Investigation of Mercury Exchange between Forest Canopy Vegetation

Johannes Fritsche, Hjalmar Laudon, Staffan Åkerblom, Mats B. Nilsson. Mercury evasion from a boreal peatland shortens the timeline for recovery f...
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Environ. Sci. Technol. 2006, 40, 4680-4688

Investigation of Mercury Exchange between Forest Canopy Vegetation and the Atmosphere Using a New Dynamic Chamber† J E N N I F E R A . G R A Y D O N , * ,‡ V I N C E N T L . ST. LOUIS,‡ STEVE E. LINDBERG,§ HOLGER HINTELMANN,| AND DAVID P. KRABBENHOFT⊥ Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada, T6G 2E9, Oak Ridge National Laboratory, P.O. Box 2008, Oak Ridge, Tennessee 37831-6083, Department of Chemistry, Trent University, 1600 West Bank Drive, Peterborough, Ontario, Canada, K9J 7B8, and U.S. Geological Survey-WRD, 8505 Research Way, Middleton, Wisconsin 53562

This paper presents the design of a dynamic chamber system that allows full transmission of PAR and UV radiation and permits enclosed intact foliage to maintain normal physiological function while Hg(0) flux rates are quantified in the field. Black spruce and jack pine foliage both emitted and absorbed Hg(0), exhibiting compensation points near atmospheric Hg(0) concentrations of ∼2-3 ng m-3. Using enriched stable Hg isotope spikes, patterns of spike Hg(II) retention on foliage were investigated. Hg(0) evasion rates from foliage were simultaneously measured using the chamber to determine if the decline of foliar spike Hg(II) concentrations over time could be explained by the photoreduction and re-emission of spike Hg to the atmosphere. This mass balance approach suggested that spike Hg(0) fluxes alone could not account for the measured decrease in spike Hg(II) on foliage following application, implying that either the chamber underestimates the true photoreduction of Hg(II) to Hg(0) on foliage, or other mechanisms of Hg(II) loss from foliage, such as cuticle weathering, are in effect. The radiation spectrum responsible for the photoreduction of newly deposited Hg(II) on foliage was also investigated. Our spike experiments suggest that some of the Hg(II) in wet deposition retained by the forest canopy may be rapidly photoreduced to Hg(0) and re-emitted back to the atmosphere, while another portion may be retained by foliage at the end of the growing season, with some being deposited in litterfall. This finding has implications for the estimation of Hg dry deposition based on throughfall and litterfall fluxes.

Introduction Numerous studies have shown that the forest canopy contributes significantly to fluxes of monomethylmercury * Corresponding author phone: (780) 492-0900; fax: (780) 4929234; e-mail: [email protected]. † Contribution No.14 of the Mercury Experiment to Assess Atmospheric Loading in Canada and the U. S. (METAALICUS). ‡ University of Alberta. § Oak Ridge National Laboratory. | Trent University. ⊥ U.S. Geological Survey-WRD. 4680

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(MMHg) and total Hg (THg; all forms of Hg in a sample) to watersheds (1-5). For example, St. Louis et al. (6) found that annual fluxes of MMHg and THg in throughfall (wet deposition that passes through the forest canopy) plus litterfall at the Experimental Lakes Area (ELA) in the Boreal ecoregion of northwestern Ontario, Canada, were approximately two and three times greater, respectively, than fluxes of MMHg (0.1 µg m-2) and THg (7 µg m-2) in wet deposition over open areas such as lakes. Almost all the increased flux of Hg under the forest canopy occurred as litterfall, and, as a result, it is important to understand whether litterfall constitutes a new and/or recycled input of Hg to the forest floor (1, 6-7). For litterfall to be considered a new input, the Hg in/on foliage must originate from the atmosphere. For example, atmospheric particulate Hg (pHg) and reactive gaseous Hg (RGM) can be dry deposited to foliar surfaces (8) and atmospheric Hg(0) can be assimilated into foliage through stomata (9-11). In addition to the uptake of new Hg(0) from the atmosphere, Hg(0) released from soils below the canopy through volatilization could also be taken up via stomata, resulting in Hg being recycled within the forest. Plants may also accumulate Hg from soil waters by root uptake and translocation to foliage (12), although previous studies have shown that there is generally little accumulation by foliage via this pathway except in areas where soil Hg content is high (9). Plant foliage also provides an excellent surface for photochemical reduction of newly deposited Hg(II) remaining in the forest canopy following precipitation events, affecting net deposition of Hg(II) to the forest floor (13). Both micrometeorological and chamber techniques have been used to measure exchange of Hg(0) at the biosphere/ atmosphere interface, but most previous studies have been conducted in areas either naturally enriched or anthropogenically contaminated with Hg (14-16). Unlike micrometeorological techniques, chamber methods utilize small plot sizes, making it possible to compare responses of enclosed vegetation to experimental treatments (17). However, the microclimate of vegetation enclosed in chambers is invariably altered from natural conditions, with the degree of alteration depending on the design of the chamber (18). Dynamic chambers, where there is a net flow of air through the chamber, are the most common design used to quantify gas exchange. Several studies have shown that low air turnover rate in dynamic chambers can result in artificially large boundary layers being established on soil/foliar surfaces, resulting in underestimates of true Hg(0) emissions (e.g., 19). Furthermore, since there is evidence that a significant amount of foliar Hg(0) exchange occurs via stomata (2, 8, 10), it is also critical that chamber designs do not interfere with normal physiological responses (e.g., photosynthesis and transpiration) of enclosed foliage. Materials used in the construction of chambers can also have a profound influence on the effectiveness of the system to measure gas exchange (18, 20). This is especially true for chambers designed to measure Hg(0) exchange, because in addition to acting as a potential source of Hg(0) contamination, some chamber materials may also adsorb/absorb Hg(0), or block spectral wavelengths such as ultraviolet (UV) radiation important for the photochemical reduction of Hg(II) to Hg(0) (21). Here, we present the design of a new dynamic chamber system that allows both full spectrum radiation transmission and enclosed foliage to maintain normal physiological function while Hg(0) flux rates are quantified. Using this Hg(0) flux chamber in conjunction with isotopically enriched Hg(II) spikes, we examined the following: (1) ambient Hg(0) exchange with foliage over a small natural range of atmo10.1021/es0604616 CCC: $33.50

