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Article

Effect of In Situ Large Soil Column Translocation on CO2 and CH4 Fluxes under Two Temperate Forests of Northeastern China

by
Xingkai Xu
1,2,*,
Tingting Xu
1,2 and
Jin Yue
1
1
State Key Laboratory of Atmospheric Boundary Layer Physics and Atmospheric Chemistry, Institute of Atmospheric Physics, Chinese Academy of Sciences, Beijing 100029, China
2
Department of Atmospheric Chemistry and Environmental Science, College of Earth and Planetary Sciences, University of Chinese Academy of Sciences, Beijing 100049, China
*
Author to whom correspondence should be addressed.
Forests 2023, 14(8), 1531; https://doi.org/10.3390/f14081531
Submission received: 23 June 2023 / Revised: 16 July 2023 / Accepted: 21 July 2023 / Published: 27 July 2023
(This article belongs to the Special Issue Responses of Soil Carbon and Nitrogen Dynamics and GHG Fluxes in Forest Ecosystems to Climate Change and Human Activity)
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Abstract

:
Global warming has a significant impact on soil carbon dioxide (CO2) and methane (CH4) fluxes in temperate forests. However, due to a lack of field observations, limited information is available about the responses of soil CO2 and CH4 fluxes to changes in temperature during the non-growing season and throughout the year in temperate forests. The broadleaf and Korean pine mixed mature forest (MF) and adjacent secondary white birch forest (BF) at different succession stages in the Changbai mountain region in northeastern China were selected, to study the effect of in situ soil column translocation on CO2 and CH4 fluxes in temperate forests. On average, the air temperature and soil temperature at 5 cm depth under BF stands from October 2018 to October 2022 increased by 0.64 and 0.42 °C during the non-growing season and by 0.49 and 0.43 °C throughout the year, respectively, compared with those under MF stands. Based on multi-year measurements in field experiments, it was shown that during the non-growing season, fluxes of CO2 and CH4 from soil columns under MF and BF stands ranged from 0.004 to 1.175 and from 0.015 to 1.401 (averages of 0.321 and 0.387) μmol CO2 m−2 s−1, and from −1.003 to 0.048 and from −1.037 to −0.013 (averages of −0.179 and −0.250) nmol CH4 m−2 s−1, respectively, accounting for approximately 20.8% and 25.3%, and 48.8% and 69.1% of the corresponding average fluxes during the growing season. When undisturbed soil columns of MF were transferred to a BF stand, to simulate warming, the cumulative soil CO2 emissions and CH4 uptake increased by 23.5% and 15.3% during the non-growing season, and by 9.5% and 16.3% across the year, respectively. However, when soil columns of BF were transferred to a MF stand, to simulate cooling, the cumulative soil CO2 emissions decreased by 16.9% and 0.1% during the non-growing season and across the year, respectively. Upon cooling, the cumulative soil CH4 uptake decreased by 21.8% during the non-growing season but increased by 15.4% across the year. The soil temperature and moisture at 5 cm depth in soil columns could explain 84–86% of the variability in CO2 fluxes and 16–51% of the variability in CH4 fluxes under the two forest stands throughout the field measurement period. The results of the in situ soil column translocation experiments highlight that a small climate warming in nature can increase soil CO2 emissions and CH4 uptake in the temperate forests of northeastern China, particularly during the non-growing season, which should be considered when predicting soil C fluxes in the temperate forests of northeastern China under global warming scenarios.

