic rate and altered water sources over recent decades, which reveal the varied impacts of each factor on tree-ring Δ13C and δ18O over time. Based on expected changes in leaf gas-exchange, we isolated the impacts of atmospheric CO2 and climate change on intrinsic water-use efficiency (iWUE) over the past century. Higher intracellular CO2 in pine than larch from 1960 onwards suggests this species may be more resilient to severe droughts in the future. Our data also illustrated no weakening of the iWUE response to increasing CO2 in trees from this permafrost region. The overall pattern of CO2 enrichment and climate impacts on iWUE of pine and larch were similar, but warming increased iWUE of larch to a greater extent than that of pine over recent two decades. Taken together, our findings highlight the importance of considering how leaf gas-exchange responses to atmospheric CO2 concentration influence species-specific responses to climate and the alteration of the hydrological environment in forests growing in regions historically dominated by permafrost that will be changing rapidly in response to future warming and increased CO2. Introduction Forests play an important role in regulating terrestrial carbon fluxes and in determining the rate of increase in atmospheric carbon dioxide concentrations [CO2] (Keenan et al. 2016). Plants assimilate CO2 through photosynthesis, so characterizing their responses to [CO2] as well as potential interactions with climate warming and other factors will be critical for predicting the consequences of global change on forests (Cao et al. 2010, Gimeno et al. 2015, Girardin et al. 2016, Becklin et al. 2017). Boreal forests represent massive terrestrial carbon stocks and fluxes that are ostensibly vulnerable to warming due to amplified rates of temperature change at higher elevations and latitudes. Therefore, these sensitive ecosystems need both intensive and extensive monitoring to reveal how different species and ecological settings within boreal forests have been impacted by the unprecedented modern rates of warming and increasing [CO2] (Trahan and Schubert 2015, Girardin et al. 2016) and to fully understand the impacts of permafrost thaw on forest growth dynamics. Moreover, some tree species in boreal forest ecosystems may be impacted in unpredictable ways by melting of permafrost soils and subsequent alterations of the hydrological environment (Rittenhouse and Rissman 2015, Saurer et al. 2016, Sidorova et al. 2016). Compared with the global temperature increase of about 0.12 °C per decade from 1951 to 2012 (IPCC 2013), the mean temperature in northeastern China’s permafrost and seasonally frozen regions increased by 0.35 °C per decade from 1961 to 2012 (Wang et al. 2013), which represents a prime example of rapid climate change (Sun et al. 2006). In northeastern China, forests account for about 30% of the national land area and stored nearly half of the national ecosystem carbon in 2010 (Zhang and Liang 2014). This remarkable climate change has likely had a profound impact on forest dynamics in this region during recent decades. Thus, understanding ecophysiological responses of forests (Gimeno et al. 2015, Kelly et al. 2016) to these remarkable rates of temperature increase and interactions with increasing [CO2] are of critical importance for improving our ability to predict future carbon and water cycle dynamics in boreal forests of northeastern China. Pairing tree-ring growth patterns with tree-ring stable carbon and oxygen isotopes (δ13C and δ18O) has the potential to reveal tree ecophysiological responses to environmental gradients as well as providing insights on how recent decades of increasing [CO2] and temperatures have impacted leaf gas-exchange and forest productivity (Scheidegger et al. 2000, Saurer et al. 2004, Sidorova et al. 2009, Battipaglia et al. 2013, Liu et al. 2014a, Frank et al. 2015, Zeng et al. 2017, Weigt et al. 2018). The stomata of plants tend to close under elevated [CO2], providing the primary mechanism for how recent increases in [CO2] have led to a higher intrinsic water-use efficiency (iWUE) (Franks et al. 2013). When stomatal limitation of photosynthesis rate (A) is strong, C3 plants exhibit a low intercellular CO2 concentration (Ci) and reduced carbon isotope discrimination, which results in improved iWUE (Saurer et al. 2004, Liu et al. 2014a). In tree rings, carbon isotope-based iWUE estimates reflect a growing season (photosynthesis-weighted) average that would be difficult to accurately assess even with an intense campaign of instantaneous leaf gas-exchange measurements. Under some situations, tree-ring δ18O can provide a separate constraint on whether variation in iWUE is caused by changes to A, stomatal conductance (gs) or some combination of both factors (Scheidegger et al. 2000). Previous investigations (Farquhar and Lloyd 1993, Cernusak et al. 2002, 2007) reported that the δ18O of plant tissue is inversely proportional to gs. In addition, tree-ring δ18O can be used to estimate the stomatal conductance from an empirical equation using the vapor pressure deficit (VPD) as a dependent variable (Managave 2014). For this framework to clearly determine which factors have modified iWUE, δ18O in tree rings are assumed to be a proxy for gs. Variation in gs can influence the δ18O of leaf water and derived photosynthate through: (i) evaporative cooling of the leaf; (ii) the diffusive resistance of water vapor; and (iii) the resulting plant transpiration-driven advection of unenriched xylem water into leaves being balanced by an opposite diffusive gradient in H218O enrichment between substomatal chambers and leaf veins described by the Péclet effect (Barbour et al. 2004). Hence, when gs decreases under elevated CO2 and photosynthetic CO2 demand is unchanged, ratio of the CO2 concentrations in the intercellular of leaves and in the atmosphere (Ci/Ca) should decrease while the δ18O signature in leaf water, would imprint upon tree rings (Roden et al. 2000). Therefore the combined analyses of tree-ring δ13C and δ18O have the potential to estimate the relative contribution of how modulations to gs or A contribute to the variations of iWUE (Scheidegger et al. 2000, Brooks and Coulombe 2009, Battipaglia et al. 2013). Recently, Roden and Siegwolf (2012) have argued that there are limitations to the conceptual dual-isotope approach. They pointed out that there were many interacting factors that influence both δ13C and δ18O, and environmental inputs can vary widely, making quantitative interpretations problematic where various pitfalls could lead to an over-interpretation of results. Because of the benefits of the dual-isotope approach (Scheidegger et al. 2000), isotopic measurements in tree rings can be used to gain insights about the physiological response of trees, especially in the stomatal behavior and water-use efficiency to ongoing and past environmental changes (Liu et al. 2014a, Sarris et al. 