Abstract
The Coeur d’Alene Lake basin in Northwestern USA has extensive contamination from legacy mining waste, which overlaps with aquatic macrophyte habitat. We examined concentrations of arsenic (As), cadmium (Cd), copper (Cu), lead (Pb), and zinc (Zn) in three macrophytes: Elodea canadensis (submerged), Myriophyllum spicatum (submerged), and Sagittaria latifolia (emergent). We collected macrophyte tissues from five contaminated sites and one uncontaminated site. Tissue concentrations were compared to sediment quality guidelines to assess potential toxicity from metal(loid)s to macrophyte-associated biota. We used threshold and probable effect concentrations to screen for potential toxicity. For the submerged species, the highest site means ± SD (analyte mg/kg dry mass) were 96 ± 61 (As), 18 ± 1.7 (Cd), 24 ± 15 (Cu), 610 ± 392 (Pb), and 1425 ± 222 (Zn). For contaminated sites, the probable effect threshold was exceeded in 38% (As), 45% (Cd), 0% (Cu), 74% (Pb), and 67% (Zn) of submerged species concentrations. Metal concentrations in S. latifolia tubers were lower than the submerged species leaves and shoots. Tuber concentrations did not exceed the probable effect threshold for any metal. Spatial differences in concentrations were most distinct for the submerged species. Our work shows significant amounts of metals are accumulating in some macrophytes of the study area and that biota associated with this vegetation may experience toxicity based upon guideline exceedances. Additionally, managers of invasive plants (e.g., M. spicatum) should consider the ramifications of control efforts given the high metal content of some plants (e.g., disposal issue).
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Data availability
The data and R scripts used in the analyses are available at https://doi.org/10.5281/zenodo.5510699.
References
Badzinski, S. S., Ankney, C. D., & Petrie, S. A. (2006). Influence of migrant tundra swans (Cygnus columbianus) and Canada geese (Branta canadensis) on aquatic vegetation at Long Point Lake Erie Ontario. In A. R. Hanson & J. J. Kerekes (Eds.), Limnology and aquatic birds (pp. 195–211). Dordrecht: Springer, Netherlands. https://doi.org/10.1007/978-1-4020-5556-0_15.
Balistrieri, L. S., & Blank, R. G. (2008). Dissolved and labile concentrations of Cd Cu Pb and Zn in the South Fork Coeur d’Alene River Idaho: Comparisons among chemical equilibrium models and implications for biotic ligand models. Applied Geochemistry, 23(12), 3355–3371. https://doi.org/10.1016/j.apgeochem.2008.06.031
Barrett, P. M., Hull, E. A., Burkart, K., Hargrave, O., McLean, J., Taylor, V. F., et al. (2019). Contrasting arsenic cycling in strongly and weakly stratified contaminated lakes: Evidence for temperature control on sediment–water arsenic fluxes. Limnology and Oceanography, 64(3), 1333–1346. https://doi.org/10.1002/lno.11119
Bender, S. F. (1991). Investigation of the chemical composition and distribution of mining wastes in Killarney Lake Coeur d’Alene area northern Idaho. Moscow: University of Idaho (M.S. thesis).
Bielmyer-Fraser, G. K., Waters, M. N., Duckworth, C. G., Patel, P. P., Webster, B. C., Blocker, A., et al. (2016). Assessment of metal contamination in the biota of four rivers experiencing varying degrees of human impact. Environmental Monitoring and Assessment, 189(1), 23. https://doi.org/10.1007/s10661-016-5738-9
Blus, L. J., Henny, C. J., Hoffman, D. J., Sileo, L., & Audet, D. J. (1999). Persistence of high lead concentrations and associated effects in tundra swans captured near a mining and smelting complex in northern Idaho. Ecotoxicology, 8(2), 125–132. https://doi.org/10.1023/A:1008918819661
Bookstrom, A. A., Box, S. E., Fousek, R. S., Wallis, J. C., Kayser, H. Z., & Jackson, B. L. (2013). Baseline and historic depositional rates and lead concentrations floodplain sediments Lower Coeur d’Alene River, Idaho. U.S. Geological Survey (Open-File Report No. 2004–1211, Version 1.1).
