Abstract
The objectives of the present study were to develop methods for propagating western pearlshell (Margaritifera falcata) for laboratory toxicity testing and evaluate acute and chronic toxicity of chromium VI [Cr(VI)] to the pearlshell and a commonly tested mussel (fatmucket, Lampsilis siliquoidea at 20 °C or in association with a co-stressor of elevated temperature (27 °C), zinc (50 µg Zn/L), or nitrate (35 mg NO3/L). A commonly tested invertebrate (amphipod, Hyalella azteca) also was tested in chronic exposures. Newly transformed pearlshell (~1 week old) were successfully cultured and tested in acute 96 h Cr exposures (control survival 100%). However, the grow-out of juveniles in culture for chronic toxicity testing was less successful and chronic 28-day Cr toxicity tests started with 4 month-old pearlshell failed due to low control survival (39–68%). Acute median effect concentration (EC50) for the pearlshell (919 µg Cr/L) and fatmucket (456 µg Cr/L) tested at 20 °C without a co-stressor decreased by a factor of > 2 at elevated temperature but did not decrease at elevated Zn or elevated NO3. Chronic 28-day Cr tests were completed successfully with the fatmucket and amphipod (control survival 83–98%). Chronic maximum acceptable toxicant concentration (MATC) for fatmucket at 20 °C (26 µg Cr/L) decreased by a factor of 2 at elevated temperature or NO3 but did not decrease at elevated Zn. However, chronic MATC for amphipod at 20 °C (13 µg Cr/L) did not decrease at elevated temperature, Zn, or NO3. Acute EC50s for both mussels tested with or without a co-stressor were above the final acute value used to derive United States Environmental Protection Agency acute water quality criterion (WQC) for Cr(VI); however, chronic MATCs for fatmucket at elevated temperature or NO3 and chronic MATCs for the amphipod at 20 °C with or without elevated Zn or NO3 were about equal to the chronic WQC. The results indicate that (1) the elevated temperature increased the acute Cr toxicity to both mussel species, (2) fatmucket was acutely more sensitive to Cr than the pearlshell, (3) elevated temperature or NO3 increased chronic Cr toxicity to fatmucket, and (4) acute WQC are protective of tested mussels with or without a co-stressor; however, the chronic WQC might not protect fatmucket at elevated temperature or NO3 and might not protect the amphipod at 20 °C with or without elevated Zn or NO3.
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References
ASTM International (2016a) Standard guide for conducting laboratory toxicity tests with freshwater mussels (E2455-06 (2013)). Annual book of ASTM standards, vol 11.06. ASTM International, West Conshohocken
ASTM International (2016b) ASTM International standard guide for conducting acute toxicity tests with fishes, macroinvertebrates, and amphibians (E729-96 (2007)). Annual book of ASTM international standards vol 11.06, ASTM International, West Conshohocken
ASTM International (2016c) Standard test method for measuring the toxicity of sediment-associated contaminants with freshwater invertebrates (E1706-05 (2010)). In: ASTM annual book of standards, vol 11.06, West Conshohocken
Barnhart MC (2006) Bucket of muckets: a compact recirculating system for rearing juvenile freshwater mussels. Aquaculture 254:227–233
Bauer G (1988) Threats to the freshwater pearl mussel Margaritifera margaritifera L. in central Europe. Biol Conserv 45:239–253
Besser JM, Brumbaugh WG, Kembel NE, May TW, Ingersoll CG (2004) Effects of sediment characteristics on the toxicity of chromium (III) and chromium (VI) to the amphipod, Hyalella azteca. Environ Sci Technol 38:6210–6216
Besser JM, Ingersoll CG, Brumbaugh WG, Kemble NE, May TW, Wang N, MacDonald DD, Roberts AD (2015) Toxicity of sediments from lead–zinc mining areas to juvenile freshwater mussels (Lampsilis siliquoidea) compared to standard test organisms. Environ Toxicol Chem 34:626–639
Bogan AE (1993) Freshwater bivalve extinctions (Mollusca: Unionoida): a search for causes. Am Zool 33:599–609
Borgmann U, Norwood WP, Clark C (1993) Accumulation, regulation and toxicity of copper, zinc, lead and mercury in Hyalella azteca. Hydrobiologia 259:79–89
Eaton AD, Clesceri LS, Rice EW, Greenberg AE (2005) Standard Methods for the Examination of Water and Wastewater, 21st edn. Washington, American Public Health Association, Water Environment Federation, American Water Works Association, 1368 pp
Erickson RJ (2015) Toxicity Relationship Analysis Program (TRAP), Ver 1.30a. EPA/600/C-11/002. US Environmental Protection Agency, Washington
