1,270
Views
12
CrossRef citations to date
0
Altmetric
Invited Reviews

Mercury cycling and isotopic fractionation in global forests

, , & ORCID Icon
Pages 3763-3786 | Published online: 12 Aug 2021

References

  • Agnan, Y., Le Dantec, T., Moore, C. W., Edwards, G. C., & Obrist, D. (2016). New constraints on terrestrial surface-atmosphere fluxes of gaseous elemental mercury using a global database. Environmental Science & Technology, 50(2), 507–524. https://doi.org/10.1021/acs.est.5b04013
  • Allan, C. J., Heyes, A., Roulet, N. T., St Louis, V. L., & Rudd, J. W. M. (2001). Spatial and temporal dynamics of mercury in Precambrian Shield upland runoff. Biogeochemistry, 52(1), 13–40. https://doi.org/10.1023/A:1026543418120
  • Amado Filho, G. M., Andrade, L. R., Farina, M., & Malm, O. (2002). Hg localisation in Tillandsia usneoides L. (Bromeliaceae), an atmospheric biomonitor. Atmospheric Environment, 36(5), 881–887. https://doi.org/10.1016/S1352-2310(01)00496-4
  • Amos, H. M., Sonke, J. E., Obrist, D., Robins, N., Hagan, N., Horowitz, H. M., Mason, R. P., Witt, M., Hedgecock, I. M., Corbitt, E. S., & Sunderland, E. M. (2015). Observational and modeling constraints on global anthropogenic enrichment of mercury. Environmental Science & Technology, 49(7), 4036–4047. https://doi.org/10.1021/es5058665
  • Arnold, J., Gustin, M. S., & Weisberg, P. J. (2018). Evidence for nonstomatal uptake of Hg by aspen and translocation of hg from foliage to tree rings in Austrian pine. Environmental Science & Technology, 52(3), 1174–1182. https://doi.org/10.1021/acs.est.7b04468
  • Bergquist, B. A., & Blum, J. D. (2007). Mass-dependent and -independent fractionation of Hg isotopes by photoreduction in aquatic systems. Science (New York, N.Y.), 318(5849), 417–420. https://doi.org/10.1126/science.1148050
  • Bishop, K. H., Lee, Y. H., Munthe, J., & Dambrine, E. (1998). Xylem sap as a pathway for total mercury and methylmercury transport from soils to tree canopy in the boreal forest. Biogeochemistry, 40(2/3), 101–113. https://doi.org/10.1023/A:1005983932240
  • Bishop, K., Shanley, J. B., Riscassi, A., de Wit, H. A., Eklöf, K., Meng, B., Mitchell, C., Osterwalder, S., Schuster, P. F., Webster, J., & Zhu, W. (2020). Recent advances in understanding and measurement of mercury in the environment: Terrestrial Hg cycling. The Science of the Total Environment, 721, 137647. https://doi.org/10.1016/j.scitotenv.2020.137647
  • Blackwell, B. D., & Driscoll, C. T. (2015). Deposition of mercury in forests along a montane elevation gradient. Environmental Science & Technology, 49(9), 5363–5370. https://doi.org/10.1021/es505928w
  • Blum, J. D., & Bergquist, B. A. (2007). Reporting of variations in the natural isotopic composition of mercury. Analytical and Bioanalytical Chemistry, 388(2), 353–359. https://doi.org/10.1007/s00216-007-1236-9
  • Blum, J. D., Drazen, J. C., Johnson, M. W., Popp, B. N., Motta, L. C., & Jamieson, A. J. (2020). Mercury isotopes identify near-surface marine mercury in deep-sea trench biota. Proceedings of the National Academy of Sciences of the United States of America, 117(47), 29292–29298. https://doi.org/10.1073/pnas.2012773117
  • Blum, J. D., Sherman, L. S., & Johnson, M. W. (2014). Mercury Isotopes in Earth and Environmental Sciences. Annual Review of Earth and Planetary Sciences, 42(1), 249–269. https://doi.org/10.1146/annurev-earth-050212-124107
  • Braune, B. M., Gaston, A. J., & Mallory, M. L. (2016). Temporal trends of mercury in eggs of five sympatrically breeding seabird species in the Canadian Arctic. Environmental Pollution (Barking, Essex: 1987), 214, 124–131. https://doi.org/10.1016/j.envpol.2016.04.006
  • Burgess, N. M., Bond, A. L., Hebert, C. E., Neugebauer, E., & Champoux, L. (2013). Mercury trends in herring gull (Larus argentatus) eggs from Atlantic Canada, 1972–2008: Temporal change or dietary shift? Environmental Pollution (Barking, Essex: 1987), 172, 216–222. https://doi.org/10.1016/j.envpol.2012.09.001
  • Bushey, J. T., Driscoll, C. T., Mitchell, M. J., Selvendiran, P., & Montesdeoca, M. R. (2008). Mercury transport in response to storm events from a northern forest landscape. Hydrological Processes, 22(25), 4813–4826. https://doi.org/10.1002/hyp.7091
  • Carpi, A., Fostier, A. H., Orta, O. R., dos Santos, J. C., & Gittings, M. (2014). Gaseous mercury emissions from soil following forest loss and land use changes: Field experiments in the United States and Brazil. Atmospheric Environment, 96, 423–429. https://doi.org/10.1016/j.atmosenv.2014.08.004
  • Chellman, N., Csank, A., Gustin, M. S., Arienzo, M. M., Vargas Estrada, M., & McConnell, J. R. (2020). Comparison of co-located ice-core and tree-ring mercury records indicates potential radial translocation of mercury in whitebark pine. The Science of the Total Environment, 743, 140695. https://doi.org/10.1016/j.scitotenv.2020.140695
  • Chen, J. B., Hintelmann, H., Feng, X. B., & Dimock, B. (2012). Unusual fractionation of both odd and even mercury isotopes in precipitation from Peterborough, ON, Canada. Geochimica Et Cosmochimica Acta, 90, 33–46. https://doi.org/10.1016/j.gca.2012.05.005
  • Clackett, S. P., Porter, T. J., & Lehnherr, I. (2018). 400-year record of atmospheric mercury from tree-rings in northwestern Canada. Environmental Science & Technology, 52(17), 9625–9633. https://doi.org/10.1021/acs.est.8b01824
  • Cui, L. W., Feng, X. B., Lin, C. J., Wang, X. M., Meng, B., Wang, X., & Wang, H. (2014). Accumulation and translocation of 198Hg in four crop species. Environmental Toxicology and Chemistry, 33(2), 334–340. https://doi.org/10.1002/etc.2443
