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Environmental Management

, Volume 63, Issue 1, pp 136–147 | Cite as

A prescription for drug-free rivers: uptake of pharmaceuticals by a widespread streamside willow

  • Carmen G. Franks
  • David W. Pearce
  • Stewart B. RoodEmail author
Article

Abstract

Following human excretion and limited removal with wastewater treatment, pharmaceuticals are accumulating in rivers worldwide. These chemicals can challenge the health of fish and aquatic organisms and since rivers provide drinking water sources, there is concern for cumulative exposure to humans. In this study, we discovered that sandbar willow (Salix exigua), a predominant riparian shrub along streams throughout North America, has the capacity to quickly remove pharmaceuticals from aqueous solutions. Our study tracked [3H]- or [14C]-labeled substances including 17α-ethynylestradiol (EE2), a synthetic estrogen in oral contraceptives; the antihypertensive, diltiazem (DTZ); and the anti-anxiety drug, diazepam (DZP); and for comparison, atrazine (ATZ), a root-absorbed herbicide. In growth chambers, willow saplings removed 40–80% of the substances from solutions in 24 h. Following uptake, the EE2 and DTZ were retained within the roots, while DZP and ATZ were partly passed on to the shoots. The absorbed EE2 was unextractable and apparently bound to the root tissue, while DTZ, DZP, and ATZ remained largely soluble (extractable). The uptake and translocation of the pharmaceuticals, reflected in the transpiration stream and root concentration factors, were reasonably predicted from their physicochemical properties, including octanol-water partitioning coefficients. These findings suggest the removal of pharmaceuticals as an unrecognized ecosystem service provided by riparian vegetation and especially the inundation tolerant sandbar willow. This encourages the conservation of riparian willows that line riverbanks, to remove pharmaceuticals and other contaminants. This phytoremediation also encourages the preservation of complex, braided channels and islands, which increase the extent of stream shorelines and riparian willows.

