2022, Vol. 59
2. 土壤与农业可持续发展国家重点实验室(中国科学院南京土壤研究所), 南京 210008
2. State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China
氧化亚氮（N2O）是重要的温室气体之一，在大气中的滞留时间长达114年，百年尺度增温潜势是二氧化碳（CO2）的265倍[1–2]。全球N2O-N排放量已从工业革命前的10~12 Tg·a–1增至目前的17 Tg·a–1，这主要是由于农业生产造成的[3]。据估算，农田土壤对工业革命以来全球陆地生态系统N2O排放量增长的贡献率高达82%[4]。在土壤中，N2O可通过多种生物和非生物过程产生，主要包括硝化作用、反硝化作用、硝酸盐异化还原成铵等。这些过程受多种因素的影响，如气象条件、土壤性质、田间管理措施等。在不同土壤和不同尺度下，控制N2O产生的因素不同，因此N2O的排放表现出较大的时空变异，极大增加了N2O排放量估算的不确定性和定量减排的挑战性[5]。
位于东北地区的黑土素以肥力高著称，是我国土壤有机碳（Soil organic carbon，SOC）含量最高的旱地土壤类型，主要分布在黑龙江、吉林、辽宁北部和内蒙古呼伦贝尔地区。黑土区耕地面积占全国总面积的1/7，粮食产量占全国总产量的1/4，对我国的粮食安全有举足轻重的作用。但是近几十年，黑土SOC含量不断下降，土壤肥力显著降低[6–8]。为保证作物的持续高产，高量投入氮肥；但较高的氮肥施用导致N2O排放量增加[4]。Shang等[9]研究发现，与1990—2003年相比，2004—2014年我国农田N2O排放量的年增速显著下降，但是黑土主要分布区的黑龙江省则表现为显著增加。Chen等[10]建立了全球尺度黑土N2O排放数据库，构建了包含降水量和氮肥用量的N2O排放模型，估算我国东北黑土N2O-N排放总量为30.0 Gg·a–1，其中化肥诱导的N2O-N排放量（不包括背景排放量）为20.6 Gg·a–1。Yue等[11]基于作物类型估算了我国农田系统化肥诱导的N2O-N排放总量为194 Gg·a–1，其中东北地区的排放量为21.5 Gg·a–1，占全国总量的11%。考虑到全国农田N2O排放量增速放缓而东北黑土区仍在加快，这一比例在今后可能会增加。目前，以土壤有机质提升为核心目标的黑土保护利用措施正在东北地区大力推广。然而最新研究指出，土壤固碳对缓解气候变化的效应可能被诱发的N2O排放抵消[12]。因此，研究黑土N2O排放与产生机制，对于在“碳达峰、碳中和”战略要求下制定黑土区合理的固碳培肥措施具有重要指导意义。
本文基于前人的研究结果，对我国东北黑土N2O排放特征、产生过程以及影响因素进行综述。收集东北黑土N2O排放田间原位观测数据，整合分析区域N2O排放量和化肥氮诱导的N2O排放系数（Emission factor，EF），从气象条件、土壤性质、田间管理措施等方面探讨东北黑土N2O排放的关键控制因子，剖析土壤N2O排放机制，为东北黑土农田N2O排放建模估算和减排措施制定提供理论支撑。
1 农田黑土N2O排放量利用文献数据库（中国知网和Web of Science）搜集筛选出中国东北黑土区N2O排放的文献，筛选标准是：（1）研究对象为东北黑土农田；（2）数据来自田间原位试验且观测时间至少包含一个完整的作物生长期；（3）具有试验时间、地点、土壤性质、田间管理措施等信息；（4）试验同时设置不施肥对照处理和施化肥处理；（5）N2O测定方法为静态箱-气相色谱法。共计采集到11个田间试验研究[10，13–22]，包括19个施用化肥处理和15个不施肥处理。
