祝國榮，張 萌，王芳俠，高 陽，曹 特，倪樂意**

(1：河南師范大學(xué)水產(chǎn)學(xué)院，新鄉(xiāng) 453007)(2：中國科學(xué)院水生生物研究所東湖湖泊生態(tài)系統(tǒng)試驗(yàn)站，武漢430072)(3：江西省環(huán)境保護(hù)科學(xué)研究院，南昌 330029)

從生物力學(xué)角度詮釋富營養(yǎng)化引發(fā)的水生植物衰退機(jī)理

祝國榮1,2，張 萌3，王芳俠1，高 陽1，曹 特2，倪樂意2**

(1：河南師范大學(xué)水產(chǎn)學(xué)院，新鄉(xiāng) 453007)(2：中國科學(xué)院水生生物研究所東湖湖泊生態(tài)系統(tǒng)試驗(yàn)站，武漢430072)(3：江西省環(huán)境保護(hù)科學(xué)研究院，南昌 330029)

水體富營養(yǎng)化誘發(fā)的水生植物衰退機(jī)理已成為近年來水域生態(tài)學(xué)領(lǐng)域的研究熱點(diǎn). 本文系統(tǒng)闡明了目前有關(guān)水生植物生物力學(xué)性能及其對(duì)水體富營養(yǎng)化的響應(yīng)和其在該進(jìn)程中水生植物衰退過程中的作用等研究進(jìn)展. 現(xiàn)有研究表明水生植物生物力學(xué)性能主要包括莖/葉/葉柄的抗拉性能(挺水植物為莖/葉柄的抗彎性能)和根的錨定性能；受水體富營養(yǎng)化主要環(huán)境變量(富營養(yǎng)底泥、水體高濃度氮磷和可利用光缺乏)的顯著影響且具種間差異；還與生長、形態(tài)、生物量分配、組織結(jié)構(gòu)、代謝等其他受水體富營養(yǎng)化顯著影響的指標(biāo)密切相關(guān)，且在應(yīng)對(duì)水體富營養(yǎng)化時(shí)與生物力學(xué)間具有一定的協(xié)同作用；此外，生物力學(xué)性能受損不僅阻斷植株的“生命進(jìn)程”，還嚴(yán)重削弱斷枝后植株的資源獲取能力和斷枝的擴(kuò)散定植能力，極大降低其適合度. 根據(jù)野外調(diào)查和現(xiàn)有研究結(jié)果，生物力學(xué)性能的改變的確在富營養(yǎng)化水體水生植物衰退進(jìn)程中起到關(guān)鍵作用. 生態(tài)系統(tǒng)是多因子共同作用的綜合系統(tǒng)，但目前的水生植物生物力學(xué)性能研究主要集中在水體富營養(yǎng)化的3大特征因子，亟需進(jìn)一步深入系統(tǒng)開展隨水體富營養(yǎng)化而改變的溶解氧、藻毒素、食草動(dòng)物等其他因子的影響研究，以便更加全面真實(shí)地詮釋水體富營養(yǎng)化造成水生植被衰退的生物力學(xué)機(jī)理.

水生植物；生物力學(xué)；富營養(yǎng)化；衰退機(jī)理

近半世紀(jì)以來，國內(nèi)外關(guān)于水體富營養(yǎng)化所誘發(fā)的水生植物衰退的學(xué)術(shù)活動(dòng)與報(bào)道層出不窮，探討富營養(yǎng)化水體中水生植物衰退已然成為當(dāng)今水生態(tài)學(xué)研究的一個(gè)熱點(diǎn). 富營養(yǎng)化水體中水生植物衰退主要原因是來自于富營養(yǎng)化水體中過量氮磷等營養(yǎng)元素和由這些營養(yǎng)增加所引發(fā)浮游植物的大量生長繁殖以及這些浮游植物過量生長所導(dǎo)致的水體可利用光和溶解氧的減少、藻毒素、硫化物等級(jí)聯(lián)效應(yīng)方面，對(duì)水生植物的形態(tài)、生物量分配、組織結(jié)構(gòu)和代謝等方面產(chǎn)生顯著影響[1-6]，從而抑制了水生植物的生長，限制了最大分布水深，阻斷了其生活史，最終導(dǎo)致富營養(yǎng)化水體中水生植物的大面積衰退[7-9].

生物力學(xué)性能是指運(yùn)用力學(xué)原理和方法研究生命系統(tǒng)的結(jié)構(gòu)與功能的一類指標(biāo)，它是衡量流體環(huán)境中生命系統(tǒng)與環(huán)境因子(如重力、風(fēng)力、土壤、水流、波浪等)和生物因子(如植物、動(dòng)物和微生物等)的相互作用過程(如接觸、擠壓、粘附、滲透、捕捉或傳輸?shù)任锢碜饔?中的行為特征、適應(yīng)能力和作用程度的重要變量[10-20]. 盡管水生植物應(yīng)對(duì)水體富營養(yǎng)化的響應(yīng)研究主要集中在生長、形態(tài)、生物量分配、組織結(jié)構(gòu)和代謝等方面[1-6]，近年來一系列研究表明水體富營養(yǎng)化帶來的底泥富營養(yǎng)、水體高濃度氮磷和可利用光缺乏等主要環(huán)境變量均可顯著影響水生植物的生物力學(xué)性能[21-25]. 水生植物生物力學(xué)性能是水生植物適應(yīng)水生生境過程中無時(shí)無處不在的，由波浪、流速和食草動(dòng)物等引起的機(jī)械脅迫的主要指標(biāo)[26-28]. 本文以水生植物的生物力學(xué)性能為核心，綜述了水生植物的生物力學(xué)性能特征及其對(duì)水體富營養(yǎng)化的響應(yīng)，并總結(jié)分析其在富營養(yǎng)化水體中對(duì)水生植物衰退的貢獻(xiàn)等.

