暖温带锐齿栎林土壤呼吸及微生物群落结构对土壤增温和降雨减少的响应
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摘要
气候变化是目前国际社会普遍关注的全球性问题。气候变暖及降水格局改变是气候变化的两大重要特征，并对陆地生态系统的碳循环过程及固碳潜力产生重大影响。因此，探讨气候变化背景下森林土壤碳库的变化规律，已成为当前土壤碳源—汇效应演化评价中的重大科学问题。掌握土壤呼吸对气候变暖与降雨减少的响应规律有助于评价土壤在碳收支过程中的源汇角色。本研究采用完全随机区组的试验设计方法在暖温带典型落叶阔叶林—锐齿栎林中开展了野外原位土壤增温与林下穿透雨减少的控制试验，并通过壕沟断根处理区分土壤异养呼吸与自养呼吸，以研究土壤呼吸及不同组分对土壤增温与降雨减少的响应规律，同时运用磷脂脂肪酸法测定土壤微生物群落结构，以分析其对气候变化的响应机理。主要研究结果如下：
(1)土壤增温与降雨减少显著改变土壤温度和湿度特征。红外辐射灯管加热导致林下土壤5cm日均温显著提高1.43-1.93℃，日均最高温的增加幅度高于最低温的增幅，白天的增温幅度高于夜晚；增温导致早春3月的土壤温度增幅最高。土壤增温与降雨减少均显著降低5cm土壤湿度(5.7-9.5%v/v)，6月份土壤湿度降幅最高。因此，本研究采用试验处理方法可有效增加土壤温度并减小土壤湿度。
(2)土壤增温与降雨减少显著提高锐齿栎林下土壤总呼吸速率。土壤总呼吸对土壤增温与降雨减少交互效应的响应程度显著高于单因子的主效应。在环境降雨条件下，土壤增温导致土壤总呼吸速率显著提高35.3%；非生长季和生长季分别显著提高23.1%和44.3%。然而，在降雨减少背景下，增温导致非生长季和生长季土壤总呼吸速率分别增加14.2%和减少0.65%，但未达显著水平。在环境温度背景下，降雨减少导致土壤呼吸速率显著增加20.5%；生长季土壤呼吸显著增加31.6%，但是在非生长季未达到显著水平。连续19个月的土壤呼吸观测表明，短期内土壤增温和降雨减少都促进生长季土壤总呼吸；此外土壤增温显著提高非生长季土壤总呼吸速率。增温与减雨导致土壤总呼吸的增加与提高的土壤微生物量碳氮以及土壤有机碳显著相关。该研究表明区域气候变暖以及降水减少会增加暖温带落叶阔叶林土壤碳排放潜力，进而对气候变化产生正反馈效应。
(3)土壤异养呼吸和自养呼吸对土壤增温与降雨减少的响应方式存在显著差异。土壤异养呼吸受增温主效应的显著影响。土壤增温导致观测期间异养呼吸显著提高27.8%；生长季和非生长季分别显著提高28.2%和27.4%。增温导致异养呼吸通量的显著增加与土壤微生物碳氮的上升显著相关。降雨减少则导致异养呼吸速率降低2.8%，生长季与非生长季均未达到显著水平。然而，在增温条件下，降雨减少导致土壤异养呼吸增加16.9%；并且生长季的增幅(22.6%)高于非生长季(9.3%)，但是与对照样地差异未达到显著水平。这表明土壤异养呼吸对温度的响应敏感性高于水分变化。
土壤自养呼吸受土壤增温与降雨减少交互效应的显著影响。环境降雨下，增温导致非生长季和生长季的自养呼吸分别增加20.1%和73.2%，后者达到显著差异；而在降雨减少条件下，增温导致非生长季和生长季自养呼吸分别下降28.6%和2.0%。环境温度下，降雨减少导致非生长季和生长季自养呼吸分别增加23.7%和89.2%，后者达显著水平。增温与减雨导致自养呼吸的增加与细根生物量的显著提高呈正相关。综上所述，可知降雨减少导致生长季土壤总呼吸的增加主要归因于土壤自养呼吸的增加；而增温引起的生长季总呼吸增加则是由异养和自养呼吸共同提高造成的。
(4)土壤呼吸及其不同组分的温度敏感性对土壤增温与降雨减少的响应方式差异显著。土壤总呼吸温度敏感性受增温主效应及其与降雨减少的交互效应显著影响。环境温度下，减雨导致总呼吸温度敏感性(2.73)显著提高；然而，增温条件下的减雨处理对总呼吸温度敏感性(2.64)无显著影响。环境降雨下，增温导致总呼吸温度敏感性(2.96)显著高于对照样地(2.22)。土壤增温与降雨减少对土壤异养呼吸温度敏感性无显著影响。自养呼吸温度敏感性则受增温与减雨的主效应和交互效应的显著影响。增温、减雨及增温与减雨均显著提高自养呼吸的温度敏感性(3.77，3.52，3.69)。不同处理下自养呼吸温度敏感均显著高于总呼吸和异养呼吸的温度敏感性。本研究还发现土壤不同组分呼吸的温度敏感性均随着土壤温度的增加而增加。这暗示呼吸温度敏感性随着区域气候变暖而呈增加趋势。
(5)土壤微生物群落结构对土壤增温与降雨减少的响应方式因断根与否而异。土壤增温、降雨减少及断根的交互效应对微生物PLFA影响程度高于单个因子的主效应。土壤增温与降雨减少显著提高未断根样地微生物总PLFA，细菌PLFA，真菌PLFA，革兰氏阴性菌PLFA(53.7-72.6)；然而对断根样地微生物PLFA无显著影响。因此，根系碳输入的减少(断根)降低了土壤微生物PLFA对增温与减雨的响应敏感敏感性，即根系碳输入对土壤微生物响应气候变化的方式有重要调节作用。减雨样地内断根处理导致土壤微生物多个类群PLFA显著低于未断根样地。这表明根系对微生物群落结构的影响还取决于土壤水分状况。对于微生物群落结构，增温减雨的双因子处理导致未断根样地细菌和革兰氏阳性菌丰富度的显著下降，这与细菌扩散及其养分吸收时对水分依赖的特殊性有关。然而在断根样地，增温处理显著提高革兰氏阳性菌的丰富度，双因子处理降低革兰氏阴性菌丰富度的同时增加放射线菌的丰富度。
