林成芳, 彭建勤, 洪慧濱, 楊智杰,*, 楊玉盛

1 福建師范大學地理科學學院, 福州 350007 2 福建師范大學濕潤亞熱帶山地生態(tài)國家重點實驗室培育基地, 福州 350007

氮、磷養(yǎng)分有效性對森林凋落物分解的影響研究進展

林成芳1,2, 彭建勤1,2, 洪慧濱1,2, 楊智杰1,2,*, 楊玉盛1,2

1 福建師范大學地理科學學院, 福州 350007 2 福建師范大學濕潤亞熱帶山地生態(tài)國家重點實驗室培育基地, 福州 350007

通過對相關研究文獻的綜述結果表明,氮(N)和磷(P)是構成蛋白質(zhì)和遺傳物質(zhì)的兩種重要組成元素,限制森林生產(chǎn)力和其他生態(tài)系統(tǒng)過程,對凋落物分解產(chǎn)生深刻影響。大量的凋落物分解試驗發(fā)現(xiàn)在土壤N有效性較低的溫帶和北方森林,凋落物分解速率常與底物初始N濃度、木質(zhì)素/N比等有很好的相關關系,也受外源N輸入的影響；而在土壤高度風化的熱帶亞熱帶森林生態(tài)系統(tǒng)中,P可能是比N更為重要的分解限制因子。然而控制試驗表明,N、P添加對凋落物分解速率的影響并不一致,既有促進效應也有抑制效應。為了深入揭示N、P養(yǎng)分有效性對凋落物分解的調(diào)控機制,“底物的C、N化學計量學”假說、 “微生物的N開采”假說以及養(yǎng)分平衡的理論都常被用于解釋凋落物分解速率的變化。由于微生物分解者具有較為穩(wěn)定的C、N、P等養(yǎng)分需求比例,在不同的養(yǎng)分供應的周圍環(huán)境中會體現(xiàn)出不同的活性,某種最缺乏的養(yǎng)分可能就是分解的最重要限制因子。未來的凋落物分解研究,應延長實驗時間、加強室內(nèi)和野外不同條件下的N、P等養(yǎng)分添加控制試驗,探討驅動分解進程的微生物群落結構和酶活性的變化。

凋落物分解；N；P；養(yǎng)分有效性；微生物；酶

植物凋落物的分解向土壤歸還養(yǎng)分,向大氣釋放CO2,是生態(tài)系統(tǒng)物質(zhì)循環(huán)和能量流動的重要環(huán)節(jié)[1-2]。自從Bocock and Gilbert于1957首次使用凋落物分解袋技術以來,關于凋落物分解的文章逐年穩(wěn)定遞增,利用Web of Science進行搜索,發(fā)現(xiàn)迄今為止文章總數(shù)已經(jīng)超過8000篇(圖1)。1990年后,人們密切關注全球升溫及與之相伴的大氣CO2濃度升高等環(huán)境問題,因此對分解過程調(diào)控機制的深入了解變得尤為迫切[3-5]。

圖1 近50年有關凋落物分解發(fā)表的SCI文章Fig.1 The papers on litter decomposition published included in SCI in the past 50 years

凋落物分解的調(diào)控機制極其復雜,涉及物理、化學和生物學過程,但主要可以歸納為兩個方面,其一是凋落物本身質(zhì)量,即其物理化學性質(zhì)和養(yǎng)分的含量,其二是分解的外在環(huán)境,特別是氣候因子(溫度、水分)以及土壤或枯枝落葉層的養(yǎng)分含量和有效性[1,6-7]。過去的研究表明在全球和區(qū)域的尺度上,氣候是調(diào)控凋落物分解的首要因素,但在局域尺度上,表征凋落物質(zhì)量的養(yǎng)分含量指標以及分解環(huán)境中的養(yǎng)分有效性則起至關重要的作用[8-13]。N、P是陸地生態(tài)系統(tǒng)植物生長最重要的兩種限制性養(yǎng)分[14-16],在全球變化背景下,自然或人為驅動的這兩種元素輸入變化,必將對凋落物分解產(chǎn)生重要影響,進而影響全球的碳平衡或碳預算。然而,N、P養(yǎng)分有效性的改變?nèi)绾斡绊懙蚵湮锏姆纸?以及分解過程中的微生物學機制等尚待闡明,直接影響到碳循環(huán)模型的構建和對生態(tài)系統(tǒng)碳吸存潛力的預測。

1 不同來源的N對凋落物分解的影響

化石燃料的燃燒、化肥的使用以及固N作物的栽培等人類活動,把N從惰性的形態(tài)(N2)轉化為活性的形態(tài),如NH3(Haber Bosch 制氮法)、NOx。而活性N經(jīng)脫N作用形成N2的速度小于活性N形成的速度,導致這些活性N在大氣、土壤和水體中儲藏[17],并在未來相當長的時間內(nèi)持續(xù)增加[18]?；钚訬的增加引發(fā)了平流層臭氧耗竭、酸沉降、海岸帶富營養(yǎng)化以及淡水的生產(chǎn)等環(huán)境問題,同時也提高了生態(tài)系統(tǒng)的凈初級生產(chǎn)力[19-20],增加了生態(tài)系統(tǒng)C、N儲量。為了進一步了解N輸入持續(xù)增加情況下,生態(tài)系統(tǒng)碳輸出的變化,需要明確N對凋落物分解的效應。

大量的凋落物分解研究表明,分解速率與N相聯(lián)系的各種指標有很好的相關關系。這體現(xiàn)在凋落物自身的N含量、C/N、木質(zhì)素/N,土壤環(huán)境中的C/N、N含量以及外源添加的N量對分解產(chǎn)生的不同效應。

