atmospheric mercury exchange with a tallgrass prairie ecosystem housed in mesocosms

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Atmospheric mercury exchange with a tallgrass prairie ecosystem housed in mesocosms Jelena Stamenkovic a , Mae S. Gustin a, , John A. Arnone III b , Dale W. Johnson a , Jessica D. Larsen b , Paul S.J. Verburg b a Department of Natural Resources and Environmental Science, University of Nevada, Reno, Nevada 89557, USA b Division of Earth and Ecosystem Sciences, Desert Research Institute, Reno, Nevada 89512, USA ARTICLE INFO ABSTRACT Article history: Received 28 March 2008 Received in revised form 27 July 2008 Accepted 28 July 2008 Available online 4 September 2008 This study focused on characterizing airsurface mercury Hg exchange for individual surfaces (soil, litter-covered soil and plant shoots) and ecosystem-level flux associated with tallgrass prairie ecosystems housed inside large mesocosms over three years. The major objectives of this project were to determine if individual surface fluxes could be combined to predict ecosystem-level exchange and if this low-Hg containing ecosystem was a net source or sink for atmospheric Hg. Data collected in the field were used to validate fluxes obtained in the mesocosm setting. Because of the controlled experimental design and ease of access to the mesocosms, data collected allowed for assessment of factors controlling flux and comparison of models developed for soil Hg flux versus environmental conditions at different temporal resolution (hourly, daily and monthly). Evaluation of hourly data showed that relationships between soil Hg flux and environmental conditions changed over time, and that there were interactions between parameters controlling exchange. Data analyses demonstrated that to estimate soil flux over broad temporal scales (e.g. annual flux) coarse- resolution data (monthly averages) are needed. Plant foliage was a sink for atmospheric Hg with uptake influenced by plant functional type and age. Individual system component fluxes (bare soil and plant) could not be directly combined to predict the measured whole system flux (soil, litter and plant). Emissions of Hg from vegetated and litter-covered soil were lower than fluxes from adjacent bare soil and the difference between the two was seasonally dependent and greatest when canopy coverage was greatest. Thus, an index of plant canopy development (canopy greenness) was used to model Hg flux from vegetated soil. Accounting for ecosystem Hg inputs (precipitation, direct plant uptake of atmospheric Hg) and modeled net exchange between litter-and-plant covered soils, the tallgrass prairie was found to be a net annual sink of atmospheric Hg. © 2008 Elsevier B.V. All rights reserved. Keywords: Mercury flux Dynamic flux chamber Modeling ecosystem exchange 1. Introduction Approaches to directly measure net ecosystem Hg exchange include micrometeorological methods (cf. Lindberg et al., 1992; Kim et al., 1995; Cobos et al., 2002) and large mesocosms (Gustin et al., 2004; Obrist et al., 2005). Because specific conditions are necessary to apply the former, and the latter are not readily available, the typical approach for measuring Hg flux is to measure individual surface fluxes with small flux chambers. Dynamic flux chambers provide a means of developing statistical relationships between surface Hg exchange and environmental conditions and understanding SCIENCE OF THE TOTAL ENVIRONMENT 406 (2008) 227 238 Corresponding author. Department NRES/MS 370, University of Nevada, Reno NV 89557, USA. Tel.: +1 775 784 4203; fax: +1 775 784 4789. E-mail address: [email protected] (M.S. Gustin). 0048-9697/$ see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.scitotenv.2008.07.047 available at www.sciencedirect.com www.elsevier.com/locate/scitotenv

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Page 1: Atmospheric mercury exchange with a tallgrass prairie ecosystem housed in mesocosms

S C I E N C E O F T H E T O T A L E N V I R O N M E N T 4 0 6 ( 2 0 0 8 ) 2 2 7 – 2 3 8

ava i l ab l e a t www.sc i enced i rec t . com

www.e l sev i e r. com/ loca te / sc i to tenv

Atmospheric mercury exchange with a tallgrass prairieecosystem housed in mesocosms

Jelena Stamenkovica, Mae S. Gustina,⁎, John A. Arnone IIIb, Dale W. Johnsona,Jessica D. Larsenb, Paul S.J. Verburgb

aDepartment of Natural Resources and Environmental Science, University of Nevada, Reno, Nevada 89557, USAbDivision of Earth and Ecosystem Sciences, Desert Research Institute, Reno, Nevada 89512, USA

A R T I C L E I N F O

⁎ Corresponding author. Department NRES/ME-mail address: [email protected] (M

0048-9697/$ – see front matter © 2008 Elsevidoi:10.1016/j.scitotenv.2008.07.047

A B S T R A C T

Article history:Received 28 March 2008Received in revised form 27 July 2008Accepted 28 July 2008Available online 4 September 2008

