蚯蚓在我国南方土壤修复中的应用
张池1, 周波2, 吴家龙1, 吕美蓉3, 陈旭飞1, 袁中友1, 肖玲1, 戴军1,*
1 (华南农业大学资源环境学院, 农业部华南耕地保育重点实验室, 广东省土地利用与整治重点实验室, 广州 510642)
2 (广东省农业科学院茶叶研究所, 广东省茶树资源创新利用重点实验室, 广州 510640)
3 (齐鲁工业大学(山东省科学院), 山东省科学院海洋仪器仪表研究所, 山东青岛 260000);
* 通讯作者 Author for correspondence. E-mail: jundai@scau.edu.cn
摘要

蚯蚓作为生物量最大的土壤动物, 对土壤生态系统和环境质量影响深远。本研究介绍了华南地区主要应用的皮质远盲蚓( Amynthas corticis)、毛利远盲蚓( A. morrisi)、壮伟远盲蚓( A. robustus)、参状远盲蚓( A. aspergillum)、南美岸蚓( Pontoscolex corethrurus)和赤子爱胜蚓( Eisenia fetida)的生态特征, 阐述了它们与土壤pH值、酶活性、金属富集和有效性改变、孔道和微团聚体形成之间的紧密关系: (1)蚯蚓生存的土壤酸碱性范围较广(pH为3.8-7.9), 其存活率与土壤类型、有机质含量和成分、土壤污染程度和蚯蚓种类相关; (2)肠道内、蚓粪和蚓触圈的酶活性分别表征了蚯蚓取食喜好、土壤养分循环及微生物种群特征; (3)蚯蚓能够富集不同种类的金属并改变其有效性, 这些变化具有蚓种间、金属种类间和土壤类型之间的差异; (4)蚯蚓活动及其生产的蚓粪能改变土体结构、产生孔道、影响土壤团聚体数量、大小和分布。蚯蚓的上述作用使其在解决中国南方红壤酸化、土壤金属污染、茶园土壤养分不平衡、高速公路建设临时用地土壤损毁等方面具有广阔的应用前景。目前, 由于华南远盲蚓的生理特征差异研究较少, 远盲蚓繁育技术的缺乏一定程度上限制了这些蚯蚓在中型和大型尺度下应用技术的研究和推广。有必要进一步挖掘蚯蚓在土壤修复中的潜力, 进行蚯蚓主导的相关技术研发, 深入探讨其影响机制。

关键词: 蚯蚓; 华南; 土壤; 应用研究; 生态环境
Application of earthworms on soil remediation in southern China
Chi Zhang1, Bo Zhou2, Jialong Wu1, Meirong Lv3, Xufei Chen1, Zhongyou Yuan1, Ling Xiao1, Jun Dai1,*
1 College of Natural Resources and Environment, South China Agricultural University, Key Laboratory of Arable Land Conservation in South China, Ministry of Agriculture of P. R. China, Key Laboratory of Land Use and Consolidation in Guangdong Province, Guangzhou 510642
2 Tea Research Institute, Guangdong Academy of Agricultural Sciences, Key Laboratory of Tea Plant Resources Innovation and Utilization in Guangdong Province, Guangzhou 510640
3 Qilu University of Technology (Shandong Academy of Sciences), Institute of Oceanographic Instrumentation, Qingdao, Shandong, 260000
Abstract

A key soil invertebrate, earthworms significantly affect soil quality and the broader ecosystem. In this paper, we review the ecological characteristics of earthworm species Amynthas corticis, A. morrisi, A. robustus, A. aspergillum, Pontoscolex corethrurus and Eisenia fetida in southern China and their effects on soil pH, enzyme activity, metal accumulation and availability, the formation of soil pores and micro-aggregates, and the decomposition of organic waste. In sum: (1) Earthworms in southern China can survive in soil with a wide range of pH (3.8-7.9), and their survival rates are related to soil type, organic matter content, soil contamination level and earthworm species; (2) Enzyme activity in earthworm guts, castings and drilosphere indicate the appetite of different earthworm species, the process of soil nutrient cycling and soil microbial characteristics, respectively; (3) Earthworms are capable of accumulating different metals and altering their availability, but this capability varies depending on earthworm species, element and soil type; (4) Earthworm activity and cast production can change soil structure, increase the amount of soil pores and affect the size, amount and distribution of soil aggregates. Moreover, we highlight the potential application of earthworms toward resolving the acidification of red soil, nutrient imbalance in tea gardens, soil metal contamination, the compaction and destruction of soil during expressway construction, and the utilization of agricultural and urban organic waste. At present, due to insufficient investigations into the physiological characteristics of earthworms and a lack of Amynthas sp. breeding technology, earthworm applications are scarcely conducted at medium and large scales. Hence the promotion of earthworm technology is especially limited in southern China. It will be necessary to explore the potential of earthworms in soil restoration further and to analyze the mechanisms earthworms employ during soil construction and management in order to develop technologies to perform the functions currently occupied by earthworms.

