RESEARCH ARTICLE

The linear accumulation of atmospheric mercuryby vegetable and grass leaves: Potential biomonitorsfor atmospheric mercury pollution

Zhenchuan Niu & Xiaoshan Zhang & Sen Wang &

Zhijia Ci & Xiangrui Kong & Zhangwei Wang

Received: 15 January 2013 /Accepted: 26 March 2013 /Published online: 16 April 2013# Springer-Verlag Berlin Heidelberg 2013

Abstract One question in the use of plants as biomonitors foratmospheric mercury (Hg) is to confirm the linear relationshipsof Hg concentrations between air and leaves. To explore theorigin of Hg in the vegetable and grass leaves, open topchambers (OTCs) experiment was conducted to study the re-lationships of Hg concentrations between air and leaves oflettuce (Lactuca sativa L.), radish (Raphanus sativus L.),alfalfa (Medicago sativa L.) and ryegrass (Lolium perenneL.). The influence of Hg in soil on Hg accumulation in leaveswas studied simultaneously by soil Hg-enriched experiment.Hg concentrations in grass and vegetable leaves and roots weremeasured in both experiments. Results from OTCs experimentshowed that Hg concentrations in leaves of the four specieswere significantly positively correlated with those in air duringthe growth time (p<0.05), while results from soil Hg-enrichedexperiment indicated that soil-borne Hg had significant influ-ence on Hg accumulation in the roots of each plant (p<0.05),and some influence on vegetable leaves (p<0.05), but no

significant influence on Hg accumulation in grass leaves(p>0.05). Thus, Hg in grass leaves is mainly originated fromthe atmosphere, and grass leaves are more suitable as potentialbiomonitors for atmospheric Hg pollution. The effect detectionlimits (EDLs) for the leaves of alfalfa and ryegrass were 15.1and 22.2 ng g–1, respectively, and the biological detection limit(BDL) for alfalfa and ryegrass was 3.4 ng m–3.

Keywords Mercury . Biomoniotors . Leaves . Grass andvegetable . Open top chambers . Effect detection limits .

Biological detection limit

Introduction

Mercury (Hg) contamination is a worldwide problem. Everyyear, thousands of tons of Hg are released into the environ-ment from natural and anthropologic sources (Pirrone et al.2010). Under the metabolism of microorganisms, Hg maybe transformed into a more toxic form — methylmercury,which could be biomagnified through food chains, inducingirreversible damage to renal and nervous systems of humanbeings (Ekino et al. 2007). Thus, it is necessary to monitorthe Hg levels in environment.

A biomonitor can be defined as an organism (part of anorganism or a community of organisms) that quantifies thequality of its environment (Markert 2007). Compared toinstrumental monitors, botanic monitors have a wider pros-pect of applications in the environmental monitoring, withthe advantages of widespread distribution, convenient sam-ple collection and low maintenance cost. The use of plantsfor monitoring air quality was started more than 100 yearsago (Nylander 1886), and a variety of plants have beenselected as biomonitors since then. Mosses are the mostcommon species of biomonitoring for air quality, and they

Responsible editor: Elena Maestri

Z. Niu :X. Zhang : Z. Ci : Z. Wang (*)Research Center for Eco-Environmental Sciences, ChineseAcademy of Sciences, P.O. Box 2871, Beijing 100085, Chinae-mail: wangzhw@rcees.ac.cn

Z. NiuKey Laboratory of Urban Environment and Health,Institute of Urban Environment, Chinese Academy of Sciences,Xiamen 361021, China

S. WangDepartment of Environmental Sciences, College of Urbanand Environmental Sciences, Northwest University,Xi’an 710027, China

