工业革命以来, 由于人类活动加剧导致大气中温室气体浓度不断升高, 由此引发的全球变暖已经成为不争的事实。根据IPCC评估报告预测到21世纪末全球地表平均温度将上升0.3-4.8 ℃ (IPCC, 2013)。气候变暖直接影响陆地生态系统的结构和功能, 进而改变生态系统碳循环的各个过程, 如光合作用、土壤呼吸、凋落物分解、细根动态、植物生产力等(Kirschbaum, 2004; Loik et al., 2004; Majdi & Öhrvik, 2004; 徐小锋等, 2007; Xu et al., 2010; 李晓杰等, 2017)。此外, 由于温度变化引起的植物生长节律、群落物种组成和结构、养分循环的改变亦会间接影响上述碳循环过程(Niu et al., 2010; Yu et al., 2010), 进而对全球气候变化产生强烈的反馈作用。
根系是连接植物地上地下的重要器官, 根系通过吸收土壤水分和养分满足植物生长(张小全和吴可红, 2001), 并且能够储存碳水化合物, 且根系通过不断的生长、死亡、周转和分解过程参与生态系统的物质交换和能量流动, 驱动生态系统的碳氮循环(卫星等, 2008; Yin et al., 2014)。根据Jackson等(1997)对全球不同植被的估计, 仅小于2 mm细根的周转, 每年要消耗全球陆地生态系统净初级生产力的30%以上, 且细根通过周转每年向地下输入有机物占总输入的50%左右(Wan et al., 2004)。另外, 细根分解后能够输送大量的有机质和养分进入土壤, 每年对土壤碳库的贡献率达25%-80% (Eldhuset et al., 2006; Sun et al., 2013)。资源在粗根和细根间的分配权衡是植物重要的生存策略, 体现着植物对环境变化的适应能力。粗根不仅对植物生长起支撑作用, 而且也在碳存储中扮演重要角色, 并且粗根生物量的增加有利于植物根系向深层分布以维持植物的正常生长(闫慧等, 2014)。同样, 根冠比是植物长期适应自然选择的结果(毛晋花等, 2018), 在一定程度上可反映植物在响应全球变化时采取的策略方式。 植物根系在调节陆地生态系统对气候变暖的响应中起着重要作用, 因此, 研究根系对气候变暖的响应, 对于理解陆地生态系统碳动态及其对气候变化的反馈至关重要。
温度上升对根系的影响体现在多个方面。首先, 气候变暖直接影响植物光合速率, 改变植物物候, 延长植物的生长季(叶旺敏等, 2019), 进而影响根系生物量; 其次, 温度能够影响土壤动物及微生物的数量和活性、土壤有机质的分解速率以及养分可利用性导致根系生物量发生改变(Bradford et al., 2016; Li et al., 2020); 再者, 温度升高会导致土壤水分含量的降低(Gimbel et al., 2015), 使土壤水分成为根系生长的限制因子, 植物为获取足够水分会增加根系的长度或密度, 导致根系生物量以及植物根冠比发生变化(Joslin et al., 2000; 尹华军等, 2008)。然而, 已有的研究表明根系生物量对温度升高的响应并不一致, 不同生态系统根系生物量对增温响应表现为增加(Hollister & Flaherty, 2010)、不变(Volder et al., 2004; Tokida et al., 2011)或减少(Zhou et al., 2011; Coldren et al., 2016)。增温幅度、增温年限、增温方式会对植物生长产生影响。例如, Usami等(2001)的结果表明增温4.5 ℃使温带森林根系生物量增加了25%, Zhou等(2011)发现增温5 ℃使哈佛森林根系生物量降低约40%, 而Han等(2018)发现增温3 ℃对温带森林根系生物量无影响。Wang等(2021)的整合分析表明增温促进了细根生物量和生产力, 随着增温幅度增加, 增温对细根生物量的影响减弱, 并且细根生物量受到增温幅度和增温年限的共同作用。另外, 本底环境也影响着增温效应, 增温对根系生物量的促进作用在湿润的生态系统更明显(Wan et al., 2004), 而在干旱生态系统, 温度升高引起的水分胁迫有可能会抑制根系生长(Bai et al., 2010)。尽管如此, 增温如何影响根系生物量及其机制还存在很大的不确定性。
本研究基于野外增温控制实验, 采用整合分析的方法, 从151篇已发表的国内外论文中收集到611组数据, 探究增温对根系生物量(总生物量、细根生物量、粗根生物量、根冠比)的影响; 通过亚组分析揭示根系生物量对增温幅度、增温年限、增温方式的响应以及不同生态系统类型之间的差异; 阐明增温对根系生物量的影响及机制, 为理解气候变暖背景下土壤碳动态和生态系统过程的变化提供理论依据。
1 材料和方法
1.1 文献选择与数据库建立
数据来源于Web of Science、Google Scholar、CNKI等中英文期刊数据库, 搜索的关键词包括: climate change、experimental warming、warming、temperature、biomass、root biomass、underground、belowground、fine root biomass、fine root。共收集到151篇已发表的国内外文献, 包括了611个配对的观测值(对照和增温处理)用于整合分析。所选用的文献须符合以下标准: (1)所选研究必须设有对照组和处理组, 均为野外田间实验; (2)对于同一研究, 实验开始前其对照组和处理组均属于同一生态系统且具有相同的气候、土壤条件; (3)对于多年实验收集全部观测结果, 并将每一年结果作为独立变量, 同一年内多次测定的变量采用平均值进行计算; (4)对于研究中包括模拟增温处理的多因素控制实验, 只选择对照组和模拟增温处理组数据; (5)所选研究对照组和处理组的平均值、样本量、标准差或标准误可以直接从文中获得或者从图表中提取。使用GetData v2.22 (