1 水生植物的生物力學(xué)性能特征

1.1 水生境的機(jī)械脅迫類型及其特征

不同于陸生植物所受的機(jī)械脅迫類型，水生植物尤其是根生水生植物所受機(jī)械脅迫類型主要有波浪、水流、船舶以及食草動(dòng)物等[29-30]. 但由于水體相對(duì)的高密度(淡水和海水密度分別是空氣密度的833和854倍[31])，同一物體所受到2 m/s水流速度的作用力相當(dāng)于58 m/s風(fēng)速的作用力，即：相同速度下，水生境的機(jī)械脅迫作用力約是陸生生境機(jī)械脅迫作用力的29倍[26,32-33].

由風(fēng)帶來的波浪、水流等類型的機(jī)械脅迫大小與湖泊、河流、海岸帶等水體的水深、受風(fēng)面湖泊的長度和湖盆坡度等[26,29,34-36]有關(guān)；而波浪、流速等機(jī)械脅迫作用于水生植物植株上的作用力大小還與植物密度、植株種類(如生長型[37-38]和葉形[39-40])、植株大小[41-42]以及植株立地角度(即植株底部半米與底泥表面所成的角度，立地角度從40°到70°時(shí)所受的機(jī)械脅迫力是垂直時(shí)的1/2到2/3[29])密切相關(guān).

1.2 水生植物所受的機(jī)械脅迫力及其對(duì)水生植物的影響

水生生境中波浪、水流等機(jī)械脅迫主要產(chǎn)生3種作用于植株上的機(jī)械脅迫作用力(圖1)：平行于水流的拖曳作用力(FD, drag force)、速度力(FA, accelerational force)以及垂直于水流的抬升作用力(FL, lift force)[36,41-43]，其中FD為主要作用力，而FA在水流速度增加或降低時(shí)，其方向也與FD方向一致或相反[44]. 由于水體浮力大，其他大多根生水生植物，如：沉水植物、浮葉植物，通常不需要強(qiáng)壯的莖來支撐植株本身重量，而且具有很大的柔韌性，使得植株能夠沿著機(jī)械脅迫方向彎曲并通過重構(gòu)改變植株的大小和形態(tài)[45]，以減少機(jī)械脅迫與植株表面的摩擦力與接觸面積，最終降低作用于植株上的機(jī)械脅迫力[41-42]. 因而，一般認(rèn)為在水流運(yùn)動(dòng)方向不固定的水環(huán)境中，大多根生水生植物受到的主要機(jī)械脅迫作用力是沿植株方向的拖曳力，起到拉伸植株的作用，即造成拉伸脅迫(σ+)[46-48]，故又稱拉伸作用力[45]. 而挺水植物，類似大多數(shù)陸生植物(作物、樹木等)需要強(qiáng)壯的莖來支撐植株重量，即重力(FG，gravitational force)，以便使植株保持直立，因而盡管植株沉沒在水中和暴露在空氣中的部分所受機(jī)械脅迫分別來自波浪和風(fēng)，但其作用于植株上的作用力仍為平行于波浪、水流或風(fēng)的機(jī)械作用力，即拖曳作用力，但表現(xiàn)為垂直于植株方向的彎曲作用力(類似于作用于其他水生植物上的平行于水流的拖曳作用力)[49-50]，即由受風(fēng)面的拉伸(σ+)和背風(fēng)面的擠壓(σ-)組合而成[46,48](圖1). 此外，值得一提的是外來種粉綠狐尾藻(Myriophyllumaquaticum(Vell.) Verdcourt)，它主要生長在沼澤區(qū)或經(jīng)常水位波動(dòng)的靜水或緩流水體的淺水區(qū)，但能夠通過異形葉性(氣生葉和沉水葉)來適應(yīng)水-陸生境轉(zhuǎn)化，最長能夠耐受9個(gè)月的只有土壤基質(zhì)保持水飽和狀態(tài)低水位時(shí)期[51-53]，因此我們推測它所受的主要機(jī)械脅迫作用力仍是平行于風(fēng)、波浪、水流的作用力，但當(dāng)植株完全淹沒水中時(shí)該作用力表現(xiàn)為平行于植株的拖曳作用力(類似于大部分水生植物)，但當(dāng)植株部分/全部暴露于空氣中時(shí)表現(xiàn)為垂直于植株的彎曲作用力(類似于挺水植物). 事實(shí)上隨著全球氣候變化引發(fā)的異常降雨情勢和水利工程調(diào)控的水文節(jié)律使得水生態(tài)系統(tǒng)，如湖泊、河流、濕地、海岸帶等洪水期淹水和枯水期退水的水深變化節(jié)律發(fā)生明顯變化[48,54-56]，使得水生植物的生境發(fā)生水-陸生境轉(zhuǎn)換，其中沉水植物的生境會(huì)在長期干枯之后面臨著陸地生境的機(jī)械脅迫，而挺水植物則會(huì)在長期的洪水期面臨著完全水生境拖曳力，這些因水-陸生境導(dǎo)致機(jī)械脅迫作用到植株上的機(jī)械脅迫作用力，即拖曳力-彎曲作用力間轉(zhuǎn)換，會(huì)挑戰(zhàn)植物長期適應(yīng)各自生境形成的生理生態(tài)和生物力學(xué)適應(yīng)性，進(jìn)而打破現(xiàn)有的水生植物群落結(jié)構(gòu)(圖1)[48].

