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Wastewater discharge with phytoplankton may favor cyanobacterial development in the main drinking water supply river in Uruguay

  • H. Olano
  • F. Martigani
  • A. Somma
  • L. AubriotEmail author
Article

Abstract

The main drinking water source supplying Uruguay (Santa Lucía River, SLR) was threatened in 2013 by a cyanobacterial bloom transported downstream to the water treatment plant that provides water to half of this country population. Several eutrophic reservoirs and stabilization ponds located in the river basin may have been the source of cyanobacterial populations. Such conditions may be common in productive basins; however, few studies have evaluated the impact of microalgae from wastewater stabilization ponds on rivers and its viability downstream. The effect of a dairy wastewater effluent on SLR was studied by means of nutrient and chlorophyll a loads, phytoplankton composition, and effluent incubation in river water in order to evaluate the potential development of cyanobacteria. Total phosphorus and nitrogen loads of the effluent reached up to 25% and 17% of SLR, respectively, while chlorophyll a was up to 37%. The upstream-downstream evaluation showed an increase in dissolved phosphorus and chlorophyll a. The effluent phytoplankton (14.16 mm3 L−1) was dominated by organisms < 10 μm and diatoms (91%), and 3% of cyanobacteria. Cyanobacteria were not detected in SLR, though it appeared downstream of the effluent discharge. At the end of the bioassay, cyanobacterial biomass became the dominant group (37%). This study shows the potential development of cyanobacteria present in industrial effluents when diluted in river water. The effect of phytoplankton discharge from stabilization ponds is not generally considered in monitoring assessments and environment management, despite representing a particular risk if the water body is used as a drinking water source.

Keywords

Dairy effluent Cyanobacterial bloom Stabilization pond Nutrient load Chlorophyll load Eutrophication 

Notes

Acknowledgments

We are grateful to Federica Hirsch, Bruno Cremella, and Mariana Illarze for field work and laboratory analyzes, as well as to the anonymous reviewers for their helpful comments.

Funding information

The study was financed by the Comisión Sectorial de Investigación Científica - Universidad de la República (UDELAR-CSIC) and the Programa de Apoyo a la Investigación Estudiantil (PAIE).

Supplementary material

10661_2019_7288_MOESM1_ESM.docx (13 kb)
ESM 1 (DOCX 12.9 kb)