1.1 凋落物底物的N含量對分解的影響

“底物的C、N化學計量學”假說認為,微生物分解者與分解底物之間存在C、N化學計量學的差異,這種對分解者生理學上的基本約束驅動凋落物分解和養(yǎng)分的釋放[21-23]。一般來說,新鮮凋落物的C/N比高于微生物分解者,微生物需要從周圍環(huán)境(土壤或降水)獲取養(yǎng)分來維持其自身的生長需求[24-25]。此外,大量的研究發(fā)現(xiàn)在分解早期,凋落物初始N含量以及與N相關的底物質(zhì)量指標和凋落物分解速率有很好的相關關系[20-21],證明N對凋落物分解的限制作用。盡管以上證據(jù)都是間接的,但C/N比和木質(zhì)素/N的比率等指標常被用于預測凋落物的分解速率[20,23,26-27],同時也被一些碳循環(huán)模型采用。

1.2 土壤N有效性對凋落物分解的影響

在熱帶山地生態(tài)系統(tǒng)的土壤年齡序列中,凋落物在養(yǎng)分有效性高的土壤中分解最快,而在養(yǎng)分有效性低且限制了地上部分生產(chǎn)力的土壤中分解最慢[28-29]。Hobbie[30]在美國明尼蘇達州的研究發(fā)現(xiàn),分解速率與土壤N有效性有顯著的相關關系。土壤養(yǎng)分有效性對分解的限制作用還表現(xiàn)在分解者和植物之間的正反饋環(huán),在低養(yǎng)分的土壤中,凋落物分解受到限制而減緩養(yǎng)分循環(huán),進一步降低植物的養(yǎng)分有效性,限制植物的生產(chǎn)力；而較低生產(chǎn)力的植物,凋落物歸還的數(shù)量和質(zhì)量都較低,抑制了分解[31]。在溫帶森林生態(tài)系統(tǒng)研究表明,高土壤N有效性提高細根底物的質(zhì)量,進而影響了細根的分解速率[32]。

1.3 外源添加的N對凋落物分解的影響

分解養(yǎng)分限制的直接證據(jù)只能通過施肥實驗,在增加外源提供的養(yǎng)分情況下,考察凋落物分解速率是否提高。然而凋落物分解對外源N輸入的響應并不一致,既有促進作用[33-34]、抑制作用[35-36],還有研究發(fā)現(xiàn)沒有明顯的作用[33,37]。

N添加對凋落物分解的促進或抑制作用以及影響的程度大小與很多因素有關,除凋落物本身質(zhì)量外,還有諸多其他因素,如氣候、大氣N沉降水平以及施N肥的類型、網(wǎng)袋的孔徑大小等。Knorr 等[38]的綜合分析表明,N施肥改變了凋落物的分解速率,但分解響應的方向和程度受到施肥的量、大氣氮沉降水平以及凋落物質(zhì)量交互作用的調(diào)節(jié)。當施肥量為氮沉降水平的2—20倍時,或者氮沉降水平達5—10 kg N hm-2a-2,再或者凋落物質(zhì)量差(高木質(zhì)素含量)時,凋落物分解受到抑制；在高N施肥的情況下(大氣氮沉降的20倍),或氮沉降水平在5kg N hm-2a-2以下,或高質(zhì)量的凋落物(低木質(zhì)素含量)時,凋落物分解被促進。因此,特定生態(tài)系統(tǒng)中,分解過程對N施肥的響應受到N沉降水平的影響,長期高N沉降下的生態(tài)系統(tǒng)可能獲得了適應性,在人為施N肥的情況下凋落物分解反應程度較小。

從有機質(zhì)中獲得N的過程非常復雜,N分布在多種等級的混合物以及腐殖大分子中,因此微生物的N獲取策略與特定種群的C底物偏好有密切聯(lián)系[39-40]。在Moorhead和Sinsabaugh[41]提出的以分解者集團為基礎的凋落物分解模型中,把微生物分成三大類：分解活性蛋白質(zhì)的機會主義者(opportunists)、需要外源N輸入分解木質(zhì)纖維素的專性分解者(decomposers)和利用氧化酶打開腐殖質(zhì)獲得所需的C和N 的“淘金分解者”(miners)。

在多樣的C和N獲取策略情況下,外源N添加試驗中發(fā)現(xiàn)土壤胞外酶活性的響應差異便不難理解了。因此,近年來很多研究者傾向于從酶活性變化的角度來解釋N添加對分解的影響[42]。用酶活性的變化來解釋N添加對分解的影響得到了多個研究的支持[42-46]。如Fog[47]發(fā)現(xiàn)在高N的情況下,白腐擔子菌被分解纖維素的子囊菌所競爭性排除,這種對木質(zhì)素分解的抑制作用導致添加N對分解的中性效應或負效應。Craine 等[48]研究也認為,是N的添加降低負責分解惰性C的微生物活性C有效性,抑制了負責惰性有機C中“N開采”的酶(如酚氧化酶、過氧化物酶)的生產(chǎn)[41,49],從而限制了凋落物的分解。添加N不僅改變了酚氧化酶,還有其他微生物獲取C、N、P酶的活性,這些酶活性的變化能較好的解釋凋落物分解速率的變化[49-51]。酶活性對外源N的不同響應,與樣地土壤養(yǎng)分有效性[52-53]、凋落物木質(zhì)素含量[53-54]、凋落物和土壤的C/N比[46,55]以及微生物生物量[56]有關。測定酶活性使人們能夠直接跟蹤微生物群落對凋落物性質(zhì)和環(huán)境變量的功能響應[44],但由于植物-凋落物-微生物交互作用具有潛在的復雜性,在地表植被、凋落物化學性質(zhì)、土壤C/N比和N有效性不同的多種林地上,凋落物分解速率和土壤的酶活性同時會對外源N添加做出何種響應,目前尚不清楚。目前,DGGE、PLFA以及高通量測序技術的成熟和應用,必將推進對N沉降背景下不同生態(tài)系統(tǒng)凋落物分解過程中微生物群落和酶活性的動態(tài)變化的準確刻畫。

