Application of a Rule-Based Modelto Estimate Mercury Exchange forThree Background Biomes in theContinental United StatesJ E L E N A S . H A R T M A N , †

P E T E R J . W E I S B E R G , † R E K H A P I L L A I , †

J O D Y A . E R I C K S E N , † T O D D K U I K E N , ‡ , ⊥

S T E V E E . L I N D B E R G , § H O N G Z H A N G , ‡

J A M E S J . R Y T U B A , | A N DM A E S . G U S T I N * , †

Department of Natural Resources and Environmental Science,University of Nevada-Reno, 1664 N Virginia Street, MS 370,Reno, Nevada 89557, Tennessee Technical University,Cookeville, Tennessee 38505, Oak Ridge National Laboratory,Oak Ridge, Tennessee 37831, United States Geological Survey,Menlo Park, California 94025, and Woodrow WilsonInternational Center for Scholars

Received January 9, 2009. Revised manuscript receivedApril 24, 2009. Accepted May 6, 2009.

Ecosystems that have low mercury (Hg) concentrations (i.e.,notenrichedor impactedbygeologicoranthropogenicprocesses)cover most of the terrestrial surface area of the earth yettheir role as a net source or sink for atmospheric Hg is uncertain.Here we use empirical data to develop a rule-based modelimplemented within a geographic information system frameworkto estimate the spatial and temporal patterns of Hg flux forsemiarid deserts, grasslands, and deciduous forests representing45% of the continental United States. This exercise providesan indication of whether these ecosystems are a net source orsink for atmospheric Hg as well as a basis for recommendationof data to collect in future field sampling campaigns. Resultsindicated that soil alone was a small net source of atmosphericHg and that emitted Hg could be accounted for based on Hginputbywetdeposition.Whenfoliarassimilationandwetdepositionare added to the area estimate of soil Hg flux these biomesare a sink for atmospheric Hg.

IntroductionGlobal mercury (Hg) models have indicated that atmosphericHg exchanges with terrestrial and ocean surfaces areimportant controls of the atmospheric Hg pool (1-3).However, there are still gaps in our understanding of themagnitude and mechanisms controlling exchange. In par-ticular, the role of ecosystems with low Hg concentrations,not enriched by geologic processes or anthropogenic activity(soil <0.1 µg Hg g-1), as sources or sinks of atmospheric Hgis not well understood (4). It has been estimated that theland surface of the contiguous United States annually releases44-150 Mg of Hg; however, in order to understand the

significance of these emissions, the inputs by way of wet anddry deposition to soil surfaces and the uptake by foliage needto be considered (5).

The uncertainty associated with estimates of Hg exchangebetween air and vegetated landscapes arises from complexi-ties in both atmosphere-soil and atmosphere-plant Hgexchange. Soil Hg flux is influenced by multiple interactingfactors, including Hg concentration and speciation in thesoil, light, temperature, soil moisture, wind speed andturbulence, and atmospheric oxidants (6-11). In addition tospecies-specific foliar exchange (12, 13), the presence of plantsand litter may also impact the soil-air Hg exchange byaltering the thickness of the boundary layer and air mixing,shading the soil, and influencing soil moisture and tem-perature (14-19).

Spatial Hg flux estimates have been developed withatmosphere-soil and atmosphere-canopy exchange mod-eled as functions of temperature and solar radiation, andtranspiration rates with modifications to account for soil Hgconcentration, vegetation type, or environmental influenceson canopy conductance (20-26). Most of these modelsapplied the assumption that plants are a net source of Hgto the atmosphere, whereas research has shown the plantcanopy to be a net sink of air Hg (19, 27-32).

Herein, an attempt was made to estimate Hg flux fromthree biomes in a parsimonious way applying few assump-tions. Empirical data on net soil Hg flux (accounting for drydeposition and emission) derived using dynamic flux cham-bers and co-occurring environmental conditions were usedto develop a rule-based model of Hg exchange. The rule-based model was implemented within a geographic infor-mation system (GIS) to derive spatially explicit estimates ofHg exchange for each month. Uncertain parameters weresystematically varied to provide ranges of Hg exchangeestimates that are reasonable given explicit model assump-tions. Uptake of atmospheric Hg by way of foliage andprecipitation inputs were considered. The objectives wereto scale air-surface Hg exchange for semiarid desert, grasslandand deciduous forest biomes in the continental United States,assess the spatial and temporal distribution of Hg flux,compare the role of these biomes as sources or sinks ofatmospheric Hg, and identify knowledge limitations that needto be addressed before more complex models can bedeveloped.