References

  1. Aguilera, A., Aubriot, L., Echenique, R. O., Salerno, G. L., Brena, B. M., Pírez, M., & Bonilla, S. (2017). Synergistic effects of nutrients and light favor Nostocales over non-heterocystous cyanobacteria. Hydrobiologia, 794(1), 241–255.  https://doi.org/10.1007/s10750-017-3099-1.CrossRefGoogle Scholar
  2. Ahmadi, A., Riahi, H., & Noori, M. (2005). Studies of the effects of environmental factors on the seasonal change of phytoplankton population in municipal waste water stabilization ponds. Toxicological & Environmental Chemistry, 87(4), 543–550.  https://doi.org/10.1080/02772240500315456.CrossRefGoogle Scholar
  3. APHA. (1985). Standard methods for the examination of water and wastewater. Washington: APHA/AWWA/WPCF.Google Scholar
  4. Arocena, R., Chalar, G., Fabián, D., de León, L., Brugnoli, E., Silva, M., et al. (2008). Evaluación ecológica de cursos de agua y biomonitoreo. ((Informe Final) ed.). Montevideo: MVOTMA -DINAMA, Universidad de la República-Facultad de Ciencias.Google Scholar
  5. Aubriot, L., & Bonilla, S. (2018). Regulation of phosphate uptake reveals cyanobacterial bloom resilience to shifting N:P ratios. Freshwater Biology, 63(3), 318–329.  https://doi.org/10.1111/fwb.13066.CrossRefGoogle Scholar
  6. Aubriot, L., Bonilla, S., & Falkner, G. (2011). Adaptive phosphate uptake behaviour of phytoplankton to environmental phosphate fluctuations. FEMS Microbiology Ecology, 77(1), 1–16.  https://doi.org/10.1111/j.1574-6941.2011.01078.x.CrossRefGoogle Scholar
  7. Aubriot, L., Delbene, L., Haakonsson, S., Somma, A., Hirsch, F., & Bonilla, S. (2017). Evolution of eutrophication in Santa Lucía river: influence of land use intensification and perspectives. INNOTEC, 07-16, doi: https://doi.org/10.26461/14.04.
  8. Azevedo, S. M. F. O., Carmichael, W. W., Jochimsen, E. M., Rinehart, K. L., Lau, S., Shaw, G. R., & Eaglesham, G. K. (2002). Human intoxication by microcystins during renal dialysis treatment in Caruaru-Brazil. Toxicology, 181-182, 441–446.CrossRefGoogle Scholar
  9. Barrera Bernal, C., Vázquez, G., Barceló Quintal, I., & Laure Bussy, A. (2008). Microalgal dynamics in batch reactors for municipal wastewater treatment containing dairy sewage water. Water, Air, and Soil Pollution, 190(1), 259–270.  https://doi.org/10.1007/s11270-007-9598-3.CrossRefGoogle Scholar
  10. Bernard, C., Ballot, A., Thomazeau, S., Maloufi, S., Furey, A., Mankiewicz-Boczek, J., et al. (2017). Appendix 2: Cyanobacteria associated with the production of cyanotoxins. In J. Meriluoto, L. Spoof, & G. A. Codd (Eds.), Handbook of cyanobacterial monitoring and cyanotoxin analysis: John Wiley & Sons, Ltd.Google Scholar
  11. Bonilla, S., Haakonsson, S., Somma, A., Gravier, A., Britos, A., Vidal, L., et al. (2015). Cianobacterias y cianotoxinas en ecosistemas límnicos de Uruguay. INNOTEC, 10, 9–22.Google Scholar
  12. Borsuk, M. E., Stow, C. A., & Reckhow, K. H. (2002). Predicting the frequency of water quality standard violations: a probabilistic approach for TMDL development. Environmental Science & Technology, 36(10), 2109–2115.  https://doi.org/10.1021/es011246m.CrossRefGoogle Scholar
  13. Chalar, G., Garcia-Pesenti, P., Silva-Pablo, M., Perdomo, C., Olivero, V., & Arocena, R. (2017). Weighting the impacts to stream water quality in small basins devoted to forage crops, dairy and beef cow production. Limnologica - Ecology and Management of Inland Waters, 65, 76–84.  https://doi.org/10.1016/j.limno.2017.06.002.CrossRefGoogle Scholar
  14. Chen, B., Nam, S.-N., Westerhoff, P. K., Krasner, S. W., & Amy, G. (2009). Fate of effluent organic matter and DBP precursors in an effluent-dominated river: a case study of wastewater impact on downstream water quality. Water Research, 43(6), 1755–1765.  https://doi.org/10.1016/j.watres.2009.01.020.CrossRefGoogle Scholar