2013, Weigt et al. 2018). Over the past century, combined with global warming, the increased atmospheric [CO2] has impacted plant sensitivity to temperature, water balance and phenology through ecophysiological strategies, either increased iWUE or Ci in arid or wet environments (Becklin et al. 2017, Drake et al. 2017, Feichtinger et al. 2017). Yet, little information is available about long-term species-specific gas-exchange responses to rising Ca and increasing water demand in the northern Great Higgnan Mountains, where profound warming and drought periods have reduced frozen soils and total area of boreal forests (Tan and Li 1995, Bao et al. 2014, Chen et al. 2013). The objectives of this study were to quantify tree-ring δ13C and δ18O in two species from northeastern China (Dahurian larch and Mongolia pine, hereafter larch and pine) to provide insights on species-specific ecophysiological responses to rising [CO2] and temperatures and associated changes to permafrost conditions. Specifically, the following questions were addressed. (i) Are there differences in environmental factors affecting the δ13C and δ18O in tree rings of larch and pine in a permafrost region? (ii) Do the species-specific ecophysiological responses of larch and pine differ with respect to warming and CO2 enrichment over the past century? (iii) What is the relative contribution of climate vs rising [CO2] to trends in iWUE in northeastern China since the sharp increase in [CO2] in the 1960s and the subsequent increase in temperature? Our demonstration of a differential contribution of increased atmospheric water demand and rising [CO2] to increases in iWUE over recent decades highlights that a mechanistic understanding of carbon and water cycling responses to climate change in boreal forests will require species-specific approaches, particularly in fast-changing permafrost regions. Methods and materials Study area and site information The Greater Higgnan Mountains (Figure 1) lie in a region characterized by a semi-humid continental monsoon climate in northeastern China (Liu et al. 2013). Dry and cold air masses enter the study area in winter, changing to wet and warm air masses in summer, leading to distinct cold/dry and warm/wet seasons. The mean monthly total precipitation from June to August accounted for 67.0% (see Figure S1 available as Supplementary Data at Tree Physiology Online) of the mean annual precipitation (473.5 mm), which ranged from 324.4 mm in 1986 to an extreme of 764.4 mm in 2013 (Zhang et al. 2018). The coldest site in China is located in the study region, with an extreme low temperature record of −58.0 °C set in winter of 2016. The annual mean temperature was −3.9 °C, with monthly mean temperatures ranging from 17.3 °C in July to −28.1 °C in January (see Figure S1 available as Supplementary Data at Tree Physiology Online). The monthly relative humidity ranges from 55% to 83%, which generally peaks in August and is lowest in spring and fall. In contrast to relative humidity, the standardized precipitation evapotranspiration index (SPEI) tends to highest in spring and fall. Figure 1. View largeDownload slide The study region, sampling sites and the nearby meteorological stations with observed climatic data. The spatial patterns of temperature (color background) and precipitation (black contour line) in June–August of the period 1957–2010 over the region were also shown. Figure 1. View largeDownload slide The study region, sampling sites and the nearby meteorological stations with observed climatic data. The spatial patterns of temperature (color background) and precipitation (black contour line) in June–August of the period 1957–2010 over the region were also shown. The Xing’an-Baikal permafrost is the second-largest expanse of permafrost in China, and represents high-latitude permafrost because it occurs at latitudes greater than 47°N. The permafrost in the study area was mainly continuous (Jin et al. 2000, Wei et al. 2011). The snow cover period of the region lasts from late September to early May, whereas the growing season can be generalized as the snow-free season from May to September (Xu 1998). In response to warming temperatures from 1960 to 2010, the depth to the permafrost has decreased steadily, at a rate of about 65 cm per decade, corresponding to depths of 0.5 m in 1983 and 1.8 m in 2004 at the Yitulihe meteorological station. In total, the permafrost area has retreated northward by at least 50–150 km across this region (Jin et al. 2007). The dominant tree species in the Greater Higgnan Mountains are larch and pine, which are adapted to permafrost conditions where frozen soils can limit tree growth. The main soils are acidic or subacidic luvisols, sometimes with a thin surface layer of mineral soil and wind-blown sandy soil. Pine and larch forests are always mixed with smaller components of Picea jezoensis, Pinus koraiensis, and Abies nephrolepis. Shrubs include Rosa davurica, Rhododendron dauricum, Vaccinium vitis-idaea, Spiraea salicifolia and Ledum palustre. The herb community is dominated by drought-tolerant species such as Lathyrus humilis, Calamagrostis turczaninowii and Vicia cracca (Wang and Song 2011). Tree-ring analysis We obtained a total of 226 tree-ring cores (two cores per tree) at breast height using 12-mm-diameter increment borers in 2013 (Figure 1). We sampled 132 larches (51 from the L1 site, 40 from the L2 site and 41 from the L3 site) and 94 pines (46 from the P1 site and 48 from the P2 site) that were apparently healthy and recently undisturbed by human activities. We measured tree-ring widths using a LINTAB 6 measuring system with a resolution of 0.01 mm. COFECHA software was used to check visual cross-dating and ARSTAN software was used to standardize, detrend and compile tree-ring chronologies by site and species (Cook and Krusic 2014). The length of the ring-width chronologies at the five sampled sites ranged from 224 years (L3 site) to 348 years (P2 site). After the measurement of ring widths, we found strong coherence in inter-annual variation in tree growth of each tree species from different sites. Tree-ring width data were pooled by species and site to construct the regional tree-ring width chronologies. The mean sensitivity of larch ring-width chronologies was higher than 0.26 whereas that of pine chronologies was lower, but still above 0.20 (Zhang et al. 2018). Inter-series correlations (RBAR) among the regional larch and pine ring-width chronologies were 0.59 (P < 0.001, period from 1783 to 2013) and 0.56 (P < 0.001, period from 1683 to 2013), respectively. Regional coherence in ring-width variability suggests the common environmental factors affected tree growth in both species. Based on data common to all periods and sites, we established regional ring-width chronologies from 1800 to 2010 for Dahurian larch and Mongolian pine (Zhang et al. 2018). Here, we present these ring-width data, but focus on variation in δ13C and δ18O