This study focused on characterizing air–surface mercury Hg exchange for individualsurfaces (soil, litter-covered soil and plant shoots) and ecosystem-level flux associated withtallgrass prairie ecosystems housed inside large mesocosms over three years. The majorobjectives of this project were to determine if individual surface fluxes could be combined topredict ecosystem-level exchange and if this low-Hg containing ecosystemwas a net sourceor sink for atmospheric Hg. Data collected in the field were used to validate fluxes obtainedin the mesocosm setting. Because of the controlled experimental design and ease of accessto the mesocosms, data collected allowed for assessment of factors controlling flux andcomparison of models developed for soil Hg flux versus environmental conditions atdifferent temporal resolution (hourly, daily andmonthly). Evaluation of hourly data showedthat relationships between soil Hg flux and environmental conditions changed over time,and that there were interactions between parameters controlling exchange. Data analysesdemonstrated that to estimate soil flux over broad temporal scales (e.g. annual flux) coarse-resolution data (monthly averages) are needed. Plant foliage was a sink for atmospheric Hgwith uptake influenced by plant functional type and age. Individual system componentfluxes (bare soil and plant) could not be directly combined to predict the measured wholesystem flux (soil, litter and plant). Emissions of Hg from vegetated and litter-covered soilwere lower than fluxes from adjacent bare soil and the difference between the two wasseasonally dependent and greatest when canopy coverage was greatest. Thus, an index ofplant canopy development (canopy greenness) was used to model Hg flux from vegetatedsoil. Accounting for ecosystem Hg inputs (precipitation, direct plant uptake of atmosphericHg) and modeled net exchange between litter-and-plant covered soils, the tallgrass prairiewas found to be a net annual sink of atmospheric Hg.

© 2008 Elsevier B.V. All rights reserved.

Keywords:Mercury fluxDynamic flux chamberModeling ecosystem exchange

1. Introduction

Approaches to directly measure net ecosystem Hg exchangeincludemicrometeorologicalmethods (cf. Lindberg et al., 1992;Kim et al., 1995; Cobos et al., 2002) and large mesocosms(Gustin et al., 2004; Obrist et al., 2005). Because specific

S 370, University of Nevad.S. Gustin).

er B.V. All rights reserved

conditions are necessary to apply the former, and the latterare not readily available, the typical approach for measuringHg flux is to measure individual surface fluxes with small fluxchambers. Dynamic flux chambers provide a means ofdeveloping statistical relationships between surface Hgexchange and environmental conditions and understanding

a, Reno NV 89557, USA. Tel.: +1 775 784 4203; fax: +1 775 784 4789.

.

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228 S C I E N C E O F T H E T O T A L E N V I R O N M E N T 4 0 6 ( 2 0 0 8 ) 2 2 7 – 2 3 8

mechanistic processes. However, it is uncertain whetherempirical relationships derived using field and laboratorydata for individual surfaces can be used to estimate wholeecosystem Hg flux and whether statistical models developedbased on measurements made during specific conditions areapplicable across space and time (Engle et al., 2001; Coolbaughet al., 2002; Gustin et al., 2006).

The initial objective of this project was to comparemesocosm-derived ecosystemHg fluxes with those developedfor individual ecosystem components and determine if thelatter could be applied to model whole ecosystem exchange.Unfortunately it was realized, after detailed investigation,that Hg flux measured at the mesocosm level for the low Hgcontaining ecosystems being studied could not be differen-tiated from the mesocosm system blank (Stamenkovic andGustin, 2007). Because of this a series of dynamic flux chambermeasurements were made from bare soil, individual plantshoots, and litter-covered soil, and these components com-bined, to address our primary research question.

Soil–air Hg exchange is controlled by numerous factors,including substrate and air Hg concentration (Edwards et al.,2001; Schroeder et al., 2005; Bahlmann et al., 2006; Gustinand Lindberg, 2005; Xin and, Gustin, 2007), light (Carpi andLindberg, 1997; Zhang et al., 2001; Gustin et al., 2002;Poissant et al., 2004), soil moisture (Gustin et al., 1999;Bahlmann et al., 2006; Gustin and Stamenkovic, 2005),temperature (Lindberg et al., 1979; Gustin et al., 1997;Zhang et al., 2001; Poissant et al., 2004; Bahlmann et al.,2006), air mixing (Bahlmann and Ebinghaus, 2003), andatmospheric oxidants (Engle et al., 2005). There is evidenceof interactions between these variables; for example, atmo-spheric oxidants may have a greater influence on Hg fluxassociated with dry soils than wet soils (Engle et al., 2005),while light and temperature are important controls on Hgfluxes from saturated soils but exert a lesser effect whensoils are dry (Moore and Carpi, 2005; Bahlmann et al., 2006;Xin et al., 2007).

Vegetation is considered a net sink for atmosphericHg (Xiao et al., 1998; Ericksen et al., 2003; Zhang et al., 2005;Lindberg et al., 1979; Bishop et al., 1998) that must beaccounted for when considering whole ecosystem-level Hgexchange. The presence of plants and litter may also impactthe soil–air Hg flux by altering air mixing, shading the soil,and influencing soil moisture and temperature (Lindberget al., 1979; Carpi and Lindberg, 1998; Zhang et al., 2001;Coolbaugh et al., 2002; Gustin et al., 2004). Thus, applicationof substrate–air Hg exchange models developed for soil aloneis most likely inadequate for estimating the landscape–air Hg exchange from vegetated surfaces (cf. Rasmussenet al., 2005).

Despite the fact that we could not resolve net ecosystemflux at the mesocosm level, the experimental design providedan easily accessible controlled setting where fluxes could bemeasured with small dynamic flux chambers over severalyears from a variety of surfaces. This provided a framework fordetailed assessment of Hg exchange and the factors control-ling flux from plants and bare soils, as well as litter-coveredand vegetated soils. With the data collected we developed ameans of estimating Hg flux for a vegetated low-Hg containingecosystem, as well as an assessment of the type of temporal

data that is needed for scaling long-term ecosystem Hgsource-sink relationships.