收集的变量包括: 根系总生物量(TRB), 细根生物量(FRB), 粗根生物量(CRB), 根冠比(R/S)。其中细根为直径小于2 mm的根系。同时收集每项研究实验地的经纬度、海拔、年降水量(MAP)、年平均气温(MAT)、生态系统类型、增温幅度、增温年限以及增温方式。根据数据结构将数据进行如下分组: 增温幅度(≤1 ℃、1-2 ℃、≥2 ℃); 增温年限(≤2年、2-5年、≥5年); 增温方式(开顶箱、红外辐射、电缆加热、温室增温、反射), 生态系统类型(农田、森林、草地、苔原、湿地)。所收集研究点的纬度跨度从42.70° S到78.17° N, 年平均气温范围为-12-28 ℃, 年降水量范围为114-2 418 mm。图1为本研究所涉及研究点的分布情况。
图1
图1
整合分析中研究点的全球分布。
Fig. 1
Global distribution of study sites in the meta-analysis.
1.2 整合分析
本文运用R 4.0.3 (
式中, Xt、Xc分别表示一个独立研究中处理组和对照组的平均值。整合分析研究中, 单个研究的加权方式对效应值的影响极大, 以往研究多采用样本方差或者标准差进行加权, 但这会提高个别观测值的重要性, 从而导致效应值受到很大影响。因此, 本研究采用处理组和对照组的样本量进行加权(Zhang et al., 2018):
式中, Wrr表示每一观测效应值的权重, Nc、Nt分别表示对照组和处理组的样本量。对于每个观测值, 使用以下模型(公式(3))检测ln RR是否与0重叠以及ln RR是否受增温幅度、增温年限、增温方式及生态系统类型等因素的影响, 并将不同研究多年实验的每一年结果作为独立变量检验增温年限对根系生物量的影响, 在混合效应模型中将每个研究作为随机变量考虑其随机效应。
式中, β为系数, πstudy为观测值的随机效应, ɛ是样本误差, M为增温幅度, D为增温年限, ME为增温方式, E为生态系统类型。β0为总体效应值, β1为增温幅度的效应值, β2为增温年限的效应值, β3为增温方式的效应值, β4为生态系统类型的效应值, 其中干旱指数(年降水量/年蒸发量)通过CGIAR-CSI全球干旱数据库获得(Zomer et al., 2008)。为了便于解释, 将ln RR及其对应的置信区间(CI)转换为相应的百分比变化。
2 结果和分析
2.1 根系生物量对模拟增温的响应
图2
图2
模拟增温对根系总生物量(TRB)、细根生物量(FRB)、粗根生物量(CRB)、根冠比(R/S)的影响。右侧数字代表样本量, 误差线代
Fig. 2
Effects of simulated warming (ln RR) on total root biomass (TRB), fine root biomass (FRB), coarse root biomass (CRB), and root:shoot ratio (R/S). The values within the graphic panel show the sample sizes for each of the variables. Error bars represent 95% confidence intervals. Solid circle represent significant warming effects (p < 0.05), and hollow circles indicate insignificant warming effects.
2.2 根系生物量对增温幅度、增温年限、增温方式的响应
图3
图3
模拟增温对根系总生物量(A)、细根生物量(B)、粗根生物量(C)、根冠比(D)的影响与增温幅度、增温年限、增温方式、生态系统类型的关系。右侧数字代表样本量, 误差线代
Fig. 3
Effects of simulated warming (ln RR) on total root biomass (A), fine root biomass (B), coarse root biomass (C) and root:shoot ratio (D) in relation to the magnitude, duration and method of warming and ecosystem types. The values within the graphic panels show the sample sizes for each of the variables. Error bars represent 95% confidence intervals. Solid circles represent significant warming effects (p < 0.05), and hollow circles indicate insignificant warming effects. OTC, open top container.
