持久性有機污染物在水生食物網中的傳遞行為

馮秋園,萬 祎,劉學勤,劉 永,*

1 北京大學環境科學與工程學院,水沙科學教育部重點實驗室,北京 100871 2 北京大學城市與環境學院,地球表面過程教育部重點實驗室,北京 100871 3 中國科學院水生生物研究所,武漢 430072

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持久性有機污染物在水生食物網中的傳遞行為

馮秋園1,萬 祎2,劉學勤3,劉 永1,*

1 北京大學環境科學與工程學院,水沙科學教育部重點實驗室,北京 100871 2 北京大學城市與環境學院,地球表面過程教育部重點實驗室,北京 100871 3 中國科學院水生生物研究所,武漢 430072

食物網是持久性有機污染物(POPs)在水生生態系統中傳遞的重要途徑,了解其傳遞行為與機制是POPs生態暴露風險評價的科學基礎。從4個方面展開了討論和分析：①食物網主要特征(營養級和食物鏈長度)與POPs環境行為的關系；②POPs在底棲及底棲-浮游耦合食物網中的環境行為；③微食物網對POPs環境行為的作用；④食物網的變化對POPs環境行為的影響。主要結論如下：①已有研究對水生生物中POPs生物放大作用存在較大爭議。一般營養級越高,POPs生物富集性越強,但由于各種生態和生理性質的影響,也存在例外情況。食物鏈長度與POPs生物富集性呈正相關。②POPs通過底棲食物網將沉積物中的POPs向上傳遞,底棲-浮游食物網的耦合提高了高營養級消費者的暴露風險,目前就POPs在底棲食物網中的生物放大性是否大于浮游食物網存在爭議。③微生物具有較大的比表面積,是吸附POPs的重要載體。另,沉積物中的微生物通過分解有機質,將POPs釋放到水柱中。微生物降解也是環境中POPs脫離環境的重要途徑。④在內、外壓力下,食物網結構和功能發生變化,使物質和能量的傳遞方向和效率發生改變,并與環境理化性質的變化互相耦合,影響POPs的環境行為。當前研究的重點多集中在POPs在浮游食物網,尤其是高營養級浮游食物網中的環境行為,對POPs在底棲及底棲-浮游耦合食物網和微食物網中環境行為的研究相對缺乏。有關POPs在食物網中環境行為的研究多集中在食物網的某個部分,時間尺度較短,缺乏對POPs環境行為動態變化的研究,未來需深入開展多尺度和多角度的POPs在食物網中環境行為的動態變化研究。新型POPs的生產和使用量不斷增加,但有關其在食物網中環境行為的相關分析還較為匱乏,需加強研究。

持久性有機污染物；傳遞行為；營養級；食物鏈長度；浮游-底棲耦合食物網；微食物網；食物網變化

持久性有機污染物(POPs)具有持久性、生物蓄積性、高毒性、半揮發性和遠距離傳輸的特點,會對人類健康和生態安全產生嚴重危害。POPs通過大氣干濕沉降、地面徑流和水-氣界面直接交換進入水生生態系統,是POPs在生態圈中傳遞的一個重要的“匯”。POPs進入水體后,被生物體通過被動擴散和攝食作用吸收,并沿食物網傳遞,成為POPs在水生生態系統中非常重要的環境行為,同時使頂級消費者受到高水平的POPs暴露風險,因此研究POPs在水生生態系統食物網中的環境行為成為國內外研究的重點和熱點[1- 3],但當前研究的重點仍集中在POPs在浮游食物網的傳遞,對在底棲及底棲-浮游耦合食物網和微食物網的研究仍不夠充分[4- 5],對各種內、外源環境壓力下,食物網變化對POPs環境行為影響的研究也相對缺乏[6- 9]。鑒于此,本文從食物網的主要特征與POPs環境行為的關系,POPs在底棲及底棲-浮游耦合食物網和微食物網中的環境行為及影響因素,以及目前較為關注的幾種內外源壓力下食物網變化對POPs環境行為的影響等4個方面,闡述了POPs在水生食物網中的環境行為,為揭示POPs在水生生態系統中的歸趨機制,判斷水生生物的POPs暴露風險,制定科學的環境標準提供參考。

1 食物網主要特征與POPs環境行為的關系

生物體所處的營養級和食物鏈長度是食物網的主要特征,是研究POPs在食物網中生物富集或生物放大時的重點考慮因素。在不同的生態系統中,其影響往往是不同的,了解特定生態系統中營養級和食物鏈長度與POPs生物富集或生物放大之間的相關關系,并探索影響這種相關關系的主要因素一直以來是生態學的熱點問題。