Bookstrom, A. A., Box, S. E., Jackson, B. L., Brandt, T. R., Derkey, P. D., & Munts, S. R. (1999). Digital map of surficial geology wetlands and deepwater habitats Coeur d’Alene River Valley Idaho. U.S: Geological Survey. https://doi.org/10.3133/ofr99548 (Open-File Report No. 99–548).
Borch, T., Kretzschmar, R., Kappler, A., Cappellen, P. V., Ginder-Vogel, M., Voegelin, A., & Campbell, K. (2010). Biogeochemical redox processes and their impact on contaminant dynamics. Environmental Science & Technology, 44(1), 15–23. https://doi.org/10.1021/es9026248
Bunluesin, S., Pokethitiyook, P., Lanza, G. R., Tyson, J. F., Kruatrachue, M., Xing, B., & Upatham, S. (2007). Influences of cadmium and zinc interaction and humic acid on metal accumulation in Ceratophyllum demersum. Water Air and Soil Pollution, 180(1), 225–235. https://doi.org/10.1007/s11270-006-9265-0
Campbell, J. K., Audet, D. J., McDonald, T. L., Kern, J., Strickland, D., & Cernera, P. J. (1999). Heavy metal concentrations in Sagittaria spp tubers (water potato) in the Coeur d’Alene Basin Idaho. Spokane, Washington: US Fish and Wildlife Service.
Cardwell, A. J., Hawker, D. W., & Greenway, M. (2002). Metal accumulation in aquatic macrophytes from southeast Queensland Australia. Chemosphere, 48(7), 653–663. https://doi.org/10.1016/S0045-6535(02)00164-9
Cheruvelil, K. S., Soranno, P. A., Madsen, J. D., & Roberson, M. J. (2002). Plant architecture and epiphytic macroinvertebrate communities: The role of an exotic dissected macrophyte. Journal of the North American Benthological Society, 21(2), 261–277. https://doi.org/10.2307/1468414
Clark, G. M., & Mebane, C. A. (2014). Sources, transport, and trends for selected trace metals and nutrients in the Coeur d’Alene and Spokane River Basins Idaho 1990–2013. U.S. Geological Survey. https://doi.org/10.3133/sir20145204 (Scientific Investigations Report No. 2014–5204).
Coeur d’Alene Tribe., & Avista Corporation. (2017). Coeur d’Alene Reservation aquatic weed management plan. 4(e) condition no. 7 Spokane River hydroelectric project FERC project no. 2545.
Cosio, C., Flück, R., Regier, N., & Slaveykova, V. I. (2014). Effects of macrophytes on the fate of mercury in aquatic systems. Environmental Toxicology and Chemistry, 33(6), 1225–1237. https://doi.org/10.1002/etc.2499
Costa, M. B., Tavares, F. V., Martinez, C. B., Colares, I. G., de Martins, C., & M. G. . (2018). Accumulation and effects of copper on aquatic macrophytes Potamogeton pectinatus L: Potential application to environmental monitoring and phytoremediation. Ecotoxicology and Environmental Safety, 155, 117–124. https://doi.org/10.1016/j.ecoenv.2018.01.062
Deng, H., Ye, Z. H., & Wong, M. H. (2004). Accumulation of lead, zinc, copper and cadmium by 12 wetland plant species thriving in metal-contaminated sites in China. Environmental Pollution, 132(1), 29–40. https://doi.org/10.1016/j.envpol.2004.03.030
Désy, J. C., Amyot, M., Pinel-Alloul, B., & Campbell, P. G. C. (2002). Relating cadmium concentrations in three macrophyte-associated freshwater invertebrates to those in macrophytes, water and sediments. Environmental Pollution, 120(3), 759–769. https://doi.org/10.1016/S0269-7491(02)00174-4
Estell, S. (2019). The growth diet, and consumption of a lentic caddisfly Nectopsyche albida in Coeur d’Alene Lake Idaho. Moscow: University of Idaho (M.S. thesis).
