四川动物  2019, Vol. 38 Issue (2): 206-213, 219

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李惠鑫, 刘刚, 卢康宁, 张玲, 朱奇, 刘芳菁, 文菀玉, 龚明昊
LI Huixin, LIU Gang, LU Kangning, ZHANG Ling, ZHU Qi, LIU Fangjing, WEN Wanyu, GONG Minghao
鄱阳湖北段白鹭和苍鹭重金属富集特征比较
Heavy Metal Bioaccumulation in Egretta garzetta and Ardea cinerea in the North Area of Poyang Lake
四川动物, 2019, 38(2): 206-213, 219
Sichuan Journal of Zoology, 2019, 38(2): 206-213, 219
10.11984/j.issn.1000-7083.20180265

文章历史

收稿日期: 2018-09-06
接受日期: 2019-01-11
鄱阳湖北段白鹭和苍鹭重金属富集特征比较
李惠鑫1,2 , 刘刚1,2 , 卢康宁3 , 张玲4 , 朱奇5 , 刘芳菁5 , 文菀玉1,2 , 龚明昊1,2*     
1. 中国林业科学研究院湿地研究所, 北京 100091
2. 湿地生态功能与恢复北京市重点实验室, 北京 100091
3. 国家林业与草原局生态定位观测网络中心, 北京 100091
4. 中国野生动物保护协会, 北京 100714
5. 江西鄱阳湖国家级自然保护区管理局, 南昌 330038
摘要:水鸟对重金属的富集水平及特征是了解湿地生态系统健康状况、水鸟生境安全的重要渠道。2016年通过非损伤取样方式采集了鄱阳湖北段白鹭Egretta garzetta和苍鹭Ardea cinerea各20个卵壳样品,并收集了2种鹭鸟觅食地的土壤样品9份,利用电感耦合等离子体质谱仪对卵壳和土样中铬(Cr)、铜(Cu)、镍(Ni)、锌(Zn)、砷(As)、铅(Pb)、镉(Cd)、汞(Hg)8种重金属的残留量进行了测量,分析了重金属在2种鹭鸟卵壳中的残留量,在此基础上分析了该区域2种鹭鸟对土壤重金属富集特征。研究结果表明,8种重金属中,白鹭和苍鹭卵壳重金属残留量均以Zn最高、Cd最低。苍鹭的Pb残留量极显著高于白鹭(P < 0.01)。白鹭和苍鹭卵壳对Hg的生物富集系数最高,As的最低,而苍鹭对Pb的生物富集系数极显著高于白鹭(P < 0.01)。
关键词白鹭     苍鹭     重金属污染     生物富集系数     鄱阳湖    
Heavy Metal Bioaccumulation in Egretta garzetta and Ardea cinerea in the North Area of Poyang Lake
LI Huixin1,2 , LIU Gang1,2 , LU Kangning3 , ZHANG Ling4 , ZHU Qi5 , LIU Fangjing5 , WEN Wanyu1,2 , GONG Minghao1,2*     
1. Institute of Wetland Research, Chinese Academy of Forestry, Beijing 100091, China;
2. Beijing Key Laboratory of Wetland Services and Restoration, Beijing 100091, China;
3. Office of China Terrestrial Ecosystem Research Network, National Forestry and Grassland Administration, Beijing 100091, China;
4. China Wildlife Conservation Association, Beijing 100714, China;
5. Jiangxi Poyang Lake National Nature Reserve Administration, Nanchang 330038, China
Abstract: The heavy metal bioaccumulation levels and characteristics of waterfowls are important to understanding the physical condition of wetland ecosystem and habitat security of waterfowls. In this research, by using non-invasively sampling method, we collected the eggshells of little egrets (Egretta garzetta) and grey herons (Ardea cinerea) and the soil samples of their foraging habitats in Da Zizui village of Duchang county, which located in the north area of Poyang Lake in 2016. Inductively Coupled Plasma Mass Spectrometry was used to analyze the abundances of residual 8 types of heavy metals (Cr, Cu, Ni, Zn, As, Pb, Cd, and Hg) in E. garzetta and A. cinerea, and the bioaccumulation profiles of 8 metals in the foraging habitat soils. The results showed that Zn had the highest concentration in the eggshells of the 2 species, while Cd had the lowest. Among these metals, only Pb was extremely significantly enriched in A. cinerea compared with that in E. garzetta (P < 0.01). In terms of bioaccumulation profiles, Hg was the highest in the eggshells of E. garzetta and A. cinerea, while As was the lowest. Comparison of heavy metal bioaccumulation between E. garzetta and A. cinerea showed that the bioaccumulation of Pb was significantly higher in A. cinerea (P < 0.01).
Keywords: Egretta garzetta     Ardea cinerea     heavy metal pollution     bioaccumulation factor     Poyang Lake    