1.1 營養級與POPs生物富集性的關系

生物放大作用是營養級對POPs生物富集性影響的直接體現。一般情況下,營養級越高,POPs生物放大效應越明顯。研究發現,除 PFOA 外,爬行動物、哺乳動物等高營養級水生動物對PFCs(PFNA、PFDA、PFUA、PFDOA和PFOS)的生物富集(BAFs)系數大于5000,顯著高于無脊椎動物和魚類,存在明顯的生物放大現象[10- 12]。諸多研究發現[13-14]生物營養級(15N值)和PCBs濃度之間顯著正相關,生物放大因子大于1。通常認為POPs生物富集性隨營養級升高而增大的一個重要原因是脂質含量增加,但實際上并不是所有食物網中生物體的脂質含量都隨15N的升高而增加。另有研究表明,單位脂質POPs含量與營養級之間仍有非常顯著的正相關關系,說明營養級增加本身對POPs生物富集也具有重要影響,但營養級和脂質含量的相對貢獻大小較難評價[15- 16]。

但污染物并不總是隨營養級的升高而顯示生物放大效應。Neff等[17]、Varanasi等[18]和Broman等[19]在波羅的海的食物鏈中沒有發現PAHs的生物放大現象,推測是由于營養級越高,生物體對PAHs的分解活性越高,與其它地區的類似研究結果一致[20-22]。Mizukawa等[23]通過污染物濃度與生物體15N之間的相關關系,分析了日本東京灣中20種PBEDs和PCBs的生物放大現象,發現PCBs和部分PBDEs存在生物放大現象,另幾種PBDE同系物的濃度則隨營養級升高而下降,其原因可能是在生物體內被轉化或代謝分解了。Nfon等[24]分析了具有不同理化性質的POPs在波羅的海浮游和底棲食物網中的傳遞,發現所有PCBs同系物和OCPs存在顯著的食物鏈放大作用(FCMFs>1),但由于生物體的代謝分解作用,PAHs和PCNs的食物鏈放大系數(FCMFs)小于1,是營養稀釋作用。上述研究說明,POPs的食物鏈放大作用受到生物轉化和代謝分解的限制,特別是在較高營養級中[25- 26]。另有研究發現,一般低營養級浮游食物網不存在污染物的生物放大或很低,在高營養級消費者體內存在明顯的生物放大,因為低營養級生物對能量的需求量較低,因此食物的攝入量相對更低,而食物攝入是POPs富集的一個重要途徑[27-29]。Lundgren等[30]發現在亞北極地區波的尼亞灣的底棲食物網中大多數高氯代PCNs沒有生物放大現象,推測其原因是由于高氯代PCNs體積較大,阻礙了其在生物體內的擴散和吸收。Evenest研究了幾種POPs在斯的巴特爾群島的孔斯峽灣底棲食物網中的生物富集情況,發現除了順式九氯,沒有觀測到POPs的生物放大現象,幾種無脊椎動物體內的POPs濃度等于甚至超過了魚類或絨鴨體內的POPs濃度,原因是這些底棲無脊椎動物是食腐性的,POPs的生物轉化和排出能力低,且直接暴露在POPs濃度較高的沉積物間隙水中[31]。

營養級對POPs生物富集性的影響通常是通過生物放大或營養級放大來分析,一般情況下,POPs的生物富集性隨營養級的升高而增強,但也有例外,因為其它各種生態和生理性質,如獵物的豐度、生長速率、生物與沉積物的接觸程度、攝食POM的量、微生物環導致的高15N和低POPs濃度等都不同程度地控制著POPs的生物富集,使POPs的實際濃度偏離了根據營養級預測得到的值[31-33]。另外,目前生物所處營養級一般用15N來表示,生物放大性通過15N與POPs濃度的相關關系來分析,但是對于底棲食物網,單純地利用15N有時并不能很好地指示底棲動物所處的實際營養級,因為某些生物或所攝食的生物具有同位素分餾作用,例如,一些攝食POM的生物,由于細菌環(bacteria loop)的分解和同位素分餾作用,POPs暴露風險降低,但是15N的值卻提高了[34]；其次,15N基準值的季節性變化也會影響15N 和POPs相關關系的斜率；再者,很多底棲無脊椎動物是雜食性/食腐性,因此導致POPs傳遞的再循環,使POPs的負荷較高,但是單純地分析15N可能并不能反映出這種循環。