2. Methods

2.1. Experimental system

This study was done within the framework of a project thatused intact monoliths of native tallgrass prairie housed inlarge controlled-environment mesocosms, as well as pairedfield sites, aimed at quantifying the effects of interannualtemperature variability on ecosystem processes over multi-ple years (2001–2006) (cf. Zhou et al., 2006; Sherry et al., 2007;Verburg et al., 2005; Arnone et al., in press). Tallgrass prairiesoil–plant monoliths were excavated from central Oklahoma(Kessler Farm Field Laboratory, University of Oklahoma,Oklahoma) and transported to the Desert Research Institute(Reno, Nevada) in November 2001 (Verburg et al., 2005). Three12-ton monoliths (2.4×1.2×1.8 m3; l×w×d) with a totalsurface area of ~9 m2 were placed in each of the four large(~180 m3 total volume) mesocosms or EcoCELLs (EcologicallyControlled Enclosed Lysimeter Laboratories, Griffin et al.,1996; Verburg et al., 2005). The mesocosms provided acontrolled environment and a well-characterized experi-mental setting that could easily be accessed allowing formeasurement of Hg fluxes on diel, monthly and yearly timesteps using dynamic gas exchange chambers (cf. Gustinet al., 2004).

In the mesocosms, the tallgrass prairie system receivednatural light (attenuation by the outer greenhouse andEcoCELL roof is 22%, Griffin et al., 1996), while air humidity,rainfall patterns (amount and frequency), diel and seasonalfluctuations in air temperature, and the soil temperatureprofile were controlled to mimic average field conditionsnear the excavation site (mean of the 1993–2000 period,Mesonet meteorological data; Brock et al., 1995). Solarirradiance, air and soil temperatures in all mesocosmswere highest, and soil water content was lowest in thesummer (Fig. 1a, for details and other environmentalparameters see Verburg et al., 2005). Canopy greenness(index of plant canopy development derived from overlayinga grid on photographs taken directly above canopy eachweek and quantifying the number of cells with a specificdegree of greenness, see Verburg et al., 2005) increased inthe spring and declined in late summer, with a sharp de-crease at the end of August due to clipping and removal ofvegetation to 10 cm above the ground surface. Subsequentre-growth after clipping resulted in an increase of canopygreenness during October (Fig. 1b, Verburg et al., 2005;Arnone et al., in press).

As a part of the interannual climate variability experiment,air temperature in two of the four mesocosms was raised by4 °C in the second year of the study (11 February 2003–10February 2004) (Verburg et al., 2005). During the treatmentyear, soil temperature at 7.5 cm depth averaged 2.3 °C higherin the two heated mesocosms, and soil water content waslower compared to the two control mesocosms (minimumsummertimemoisture ca. 17% compared to 21% in the controlmesocosms). Details on the effects of warming treatment on

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Fig. 1 –Environmental parameters in control mesocosms: a. Average weekly air temperature, soil temperature at the top 1 cm,and % soil water content at the 7.5 cm depth, and b. canopy greenness and monthly averages calculated for ƒ=1−% canopygreenness/100.

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the net primary productivity, soil CO2 efflux, canopy develop-ment and other ecosystem responses are available elsewhere(Verburg et al., 2005; Arnone et al., in press).

2.2. Total Hg in plant tissue, soil and water

Collection of most plant and soil samples for Hg analyses waslimited to those times when these materials were beingcollected for the larger scale experiment. Bulk plant tissue forthe mass balance estimate was collected at the harvest at theendofAugust (2002–2004). Surface soils (top 1 cm)were sampledtwice a year from all monoliths and soil and root samples wereobtained from cores of eachmonolith (n=12) collected inwinterand summer of 2003 (soil only) and 2004. Individual forb (broadleaf herbaceous plant) and grass foliage samples were collectedfromeachmesocosmduring thegrowingseason, andduring thefall re-growth period following harvest.

Soil samples and plant tissues (rinsed in Millipore® ultraclean water) were placed in clean vials, lyophilized for 48 h,

and stored at −20 °C until analysis. Rinsing of plant tissue wasdone to remove dust allowing for assessment of leaf concen-trations only (c.f. Ericksen et al., 2003; Millhollen et al., 2006).Samples were analyzed for total Hg content using a MilestoneDMA 80 (EPA method 7473). Measurement errors for certifiedreference materials (apple leaves NIST 1515, peach leavesNIST 1547, and San Joaquin Soil NIST 2709) were b5%, whileaverage coefficients of variation of soil samples analyzed intriplicate were 7.5±3.1% (n=22 triplicates), and 9.0±4.5% forplant tissues (n=14).

Water was added to the monoliths by a ceiling mountedsystem developed to simulate precipitation. Water sampleswere collected from this system bimonthly for total Hganalysis. After bromine monochloride oxidation, and stan-nous chloride reduction, Hg from the solution was purgedonto gold-coated sand traps, and quantified using dualamalgamation and cold vapor atomic fluorescence spectro-metry (Bloom and Fitzgerald, 1988). Based on the average totalHg concentration in the water 3.3±0.4 ng L−1 (n=21), and the

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880 mm H2O m−2 applied annually, the total amount of Hginput by way of watering in EcoCELLs was 2.9 μg Hgm−2 year−1

(29 mg ha−1 year−1).

2.3. Hg flux measurements in the mesocosms

For this project two dynamic flux chambers (c.f. Engle et al.,2001; Millhollen et al., 2006) constructed of clear polycarbonatewere applied. In both cases the inlet air was sampled in themesocosm adjacent to the inlet air ports and the outlet air wasthat pulled from the top of the chamber. One chamber, calledthe “tall chamber” (volume=11 L, h=60 cm, d=15 cm, turnover time=1.6 to 5.5 min) was used to measure Hg flux fromplant shoots, the bare soil during the footprint measurement(see below), and from the whole plant–litter–soil system. Dielfluxes were obtained for individual forbs (n=22, species fromthe genera Lactuca, Cirsium, Ambrosia, Erigeron, Rudbeckia) andgrasses (n=20, Andropogon and Sorghastrum) in spring andsummer of 2004 and 2005. Plant fluxes were measured byplacing the chamber over the plant shoots, and sealing thechamber base around the stem using two semi-circular platesand Teflon tape (Millhollen et al., 2006). Measured fluxes werenormalized by the total one-sided leaf area (m2) enclosed inthe flux chamber (leaf flux).