 2006 American Chemical Society Published on Web 07/04/2006

FIGURE 1. Schematic of the dynamic Hg(0) flux chamber in use on a jack pine branch in the field. spheric Hg(0) concentrations, (2) the pattern of spike Hg(II) retention on foliar surfaces, (3) spike re-emission rates (as Hg(0)) from foliage, and (4) the radiation spectrum responsible for the photoreduction of newly deposited spike Hg(II) on foliage.

Materials and Methods Field Site Description. All field tests of our dynamic chamber and foliar flux measurements were conducted in the upland portion of the Lake 302 (L302) watershed and in the upland and wetland areas of the Lake 658 (L658) watershed at the ELA. This area of the Boreal ecoregion is underlain by Precambrian Shield geology with upland forests dominated by stands of jack pine (Pinus banksiana), black spruce (Picea mariana), balsam fir (Abies balsamea), and white birch (Betula papyrifera) of varying age due to past forest fires. Wetland regions typically contain mixed black spruce, jack pine, and tamarack (Larix laricina) canopies with alder (Alnus rugosa) shrub understory. Measurements within the L658 watershed were conducted as part of the Mercury Experiment To Assess Atmospheric Loading in Canada and the U.S. (METAALICUS), a whole ecosystem Hg loading experiment to examine the relationship between atmospheric inputs of Hg and the rate of MMHg bioaccumulation in fish. The experimental approach of METAALICUS involved applying different enriched stable Hg isotope solutions to each of the lake surface (202Hg(II)), upland (200Hg(II)), and wetland (198Hg(II)) portions of the watershed to also assess how route of entry into the system affects Hg accumulation in fish. Chamber Design. The dynamic chamber used in this study to measure Hg(0) fluxes from living vegetation consisted of an inflatable heat-sealed bag (approximately 10 L volume)

made of polyvinylidene chloride-coated polypropylene film (Propafilm-C; 31.75 µm thickness) (Figure 1). Propafilm-C has been used previously in photosynthetic measurement chambers due to its high radiation transmission (Figure S1, Supporting Information), high percent thermal transmission, and low permeability to carbon dioxide (CO2) and water (18). Inlet and outlet tubing attachments were Teflon straight compression fittings mounted into threaded holes in a flat, oval piece of 6.4 mm thick Teflon sheeting. A plastic DC brushless computer fan (0.75 m3 min-1) for mixing the air within the chamber was mounted on the Teflon sheet using nylon screws. The chamber film was then sealed around the oval Teflon sheet using a large O-ring that stretched tightly into the grooved edge of the sheet. Air was pumped into the chamber through 6.35 mm o.d. Teflon tubing with two Brailsford DC TD-4X2NA brushless pumps (Figure 1). Airflow through the system was maintained at approximately 10 L min-1. Total airflow into the chamber was measured by a GFM17S Aalborg stainless steel thermal mass flow meter (0-30 L min-1 capacity, 0.1 L min-1 precision) at the chamber inlet. Temperatures inside and outside the chamber, measured with T-type Teflon-coated thermocouples attached to a Campbell Scientific CR10X datalogger, were not significantly different (unpublished data). The foliage under study was placed inside the chamber, and the bag was tightened around the branch using cable ties. Small Brailsford TD-2NA vacuum pumps sub-sampled inlet and outlet lines between 0.7 and 1 L min-1 through gold-coated glass bead traps (gold traps) that stripped Hg(0) completely from the air. This arrangement ensured that Hg(0) was not stripped from the air entering the chamber, which would have resulted in an artificially low Hg(0) concentration in the air surrounding the foliage. VOL. 40, NO. 15, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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Aalborg GFM17 thermal mass flow meters (0-5 L min-1 capacity, 0.01 L min-1 precision) and TOT10 totalizers measured total air flow through the gold traps. Soda lime traps (8-14 mesh, Alfa Aesar) were used in-line upstream of the gold traps to remove humidity from the sub-sampled air, as done when bubbling Hg(0) from water samples (U.S. EPA method 1631). Hg(0) Flux Rate Calculations. Direction and rate of ambient and spike Hg(0) fluxes (F; ng g-1 h-1 or ng m-2 h-1) from foliage enclosed in the dynamic chamber were calculated using the following equation:

F)