  • de Wit, H. A., Granhus, A., Lindholm, M., Kainz, M. J., Lin, Y., Braaten, H. F. V., & Blaszczak, J. (2014). Forest harvest effects on mercury in streams and biota in Norwegian boreal catchments. Forest Ecology and Management, 324, 52–63. https://doi.org/10.1016/j.foreco.2014.03.044
  • Demers, J. D., Blum, J. D., & Zak, D. R. (2013a). Mercury isotopes in a forested ecosystem: Implications for air-surface exchange dynamics and the global mercury cycle. Global Biogeochemical Cycles, 27(1), 222–238. https://doi.org/10.1002/gbc.20021
  • Demers, J. D., Driscoll, C. T., Fahey, T. J., & Yavitt, J. B. (2007). Mercury cycling in litter and soil in different forest types in the Adirondack region, New York, USA. Ecological Applications, 17(5), 1341–1351. https://doi.org/10.1890/06-1697.1
  • Demers, J. D., Yavitt, J. B., Driscoll, C. T., & Montesdeoca, M. R. (2013b). Legacy mercury and stoichiometry with C, N, and S in soil, pore water, and stream water across the upland-wetland interface: The influence of hydrogeologic setting. Journal of Geophysical Research: Biogeosciences, 118(2), 825–841. https://doi.org/10.1002/jgrg.20066
  • Eklof, K., Kraus, A., Weyhenmeyer, G. A., Meili, M., & Bishop, K. (2012). Forestry influence by stump harvest and site preparation on methylmercury, total mercury and other stream water chemistry parameters across a boreal landscape. Ecosystems, 15(8), 1308–1320. https://doi.org/10.1007/s10021-012-9586-3
  • Eklof, K., Meili, M., Akerblom, S., von Bromssen, C., & Bishop, K. (2013). Impact of stump harvest on run-off concentrations of total mercury and methylmercury. Forest Ecology and Management, 290, 83–94. https://doi.org/10.1016/j.foreco.2012.05.039
  • Eklof, K., Schelker, J., Sorensen, R., Meili, M., Laudon, H., von Bromssen, C., & Bishop, K. (2014). Impact of forestry on total and methyl-mercury in surface waters: Distinguishing effects of logging and site preparation. Environmental Science & Technology, 48(9), 4690–4698. https://doi.org/10.1021/es404879p
  • Ericksen, J. A., Gustin, M. S., Schorran, D. E., Johnson, D. W., Lindberg, S. E., & Coleman, J. S. (2003). Accumulation of atmospheric mercury in forest foliage. Atmospheric Environment, 37(12), 1613–1622. https://doi.org/10.1016/S1352-2310(03)00008-6
  • Evans, M., Muir, D., Brua, R. B., Keating, J., & Wang, X. (2013). Mercury trends in predatory fish in Great Slave Lake: The influence of temperature and other climate drivers. Environmental Science & Technology, 47(22), 12793–12801. https://doi.org/10.1021/es402645x
  • Feng, X. B., Foucher, D., Hintelmann, H., Yan, H. Y., He, T. R., & Qiu, G. L. (2010). Tracing mercury contamination sources in sediments using mercury isotope compositions. Environmental Science & Technology, 44(9), 3363–3368. https://doi.org/10.1021/es9039488
  • Frescholtz, T. F., Gustin, M. S., Schorran, D. E., & Fernandez, G. C. J. (2003). Assessing the source of mercury in foliar tissue of quaking aspen. Environmental Toxicology and Chemistry, 22(9), 2114–2119. https://doi.org/10.1002/etc.5620220922
  • Fu, X. W., Feng, X. B., Zhu, W. Z., Rothenberg, S., Yao, H., & Zhang, H. (2010). Elevated atmospheric deposition and dynamics of mercury in a remote upland forest of southwestern China. Environmental Pollution (Barking, Essex: 1987), 158(6), 2324–2333. https://doi.org/10.1016/j.envpol.2010.01.032
  • Fu, X., Zhang, H., Liu, C., Zhang, H., Lin, C. J., & Feng, X. (2019). Significant seasonal variations in isotopic composition of atmospheric total gaseous mercury at forest sites in China caused by vegetation and mercury sources. Environmental Science & Technology, 53(23), 13748–13756. https://doi.org/10.1021/acs.est.9b05016
  • Fu, X. W., Zhang, H., Yu, B., Wang, X., Lin, C. J., & Feng, X. B. (2015). Observations of atmospheric mercury in China: A critical review. Atmospheric Chemistry and Physics, 15(16), 9455–9476. https://doi.org/10.5194/acp-15-9455-2015
  • Fu, X., Zhu, W., Zhang, H., Sommar, J., Yu, B., Yang, X., Wang, X., Lin, C.-J., & Feng, X. (2016). Depletion of atmospheric gaseous elemental mercury by plant uptake at Mt. Changbai, Northeast China. Atmospheric Chemistry and Physics, 16(20), 12861–12873. https://doi.org/10.5194/acp-16-12861-2016
  • Gabriel, M. C., Williamson, D. G., Brooks, S., Zhang, H., & Lindberg, S. (2005). Spatial variability of mercury emissions from soils in a southeastern US urban environment. Environmental Geology, 48(7), 955–964. https://doi.org/10.1007/s00254-005-0043-x
  • Garcia, E., & Carignan, R. (2005). Mercury concentrations in fish from forest harvesting and fire-impacted Canadian boreal lakes compared using stable isotopes of nitrogen. Environmental Toxicology and Chemistry, 24(3), 685–693. https://doi.org/10.1897/04-065R.1
  • Ghotra, A., Lehnherr, I., Porter, T. J., & Pisaric, M. F. J. (2020). Tree-ring inferred atmospheric mercury concentrations in the Mackenzie Delta (NWT, Canada) peaked in the 1970s but are increasing once more. ACS Earth and Space Chemistry, 4(3), 457–466. https://doi.org/10.1021/acsearthspacechem.0c00003
  • Godbold, D. L., & Huttermann, A. (1985). Effect of zinc, cadmium and mercury on root elongation of Picea-abies (Karst) seedlings, and the significance of these metals to forest dieback. Environmental Pollution Series a-Ecological and Biological, 38(4), 375–381. https://doi.org/10.1016/0143-1471(85)90108-4
  • Gong, P., Wang, X. P., Xue, Y. G., Xu, B. Q., & Yao, T. D. (2014). Mercury distribution in the foliage and soil profiles of the Tibetan forest: Processes and implications for regional cycling. Environmental Pollution (Barking, Essex: 1987), 188, 94–101. https://doi.org/10.1016/j.envpol.2014.01.020
