我国部分地区大气污染严重,已对人类健康和生态系统安全造成负面影响（Peng et al. 2019）。我国大气元素沉降监测以仪器监测法（instrumental methods）为主（Lü et al. 2019）,费用昂贵、操作繁琐、技术水平要求高、监测样点和监测项目数量有限、难以在偏远地区实施。地衣是真菌与蓝细菌或绿藻构成的共生体,在营养上依赖大气沉降,对大气沉降物质具有高度的通透性和持留能力,其元素含量特别是重金属含量与大气沉降量之间具有密切的正相关关系（Paoli et al. 2018）,在大气元素沉降监测中已经得到应用（Brunialti & Frati 2014;Conti et al. 2020;Abas 2021）。
地衣原位监测法（in situ lichen biomonitoring method）基于本地地衣元素含量的时空变异,探索大气元素沉降的水平、传输与源汇关系（Abas 2021）。地衣的广泛分布使原位监测法适用于大尺度空间上的大气元素沉降监测（Abas 2021）,该方法已在我国内蒙古半干旱地区（Liu et al. 2016a,2017;Wu et al. 2020）和太行山区（Liu et al. 2016b;贾晟菊等 2018）应用。
应用地衣原位监测法需考虑地衣物种和个体对地衣元素含量的影响。地衣的元素积累能力具有物种间差异（Balabanova et al. 2012;Liu et al. 2016a,2017;贾晟菊等 2018;Zhao et al. 2019;Wu et al. 2020）,为降低这种影响,常使用同种地衣为监测生物;否则,需摸清不同物种间的元素含量比例关系以进行种间校正。同种地衣的不同个体因地衣年龄、大小、形态学/生理学和微气候条件的不同而具有元素含量差异（Godinho et al. 2009;Adams & Gottardo 2012;Dołęgowska et al. 2021;Gao et al. 2021）。为降低个体间差异的影响,常在同一样点使用由多个个体构成的1个混合样品来代表地衣元素积累的平均水平。在欧洲大陆大气元素沉降的藓类原位法监测中,Frontasyeva & Harmens（2014）建议在每个监测点选取1个50×50m2样方,自该样方内采集5-10个藓类子样品构成1个混合样品;这种采样原则在地衣原位监测法中应用广泛（Barre et al. 2015;Hanedar 2015; Kurnaz & Cobanoglu 2017;Ratier et al. 2018）。在河北太行山区的21个样点中,Liu et al.（2016b）也基于这种采样原则采集了中国石黄衣Xanthoria mandschurica (Zahlbr.) Asahina的混合样品。
但是,混合样品对地衣元素积累平均水平的代表性如何?这种代表性在元素积累能力不同的地衣物种间是否有差异?在地衣原位监测法中,由于使用多个重复会使工作量和费用大大增高,这些问题的研究较少。
在人源排放轻微、沙尘沉降严重的内蒙古多伦县（图1A）的1个偏远样点（图1B）,分布有两种石生叶状地衣 [丽石黄衣,Xanthoria elegans (Link) Th. Fr.,图1C;皮果衣Dermatocarpon miniatum (L.) W. Mann,图1D]。虽然两种地衣的元素含量差异尚不清楚,但二者形态学和生态学特征差异较大,是研究地衣元素含量的物种差异和检验混合样品的代表性的理想物种。因此,本研究采集皮果衣和丽石黄衣的5个混合样品,测试了52种元素（Li、Be、B、Na、Mg、Al、P、S、K、Ca、Sc、Ti、V、Cr、Mn、Fe、Co、Ni、Cu、Zn、Ge、As、Se、Rb、Sr、Y、Nb、Mo、Cd、Sb、Cs、Ba、La、Ce、Pr、Nd、Sm、Eu、Gd、Tb、Dy、Ho、Er、Tm、Yb、Lu、Hg、Ti、Pb、Bi、Th和U）的含量,目的是比较两种地衣的元素积累能力及其在大气元素沉降监测方面的可行性;分析地衣元素含量的样点内变异以检验混合样品的代表性。本研究是我国皮果衣属地衣金属/类金属元素含量的首次测试研究,所测试的元素数量在同类研究中也最多。
图1
图1
（A）多伦县地理位置;（B）采样时的样点周边环境,绿色阴影部分代表丘陵山区,黑色实心圆圈代表采集区的位置;（C）丽石黄衣Xanthoria elegans;（D）皮果衣Dermatocarpon miniatum
Fig. 1
(A) Location of Duolun County; (B) Surrounding environment of the sample site during sampling, green shadows denote hills, and black circle denotes sampling site; (C) Xanthoria elegans; (D) Dermatocarpon miniatum.