Keyword: earthworm; South China; soil; application; ecology and environment

随着人类对土地利用强度和范围的扩大, 土壤生态系统承受的压力不断增加, 土壤结构退化、酸化、养分不平衡、污染、生物多样性丧失等问题日趋严峻(Marrugo-Negrete et al, 2017; Kovacs & Szemmelveisz, 2017)。作为“ 生态系统工程师” (Jones et al, 1994), 蚯蚓活动能够有效地改变土壤环境, 它对土壤生态系统的贡献已被广泛认识(张卫信等, 2007; 陈旭飞等, 2012; Blouin et al, 2013)。在蚯蚓的分类、生理特征及其对土壤形成、结构、有机质分解、养分转化, 以及对环境和生物多样性的影响等方面已有大量研究(Lavelle & Spain, 2001; Karaca, 2011)。在我国, 蚯蚓作为废弃物肥料化的生物工具和生活污水过滤处理的生物介质也被应用于农业生产和环境保护的实践中(邱江平, 2000; 孙振钧, 2004)。

目前全世界已知的蚯蚓约有4, 000种, 但人们仅仅对其中少数种类的生物学特性和生态学功能有过研究(Edwards, 2004; 张卫信等, 2007), 且针对亚洲地区特别是中国南部蚯蚓的研究甚少。本文归纳了华南地区主要用于应用研究的蚯蚓的生态特征及功能, 针对当前土壤酸化、养分不均衡、金属污染、物理结构破坏等问题, 综述了蚯蚓在生态建设、环境质量管理中的应用现状, 以期为蚯蚓主导的生物技术的研发和应用提供参考。

1 华南地区的主要蚯蚓种类及其生态特征

远盲蚓属(Amynthas)蚯蚓属于环节动物门寡毛纲单向蚓目巨蚓科, 以57.8%的比例在巨蚓科中成为优势属(赵琦, 2015)。我国是世界上远盲蚓属蚯蚓分布最多的国家。据孙静(2013)调查, 该属蚯蚓在华南地区有175个分布点。其中毛利远盲蚓(A. morrisi)、壮伟远盲蚓(A. robustus)、皮质远盲蚓(A. corticis)和参状远盲蚓(A. aspergillum)等均是分布较广且研究较多的蚯蚓(张池等, 2012; 陈旭飞等, 2014; 代金君等, 2015; Zhang et al, 2016)。另外, 一些外来种蚯蚓, 如南美岸蚓(Pontoscolex corethrurus) 和人工养殖蚓赤子爱胜蚓(Eisenia fetida)也是目前应用研究的主要种类(刘婷等, 2012a, b; 李静娟等, 2013; 周波等, 2011; Huang et al, 2015; Lv et al, 2016)。根据不同生态类型和特征, 华南地区蚯蚓可被分为表栖型、内栖型和深栖型(Lavelle & Spain, 2001)。皮质远盲蚓常见于富含枯枝落叶或腐殖质的林地的0-10 cm土层, 体型较小、体表颜色较深、生长速度快、繁殖力强、以有机物和土壤的混合物为食, 是华南地区表栖型蚯蚓中的主要种类。具有同样生长和繁殖特征、生活在耕地或园地0-15 cm土层的毛利远盲蚓, 因其以有机物和矿质土壤混合物为食而被列为表-内栖型蚯蚓(Zhang et al, 2016)。壮伟远盲蚓和南美岸蚓主要以矿质土壤为食, 生活在5-15 cm土层, 体色较浅、体型中等、运动较缓、繁殖较慢, 被认为是内栖型蚯蚓(Fragoso & Lavelle, 1992; 张池等, 2012)。在土表取食有机物、栖居于土层深处、体表颜色较深、体型较大、繁殖较弱的参状远盲蚓被认为是深栖型蚯蚓(Wu et al, 2018)。此外, 人工养殖蚓赤子爱胜蚓是应用广泛的堆肥蚓种, 以高腐殖有机物质为食, 以繁育能力强、适应性强著称, 但其在自然环境中抗扰动能力相对较差, 野外存活率较低。