湿地生态系统处于水陆交错的生态脆弱区域,易受到自然与人为因素干扰(崔丽娟,张曼胤,2006)。由于人类活动,湿地生态系统受到大量的、多种类污染物的污染,这些污染物会对水鸟的栖息地生态健康产生较大的影响(Liu et al., 2015)。重金属是一类持续时间长、难降解、毒性大、可通过食物链传递和富集的污染物,以自然和人类活动的方式进入湿地生态系统(Matagi,1998Burger et al., 2007权轻舟,2017)。

重金属以生物体直接吸入、食物摄取、皮肤接触等方式进入湿地食物链,沿着食物链进行传递和放大,在各级动物组织器官富集,对高营养级的物种危害更大(Wiener et al., 2003Shahbaz et al., 2013)。具有长生命周期的水鸟是湿地食物链的顶级捕食者,其蛋白质和脂质代谢易受重金属的影响,是理想的湿地生态系统重金属污染指示物(Furness,1993王强,吕宪国,2007;Koivula et al., 2010)。重金属对水鸟的生长发育和繁殖成功率等方面有影响(Donald et al., 1981Di & Scanlon,1985Drent & Woldendorp,1989Bize et al., 2002),因此,有必要对水鸟进行重金属浓度监测,避免因出生率降低和死亡率升高而导致种群数量减少。

鹭科Ardeidae水鸟对重金属污染极为敏感,是良好的湿地重金属污染监测指示物种(Burger & Gochfeld, 2004, 2007;周立志等,2005Lucia et al., 2010陈小麟,2011Zhang & Ma,2011Luo et al., 2015)。研究者利用鹭科鸟类组织和器官,如肝脏、肾脏、血液、肌肉、骨骼、羽毛以及卵等进行重金属富集的相关研究(董元华等,2002纪伟涛等,2006Zhang et al., 2006刘利等,2017)。在卵的形成过程中,雌鸟将体内污染物分泌到卵壳中,因此可通过监测卵壳重金属浓度来了解鸟类所暴露环境的状况(Connell et al., 2002Lam et al., 2004Kitowski et al., 2014Kim & Oh,2015)。卵壳是水鸟到达繁殖地后一段时间形成的,可以替代水鸟用作监测繁殖地环境重金属污染的生物指示物(Ayaş,2007)。此外,卵壳可通过非损伤取样方式获得,是评估鸟类体内重金属浓度的理想样品(林琳,陈小麟,2005Abdullah et al., 2015Luo et al., 2015)。

鄱阳湖是我国水域面积最大的淡水湖,是亚洲最大的水鸟越冬地,每年冬季有数十万只水鸟到此越冬(纪伟涛等,2006朱奇等,2012)。环鄱阳湖经济区发展迅速,重金属污染严重且已影响到栖息于此的候鸟种群健康(简敏菲等,2004夏秋烨等,2014)。鹭科鸟类是鄱阳湖湿地的优势种群,分布广泛且具有代表性。本文对鄱阳湖白鹭Egretta garzetta和苍鹭Ardea cinerea的卵壳进行重金属残留量检测分析,旨在(1)获得鄱阳湖北段地区白鹭和苍鹭8种重金属(Cr、Cu、Ni、Zn、As、Pb、Cd、Hg)的残留量;(2)发现2种鹭鸟卵壳和觅食地土壤样品中8种重金属富集的特征;(3)评价2种鹭鸟在鄱阳湖北段地区的生境生态环境质量状况。