Keywords

Atrazine Diazepam Diltiazem Ethynylestradiol Phytoremediation Salix exigua 

Notes

Acknowledgements

This study extended from the MSc thesis of the first author and we extend thanks to committee members Alice Hontela and Bryan Kolb (University of Lethbridge) and external examiner David Reid (University of Calgary). Funding to SBR was provided by the Natural Sciences and Engineering Research Council of Canada, Alberta Innovates and Alberta Environment and Parks.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Adeel M, Song X, Wang Y, Francis D, Yang Y (2017) Environmental impact of estrogens on human, animal and plant life: a critical review. Environ Int 99:107–119.  https://doi.org/10.1016/j.envint.2016.12.010 CrossRefGoogle Scholar
  2. Amlin NA, Rood SB (2001) Inundation tolerances of riparian willows and cottonwoods. JAWRA J Am Water Resour As 37:1709–1720.  https://doi.org/10.1111/j.1752-1688.2001.tb03671.x CrossRefGoogle Scholar
  3. Bircher S, Card M, Zhai G, Chin YP, Schnoor JL (2015) Sorption, uptake, and biotransformation of 17β‐estradiol, 17α‐ethinylestradiol, zeranol, and trenbolone acetate by hybrid poplar. Environ Toxicol Chem 34:2906–2913.  https://doi.org/10.1002/etc.3166 CrossRefGoogle Scholar
  4. Boxall ABA, Rudd MA, Brooks BW et al. (2012) Pharmaceuticals and personal care products in the environment: What are the big questions? Environ Health Persp 120:1221–1229.  https://doi.org/10.1289/ehp.1104477 CrossRefGoogle Scholar
  5. Briggs GG, Bromilow RH, Evans AA (1982) Relationships between lipophilicity and root uptake and translocation of non-ionised chemicals by barley. Pestic Sci 13:495–504.  https://doi.org/10.1002/ps.278013056 CrossRefGoogle Scholar
  6. Burken JG, Schnoor JL (1997) Uptake and metabolism of atrazine by poplar trees. Environ Sci Technol 31:1399–1406.  https://doi.org/10.1021/es960629v CrossRefGoogle Scholar
  7. Burken JG, Schnoor JL (1998) Predictive relationships for uptake of organic contaminants by hybrid poplar trees. Environ Sci Technol 32:3379–3385.  https://doi.org/10.1021/es970817 CrossRefGoogle Scholar
  8. Busov V, Meilan R, Pearce DW, Rood SB, Ma C, Tschaplinski TJ, Strauss SH (2006) Transgenic modification of gai orrgl1 causes dwarfing and alters gibberellins, root growth, and metabolite profiles in Populus. Planta 224:288–299.  https://doi.org/10.1007/s00425-005-0213-9 CrossRefGoogle Scholar
  9. Carter LJ, Williams M, Martin S, Kamaludeen SPB, Kookana RS (2018) Sorption, plant uptake and metabolism of benzodiazepines. Sci Total Environ 628:18–25.  https://doi.org/10.1016/j.scitotenv.2018.01.337 CrossRefGoogle Scholar
  10. Carvalho PN, Basto MCP, Almeida CMR, Brix H (2014) A review of plant-pharmaceutical interactions: from uptake and effects in crop plants to phytoremediation in constructed wetlands. Environ Sci Pollut Res 21:11729–63.  https://doi.org/10.1007/s11356-014-2550-3 CrossRefGoogle Scholar
  11. Clausen LPW, Trapp S (2017) Toxicity of 56 substances to trees. Environ Sci Pollut Res 24:1–13.  https://doi.org/10.1007/s11356-017-9398-2 CrossRefGoogle Scholar
  12. Dettenmaier EM, Doucette WJ, Bugbee B (2009) Chemical hydrophobicity and uptake by plant roots. Environ Sci Technol 43:324–329.  https://doi.org/10.1021/es801751 CrossRefGoogle Scholar
  13. Dong B, Kahl A, Cheng L, Vo H, Ruehl S, Zhang T, Snyder S, Sáez A, Quanrud D, Arnold R (2015) Fate of trace organics in a wastewater effluent dependent stream. Sci Total Environ 518-519:479–490.  https://doi.org/10.1016/j.scitotenv.2015.02.074 CrossRefGoogle Scholar
  14. Doucette WJ, Shunthirasingham C, Dettenmaier EM, Zaleski RT, Fantke P, Arnot JA (2018) A review of measured bioaccumulation data on terrestrial plants for organic chemicals: Metrics, variability, and the need for standardized measurement protocols. Environ Toxicol Chem 37:21–33.  https://doi.org/10.1002/etc.3992 CrossRefGoogle Scholar
  15. Ebele AJ, Abdallah MA-E, Harrad S (2017) Pharmaceuticals and personal care products (PPCPs) in the freshwater aquatic environment. Emerg Contam 3:1–16.  https://doi.org/10.1016/j.ecmcon.2016.12.004 CrossRefGoogle Scholar