目前,有關POPs在水生食物網中的生物放大作用具有很大的爭議,如Bruner等[35]、Losser等[36]和Gobas等[37]等認為生物放大在整個食物網都存在,但Borga等[38]認為在低營養級中,由于生物體攝食吸收的POPs可以忽略,所以不存在生物放大作用。Guruge等[39]認為生物放大只存在于直接呼吸空氣的生物體內。當前,對營養級升高造成的POPs生物富集性增強,主要還是從脂質含量增加來解釋[40],但實際上,營養級升高本身也是一個重要的影響因素,但是其具體影響機制紛繁復雜,存在很多疑問和不確定性。Gobas等[31]推測一是因為大部分生物量在沿營養級傳遞過程中轉化成了能量被耗散,造成污染物的濃縮,二是由于食物在胃腸道中被消化,提高了化學物質的逸度。綜上發現,營養級與POPs在食物網中生物富集性之間的關系,及潛在的具體機制仍存在很多疑問。在具體的研究中,需要根據生物體的生理特征,結合POPs理化性質和生態系統的特點綜合考慮,才能得到較為準確的預測結果。

1.2 食物鏈長度與POPs生物放大效應的關系

目前研究認為,食物鏈延長會增加頂級消費者體內的污染物濃度[2,41- 42]。Kidd等[43]發現加拿大拉柏吉湖中,魚體內的毒殺酚濃度異常高,明顯高于其它湖泊的同種魚類。通過對比湖泊的污染輸入、營養級結構等發現,拉柏吉湖比其它湖泊的食物鏈更長,同種魚在拉柏吉湖中的N15要顯著高于其他湖泊,從而導致其體內有異常高的污染物濃度,由此揭開了食物鏈長度會提高POPs生物放大效應的認識。Whittle等[44]通過研究蘇必利爾湖、安大略湖、休倫湖、伊利湖的食物鏈長度和生物放大系數發現食物鏈長度和生物放大系數呈正相關,進一步證明食物鏈延長會提高POPs的生物放大作用。另有諸多研究發現食物鏈延長會導致生物體脂質含量增加,那POPs生物富集的提高是否只是由于食物鏈延長引起的脂質含量增加而導致的？根據是否存在糠蝦和草食性魚類,Rasmussen等[2]對北美五大湖區的81個湖泊劃分為3類,通過對比頂級消費者湖紅點鮭(Salvelinusnamaycush) 體內的PCBs 濃度發現,增加1個營養級,湖紅點鮭(Salvelinusnamaycush)體內的PCBs濃度增加3.5倍,但脂質含量只增加了1.5倍,因此認為食物鏈延長本身也會導致POPs在頂級消費者體內生物富集性的提高。Bentzen等[40]進一步分析其原因得到：①糠蝦具有晝夜遷移行為,會攝食部分沉積物,導致其體內的POPs濃度比其它同營養級浮游生物更高；②捕食浮游動物的魚類通過捕食降低了浮游動物的生物量,降低了生物量稀釋作用,提高了POPs濃度；③頂級消費者由捕食浮游動物改為捕食體型較大且營養級相對較高的糠蝦,攝食能耗降低,脂質含量增加[45],POPs濃度升高。

2 底棲及底棲-浮游耦合食物網中POPs的環境行為

目前,有關POPs在食物網中傳遞的研究多集中在浮游食物網,但底棲食物網是生態系統中物質循環和能量流動的重要環節,并通過與浮游食物網相耦合,共同影響POPs在水生生態系統中的傳遞。據研究：①底棲初級和次級生產力的貢獻非常大,大多魚類對底棲初級、次級生產力的依賴程度甚至高于浮游初級和次級生產力[46- 48]。②底棲大型無脊椎動物在營養鹽的循環和輸入方面起到非常重要的作用[49]。③底棲細菌的生產力往往高于浮游細菌[50]。另外,底棲生境是POPs在水生生態系統中循環流動的“匯”,底棲生物通過攝食和被動吸收從沉積物中獲取POPs,并通過底棲食物網向上傳遞到頂級消費者體內,是POPs循環的關鍵部分。但POPs在浮游和底棲食物網中的傳遞特征具有一定的差異。Kidd等[16]在馬拉維湖研究發現,同一污染物在浮游食物網中生物富集程度大于底棲食物網,其原因是同一營養級的底棲(藻類和腹足類等)生物比浮游動物、毛翅類昆蟲、腹足類生物的脂質含量低,且底棲藻類的生長率更高,產生“生長稀釋”作用。Nfon等[24]發現PCBs在底棲食物鏈中的食物鏈放大系數要低于浮游食物鏈,推測是由于浮游生物缺少分解PCBs的酶。但Campfens等[51]認為沉積物中POPs的逸度通常遠大于水體,底棲生物受到的污染會更嚴重。目前,已普遍認識到底棲食物網對POPs環境行為的重要影響,但底棲食物網在POPs傳遞過程中所起的作用仍莫衷一是,傳遞機制尚不清晰,未來還需要進一步的深入研究。