2 蚯蚓对酸化土壤修复的作用及其机制
2.1 蚯蚓对酸化土壤的修复作用

蚯蚓活动能够显著影响土壤pH值(Laverack, 1963; Basker et al, 1994; Yu et al, 2005; 王斌等, 2013)。刘婷等(2012b)发现赤子爱胜蚓将有机物料pH值降低了0.07个单位。张池等(2012)研究发现壮伟远盲蚓和皮质远盲蚓使华南地区某水稻土的pH值分别提高了0.09和0.19个单位。袁中友等(2017a)研究显示与化肥处理相比, 赤子爱胜蚓蚓粪施用能显著提高土壤pH。Wu等(2018)接种南美岸蚓、壮伟远盲蚓和参状远盲蚓到酸性旱地土, 土壤pH值显著提高0.2-0.8个单位, 而且三者均使土壤趋于中性, 并显著降低蚓粪和未吞食土壤的交换态铝含量。唐劲驰等(2008)研究显示, 远盲蚓属蚯蚓与有机物料联合生物体系修复酸化黄金桂茶园土壤, 蚯蚓处理土壤的pH值下降程度明显低于复合肥处理。

综上所述, 在实验室条件下, 蚯蚓活动对土壤酸碱度有一定的调节作用, 但是目前未见在大尺度下大规模利用蚯蚓进行酸化土壤修复的研究。

2.2 蚯蚓修复酸化土壤的作用机制: 蚯蚓对pH的耐受能力

pH值是影响土壤生物活动的重要因子, 不同的蚯蚓对pH的耐受能力不同。Butt和Lowe (2011)指出, 赤子爱胜蚓最适生长的pH为6.5, 国内大部分研究结果也显示其适宜生长的物料pH值在6-9之间(周波等, 2011; 刘婷等, 2012b; 李静娟等, 2013)。Butt和Lowe (2011)研究显示温带内栖型蚯蚓绿色异唇蚓(Allolobophora Chlorotica)、Aporrectodea caliginosa和深栖型蚯蚓Aporrectodea longa和陆正蚓(Lumbricus terrestris)最适生存pH值在6-7之间; 而在我国华南地区, Wu等(2018)发现南美岸蚓, 壮伟远盲蚓和参状远盲蚓在pH 4.25的酸性林地土壤中的存活率分别为79%、97%和85.8%; Huang等(2015)和Shao等(2017)在pH 3.8的土壤中接种远盲蚓属蚯蚓和南美岸蚓, 进行了微宇宙盆钵实验或林地可控实验, 均发现蚯蚓能够正常生长, 甚至数量有一定的增加。由此可见, 远盲蚓和南美岸蚓在pH值为3.8-7.9范围内均能生长, 但最适合蚯蚓生存的pH值却鲜有报道。

蚯蚓能够耐受一定的酸性环境也许与蚓体钙腺或其他肠道或体表分泌物有关。蚯蚓能通过体内的钙腺合成CaCO3并排出体外(Lee, 1985; Garcí a-Montero et al, 2013), 使得蚓粪的pH值高于周围土壤, 这可能是土壤pH升高的原因之一。自1820年发现蚯蚓钙腺以来, 几乎所有的正蚓科(如赤子爱胜蚓)和舌文蚓科(如南美岸蚓)蚯蚓均被解剖实验证实具有钙腺(Lee, 1985; Briones et al, 2008; Karaca, 2011)。蚯蚓可以通过钙腺调节环境酸碱性, 使自身具有较强的pH耐受能力。然而孙静(2013)和赵琦(2015)发现大部分远盲蚓属蚯蚓没有钙腺, 因此关于在华南红壤中远盲蚓属蚯蚓如何调控酸碱平衡以及如何影响土壤pH, 目前尚无报道。有研究显示蚯蚓的表皮能分泌大量粘液, 肠道排泄产物中也含有甘氨酸、丙氨酸、苏氨酸等18种氨基酸、糖类(结合糖)、较高的交换性Ca2+、Mg2+和K+等可溶性无机盐和具有-COOH、-NH2、-C=O等活性基团的大分子量胶黏物质(冯凤玲等, 2006; Sizmur & Hodson, 2009; Wu et al, 2018), 也许这些组分也是蚯蚓活动能够调节土壤pH的原因之一。