A smaller volume chamber (volume=1.4 L, h=13 cm,d=12 cm, turn over time=1 min) referred to as the “shortchamber” was used to measure flux from an area establishedon each monolith defined by a polycarbonate ring thatremained litter- and plant-free for the whole experiment,and from adjacent areas of litter-covered soil. Bare soil fluxeswere measured for 24 h on each monolith (n=12) bimonthlyfrom 2003 to 2005. Fluxes from litter-covered soil weremeasured in January 2004 and February 2005.

The overall tallgrass prairie Hg exchange (footprint flux)was measured in May 2005 by placing the tall chamber overplants and litter-covered soil, and in the winter by usingthe smaller chamber placed on litter-covered soil. Footprintflux was calculated using the monolith area covered by thebase of the chamber following the standard method forreporting a whole ecosystem flux, that is, flux per groundsurface area. To understand the relative contribution of theindividual components to the overall system flux, measure-ments were made sequentially from the whole plant–litter–soil system and individual plants and bare soil using the tallchamber.

To compare the data collected from the two differentchambers, the tall and short chambers were used to quantifyHg exchange from the same bare soil location and fluxes werecomparable (flux range 3.61 to 4.84 ng m−2 h−1, and 3.17 to5.90 ng m−2 h−1, respectively). In addition, tests have shownthat for low Hg soils similar fluxes will be obtained fromchamberswith turnover times ranging from 0.5 to 5min. Shortand tall chamber blanks were determined between eachmeasurement using a clean polycarbonate lid as the chamberbase, and were 0.02±0.04 ng m−2 h−1 (n=1105) and −0.01±0.02 ng m−2 h−1 (n=204), respectively. Blank fluxes for bothchambers were not different from zero (one sample t-testp=0.690 and p=0.536, respectively).

Air Hg concentrations for flux measurements were quanti-fied using a Tekran® cold vapor atomic fluorescence spectro-

meter (Model 2537A, Tekran Instruments), thought to quantifytotal gaseous Hg (Temme et al., 2003). The air was sampled atthe flow rate of 1.4 L min−1 (2.5-minute sampling interval withdetection limit of b0.1 ng m−3, Tekran, 1999), and a Tekran®Automated Dual Sampling System allowed sampling of air atthe chamber inlet ports and air evacuated from the chamberevery 5min to achieve a 10-minute flux resolution. Particulatematter was removed by a Teflon® filter (0.2 μm pore size) atthe beginning of the sampling lines. All tubing and connec-tions were made of Teflon® and were acid cleaned andchecked for contamination. The analytical quality controlconsisted of automated daily calibrations in Hg-free air, andmanual injections air from a controlled temperature saturatedmercury vapor source into ambient air between bimonthlymeasurements of soil flux. When recoveries dropped below90%, the gold cartridges inside Tekran 2537A were cleaned orreplaced to achieve efficiency of 95% or better.

2.4. Measurements at the field site

Plant shoot tissue and surface soil sampleswere collected, andHgexchange sequentiallymeasured for bare soils, plant shootsand the plant–soil–litter system in the field at experimentalplots replicating the monoliths at the Kessler Farm FieldLaboratory in Oklahoma (described by Zhou et al., 2006) in June2005. Bare soil fluxes weremeasured using the short chamber,while plant shoots and whole system exchange were quanti-fiedusing the tall chamber. Soilmoisture (expressed aspercentdry soil on a mass basis) was gravimetrically determined: theaverage soil moisture was 5±2%, and increased to 25±1% aftera rain event.

2.5. Data analysis

The database used for statistical analyses consisted ofindividual Hg flux measurements paired with the environ-mental conditions measured concurrently in the correspond-ing mesocosm and monolith. Six flux measurements wereaveraged to calculate hourly fluxes. Hourly fluxes wereaveraged to obtain daily means, and the daily means for allyears were used to calculate monthly values. Correlationcoefficients developed between fluxes of different resolution(hourly, daily, and monthly) and spanning different timeperiods (days, months, years) with environmental parametersaveraged on the same time step were assessed to evaluatehow data resolution and temporal extent affected modeledrelationships.

All data analyses were completed using Stata® StatisticalSoftware (Release 6.0 for Windows, StataCorp, College Station,Texas) and MINITAB® Statistical Software (Release 13.32 forWindows, State College, Pennsylvania). Results were consid-ered significant at pb0.05.

3. Results and discussion

3.1. Hg content in soil and plants

Soil Hg concentration of the monoliths decreased withdepth, from 16±3 ng g−1 in the top 1 cm to b4 ng g−1 in layers

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Table 1 – Soil Hg concentrations (mean±SE), % soil organiccarbon, soil bulkdensity, rootHgconcentrations (dryweight),and estimated soil pools at different depths averaged overthe whole study period

Depth(cm)

Soil Hg(ng g−1)

Root Hg(ng g−1)

%organiccarbona

Soil bulkdensity(g cm−3)a

Hg storagein layer(g ha−1)

0–15 12.0±0.9 38.5±6.4 0.85±0.12 1.22 22±215–30 10.2±1.1 27.3±6.0 0.67±0.10 1.27 19±230–60 6.9±0.7 8.7±4.0 0.52±0.06 1.35 28±360–90 4.8±0.6 8.9±3.2 0.38±0.10 1.53 22±290–120 3.8±0.3 12.0±8.7 b0.1 1.72 20±1120–150 3.6±0.4 12.5±3.6 b0.1 1.76 19±1Totalstorageb

130±3

aUnpublished data, P. Verburg.bCalculated soil pool per hectare down to 150 cm depth.