圖1 水生生境和陸生生境中各自的主要環(huán)境作用力、機(jī)械脅迫類型(細(xì)箭頭表示)、作用于植株上的主要力(粗箭頭表示)及植株的主要生物力學(xué)性能示意圖(改自文獻(xiàn)[44,46-48])Fig.1 Schematic overview of the main environmental forces, mechanical forms (thin arrows) and main forces (thick arrows) acting on a sessile plant in aquatic and terrestrial environment as well as the main biomechanical properties of plants

盡管大多水生植物能夠隨水流擺動(dòng)避開垂直水流的抬升力，一旦波浪、水流等機(jī)械脅迫作用于植株上的拖曳力超過水生植物本身的柔韌性能臨界值，植株就會(huì)發(fā)生斷枝、拔根等機(jī)械損傷[26,39,43]. 其中，斷枝，尤其是植株具有頂芽或頂端分生組織的頂段部位的斷裂，會(huì)造成植株生物量、能量和光合作用能力多重?fù)p失[23,57-59]；且這種由機(jī)械脅迫造成的非主動(dòng)斷枝的擴(kuò)散和定植能力遠(yuǎn)低于該種植物在生長階段后期(當(dāng)植株生物量達(dá)最大值后完成須根、細(xì)胞木質(zhì)化和碳水化合物等準(zhǔn)備時(shí))自發(fā)形成的主動(dòng)斷枝的擴(kuò)散和定植能力[53,60-61]，因?yàn)闄C(jī)械脅迫造成的斷枝損失最終會(huì)影響水生植物的生存、繁殖、分布和群落結(jié)構(gòu)[31,37]. 拔根一般有根斷裂、須根從底泥中滑脫出來、根系整體被移除3種情況[26,62]，對(duì)水生植物而言主要是根滑脫或根整個(gè)系統(tǒng)被移除方式的拔根[26]. 拔根不僅會(huì)嚴(yán)重?fù)p傷水生植物尤其是多年生水生植物依靠地下組織進(jìn)行繁殖的能力，直接導(dǎo)致挺水植物和浮葉植物的死亡，還會(huì)增加水生植物恢復(fù)工程的定植難度[23,37,63].

1.3 水生植物的主要生物力學(xué)性能特征

水陸生境的差異造成水陸植物生長、形態(tài)和組織結(jié)構(gòu)等方面的巨大差異：大多數(shù)陸生植物(作物、樹木等)和挺水植物主要靠植物的莖支撐植株重量，使植株保持直立；生活史上基本完全淹水的根生水生植物(如浮葉植物和沉水植物)由于水體的浮力作用，類似于攀爬、匍匐陸生植物，不需要莖/葉/葉柄的支撐就能使植株在靜水時(shí)保持直立狀態(tài)，但需要莖/葉/葉柄有足夠的柔韌性使得植株能夠承受水體流動(dòng)帶來的一定程度的拖曳負(fù)荷[41-42,49-50]. 因而大多數(shù)陸生和挺水植物采取以提高抗彎性能為代表的“強(qiáng)度和硬度”機(jī)械抵抗應(yīng)對(duì)策略，而完全淹水的根生水生植物則類似陸生攀爬匍匐植物采取以提高抗拉性能為代表的“柔韌和延展”機(jī)械抵抗應(yīng)對(duì)策略來適應(yīng)各自生境的機(jī)械脅迫類型(圖1)[28,64]. 然而，由于全球氣候變化和人類活動(dòng)日益加劇的雙重作用會(huì)導(dǎo)致湖濱帶、河岸、濕地、海岸帶等水-陸生境轉(zhuǎn)變節(jié)律發(fā)生變化[48,54-56]，沿岸帶水生植物需要提升以抗彎性能為代表的“強(qiáng)度和硬度”(機(jī)械抵抗應(yīng)對(duì)策略使植株能直立生長以適應(yīng)枯水期短暫出現(xiàn)的陸生生境條件下的機(jī)械脅迫)[48].

與陸生植物類似，根生水生植物也需要通過根的錨定作用和底泥黏著作用來固定植株[26,37,65]，這在強(qiáng)波浪、暴雨以及植被生態(tài)修復(fù)初期至關(guān)重要，沒有足夠的定植能力，植株往往會(huì)被大面積連根拔起，最終影響生長、分布、繁殖、甚至存活. 陸生植物絕大多數(shù)養(yǎng)分僅來源于土壤基質(zhì)，但根生水生植物不僅可通過根系從底泥沉積相中吸取營養(yǎng)，還能通過莖葉等營養(yǎng)組織器官從上覆水相中獲取營養(yǎng)[2,66]. 加上水體浮力很大，除挺水植物存在類似作物、樹木等陸生植物保持植株直立狀態(tài)的主根外，其他水生植物的根與攀爬和匍匐植物的根類似,均為細(xì)且密集的須根[26,30]，這對(duì)大部分水生植物而言不僅可擁有較大的比表面積來增加營養(yǎng)物質(zhì)吸收，而且還能減少整個(gè)植株根生物量分配比率，將利于植株伸長和可利用光獲取能力增長. 因而，除挺水植物外，水生植物的根類似于攀爬和匍匐植物的根,主要受到拉伸作用力，且其根錨定強(qiáng)度與整個(gè)根系水平分布范圍以及底泥的類型有關(guān)[26,67].