Farag, A. M., Woodward, D. F., Goldstein, J. N., Brumbaugh, W., & Meyer, J. S. (1998). Concentrations of metals associated with mining waste in sediments biofilm benthic macroinvertebrates and fish from the Coeur d’Alene River Basin Idaho. Archives of Environmental Contamination and Toxicology, 34(2), 119–127. https://doi.org/10.1007/s002449900295
Gustavson, K. E., Barnthouse, L. W., Brierley, C. L., Clark, E. H., II., & I., & Ward, C. H. . (2007). Superfund and mining megasites. ACS Publications. https://doi.org/10.1021/es0725091
Hansel, C. M., Fendorf, S., Sutton, S., & Newville, M. (2001). Characterization of Fe plaque and associated metals on the roots of mine-waste impacted aquatic plants. Environmental Science & Technology, 35(19), 3863–3868. https://doi.org/10.1021/es0105459
Haus, K. L., Hooper, R. L., Strumness, L. A., & Mahoney, J. B. (2008). Analysis of arsenic speciation in mine contaminated lacustrine sediment using selective sequential extraction HR-ICPMS and TEM. Applied Geochemistry, 23(4), 692–704. https://doi.org/10.1016/j.apgeochem.2007.11.005
Helsel, D. R. (2012). Statistics for censored environmental data using Minitab and R (2nd ed., vol. 77). Hoboken, New Jersey: John Wiley & Sons.
Helsel, D. R., Hirsch, R. M., Ryberg, K. R., Archfield, S. A., & Gilroy, E. J. (2020). Statistical methods in water resources (p. 484). Reston, Virginia: US Geological Survey. https://doi.org/10.3133/tm4A3 (USGS Numbered Series No. 4-A3).
Horowitz, A. J., Elrick, K. A., Robbins, J. A., & Cook, R. B. (1995). A summary of the effects of mining and related activities on the sediment-trace element geochemistry of Lake Coeur d’Alene, Idaho, USA. Journal of Geochemical Exploration, 52(1), 135–144. https://doi.org/10.1016/0375-6742(94)00041-9
Idaho Department of Environmental Quality., & Coeur d’Alene Tribe. (2009). Coeur d’Alene Lake Management Plan. Retrieved July 13, 2021, from https://www.cdatribe-nsn.gov/lake/wp-content/uploads/sites/7/2020/03/LMP09.pdf
Jackson, L. (1998). Paradigms of metal accumulation in rooted aquatic vascular plants. Science of the Total Environment, 219(2), 223–231. https://doi.org/10.1016/S0048-9697(98)00231-9
Jackson, L. J., & Kalff, J. (1993). Patterns in metal content of submerged aquatic macrophytes: The role of plant growth form*. Freshwater Biology, 29(3), 351–359. https://doi.org/10.1111/j.1365-2427.1993.tb00769.x
Jacob, D. L., & Otte, M. L. (2003). Conflicting processes in the wetland plant rhizosphere: Metal retention or mobilization? Water Air & Soil Pollution: Focus, 3(1), 91–104. https://doi.org/10.1023/A:1022138919019
Kuwabara, J. S., Topping, B. R., Woods, P. F., & Carter, J. L. (2007). Free zinc ion and dissolved orthophosphate effects on phytoplankton from Coeur d’Alene Lake Idaho. Environmental Science & Technology, 41(8), 2811–2817. https://doi.org/10.1021/es062923l
Lahive, E., O’Halloran, J., Jansen, M., & a. K. . (2015). A marriage of convenience; a simple food chain comprised of Lemna minor (L) and Gammarus pulex (L) to study the dietary transfer of zinc. Plant Biology, 17(s1), 75–81. https://doi.org/10.1111/plb.12179
Langman, J. B., Ali, J. D., Child, A. W., Wilhelm, F. M., & Moberly, J. G. (2020). Sulfur species, bonding environment, and metal mobilization in mining-impacted lake sediments: Column experiments replicating seasonal anoxia and deposition of algal detritus. Minerals, 10(10), 849. https://doi.org/10.3390/min10100849
Langman, J. B., Torso, K., & Moberly, J. G. (2018). Seasonal and basinal influences on the formation and transport of dissolved trace metal forms in a mining-impacted riverine environment. Hydrology, 5(3), 35. https://doi.org/10.3390/hydrology5030035
Lee, L. (2017). NADA: nondetects and data analysis for environmental data. https://CRAN.R-project.org/package=NADA
Liao, F. H., Wilhelm, F. M., & Solomon, M. (2016). The effects of ambient water quality and Eurasian watermilfoil on lakefront property values in the Coeur d’Alene area of northern Idaho USA. Sustainability, 8(1), 44. https://doi.org/10.3390/su8010044
MacDonald, D. D., Ingersoll, C. G., & Berger, T. A. (2000). Development and evaluation of consensus-based sediment quality guidelines for freshwater ecosystems. Archives of Environmental Contamination and Toxicology, 39(1), 20–31. https://doi.org/10.1007/s002440010075
Marburger, J. E. (1993). Biology and management of Sagittaria latifolia Willd (broad-leaf arrow-head) for wetland restoration and creation. Restoration Ecology, 1(4), 248–255. https://doi.org/10.1111/j.1526-100X.1993.tb00034.x
Martinez, E. A., Moore, B. C., Schaumloffel, J., & Dasgupta, N. (2002). The potential association between menta deformities and trace elements in Chironomidae (Diptera) taken from a heavy metal contaminated river. Archives of Environmental Contamination and Toxicology, 42(3), 286–291. https://doi.org/10.1007/s00244-001-0190-0
McCune, B., Grace, J., & Urban, D. (2002). Analysis of ecological communities. Gleneden Beach, Oregon: MjM Software Design.