Climate change is truly a global issue, which has got unprecedented concern and awareness across the international community. The climate warming and changing precipitation pattern, as two remarkable features of climate change, exert a strong effect on terrestrial ecosystem carbon cycle and carbon sequestration. Hence, understanding the feedback of soil carbon in forest ecosystems to climate change is necessary when we assess the role of soil carbon in sink-source transition. Quantifying the response magnitudeof soil respiration to climate warming and precipitation pattern change will be helpful in evaluating soil carbon balance and budget. In this study, a field experiment based on
a randomized complete block design was conducted with soil warming (W) and throughfall exclusion (TE)(the factorial combinations of soil warming with throughfall exclusion) in a temperate oak (Quercus aliena var. acuteserrata) forest in centre China. Combined with plot trenching, we examined how soil warming and throughfall exclusion influence the soil respirations from different components and corresponding temperature sensitivities. Phospholipid fatty acids (PLFAs) analysis was used to characterize soil microbial community, and its response to soil warming and throughfall exclusion was further
analyzed. The main results are as follows:
(1) Soil temperature and moisture at5cm were significantly altered by simulated soil warming and throughfall exclusion. Soil warming through infrared heaters significantly increased soil temperature by1.43-1.93℃, with higher increment in daily mean maximum soil temperature compared to mean minimum temperature. Besides, diurnal soil temperature increased greater than that in night. Enhancement of soil temperature resulted
from experimental warming in early spring was higher than those in other seasons. Soil moisture was significantly decreased by5.7-9.5v/v under soil warming and throughfall exclusion treatments, with the maximum reduction in June. Therefore, increased tempe rature and decreased precipitation can be imitated through infrared heater and throughfall exclusion.