Materials and MethodsSoil flux data from three locations were used to representthree biomes of interest: a semiarid desert (33), grassland(19), and a deciduous forest (34) over all seasons (seeSupporting Information (SI) Table S1 for details). All threebiomes had soil concentrations <0.1 µg Hg g-1 and weredistant from anthropogenic point sources. The desert sitelocated in northwestern Nevada was sparsely vegetated andsoil received direct sunlight (33). Grassland Hg flux wasmeasured from intact soil-plant monoliths housed in largeenvironmentally controlled growth chambers (EcologicallyControlled Enclosed Lysimeter Laboratories, in further textEcoCELLs 35, 36), and the field site from which the monolithswere derived in Oklahoma (19). The deciduous forestsampling site was in the Standing Stone State Forest inTennessee, a secondary growth mixed forest and flux wasmeasured from litter-covered soil (34).

At all sites, atmosphere-soil Hg exchange was quantifiedusing dynamic flux chambers, environmental variables weremeasured simultaneously, and data were collected on a

* Corrresponding author phone: (775)784-4203; fax: (775)784-4789; e-mail: mgustin@cabnr.unr.edu.

† University of Nevada-Reno.‡ Tennessee Technical University.§ Oak Ridge National Laboratory.| United States Geological Survey.⊥ Woodrow Wilson International Center for Scholars.

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Published on Web 05/21/2009

seasonal time-step. Measurements using dynamic fluxchambers result in a net soil Hg flux accounting for drydeposition and emission. Positive flux values indicate emis-sion while negative values indicate deposition of Hg fromthe air to the soil. Detailed sampling protocols are given inthe respective references (19, 33, 34).

For the purpose of this modeling exercise, data wereaggregated to daily means of Hg flux and environmentalparameters by averaging 24 hourly data points. When fewerthan 24 hourly data points were available, Hg flux data, solarirradiance, and air temperature were adjusted using a methodthat assumes a Gaussian distribution of these data asdeveloped by Engle et al. (37) and then daily averages werecalculated. The final numbers of days for each biome weredesert n ) 18, grassland n ) 4 field and n ) 158 EcoCELL,and deciduous forest n ) 21.

To estimate soil Hg flux over a year a rule-based modelwas developed using classification and regression tree (CART)analysis (38). CART creates a decision tree where a data setis partitioned into increasingly homogeneous subsets usinga sequence of binary splits (i.e., “branches” or nodes). Ateach node a particular predictor variable and threshold valuefor that variable is selected to split the data, such that within-group variance of the resulting subsets is minimized. Splittingcontinues until nodes are pure (maximal homogeneity) ordata too sparse according to a user-defined threshold forsample size. Generally, a full tree constructed with manysplits is subsequently pruned to a smaller, more parsimonioustree with fewer terminal nodes (“leaves”). Terminal nodesare defined by the mean value of the response variable (inthis case, Hg flux) and by the values of the predictor variablesthat define previous splitting decisions. CART trees based onspatial variables can be readily implemented in a GISframework as a series of “if-then-else” logical statements.CART methods are nonparametric and nonlinear, and havethe advantage of making no assumption about the underlyingrelationships between variables, being able to includecontinuous, categorical variables and variety of distributions,and to use explanatory variables more than once in ahierarchical manner (39, 40). Additionally, CART is robust tooutliers, and treats missing values by using surrogate splits,making it a suitable approach for data sets with dataoriginating from multiple sources, and with mixed sets ofpredictor variables. Within CART a model developed usingspecific data can be modified allowing for rules to be refinedbased on literature data.

CART analysis was performed using the S-Plus 6.2 forWindows (Insightful Corp., Washington) software includingthe RPART library addition (recursive PARTitioning (41)).We used v-fold crossvalidation (as recommended by ref 40)for deriving optimally sized classification trees and validatingthe outcome. Given a nested sequence of best-fitting treesfor each tree size (i.e., number of terminal nodes), data wererandomly divided into 10 subsets. Each subset was removedsequentially, its response predicted using CART models fitto the remaining subsets, and estimated error calculated asthe sum of deviances from a maximum likelihood fit. Thefinal tree size was selected as the one with the smallestestimated error rate.