另外, 相同pH下, 蚯蚓对pH耐受能力与土壤类型、有机物成分及含量、土壤污染程度及相关的种间差异有一定关系。张池等(2012)研究显示相对于表栖种皮质远盲蚓, 内栖种壮伟远盲蚓在覆盖青草的水稻土和菜园土中存活率更高; 与前者相比, 后者取食更多矿质土粒, 在净土中对土壤类型、有机质组分及其丰缺程度等变化欠敏感可能是上述现象发生的原因。陈旭飞等(2014)研究显示接种毛利远盲蚓和赤子爱胜蚓于混合造纸污泥的水稻土和旱地土后, 仅赤子爱胜蚓数量明显增加。代金君等(2015)发现壮伟远盲蚓在pH为4.5和7.9的多金属污染土壤中的存活率分别为50%和45%, 而赤子爱胜蚓的存活率则分别为97.3%和73.3%。Zhang等(2016)研究发现毛利远盲蚓在pH值为4.18的金属污染土壤中存活率仅9.5%, 在添加有机物料、土壤pH上升至5.5后, 蚯蚓存活率显著提高并有幼蚓出现, 推断有机物质的添加在一定程度上可以减少蚯蚓对污染物的暴露和摄食是这种现象发生的原因。同时, 研究也显示赤子爱胜蚓在添加和未添加有机物料的两种土壤中存活率分别为80%和95%。在污染条件下, 野生种对环境变化更加敏感, 受金属离子影响大, 可能是上述现象发生的原因(Langdon et al, 2005)。

综上所述, 进一步明确不同蚯蚓对pH的耐受机制, 分析它们在不同土壤酸化过程中的作用, 有助于为土壤酸化的生物修复提供理论依据。

3 蚯蚓在污染土壤修复中的应用及其作用机制
3.1 蚯蚓在污染土壤修复中的应用

蚯蚓活动不仅能提高土壤金属的有效性, 而且能够促进超富集植物生长, 进而增强超富集植物吸收金属的能力, 最终达到修复污染土壤的目的(Yu et al, 2005; Zhang, 2011; 黄钰婷, 2016( 黄玉婷 (2016) 有机质-蚯蚓联合使用对籽粒苋累积重金属的影响. 硕士学位论文, 华南农业大学, 广州.))。Zhang (2011)在实验室条件下, 使用超富集植物东南景天(Sedum alfredii)作为修复植物, 通过投放毛利远盲蚓和添加有机物料构建修复体系, 研究植物生长和金属迁移转化特征, 结果显示蚯蚓处理显著促进了东南景天组织器官的金属富集量和金属由地下部向地上部的转运能力。黄钰婷(2016)应用籽粒苋(Amaranthus hypochondriacus)作为修复植物, 选用秸秆和两种不同生态类型的蚯蚓(赤子爱胜蚓和壮伟远盲蚓)作为提高植物修复效率的因子, 以华南地区典型矿区酸性重金属污染土壤为对象, 构建“ 秸秆 + 蚯蚓 + 籽粒苋” 的联合修复体系, 进行盆栽实验, 结果表明土壤中镉含量显著降低、土壤质量明显提高。

然而, 上述利用远盲蚓进行重金属污染土壤修复的研究只集中在室内小规模的实验, 且主要集中在少数蚯蚓品种和超富集植物上, 有必要进一步针对不同污染土壤特征进行蚓种和超富集植物的筛选, 在更大尺度下进行蚯蚓-植物修复金属污染土壤技术的田间实验。另外, 随着新材料和新技术的应用, 生物炭和纳米吸附材料对土壤金属的吸附能力及其与生物间较好的相容性已被广泛认识。利用这些先进材料与远盲蚓共同构建新的生物修复体系, 更高效地修复重金属污染土壤, 值得进一步探讨。鉴于蚯蚓对金属的活化作用, 在进行蚯蚓主导的生物修复技术体系构建时, 应当对蚯蚓活化金属的速率、植被生长速率和金属吸收效率进行定量评估, 防止被蚯蚓活化的金属离子过早过快地进入水体和其他动植物体, 带来环境风险(Zhang et al, 2016)。

