Journal of Radioanalytical and Nuclear Chemistry, Vol. 261, No. 3 (2004) 679–687

0236–5731/2004/USD 20.00 Akadémiai Kiadó, Budapest© 2004 Akadémiai Kiadó, Budapest Kluwer Academic Publishers, Dordrecht

Mercury in lichens of Nahuel Huapi National Park, Patagonia, ArgentinaS. Ribeiro Guevara,1* D. Bubach,1 M. Arribére1,2

1 Laboratorio de Análisis por Activación Neutrónica, Centro Atómico Bariloche, Argentina2 Instituto Balseiro, Universidad Nacional de Cuyo, Bariloche, Argentina

(Received March 22, 2004)

Mercury and other elements of interest are determined in lichens collected in Nahuel Huapi National Park, Northern Patagonia, Argentina. Pooledsamples are analyzed by instrumental neutron activation analysis. Mercury contents in Usnea sp. collected from undisturbed sites range from0.0558±0.0083 to 1.38±0.18 µg.g–1. Other potential pollutants are identified by the analysis of Usnea sp. samples, namely Sb, As, Br, Zn, and Se.Previous experiments with foliose and fruticose lichens are also discussed. The analysis of mercury contents of foliose lichens sampled from urbanand periurban sites of Bariloche city, and from undisturbed regions, demonstrate that the atmosphere of Bariloche city is enriched in mercurycompared to the surroundings. The result is confirmed by transplantation experiments from undisturbed zones to urban sites.

Introduction

Lichens are long-lived organisms that incorporatemetals in their thalli by the interception of soluble orparticulate matter. Soluble metals tend to settle in extra –or intracellular locations. In the first case, lichensoperate as ions exchange resins, absorbing metal ionsfrom rainwater and releasing H+ ion or metal ions of lowbinding affinity as the uptake proceeds. These kinds ofprocesses are fast, passive, and unaffected by metabolicinhibitors. On the opposite, the intracellular location ofsoluble metals is a slow process, stimulated by light. Forshort-term lichen exposure (few hours), extra cellularuptake is predominant. Lichen can also incorporatemetals included in particulate matter, as particulate isentrapped in the thallus.1 Lichens fulfill the basicconditions to be biomonitors, allowing their use inenvironmental contamination studies. The study of theirelemental composition has proved to be a useful tool toassess air pollution by trace-elements, particularly byheavy metals.1–5 Many works have been fulfilled usinglichens as atmospheric biomonitors of mercury.

The analysis of 10 sediment cores sampled from sixwater bodies of Nahuel Huapi National Park, namely oflakes El Trébol, Escondido, Espejo Chico, Morenito,Moreno West, and Nahuel Huapi, showed high mercuryconcentrations in upper layers, ranging from 0.6 to7 µg.g–1.6 The mercury contents of these layers areclearly higher than the background values obtained fromdeep layers, which range from less than 0.08 to0.2 µg.g–1 for the pre-industrial period and from 0.2 to0.3 µg.g–1 for the modern times. These backgroundlevels are similar to those obtained in other regions.7–13A sediment core sampled from lake Traful showedmercury contents similar to background levels all alongthe core profile, without any enrichment in the upperlayers.6 Lake Traful is situated also within Nahuel HuapiNational Park but is considered as a reference since it

* E-mail: ribeiro@cab.cnea.gov.ar

belongs to a different watershed and is subject of littlehuman impact. The accumulation period of the enrichedsediment core layers corresponds to the second half ofthe 20 th century.6 Suspended load sampled from lakeNahuel Huapi as well as the biota studied (fish andmussels) also showed high mercury contents (from 0.85to 7.3 µg.g–1) (unpublished data and Reference 14).These results let us conclude that the region comprizingthe six lakes received mercury inputs during the secondhalf of 20 th century and at present, but the spatialdistribution of mercury concentrations in the sedimentsand biota did not allow the identification of mercurysources, and no point or diffuse mercury source wasidentified in the region by other means as well. Theanalysis of mercury contents in lichens was performed toprovide background data for biomonitoring discussingalso the results of previous research in this region.15–17The global transport of mercury with wet deposition iswell-known in undisturbed regions. Following the steepprecipitation gradient in the Nahuel Huapi National Parkthe collected pooled samples of Usnea sp. were analyzedin order to determine variations that could be associatedwith this potential source. To assess the impact of wetdeposition in the environments studied, the 137Cscumulative flux were also measured in sediment coressampled nearby lichens sampling sites. 137Cs inputs inNahuel Huapi National Park environments wereproduced only by atmospheric fallout.18 Therefore, itsbehavior will provide information about the impact ofatmospheric fallout in the environments studied.