1 研究区域概况

鄱阳湖国家级自然保护区(115°55′~116°03′E,29°05′~29°15′N)位于鄱阳湖的西北角,总面积22 400 hm2。保护区内湿地生态系统结构完整,生物资源丰富,现已统计到330种鸟类,其中,国家Ⅰ级重点保护野生鸟类9种,国家Ⅱ级重点保护野生鸟类47种(曾南京等,2016)。保护区属于亚热带湿润季风型气候,热量丰富,雨量充沛,无霜期长,四季分明,年均气温17.1 ℃,最低气温-9.8 ℃,最高气温40.2 ℃,年平均降水量1 426.4 mm。达子咀村地处保护区北端(图 1),都昌县的西北部,与湖口县屏峰乡交界,被处于鄱阳湖与长江的连接处,实现南连五河、北通长江功能的谢家湖围绕,因此谢家湖及周边水域具有承接环鄱阳湖经济体排放的工业、农业及生活废水,净化湖水的作用。谢家湖岸边的杉木Cunninghamia lanceolata林是多种鹭鸟的主要筑巢地,而谢家湖是其主要的觅食地。2016年3月初,鹭鸟陆续在湖边的杉木林中筑巢,2016年5—6月调查结果显示,白鹭约2 000巢,每巢2~5枚卵,苍鹭约500巢,每巢不少于2枚卵。

图 1 鄱阳湖北段的研究区域 Fig. 1 Study area in the north area of Poyang Lake
2 采样与方法 2.1 样品采集

2016年5月13日在达子咀村从白鹭和苍鹭混居筑巢的杉木林内随机捡拾掉落地面的卵壳各20个,所有卵壳碎片均单独保存于自封袋内,按顺序编号并标明卵壳碎片的种类,常温保存。白鹭和苍鹭主要在距离筑巢地不远的水面(湖和人工鱼塘)觅食,调查期间共观察到3个觅食点,分别在3个觅食地点随机布置3个样点,每个样点采集1份土壤样品,共9份。

2.2 样品处理

卵壳碎片表面用双蒸水清洗干净,再用超纯水和丙酮反复浸泡清洗3次,壳膜与壳不分离,放入烘箱内烘至恒重。土壤样品放置阴凉处风干,用玛瑙研钵磨碎,过200目筛。称取卵壳碎片样品0.3 g于微波消解管内,加入混酸5 mL(HNO3: HCl=4: 1)(Mos级,北京化学试剂研究所)微波消解,蒸馏水定容至50 mL。称量土壤样品0.3 g于微波消解管内,加入混酸8 mL(HNO3: HCl=3: 1)(Mos级,北京化学试剂研究所)微波消解,蒸馏水定容至50 mL。所有样品使用电感耦合等离子体质谱仪(ICP-MS)测量Cr、Ni、Cu、Zn、Pb、Hg、Cd、As含量,设置10个空白样本对照。

2.3 样品分析

在干重状态下所有重金属浓度使用计量单位为μg·g-1。浓度低于测量底线的表示为“未测量到(ND)”,做0处理。

重金属的生物富集系数(bioaccumulation factors,BAF)利用BAF=C卵壳/C土壤×100%(Arnot & Gobas,2006)计算,式中,C卵壳指白鹭或苍鹭卵壳样品的重金属残留量(μg·g-1),C土壤指土壤样品的重金属残留量(μg·g-1)。

数据采用SPSS 19.0进行统计分析。符合正态分布的数据,样本间的显著性检验采用独立样本t检验;不符合正态分布的数据,样本间的显著性检验采用Mann-Whitney U检验。

