冻融作用对土壤碳、氮、磷循环的影响

宋　阳，于晓菲，邹元春，王国平，张琳琳

(1.中国科学院 东北地理与农业生态研究所 湿地生态与环境重点实验室，吉林 长春 130102；2.中国科学院大学，资源与环境学院，北京 100049)



冻融作用对土壤碳、氮、磷循环的影响

宋阳1,2，于晓菲1，邹元春1，王国平1，张琳琳1,2

(1.中国科学院 东北地理与农业生态研究所 湿地生态与环境重点实验室，吉林 长春 130102；2.中国科学院大学，资源与环境学院，北京 100049)

摘要：冻融作用是中高纬度地区普遍存在的一种非生物营力，对土壤生物地球化学过程影响显著，并随着全球变暖的持续，受到越来越多的关注。文章综述了冻融作用影响土壤碳、氮、磷循环的几个主要方面：包括可溶性有机碳(DOC)变化、温室气体的排放、氮的迁移转化以及土壤对磷的吸附解吸等。现有研究结果表明：冻融作用损伤微生物细胞和植物根系，释放其中的有机质并增加相应的土壤溶液浓度。随着冻融循环的持续，冻胀作用使大团聚体不断裂解成小团聚体，释放作为粘结物的有机质，使原本不能被微生物利用的基质暴露出来，并且团聚体的比表面积增大提供了更多的微生物接触位点和离子吸附位点。在冻融期微生物可以利用上述作用中产生的大量营养物质和反应底物从而促进CO2、 N2O等温室气体的产生，促进有机碳、氮、磷的矿化分解以及氮的硝化、反硝化作用等土壤营养元素的周转，也提高了潜在的土壤养分流失的可能。由于土壤类型、植被组成、微生物活性的复杂差异，冻融期土壤碳、氮、磷循环及其影响因素仍有诸多分歧。文章简要剖析了当前冻融实验的研究内容、方法和存在的问题，并对今后冻融对土壤碳、氮、磷循环影响的研究方向提出建议。图1，参128。

关键词：冻融；土壤；碳；氮；磷

0引言

冻融作用是指土壤温度受到气温影响而使其在凝固点上下变化导致的土壤冻结、融化现象。冻融现象主要发生在全球的高纬度及高海拔地区[1-2]。土壤冻融的强度和频率主要取决于当地的气候条件以及雪层的厚度[3]。因为雪层可以隔绝土壤直接与空气接触，所以在一定程度上对土壤起着隔温作用，使得土壤温度变化幅度减小[4]。然而根据IPCC[5]的报告，预计到本世纪末，大气中不断增加的CO2及其它温室气体将导致全球地表温度升高1.1℃～6.4℃，冬季的增温幅度要高于夏季。冬季气候变化不仅导致冻融期气温波动变化剧烈，也会减小雪层的厚度以及雪被覆盖的时间[6]。失去雪被覆盖的土壤直接受到气温的影响，其冻融现象将会愈加频繁的发生[7]。

土壤处在大气圈、水圈、生物圈和岩石圈的中心位置，是它们长期共同作用的产物[8]。土壤作为生态系统中重要的有机碳库之一，其生物地球化学循环的改变对全球生态环境的影响是显而易见的。土壤碳、氮、磷循环过程是决定生态系统功能和服务的关键过程，是土壤肥力的基础，决定着生态系统的生产力的大小。在全球变暖持续和大气氮沉降增加的背景下对土壤碳、氮、磷循环过程已经做了大量的研究：包括碳、氮、磷的同化矿化，含碳、氮温室气体的产生以及氮、磷的流失等。这些研究对提高和保持土壤生产力来讲十分重要。过去的研究主要关注生长季间土壤的碳、氮、磷循环，但是越来越多的研究发现冬季非生长季以及由于全球变暖造成的雪被厚度变化所导致的冻融过程对土壤碳、氮、磷循环影响在年际尺度上是不可忽视的[9]。土壤根系和微生物活动在0～5℃的低温甚至冻结条件下仍然呈现较高的活性，大约20%～50%的碳、氮、磷循环过程以及温室气体排放发生在冬季[10-13]。冻融过程不仅直接影响非生长季的碳、氮、磷循环，长期的生态系统监测显示冷冬及频繁的冻融对生态系统的影响会延续到其后的生长季[6,14]。这种影响与土壤性质、微生物活性及群落结构、气候条件、植被组成及管理方式均有密切联系[15-16]，但是由于研究方式方法的差别导致目前诸多有关冻融作用影响土壤碳、氮、磷循环的研究结果分歧较大。所以有必要综述现有研究结果，明确冻融作用下不同土壤类型碳、氮、磷循环的过程与模式，梳理影响结果的原因和机理，对具有分歧的实验内容与方法进行对比并找到症结，为冻融作用下土壤碳、氮、磷循环提供重要依据和参考。冻融作用下土壤碳、氮、磷循环模式如图1所示。