(2) Soil warming and throughfall exclusion significantly increase total soil respirations. Significant interactive effects relative to main ones of soil warming and throughfall
exclusion were found on soil respirations. Soil warming significantly elevated soil respirations by35.3%in ambient precipitation plots, with23.1%and44.3%increments inungrowing and growing season, respectively. However, soil respirations were not significantly affected (+14.2%,-0.65%) by soil warming in both growing and ungrowing season under throughfall exclusion. Throughfall exclusion significantly increased soil respirations by20.5%under ambient temperature, with significant increases (31.6%) in growing
season. The finding from the data of continuous19months indicated that soil warming and throughfall exclusion can stimulate soil respirations in growing season. Besides, soil warming also increased soil respirations in ungrowing season. Increases of soil respiration by treatments are mainly resulted from the elevated soil microbial biomass carbon and soil organic carbon. The study indicates that regional climate warming and precipitation reduction may promote the emission potencial of soil carbon and act as a positive feedback to cliamte change.
(3) There were significant differences in the response patterns of soil heterotrophic
respiration (RH) and autotrophic respiration (RR) to soil warming and throughfall exclusion. RHwas signficantly affected by the main effect of soil warming. RHwas significantly elevated by27.8%during the whole period, and signficantly increased by28.2%and27.4%in growing and ungrowing season, respectively. The enhancement of RHwas
positively correlated with soil microbial carbon and nitrogen. Throughfall exclusion decreased RHby2.8%in ambient temperature, without significant difference in both growing and ungrowing season. However, RHwas stimulated by16.9%under througfall exclusion with warming, with higher increases in growing season (22.6%) than that in ungr owing season(9.3%). The results implied that RHis more sensitive to soil temperature than soil water availability changes.
Warming significantly interacted with the throughfall exclusion in terms of their effects on RR.Soil warming enhanced RRby20.1%and73.2%under ambient preciptation in ungrowing and growing season,respectively, but reduced it by28.6%and2.0%under precipitation exclusion treatment in ungrowing and growing season. RRwas increased by23.7%and89.2%by throughfall exclusion in ungrowing and growing season under ambient temperature, respectively. Increases of RRinduced by warming and decreased precipitation were positively correlated to fine root biomass. Our experiment indicates
that increases of soil respirations under througfall exclusion treatment were mainly induced by the enhancement of autotrophic respiration, while that under soil warming was
resulted from both RHand RR.
(4) There were significant differences in the response of temperature sensitivity (Q10) for soil respirations and different components to soil warming and throughfall exclusion. Q10of soil total respirations was significantly influenced by the main effect of warming and its interaction with throughfall exclusion. Throughfall exclusion significantly increased Q10of RS(2.73) in ambient temperature, but had no significant effects on it(2.64) under warming treatment. Q10of RSunder warming treatment in ambient precipitation was significantly higher than that under ambient temperature (2.22). Both soil warming and throughfall exclusion had no significant effects on Q10of RH. Q10of RRwas
significantly elevated by soil warming and throughfall exclusion and their interaction(3.77,3.52and3.69). RRhad a significantly greater Q10than those of RSand RHunder all treatments. Moreover, Q10of all respiration components increases with elevated soil temperature,which implies that Q10of soil respiration may increase under global warming.
(5) Response of soil microbial community to soil warming and precipitation varies
with trench treatment. Interactive effects of soil warming, throughfall exclusion and tre nch significantly influenced microbial PLFA relative to main effects of single environmental factor. In untrenched plots, single factor of soil warming and throughfall exclusion
significantly elevated microbial total PLFA, bacterial PLFA, fungal PLFA, and gram-negative bacterial PLFA by53.7-72.6%. However, both warming and decreased precipitation had no effects on microbial PLFA in trenched plots. These findings indicate that thesensitivity of microbial PLFA to climate change in untrenched plots was greater than that in trenched plots. Besides, trench treatment resulted in significant reduction in microbial PLFA under throughfall exclusion. In terms of microbial community structure, however, combination of soil warming and throughfall exclusion significantly decreased bacterial and gram-positive bactierial relative abundance in untrenched plots, which may be
explained by the dependence of bacterial on soil water availability. In trenched plots,soil warming significantly increased gram-positive bacterial abundance under ambient precipitation, while combination of soil warming and throughfall exclusion reduced abundance of gram-negative bacterial, but increase abundance of actinomycosis.