  16. Elias AA, Busov VB, Kosola KR, Ma C, Etherington E, Shevchenko O, Gandhi H, Pearce DW, Rood SB, Strauss SH (2012) Green revolution trees: Semidwarfism transgenes modify gibberellins, promote root growth, enhance morphological diversity, and reduce competitiveness in hybrid poplar. Plant Physiol 160:1130–44.  https://doi.org/10.1104/pp.112.200741 CrossRefGoogle Scholar
  17. Franks CG (2006) Phytoremdiation of pharmaceuticals with Salix exigua. MSc Thesis, University of Lethbridge, Lethbridge, AB, Canada, 216 pp.Google Scholar
  18. Gibeaut DM, Hulett J, Cramer GR, Seemann JR (1997) Maximal biomass of Arabidopsis thaliana using a simple, low-maintenance hydroponic method and favorable environmental conditions. Plant Physiol 115:317–319.  https://doi.org/10.1104/pp.115.2.317 CrossRefGoogle Scholar
  19. Gilliom RJ, Barbash JE, Crawford CG, Hamilton PA, Martin JD, Nakagaki N, Nowell LH, Scott JC, Stackelberg PE, Thelin GP, Wolock DM (2006) The quality of our nation’s waters: Pesticides in the nation’s streams and ground water, 1992-2001. US Geol Surv Circ 1291:172Google Scholar
  20. Grassi M, Rizzo L, Farina A (2013) Endocrine disruptors compounds, pharmaceuticals and personal care products in urban wastewater: Implications for agricultural reuse and their removal by adsorption process. Environ Sci Pollut Res 20:3616–3628.  https://doi.org/10.1007/s11356-013-1636-7 CrossRefGoogle Scholar
  21. Hayes TB, Anderson LL, Beasley VR et al. (2011) Demasculinization and feminization of male gonads by atrazine: Consistent effects across vertebrate classes. J Steroid Biochem Mol Biol 127:64–73.  https://doi.org/10.1016/j.jsbmb.2011.03.015 CrossRefGoogle Scholar
  22. Heberer T (2002) Occurrence, fate, and removal of pharmaceutical residues in the aquatic environment: a review of recent research data. Toxicol Lett 131:5–17.  https://doi.org/10.1016/S0378-4274(02)00041-3 CrossRefGoogle Scholar
  23. Iori V, Zacchini M, Pietrini F (2013) Growth, physiological response and phytoremoval capability of two willow clones exposed to ibuprofen under hydroponic culture. J Hazard Mater 262:796–804.  https://doi.org/10.1016/j.jhazmat.2013.09.017 CrossRefGoogle Scholar
  24. Jackson MB, Attwood PA (1996) Roots of willow (Salix viminalis L.) show marked tolerance to oxygen shortage in flooded soils and in solution culture. Plant Soil 187:37–45.  https://doi.org/10.1007/BF00011655 CrossRefGoogle Scholar
  25. Jackson J, Sutton R (2008) Sources of endocrine-disrupting chemicals in urban wastewater, Oakland, CA. Sci Total Environ 405:153–160.  https://doi.org/10.1016/j.scitotenv.2008.06.033 CrossRefGoogle Scholar
  26. Karrenberg S, Edwards PJ, Kollmann J (2002) The life history of Salicaceae living in the active zone of floodplains. Freshw Biol 47:733–748.  https://doi.org/10.1046/j.1365-2427.2002.00894.x CrossRefGoogle Scholar
  27. Kolpin DW, Furlong ET, Meyer MT, Thurman EM, Zaugg SD, Barber LB, Buxton HT (2002) Pharmaceuticals, hormones, and other organic wastewater contaminants in US streams, 1999-2000: A national reconnaissance. Environ Sci Technol 36:1202–1211.  https://doi.org/10.1021/es011055j CrossRefGoogle Scholar
  28. Koning CW, Saffran KA, Little JL, Fent L (2006) Water quality monitoring: the basis for watershed management in the Oldman River Basin, Canada. Water Sci Technol 53:153–161.  https://doi.org/10.2166/wst.2006.308 CrossRefGoogle Scholar
  29. Lamshoeft M, Gao Z, Resseler H, Schriever C, Sur R, Sweeney P, Webb S, Zillgens B, Reitz M (2018) Evaluation of a novel test design to determine uptake of chemicals by plant roots. Sci Total Environ 613:10–19.  https://doi.org/10.1016/j.scitotenv.2017.08.314 CrossRefGoogle Scholar
  30. Maharjan, R (2014) Phytoremediation of selected pharmaceuticals and their phytotoxicity to aquatic macrophytes. University of Toledo, Theses and Dissertations. 1710. http://utdr.utoledo.edu/theses-dissertations/1710