2 水生植物生物力學(xué)性能對(duì)水體富營養(yǎng)化的響應(yīng)

由人類活動(dòng)(城市污水、農(nóng)業(yè)污水排放等)帶來的水體富營養(yǎng)化主要體現(xiàn)在以硝態(tài)氮、銨態(tài)氮為主要形態(tài)的高濃度氮和以正磷酸鹽為主要形態(tài)的高濃度磷[68-69]. 水體高濃度營養(yǎng)物質(zhì)促進(jìn)藻類過度生長繁殖，從而降低水體可利用光，而長時(shí)間的沉積作用會(huì)導(dǎo)致底泥營養(yǎng)水平的增加,進(jìn)而影響底泥顆粒結(jié)構(gòu)、溶解氧水平、微生物群落組成和黏著能力[26,70-71]. 研究表明富營養(yǎng)化帶來的底泥營養(yǎng)類型、水體營養(yǎng)水平和水體可利用光多少等主要環(huán)境變量均會(huì)顯著影響水生植物的生物力學(xué)性能.

2.1 富營養(yǎng)化底泥對(duì)水生植物生物力學(xué)性能的影響

研究表明，水體富營養(yǎng)化生境的底泥不僅營養(yǎng)水平高，其黏著力(<0.2 kPa)也比其他營養(yǎng)水平水體底泥的(>1.0 kPa)小[26]，生長在富營養(yǎng)化底泥的水生植物根系也通常較短較少[2-3,24,66]，而底泥黏著力和植株根系是決定植株根錨定性能的主要指標(biāo)(表1)[26-27,72]，因而生長在富營養(yǎng)化底泥中的植物具有較低的根錨定性能[26]，極易發(fā)生根滑脫或根整個(gè)系統(tǒng)被移除的拔根機(jī)械損傷，不利于富營養(yǎng)化水體中水生植物修復(fù)和重建工程中植被的定植以及受機(jī)械損傷的植株地下組織儲(chǔ)藏物質(zhì)的保存.

表1 與水陸生植物根錨定性能相關(guān)的根形態(tài)(改自文獻(xiàn)[73])

與陸生植物類似[92-94]，通常生長在中營養(yǎng)水平底泥的植株較生長在富營養(yǎng)底泥的植株的莖/葉/葉柄具有較高的生物力學(xué)性能[22-25]. 本人前期室內(nèi)研究發(fā)現(xiàn)與富營養(yǎng)底泥(總磷(TP)=1.40 mg/g DW、總氮(TN)=6.32 mg/g DW、有機(jī)質(zhì)(OM)=11.70%)和貧營養(yǎng)底泥(0.1 cm 細(xì)砂：TP、TN和OM含量均低于檢測限)相比，中營養(yǎng)水平底泥(TP=0.70 mg/g DW、TN=3.41 mg/g DW 、OM =8.13%)更有利于輪葉黑藻(Hydrillaverticillata)形成更大的抗拉應(yīng)力和彎曲能力[23]；而富營養(yǎng)水平底泥(TP=2.43 mg/g DW、TN=3.56 mg/g DW、OM=7.70%)較中營養(yǎng)水平底泥(TP=0.57 mg/g DW、TN=2.44 mg/g DW、OM=4.15%)更有利于穗狀狐尾藻(M.spicatum)形成較大的抗拉應(yīng)力、彎曲應(yīng)力和較小的拉伸率和結(jié)構(gòu)剛性[24-25]；但野外調(diào)查發(fā)現(xiàn)：隨著湖泊營養(yǎng)水平增加，穗狀狐尾藻的抗拉應(yīng)力和拉伸率以及篦齒眼子菜(Potamogetonpectinatus)的抗拉應(yīng)力均顯著增加；而篦齒眼子菜的拉伸率在中營養(yǎng)水平湖泊最大，微齒眼子菜(P.maackianus)的抗拉應(yīng)力和拉伸率則不受湖泊營養(yǎng)水平的顯著影響[25]. La Nafie等[22]野外原位實(shí)驗(yàn)發(fā)現(xiàn)，與原位基質(zhì)相比，通過添加0.5 kg/m2緩釋肥(N∶ P∶ K=18∶ 9∶ 3; Osmocote?)模擬獲得的富營養(yǎng)水平底泥會(huì)降低喜鹽草(Halophilaovalis)的抗拉強(qiáng)度而增加其拉伸率，而對(duì)二藥藻(Haloduleuninervis)的抗拉性能沒有顯著影響. 這一方面可能是由于植株的生物力學(xué)性能與其形態(tài)特征密切相關(guān)，如在上述各研究中各水生植物的莖/葉不僅在生物力學(xué)性能方面，也在形態(tài)(莖的橫截面面積或葉的長、寬和厚度)方面對(duì)底泥營養(yǎng)水平具有不同程度的響應(yīng)[22-24]，其中常生長在沙質(zhì)底泥的海草如喜鹽草葉片長度、寬度和厚度均隨底泥營養(yǎng)水平增加而增加，而能夠在多種類型底泥生長的海草如二藥藻的葉子寬度和厚度則沒有顯著變化[22]；另一方面也可能與兩種植物本身的生長環(huán)境有關(guān)，喜鹽草本身多生長在砂質(zhì)基質(zhì)，而二藥藻則能在多種基質(zhì)上生長[95].