1 材料与方法
1.1 研究区域和采集样点
内蒙古多伦县在北京正北方向约180km处（图1A）,为典型的半干旱区农牧交错带,年均降雨量（约320mm）远低于年均蒸发量（约1 750mm）。年均气温2.1℃,最高月均气温为18.9℃（7月）,最低月均气温-17.5℃（1月）。2013年之前,过度放牧和农业操作已造成草原的退化/沙化和沙漠面积的扩大,其大气元素沉降受严重的沙尘沉降与一定程度上的工矿业和交通释放影响（Liu et al. 2017）。
采样点（42°01ʹ02″N,116°17ʹ30″E）位于多伦县城西南23km的典型草原生态系统的丘陵地带,距中国科学院植物研究所多伦恢复生态学试验示范研究站（Duolun restoration ecology experimentation and demonstration station,DREEDS）约2km（图1B）。样点周围10km内无明显工业活动,人类干扰主要为放牧和农业活动,农田中不施加农药和化肥,有点状分布的退化和沙化草地,土壤类型主要为钙质土（calcisols）。样点距最近的公路约2km,截至2013年,该公路车流量小,周边交通干线极少。
1.2 地衣采集
于2013年9月4日采样。为控制元素含量的样点内变异,在丘陵阳坡选择200×200m2的样点采样。相关研究常采用降低采样面积的方法控制样点内变异,如Ratier et al.（2018）将树生地衣的采样面积设置为200m2;Adams & Gottardo（2012）甚至建议仅在一棵树上采样。样点内植被类型主要为稀疏草地,丽石黄衣和皮果衣分布较多。丽石黄衣裂片狭细（宽常1-2mm）,以下表面贴生于阳光充足的开阔地带岩石表面（图1C）;皮果衣裂片更为宽圆（直径常10-20mm）,以下表面中部的脐固着于岩石上,周缘常游离,多见于相对阴湿的石崖或石缝间（图1D）。
在样点内随机选取10个10×10m2的样方,其中5个样方用于采集丽石黄衣,另外5个用于采集皮果衣。每个样方中采集1个混合样品,该混合样品由>15个直径2-4cm的地衣个体构成。两种地衣采自不同样方,是因为在给定大小的样方中,常仅能得到一种地衣的足量样品。采集时,将地衣体用小刀片轻轻刮下,必要时用蒸馏水稍湿润后再采集,以保证地衣体的完整性。采集的地衣置于牛皮纸袋中,密封,于阴暗处自然风干。
1.3 预处理与元素测试
在体视显微镜下清除地衣体表面附着杂物,然后于烘箱中70℃烘干地衣体72h至恒重;用球磨仪（Retsch MM400,配备碳化钨罐）将地衣样品粉碎和混匀至粉末状,过20目筛;用HNO3-H2O2微波消解系统,于聚四氟乙烯罐中消解200-300mg的混匀后样品。在河北省地质实验测试中心使用电感耦合等离子体质谱法（inductively coupled plasma mass spectrometry,ICP-MS）测试了52种元素（Li、Be、B、Na、Mg、Al、P、S、K、Ca、Sc、Ti、V、Cr、Mn、Fe、Co、Ni、Cu、Zn、Ge、As、Se、Rb、Sr、Y、Nb、Mo、Cd、Sb、Cs、Ba、La、Ce、Pr、Nd、Sm、Eu、Gd、Tb、Dy、Ho、Er、Tm、Yb、Lu、Hg、Ti、Pb、Bi、Th和U）。所用仪器为Agilent 7700X（Agilent Technologies,Tokyo,Japan）。
元素测试中使用了4种标准物质进行质量控制：由国际原子能组织机构提供的地衣标准物质IAEA-336,由中国地质科学院地球物理地球化学勘查研究所提供的国家一级标准物质GBW10015（菠菜）、GBW10052（绿茶）和GBW10014（圆白菜）。
1.4 统计分析
以变异系数（coefficient of variation,CV）表征每种元素的样点内变异,CV=SD/mean× 100%,SD（standard deviation）为标准偏差。以D/X比值量化皮果衣和丽石黄衣间的元素含量差异程度;对于每种元素,D/X= [Dermatocarpon miniatum]/[Xanthoria elegans],其中“[]”表示元素含量均值。使用独立样本t检验（independent samples t test）分析每种元素在两种地衣间的含量差异显著性。数据分析在软件SPSS 25.0（SPSS Inc.,Chicago,IL,USA）中完成。
2 结果与分析