3.2 蚯蚓对污染土壤修复的作用机制: 蚯蚓对金属的影响

蚯蚓对金属胁迫具有较高的耐性和极强的生物累积能力(Dai et al, 2004; Yu et al, 2005)。Becquer等(2005)研究显示镉可通过皮肤渗入蚓体, 而铜、铅和锌等则主要通过蚯蚓吞食进入蚓体。同时, 金属在蚓体内的富集区域与蚯蚓种类和金属种类有关。很多研究显示, 镉主要分布在Aporrectodea caliginosa体内的后消化道(Morgan & Morgan, 1998)、Lumbricus rubellus的黄色细胞区域组织(Vijver et al, 2005)、赤子爱胜蚓的细胞溶质(Li LZ et al, 2009)和表皮(段晓尘, 2015)、安德爱胜蚓(Eisenia andrei)金属硫蛋白(Yu & Lanno, 2010)中, 而锌广泛分布于蚯蚓各器官及连接组织中(Vijver et al, 2005)。目前对于不同金属在华南的远盲蚓体内的富集位置和水平仍缺乏研究。另外, 金属在蚓体内的富集量与有效态含量密切相关, 大部分研究结果显示二者呈显著正相关关系(Dai et al, 2004; Becquer et al, 2005; 瑟竞, 2017 瑟竞 (2017) 赤子爱胜蚓(Eisenia fetida)抗氧化系统对土壤有效态镉响应的研究. 硕士学位论文, 华南农业大学, 广州.))。不同蚯蚓对金属富集能力的差异可以通过金属生物富集系数来表示(陈旭飞等, 2012)。内栖型蚯蚓往往比表栖型蚯蚓更容易富集镉、铜、铅等重金属(Morgan & Morgan, 1999; Dai et al, 2004)。已有的研究结果表明在不同污染水平的土壤中, 内栖型壮伟远盲蚓对镉的富集系数显著高于锌和铅, 远大于铜; 表栖型皮质远盲蚓具有更强的锌富集能力, 在高污染土壤中具有较强的铜富集能力, 在低污染土壤中则具有较高的镉富集能力(陈旭飞, 2014)。此外, Zhang (2011)通过在添加10%有机物料的金属污染土壤中接种不同蚯蚓, 发现了相似的结果。内栖型蚯蚓壮伟远盲蚓的镉、锌、铅和铜的生物富集能力均为最强, 表栖型皮质远盲蚓 和毛利远盲蚓对镉、锌和铜的生物富集能力较强, 而表栖型赤子爱胜蚓金属富集能力最弱。Wu等(2018)研究显示金属铝生物富集系数壮伟远盲蚓(0.158) > 南美岸蚓(0.087) > 参状远盲蚓(0.002)。由此可见, 食土性本地种对金属的富集能力较强, 特别是内栖型壮伟远盲蚓。

蚯蚓在取食、掘穴和排泄等生命活动过程中可提高土壤重金属的生物有效性(Yu et al, 2005; Zhang et al, 2016), 这可能与土壤pH、Eh值改变、可溶性碳与金属形成螯合物以及蚯蚓肠道内的微生物群落特征有关系(Sizmur & Hodson, 2009; Zhang et al, 2016)。蚯蚓体内微生物优势菌种特征变化与其取食的土壤和有机物料类型有关(Aira et al, 2016; 龙建亮等, 2018)。由于金属污染土壤有机质含量少、金属含量高(Li YT et al, 2009), 蚯蚓往往取食富含微生物的土壤颗粒以维持生存(Garvin et al, 2000)。这些携带重金属的菌种进入蚯蚓肠道后可能通过两种方式影响重金属的生物有效性(图1): 一方面, 一部分菌种(特征菌I)可能在蚯蚓肠道内纤维素酶、蛋白酶、磷酸酶等作用下被消化, 菌体内各种有机无机复合体固定的金属因而能够被释放出来, 在蚯蚓体内络合成其他金属形态(碳酸盐结合态或铁锰结合态等)并最终随代谢物排出体外; 另一方面, 一部分菌种(特征菌II)在蚓体肠道液的作用下可能被激活(Brown et al, 1995), 其数量、生物量或活性大幅度提高, 能够更大程度地改变蚯蚓肠道内与金属密切相关的理化特征, 进而影响重金属形态和迁移转化进程。如被激活的微生物种群作用可能引起肠道内容物pH的上升或下降, 间接影响金属的形态特征(Ma et al, 2002; Wen et al, 2004; Udovic et al, 2007; Maity et al, 2008); 也可能会造成Eh的降低, 提高Fe和Mn离子的有效性(Lin et al, 2007), 最终增加铁锰结合态金属含量; 微生物加速分解土壤有机质, 释放更多低分子有机物, 也能促进有机结合态金属的形成。代金君等(2015)发现, 蚯蚓-金属污染土壤体系中蚯蚓肠道微生物种群变化显著, 其中香味菌属(Myroides)、芽孢杆菌属(Bacillus)、鞘氨醇杆菌属(Sphingobacterium)、金黄杆菌属(Chryseobacterium)、假单胞杆菌属(Pseudomonas)、丛毛单胞菌属(Comamonas)、不动杆菌属(Acinetobacter)为优势菌群, 且与重金属的迁移转化紧密相连。因此, 探寻污染土壤中协同蚯蚓活化重金属的这些优势菌的功能及作用机制是近年的研究热点。

图1 特征菌进入蚯蚓肠道的可能途径及其对金属迁移和转化过程的影响Fig. 1 The possible pathway of microorganisms entering the earthworm gut and their effects on metal movement and transformation