  15. Chorus, I., & Bartram, J. (1999). Toxic cyanobacteria in water. A guide to their public health consequences, monitoring and management. London: World Health Organization.CrossRefGoogle Scholar
  16. Codd, G. A., Morrison, L. F., & Metcalf, J. S. (2005). Cyanobacterial toxins: risk management for health protection. Toxicology and Applied Pharmacology, 203(3), 264–272.  https://doi.org/10.1016/j.taap.2004.02.016.CrossRefGoogle Scholar
  17. Conover, W. J., & Iman, R. L. (1976). On some alternative procedures using ranks for the analysis of experimental designs. Communications in Statistics - Theory and Methods, 5(14), 1349–1368.  https://doi.org/10.1080/03610927608827447.CrossRefGoogle Scholar
  18. Cox, P. A., Banack, S. A., Murch, S. J., Rasmussen, U., Tien, G., Bidigare, R. R., Metcalf, J. S., Morrison, L. F., Codd, G. A., & Bergman, B. (2005). Diverse taxa of cyanobacteria produce β-N-methylamino-L-alanine, a neurotoxic amino acid. Proceedings of the National Academy of Sciences of the United States of America, 102(14), 5074–5078.  https://doi.org/10.1073/pnas.0501526102.CrossRefGoogle Scholar
  19. DINAMA (2015). Evolución de la calidad en la cuenca del Santa Lucía. 10 años de información. (pp. 132). Montevideo: MVOTMA.Google Scholar
  20. DINAMA-JICA. (2011). Proyecto sobre control de contaminación y calidad de agua en la cuenca del Río Santa Lucía. Informe final del proyecto. Montevideo: DINAMA.Google Scholar
  21. Divina de Oliveira, M., & Calheiros, D. F. (2000). Flood pulse influence on phytoplankton communities of the south Pantanal floodplain, Brazil. Hydrobiologia, 427(1), 101–112.  https://doi.org/10.1023/a:1003951930525.CrossRefGoogle Scholar
  22. Dodds, W. K., Bouska, W. W., Eitzmann, J. L., Pilger, T. J., Pitts, K. L., Riley, A. J., Schloesser, J. T., & Thornbrugh, D. J. (2009). Eutrophication of U.S. freshwaters: analysis of potential economic damages. Environmental Science & Technology, 43(1), 12–19.  https://doi.org/10.1021/es801217q.CrossRefGoogle Scholar
  23. Dolman, A. M., Rücker, J., Pick, F. R., Fastner, J., Rohrlack, T., Mischke, U., et al. (2012). Cyanobacteria and cyanotoxins: the influence of nitrogen versus phosphorus. PLoS One, 7(6), e38757.  https://doi.org/10.1371/journal.pone.0038757.CrossRefGoogle Scholar
  24. Dreher, T. W., Collart, L. P., Mueller, R. S., Halsey, K. H., Bildfell, R. J., Schreder, P., Sobhakumari, A., & Ferry, R. (2018). Anabaena/Dolichospermum as the source of lethal microcystin levels responsible for a large cattle toxicosis event. Toxicon: X, 100003, 100003.  https://doi.org/10.1016/j.toxcx.2018.100003.CrossRefGoogle Scholar
  25. Drury, B., Rosi-Marshall, E., & Kelly, J. J. (2013). Wastewater treatment effluent reduces the abundance and diversity of benthic bacterial communities in urban and suburban rivers. Applied and Environmental Microbiology, 79(6), 1897–1905.  https://doi.org/10.1128/aem.03527-12.CrossRefGoogle Scholar
  26. Elshorbagy, A., Teegavarapu, R. S. V., & Ormsbee, L. (2005). Total maximum daily load (TMDL) approach to surface water quality management: concepts, issues, and applications. Canadian Journal of Civil Engineering, 32(2), 442–448.  https://doi.org/10.1139/l04-107.CrossRefGoogle Scholar
  27. Fabre, A., Carballo, C., Hernández, E., Piriz, P., Bergamino, L., Mello, L., et al. (2010). El nitrógeno y la relación zona eufótica/zona de mezcla explican la presencia de cianobacterias en pequeños lagos subtropicales, artificiales de Uruguay. Pan-American Journal of Aquatic Sciences, 5, 112–125.Google Scholar
  28. Garnier, J., Ramarson, A., Thieu, V., Némery, J., Théry, S., Billen, G., & Coynel, A. (2018). How can water quality be improved when the urban waste water directive has been fulfilled? A case study of the Lot river (France). Environmental Science and Pollution Research, 25(12), 11924–11939.  https://doi.org/10.1007/s11356-018-1428-1.CrossRefGoogle Scholar