Based on environmental variables determined to besignificant in CART analysis and those necessary for calcu-lating plant Hg uptake, GIS layers constructed to estimatesoil-air Hg exchange were vegetation cover type, leaf areaindex (LAI), clear sky solar irradiance, average monthlytemperature, and percent soil-water content (%swc) (seeSI). Application of CART-developed flux values based onenvironmental thresholds was implemented using ArcGIS9.2, with the spatial analyst extension. All data were re-projected to Albers NAD83 projection, and resulting gridsresampled to a cell size of 10 × 10 km. GIS models were

constructed using the ModelBuilder application of ArcGIS,and iterated 100 times, each time drawing an outcome fromnormal data distributions defined by mean and standarddeviation of Hg flux in terminal nodes of a classification tree.Sensitivity to threshold value for each decision was conductedby changing those values in steps of (10% of the basethreshold values and examining the effect on monthly andannual Hg flux.

To estimate the uptake of atmospheric Hg by vegetation,a specific leaf area range of 100-150 cm2 g-1 (e.g. refs 42, 43)and the median value for leaf Hg concentrations reported inthe literature of 25 ng g-1 (cf., ref 44) were combined withthe maximum annual value of LAI for any given pixel.

Wet deposition estimates were based on data from theNational Atmospheric Deposition Program Mercury Deposi-tion Network (http://nadp.sws.uiuc.edu/mdn/).

Model sensitivity to two additional assumptions wasassessed. The first assumption was that no net Hg exchangebetween surfaces and the atmosphere occurs at temperaturesat or below freezing (cf., ref 26). The second issue was howusing clear-sky radiation versus light transmitted throughthe canopy affected the Hg exchange estimates in deciduousforests, as the light and Hg flux in this biome was measuredunder the canopy (34). To assess the influence of using clear-sky versus radiation passing through the canopy in deciduousforests on the model output, monthly LAI and a coefficientof attenuation of 0.5 (cf., ref 45) were applied to clear-skyirradiance following the Lambert-Beer’s law (46).

ResultsApplying CART analysis to the empirical data yielded aclassification tree with soil temperature, biome, solar radia-tion, and %swc being important parameters influencing theflux values applied. Soil temperature was the most importantvariable influencing flux and therefore the first split in thedecision tree. Air temperature was used instead of soiltemperature in the GIS model because air and soil temper-atures from field data were correlated (r ) 0.93, p < 0.001,slope ) 1.1), and this was the data layer available. At meandaily air temperature below 12.5 °C, solar irradiance and airtemperatures were the only two variables correlated with Hgflux. Biome type was the major variable correlated with Hgflux during periods when average daily air temperature wasabove 12.5 °C, and %swc was the next significant regressionparameter within the grassland and desert biomes. Terminalnode values for %swc the grassland and forest biomes wereset by the CART analysis, whereas for the desert a decisionwas added to the terminal node with a threshold value setat 2% based on data in the literature (47). The final result wasan eight-leaf tree with the flux values applied given at eachterminal node (Figure 1).

The CART results were then applied in monthly incre-ments (SI Figure S1) within the GIS, resulting in an annualsoil flux of 6760 ( 10 kg Hg (Figure 2A). The greatestcontribution to the total annual Hg soil emission was fromthe grassland (43%, area 1 222 400 km2), followed by 32%from deciduous forest (917 700 km2), and the remaining 25%from the desert biome (1 415 300 km2). For comparison, theupper limit of possible Hg emission associated with soil inthe three biomes in the contiguous U.S., determined usingthe highest Hg exchange rate in the rule-based model (1.1ng m-2 h-1) and applied to all pixels for the entire yearregardless of the rules, was 34 260 kg Hg year -1.

Air-soil Hg exchange exhibited seasonality in all threebiomes (Figure 3). For example, deposition occurred in thesummer to dry soils in the semiarid desert, while emissionoccurred in the winter. In the deciduous forest and grasslandsystems lower soil emission was found in spring and summerrelative to the fall and winter.

