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Resolving a paradox—high mercury deposition, but low bioaccumulation in northeastern Puerto Rico

  • James B. ShanleyEmail author
  • Mark Marvin-DiPasquale
  • Oksana Lane
  • Wayne Arendt
  • Steven Hall
  • William H. McDowell
Article

Abstract

At a “clean air” trade winds site in northeastern Puerto Rico, we found an apparent paradox: atmospheric total mercury (THg) deposition was highest of any site in the USA Mercury Deposition Network, but assimilation into the local food web was quite low. Avian blood THg concentrations (n = 31, from eight species in five foraging guilds) ranged widely from 0.2 to 32 ng g−1 (median of 4.3 ng g−1). Within this population, THg was significantly greater at a low-elevation site near a wetland compared to an upland montane site, even when the comparison was limited to a single species. Overall, however, THg concentrations were approximately an order of magnitude lower than comparable populations in the continental U.S. In surface soil and sediment, potential rates of demethylation were 3 to 9-fold greater than those for Hg(II)-methylation (based on six radiotracer amendment incubations), but rates of change of ambient MeHg pools showed a slight net positive Hg(II)-methylation. Thus, the resolution of the paradox is that MeHg degradation approximately keeps pace with MeHg production in this landscape. Further, any net production of MeHg is subject to frequent flushing by high rainfall on chronically wet soils. The interplay of these microbial processes and hydrology appears to shield the local food web from adverse effects of high atmospheric mercury loading. This scenario may play out in other humid tropical ecosystems as well, but it is difficult to evaluate because coordinated studies of Hg deposition, methylation, and trophic uptake have not been conducted at other tropical sites.

Keywords

Methylmercury Trophic uptake Demethylation Puerto Rico Sulfate reduction Iron reduction 

Notes

Acknowledgements

We thank Angel Torres and Manuel Rosario for help with sampling, and USGS staff in Menlo Park (CA) for laboratory analyses (Jennifer Agee, Le Kieu, Evangelos Kakouros, and Michelle Beyer). We acknowledge Michael Bank for facilitating analysis of biota and vegetation samples, which motivated this study. This research was supported by the USGS Water, Energy, and Biogeochemical Budgets (WEBB) program, which was funded by USGS Climate Research and Development (now Land Resources Science Program). Supplemental support for MM-D was provided by the USGS Toxic Substances Hydrology Program. Support was also provided by NSF grant DEB-1457805 and the Luquillo Critical Zone Observatory NSF grant EAR-1331841. Part of this research was carried out in cooperation with the University of Puerto Rico. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