  • Graydon, J. A., Louis, V. L. S., Hintelmann, H., Lindberg, S. E., Sandilands, K. A., Rudd, J. W. M., Kelly, C. A., Hall, B. D., & Mowat, L. D. (2008). Long-term wet and dry deposition of total and methyl mercury in the remote boreal ecoregion of Canada. Environmental Science & Technology, 42(22), 8345–8351. https://doi.org/10.1021/es801056j
  • Graydon, J. A., St Louis, V. L., Hintelmann, H., Lindberg, S. E., Sandilands, K. A., Rudd, J. W., Kelly, C. A., Tate, M. T., Krabbenhoft, D. P., & Lehnherr, I. (2009). Investigation of uptake and retention of atmospheric Hg(II) by boreal forest plants using stable Hg isotopes. Environmental Science & Technology, 43(13), 4960–4966. https://doi.org/10.1021/es900357s
  • Greger, M., Wang, Y., & Neuschutz, C. (2005). Absence of Hg transpiration by shoot after Hg uptake by roots of six terrestrial plant species. Environmental Pollution (Barking, Essex: 1987), 134(2), 201–208. https://doi.org/10.1016/j.envpol.2004.08.007
  • Grigal, D. F. (2002). Inputs and outputs of mercury from terrestrial watersheds: A review. Environmental Reviews, 10(1), 1–39. https://doi.org/10.1139/a01-013
  • Grigal, D. F. (2003). Mercury sequestration in forests and peatlands: A review. Journal of Environmental Quality, 32(2), 393–405. https://doi.org/10.2134/jeq2003.3930
  • Guédron, S., Amouroux, D., Tessier, E., Grimaldi, C., Barre, J., Berail, S., Perrot, V., & Grimaldi, M. (2018). Mercury isotopic fractionation during pedogenesis in a tropical forest soil catena (French Guiana): Deciphering the impact of historical gold mining. Environmental Science & Technology, 52, 11573–11582.
  • Gustin, M. S., Lindberg, S., Marsik, F., Casimir, A., Ebinghaus, R., Edwards, G., Hubble-Fitzgerald, C., Kemp, R., Kock, H., Leonard, T., London, J., Majewski, M., Montecinos, C., Owens, J., Pilote, M., Poissant, L., Rasmussen, P., Schaedlich, F., Schneeberger, D., … Zhang, H. (1999). Nevada STORMS project: Measurement of mercury emissions from naturally enriched surfaces. Journal of Geophysical Research: Atmospheres, 104(D17), 21831–21844. https://doi.org/10.1029/1999JD900351
  • Hanson, P. J., Lindberg, S. E., Tabberer, T. A., Owens, J. G., & Kim, K. H. (1995). Foliar exchange of mercury-vapor - evidence for a compensation point. Water, Air, & Soil Pollution, 80(1–4), 373–382. https://doi.org/10.1007/BF01189687
  • Hanson, P. J., Tabberer, T. A., & Lindberg, S. E. (1997). Emissions of mercury vapor from tree bark. Atmospheric Environment, 31(5), 777–780. https://doi.org/10.1016/S1352-2310(96)00231-2
  • Hultberg, H., Munthe, J., & Iverfeldt, A. (1995). Cycling of methyl mercury and mercury - responses in the forest roof catchment to 3 years of decreased atmospheric deposition. Water Air and Soil Pollution, 80, 415–424. https://doi.org/10.1007/BF01189691
  • Jiskra, M., Sonke, J. E., Agnan, Y., Helmig, D., & Obrist, D. (2019). Insights from mercury stable isotopes on terrestrial–atmosphere exchange of Hg(0) in the Arctic tundra. Biogeosciences, 16(20), 4051–4064. https://doi.org/10.5194/bg-16-4051-2019
  • Jiskra, M., Sonke, J. E., Obrist, D., Bieser, J., Ebinghaus, R., Myhre, C. L., Pfaffhuber, K. A., Wangberg, I., Kyllonen, K., Worthy, D., Martin, L. G., Labuschagne, C., Mkololo, T., Ramonet, M., Magand, O., & Dommergue, A. (2018). A vegetation control on seasonal variations in global atmospheric mercury concentrations. Nature Geoscience, 11(4), 244–250. https://doi.org/10.1038/s41561-018-0078-8
  • Jiskra, M., Wiederhold, J. G., Skyllberg, U., Kronberg, R.-M., Hajdas, I., & Kretzschmar, R. (2015). Mercury deposition and re-emission pathways in boreal forest soils investigated with Hg isotope signatures. Environmental Science & Technology, 49(12), 7188–7196. https://doi.org/10.1021/acs.est.5b00742
  • Jiskra, M., Wiederhold, J. G., Skyllberg, U., Kronberg, R. M., & Kretzschmar, R. (2017). Source tracing of natural organic matter bound mercury in boreal forest runoff with mercury stable isotopes. Environmental Science. Processes & Impacts, 19(10), 1235–1248. https://doi.org/10.1039/c7em00245a
  • Kelly, E. N., Schindler, D. W., St Louis, V. L., Donald, D. B., & Vladicka, K. E. (2006). Forest fire increases mercury accumulation by fishes via food web restructuring and increased mercury inputs. Proceedings of the National Academy of Sciences of the United States of America, 103(51), 19380–19385. https://doi.org/10.1073/pnas.0609798104
  • Kronberg, R.-M., Drott, A., Jiskra, M., Wiederhold, J. G., Bjorn, E., & Skyllberg, U. (2016). Forest harvest contribution to Boreal freshwater methyl mercury load. Global Biogeochemical Cycles, 30(6), 825–843. https://doi.org/10.1002/2015GB005316
  • Kumar, A., Wu, S., Huang, Y., Liao, H., & Kaplan, J. O. (2018). Mercury from wildfires: Global emission inventories and sensitivity to 2000–2050 global change. Atmospheric Environment, 173, 6–15. https://doi.org/10.1016/j.atmosenv.2017.10.061
  • Kwon, S. Y., Blum, J. D., Yin, R., Tsui, M. T.-K., Yang, Y. H., & Choi, J. W. (2020). Mercury stable isotopes for monitoring the effectiveness of the Minamata Convention on Mercury. Earth-Science Reviews, 203, 103111. https://doi.org/10.1016/j.earscirev.2020.103111
  • Laacouri, A., Nater, E. A., & Kolka, R. K. (2013). Distribution and uptake dynamics of mercury in leaves of common deciduous tree species in Minnesota. Environmental Science & Technology, 47(18), 10462–10470. https://doi.org/10.1021/es401357z
  • Lawson, S. T., Scherbatskoy, T. D., Malcolm, E. G., & Keeler, G. J. (2003). Cloud water and throughfall deposition of mercury and trace elements in a high elevation spruce-fir forest at Mt. Mansfield, Vermont. Journal of Environmental Monitoring: JEM, 5(4), 578–583. https://doi.org/10.1039/b210125d