图1　冻融作用下土壤碳、氮、磷循环的示意图Fig.1　The diagram of carbon，nitrogen and phosphorus cycles in soil affected by freeze-thaw events

1冻融对土壤碳循环的影响

1.1冻融对土壤可溶性有机碳(DOC)的影响

土壤可溶性有机碳DOC(Dissolved organic carbon)虽然仅占土壤有机碳库的很小部分，但却是其最活跃的组分之一[17]。可溶性有机碳的可利用性是调控异养微生物活性[18-19]以及有机物质分解与转化的关键因素[20]。由于可溶性有机碳能直接被微生物利用，因此对春季融化期的N2O和CO2等温室气体的迅速大量排放有重要直接关系[21]。

Schimel等[22]对苔原生态系统的研究表明，冻融交替如同干湿交替和氯仿熏蒸等作用一样会裂解微生物造成土壤微生物死亡，小分子的氨基酸和糖类释放到土壤溶液中，提高了土壤中DOC的含量。周旺明等[17]对三江平原沼泽湿地的DOC研究中则发现在第一个冻融周期后DOC含量达到最大值。而在随后的循环中，土壤中的DOC含量逐渐减小，随着微生物的利用、土壤对其的吸附以及淋溶而浓度下降。Yu等[19]在中国东北三江平原两种典型湿地和一处开垦湿地开展的研究表明冻融循环可以增加这三种土壤对DOC的吸附能力并降低对其的解吸作用。并且常年淹水的湿地比季节性湿地对DOC的吸附性更强，开垦后的湿地对DOC的吸附能力下降并且解吸能力增强[19]。

综上所述，土壤可溶性有机碳的浓度在冻融循环初期存在迅速上升的过程，随着冻融循环的持续，可溶性有机碳浓度存在下降的趋势。在冻融初期，微生物没有适应冰晶的冻胀作用而出现大量的裂解死亡，释放出小分子糖、氨基酸，增加了土壤的可溶性有机碳含量。Skogland等[23]认为第一次冻融循环可以杀灭土壤中微生物总量的一半以上，微生物量碳、氮减少[24]，这直接导致了包括DOC的细胞物质的释放从而使土壤溶液中DOC浓度迅速增加。其次，冻融作用也可以直接破碎生长季残留的凋落物等有机体，进入土壤中的大分子有机物质中的分子键可以继续被冻融过程破坏，从而产生更多的可溶性有机物[25]。另外土壤团聚体是决定土壤可溶性有机碳的重要因素。冻融作用使团聚体发生膨胀与收缩从而破坏团聚体间的结合，使大团聚体分解成小团聚体[26-27]。多糖或菌丝根系等起胶结作用的有机物质进入土壤溶液中[28]。大多数研究表明，大团聚体(>2 mm)中的碳活性和氮活性较高，主要是新沉积的有机物，而小团聚体中的有机质主要以化学保护为主，与黏粒结合，分解较慢[29]。另外冻融过程会造成土壤孔隙度和孔隙大小增加。团聚体间和团聚体内部孔隙大小制约着土壤中水分的运移速度，大孔隙促使优先流的产生，进而带动可溶性有机碳在土体中迁移[30-31]，增加了可溶性有机碳流失的风险。Ghafoor等[32]发现土壤优先流的产生与土壤有机碳有着密切的联系，有机碳含量较高的土壤优先流较弱，有机碳可以更加稳定的存储在土壤中。多次冻融后，由于大团聚体逐渐减少，所释放的DOC也有所减少。微团聚体的比表面积大，有更多的微生物接触位点以及离子吸附位点，促进了微生物对DOC的利用和团聚体本身对DOC的吸附。土壤对DOC的吸附能力与土壤本身的性质密切相关，含有大量铁、铝氧化物的土壤其吸附DOC的能力也相应增强[33-34]。随着冻融循环的持续，微生物逐渐适应冻融影响。冻融交替致死的微生物的绝对量在减少[35,17]，微生物群落结构也发生了变化。一般认为冬季的主导微生物是真菌[36]，而Larsen等[25]的研究认为多次冻融循环可以使土壤微生物群落由C/N比较高的真菌群落转变为C/N比较低的细菌群落从而改变土壤中有机质分解与固持的能力。