10646_2019_2108_MOESM1_ESM.docx (295 kb)
Supplementary Materials

References

  1. Achá D, Hintelmann H, Yee J (2011) Importance of sulfate reducing bacteria in mercury methylation and demethylation in periphyton from Bolivian Amazon region. Chemosphere 82:911–916CrossRefGoogle Scholar
  2. Ackerman JD, Rodríguez-Robles JA, Meléndez-Ackerman EJ (1994). A meager nectar offering by an epiphytic orchid is better than nothing. Biotropica 26:44–49CrossRefGoogle Scholar
  3. Allen R (1961) Birds of the Caribbean. The Viking Press, New YorkGoogle Scholar
  4. Belger L, Forsberg BR (2006) Factors controlling Hg levels in two predatory fish species in the Negro river basin, Brazilian Amazon. Sci Total Environ 367:451–459CrossRefGoogle Scholar
  5. Black FJ, Bokhutlo T, Somoxa A, Maethamako M, Modisaemang O, Kemosedile T, Cobb-Adams C, Mosepele K, Chimbari M (2011) The tropical African mercury anomaly: lower than expected mercury concentrations in fish and human hair. Sci Total Environ 409:1967–1975CrossRefGoogle Scholar
  6. Bowles KC, Apte SC, Maher WA, Kawei M, Smith R (2001) Bioaccumulation and biomagnification of mercury in Lake Murray, Papua New Guinea. Can. J Fish Aquat Sci 58:888–897CrossRefGoogle Scholar
  7. Bradley PM, Burns DA, Murray KR, Brigham ME, Button DT, Chasar LC, Marvin-DiPasquale MC, Lowery MA, Journey CA (2011) Spatial and seasonal variability of dissolved methylmercury in two stream basins in the eastern United States. Environ Sci Technol 45:2048–2055CrossRefGoogle Scholar
  8. Burger J, Cooper K, Saliva J, Gochfeld D, Lipsky D, Gochfeld M (1992a) Mercury bioaccumulation in organisms from three Puerto Rican estuaries. Environ Mon Assess 22:181–197CrossRefGoogle Scholar
  9. Burger J, Gochfeld M (1991) Lead, mercury, and cadmium in feathers of tropical terns in Puerto Rico and Australia. Arch Environ Contam Toxicol 21:311–315CrossRefGoogle Scholar
  10. Burger J, Parsons K, Benson T, Shukla T, Rothstein D, Gochfeld M (1992b) Heavy metal and selenium levels in young cattle egrets from nesting colonies in the northeastern United States, Puerto Rico, and Egypt. Arch Environ Contam Toxicol 23:435–439Google Scholar
  11. Cabana G, Rasmussen JB (1994) Modelling food chain structure and contaminant bioaccumulation using stable nitrogen isotopes. Nature 372:255CrossRefGoogle Scholar
  12. Correia RRS, Miranda MR, Guimarães JRD (2012) Mercury methylation and the microbial consortium in periphyton of tropical macrophytes: effect of different inhibitors. Environ Res 112:86–91CrossRefGoogle Scholar
  13. Cristol DA, Brasso RL, Condon AM, Fovargue RE, Friedman SL, Hallinger KK, Monroe AP, White AE (2008) The movement of aquatic mercury through terrestrial food webs. Science 320:335CrossRefGoogle Scholar
  14. Cruz A (1980) Feeding ecology of the Black-Whiskered Vireo and associated gleaning birds in Jamaica. Wilson Bull 92:40–52Google Scholar
  15. Driscoll CT, Mason RP, Chan HM, Jacob DJ, Pirrone N (2013) Mercury as a global pollutant: Sources, pathways, and effects. Environ Sci Technol 47:4967–4983CrossRefGoogle Scholar
  16. Dubinsky EA, Silver WL, Firestone MK (2010) Tropical forest soil microbial communities couple iron and carbon biogeochemistry. Ecology 91:2604–2612CrossRefGoogle Scholar
  17. Edmonds ST et al. (2010) Geographic and seasonal variation in mercury exposure of the declining Rusty Blackbird. Condor 112:789–799CrossRefGoogle Scholar
  18. Eldridge N (1998) Life in the balance: humanity and the biodiversity crisis. Princeton Univ. Press., Princeton NJ, p. 240Google Scholar
  19. EPA US (1998) Method 7473 (SW-846): mercury in solids and solutions by thermal decomposition, amalgamation, and atomic absorption spectrophotometry, Revision 0. Washington, D.C., p. 17Google Scholar
  20. Evers DC (2008) Mercury in terrestrial birds of Belize. BioDiversity Research Institute, Gorham, Maine. Report BRI 2008-05, p. 14.Google Scholar