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deeper than 90 cm (Table 1) and did not change from year toyear. Average soil Hg concentrations for individual depthswere correlated with organic carbon concentrations (soil Hg(ng g−1)=16×% organic carbon−1.2, r2=0.98). Root Hg concen-trations followed the general depth profile observed for soilHg, but were approximately three times higher (Table 1). Therewere no differences in Hg concentrations of soil, roots andfoliage (described below) between mesocosms.

At the end of growing season, forb foliage contained 28±9 ng Hg g−1 dry weight, while grasses contained 5±2 ng Hg g−1

(Fig. 2). The concentration increase in forb foliage during thegrowing season was estimated at 0.2 ng g−1 Hg day−1 (linearregression slope, pb0.001, Fig. 2), while the accumulation of Hgin the sampled grass tissues during the growing season wasnot statistically significant (p=0.170, Fig. 2). The concentrationincrease rates and allometric relationships betweenmass and

Fig. 2 –Median tissueHg concentration in forb and grass leaves ovfor forbs). Accumulation rates (units of ng Hg g−1 day−1) for Mayindividual tissue samples collected 2002–2004 (represented by crmeasured in foliage from September to October represent that in

leaf area (forbs: 140 cm2 g−1 dry mass and grasses: 120 cm2 g−1)were used to calculate Hg accumulation rates normalized byleaf area. Hg accumulation in forb tissues in the spring andsummerwas 14 ngm−2 day−1 (equivalent to 0.6 ngm−2 h−1). Nochange was detected in grass tissue Hg concentration over thegrowing season. The lack of increase in grass leaf concentra-tions over time may reflect the fact that grass shoots weresampled at the terminus each sampling period and sincegrass grows from the base this material represented the oldesttissue.

Hg contents of soil and tissues inmesocosmswere similar tothat measured in samples collected in June 2005 at the KesslerFarm in Oklahoma. Average soil Hg concentration in the top1 cm was 15±4 ng g−1, and concentrations in foliar tissuescollected in exhibited a general trend of higher Hg content inforbs (12±3 ng Hg g−1) than in grasses (3±1 ng Hg g−1).

3.2. Leaf–air Hg exchange

All reported fluxes represent net flux associated with a surfacebecause deposition, emission and re-emission of Hg may all becontributing to the total exchange measured with dynamicchambers (Millhollen et al., 2006; Graydon et al., 2006; Gustinet al., 2006). Daily averaged foliar Hg exchange rates betweentallgrass prairie plants and the atmosphere rangedfrom −3.31 ng m−2 h−1 to 0.45 ng m−2 h−1 (negative flux re-presents deposition, positive flux is emission, Fig. 3). Overall,there was no net Hg flux associated with grasses (meanflux −0.03±0.02 ng m−2 h−1, one sample t-test p=0.121), whilethere was a significant daily net deposition to forbs (overallmean flux −0.51±0.06 ng m−2 h−1, one sample t-test pb0.001).

Dynamic flux measurements indicated that deposition toforb shoots typically followed a diel pattern with a maximumdeposition at midday (typical exchange is shown in Fig. 3a),increasing with air temperature (r=−0.77, pb0.001), and solarirradiance (r=−0.54, p=0.006). Forb Hg uptake was notcorrelated with the air Hg concentration (Pearson r=−0.05,p=0.748).

er time (error bars represent interquartile range, and are b0.02to August were estimated with linear regressions usingosses and open circles) and time. Mercury concentrationsnewmaterial sprouting after the harvest at the end of August.

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Fig. 3 –Representative foliar Hg exchange rates measured from tallgrass prairie plants inside EcoCELLs: hourly averaged Hgexchange (average daily flux ± SD in ng m−2 h−1 are inserted in each panel) from a. one forb (June 2004), and b. one grass(July 2004), c. daily averaged ± SD exchange rates measured in 2004 and 2005 (each symbol represents one plant).

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3.3. Bare soil–air Hg exchange

Net Hg deposition to bare soils was observed in wintermonths, while emission was the dominant flux during othertimes of the year (Fig. 4, Table 2). Annual variability in bare soilHg fluxes was consistent between months of different years(Fig. 4). The seasonal pattern in bare soil Hg flux resembled the

Fig. 4 –Bare soil Hg exchange rates measured from tallgrass praiaverage exchange rate (± SE) calculated using all 24-hour diel mesampling campaign. The region delimited by dashed lines shows

pattern observed for percent canopy greenness (Fig. 1), that is,it increased and peaked in the summer and then increasedagain in October during canopy re-growth (compare Figs. 1and 4). Fluxes from bare soil also exhibited diel variability,with daytime (8:00–16:00 h) Hg exchanges typically beingsignificantly higher than those measured during the night-time (20:00–04:00 h) periods (Table 2, Fig. 5).

rie monoliths inside EcoCELLs. Filled circles represent theasurements taken on each (approximately) bimonthlyone standard deviation around the compositemonthlymean.