1.2冻融对土壤CO2排放的影响

土壤中的碳流失主要是以CO2的形式，以DOC形式流失的量很少，以CH4形式流失主要存在于湿地中[3]。冻融影响土壤含碳气体的产生与排放是当前的热点研究问题，但是目前对冻融作用是否在年际尺度增加土壤呼吸量有巨大的分歧。森林生态系统[37]、高山苔原[38]、北极荒原[39]、草原[39]、泥炭沼泽[40]和南极洲[41]的研究表明融化期的土壤会有一段大量排放CO2时期。但是Dörsch等[42]研究认为整个冻融期过后，额外的CO2排放量相对很少，只有180 kgC·hm-2。Priemé等[43]对苔原生态系统的研究发现：随着冻融循环次数的增加，土壤释放的CO2的量在减少，在融化期排放的CO2大约有0～130 kgC·hm-2，且不足全年土壤呼吸量的5%[3]。Monson等[44]经过对山地生态系统6年的野外研究认为：土壤在融化期大量排放的CO2并不能完全补偿冰冻期土壤呼吸的减少量。而在生长季中土壤95%的CO2排放量都是由土壤温度与湿度决定的，与冻融期情况并无关联[3]。

融化期土壤CO2产生和排放量增加主要有以下几种原因：(1)冻结期微生物会由于冻胀作用裂解死亡，释放出小分子糖和氨基酸等容易利用的小分子有机物并被存活下来的微生物迅速分解。Herrmann 和 Witter[45]研究了冻融作用下土壤微生物在土壤养分循环中的作用：把微生物用14C标记后，发现农田生态系统的土壤在融化时释放的CO2中，有65%是由原来微生物体内的有机物矿化而来的。(2)植物根系在土壤冻结期的损伤和随后的分解可能是影响融化期土壤CO2排放的重要因素[3]。Groffman等[46]估算冻融后实验样地的根系死亡残体为300 kg·hm-2，相当于150 kgC·hm-2，若其中50%的碳矿化为下一生长季的CO2，那么CO2通量为75 kgC·hm-2，仅占全年土壤呼吸的2% ～ 3%。但是土壤在融化期短时间内大量释放的CO2确实可能与根系细胞物质的迅速分解相关。根系死亡后，土壤中含有大量的根系腐烂残体，加上融化期土壤含水量和温度迅速升高，共同促进了微生物活性的提高，使得土壤呼吸速率加快[47-48]。(3)Teepe等[49]和Koponen等[50]认为土壤冰冻层以下气体的缓慢扩散和对流导致土壤深层以及土粒表面未冻结水膜中的微生物代谢活动和植物根系呼吸产生的CO2积聚在土壤内部，并在融化期迅速排放出来。CO2的排放模式一般与DOC类似，通常在初始的几个冻融循环后达到高峰，之后土壤中DOC减少，微生物新陈代谢产生的CO2量也逐渐减少。诸多的研究表明在土壤有机碳库充足的情况下，CO2的排放量更多的与融化期土壤温度相关[51-52]。融化期土壤温度越高，微生物和植物根系活性越高，产生的CO2越多。当融化期排放的CO2量弥补了冻结期由于微生物和植物根系死亡造成的土壤CO2的减少量时，在年际尺度上就表现出冻融过程对CO2排放的促进作用。