of the same trees during the 20th century, when the climatic data from meteorological stations and Climatic Research Unit (CRU) are available. The δ13C and δ18O analyses Five cores from five trees showing the highest correlation with the species-specific tree-ring chronology were selected for isotopic analysis. Detailed information about the selection of the cores for isotopic analyses can be found in Liu et al. (2017) and Zhang et al. (2018). The annual rings of five cores were pooled by year, and the wood materials were ground with a centrifugal mill to ensure homogeneity and efficiency of α-cellulose extraction. Cellulose was extracted with the methods from Leavitt and Danzer (1993) with some modifications for the pooled samples. After purification of cellulose, following the method of Laumer et al. (2009), homogenization of cellulose was performed again using an ultrasonic machine (JY92–2D, http://www.scientzbio.com/). The α-cellulose was then freeze-dried for 72 h using a vacuum freeze dryer prior to the isotope analysis. The δ13C values were determined by an element analyzer (Flash EA 1112; Bremen, Germany) coupled with an isotope-ratio mass spectrometer (Delta-plus, Thermo Electron Corporation, Bremen, Germany) at the Key Laboratory of Western China’s Environmental Systems, Lanzhou University. The oxygen isotope composition of aliquots of the same α-cellulose was determined at the State Key Laboratory of Cryospheric Sciences, Northwest Institute of Eco-Environment and Resources, Chinese Academy Sciences, Lanzhou, China, respectively, by continuous-flow isotope ratio mass spectrometry (Finnigan MAT-253, Bremen, Germany) (Liu et al. 2017). The analytical errors (standard deviations) of the isotope measurements were less than 0.05‰ and 0.3‰ for δ13C and δ18O, respectively. Calibration was done by measurement of International Atomic Energy Agency (IAEA) USGS-24 (Graphite) and by measurement of IAEA - CH3 (cellulose). All δ13C and δ18O values are expressed relative to their respective standard (Vienna Pee Dee Belemnite for carbon isotopes and Vienna Standard Mean Ocean Water for oxygen isotopes). Measured tree-ring δ13C of both species displayed a strong decline from 1950 onwards due to the combustion of fossil fuels on atmospheric 13CO2 concentrations (see Figure S2 available as Supplementary Data at Tree Physiology Online). To remove the fossil-fuel derived impact on tree-ring δ13C we calculated the carbon discrimination (Δ13C) of cellulose following Farquhar et al. (1982): ΔC13=δCair13−δCplant131+δCplant13 (1) where δ13Cair was determined by the estimates of McCarroll and Loader (2004) merged with measurements made at the Mauna Loa observatory (http://cdiac.ornl.gov/trends/co2/sio-mlo.html). Cellulose Δ13C values are then converted to Ci/Ca ratios using the following (Farquhar et al. 1989): ΔC13=a+(b−a)*(Ci/Ca) (2) where a is fractionation resulting from diffusion (4.4‰), and b is the fractionation associated with carboxylation by Rubisco (27.0‰). Note that Δ13C should be directly related to [CO2] in chloroplasts rather that Ci. As a result, using Ci may create complications if variability in mesophyll conductance, and its potential for limiting A is not small compared with the impact of stomatal closure on Ci (Seibt et al. 2008). For simplicity of interpretations of tree-ring isotope data, we here consider canopy-integrated variation in mesophyll conductance to have been negligible, such that iWUE can be estimated from Ci and Ca as follows (Ehleringer et al. 1993): iWUE=A/gs=(Ca−Ci)/1.6 (3) where 1.6 is the ratio of diffusivities of water and CO2 in air. Climate data We obtained meteorological data for our study area from the China National Meteorological Information Center (http://eng.weather.gov.cn/) from 1957 to 2013. We calculated the SPEI to represent the severity of drought using the procedure of Vicente-Serrano et al. (2010). To obtain a better representation of climate conditions throughout the study area, we averaged observation data from three local meteorological stations nearby the sampling sites (Figure 1 and see Table S1 available as Supplementary Data at Tree Physiology Online). To describe regional climate change trends, we used the linear regression of mean monthly temperature, mean monthly maximum temperature, mean monthly minimum temperature, monthly total precipitation, mean monthly relative humidity and mean monthly SPEI from 1957 to 2013 (Figure 2). We also obtained regional climatic data from the nearest four CRU (Climate Research Unit, UK) grid points from the KNMI climate Explorer (Trouet and Van Oldenborgh 2013) and averaged these data to assess isotope dendroclimatic responses before 1957, when local meteorological data became unavailable (see Figure S3 available as Supplementary Data at Tree Physiology Online). Our previous research has shown that the local meteorological data corresponded strongly with nearby CRU grid-cells data (Liu et al. 2017). Figure 2. View largeDownload slide Temporal variations of mean temperature (a), mean maximum temperature (b), mean minimum temperature (c), total precipitation (d), relative humidity (e), SPEI (f) and VPD (g) in summer (June–August). The climatic data were obtained from the nearby three meteorological stations, which are shown in Figure 1. The regression trends and functions of each climatic variable in 1957–2010 were also provided. Figure 2. View largeDownload slide Temporal variations of mean temperature (a), mean maximum temperature (b), mean minimum temperature (c), total precipitation (d), relative humidity (e), SPEI (f) and VPD (g) in summer (June–August). The climatic data were obtained from the nearby three meteorological stations, which are shown in Figure 1. The regression trends and functions of each climatic variable in 1957–2010 were also provided. Data analysis Temporal trends in climate variables (i.e., temperature, precipitation, relative humidity, etc.) were tested using least-square linear regression. Pearson’s correlation coefficients were calculated between tree-ring isotopes and monthly climatic parameters from October of previous year to September of current year for the period from 1957 to 2010. To confirm the influence of the climatic parameters on tree-ring isotopes at different frequencies, we calculated correlations between isotopes and the climatic variables for both annual values and the first-order differences (i.e., the value of the previous year isotopic value subtracted from the current year isotopic value). The temporal coherence of variability between two isotopic signals and the climatic responses of larch and pine over time were visualized with 21-year moving correlations. For both species, the expected contributions of increasing [CO2] to changes in iWUE were calculated following predictions from a global meta-analysis of CO2-effects on leaf gas-exchange inferred from carbon isotope records (Voelker et al. 2016). The trends reported by