陸光華,覃冬葒,宗永臣
(1. 河海大學(xué)環(huán)境學(xué)院,江蘇 南京 210098;2. 西藏農(nóng)牧學(xué)院水利土木工程學(xué)院,西藏 林芝 860000)
硫丹(endosulfan)是一種合成有機(jī)氯殺蟲劑,自20世紀(jì)50年代開始使用,主要用于控制各種作物(棉花、水稻、高粱、大豆、煙草、茶葉、咖啡等)害蟲。硫丹的化學(xué)名稱為1,2,3,4,7,7-六氯雙環(huán)[2.2.1]庚-2-烯-5,6-雙羥甲基亞硫酸酯,包括α-硫丹和β-硫丹2 種異構(gòu)體,其結(jié)構(gòu)及主要理化性質(zhì)見表1。技術(shù)硫丹(CAS:115-29-7)為α-硫丹和β-硫丹的混合物,二者的比例約為7∶3。硫丹的長期生產(chǎn)和使用導(dǎo)致硫丹在環(huán)境中無處不在。農(nóng)業(yè)灌溉和降雨導(dǎo)致的土壤徑流和滲透是硫丹進(jìn)入水環(huán)境的主要途徑,在稻田附近的水體中硫丹質(zhì)量濃度高達(dá)13.5 μg/L,而在山區(qū)河流的硫丹質(zhì)量濃度也達(dá)到0.7 μg/L[1]。因具有較強(qiáng)親脂性,進(jìn)入水環(huán)境的硫丹可以累積在水生生物體內(nèi),在魚組織中的硫丹殘留水平可達(dá)到10~400 ng/g[2],生物富集因子在2 400~11 000[3]。
硫丹具有環(huán)境持久性、生物蓄積性和遠(yuǎn)距離環(huán)境遷移能力,其對生態(tài)系統(tǒng)的風(fēng)險(xiǎn)和對人類健康的影響日益引起關(guān)注。2011年硫丹及其相關(guān)異構(gòu)體被斯德哥爾摩公約列入持久性有機(jī)污染物(persistent organic pollutants, POPs)附件A(消除類)。我國自2014年3月26日起,除特定豁免用于防治棉花棉鈴蟲、煙草煙青蟲的生產(chǎn)和使用外,禁止硫丹的生產(chǎn)、流通、使用和進(jìn)出口。根據(jù)《中華人民共和國食品安全法》《農(nóng)藥管理?xiàng)l例》有關(guān)規(guī)定以及《關(guān)于持久性有機(jī)污染物的斯德哥爾摩公約》的履約要求,農(nóng)業(yè)部擬自2018年7月1日起,撤銷所有硫丹產(chǎn)品的農(nóng)藥登記證;自2019年3月27日起,禁止所有硫丹產(chǎn)品在農(nóng)業(yè)上使用。目前世界上已經(jīng)有60多個(gè)國家禁止使用硫丹。
表1 2種硫丹異構(gòu)體的結(jié)構(gòu)式及理化性質(zhì)
注:Kow為辛醇-水分配系數(shù);Koc為標(biāo)化分配系數(shù)。
很多研究表明,硫丹對水生生物、陸生生物和人類具有高毒性[4-6]。作為一種持久性有機(jī)污染物,即使天然水體中硫丹的殘留濃度不高,但是長期暴露可能產(chǎn)生生物累積和放大效應(yīng)[7],不僅影響魚類正常的生長繁殖,也給食品安全帶來潛在威脅[8]。日本規(guī)定水產(chǎn)品中硫丹最大殘留量為4 μg/kg,而我國尚無相關(guān)限量標(biāo)準(zhǔn)[9]。