(1)土壤增温与降雨减少显著改变土壤温度和湿度特征。红外辐射灯管加热导致林下土壤5cm日均温显著提高1.43-1.93℃，日均最高温的增加幅度高于最低温的增幅，白天的增温幅度高于夜晚；增温导致早春3月的土壤温度增幅最高。土壤增温与降雨减少均显著降低5cm土壤湿度(5.7-9.5%v/v)，6月份土壤湿度降幅最高。因此，本研究采用试验处理方法可有效增加土壤温度并减小土壤湿度。
(2)土壤增温与降雨减少显著提高锐齿栎林下土壤总呼吸速率。土壤总呼吸对土壤增温与降雨减少交互效应的响应程度显著高于单因子的主效应。在环境降雨条件下，土壤增温导致土壤总呼吸速率显著提高35.3%；非生长季和生长季分别显著提高23.1%和44.3%。然而，在降雨减少背景下，增温导致非生长季和生长季土壤总呼吸速率分别增加14.2%和减少0.65%，但未达显著水平。在环境温度背景下，降雨减少导致土壤呼吸速率显著增加20.5%；生长季土壤呼吸显著增加31.6%，但是在非生长季未达到显著水平。连续19个月的土壤呼吸观测表明，短期内土壤增温和降雨减少都促进生长季土壤总呼吸；此外土壤增温显著提高非生长季土壤总呼吸速率。增温与减雨导致土壤总呼吸的增加与提高的土壤微生物量碳氮以及土壤有机碳显著相关。该研究表明区域气候变暖以及降水减少会增加暖温带落叶阔叶林土壤碳排放潜力，进而对气候变化产生正反馈效应。
(3)土壤异养呼吸和自养呼吸对土壤增温与降雨减少的响应方式存在显著差异。土壤异养呼吸受增温主效应的显著影响。土壤增温导致观测期间异养呼吸显著提高27.8%；生长季和非生长季分别显著提高28.2%和27.4%。增温导致异养呼吸通量的显著增加与土壤微生物碳氮的上升显著相关。降雨减少则导致异养呼吸速率降低2.8%，生长季与非生长季均未达到显著水平。然而，在增温条件下，降雨减少导致土壤异养呼吸增加16.9%；并且生长季的增幅(22.6%)高于非生长季(9.3%)，但是与对照样地差异未达到显著水平。这表明土壤异养呼吸对温度的响应敏感性高于水分变化。
土壤自养呼吸受土壤增温与降雨减少交互效应的显著影响。环境降雨下，增温导致非生长季和生长季的自养呼吸分别增加20.1%和73.2%，后者达到显著差异；而在降雨减少条件下，增温导致非生长季和生长季自养呼吸分别下降28.6%和2.0%。环境温度下，降雨减少导致非生长季和生长季自养呼吸分别增加23.7%和89.2%，后者达显著水平。增温与减雨导致自养呼吸的增加与细根生物量的显著提高呈正相关。综上所述，可知降雨减少导致生长季土壤总呼吸的增加主要归因于土壤自养呼吸的增加；而增温引起的生长季总呼吸增加则是由异养和自养呼吸共同提高造成的。
(4)土壤呼吸及其不同组分的温度敏感性对土壤增温与降雨减少的响应方式差异显著。土壤总呼吸温度敏感性受增温主效应及其与降雨减少的交互效应显著影响。环境温度下，减雨导致总呼吸温度敏感性(2.73)显著提高；然而，增温条件下的减雨处理对总呼吸温度敏感性(2.64)无显著影响。环境降雨下，增温导致总呼吸温度敏感性(2.96)显著高于对照样地(2.22)。土壤增温与降雨减少对土壤异养呼吸温度敏感性无显著影响。自养呼吸温度敏感性则受增温与减雨的主效应和交互效应的显著影响。增温、减雨及增温与减雨均显著提高自养呼吸的温度敏感性(3.77，3.52，3.69)。不同处理下自养呼吸温度敏感均显著高于总呼吸和异养呼吸的温度敏感性。本研究还发现土壤不同组分呼吸的温度敏感性均随着土壤温度的增加而增加。这暗示呼吸温度敏感性随着区域气候变暖而呈增加趋势。
(5)土壤微生物群落结构对土壤增温与降雨减少的响应方式因断根与否而异。土壤增温、降雨减少及断根的交互效应对微生物PLFA影响程度高于单个因子的主效应。土壤增温与降雨减少显著提高未断根样地微生物总PLFA，细菌PLFA，真菌PLFA，革兰氏阴性菌PLFA(53.7-72.6)；然而对断根样地微生物PLFA无显著影响。因此，根系碳输入的减少(断根)降低了土壤微生物PLFA对增温与减雨的响应敏感敏感性，即根系碳输入对土壤微生物响应气候变化的方式有重要调节作用。减雨样地内断根处理导致土壤微生物多个类群PLFA显著低于未断根样地。这表明根系对微生物群落结构的影响还取决于土壤水分状况。对于微生物群落结构，增温减雨的双因子处理导致未断根样地细菌和革兰氏阳性菌丰富度的显著下降，这与细菌扩散及其养分吸收时对水分依赖的特殊性有关。然而在断根样地，增温处理显著提高革兰氏阳性菌的丰富度，双因子处理降低革兰氏阴性菌丰富度的同时增加放射线菌的丰富度。