Voelker et al. (2016) showed that woody plants tend to regulate leaf gas-exchange toward minimizing water loss per unit C gain at low Ca (i.e., low Ci/Ca and Ca − Ci) and an enhanced avoidance of drought stress at high Ca (i.e., high Ci/Ca and Ca − Ci). More specifically, we used the following relationship for the expected total change in Ci/Ca from the full glacial Ca minima of 190 ppm (i.e., ΔCi/Ca) as: ΔCi/Ca=−0.3974+0.5163×(1–e(−0.0067*Ca)) (4) For each annual value of Ci/Ca estimated from tree-ring Δ13C obtained by rearranging Eq. (2), we subtracted the corresponding first-order difference from the predicted ΔCi/Ca from Eq. (4) to arrive at variability in Ci/Ca that does not include the expected effect of increasing Ca on leaf gas-exchange. Thereafter, Eq. (3) was again employed to convert these annually adjusted Ci/Ca values to iWUE without the effects of changing [CO2]. Results Regional climate change Mean, maximum and minimum temperatures in summer (June–August) during 1957–2010 reveal marked warming trends (Figure 2a–c). Minimum temperatures increased at 0.62 °C per decade over this period, which was a faster rate of change compared with mean or maximum temperatures. Precipitation exhibited no significant trend, but did increase slightly by 4.18 mm per decade (Figure 2d). Relative humidity declined significantly, with the lowest value (67.0%) in 2007 (Figure 2e). Standardized precipitation evapotranspiration index showed a similar pattern to relative humidity but the trend was not significant (Figure 2f). However, trends in VPD increased significantly (Figure 2g). Overall, these trends document that the summer regional climate has become warmer, without increases in precipitation that can fully offset increased evaporative demand. Gridded regional data that extend over the past century largely corroborate local meteorological records since the 1950s, which notably display a previous period of warm temperatures but relatively little variation in precipitation around the 1940s (see Figure S3 available as Supplementary Data at Tree Physiology Online). Long-term changes in Δ13C and δ18O Both tree-ring Δ13C chronologies show remarkably similar variation and trends apart from a disparity centered near 1960 (Figure 3a). However, changes in Δ13C between two tree species seems to be related more to low-frequency variation (e.g., decadal scale) although significant correlations existed among inter-annual variation in each record. There was no significant difference in mean δ13C values between pine (mean and standard deviation: −22.79 ± 0.70‰) and larch (mean and standard deviation: −22.75 ± 0.63‰) across the last century. Both species displayed a similar declining trend in Δ13C over recent decades, although larch had mean lower Δ13C values than that of pine by 0.38‰ over the past 20 years, yielding some initial indication that this species may have been more sensitive to recent warming. For tree-ring δ18O, pine was significantly enriched by about 1.73‰ compared with larch across the entire study period (Figure 3b). However, this offset has apparently diminished since AD 2000. In both species, tree-ring δ18O showed stronger coherence in inter-annual variability compared with tree-ring Δ13C (Figure 3a and b). For larch, tree-ring Δ13C and δ18O seemed to change synchronously, although with less agreement over the period 1970–1990 followed by increased coherence thereafter up to 2010 (Figure 3c). Before 1960, variation in both isotopes in pine were also coherent, however, variation in Δ13C and δ18O diverged strongly during 1970–1990 (Figure 3d), suggesting that driving factors of Δ13C and δ18O changed after about 1970. Figure 3. View largeDownload slide Comparisons and correlations of Δ13C and δ18O of larch and pine during the period of 1900–2010. (a) Δ13C of larch and pine; (b) δ18O of larch and pine; (c) larch Δ13C and δ18O; (d) pine Δ13C and δ18O. The 21-year window moving correlations of both isotopes of larch and pine are provided in (a) to (d), respectively. The dashed lines represented the confidence of P = 0.05. The linear functions in (a) to (d) represent the relationships of two isotopes. Figure 3. View largeDownload slide Comparisons and correlations of Δ13C and δ18O of larch and pine during the period of 1900–2010. (a) Δ13C of larch and pine; (b) δ18O of larch and pine; (c) larch Δ13C and δ18O; (d) pine Δ13C and δ18O. The 21-year window moving correlations of both isotopes of larch and pine are provided in (a) to (d), respectively. The dashed lines represented the confidence of P = 0.05. The linear functions in (a) to (d) represent the relationships of two isotopes. Correlations between Δ13C and δ18O of two tree species Over the 20th century, there were no constant relationships in the same isotope chronologies among species, nor among different isotope chronologies within a single species. Moving window correlations between tree-ring Δ13C of larch and pine, remained positive and significant over the past century except for the short epoch of 1950–70 (Figure 3a). In contrast, moving correlations between tree-ring δ18O of larch and pine displayed strong significant correlations up to 1980 followed by a substantial decline in signal coherences that is driven primarily by differences among species during the period from about 1990–2000 (Figure 3b). For larch (Figure 3c), correlations between Δ13C and δ18O were significant across the entire study period and appeared to be weakest near 1970. In pine (Figure 3d), however, correlations between Δ13C and δ18O were significant before 1960, and then the correlation became weak or even in the opposite direction. In general, the relationship between isotope chronologies was generally stronger for larch compared with pine. Climatic responses To clarify the climatic controls at different time frequencies, Pearson’s correlation analyses were conducted between climate data and isotope chronologies using raw isotope data as well as first-order differences (FOD) variations. Temperatures and moisture conditions in June to August had a significant influence on tree-ring Δ13C and δ18O in both larch and pine (Figure 4). Overall, climatic response patterns revealed that climate earlier in the summer (June–July) was more important for tree-ring Δ13C, compared with climate variation of later summer (July–August) for tree-ring δ18O. Figure 4. View largeDownload slide Climatic responses of tree-ring Δ13C and δ18O of larch and pine. Yearly and FOD represent the annual and first-order difference variations, respectively. The significant correlations have been shown in red (positive) and blue (negative) circles with differing size. Figure 4. View largeDownload slide Climatic responses of tree-ring Δ13C and δ18O of larch and pine. Yearly and FOD represent the annual and first-order difference variations, respectively. The significant correlations have been shown in red (positive) and blue (negative) circles with differing size. We