隨著硫丹在全世界范圍的地表水中頻繁檢出,其對非靶生物的毒性效應(yīng)引起了廣泛關(guān)注。硫丹通常對魚類的毒性大于對水生無脊椎動(dòng)物的毒性[13],它可以影響魚類中樞神經(jīng)、免疫和生殖系統(tǒng),并可能導(dǎo)致魚類行為異常,嚴(yán)重情況下可導(dǎo)致魚類死亡[14]。魚類致死毒性通常以96 h半致死濃度(ρLC50)為測試終點(diǎn),表2總結(jié)了硫丹對不同魚類的96 hρLC50數(shù)據(jù)。大多數(shù)研究針對技術(shù)硫丹進(jìn)行毒性測試,受試魚類個(gè)體通常較小,而且多數(shù)為幼魚。從表2可見,硫丹對魚類的急性毒性變化很大,96 hρLC50的范圍為0.1~70 μg/L。毒性數(shù)據(jù)變化的主要原因是不同魚種對硫丹的敏感性(或耐受性)不同,而魚的個(gè)體大小、不同發(fā)育階段、性別也對毒性測試結(jié)果有影響。一般認(rèn)為,生命早期階段的魚比青年或成年的魚更敏感[15],而性別差異的主要原因是由于雌魚脂質(zhì)含量高于雄魚[16]。魚體脂含量高有利于保護(hù)機(jī)體免受親脂性化學(xué)品的毒性影響,因?yàn)槟軌蜻_(dá)到靶器官的化學(xué)品相對更少,因此,雌魚對親脂性毒物的耐受性更強(qiáng)[16-17]。此外,對同一測試魚種,不同的暴露方式(流動(dòng)/靜態(tài)/半靜態(tài))也影響毒性結(jié)果。如,Sunderam等[18]發(fā)現(xiàn)硫丹對彩虹魚(Pseudomugilfurcatus)的96hρLC50值在流動(dòng)暴露條件下為0.5 μg/L,而在靜態(tài)條件下為11.4 μg/L。硫丹在流動(dòng)暴露條件下對翠鱧(Channapunctatus)的96hρLC50值為7.75 μg/L[19],而在靜態(tài)條件下為5.58 μg/L[20],由于這兩個(gè)數(shù)據(jù)來自不同實(shí)驗(yàn)室,因此,可能存在其他方面的影響因素。此外,研究還發(fā)現(xiàn),水溫和堿度對硫丹暴露下虹鱒魚的存活率有顯著影響[4]。
根據(jù)我國GB/T 31270—2014《化學(xué)農(nóng)藥環(huán)境安全評(píng)價(jià)試驗(yàn)準(zhǔn)則》的毒性劃分標(biāo)準(zhǔn),當(dāng)農(nóng)藥對魚類的96 hρLC50值小于0.1 mg/L時(shí),說明該農(nóng)藥對魚類有劇毒。從表2可見,硫丹對所有受試魚類的毒性都屬于劇毒。
表2 硫丹對不同魚類的96 h半致死濃度(ρLC50)數(shù)據(jù)
細(xì)胞凋亡是維持健康細(xì)胞群體的重要細(xì)胞機(jī)制,也是胚胎發(fā)育和免疫系統(tǒng)活動(dòng)的重要組成部分。逃避凋亡的受損細(xì)胞一般都會(huì)衰老,很多環(huán)境污染物都會(huì)誘發(fā)水生生物細(xì)胞衰老。硫丹對魚類的細(xì)胞毒性依賴于細(xì)胞類型、暴露濃度、暴露方式(活體/離體)和暴露時(shí)間。