  • Lee, Y. H., Bishop, K. H., & Munthe, J. (2000). Do concepts about catchment cycling of methylmercury and mercury in boreal catchments stand the test of time? Six years of atmospheric inputs and runoff export at Svartberget, northern Sweden. The Science of the Total Environment, 260(1–3), 11–20. https://doi.org/10.1016/S0048-9697(00)00538-6
  • Lee, Y. H., Bishop, K. H., Munthe, J., Iverfeldt, A., Verta, M., Parkman, H., & Hultberg, H. (1998). An examination of current Hg deposition and export in Fenno-Scandian catchments. Biogeochemistry, 40(2/3), 125–135. https://doi.org/10.1023/A:1005926321337
  • Leonard, T. L., Taylor, G. E., Gustin, M. S., & Fernandez, G. C. J. (1998a). Mercury and plants in contaminated soils: 1. Uptake, partitioning, and emission to the atmosphere. Environmental Toxicology and Chemistry, 17(10), 2063–2071. https://doi.org/10.1002/etc.5620171024
  • Leonard, T. L., Taylor, G. E., Gustin, M. S., & Fernandez, G. C. J. (1998b). Mercury and plants in contaminated soils: 2. Environmental and physiological factors governing mercury flux to the atmosphere. Environmental Toxicology and Chemistry, 17(10), 2072–2079. https://doi.org/10.1002/etc.5620171025
  • Lin, Y., Larssen, T., Vogt, R. D., Feng, X. B., & Zhang, H. (2011). Transport and fate of mercury under different hydrologic regimes in polluted stream in mining area. Journal of Environmental Sciences, 23(5), 757–764. https://doi.org/10.1016/S1001-0742(10)60473-1
  • Lindberg, S., Bullock, R., Ebinghaus, R., Engstrom, D., Feng, X. B., Fitzgerald, W., Pirrone, N., Prestbo, E., Seigneur, C., & Panel on Source Attribution of Atmospheric Mercury. (2007). A synthesis of progress and uncertainties in attributing the sources of mercury in deposition. Ambio, 36(1), 19–32. https://doi.org/10.1579/0044-7447(2007)36[19:ASOPAU2.0.CO;2]
  • Lindberg, S. E., Dong, W. J., & Meyers, T. (2002). Transpiration of gaseous elemental mercury through vegetation in a subtropical wetland in Florida. Atmospheric Environment, 36(33), 5207–5219. https://doi.org/10.1016/S1352-2310(02)00586-1
  • Lindberg, S. E., Meyers, T. P., & Munthe, J. (1995). Evasion of mercury vapor from tee surface of a recently limed acid forest lake in Sweden. Water, Air, & Soil Pollution, 85(2), 725–730. https://doi.org/10.1007/BF00476915
  • Lu, Z., Yuan, W., Luo, K., & Wang, X. (2021). Litterfall mercury reduction on a subtropical evergreen broadleaf forest floor revealed by multi-element isotopes. Environmental Pollution (Barking, Essex: 1987), 268(Pt A), 115867. https://doi.org/10.1016/j.envpol.2020.115867
  • Luo, Y., Duan, L., Wang, L., Xu, G. Y., Wang, S. X., & Hao, J. M. (2014). Mercury concentrations in forest soils and stream waters in northeast and south China. The Science of the Total Environment, 496, 714–720. https://doi.org/10.1016/j.scitotenv.2014.07.036
  • Luo, K., Xu, Z., Wang, X., Quan, R.-C., Lu, Z., Bi, W., Zhao, H., & Qiu, G. (2020). Terrestrial methylmercury bioaccumulation in a pine forest food chain revealed by live nest videography observations and nitrogen isotopes. Environmental Pollution, 263, 114530. https://doi.org/10.1016/j.envpol.2020.114530
  • Manceau, A., Lemouchi, C., Enescu, M., Gaillot, A. C., Lanson, M., Magnin, V., Glatzel, P., Poulin, B. A., Ryan, J. N., Aiken, G. R., Gautier-Luneau, I., & Nagy, K. L. (2015). Formation of mercury sulfide from Hg(II)-thiolate complexes in natural organic matter. Environmental Science & Technology, 49(16), 9787–9796. https://doi.org/10.1021/acs.est.5b02522
  • Manceau, A., Wang, J. X., Rovezzi, M., Glatzel, P., & Feng, X. B. (2018). Biogenesis of mercury-sulfur nanoparticles in plant leaves from atmospheric gaseous mercury. Environmental Science & Technology, 52(7), 3935–3948. https://doi.org/10.1021/acs.est.7b05452
  • Mao, H. T., Cheng, I., & Zhang, L. M. (2016). Current understanding of the driving mechanisms for spatiotemporal variations of atmospheric speciated mercury: A review. Atmospheric Chemistry and Physics, 16(20), 12897–12924. https://doi.org/10.5194/acp-16-12897-2016
  • Mazur, M., Mitchell, C. P. J., Eckley, C. S., Eggert, S. L., Kolka, R. K., Sebestyen, S. D., & Swain, E. B. (2014). Gaseous mercury fluxes from forest soils in response to forest harvesting intensity: A field manipulation experiment. The Science of the Total Environment, 496, 678–687. https://doi.org/10.1016/j.scitotenv.2014.06.058
  • Meili, M. (1991a). The coupling of mercury and organic-matter in the biogeochemical cycle - towards a mechanistic model for the boreal forest zone. Water Air & Soil Pollution, 56(1), 333–347. https://doi.org/10.1007/BF00342281
  • Meili, M. (1991b). Fluxes, pools, and turnover of mercury in Swedish forest lakes. Water Air & Soil Pollution, 56(1), 719–727. https://doi.org/10.1007/BF00342312
  • Meng, B., Li, Y., Cui, W., Jiang, P., Liu, G., Wang, Y., Richards, J., Feng, X., & Cai, Y. (2018). Tracing the uptake, transport, and fate of mercury in sawgrass (Cladium jamaicense) in the Florida Everglades using a multi-isotope technique. Environmental Science & Technology, 52(6), 3384–3391. https://doi.org/10.1021/acs.est.7b04150
  • Navratil, T., Hojdova, M., Rohovec, J., Penizek, V., & Varilova, Z. (2009). Effect of fire on pools of mercury in forest soil, Central Europe. Bulletin of Environmental Contamination and Toxicology, 83(2), 269–274. https://doi.org/10.1007/s00128-009-9705-9
  • Navratil, T., Shanley, J., Rohovec, J., Hojdova, M., Penizek, V., & Buchtova, J. (2014). Distribution and pools of mercury in Czech forest soils. Water Air and Soil Pollution, 225(3), 1829. https://doi.org/10.1007/s11270-013-1829-1