52种元素在两种地衣中的含量平均值与变异系数见表1。变异系数最大的元素是Ca（CV：32%-37%）,其次是Tl（27%）,其他50种元素的变异系数均<21%。丽石黄衣中的元素按含量由高到低依次为：Al > Ca > Fe > K > S > P > Na > Mg > Ti > Mn > Ba > Zn > Sr > Pb > Cr > V > Rb > Cu > Ce > B > Ni > Li > La > Nd > Co > Y > As > Cs > Sc > Th > Pr > Bi > Sm > Mo > Gd > Se > Nb > Dy > Sb > Er > Tl > Be > U > Yb > Cd > Eu > Ge > Hg > Ho > Tb > Lu > Tm。皮果衣中的元素排序与丽石黄衣基本相似（图2）,二者排序位数之差为0、1、2和3的元素分别为18、17、13和4个。
表1 两种地衣的元素含量
Table 1
| Element | Dermatocarpon miniatum | Xanthoria elegans | Dermatocarpon miniatum | Xanthoria elegans | |||||
|---|---|---|---|---|---|---|---|---|---|
| Mean (μg/g) | CV (%) | Mean (μg/g) | CV (%) | Mean (μg/g) | CV (%) | Mean (μg/g) | CV (%) | ||
| Al | 13826 | 13.90 | 10281 | 20.22 | Mn | 267.5 | 18.99 | 144.7 | 14.43 |
| As | 5.095 | 19.00 | 2.851 | 14.87 | Mo | 0.866 | 9.49 | 0.776 | 17.12 |
| B | 14.95 | 17.24 | 8.193 | 13.58 | Na | 2850 | 13.88 | 1824 | 8.15 |
| Ba | 65.85 | 17.94 | 46.14 | 11.19 | Nb | 1.160 | 16.51 | 0.619 | 15.40 |
| Be | 0.430 | 14.17 | 0.262 | 17.14 | Nd | 8.323 | 16.26 | 4.509 | 16.23 |
| Bi | 1.274 | 13.97 | 0.833 | 13.80 | Ni | 13.83 | 14.67 | 7.936 | 12.65 |
| Ca | 10530 | 37.11 | 8342 | 31.86 | P | 1769 | 13.11 | 1907 | 8.07 |
| Cd | 0.464 | 14.52 | 0.248 | 18.48 | Pb | 30.87 | 12.41 | 21.16 | 16.75 |
| Ce | 16.13 | 14.00 | 9.468 | 13.96 | Pr | 2.061 | 14.67 | 1.193 | 15.63 |
| Co | 6.223 | 18.21 | 3.685 | 13.23 | Rb | 17.02 | 17.68 | 14.62 | 15.49 |
| Cr | 26.90 | 8.64 | 18.33 | 18.31 | S | 2844 | 18.27 | 3020 | 11.86 |
| Cs | 2.246 | 10.69 | 1.674 | 10.18 | Sb | 0.665 | 18.41 | 0.335 | 16.75 |
| Cu | 24.00 | 14.55 | 12.58 | 12.60 | Sc | 1.935 | 9.71 | 1.327 | 15.24 |
| Dy | 1.016 | 14.27 | 0.564 | 15.29 | Se | 0.707 | 14.82 | 0.765 | 9.66 |
| Er | 0.520 | 15.56 | 0.274 | 14.81 | Sm | 1.459 | 14.95 | 0.793 | 14.96 |
| Eu | 0.287 | 14.21 | 0.154 | 14.33 | Sr | 60.41 | 14.56 | 42.70 | 17.68 |
| Fe | 10633 | 11.16 | 7883 | 16.14 | Tb | 0.189 | 11.04 | 0.102 | 17.16 |
| Gd | 1.408 | 14.68 | 0.769 | 14.64 | Th | 2.497 | 18.12 | 1.236 | 18.08 |
| Ge | 0.262 | 18.35 | 0.143 | 17.68 | Ti | 861.8 | 10.08 | 653.5 | 15.20 |