Mebane, C. A. (2010). Cadmium risks to freshwater life: derivation and validation of low-effect criteria values using laboratory and field studies (version 1.2) (Scientific Investigations Report No. 2006–5245) (p. 130). U.S. Geological Survey. Retrieved October 31, 2019, from https://pubs.usgs.gov/sir/2006/5245/
Mix, M. C. (2016). Leaded: The poisoning of Idaho’s Silver Valley. Oregon State University Press.
National Research Council. (2005). Superfund and mining megasites: lessons from the Coeur d’Alene River Basin. Washington, D.C.: National Academies Press. https://doi.org/10.17226/11359
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., et al. (2019). vegan: community ecology package. https://CRAN.R-project.org/package=vegan
Pohlert, T. (2020). PMCMRplus: calculate pairwise multiple comparisons of mean rank sums extended. https://CRAN.R-project.org/package=PMCMRplus
R Core Team. (2019). R v. 3.6.2: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/
Rabe, F., & Bauer, S. (1977). Heavy metals in lakes of the Coeur d’Alene River Valley, Idaho. Northwest Science, 51(3).
Rai, P. K. (2009). Heavy metal phytoremediation from aquatic ecosystems with special reference to macrophytes. Critical Reviews in Environmental Science and Technology, 39(9), 697–753. https://doi.org/10.1080/10643380801910058
Scheffer, M., & van Nes, E. H. (2007). Shallow lakes theory revisited: Various alternative regimes driven by climate, nutrients, depth and lake size. Hydrobiologia, 584(1), 455–466. https://doi.org/10.1007/s10750-007-0616-7
Smith, K. S., Balistrieri, L. S., & Todd, A. S. (2015). Using biotic ligand models to predict metal toxicity in mineralized systems. Applied Geochemistry, 57, 55–72. https://doi.org/10.1016/j.apgeochem.2014.07.005
Spalinger, S. M., von Braun, M. C., Petrosyan, V., & von Lindern, I. H. (2007). Northern Idaho house dust and soil lead levels compared to the Bunker Hill superfund site. Environmental Monitoring and Assessment, 130(1), 57–72. https://doi.org/10.1007/s10661-006-9450-z
Spears, B. L., Hansen, J. A., & Audet, D. J. (2007). Blood lead concentrations in waterfowl utilizing Lake Coeur d’Alene, Idaho. Archives of Environmental Contamination and Toxicology, 52(1), 121–128. https://doi.org/10.1007/s00244-006-0061-z
Sprague, R. (1999). An anthropological summary of the dependence of the Coeur d’Alene Tribe upon Coeur d’Alene Lake. Moscow, ID.