X. KongDepartment of Chemistry, Atmospheric Science,University of Gothenburgs, 412 96 Gothenburg, Sweden

Environ Sci Pollut Res (2013) 20:6337–6343DOI 10.1007/s11356-013-1691-0

have been used for monitoring of heavy metals including Hgin the surrounding of chlor-alkali plant (Fernández et al.2000), thermal power plant (Carballeira and Fernández2002), thermometer plant (Krishna et al. 2003), even inregional area, such as entire Europe (Harmens et al. 2008).Spanish moss (Tillandsia usneoides L.), neither a moss nor alichen, grown hanging from tree branches, is proved to be anefficient biomonitor for atmospheric Hg in the surroundingof a chlor-alkali plant in Brazil (Calasans and Malm 1997).It has been proved that it is feasible to monitor the atmo-spheric Hg pollution by vegetable and grass leaves. Somegrass species have been successfully used for the atmospher-ic Hg biomonitoring, such as perennial ryegrass (Loliumperenne L.) (De Temmerman et al.1986) and Italian rye-grass (Lolium multiflorum Lam.) (VDI 3957/2 2003;De Temmerman et al. 2007). In addition, some leafy vege-tables also show the possibility for sensing atmospheric Hg(De Temmerman et al. 2009). However, the key question inthe use of herbaceous plants as biomonitors is that the originof Hg in their leaves is still in argument. Some studies showthat Hg in soil has little influence on Hg accumulation in theleaves of herbaceous plants (Greger et al. 2005; Millhollenet al. 2006b), while other studies show that there is substan-tial Hg in leaves originating from soil (Barghigiani andRistori 1995; Cocking et al. 1995; Dunagan et al. 2007;Schwesig and Krebs 2003).

Previous studies on plants monitoring for atmosphericHg, however, were mainly conducted in the field, where itis difficult to control the actual Hg concentrations in longtime range due to the unstable ambient conditions. Thus, toomany factors (e.g., temperature, wind speed, radiation) wereinvolved, giving errors in the relationship of Hg concentra-tion in air and plant leaves. This study presented here aimsto further validate this relationship for vegetable and grassleaves under the well-controlled air Hg concentration con-dition by open top chambers (OTCs) experiment. Addition-ally, the influence of soil-borne Hg on the Hg accumulationin leaves was studied by another experiment, i.e., soil Hg-enriched experiment. Moreover, the differences in Hg accu-mulation from the atmosphere were compared between theleaves of vegetables and grasses.

Materials and methods

Site description

The experimental site is located in a farmland in a smallvillage (N38.70°, E115.23°) in Hebei, China, which has atypical warm and continental monsoon climate. The averageannual temperature and rainfall are 12.3°C and 555.0 mm,respectively. This site is far from cities and factories. It has asoil Hg concentration of 60±30 ng g−1 and atmospheric Hg

concentration of 2±1 ng m−3, which is close to the back-ground level.

Experimental plants

Lettuce (Lactuca sativa L.) and radish (Raphanus sativusL.) were selected as the typical representatives of vegeta-bles, and alfalfa (Medicago sativa L.) and perennial ryegrass(Lolium perenne L.) as the representatives of grasses. Forthe two experiments (i.e., OTCs experiment and soil Hgenriched experiment), seeds of these plants were sown inthe yellow fluvo-aquic soil, with a pH of 7.4±0.2, alkali-hydrolyzable nitrogen of 62.0±15.0 μg g–1, available phos-phorus of 12.0±4.0 μg g–1, available potassium of 98.0±4.0 μg g–1. The two experiments were conducted simulta-neously from May to June, lasting for approximately40 days. The temperatures during the experimental periodvaried from 18.1°C to 33.5°C, and daily managementfollowed local agronomic manners.

Open top chambers experiment

OTCs provide an environment closely resembling ambientconditions (Heagle et al. 1973), and also maintain nearlystable gaseous pollutant concentrations inside the chambers.In this study, OTCs experiment was carried out to confirmthe relationship between atmospheric and foliar Hg concen-trations of vegetables and grasses. Because gaseous elemen-tal mercury (GEM) accounts for most (95 %) of theatmospheric Hg (Fitzgerald et al., 1991), the form of air-borne Hg in this study all indicated GEM. Four Hg concen-trations in the air, i.e., 2±1 (CK1), 10±1, 20±2 and 70±2 ng m–3, were set in this experiment, and each concentra-tion level with three replicate chambers.