  • Novakova, T., Navratil, T., Demers, J. D., Roll, M., & Rohovec, J. (2021). Contrasting tree ring Hg records in two conifer species: Multi-site evidence of species-specific radial translocation effects in Scots pine versus European larch. Science of the Total Environment, 762, 144022. https://doi.org/10.1016/j.scitotenv.2020.144022
  • Obrist, D., Fain, X., & Berger, C. (2010). Gaseous elemental mercury emissions and CO2 respiration rates in terrestrial soils under controlled aerobic and anaerobic laboratory conditions. The Science of the Total Environment, 408(7), 1691–1700. https://doi.org/10.1016/j.scitotenv.2009.12.008
  • Obrist, D., Johnson, D. W., & Lindberg, S. E. (2009). Mercury concentrations and pools in four Sierra Nevada forest sites, and relationships to organic carbon and nitrogen. Biogeosciences, 6(5), 765–777. https://doi.org/10.5194/bg-6-765-2009
  • Obrist, D., Johnson, D. W., Lindberg, S. E., Luo, Y., Hararuk, O., Bracho, R., Battles, J. J., Dail, D. B., Edmonds, R. L., Monson, R. K., Ollinger, S. V., Pallardy, S. G., Pregitzer, K. S., & Todd, D. E. (2011). Mercury distribution across 14 US forests. Part I: Spatial patterns of concentrations in biomass. Litter, and Soils. Environmental Science, & Technology 45, 3974–3981.
  • Obrist, D., Kirk, J. L., Zhang, L., Sunderland, E. M., Jiskra, M., & Selin, N. E. (2018). A review of global environmental mercury processes in response to human and natural perturbations: Changes of emissions, climate, and land use. Ambio, 47(2), 116–140. https://doi.org/10.1007/s13280-017-1004-9
  • Obrist, D., Pearson, C., Webster, J., Kane, T., Lin, C. J., Aiken, G. R., & Alpers, C. N. (2016). A synthesis of terrestrial mercury in the western United States: Spatial distribution defined by land cover and plant productivity. The Science of the Total Environment, 568, 522–535. https://doi.org/10.1016/j.scitotenv.2015.11.104
  • Outridge, P. M., Mason, R. P., Wang, F., Guerrero, S., & Heimburger-Boavida, L. E. (2018). Updated global and oceanic mercury budgets for the United Nations Global Mercury Assessment 2018. Environmental Science & Technology, 52(20), 11466–11477. https://doi.org/10.1021/acs.est.8b01246
  • Poissant, L., Pilote, M., Yumvihoze, E., & Lean, D. (2008). Mercury concentrations and foliage/atmosphere fluxes in a maple forest ecosystem in Quebec, Canada. Journal of Geophysical Research, 113(D10307), 1–12. https://doi.org/10.1029/2007JD009510
  • Pokharel, A. K., & Obrist, D. (2011). Fate of mercury in tree litter during decomposition. Biogeosciences, 8(9), 2507–2521. https://doi.org/10.5194/bg-8-2507-2011
  • Rea, A. W., Keeler, G. J., & Scherbatskoy, T. (1996). The deposition of mercury in throughfall and litterfall in the Lake Champlain watershed: A short-term study. Atmospheric Environment, 30(19), 3257–3263. https://doi.org/10.1016/1352-2310(96)00087-8
  • Rea, A. W., Lindberg, S. E., & Keeler, G. J. (2001). Dry deposition and foliar leaching of mercury and selected trace elements in deciduous forest throughfall. Atmospheric Environment, 35(20), 3453–3462. https://doi.org/10.1016/S1352-2310(01)00133-9
  • Rodríguez Martin, J. A., Gutiérrez, C., Torrijos, M., & Nanos, N. (2018). Wood and bark of Pinus halepensis as archives of heavy metal pollution in the Mediterranean Region. Environmental Pollution (Barking, Essex: 1987), 239, 438–447. https://doi.org/10.1016/j.envpol.2018.04.036
  • Sauer, A. K., Driscoll, C. T., Evers, D. C., Adams, E. M., & Yang, Y. (2020). Mercury exposure in songbird communities within Sphagnum bog and upland forest ecosystems in the Adirondack Park (New York, USA). Ecotoxicology (London, England), 29(10), 1815–1829. https://doi.org/10.1007/s10646-019-02142-x
  • Scanlon, T. M., Riscassi, A. L., Demers, J. D., Camper, T. D., Lee, T. R., & Druckenbrod, D. L. (2020). Mercury accumulation in tree rings: Observed trends in quantity and isotopic composition in Shenandoah National Park, Virginia. Journal of Geophysical Research: Biogeosciences, 125(2), e2019JG005445. https://doi.org/10.1029/2019JG005445
  • Schneider, L., Allen, K., Walker, M., Morgan, C., & Haberle, S. (2019). Using tree rings to track atmospheric mercury pollution in Australia: The legacy of mining in Tasmania. Environmental Science & Technology, 53(10), 5697–5706. https://doi.org/10.1021/acs.est.8b06712
  • Schwesig, D., & Matzner, E. (2000). Pools and fluxes of mercury and methylmercury in two forested catchments in Germany. The Science of the Total Environment, 260(1–3), 213–223. https://doi.org/10.1016/S0048-9697(00)00565-9
  • Selin, N. E. (2009). Global biogeochemical cycling of mercury: A review. Annual Review of Environment and Resources, 34(1), 43–63. https://doi.org/10.1146/annurev.environ.051308.084314
  • Selvendiran, P., Driscoll, C. T., Bushey, J. T., & Montesdeoca, M. R. (2008a). Wetland influence on mercury fate and transport in a temperate forested watershed. Environmental Pollution (Barking, Essex: 1987), 154(1), 46–55. https://doi.org/10.1016/j.envpol.2007.12.005
  • Selvendiran, P., Driscoll, C. T., Montesdeoca, M. R., & Bushey, J. T. (2008b). Inputs, storage, and transport of total and methyl mercury in two temperate forest wetlands. Journal of Geophysical Research-Biogeosciences, 113, G00C01. https://doi.org/10.1029/2008JG000739
  • Smith, C. N., Kesler, S. E., Blum, J. D., & Rytuba, J. J. (2008). Isotope geochemistry of mercury in source rocks, mineral deposits and spring deposits of the California Coast Ranges, USA. Earth and Planetary Science Letters, 269(3–4), 399–406. https://doi.org/10.1016/j.epsl.2008.02.029