2 P對凋落物分解的影響

長期復雜的成土過程中形成了土壤在地理學上的分異,中髙緯度地區(qū)的土壤較為年輕, N含量較少,而低緯度地區(qū)土壤古老, P含量有限[57]。P和N對初級生產(chǎn)力以及其他生態(tài)系統(tǒng)過程的限制作用已經(jīng)在多種多樣的陸地生態(tài)系統(tǒng)中被證明[16]。與N不同,土壤P來源于巖石風化,每個生態(tài)系統(tǒng)發(fā)生時都有一個固定P儲量,隨生態(tài)系統(tǒng)發(fā)育,P不斷流失且不能輕易得到補充。這導致老的土壤中P的總量和生物有效性都較低,從而對生態(tài)系統(tǒng)NPP、凋落物分解等其他生態(tài)學過程產(chǎn)生了深刻的影響[28,15]。

在熱帶亞熱帶的酸性土壤里, P易于被其中的鐵鋁氧化物固定,發(fā)生強的吸附作用, N相對過剩而由礦石來源的P等必要養(yǎng)分處于耗竭狀態(tài),全球氣候變化下的N/S沉降更加劇了生態(tài)系統(tǒng)潛在的P限制[31,58-60]。研究已證實P有效性限制了熱帶、亞熱帶生態(tài)系統(tǒng)的NPP(凈初級生產(chǎn)力)。凋落物分解的初級階段經(jīng)常需要富集P,說明新鮮凋落物中的P養(yǎng)分不足以維持分解者的生長,而凋落物分解速率常與P及其相聯(lián)系的凋落物質(zhì)量指標顯著相關[1,61-65],表明凋落物分解可能受P限制。此外熱帶生態(tài)系統(tǒng)土壤高度風化,N過剩而P有效性低,在此土壤上生長的凋落物也具有高N/P比的特征[58,66]。因此相比于N,微生物在分解中更難以從凋落物本身及周圍環(huán)境獲得P,根據(jù)李比希最小值定律(Liebig′s law of the minimum),P可能是該區(qū)域凋落物分解更為重要的限制性因子。然而,現(xiàn)有的生態(tài)系統(tǒng)C循環(huán)機理模型很少考慮P的循環(huán)[40,67]。

不同于N的循環(huán),P循環(huán)可分為生物和地球化學循環(huán)。生物循環(huán)是指植物和微生物吸收的P在死亡后變成土壤有機P,這部分的P能夠被重新礦化和吸收；地球化學循環(huán)則是由于母巖風化或外源添加提供給生態(tài)系統(tǒng)的P,與土壤礦物發(fā)生化學反應被固定在土壤中[68-70]。但有證據(jù)表明,微生物能迅速利用外源添加的P,在生物吸收和土壤吸附有效P的競爭中起支配作用[71-73]。已有研究通過測定呼吸速率,探討P添加后高度風化土壤凋落物分解過程中微生物活性變化,來解釋P有效性對分解的限制作用[73-75]。而直接測定P添加對分解過程中微生物動態(tài)效應的研究很少,這是由于當前的生態(tài)系統(tǒng)模型都把土壤微生物當作一個黑箱[76-78]。

與N相比,人們對P與微生物結構和功能的關系了解較少[61]。在外源P添加的情況下,P的有效性提高,微生物運用更少的能量獲得P[43,79],那么微生物是否重新分配它的資源,轉向提高獲得C、N的胞外酶活性呢？ 這些酶的活性能用于解釋P添加情況下凋落物分解速率的變化么？土壤化學性質(zhì)：如 pH,N、P等養(yǎng)分有效性和凋落物質(zhì)量的變化不僅影響酶的合成,同時影響細菌和真菌的比例及其群落結構的變化[45,78,80]。如富含養(yǎng)分的活性有機質(zhì)由快速生長的細菌侵染,因其快速的細胞分裂需要大量富P的RNA,而養(yǎng)分貧乏難分解的有機質(zhì)易于生長真菌[81-83]。因而直接測定酶活性和主要微生物類群結構對凋落物性質(zhì)和環(huán)境變量的響應,能獲得對凋落物分解機理更為清晰的了解。

3 其他元素對凋落物分解的影響

N和P是限制生態(tài)系統(tǒng)過程的兩種關鍵元素,被大部分分解試驗關注。目前的研究表明,北方森林和溫帶森林,富N比貧N的凋落物分解快[84]；而低地熱帶雨林N相對豐富, P含量隨時間不斷耗竭[85],從而使P在該區(qū)域凋落物分解中起主導作用[33,46,59,67]。除這兩種元素外,尚有少量研究表明其它元素也在分解中有重要作用。

凋落物分解是個多種底物(如蠟類、酚類、木質(zhì)素和纖維素等)連續(xù)降解的過程,需要微生物合成多種(metallomic enzymes)金屬酶的參與[86],這個過程中會出現(xiàn)包括N、P等其它多種養(yǎng)分供應的不足。Kaspari[86]在熱帶低地森林的分解試驗發(fā)現(xiàn),P的添加提高凋落物分解速率33%而微量元素(如 B, Ca,Cu, Fe, Mg, Mn, Mo, S, Zn)的添加則提高了81%。這說明除P之外,另有其它元素可能參與并促進凋落物的分解。據(jù)統(tǒng)計,大約需要25種化學元素才能驅動整個生態(tài)系統(tǒng)碳循環(huán)過程中的樹木生長、分解中的微生物繁殖[87]。如果要對限制凋落物分解的養(yǎng)分重要性進行排序,需設計析因實驗,然而這樣的試驗目前仍很少[88]。

4 N/P比率對凋落物分解的影響

Alfred Redfield在1958年觀測到,海洋浮游生物生物量中C、 N 、P原子比為 106∶16∶1,這與海水中C、 N 、P比例相似。這種化學計量學關系簡潔的反映了有機體和環(huán)境之間的交互作用,被稱為“Alfred比率”,其有助于深入了解海洋生態(tài)系統(tǒng)NPP和C儲量受養(yǎng)分限制的性質(zhì)和程度,以及海洋中N、P生物地球化學循環(huán)過程?！癆lfred比率”在海洋生態(tài)系統(tǒng)的預測能力,推動生態(tài)學家在陸地生態(tài)系統(tǒng)尋找相似的養(yǎng)分格局和關系,因而誕生了一門新的學科——生態(tài)化學計量學,這門學科著眼于了解生態(tài)學交互作用過程中的多種化學元素的平衡[89-90]。然而,我們當前對化學計量關系以及其在陸地生態(tài)系統(tǒng)中的重要意義所知還很有限[91]。