2.2 水體營養(yǎng)水平對(duì)水生植物生物力學(xué)性能的影響

2.3 富營養(yǎng)化水體可利用光缺乏對(duì)水生植物生物力學(xué)性能的影響

植物可利用光的缺乏是富營養(yǎng)化引發(fā)藻類過量生長帶來的重要結(jié)果[8,100]，不僅顯著地影響水生植物的形態(tài)和生理生化過程[1,3-5,99]，也會(huì)顯著地影響水生植物的生物力學(xué)性能[22,59]. La Nafie等[22]研究發(fā)現(xiàn)遮光處理顯著增加二藥藻的拉伸率而降低其抗拉應(yīng)力；但與之相比，遮光條件下喜鹽草具有相對(duì)較大的抗拉應(yīng)力和較小的拉伸率. 祝國榮等[59]通過野外原位浮床實(shí)驗(yàn)發(fā)現(xiàn)在隨著水深帶來的低可利用光(15.416～290.268 μmol/(m2·s))生境下，5種實(shí)驗(yàn)水生植物中，只有金魚藻(Ceratophyllumdemersum)能夠在一定程度上調(diào)整其生物力學(xué)性能，例如增加其莖抗拉性能和根的錨定性能(其根系則在中度水深區(qū)最大，此時(shí)可利用光約為69.372 μmol/(m2·s))來適應(yīng)此生境變化；而微齒眼子菜、穗狀狐尾藻、輪葉黑藻和竹葉眼子菜(P.malaianus)這4種水生植物的根系和莖的生物力學(xué)性能(抗拉應(yīng)力和/或拉伸率)呈顯著降低趨勢；此外，輪葉黑藻和竹葉眼子菜的生物力學(xué)性能在淺水區(qū)時(shí)最大，在中度水深區(qū)最小，而微齒眼子菜則在中度水深區(qū)具有最大的莖生物力學(xué)性能.

3 在水體富營養(yǎng)化條件下生物力學(xué)性能變化在水生植物衰退中的作用

3.1 生物力學(xué)損傷對(duì)水生植物的影響

根據(jù)水動(dòng)力學(xué)研究，水生境機(jī)械脅迫力隨著水深呈指數(shù)下降[37,43]，這表明，處于任何水深的根生水生植物都會(huì)受到一定的機(jī)械脅迫作用力，而且莖/葉/葉柄的底段部分所受到的機(jī)械作用力遠(yuǎn)遠(yuǎn)小于其他部位，尤其是頂部. 而水生植物的個(gè)體發(fā)生學(xué)的差異會(huì)造成水生植物莖/葉/葉柄等部位從底端到頂端的物質(zhì)含量和解剖結(jié)構(gòu)間存在顯著差異[23, 30]，因而，水生植物的莖/葉/葉柄的生物力學(xué)性能從底端到頂端具有顯著差異[23-24,30]. 水生植物的莖/葉/葉柄的生物力學(xué)性能、根錨定性能與機(jī)械脅迫作用力的大小共同決定著植株是否會(huì)發(fā)生機(jī)械損傷、發(fā)生何種類型機(jī)械損傷(如：斷枝、拔根等)以及發(fā)生機(jī)械損傷的程度(植株的頂段、中段或底段；大型海藻的固著器、柄部或葉片)(圖2)[26,101-102].

圖2 根生水生植物在面臨波浪、水流等機(jī)械脅迫時(shí)，由于作用于植株上的作用力、植株根錨定性能和莖/葉/葉柄的生物力學(xué)性能不同，會(huì)出現(xiàn)的機(jī)械損傷情況(改自文獻(xiàn)[26])Fig.2 Conceptual model showing the potential fates of a rootedmacrophyte subjected to mechanical force encountered by aquatic macrophytes, as cohesive strength of the sediment, root anchorage strength, and the biomechanical indices of stems/leaves/petioles varies

盡管通過斷枝或地下組織如根狀莖、匍匐莖、塊莖等營養(yǎng)器官進(jìn)行的營養(yǎng)繁殖是水生植物的重要繁殖擴(kuò)散方式[26]，且前期大多數(shù)研究認(rèn)為莖底段斷裂是對(duì)根部等地下組織器官的保護(hù)[26,30,65]，不僅能夠增強(qiáng)受機(jī)械損傷的植株通過地下組織器官再次萌發(fā)生長的能力，也通過增加斷枝的長度和生物量提高了斷枝的擴(kuò)大和再生能力[103]. 但是與主動(dòng)斷枝不同，機(jī)械脅迫帶來的非主動(dòng)斷枝因?yàn)槿狈χ鲃?dòng)斷枝形成前期的物質(zhì)能量儲(chǔ)備和須根的形成，通常具有較低的擴(kuò)散、定植、發(fā)芽等再生能力[60-61,104]. 因而，在富營養(yǎng)化生境，相對(duì)底段斷裂而言，更易發(fā)生具有頂芽或頂端分生組織和葉密集生長區(qū)的頂段斷枝. 有研究表明[105],10%～30%和70%的葉子損傷可分別降低其飽和光合速率至40%和60%，這預(yù)示著斷枝后的植株會(huì)有生物量、能量和光合作用能力的多重?fù)p失[23,57-59]，不利于斷枝后植株的再生；此外，研究還表明植株的大小與主動(dòng)斷枝的生成呈顯著正相關(guān)[104]，而富營養(yǎng)化生境通常形成較小的植株[24,63,98]，這可能預(yù)示著富營養(yǎng)化生境會(huì)產(chǎn)生較少的主動(dòng)斷枝和較多的非主動(dòng)斷枝，從而降低水生植物的無性繁殖能力.