Climate change is truly a global issue, which has got unprecedented concern and awareness across the international community. The climate warming and changing precipitation pattern, as two remarkable features of climate change, exert a strong effect on terrestrial ecosystem carbon cycle and carbon sequestration. Hence, understanding the feedback of soil carbon in forest ecosystems to climate change is necessary when we assess the role of soil carbon in sink-source transition. Quantifying the response magnitudeof soil respiration to climate warming and precipitation pattern change will be helpful in evaluating soil carbon balance and budget. In this study, a field experiment based on
a randomized complete block design was conducted with soil warming (W) and throughfall exclusion (TE)(the factorial combinations of soil warming with throughfall exclusion) in a temperate oak (Quercus aliena var. acuteserrata) forest in centre China. Combined with plot trenching, we examined how soil warming and throughfall exclusion influence the soil respirations from different components and corresponding temperature sensitivities. Phospholipid fatty acids (PLFAs) analysis was used to characterize soil microbial community, and its response to soil warming and throughfall exclusion was further
analyzed. The main results are as follows:
(1) Soil temperature and moisture at5cm were significantly altered by simulated soil warming and throughfall exclusion. Soil warming through infrared heaters significantly increased soil temperature by1.43-1.93℃, with higher increment in daily mean maximum soil temperature compared to mean minimum temperature. Besides, diurnal soil temperature increased greater than that in night. Enhancement of soil temperature resulted
from experimental warming in early spring was higher than those in other seasons. Soil moisture was significantly decreased by5.7-9.5v/v under soil warming and throughfall exclusion treatments, with the maximum reduction in June. Therefore, increased tempe rature and decreased precipitation can be imitated through infrared heater and throughfall exclusion.