肝臟是魚類重要的代謝和解毒器官,因此常用于環(huán)境污染物的細(xì)胞毒性測試。通過含1 μg/g和0.5 μg/g的硫丹喂食暴露21d,硫丹誘導(dǎo)了尼羅羅非魚肝細(xì)胞破壞、血管內(nèi)皮細(xì)胞破裂,并增加了黑色素吞噬細(xì)胞的聚集;而低至0.1 μg/g和0.001 μg/g的劑量暴露35d,增加了肝細(xì)胞空泡化和嗜酸性粒細(xì)胞聚集[35]。頭腎是硫丹代謝過程中重要的魚類免疫器官。將鯰魚(Clariasgariepinus)暴露于2.884 μg/L的硫丹30d,隨后在不含硫丹的水中恢復(fù)30d,發(fā)現(xiàn)頭腎體細(xì)胞指數(shù)降低,并導(dǎo)致白細(xì)胞死亡[36]。此外,硫丹活體暴露可降低魚類紅細(xì)胞數(shù)量和血紅蛋白濃度,使魚處在貧血狀態(tài),同時(shí),出現(xiàn)紅細(xì)胞腫脹,影響其攜氧能力[22-23]。
魚類在細(xì)胞水平上的毒性響應(yīng)往往伴隨著組織水平上的病理學(xué)損傷,包括鰓上皮細(xì)胞增生和鰓損傷、肝水腫變性和局灶性壞死、睪丸損傷等。這些重要器官中度的病理反應(yīng)在魚類繁殖期和長時(shí)間暴露期可能變得至關(guān)重要[22]。4 μg/L的硫丹喂食暴露35 d導(dǎo)致大西洋鮭魚(Salmosalar)肝臟和腸道的組織學(xué)改變,后腸病理學(xué)特征是絨毛的空泡化和融合,而在最嚴(yán)重的情況下,絨毛尖端上皮完整性喪失;對肝臟的主要影響是糖原消耗和脂質(zhì)沉積[37]。這些變化屬于典型的普遍應(yīng)激反應(yīng)。此外,0.16 μg/L或0.48 μg/L的硫丹對成年斑馬魚肝組織損傷表現(xiàn)為肝細(xì)胞肝肥大、壞死和完整性改變[38]。0.76 μg/L的硫丹暴露下四眼魚肝臟中出現(xiàn)了可逆的組織學(xué)改變(如水腫變性和竇狀膨脹),而在1.26 μg/L和2.1 μg/L濃度下肝臟產(chǎn)生了不可逆轉(zhuǎn)的變化,如肝臟壞死[16]。
鰓與水環(huán)境直接接觸,因此對污染物非常敏感。研究發(fā)現(xiàn),18.5 μg/L的硫丹暴露96 h引起遮目魚(Chanoschanos)鰓上繼發(fā)性片段的卷曲、原發(fā)性上皮的增厚、上皮增生、次級(jí)層融合等;較高濃度(21.5 μg/L)下肝細(xì)胞出現(xiàn)嚴(yán)重壞死[27]??梢?,魚肝臟、腸、鰓等都是硫丹毒性作用的靶器官,而且組織病理學(xué)損傷程度存在明顯的濃度依賴性。
亞致死濃度的硫丹除了在個(gè)體、組織和細(xì)胞水平上對魚類產(chǎn)生毒性效應(yīng)以外,在分子水平上也會(huì)產(chǎn)生不利影響,包括代謝轉(zhuǎn)化、抗氧化防御、激素調(diào)節(jié)、神經(jīng)傳遞等生物過程的脅迫響應(yīng)。表3總結(jié)了硫丹對不同魚類生理生化指標(biāo)的影響。
表3 硫丹暴露下魚類生理生化指標(biāo)的響應(yīng)
有研究表明,硫丹對鯽魚、南美慈鯛魚、四眼魚、遮目魚、羅非魚等抗氧化防御系統(tǒng)都產(chǎn)生了干擾效應(yīng)。抗氧化防御系統(tǒng)常用的生物標(biāo)志物包括超氧化物歧化酶(SOD)、過氧化氫酶(CAT)、谷胱甘肽還原酶(GR)活性和還原型谷胱甘肽(GSH)、硫代巴比妥酸反應(yīng)物質(zhì)(TBARS)、脂質(zhì)過氧化(LPO)含量等。SOD和CAT是敏感的抗氧化酶,不同魚類對硫丹暴露的脅迫響應(yīng)不一致,多數(shù)為誘導(dǎo)效應(yīng),也有抑制效應(yīng),表現(xiàn)出不同的響應(yīng)機(jī)制。