  21. Evers DC, Duron M (2006) Developing an exposure profile for mercury in breeding birds of New York and Pennsylvania, 2005. BioDiversity Research Institute, Gorham, Maine. Report BRI 2006-11, p. 32Google Scholar
  22. Fadini PS, Jardim WF (2001) Is the Negro River Basin (Amazon) impacted by naturally occurring mercury? Sci Total Environ 275:71–82CrossRefGoogle Scholar
  23. Fleming EJ, Mack EE, Green PG, Nelson DC (2006) Mercury methylation from unexpected sources: molybdate-inhibited freshwater sediments and an iron-reducing bacterium. Appl Environ Microbiol 72:457–464CrossRefGoogle Scholar
  24. Fostier AH, Forti MC, Guimaraes JRD, Melfi AJ, Boulet R, Espirito Santo CM, Krug FJ (2000) Mercury fluxes in a natural forested Amazonian catchment (Serra do Navio, Amapa State, Brazil). Sci Total Environ 260:201–211CrossRefGoogle Scholar
  25. Gilmour CC, Podar M, Bullock AL, Graham AM, Brown SD, Somenahally AC, Johs A, Hurt RA, Bailey KL, Elias DA (2013) Mercury methylation by novel microorganisms from new environments. Environ Sci Technol 47:11810–11820CrossRefGoogle Scholar
  26. Guentzel JL, Landing WM, Gill GA, Pollman CD (2001) Processes influencing rainfall deposition of mercury in Florida. Environ Sci Technol 35:863–873CrossRefGoogle Scholar
  27. Guimarães JRD, Meili M, Hylander LD, Silva EdCe, Roulet M, Mauro JBN, de Lemos RA (2000) Mercury net methylation in five tropical flood plain regions of Brazil: high in the root zone of floating macrophyte mats but low in surface sediments and flooded soils. Sci Total Environ 261:99–107CrossRefGoogle Scholar
  28. Hall SJ, Liptzin D, Buss HL, DeAngelis K, Silver WL (2016) Drivers and patterns of iron redox cycling from surface to bedrock in a deep tropical forest soil: a new conceptual model. Biogeochemistry 130:177–190CrossRefGoogle Scholar
  29. Hall SJ, McDowell WH, Silver WL (2013) When wet gets wetter: decoupling of moisture, redox biogeochemistry, and greenhouse gas fluxes in a humid tropical forest soil. Ecosystems 16:576–589CrossRefGoogle Scholar
  30. Hall SJ, Silver WL (2013) Iron oxidation stimulates organic matter decomposition in humid tropical forest soils. Glob Change Biol 19:2804–2813CrossRefGoogle Scholar
  31. Hall SJ, Silver WL (2015) Reducing conditions, reactive metals, and their interactions can explain spatial patterns of surface soil carbon in a humid tropical forest. Biogeochemistry 125:149–165CrossRefGoogle Scholar
  32. Hansen AM, Gay DA (2013) Observations of mercury wet deposition in Mexico. Environ Sci Pollut Res 20:8316–8325CrossRefGoogle Scholar
  33. Howard J, Trotz MA, Thomas K, Omisca E, Chiu HT, Halfhide T, Akiwumi F, Michael R, Stuart AL (2011) Total mercury loadings in sediment from gold mining and conservation areas in Guyana. Environ Mon Assess 179:555–573CrossRefGoogle Scholar
  34. Hyacinthe C, Bonneville S, Van Cappellen P (2006) Reactive iron(III) in sediments: chemical versus microbial extractions. Geochim Cosmochim Acta 70:4166–4180CrossRefGoogle Scholar
  35. Jackson AK et al. (2015) Songbirds as sentinels of mercury in terrestrial habitats of eastern North America. Ecotoxicology 24:453–467CrossRefGoogle Scholar
  36. Johnson AH, Xing HX, Scatena FN (2015) Controls on soil carbon stocks in El Yunque National Forest. Puerto Rico Soil Sci Soc Am J 79:294–304CrossRefGoogle Scholar
  37. Kerin EJ, Gilmour CC, Roden E, Suzuki M, Coates J, Mason R (2006) Mercury methylation by dissimilatory iron-reducing bacteria. Appl Envirob Microbio 72:7919–7921CrossRefGoogle Scholar
  38. Krabbenhoft DP, Branfireun BA, Heyes A (2005) Biogeochemical cycles affecting the speciation, fate and transport of mercury in the environment. In: Parsons MB, Percival JB (eds). Mercury: sources, measurements, cycles, and effects, vol. 34. Mineralogical Association of Canada, Halifax, pp. 139–156Google Scholar
  39. Landing WM, Caffrey JM, Nolek SD, Gosnell KJ, Parker WC (2010) Atmospheric wet deposition of mercury and other trace elements in Pensacola, Florida. Atmos Chem Phys 10:4867–4877CrossRefGoogle Scholar