  29. Hickey, C. W., Quinn, J. M., & Davies-Colley, R. J. (1989). Effluent characteristics of dairy shed oxidation ponds and their potential impacts on rivers. New Zealand Journal of Marine and Freshwater Research, 23(4), 569–584.  https://doi.org/10.1080/00288330.1989.9516393.CrossRefGoogle Scholar
  30. Hillebrand, H., Dürselen, C., Kirschtel, D., Zohary, T., & Pollingher, U. (1999). Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology, 35, 403–424.CrossRefGoogle Scholar
  31. Hilton, J., O'Hare, M., Bowes, M. J., & Jones, J. I. (2006). How green is my river? A new paradigm of eutrophication in rivers. Science of the Total Environment, 365(1), 66–83.  https://doi.org/10.1016/j.scitotenv.2006.02.055.CrossRefGoogle Scholar
  32. Huisman, J., & Hulot, F. (2005). Population dynamics of harmful cyanobacteria. In J. Huisman, H. Matthijs, & P. Visser (Eds.), Harmful Cyanobacteria (Vol. 3, pp. 143-176, Aquatic Ecology Series): Springer Netherlands.Google Scholar
  33. Jarvie, H. P., Neal, C., Williams, R. J., Neal, M., Wickham, H. D., Hill, L. K., Wade, A. J., Warwick, A., & White, J. (2002). Phosphorus sources, speciation and dynamics in the lowland eutrophic River Kennet, UK. Science of the Total Environment, 282-283, 175–203.  https://doi.org/10.1016/S0048-9697(01)00951-2.CrossRefGoogle Scholar
  34. Jarvie, H. P., Neal, C., & Withers, P. J. A. (2006). Sewage-effluent phosphorus: a greater risk to river eutrophication than agricultural phosphorus? Science of the Total Environment, 360(1), 246–253.  https://doi.org/10.1016/j.scitotenv.2005.08.038.CrossRefGoogle Scholar
  35. Jüttner, F., & Watson, S. B. (2007). Biochemical and ecological control of geosmin and 2-methylisoborneol in source waters. Applied and Environmental Microbiology, 73(14), 4395–4406.  https://doi.org/10.1128/aem.02250-06.CrossRefGoogle Scholar
  36. Kasprzyk-Hordern, B., Dinsdale, R. M., & Guwy, A. J. (2009). The removal of pharmaceuticals, personal care products, endocrine disruptors and illicit drugs during wastewater treatment and its impact on the quality of receiving waters. Water Research, 43(2), 363–380.  https://doi.org/10.1016/j.watres.2008.10.047.CrossRefGoogle Scholar
  37. Komárek, J. (2013). Cyanoprokaryota: Heterocytous Genera (Vol. 3, Süßwasserflora von Mitteleuropa, Vol. 19/3): Springer Spektrum.Google Scholar
  38. Komárek, J., & Anagnostidis, K. (1998). Cyanoprokaryota. Chroococcales (Vol. 1, Süßwasserflora von Mitteleuropa). Stuttgart: Gustav Fisher Verlag.Google Scholar
  39. Komárek, J., & Anagnostidis, K. (2007). Cyanoprokaryota. Oscillatoriales (Vol. 2, Süßwasserflora von Mitteleuropa). München: Spektrum Akademischer Verlag.Google Scholar
  40. Komárek, J., Kaštovský, J., Mareš, J., & Johansen, J. R. (2014). Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach. Preslia, 86(4), 295–335.Google Scholar
  41. Longhurst, R. D., Roberts, A. H. C., & O'Connor, M. B. (2000). Farm dairy effluent: a review of published data on chemical and physical characteristics in New Zealand. New Zealand Journal of Agricultural Research, 43(1), 7–14.  https://doi.org/10.1080/00288233.2000.9513403.CrossRefGoogle Scholar
  42. Maberly, S. C., King, L., Dent, M. M., Jones, R. I., & Gibson, C. E. (2002). Nutrient limitation of phytoplankton and periphyton growth in upland lakes. Freshwater Biology, 47(11), 2136–2152.  https://doi.org/10.1046/j.1365-2427.2002.00962.x.CrossRefGoogle Scholar
  43. Maere, T., Neethling, J. B., Clark, D., Pramanik, A., & Vanrolleghem, P. A. (2016) Wastewater treatment nutrient regulations: an international perspective with focus on innovation. In WEF/IWA Nutrient Removal and Recovery, Colorado, USA, July 2016 (pp. 10–13): Water Environment Federation and International Water Association.Google Scholar