(Hg(0)o/βo - Hg(0)i/βi) × fm W

(1)

where Hg(0)o ) total ambient or spike Hg(0) on the outlet gold trap (ng); βo ) total air flow through the outlet gold trap (L); Hg(0)i ) total ambient or spike Hg(0) on the inlet gold trap (ng); βi ) total air flow through the inlet gold trap (L); fm ) volume of air exiting the chamber (L hr-1); and W ) freeze-dried weight of foliage and branch inside chamber (g) or total leaf area (m2) of foliage inside chamber. Effects of the Chamber on Plant Photosynthesis and Transpiration. Since factors that alter CO2 assimilation also affect stomatal opening and Hg(0) exchange (8), we tested the dynamic chamber in the laboratory to determine if it affected normal apparent photosynthesis (APS) and transpiration (E) responses of enclosed vegetation. Photosynthetic and transpiration radiation response curves were generated for a loblolly pine (Pinus taeda) by moving a 250 W H5/H37 Hg vapor lamp incrementally closer to the tree. Concentrations of CO2 and H2O entering and exiting the Hg(0) flux chamber were logged by an ADC 2250 infrared gas analyzer (IRGA) every 10 s at each radiation level until the CO2 concentrations leveled off and remained steady for several minutes. Photosynthetically active radiation (PAR) was measured using a LI-COR 190-SA quantum sensor and logged by the IRGA. Steady-state rates of APS and E were calculated using the equations presented in Field et al. (22). An ADC conifer cuvette and LCA-2 portable photosynthesis system was simultaneously attached to the loblolly pine for direct comparison of APS to that measured within our dynamic Hg(0) flux chamber. For the portable ADC system, PAR was measured using a LI-COR sensor and radiation meter, and ∆[CO2] and PAR measurements were made once at each radiation level at steady state. Following the run, enclosed foliage was collected to determine single-sided leaf area using a computer scanner and SigmaScan digital imaging software. Single-sided leaf area was doubled as an estimate of total leaf area. Quality Control. Efficiency of new gold traps used in this study was verified in the lab using a Hg vapor standard. Immediately prior to use in the field, residual Hg was thermally desorbed from gold traps, which were then sealed using Teflon plugs and Teflon tape, and individually bagged. After use, gold traps were again plugged, Teflon taped, and bagged. Gold traps that were not analyzed within a few hours were sealed in acid-cleaned glass mason jars purged with ultrahigh purity N2 and kept under positive N2 pressure to prevent scrubbing of atmospheric Hg(0) during transport. Ambient Hg on travel blank traps was insignificant compared to levels on sample traps and no enriched isotope was ever detected on a travel blank trap, indicating that the gold traps were not contaminated with spike or ambient Hg. The chamber body (Propafilm-C bag) was replaced daily to eliminate the possibility of carryover of any ambient and isotopic Hg deposited on chamber walls during previous flux measurements. In addition, all Teflon chamber components were acid bathed daily in 30% Baker Instra-analyzed HCl, 4682

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thoroughly rinsed with Milli-Q water, and air-dried in a Hg clean room. Before, between, and after flux measurements in the field, the empty chamber was routinely tested to determine if it acted as a source or sink of Hg(0) (n ) 17). During blank chamber measurements, no enriched isotope spike was ever detected at either the inlet or the outlet, indicating that the chamber was not contaminated with the spike during flux measurements. The mean difference between inlet and outlet ambient Hg(0) concentrations (( SD) was -0.09 ( 0.31 ng m-3, with no significant difference between Hg(0) entering and leaving the chamber (t-test, n ) 17, R ) 0.05, p ) 0.627). Hence, chamber blanks were not subtracted when calculating Hg(0) fluxes from canopy foliage. Since foliar flux measurements were normalized to either the weight or surface area of enclosed foliage, and the blank chamber contained no foliage, it was not possible to calculate a blank chamber flux value typical of ground flux chambers with false bottoms. Instead, fluxes were deemed within error of the blank chamber or below detection when the difference between inlet and outlet Hg(0) concentrations was less than that observed for a blank chamber (( SD). In this study, we identify such very low fluxes, but their absolute magnitude should be considered uncertain. Since the chamber acted on average as a slight sink for Hg(0), detectable positive ambient and isotopic Hg(0) fluxes should be considered conservative estimates. True replicate flux measurements were impossible due to having a single chamber system, and also because of inherent differences between adjacent branches on a given tree. However, fluxes were often measured sequentially on the same branch, with good agreement (within 10% for both ambient and spike fluxes). Ambient and Hg Isotope Spike Analysis. In Air. Throughout this paper, ambient Hg refers to the indigenous Hg that is naturally present in the area where we conducted our experiments. 198Hg, 200Hg, and 202Hg refer to enriched Hg stable isotopes used in our spike experiments. In experiments where Hg isotope spikes were not used (e.g., blank chamber flux measurements), Hg(0) was thermally desorbed from the gold traps at 350 °C into an ultrahigh purity argon carrier gas, and detected by cold-vapor atomic fluorescence spectrometry (CVAFS, Tekran model 2500). In contrast, samples from experiments using Hg isotope spikes were analyzed on a Finnigan Element 2 inductively coupled plasma mass spectrometer (ICP-MS). Since the ICP-MS measured amounts of individual Hg isotopes, it was possible to distinguish and calculate concentrations of both ambient Hg and experimentally applied Hg spikes in samples. It should be noted that while spike solutions were greatly enriched in a given Hg isotope, they still contained minor amounts of other Hg isotopes that needed to be accounted for (23). Therefore, fluxes and concentrations of the enriched Hg spikes reported hereafter represent all experimentally applied Hg(II). To calculate concentrations of ambient Hg, an isotope that was not used as a spike in a particular experiment was used as an ambient Hg surrogate. When the only spike used in experiments was 202Hg, 200Hg was selected as the ambient Hg surrogate. To calculate ambient Hg levels in the sample from the ICP-MS data, contributions of 200Hg from the spike solutions were mathematically subtracted from the total 200 Hg measured in the sample and the remaining 200Hg was divided by 0.231 (the natural abundance of 200Hg, 24). When 200Hg or 198Hg were applied as a spike, 199Hg was used as the surrogate for ambient Hg instead. All samples containing Hg isotope spikes were analyzed at the Trent University Water Quality Centre. In Foliage. All foliage samples analyzed for spike and ambient Hg(II) concentrations were collected using strict clean-hands/dirty-hands protocol to prevent sample con-