found a stronger influence on both temperature- and moisture-related variables for July–September on Δ13C of larch compared with pine. Variation in FOD isotope chronologies resulted in weakened responses to inter-annual variation in climate for larch. However, FOD Δ13C chronologies showed increased sensitivity to inter-annual variation in temperature and moisture for pine (Figure 4). These results suggest that tree-ring Δ13C of pine was more sensitive to high-frequency, inter-annual variation in temperature and moisture conditions compared with that of larch. Larch δ18O correlated more strongly with moisture conditions in July–August (relative humidity and VPD) than pine δ18O at the yearly variations (Figure 4). Mean maximum temperatures in July–August also impacted the tree-ring δ18O of both tree species positively. In both species, FOD δ18O chronologies displayed a weaker influence of temperature whereas the influence of moisture remained the same compared with the raw chronologies (Figure 4). Climate–isotopes relationships over the past century To help visualize how climatic impacts on tree-ring Δ13C and δ18O of larch and pine have changed over time, we calculated 21-year moving correlations between observed meteorological data from 1957 to 2010 and CRU gridded data from 1900 to 2010 with tree-ring isotope chronologies (Figure 5 and see Figure S4 available as Supplementary Data at Tree Physiology Online). To facilitate more intuitive comparisons among isotope responses, the signal direction of moving correlations for Δ13C vs meteorological variables was reversed. We found the most significantly negative correlations between maximum temperatures and Δ13C in tree rings of both tree species since 1900 onward, with increases in correlation values over recent decades. Correlations between δ18O and mean or maximum temperatures also increased over recent decades, but were weaker overall compared with Δ13C signals. It is also notable that the minimum temperatures appear to have had strong positive influences on larch Δ13C before 1990. Correlations between both isotopic values and moisture-related variables reinforce that increasing temperatures since 1970 have driven greater climatic control over stable isotope signals (Figure 5d–g), suggesting the recent emergence of water stress and greater control by stomatal conductance on leaf gas-exchange. Apart from these overall trends, tree-ring Δ13C was more sensitive to water stress than δ18O across most of the study period for both species. Figure 5. View largeDownload slide The 21-year window moving correlations of tree-ring Δ13C and δ18O with climatic variables in June–August during the meteorological observation period of 1957–2010. The values outside of the shaded areas represent the significance at 95% confidence level. The signal direction of Δ13C was multiplied by −1 to facilitate the comparison with the climatic-signal strength of δ18O in tree rings. RH, relative humidity. Figure 5. View largeDownload slide The 21-year window moving correlations of tree-ring Δ13C and δ18O with climatic variables in June–August during the meteorological observation period of 1957–2010. The values outside of the shaded areas represent the significance at 95% confidence level. The signal direction of Δ13C was multiplied by −1 to facilitate the comparison with the climatic-signal strength of δ18O in tree rings. RH, relative humidity. During the past century, maximum temperature clearly drove isotopic discrimination more than minimum or mean temperatures. There were two periods (1920–1960 and 1980–2010) with significantly positive correlations between maximum temperature and tree-ring Δ13C and δ18O (see Figure S4 available as Supplementary Data at Tree Physiology Online). The sensitivity of tree-ring Δ13C and δ18O to maximum temperatures during the period 1920–1960 were very similar. However, during recent decades the temperature dependence of Δ13C increased much more dramatically compared with δ18O. A similar pattern emerged from correlations between isotope chronologies and precipitation, whereby correlations for both isotopes were generally strong during 1920–1960, followed by a moderate decline and subsequent rebound in isotopic sensitivity that was stronger for Δ13C compared with δ18O (see Figure S4 available as Supplementary Data at Tree Physiology Online). Again, the correlations between Δ13C and precipitation were stronger compared with tree-ring δ18O. For both isotopes correlations with VPD (positive responses) and SPEI (negative responses) generally followed the same temporal patterns as maximum temperatures and precipitation, respectively. Long-term changes of iWUE and the contribution of climate and CO2 We evaluated changes in iWUE of larch and pine in response to increasing atmospheric CO2 concentration and climatic changes using the relationships presented in Eqs (3) and (4). The Ci/Ca of both species increased at about the rate predicted by Eq. (4) up through about 1990 and decreased thereafter, reflecting the expected effects of increasing Ca on leaf gas-exchange until the past two decades, which corresponded to rapid warming in this region (Figure 2). Across the 20th century, both Ca and Ci increased, yielding gains in iWUE of 31.8% and 22.7% for larch and pine, respectively (see Figure S5 available as Supplementary Data at Tree Physiology Online). A combination of climate variability and rising [CO2], is estimated to have increased iWUE of larch and pine by only a few percent from 1900 to 1960. However, after 1960, iWUE increased dramatically (Figure 6a). To isolate the effect of climate change on iWUE, we removed the effects of changing [CO2] by calculating and removing the expected change in iWUE based on Eq. (4) (Figure 6a, after Voelker et al. 2016). This approach suggested that the change in iWUE attributed to variation in climate was modestly negative for both species over the period 1961–90. This contrasts with the combined effects of [CO2] and climate, which show modestly positive changes in iWUE (2.8% per decade for larch and 2.85% per decade for pine) over the same period (Figure 6a). For the most recent period 1990–2010, rapidly rising CO2 is estimated to have increased iWUE by about 4.5% per decade for both tree species. However, most of the dramatic increase in iWUE for both species, about 9.1% per decade and 6.5% per decade for larch and pine, respectively, can be attributed to warming temperatures and climate change since about 1990 (Figure 6b). Although there are differences among species, the overall trends indicate that enhanced water stress over the past two decades (Figure 2) has ostensibly caused about two-thirds of the increase in iWUE whereas the remainder can be attributed to rising CO2 (Figure 6). Figure 6. View largeDownload slide Percent change in iWUE (1901–10 as a reference period) for larch and pine since 1901–2010 (a). Solid lines in blue (larch) and red (pine) represent the percent