1. Introduction

Climate change is expected to increase global surface temperatures by 1.4 to 4.4 °C above pre-industrial levels by the end of the 21st century, mainly due to increased atmospheric greenhouse gas (GHG) concentrations resulting from human activities [1]. Rising air temperatures have been shown to affect the growth of vegetation and the activity of soil microorganisms, probably influencing carbon (C) cycling in soil and the C fluxes between soil and the atmosphere [2,3,4,5]. As a vital process of soil C cycling, soil respiration can account for more than 60% of forest ecosystem respiration [6,7], and a small change in soil respiration due to climate change may lead to a significant change in forest ecosystem respiration. Based on an updated global soil respiration database, it was documented that the ratios of soil heterotrophic respiration to total soil respiration around the globe increased significantly from 0.54 to 0.63 between 1990 and 2014, indicating that climate-driven losses of soil C are currently occurring in many terrestrial ecosystems around the globe [4]. Apart from soil C loss as CO2, well-drained forest soils are a major sink for atmospheric CH4 and can play an important role in modulating the global CH4 budget [8,9]. Climate warming and its attendant changes in precipitation are known to remarkably affect soil CO2 emissions and CH4 uptake in forest ecosystems across different climate zones, especially in temperate forests [2,4,5,8,10,11,12,13,14]. The interaction between soil temperature and soil moisture can make the responses of soil CO2 and CH4 fluxes to climate change more complicated [5,12,15,16]. Therefore, it is of great importance to study the effects of climate warming on soil CO2 and CH4 fluxes in temperate forest ecosystems.
In recent decades, soil warming experiments conducted in forest ecosystems around the globe have shown that warming generally results in a considerable short-term soil C loss [3,10,13,17,18,19,20]. However, some experimental observations showed that soil warming did not affect soil CO2 emissions under boreal-temperate forests [15] and a subtropical planation forest [21]. Compared with the response of soil CO2 emissions to climate warming, relatively less attention has so far been paid to the CH4 uptake by soils in forest ecosystems under warming [15,16,22]. In recent meta-analyses, Liu et al. [23] and Yan et al. [5] reported that soil warming could increase soil CH4 uptake across different upland ecosystems by 7.5% and 15%, respectively. Due to minimal changes in soil moisture and NH4-N contents, no effects of warming on soil CH4 fluxes were observed for boreal-temperate forests [15,22]. During the decadal soil warming of a temperate mountain forest, Heinzle et al. [16] reported that soil warming by 4 °C reduced the CH4 uptake by 19.5% during the initial years of warming, whereas no warming effects occurred during the later years. Taken together, the different responses of CO2 and CH4 fluxes in forest soils to warming during the growing season are mainly ascribed to various changes in the duration and intensity of soil warming, climate types, as well as soil physicochemical and microbial properties associated with soil warming at different experimental sites [5,10,13,16,22,24,25,26]. More importantly, to date, few studies have been paid attention to the C fluxes between soils and the atmosphere in temperate forests, considering the background of global warming, especially during the non-growing season [12,16,27].
In a recent meta-analysis, all in situ soil warming experiments were characterized by different levels of warming intensity (from 0.5 to 9 °C) and mostly by relatively short durations during the growing season [13], which implies some limitations for simulating global climate changes in nature, i.e., the gradual increase in both soil and air temperature over decadal time scales. The relatively high magnitude of changes in temperature relative to the smaller climate changes in nature, and the differences in soil properties and annual precipitation across soil warming experiments, can to some extent lead to different responses of soil CO2 and CH4 fluxes to climate changes [5,16,22]. Unlike infrared or cable heating manipulations, translocation experiments can result in the air and soil being warmed under natural conditions, by transferring soil columns from high-latitude to low-latitude zones. Among the soil translocation experiments previously reported, most studies focused on the measurement of C fluxes between soils and the atmosphere within and across years at different sites with varying annual precipitation, with less attention given to the soil CH4 flux [24,28,29,30]. The coupled relationship between annual average soil temperature and annual precipitation across different soil-translocation experimental sites can, in turn, make the response of annual soil CO2 and CH4 fluxes to climate change more complicated [5,16,24,29]. Furthermore, to date, there has been a lack of knowledge about soil CO2 and CH4 fluxes in response to small temperature changes in nature, which is associated with precisely evaluating the responses of annual soil CO2 and CH4 fluxes in temperate forests to future climate changes.
Translocation experiments with a small gradient in micrometeorological factors (e.g., temperature and rainfall) can provide an opportunity to simulate climate change in nature and, thus, to evaluate the long-term effects of climate change within a natural environment [19,28,29,30]. Northeastern China is located on the northeastern edge of the global monsoon climate and is affected by the continental climate, with long cold winters and short summers; this region, which recorded an annual increase of 0.04 °C per year from 1961 to 2004, is currently becoming sensitive to climate change [31]. It is likely that C fluxes between soils and the atmosphere in the temperate forest ecosystems of northeastern China would be sensitive to future climate changes. The forest coverage in northeastern China accounts for approximately 27% of national forest coverage [32]. Broadleaf and Korean pine mixed mature forest (MF) represents the main zonal forest ecosystem in northeastern China, and the near-surface air temperature under MF is lower than under the adjacent secondary white birch forest (BF) across the year, particularly in the non-growing season (from November to April), due to differences in vegetation cover and understory light availability [33]. Furthermore, the properties of soil and aboveground litter in MF stands differ from those in BF stands [34,35]. The differences in annual average near-surface air temperature and soil properties under MF and BF stands can thus provide a good platform for studying the effects of warming and cooling in nature on soil CO2 and CH4 fluxes in temperate forests over the year, using reciprocal translocation experiments of large in situ soil columns between the two forest stands.
We predicted that changes in air temperature in nature would affect the CO2 and CH4 fluxes from temperate forest soil during the non-growing season and throughout the year and that the C fluxes between the soil and the atmosphere during the non-growing season would be more sensitive to climate change. To reduce the effects of other environmental factors, as much as possible, in situ large soil column reciprocal translocation experiments were used, as an effective method for studying the effects of changes in air temperature and/or precipitation on C fluxes between the soil and the atmosphere in forest and grassland ecosystems [19,24,28,29,30]. Based on multi-year field measurements of soil column reciprocal translocation experiments under MF and BF stands, the objectives of this study were to explore how climate warming and cooling in nature can affect CO2 and CH4 fluxes from temperate forest soils during the non-growing season and throughout the year. The results can provide a basis for understanding the responses of C fluxes between soils and the atmosphere in the temperate forests of northeastern China to future climate change.

2. Materials and Methods

2.1. Site Description and Collection of Soil Columns

The soil column reciprocal translocation experiments were carried out under MF and BF stands near the National Research Station of Changbai Mountain Forest Ecosystems (42°24′ N and 128°6′ E), at the foot of Changbai mountains, northeastern China. The Changbai mountain region is located on the northeastern edge of the global monsoon climate and is influenced by the continental climate, with long cold winters and short summers. MF represents the main zonal forest ecosystem in northeastern China, and its aboveground litter and soil properties are different from those of BF [34,35]. The dominant trees of the MF include Korean pine (Pinus koraiensis Sieb. et Zucc.), Tuan linden (Tilia amurensis Rupr.), Mongolian oak (Quercus mongolica Fisch. ex Turcz), and Manchurian ash (Fraxinus mandshurica Rupr.), mostly >200 years old, and their stand densities are 98.9, 117.1, 37.1, and 27.2 trees ha−1, respectively [36]. The BF is dominated by white birch (Betula platyphylla Suk.) and mountain poplar (Populus davidiana Dode), mostly >70 years old, and its stand density is 1402 stem ha−1; white birch and mountain polar account for approximately 51.5% and 23.1% of the basal area of tree species, respectively [33]. Due to the differences in vegetation cover and photophilic tree species, the air temperature and understory photosynthetically active radiation transmittances for BF in the non-growing season are normally higher than for MF [33]. The temperate forest soil is classified as an Andosol, with a 3–5 cm organic horizon and approximately 10 cm depth of A horizon. The main soil properties and the properties of the aboveground litter for the MF and BF stands were reported in detail by Xu et al. [37,38] and Wu et al. [34,35].
Eight 2 m × 2 m small plots with well-preserved aboveground litter layers were selected under MF and BF stands in October 2017, prior to autumn freeze–thaw events, to collect large undisturbed soil columns at approximately 30 cm depth. At the center of each small plot, a stainless steel cylindrical grinding tool (20 cm in diameter and 40 cm in height) was first driven into the soil to approximately 30 cm depth and then replaced by thickened UPVC (unplasticized polyvinyl chloride) tubes (20 cm in diameter and 40 cm in height), and the soil column was finally taken out as one undisturbed large soil column, with the aboveground litter. In total, there were eight undisturbed large soil columns for each forest stand for the layout of the soil translocation experiments in the field.