OTCs contain chambers (diameter 1.5 m, height 2.0 m,with a 23.6° tilted frustum), gaseous elemental Hg (GEM)generation systems and air dispersion systems. First,GEM was generated from a small amount of liquid ele-mental Hg in a glass tube buried in the deep soil, and thenbrought out by a N2 gas flowing in a Teflon tube with aninner diameter of 2.0 mm. Second, the carried out GEMwas mixed with air emitted by a centrifugal blower(2.5 m3 min–1, 380 Pa), and then was transferred to achamber from its bottom through PVC pipes, which wereperforated equidistantly. Finally, the air in the chamberwas vented from the top of chamber, and every completeexchange required 80 s. N2 gas rate was the main factor tocontrol the GEM concentration in chamber, and the con-centration was monitored by a RA-915+ Zeeman atomicabsorption spectrometry Hg analyzer (Lumex Inc., Rus-sia). When the variation of GEM concentration was over10 %, the N2 gas rates were adjusted by rotameters togenerate the needed GEM concentrations.

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After fumigation, the soil Hg concentrations in the cham-bers were analyzed and compared with those before thefumigation, and results showed that there were no signifi-cant differences (p>0.05), indicating that GEM fumigationhad little influence on soil Hg concentrations in chambers.

Soil Hg-enriched experiment

Soil Hg-enriched experiment was conducted to evaluate theinfluence of Hg in soil on foliar Hg accumulation for grass andvegetable plants. In this study, the form of mercury in soil andleaves referred to total mercury. Four Hg concentrations insoil, i.e., 60±30 (CK2), 124±28, 248±48 and 547±47 ng g

–1,were set in this experiment. To get the needed concentrations,the soils were treated by HgCl2 solutions of different concen-trations, and then homogenized, respectively, by thoroughlymixing. The enriched soils were aged for about 6 months, andthen covered by the non-enriched soil (1–2 cm in thickness) toestablish a buffer layer to minimize the photoreduction andemission of Hg. Zhu et al. (1996) indicated that residual Hgwas the dominant speciation (50–75 %) after the soil wasenriched by HgCl2 solution 6 months later, and the fractionof active Hg was gradually decreased. Ericksen et al. (2005)reported that the release of Hg from the soil enriched byHgCl2solution to the atmosphere was at a relatively low and steadylevel after 62 days. So, evaporation of Hg from the enrichedsoil had little influence on the levels of airborne Hg in thisstudy, and the bioavailability of Hg in the treated soils wasclose to that in natural soils.

Sample collection and measurement

Leaves and roots of radish, lettuce, alfalfa and perennialryegrass were collected in plastic self-sealing bags for twotimes, with about an interval of 20 days. The samples wererinsed by tap water and ultra-pure deionized water, dried at55 °C, ground, and then stored at −20 °C for analysis.

Total Hg concentrations in leaves and soil were determinedby a RA-915+ analyzer attached with PYRO-91 thermal de-composition accessory (Lumex Inc., Russia). The sampleswere directly thermally decomposed in an atomizer chamberat 750 °C with the aided catalytic action, and then Hg0 wasdetected by the RA-915+ analyzer. The instrument detectionlimit was 5 pg for solid samples. Calibration curves coveringthe appropriate concentrations were determined by using soilstandards (GBW07404, 590 ng g–1) and peach foliage stan-dards (GBW08501, 40 ng g–1), respectively.

Data analysis

Data are presented as mean and standard deviation. Correla-tions were analyzed between Hg concentrations in plant leavesand those in air/soil. Variance analysis of Hg concentrations in

plant leaves were performed among different Hg level treat-ments. Statistical significance was considered at p<0.05.

Results and discussion

The relationship of Hg concentrations between leavesand air

Figure 1 shows the obvious linear correlations between theHg concentrations in air and those in leaves in the twoexposure periods. For lettuce, the Hg concentrations inleaves were significantly positively correlated with Hg con-centrations in air in both period 1 (R2=0.933, p<0.05) andperiod 2 (R2=0.996, p<0.01). The same results were alsoobserved for radish (R2=0.968, p<0.05; R2=0.999, p<0.01)(Fig. 1). For the two grasses, Hg concentrations in the leavesof alfalfa had significantly positive correlations with theconcentrations in air in the two periods (R2=0.987, p<0.01; R2=0.985, p<0.01), and Hg concentrations in theleaves of ryegrass were increased linearly with the increaseof air concentrations in both periods (R2=0.997, p<0.01;R2=0.995, p<0.01) (Fig. 1). Thus, results from OTCs ex-periment indicated that the impact of airborne Hg on Hgaccumulation in leaves was very effective.