2冻融对土壤氮循环的影响

2.1冻融对土壤氮矿化作用的影响

2.2冻融过程中硝化作用与无机氮流失的关系

2.3冻融对土壤反硝化作用及N2O排放的影响

冻融作用促进N2O排放的机制与促进N2O产生的机制有着紧密的联系同时又有着细微的区别。目前，关于春季土壤融化期N2O大量排放的机理仍有争议，Burton和Beauchamp[100]描述了春季融化期土壤的剖面特点：首先是土壤表面经历着剧烈的温度波动并积累了融化的水，其次土壤表面以下仍然存在一个冻结的冰层，最后是冰层以下温度较高且有机物逐渐减少的深层土层。由此而延伸出的N2O排放机理归纳起来主要有以下三点：(1)融化期土壤温度升高造成的气体溶解性的变化。N2O在水中的溶解度很高，略小于CO2的溶解度，是O2的2 000%[16]。它的溶解度与温度呈负相关，0℃的水中溶解的饱和N2O量是20℃水中的两倍[101]。因此冬季土壤的液态水膜中储存有大量的N2O，随着土壤温度在春季升高，其能溶解的N2O量下降导致N2O的大量排放。(2)物理性释放的结果。土壤冰层的屏障导致土壤冻结期深层土壤产生的N2O无法扩散，随着土壤融化、冰冻层的消失导致N2O大量排放。Bremner等[102]最早提出了物理释放的观点，其认为N2O在不同深度土壤的累积量是十分巨大的。这个观点一直是解释冻融作用与N2O排放关系的主要机制。但是一些研究表明[84]N2O的释放波峰与不同深度N2O的减少量不相关。Furon等[103]认为N2O的排放主要与0～5 cm的浅层土壤相关。(3)N2O在土壤融化期的重新产生。春季融化期土壤中营养物质和反应底物导致微生物活性增加，在冻结冰层的上部通常会形成一个比较浅的水饱和土层[104]，连同缺氧环境和土壤表面剧烈的温度波动创造了反硝化作用的理想环境。Smith等[64]认为N2O大量排放期之前和期中的土壤硝化和反硝化微生物群落和多样性有着显著的变化，这预示了N2O的重新产生是春季N2O大量排放的主要机制。

3冻融对土壤磷循环的影响

生态系统的生物可利用磷的浓度需要控制在适当的浓度，过低的磷浓度会对生态系统的生产力造成影响，过高的磷浓度又会提高磷流失到地表水体的风险，造成水体的富营养化等问题。土壤中的磷形态比较复杂，无机磷和有机磷按照不同的浸提方式分类有多种的分级方法[105-106]。但是总体来说可以分为活性磷和非活性磷两部分[107-108]：活性磷是指容易被植物吸收利用的磷。包括水溶性磷、部分吸附态磷和部分有机磷。非活性磷指不溶性磷化合物和在黏粒内部或有机质中的固持态磷，非活性磷占土壤全磷95%以上。研究冻融作用对非活性磷和活性磷之间的转化对土壤磷的供应和贮存具有重要意义。

