沉水植物莖葉微界面特性研究進展

董 彬,韓睿明,王國祥

1 臨沂大學資源環境學院, 臨沂 276000 2 南京師范大學環境學院, 南京 210023 3 江蘇省地理信息資源開發與利用協同創新中心, 南京 210023

沉水植物莖葉微界面特性研究進展

董 彬1,*,韓睿明2,3,王國祥2,3

1 臨沂大學資源環境學院, 臨沂 276000 2 南京師范大學環境學院, 南京 210023 3 江蘇省地理信息資源開發與利用協同創新中心, 南京 210023

沉水植物莖葉-水界面是淺水湖泊的重要界面之一,對湖泊生物地球化學循環和水環境質量具有重要影響。富營養化水體中,大量的附著物常富集在沉水植物莖葉表面,形成了特殊的生物-水微界面。對該微界面特性進行深入研究,有助于揭示沉水植物在微環境層面對富營養化水體中物質循環的調控過程和機制。沉水植物莖葉微界面具有促進水體養分轉化、改變環境因子及可溶性物質的空間分布,增加物質運輸的阻力和距離、降低植物光合作用、調控重金屬等生態功能；微界面結構及環境因子受水體營養鹽濃度、沉水植物種類及生長階段等因素的影響。對微界面結構功能的主要研究方法進行了分析總結,并對沉水植物莖葉微界面的研究前沿進行了展望。

沉水植物；微界面；功能；富營養化

富營養化水體中,大量的藻類、微生物、顆粒物、碎屑等附著在沉水植物莖葉表面,形成了特殊的生物-水微界面[1- 3]。沉水植物莖葉微界面是淺水湖泊的重要界面之一,對湖泊生物地球化學循環和水環境質量具有重要影響[4]。由于莖葉微界面內附著物復雜的物質組成,光合作用和異養過程都有可能在微界面內發生,可能會出現因這些生物通過代謝消耗或生產而造成的陡化學梯度分布。因此,微界面內環境因子及溶解性物質的分布可能與在上覆水中的分布存在很大差異[1,5-6]。微界面附著物及其內氧化還原異質微環境對植物生長發育和生態系統的養分遷移轉化可能具有重要的影響[7- 9]。沉水植物莖葉微界面作為一種特殊的微界面,關于其特性的知識可以豐富人們對莖葉微界面結構和生態功能的認識,加深對沉水植物對水環境生態調控功能的理解,促進沉水植物莖葉微界面對富營養化水體物質遷移轉化的調控過程和機制的研究。本文在總結分析當前國內外文獻的基礎上,對沉水植物莖葉微界面生態功能、影響因素和研究方法進行了綜述和分析,并對沉水植物莖葉微界面的研究前沿進行了展望。

1 沉水植物莖葉微界面生態功能

1.1 調控水體中營養物質的遷移轉化

環境微界面是在相對微觀的環境中,對物質交換、轉移、轉化、反應等具有影響的非均相介質間的微觀界面[10]。沉水植物莖葉微界面由于植物的代謝作用和附著層內好氧有機質的分解作用而存在相互分異的氧化-還原微環境,是有機物降解、物質循環及生命活動最強烈的場所,為物質的交換、降解、轉化和沉積等提供了環境條件[11- 13]。沉水植物莖葉微界面附著物還為營養物質的遷移轉化提供了物質和能源條件[14]。沉水植物由于具有比較大的比表面積,為附著物提供了巨大的附著表面。微界面附著物可大量富集水體中的氮磷和有機質,植物-附著物亦可釋放大量的可溶性有機碳(DOC),平均釋放速率可達4.57 mgC m-2h-1[15],為養分的轉化提供物質基礎。附著藻類可通過吸附顆粒物、自身生長吸收營養鹽、光合作用和代謝活動改變水體中的溶解氧(DO)、pH值等理化條件促進水體中營養物質的遷移轉化[16-17]。沉水植物莖葉表面還為附著細菌提供了巨大的生態位[18-19],克隆測序的研究表明沉水植物附著細菌的OTU 在幾十到上百的范圍內[20]。在群落結構上,Betaproteobacteria、Bacteroidetes、Alphaproteobacteria、Actinobacteria、Planctomycetes、Cyanobacteria等門類的細菌較為常見[21],其中包括大量的參與物質循環過程的功能菌,大量碳、氮、磷等相關功能菌促進了營養物質的轉化[22]。目前的研究僅初步揭示了附著細菌在元素循環過程中的功能及作用,但鮮有文獻涉及其機理方面的信息。