change in iWUE in response to increasing CO2 concentration and changes in stomatal conductance resulting from climate change. Dashed lines in blue (larch) and red (pine) indicate the percent changes in iWUE in response to only changes in stomatal conductance resulting from climate change (no CO2 effects). The atmospheric CO2 concentration increased continuously but with clearly acceleration starting around 1960 (a). The iWUE was calculated for each tree-ring record using method from Voelker et al. (2016). Ca was held constant (296.7 ppm) at the year 1900 level for dashed lines. The reconstructed VPD in June–August (Liu et al. 2017) was provided to examine the impacts of climate to iWUE. (b) The estimation of contribution of CO2 and of climate to change rate in iWUE for larch and pine during the periods of 1961–90 and 1991–2010 with accelerated CO2 concentration. Figure 6. View largeDownload slide Percent change in iWUE (1901–10 as a reference period) for larch and pine since 1901–2010 (a). Solid lines in blue (larch) and red (pine) represent the percent change in iWUE in response to increasing CO2 concentration and changes in stomatal conductance resulting from climate change. Dashed lines in blue (larch) and red (pine) indicate the percent changes in iWUE in response to only changes in stomatal conductance resulting from climate change (no CO2 effects). The atmospheric CO2 concentration increased continuously but with clearly acceleration starting around 1960 (a). The iWUE was calculated for each tree-ring record using method from Voelker et al. (2016). Ca was held constant (296.7 ppm) at the year 1900 level for dashed lines. The reconstructed VPD in June–August (Liu et al. 2017) was provided to examine the impacts of climate to iWUE. (b) The estimation of contribution of CO2 and of climate to change rate in iWUE for larch and pine during the periods of 1961–90 and 1991–2010 with accelerated CO2 concentration. Discussion Temporal changes in tree-ring δ13C and δ18O The past century was characterized mainly by climatic warming and increasing CO2 concentration (IPCC 2013). The 20th century seems to be the warmest century in China for the last millennia (Wang et al. 2001). In this study, the two conifer species differ in a number of life history characteristics and physiological traits that could potentially impact tree-ring isotopic responses to environmental variation during the past century. The most visible difference among species is that larch is deciduous whereas pine is an evergreen. Indeed, several lines of evidence have revealed the tree-ring carbon and oxygen isotope responses to environmental variation can have important differences among species (Liu et al. 2007, Sidorova et al. 2016, Feichtinger et al. 2017). Regardless of differences in species features, the similar trends and inter-annual variability displayed by tree-ring Δ13C of both species over the past century (Figure 3a), as indicated by significant correlation (R2 = 0.182, P < 0.001) over the investigated period, indicate important environmental factors control Δ13C in these species. The most common driver of high-frequency, inter-annual variation in Δ13C is moisture stress (Figure 4), which impacts stomatal closure through water supply (i.e., precipitation in previous weeks to months) and evaporative demand during the current growing season. Meanwhile, atmospheric [CO2] is predicted to contribute to low-frequency variation in Δ13C (Frank et al. 2015, Voelker et al. 2016). The relatively lower values of Δ13C around the 1940s and across the recent two decades correspond to periods of warming during both time periods in the Greater Higgnan Mountains (Figure 2 and see Figure S2 available as Supplementary Data at Tree Physiology Online). This trend is similar to other recent studies of boreal forests (Trahan and Schubert 2015), potentially revealing that warming has significantly impacted tree-ring Δ13C at other high-latitude locations. The period from 1950 to 1970 was characterized by weak or nearly opposite climate responses of Δ13C to meteorological variables (Figure 5). We attribute these responses to the lower temperatures of this period, which resulted in relatively low levels of moisture stress and stomatal control having been recorded in the tree-ring isotopes. The progressive increases in climate sensitivity of Δ13C for both tree species from 1980 to present (Figure 5) strongly implicate enhanced water stress causing stomatal closure to increasingly control carbon discrimination (Liu et al. 2017). This interpretation is further supported by observed warming and atmospheric drying over the same period in this region (Figure 2). The correlations of δ18O chronologies among the two species were much stronger compared with the Δ13C chronologies (Figure 3a and b), suggesting that collectively, the water source and leaf water enrichment contribution to cellulose δ18O between pine and larch was more consistent compared with environmental controls on Δ13C. Although agreement on inter-annual variation in δ18O among species is apparent, the strength of this relationship is also consistent with the strong spatial coherence in low-frequency tree-ring δ18O variation that is evident across much of the south-Asia monsoon region (Liu et al. 2014b), reflecting the predominance of synoptic atmospheric circulation patterns and their forcing over isotopic signals in precipitation and the potential advantage of tree-ring δ18O compared with Δ13C for regional climatic reconstructions from some locations. Recent multi-temporal scales isotope evidence also confirmed that tree-ring δ18O is more robust as climate proxy than δ13C, and that δ13C may be better suited to identifying physiological responses to the local environment (Zeng et al. 2017), which supports our results that tree-ring δ18O shares more consistent variability than that of δ13C in tree rings between species. The moving correlation functions permit the dynamics of climate control over isotopic variation to be addressed in detail over time. Tree-ring δ18O of both tree species displayed strong coherence before 1980. However, thereafter, the formerly high correlations among δ18O chronologies quickly declines below the level of significance (Figure 3b), indicating a recent shift in the drivers of oxygen isotope signals among the two tree species. As we know, tree-ring δ13C record the balance between stomatal conductance and photosynthetic rate, but δ18O in tree rings record the δ18O of source water and leaf transpiration (McCarroll and Loader 2004). This differing strength in correlations of tree-ring Δ13C and δ18O reveal the different contributions of stomatal conductance (gs), photosynthetic rate and δ18O of water source on isotopic enrichment. The alteration of stomatal conductance would bring similar influence on carbon and oxygen discrimination; however, changes in the photosynthetic rate and water source will alter the correlation strength. Given