根系生物量对增温持续时间的响应也不一致, 其中短期增温和中期增温能够提高根系总生物量和粗根生物量, 相反, 长期增温对二者起抑制作用, 但影响均不显著。相比短期和中期增温提高根系生物量, 长期增温使细根生物量有降低趋势(p > 0.05)。
2.3 根系生物量对模拟增温的响应与环境因子的关系
表1 模拟增温对根系总生物量(TRB)、细根生物量(FRB)、粗根生物量(CRB)、根冠比(R/S)的影响(ln RR)与年平均气温(MAT)、年降水量(MAP)、干旱指数(AI)的关系
Table 1
| 根系生物量效应值 Effect size of root biomass | MAT | MAP | AI | ||||||
|---|---|---|---|---|---|---|---|---|---|
| df | F | p | df | F | p | df | F | p | |
| TRB | 113 | 0.235 2 | 0.603 | 113 | 1.110 7 | 0.187 | 113 | 2.597 4 | 0.110 |
| FRB | 360 | 34.760 0 | 0.000*** | 360 | 43.652 0 | 0.000*** | 360 | 16.726 0 | 0.000*** |
| CRB | 26 | 0.082 6 | 0.776 | 26 | 1.400 2 | 0.248 | 26 | 3.448 9 | 0.075 |
| R/S | 108 | 2.766 0 | 0.099 | 108 | 0.103 0 | 0.749 | 108 | 0.109 4 | 0.742 |
***, p < 0.001.
图4
图4
增温对细根生物量的影响(ln RR)与年平均气温(MAT)(A)、年降水量(MAP)(B)、干旱指数(AI)(C)的关系。
Fig. 4
Effect of simulated warming (ln RR) on fine-root biomass in relation to mean annual air temperature (MAT)(A), mean annual precipitation (MAP)(B), and aridity index (AI)(C).
3 讨论
3.1 模拟增温对根系生物量的影响
本研究结果表明, 模拟增温对陆地生态系统根系生物量具有促进作用, 且主要体现在细根生物量, 这与Wang等(2021)整合分析的结果一致。增温显著增加了陆地生态系统细根生物量, 表明细根对气候变暖敏感性更高。增温对细根的促进作用主要有以下几个方面的原因。首先, 增温能够延长植物的生长季(Zhao et al., 2017), 对植物根系产生直接影响; 其次, 相比粗根, 细根对环境的变化更敏感(Leppälammi-Kujansuu et al., 2013), Wan等(2004)和Bai等(2010)研究结果均表明细根生物量会随土壤温度升高而增加, 而模拟增温能够提高土壤温度; 再者, 实验增温会导致植物蒸发量增加引起土壤水分的降低(Chen et al., 2016), 细根是植物吸收水分的主要器官, 因此会增加细根生物量来缓解水分限制; 此外, 土壤氮有效性也是影响细根生物量的重要原因, 已有研究表明模拟增温能够使土壤氮矿化速率提高46%, 土壤氮含量增加能够提高细根生物量(Rustad et al., 2001; Lee et al., 2007)。
环境因子的改变会影响植物生物量的分配模式(Domisch et al., 2002), 本研究结果表明增温未改变植物地上、地下分配, 这可能是植物本身通过地上和地下生长协同变化共同抵御外界温度的升高, 增温促进植物地上部分生长, 因此需要更多水分、养分维持植物地上生长, 从而导致植物地下生物量增加, 故而未改变植物根冠比。
3.2 增温幅度、增温年限、增温方式对根系生物量的影响
Rustad等(2001)和Lin等(2010)的整合分析表明, 陆地植物生物量对不同幅度增温的响应没有差异。但本研究发现中等强度(1-2 ℃)增温显著增加细根生物量, 与高强度增温相比, 中等强度增温对土壤温度和土壤水分的影响较小。Li等(2011)在青藏高原高寒草甸的模拟增温结果表明, 当增温幅度为5.16 ℃时土壤水分减少了7.7%, 而当增温幅度为2.59 ℃时土壤水分只减少1.8%, 在西藏高山生态系统的研究发现, 土壤温度升高1.52 ℃不会显著影响土壤水分, 而土壤温度升高1.98 ℃则使得土壤水分显著降低了16.1% (Zhong et al., 2016)。由此可知, 较高的增温幅度导致土壤水分大幅度降低可能会加重水分胁迫, 抑制细根的生长。本研究发现不同增温年限对根系生物量的影响均不显著, 与中短期增温相反, 长期增温对细根生物量产生一定的抑制作用, 这可能是由于长期增温后导致植物群落结构发生改变, 将会导致根系深度或根系碳分配发生变化(Liu et al., 2018), 进而影响细根生物量。