整合分析表明，不施肥处理的黑土N2O-N背景排放量变化范围为0.14~1.32 kg·hm–2，平均值为0.56 kg·hm–2（图 1），显著低于全球农田N2O-N背景排放量的平均值（1.10 kg·hm–2）[23]以及中国农田N2O-N背景排放量的平均水平（0.93~1.40 kg·hm–2）[24–25]。施用化肥条件下黑土N2O-N排放量为0.20~3.71 kg·hm–2，平均值为1.49 kg·hm–2。化肥诱导的N2O排放系数（EF）为0.03%~1.49%，平均值为0.45%，与Yue等[11]统计得到的东北黑土区玉米种植土壤N2O的EF（0.51%）相当，但显著低于中国旱地农田N2O-EF（0.60%~0.84%）（表 1）[26–29]。与世界上其他黑土相比，我国东北农田黑土EF也较低。Romanovskaya[30]报道俄罗斯黑土N2O排放系数为1.26%，Nevison等[31]发现美国“玉米带”土壤（主要为黑土）N2O排放系数为1.70%，Rochette等[32]报道加拿大黑土N2O排放系数为1.07%。因此，无论是N2O背景排放量还是肥料氮诱导的N2O-EF，东北农田黑土均处于较低水平，若仍采用IPCC缺省值（N2O-N背景排放量为1.0 kg·hm–2，EF为1.0%）[33]进行估算，将极大地高估东北农田黑土N2O的排放。
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图 1 不施肥和施化肥处理下东北农田黑土N2O排放量和肥料氮诱导的N2O排放系数 Fig. 1 N2O emissions from cultivated black soils without fertilizers and applied with synthetic fertilizers and synthetic fertilizer induced N2O emission factor in Northeast China |
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表 1 东北农田黑土、中国旱地农田化肥氮诱导N2O排放系数文献数据整合 Table 1 Integration of literature results of synthetic fertilizer induced N2O emission factor from cultivated black soils in Northeast China and Chinese croplands |
对收集的数据进行统计分析发现，东北农田黑土N2O排放量与年降水量（R2 < 0.01，P =0.88）、年均气温（R2 =0.24，P =0.19）、土壤pH（R2 < 0.01，P =0.98）均无显著相关关系，但是与SOC含量（图 2a）和土壤碳氮比（C/N）（图 2b）呈显著负相关，与土壤容重则存在显著正相关关系（图 2c）。随着氮肥用量的增加，黑土N2O排放量表现为指数增长趋势（图 2d）。
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图 2 东北农田黑土N2O排放量与土壤有机碳含量（a）、碳氮比（b）、容重（c）和施氮量（d）的关系 Fig. 2 Relationships between N2O emissions and soil organic carbon content (a), C/N ratio (b), bulk density (c) and synthetic fertilizer N application rate (d) from cultivated black soils of Northeast China |
土壤氮素循环的多个过程能够产生N2O，包括自养硝化、异养硝化、反硝化、硝化细菌反硝化、同步硝化-反硝化、硝酸盐异化还原成铵（DNRA）等。此外，化学反硝化、共反硝化等非生物学过程也可能是土壤N2O的来源（图 3）[34–35]。