2.2. Setup of the In Situ Large Soil Column Translocation Experiments

As mentioned above, the air temperature under BF stands is normally higher than under MF stands, especially in the non-growing season, due to differences in vegetation cover and understory light availability [33], which provides a good platform for simulating climate change in the field. To study changes in soil CO2 and CH4 fluxes in temperate forests with warming and cooling throughout the year, half of the undisturbed large soil columns (n = 4) from the MF stand were translocated to the BF stand, to simulate warming, and half of the undisturbed large soil columns (n = 4) from the BF stand were translocated to the MF stand, to simulate cooling; the other soil columns (n = 4) were separately incubated in situ under the MF and BF stands as controls. To eliminate the effects of fine root decomposition on the soil CO2 and CH4 fluxes as much as possible, all undisturbed large soil columns were placed into MF and BF stands for one year, following the reciprocal translocation of soil columns, considering that the turnover rates of fine roots in the 0–10 cm soil depth ranged from 0.49 year−1 to 1.0 year−1 for five forest types in northeastern China [39]. Starting from October 2018, the CO2 and CH4 fluxes from the soil columns under MF and BF stands were determined on non-rainy days, mostly between 9:00 and 11:30 in the morning, using a portable greenhouse gas analyzer (915-0011, Los Research Inc., Fremont, CA, USA) coupled to a smart respiratory chamber (SC-11, Beijing LICA United Technology Limited, Beijing, China). From December to February each year, the soil CO2 and CH4 fluxes were generally measured once each month, because of low fluxes; in the other months of the year, the soil CO2 and CH4 fluxes were generally measured twice to three times each month. From January to September 2020, the measurement of soil CO2 and CH4 fluxes was not performed, due to equipment problems. During the non-freezing period of each year, the soil temperature and volumetric water contents (v/v, %) at 5 cm depth in the soil columns were determined using a temperature and moisture device attached to a portable greenhouse gas analyzer (915-0011, Los Research Inc., Fremont, CA, USA). During the period from October 2017 to October 2022, the air temperature and soil temperature at 5 cm depth under the MF and BF stands were recorded using an ONSET HOBO temperature logger (HOBO U23-003, Onset Computer Corporation, Bourne, MA, USA) at 30 min intervals.

2.3. Data Calculation and Statistical Analysis

Soil CO2 and CH4 fluxes per unit area (m−2) were calculated, only concerning the surface area of the soil columns. The mean and standard error of four replicates were calculated in each experimental treatment. Cumulative soil CO2 and CH4 fluxes during the non-growing and growing seasons and for the year were calculated. All variables for air temperature, soil temperature, and moisture at 5 cm depth, as well as CO2 and CH4 fluxes, were first tested for normality using a Shapiro–Wilk test and homogeneity of variance using Levene’s test, and log-transformed where necessary. The monthly and seasonal CO2 and CH4 fluxes, as well as soil temperature and volumetric water contents at 5 cm depth in all treatments were described with box and box normal plots using OriginPro 2021 (OriginLab Corporation, Northampton, MA, USA). The monthly and seasonal changes in air temperature and soil temperature at 5 cm depth under MF and BF stands were also described with box and box normal plots, respectively, using OriginPro 2021 (OriginLab Corporation, Northampton, MA, USA). Pair-wise comparisons of significant effects were conducted using Tukey’s HSD post hoc test, with significant differences identified at p < 0.05. The relationships among the soil CO2 and CH4 fluxes, soil temperature, and volumetric water contents at 5 cm depth in soil columns were fitted with nonlinear regressions using OriginPro 2021 (OriginLab Corporation, Northampton, MA, USA). The temperature sensitivity of the soil CO2 fluxes during the non-growing season and throughout the year were calculated. All statistical analyses were conducted using SPSS for Windows software (version 19.0) (IBM Corp., New York, NY, USA).

3. Results

3.1. Changes in Air Temperature and Soil Temperature at 5 cm Depth under MF and BF Stands

On average, the monthly air temperature and soil temperature at 5 cm depth under the BF stand from October 2018 to October 2022 were higher than those under the MF stand (p < 0.01), with the exception of the soil temperature in November (Figure 1a,b). Compared with the MF stand, the air temperature and soil temperature at 5 cm depth under the BF stand, on average, increased by 0.64 °C and 0.42 °C during the non-growing season (p < 0.001) and by 0.33 °C and 0.45 °C during the growing season (p < 0.001), respectively (Figure 1c,d). The persistent air and soil temperature gradients under MF and BF stands that occurred with a short distance of less than 500 m, enabled the effects of small climate changes in nature (e.g., warming and cooling) on soil CO2 and CH4 fluxes to be studied, using the means of the large soil column reciprocal translocation experiments between the two forest stands.