tamination (25). Samples were freeze-dried and homogenized using stainless steel coffee grinders rinsed with deionized water and cleaned with paper towels between samples. Subsamples (100 mg) were spiked with an internal standard (Hg enriched with 201Hg) and digested in 20 mL glass vials using 10 mL of 7:3 (vol/vol) HNO3/H2SO4. Vials were covered with glass marbles, and samples were slowly refluxed on a hotplate at 80 °C until the production of brown nitrous gases ceased. The remaining acid solution was diluted with deionized water to a final volume of 10 mL. THg content of the digests was determined by continuous flow cold vapor generation with ICP-MS detection. The sample digest was continuously mixed in-line with a solution of stannous chloride using peristaltic pumps. The gaseous Hg(0) formed was separated in a custommade gas liquid separator and swept into the plasma of the ICP-MS (23). To detect spike Hg in a sample with certainty, it had to be present at a concentration >0.5-1% of ambient Hg in the same sample (23). The limit of detection (LOD) varied with the precision of the isotope ratio measurement for each set of measured samples, and typically ranged from 0.05 to 0.2 ng g-1. NIST apple leaves no. 1515 was used as the standard reference material. Ambient Hg(0) Fluxes from Black Spruce and Jack Pine Trees. Between 2001 and 2003, ambient Hg(0) fluxes from black spruce and jack pine trees in the L658 watershed were measured 33 and 20 times, respectively. Flux measurements were conducted during daylight hours (between 9 a.m. and 3 p.m.). Branches enclosed within the chamber were collected after measurements to obtain total leaf areas. Fate of Hg in Canopy Foliage. Long-Term Retention of Hg by Birch and Jack Pine Trees. We examined the buildup of ambient Hg in foliage over time while simultaneously monitoring losses of Hg from foliar surfaces using enriched stable Hg isotope experiments. This experiment was conducted after full leaf-out of birch and jack pine foliage. A working 202Hg(II) spike solution was prepared using 500 µL of primary 202HgCl2 spike solution (40 mg L-1 in concentrated HCl) mixed into 1 L of Winnange Lake water (see below) in a hand-held plastic garden sprayer. The pH of the solution was adjusted to approximately 3.5 with 100 µL of 27% NaOH. The final 202Hg(II) concentration of the spike was 20 µg L-1, and the total mass of 202Hg(II) applied to the foliage was 20 µg in 1 L of water. This water volume was equivalent to a 1 mm rain event on 1 m2 of ground surface area. At 21:30 pm on May 30, 2000, after sundown, the spike solution was applied using a hand-sprayer to two small jack pine and two small birch trees in the Lake 302 uplands. The entire liter of solution was applied so that foliage was dripping. The trees dried overnight and foliage samples were collected prior to sunrise at 5:30 a.m. the next morning (May 31, 2000). All four trees were sampled again at 15:30 on May 31, and again on June 2, June 9, July 11, August 22, and September 28. Three days after the spike application there was a 10 mm rain event, and 58 mm of rain fell in total between June 9 and July 11. Loss Mechanisms of Hg Deposited on Foliar Surfaces. To evaluate whether re-emission of spike Hg(II) as Hg(0) alone could explain the decline in spike Hg concentration of foliage over time, we repeated the tree-spraying experiment and measured flux rates of spike Hg as Hg(0) from foliage in addition to monitoring the spike Hg concentrations of the foliage over time. As part of the METAALICUS experiment, the upland and wetland portions of the L658 watershed were sprayed with 200Hg(II) and 198Hg(II) spike solutions, respectively, on May 18, 2003. 200Hg and 198Hg spike purities were 80.45% and 90.70%, respectively. Prior to spraying each area, the appropriate Hg spike was mixed into water from Eagle Lake at Vermillion Bay, ON. The spikes were applied using a Cessna 188 crop-duster aircraft at the beginning of a day-long rain event (∼22 mm total). Figure S2 (Supporting Information)