Similar results were also found from studies conducted intrees. Using closed-system, Frescholtz et al. (2003) showedthat Hg in the atmosphere primarily influenced foliar uptakeof quaking aspen (Populus tremuloides), and Hg accumula-tion in leaves occurred as a function of time and air concen-tration. Ericksen et al. (2003) also showed that almost all theHg in the foliar tissue of quaking aspen originated from theatmosphere. Millhollen et al. (2006a) pointed out that foliarHg concentrations of Juniperus scopulorum, Pinus ponderosaand Robinia pseudoacacia were found to be influencedprimarily by atmospheric Hg concentrations and to alesser extent by soil exposures. For herbaceous plants, DeTemmerman et al. (2007, 2009) showed that Hg concentra-tions in leaves of grass and vegetables correlated well with theambient total gaseous mercury (TGM) concentrations as theatmospheric Hg was by far the most important source of Hg invegetable leaves.

Foliar uptake of atmospheric Hg might be controlled byleaf physiological activities and environmental factors. Sto-matal conductance, temperature, irradiance and atmosphericHg concentrations are the critical factors governing thefoliar Hg flux. Millhollen et al. (2006b) indicated that thereduced stomatal conductance might result in lower foliarHg concentrations at the higher CO2 exposures. Leonard etal. (1998) found that foliar Hg flux increased linearly as afunction of temperature and irradiance within a set range.Studies demonstrate that there is a species-specific compen-sation point (no net exchange occurs) for the foliar Hg flux,

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and leaves uptake the atmospheric Hg through stomata asthe atmospheric Hg concentration exceeds the compensationpoint (Ericksen and Gustin 2004; Hanson et al. 1995).Besides, nonstomatal pathway also plays an important rolein the foliar accumulation of atmospheric Hg (Stamenkovicand Gustin 2009). Therefore, the accumulation of atmo-spheric Hg by the leaves of grasses and vegetables in thisstudy might be a combination of stomatal and nonstomatalpathways under the control of environmental factors, and itwas mainly influenced by Hg levels in the air.

The influence of soil-borne Hg on Hg accumulationin leaves

Figure 2 shows the influence of Hg in soil on Hg accumu-lation in leaves. Hg concentrations in the leaves of lettuceand radish at the concentration of 60 ng g–1 were signifi-cantly lower than those at other soil Hg concentrations inboth periods, respectively (p<0.05) (Fig. 2). Furthermore,Hg concentrations in the roots of lettuce and radish werelinearly increased with Hg concentrations in soil for bothperiods (Fig. 3), indicating that the increase in Hg accumu-lation in lettuce and radish leaves might be partly driven byroot systems. Similar results were also shown in previousstudies. Cocking et al. (1995) found that Hg concentrationsin Asclepias leaves were correlated with soil concentrations.Barghigiani and Ristori (1995) observed a significant corre-lation between the leaves of rosemary and soil, yet found

none for air and leaves. Dunagan et al. (2007) showed thatfoliar Hg concentration of mustard spinach was positivelycorrelated with Hg concentration in soil. In the experimentof Fay and Gustin (2007), foliar Hg concentrations ofA. tridentate showed a statistically significant influence ofsoil Hg concentrations.