沉水植物莖葉微界面附著物主要是通過P吸收和促進磷的沉淀、過濾水體中顆粒態的磷,通過光合作用升高水體的pH,加速Ca-P和碳酸鹽-磷酸鹽復合體的沉淀[16],促進磷的遷移轉化。同時,沉水植物莖葉微界面是水中氨化、反硝化及厭氧氨氧化等脫氮行為機制的重要載體。沉水植物微界面附著物能通過水體理化條件、流速、自身吸收和硝化反硝化等途徑對水體氮循環產生影響[7,23-24]。Eriksson等經多年對富營養化水體中篦齒眼子菜(Potamogetonpectinatus)附著生物反硝化作用進行研究,發現附著生物反硝化作用比較重要,可與沉積物的相當[7, 25]。Toet等發現污水處理廠出水的濕地中伊樂藻(Elodeanuttallii)附著生物的反硝化作用速率(14.8—33.1 mg N m-2d-1)顯著高于(0.5—25.5 mg N m-2d-1)和水體的(0.4—3.9 mg N m-2d-1)[8]?，F有研究在一定程度上顯示了微界面對氮磷的遷移轉化具有明顯促進作用,可能進而將影響水生態系統的功能。與對海洋、湖泊沉積物-水界面物質遷移轉化的深入研究相比[26-27],對淡水植物-水界面的物質遷移轉化的研究相對較少[7, 28],難以揭示微界面物質遷移轉化的過程和機制。

1.2 改變環境因子及可溶性物質的空間分布,增加物質運輸的阻力和距離

一般來說,微界面厚度越大,環境因子及可溶性物質的分布梯度越陡,物質擴散的阻力和距離越大[1,3,6]。微界面的厚度一般通過氧氣(O2)產生的波動結合鏡下觀測表征,厚度從幾十微米至幾個毫米不等[1,3,6]。微界面厚度主要受附著層厚度、水體流速[29]、養分濃度、光照、溫度等因素的影響。運用微電極技術測定水生植物菹草(Potamogetoncrispus)[3, 6]馬來眼子菜(Potamogetonmalaianus)[1]、大葉藻(Zosteramarina)和宣藻(Scytosiphonlomentaria)[5]葉微界面O2和pH,發現空間上(2 mm范圍內),在垂直葉片表面方向由外向內,越接近植物葉表面O2濃度和pH越高,空間分布梯度越明顯,而氧化還原電位(ORP)則越接近葉表面越低[1]。初步的研究表明：在附著層較厚的沉水植物微界面內,環境因子O2濃度和pH分布梯度較陡,空間差異較大,去除附著物這一屏障后,波動幅度明顯減小[1, 3, 6],氧化還原電位亦存在類似的變化[1]。目前對其他溶解物質空間分布的研究尚比較少見。

沉水植物葉表附著物的存在可增加微界面厚度,使游離態O2、二氧化碳(CO2)、可溶性無機碳(DIC)、DOC、氮、磷等可溶物質運輸和擴散的距離和阻力增加[2, 15, 30]。葉表面游離態O2通量可通過菲克第一定律(Fick′s first law)計算,董彬等發現去除附著層之后,馬來眼子菜成熟莖葉微界面O2通量明顯增加了[1],表明微界面附著層阻礙了O2從莖葉表面向水體的遷移和擴散。微界面內其他溶解物質的運輸過程在沉積物-水界面、根-沉積物界面以及廢水生物膜中已得到深入研究[31- 33],但由于對沉水植物具有生理代謝活性,給莖葉微界面物質運輸研究帶來了一定的困難,致使微界面其他可溶性物質分布的研究尚未得到開展。