早期的研究中,底棲食物網和浮游食物網被認為是互相獨立的,但是隨著研究的深入,逐漸認識到二者是通過各種方式耦合在一起的,通過物質和能量的互相傳遞和交換共同支持生態系統的功能[52],POPs在此過程中隨物質循環、能流流動出現耦合。一般情況下,浮游-底棲食物網主要通過以下方式耦合：懸浮顆粒從水柱中沉降,實現浮游生境對底棲動物的營養供給[53- 56]；底棲生物降解顆粒有機質為營養鹽,并再循環進入水柱[57- 58],底棲沉積物的再懸浮加強浮游-底棲耦合過程[59]；雜食性魚類捕食生境多變,能廣泛捕食浮游、底棲生物及一些陸地的無脊椎動物[47],從而實現不同生境之間物質和能量的傳遞與交換[60- 61]。在上述過程中,POPs隨之一起實現浮游-底棲食物網的耦合,因此只分析一種POPs傳遞路徑,不能準確地判斷頂級捕食者體內POPs的來源和暴露風險。例如,通過底棲-浮游食物網的耦合,沉積物中的有機碳可以再循環進入到浮游生物體內,同時將沉積物中與有機碳相絡合的POPs通過食物網向上傳遞,沉積物中積累多年的POPs使得水柱中捕食者體內的污染物濃度維持在一定的水平[15,62]。糠蝦等白天在湖泊底部攝食底棲生物,晚上遷移到上層水柱中,捕食浮游生物,實現能量和POPs的浮游-底棲耦合。通過模擬糠蝦的3種生活情景：①只生活在浮游生境；②部分時間生活在浮游生境,部分時間生活在底棲生境；③只生活在底棲生境。模擬結果顯示情景①中糠蝦體內的PCBs濃度最小,情景③最大,情景②介于兩者之間,且其模擬結果與實測值最相符[92]。這說明了浮游-底棲食物網的耦合,及耦合提高了浮游動物和魚類的POPs暴露風險。

在過去,底棲生境往往只作為污染物在水生生態系統中傳遞的 “匯”,且由于采樣困難等原因,POPs在底棲食物網中環境行為的研究相對較少,但了解POPs在底棲食物網中的環境行為是解析POPs在水生生態系統中歸趨機制必不可少的內容,需進一步加強研究。另外,底棲食物網通過多種過程和浮游食物網耦合,對POPs的環境行為產生復雜影響,但目前對POPs在底棲-浮游耦合食物網中的歸趨機制知之甚少,是未來探索的一個重點。

3 微食物網對POPs環境行為的作用

微生物,包括病毒、細菌、鞭毛蟲、纖毛蟲、浮游植物和微型的浮游動物,在生態系統中具有非常重要的作用,這些生物形成一個非常復雜的微食物網。微食物網通過以下機制影響食物網的結構、功能：①礦化分解有機質為浮游植物提供營養鹽；②有機碎屑消耗殆盡時,細菌會與浮游植物競爭無機營養鹽[63- 64]。③細菌可以替代小型浮游動物,緩解初級生產者的被捕食壓力。④沉積物中的細菌是大型無脊椎動物的食物來源,但有關這一點存在較大的爭議[65- 66]。研究表明,微食物網在POPs的傳遞過程中也起到重要作用,微生物吸附是POPs傳遞的一個重要途徑,可以通過微食物網向高營養級生物傳遞。微生物豐度高、體型小、周轉速率快、具有最大的比表面積,在水生生態系統中異養細菌通常占到了生物表面積的80%,因此成為一個非常重要的POPs吸附體。且由于微生物體型較小,POPs在微生物與水相之間很快達到平衡,幾乎不受“生長稀釋”的影響,因此微生物成為比浮游植物更重要的POPs吸收介質[67]。另外,顆粒物沉降過程中有機質被不斷分解,在一個較短的時間內,細菌分解不會影響PCBs在顆粒物與水之間的分配,導致PCBs濃度不斷升高[68]。同時,礦化分解提高了顆粒物的表面積,增加了PCBs的吸附[69- 70]。當顆粒物沉降到沉積物表層時,微生物豐度較大,有機質被大量分解,然后大部分PCBs再次進入到水柱中,進行再循環。由此可見,微食物網對POPs在水生生態系統中的傳遞和再循環起到了非常重要的作用。另外,眾所周知,微生物分解是POPs離開水生生態系統的重要途徑,但由于微食物網采集及分析存在諸多困難,其相關研究還非常缺乏。