(2) Soil warming and throughfall exclusion significantly increase total soil respirations. Significant interactive effects relative to main ones of soil warming and throughfall
exclusion were found on soil respirations. Soil warming significantly elevated soil respirations by35.3%in ambient precipitation plots, with23.1%and44.3%increments inungrowing and growing season, respectively. However, soil respirations were not significantly affected (+14.2%,-0.65%) by soil warming in both growing and ungrowing season under throughfall exclusion. Throughfall exclusion significantly increased soil respirations by20.5%under ambient temperature, with significant increases (31.6%) in growing
season. The finding from the data of continuous19months indicated that soil warming and throughfall exclusion can stimulate soil respirations in growing season. Besides, soil warming also increased soil respirations in ungrowing season. Increases of soil respiration by treatments are mainly resulted from the elevated soil microbial biomass carbon and soil organic carbon. The study indicates that regional climate warming and precipitation reduction may promote the emission potencial of soil carbon and act as a positive feedback to cliamte change.
(3) There were significant differences in the response patterns of soil heterotrophic
respiration (RH) and autotrophic respiration (RR) to soil warming and throughfall exclusion. RHwas signficantly affected by the main effect of soil warming. RHwas significantly elevated by27.8%during the whole period, and signficantly increased by28.2%and27.4%in growing and ungrowing season, respectively. The enhancement of RHwas
positively correlated with soil microbial carbon and nitrogen. Throughfall exclusion decreased RHby2.8%in ambient temperature, without significant difference in both growing and ungrowing season. However, RHwas stimulated by16.9%under througfall exclusion with warming, with higher increases in growing season (22.6%) than that in ungr owing season(9.3%). The results implied that RHis more sensitive to soil temperature than soil water availability changes.
Warming significantly interacted with the throughfall exclusion in terms of their effects on RR.Soil warming enhanced RRby20.1%and73.2%under ambient preciptation in ungrowing and growing season,respectively, but reduced it by28.6%and2.0%under precipitation exclusion treatment in ungrowing and growing season. RRwas increased by23.7%and89.2%by throughfall exclusion in ungrowing and growing season under ambient temperature, respectively. Increases of RRinduced by warming and decreased precipitation were positively correlated to fine root biomass. Our experiment indicates
that increases of soil respirations under througfall exclusion treatment were mainly induced by the enhancement of autotrophic respiration, while that under soil warming was
resulted from both RHand RR.
(4) There were significant differences in the response of temperature sensitivity (Q10) for soil respirations and different components to soil warming and throughfall exclusion. Q10of soil total respirations was significantly influenced by the main effect of warming and its interaction with throughfall exclusion. Throughfall exclusion significantly increased Q10of RS(2.73) in ambient temperature, but had no significant effects on it(2.64) under warming treatment. Q10of RSunder warming treatment in ambient precipitation was significantly higher than that under ambient temperature (2.22). Both soil warming and throughfall exclusion had no significant effects on Q10of RH. Q10of RRwas
significantly elevated by soil warming and throughfall exclusion and their interaction(3.77,3.52and3.69). RRhad a significantly greater Q10than those of RSand RHunder all treatments. Moreover, Q10of all respiration components increases with elevated soil temperature,which implies that Q10of soil respiration may increase under global warming.
(5) Response of soil microbial community to soil warming and precipitation varies
with trench treatment. Interactive effects of soil warming, throughfall exclusion and tre nch significantly influenced microbial PLFA relative to main effects of single environmental factor. In untrenched plots, single factor of soil warming and throughfall exclusion
significantly elevated microbial total PLFA, bacterial PLFA, fungal PLFA, and gram-negative bacterial PLFA by53.7-72.6%. However, both warming and decreased precipitation had no effects on microbial PLFA in trenched plots. These findings indicate that thesensitivity of microbial PLFA to climate change in untrenched plots was greater than that in trenched plots. Besides, trench treatment resulted in significant reduction in microbial PLFA under throughfall exclusion. In terms of microbial community structure, however, combination of soil warming and throughfall exclusion significantly decreased bacterial and gram-positive bactierial relative abundance in untrenched plots, which may be
explained by the dependence of bacterial on soil water availability. In trenched plots,soil warming significantly increased gram-positive bacterial abundance under ambient precipitation, while combination of soil warming and throughfall exclusion reduced abundance of gram-negative bacterial, but increase abundance of actinomycosis.
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