3 研究结果 3.1 白鹭和苍鹭卵壳重金属残留的差异分析

白鹭和苍鹭卵壳重金属残留量均以Zn最高,分别为4.07 μg·g-1±1.32 μg·g-1和4.81 μg·g-1±1.00 μg·g-1,而Cd最低,分别为0.01 μg·g-1±0.01 μg·g-1和0.02 μg·g-1±0.01 μg·g-1(表 1)。8种重金属残留量从高到低为,白鹭:Zn>Cu>Cr>Ni>Pb>Hg≥As>Cd,苍鹭:Zn>Cu>Cr>Pb>Ni>Hg≥As>Cd。白鹭与苍鹭Cr、Ni、Cu、Zn、As、Cd、Hg浓度之间的差异无统计学意义(P>0.05),但Pb的差异有高度统计学意义(P<0.01)。

表 1 鄱阳湖北段白鹭和苍鹭卵壳重金属残留量 Table 1 Heavy metal residues in the eggshells of Egretta garzetta and Ardea cinerea in the north area of Poyang Lake
重金属
Heavy metal
卵壳重金属残留量Heavy metal residue in the eggshells(范围Range)/μg·g-1 P
P-value
白鹭Egretta garzetta(n=20) 苍鹭Ardea cinerea(n=20)
Cr 0.87±0.35(0.31~1.38) 1.16±0.43(0.62~2.04) 0.571
Ni 0.37±0.14(0.14~0.58) 0.38±0.16(0.21~0.77) 0.617
Cu 1.65±0.61(0.52~2.38) 1.70±0.44(0.89~2.40) 0.192
Zn 4.07±1.32(1.84~6.47) 4.81±1.00(3.13~7.18) 0.077
As 0.03±0.02(ND~0.06) 0.03±0.02(ND~0.06) 0.764
Cd 0.01±0.01(ND~0.05) 0.02±0.01(ND~0.06) 0.082
Hg 0.03±0.02(0.01~0.08) 0.03±0.02(0.01~0.06) 0.330
Pb 0.15±0.06(0.07~0.27) 0.53±0.17(0.26~0.87) <0.01
注Note:ND.未检出not detected
3.2 白鹭和苍鹭觅食地土壤重金属

觅食地土壤所含重金属平均浓度以Zn最高,Hg最低,分别为22.85 μg·g-1、0.02 μg·g-1(表 2),所有样品的重金属元素含量符合《国家土壤环境质量标准(GB 15618-1995)》(国家环境环保局,国家技术监督局,1995)Ⅰ类土壤标准。8种重金属残留量从高到低为Zn>Cr>Ni>Pb>Cu>As>Cd>Hg。

表 2 鄱阳湖北段白鹭和苍鹭觅食地土壤样品重金属残留量 Table 2 Heavy metal residues in the soil samples of Egretta garzetta and Ardea cinerea's foraging sites in the north area of Poyang Lake
重金属残留量Heavy metal residue/μg·g-1
Cr Ni Cu Zn As Cd Hg Pb
样品量 9 9 9 9 9 9 9 9
均值 13.41 9.23 8.36 22.85 5.62 0.14 0.02 8.65
国标 Ⅰ(<90) Ⅰ(<40) Ⅰ(<35) Ⅰ(<100) Ⅰ(<15) Ⅰ(<0.20) Ⅰ(<0.15) Ⅰ(<35)
3.3 白鹭和苍鹭对8种土壤重金属的生物富集系数

白鹭和苍鹭对土壤重金属的生物富集系数为0.4%~168.9%,其中,As的生物富集系数最低(苍鹭、白鹭均为0.4%),生物富集系数<1,不构成富集(表 3)。Hg的生物富集系数最高(白鹭:168.9%,苍鹭:159.9%)。苍鹭对Pb的生物富集系数为6.2%,白鹭的为1.7%,苍鹭极显著高于白鹭(P<0.01)。其余7种重金属的生物富集系数之间的差异无统计学意义。