由于增温装置在设计、技术和增温原理上的差别, 可能会导致植物对模拟增温的响应并不相同(牛书丽等, 2007)。目前, 采用的增温装置主要分为主动增温和被动增温两类, 土壤加热管道、电缆加热和红外线辐射器属于主动增温装置, 而开顶式生长箱、温室和反射属于被动增温装置(甘琦杰等, 2021)。本研究发现开顶式生长箱和红外线辐射器两种增温装置能够显著提高细根生物量。开顶箱增温原理如同温室效应, 降低了风速, 减弱了空气流动强度, 使得生长箱内热量不容易散失, 形成较为稳定的增温环境, 温度升高通常会导致开顶式生长箱内水分蒸发增强, 导致生长箱内空气湿度降低, 利于植物根系生长(杨兵等, 2010; 朱彪和陈迎, 2020)。红外辐射技术利用红外线的电磁辐射热传递, 以辐射方式传递热量而达到增温的目的, 红外辐射装置可以使整个系统增温(侯彦会等, 2013), 从而使土壤温度升高, 提高根系呼吸速率, 促进根系生长。本研究发现电缆加热导致细根生物量和粗根生物量显著降低, 原因在于电缆加热直接作用于土壤, 地表蒸散作用加剧, 引起土壤湿度的降低比其他增温方式更为显著, 而根系生长易受到水分胁迫, 导致生物量降低。同时本研究发现电缆加热对细根生物量影响程度大于粗根生物量, 可能是因为粗根起到运输根的作用, 其木质化程度较高, 对土壤温度和水分变化的响应不如细根明显。
3.3 根系生物量对模拟增温的响应与本底环境条件的关系
本研究发现增温显著提高苔原生态系统细根生物量, 这与Zamin等(2014)在北极苔原地区的研究结果一致。首先, 高纬度地区生态系统中的植物主要受低温限制, 因此比低纬度地区的植物更容易受到温度的影响(Parmesan, 2007), 增温缓解了苔原地区植物的低温限制, 提高了土壤微生物的活性, 加快根系周转, 从而对根系生长起促进作用。Lin等(2010)的整合分析也表明高纬度苔原生态系统比低纬度的草原和森林生态系统受气候变暖的影响更大。其次, 在苔原生态系统中通过模拟增温提高了环境温度, 较高的温度会延长植物的生长期, 从而提高植物的生产力, 增加植物地下分配, 导致细根生物量增加。
本研究发现细根生物量对模拟增温的响应随着年平均气温、年降水量和干旱指数增加而逐渐降低。这表明寒冷地区, 如北极苔原生态系统, 易受到低温限制, 而增温可以延长植物的生长季, 促进地下生物量的增加(Zamin et al., 2014)。Malhotra等(2020)在SPRUCE泥炭地进行的模拟增温实验结果表明, 增温引起植物细根生物量显著提高与土壤干旱有关, 由于水分或养分的限制, 相比地上部分, 植物增加了地下细根的投资。相反, 在热带地区, 如热带雨林水热条件较好, 环境温度较高, 模拟增温对该地区植物根系产生的效应较小。
增温对细根生物量的促进作用在干旱地区更明显, 干旱地区通常年降水量和干旱指数较小, 土壤水分是影响植物生长的主要限制因素, 对干旱地区增温后易造成土壤干旱, 植物为获得足够水分及养分会增加对地下部分的投资, 提高根系生物量; 而在湿润地区, 模拟增温引起的水分变化可能并没有产生水分胁迫, 因此对细根生长的影响较小。Song等(2019)的研究结果表明增温提高干旱地区的根冠比, 说明在干旱地区增温能够提高植物对根系的投资, 而在湿润地区增温则提高了植物对地上茎的投资。
4 结论
(1)模拟增温显著提高了细根生物量, 并且细根生物量对增温的响应受本底环境的影响。增温对细根的促进作用在寒冷、干旱的地区更明显。
(2)增温对根系生物量的影响受增温幅度、增温年限、增温方式的影响。中等强度增温(1-2 ℃)显著增加细根生物量, 中短期(<5年)增温实验促进根系生物量, 而长期(≥5年)实验使得根系生物量有降低趋势。
(3)电缆加热引起的土壤干旱程度高于开顶箱和红外辐射增温这两种增温方式, 从而导致根系生物量降低, 表明在评估增温对根系的影响时需考虑不同增温装置的差异。
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Fig 1
表1