1.3 降低植物光合作用

沉水植物莖葉微界面附著物可通過遮蔭和資源競爭減緩植物光合作用和生長。光通過附著層到達植物葉表面時會發生衰減,附著層厚度越大光衰減越多；光衰減在一定條件下會降低沉水植物的光合作用速率,最終對植物生長產生重要影響[34]。Jones等發現由于附著生物對水中CO2的利用,使沉水植物葉微界面CO2濃度降低至 2 μmol/L,無機碳濃度成為沉水植物光合作用的關鍵限制因子,對沉水植物光合作用產生了不利影響[35]。微界面附著物可使沉水植物葉綠素含量發生改變、葉片枯死量增加和光合作用產量下降[1, 36]。Laugaste等認為：在富營養化湖泊藻類暴發過程中,首先發生附著生物的大量增殖,而后才發生浮游藻類暴發,并指出附著生物的大量繁殖可能是藻類暴發和沉水植物消亡的重要誘因[37]。附著生物的大量增殖可能是富營養化水體中沉水植物消亡的一個重要原因,但在附著生物大量增殖是否是沉水植物消亡的最直接原因這一問題上,目前的觀點并不一致[38-39]。一部分學者認為,由于浮游藻類大量繁殖所導致的水體透明度降低以及遮光作用所引起的水下光照缺乏是沉水植物消亡的直接原因；但還有人認為是附著生物與水生植物對營養鹽和光等生態資源的競爭以及其產生的代謝產物對沉水植物光合作用的抑制,可能是造成沉水植物在富營養化水體中退化的關鍵[40]。研究證實,附著生物對沉水植物的抑制作用比營養鹽更加直接,對沉水植物產生遮蔭和資源競爭作用,降低了沉水植物的光合作用,影響了沉水植物的生長發育,加速沉水植物退化甚至消失[6, 9, 41]。

1.4 對重金屬的調控作用

與挺水植物和浮葉植物相比,沉水植物對水體中的重金屬有較強的吸收作用,主要通過吸附-解吸、沉積-溶解、離子交換、螯合-分解和氧化-還原反應等過程進行[42-43],重金屬進入沉水植物體內后,主要以螯合態和毒性較大的可溶態的形式存在。重金屬離子在進入植物前首先接觸微界面附著物這一高度異質性環境,其中的附著藻類可吸收重金屬[44]；其中的非生物有機成分可與重金屬離子結合,降低重金屬離子活度,調節重金屬吸收速率；其中的氧化還原微環境可能改變重金屬離子理化反應活性,影響重金屬吸收速率。因此,理論上沉水植物莖葉微界面附著物在水體重金屬離子進入植物莖葉過程中發揮一定的調控作用。雖然對沉水植物吸收重金屬的研究已相當深入細致,但沉水植物莖葉微界面對重金屬的調控作用的研究尚比較欠缺,但具體的調控過程和機制還有待進一步探究。

2 沉水植物莖葉微界面的影響因素

沉水植物莖葉微界面的影響因素比較多,如植物種類、生長階段、光照、水體營養狀態、流速、生境等均可對微界面結構和功能產生影響。不同種類的植物葉片由于其獨特的化學組成、物理結構、葉片分泌或滲出的物質,如糖類、脂蛋白、有機酸、酚類等,它們作為微生物和藻類細菌生長的營養物質、干擾物質或者信號轉導物質,都會對微界面附著物的結構、數量和多樣性造成影響[19]。隨著植物進入生長期,附著物持續增加,附著層和擴散邊界層厚度逐漸增大,植物生理活性逐漸增強,微界面環境因子如DO、pH和ORP波動幅度和空間差異逐漸增大；進入衰亡期,則出現相反的變化趨勢。在生長期,由于附著物比較稀疏,微界面主要受植物的影響。在衰亡期,由于植物生理活性的降低和附著物的持續積累增厚,微界面主要受附著物的影響[3]。