硫丹通過釋放氧自由基誘導(dǎo)組織的氧化損傷[46],SOD和CAT的活性升高有助于清除氧自由基,保護(hù)魚體組織免受氧化損傷。但是,強(qiáng)氧化劑能夠克服生物的抗氧化防御系統(tǒng),產(chǎn)生過量的H2O2損傷酶的活性位點(diǎn),從而抑制SOD的催化活性[47-48]。從表3可見,硫丹增加了不同魚類的TBARS和LPO水平,這是由于生成的活性氧(ROS)攻擊細(xì)胞膜產(chǎn)生了抗氧化酶損傷,繼而對細(xì)胞完整性和細(xì)胞功能產(chǎn)生影響。
細(xì)胞色素P450 1A(CYP1A)表達(dá)及其相關(guān)乙氧異吩惡唑酮—O—脫乙基酶(EROD)活性通常用來反映有機(jī)污染物Ⅰ相生物轉(zhuǎn)化途徑,谷胱甘肽—S—轉(zhuǎn)移酶(GST)活性反映Ⅱ相生物轉(zhuǎn)化和解毒途徑。表3的結(jié)果顯示,通過不同方式暴露的硫丹誘導(dǎo)了不同魚類的CYP1A表達(dá)及EROD和GST活性。來自不同實(shí)驗(yàn)室的研究得到了一致的結(jié)果,表明進(jìn)入魚體內(nèi)的硫丹可以進(jìn)行代謝轉(zhuǎn)化和解毒。不同濃度的硫丹暴露增加了遮目魚肝、鰓和腦的乳酸脫氫酶(LDH)和蘋果酸脫氫酶(MDH)的活性,表明魚體為維持自身能量需求應(yīng)激誘導(dǎo)了無氧代謝[27]。天冬氨酸轉(zhuǎn)氨酶(ALT)和丙氨酸氨基轉(zhuǎn)氨酶(AST)是相關(guān)的應(yīng)激指標(biāo),通常用于診斷魚類疾病和檢測由環(huán)境污染引起的組織損傷,ALT和AST活性增加表明通過魚糖異生反應(yīng)促進(jìn)天冬氨酸和丙氨酸產(chǎn)轉(zhuǎn)化成葡萄糖以承受污染物的脅迫作用[49]。此外,研究發(fā)現(xiàn)雄性和雌性斑馬魚之間存在基于性別的硫丹解毒差異[39]。
乙酰膽堿酯酶(AChE)是生物神經(jīng)傳導(dǎo)中的一種關(guān)鍵酶,對魚類正常行為和肌肉功能至關(guān)重要。水體暴露的硫丹顯著降低了不同魚類AChE的活性,最大抑制率達(dá)到79%[26]。AChE的抑制率達(dá)到40%就會(huì)導(dǎo)致魚的行為異常,包括游泳活力降低、探索能力下降,影響逃避和捕食行為,并且可能破壞它們的生態(tài)和種間相互作用[40-42,50]。
現(xiàn)有研究表明,μg/L級(jí)的硫丹通過急性、亞急性或者亞慢性暴露,都對魚類正常的生理功能產(chǎn)生了干擾效應(yīng)。通過實(shí)驗(yàn)室暴露研究,篩選出敏感的魚類分子生物學(xué)指標(biāo),對自然水體中硫丹的生態(tài)風(fēng)險(xiǎn)評(píng)估具有重要意義。
體內(nèi)和體外實(shí)驗(yàn)都已證明硫丹具有致突變和致畸效應(yīng),以前的研究主要以哺乳動(dòng)物為模式生物,對水生生物的研究相對較少。DNA損傷、微核形成和染色體畸變在評(píng)估農(nóng)藥誘導(dǎo)的魚類遺傳毒性方面發(fā)揮了重要作用。
不同質(zhì)量濃度(1.25、2.50、3.75、5.00、6.25 μg/L)硫丹暴露4 d導(dǎo)致葛氏鱸塘鱧外周血紅細(xì)胞核異常率升高,并呈現(xiàn)較明顯的劑量—效應(yīng)關(guān)系,表明硫丹對葛氏鱸塘鱧具有潛在的遺傳毒性[51]。Pandey等[19]采用彗星試驗(yàn)方法研究了硫丹對淡水硬骨魚翠鱧的遺傳毒性,4.0 μg/L的硫丹暴露4 d后,在魚鰓和腎組織細(xì)胞觀察到了明顯的DNA損傷,而且鰓細(xì)胞對硫丹暴露比腎細(xì)胞更敏感。