4 蚯蚓在土壤复垦中的应用及其机制
4.1 在公路临时用地土壤复垦中的应用

生产建设临时占用和损毁了大量土壤。如高速公路建设临时占用土壤由于机械压实和人为践踏等, 一般具有结构性差、含水率低、土质松散和抗冲刷能力低等特点(余海龙等, 2009)。袁中友(2015)调查发现, 高速公路临时用地损毁后土壤颜色变浅、结构和层次混乱、容重增大、紧实度增强、孔隙度降低、含水量和田间持水量减少; 除土壤pH值和速效钾含量略有增加外, 有机质、全氮、碱解氮和速效磷等养分含量急剧减少, 肥力普遍降低。受损毁后土地利用、覆盖变化和土壤理化性质恶化的影响, 土壤酶活性显著降低, 土壤呼吸作用减弱。因此, 保护表土层、重构土壤物理层次和结构、科学施肥是临时用地土壤复垦的重要内容。目前以蚯蚓为主导的生物技术应用在建设用地土地复垦中的研究相对较少, 仅有袁中友等(2017a, b, 2018)报道通过施加蚯蚓粪来修复土壤。袁中友等(2017a)将类芦(Neyraudia reynaudiana)种植于高速公路工程建设损毁的土壤施加赤子爱胜蚓的粪便后, 土壤容重显著降低, 土壤孔隙度和田间持水量明显增加, 同时类芦的根系总根长、根表面积、根体积和根均直径显著增加。以蚯蚓为主导的生物技术能显著改善土壤结构和质量, 提高转化酶、脲酶、过氧化氢酶、酸性磷酸酶、β -葡萄糖苷酶、乙酰氨基葡萄糖苷酶、多酚氧化酶和过氧化物酶活性, 促进植物生长(袁中友, 2017b, 2018)。另外, 蚯蚓形成的团聚体能有效抵抗雨水冲蚀(Jouquet et al, 2007), 有利于防止公路建设用地土壤侵蚀进一步加剧。

4.2 蚯蚓对公路临时用地土壤复垦的作用机制: 蚯蚓对土壤物理结构的影响

蚯蚓对土壤结构(孔道和团聚体)的形成作用极大(张卫信等, 2007), 这与不同生态类型蚯蚓具有不同的取食偏好和生境有关。表栖型蚯蚓蚓体直径1-2.5 mm, 且无明显的蚓道, 对土壤结构的影响较小; 而内栖型蚯蚓蚓体直径2-4.5 mm, 上食下栖型蚯蚓蚓体直径4-8 mm, 且内栖型和上食下栖型蚯蚓均能显著影响土壤的透气性以及水分运移(Lavelle & Spain, 2001; Kavdir & Ilay, 2011)。Langmaack等(1999)报道L. terrestris 蚯蚓活动形成的孔道每年可达82.3 km/ha。Bastardie等(2005)发现深栖型蚯蚓活动形成的孔道远大于内栖型蚯蚓。Ernst等(2009)研究发现内栖型和深栖型的蚯蚓活动过程形成的大型孔道可造成土壤的水分流失。关于华南地区蚯蚓对土壤孔道影响的研究目前仍缺乏。蚓粪是引起土壤大团聚体总量增加的重要原因(Blanchart et al, 1997)。已有室内培养实验显示, 在赤红壤中, 内栖型蚯蚓南美岸蚓壮伟远盲蚓蚓粪产生率显著高于深栖型蚯蚓参状远盲蚓, 分别为0.118、0.076和0.039 g· g-1fw· d-1(Wu et al, 2018); 而添加10%有机物料的污染土壤中, 表栖型赤子爱胜蚓皮质远盲蚓和表内栖型蚯蚓毛利远盲蚓的产粪率显著高于内栖型蚯蚓壮伟远盲蚓, 其中毛利远盲蚓产粪率最高(0.460 g· g-1fw· d-1), 壮伟远盲蚓产粪率最低(为0.243 g· g-1fw· d-1) (Zhang, 2011; Zhang et al, 2016)。与欧洲广泛研究的A. caliginosa产粪率0.5-1.5 g· g-1fw· d-1相比, 华南地区蚯蚓产粪率相对较低(Zhang et al, 2009)。Winsome和McColl (1998)发现, 土壤水稳性大团聚体的比例随蚯蚓数量和蚓粪量的增加而增加。这些团聚体能显著降低土壤容重、增强土壤的保水能力(Six et al, 2000; 李静娟等, 2013), 微团聚体中有机质的有效保护对土壤有机质的动力学特征以及氮磷钾等其他营养元素的变化产生重大影响(Shipitalo & Protz, 1989; Barois et al, 1993)。当前, 针对不同远盲蚓对华南地区不同土壤物理结构的影响及调节机制的研究仍较少。