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Table 2 – Monthly composite Hg exchange rates (ng m−2 h−1) for 24 h (diel), and daytime (8:00 to 16:00 h) and nighttimeperiods separately based on measurements from bare soil from 2003 to 2005 at the same location for each monolith (n=12)

Month N Diel Hg flux SE Daytime Hg flux SE Nighttime Hg flux SE p Air Hg

January 23 −0.44 0.17 −0.37 0.19 −0.49 0.18 0.220 2.67February 27 0.11 0.11 0.22 0.13 −0.14 0.12 0.006 2.49March 25 0.90 0.15 1.25 0.22 0.59 0.13 b0.001 2.14April 14 2.00 0.43 2.76 0.58 1.04 0.44 0.002 2.40May 33 3.92 0.58 4.05 0.60 3.92 0.84 0.101 2.63June 16 3.75 0.69 4.64 0.80 2.55 0.43 b0.001 4.43July 3 4.29 1.64 4.61 1.89 3.50 1.20 0.386 1.34August 19 1.46 0.23 1.84 0.26 0.97 0.29 0.008 3.27September 15 0.62 0.08 0.66 0.08 0.63 0.15 0.901 5.86October 7 1.49 0.32 1.92 0.42 1.18 0.25 0.028 1.68November 11 −0.46 0.10 −0.43 0.09 −0.56 0.12 0.054 2.44December 28 −0.83 0.17 −0.63 0.16 −0.94 0.20 0.015 2.74

Average diel Hg exchange rates significantly different from zero are in bold, and p-values for paired t-test comparing daytime and nighttimeexchange rates are given. Last column shows average air Hg concentrations (ng m−3) measured at the chamber inlet port.N = number of days in each month when Hg flux was measured.

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In June 2005, bare soil flux was measured at the field site inOklahoma where soils were initially very dry (5% soilmoisture), and low emission of Hg (0.11±0.33 ng m−2 h−1,significantly different from the chamber blank, one sample t-test pb0.001), was measured. However, after a rain event Hgemissions measured from bare soil (25% soil moisture)increased substantially (9.09±2.31 ng m−2 h−1 at 11–13 h),and calculated average diel Hg flux of 5±3 ng m−2 h−1

(estimated using the method of Engle et al., 2001) for the wetsoil was comparable to Hg flux measured inside EcoCELLs(where soils were always wet) in June (Fig. 4).

The correlations between hourly flux and environmentalconditions were not consistent from month to month (Fig. 6)illustrating that relationships between environmental para-meters and flux developed for one period of time may not be

Fig. 5 –Hourly averaged bare soil Hg flux and solar irradiance (phconsecutive days in April 2005, average daily air temperature waand coefficient of determination for simple linear regression betw(midnight to midnight) are inserted in the graph.

used to predict flux for all times of the year. Additionally thissuggests that not one individual parameter may be ideal formodeling flux over time due to interactions between para-meters controlling soil Hg flux. For example, bare soil Hg fluxwas negatively correlatedwith soil moisture at 7.5 cm depth inMay, when it was warm and soil water content was greaterthan 25% (r=−0.41, pb0.001), while the correlation becamepositive in June and July, when soil moisture decreased below25% (r=0.56, pb0.001). In October when soil moisture wasagain N25%, Hg flux was again negatively correlated with soilmoisture (r=−0.61, pb0.001).

The relationships between soil Hg flux and environmentalparameters were affected when the resolution of the dataapplied was changed, with correlations using all data overseasons improving when coarser temporal resolution

oton flux density) measured from the same location on twos 21 °C, and soil moisture at 7.5 cm depth was 29%. Equationeen soil Hg flux and solar irradiance for each 24-hour period

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Fig. 6 –Pearson correlation coefficients calculated between bare soil Hg flux (hourly resolution) and environmental parametersin different intervals considered. Only statistically significant (pb0.005) correlations are shown. ‘ALL’ represents correlationscalculated using all data, and is identical to first row in Table 3. Note: Direct comparison of relationships derived for differentmonths is not straightforward, as data were available for different number of days in each month (see Table 2).

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(monthly average instead of daily or hourly) was used(Table 3). Across all data resolutions, air temperature bestexplained averaged soil Hg exchange rates (Table 3), account-ing for ~1/3 of the variability when daily resolution was used(r2=0.34, pb0.001). Adding ambient air Hg concentrationimproved the regression coefficient and resulted in the follow-ing equation for daily Hg flux from bare soil (r2=0.43, pb0.001):

Bare soil f lux ¼ 0:14� air temperature� 0:53� air Hg concentrationþ 0:35

Addition of other variables did not significantly improvethe regression model.

Comparison of hourly averaged Hg fluxes measured frombare soil inheatedand controlmesocosmsduring the treatmentyear indicated therewasnoeffect of this temperaturedifference(4 °C) on bare soil Hg flux. In order to do this analysismonth andtime of day were used as covariates to account for seasonal and

Table 3 – Correlation coefficients (r, associated p-valuein parenthesis) between Hg flux from bare soil and airtemperature (Air T), soil temperature at the top 1 cm (Soil T),soil water content at the 7.5 cm depth (% swc), air Hgconcentration at the flux chamber inlet (Inlet Hg) and solarirradiance (Light) measured inside EcoCELLs during Hg fluxsampling

Resolution Air T Soil T % swc Inlet Hg Light

Hourlya 0.510(b0.001)

0.489(b0.001)

−0.017(0.338)

−0.152(b0.001)

0.340(b0.001)n=5137

Daily 0.584(b0.001)

0.540(b0.001)

−0.031(0.678)

−0.177(0.030)

0.414(b0.001)n=218

Monthly 0.807(0.002)

0.753(0.005)

−0.376(0.229)

−0.290(0.387)

0.845(0.001)n=22

Correlationswere calculated for data of different resolution (see text).a Data in this row are identical to category ‘ALL’ in Fig. 6.

diel variability (ANCOVA, p=0.152). Although correlation analy-sis showed a positive association between temperature and soilHg fluxes (Table 3), it is possible that potential stimulation of Hgemissiondue to increased temperature in thewarmedEcoCELLswas countered by a concurrent decrease in soil moisture inwarmed mesocosms (cf. Verburg et al., 2005), resulting in nomeasurable effect on the net Hg exchange from bare soils.