Eybe T, Thielen F, Bohn T, Sures B (2013) The first millimetre—rearing juvenile freshwater pearl mussels (Margaritifera margaritifera L.) in plastic boxes. Aquatic Conserv: Mar Freshw Ecosyst 23:964–975
Gillis PL (2011) Assessing the toxicity of sodium chloride to the glochidia of freshwater mussels: implications for salinization of surface waters. Environ Pollut 159:1702–1708
Haag WR (2012) North American freshwater mussels: natural history, ecology, and conservation. Cambridge University Press, New York
Helmstetler H (2006) Population structure and pollutant levels of freshwater mussels in the mid-Columbia River (Master Thesis). Walla Walla College, Walla Walla
Hulstrom LC, Tiller BL (2010) Field summary report for remedial investigation of Hanford Site Releases to the Columbia River, Hanford Site, Washington. Collection of Surface Water, Pore Water, and Sediment Samples for Characterization of Groundwater Upwelling. WCH-380, Rev. 0. [cited 2016 December 16]. http://digital.library.unt.edu/ark:/67531/metadc829169/m1/64/
Ince N, Dirilgen N, Apikyan I (1999) Assessment of toxic interactions of heavy metals in binary mixtures: a statistical approach. Arch Environ Contam Toxicol 36:365
Ingersoll CG, Kunz JL, Hughes JP, Wang N, Ireland DS, Mount DR, Hockett JR, Valenti TW (2015) Relative sensitivity of an amphipod Hyalella azteca, a midge Chironomus dilutus, and a unionid mussel Lampsilis siliquoidea to a toxic sediment. Environ Toxicol Chem 34:1134–1144
Ivey CD, Ingersoll CG, Brumbaugh WG, Hammer E, Mount DR, Hockett JR, Norberg-King TJ, Soucek DJ, Taylor L (2016) Using an inter-laboratory study to revise methods for conducting 10- to 42-day water or sediment toxicity tests with Hyalella azteca. Environ Toxicol Chem 35:2439–2447
Kemble NE, Hardesty DK, Ingersoll CG, Kunz JL, Sibley PK, Calhoun DL, Gilliom RJ, Kuivila KM, Nowell LH, Moran PW (2013) Contaminants in stream sediments from seven US metropolitan areas: II. Sediment toxicity to the amphipod Hyalella azteca and the midge Chironomus dilutus. Arch Environ Contam Toxicol 64:52–64
Lydeard C, Cowie RH, Ponder WF, Bogan AE, Bouchet P, Clark SA, Cummings KS, Frest TJ, Gargominy O, Herbert DG, Hershler R, Perez KE, Roth B, Seddon M, Strong EE, Thompson FG (2004) The global decline of nonmarine mollusks. Bioscience 54:321–330
Lyman RL (1980) Bivalve molluscs in Southern Plateau Prehistory: a discussion and description of three genera. Northwest Sci 54:121–136
March FA, Dwyer FJ, Augspurger T, Ingersoll CG, Wang N, Mebane CA (2007) An evaluation of freshwater mussel toxicity data in the derivation of water quality guidance and standards for copper. Environ Toxicol Chem 26:2066–2074
Miao J, Barnhart MC, Brunson EL, Hardesty DK, Ingersoll CG, Wang N (2010) An evaluation of the influence of substrate on the response of juvenile freshwater mussels (Fatmucket, Lampsilis siliquoidea) in acute water exposure to ammonia. Environ Toxicol Chem 29:2112–2116
Mount DI, Brungs WA (1967) A simplified dosing apparatus for fish toxicology studies. Water Res 1:21–29
Mueller RP, Turner GK, Tiller BL, Welch ID, Bleich MD (2011) Assessment of the species composition, densities, and distribution of native freshwater mussels along the Benton County shoreline of the Hanford Reach, Columbia River, 2004. PNNL-19933. http://www.pnl.gov/main/publications/external/technical_reports/PNNL-19933.pdf. Accessed 16 Dec 2016
Napier BA, Batishko NC, Heise-Craff DA, Jarvis MF, Snyder SF (1995) Identification of contaminants of concern Columbia River Comprehensive Impact Assessment. PNL-10400. http://www.iaea.org/inis/collection/NCLCollectionStore/_Public/26/045/26045343.pdf. Accessed 16 Dec 2016
Pandolfo TJ, Cope WG, Arellano C, Bringolf RB, Barnhart MC, Hammer E (2010) Upper thermal tolerances of early life stages of freshwater mussels. J N Am Benthol Soc 29:959–969
Scheder C, Lerchegger B, Jung M, Csar D, Gumpinger C (2014) Practical experience in the rearing of freshwater pearl mussels (Margaritifera margaritifera): advantages of a work-saving infection approach, survival, and growth of early life stages. Hydrobiologia 735:203–212
Strayer DL, Downing JA, Haag WR, King TL, Layzer JB, Newton TJ, Nichols SJ (2004) Changing perspectives on pearly mussels, North America’s most imperiled animals. Bioscience 54:429–439
Tiller BL, Marceau TE (2006) Radionuclides, trace metals, and organic compounds in shells of native freshwater mussels along the Hanford Reach of the Columbia River: 6000 years before present to current times. WCH-29, Washington Closure Hanford. http://www.osti.gov/scitech/servlets/purl/973105. Accessed 16 Dec 2016