5 蚯蚓在茶园土壤质量提升方面的应用
5.1 蚯蚓对茶园土壤质量的提升

蚯蚓及其蚓粪对植物生长和品质的影响已有大量的报道, 特别是禾本科的水稻和玉米以及木本科的南美红木、茶树和思帝果树的生长受蚯蚓影响极其明显(Lavelle & Spain, 2001; 张聪俐等, 2013; 李静娟等, 2013)。研究显示土壤中平均30-40 g/m2蚯蚓的投入量就能显著促进作物生长(Lavelle & Spain, 2001)。在我国华南地区, 目前蚯蚓促进植物生长的应用推广仅限于茶园, 推广面积约达18万亩。茶园是典型的相对稳定的农田生态系统, 但是近几十年大量化肥的施用造成了严重的土壤板结、酸化等问题(唐劲驰等, 2008; 唐灏等, 2011)。已有研究显示添加蚯蚓能够加速有机肥的分解、促进茶园土壤生态系统的恢复(Zhang et al, 2005; Dai et al, 2007; 周波等, 2017)。Dai等(2007)将远盲蚓(以皮质远盲蚓、毛利远盲蚓、壮伟远盲蚓为主)接种到黄金桂茶园土壤, 连续3年的实验显示蚯蚓处理的土壤转化酶、脲酶、过氧化氢酶活性显著增加。唐劲驰等(2016)在金萱茶园进行连续5年田间实验研究得出相似的结果, 添加远盲蚓处理可以显著增加0-20 cm土层过氧化氢酶、脲酶、转化酶和碱性磷酸酶的活性。土壤酶活性作为土壤养分有效化强度的表征, 与茶叶的优质高产关系密切。Zhang等(2005)和唐劲驰等(2008)研究显示这一蚯蚓培肥体系能显著提高土壤有机质碳和微生物量碳、速效氮和速效磷、钾的含量。唐灏等(2011)发现该体系能够提升茶叶的品质, 使茶叶的茶多酚含量明显增加, 感官品质优于对照。周波等(2017)发现, 这一蚯蚓培肥技术对茶叶水浸出物、茶多酚影响较小, 但能显著降低茶叶中咖啡碱含量, 提升可溶性糖含量, 提高了金萱茶叶3.5-5.7%的综合品质。

5.2 蚯蚓提升茶园土壤质量的机制探讨: 蚯蚓与土壤酶活性的关系

土壤酶主要由土壤微生物分泌, 其活性是土壤质量的重要评价指标(Gil-Stores et al, 2005), 与有机质的分解、养分的循环、微生物活性等密切相关 (Paul & Clark, 1996; 张卫信等, 2007)。蚯蚓和土壤微生物以及酶的关系如图2所示: 一方面, 富含有机物的土壤颗粒被蚯蚓吞食进入蚯蚓肠道, 肠道分泌物中富含大量碳氮磷等营养元素和水, 能够“ 唤醒” 土壤中的微生物, 为其提供足够的养分、水分和能量, 影响微生物的繁殖和活性(Lavelle et al, 1995; Merino-Trigo et al, 1999); 另一方面, 微生物与蚯蚓互惠共生, 它们根据自身和土壤环境中各元素化学计量比平衡情况调整营养获取的过程, 分泌土壤酶以利于土壤有机物的分解和转化, 最终影响碳氮磷等养分的释放(Lavelle & Spain, 2001)。

图2 蚯蚓取食进程(虚线框内代表有机物进入蚯蚓肠道内进程; 实线框内代表蚓触圈)Fig. 2 Earthworm digestion processes. Dotted lines refer to earthworm gut associated processes, and solid lines extend to the earthworm drilosphere.

在蚯蚓肠道内, 酶活性特征体现了不同蚯蚓取食有机物的偏好和多样性。在热带和温带, 表栖型蚯蚓Lumbricus rubellusE. fetida肠道内纤维素酶活性极高, 表明其具有较强分解新鲜或者腐熟植物的能力(Zhang & Li, 2000)。对于内栖型蚯蚓南美岸蚓(Zhang et al, 1993)、Polypheretima elongata (Lattaud et al, 1997a)、Millsonia anomala (Lattaud et al, 1997b)、Hormogaster elisae (Garví n et al, 2000), 它们的前肠、中肠和后肠酶活性特征显示了对蔗糖、麦芽糖、淀粉、纤维素、昆布多糖、α -葡萄糖苷、β -葡萄糖苷、甘露聚糖等11种碳源的降解能力, 其中昆布多糖和β -葡萄糖苷与植物根、真菌细胞壁组分几丁质密切相关, 这些酶的存在证实了蚯蚓在有机质含量低的土壤中以植物根和真菌为食的特点(Lattaud et al, 1997; Garvin et al, 2000)。对于深栖型蚯蚓, 有限的资料显示M. guillemi相对于E. fetida肠道具有较高的蛋白酶和磷酸酶活性和较低的纤维素酶活性(Zhang & Li, 2000), 说明这些蚯蚓喜欢从地表取食富含微生物的有机物。目前对于华南地区远盲蚓的肠道内酶活性特征研究仍十分缺乏。