表 3 鄱阳湖北段白鹭和苍鹭对土壤重金属生物富集系数 Table 3 Bioaccumulation factors of 8 heavy metals in Egretta garzetta and Ardea cinerea in the north area of Poyang Lake
物种
Species
生物富集系数Bioaccumulation factor/%
Cr Ni Cu Zn As Cd Hg Pb
白鹭 6.5 3.6 19.7 13.0 0.4 4.8 168.9 1.7
苍鹭 9.0 3.5 19.8 18.8 0.4 10.4 159.9 6.2
差异性 NS NS NS NS NS NS NS P<0.01
注Note:NS.差异无统计学意义there is no significant difference
4 讨论 4.1 种间差异

Pb主要沉积在富含钙质的组织,如骨骼和卵壳;卵壳也被认为是雌性鸟类排泄Pb的一个途径(Sorensen,1991Burger,1994)。鹭鸟的相关研究发现卵壳Pb含量极显著高于卵内容物,更适于反映其体内Pb的残留量(周立志等,2006林琳,2007刘利等,2017)。在本研究中,苍鹭卵壳Pb的残留量极显著高于白鹭,意味着苍鹭体内Pb的残余水平极显著高于白鹭;苍鹭卵壳Pb的生物富集系数极显著高于白鹭,这一结果与2种鹭鸟的卵壳重金属残留量一致。此外,苍鹭卵壳中Cr、Cu、Zn和Cd的残留量、重金属生物富集系数均略高于白鹭。本研究中苍鹭和白鹭暴露于相同的重金属环境中,其重金属残留量的差异可能是由物种、食物链结构等因素导致的。有研究表明,鸟类富集的重金属受饮食模式和食物类型、身体条件和年龄、产卵时间、种间新陈代谢、酶的解毒机制的影响(Kojadinovic et al., 2007Shin,2009Hashmi et al., 2013Kim & Oh,2014)。对于集群营巢的苍鹭和白鹭,在系统分类上相近,但在竞争等种间关系影响下,它们在取食生态位上和食物链结构上有明显的差异(郝宇奇等,2015)。苍鹭倾向于捕食深水中个体较大的鱼,而个体大的鱼类比个体小的重金属浓度高,因此苍鹭富集了更多的重金属(Fasola,1986Burger & Gochfeld,2009Naccari et al., 2009Shahbaz et al., 2013Jackson et al., 2017)。此外,苍鹭的消化系统效率高,能消化大部分的骨骼、鳞片和卵(Jakubas & Mioduszewska,2005)。基于上述原因,苍鹭卵壳中Pb、Cr、Zn和Cd的残留量及对土壤重金属的生物富集系数均高于白鹭。Pb是一种神经毒素,可以引起认知和行为异常,降低繁殖率和存活率,影响生长发育和新陈代谢(Burger,1998Provencher et al., 2016)。有必要监测鄱阳湖北段Pb的污染水平,苍鹭卵壳是有效的监测环境中Pb污染水平的生物指示物。

苍鹭和白鹭卵壳中Hg的残留量较低,但2种鹭鸟对Hg的生物富集系数均显著高于其余7种重金属。这一研究结果与其他研究相符,Hg在羽毛、卵等组织的生物富集系数较高(Boncompagni et al., 2003Zhang et al., 2006)。湿地生态系统中鹭鸟对Hg的富集主要受营养级、年龄、环境等影响(Wiener et al., 2003Covaci et al., 2006Katner et al., 2013)。Hg对水鸟的危害是长时间的、持续的和累积性的,导致一些鸟类产卵数量减少(Tartu et al., 2013Mccullagh et al., 2015);卵壳变薄,降低胚胎存活率和繁殖率(Miljeteig et al., 2012Orłowski et al., 2012Oliveroverbel et al., 2013);双亲抚育后代行为发生改变(Tartu et al., 2015);轴索变性及其他神经系统疾病;听力损伤;皮质酮、睾酮及其他激素的代谢紊乱(Jayasena et al., 2011Tartu et al., 2013Moore et al., 2014),长期的影响会改变种群结构(Scheuhammer et al., 2007Ackerman et al., 2016)。因此需密切监测Hg在湿地生态系统中的污染状况。