3.2. Effects of Soil Column Translocation on Soil CO2 and CH4 Fluxes under MF and BF Stands

Prior to the field experiments, the CO2 and CH4 fluxes from the soil columns under MF and BF stands (n = 8, for each forest type) varied little, indicating that the spatial variability of the background conditions across soil columns would be negligible in the subsequent analysis of CO2 and CH4 fluxes in the soil column reciprocal translocation experiment.
During the period from October 2018 to October 2022, the monthly average soil temperature at 5 cm depth in soil columns during the non-growing season was higher under the BF stand than under the MF stand (p < 0.05) (Figure 2a,b). However, due to the relatively high volumetric water contents of the soil columns under the BF stand during the growing season (Figure 2c,d), the monthly average soil temperature at 5 cm depth for the MF and BF soil columns under the BF stand was smaller than under the MF stand in May and June (p < 0.001) (Figure 2a,b), and the same trend for the BF soil columns occurred in September (p < 0.01) (Figure 2b). The average monthly CO2 emissions from soil columns under the MF and BF stands were the maximum in July and the minimum in January (Figure 2e,f). Upon the translocation of soil columns from the MF stand to the BF stand, a significant increase in monthly average soil CO2 emissions occurred in December, April, and May, due to warming (p < 0.05) (Figure 2e), and the monthly average CH4 fluxes decreased significantly in April and May (p < 0.001) (Figure 2g). When the BF soil columns were transferred to the MF stand, the monthly average soil CO2 emissions decreased significantly in December (p < 0.05), due to cooling, and increased significantly in June (p < 0.01) (Figure 2f), partially due to the relatively high volumetric water contents of the BF soil columns incubated in situ in June (Figure 2d); the monthly average soil CH4 fluxes decreased significantly in May, June, and July following the translocation of the BF soil columns to the MF stand (p < 0.05) (Figure 2h), which paralleled the decrease in monthly soil volumetric water contents (Figure 2d). The monthly average CH4 fluxes from soil columns under the MF and BF stands remained lowest in October and November (Figure 2g,h), suggesting the maximum seasonal soil CH4 uptake over the year in this study region.
On average, the daily average soil temperature at 5 cm depth across MF and BF soil columns during the non-growing season were higher under the BF stand than under the MF stand (p < 0.001) (Figure 3a), which paralleled the changes in average soil CO2 emissions during the non-growing season (Figure 4a). The relatively high average soil volumetric water contents under the BF stand during the growing season (Figure 3d) contributed to the lower average soil temperature at 5 cm depth in the soil columns under the BF stand than under the MF stand (p < 0.01) (Figure 3b). This phenomenon did not lead to any significant differences in the average CO2 emissions from the MF and BF soil columns between BF and MF stands during the growing season (Figure 4b). The average CH4 fluxes from the soil columns during the non-growing season appeared to be smaller under the BF stand than under the MF stand, due to the relatively low soil moisture (Figure 3c), but the differences were not significant (Figure 4c). During the growing season, CH4 fluxes from the MF soil columns under the BF stand were smaller than under the MF stand (p < 0.05), whereas the CH4 fluxes from the BF soil columns under the MF stand were smaller than under the BF stand (p < 0.05) (Figure 4d).

3.3. Effects of Soil Temperature and Moisture on Soil CO2 and CH4 Fluxes

The combined effects of soil temperature and moisture on the daily CO2 and CH4 fluxes from the MF and BF soil columns under MF and BF stands are shown in Figure 5 and Figure 6. The 84%–86% variation in soil CO2 emissions and 16%–51% variation in soil CH4 fluxes were explained by the soil temperature and moisture at 5 cm depth, respectively. The maximum daily CH4 uptake occurred at soil temperature at 5 cm depth ranging from 7.5 to 14 °C, with soil volumetric water contents at 5 cm depth ranging from 38% to 48% (v/v) (Figure 6). The daily CO2 emission increased significantly with the increase in soil temperature at 5 cm depth, and it reached a maximum at soil volumetric water contents ranging from 55% to 64% (v/v) under the experimental conditions (Figure 5).
On average, the temperature sensitivity (Q10) of CO2 emissions from MF and BF soil columns over the year from October 2018 to October 2022 ranged from 2.86 to 2.96 under MF and BF stands, which was not significantly affected by the soil column translocation (Figure 7c,d). The Q10 values of CO2 emissions over the year were smaller than those during the non-growing season (p < 0.05) (Figure 7a,b). When the MF soil columns were translocated to the BF stand, the Q10 values of the soil CO2 emissions decreased, on average, from 8.73 to 7.22 during the non-growing season (Figure 7a), which differed from the changes in the Q10 values of the soil CO2 emissions (5.85 to 7.46) following the translocation of BF soil columns to the MF stand (Figure 7b). Due to the large annual variability, differences in the Q10 values of CO2 emissions during the non-growing season across all soil columns were not significant (Figure 7a,b).

3.4. Effects of Warming and Cooling on Cumulative Soil CO2 and CH4 Fluxes in Temperate Forests

Due to differences in the vegetation cover and understory light availability for the MF and BF stands, the translocation of the MF soil columns to BF stand simulated climate warming, with an increase of 0.64 °C and 0.33 °C in air temperature during the non-growing and growing seasons, respectively, and with a climate cooling phenomenon occurring following the translocation of the BF soil column to the MF stand (Figure 1). Cumulative CO2 emissions from the MF soil columns during the non-growing season were significantly increased upon climate warming (p < 0.05), and the warming appeared to enhance the emissions during the growing season and throughout the year, but no significant differences were observed (Figure 8a). When the BF soil columns were translocated to the MF stand, to simulate climate cooling, the cumulative soil CO2 emissions during the non-growing season were significantly reduced (p < 0.05) (Figure 8b). However, there were no differences in the cumulative CO2 emissions from the BF soil column under the growing season and across the year with cooling (Figure 8b). Following the translocation of MF soil columns to the BF stand, the cumulative soil CH4 fluxes appeared to decrease during the non-growing and growing seasons and across the year, due to climate warming, but no significant differences were observed (Figure 8c). Upon the translocation of BF soil columns to the MF stand, the cumulative soil CH4 fluxes significantly decreased during the growing season, due to climate cooling (p < 0.05) but appeared to increase during the non-growing season (Figure 8d). Taken together, these results indicate that the effects of warming and cooling on cumulative soil CO2 and CH4 fluxes in the temperate forests of the study region varied between the non-growing and growing seasons.
Based on multi-year measurements of field experiments, on average, a slight warming and cooling of approximately 0.5 °C in annual mean air temperature (Figure 1) increased the cumulative CO2 emissions from MF soil columns by 23.5% during the non-growing season (p < 0.05) and by 9.6% across the year and decreased the cumulative CO2 emissions from the BF soil columns by 16.8% during the non-growing season (p < 0.05) and by 0.1% across the year, respectively (Figure 9a,b). Compared with those during the growing season (Figure 8a,b), the cumulative soil CO2 emissions in the temperate forests in the study region became more sensitive to small climate changes during the non-growing season (Figure 9a). The small climate warming appeared to increase the cumulative CH4 uptake of the MF soil columns by 15.3% during the non-growing season and by 16.3% across the year (Figure 9a,b), suggesting that even such a slight warming of the climate can promote soil CH4 uptake in temperate forests in the study region. With such a slight climate cooling, the cumulative CH4 uptake of the BF soil columns during the non-growing season decreased by 21.8% (Figure 9a), whereas it significantly increased, by 40.7%, during the growing season (p < 0.05) (Figure 8d). This led to a 15.4% increase in the annual cumulative CH4 uptake in the BF soil columns due to the cooling (Figure 9b).