  44. Mainstone, C. P., & Parr, W. (2002). Phosphorus in rivers — ecology and management. Science of the Total Environment, 282-283, 25–47.  https://doi.org/10.1016/S0048-9697(01)00937-8.CrossRefGoogle Scholar
  45. Masseret, E., Amblard, C., Bourdier, G., & Sargos, D. (2000). Effects of a waste stabilization lagoon discharge on bacterial and phytoplanktonic communities of a stream. Water Environment Research, 72(3), 285–294.  https://doi.org/10.2175/106143000X137509.CrossRefGoogle Scholar
  46. Michalak, A. M., Anderson, E. J., Beletsky, D., Boland, S., Bosch, N. S., Bridgeman, T. B., Chaffin, J. D., Cho, K., Confesor, R., Daloglu, I., DePinto, J. V., Evans, M. A., Fahnenstiel, G. L., He, L., Ho, J. C., Jenkins, L., Johengen, T. H., Kuo, K. C., LaPorte, E., Liu, X., McWilliams, M. R., Moore, M. R., Posselt, D. J., Richards, R. P., Scavia, D., Steiner, A. L., Verhamme, E., Wright, D. M., & Zagorski, M. A. (2013). Record-setting algal bloom in Lake Erie caused by agricultural and meteorological trends consistent with expected future conditions. Proceedings of the National Academy of Sciences, 110(16), 6448–6452.  https://doi.org/10.1073/pnas.1216006110.CrossRefGoogle Scholar
  47. Minnow-Environmental-Inc. (2005). Environmental risk-based approaches for managing municipal wastewater effluent (MWWE). (pp. 230). Ontario The Canadian Council of Ministers of the Environment.Google Scholar
  48. Mosley, L. M. (2015). Drought impacts on the water quality of freshwater systems; review and integration. Earth-Science Reviews, 140, 203–214.  https://doi.org/10.1016/j.earscirev.2014.11.010.CrossRefGoogle Scholar
  49. MVOTMA. (1979). Código de aguas (p. 14). Montevideo: MVOTMA.Google Scholar
  50. MVOTMA (2013). Plan de acción para la protección del agua en la cuenca del Santa Lucía. In MVOTMA (Ed.). Montevideo: Ministerio de Vivienda, Ordenamiento Territorial y Medio Ambiente.Google Scholar
  51. MVOTMA (2017). Plan Nacional de Aguas. In MVOTMA (Ed.). Montevideo: Ministerio de Vivienda, Ordenamiento Territorial y Medio Ambiente.Google Scholar
  52. Neal, C., Jarvie, H. P., Neal, M., Love, A. J., Hill, L., & Wickham, H. (2005). Water quality of treated sewage effluent in a rural area of the upper Thames Basin, southern England, and the impacts of such effluents on riverine phosphorus concentrations. Journal of Hydrology, 304(1), 103–117.  https://doi.org/10.1016/j.jhydrol.2004.07.025.CrossRefGoogle Scholar
  53. Nusch, E. (1980). Comparisons of different methods for chlorophyll and phaeopigments determination. Archiv für Hydrobiologie Ergebnisse der Limnologie, 14, 14–36.Google Scholar
  54. O’Neill, K., Musgrave, I. F., & Humpage, A. (2016). Low dose extended exposure to saxitoxin and its potential neurodevelopmental effects: a review. Environmental Toxicology and Pharmacology, 48, 7–16.  https://doi.org/10.1016/j.etap.2016.09.020.CrossRefGoogle Scholar
  55. Padulles, M. L., Conforti, V. T. D., Nannavecchia, P. S., & O'Farrell, I. (2017). Impacto de la contaminación orgánica sobre el fitoplancton de un arroyo de la llanura pampeana. Ecología Austral, 27, 437–448.  https://doi.org/10.25260/EA.17.27.3.0.579.CrossRefGoogle Scholar
  56. Paerl, H. W., & Huisman, J. (2008). Blooms like it hot. Science, 320, 57–58.CrossRefGoogle Scholar
  57. Reichwaldt, E. S., & Ghadouani, A. (2012). Effects of rainfall patterns on toxic cyanobacterial blooms in a changing climate: between simplistic scenarios and complex dynamics. Water Research, 46(5), 1372–1393.  https://doi.org/10.1016/j.watres.2011.11.052.CrossRefGoogle Scholar
  58. Reynolds, C. S. (2006). The ecology of phytoplankton. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  59. Reynolds, C. S., & Descy, J.-P. (1996). The production, biomass and structure of phytoplankton in large rivers. Archiv für Hydrobiologie, Supplement. Large Rivers, 10(1–4), 161–187.  https://doi.org/10.1127/lr/10/1996/161.CrossRefGoogle Scholar