US Department of Energy. 2014. Hanford Site Environmental Report for Calendar Year 2014. DOE-RL-2014-52, Revision 0. http://msa.hanford.gov/files.cfm/DOE-RL-2014-52.pdf. Accessed 16 Dec 2016
US Environmental Protection Agency (1995) 1995 Updates: Water Quality Criteria Documents for the Protection of Aquatic Life in Ambient Water. EPA-820-B-96-001. Office of Water: Washington
US Environmental Protection Agency (2003) Determination of total organic carbon and specific UV absorbance at 254 nm in source water and drinking water. Method 415:3
US Environmental Protection Agency (2007a) Inductively coupled plasma-mass spectrometry, Method 6020A. SW-846 Online—Test methods for evaluating solid waste, physical/chemical methods
US Environmental Protection Agency (2007b) Determination of inorganic anions by ion chromatography, Method 9056. SW-846 Online—Test methods for evaluating solid waste, physical/chemical methods
US Environmental Protection Agency (2016) National Recommended Water Quality Criteria. https://www.epa.gov/wqc/national-recommended-water-quality-criteria-aquatic-life-criteria-table. Accessed 16 Dec 2016
Wang N, Ingersoll CG, Hardesty DK, Ivey CD, Kunz JL, May TW, Dwyer FJ, Roberts AD, Augspurger T, Kane CM, Neves RJ, Barnhart MC (2007a) Acute toxicity of copper, ammonia, and chlorine to glochidia and juveniles of freshwater mussels (Unionidae). Environ Toxicol Chem 26:2036–2047
Wang N, Ingersoll CG, Greer IE, Hardesty DK, Ivey CD, Kunz JL, Brumbaugh WG, Dwyer FJ, Roberts AD, Augspurger T, Kane CM, Neves RJ, Barnhart MC (2007b) Chronic toxicity of copper and ammonia to juvenile freshwater mussels (Unionidae). Environ Toxicol Chem 26:2048–2056
Wang N, Ingersoll CG, Ivey CD, Hardesty DK, May TW, Augspurger T, Roberts AD, van Genderen E, Barnhart MC (2010) Sensitivity of early life stages of freshwater mussels (Unionidae) to acute and chronic toxicity of lead, cadmium, and zinc in water. Environ Toxicol Chem 29:2053–2063
Wang N, Consbrock R, Ingersoll CG, Barnhart MC (2011) Evaluation of influence of sediment on the sensitivity of a unionid mussel (Lampsilis siliquoidea) to ammonia in 28-day water exposures. Environ Toxicol Chem 30:2270–2276
Wang N, Ingersoll CG, Kunz JL, Brumbaugh WG, Kane CM, Evans RB, Alexander S, Walker C, Bakaletz S, Lott RC (2013) Toxicity of sediments potentially contaminated by coal or natural gas mining-related activities to unionid mussels and commonly tested benthic invertebrates. Environ Toxicol Chem 32:207–221
Wang N, Dorman RA, Ingersoll CG, Hardest DK, Brumbaugh WG, Hammer EJ, Bauer CR, Mount DR (2016a) Acute and chronic toxicity of sodium sulfate to four freshwater organisms in water-only exposures. Environ Toxicol Chem 35:115–127
Wang N, Ivey CD, Ingersoll CG, Brumbaugh WG, Alvarez D, Hammer EJ, Bauer CR, Augspurger T, Raimondo S, Barnhart MC (2016b) Acute sensitivity of a broad range of freshwater mussels to chemicals with different modes of toxic action. Environ Toxicol Chem. doi:10.1002/etc.3642
Acknowledgments
This project was sponsored in part by United States Fish and Wildlife Service (USFWS) under Inter/Intra-Agency Agreement 4500034106 and United States Environmental Protection Agency (USEPA) under Interagency Agreement/Amendment DW-14-95822701-0. The authors thank the members of the Hanford Natural Resource Trustee Council, and Burt Shephard and Teresa Norberg-King of the USEPA for their suggestions on study designs. The authors also thank the staff in the Toxicology Branch and Environmental Chemistry Branch of the United States Geological Survey, Columbia Environmental Research Center, for technical assistance, Howard JK of the Nature Conservancy, CA, for collecting adult western pearlshell, and two anonymous journal reviewers for their comments. The views expressed herein do not necessarily represent the views of the USFWS and USEPA. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the United States Government.
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Wang, N., Kunz, J.L., Ivey, C.D. et al. Toxicity of Chromium (VI) to Two Mussels and an Amphipod in Water-Only Exposures With or Without a Co-stressor of Elevated Temperature, Zinc, or Nitrate. Arch Environ Contam Toxicol 72, 449–460 (2017). https://doi.org/10.1007/s00244-017-0377-x
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DOI: https://doi.org/10.1007/s00244-017-0377-x