光照對植物莖葉微界面的影響主要體現在兩個空間等級。光照隨著水體深度的增加而減弱,也會隨著進入附著生物內部的深度而削弱。光照隨著深度的增加而減弱主要是受懸浮固體的影響,進而影響植物生長和附著生物的群落組成[45]。附著生物隨著深度梯度受光照調節而形成群落結構、外形、密度和功能上的差異。附著生物群落自身也可以強烈地減弱光照,能夠極大的改變到達宿主植物的光照質量[46]。水體營養狀態可影響微界面厚度和結構。微界面附著物是水生態系統中的重要化學調節器,在其生長過程中能大量吸收水體和宿主中的養分。隨著營養鹽負荷的增加,沉水植物莖葉微界面附著物增加[9, 47]。在超富營養化水體中,透明度較低,但附著生物比浮游藻類更能適應低光強環境；在較高濃度的氮、磷和光照充足的情況下,附著生物的生物量能達到最大,對氮、磷的吸收和轉化率也較高。水體流速對微界面的影響研究主要集中在沉積物-水微界面[48]和生物膜[49]上,對沉水植物-水微界面的研究較少[50-51]。一般來說,隨著流速的增大,微界面厚度降低,附著物厚度降低,促進微界面物質遷移轉化[48, 51]。

3 研究方法

3.1 對微界面結構的研究

對沉水植物莖葉微界面結構研究方法進行了分析總結(表1)。光學顯微鏡只能大體觀測到微界面的表面結構,協助檢測微界面附著物的全貌。聲學和光學速度計可用來描述附著生物群落附近和內部的水力條件、去向和來自附著生物的邊界層運輸。后來發展起來的掃描電鏡技術大大促進了人們對微界面結構的了解[52- 54]。其中環境掃描電子顯微鏡,沉水植物樣品可不經任何前處理,在環境真空條件下直接分析的微界面結構,可更直觀地呈現微界面的真實結構,是研究沉水植物莖葉微界面結構的理想工具。

表1 沉水植物莖葉微界面結構研究方法比較

3.2 對微界面環境因子和可溶性物質分布的研究

4 研究展望

近幾十年來,淡水沉水植物莖葉微界面的研究得到了快速發展,對沉水植物莖葉微界面附著微生物、藻類、微界面理化指標、硝化作用、反硝化作用過程以及氮循環主要功能細菌已展開研究,并逐漸受到越來越多的關注。但是,由于沉水植物莖葉微界面的研究涉及植物生理生態學、環境化學、生物地球化學和微生物學等多種學科,同時還有賴于先進的分析測試手段和微觀觀測手段的融合,因此對沉水植物莖葉微界面特性的研究亟需加強。今后的研究重點應集中在如下幾方面：

(1)建立沉水植物微界面各指標的測定方法。綜合利用掃描電鏡技術、高分辨率微電極測定技術、微量化學分析技術、分子生物學技術和同位素示蹤技術,對沉水植物莖葉微界面結構組成、環境特征及影響因素等進行深入研究,揭示微界面的時空變化規律,闡明微界面在富營養化水體中的生態功能。

(2)加強沉水植物莖葉微界面養分物質遷移轉化主要過程的研究,探明微界面結構組成與養分轉化功能的耦合關系,揭示微界面結構組成、微環境變化對養分循環的驅動和調控機制。

(3)在野外調查研究的基礎上,開展受控條件下的實驗室長期研究,探討不同影響因素下沉水植物微界面的結構特征及功能變化,進一步建立可溶物質的分布和運輸模型,提出沉水植物莖葉微界面理論。

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Research advances in and perspectives on characteristics of the micro-boundary layer around leaves and stems of submerged macrophytes

DONG Bin1,*, HAN Ruiming2,3, WANG Guoxiang2,3

1CollegeofResourceandEnvironment,LinyiUniversity,Linyi276000,China2SchoolofEnvironment,NanjingNormalUniversity,Nanjing210023,China3JiangsuCenterforCollaborativeInnovationinGeographicalInformationResourceDevelopmentandApplication,Nanjing210023,China