Campbell等[109]和Nyborg等[110]认为冬春季节的土壤总可溶性磷(TDP)浓度会显著高于之前秋季的土壤TDP浓度。周旺明等[111]的研究发现冻融过程提高了土壤淋溶液中的总磷和磷酸根浓度，增加了磷元素的流失量。冻融作用提高土壤中可溶性磷浓度是一种比较普遍的现象。土壤有机层的研究表明冻融作用可以通过使凋落物破碎、微生物死亡裂解、植物根系细胞损伤释放其中的有机磷，大分子有机质的分子键可以继续被冻融作用破坏形成小分子的可溶性有机物从而增加土壤溶液中可溶性有机磷(DOP)的含量，并成为TDP的主要组成成分[112]。Yavitt和Fahey[113]的研究认为95%的TDP是以有机物DOP的形式存在的。此外有机质分解产生的有机酸可以与土壤中难溶性磷酸盐的金属离子络合释放其中的磷，腐殖质又可在铁铝氧化物表面形成保护膜，减缓土壤对磷的吸附解吸[114]。以上作用共同提高了冻融过程后TDP的浓度。可溶性有机磷可以通过微生物作用进一步分解或水解为无机磷，在春季被植物、微生物利用重新转化为生物体内的有机磷。对土壤矿质层的研究发现，冻融作用可以提高碳酸氢钠提取磷的含量[115]，Oztas和Fayetorbay[116]认为这种现象是由冰晶使团聚体破碎造成的。团聚体的破碎可以形成新的反应界面，这种反应界面的增加会造成两种作用机制同时发生。一方面，土壤团聚体破坏后，不仅直接导致闭蓄态磷和矿物态磷的释放，也会导致团聚体或矿物晶格中的其他离子释放到土壤溶液中，这些重新释放的离子与磷酸盐共同竞争土壤表面的吸附位点，取代原本吸附在土粒表面的磷酸盐，使土壤对磷的吸附能力减弱[117-118]。另一方面，冻融使土壤颗粒的粒径变小，比表面积增大，吸附位点增多，土壤的吸附能力增强[118-120]。冻结作用造成土壤溶液的浓缩，土壤溶液离子强度的增加以及扩散层厚度的减小也会促进土壤对磷的吸附[121]。此外，冻融作用可以破坏有机物与铁铝化合物的胶合[118,122]，铁铝化合物的释放也会增加土壤对磷的吸附。土壤对磷的吸附作用是土壤贮存磷的主要方式之一，但是由于以上几种同时发生又互相制约的机制导致目前对冻融作用下土壤对磷的吸附与解吸结果的分歧较大。Yu等[1]研究冻融过程对土壤吸附TDP的影响发现：冻融组土柱的总可溶性磷的浓度低于对照组，这说明冻融循环会增加对磷的吸附。这与Wang等[123]对中国东北三江平原的碟形湿地和河流湿地中冻融作用对磷元素影响结果一致，湿地土壤对磷的吸附等温线能通过Langmuir吸附等温线较好的描述。经过冻融循环的土壤样品比对照土壤吸附更多的磷，也就是说冻融作用会增大土壤对磷的缓冲性能。随着冻融次数的增加，土壤溶液中的磷浓度逐渐降低，从而保持地表水中磷的低负荷，因此对环境产生有利的影响。然而钱多等[124-125]研究棕壤中冻融对磷的影响表明冻融使土壤对磷的吸附性能减弱、土壤对磷的解吸能力增强。如此矛盾的结论表明土壤本身的理化性质对磷的吸附解吸影响的作用是十分巨大的。如何控制冻融过程导致的TDP流失是科研工作者关注的一个问题：Soinne等[126]把猪粪作为有机肥施入土壤中并进行冻融循环，发现土壤矿质层对磷的吸附能力增大，经过冻融循环后的土壤溶液中TDP的浓度并没有发生变化，土壤对磷的固持能力增加。另外土壤含水率、冻结温度和冻融频次也影响着冻融作用下土壤磷的迁移转化。含水量高的土壤在冻结时，由于冰对离子的排斥效应[127]，使磷向土体下部迁移，如果没有被土壤吸附则提高了磷流失的风险。冻结温度的降低和冻融循环次数的增加通常会放大冻融作用对磷的影响。