4 主要內外源壓力下的食物網變化及對POPs環境行為的影響

食物網是POPs在水生生態系統中傳遞的關鍵路徑,在受到一系列的內源驅動和外源壓力時,食物網的組成、結構和功能會發生很大的變化,從而使食物網的動力學特征發生較大的變化。其中,季節變化會使水生生態系統發生規律性變化,探索由于季節演替導致的POPs在環境介質與食物網之間,及食物網內部環境行為的規律性變化是生態學研究的重點之一；另外,富營養化和外來物種入侵或引進導致的生態和環境災變是目前國際上水生生態系統普遍存在的兩個問題,在這種外源壓力下,水生生態系統的結構和功能會發生顯著變化,甚至發生穩態轉換,從而使POPs在食物網中的環境行為和歸趨機制發生變化。因此,本文從季節變化、富營養化和外來物種入侵或引進這3個較為常見和普遍關注的內、外源壓力入手,探討了食物網變化對POPs環境行為的影響。

4.1 食物網的季節演替對POPs傳遞的影響

光照、溫度、風和徑流輸入等的季節變化會導致水生生態系統的理化性質,生物體的生理特征和種群結構發生周期性變化,進而引起食物網結構和功能的變化,使POPs的環境行為發生變化。

研究認為,溫度、光照、營養鹽和水動力條件的變化使浮游植物的生物量及物種組成發生季節演替,浮游植物是食物網中物質循環和能量流動的起點,通過“上行控制”作用使高營養級消費者的棲息環境、生長率、食性等發生較大的變化,進而引起整個食物網的變化。在諸多地區的浮游和底棲食物網中都觀察到了明顯的季節變化[31，71- 73]。研究表明,水生生態系統中POPs濃度具有明顯的季節變化,7月份最低、9月底最高,之后又不斷下降,其原因主要是由于藻類生產力的季節變化造成的[74- 75]。Nizzetto[8]研究發現,浮游動物體內的PCBs濃度在水華后期劇烈下降,生物富集系數(BAF)最低,不存在生物放大作用,在水華爆發前期和爆發期存在明顯的生物放大作用。因為在水華期間,浮游動、植物快速生長,生物量劇烈變化,通過“生長稀釋”和 “生物量稀釋”改變了PCBs的暴露風險。另外,浮游動物物種組成、捕食者和生理學特征的季節性變化也會影響POPs的生物富集性。魚類的生長率和種群結構與初級生產力和浮游生物的密度密切相關,浮游動、植物的季節性演替,使得魚類的攝食習性也有周期性的變化,進而導致魚類POPs生物富集性的季節變化[44]。另外,各種不同魚類其單位脂質POPs濃度的季節變化不一樣,其原因目前還不是十分明確,推測可能是食性不同和遷移方式不同造成的[27,31]。

此外,浮游植物的季節性生長會影響有機質的沉降,有研究發現一年中大約有70%脂質沉降發生在春季水華時期,與此同時POPs沉降量也最大,底棲生境的POPs暴露風險增加[76],而在冬季,脂質的沉降量較低,POPs主要在浮游食物網中富集[67]。底棲群落的能量很大程度上依靠浮游生境的浮游碎屑[53],同位素分析顯示浮游植物是底棲無脊椎動物的主要食物來源[77]。浮游碎屑沉降量的顯著季節變化,使底棲群落的生存環境和食物資源發生顯著的季節變化[65],進而使底棲大型無脊椎動物的脂質含量發生季節變化[78],而脂質含量是影響POPs生物富集的主要因素；另外,攝食作用是生物體POPs的主要來源之一,因此浮游生態系統中污染物的季節性變化會反映到底棲群落中,但其變化趨勢和幅度可能會存在差異,因為很多底棲動物是雜食性的,能夠緩解季節變化的影響,而且新沉降的物質能夠很快地與老的沉積物混合(生物擾動),使得POPs分布特征發生混合。總體上,底棲食物網生物富集性的季節性變化不如浮游食物網顯著。另外,不同底棲種群之間的季節變化趨勢和幅度也各不相同,因為它們的生態特征(攝食模式、死亡率)和生理特征(氧吸收速率、生物轉化能力、新陳代謝等)不同,這些都會影響污染物吸收、傳遞、排泄[31]。Hummel等[79]和Capuzzo等[80]的研究發現,底棲軟體動物體內的PCBs濃度受到季節性產卵和生殖的影響,會發生明顯的季節變化,生殖會減少軟體動物體內50%—66%的PCBs含量[81]。