Regardless of the soil Hg concentrations, Hg concentra-tions in alfalfa leaves were not significantly different (p>0.05) in both periods, and same results were also found forryegrass leaves (Fig. 2). However, the soil-borne Hg hadsignificant (p<0.05) influence on Hg accumulation in theroots of grasses, indicating that roots of grasses acted as abarrier for the translocation of soil-borne Hg to the above-ground. Results of Cavallini et al. (1999) showed mercuryion is preferentially bound to the cell walls of the outerlayers of the root cortical cylinder as well as the centralcylinder. Many other studies that also showed that the in-fluence of Hg in soil on Hg accumulation in aboveground oftrees was limited (e.g., Frescholtz et al. 2003; Ericksen et al.2003; Ericksen and Gustin 2004; Millhollen et al. 2006a).Therefore, it can be concluded that the influence of soil-borne Hg on foliar Hg accumulation is species-dependent.Possible explanations for the differences in soil Hg accumu-lation between vegetable and grass leaves include the fol-lowing: (1) the different roles between vegetable and grassroots in the translocation of soil-borne Hg to the above-ground, and grass roots act more as a barrier for that trans-location; (2) the limited soil covered by the vegetable

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200lettuce in period 1, Y=2.04X+11.52, R2=0.933lettuce in period 2, Y=3.09X+13.11, R2=0.996radish in period 1, Y=3.81X+7.66, R2=0.968radish in period 2, Y=4.11X+20.49, R2=0.999

Hg

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alfalfa in period 1, Y=0.92X+4.54, R2=0.987alfalfa in period 2, Y=1.23X+10.89, R2=0.985ryegrass in period 1, Y=1.67X+3.59, R2=0.997ryegrass in period 2, Y=2.30X+14.44, R2=0.995

Fig. 1 The correlations offoliar Hg concentrations inlettuce, radish, alfalfa andryegrass with air Hgconcentrations during period 1and period 2. Error bars denotestandard error of the mean

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Fig. 2 The influence of soil-borne Hg on the foliar Hgaccumulation in lettuce, radish,alfalfa and ryegrass during theperiod 1 and period 2. Errorbars denote standard error of themean. Columns with differentletters denote significantdifferences at p<0.05 amongdifferent soil Hg treatments

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leaves, which increases the air movement and probably alsoa higher emission of Hg from the soil.

The relationship of Hg concentrations in leaves and time

In the OTCs experiment, the Hg concentration in leaves inperiod 1 was lower than that in period 2 for each species. Itis an indication that leaves of vegetables and grass indeedaccumulate Hg as a function of time, which is in accordancewith the results of Frescholtz et al. (2003), Millhollen et al.(2006a, b) and Fay and Gustin (2007). In soil Hg-enrichedexperiment, the Hg concentration in leaves of lettuce andryegrass in period 1 was lower than that in period 2, respec-tively, while contrary results were observed for radish andalfalfa. After 40 days, some basal leaves of radish andalfalfa were deciduous, which may cause the decrease inHg concentration in leaves. Ericksen et al. (2003) also foundthat the foliar Hg concentrations in quaking aspen leveledoff around 2–3 months, and then slightly decreased in thefourth month because of senescence.

Comparison of Hg concentrations in leaves among differentspecies

The accumulation of Hg in plant leaves is highly species-dependent. Under the same conditions of air concentrationsand time, the foliar Hg concentration in the four speciesincreased in the order of alfalfa<ryegrass<lettuce<radish.Vegetables appear to accumulate more airborne Hg thangrass. De Temmerman et al. (1986) found that the Hgaccumulation in perennial herbs was far higher than that in

grasses and leafy vegetables. Furthermore, De Temmermanet al. (2009) showed that leaves of spinach accumulatedmarkedly more Hg than grass and lettuce in another exper-iment. Under the same soil Hg concentration and time, thefoliar Hg concentration in the four species showed the trendof alfalfa<lettuce<ryegrass<radish.

The potential biomonitors for atmospheric Hg pollution

Though results from the two experiments demonstrated thatthe influence of airborne Hg was more effective than that ofsoil-borne Hg on the foliar Hg accumulation, Hg in vegetableleaves may result from a combination of uptake from theatmosphere and translocation or emission from the soil, whileHg in grass leaves originated mainly from the atmosphere.Therefore, leaves of grasses could be better indications of theHg concentrations in ambient air, compared to vegetables.Grass is commonly used for biomonitoring as it is cheap andwidespread. In Germany, Italian ryegrass (Lolium multiflorumLAM cv Lema) has been a VDI guideline for air Hgbiomonitoring (VDI 3957/2, 2003). De Temmerman et al.(2007, 2009) established a biomonitoring network near achlor-alkali plant by perennial ryegrass and leafy vegetables.