Changing the time span (extent) of the regression modelaffected both the relationship between soil Hg flux andenvironmental parameters, and the amount of variabilitythat could be explained (r2). For instance, solar irradiancecould account for more than 90% of hourly Hg flux variabilitymeasured during one day, but the relationship changed thefollowing day, even though average air temperature and soilmoisture were essentially unchanged (Fig. 5). As the temporalextent of the model was broadened with inclusion of moredata (i.e. applying the same resolution (hourly average) data,but over a longer time period), the coefficient of determinationand the slope decreased further, and the same was true for allexamined environmental parameters (data not shown).

3.4. Overall tallgrass prairie (footprint) Hg exchange

Daily averaged exchange rates measured using a chambersituated over plants and litter-covered soil in the summer andlitter-covered soil in the winter (footprint flux) rangedfrom −1.99 to 2.35 ng m−2 h−1 (Fig. 7) and in contrast withfluxes from bare soils or plant shoots, footprint exchange didnot exhibit diel variability, nor were there any correlationswith environmental parameters. In May, average daytime(8:00–16:00 h) footprint Hg fluxes exhibited low emissions(0.52–1.23 ng m−2 h−1) or deposition (−0.77 ng m−2 h−1), whilefluxes measured from adjacent bare soil ranged from 3.61 to4.84 ng m−2 h−1 (Fig. 8a). The magnitude of the footprint fluxwas similar to that reported for litter-covered soil surfaces atforested sites surveyed throughout the year (overall averagedaytime flux 0.2±0.9 ng Hgm−2 h−1, Kuiken et al., 2008), and to

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Fig. 7 –Overall tallgrass prairie Hg exchange (footprint fluxes) quantified in winter 2004 and 2005 (soil+litter), and spring 2005(soil+litter+plants) for monoliths housed in EcoCELLs.

235S C I E N C E O F T H E T O T A L E N V I R O N M E N T 4 0 6 ( 2 0 0 8 ) 2 2 7 – 2 3 8

measurements made in late fall over a stubble-covered field(average flux 0.1±0.2 ng Hg m−2 h−1, Cobbett and Van Heyst,2007). The footprint Hg flux measured from dry and wetsoils in the field was the same suggesting that response of Hgflux from litter and plant covered surfaces to changes in soilmoisture may not be as fast and dramatic for vegetated

Fig. 8 –Average (± SD) daytime (8–16 h) Hg fluxes measured fromflux adjusted for canopy greenness ((1−% greenness/100)×(bare100)×(bare soil flux)+(leaf flux×LAI)): a. inside EcoCELLs in Mayand after precipitation.

systems as is the case for bare soils (Fig. 8b). The lack ofsignificant relationships between the footprint flux andenvironmental parameters may reflect the fact that Hg fluxesfrombare soil and foliage are affected by the sameparameters,but sometimes in the opposite direction (e.g. compare Figs. 3aand 5). In addition to direct contribution of foliar Hg exchange

bare soil, plant shoot, and footprint on consecutive days, soilsoil flux)), and the calculated footprint flux ((1−% greenness/2005, and b. at the field site in Oklahoma in June 2005 before

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Fig. 9 –Tallgrass prairie Hgbudget. Soil, root, and abovegroundvegetation pools were estimated using Hg concentrationsmeasured in different soil horizons, root tissue, bulk leafsamples collected at the end of growing season, and respectivemass of each compartment. Input via precipitation wascalculated based onmean Hg concentration in irrigationwaterand volume applied. Emission from litter-and-plant coveredsoil is modeled asmeasured bare soil Hg fluxes adjusted for %canopy greenness (see text and Fig. 8). Note that soil flux andfoliar uptake take into account dry deposition.

236 S C I E N C E O F T H E T O T A L E N V I R O N M E N T 4 0 6 ( 2 0 0 8 ) 2 2 7 – 2 3 8

to the footprint flux, plant and litter cover have been shown toattenuate the bare soil exchange (Zhang et al., 2001; Gustinet al., 2004).

Wintertime footprint fluxes measured when dry plantstubble and leaf litter covered the soil were approximatelyequal to the bare soil exchange (−0.44 ng m−2 h−1, and −0.31±0.25 ng m−2 h−1, respectively for n=11 days in January; 0.16±0.10ngm−2 h−1, and 0.11ngm−2 h−1, respectively forn=7days inFebruary).

Comparison of footprint flux and exchange rates fromadjacent bare soils and plant shoots (if present) measured onconsecutive days revealed that bare soil and plant Hg exchangecould not be summed directly to explain the overall ecosystem-level fluxwhen plant canopywas present (Fig. 8). In addition, asdescribed above, the difference between footprint flux and baresoil flux varied over the course of the year.