  40. Lane OP, Arendt WJ, Tórrez MA, Castellón JCG (2013) Pilot assessment of mercury exposure in selected biota from the lowlands of Nicaragua. Mesoamericana 17:19–28Google Scholar
  41. Lázaro WL, Díez S, da Silva CJ, Ignácio ÁRA, Guimarães JRD (2016) Waterscape determinants of net mercury methylation in a tropical wetland. Environ Res 150:438–445CrossRefGoogle Scholar
  42. Lovley DR, Klug MJ (1986) Model for the distribution of sulfate reduction and methanogenesis in freshwater sediments. Geochim Cosmochim Acta 50:11–18CrossRefGoogle Scholar
  43. Lovley DR, Phillips EJ (1987) Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl Environ Microbio 53:1536–1540Google Scholar
  44. Lyman SN, Jaffe DA (2012) Formation and fate of oxidized mercury in the upper troposphere and lower stratosphere. Nat Geosci 5:114–117CrossRefGoogle Scholar
  45. Mansilla-Rivera I, Rodríguez-Sierra CJ (2011) Metal levels in fish captured in puerto rico and estimation of risk from fish consumption. Arch Environ Contam Toxicol 60:132–144CrossRefGoogle Scholar
  46. Marvin-DiPasquale MC, Agee J (2003) Microbial mercury cycling in sediments of the San Francisco Bay-Delta. Estuaries 26:1517–1528CrossRefGoogle Scholar
  47. Marvin-DiPasquale MC, Agee J, Bouse R, Jaffe B (2003) Microbial cycling of mercury in contaminated pelagic and wetland sediments of San Pablo Bay, California. Environ Geol 43:260–267CrossRefGoogle Scholar
  48. Marvin-DiPasquale MC, Agee J, McGowan C, Oremland RS, Thomas M, Krabbenhoft D, Gilmour CC (2000) Methyl-mercury degradation pathways: a comparison among three mercury-impacted ecosystems. Environ Sci Technol 34:4908–4916CrossRefGoogle Scholar
  49. Marvin-DiPasquale MC, Agee JL, Kakouros E, Kieu LH, Fleck JA, Alpers CN (2011) The effects of sediment and mercury mobilization in the South Yuba River and Humbug Creek confluence area, Nevada County, California: Concentrations, speciation and environmental fate-Part 2: Laboratory Experiments. U.S. Geological Survey. Open-File Report no. 2010–1325B. Reston VAGoogle Scholar
  50. Marvin-DiPasquale MC, Alpers CN, Fleck JA (2009a) Mercury, methylmercury, and other constituents in sediment and water from seasonal and permanent wetlands in the Cache Creek Settling Basin and Yolo Bypass, Yolo County, California, 2005−06. U.S. Geological Survey. Open-File Report no. 2009–1182Google Scholar
  51. Marvin-DiPasquale MC, Lutz MA, Brigham ME, Krabbenhoft DP, Aiken GR, Orem WH, Hall BD (2009b) Mercury cycling in stream ecosystems. 2. Benthic methylmercury production and bed sediment-pore water partitioning. Environ Sci Technol 43:2726–2732CrossRefGoogle Scholar
  52. Marvin-DiPasquale MC, Lutz MA, Krabbenhoft DP, Aiken GR, Orem WH, Hall BD, DeWild JF, Brigham ME (2008) Total mercury, methylmercury, methylmercury production potential, and ancillary streambed-sediment and pore-water data for selected streams in Oregon, Wisconsin, and Florida, 2003–04. U.S. Geological Survey. Data Series 375. Report no. 2327-638X,  https://doi.org/10.3133/ds375
  53. Marvin-DiPasquale MC, Oremland RS (1998) Bacterial methylmercury degradation in Florida Everglades peat sediment. Environ Sci Technol 32:2556–2563CrossRefGoogle Scholar
  54. Marvin-DiPasquale MC, Windham-Myers L, Agee JL, Kakouros E, Kieu LH, Fleck JA, Alpers CN, Stricker CA (2014) Methylmercury production in sediment from agricultural and non-agricultural wetlands in the Yolo Bypass, California, USA. Sci Total Environ 484:288–299CrossRefGoogle Scholar
  55. Matthes WJJ, Sholar CJ, George JR (1992) Quality-Assurance Plan for the Analysis of Fluvial Sediment by Laboratories of the U.S. Geological Survey. U.S. Geological Survey, Open-File Report 91–467, Reston VA, p. 37Google Scholar
  56. Mauro J, Guimarães J, Hintelmann H, Watras C, Haack E, Coelho-Souza S (2002) Mercury methylation in macrophytes, periphyton, and water—comparative studies with stable and radio-mercury additions. Anal Bioanal Chem 374:983–989CrossRefGoogle Scholar