即使在環(huán)境相關(guān)濃度暴露下,硫丹對一些敏感魚類也會(huì)產(chǎn)生遺傳毒性。硫丹在0.5 μg/L 或者1.0 μg/L質(zhì)量濃度下暴露4 d對金頭鯛(SparusaurataL.)產(chǎn)生了明顯的染色體損傷[52]。0.02 μg/L的硫丹暴露24 h增加了南美慈鯛紅細(xì)胞的核異常率,5 μg/L增加了微核形成率[49]。魚的微核形成率、核異常率和染色體畸變率的增加常伴隨著氧化脅迫效應(yīng)的增強(qiáng)和抗氧化酶的干擾,因此,Dar等[21]推測硫丹的遺傳毒性機(jī)制可能為氧化應(yīng)激路徑。
考慮到很多地表水環(huán)境中硫丹的賦存濃度高達(dá)μg/L級(jí),長期暴露可能會(huì)通過影響個(gè)體生長發(fā)育、流動(dòng)性、覓食成功率、繁殖能力,進(jìn)而對魚類種群健康產(chǎn)生嚴(yán)重影響。
0.5 μg/L和1 μg/L的硫丹暴露30 d,顯著干擾了雄性華生小鯉(Cyprinionwatsoni)的睪酮水平,并對生殖健康產(chǎn)生了負(fù)面影響[53]。將日本青鳉(Oryziaslatipes)的受精卵暴露于0.01 μg/L、0.10 μg/L和1 μg/L的硫丹24 h,導(dǎo)致孵化時(shí)間更長,而且孵出的魚苗個(gè)體較小,活動(dòng)性降低;當(dāng)這些魚達(dá)到性成熟時(shí),產(chǎn)卵量減少,孵化時(shí)間延長[54]??梢?,短期暴露于環(huán)境相關(guān)濃度的殺蟲劑可能會(huì)對魚類的發(fā)育和繁殖產(chǎn)生長期影響。然而,Beyger等[55]將孵化78 d后的旗魚(Jordanellafloridae)脈沖暴露于硫丹4 h,監(jiān)測魚的生長和繁殖,結(jié)果表明,濃度高達(dá)10.8 μg/L的硫丹都沒有顯著影響旗魚的生長和繁殖能力。這一結(jié)果可能與暴露方式有關(guān),該研究采用高濃度硫丹急性脈沖暴露4 h,然后將魚轉(zhuǎn)入清水,吸收進(jìn)入魚體中的硫丹可能逐漸被代謝、清除,從而恢復(fù)了正常的生理功能。
將成年斑馬魚暴露于硫丹28 d,發(fā)現(xiàn)0.16 μg/L暴露組斑馬魚生產(chǎn)的幼魚心跳頻率明顯低于對照組,并出現(xiàn)嚴(yán)重的脊柱前凸、腹水等形態(tài)學(xué)變化(圖1)[38]??梢姡趤喼滤罎舛认?,成年斑馬魚即使能夠成功繁殖,但是后代發(fā)育異??赡苡绊懰鼈兊拈L期存活。因此,在硫丹的環(huán)境風(fēng)險(xiǎn)評(píng)估中應(yīng)考慮其對魚類的代際危害。