微生物生物量C與土壤C有效性有很強的相關關系,同時也與土壤微生物中N和P的含量密切相關,這種養(yǎng)分之間的線性相關關系表明土壤微生物生物量C的增加依賴于充足的土壤N和P養(yǎng)分供應來維持微生物生長所需要的養(yǎng)分元素化學計量比[90]。植物葉片養(yǎng)分比率反映了土壤N和P的相對豐度從低緯度到高緯度的增長[58,92-93],而土壤微生物量中的N/P比率并不隨著緯度的變化而變化,也與土壤中N∶P供應比率沒有相關關系,而是維持在類似“Alfred比率”的比例[94]。土壤微生物相對嚴格的養(yǎng)分需求以及低緯度地區(qū)土壤低P有效性解釋了P對這些生態(tài)系統(tǒng)微生物生物量和活性的限制[59,72,95-97],進而限制凋落物的分解。由于N、P有效性在不同生態(tài)系統(tǒng)間的差異,因此有些研究者認為N和P對生態(tài)系統(tǒng)過程(包括凋落物分解)限制的相對重要性也不同,當N/P比低時受N限制,當N/P比高時受P限制(通常認為N/P比<14時受N限制,N/P比>16時受P限制,當N/P比在14和16之間受到N、P的共同限制)[83]。人類活動可以通過添加P而轉變P限制的生態(tài)系統(tǒng)為其它養(yǎng)分限制系統(tǒng),也可以通過有意和無意的影響其它養(yǎng)分(主要是N)的供給,導致P限制生態(tài)系統(tǒng)的出現(xiàn)。例如,歐洲西北地區(qū)由于極端高水平的大氣N沉降克服了許多生態(tài)系統(tǒng)的N限制而轉變成首先受P限制的生態(tài)系統(tǒng)[46,96],在北美地區(qū)進行的控制試驗也獲得類似的結果[97-99]。

5 展望

凋落物分解是一個貫穿著淋溶、凍融粉碎等物理作用以及土壤生物參與的生物化學作用交織在一起的復雜過程,并最終通過微生物的作用釋放CO2到大氣,釋放養(yǎng)分回歸土壤中。對同一種底物而言,控制微生物活性的溫度、水分條件以及微生物所需的養(yǎng)分有效性,決定了凋落物最終的分解速率。因此,當前凋落物分解研究存在以下主要問題：(1)影響凋落物分解的N、P養(yǎng)分因素與其他因素同時存在或發(fā)生交互作用,導致難以確定影響分解的主導因素。且確定影響分解速率的因素時,常采用相關分析的方法。相關分析可以為確定主導因素提供很好的線索,然而需要控制試驗加以驗證；(2)較少考慮P有效性對凋落物分解的影響。早期的分解研究主要集中在北方森林和溫帶森林,研究結果認為N及木質(zhì)素/N比是調(diào)控凋落物分解的主要因素,現(xiàn)有的生態(tài)系統(tǒng)過程模型也只考慮N的作用而忽略了P,然而近年來熱帶、亞熱帶發(fā)育在高度風化土壤上生態(tài)系統(tǒng)的多項研究表明P對生態(tài)系統(tǒng)過程的限制作用。即使在熱帶和亞熱帶,不同生態(tài)系統(tǒng)或同一生態(tài)系統(tǒng)不同的發(fā)育階段受N、P養(yǎng)分限制情況也不一致；(3)分解底物的異質(zhì)性。即便同種植物,其不同位置或不同時間產(chǎn)生的凋落物N、P養(yǎng)分含量具有較大的差異。(4)較少考慮影響分解過程各種酶的活性和微生物群落結構的變化。N、P無疑是生態(tài)系統(tǒng)過程中兩種最重要的養(yǎng)分,但它們對凋落物分解的影響及作用機制尚未明確的闡述,影響了對全球環(huán)境變化下生態(tài)系統(tǒng)過程的預測。今后應著重通過室內(nèi)結合野外的控制試驗獲取直接的證據(jù),主要考慮以下幾個方面的工作：

(1)養(yǎng)分添加試驗是確定養(yǎng)分限制屬性的良好手段,然而需要認真的考慮養(yǎng)分添加量以及觀測的時間。養(yǎng)分添加量會改變生態(tài)系統(tǒng)養(yǎng)分受限性質(zhì),有效體現(xiàn)養(yǎng)分添加效應需要延長觀測的時間。例如,現(xiàn)有的凋落物分解試驗大部分少于2a,有的凋落物在此期間尚處于分解的初期階段。

(2)要充分考慮分解環(huán)境變化對N、P添加效應的影響。例如熱帶雨林凋落物分解過程中淋溶起主導作用,因此養(yǎng)分添加對凋落物的干質(zhì)量損失沒有顯著影響,但卻促進了凋落物淋溶部分物質(zhì)的礦化分解。

(3)養(yǎng)分平衡對凋落物分解的作用。微生物分解者的生長有嚴格的化學計量學要求,是否某種養(yǎng)分有效性的缺乏限制了凋落物分解。

(4)通過對分解過程中微生物和酶活性變化的觀測,揭示凋落物分解的機理,闡明養(yǎng)分添加對凋落物分解的不同效應,最終弄清楚不同生態(tài)系統(tǒng)凋落物分解的主要限制性因子。

[1] Swift M J, Heal O W, Anderson J M. Decomposition in Terrestrial Ecosystems. Berkeley: University of California Press, 1979.

[2] Cornwell W K, Cornelissen J H C, Amatangelo K, Dorrepaal E, Eviner V T, Godoy O, Hobbie S E, Hoorens B, Kurokawa H, Pérez-Harguindeguy N, Quested H M, Santiago L S, Wardle D A, Wright I J, Aerts R, Allison S D, Van Bodegom P, Brovkin V, Chatain A, Callaghan T V, Díaz S, Garnier E, Gurvich D E, Kazakou E, Klein J A, Read J, Reich P B, Soudzilovskaia N A, Vaieretti M V, Westoby M. Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecology Letters, 2008, 11(10): 1065-1071.