| Hg | 0.128 | 17.72 | 0.123 | 13.98 | Tl | 0.436 | 27.39 | 0.266 | 27.08 |
| Ho | 0.197 | 14.03 | 0.105 | 15.58 | Tm | 0.0624 | 15.77 | 0.0330 | 17.80 |
| K | 6034 | 11.56 | 5517 | 8.89 | U | 0.512 | 17.54 | 0.250 | 12.51 |
| La | 9.130 | 17.42 | 4.831 | 19.06 | V | 20.72 | 13.71 | 14.66 | 14.72 |
| Li | 11.20 | 14.98 | 7.543 | 16.13 | Y | 6.315 | 16.13 | 3.182 | 16.21 |
| Lu | 0.0618 | 16.84 | 0.0332 | 15.85 | Yb | 0.453 | 11.28 | 0.248 | 16.20 |
| Mg | 2241 | 10.80 | 1545 | 15.22 | Zn | 90.87 | 14.82 | 45.30 | 19.63 |
注：标粗体元素的变异系数（CV）>27%
Note: Elements in bold face have CVs of >27%.
图2
图2
丽石黄衣和皮果衣的元素含量排序散点图 阴影部分中的实线表示元素排序在两种地衣中相同,阴影部分表示元素排序在两种地衣之间的差值≤2
Fig. 2
Scattergram of element concentration ranks in the lichen Xanthoria elegans vs. ranks in Dermatocarpon miniatum. The solid line in the shadow denotes a same rank in both lichens. The shadow indicates that the element rank difference between the two lichens is ≤2.
两种地衣的元素含量差异显著性及差异程度见图3。结果显示可将52个元素分为两类。I类元素共8种（Ca、K、Mo、P、Rb、S、Se和Hg）,其含量在两种地衣中差异不显著（独立样本t检验,P>0.05）,D/X比值为0.92-1.26。II类元素共44种,其含量在两种地衣之间差异显著（独立样本t检验,P≤0.05）,D/X比值为1.32-2.05。根据D/X比值,II类元素还可以细分为2个亚类：IIa类元素共14种（Al、Ba、Bi、Cr、Cs、Fe、Li、Na、Mg、Pb、Sc、Sr、Ti和V）,D/X比值为1.32-1.56;IIb类元素共30种,其D/X比值为1.64-2.05（均值为1.85）,即As、B、Be、Cd、Co、Cu、Ge、Mn、Nb、Ni、Sb、Th、Ti、U、Y、Zn和14种镧系元素（Lanthanides;La、Ce、Pr、Nd、Sm、Eu、Gd、Tb、Dy、Ho、Er、Tm、Yb和Lu;D/X比值为1.70-1.90,均值为1.84）。
图3
图3
元素含量的D/X比值 D/X比值表示皮果衣和丽石黄衣的含量平均值之比. 空心柱表示该元素在两种地衣之间含量差异不显著,实心柱表示该元素在两种地衣之间含量差异显著（独立样本t检验,α=0.05）
Fig. 3
D/X ratios of element concentrations. D/X ratio is calculated by dividing mean value of element concentrations in Dermatocarpon miniatum by that in Xanthoria elegans. The hollow bar denotes nonsignificant difference in element concentration between Dermatocarpon miniatum and Xanthoria elegans. The solid bar denotes significant difference in element concentration between Dermatocarpon miniatum and Xanthoria elegans (independent samples t test, α=0.05).