4. Discussion

4.1. Effects of Warming and Cooling on Soil CO2 Emissions under Temperate Forest Stands

Under the experimental conditions, the cumulative CO2 emissions from the soil columns under the MF and BF stands in the non-growing season ranged from 38.31 to 39.31 and from 47.26 to 47.35 g C per m2, respectively, which accounted for 9.6% to 11.4% of the annual average soil CO2 emissions (Figure 8a,b). The soil cumulative CO2 emissions during the non-growing season and their contributions to annual soil CO2 emissions for the two temperate forests were within the range reported by previous studies under temperate forests in Northeast Asia region [40,41,42].
In this study, an increase of approximately 0.5 °C in the annual mean near-surface air temperature (Figure 9b) resulted in a 9.6% increase in annual CO2 emissions from the MF soil columns, which was much smaller than the values reported by many previous soil column translocation experiments [19,28,29]. Hart [19] reported a 120% increase in soil CO2 emissions in a spruce–fir forest in the American Southwest as the result of an increase of 2.5 °C in soil temperature. Based on a reciprocal translocation experiment, Luan et al. [29] reported a 44% increase in soil CO2 emissions under a warm-temperate oak forest in China, with a 13-month warming of soil temperatures by approximately 3.3 °C. The relatively low response of soil CO2 emissions in this study may have resulted from the small magnitude of soil warming (approximately 0.4 °C across the year) and differences in soil physiochemical and microbial properties (e.g., soil C:N ratio, C substrate quality and quantity, nutrient and moisture availability, soil texture, and shifts in the microbial community) at the different experimental sites [5,20,24,30,43]. Additionally, used to reduce the effects of the decomposition of fine roots remaining inside the soil columns on the soil CO2 emissions, as much as possible, the delay of one year following the soil column reciprocal translocation experiments between the two forest stands was partially responsible for the relatively low responses to the slight climate warming, because the initial large stimulating effect of climate warming on the soil CO2 emissions was excluded [28]. Nonetheless, the cumulative CO2 emissions from the MF soil columns during the non-growing season with such warming significantly increased by 23.5% (p < 0.05), and vice versa (a decrease of 16.8%, p < 0.05) for those from the BF soil columns under cooling conditions (Figure 9a). Hence, the results indicated that slight soil warming can lead to a remarkable increase in soil CO2 emissions in temperate forests in the study region, particularly in the non-growing season. An earlier meta-analysis indicated that experimental warming can increase soil respiration by 7%–11% across different terrestrial ecosystems [2], which is close to the 9.6% increase in annual soil CO2 emissions with such small climate warming in this study (Figure 9b). The magnitude of the increase in annual soil heterotrophic respiration (9.6%) upon soil warming was also close to the results reported by Yan et al. [5] in a recent meta-analysis, who summarized a 9.9% increase in soil CO2 emissions with experimental warming across multiple terrestrial ecosystems around the globe.
Our study showed that, under warming or cooling conditions, soil temperature and moisture at 5 cm depth could account for 84%–86% of the variation in daily soil CO2 emissions during the period from October 2018 to October 2022 (Figure 5). Furthermore, the maximum daily soil CO2 emission occurred at soil volumetric water contents ranging from 55% to 64% (v/v) under the experimental conditions (Figure 5), suggesting that soil CO2 emissions decrease when soil moisture becomes either relatively wetter or drier [44,45,46,47]. This was obviously different from the results observed by Luan et al. [29] for a warm-temperate forest, who reported that the responses of soil CO2 emission to a soil column translocation experiment were mainly caused by changes in soil temperature, rather than soil moisture. This negligible effect of soil moisture could be ascribed to a small range of soil volumetric water contents (0.15 to 0.35 cm−3 cm−3), which was much less than the soil moisture observed in our study (Figure 2c,d).
The surface soil at 10 cm depth under the BF stand was characterized by a relatively small sand content and relatively large silt content compared with surface soils of the MF stand [35], and the annual throughfall for the BF was generally larger than for the MF stand during the growing season (data not shown), due to the forest canopy vegetation [33]. These phenomena may have partially contributed to the relatively large volumetric water contents in the BF soil columns incubated in situ during the growing season (Figure 2d). The changes in soil moisture during the growing season could have weakened, to a greater extent, the negative responses of the cumulative CO2 emissions from the BF soil columns to climate cooling, compared with those during the non-growing season (Figure 8b), thus resulting in a decrease of approximately 0.1% in the annual cumulative CO2 emissions from the BF soil columns upon climate cooling (Figure 9b). These results indicate that changes in soil moisture induced by throughfall can, to some extent, affect the response to climate change in soil CO2 emissions under temperate forests [11,15]. Based on various recent meta-analyses, soil CO2 emissions in temperate forests are becoming more sensitive to climate changes, such as warming and precipitation, compared to those in boreal forests [13,14]. Hence, more field experiments on warming should be carried out at various specific sites in temperate forests, to precisely characterize the response of soil CO2 emissions, especially soil heterotrophic respiration, to climate change.