富營養(yǎng)化生境由于底泥疏松對(duì)植株根系的黏著力非常低[26]，與此同時(shí)富營養(yǎng)化底泥會(huì)顯著抑制水生植物根的生長[2-3,24,66]，形成不發(fā)達(dá)的根系，最終降低植株的根錨定性能，使得富營養(yǎng)化生境的水生植物更易發(fā)生拔根機(jī)械損傷[26]. 拔根對(duì)水生植物的影響不僅預(yù)示著地下組織的機(jī)械損傷和根部生物量的損失，還意味著水生植物尤其是多年生水生植物依靠地下組織進(jìn)行繁殖能力的喪失，這也可能是水生植物生物力學(xué)性能研究最初只關(guān)注莖/葉/葉柄底部的拉伸性能或彎曲性能的主要原因[26,38,64]. 而拔根后的水生植物的生存能力因生活型不同而可能不同：對(duì)于沉水植物而言，拔根后意味著初始用于來年或者合適條件種群擴(kuò)展而萌發(fā)新植株的地下組織，被迫隨水流飄蕩直至到達(dá)合適生境定植再生，雖然其生存能力因擁有地下組織而比非主動(dòng)斷枝強(qiáng)很多，但這拔根機(jī)械損傷畢竟是以原生境的植株為代價(jià)，故認(rèn)為植株具有較小的生物力學(xué)性能的莖/葉/葉柄底部是保存原生境植株生存和繁殖能力的“機(jī)械引信(mechanical fuse)”[15, 26, 30,65]；而挺水植物和浮葉植物不僅依靠根獲取營養(yǎng)，還需要暴露于空氣中的部分進(jìn)行光合作用，而發(fā)生拔根機(jī)械損傷后的植株既不能通過根獲得足夠養(yǎng)分生長，也幾乎喪失了地上部分的光合作用能力，且漂浮在水體中拔根植株難以直立極易發(fā)生腐爛[106]，因而拔根對(duì)它們而言更多地意味著死亡. 此外，拔根還不利于該水域中水生植物恢復(fù)工程的定植[23,37,63]，從而增加水生植物修復(fù)工程的難度，不利于富營養(yǎng)水體植被的重建和整個(gè)生態(tài)系統(tǒng)的恢復(fù).

3.2 生物力學(xué)性能與受富營養(yǎng)化顯著影響的其他方面的協(xié)同作用

水生植物的生物力學(xué)性能不僅受水體富營養(yǎng)化進(jìn)程中的富營養(yǎng)化底泥、水體高濃度氮磷和可利用光缺乏3大要素的顯著影響[22-24]，而且與受富營養(yǎng)化水體顯著影響的水生植物形態(tài)、生物量分配、組織結(jié)構(gòu)、物質(zhì)含量等方面密切相關(guān)[23-24,30,32-33].

3.2.1 受富營養(yǎng)化生境影響的水生植物形態(tài)與生物力學(xué)間的關(guān)聯(lián) 以底泥富營養(yǎng)化、水體高濃度氮磷和可利用光缺乏為主要特征的富營養(yǎng)生境：通常當(dāng)營養(yǎng)超過一定閾值時(shí)，一方面會(huì)顯著抑制水生植物的生長，形成分枝少、莖葉狹長的矮小植株[1,5,24-25,63,98]，且這些細(xì)長莖/葉通常比較脆弱易發(fā)生斷裂[22,59]；另一方面會(huì)顯著抑制植株根系的生長(例如較少的根數(shù)、較短的根、較小的根表面積和根分布范圍)從而增加地上生物量的分配以便獲得更多的可利用光、二氧化碳等資源[2-3]，而較低的地下/地上生物量比例和較低的根系，則預(yù)示著較低的植株根錨定性能[24,26].

3.2.2 受富營養(yǎng)化生境影響的水生植物的組織結(jié)構(gòu)和物質(zhì)含量與生物力學(xué)間的關(guān)聯(lián) 以底泥富營養(yǎng)化、水體高濃度氮磷和水下可利用光缺乏為主要特征的富營養(yǎng)生境會(huì)顯著降低植株的莖/葉/葉柄組織密度、機(jī)械組織比例，增加通氣組織[6,21]，從而降低植株莖/葉/葉柄的生物力學(xué)性能[6,14,21,50]；值得注意的是富營養(yǎng)化生境也會(huì)造成水生植物的碳、氮、磷等代謝失調(diào)，影響其在根、莖、葉等部位間的分配情況，為了緩解富營養(yǎng)化生境造成的低光、低氧和高銨脅迫，植物會(huì)將淀粉、可溶性總糖等非結(jié)構(gòu)性碳水化合物作為物質(zhì)和能量大量消耗，以降低植株體內(nèi)過量的銨離子和增加植物纖維素和木質(zhì)素等結(jié)構(gòu)性物質(zhì)合成來提高耐受能力[1,5-6]；有研究表明作為植物細(xì)胞壁主要成分的纖維素和木質(zhì)素等結(jié)構(gòu)性碳水化合物和作為能量存儲(chǔ)物質(zhì)的淀粉、可溶性總糖等非結(jié)構(gòu)性碳水化合物的含量通常與植株的生物力學(xué)性能呈顯著正相關(guān)[6,23-24,50,107].

3.3 受富營養(yǎng)化影響的水生植物各方面與植株適合度的關(guān)聯(lián)

水生植物的生長、形態(tài)、代謝、生物力學(xué)等均對(duì)植株的生存和繁殖能力，即適合度，具有一定影響，且相關(guān)功能間存在一定的權(quán)衡.