4冻融影响下土壤物质循环研究的欠缺与今后研究方向

在研究方法上，冻融的温度、时间、频率的确定以及土壤的采样方法、采样时间需要尽可能的贴近实际环境情况。Baker等[128]对冻融频率和冻融温度做了细致的研究，除了得出土壤温度与空气温度之间的不同步性外，还发现采取不同冻融温度所确定的冻融计数周期及实验结果也完全不同。不同的实验方案以及测量方法的不同也会造成实验结果的变化，这也是诸多研究结果互相矛盾的原因之一。冻融研究的室内模拟实验和野外原位实验各有利弊：实验室模拟的优势是可控性强，数据精确且有科学的对照组比较，但是也因为可控性使得不能够完全模拟野外的冻融温度及冻融频率。实际冻融期土壤温度的变化情况是复杂的，冻融期土壤可能因为天气变化而在短时间内经历多个冻融周期，也可能在一段时间内都不出现冻融周期，因此较难在实验室进行精准的模拟。野外原位实验的优势在于数据的真实性，雪被去除与添加实验可以真实的模拟未来气候变化、雪被减少所造成的冻融现象对土壤碳、氮、磷循环的影响，但是无法控制每次冻融的时间和强度。无论室内模拟实验还是野外原位实验，对照组的温度设置都是绝对不容忽视的问题[3]：由于冻融实验的特殊性质，对照组的温度不同使之与冻融组相比会产生不一致的结果。Matzner和Broken[3]认为在今后的实验室模拟实验中，对照组与冻融组的温度应该平行设置，直到对照组的温度达到0℃。在冻融组到达0℃以上的融化期时，对照组的温度应该完全与冻融组保持一致。

在研究内容上主要存在两个方面的欠缺，一是研究仅专注于冻融作用对土壤物质循环的单一影响，比如：微生物活性、氮的矿化等。由于物质循环受到不同自然条件的制约，并与地表植物、临近生态系统存在紧密的联系，所以未来的研究需要以整体的观念研究冻融对土壤物质循环的影响。二是对冻融影响机理没有细致透彻的认识，大多数停留在表观影响或推断原因的层次上，并没有在生物化学、环境化学及物理化学的层次上深入研究，因此今后的研究有必要加强这方面的探索。

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Progress of Freeze-thaw Effects on Carbon,Nitrogen and Phosphorus Cyclings in Soils

SONG Yang1,2,YU Xiaofei1,ZOU Yuanchun1,WANG Guoping1,ZHANG Linlin1,2

(1.KeyLabofWetlandEcologyandEnvironment,NortheastInstituteofGeographyandAgroecology,CAS,Changchun130012,China; 2.CollegeofResourcesandEnvironment,UniversityofChineseAcademyofSciences,Beijing100049,China)

Abstract：As a ubiquitous non-biological stress in high latitudes,freeze-thaw effects are sensitive to climate change.Along with global climate warming,freeze-thaw phenomenon is receiving ever-significant attention.The biogeochemistry processes in soils keep notable response to freeze-thaw influence.Here we review the primary researches about carbon,nitrogen,phosphorus cyclings under freeze-thaw treatment in soils.We mainly focus on changes of dissolved organic carbon,greenhouse gas emission,nitrogen and phosphorus turnover in soils.On the basis of available literature,freeze-thaw effects could damage microbes and root cells,lead their internal carbon and nitrogen release which increase corresponding concentration in soil solution.Macroaggregates in soils could be destroyed into microaggregates with successive freeze-thaw cycles,which increase the availability of nutrients to soil microorganisms by larger surface area.During freeze-thaw period,nutrients and substrates produced in above-mentioned mechanisms would stimulate metabolisms of microbes and turnover of carbon,nitrogen and phosphorus in soils which however increase potential nutrients run-off in turn.Because of differences in soil types,vegetation constitutes and microorgnisms diversity,there are still debates on how continuous freeze-thaw effects influence nutrients cyclings in soils.Besides,our review points out the weakness of research methods in freeze-thaw studies.The recommendations for future freeze-thaw researches are also indicated.

Key words：freeze-thaw; soils; carbon; nitrogen; phosphorus

中图分类号：S154.1

文献标识码：A

第一作者简介：宋阳(1992-),男,黑龙江佳木斯人,在读硕士,研究方向为湿地生态系统生物地球化学循环.通讯作者：于晓菲(1982-),女,吉林四平人,副研究员,主要从事湿地生态与环境研究.

基金项目：中国科学院东北地理与农业生态研究所优秀青年基金项目(DLSYQ2012006); 国家自然科学基金面上项目(41471079，41271107); 中国科学院青年创新促进会项目(2014204).

收稿日期：2016-01-12;修回日期：2016-02-21.

文章编号：2095-2961(2016)02 -0078-13

doi:10.11689/j.issn.2095-2961.2016.02.003