Polybrominated diphenyl ether accumulation in an agricultural soil ecosystem receiving wastewater sludge amendments

Environmental Science and Technology

Volumn 48, Issue 12, 2014, Pages 7034-7043

  Gaylor, Michael O ^a,b   Mears, Greg L ^a   Harvey, Ellen ^a   La Guardia, Mark J ^a   Hale, Robert C ^a  

^a VIRGINIA INSTITUTE OF MARINE SCIENCE   (United States)

^b DAKOTA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; ECOSYSTEMS; ISOTOPES; SOILS;

AGRICULTURAL SOILS; BIOTA-SOIL ACCUMULATION FACTORS; POLYBROMINATED DIPHENYL ETHER (PBDES); QUANTITATION LIMITS; SLUDGE-AMENDED SOILS; SOIL INVERTEBRATES; TOTAL ORGANIC CARBON; WASTEWATER SLUDGE;

ORGANIC POLLUTANTS;

CARBON 13; NITROGEN 15; POLYBROMINATED DIPHENYL ETHER;

BIOACCUMULATION; ORGANIC POLLUTANT; PBDE; POLLUTION EFFECT; SOIL AMENDMENT; SOIL BIOTA; SOIL ECOSYSTEM; SOIL POLLUTION; SPECIES DIVERSITY; WASTEWATER;

ARTICLE; BIOACCUMULATION; BIOTA; CARABIDAE; EARTHWORM; ECOSYSTEM; FOOD WEB; LIMIT OF QUANTITATION; MANURE; MILLIPEDE; NONHUMAN; SLUDGE; SLUDGE AMENDMENT; SOIL; SOIL AMENDMENT; SOIL INVERTEBRATE; SPIDER; TOTAL ORGANIC CARBON; VEGETATION; WASTE WATER; WASTE WATER MANAGEMENT;

AGRICULTURE; ANIMALS; ARTHROPODS; CARBON ISOTOPES; ECOSYSTEM; ENVIRONMENTAL MONITORING; HALOGENATED DIPHENYL ETHERS; LEAST-SQUARES ANALYSIS; NITROGEN ISOTOPES; OLIGOCHAETA; PLANTS; PRINCIPAL COMPONENT ANALYSIS; SEWAGE; SOIL; SOIL POLLUTANTS; WASTE WATER;

EID: 84902590458     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es5014032     Document Type: Article

References (58)