Experimental

Study area

Nahuel Huapi National Park is a natural area thatincludes pristine zones and human settlements, separatedby buffer areas. No relevant industrial or extensive

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Fig. 1. Nahuel Huapi National Park, Patagonia, Argentina. Usnea sp. lichens sampling sites

agriculture activities exist within the National Park ornearby. The main activity of the region is tourism. SanCarlos de Bariloche is the only important city in theregion, located in the South margin of lake NahuelHuapi (Fig. 1), with a population of 100,000 inhabitants.Lake Nahuel Huapi is the largest of several lakes locatedin Nahuel Huapi National Park, with 557 km2 total area,464 m maximum depth, 764 m above see level. It isconsidered as an ultraoligotrophic system, which showssome mesotrophic areas located near Bariloche city andVilla La Angostura (Fig. 1), due to wastewaterdischarges. There is a strong vegetation gradient fromdense rainforest (mainly Nothofagus dombeyii andAustrocedrus chilensis) in the West, to dry grasslands(econtonal forest) in the East.19 The vegetation variationis associated to the steep precipitation gradient, from3042 mm.y–1 in western Puerto Blest, to 473 mm.y–1 in

eastern Ñirihuau (Table 1). Predominant winds run fromWest to East in the area of Nahuel Huapi National Park.

No point or diffuse mercury source was identified inthe region at present. Electricity came from localproduction in Bariloche for many years, burning fossilfuel from oil processing, a well-known mercury source.Two small production plants are located in Bariloche,but they are working only occasionally since the mideighties. Mercury inputs in the aquatic environmentscould be explained by global transport and wetdeposition,20 or could come from local sources, insidethe National Park, or nearby places. Local sources canbe natural or anthropogenic. Volcanic activity affectedstrongly the study region. This has been a potentialsource of natural mercury inputs in the past, stored insediments and soil, or in present time, associated withgaseous emission.1,21,22 The human activity, mainly in

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Bariloche city, could also involve mercury releases tothe environment. City waste burning, performed in thedry zone of the Park, near Bariloche city, is anotherpotential source.

Sampling and analysisSince global transport with wet deposition is a

potential mercury source, an association between theprecipitation gradient and mercury contents in theenvironment could provide useful information toidentify this pathway. Therefore, sampling sites weredefined in undisturbed places of Nahuel Huapi NationalPark following the precipitation gradient throughout thePark, along the West-East direction and close to lakeNahuel Huapi margins (Fig. 1 and Table 2).

A first field evaluation of the sampling sites wascarried out, searching for the presence, morphology, andother characteristics of lichen species, since theenvironments involved in this work are quite different.Only Usnea sp. was present in all sites, with similarbiomasses and homogeneous characteristics. Usneafruticose lichens show an advantage when compared tofoliose lichens studied in the Nahuel Huapi NationalPark. Lichens can incorporate clastic particulate, actingas traps, as well as absorb elements present in theirenvironment. The elements included in clasticparticulate maintain the proportion of the rock thatoriginated them, and do not reflect environmentalchanges. These elements could interfere with thedetermination of the elements of interest. Theconcentration of the lithophile elements associated toclastic particulate in lichen was found to be as high as40% of their concentration in the sediments of folioselichen of the Nahuel Huapi National Park.15 The average

detritical material entrapped by the lichens has a directconnection with the site exposure to wind, but fruticoseUsnea fastigiata showed lower lithophile elementconcentrations than foliose species did.15

Usnea sp. individuals, with similar developmentcharacteristics, were sampled without distinguishing thespecies having very slight differences. The differenceswhich cannot be distinguished during sampling and arenot relevant for bioindication purposes, characterizeUsnea species in the study region. Concentrationvariations between individuals sampled at the same sitecan be found, but they do not reflect necessaryenvironmental changes. RASMUSSEN5 has suggested thatit is recommended to sample at least three separateindividuals of one species in order to obtain arepresentative Hg value for one site. Pooled samples,collected from the same site, obtained from at least 10individuals with similar development characteristics,were studied.