4.2. Effects of Warming and Cooling on Soil CH4 Flux under Temperate Forest Stands

Under the experimental conditions, the cumulative soil CH4 fluxes in the non-growing season under the MF and BF stands ranged from –27.72 to –25.73 and from –35.43 to –29.67 mg C per m2, which accounted for 27.4% to 40.5% of the annual average soil CH4 fluxes (Figure 8c,d). The contribution of soil CH4 fluxes during the non-growing season to the annual soil CH4 fluxes in this study is in agreement with the results reported by Heinzle et al. [16] for control and warmed plots in a temperate mountain forest in Austria (from 28% to 35% and from 24% to 38%, respectively). When MF soil columns were transferred to BF stands to simulate soil warming in nature, the annual average cumulative soil CH4 uptake throughout the experimental period increased from 0.88 ± 0.20 to 1.02 ± 0.20 Kg C per hectare, due to soil warming of 0.43 °C (Figure 8c,d). The magnitude of the increase in the soil CH4 uptake with soil warming is in agreement with the results described in recent meta-analyses [5,23]. However, Heinzle et al. [16] reported that soil warming by 4 °C reduced the soil CH4 uptake by 19.5% during the initial years of warming in a temperate mountain forest in Austria with high annual precipitation, whereas no warming effects occurred during the later years. This difference could be mainly ascribed to changes in the soil moisture induced by annual precipitation across the different field experimental sites [8,11,16], because soil moisture is normally considered the most important factor in regulating the diffusion of atmospheric CH4 into the soil in upland ecosystems [18,48].
Under soil warming conditions, soil moisture can, to some extent, decrease, which then strengthens the CH4 uptake in soils by microbes via increasing gas diffusion [49]. However, soil warming can affect the availability of soil nutrients (e.g., NH4-N) [22,25,50], the quantity and quality of substances (e.g., amount and biodegradation of dissolved organic C) [50,51,52,53], soil pH [50,54], and shifts in the population and activity of methanotrophic bacteria [25,54], thus influencing the soil CH4 uptake [11,12,13,26,55]. In this study, an increase of approximately 0.5 °C in annual mean near-surface air temperature (Figure 9b) led to a 16.3% increase in the annual soil CH4 uptake in temperate forests in northeastern China, which was higher than the results described in several recent meta-analyses [5,23], which documented that, on average, a 7.5% or 15% increase in the soil CH4 uptake occurred in upland ecosystems under warming conditions. Furthermore, Hart [19] reported a 90% increase in soil CH4 consumption in a spruce-fir forest in the American Southwest, as the result of an increase of 2.5 °C in soil temperature, which paralleled a 80% increase in net N mineralization and nitrification in transferred soil cores compared with in situ soil cores. The results of Hart [19] show that small increases in mean annual air temperature can have large impacts on soil nitrogen cycling and CH4 consumption, even in ecosystems where water availability is a limited resource. However, due to minimal changes in soil moisture and NH4-N contents, soil warming in a Swiss alpine tree line did not affect CH4 fluxes from the forest soils [22]. Taken together, these different effects of climate warming on CH4 fluxes in forest ecosystems during the growing season can be mainly ascribed to various changes in soil properties (e.g., soil water and nutrient availability [12,48,50], pH [50,54,55], quantity and quality of substances [12,50,51], and the population and activity of methanotrophic bacteria [5,22,25]) associated with soil warming at different experimental sites.
To date, limited information has been available about the responses of soil CH4 fluxes to climate changes in the non-growing season in forest ecosystems at a global scale [16,27]. The results of this study showed that soil CH4 fluxes appeared to be more sensitive to climate changes during the non-growing season than across the year in temperate forests in northeastern China (Figure 9a,b), probably due to the impacts of changes in soil moisture induced by throughfall during the growing season under MF and BF stands (Figure 2c,d). In a previous warming experiment in a northern hardwood forest in the USA, McHale et al. [18] reported that soil water content exhibited the most influence on soil CH4 fluxes in the second year. Under warming or cooling conditions, soil temperature and soil moisture at 5 cm depth explained 16%–51% of the variation in soil CH4 fluxes throughout the experimental period, and a maximum daily CH4 uptake was observed at soil temperature ranging from 7.5 to 14 °C, along with soil volumetric water contents ranging from 38% to 48% (v/v) (Figure 6). Although there is a maximum CH4 uptake capacity in temperate forest surface soils at 25 °C under optimum soil moisture conditions [55], the decrease in the soil CH4 uptake at high soil temperatures in this study may have been, to a large extent, caused by the limitation of high soil moisture on CH4 diffusivity during the growing season, particularly inside the BF soil columns incubated in situ (Figure 2d,h). This would partly explain the relatively large soil CH4 uptake during the growing season when the BF soil columns were transferred to MF stands (Figure 2h and Figure 8d). When the soil moisture is not limited, the CH4 uptake by microbes in soils can increase linearly with increasing soil temperature up to 35 °C [56]. In mesic environments with soil moisture levels typically above optimum, soil warming normally increases the CH4 uptake, which is opposite to the effect of warming on CH4 uptake when soils are dry [49]. Nonetheless, contrary experimental results were reported for the warming effects of CH4 fluxes between two alpine grasslands with a contrasting soil water status [25] and in a temperate mountain forest with high annual precipitation [16]. Together with the responses of soil CO2 emissions to climate warming, the results of this study indicate that a remarkable response to climate warming of C fluxes between soils and the atmosphere is currently occurring in temperate forests of northeastern China, especially during the non-growing season. Considering that climate warming-induced soil C fluxes across different terrestrial ecosystems are dependent on the magnitude of changes in soil moisture, the intensity and duration of soil warming, and changes in other associated soil properties [3,5,18,25,27,50,51,57], long-term field observations of warming across different terrestrial ecosystems of northeastern China are needed, to evaluate the response and feedback of soil C fluxes in northeastern China to future climate changes.