1. Hardy, M. L. The toxicology of the three commercial polybrominated diphenyl oxide (ether) flame retardants Chemosphere 2002, 46, 757-777
2. Lindberg, P.; Sellström, U.; Häggberg, L.; de Wit, C. A. Higher brominated diphenyl ethers and hexabromocyclododecane found in eggs of peregrine falcons (Falco peregrinus) breeding in Sweden Environ. Sci. Technol. 2004, 38, 93-96
3. Chen, D.; Hale, R. C. A global review of polybrominated diphenyl ether flame retardant contamination in birds Environ. Int. 2010, 36, 800-811
4. La Guardia, M. J.; Hale, R. C.; Harvey, E. Evidence of debromination of decabromodiphenyl ether (BDE-209) in biota from a wastewater receiving stream Environ. Sci. Technol. 2007, 41, 6663-6670
5. La Guardia, M. J.; Hale, R. C.; Harvey, E.; Mainor, T. M.; Ciparis, S. In situ accumulation of HBCD, PBDEs, and several alternative flame retardants in the bivalve (Corbicula fluminea) and gastropod (Elimia proxima) Environ. Sci. Technol. 2012, 46, 5798-5805
6. Hale, R. C.; La Guardia, M. J.; Harvey, E.; Mainor, T. M. Potential role of fire retardant-treated polyurethane foam as a source of brominated diphenyl ethers to the US environment Chemosphere 2002, 46, 729-735
7. Hale, R. C.; La Guardia, M. J.; Harvey, E.; Gaylor, M. O.; Mainor, T. M. Brominated flame retardant concentrations and trends in abiotic media Chemosphere 2006, 64, 181-186
8. Allen, J. G.; McClean, M. D.; Stapleton, H. M.; Webster, T. F. Linking PBDEs in house dust to consumer products using x-ray fluorescence Environ. Sci. Technol. 2008, 42, 4222-4228
9. Webster, T. F.; Harrad, S.; Millette, J. R.; Holbrook, R. D.; Davis, J. M.; Stapleton, H. M.; Allen, J. G.; McClean, M. D.; Ibarra, C.; Abdallah, M. A.; Covaci, A. Identifying transfer mechanisms and sources of decabromodiphenyl ether (BDE 209) in indoor environments using environmental microscopy Environ. Sci. Technol. 2009, 43, 3067-3072
10. Andrade, N. A.; McConnell, L. L.; Torrents, A.; Ramirez, M. Persistence of polybrominated diphenyl ethers in agricultural soils after biosolids applications J. Agric. Food Chem. 2010, 58, 3077-3084
11. Eljarrat, E.; Marsh, G.; Labandeira, A.; Barcelo, D. Effects of sewage sludges contaminated with polybrominated diphenyl ethers on agricultural soils Chemosphere 2008, 71, 1079-1086
12. Gaylor, M. O.; Harvey, E.; Hale, R. C. Polybrominated diphenyl ether (PBDE) accumulation by earthworms (Eisenia fetida) exposed to biosolids-, polyurethane foam microparticle-, and Penta-BDE-amended soils Environ. Sci. Technol. 2013, 47, 13831-13839
13. Hale, R. C.; La Guardia, M. J.; Harvey, E.; Gaylor, M. O.; Mainor, T. M.; Duff, W. H. Persistent pollutants in land-applied sludge Nature 2001, 412, 140-141
14. Hale, R. C.; La Guardia, M. J.; Havey, E.; Chen, D.; Mainor, T. M.; Luellen, D. R. Polybrominated diphenyl ethers in U.S. sewage sludges and biosolids: temporal and geographical trends and uptake by corn following land application Environ. Sci. Technol. 2012, 46, 2055-2063
15. Xia, K.; Hundal, L. S.; Kumar, K.; Armbrust, K.; Cox, A. E.; Granato, T. C. Triclocarban, triclosan, polybrominated diphenyl ethers, and 4-nonylphenol in biosolids and in soil receiving 33-year biosolids application Environ. Toxicol. Chem. 2010, 29, 597-605
16. Emerging technologies for biosolid management; EPA 832-R-06-005, U.S. Environmental Protection Agency: Washington, DC, 2006. http://water.epa.gov/ scitech/wastetech/upload/2007-04-24-mtb-epa-biosolids.pdf.
17. Targeted national sewage sludge survey sampling and analysis technical report; EPA-822-R-08-016, United States EPA Office of Water: Washington, DC, 2009. http://www.epa.gov/waterscience/biosolids/tnsss-stat.pdf.
18. Harrison, E. Z.; Oakes, S. R.; Hysell, M.; Hay, A. Organic chemicals in sewage sludges Sci. Total Environ. 2006, 367, 481-497
19. Kinney, C. A.; Furlong, E. T.; Zaugg, S. D.; Burkhardt, M. R.; Werner, S. L.; Cahill, J. D.; Jorgensen, G. R. Survey of organic wastewater contaminants in biosolids destined for land application Environ. Sci. Technol. 2006, 40, 7207-7215