Lichen individuals were collected in polyethylenebags, using latex gloves. At least 10 individuals withsimilar development characteristics were collected foreach sampling site. The thalli were examined andcleaned under a dissecting microscope to eliminatesubstrate remains and dust particles. Thereafter, all thalliwere washed three times during 10 minutes using ASTMgrade 1 water. After the last rinse, they were dried atroom temperature. The samples were cut, ground to afine powder, and homogenized by means of titanium andTeflon tools and devices. Each ground and homogenizedsample was freeze-dried to constant weight.

Elemental contents were determined by instrumentalneutron activation analysis (INAA) using the absoluteparametric method. The experimental set-up and theanalysis method have been described elsewhere.15

Table 1. Precipitation in Nahuel Huapi National ParkStation Mean precipitation

per year, mm.y–1Calculation periodof the mean values

Number of years consideredfor computing the mean values

Puerto Blest 3042 1936–1963 20Brazo Rincón 2554a – –Lago Espejoc 2065 1940–1969 21Isla Victoria 1507 1933–1957 25Colonia Suizad 1507b – –Bariloche FC 782 1955–1993 27Bariloche aeropuerto 771 1951–2001 49Ñirihuau 473 1937–1965 29

a Estimated from measurements in Puerto Blest and Lago Espejo.b Estimated from measurements in Isla Victoria. Measurements in Colonia Suiza in period 1933–1941 showed thesame mean value than Isla Victoria measurements in the same period. Isla Victoria values are considered because25 values were used for mean calculation, and only 8 were available in Colonia Suiza.c Close to Lake Espejo in Fig. 1.d Close to Lake Moreno in Fig. 1.

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Table 2. Usnea sp. lichens and sediment core sampling sites, including mean annual precipitationLichen

sample codeCore

sample codeSampling site Mean precipitation,

mm.y–1

UL8 UL8 Lake Nahuel Huapi, Brazo Rincón 2554UL7 – Lake Correntoso 2065aUL6 – Lake Escondido 1507cUL5 – Lake Nahuel Huapi, Brazo Tristeza 1507c

– LLAO Lake Moreno 1507c– TRE Lake El Trébol 1507c

UL4 – Lake Nahuel Huapi, Brazo Huemul, branch end 1000bUL3 – Lake Nahuel Huapi, Brazo Huemul, branch mouth 1000bUL2 UL2 Dry environment, near Puerto Cisnes 622dUL1 – Dry environment, near river Limay mouth 473

a Estimated from measurements in Lago Espejo (Table 1).b Estimated from measurements in Lago Espejo, Isla Victoria, and Bariloche (Table 1).c Estimated from measurements in Isla Victoria (Table 1).d Estimated from measurements in Ñirihuau, and Bariloche (Table 1).

Table 3. Lichen Standard Reference Material IAEA 336 resultsMeasured, µg.g–1

Element Sample 1 Sample 2Certified or

informed (*), µg.g–1Confidence

interval, µg.g–1

As 0.657 ± 0.056 0.620 ± 0.058 0.64 0.56 – 0.72Br 12.9 ± 1.1 12.3 ± 1.1 12.9 11.2 – 14.6Ce 1.30 ± 0.15 1.22 ± 0.13 1.27 1.09 – 1.44Cs 0.115 ± 0.013 0.109 ± 0.011 0.11 0.097 – 0.123Co 0.298 ± 0.025 0.282 ± 0.024 0.29 0.25 – 0.33Eu 0.0217 ± 0.0024 0.0214 ± 0.0021 0.023* 0.019 – 0.027Fe 419 ± 62 402 ± 59 425 380 – 470Hg 0.196 ± 0.023 0.198 ± 0.024 0.20 0.17 – 0.23La 0.576 ± 0.032 0.541 ± 0.028 0.66* 0.55 – 0.76Na 307 ± 16 299 ± 17 320* 280 – 360Rb 2.14 ± 0.31 1.94 ± 0.33 1.72* 1.52 – 1.92Sb 0.0749 ± 0.0085 0.0711 ± 0.0082 0.073 0.063 – 0.083Sc 0.170 ± 0.012 0.169 ± 0.012 0.17 0.148 – 0.192Se 0.242 ± 0.031 0.240 ± 0.028 0.22 0.18 – 0.25Sm 0.102 ± 0.066 0.099 ± 0.070 0.106 0.092 – 0.120Th 0.142 ± 0.013 0.138 ± 0.012 0.14* 0.12 – 0.16Zn 32.1 ± 4.5 31.0 ± 4.3 31.5 28 – 35