4.2 与其他区域研究比较

与国内外其他研究进行比较,本区域2种鹭鸟卵壳的重金属残留量只有Cr水平略高,其他7种水平均较低。如波兰东南部和东部苍鹭繁殖区采集到的苍鹭卵壳Cr的残留量分别为1.07 μg·g-1和0.78 μg·g-1(Kitowski et al., 2013, 2014)、巴基斯坦牛背鹭Bubulcus ibis和小白鹭的分别为0.35~0.80 μg·g-1和0.7 μg·g-1(Hashmi et al., 2013)、日本的短尾信天翁Phoebastria albatrus和黑脚信天翁Phoebastria nigripes的分别为0.07 μg·g-1和0.084 μg·g-1(Ikemoto et al., 2005)、阿根廷美洲蛎鹬Haematopus palliatus的为0.78 μg·g-1 (Simonetti et al., 2015)、香港夜鹭Nycticorax nycticorax和牛背鹭的分别为0.15~0.13 μg·g-1和0.09~0.70 μg·g-1(Lam et al., 2004)、厦门黄嘴白鹭Egretta eulophotes的为0.490~0.868 μg·g-1(王晓彦等,2009)。Cr是动物必需营养元素,起到调节胰岛素、激活某些酶、稳定蛋白质和核酸的作用;但浓度过高时,Cr会对生物产生诱变、致癌和致畸作用(ŞAhiN et al., 2009),需要对本研究区域Cr的排放源、环境中Cr的含量和苍鹭体内Cr的残留水平进行监测。鄱阳湖北段白鹭和苍鹭的觅食地土样的8种重金属浓度均符合《国家土壤环境质量标准(GB 15618-1995)》(国家环境环保局,国家技术监督局,1995)Ⅰ类土壤标准,而且2种鹭鸟卵壳内8种重金属残留水平较低,鹭鸟在本区域的生境状况良好。

表 4 与其他文献中卵壳重金属残留量比较 Table 4 Comparison of the mean residual heavy metal levels in the eggshells with other literatures
来源
Resource
研究区域
Study area
物种
Species
重金属残留量Heavy metal residue/μg·g-1
Cr Ni Cu Zn As Cd Hg Pb
本研究 鄱阳湖北段 白鹭 0.87 0.37 1.65 4.07 0.03 0.01 0.03 0.15
苍鹭 1.16 0.38 1.70 4.81 0.03 0.02 0.03 0.53
Hashmi等(2013) 巴基斯坦 牛背鹭 0.35~0.80 0.03~0.11 0.06~0.29 2.35~20.27 0.37~1.23 0.13~5.40
小白鹭 0.70 0.13~0.19 0.12~0.29 2.10~2.35 0.75~1.02 1.09~1.90
Kitowski等(2013) 波兰东南部 苍鹭 1.07 0.66 2.16 8.26 0.80 0.06 0.39
Kitowski等(2014) 波兰东部 苍鹭 0.78 0.53 2.04 12.10 0.94 0.06 0.47
Ikemoto等(2005) 日本 短尾信天翁 0.07 0.766 5.61
黑脚信天翁 0.084 0.784 3.39
Simonetti等(2015) 阿根廷 美洲蛎鹬 0.78 6.05 2.02 2.22 13.28 7.23
Lam等(2004) 香港 夜鹭 0.05~0.13 0.78~1.83 0.76~12.40 0.02~0.05
牛背鹭 0.95~2.85 0.09~0.70 0.83~33.08 0.04~0.56
王晓彦等(2009) 厦门 黄嘴白鹭 0.868 4.575 2.739 4.143 0.231 3.650
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