  • Sonke, J. E. (2011). A global model of mass independent mercury stable isotope fractionation. Geochimica Et Cosmochimica Acta, 75(16), 4577–4590. https://doi.org/10.1016/j.gca.2011.05.027
  • Sorensen, R., Meili, M., Lambertsson, L., von Bromssen, C., & Bishop, K. (2009). The effects of forest harvest operations on mercury and methylmercury in two boreal streams: Relatively small changes in the first two years prior to site preparation. Ambio, 38(7), 364–372. https://doi.org/10.1579/0044-7447-38.7.364
  • Spawn, S. A., Sullivan, C. C., Lark, T. J., & Gibbs, H. K. (2020). Harmonized global maps of above and belowground biomass carbon density in the year 2010. Scientific Data, 7(1), 112. https://doi.org/10.1038/s41597-020-0444-4
  • St Louis, V. L., Graydon, J. A., Lehnherr, I., Amos, H. M., Sunderland, E. M., St Pierre, K. A., Emmerton, C. A., Sandilands, K., Tate, M., Steffen, A., & Humphreys, E. R. (2019). Atmospheric concentrations and wet/dry loadings of mercury at the remote experimental Lakes Area, Northwestern Ontario. Environmental Science & Technology, 53(14), 8017–8026. https://doi.org/10.1021/acs.est.9b01338
  • St Louis, V. L., Rudd, J. W. M., Kelly, C. A., Hall, B. D., Rolfhus, K. R., Scott, K. J., Lindberg, S. E., & Dong, W. (2001). Importance of the forest canopy to fluxes of methyl mercury and total mercury to boreal ecosystems. Environmental Science & Technology, 35(15), 3089–3098. https://doi.org/10.1021/es001924p
  • Stamenkovic, J., & Gustin, M. S. (2009). Nonstomatal versus stomatal uptake of atmospheric mercury. Environmental Science & Technology, 43(5), 1367–1372. https://doi.org/10.1021/es801583a
  • Stamenkovic, J., Gustin, M. S., Arnone, J. A., Johnson, D. W., Larsen, J. D., & Verburg, P. S. J. (2008). Atmospheric mercury exchange with a tallgrass prairie ecosystem housed in mesocosms. The Science of the Total Environment, 406(1–2), 227–238. https://doi.org/10.1016/j.scitotenv.2008.07.047
  • Stankwitz, C., Kaste, J. M., & Friedland, A. J. (2012). Threshold increases in soil lead and mercury from tropospheric deposition across an elevational gradient. Environmental Science & Technology, 46(15), 8061–8068. https://doi.org/10.1021/es204208w
  • Streets, D. G., Devane, M. K., Lu, Z. F., Bond, T. C., Sunderland, E. M., & Jacob, D. J. (2011). All-time releases of mercury to the atmosphere from human activities. Environmental Science & Technology, 45(24), 10485–10491. https://doi.org/10.1021/es202765m
  • Streets, D. G., Hao, J. M., Wu, Y., Jiang, J. K., Chan, M., Tian, H. Z., & Feng, X. B. (2005). Anthropogenic mercury emissions in China. Atmospheric Environment, 39(40), 7789–7806. https://doi.org/10.1016/j.atmosenv.2005.08.029
  • Sun, R., Jiskra, M., Amos, H. M., Zhang, Y., Sunderland, E. M., & Sonke, J. E. (2019a). Modelling the mercury stable isotope distribution of Earth surface reservoirs: Implications for global Hg cycling. Geochimica Et Cosmochimica Acta, 246, 156–173. https://doi.org/10.1016/j.gca.2018.11.036
  • Sun, L. M., Lu, B. Y., Yuan, D. X., Hao, W. B., & Zheng, Y. (2017). Variations in the isotopic composition of stable mercury isotopes in typical mangrove plants of the Jiulong estuary, SE China. Environmental Science and Pollution Research International, 24(2), 1459–1468. https://doi.org/10.1007/s11356-016-7933-1
  • Sun, T., Ma, M., Wang, X., Wang, Y., Du, H., Xiang, Y., Xu, Q., Xie, Q., & Wang, D. (2019b). Mercury transport, transformation and mass balance on a perspective of hydrological processes in a subtropical forest of China. Environmental Pollution (Barking, Essex: 1987), 254(Pt B), 113065. https://doi.org/10.1016/j.envpol.2019.113065
  • Sun, G., Sommar, J., Feng, X., Lin, C.-J., Ge, M., Wang, W., Yin, R., Fu, X., & Shang, L. (2016). Mass-dependent and -independent fractionation of mercury isotope during gas-phase oxidation of elemental mercury vapor by atomic Cl and Br. Environmental Science & Technology, 50(17), 9232–9241. https://doi.org/10.1021/acs.est.6b01668
  • Tang, R. G., Luo, J., She, J., Chen, Y. C., Yang, D. D., & Zhou, J. (2015). The cadmium and lead of soil in timberline coniferous forests. Environmental Earth Sciences, 73(1), 303–310. https://doi.org/10.1007/s12665-014-3424-1
  • Townsend, J. M., Driscoll, C. T., Rimmer, C. C., & McFarland, K. P. (2014). Avian, salamander, and forest floor mercury concentrations increase with elevation in a terrestrial ecosystem. Environmental Toxicology and Chemistry, 33(1), 208–215. https://doi.org/10.1002/etc.2438
  • Townsend, J. M., Rimmer, C. C., Driscoll, C. T., McFarland, K. P., & Inigo-Elias, E. (2013). Mercury concentrations in tropical resident and migrant songbirds on Hispaniola. Ecotoxicology (London, England), 22(1), 86–93. https://doi.org/10.1007/s10646-012-1005-1
  • Tsui, M. T.-K., Adams, E. M., Jackson, A. K., Evers, D. C., Blum, J. D., & Balogh, S. J. (2018). Understanding sources of methylmercury in songbirds with stable mercury isotopes: Challenges and future directions. Environmental Toxicology and Chemistry, 37(1), 166–174. https://doi.org/10.1002/etc.3941
  • Tsui, M. T., Blum, J. D., & Kwon, S. Y. (2019). Review of stable mercury isotopes in ecology and biogeochemistry. Science of the Total Environment, 716, 135386. https://doi.org/10.1016/j.scitotenv.2019.135386
  • Tsui, M. T. K., Uzun, H., Ruecker, A., Majidzadeh, H., Ulus, Y., Zhang, H., Bao, S., Blum, J. D., Karanfil, T., & Chow, A. T. (2020). Concentration and isotopic composition of mercury in a blackwater river affected by extreme flooding events. Limnology and Oceanography, 65(9), 2158–2169. https://doi.org/10.1002/lno.11445
  • UN-Environment. (2019). Global Mercury Assessment 2018. UN-Environment Programme, Chemicals and Health Branch.