presents subdivisions of the L658 watershed for the purpose of spike application and the spray tracks of the aircraft. We accept as part of our experimental design that we may not have simulated the natural speciation and complexation of Hg in precipitation for three reasons: (1) at this time, the speciation and complexation of Hg in precipitation is not thoroughly understood, (2) it was impossible to carry adequate amounts of water in the 500 L tank of the cropduster to apply the spike at a concentration comparable to that in natural wet deposition, and (3) because the resulting Hg concentrations were so high in the tank, they would have overwhelmed any ligands regardless of whether we used distilled, rain, or lake water. However, as stated above, this concentrated application occurred at the beginning of a daylong precipitation event. After spike applications, evasion of spike Hg as Hg(0) was measured from two black spruce trees and a jack pine tree in the upland forest, and from an alder shrub in the wetland using the Hg(0) flux chamber (Figure S2, Supporting Information). Target application rates for 2003 were 24.4 µg spike 200Hg m-2 for the black spruces in upland areas A and B, 21.1 µg spike 200Hg m-2 for the jack pine in upland area C, and 53.6 µg spike 198Hg m-2 for the alder in wetland area E (Figure S2, Supporting Information). Flux measurements were performed the first day post-spray, repeated several times between 2 and 10 days post-spray, and then approximately monthly thereafter until the end of August. In all cases, flux measurements lasted 1 h and gold traps were analyzed for spike Hg(0) by ICP-MS as described above. For consistency, all flux measurements from a given tree were performed using the same branch on every occasion. This branch was collected following the final flux measurements for determination of freeze-dried weight and total leaf area. Adjacent branches were collected every time a flux measurement was performed, and at some additional times throughout the summer. These samples were analyzed for spike THg concentrations as described above. Since foliar sampling and analysis was destructive, it was impossible to monitor the spike concentrations of individual leaves over the course of the experiment. A model was used to determine if loss of spike as Hg(0) to the atmosphere measured with the dynamic chamber could account for the decrease in foliar spike Hg(II) content over time. First, a power or log curve was best-fit to the measured spike Hg(0) fluxes from each tree to model daily flux rates of spike Hg(0) to the atmosphere. Using the initial concentrations of spike Hg(II) on the foliage, the spike Hg(II) concentrations expected to remain on the foliage in subsequent days was calculated given the modeled daily loss of spike Hg(0) to the atmosphere. Here we assumed that the spike Hg(0) would flux from foliage at the measured rate for 8 h d-1. Effect of Radiation Spectrum on Reduction of Hg(II) to Hg(0) on Foliage Surfaces. We tested the hypothesis that there would be a decrease in the flux of spike 202Hg(0) as shorter, more energetic wavelengths were removed from the solar spectrum reaching the foliage within the chamber. This treespraying experiment was performed three times on cloudfree days in mid-June 2003 using small jack pine trees in the L302 upland watershed. 202HgCl2 spike solution (40 mg L-1 in concentrated HCl) was used to generate 8 µg of 202Hg(II) in 1 L of Winnange water which was then applied to the tree with a hand sprayer. When the foliage was dry, the first flux measurement was performed (plain chamber treatment) for 30 min. During subsequent flux measurements, film filters that selectively removed certain wavelengths from the solar radiation spectrum were draped over the chamber to determine the importance of UV wavelengths on the photoreduction of spike 202Hg(II). Lee UV 260 film blocked all UV-B and UV-A, type-D Mylar removed UV-B, a second layer of Propafilm-C VOL. 40, NO. 15, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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was used as a control for the presence of a second layer of film, and a black plastic bag removed all radiation (Figure S1 presents % radiation transmission of the selective filters). PAR was measured directly outside the Hg(0) flux chamber using a LI-COR Li-190SA quantum sensor every 10 s, and averaged every minute by a CR10X datalogger. In the case of the first jack pine sprayed, spike re-emission rates were measured additionally at 27, 51, and 73 h post-spray using the unfiltered flux chamber to best describe the natural exponential decline in flux rates over time. All branches enclosed in the chamber were collected following the final flux measurement to determine total leaf area.

Results and Discussion Chamber Design. Effects of the Chamber on Plant Physiology. Apparent photosynthesis (APS) and transpiration (E) rates increased as the radiation was moved closer to the loblolly pine foliage enclosed in the dynamic chamber (Figure S3). The calculated rates of APS in both our dynamic chamber and conifer cuvette were quite comparable. In both chambers, slopes of the radiation response curves were similar, and leveling to maximal APS rates began to occur at around 1.5 µmol CO2 m-2 s-1 (Figure S3, Supporting Information). These results indicated that our dynamic chamber was not affecting the normal photosynthetic function of the plant under study any more than a chamber specifically designed to measure photosynthesis. Since Hg(0) fluxes occur, at least in part, through stomata, this is an important component of the chamber design. Ambient Hg(0) Fluxes from Black Spruce and Jack Pine Trees. Ambient Hg(0) fluxes ranged from -24.2 to 38.5 ng m-2 hr-1 for black spruce (Figure 2a) and from - 19.1 to 39.8 ng m-2 hr-1 for jack pine (Figure 2b). Because the ELA is situated in a relatively pristine region with no point sources of Hg contamination or naturally high Hg levels, measured ambient Hg(0) fluxes from foliage were sometimes extremely low and not significantly different from blank chamber measurements (Figure 2). Still, 76% of ambient Hg(0) fluxes from black spruce, and 71% of fluxes from jack pine foliage, had differences between their inlet and outlet Hg(0) concentrations greater than 1 standard deviation of the differences observed for the blank chamber (Figure 2). Ambient Hg(0) fluxes from both black spruce (Figure 2a) and jack pine (Figure 2b) were almost all positive to the atmosphere at inlet Hg(0) concentrations near global background levels of ∼1.7 ng m-3 or less. Both species showed apparent Hg(0) compensation points (the atmospheric Hg(0) concentration at which no net exchange of Hg(0) occurs) between 2 and 3 ng m-3 Hg(0) in inlet air. The regression for black spruce (Figure 2a) was statistically significant (y ) -9.2398x + 24.9389, R 2 ) 0.166, p ) 0.0187). The regression for jack pine was weakly statistically significant, but it was mainly driven by one data point (y ) -10.2737x + 23.1628, R 2 ) 0.212, p ) 0.0413). No such compensation point behavior was observed in blank chamber runs (y ) 0.0282x - 0.1262, R 2 ) 0.0006). These observations of Hg(0) compensation points for canopy foliage in a natural setting are consistent with observations from previous laboratory studies (10, 26). For example, Frescholtz and Gustin (27) observed consistent Hg(0) emission to the atmosphere (1.8-3.5 ng m-2 h-1) when they examined Hg exchange from ponderosa pine (Pinus ponderosa) and quaking aspen (Populus tremuloides) seedlings using Hg-scrubbed air. Hanson et al. (10) found that when air Hg(0) concentrations were at or below ambient levels of 0.5-1.5 ng m-3, seedlings of four tree species emitted between ∼1 and 10 ng Hg m-2 h-1. Little net exchange occurred at air Hg(0) concentrations ranging between 9 and 20 ng m-3 (representing the compensation point concentration range), and at air Hg(0) levels of between 50 and 70 ng 4684