Elemental concentrations and certified values were measured by instrumental neutron activation analysis.

Aliquots of the samples, ranging in mass from 100 to120 mg, were placed in Suprasil AN quartz ampoulesfor irradiation, and sealed. The samples were irradiated24 hours in the RA-6 Research Reactor, Centro AtómicoBariloche. Two gamma-ray spectra were collected after7- and 20-day decay times. Mercury and other 24elements (Sb, As, Ba, Br, Ca, Ce, Cs, Zn, Co, Cr, Eu, Sc,Sr, Hf, Fe, La, K, Rb, Sm, Se, Na, Ta, Tb, Th) weremeasured in each sample. Corrections for interferencesof other elements or U fission products were performedwhen needed. Lichen Standard Reference MaterialIAEA-336 was analyzed using the same methodology asabove to control the results (Table 3).

137Cs cumulative fluxes, in sediment cores, samplednearby lichens sampling sites, were measured in order toassess the impact of wet deposition in the sampling sites.

Sediment cores were taken from lake Nahuel Huapi andother smaller neighboring lakes, namely lakes El Tréboland Moreno West (Fig. 1 and Table 2). The sedimentcores were extracted with a messenger activated gravitytype corer. They were cut open, visually inspected, andsub-sampled in every 1 cm. Each sample was freeze-dried, homogenized, weighted, placed in the countingcontainers and sealed. The specific activity of 137Cs wasmeasured in each sub-sample, to obtain the specificactivity profile of 137Cs of each core. The experimentalset-up and the analysis method have been describedelsewhere.18 The cumulative flux of 137Cs of eachsediment core was determined from the 137Cs inventory,and corrected for the nuclear decay to the sampling dateof the first core for comparison.

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Results

The elemental concentrations measured in lichens byINAA were classified according to their relation to Scconcentrations, in order to distinguish those elementsthat are mainly associated with particulate matterentrapped by the lichen thalli from those absorbed fromthe atmosphere, and identified hence as potentialpollutants. When many lichen thalli sampled from thesame site are analyzed, the lithophile elementconcentrations show a linear relation with Scconcentration.15 The same method can be used forhomogenated samples from different sites if the clasticinputs have the same origin. In Fig. 2 the concentrationof lithophile elements Co, Eu, Fe, and Hf is plotted vs Scconcentration, showing good linear correlationcoefficients (ranging from 0.85 to 0.88; see also Table4). Fe and Hf show the best linear correlationcoefficients with Sc, and the rare earths elements (REE)Ce, Eu, La, Sm as well as Tb, Ba, Co, Na, Ta and Thalso show linear correlation with Sc. Similar resultswere found in previous works, analyzing different lichenthalli sampled in the same site.15 Therefore, theseelements (Ba, Ce, Co, Eu, Fe, Hf, La, Sm, Na, Ta, Tb,and Th) can be associated to clastic inputs to lichens.

It should be noted that the UL1 sampling site is the mostexposed to winds, where almost no vegetation protectslichen thalli around the tree that hold them, and here thehighest lithophile element concentrations can be found.The concentration values of Sb, As, Br, Ca, Cs, Zn, Cr,Sr, Hg, K, Rb, and Se do not correlate with Sc,therefore, they can be associated with lichen physiologyor they could be absorbed from the atmosphere. Sb, As,Br, Zn, Hg, and Se concentrations, reported in Table 5,can be identified as potential pollutants, since theseelements can be associated with human activities and donot show any association with clastic inputs to lichens.Figure 3 shows the mercury contents, plotted vs.precipitation in sample sites.