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Sensitivity of model output to ( 10% change of thresholdvalues in the CART model showed that the greatest sensitivitywas to the threshold of the first decision (air temperature<12.5 °C), resulting in changes of up to 5.4% in the estimatedannual Hg flux (Table 1). Given the importance of the firstdecision, the threshold was changed to assess the influencea broader range of cutoff values would have on the modeloutcome. Assigning a threshold of 10 and 15 °C at the firstsplit led to the change in annual Hg emission of -11 and+11%, respectively. Changing %swc thresholds led to onlyminor change in model output. A (50% change in thresholdvalues for %swc in desert and grassland resulted in less than3% change in the model output indicating that these chosenvalues were not significantly affecting model results.

If an assumption of no net Hg exchange when soiltemperatures were freezing was applied, the model resultedin reduced annual Hg emission by 23%. The empirical datafor the deciduous forest biome were collected underneaththe canopy. Because of this the impact of the use of clear-skyradiation at the top of the canopy versus light adjusted toaccount for the plant canopy on estimated flux results wastested. Use of the latter was found to reduce annual Hgemission by 11%. The combined effect of frozen soil andcanopy light transmittance on model resulted in an annualsoil Hg emission of almost one-third lower (-31%) than theinitial rule-based model.

Adding a layer within GIS that allowed for estimate of theannual Hg uptake into leaves and subsequent deposition vialitterfall resulted in areas with no uptake, due to lack of plantcoverage, to uptake of 18 µg Hg m-2 in locations with thegreatest LAI (Figure 2B). Total annual uptake for the threebiomes was on the order of 15 Mg. The value used for specificleaf area significantly impacted estimated uptake (i.e.,11 470-17 210 kg Hg for leaf areas of 100 and 150 cm2 g-1,respectively).

Because of data limitations a GIS layer could not bedeveloped for wet deposition for the entire area. Crudelyestimating wet deposition was done by applying a rate of 13

FIGURE 1. The decision tree and scatter plots created in CART and implemented within GIS framework to derive the spatialestimate of Hg flux from desert, grassland and deciduous forest biome soils within the contiguous U.S. The threshold value wherethe decision is split is given at the top of each node. Scaterplotts show Hg flux against variables that were used for the split.Branches lead to the left if the decision rule is true, otherwise the tree branches to the right. Terminal nodes end with the mean (SD of the Hg flux rate applied and the number of days falling into each node.

FIGURE 2. A. Annual soil Hg exchange (negative values aredeposition from the atmosphere, positive values indicateemission from the subrate), and B. Annual Hg uptake(deposition from the atmosphere) by plant canopy in desert,grassland, and deciduous forest in the contiguous UnitedStates.

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µg m-2 y-1 to the forest area, 6 µg m-2 y-1 to the grassland,and 3 µg m-2 y-1 to the semiarid area, resulting in a netdeposition of 12, 7.3, and 4.3 Mg y-1, respectively.

DiscussionThe range of flux rates applied in our model for soils (from-0.5 to 1.1 ng Hg m-2 h-1) are similar to values obtained byother studies in comparable systems (47-51); however, mostof these studies provide a measurement of flux for only oneseason. The conservative range of Hg exchange rates appliedto monthly input data in our rule-based model is likelyrepresentative of average monthly Hg exchange rates, asopposed to more extreme flux events that occur over shortertime periods.

The GIS output using the CART model parametersindicated that the soil alone was a small net source of Hg tothe atmosphere (5.4-6.8 Mg year-1), and when uptake byvegetation was accounted for (11.5-17.2 Mg of Hg), thesebiomes were a net sink of Hg, accounting for removal of ∼4.7to 11.8 Mg Hg from the atmosphere. Estimated annual wetdeposition was on the order of 23 Mg and could account forthe Hg emitted from soil. Overall, our scaling exercise suggeststhat these biomes are a net sink for atmospheric Hg.

The assimilation of atmospheric Hg by foliage is mostlikely an underestimate as conservative value of specific leafarea (42, 43) and foliar Hg concentrations (44) was applied.In addition, Hg is taken up from the atmosphere by otherplant compartments and the amount of Hg in leaves withrespect to the total aboveground plant (tree bark, branchesetc) has been estimated to be 20-30% in forests, and up to80% in herbaceous-dominated areas (44, 52, 53). Mercury inthe plant will be eventually deposited to the soil where itmay be sequestered, mobilized by water, or volatilized backinto the atmosphere. The relative importance of theseprocesses is not known.