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FIGURE 2. Ambient Hg(0) fluxes from (a) black spruce and (b) jack pine foliage measured at the Experimental Lakes Area (NW Ontario) between 2001 and 2003 with the Hg(0) flux chamber. Closed circles indicate fluxes where the difference between inlet and outlet Hg(0) concentrations was greater than that observed for a blank chamber ((1 SD) (above detection). Open circles indicate those fluxes that were within ( 1 SD of the blank chamber (below detection). m-3, Hg(0) deposited to foliage at a rate of 20-40 ng m-2 h-1. Ericksen and Gustin (11) also observed Hg(0) fluxes of 1.65.5 ng m-2 h-1 from aspen (Populus sp.) seedlings grown under relatively low air Hg(0) concentrations of 2.4 ng m-3. They observed compensation points at air Hg(0) concentrations of 3-4 ng m-3, concentrations that were lower than those observed by Hanson et al. (10), but very close to those observed in our study. All these studies suggest that foliage acts as a bi-directional exchange surface for Hg(0) and show that foliage emits Hg(0) at global background air Hg(0) concentrations. The proposed source of the emitted Hg(0) from foliage in these studies was Hg(0) in soil solution (10, 13), however, as we show below there is probably also a surface (nonstomatal) component to fluxes of Hg(0) from foliage. Fate of Hg in Canopy Foliage. Long-Term Retention of Hg by Birch and Jack Pine Trees. Initial average spike 202Hg concentrations of birch foliage were higher (44 ng g-1) than those of jack pine foliage (24 ng g-1), but both species showed a rapid exponential decline in spike 202Hg concentration (Figure 3). Between 5:30 and 15:30 on May 31, 2000, 30% and 25% of spike 202Hg was gone from birch and jack pine foliage, respectively. These large reductions in spike 202Hg concentrations over only 10 h obviously cannot be explained by growth dilution. By day 2 post-spray, 52% and 42% of spike 202Hg was gone from birch and jack pine foliage, respectively. Rain events (e.g., 10 mm at 2 days post-spray) had no distinguishable effect on the exponential decline in the spike 202Hg concentration, suggesting that it was not washoff by rain primarily driving the exponential decline. In contrast to

FIGURE 3. Spike 202Hg and ambient Hg concentrations on birch and jack pine trees over time (n ) 2 for each species). the rapid initial loss of spike 202Hg, spike 202Hg concentrations remained low and more consistent toward the end of the experiment. For example, between July 11 and September 28 only 12% and 5% of spike 202Hg was lost from jack pine and birch foliage, respectively. At the end of the experiment, 202Hg concentrations of jack pine foliage were higher (3.81 ng g-1) than those of birch foliage (0.35 ng g-1) and a greater proportion of spike 202Hg was lost over the entire course of the experiment by birch than by jack pine trees (99% and 84%, respectively). Below we discuss possible mechanisms to explain the rapid decline in spike 202Hg(II) on canopy foliage. Foliar ambient Hg concentrations increased almost linearly over the course of the experiment. This trend in ambient Hg over the course of a growing season has been observed previously for both deciduous and coniferous tree species (28-29). The increase has been hypothesized to originate from uptake of atmospheric Hg(0) through stomata. Loss Mechanisms of Hg Deposited on Foliar Surfaces. After the aerial spike Hg(II) applications to the METAALICUS watershed, the highest initial spike Hg(0) re-emission rates were observed from trees with the highest initial spike Hg(II) concentrations (Figure 4 a-d). Spike Hg(0) re-emission rates declined rapidly over the next few days and leveled off to near detection limits by the end of the season. Foliar concentrations of spike Hg(II) on all trees showed a consistent rapid decline after spray application. For example, by 100 days post-spray, average foliar concentrations of spike Hg(II) were only 35% (range of 16-55%) of their initial concentrations. Most of the decrease in foliar spike Hg(II) concentration occurred within approximately the first 15 days post-spray and after this initial loss period, concentrations decreased much more slowly or remained constant. These rapid exponential declines in foliar spike Hg concentration are identical to those observed in the previous section for the small-scale tree-spraying experiments. However, here there was greater variability in the spike Hg concentrations of adjacent branches of trees, and the fit to the data was not as smooth. This result is not surprising considering that the spike application occurred here by aircraft rather than by hand-sprayer, and consequently there is a larger potential for heterogeneity of spike Hg application. Even so, the spray tracks of the aircraft indicate that there was reasonably good coverage of most areas within the watershed with spike (Figure S2, Supporting Information). Using exponential or power equations fit to the spike Hg(0) fluxes measured with the chamber, and a period of 8 h a day during which these fluxes occurred, we modeled the daily loss of spike Hg(II) from foliar surfaces by evasion to compare with the actual observed decreases in foliage spike