Table 4. Classification of the elements measured in lichensaccording to the correlation coefficient values corresponding to the

elemental concentration vs. Sc concentration plotsCorrelation coefficient Element

0.80 > ρ Sb, As, Br, Ca, Cs, Zn, Cr, Sr, Hg, K, Rb, Se0.85 > ρ ≥ 0.80 Ba, Ta0.90 > ρ ≥ 0.85 Ce, Co, Eu, La, Sm, Tb, Th0.95 > ρ ≥ 0.90 Fe, Na0.98 > ρ ≥ 0.95

ρ ≥ 0.98 Hf

Fig. 2. Usnea lichen pooled samples. Eu, Co, Fe, and Hf vs. Sc concentrations

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Fig. 3. Usnea lichen pooled samples. Mercury concentration plottedvs. precipitation in the sampling sites (Table 2)

Fig. 4. 137Cs cumulative flux from core sediment inventories vs.precipitation in the sampling sites (Table 2). The cumulative fluxes

of 137Cs are corrected for nuclear decay

Cumulative fluxes of 137Cs determined from coresediment inventories nearby the Usnea lichen samplingsites are plotted in Fig. 4 vs. precipitation.

Discussion

Background concentrations of mercury in lichens

RASMUSSEN5 reports a narrow range of Hg contentsfor 5 lichen species (genus Cladina and Cladonia) of theCanadian Shield, i.e., 0.017 to 0.067 µg.g–1, similar tothe range of 0.004 to 0.040 µg.g–1 reported for samplesof genus Cladonia collected in Alaska, Iceland, andMassachusetts. MAKHOLM and BENNETT23 studied themercury impact of a chlor-alcali plant for itssurroundings by transplanting Hipogymnia physodeslichen thalli. This work reports that the mercurybackground values for Hipogymnia physodes inWisconsin, USA, are in the range between 0.11 and0.15 µg.g–1, i.e., lower than those ranging from 0.2 to0.4 µg.g–1 observed previously in other parts of theworld. In this study the authors ascribe the difference to

the more clean Wisconsin environment, and to samplehandling and analysis features. Two other worksreported 0.10 and 0.16 µg.g–1 for that background.23 Anexperiment with transplanted lichens was carried out inMolve, Croatia, to assess the contamination impact ofthe INA’s Nagtplin gas treatment plant. The backgroundHg concentration for Hipogymnia physodes was here0.11 µg.g–1.24 In general, it shows a wide variationrange if different lichen species are considered, but thelower values are below 0.15 µg.g–1.1

Hg concentration values measured in Hipogymniaphysodes sampled in contaminated environments werehigher as 0.77 µg.g–1, i.e., near Hg contaminationsources like mercury mines, iron smelter plant, andchlor-alkali plants.23 In situ lichens were also sampled inthe Molve experiment. Hg concentration valuesassociated with Hg contaminated environment werereported to range from 0.54 to 1.17 µg.g–1 for Parmeliasulcata, and from 0.53 to 2.80 µg.g–1 for Xanthoriaparietina.24 In general, Hg concentration values of insitu lichens sampled in regions with Hg contaminationsources can be as low as 0.1 µg.g–1,1 but these lowvalues do not necessarily mean contaminated conditions.As a general remark, the most valuable results obtainedusing lichens as biomonitors are gained by comparativestudies in the same or nearby regions, or withtransplantation of thalli from undisturbed regions to thestudy site. The lower limits for the various range of Hgconcentrations in lichen associated with contaminatedsites are around 0.5 to 0.8 µg.g–1, considering the resultsreported by MAKHOLM et al.23 and HORVAT et al.24

Mercury concentrations measured in this work inUsnea sp. pooled samples ranged from 0.06 to1.38 µg.g–1 (Table 5), the values are clearly higher thanthe mercury contents of lichen sampled from otherundisturbed regions or background values forcontamination studies. The fact that foliose lichens andfruticose Usnea fastigiata sampled from periurban zonesof the Bariloche city and Puerto Blest forest, anundisturbed area of the Nahuel Huapi National Park,have similar mercury contents than Usnea lichencollected also from undisturbed areas of the NahuelHuapi National Park, suggest that this wide variationrange could be associated to background level of theregion, since the sampling points are spread over thePark (Fig. 1). Mercury contents of foliose lichenssampled in Bariloche urban areas (Table 6) are higher,and in the same range than other lichen studied.