  57. McDowell WH, Bowden WB, Asbury CE (1992) Riparian nitrogen dynamics in two geomorphologically distinct tropical rain forest watersheds: subsurface solute patterns. Biogeochem 18:53–75CrossRefGoogle Scholar
  58. McDowell WH, McSwiney CP, Bowden WB (1996) Effects of hurricane disturbance on groundwater chemistry and riparian function in a tropical rain forest. Biotropica 28:577–584CrossRefGoogle Scholar
  59. McDowell WH, Scatena FN, Waide RB, Brokaw N, Camilo GR, Covich AP, Crowl TA, Gonzalez G, Greathouse EA, Klawinski P, Lodge DJ, Lugo AE, Pringle CM, Richardson BA, Richardson MJ, Schaefer DA, Silver WL, Thompson J, Vogt DJ, Vogt KA, Willig MR, Woolbright LL, Zou X, Zimmerman JK (2012) Geographic and ecological setting of the Luquillo Mountains. In: Brokaw N, Crowl TA, Lugo AE, McDowell WH, Scatena FN, Waide RB, Willig MR (eds) A Caribbean forest tapestry: the multidimensional nature of disturbance and response. Oxford University Press, New York, pp. 72–163Google Scholar
  60. Meléndez-Ackerman EJ, Ackerman JD, Rodríguez-Robles JA (2000) Reproduction in an orchid can be resource-limited over its lifetime. Biotropica 32(2):282–290CrossRefGoogle Scholar
  61. Michener R, Lajtha K (2007) Stable isotopes in ecology and environmental science. 2nd edn. Blackwell Publishing, Ltd. OxfordGoogle Scholar
  62. Molina CI, Gibon F-M, Duprey J-L, Dominguez E, Guimarães J-RD, Roulet M (2010) Transfer of mercury and methylmercury along macroinvertebrate food chains in a floodplain lake of the Beni River, Bolivian Amazonia. Sci Total Environ 408:3382–3391CrossRefGoogle Scholar
  63. Murphy SF, Stallard RF (2012) Hydrology and Climate of Four Watersheds in Eastern Puerto Rico. In: Murphy SF, Stallard RF (eds). Water quality and landscape processes of four watersheds in eastern Puerto Rico. Professional Paper 1789. U.S. Geological Survey. Reston VA, pp. 43–83Google Scholar
  64. Murphy SF, Stallard RF, Scholl MA, González G, Torres-Sánchez AJ (2017) Reassessing rainfall in the Luquillo Mountains, Puerto Rico: Local and global ecohydrological implications. PLOS ONE 12:e0180987CrossRefGoogle Scholar
  65. Ortiz-Roque C, López-Rivera Y (2004) Mercury contamination in reproductive age women in a Caribbean island: Vieques. J Epidemiol Community Health 58:756–757CrossRefGoogle Scholar
  66. Pérez ME, Meléndez-Ackermana EJ, Monsegur-Rivera OA (2011) Breeding system and pollination of Gesneria pauciflora (Gesneriaceae), a threatened Caribbean species. Flora 242:8–15CrossRefGoogle Scholar
  67. Peters NE, Shanley JB, Aulenbach BT, Webb RMT, Campbell DH, Hunt RJ, Larsen MC, Stallard RF, Troester J, Walker JF (2006) Water and solute mass balance of five small, relatively undisturbed watersheds in the US. Sci Total Environ 358:221–242CrossRefGoogle Scholar
  68. Rimmer CC, McFarland KP, Evers DC, Miller EK, Aubry Y, Busby D, Taylor RJ (2005) Mercury concentrations in Bicknell’s Thrush and other insectivorous passerines in montane forests of northeastern North America. Ecotoxicology 14:223–240CrossRefGoogle Scholar
  69. Risch MR (2017) Mercury and methylmercury concentrations and litterfall mass in monthly litterfall samples collected at National Atmospheric Deposition Program site at El Verde, Puerto Rico in 2014-2016: U.S. Geological Survey data release,  https://doi.org/10.5066/F7JW8CSF
  70. Roulet M, Guimarães J-RD, Lucotte M (2001) Methylmercury production and accumulation in sediments and soils of an amazonian floodplain—effect of seasonal inundation. Water Air Soil Pollut 128:41–60CrossRefGoogle Scholar
  71. Sastre M, Reyes P, Ramos H, Romero R, Rivera J(1999) Heavy Metal Bioaccumulation in Puerto Rican Blue Crabs (Callinectes spp.) Bull Mar Sci B 4:209–217Google Scholar
  72. Scholl MA, Murphy SF (2014) Precipitation isotopes link regional climate patterns to water supply in a tropical mountain forest, eastern Puerto Rico. Water Resour Res 50:4305–4322CrossRefGoogle Scholar