  60. Rojo, C., Cobelas, M. A., & Arauzo, M. (1994). An elementary, structural analysis of river phytoplankton. Hydrobiologia, 289(1), 43–55.  https://doi.org/10.1007/bf00007407.CrossRefGoogle Scholar
  61. Schindler, D. W. (1977). Evolution of phosphorus limitation in lakes. Science, 195, 260–262.CrossRefGoogle Scholar
  62. Schindler, D. W., Hecky, R. E., Findlay, D. L., Stainton, M. P., Parker, B. R., Paterson, M. J., Beaty, K. G., Lyng, M., & Kasian, S. E. M. (2008). Eutrophication of lakes cannot be controlled by reducing nitrogen input: results of a 37-year whole-ecosystem experiment. Proceedings of the National Academy of Sciences of the United States of America, 105(32), 11254–11258.  https://doi.org/10.1073/pnas.0805108105.CrossRefGoogle Scholar
  63. Sinha, E., Michalak, A. M., & Balaji, V. (2017). Eutrophication will increase during the 21st century as a result of precipitation changes. Science, 357(6349), 405–408.  https://doi.org/10.1126/science.aan2409.CrossRefGoogle Scholar
  64. Sournia, A. (1978). Phytoplankton Manual (Monographs on Oceanographic Methodology. N° 6). Paris: UNESCO.Google Scholar
  65. Sukias, J. P. S., Tanner, C. C., Davies-Colley, R. J., Nagels, J. W., & Wolters, R. (2001). Algal abundance, organic matter, and physico-chemical characteristics of dairy farm facultative ponds: Implications for treatment performance. New Zealand Journal of Agricultural Research, 44(4), 279–296.  https://doi.org/10.1080/00288233.2001.9513485.CrossRefGoogle Scholar
  66. Svirčev, Z., Drobac, D., Tokodi, N., Vidović, M., Simeunović, J., Miladinov-Mikov, M., et al. (2013). Epidemiology of primary liver cancer in Serbia and possible connection with cyanobacterial blooms. Journal of Environmental Science and Health, Part C, 31(3), 181–200.  https://doi.org/10.1080/10590501.2013.824187.CrossRefGoogle Scholar
  67. UDELAR. (2013). Informe sobre la calidad del agua en la cuenca del Río Santa Lucía: estado de situación y recomendaciones (p. 29). Montevideo: Universidad de la República.Google Scholar
  68. URSEA (2017). Informe de situación de las medidas que se están implementado para el aseguramento de la potabilización del agua del sistema de abastecimiento de Montevideo y Laguna del Sauce. In L. A. 5/2016 (Ed.), (pp. 90). Montevideo.Google Scholar
  69. Uruguay (1979). (Vol. 31 de mayo de 1979, pp. p. 1473). Montevideo: Diario Oficial.Google Scholar
  70. Valderrama, J. C. (1981). The simultaneous analysis of total nitrogen and total phosphorus in natural waters. Marine Chemistry, 10, 109–122.CrossRefGoogle Scholar
  71. Vidal, F., Sedan, D., D’Agostino, D., Cavalieri, M., Mullen, E., Parot Varela, M., Flores, C., Caixach, J., & Andrinolo, D. (2017). Recreational exposure during algal bloom in Carrasco Beach, Uruguay: a liver failure case report. Toxins, 9(9), 267.CrossRefGoogle Scholar
  72. Wool, T. A., Davie, S. R., & Rodriguez, H. N. (2003). Development of three-dimensional hydrodynamic and water quality models to support total maximum daily load decision process for the Neuse River Estuary, North Carolina. Journal of Water Resources Planning and Management, 129(4), 295–306.  https://doi.org/10.1061/(ASCE)0733-9496(2003)129:4(295).CrossRefGoogle Scholar
  73. Yu, Q., Chen, Y., Liu, Z., de Giesen, N., & Zhu, D. (2015). The influence of a eutrophic lake to the river downstream: spatiotemporal algal composition changes and the driving factors. Water, 7(5), 2184–2201.CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Grupo de Ecología y Fisiología de Fitoplancton, Sección Limnología, Facultad de CienciasUniversidad de la RepúblicaMontevideoUruguay

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