that the tree species we sampled were exposed to the same meteorological conditions, mechanistic models of leaf water enrichment and resulting cellulose isotopic signals suggest the only factors that can explain these abrupt differences are recent changes in water source isotopic signature and/or species-specific changes in stomatal conductance. Leaf water enrichment is actually relatively insensitive to stomatal conductance compared with source water variation or relative humidity (Voelker et al. 2014). Moreover, there is no reason to suspect that one species would be much more sensitive to warming considering both belong to the Pinaceae, in which anisohydric stomatal behavior is broadly conserved (Brodribb et al. 2014). These circumstances suggest that the lower correlations and the recent convergence in δ18O among species (Figure 3b) were patterns caused by differences in the isotopic signals of source water uptake. Indeed, the species display a long-term (negative) trend in δ18O is pine, which is opposite to the direction predicted by mechanistic models for a warming climate, assuming source water isotopic signals have been constant. In permafrost regions, the depth of the active soil layer is crucial for determining sub-surface hydrology, rooting space and tree growth (Throckmorton et al. 2016, Zhang et al. 2016). With the increasing thaw depth, more water melted from permafrost becomes available to trees. We have not yet studied soil water isotopic signals, but melted permafrost water can be safely assumed to have a depleted δ18O signature compared with recent monsoon precipitation. Seasonal variations of precipitation δ18O over the region reach to the amplitude of almost 20‰ (see Figure S6 available as Supplementary Data at Tree Physiology Online), which makes seasonal uptake of different water sources very critical. Greater incorporation of depleted permafrost water would help account for expected responses to warming that were either absent in the case of larch δ18O or opposite of that predicted for declining pine δ18O. This pattern is not without precedent. Recently, Saurer et al. (2016), in Siberia, reported an unexpected ‘inverse’ climate–isotope relationship, whereby dry and warmer summer conditions resulted in lower soil and root δ18O values. They also argued that this unexpected climatic–isotopic relationship was due to permafrost meltwater altering tree water source isotopic composition. Permafrost meltwater should ostensibly serve as a relatively important source for trees during drought years. As such, the mixture of recent precipitation and permafrost meltwater would shift the water source signal retained in tree-ring δ18O. From this perspective, specific-species rooting depth and structure of larch and pine has likely contributed to the recent changes in cellulose δ18O values among these species. In addition, pine is evergreen and larch is deciduous, which also could influence the earlywood δ18O values if there were corresponding differences in the degree of utilization of previously stored non-structural carbohydrates. Alternatively, differences in canopy albedo between the deciduous larch vs the evergreen pine may also contribute to local differences in soil warming and permafrost thaw, but additional data collection would be necessary to test the relative contributions of species-specific root morphology, utilization of stored carbon or differential permafrost melting. Strong relationships between Δ13C and δ18O indicate that variation in stomatal conductance and water stress-induced changes in the degree of stomatal limitation of net photosynthesis were the primary controls on δ13C and biomass production based on the stable isotopic discrimination model in tree rings (Roden et al. 2000, Scheidegger et al. 2000, Flanagan and Farquhar 2014). Where differences in these relationships exist among species, they can lead to insights on ecophysiological responses to climate change. Correlations in δ13C and δ18O for larch are stronger than that of pine (Figure 3c and d), indicating closer uniformity of driving factors on carbon and oxygen fractionation for larch than pine. The 21-year moving correlations revealed that variations of pine δ13C and δ18O were synchronous during the most part of the 21st century, with only weak relatedness in the period 1970–80 (Figure 3d), suggesting the stronger regulation of stomatal conductance on isotopic discrimination than photosynthetic rate or water sources (Scheidegger et al. 2000, Sidorova et al. 2009, Liu et al. 2014a). For pine, however, there was a significant shift in correlations between δ13C and δ18O in tree rings starting from 1960 onwards, which changed from significant negative to positive correlations (Figure 3d). This evident shift in pine implied the reduction of the impacts of stomatal conductance on both isotopes, and the variations of photosynthetic rate (Flanagan and Farquhar 2014) or the water source changes related to melting permafrost disturbed the carbon and oxygen isotopic discrimination (Roden et al. 2000). Over the past century, the summer VPD (see Figure S3 available as Supplementary Data at Tree Physiology Online; Liu et al. 2017) revealed the highest atmospheric water demand around 1920–30 and gradually increased VPD since 1960 to present. To a certain degree, enhanced atmospheric water demand should substantiality influence how the correlations are synchronized between δ13C and δ18O in tree rings (Weigt et al. 2018). The substantial shift in the correlations between δ13C and δ18O in tree rings indicate that caution is needed to detect possible biases in climate reconstruction when isotopic or other tree-ring signals are calibrated against meteorological data during a period of unprecedented warming that result in altered and unpredictable hydrological conditions. The contribution of the climate and CO2 to changes in iWUE The water-use efficiency of plants plays an important part in determining the water–energy balance between terrestrial ecosystems and the atmosphere (Frank et al. 2015, Keenan et al. 2016). Hence, quantifying how shifts in climate and/or [CO2] have modified iWUE will be critical for predicting how trees will respond to projected future conditions (Frank et al. 2015, Gimeno et al. 2015, Voelker et al. 2016). For much of the 20th century leaf gas-exchange, as indicated by trends in Ci/Ca as well as Ci, tracks predicted values from a global meta-analyses of [CO2] effects on leaf gas-exchange (see Figure S5a–c available as Supplementary Data at Tree Physiology Online, after Voelker et al. 2016). Clearly, much of this trend is driven by [CO2] stimulating enhanced photosynthetic accumulation (Gimeno et al. 2015). However, after 1990 both species display a prominent decline in Ci/Ca and an associated leveling off of Ci compared with that predicted (see Figure S5a and b available as Supplementary Data at Tree Physiology Online). The iWUE of both larch and pine