[3] Chapin III F S, McFarland J, McGuire A D, Euskirchen E S, Ruess R W, Kielland K. The changing global carbon cycle: linking plant-soil carbon dynamics to global consequences. Journal of Ecology, 2009, 97(5): 840-850.

[4] Currie W S, Harmon M E, Burke I C, Hart S C, Parton W J, Silver W. Cross-biome transplants of plant litter show decomposition models extend to a broader climatic range but lose predictability at the decadal time scale. Global Change Biology, 2010, 16(6): 1744-1761.

[5] Brovkin V, van Bodegom P M, Kleinen T, Wirth C, Cornwell W K, Cornelissen J H C, Kattge J. Plant-driven variation in decomposition rates improves projections of global litter stock distribution. Biogeosciences, 2012, 9(1): 565-576.

[6] Berg B, McClaugherty C. Plant Litter: Decomposition, Humus Formation, Carbon Sequestration. Berlin Heidelberg: Springer-Verlag, 2003.

[7] Prescott C E. Litter decomposition: what controls it and how can we alter it to sequester more carbon in forest soils?. Biogeochemistry, 2010, 101(1-3): 133-149.

[8] Berg B, Berg M P, Bottner P, Box E, Breymeyer A, De Anta R C, Couteaux M, Escudero A, Gallardo A, Kratz W, Madeira M, M?lk?nen E, McClaugherty C, Meentemeyer V, Muoz F, Piussi P, Remacle J A, De Santo A V. Litter mass loss rates in pine forests of Europe and Eastern United States: some relationships with climate and litter quality. Biogeochemistry, 1993, 20(3): 127-159.

[9] Aerts R. Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos, 1997, 79(3): 439-449.

[10] Cadisch G, Giller K E. Driven by Nature: Plant Litter Quality and Decomposition. Wallingford: CAB International, 1997.

[11] Wall D H, Bradford M A, St John M G, Trofymow J A, Behan-Pelletier V, Bignell D E, Dangerfield J M, Parton W J, Rusek J, Voigt W, Wolters V, Gardel H Z, Ayuke F O, Bashford R, Beljakova O I, Bohlen P J, Brauman A, Flemming S, Henschel J R, Johnson D L, Jones T H, Kovarova M, Kranabetter J M, Kutny L, Lin K C, Maryati M, Masse D, Pokarzhevskii A, Rahman H, Sabará M G, Salamon J A, Swift M J, Varela A, Vasconcelos H L, White D, Zou X M. Global decomposition experiment shows soil animal impacts on decomposition are climate-dependent. Global Change Biology, 2008, 14(11): 2661-2677.

[12] Zhou G Y, Guan L L, Wei X H, Tang X L, Liu S G, Liu J X, Zhang D Q, Yan J H. Factors influencing leaf litter decomposition: an intersite decomposition experiment across China. Plant and Soil, 2008, 311(1-2): 61-72.

[13] Powers J S, Montgomery R A, Adair E C, Brearley F Q, DeWalt S J, Castanho C T, Chave J, Deinert E, Ganzhorn J U, Gilbert M E, González-Iturbe J A, Bunyavejchewin S, Grau H R, Harms K E, Hiremath A, Iriarte-Vivar S, Manzane E, De Oliveira A A, Poorter L, Ramanamanjato J B, Salk C, Varela A, Weiblen G D, Lerdau M T. Decomposition in tropical forests: a pan-tropical study of the effects of litter type, litter placement and mesofaunal exclusion across a precipitation gradient. Journal of Ecology, 2009, 97(4): 801-811.

[14] Chapin III F S, Kedrowski R A. Seasonal changes in nitrogen and phosphorus fractions and autumn retranslocation in evergreen and deciduous taiga trees. Ecology, 1983, 64(2): 376-391.

[15] Vitousek P M, Howarth R W. Nitrogen limitation on land and in the sea: how can it occur?. Biogeochemistry, 1991, 13(2): 87-115.

[16] Vitousek P M, Porder S, Houlton B Z, Chadwick O A. Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecological Applications, 2010, 20(1): 5-15.

[17] Galloway J N, Cowling E B. Reactive nitrogen and the world: 200 years of change. AMBIO: A Journal of the Human Environment, 2002, 31(2): 64-71.

[18] Galloway J N, Dentener F J, Capone D G, Boyer E W, Howarth R W, Seitzinger S P, Asner G P, Cleveland C C, Green P A, Holland E A, Karl D M, Michaels A F, Porter J H, Townsend A R, V?osmarty C J. Nitrogen cycles: past, present, and future. Biogeochemistry, 2004, 70(2): 153-226.

[19] Nadelhoffer K J, Emmett B A, Gundersen P, Kj?naas O J, Koopmans C J, Schleppi P, Tietema A, Wright R F. Nitrogen deposition makes a minor contribution to carbon sequestration in temperate forests. Nature, 1999, 398(6723): 145-148.

[20] Aber J D, Melillo J M. Nitrogen immobilization in decaying hardwood leaf litter as a function of initial nitrogen and lignin content. Canadian Journal of Botany, 1982, 60(11): 2263-2269.

[21] Magill A H, Aber J D, Berntson G M, McDowell W H, Nadelhoffer K J, Melillo J M, Steudler P. Long-term nitrogen additions and nitrogen saturation in two temperate forests. Ecosystems, 2000, 3(3): 238-253.

[22] Hessen D O, ?gren G I, Anderson T R, Elser J J, de Ruiter P C. Carbon sequestration in ecosystems: the role of stoichiometry. Ecology, 2004, 85(5): 1179-1192.

[23] Parton W, Silver W L, Burke I C, Grassens L, Harmon M E, Currie W S, King J Y, Carol Adair E, Brandt L A, Hart S C, Fasth B. Global-scale similarities in nitrogen release patterns during long-term decomposition. Science, 2007, 315(5810): 361-364.

[24] Gosz J R, Likens G E, Bormann F H. Nutrient release from decomposing leaf and branch litter in the Hubbard brook forest, New Hampshire. Ecological Monographs, 1973, 43(2): 173-191.