3 讨论
3.1 与相关研究的元素含量比较
与其他地区的地衣元素含量结果进行比较以评估研究区域的大气沉降程度,是地衣原位监测法的常用手段（Cecconi et al. 2018;Conti et al. 2020;Wu et al. 2020）。由于不同地衣物种对大气沉降元素的积累能力存在差异（Balabanova et al. 2012;Wu et al. 2020）,此类比较研究需选用同种或同属地衣以保证不同研究结果的可比性。由于气候条件也是地衣元素积累的重要影响因素（Cecconi et al. 2018）,需选取宏观气候大致相似的地区进行比较。因此,本研究选取了中国北方3个地区的石黄衣属地衣,与丽石黄衣进行了元素含量比较,比较结果见电子附件表1（electronic supplementary material,ESM Table 1）。
结果表明丽石黄衣反映了研究区域沙尘沉降较高、人源排放水平较低的大气元素沉降特征,与该地草原退化和荒漠化严重、沙尘沉降剧烈、工农业活动较弱的事实相符。采自内蒙古锡林浩特草原偏远地区的丽石黄衣中（Liu et al. 2016a）,23种元素的含量与本研究数据接近,仅Mo和Pb含量偏低（ESM Table 1）。鄂尔多斯沙地一个采煤区公路边的2种石黄衣属地衣（Xanthoria alfredii和Xanthoria ulophyllodes）的42种元素中（Wu et al. 2020）,3种典型的交通污染元素（Cd、Sb和Zn）的含量是本研究的2-4倍,5种地壳源元素（Al、Ca、Fe、Tl和Pb）是本研究的35%-65%,而其他34种元素则与本研究结果接近;此结果表明,虽然本研究样点北侧2km有公路,但交通释放对大气元素组成的贡献相对较小。大气污染严重的河北太行山区21个地点的中国石黄衣Xanthoria mandschurica的30种元素中,15种元素高于本研究的数据,特别是人源排放的金属元素如Cr（其平均值是本研究数据的11倍）、Cd（4倍）、Sb（2.4倍）、Pb（2.3倍）、Zn（2.3倍）、Mn（1.8倍）和Cu（1.7倍）,其他15种元素与本研究数据大致接近,也表明研究区域的人源排放水平较低。
3.2 元素含量的物种间差异
I类元素中,除Hg之外均为植物必需元素。除了被动积累,这些植物必需元素可通过阳离子交换被地衣选择性积累,在地衣体内转运,从而避免过量积累或亏缺（Godinho et al. 2009;Osyczka et al. 2015;Catalano et al. 2016）。植物必需元素也可通过颗粒物捕获的形式在地衣体内被动积累（Brunialti & Frati 2014）。但考虑到两种地衣的来源相同,且II类元素在皮果衣中较高,生理调节极有可能是这些必需元素在物种之间含量差异不显著的主要原因。因此,在地衣原位监测法中,对植物必需元素的解释需十分谨慎。
I类元素中,皮果衣的Ca含量是丽石黄衣的1.26倍,但Ca的物种差异不显著。两种地衣的Ca积累应受生理调节和颗粒物积累的复杂影响。研究区域的土壤类型主要为富含Ca的栗钙土,这应是地衣体内Ca的主要本地来源;但Ca的物种差异格局与土壤中的大量元素（如Al和Fe）以及镧系元素不同（图3）。因此,利用地衣监测Ca的大气沉降,对数据的解释应十分谨慎。
I类元素中,Hg含量在两种地衣中相同（D/X比值：1.04）。Hg与II类元素中的重金属元素的物种格局不同,其可能原因是,Hg的挥发性较强且以气态形式传输和沉降,而其他重金属以颗粒物形式沉降并可在地衣体内长期持续积累。气态单质Hg是可进行长途迁移的全球性污染物,占大气总Hg量的95%以上;距多伦县较近的河北和辽宁,是我国人源Hg排放量较大的省份（吴晓云等 2015）。