  31. Marmiroli M, Pietrini F, Maestri E, Zacchini M, Marmiroli N, Massacci A (2011) Growth, physiological and molecular traits in Salicaceae trees investigated for phytoremediation of heavy metals and organics. Tree Physiol 31:1319–1334.  https://doi.org/10.1093/treephys/tpr090 CrossRefGoogle Scholar
  32. Miller EL, Nason SL, Karthikeyan KG, Pedersen JA (2016) Root uptake of pharmaceuticals and personal care product ingredients. Environ Sci Technol 50:525–41.  https://doi.org/10.1021/acs.est.5b01546 CrossRefGoogle Scholar
  33. Petrie B, Barden R, Kasprzyk-Hordern B (2015) A review on emerging contaminants in wastewaters and the environment: Current knowledge, understudied areas and recommendations for future monitoring. Water Res 72:3–27.  https://doi.org/10.1016/j.watres.2014.08.053 CrossRefGoogle Scholar
  34. Petrie B, Smith BD, Youdan J, Barden R, Kasprzyk-Hordern B (2017) Multi-residue determination of micropollutants in Phragmites australis from constructed wetlands using microwave assisted extraction and ultra-high-performance liquid chromatography tandem mass spectrometry. Anal Chim Acta 959:91–101.  https://doi.org/10.1016/j.aca.2016.12.042 CrossRefGoogle Scholar
  35. Rood SB, Braatne JH, Hughes FMR (2003) Ecophysiology of riparian cottonwoods: stream flow dependency, water relations and restoration. Tree Physiol 23:1113–1124.  https://doi.org/10.1093/treephys/23/16/1113 CrossRefGoogle Scholar
  36. Rood SB, Goater LA, Gill KM, Braatne JH (2011a) Sand and sandbar willow: a feedback loop amplifies environmental sensitivity at the riparian interface. Oecologia 165:31–40.  https://doi.org/10.1007/s00442-010-1758-2 CrossRefGoogle Scholar
  37. Rood SB, Bigelow SG, Hall AA (2011b) Root architecture of riparian trees: River cut-banks provide natural hydraulic excavation, revealing that cottonwoods are facultative phreatophytes. Trees 25:907.  https://doi.org/10.1007/s00468-011-0565-7 CrossRefGoogle Scholar
  38. Shone MGT, Wood AV (1974) A comparison of the uptake and translocation of some organic herbicides and a systemic fungicide by barley: I. Absorption in relation to physico-chemical properties. J Exp Bot 25:390–400.  https://doi.org/10.1093/jxb/25.2.390 CrossRefGoogle Scholar
  39. Shone MGT, Bartlett BO, Wood AV (1974) A comparison of the uptake and translocation of some organic herbicides and a systemic fungicide by barley: II. Relationship between uptake by roots and translocation to shoots. J Exp Bot 25:401–409.  https://doi.org/10.1093/jxb/25.2.401 CrossRefGoogle Scholar
  40. Trapp S (2000) Modelling uptake into roots and subsequent translocation of neutral and ionisable organic compounds. Pest Manag Sci 56:767–778.  https://doi.org/10.1002/1526-4998(200009)56:9<767::AID-PS198>3.0.CO;2-Q CrossRefGoogle Scholar
  41. Trapp S (2004) Plant uptake and transport models for neutral and ionic chemicals. Environ Sci & Pollut Res 11:33–39.  https://doi.org/10.1065/espr2003.08.169 CrossRefGoogle Scholar
  42. USDA, NRCS (2018) The PLANTS database. National Plant Data Team, Greensboro, NC, http://plants.usda 14 February 201827410-4901 USAGoogle Scholar
  43. Verlicchi P, Al Aukidy M, Zambello E (2012) Occurrence of pharmaceutical compounds in urban wastewater: Removal, mass load and environmental risk after a secondary treatment—A review. Sci Total Environ 429:123–55.  https://doi.org/10.1016/j.scitotenv.2012.04.028 CrossRefGoogle Scholar
  44. Wu X, Ernst F, Conkle JL, Gan J (2013) Comparative uptake and translocation of pharmaceutical and personal care products (PPCPs) by common vegetables. Environ Int 60:15–22.  https://doi.org/10.1016/j.envint.2013.07.015 CrossRefGoogle Scholar
  45. Zhang D, Gersberg RM, Ng WJ, Tan SK (2014) Removal of pharmaceuticals and personal care products in aquatic plant-based systems: a review. Environ Pollut 184:620–39.  https://doi.org/10.1016/j.envpol.2013.09.009 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of LethbridgeLethbridgeCanada

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