在蚓粪和蚓触圈中, 与有机物分解或土壤碳、氮、磷养分循环相关的酶: 如纤维素酶、淀粉酶、β -葡萄糖苷酶、脲酶、蛋白酶、碱性磷酸酶、酸性磷酸酶、过氧化氢酶和脱氢酶等的研究已成为热点(Zhang et al, 2016)。较多研究结果证实蚯蚓活动后蚓粪、土壤或有机物料酶的活性高于对照土壤(Tao et al, 2009; 张池等, 2012; 刘婷等, 2012b; Zhang et al, 2016)。刘婷等(2012b)以牛粪和稻秆为原料培养E. fetida, 研究显示伴随着E. fetida消化后的基质有机质分解、碳氮比降低, 基质的转化酶、磷酸酶活性提高, 氮素和磷素养分也显著提高。张池等(2012)接种皮质远盲蚓和壮伟远盲蚓于水稻土和菜园土中, 皮质远盲蚓对水稻土过氧化氢酶和脲酶活性的提高作用极其显著; 在菜园土中两种蚯蚓则均能显著增加脲酶活性, 壮伟远盲蚓能促进转化酶活性提高, 皮质远盲蚓能促进土壤过氧化氢酶活性提高。这些蚯蚓消化后的蚓粪的团粒结构使其具有较好的通气性、透水性和持水性以及良好的养分供应与保肥能力, 有利于提高微生物活性和酶的分泌(Ferná ndez-Luqueñ o et al, 2009)。但是也有研究显示蚯蚓活动后酶活性下降。Buck等(2000)将蚯蚓接种到压实的土壤中, 发现蚓粪中的磷酸酶活性显著降低。陈旭飞等(2014)将赤子爱胜蚓和毛利远盲蚓接种在添加污泥的水稻土和旱地土中, 结果显示毛利远盲蚓显著促进水稻土过氧化氢酶活性提高, 而两种蚯蚓在旱地土壤中则显著降低过氧化氢酶、β -葡萄糖苷酶、脲酶、N-乙酰-氨基葡萄糖苷酶、酸性磷酸酶活性。Zhang等(2016)接种赤子爱胜蚓与毛利远盲蚓于多金属污染土壤中, 发现未添加有机物料盆钵中蚓粪酶活性显著高于对照, 而添加有机物料后蚓粪酶活性显著降低。Lv等(2016)对华南人工林进行的蚯蚓控制实验, 发现南美岸蚓降低了32%的ß -葡萄糖苷酶活性和54%的N-乙酰-氨基葡萄糖苷酶活性, 土壤的碳氮磷含量不均衡和土壤可利用性磷极为亏缺是上述现象的原因。因此, 蚓触圈酶活性变化不能一概而论, 上述现象的发生与土壤紧实程度、土壤类型和自身各化学元素计量、有机质和粘粒含量、外源有机物料组分、蚯蚓品种、酶的种类等均密切相关(张池等, 2012; 陈旭飞等, 2014; Lv et al, 2016; Zhang et al, 2016)。

6 结论

蚯蚓对土壤生态系统和环境变化具有重要的影响, 但是目前多数研究均集中在欧洲和美洲。华南地区拥有丰富的蚯蚓物种资源, 已知的壮伟远盲蚓、南美岸蚓、皮质远盲蚓、毛利远盲蚓以及参状远盲蚓等对土壤酸化、酶活性、金属污染及物理结构等方面的应用和作用机制研究有限。同时, 华南地区几种蚯蚓的生理特征差异研究较为缺乏, 且大部分研究仍为小型微宇宙实验或盆栽实验, 迫切需要中、大型尺度的研究。在充分认识华南地区的蚯蚓本身特性和对生态环境影响特征的基础上, 对其土壤生态建设及环境质量管理中的潜力进行发掘, 对今后华南地区蚯蚓资源化科学利用与管理具有重大的意义。此外, 远盲蚓属蚯蚓繁育技术是进行蚯蚓技术推广的基础, 而这方面的研究仍十分缺乏, 需要继续加强。

作者声明没有竞争性利益冲突.

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