Hg(II) concentration (Figure 4). Except in the case of the black spruce (Figure 4a), measured spike Hg(0) evasion rates alone underestimated both the initial rapid decrease in foliar spike Hg(II) content and the final observed concentration of spike Hg(II) on foliage after 100 days. To determine by how much, on average, the measured evasion rates underestimated the actual loss of Hg(II) from foliage from the four trees (Figure 4), we first calculated for each tree the percentage of the initial concentration remaining on the foliage on a given day using (1) the equation fit to the measured foliage spike Hg(II) concentrations, and (2) the equation describing the expected foliage spike Hg(II) concentration given loss due to reduction and evasion (Figure 4). The day 100 modeled concentrations were higher than the measured concentrations by on average 22% for all four trees using an 8 h flux day. In fact, the average length of flux day required for the modeled and measured day 100 concentrations to match was an unreasonably high 16 h (range of 8-26 h). The discrepancy between modeled and measured spike concentrations was not unexpected because the measured spike Hg(II) on exposed foliage at any given time resulted from the cumulative effects of all environmental factors which influenced the loss of spike Hg(II) from foliar surfaces, whereas our dynamic chamber only measured flux of Hg(0). It is also possible that through its design, our chamber simply underestimated spike Hg(0) flux rates. Gustin et al. (15) concluded that suppression of fluxes by chambers occurred due to low air turnover rates that inadequately mimicked the turbulent flow conditions outside the chamber. Hg(0) fluxes estimated using chambers were ∼3 times lower than those using micrometeorological techniques, which do not affect the microclimate of surfaces under study (15). The possibility that our dynamic chamber underestimated the true flux rate exists even though precautions were taken to ensure normal physiological functioning of enclosed foliage (e.g., an internal fan and a relatively high air flow rate compared to other field Hg(0) flux chambers, 19) and full transmission of all solar radiation wavelengths through the chamber wall material. In our study, mechanisms of spike Hg(II) loss in addition to reduction and subsequent evasion may have remained unaccounted for. Growth dilution could have perhaps accounted for a small portion of the observed reductions in spike Hg(II) concentrations on foliage. For example, foliage from the jack pine in Figure 4d increased in weight by 7% due to new growth over the 23 days postspray, but there was a reduction in spike Hg(II) concentration of 54% over this same time period. Some proportion of applied spike Hg(II) may also have been lost by processes such as cuticle weathering (30). But in 2004, particle-bound spike concentrations in air were only 3 and 10 pg m-3 at two upland sites immediately after the aerial spike application. These extremely low concentrations rapidly dropped below detection over the following few days post-spray, so it seems unlikely that particles from leaf cuticle weathering represents a significant pathway for spike loss from foliage. It is also possible that spike Hg could have been absorbed by the leaves and translocated away from the foliage. We continue to examine all possible fates of the applied spike Hg(II) at the ecosystem level in the METAALICUS watershed. Effect of Radiation Spectrum on Reduction of Hg(II) to Hg(0) on Foliage Surfaces. On three occasions, we examined the importance of UV wavelengths in the reduction of newly deposited spike 202Hg(II) on foliage to 202Hg(0) by using selective radiation filters draped over the chamber. The design of this experiment resulted in a set of experimental filter treatments embedded within a time series. Because we consistently saw an exponential decline in flux rates of spike VOL. 40, NO. 15, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 4. Upper graphs: fluxes of spike Hg(0) from the foliage of (a) upland black spruce (open deciduous canopy), (b) upland jack pine (fire regenerated canopy), (c) wetland alder, and (d) upland black spruce (old growth fir/black spruce canopy) measured using the Hg(0) flux chamber and power function fit to the measured fluxes. Lower graphs: measured foliage concentrations of spike Hg(II) of these same trees, and modeled spike Hg(II) concentrations determined using the initial measured concentrations on foliage and modeled daily fluxes to the atmosphere using a 8-hour flux day.