5. Conclusions and Future Perspectives

The results from multi-year field measurements indicated that following the translocation of MF soil columns to a BF stand, the increase of approximately 0.5 °C in annual average near-surface air temperature, on average, increased the annual soil CO2 emission by 9.6% and CH4 uptake by 16.3% in temperate forests in the study region. These increases amounted to 760 kg ha−1 year−1 of soil C loss and 0.286 kg ha−1 year−1 of CH4 uptake per 1 °C increase in the temperate forests of the study region. The combined effects of soil temperature and moisture could account for 84%–86% of the variability in soil CO2 emissions and 16%–51% of the variability in soil CH4 fluxes under the experimental conditions, respectively. Assuming a similar magnitude of response of soil C fluxes to climate warming across different temperate forests in northeastern China and an estimated forest coverage for this region of 58.6 million hectare [32], our results further illustrate that a moderate warming of 1 °C would increase the annual soil heterotrophic respiration and annual CH4 uptake in the temperate forests of northeastern China by a magnitude of 44.536 Tg CO2-C (1 Tg = 1012 g) and 0.0168 Tg CH4-C, respectively. Provided that CH4 from fossil sources has the ability to trap 29.8 times as much thermal radiation as CO2 on a molar basis over a 100-year timescale [1], an increase in C fluxes between soils and the atmosphere from 1 °C warming across temperate forests in northeastern China was estimated at approximately 44.04 Tg CO2-C-equivalent year−1, indicating the remarkable positive feedback of forest soil C fluxes to future climate change in northeastern China. Considering an annual air temperature increase rate of 0.04 °C per year from 1961 to 2004 in northeastern China [31], this finding highlights that the temperate forests in northeastern China may trigger an overall positive feedback of soil C fluxes to climate warming, which should be effectively incorporated into soil C cycling-related models, to precisely predict soil C fluxes in the temperate forests of northeastern China under global warming scenarios.

Author Contributions

Conceptualization, methodology, investigation, formal analysis, resources, investigation, writing—original draft preparation, writing—review and editing, supervision, funding acquisition, X.X.; formal analysis, investigation, writing—review and editing, T.X.; formal analysis, writing—review and editing, J.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (grant number: 41175133, 41775163, 41975121 and 42275130).