硫丹對生殖系統(tǒng)的影響主要是通過激素作用介導(dǎo),而不是直接毒性作用[56]。性激素在低等脊椎動(dòng)物(包括魚類)的性別分化中起重要作用。因此,由內(nèi)分泌干擾物引起的性激素水平略有變化,對水生脊椎動(dòng)物的性腺發(fā)育就會(huì)產(chǎn)生明顯的影響。硫丹通過與雌二醇競爭與雌激素受體(ER)結(jié)合,從而誘導(dǎo)雌激素響應(yīng)[57]。但是硫丹與ER結(jié)合的親和力低,其雌激素活性比雌二醇低105~106倍[58]。活體試驗(yàn)表明,硫丹通過觸發(fā)雌魚早熟發(fā)育,加快其卵巢生長[59-60]。硫丹還是一種弱的抗雄激素,可以通過調(diào)節(jié)睪丸相關(guān)轉(zhuǎn)錄因子和類固醇生成酶的轉(zhuǎn)錄表達(dá),使雄魚睪丸分化或發(fā)育受損[56,61]。這些研究證實(shí)了硫丹對魚生殖軸的內(nèi)分泌干擾作用,而性腺的組織病理學(xué)變化、卵黃蛋白原水平變化和兩性異形可對魚類繁殖產(chǎn)生嚴(yán)重影響[62]。
(a) 對照組與0.16 μg/L暴露組
(b) 0.48 μg/L暴露組
注:(a)圖箭頭指向?yàn)閷φ战M,下方為0.16 μg/L暴露組,顯示了嚴(yán)重的脊柱前凸;(b) 圖為0.48 μg/L暴露組,顯示了嚴(yán)重腹水。
圖1斑馬魚親魚暴露硫丹28d導(dǎo)致仔魚發(fā)育異常[38]
硫丹作為新列入POPs清單的有機(jī)氯殺蟲劑,目前仍有很多國家在生產(chǎn)和使用。硫丹具有長距離遷移能力和環(huán)境持久性,今后相當(dāng)長的時(shí)間內(nèi)都是重要的環(huán)境污染物,其在一些地區(qū)的環(huán)境殘留可能繼續(xù)升高。目前,發(fā)達(dá)國家對水產(chǎn)品農(nóng)藥殘留的限量要求日益嚴(yán)格,這已對我國魚類產(chǎn)品出口產(chǎn)生了巨大影響,因此,我國亟須完善水產(chǎn)品藥物殘留限量標(biāo)準(zhǔn)體系,針對硫丹等新POPs制定嚴(yán)格的限量標(biāo)準(zhǔn),同時(shí)在漁業(yè)水質(zhì)標(biāo)準(zhǔn)中增設(shè)相應(yīng)指標(biāo)。此外,還需要在源頭上加強(qiáng)對硫丹使用的管控。
目前,有關(guān)硫丹對魚類的毒理學(xué)研究取得了一些進(jìn)展,尤其在急性毒性方面,積累了豐富的數(shù)據(jù)?,F(xiàn)有研究成果也證實(shí)了亞致死濃度下硫丹對魚類具有細(xì)胞毒性、遺傳毒性和組織損傷,長期暴露對親代繁殖能力和子代生長發(fā)育產(chǎn)生不利影響。鑒于在真實(shí)水環(huán)境中硫丹通常與其他殺蟲劑共存,因此,研究硫丹與其他污染物共暴露對魚類的聯(lián)合毒性,探明是否存在協(xié)同效應(yīng),將有助于客觀評(píng)價(jià)硫丹污染水體的生態(tài)風(fēng)險(xiǎn)。另外,在魚類毒性作用機(jī)制方面,目前提出了細(xì)胞和分子機(jī)制,包括線粒體功能障礙、誘導(dǎo)氧化應(yīng)激、應(yīng)激反應(yīng)信號(hào)轉(zhuǎn)導(dǎo)途徑的調(diào)節(jié)、增加細(xì)胞外信號(hào)調(diào)節(jié)激酶等,但是確定硫丹對魚類的毒性機(jī)制需要更多實(shí)驗(yàn)證據(jù)。硫丹將長期在水環(huán)境中殘留,因此需要加強(qiáng)魚類全生命周期暴露、子代傳遞效應(yīng)、多代繁殖影響等方面的研究,揭示水環(huán)境中硫丹持續(xù)暴露對魚類種群健康的影響。
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