FIGURE 5. Effects of PAR, UV-A, and UV-B on fluxes of spike 202Hg(0) from foliage of 3 jack pine trees. as 202Hg(0) postapplication (Figure S4, Supporting Information), we had to differentiate this expected pattern of flux rate decline from the reduction in flux rate due to filter treatments. For each tree, power functions were fit through the plain chamber and film control fluxes to represent the expected pattern of 202Hg(0) flux behavior without filters. PAR levels remained fairly constant throughout all three experimental runs (Figure 5 a-c). Fluxes measured with all UV wavelengths removed were consistently lower than fluxes expected from a best-fit exponential decline curve fit to nontreatment fluxes, however the difference was not quite statistically significant (p ) 0.074) likely due to the small number of replicates. When only UV-B was removed, fluxes were also always below those expected, but not significantly so (p ) 0.448). Preventing all radiation from reaching the foliage in the chamber (dark treatment) resulted in spike 202Hg(0) fluxes being significantly lower (p ) 0.001) than those expected if the foliage was exposed to all wavelengths (Figures 5a-c). If the observed reduction of Hg(II) on foliar surfaces resulted from microbial reduction via induction of reduction enzymes, we would have expected some lag phase before fluxes of spike 202Hg(0) were detectable (31). The absence of lag phases in these experiments suggests that there was an immediate photoreduction of Hg(II) to Hg(0) on foliage surfaces. UV radiation seems to play a role in this reduction, as has been found in other studies of Hg photoreduction in

water (32) and snow (33), however more replicate experiments are needed to confirm this trend. Factors affecting photochemical reduction include the presence of reducible Hg(II)-humic acid complexes and the intensity and wavelength of radiation (34). In a field experiment at the ELA in 2000, 1 L of 20 µg L-1 202Hg(II) was applied to a small jack pine and birch tree, as well as to a foil surface. Volatilization rates of 202Hg(0) from detached foliage immediately after application (131 ng m-2 hr-1 for jack pine and 96 ng m-2 hr-1 for birch) were much greater than those from the foil surface (9 ng m-2 hr-1, all fluxes normalized to the areal footprint of the ground flux chamber; S. Lindberg, unpublished data). Therefore, it appears likely that some component(s) of the foliar surfaces may enhance reduction of Hg(II) and subsequent volatilization of Hg(0). The behavior of surface-applied 202Hg in these experiments, together with the observation of compensation point fluxes (Figure 2), suggests that net Hg(0) emission from plants may be in part the sum of both leaf surface reduction of newly deposited Hg(II) and transport of Hg(0) through stomata. Ecological Significance. In a previous study at the ELA, St. Louis et al. (6) found that 70 mg ha-1 of THg was annually deposited to open areas in wet deposition and 80 mg ha-1 of THg was deposited under the forest canopy in throughfall, and greater than 98% of the THg in both open area wet deposition and throughfall was inorganic Hg(II), not MMHg. The authors concluded that the difference between deposition in the open and deposition under the forest canopy (i.e., 10 mg ha-1) was due to dry deposition of RGM or pHg to the forest canopy. However, in this study we determined that a significant portion of wet deposited spike Hg(II) initially retained in the forest canopy was rapidly photoreduced to Hg(0) and evaded to the atmosphere, whereas a smaller portion was still retained on the foliage at the end of the growing season (Figure 4). Therefore, if ambient Hg in wet deposition behaves like our experimentally applied spike Hg on foliage, some of the Hg annually deposited to the forest canopy in wet deposition is never available to pass through the forest canopy in throughfall. As a result, the contribution of dry deposition to fluxes of Hg into forested ecosystems could be larger than previously thought. We are currently quantifying concentrations of RGM and pHg at the ELA on an ongoing basis to directly quantify dry deposition of these two Hg(II) species. Because most foliage emitted ambient Hg(0) to the atmosphere at background atmospheric Hg(0) concentrations of ∼1.7 ng m-3 (Figure 2), it is difficult to reconcile a total atmospheric source of foliar/litterfall Hg. However, we have observed on a few occasions sufficient levels of atmospheric Hg(0) within forest canopies to exceed low foliar compensation points and result in periodic deposition of Hg(0) to foliage (Figure 2). Hg(0) concentrations elevated above background levels could result from localized Hg(0) evasion sources below canopies including forest soils. In addition to monitoring concentrations of atmospheric RGM and pHg at the ELA, we are simultaneously quantifying Hg(0) on an ongoing basis to look for these spikes in atmospheric Hg(0) concentration. Another possible explanation consistent with our observations is that some of the Hg(0) transpired to the atmosphere through vascular tissues, (e.g., 10, 35) is bound in the leaves on the way out and results in an accumulation of Hg in leaves over time. We are currently investigating this possibility at the ELA using soil-applied stable Hg isotope spikes and monitoring canopy foliage for traces of the labeled Hg(II).

Acknowledgments We thank summer students Shawn Harriman, Jasmin Finch, and Joanna Januszkiewicz. We also greatly appreciate field and laboratory help from Ken Sandilands, Michael Tate, Mark VOL. 40, NO. 15, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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Olson, Brian Dimock, Art Robinson, George Southworth, Mark Peterson, Weijin Dong, and Barry McCashin. This project was funded by grants from the Natural Sciences and Engineering Research Council of Canada (NSERC), Collaborative Mercury Research Network (COMERN), Canadian Circumpolar Institute, Electric Power Research Institute (EPRI), the Department of Fisheries and Oceans Canada, the Alberta Heritage Fund, and the University of Alberta.

Supporting Information Available Additional figures and map of watershed. This material is available free of charge via the Internet at http://pubs.acs.org.

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Received for review February 27, 2006. Revised manuscript received May 2, 2006. Accepted May 15, 2006. ES0604616