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注：AMO，氨单加氧酶；HAO，羟胺氧化还原酶；NXR，亚硝态氮还原酶；NAR/NAP，硝酸异化还原酶；NirK/NirS，亚硝酸异化还原酶；NOR，NO还原酶；NOS，N2O还原酶。- - - - 表示文献中已有报道的黑土中产生N2O途径。 Note: AMO, Ammonia monooxygenase; HAO, Hydroxylamine oxidoreductase; NXR, Nitrite oxidoreductase; NAR/NAP, Membrane-bound nitrate reductase/ Periplasmic nitrate reductase; NirK/NirS, Copper-containing nitrite reductase/Cytochrome cd1 nitrite reductase; NOR, Nitric oxide reductase; NOS, Nitrous oxide reductase; - - - - refers to the N2O production pathway in black soil reported in the literature. 图 3 土壤中N2O主要产生过程 Fig. 3 Main process of N2O production in the soils |
硝化作用发生在好氧区域，是黑土N2O产生的主要过程，可以进一步区分为化能自养型和异养型，前者是指自养硝化微生物以CO2作为唯一碳源将铵态氮（NH4+）转化成硝态氮（NO3–）的过程，后者是指异养硝化微生物以有机物为碳源将低价态氮氧化成高价态氮的过程。传统观点认为自养硝化是农田土壤的主要硝化过程，而异养硝化则更多见于草原和森林等自然生态系统[36–37]。然而，有研究发现，黑土中异养硝化对N2O排放的贡献率可以达到自养硝化的2倍；其原因是，与其他类型农田土壤相比，黑土具有较高的SOC含量和C/N以及较低的pH和容重，有利于异养硝化作用的进行[38–39]。与细菌相比，真菌更能有效地利用难分解有机物、更适应酸性和低氧环境[40]。而异养硝化的发生多与真菌有关，特别是pH较低的土壤中[40–41]，因此真菌驱动的异养硝化对黑土N2O产生的作用可能强于其他农田土壤[42]。但是，目前黑土中异养硝化的微生物分子生物学机制尚不清楚，需要对功能微生物类群及其生化过程开展更深入研究。
硝化细菌反硝化是氨氧化细菌（Ammonia-oxidizing bacteria，AOB）在低氧环境中将氨氧化产生的NO2–还原成N2O和N2的过程，是微生物规避NO2–累积毒害的重要机制[35]。研究发现，长期施肥的黑土在高含水量（70%WHC）条件下硝化细菌反硝化对N2O排放的贡献达到15%，较高的水分含量形成有利于硝化细菌反硝化进行的厌氧微域[38]。但是，目前还没有研究直接测定硝化细菌反硝化对黑土N2O排放的贡献，有待利用18O-15N同位素共同标记技术来确定黑土硝化细菌反硝化对N2O产生的贡献[43]。
厌氧条件下NO3–还原成N2O和N2的过程统称为反硝化作用。反硝化作用产生N2O的能力远大于硝化作用，也是唯一能将N2O还原为N2的过程，主要包括化学反硝化和生物反硝化两种。化学反硝化是指氨氧化过程的产物NH2OH与NO2–发生化学分解，产生NO、N2O和N2，通常发生在pH < 4.5的酸性土壤[44]。迄今，未见黑土中化学反硝化产生N2O的报道。考虑到黑土pH一般为5.8~6.2[8]，化学反硝化对黑土N2O产生的贡献可能很低。
生物反硝化可由细菌或真菌驱动。真菌反硝化由于缺少N2O还原酶而只能进行不完整的反硝化作用，最终产物是N2O。目前真菌反硝化对黑土N2O排放的贡献尚不清楚。东北黑土区主要为雨养旱作农田，土壤水分主要来自降水。有研究发现，在正常降水条件下，反硝化作用对黑土N2O产生的贡献不足30%[45]。这主要是因为，土壤孔隙含水量（WFPS）小于70%，没有形成充分的厌氧环境；此外，黑土较低的活性碳含量也是限制反硝化作用的重要原因[39，45]。通常，在较大的空间尺度上N2O排放量与SOC含量表现为正相关关系，较高的SOC含量会增强微生物活性，促进反硝化作用产生更多N2O[46]。但是，黑土尽管SOC含量相对较高，但主要由分子量较大且芳香程度较高的胡敏素和腐殖酸组成，不易矿化，碳水化合物、氨基酸等能被微生物直接利用的活性碳含量较低[47–48]。并且，SOC含量越高，黑土的C/N也越高，其可分解性越低，限制了反硝化作用产生N2O，因此东北黑土N2O排放量随SOC含量和C/N的增加而降低（图 2）。容重大的土壤中，孔隙度较低、通气性较差，容易产生厌氧环境[49]，从而可能部分解除黑土中反硝化作用的水分和活性碳的“双低”限制，进而促进N2O排放。