  73. Scholl MA, Shanley JB, Murphy SF, Willenbring JK, Occhi M, González G (2015) Stable-isotope and solute-chemistry approaches to flow characterization in a forested tropical watershed, Luquillo Mountains, Puerto Rico. Appl Geochem 63:484–497CrossRefGoogle Scholar
  74. Selin NE, Jacob DJ, Yantosca RM, Strode S, Jaeglé L, Sunderland EM (2008) Global 3-D land-ocean-atmosphere model for mercury: present-day versus preindustrial cycles and anthropogenic enrichment factors for deposition. Glob Biogeochem Cycle 22:1–13Google Scholar
  75. Shanley JB, Bishop K (2012) Mercury cycling in forested watersheds. In: Bank MS (ed). Mercury in the environment: pattern and process. University of California Press, Berkeley, CAGoogle Scholar
  76. Shanley JB, Engle MA, Scholl M, Krabbenhoft DP, Brunette R, Olson ML, Conroy ME (2015) High mercury wet deposition at a “clean air” site in Puerto Rico. Environ Sci Technol 49:12474–12482CrossRefGoogle Scholar
  77. Shanley JB, Mast MA, Campbell DH, Aiken GR, Krabbenhoft DP, Hunt RJ, Walker JF, Schuster PF, Chalmers A, Aulenbach BT, Peters NE, Marvin-DiPasquale M, Clow DW, Shafer MM (2008) Comparison of total mercury and methylmercury cycling at five sites using the small watershed approach. Environ Pollut 154:143–154CrossRefGoogle Scholar
  78. Silva-Filho EV, Machado W, Oliveira RR, Sella SM, Lacerda LD (2006) Mercury deposition through litterfall in an Atlantic Forest at Ilha Grande, Southeast Brazil. Chemosphere 65:2477–2484CrossRefGoogle Scholar
  79. Silver WL, Lugo A, Keller M (1999) Soil oxygen availability and biogeochemistry along rainfall and topographic gradients in upland wet tropical forest soils. Biogeochemistry 44:301–328Google Scholar
  80. Sprovieri F et al. (2017) Five-year records of mercury wet deposition flux at GMOS sites in the Northern and Southern hemispheres. Atmos Chem Phys 17:2689–2708CrossRefGoogle Scholar
  81. St. Louis VL, Rudd JWM, Kelly CA, Hall BD, Rolfhus KR, Scott KJ, Lindberg SE, Dong W (2001) Importance of the forest canopy to fluxes of methyl mercury and total mercury to boreal ecosystems. Environ Sci Technol 35:3089–3098CrossRefGoogle Scholar
  82. Stiles FG, Skutch AF (1989) A guide to the birds of Costa Rica. Cornell University Press, Ithica, New YorkGoogle Scholar
  83. Swartzendruber PC, Jaffe DA, Prestbo EM, Weiss-Penzias P, Selin NE, Park R, Jacob D, S Strode S, Jaegle L (2006) Observations of reactive gaseous mercury in the free-troposphere at the Mount Bachelor Observatory. J Geophys Res 111:D24301CrossRefGoogle Scholar
  84. Townsend JM, Rimmer CC, Driscoll CT, McFarland KP, Iñigo-Elias E (2013) Mercury concentrations in tropical resident and migrant songbirds on Hispaniola. Ecotoxicology 22:86–93CrossRefGoogle Scholar
  85. Wardsworth FH (1949) The development of the forest land resources of the Luquillo Mountains of Puerto Rico. Ph.D thesis, Univ. Michigan, AnnArbor, p. 481Google Scholar
  86. Wiener JG, Knights BC, Sandheinrich MB, Jeremiason JD, Brigham ME, Engstrom DR, Woodruff LG, Cannon WF, Balogh SJ (2006) Mercury in soils, lakes, and fish in Voyageurs National Park (Minnesota): importance of atmospheric deposition and ecosystem factors. Environ Sci Technol 40:6261–6268CrossRefGoogle Scholar
  87. Wunderle JM, Arendt WJ (2011) Avian studies and research opportunities in the Luquillo Experimental Forest: a tropical rain forest in Puerto Rico. For Ecol Mgmt 262:33–48CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.U.S. Geological SurveyMontpelierUSA
  2. 2.U.S. Geological SurveyMenlo ParkUSA
  3. 3.Biodiversity Research InstitutePortlandUSA
  4. 4.USFS, International Institute of Tropical ForestryLuquilloUSA
  5. 5.Department of Ecology and Evolutionary BiologyIowa State UniversityAmesUSA
  6. 6.Department of Natural Resources and the EnvironmentUniversity of New HampshireDurhamUSA

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