Our model result is significantly different than previousmodels of ecosystem Hg flux (cf., refs 20-26). Although thesemodels of Hg air-ecosystem exchange applied a relativelysophisticated approach to estimate canopy conductance asa function of environmental conditions and calculate Hgexchange associated with vegetation (20, 24, 25), the as-sumptions regarding atmosphere-vegetation exchange are

in disagreement with research indicating that plant canopyis a net sink for atmospheric Hg (cf., refs 27-32).

Overall, Hg emission from the three biomes was thegreatest in fall and winter, possibly reflecting increased Hgflux related to increased soil moisture and lack of shadingby the plant canopy (18, 47, 54). Decreased air mixing andshading due to canopy coverage during the growing seasonmayhaveledtoloweremissionsinspringandsummer(14-19).

We adopted a parsimonious modeling approach thatgreatly simplified reality; the precision of predicted Hg fluxis limited by our field data and approach. The modeled surfacearea covers 45% of the contiguous United States and as such,the caveat that we are applying data from small areas collectedunder specific environmental conditions to estimate flux fora large spatial area needs to be considered. However, the lowsoil Hg concentrations and the low fluxes measured acrossthese ecosystems, as well as the comparability of the fluxesapplied with those reported in the literature for similarsystems suggests that use of our limited data to understandthe direction and relative magnitude of air-surface Hgexchange is a reasonable approach.

Our results are also limited in that our empirical databasewas small and average meteorology (air temperature) andgeneralized environmental conditions (clear sky radiation,potential evapotranspiration) were used. Our treatment of%swc was extremely simplified. Precipitation data used inwater balance calculations were based on weather stationdata and thus represented real input, however potentialevapotranspiration rates reflect the maximum potential waterloss, leading to more water loss than would be expected inthe field. Since precipitation has been shown to significantlyinfluence Hg release from soils (33, 47) our simplistic methodfor modeling %swc most likely does not account for thisrelease and is an important limitation. The model also didnot take into account air Hg concentrations or the presenceof atmospheric oxidants, which have been shown to influenceHg flux (11).

The modeling approach allowed for spatially explicitestimation of Hg flux by applying values based on environ-mental thresholds without making complex assumptionsabout underlying processes of atmosphere-surface ex-change. In order to improve or expand the rule-based model,

FIGURE 3. Monthly Hg flux for desert, grassland, and deciduous forest soils, and the sum across the three biomes based on therule-based model.

TABLE 1. Percent Change of Modeled Annual Hg Emission from Desert, Grassland and Deciduous Forest in the Contiguous U.S.Due to ±10% Variation in Decision Threshold Values for the Rule-Based Model

decision variable node 1 air temp node 2 irradiance node 3 air temp node 6 swc desert node 7 swc grassland

threshold value 12.5 °C 150 kWh d-1 2 °C 2% 25%

-10% -5.40% -3.10% +0.02% +0.3% +0.2%+10% +5.2% -1.50% -0.02% -0.30% -0.20%

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more empirical data collected over 24 h and on a seasonaltime-step would be required. Parameters important to collectwhen making field measurements include incident radiation,temperature, and soil moisture. Estimates of Hg flux betweenmodeled biomes and the atmosphere were sensitive tochanges that accounted for exchange from frozen surfaces,light conditions under the canopy, and specific leaf area,indicating the need to collect more data associated with thoseaspects of atmospheric Hg exchange.

AcknowledgmentsThis study was made possible by grants from the NationalScience Foundation, Atmospheric Sciences Division (0214765),theEnvironmentalProtectionAgency(STARgrantR_82980001_0),and funding from United States Geological Survey, the ElectricPower Research Institute, and the Environmental SciencesGraduate Program at University of Nevada, Reno. Opinionspresented herein do not represent views of these agencies.We thank three anonymous reviewers for their thoughtfuland constructive comments.

Supporting Information AvailableDescription of the GIS layers used in modeling; tablecontaining summary description of field sampling sites;figures showing average monthly Hg exchange rates derivedfrom the rule-based model of Hg emission without uptakein plant leaves, and net annual Hg flux (emission and drydeposition including uptake of atmospheric Hg by plants)from desert, grassland, and deciduous forest in the contiguousUnited States. This material is available free of charge via theInternet at http://pubs.acs.org.

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