環境理化性質和生物因素的季節變化造成POPs在環境和食物網中的分配和行為發生變化。如,夏季水溫升高,底棲生物和微生物活性增強,表層水流變慢和熱分層出現,加劇了底部的缺氧,促進DDT厭氧分解,DDD濃度升高[82]。另外,夏季水溫升高改變生物的呼吸率和膜的通透性,POPs吸收速率加快,生物富集性增強,POPs暴露風險升高[83]。

季節演替通過溫度、風速、光照、DO等因素的周期性變化,驅動食物網發生規律性變動,造成POPs在食物網中的環境行為的季節性變化。環境介質、POPs的性質與食物網變化互相影響,共同作用于POPs的環境行為,但目前往往只考慮某一方面對POPs環境行為的影響,對三者之間的聯系關注不夠。另外,大多數研究只集中在食物網的某一環節,如低營養級浮游食物網,缺乏從整體角度的探索,且研究的時間尺度較短,多集中在某年的特定季節,難以發掘其規律性變化。因此,未來的研究需要從多角度、整體性和長時間尺度上深入研究POPs在水生食物網中環境行為的季節性變化。

4.2 富營養化條件下食物網變化對POPs環境行為的影響

富營養化和POPs污染是水生態系統目前遇到的兩個重要環境問題,這兩者之間往往是同時發生、互相聯系的。傳統上,富營養化和POPs污染的研究通常是分開的,但后來的研究發現,營養水平能夠影響污染物的循環和可生物利用水平[8](圖1)。瑞典環境保護局于1995年開展了揭示白令海附近海域及湖泊的富營養與污染物(POPs,微量金屬)之間互相聯系的5年研究計劃(EUCON)[6]。

富營養化會促進水-氣界面的POPs輸入[74],或減少揮發[4],改變食物網組成、多樣性和優勢種以及生態作用機制和能流傳遞效率、方向,直接或間接地影響POPs的環境行為和傳遞機制[6,84- 85]。對于初級生產者,富營養化促使浮游植物的優勢種由藍、綠藻取代硅藻、金藻等,初級生產力大大提高,生物量增加,大型水生植物和底棲藻類死亡,初級生產力從底棲為主導變為浮游占主導。由于藍藻的食物品質較差,使消費者的食物類型從浮游向底棲轉變[86- 87],從而改變了食物網中物質流的傳遞方向,同時改變了POPs沿食物網的流動路徑。浮游生物POPs濃度降低,其原因在于：相較于硅藻和金藻等,藍藻的脂質含量較低[88- 89]；且生物量大大增加導致“生物量稀釋”,生長速率較快,發生“生長稀釋”[90- 93]；另外,在富營養條件下,藻類的脂質含量相較于貧營養條件下更低[16,67]。

對于浮游和底棲動物,富營養化導致透光度下降,附生藻類和大型水生植物死亡,①使得浮游和底棲動物的棲息、避難生境減少,增強了魚類的捕食作用[94- 95],大型無脊椎動物減少,且小型化；②藍藻爆發,可攝食的食物資源減少,質量變差,導致初級消費者豐度下降、優勢種改變,且食性發生變化。因此POPs在食物網中的傳遞路徑發生變化；③藻類爆發導致有機質的沉降量增加。首先,有機質大量分解造成沉積物-水界面缺氧[97],底棲生物大量死亡,優勢種變為耐受低氧種[6,87,95- 96],使得底棲食物網發生較大的變化,POPs沿食物網的傳遞發生改變。其次,POPs隨顆粒物沉降的通量增加[67,97],大部分POPs從水柱中移除,降低了浮游生境的POPs暴露風險[98- 99],多項研究表明浮游食物鏈中POPs濃度與富營養化水平呈負相關[92,100]。同時沉積物中POPs濃度升高[4,89],底棲食物網的暴露風險提高[75,101- 102]。