[25] Staaf H, Berg B. Accumulation and release of plant nutrients in decomposing Scots pine needle litter. Long-term decomposition in a Scots pine forest II. Canadian Journal of Botany, 1982, 60(8): 1561-1568.

[26] Taylor B R, Parkinson D, Parsons W F J. Nitrogen and lignin content as predictors of litter decay rates: a microcosm test. Ecology, 1989, 70(1): 97-104.

[27] Aber J D, Melillo J M, McClaugherty C A. Predicting long-term patterns of mass loss, nitrogen dynamics, and soil organic matter formation from initial fine litter chemistry in temperate forest ecosystems. Canadian Journal of Botany, 1990, 68(10): 2201-2208.

[28] Crews T E, Kitayama K, Fownes J H, Riley R H, Herbert D A, Mueller-Dombois D, Vitousek P M. Changes in soil phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii. Ecology, 1995, 76(5): 1407-1424.

[29] Vitousek P M, Farrington H. Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry, 1997, 37(1): 63-75.

[30] Hobbie S E. Effects of plant species on nutrient cycling. Trends in Ecology & Evolution, 1992, 7(10): 336-339.

[31] Vitousek P. Nutrient cycling and nutrient use efficiency. The American Naturalist, 1982, 119(4): 553-572.

[32] Hendricks J J, Aber J D, Nadelhoffer K J, Hallett R D. Nitrogen controls on fine root substrate quality in temperate forest ecosystems. Ecosystems, 2000, 3(1): 57-69.

[33] Hobbie S E, Vitousek P M. Nutrient limitation of decomposition in Hawaiian forests. Ecology, 2000, 81(7): 1867-1877.

[34] Vestgarden L S. Carbon and nitrogen turnover in the early stage of Scots pine (PinussylvestrisL.) needle litter decomposition: effects of internal and external nitrogen. Soil Biology Biochemistry, 2001, 33(4-5): 465-474.

[35] Magill A H, Aber J D. Long-term effects of experimental nitrogen addition on foliar litter decay and humus formation in forest ecosystems. Plant and Soil, 1998, 203(2): 301-311.

[36] Micks P, Downs M R, Magill A H, Nadelhoffer K J, Aber J D. Decomposing litter as a sink for15N-enriched additions to an oak forest and a red pine plantation. Forest Ecology and Management, 2004, 196(1): 71-87.

[37] Johnson D W, Cheng W, Ball J T. Effects of CO2and N fertilization on decomposition and N immobilization in ponderosa pine litter. Plant and Soil, 2000, 224(1): 115-122.

[38] Knorr M, Frey S D, Curtis P S. Nitrogen additions and litter decomposition: a meta-analysis. Ecology, 2005, 86(12): 3252-3257.

[39] McGill W B, Cole C V. Comparative aspects of cycling of organic C, N, S and P through soil organic matter. Geoderma, 1981, 26(4): 267-286.

[40] Manzoni S, Jackson R B, Trofymow J A, Porporato A. The global stoichiometry of litter nitrogen mineralization. Science, 2008, 321(5889): 684-686.

[41] Moorhead D L, Sinsabaugh R L. A theoretical model of litter decay and microbial interaction. Ecological Monographs, 2006, 76(2): 151-174.

[42] Rejmánková E, Sirová D. Wetland macrophyte decomposition under different nutrient conditions: relationships between decomposition rate, enzyme activities and microbial biomass. Soil Biology and Biochemistry, 2007, 39(2): 526-538.

[43] Alvarez S, Guerrero M C. Enzymatic activities associated with decomposition of particulate organic matter in two shallow ponds. Soil Biology and Biochemistry, 2000, 32(13): 1941-1951.

[44] Carreiro M M, Sinsabaugh R L, Repert D A, Parkhurst D F. Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology, 2000, 81(9): 2359-2365.

[45] Allison S D, Vitousek P M. Extracellular enzyme activities and carbon chemistry as drivers of tropical plant litter decomposition. Biotropica, 2004, 36(3): 285-296.

[46] Waldrop M P, Zak D R, Sinsabaugh R L, Gallo M, Lauber C. Nitrogen deposition modifies soil carbon storage through changes in microbial enzymatic activity. Ecological Applications, 2004, 14(4): 1172-1177.

[47] Fog K. The effect of added nitrogen on the rate of decomposition of organic matter. Biological Reviews, 1988, 63(3): 433-462.

[48] Craine J M, Morrow C, Fierer N. Microbial nitrogen limitation increases decomposition. Ecology, 2007, 88(8): 2105-2113.

[49] Stursova M, Crenshaw C L, Sinsabaugh R L. Microbial responses to long-term N deposition in a semiarid grassland. Microbial Ecology, 2006, 51(1): 90-98.

[50] Saiya-Cork K R, Sinsabaugh R L, Zak D R. The effects of long term nitrogen deposition on extracellular enzyme activity in anAcersaccharumforest soil. Soil Biology and Biochemistry, 2002, 34(9): 1309-1315.

[51] Sinsabaugh R L, Gallo M E, Lauber C, Waldrop M P, Zak D R. Extracellular enzyme activities and soil organic matter dynamics for northern hardwood forests receiving simulated nitrogen deposition. Biogeochemistry, 2005, 75(2): 201-215.

[52] Treseder K K, Vitousek P M. Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology, 2001, 82(4): 946-954.

[53] Sinsabaugh R L, Carreiro M M, Repert D A. Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry, 2002, 60(1): 1-24.

[54] Waldrop M P, Zak D R. Response of oxidative enzyme activities to nitrogen deposition affects soil concentrations of dissolved organic carbon. Ecosystems, 2006, 9(6): 921-933.

[55] Michel K, Matzner E. Response of enzyme activities to nitrogen addition in forest floors of different C-to-N ratios. Biology and Fertility of Soils, 2003, 38(2): 102-109.

[56] Ajwa H A, Dell C J, Rice C W. Changes in enzyme activities and microbial biomass of tallgrass prairie soil as related to burning and nitrogen fertilization. Soil Biology and Biochemistry, 1999, 31(5): 769-777.