除反硝化过程外，NO3–还可以通过异化还原过程转化为NH4+，即硝酸盐异化还原成铵（DNRA）过程，N2O为其中间产物[50]。与反硝化作用相比，DNRA所需还原条件更为严格，因此多见于稻田、湿地、热带森林等缺氧或者有机碳含量高的生态系统[51–52]。然而，有研究发现在高含水量（70%WFPS）的农田黑土中，DNRA也可以进行，是黑土的重要保氮机制[39]。理论上，DNRA的发生能够降低N2O产生[53]，但目前DNRA对黑土N2O排放能力的影响尚不清楚。
3 农田黑土N2O产生的主要影响因素 3.1 温度硝化和反硝化作用能在较宽范围的温度下进行，最适温度为25~35℃[54]。一般认为，低温条件下微生物活性受到抑制，N2O排放较低，温度接近0℃时甚至出现负排放[55]。微生物活性的最低生理阈值是–7℃[56]，但在东北黑土区观测到冬季土壤温度低至–15℃时仍存在微生物活动与N2O排放，可能是微生物长期处于寒冷环境下形成的适应性[57]。黑土N2O排放对温度升高的响应在低温条件下更加明显，可能是由于nirS型反硝化细菌的温度敏感性驱动[58]。考虑到气候变化的影响，在降雪量增加的情况下，更厚的“雪被”能够对黑土产生更强的物理隔离效应，有利于形成稳定且温和的结冰状态[59]，从而可能提高黑土低温季节N2O排放。
3.2 水分条件土壤水分通过改变土壤中O2含量、有效碳氮底物运输分布、微生物活性等影响N2O产生。在水分含量低、通气良好的土壤中，硝化作用主导N2O产生[60]，且随着土壤含水量增加而增加（30%~70% WFPS）。较高的含水量（70%~90%WFPS）导致土壤通气性变差，O2含量减少，促进厌氧微域的形成，刺激反硝化作用并减弱硝化作用，此时硝化和反硝化作用同时存在，反硝化作用逐渐占主导地位，N2O排放量达到最大。在东北黑土区的研究表明，降雨、灌溉、融雪等事件后，土壤水分含量显著增加，短期内N2O产生脉冲式排放[45，61]。当土壤含水量进一步增加并高于田间持水量时，土壤孔隙被水充满或因黏土吸水膨胀而关闭，将抑制N2O向大气中排放，并促进N2O被进一步还原为N2[62]。例如，极端降雨事件导致黑土农田滞水，N2O几乎没有排放，但是在随后的变干期，N2O出现爆发式排放[45]。因此，水分对黑土N2O排放的影响不仅与土壤含水量有关，也与降水的频次和强度以及降水前的土壤水分条件等因素有关。
3.3 冻融作用东北黑土区的的冻融作用主要发生在秋季作物收获后至次年春季播种前，可以分为四个时间段：土壤冻结期、覆雪期、融雪期和解冻期，N2O的爆发式排放主要发生在融雪期和解冻期[63]。春融初期土壤水分频繁发生“固-液”交替，冰晶的融化在土壤中形成大量有氧-低氧-无氧微域连续体，创造独特的氧化还原条件，有利于硝化和反硝化作用的同时进行[64]。与细菌相比，真菌可利用菌丝获取更多液态水和溶解在其中的养分，因此结冰土壤中可能更易发生真菌反硝化[65]。中后期土壤中液体水的体积显著增加，作物残留细根和微生物残体分解[66]，团聚体破碎、养分释放，活性碳氮底物供应量显著提高，进而刺激微生物活性[67]。有研究发现，黑土冻融循环过程中大粒径团聚体中产生的N2O大于小粒径，因此在秋季作物收获后土壤冻结前减少翻耕可能会降低冻融过程诱导的N2O排放[68–69]。