also tracked predicted values during most of the 20th century, but accelerated faster than that predicted by [CO2] alone after 1990. Although both species show this overall trend, greater gains in iWUE for larch, particularly after 1990, are again indicative of how enhanced evaporative demand (Figure 2) has resulted in stronger stomatal constraints on leaf gas-exchange compared with pine. Pines have apparently been relatively buffered from drought stress (Kelly et al. 2016), presumably by being able to utilize more permafrost meltwater, as indicated by the declining trend in tree-ring δ18O, when meteorological variables suggest it should be increasing. Overall, there is no clear long-term change in iWUE of either species before 1960 and from 1960 to 1990, and the gains in iWUE were entirely attributable to the predicted effects of [CO2] due to a lack of significant change in VPD (Figure 6a). Thereafter, evaporative demand increased greatly from 1991 to 2010 (Figure 2), resulting in enhanced iWUE being mostly driven by climate, with a smaller but substantial impact of rising [CO2] concentration over this period (Figure 6b). When the contribution of all factors (CO2 enrichment, climate, and nutrients, etc.) on iWUE over the entire period were included, VPD had only a weak correlation with iWUE (P = 0.021) for larch, and no significant correlation for pine. However, after removing predicted CO2 effects on iWUE, VPD explained about 20.6% and 12.2% of the enhancement of iWUE for larch and pine, respectively (see Figure S7c and d available as Supplementary Data at Tree Physiology Online), suggesting that the higher sensitivity of larch to climate stress (Figure 6b) was likely more driven by ecophysiological responses to VPD on sites that are increasingly prone to drought stress. Although temperatures have traditionally limited tree radial growth in this cold environment, there is evidence that iWUE has interacted with temperature in determining tree growth for larch, but not for pine (Zhang et al. 2018). This line of evidence supports the view that among species, even small differences in iWUE that are attributable to climate (Figure 6b), as modified by permafrost meltwater utilization, can result in a significant divergence in ecophysiological function. We have compared the changes in tree growth and iWUE of larch and pine over the 20th century (see Figure S8 available as Supplementary Data at Tree Physiology Online). For larch, increased iWUE did not increase tree growth whether considering the impacts of CO2 and climate together or separately. However, there were several periods when tree growth and iWUE varied in a same way (e.g., 1940–58, 1965–90). For pine, there was a weak negative correlation between tree growth and iWUE when considering the influence of CO2 and climate together, whereas after removing the expected effects of CO2, enhanced iWUE was positively related to tree growth. Pine growth and iWUE changed synchronously, especially from 1980 onward (see Figure S8d available as Supplementary Data at Tree Physiology Online). Together this evidence argues that pines were able to take advantage of increased permafrost meltwater availability and grow faster as climate warmed, whereas warming has been detrimental to the growth of larch due to increased drought stress. The differences between how tree growth and iWUE responded after expected CO2 effects were removed demonstrates the importance of understanding species-specific ecophysiological responses to complex hydrological conditions in permafrost forests. Predicting when pine may run out of the permafrost meltwater subsidy and its subsequent reaction to much greater evaporative demand will take further investigation and modeling. However, the higher overall Ci values of both species should presumably provide some protection for these isohydric species against carbon starvation. Conclusions This study has documented responses of tree-ring Δ13C and δ18O to climate change and increased [CO2] over the past century. Although [CO2] has driven increased iWUE in both tree species, warming summer temperatures and enhanced atmospheric water demand and the emergence of drought stress over the past two decades have also greatly increased iWUE. These gains in iWUE have been particularly strong in larch compared with pines. Such differential drought sensitivity has resulted in larch having a greater climate-driven increase in iWUE over recent decades compared with pine. Species differences appear to be driven by pine utilizing relatively greater amounts of isotopically depleted permafrost meltwater, as evidenced by the declining trend in pine tree-ring δ18O, when mechanistic models suggest δ18O should have been increasing. If larch did indeed have lower variability in permafrost meltwater uptake compared with pine, Δ13C from this species may provide the most straightforward climate proxy for maximum temperatures or VPD. Nonetheless, our results revealed stronger coherence for tree-ring δ18O compared with Δ13C. Together these results suggest there is a strong potential for multi-species/isotope climate reconstruction based on using larch Δ13C for reconstructing inter-annual variation, but with pine δ18O to help discern variability in past source water uptake, as influenced by low-frequency variation in temperatures. Overall, our results underscore that boreal forest responses to climate warming and melting permafrost can be unique at the species level and therefore deserve due consideration in earth system models. It should therefore be a priority to continue research efforts aimed at documenting these mechanisms. More specifically, future studies should ideally combine data on seasonal soil-water isotopic variation (Throckmorton et al. 2016), CO2 effects on plant–microbe interactions (Becklin et al. 2017) and nutrient cycling (Gessler et al. 2017) to explore divergent tree-ring isotope responses to warming and [CO2] in regions where melting permafrost is causing profound environmental alterations. Acknowledgments We gratefully acknowledge the journal’s anonymous reviewers for their constructive comments on earlier versions of this manuscript. Conflict of interest None declared. Funding This research was supported by the National Natural Science Foundation of China (41571196 & 41721091), by the Youth Innovation Promotion Association, Chinese Academy of Sciences and by the Fundamental Research Funds for the Central Universities (Projects No. GK201801007). 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TI - Warming and CO2 enrichment modified the ecophysiological responses of Dahurian larch and Mongolia pine during the past century in the permafrost of northeastern China
JO - Tree Physiology
DO - 10.1093/treephys/tpy060
DA - 2019-01-01
UR - https://www.deepdyve.com/lp/oxford-university-press/warming-and-co2-enrichment-modified-the-ecophysiological-responses-of-FcLtJvb579
SP - 88
VL - 39
IS - 1
DP - DeepDyve
ER -