Submerged macrophytes constitute an important component of shallow aquatic ecosystems. They provide most of the accessible surface area, constant survival substrates, and available nutrients for periphyton, which remains attached to the stem and leaf surfaces of submerged macrophytes and forms a special bio-water boundary layer. As one of the most important interfaces in shallow lakes, the submerged macrophyte-water boundary layer plays roles in macrophyte growth, biogeochemical cycling, water environment maintenance, and ecological regulation. The present study summarizes the research advancements regarding characteristics of the micro-boundary layer (MBL) around leaves and stems of submerged macrophytes. The ecological functions, biotic and environmental factors, and research methods are identified and reviewed. Perspectives for the focus of future research on MBL around submerged macrophytes are raised.The MBL around submerged macrophytes has important ecological functions. The dense periphyton in MBL exerts negative effects on photosynthesis in submerged macrophytes, creates a barrier hindering the transport of dissolved substances, such as O2, and leads to the degradation and even disappearance of submerged macrophytes in eutrophic waters. The plant stress derived from pollutants may be alleviated because of the periphytic barrier in the MBL. The epiphytic bacteria in the MBL can be of considerable importance for nutrient transformation and cycling in eutrophic ecosystems. Periphyton is an assemblage of algae, bacteria, fungi, protozoan, inorganic matter, and organic detritus that remains attached to submerged macrophyte surfaces where significant spatio-temporal variations exist in the MBL. The heterogeneity of micro-environmental parameters is the key factor shaping the MBL around submerged macrophytes, given the complex constituents, changing spatial structure, and fluctuation of oxidation-reduction status within this microcosm. At the spatial heterogeneity, in the vertical direction of stem and leaf surfaces, O2concentration and pH in the MBL increase markedly with decreasing distance to the surface of leaves and stems and peak at the surface. The trend of the oxidation-reduction potential (ORP) is reverse.Plant species and growing stages are biotic factors that affect the MBL, and nutrients load, light intensity, flow velocity, and habitat are the major environmental factors. The growth stages of macrophytes create large fluctuations and dynamics in O2, pH, ORP, and soluble substrates at the surface of stems and leaves by changing the thickness of the diffusive boundary layer around the macrophyte. O2concentration and pH in the MBL around the leaves and stems of submerged macrophytes increase when macrophytes begin the rapid growing stage, which is accompanied by gradually increasing spatial differentiation. O2concentration and pH in the MBL around the leaves and stems reach peaks at the stable growth stage, and increase slightly or decline when the periphyton layer begins the declining stage. However, the ORP shows the opposite trend to that of O2, and pH. MBL is mainly affected synergistically by plant physiological and periphyton characteristics during the life cycle of macrophytes. Environmental factors affect the MBL via periphyton composition, periphyton mass, and macrophytes growth. Scanning electron microscopy, high spatial resolution of microsensors, microchemical analysis, molecular biology techniques, and isotope tracer techniques are applicable approaches for the study of the characteristics of MBL; however, they have not yet been comprehensively utilization. To further investigate the leaf and stem MBL, we must focus on establishing standard methods and models of the MBL structure and functions to verify the modulation processes and mechanism of the MBL on the biogeochemical cycling in eutrophicated waters. Long-term ecological research under controlled conditions is required.

submerged macrophytes; micro-boundary layer; functions; eutrophication

國家自然科學基金資助項目(41173078,41403064)； 江蘇省自然科學基金青年基金資助項目(BK20140922)；江蘇省教育廳高校自然科學研究面上項目(14KJB610007)

2015- 11- 11;

日期:2016- 08- 02

10.5846/stxb201511112288

*通訊作者Corresponding author.E-mail: dongbin@lyu.edu.cn

董彬,韓睿明,王國祥.沉水植物莖葉微界面特性研究進展.生態學報,2017,37(6):1769- 1776.

Dong B, Han R M, Wang G X.Research advances in and perspectives on characteristics of the micro-boundary layer around leaves and stems of submerged macrophytes.Acta Ecologica Sinica,2017,37(6):1769- 1776.