With relatively lower slopes of the equations (Table 1),Hg concentrations and daily Hg accumulation rates in leavesin this study are lower than those in the experiment of DeTemmerman et al. (2007). The leaves in the experiments ofDe Temmerman et al. (2007, 2009) seemed to accumulatemore atmospheric Hg than those in this study, which mayresult from the different growth conditions between the twostudies.

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radish in period 1, R2=0.60

radish in period 2, R2=0.83

Fig. 3 The correlations of rootHg concentrations in lettuceand radish with soil Hgconcentrations during theperiod 1 and period 2. Errorbars denote standard error of themean

Table 1 Comparison for grasses between this study and De Temmerman et al. (2007)

Species Equation 1 Equation 2 EDL(ng g–1) BDL(ng m–3) Reference

Ryegrass Y=9.99X−2.42 Y′=0.357X−0.086 30 3.2 De Temmerman et al. (2007)

Alfalfa Y=1.23X+10.89 Y′=0.03X+0.2 15.1 3.4 This study

Ryegrass Y=2.30X+14.44 Y′=0.06X+0.3 22.2 3.4 This study

Y is the Hg concentration in leaves (ng g–1 ), Y′ is the Hg accumulation rate in leaves (ng g–1 day–1 ), X is the Hg concentration in air (ng m–3 ); EDLeffect detection limits, BDL biological detection limit

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According to the VDI Guideline (2003), the effect detec-tion limits (EDL) of Hg in leaves is the lowest value thatindicates significant pollution, and is three times of the stan-dard deviation added to the background value. The biologicaldetection limit (BDL) of atmospheric Hg concentration, i.e.,the lowest Hg concentration causing a significant increase ofHg in leaves, can be calculated from the regression equationsthrough the corresponding EDL value. In this study, the air Hgconcentration of 2 ng m–3 is very close to the global back-ground atmospheric Hg concentration 2.02±0.39 ng m–3

(Slemr and Langer 1992), so the Hg concentration in leavesat 2 ng m–3 was regarded as the background value. The EDLsof Hg in this study (15.1 and 22.2 ng g–1) are lower than that(30 ng g–1) reported by De Temmerman et al. (2007), whilethe BDLs values of 3.4 and 3.4 ng m–3 are in good agreementwith the value of 3.2 ng m–3 reported by De Temmerman et al.(2007) (Table 1). It should be noted that this experiment wascarried out under controlled conditions, while the study of DeTemmerman et al. (2007) was carried out in different yearsunder different climatic conditions, which may result in ahigher standard deviation. In other words, the leaves of alfalfaand ryegrass could be selected as excellent biomonitors foratmospheric Hg pollution.

Conclusions

The OTCs experiment indicated that Hg concentrations inthe leaves of lettuce, radish, alfalfa and perennial ryegrasswere the function of air Hg concentrations and time. Thevegetables could accumulate more Hg than grass under thesame air Hg concentration and time. However, in view ofthe influence of soil-borne Hg on the foliar Hg accumulationin vegetables, the appropriate species as the atmospheric Hgbiomonitors should be grass. The EDL values of Hg foralfalfa and ryegrass were 15.1 and 22.2 ng g–1, respectively,and BDL values for alfalfa and ryegrass were 3.4 ng m–3.Even if the leaves of grass show a linear relationship withthe atmospheric Hg, growth time is another factor affectingthe Hg concentration in leaves, and plant leaves do not growin unanimity. Thus, it should be difficult to indicate exactlythe atmospheric Hg concentration only by grass leaves inthe field, which could be as a complementary technique ofthe monitor for the atmospheric Hg pollution.

Acknowledgments This work was funded by the National NaturalScience Foundation of China (No. 40803033 and 41073092), and StateKey Laboratory of Environmental Chemistry and Ecotoxicology, Re-search Center for Eco-Environmental Sciences, Chinese Academy ofSciences (No: KF2011–11). The anonymous reviewers are acknowl-edged for their valuable comments.

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