[57] Reich P B, Oleksyn J. Global patterns of plant leaf N and P in relation to temperature and latitude. Proceedings of the National Academy of Sciences of the United States of America, 2004, 101(30): 11001-11006.

[58] Cleveland C C, Reed S C, Townsend A R. Nutrient regulation of organic matter decomposition in a tropical rain forest. Ecology, 2006, 87(2): 492-503.

[59] Lambers H, Raven J A, Shaver G R, Smith S E. Plant nutrient-acquisition strategies change with soil age. Trends in Ecology & Evolution, 2008, 23(2): 95-103.

[60] Hedin L O, Brookshire E N J, Menge D N L, Barron A R. The nitrogen paradox in tropical forest ecosystems. Annual Review of Ecology, Evolution, and Systematics, 2009, 40(1): 613-635.

[61] DeForest J L, Smemo K A, Burke D J, Elliott H L, Becker J C. Soil microbial responses to elevated phosphorus and pH in acidic temperate deciduous forests. Biogeochemistry, 2012, 109(1-3): 189-202.

[62] McGroddy M E, Silver W L, de Oliveira R C Jr. The effect of phosphorus availability on decomposition dynamics in a seasonal lowland Amazonian forest. Ecosystems, 2004, 7(2): 172-179.

[63] Güsewell S, Verhoeven J T A. Litter N:P ratios indicate whether N or P limits the decomposability of graminoid leaf litter. Plant and Soil, 2006, 287(1-2): 131-143.

[64] Cleveland C C, Townsend A R, Taylor P, Alvarez-Clare S, Bustamante M M C, Chuyong G, Dobrowski S Z, Grierson P, Harms K E, Houlton B Z, Marklein A, Parton W, Porder S, Reed S C, Sierra C A, Silver W L, Tanner E V J, Wieder W R. Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis. Ecology Letters, 2011, 14(9): 939-947.

[65] Lin C F, Yang Y S, Guo J F, Chen G S, Xie J S. Fine root decomposition of evergreen broadleaved and coniferous tree species in mid-subtropical China: dynamics of dry mass, nutrient and organic fractions. Plant and Soil, 2011, 338(1-2): 311-327.

[66] Manzoni S, Porporato A. Soil carbon and nitrogen mineralization: theory and models across scales. Soil Biology and Biochemistry, 2009, 41(7): 1355-1379.

[67] Yanai R D. Phosphorus budget of a 70-year-old northern hardwood forest. Biogeochemistry, 1992, 17(1): 1-22.

[68] Olander L P, Vitousek P M. Biological and geochemical sinks for phosphorus in soil from a wet tropical forest. Ecosystems, 2004, 7(4): 404-419.

[69] Austin A T, Vivanco L, González-Arzac A, Pérez L I. There′s no place like home? An exploration of the mechanisms behind plant litter-decomposer affinity in terrestrial ecosystems. New Phytologist, 2014, 204(2): 307-314.

[70] Richardson A E, Simpson R J. Soil microorganisms mediating phosphorus availability. Plant Physiology, 2011, 156(3): 989-996.

[71] Esberg C, Toit B D, Olsson R, Ilstedt U, Giesler R. Microbial responses to P addition in six South African forest soils. Plant and Soil, 2010, 329(1-2): 209-225.

[72] Cleveland C C, Townsend A R, Schmidt S K. Phosphorus limitation of microbial processes in moist tropical forests: evidence from short-term laboratory incubations and field studies. Ecosystems, 2002, 5(7): 680-691.

[73] Gnankambary Z, Ilstedt U, Nyberg G, Hien V, Malmer A. Nitrogen and phosphorus limitation of soil microbial respiration in two tropical agroforestry parklands in the south-Sudanese zone of Burkina Faso: the effects of tree canopy and fertilization. Soil Biology and Biochemistry, 2008, 40(2): 350-359.

[74] Ilstedt U, Giesler R, Nordgren A, Malmer A. Changes in soil chemical and microbial properties after a wildfire in a tropical rainforest in Sabah, Malaysia. Soil Biology and Biochemistry, 2003, 35(8): 1071-1078.

[75] Kuzyakov Y, Biryukova O, Kuznetzova T, M?lter K, Kandeler E, Stahr K. Carbon partitioning in plant and soil, carbon dioxide fluxes and enzyme activities as affected by cutting ryegrass. Biology and Fertility of Soils, 2002, 35(5): 348-358.

[76] Cheng W X, Kuzyakov Y. Root effects on soil organic matter decomposition//Zobel R W, ed. Roots and Soil Management: Interactions between Roots and the Soil. Madison, WI: American Society of Agronomy, 2005: 119-119.

[77] Leff J W, Nemergut D R, Grandy A S, O′Neill S P, Wickings K, Townsend A R, Cleveland C C. The effects of soil bacterial community structure on decomposition in a tropical rain forest. Ecosystems, 2012, 15(2): 284-298.

[78] Kourtev P S, Ehrenfeld J G, Huang W Z. Enzyme activities during litter decomposition of two exotic and two native plant species in hardwood forests of New Jersey. Soil Biology and Biochemistry, 2002, 34(9): 1207-1218.

[79] Olander L P, Vitousek P M. Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry, 2000, 49(2): 175-191.

[80] Zheng J Q, Han S J, Wang Y, Zhang C G, Li M H. Composition and function of microbial communities during the early decomposition stages of foliar litter exposed to elevated CO2concentrations. European Journal of Soil Science, 2010, 61(6): 914-925.

[81] Elser J J, Acharya K, Kyle M, Cotner J, Makino W, Markow T, Watts T, Hobbie S, Fagan W, Schade J, Hood J, Sterner R W. Growth rate-stoichiometry couplings in diverse biota. Ecology Letters, 2003, 6(10): 936-943.

[82] van der Wal A, van Venn J A, Smant W, Boschker H T S, Bloem J, Kardol P, van der Putten W H, de Boer W. Fungal biomass development in a chronosequence of land abandonment. Soil Biology and Biochemistry, 2006, 38(1): 51-60.