Mercury in Bariloche city environmentMercury contents measured in lichens sampled from

Bariloche urban and periurban zones, and from theundisturbed regions of the Nahuel Huapi National Parkare shown in Table 615,17. Mercury contents offoliose lichen species Hypotrachyna brevirhiza and

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Candelariella vitellina are enriched by a factor of 2.4and 3.8 in urban collections over those of periurbansites. The reference mercury concentration values are inthe same range as the mercury contents of folioseParmelia cunninghamii and fruticose Usnea fastigiata(Table 6), sampled from undisturbed zones of theNahuel Huapi National Park, which can be considered asa background line for the region of study. Mean mercuryconcentrations determined in foliose lichens Physciaadscendens, Hypotrachyna brevirhiza, andCandelariella vitellina sampled in the urban area areabove 0.8 µg.g–1, in the range of contents associatedwith mercury contamination.

The impact of human activities in Bariloche city wasstudied by transplanting Protousnea magellanica thalli,a fruticose lichen with large biomass.17 Ten thalli werecollected from Puerto Blest’s undisturbed zone (Fig. 1),three of them were transplanted in the same zone forcontrol, and the other were transplanted to three urbansites. The transplanted lichens were analyzed after one-year exposure. The mean enrichment factor of mercuryconcentration in urban sites (see the last row of Table 6,‘urban, transplanted’),c,f against transplanted controls(see the last row of Table 6, ‘undisturbed, trans-planted’),e,f was 2.0. This enrichment of mercury inurban sites over controls transplanted in undisturbedsites confirms the in situ lichen results, showing thatmercury concentration in the atmosphere of the city ishigher than that of the forest and periurban sites.

Mercury and the precipitation gradientThe cumulative fluxes of 137Cs determined from

core sediment inventories nearby lichen sampling pointsshow a clear association with precipitation (Fig. 4).Since 137Cs can reach the Nahuel Huapi National Parkenvironments only by atmospheric transport, mainlytropospheric,18 and by wet deposition, therefore, thewater bodies at these sampling sites are reflecting whatis collected from the atmosphere in the catchment area.Figure 3 shows that mercury contents measured inUsnea lichens do not correlate with precipitation. Thehighest value was measured in UL2 sampling site,located in the dry zone (Fig. 1). Mercury contents insampling sites UL1 and UL8, in the driest and mostrainy zones, as well as two intermediate points, UL5 andUL7, show similar values, ranging from 0.42 to0.67 µg.g–1 (Table 5). These values are in the samerange than those of foliose lichens and fruticose Usneafastigiata sampled from the periurban zones ofBariloche city, and from the undisturbed areas of theNahuel Huapi National Park (Table 6). The lowestmercury concentration was measured in lichens fromUL3 site. The highest mercury content, 1.38 µg.g–1 wasmeasured in lichens collected in UL2 sampling site, andthe concentration of samples collected in UL4 and UL6

sites, showing intermediate 1.06 and 0.90 µg.g–1 values,are in the range of that of foliose lichens sampled fromthe urban zones of Bariloche city (Table 6). Therefore,no direct relation between atmospheric mercury comingfrom wet deposition and lichen Hg contents wasobserved. Mercury could follow different pathways thancesium after atmospheric deposition within theecosystem, and a mercury transport within the aquaticmedia and biota may occur. The mercury concentrationsin the upper layers of sediment cores do not show anassociation with precipitation. Only correlation withorganic matter contents was observed, suggesting thatmercury circulation is mainly associated with the biota.6The lack of correlation between precipitation andmercury concentration could be due to the low relevanceof the global transport and wet deposition as a mercurysource in this region or to the strong influence ofmercury cycling in the biota after deposition.

*

We thank the reactor RA-6 operation staff for their assistance insample analysis. We also want to acknowledge Andrea RIZZO andRicardo SÁNCHEZ for core sampling. This work was partially fundedby International Atomic Energy Agency Project ARG/7/006.

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