冻融期N2O的爆发式排放时间较短，但是一旦发生，就可能主导全年排放量。有研究发现，在加拿大季节性冻结农田，非生长季对N2O全年排放量的贡献可达33%~48% [59，70]。对我国东北黑土区的最新研究报道，在降雪量较高的年份，春融期N2O排放占全年总量的54%~76%，解冻后土壤中较高的含水量和活性碳底物激发反硝化作用是N2O脉冲式排放的主要诱因[71]。施用硝化抑制剂显著抑制黑土农田生长季N2O排放，但是不影响甚至促进春融期N2O排放，因此较高的冻融N2O排放能够降低甚至抵消作物生长季硝化抑制剂对黑土N2O的减排效果[71]。因此，应加强非生长季特别是冻融期黑土N2O排放的测定频率，以免错失脉冲式排放峰值，低估全年累积排放量；同时也需要研发更加有效的调控措施，靶向削减黑土冻融N2O排放。
3.4 田间管理措施在农田生态系统中，施肥是影响土壤N2O排放的重要因素。通常认为，农田土壤N2O排放量与施氮量呈线性相关；Shcherbak等[72]对全球农田土壤N2O排放的整合分析表明，N2O排放量对氮输入量的响应明显快于线性增长，当氮肥用量高于作物需求时，N2O排放量表现出指数增长趋势。本研究结果显示，东北黑土N2O排放量与施氮量具有显著的指数关系（图 2d）。这表明，施氮量过高导致氮素冗余时，将导致农田黑土N2O排放量急剧增加。因此，根据作物氮素需求，合理制定氮肥用量是减少黑土N2O排放的重要措施[73-74]。
与化肥相比，有机肥能够提供大量有效碳，增强土壤反硝化作用，对非生长季黑土N2O排放的促进效应更明显[14，75]。研究发现，活性碳供应较无机氮对黑土N2O排放的促进作用更为明显[57，75]，因此施用分解率高的猪粪比鸡粪诱导黑土N2O排放的能力更强[45]。同样地，秸秆还田可能会促进土壤反硝化作用进而导致N2O排放显著增加[76]；但是，有研究表明秸秆还田降低了黑土N2O排放[21]，分析其原因可能是秸秆的施用带入大量活性碳，提高了异养微生物的活性促进其对无机氮的固定，或促进N2O的还原，从而导致N2O排放量降低。在东北黑土区，秸秆还田多在秋季作物收获后进行，这可能会促进次年春融期N2O排放；但是，目前关于秸秆还田对东北黑土N2O全年排放效应的研究未见报道。
4 结论与展望东北农田黑土活性有机碳底物供应不足，且在正常降雨年份土壤含水量较低，从而限制了反硝化作用的进行，N2O主要由硝化作用产生，因此其背景排放量和氮肥诱导的N2O排放系数均较低。与我国其他农田相比，东北黑土区N2O排放的田间研究较少（尤其是涵盖非生长季的周年尺度研究目前仅有4例）。冻融过程可能产生大量N2O，但是其排放强度的时空变化以及对整个黑土区N2O排放量的贡献并不清楚。关于黑土N2O排放对不同农艺管理措施和气候变化响应的研究也非常有限。因此，今后亟需加强以下几方面的研究：
1）N2O排放通量的原位监测。已有的田间原位试验集中在黑龙江省中部地区（海伦和哈尔滨）。不同黑土区气候条件和土壤性质不同，N2O排放可能存在很大差异。需要加强气候较湿润的黑龙江东部黑土区、气候较干旱的呼伦贝尔黑钙土区以及温度较高的吉林和辽宁北部薄层黑土区N2O排放的原位观测研究。此外，原位观测研究方法多为静态箱-气相色谱法，应考虑采用不同的方法进行监测，如涡度相关法等，完善东北黑土区N2O排放通量的原位监测网络。
2）冻融过程中N2O爆发式排放机制。目前东北黑土区冻融过程中N2O排放的观测和机理研究十分匮乏，需要加强冻融期田间N2O排放通量的观测频率，探究冻融对土壤氮素转化与N2O产生过程的影响与微生物机制，进而构建黑土冻融N2O减排技术。
3）不同管理措施对黑土N2O排放的效应。以有机质为核心的土壤质量退化是黑土地面临的重大问题，国家已经制定黑土地保护和利用的战略决策，今后将重点通过保护性耕作、秸秆还田、有机肥施用等措施阻控黑土地退化、提高产能。应加强研究上述措施对黑土N2O排放的影响与机制，从而制定实现黑土提质增效和N2O减排的“双赢”措施。
4）全球变化对黑土N2O排放的影响。随着气候变化发展，极端气候事件频发和强度不断提高，位于中高纬度的东北黑土区是气候变化的敏感区，可能成为N2O排放的“热点”区域，需要加强气候变化对黑土N2O排放的效应与机制研究。同时需要结合气候变化和N2O排放模型，评估极端气候情势下农田黑土N2O的排放强度。
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