  • Vidon, P. G., Mitchell, C. P., Jacinthe, P. A., Baker, M. E., Liu, X., & Fisher, K. R. (2013). Mercury dynamics in groundwater across three distinct riparian zone types of the US Midwest. Environmental Science: Processes & Impacts, 15(11), 2131–2141. https://doi.org/10.1039/c3em00254c
  • Vijayaraghavan, K., Levin, L., Parker, L., Yarwood, G., & Streets, D. (2014). Response of fish tissue mercury in a freshwater lake to local, regional, and global changes in mercury emissions. Environmental Toxicology and Chemistry, 33(6), 1238–1247. https://doi.org/10.1002/etc.2584
  • Wang, X., Bao, Z., Lin, C.-J., Yuan, W., & Feng, X. (2016a). Assessment of global mercury deposition through litterfall. Environmental Science & Technology, 50(16), 8548–8557. https://doi.org/10.1021/acs.est.5b06351
  • Wang, J. J., Guo, Y. Y., Guo, D. L., Yin, S. L., Kong, D. L., Liu, Y. S., & Zeng, H. (2012). Fine root mercury heterogeneity: Metabolism of lower-order roots as an effective route for mercury removal. Environmental Science & Technology, 46(2), 769–777. https://doi.org/10.1021/es2018708
  • Wang, X., Lin, C. J., Feng, X. B., Yuan, W., Fu, X. W., Zhang, H., Wu, Q. R., & Wang, S. X. (2018). Assessment of regional mercury deposition and emission outflow in Mainland China. Journal of Geophysical Research: Atmospheres, 123(17), 9868–9890. https://doi.org/10.1029/2018JD028350
  • Wang, X., Lin, C.-J., Lu, Z., Zhang, H., Zhang, Y., & Feng, X. (2016b). Enhanced accumulation and storage of mercury on subtropical evergreen forest floor: Implications on mercury budget in global forest ecosystems. Journal of Geophysical Research: Biogeosciences, 121(8), 2096–2109. https://doi.org/10.1002/2016JG003446
  • Wang, X., Luo, J., Yin, R., Yuan, W., Lin, C.-J., Sommar, J., Feng, X., Wang, H., & Lin, C. (2017a). Using mercury isotopes to understand mercury accumulation in the montane forest floor of the Eastern Tibetan Plateau. Environmental Science & Technology, 51(2), 801–809. https://doi.org/10.1021/acs.est.6b03806
  • Wang, X., Luo, J., Yuan, W., Lin, C. J., Wang, F., Liu, C., Wang, G., & Feng, X. (2020a). Global warming accelerates uptake of atmospheric mercury in regions experiencing glacier retreat. Proceedings of the National Academy of Sciences of the United States of America, 117(4), 2049–2055. https://doi.org/10.1073/pnas.1906930117
  • Wang, F., Outridge, P. M., Feng, X., Meng, B., Heimburger-Boavida, L. E., & Mason, R. P. (2019a). How closely do mercury trends in fish and other aquatic wildlife track those in the atmosphere? - Implications for evaluating the effectiveness of the Minamata Convention. The Science of the Total Environment, 674, 58–70. https://doi.org/10.1016/j.scitotenv.2019.04.101
  • Wang, T., Yang, G., Du, H., Guo, P., Sun, T., An, S., Wang, D., & Ma, M. (2021a). Migration characteristics and potential determinants of mercury in long-term decomposing litterfall of two subtropical forests. Ecotoxicology and Environmental Safety, 208, 111402. https://doi.org/10.1016/j.ecoenv.2020.111402
  • Wang, X., Yuan, W., & Feng, X. (2017b). Global review of mercury biogeochemical processes in forest ecosystems. Progress in Chemistry, 29, 970–980.