Increased bare soil Hg emission rates in October duringvegetation re-growth after the harvest co-occurred withincreases in soil carbon dioxide (CO2) efflux (a measure ofplant root and microbial respiration) and canopy greenness(Verburg et al., 2005). Because of the similar trend betweenbare soil flux and canopy greenness (an index of plantphenology, Verburg et al., 2005) we hypothesized that this ora related parameter, measured at the ecosystem level, couldbe used to adjust the bare soil flux to reflect the footprint fluxas follows:

Footprint f lux ¼ 1�k greenness=100ð Þ � bare soil f luxð Þþ leaf f lux� LAIð Þ:

Fig. 8 shows the results of applying this equation to the soilfluxes measured in May inside mesocosms and in June in thefield by applying greenness reported by Verburg et al. (2005) formesocosms and that visually estimated at 70–90% in the field,respectively, and adding the measured plant flux. Thisresulted in a Hg flux estimate that was similar to the footprintfluxes quantified inmesocosms and the field (Fig. 8). AlthoughHg fluxes measured for this system are very low, this analysisshows that bare soil fluxes and individual plant fluxesmay notbe added to account for the whole ecosystem flux and thatcanopy greenness, a simple parameter, could be used to adjustindividual bare soil flux that can then be applied to estimatethe ecosystem-level Hg exchange.

3.5. Mass balance

Using data obtained for the tallgrass prairie monoliths housedinmesocosmswe developed amass balance for Hg within thistallgrass prairie system using measured inputs and outputsand Hg concentrations of soil and plant tissues. Hg in the soilpool, estimated using soil bulk densities measured in the fieldduring excavation of the monoliths and average soil Hgconcentrations (Table 1) to a depth of 150 cm was 130±3 gHg ha−1. Hg storage in the roots was almost three orders ofmagnitude lower than in soil (about 0.1%, Fig. 9).

Assuming equal presence of grass and forb species, andusing the range of aboveground plant biomass in EcoCELLs of400 to 600 g m−2 at the peak of the growing season (ca. 5 Mgbiomass ha−1, J. Arnone and P. Verburg, unpublished data); theHg uptake by vegetation was estimated at 70 mg ha−1 year−1.

Annual bare soil net Hg flux taking into account emissionand deposition estimated using the monthly averaged Hgexchange rates was ~12 µg Hgm−2 (ca. 120 mg ha−1 year−1). Inorder to estimate the annual gaseous Hg exchange asso-ciated with the tallgrass prairie in this study, we appliedcalculated monthly % canopy greenness to Hg exchangemeasured from bare soil as a rough adjustment for thevegetation and litter cover (similar to footprint calculationsin Fig. 8). The resulting Hg flux of 25 mg ha−1 year−1 thataccounts for emission and dry deposition from litter andplant covered soil was nearly balanced by inputs viaprecipitation (ca. 29 mg Hg ha−1 year−1), and with the uptakeof atmospheric Hg by vegetation, there was a net depositionto the tallgrass prairie (Fig. 9). The largest uncertainties inthe constructed Hg budget are associated with modeledeffects of litter and plant cover on soil Hg emissions using %canopy greenness (the use of this approach requiresfurther validation), and precipitation inputs for reportedwet deposition can be up to 5 times greater than thatoccurring in mesocosms (NADP, 2008).

The tallgrass prairie ecosystem in the mesocosms was anet sink of atmospheric Hg as indicated by the mass balanceestimate. The long term potential for this ecosystem as a sinkis supported by the soil Hg concentration profile that showedhigher Hg storage in the top 30 cm relative to depths below(Table 1). It is thought that Hg concentrations in deeperhorizons reflect the Hg concentration of the parent rockmaterial (Engle et al., 2006). The additional Hg in the topsoilmay have been supplied via wet and dry atmosphericdeposition and input by vegetation, and was subsequentlyretained due to binding with organic matter and internal

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recycling by the roots (Schwesig and Matzner, 2000; Grigal,2003; Millhollen et al., 2006).

4. Conclusions

The above discussion suggests that the relationships for Hgflux with environmental parameters were not fixed over timeand that different parameters were limiting controls underdifferent environmental conditions. Additionally, analysesshowed that relationships depended on the resolution of thedata and model extent, and that correlations were weakerwhen data of fine resolution at broader temporal extent wereused. This is in agreement with theory developed in ecology,suggesting that broad-scale inferences may not be developedthrough direct extrapolation of fine-scale data (cf.Wiens, 1989;King, 1991; Grace et al., 1997; Hobbs, 2003). Relationshipsdeveloped using well resolved data of narrow extent (com-monly collected for Hg exchange) may be useful for under-standing the underlying processes driving Hg flux; however toestimate Hg flux over longer periods of time, coarse-resolutiondata are needed.

Bare soil flux alone is not sufficient to estimateHg exchangefrom vegetated ecosystems and to develop an estimate uptakeby vegetation must be accounted for as must the influence ofthe presence of living vegetation- and litter-covered soils. Inthis paper we showed that canopy greenness for a tallgrassprairie ecosystem may be used to adjust bare soil flux toaccount for the change in flux observed with litter and plantcoverage.

Acknowledgments

This research was funded by the National Science Foundation,with grants from the Division of Atmospheric Sciences(0214765) and the Integrated Research Challenges in Environ-mental Biology Program (DEB 0078325). Thanks to H. Saundersand R. Bergin for assistance with tasks in EcoCELLs, M. Engle,B. Coulombe and R. Zehner for help with equipment, and B.Hanson and B. Sedinger for sample analysis. We are gratefulfor the use of facilities at the Desert Research Institute (Reno,Nevada) and the Kessler Farm Field Laboratory (University ofOklahoma, Norman, Oklahoma). Special thanks to Dr. EdwinKessler for hospitality during the field campaign. We greatlyappreciate the detailed review given this manuscript by threeanonymous reviewers.

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