盡管在水體富營養(yǎng)化進(jìn)程中，在早期貧營養(yǎng)階段，一些可以耐受低營養(yǎng)脅迫的植物種類(例如輪藻類Characeae和水韭類Isoetids)最先定居，營養(yǎng)水平的初始增加會(huì)促進(jìn)植株的生長、種群的擴(kuò)展和物種多樣性的增加(例如微齒眼子菜、苦草等)[23]，但隨著營養(yǎng)水平進(jìn)一步增加會(huì)首先抑制喜好生長在貧、中營養(yǎng)水體的物種，即不耐污種的生長和擴(kuò)散，從而降低物種多樣性，形成以耐污種(金魚藻、穗狀狐尾藻、篦齒眼子菜等)為優(yōu)勢種的群落結(jié)構(gòu)，趨于水生植物多樣性較低的生態(tài)系統(tǒng)，如果營養(yǎng)水平進(jìn)一步增加，形成富營養(yǎng)型、超富營養(yǎng)生境，這些耐污種的生存和繁殖也會(huì)嚴(yán)重受損[25,108-109]. 總體而言，富營養(yǎng)化生境通常會(huì)抑制植株生長、降低植株高度、減少分枝數(shù)量和降低分枝長度，這從機(jī)械形態(tài)學(xué)角度來說，有利于通過降低機(jī)械脅迫與植株間的受力面積進(jìn)而降低水動(dòng)力作用于植株上的拖曳力[27,37,39,91]，但是矮小植株和較少較短的分枝也會(huì)顯著降低植株獲取可利用光的能力[24,91]和有性繁殖能力[110-111]，而分枝數(shù)、分枝長度和總分枝生物量均與無性繁殖體間呈顯著正相關(guān)[6,60-61,91]，因而富營養(yǎng)化生境生長的矮小、分枝少、分枝短的植株的適合度較低[25,91,103]. 而受富營養(yǎng)化顯著影響的代謝方面，尤其是植株體內(nèi)較低的碳水化合物含量會(huì)顯著降低植株對(duì)寒冷、低氧、蟲害等其他脅迫的耐受能力[1,60,96,107]，進(jìn)而不利于植物的生存和繁殖，即適合度的降低.

4 研究展望

4.1 富營養(yǎng)化生境其他因素對(duì)水生植物生物力學(xué)性能的可能性影響

富營養(yǎng)化水體除具有富營養(yǎng)化底泥、水體高濃度氮磷和可利用光缺乏3大主要特征外，還存在因大量藻類生長繁殖釋放的藻毒素等化學(xué)物質(zhì)、水體低溶解氧、底泥含高濃度硫化物等其他因素，這些因素積累到一定程度也會(huì)顯著影響水生植物的生長、形態(tài)、組織結(jié)構(gòu)和代謝等[70,112]. 其中，微囊藻毒素是太湖水華期主要的毒素，野外調(diào)查研究發(fā)現(xiàn)太湖藍(lán)藻水華暴發(fā)區(qū)的優(yōu)勢水生植物(竹葉眼子菜和荇菜)葉、莖中淀粉、可溶性糖和蔗糖含量均大幅度低于清水區(qū)的含量，微囊藻毒素的毒性脅迫還能導(dǎo)致挺水植物菰和蘆葦體內(nèi)的糖類物質(zhì)減少[112]；已有實(shí)驗(yàn)研究發(fā)現(xiàn)微囊藻毒素能導(dǎo)致植物蔗糖代謝失衡、光合作用受抑制以及葉的壞死[113-114]. 除了藻毒素以外，低氧與竹葉眼子菜和荇菜不同器官的碳氮代謝平衡指數(shù)呈顯著負(fù)相關(guān)，這表明在水華高發(fā)的夏季，植物的碳氮代謝平衡受到低氧的脅迫[112]. 而硫化物也能毒害水生植物，導(dǎo)致蘆葦植物組織學(xué)結(jié)構(gòu)改變[115]、野外植株生長矮小[116]以及限制種群的生存和擴(kuò)展[109]，室內(nèi)實(shí)驗(yàn)還發(fā)現(xiàn)硫化物能導(dǎo)致植物生長緩慢以及氮的吸收降低[117-118].

鑒于水生植物生物力學(xué)與形態(tài)、生物量分配、化學(xué)物質(zhì)含量及組織結(jié)構(gòu)的密切相關(guān)性(詳見3.2節(jié))，我們推測藻毒素、低溶解氧和高濃度硫化物等富營養(yǎng)化生境中次因素也會(huì)在一定程度上通過改變水生植物的形態(tài)、生物量分配、組織結(jié)構(gòu)和化學(xué)物質(zhì)含量等影響植株的生物力學(xué)性能及其受到的機(jī)械作用力，進(jìn)一步影響植株的機(jī)械損傷類型和程度. 但這需要進(jìn)一步的室內(nèi)實(shí)驗(yàn)和野外實(shí)驗(yàn)綜合研究證實(shí).