對于魚類等高營養級生物,富營養化會減少物種進化過程中對環境變化的生態響應,導致物種滅絕,降低多樣性[103],另外浮游和底棲群落的變化,使魚類的攝食食性、生長率和脂質含量都會發生較大的,影響POPs的生物富集和傳遞效率[93，104- 105]。例如,Lasson等[98]對瑞典的61個湖泊研究發現,魚類體內PCBs生物富集系數(BAF)與湖泊生產力呈顯著負相關,因為富營養化條件下生產力提高,魚類生長加快,發生“生長稀釋”。另外,魚類等高營養級的生物,其攝食吸收的POPs所占比例較大,低營養級POPs濃度的變化會沿食物鏈影響魚類體內的POPs濃度[93,106]。但是上述幾個不同的影響因素,在不同的生態系統中或是不同的條件下,起主導作用的因素不同。

對于微生物,富營養化會直接或通過改變棲息生境的理化性質間接地影響微生物對POPs的分解速率,Graham等[107]研究認為富營養條件下微生物降解POPs的速率要高于寡營養水平,但是目前這方面的研究相對較少。另如前文所述,富營養化會擴大和加強底棲生境的缺氧程度,促使微生物將DDT轉化為DDD[82- 83]。

圖1 富營養化條件下食物網變化對POPs環境行為的影響Fig.1 Influences of foodweb changes caused by eutrophication on environmental behaviors of POPs

4.3 物種入侵或引進對POPs環境行為的影響

外來物種的入侵或引進是目前水生生態系統遇到的危機之一,對食物網的組成、結構和動態變化產生了重要的影響,例如,生物體的食性、生長率、營養位等,進而影響POPs的暴露風險,及在食物網中的環境行為和傳遞機制。研究發現,中營養級物種入侵會導致浮游動物和攝食浮游動物魚類的營養位(trophic position)增加,提高其捕食者體內的污染物濃度,例如,尾突蚤或胡瓜魚等中營養級物種入侵后,改變了浮游動物的群落結構,優勢種由枝角類變為橈足類,浮游動物生物量降低[108- 109],提高了浮游動物和魚類的營養位,進而導致其體內的污染物濃度升高[9,110]。另外,在食物網中引入糠蝦等新物種,會延長食物鏈長度,且由于糠蝦的晝夜遷移行為,會增加浮游-底棲食物網的耦合程度,導致POPs在頂級消費者體內的濃度升高[2]。

但其它研究發現,外來種入侵并不總是引起較高營養級生物污染物暴露風險的增加。在加拿大實驗湖L227和L110中引入梭子魚或肉食性白斑狗魚后,生態系統的群落結構、物種豐度和優勢種都發生了改變,很多魚類的攝食習慣發生變化,從主要攝食浮游動物轉變為攝食底棲動物,提高了營養位,但魚類體內的PCBs、DDT、HCH和Hg等污染物的濃度或是沒有變化,或是下降了,推測這可能是由于營養級之間復雜的級聯作用導致的[111]。例如,中營養級物種入侵,導致浮游動物減少,浮游植物的生物量增加,產生“生物量稀釋”[109,112- 113],或因為入侵的物種比傳統獵物的營養位更高[110,114]、密度更大[115],消費者的捕食偏好改變,覓食效率提高,生長率更高[9],從而導致“生長稀釋”,使污染物濃度下降。

物種入侵或是人工引入會通過營養級聯作用對多個營養級產生不同程度的影響,從而對食物網的結構、功能和生態過程產生影響,進而導致POPs沿食物網的傳遞發生很大的變化,但目前對這方面的研究還相對較少,作用機制還不甚清晰。

5 結論與展望

營養級和食物鏈長度是食物網的2個主要特征,是研究POPs生物富集或生物放大時的重點考慮因素。一般情況下,POPs生物富集與營養級呈正相關,但受到生物體各種生理、生態因素和POPs理化性質的影響,有時會出現例外。各種影響因素紛繁復雜,如何互相聯系作用于營養級與POPs生物富集性之間的相關關系尚不十分明確,需進一步探索。食物鏈長度與生物富集呈正相關,除脂質的影響外,其它具體作用機制還需深入研究。底棲食物網是POPs在水生生態系統中傳遞的一個重要途徑,但目前對POPs在底棲食物網中環境行為的認識莫衷一是,尚不明確。另外,底棲食物網通過各種過程與浮游食物網耦合,對POPs的環境行為產生復雜的影響,但相關研究甚少,需要加強關注。微食物網對POPs環境行為的影響逐漸被關注,目前相關研究主要集中在細菌對POPs的分解和吸附作用,由于微生物體型小,分析困難,微食物網中POPs環境行為的動態研究和定量研究還相對缺乏。在內源驅動和外源壓力的作用下,比如季節演替、富營養化、物種入侵等,使環境介質、食物網和POPs的結構、性質發生復雜的變化,三者之間互相反饋導致POPs沿食物網的環境行為發生更為錯綜復雜的變化,但是目前這方面的研究還不夠全面和系統,是研究的重點和難點。