20. Clarke, B. O.; Smith, S. R. Review of emerging organic contaminants in biosolids and assessment of international research priorities for the agricultural use of biosolids Environ. Int. 2011, 37, 226-247
21. Matscheko, N.; Tysklind, M.; De Wit, C.; Bergek, S.; Andersson, R.; Sellström, U. Application of sewage sludge to arable land-soil concentrations of polybrominated diphenyl ethers and polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls, and their accumulation in earthworms Environ. Toxicol. Chem. 2002, 21, 2515-2525
22. Sellström, U.; de Wit, C. A.; Lundgren, N.; Tysklind, M. Effect of sewage-sludge application on concentrations of higher brominated diphenyl ethers in soils and earthworms Environ. Sci. Technol. 2005, 39, 9064-9070
23. Chen, D.; La Guardia, M. J.; Harvey, E.; Amaral, M.; Wohlfort, K.; Hale, R. C. Polybrominated diphenyl ethers in Peregrine Falcon (Falco peregrinus) eggs from the northeastern US Environ. Sci. Technol. 2008, 42, 7594-7600
24. La Guardia, M. J.; Hale, R. C.; Harvey, E. Detailed polybrominated diphenyl ether (PBDE) congener composition of the widely used penta-, octa-, and deca-PBDE technical flame retardant mixtures Environ. Sci. Technol. 2006, 40, 6247-6254
25. Simonich, S. L.; Hites, R. A. Organic pollutant accumulation in vegetation Environ. Sci. Technol. 1995, 29, 2905-2914
26. Huang, H.; Zhang, S.; Christie, P.; Wang, S.; Xie, M. Behavior of decabromodiphenyl ether (BDE-209) in the soil-plant system: uptake, translocation, and metabolism in plants and dissipation in soil Environ. Sci. Technol. 2010, 44, 663-667
27. Vrkoslavová, J.; Demnerová, K.; Macková, M.; Zemanová, T.; Macek, T.; Hajšlová, J.; Pulkrabová, J.; Hrádková, P.; Stiborová, H. Absorption and translocation of polybrominated diphenyl ethers (PBDEs) by plants from contaminated sewage sludge Chemosphere 2012, 81, 381-386
28. Mueller, K. E.; Mueller-Spitz, S. R.; Henry, H. F.; Vonderheide, A. P.; Soman, R. S.; Kinkle, B. K.; Shann, J. R. Fate of pentabrominated diphenyl ethers in soil: abiotic sorption, plant uptake, and the impact of interspecific plant interactions Environ. Sci. Technol. 2006, 40, 6662-6667
29. Blankenship, A. L.; Zwiernik, M. J.; Coady, K. K.; Kay, D. P.; Newsted, J. L.; Strause, K.; Park, C.; Bradley, P. W.; Neigh, A. M.; Millsap, S. D.; Jones, P. D.; Giesy, J. P. Differential accumulation of polychlorinated biphenyl congeners in the terrestrial food web of the Kalamazoo River superfund site, Michigan Environ. Sci. Technol. 2005, 39, 5954-5963
30. Jager, T.; Fleuren, R. H. L. J.; Hogendoorn, E. A.; De Korte, G. Elucidating routes of exposure for organic chemicals in the earthworm, Eisenia andrei (Oligochaeta) Environ. Sci. Technol. 2003, 37, 3399-3404
31. Alexander, M. Aging, bioavailability, and overestimation of risk from environmental pollutants Environ. Sci. Technol. 2000, 34, 4259-4265
32. Gaylor, M. O.; Harvey, E.; Hale, R. C. House crickets accumulate polybrominated diphenyl ethers (PBDEs) directly from polyurethane foam common in consumer products Chemosphere 2012, 86, 500-505
33. Nyholm, J. R.; Asamoah, R. K.; van der Wal, L.; Danielsson, C.; Andersson, P. L. Accumulation of polybrominated diphenyl ethers, hexabromobenzene, and 1,2-dibromo-4-(1,2-dibromoethyl)-cyclohexane in earthworm (Eisenia fetida): effects of soil type and aging Environ. Sci. Technol. 2010, 44, 9189-9194
34. Liang, X.; Zhu, S.; Chen, P.; Zhu, L. Bioaccumulation and bioavailability of polybrominated diphenyl ethers (PBDEs) in soil Environ. Pollut. 2010, 158, 2387-2392
35. Wu, J.; Luo, X.; Zhang, Y.; Chen, S.; Mai, B.; Guan, Y.; Yang, Z. Residues of polybrominated diphenyl ethers in Frogs (Rana limnocharis) from a contaminated site, South China: tissue distribution, biomagnification and maternal transfer Environ. Sci. Technol. 2009, 43, 5212-5217
36. Stroomberg, G. J.; Ariese, F.; Gestel, C. A. M.; Van Hattum, B.; Velthorst, N. H.; Van Straalen, N. M. Pyrene biotransformation products as biomarkers of polycyclic aromatic hydrocarbon exposure in terrestrial isopoda: concentration-response relationship and field study in a contaminated forest Environ. Toxicol. Chem. 2003, 22, 224-231