4.2 富營養(yǎng)化水體中各因子間對(duì)水生植物生物力學(xué)性能的可能性影響

生態(tài)系統(tǒng)是多因子共同作用的綜合系統(tǒng)，每個(gè)因子并不是孤立、單獨(dú)存在的，某項(xiàng)因子總與其他因子相互聯(lián)系、相互制約. 不僅水體富營養(yǎng)化會(huì)引發(fā)底泥富營養(yǎng)化、水體氮磷濃度升高、可利用光降低、藻毒素產(chǎn)生、溶解氧濃度降低和硫化物濃度升高等一系列因素的改變，對(duì)水生植物產(chǎn)生直接機(jī)械損傷的波浪、水流、船舶以及食草動(dòng)物等水生境的機(jī)械脅迫，在對(duì)根生水生植物產(chǎn)生機(jī)械作用力[36,41-43]的同時(shí)，也會(huì)促進(jìn)水-氣界面氣體交換、水-泥界面氮磷釋放和底泥再懸浮等，從而在一定程度上增加水體溶解氧、二氧化碳和氮磷等營養(yǎng)物質(zhì)濃度、減少可利用光[119-120]，這無疑進(jìn)一步加劇了水體富營養(yǎng)化對(duì)水生生物的脅迫作用. 已有部分研究表明波浪和營養(yǎng)、營養(yǎng)和光照間對(duì)水生植物的形態(tài)、代謝、生物力學(xué)性能等方面的影響存在一定的相互作用[22,63,107]. 但目前研究多集中在單一或少數(shù)物種對(duì)兩三個(gè)因素在實(shí)驗(yàn)室條件下的短期響應(yīng)，湖泊、河流、海岸帶等自然水體中多個(gè)水生植物物種甚至群落對(duì)多重因子的綜合的、長期的響應(yīng)還缺乏深入系統(tǒng)了解.

綜上所述，水生植物生物力學(xué)性能不僅直接受到波浪、流速和食草動(dòng)物等機(jī)械脅迫的影響，也間接受到富營養(yǎng)化生境富營養(yǎng)底泥、水體的高濃度氮磷和低可利用光3大主要特征因素的影響，且具有一定的協(xié)同作用；水生植物生物力學(xué)性能與植株的生長、形態(tài)、生物量分配、組織結(jié)構(gòu)、代謝等方面密切相關(guān)，表明其還可能受到對(duì)這些方面有顯著影響的富營養(yǎng)化生境中次因素，如藻毒素和高濃度硫化物等的影響；考慮到機(jī)械脅迫在一定程度上會(huì)加劇水體富營養(yǎng)化帶來的各變化因子的變化程度，水生植物更易發(fā)生機(jī)械損傷. 此外，水生植物的生物力學(xué)性能如果不足以抵抗隨著全球氣候變化引發(fā)的異常降雨情勢和水利工程調(diào)控的水文節(jié)律帶來的水生植物在水-陸生生境不斷更替的機(jī)械脅迫作用力，則會(huì)造成植株斷枝、拔根等機(jī)械損傷，這不僅會(huì)降低植株利用資源和物質(zhì)合成、耐受能力，也會(huì)嚴(yán)重影響機(jī)械斷枝的擴(kuò)散和生根定植能力. 總之，目前研究表明水生植物的生物力學(xué)性能在水體富營養(yǎng)化引發(fā)的水生植物衰退中具有非常重要作用，但其生物力學(xué)機(jī)理還需要長期的、系統(tǒng)的、多重因子綜合作用的、多種的、群落的自然水體和室內(nèi)實(shí)驗(yàn)相結(jié)合的研究來探討總結(jié).

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Role of biomechanics in decline of aquatic macrophytes during the progress of eutrophication

ZHU Guorong1,2, ZHANG Meng3, WANG Fangxia1, Gao Yang1, CAO Te2**& NI Leyi2**

(1:CollegeofFisheries,HenanNormalUniversity,Xinxiang453007,P.R.China)(2:DonghuExperimentalStationofLakeEcosystem,InstituteofHydrobiology,ChineseAcademyofSciences,Wuhan430072,P.R.China)(3:JiangxiAcademyofEnvironmentalSciences,Nanchang330029,P.R.China)

The mechanism of the decline of aquatic macrophytes in eutrophic waters has recently become a central and growing interest to aquatic ecologists. Here, we described the biomechanical properties of aquatic macrophytes, their responses to eutrophication and their possible contribution to the decline caused by eutrophication. Different from most terrestrial plants, the biomechanical properties of aquatic macrophytes mainly included the tensile properties of stems/leaves/petioles (the bending properties of stems/petioles for emergent macrophytes) and root anchorage strength. Three vital factors of eutrophication, the fertile sediment, higher concentrations of nitrogen and phosphorus in water-column and limited light availability, had significantly negative and species-specific influences on the biomechanical properties of aquatic macrophytes. Additionally, there were strong relationships between the biomechanical properties and the other aspects, which were also significantly affected on, such as plant growth, morphology, biomass allocation, anatomic structure and metabolism, as well as collaboration between these factors during their response to the eutrophication. What’s more, the mechanical damages interrupted the life progress because of a vital reduce in resource acquisition for parent plants and a relative low spreading and colonize ability for all fragments, resulting in a low fitness. Numerous field investigations and laboratory experiments can imply that the changed biomechanical properties do play a key role in the decline of aquatic macrophytes during the progress of eutrophication. As the multiple interactions among the environmental factors existed in natural waters, most studies only focused on the effects of the three vital factors resulted from eutrophication on the biomechanical properties of aquatic macrophytes. Therefore, further and systematical studies should be conducted on the plant biomechanical properties responding to multiply factors (dissolved oxygen, algal toxins and herbivores) because these factors also have significant effects during eutrophication. Thus the biomechanical mechanism for the decline of aquatic macrophytes in eutrophic waters can be well revealed.

Aquatic macrophytes; biomechanics; eutrophication; the decline mechanism

國家自然科學(xué)基金項(xiàng)目(31400402，31460130)、河南省科技廳項(xiàng)目(142102310476)和河南師范大學(xué)項(xiàng)目(qd13049)聯(lián)合資助. 2016-06-15收稿；2016-10-21收修改稿. 祝國榮(1982～)，女，博士，講師；E-mail：zhuguorong2012@hotmail.com.

；E-mail：caote@ihb.ac.cn; nily@ihb.ac.cn.

DOI 10.18307/2017.0501