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Forests 14 01531 g001 550
Figure 1. Overall pattern of air temperature and soil temperature at 5 cm depth under MF and BF stands from October 2018 to October 2022: (a,b) box plots of monthly air temperature and monthly soil temperature, (c,d) box normal plots of air temperature and soil temperature during the non-growing and growing seasons. Boxes represent interquartile ranges (IQRs), and horizontal lines and circles within boxes indicate median and mean values, respectively. Upper and lower whiskers (x) show 75 percentiles plus 1.5 IQR and 25 percentiles minus 1.5 IQR, respectively. ** p < 0.01; *** p < 0.001.
Figure 1. Overall pattern of air temperature and soil temperature at 5 cm depth under MF and BF stands from October 2018 to October 2022: (a,b) box plots of monthly air temperature and monthly soil temperature, (c,d) box normal plots of air temperature and soil temperature during the non-growing and growing seasons. Boxes represent interquartile ranges (IQRs), and horizontal lines and circles within boxes indicate median and mean values, respectively. Upper and lower whiskers (x) show 75 percentiles plus 1.5 IQR and 25 percentiles minus 1.5 IQR, respectively. ** p < 0.01; *** p < 0.001.
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Figure 2. Box plots of monthly soil temperature (a,b) and moisture (c,d) at 5 cm depth, CO2 emission (e,f), and CH4 flux (g,h) from the MF and BF soil columns under MF and BF stands from October 2018 to October 2022. * p < 0.05; ** p < 0.01; *** p < 0.001. Descriptions of the box plots are shown in the caption of Figure 1.
Figure 2. Box plots of monthly soil temperature (a,b) and moisture (c,d) at 5 cm depth, CO2 emission (e,f), and CH4 flux (g,h) from the MF and BF soil columns under MF and BF stands from October 2018 to October 2022. * p < 0.05; ** p < 0.01; *** p < 0.001. Descriptions of the box plots are shown in the caption of Figure 1.
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Forests 14 01531 g003a 550Forests 14 01531 g003b 550
Figure 3. Box normal plots of soil temperature (a,b) and moisture (c,d) at 5 cm depth in the MF and BF soil columns under MF and BF stands during the non-growing and growing seasons from October 2018 to October 2022. * p < 0.05; ** p < 0.01; *** p < 0.001. Descriptions of the box plots are shown in the caption of Figure 1.
Figure 3. Box normal plots of soil temperature (a,b) and moisture (c,d) at 5 cm depth in the MF and BF soil columns under MF and BF stands during the non-growing and growing seasons from October 2018 to October 2022. * p < 0.05; ** p < 0.01; *** p < 0.001. Descriptions of the box plots are shown in the caption of Figure 1.
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Figure 4. Box normal plots of CO2 emissions (a,b) and CH4 fluxes (c,d) from the MF and BF soil columns under MF and BF stands during the non-growing and growing seasons from October 2018 to October 2022. * p < 0.05; ** p < 0.01; *** p < 0.001. Descriptions of the box plots are shown in the caption of Figure 1.
Figure 4. Box normal plots of CO2 emissions (a,b) and CH4 fluxes (c,d) from the MF and BF soil columns under MF and BF stands during the non-growing and growing seasons from October 2018 to October 2022. * p < 0.05; ** p < 0.01; *** p < 0.001. Descriptions of the box plots are shown in the caption of Figure 1.
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Figure 5. Combined effects of soil temperature and moisture at 5 cm depth on the daily CO2 emissions from the MF (a,c) and BF (b,d) soil columns under MF and BF stands from October 2018 to October 2022. For winter (from late November to early March), soil moisture is not included, due to soil freezing. The combined effects of soil temperature and soil moisture on daily CO2 emissions were fitted with multivariate regression curves. Legends with different gray scales represent the different ranges of soil CO2 emissions.
Figure 5. Combined effects of soil temperature and moisture at 5 cm depth on the daily CO2 emissions from the MF (a,c) and BF (b,d) soil columns under MF and BF stands from October 2018 to October 2022. For winter (from late November to early March), soil moisture is not included, due to soil freezing. The combined effects of soil temperature and soil moisture on daily CO2 emissions were fitted with multivariate regression curves. Legends with different gray scales represent the different ranges of soil CO2 emissions.
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Figure 6. Combined effects of soil temperature and moisture at 5 cm depth on daily CH4 fluxes from the MF (a,c) and BF (b,d) soil columns under MF and BF stands from October 2018 to October 2022. For winter (from late November to early March), soil moisture is not included, due to soil freezing. The combined effects of soil temperature and soil moisture on daily CH4 fluxes were fitted with multivariate linear regressions. Legends with different gray scales represent different ranges of soil CH4 fluxes.
Figure 6. Combined effects of soil temperature and moisture at 5 cm depth on daily CH4 fluxes from the MF (a,c) and BF (b,d) soil columns under MF and BF stands from October 2018 to October 2022. For winter (from late November to early March), soil moisture is not included, due to soil freezing. The combined effects of soil temperature and soil moisture on daily CH4 fluxes were fitted with multivariate linear regressions. Legends with different gray scales represent different ranges of soil CH4 fluxes.
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Figure 7. Relationships of soil temperature at 5 cm depth and daily CO2 emissions from the MF and BF soil columns under MF and BF stands during the non-growing season (a,b) and for the whole year (c,d) from October 2018 to October 2022. In winter (from late November to early March), soil temperature in soil columns for the measurement of CO2 emissions was collected with automatic monitoring of the soil temperature at 5 cm depth under the two forest stands.
Figure 7. Relationships of soil temperature at 5 cm depth and daily CO2 emissions from the MF and BF soil columns under MF and BF stands during the non-growing season (a,b) and for the whole year (c,d) from October 2018 to October 2022. In winter (from late November to early March), soil temperature in soil columns for the measurement of CO2 emissions was collected with automatic monitoring of the soil temperature at 5 cm depth under the two forest stands.
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Figure 8. Changes in average cumulative soil CO2 emissions (a,b) and CH4 fluxes (c,d) from the MF and BF soil columns under MF and BF stands during the non-growing and growing seasons and for the whole year from October 2018 to October 2022. NG and G represent non-growing and growing seasons, respectively. All signifies the whole year. Bars represent standard errors (n = 4). * p < 0.05.
Figure 8. Changes in average cumulative soil CO2 emissions (a,b) and CH4 fluxes (c,d) from the MF and BF soil columns under MF and BF stands during the non-growing and growing seasons and for the whole year from October 2018 to October 2022. NG and G represent non-growing and growing seasons, respectively. All signifies the whole year. Bars represent standard errors (n = 4). * p < 0.05.
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Figure 9. Conceptual model illustrating the effects of warming and cooling on soil cumulative CO2 emissions and CH4 uptake under MF and BF stands during the non-growing season (a) and across the year (b). Ta and Ts represent the average air temperature and soil temperature at 5 cm depth under MF and BF stands during the non-growing season and across the year from October 2018 to October 2022, respectively. Data in brackets indicate the percentile changes in soil cumulative CO2 emissions and CH4 uptake following the soil column translocation, relative to the soil columns incubated in situ. Upward and downward arrows represent the increase and decrease in cumulative CO2 emissions and CH4 uptake, respectively. * p < 0.05.
Figure 9. Conceptual model illustrating the effects of warming and cooling on soil cumulative CO2 emissions and CH4 uptake under MF and BF stands during the non-growing season (a) and across the year (b). Ta and Ts represent the average air temperature and soil temperature at 5 cm depth under MF and BF stands during the non-growing season and across the year from October 2018 to October 2022, respectively. Data in brackets indicate the percentile changes in soil cumulative CO2 emissions and CH4 uptake following the soil column translocation, relative to the soil columns incubated in situ. Upward and downward arrows represent the increase and decrease in cumulative CO2 emissions and CH4 uptake, respectively. * p < 0.05.
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MDPI and ACS Style

Xu, X.; Xu, T.; Yue, J. Effect of In Situ Large Soil Column Translocation on CO2 and CH4 Fluxes under Two Temperate Forests of Northeastern China. Forests 2023, 14, 1531. https://doi.org/10.3390/f14081531

AMA Style

Xu X, Xu T, Yue J. Effect of In Situ Large Soil Column Translocation on CO2 and CH4 Fluxes under Two Temperate Forests of Northeastern China. Forests. 2023; 14(8):1531. https://doi.org/10.3390/f14081531

Chicago/Turabian Style

Xu, Xingkai, Tingting Xu, and Jin Yue. 2023. "Effect of In Situ Large Soil Column Translocation on CO2 and CH4 Fluxes under Two Temperate Forests of Northeastern China" Forests 14, no. 8: 1531. https://doi.org/10.3390/f14081531

APA Style

Xu, X., Xu, T., & Yue, J. (2023). Effect of In Situ Large Soil Column Translocation on CO2 and CH4 Fluxes under Two Temperate Forests of Northeastern China. Forests, 14(8), 1531. https://doi.org/10.3390/f14081531

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