Stow, C. A., Webster, K. E., Wagner, T., Lottig, N., Soranno, P. A., & Cha, Y. (2018). Small values in big data: The continuing need for appropriate metadata. Ecological Informatics, 45, 26–30. https://doi.org/10.1016/j.ecoinf.2018.03.002
Strawn, D. G. (2018). Review of interactions between phosphorus and arsenic in soils from four case studies. Geochemical Transactions, 19(1), 10. https://doi.org/10.1186/s12932-018-0055-6
Strawn, D. G., Hickey, P. J., McDaniel, P. A., & Baker, L. L. (2012). Distribution of As, Cd, Pb, and Zn in redox features of mine-waste impacted wetland soils. Journal of Soils and Sediments, 12(7), 1100–1110. https://doi.org/10.1007/s11368-012-0543-8
Thiébaut, G., Gross, Y., Gierlinski, P., & Boiché, A. (2010). Accumulation of metals in Elodea canadensis and Elodea nuttallii: Implications for plant–macroinvertebrate interactions. Science of the Total Environment, 408(22), 5499–5505. https://doi.org/10.1016/j.scitotenv.2010.07.026
Torso, K., Scofield, B. D., & Chess, D. W. (2020). Variations in aquatic macrophyte phenology across three temperate lakes in the Coeur d’Alene Basin. Aquatic Botany, 162, 103209. https://doi.org/10.1016/j.aquabot.2020.103209
U.S. Environmental Protection Agency. (1996). Method 3050B: Acid digestion of sediments, sludges, and soils. Revision 2. Washington, DC. Retrieved August 10, 2021, from https://www.epa.gov/sites/default/files/2015-06/documents/epa-3050b.pdf
U.S. Environmental Protection Agency. (2002). The Bunker Hill mining and metallurgical complex: operable unit 3, record of decision. Region 10. Retrieved October 31, 2019, from https://nepis.epa.gov/Exe/ZyPURL.cgi?Dockey=P100SHZQ.TXT
U.S. Environmental Protection Agency. (2014). Method 6010D (SW-846): Inductively coupled plasma-atomic emission spectrometry, revision 4. Washington, DC. Retrieved August 10, 2021, from https://www.epa.gov/sites/default/files/2015-12/documents/6010d.pdf
U.S. Environmental Protection Agency. (2015). Fourth five-year review report for Bunker Hill superfund site Shoshone and Kootenai counties, Idaho. Region 10. Retrieved August 17, 2021, from https://semspub.epa.gov/src/document/10/500018092
U.S. Geological Survey. (2019). National water information system data available on the world wide web. station 12413860 water years 2005–2018. Retrieved October 31, 2019, from https://waterdata.usgs.gov/id/nwis/wys_rpt/?site_no=12413860
Weis, J. S., & Weis, P. (2004). Metal uptake, transport and release by wetland plants: Implications for phytoremediation and restoration. Environment International, 30(5), 685–700. https://doi.org/10.1016/j.envint.2003.11.002
Wickham, H. (2017). tidyverse: easily install and load the “tidyverse.” https://CRAN.R-project.org/package=tidyverse
Woods, P. F., & Beckwith, M. A. (1997). Nutrient and trace-element enrichment of Coeur d’Alene Lake, Idaho (p. 93). U.S. Geological Survey. https://doi.org/10.3133/wsp2485 (USGS Numbered Series No. 2485).
Woods, P. F., & Berenbrock, C. E. (1994). Bathymetric map of Coeur D’Alene Lake, Idaho. U.S. Geological Survey. https://doi.org/10.3133/wri944119 (USGS Numbered Series No. 94–4119).
Acknowledgements
The authors would like to thank the Coeur d’Alene Tribe for their unwavering support in protecting the waters of their homeland. Phillip Cernera, Rebecca Stevens, and Laura Laumatia were also instrumental in supporting this work. We thank Darren Lantzer of Tshimakain Creek Laboratories for his helpful suggestions concerning the laboratory analyses. We also acknowledge the field support from Michael George, Styels Peters, and Damien Trevino. We thank the anonymous reviewers who provided insightful comments that greatly improved the manuscript. Lastly, we would like to thank the US Bureau of Reclamation for its support of Tribal Water Quality Programs through grant number R17AP00237-002. This research was also supported by NSF award #1249400.
Funding
The Coeur d’Alene Tribe’s Lake Management Department supported this work through all stages of the project. Lab analyses were funded by a grant (R17AP00237-002) awarded to the Coeur d’Alene Tribe from the U.S. Bureau of Reclamation. Kathleen Torso’s work on the project was supported by the University of Idaho and NSF award #1249400.
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Scofield, B.D., Torso, K., Fields, S.F. et al. Contaminant metal concentrations in three species of aquatic macrophytes from the Coeur d’Alene Lake basin, USA. Environ Monit Assess 193, 683 (2021). https://doi.org/10.1007/s10661-021-09488-y
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DOI: https://doi.org/10.1007/s10661-021-09488-y