[83] Güsewell S, Gessner M O. N:P ratios influence litter decomposition and colonization by fungi and bacteria in microcosms. Functional Ecology, 2009, 23(1): 211-219.

[84] Berg B, Laskowski R. Litter Decomposition: A Guide to Carbon and Nutrient Turnover. San Diego: Elsevier Science, 2006.

[85] Walker T W, Syers J K. The fate of phosphorus during pedogenesis. Geoderma, 1976, 15(1): 1-19.

[86] Kaspari M, Garcia M N, Harms K E, Santana M, Wright S J, Yavitt J B. Multiple nutrients limit litterfall and decomposition in a tropical forest. Ecology Letters, 2008, 11(1): 35-43.

[87] Sterner R W, Elser J J. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere. Princeton: Princeton University Press, 2002.

[88] Tilman D. Secondary succession and the pattern of plant dominance along experimental nitrogen gradients. Ecological Monographs, 1987, 57(3): 189-214.

[89] Elser J J, Sterner R W, Gorokhova E, Fagan W F, Markow T A, Cotner J B, Harrison J F, Hobbie S E, Odell G M, Weider L W. Biological stoichiometry from genes to ecosystems. Ecology Letters, 2000, 3(6): 540-550.

[90] Elser J J, Bracken M E S, Cleland E E, Gruner D S, Harpole W S, Hillebrand H, Ngai J T, Seabloom E W, Shurin J B, Smith J E. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters, 2007, 10(12): 1135-1142.

[91] Cleveland C C, Liptzin D. C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass?. Biogeochemistry, 2007, 85(3): 235-252.

[92] 宋飄, 張乃莉, 馬克平, 郭繼勛. 全球氣候變暖對凋落物分解的影響. 生態(tài)學報, 2014, 34(6): 1327-1339.

[93] 曾昭霞, 王克林, 劉孝利, 曾馥平, 宋同清, 彭晚霞, 張浩, 杜虎. 桂西北喀斯特區(qū)原生林與次生林鮮葉和凋落葉化學計量特征. 生態(tài)學報, 2016, 36(7): 1907-1914.

[94] Gallardo A, Schlesinger W H. Factors limiting microbial biomass in the mineral soil and forest floor of a warm-temperate forest. Soil Biology and Biochemistry, 1994, 26(10): 1409-1415.

[95] Fanin N, Fromin N, Buatois B, H?ttenschwiler S. An experimental test of the hypothesis of non-homeostatic consumer stoichiometry in a plant litter-microbe system. Ecology Letters, 2013, 16(6): 764-772.

[96] Berendse F, Aerts R, Bobbink R. Atmospheric nitrogen deposition and its impact on terrestrial ecosystems//Vos C C, Opdam P, eds. Landscape Ecology of A Stressed Environment. Netherlands: Springer, 1993: 104-121.

[97] Allison S D, Lu Y, Weihe C, Goulden M L, Martiny A C, Treseder K K, Martiny J B H. Microbial abundance and composition influence litter decomposition response to environmental change. Ecology, 2013, 94(3): 714-725.

[98] Huenneke L F, Hamburg S P, Koide R, Mooney H A, Vitousek P M. Effects of soil resources on plant invasion and community structure in Californian serpentine grassland. Ecology, 1990, 71(2): 478-491.

[99] Suding K N, Collins S L, Gough L, Clark C, Cleland E E, Gross K L, Milchunas D G, Pennings S. Functional- and abundance-based mechanisms explain diversity loss due to N fertilization. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(12): 4387-4392.

Effect of nitrogen and phosphorus availability on forest litter decomposition

LIN Chengfang1,2,， PENG Jianqin1,2, HONG Huibin1,2, YANG Zhijie1,2,*,YANG Yusheng1,2

1SchoolofGeographicalScience,FujianNormalUniversity,Fuzhou350007,China2StateKeyLaboratoryofSubtropicalMountainEcology(FoundedbyMinistryofScienceandTechnologyandFujianProvince),FujianNormalUniversity,Fuzhou350007,China

Nitrogen (N) and phosphorus (P) are the two most important elements for building plant proteins and genetic material, limiting forest production, and other ecosystem processes, and they profoundly affect litter decomposition. Litter-quality parameters, particularly initial lignin and N contents, ratios of C∶N, and lignin:N often correlate strongly with rates of litter mass loss in temperate and boreal forests. Furthermore, soil N availability and N addition also affect litter decomposition. In tropical and subtropical forests, where highly weathered soil is frequently observed, P could be more important than N in inhibiting litter decomposition. However, P has not been considered in most current ecosystem carbon cycling models, but fertilization experiments show different responses of litter decomposition rates to nutrition addition. Synergistic, antagonistic, and neutral effects can be observed. Both the “basic stoichiometric decomposition theory” and “microbial nitrogen mining” hypothesis have been used to explain litter decomposition rate variations with nutrition addition. Regarding rigid C∶N∶P ratios in microbial decomposers, different nutrition sources could result in altered microbial activity, and limited nutrient supplies could result in restricted litter decomposition. To clearly understand the effects of N and P regulation on decomposition, we need longer decomposition experiment durations, more intensive field and laboratory fertilization experiments, and simultaneously, microbe and enzyme dynamics in the decomposition process should be further investigated.

litter decomposition; N; P; nutrient availability; microbes; enzymes

國家自然科學基金面上資助項目(31270584)；國家自然科學基金重點資助項目(31130013)

2016- 08- 09;

2016- 11- 17

10.5846/stxb201608091636

*通訊作者Corresponding author.E-mail: zhijieyang@fjnu.edu.cn

林成芳，彭建勤, 洪慧濱, 楊智杰,楊玉盛.氮、磷養(yǎng)分有效性對森林凋落物分解的影響研究進展.生態(tài)學報,2017,37(1):54- 62.

Lin C F, Peng J Q, Hong H B, Yang Z J,Yang Y S.Effect of nitrogen and phosphorus availability on forest litter decomposition.Acta Ecologica Sinica,2017,37(1):54- 62.