II类元素的含量均在皮果衣中较高,但其物种差异程度在不同元素之间差别较大,D/X比值从IIa类元素的1.32-1.56变化到IIb类元素的1.64-2.05,表明皮果衣和丽石黄衣的元素积累能力不仅具有物种差异,也具有元素差异。地衣元素积累能力的元素特异性在其他相关研究中也有发现（Cecconi et al. 2019;Zhao et al. 2019;Wu et al. 2020）。本研究中,这种元素特异性特别突出地表现在镧系元素与IIa类元素的D/X比值的差异上。镧系元素以颗粒物形式沉降,是地衣体内颗粒物地球化学过程的示踪元素（Cecconi et al. 2018）,其D/X比值相近（1.70-1.90,均值1.84;图3）且高于IIa元素,特别是高于颗粒物中的大量元素Al（D/X：1.34）和Fe（1.35）。
另外,虽然缺乏其他地区的皮果衣数据,难以从元素含量的角度考量皮果衣对研究区域的大气元素沉降水平的反映可靠性,但镧系元素彼此之间相近的D/X比值表明,皮果衣在反映大气沉降颗粒物的元素组成方面,具有与丽石黄衣相同的有效性。从现有数据出发,本研究认为两种地衣均可用于大气元素沉降监测,但在绝大多数元素方面,不能相互替代。
3.3 样点内变异与混合样品法的有效性
通过混合样品的元素含量样点内变异,可评估混合样品对局域大气元素沉降平均水平的代表性。在大气元素沉降时空格局的地衣原位监测法中,地衣样品的元素含量在局域水平上（local level）变异越小,单个混合样品对监测样点大气沉降平均值的代表性就越大,不同地点之间的可比性就越强。相关研究中,地衣元素含量的局域变异一般不超过30%,如葡萄牙一个森林生态系统中,Flavoparmelia caperata和Evernia prunastri的20种元素的局域变异为1%-33%（Godinho et al. 2009）;法国一个森林生态系统中,E. prunastri的10种元素的局域变异≤30%（Ayrault et al. 2007）;意大利一个偏远地区森林中,Pseudevernia furfuracea的18种元素的局域变异为0.5%-35.7%（Malaspina et al. 2014）;内蒙古鄂尔多斯沙地一个2km2的样点中,两种地衣中的42种元素的CV为10%-29%（Wu et al. 2020）。
本研究以样点内变异表征地衣元素含量的局域变异。除Ca之外的其他51种元素的样点内变异在两种地衣中均较小（CV：8%-27%;表1）,表明在皮果衣和丽石黄衣中,1个混合样品即可有效地反映元素环境输入的平均效应。但是,Ca的CV>30%（皮果衣：37%;丽石黄衣：32%）,表明本研究的采样措施未能完全控制Ca的地衣样点内变异,除地衣的生物学、生态学特性与大气沉降之外,其他因素对地衣Ca含量具有不可忽视的影响。因此,在大气沉降的地衣监测法研究中,需谨慎解释地衣体内Ca的积累。
4 结论
皮果衣和丽石黄衣两种地衣的元素含量均可作为大气元素沉降的监测生物,特别是丽石黄衣反映了研究区域沙尘多、人源释放少的大气元素沉降特点。两种地衣的元素来源相同,其中植物必需营养元素（Ca、K、Mo、P、Rb、S和Se）因受地衣的生理调节控制而在地衣之间差异不显著,在将其含量变异与大气元素沉降水平相联系时应十分谨慎。两种地衣的Hg积累能力相近。皮果衣对其他44种元素的积累能力高于丽石黄衣,且这种积累能力的差异程度具有元素特异性。混合样品对除Ca之外的51种元素在两种地衣中的平均积累水平的代表性强,可以有效地反映局域大气沉降的平均水平。
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