目前,POPs在食物網中環境行為的研究主要集中在“classic” POPs,包括PCBs、OCPs和PAHs等,但在傳統POPs被禁用多年后,很多替代性的新型POPs被越來越多地使用,并在世界范圍內的不同環境中都有檢出。例如,在中國,海洋哺乳動物和沉積物中傳統PBDE開始逐漸被新型阻燃劑BFRs替代[116- 117],渤海地區更是遭到了新型POPs的嚴重污染[118]。在南、北極地區也分別都檢測到了新型POPs,并認為存在生物放大的可能。目前對于新型POPs可以獲取的數據還很少[119- 121],對于其生物富集性的研究也多集中在少數地區的極少數大型哺乳動物和魚類中。未來,需要加大對新型POPs在水生食物網中的研究。

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Environmental behavior of persistent organic pollutants in aquatic food web

FENG Qiuyuan1, WAN Yi2, LIU Xueqin3, LIU Yong1,*

1CollegeofEnvironmentalScienceandEngineering,TheKeyLaboratoryofWaterandSedimentSciencesMinistryofEducation,PekingUniversity,Beijing100871,China2CollegeofUrbanandEnvironmentalScience,MOELaboratoryforEarthSurfaceProcess,PekingUniversity,Beijing100871,China3InstituteofHydrobiologyChineseAcademyofSciences,Wuhan430072,China

Food web is an import transfer path in aquatic ecosystem. It is essential to explore the environmental behavior of persistent organic pollutants (POPs) along the food web, which will provides cientific foundations for risk evaluation of ecological exposure. Here, we analyzed and summarized the environmental behavior of POPs in aquatic food web, including (a) relationships between trophic levels and food chain length and biomagnification; (b) POPs transfer along benthic and benthic-pelagic coupling food web; (c) adsorption and degradation of POPs by microbes; (d) influences of food web changes caused by several common environmental pressures on the environmental behavior of POPs. The results showed increased bioaccumulation in higher trophic levels, but exceptions were noted because of ecological and physiological factors, such as diet, prey abundance, POPs degradation and isotope enrichment by microbial loop, growth rate, and lipid content. Food chain length was positively correlated with bioaccumulation. When POPs were transferred from the sediment to top consumers, the coupling of pelagic-benthic food web would enhance the exposure risks of higher trophic level consumers to POPs. Controversies existed whether the biomagnification of POPs along benthic food web was greater than that along the pelagic food web. Microbes could adsorb POPs more efficiently because of having a larger surface area. Microbes in the sediment decomposed organic materials, recycling POPs into the water column. Microbial degradation is an important way for POPs leaving aquatic ecosystem. Food web changes caused by seasonal succession, eutrophication and exotic invasions could change the direction and efficiency of energy transfer, and further resulted in changes of the environmental behavior of POPs. Most current studies mainly focused on the environmental behavior of POPs in pelagic food web, especially on the higher trophic levels, lacking researches on the environmental behavior of POPs in benthic and pelagic-benthic coupling food webs and microbial loops. Furthermore, the studies on environmental behaviors of POPs were always restricted to parts of the food web on small temporal and spatial scales, lacking researches on dynamic changes of the environmental behavior of POPs from multiple perspectives and large scales. New POPs have been increasing in production and usage, but studies about its environmental behavior along food web were still scare. Future studies should be conducted considering the above.

persistent organic pollutants (POPs); environmental behavior; trophic level; length of food chain; pelagic-benthic coupling food web; microbial food web; food web changes

國家重點基礎研究發展計劃(973計劃)(2015CB458900)

2016- 02- 04; 網絡出版日期:2016- 12- 19

10.5846/stxb201602040256

*通訊作者Corresponding author.E-mail: yongliu@pku.edu.cn

馮秋園,萬祎,劉學勤,劉永.持久性有機污染物在水生食物網中的傳遞行為.生態學報,2017,37(9):2845- 2857.

Feng Q Y, Wan Y, Liu X Q, Liu Y.Environmental behavior of persistent organic pollutants in aquatic food web.Acta Ecologica Sinica,2017,37(9):2845- 2857.