37. Xia, K.; Luo, M. B.; Lusk, C.; Armbrust, K.; Skinner, L.; Sloan, R. Polybrominated diphenyl ethers (PBDEs) in biota representing different trophic levels of the Hudson River, New York: From 1999 to 2005 Environ. Sci. Technol. 2008, 42, 4331-4337
38. Bartrons, M.; Grimalt, J. O.; Catalan, J. Concentration changes of organochlorine compounds and polybrominated diphenyl ethers during metamorphosis of aquatic insects Environ. Sci. Technol. 2007, 41, 6137-6141
39. Li, M. H.; McKee, M. J. Toxicokinetics of 2,2′,4,4′- and 3,3′,4,4′-tetrachlorobiophenyl congeners in the house cricket Ecotoxicol. Environ. Saf. 1992, 24, 309-318
40. He, S. X.; Nicholson, R. A.; Law, F. C. Benzo(a)pyrene toxicokinetics in the cricket following injection into the hemolymph Environ. Toxicol. Pharmacol. 1998, 6, 81-89
41. Foelix, R. F. Biology of Spiders, 3 rd ed.; Oxford University Press: New York, 2011.
42. Walters, D. M.; Fritz, K. M.; Otter, R. R. The dark side of subsidies: adult stream insects export organic contaminants to riparian predators Ecol. Appl. 2008, 18, 1835-1841
43. Walters, D. M.; Mills, M. A.; Fritz, K. M.; Raikow, D. F. Spiders-mediated flux of PCBs from contaminated sediments to terrestrial ecosystems and potential risks to arachnivorous birds Environ. Sci. Technol. 2010, 44, 2849-2856
44. Wilczek, G. Apoptosis and biochemical biomarkers of stress in spiders from industrially polluted areas exposed to high temperature and dimethoate Comp. Biochem. Physiol. 2005, 141 (C) 194-206
45. Di Toro, D. M. Technical basis for establishing sediment quality criteria for nonionic organic chemicals using equilibrium partitioning Environ. Toxicol. Chem. 1991, 10, 1541-1583
46. Achazi, R. K.; Van Gestel, C. A. M. Uptake and accumulation of PAHs by terrestrial invertebrates. In PAHs: an ecotoxicological perspective; Douben, P. E. T., Ed.; John Wiley & Sons: West Sussex, UK, 2003; pp 173-190.
47. Choi, W.; Chang, S. X.; Allen, H. L.; Kelting, D. L.; Ro, H. Irrigation and fertilization effects on foliar and soil carbon and nitrogen isotope ratios in a loblolly pine stand For. Ecol. Manage. 2005, 213, 90-101
48. Wang, H.; Magesan, G. N.; Kimberley, M. O.; Payn, T. W.; Wilks, P. J.; Fisher, C. R. Environmental and nutritional responses of a Pinus radiata plantation to biosolids application Plant Soil 2004, 267, 255-262
49. 15N abundances to trace the fate of waste-derived nitrogen in forest ecosystems: New Zealand case studies Isot. Environ. Health Stud. 2006, 41, 31-38
50. Arenillas, A.; García, R.; Sun, C.; Snape, C. E.; Moreno, A. H.; Rubiera, F.; Pis, J. J. Use of nitrogen stable isotope analysis to understand char nitrogen evolution during the fluidized-bed co-combustion of coal and sewage sludge Energy Fuel. 2005, 19, 485-488
51. Costanzo, S. D.; O'Donohue, M. J.; Dennison, W. C.; Loneragan, N. R.; Thomas, M. A new approach for detecting and mapping sewage impacts Mar. Pollut. Bull. 2001, 42, 149-156
52. Fair, J. M.; Heikoop, J. M. Stable isotope dynamics of nitrogen sewage effluent uptake in a semi-arid wetland Environ. Pollut. 2006, 140, 500-505
53. Van Dover, C. L.; Grassle, J. F.; Fry, B.; Garritt, R. H.; Starczak, V. R. Stable isotope evidence for entry of sewage-derived organic material into a deep-sea food web Nature 1993, 360, 153-156
54. McNabb, D. M.; Halaj, J.; Wise, D. H. Inferring trophic positions of generalist predators and their linkage to the detrital food web in agroecosystems: a stable isotope analysis Pedobiologia 2001, 45, 289-297
55. Wise, D. H.; Moldenhauer, D. M.; Halaj, J. Using stable isotopes to reveal shifts in prey consumption by generalist predators Ecol. Appl. 2006, 16, 865-876
56. Haagvar, S. Log-normal distribution of dominance as an indicator of stressed soil microarthropod communities Acta Zool. Fenn. 1994, 195, 71-80
57. Braekevelt, E.; Tittlemier, S. A.; Tomy, G. T. Direct measurement of octanol-water partition coefficients of some environmentally relevant brominated diphenyl ether congeners Chemosphere 2003, 51, 563-567
58. Wania, F.; Dugani, C. B. Assessing the long-range transport potential of polybrominated diphenyl ethers: a comparison of four multimedia models Environ. Toxicol. Chem. 2003, 22, 1252-1261