  • Wang, X., Yuan, W., Feng, X., Wang, D., & Luo, J. (2019b). Moss facilitating mercury, lead and cadmium enhanced accumulation in organic soils over glacial erratic at Mt. Gongga, China. Environmental Pollution (Barking, Essex: 1987), 254(Pt A), 112974. https://doi.org/10.1016/j.envpol.2019.112974
  • Wang, X., Yuan, W., Lin, C. J., Luo, J., Wang, F., Feng, X., Fu, X., & Liu, C. (2020b). Underestimated sink of atmospheric mercury in a deglaciated forest chronosequence. Environmental Science & Technology, 54(13), 8083–8093. https://doi.org/10.1021/acs.est.0c01667
  • Wang, X., Yuan, W., Lin, C.-J., Wu, F., & Feng, X. (2021b). Stable mercury isotopes stored in Masson Pinus tree rings as atmospheric mercury archives. Journal of Hazardous Materials, 415, 125678. https://doi.org/10.1016/j.jhazmat.2021.125678
  • Wang, X., Yuan, W., Lin, C. J., Zhang, L. M., Zhang, H., & Feng, X. B. (2019c). Climate and vegetation as primary drivers for global mercury storage in surface soil. Environmental Science & Technology, 53(18), 10665–10675. https://doi.org/10.1021/acs.est.9b02386
  • Wang, X., Yuan, W., Lu, Z. Y., Lin, C. J., Yin, R. S., Li, F., & Feng, X. B. (2019d). Effects of precipitation on mercury accumulation on subtropical montane forest floor: Implications on climate forcing. Journal of Geophysical Research: Biogeosciences, 124(4), 959–972. https://doi.org/10.1029/2018JG004809
  • Wang, Z., Zhang, X., Xiao, J., Zhijia, C., & Yu, P. (2009). Mercury fluxes and pools in three subtropical forested catchments, southwest China. Environmental Pollution (Barking, Essex: 1987), 157(3), 801–808. https://doi.org/10.1016/j.envpol.2008.11.018
  • Webster, J. P., Kane, T. J., Obrist, D., Ryan, J. N., & Aiken, G. R. (2016). Estimating mercury emissions resulting from wildfire in forests of the Western United States. Science of the Total Environment, 568, 578–586. https://doi.org/10.1016/j.scitotenv.2016.01.166
  • Woerndle, G. E., Tsz-Ki Tsui, M., Sebestyen, S. D., Blum, J. D., Nie, X., & Kolka, R. K. (2018). New insights on ecosystem mercury cycling revealed by stable isotopes of mercury in water flowing from a headwater peatland catchment. Environmental Science & Technology, 52(4), 1854–1861. https://doi.org/10.1021/acs.est.7b04449
  • Wu, Q., Wang, S., Li, G., Liang, S., Lin, C.-J., Wang, Y., Cai, S., Liu, K., & Hao, J. (2016). Temporal trend and spatial distribution of speciated atmospheric mercury emissions in China during 1978–2014. Environmental Science & Technology, 50(24), 13428–13435. https://doi.org/10.1021/acs.est.6b04308
  • Yanai, R. D., Yang, Y., Wild, A. D., Smith, K. T., & Driscoll, C. T. (2020). New approaches to understand mercury in trees: Radial and longitudinal patterns of mercury in tree rings and genetic control of mercury in maple sap. Water, Air, & Soil Pollution, 231(5), 231–248. https://doi.org/10.1007/s11270-020-04601-2
  • Yang, Y., Yanai, R. D., Montesdeoca, M., & Driscoll, C. T. (2017). Measuring mercury in wood: Challenging but important. International Journal of Environmental Analytical Chemistry, 97(5), 456–467. https://doi.org/10.1080/03067319.2017.1324852
  • Yu, Q., Luo, Y., Xu, G., Wu, Q., Wang, S., Hao, J., & Duan, L. (2020). Subtropical forests act as mercury sinks but as net sources of gaseous elemental mercury in South China. Environmental Science & Technology, 54(5), 2772–2779. https://doi.org/10.1021/acs.est.9b06715
  • Yuan, W., Sommar, J., Lin, C.-J., Wang, X., Li, K., Liu, Y., Zhang, H., Lu, Z., Wu, C., & Feng, X. (2019a). Stable isotope evidence shows re-emission of elemental mercury vapor occurring after reductive loss from foliage. Environmental Science & Technology, 53(2), 651–660. https://doi.org/10.1021/acs.est.8b04865
  • Yuan, W., Wang, X., Lin, C.-J., Sommar, J., Lu, Z., & Feng, X. (2019b). Process factors driving dynamic exchange of elemental mercury vapor over soil in broadleaf forest ecosystems. Atmospheric Environment, 219, 117047. https://doi.org/10.1016/j.atmosenv.2019.117047
  • Yuan, W., Wang, X., Lin, C. J., Wu, C., Zhang, L., Wang, B., Sommar, J., Lu, Z., & Feng, X. (2020). Stable mercury isotope transition during postdepositional decomposition of biomass in a forest ecosystem over five centuries. Environmental Science & Technology, 54(14), 8739–8749. https://doi.org/10.1021/acs.est.0c00950
  • Zayed, J., Loranger, S., & Kennedy, G. (1992). Variations of trace-element concentrations in red spruce tree rings. Water, Air, & Soil Pollution, 65(3–4), 281–291. https://doi.org/10.1007/BF00479892
  • Zhao, Z., Wang, D. Y., Wang, Y., Mu, Z. J., & Zhu, J. S. (2015). Wet deposition flux and runoff output flux of mercury in a typical small agricultural watershed in Three Gorges Reservoir areas. Environmental Science and Pollution Research International, 22(7), 5538–5551. https://doi.org/10.1007/s11356-014-3701-2
  • Zheng, W., Demers, J. D., Lu, X., Bergquist, B. A., Anbar, A. D., Blum, J. D., & Gu, B. (2019). Mercury stable isotope fractionation during abiotic dark oxidation in the presence of thiols and natural organic matter. Environmental Science & Technology, 53(4), 1853–1862. https://doi.org/10.1021/acs.est.8b05047
  • Zheng, W., & Hintelmann, H. (2010). Nuclear field shift effect in isotope fractionation of mercury during abiotic reduction in the absence of light. The Journal of Physical Chemistry. A, 114(12), 4238–4245. https://doi.org/10.1021/jp910353y
  • Zheng, W., Obrist, D., Weis, D., & Bergquist, B. A. (2016). Mercury isotope compositions across North American forests. Global Biogeochemical Cycles, 30(10), 1475–1492. https://doi.org/10.1002/2015GB005323
  • Zhou, J., Obrist, D., Dastoor, A., Jiskra, M., & Ryjkov, A. (2021). Vegetation uptake of mercury and impacts on global cycling. Nature Reviews Earth & Environment, 2(4), 269–284. https://doi.org/10.1038/s43017-021-00146-y
  • Zhu, W., Lin, C. J., Wang, X., Sommar, J., Fu, X., & Feng, X. (2016). Global observations and modeling of atmosphere–surface exchange of elemental mercury: A critical review. Atmospheric Chemistry and Physics, 16(7), 4451–4480. https://doi.org/10.5194/acp-16-4451-2016

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.