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Ammonium threshold values for groundwater quality in the EU may not protect groundwater fauna: evidence from an alluvial aquifer in Italy

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Abstract

The European Union (EU) threshold values for \({\text{NH}}_{4}^{ + }\) in groundwater range from a minimum of 0.084 mg l−1 to the maximum allowed of 5 mg l−1. The aim of our study was to determine whether these values are adequate to protect groundwater copepods in alluvial aquifers underlying intensive agriculture. To this end, we analyzed abiotic (including \({\text{NH}}_{4}^{ + }\) concentration) and biological patterns (copepod assemblages) in an alluvial aquifer in an area of intensive agriculture. Groundwater was collected from pre-existing farmer-owned bores. Abiotic and biological patterns were not related to seasonal variation in agricultural practices, and pollutant concentrations were typically below the legal maximum threshold values. However, both abiotic and biological variables differed significantly between two groups of bores, with high and low \({\text{NH}}_{4}^{ + }\) conditions based on separate ecotoxicological assays that set the \({\text{NH}}_{4}^{ + }\) toxicity threshold for stygobiotic copepods at 2.5× below the current EU lowest legal threshold. In particular, phosphorus concentration was higher, and oxygen and copepod abundance and richness were lower in high \({\text{NH}}_{4}^{ + }\) bores. Our results suggest that the present threshold value range for \({\text{NH}}_{4}^{ + }\) adopted by EU Member States may not protect stygobiotic copepod assemblages in alluvial aquifers underlying densely cultivated areas.

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References

  • Aarset, V. & T. Aunaas, 1990. Effects of osmotic stress on oxygen consumption and ammonia excretion of the Arctic sympagic amphipod Gammarus wilkitzkii. Marine Ecology Progress Series 58: 217–224.

    Article  Google Scholar 

  • Anderson, M. J., R. N. Gorley & K. R. Clarke, 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER–E Ltd, Plymouth.

    Google Scholar 

  • Autorità di Bacino dell’Adige, 2008. Quaderno sul bilancio idrico superficiale di primo livello—Bacino idrografico del fiume Adige. A cura della Segreteria Tecnico Operativa. Trento, Maggio 2008. http://www.bacino-adige.it/sito/index.php?option=com_content&view=article&id=104&Itemid=324. Accessed 22 July 2014.

  • Blann, K. L., J. L. Anderson, G. R. Sands & B. Vondracek, 2009. Effects of agricultural drainage on aquatic ecosystems: a review. Critical Reviews in Environmental Science and Technology 39: 909–1001.

    Article  CAS  Google Scholar 

  • Boulton, A. J., G. Fenwick, P. J. Hancock & M. S. Harvey, 2008. Biodiversity, functional roles and ecosystem services of groundwater invertebrates. Invertebrate Systematics 22: 103–116.

    Article  Google Scholar 

  • Camargo, J. A. & A. Alonso, 2006. Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: a global assessment. Environment International 32: 831–849.

    Article  CAS  PubMed  Google Scholar 

  • Camargo, J. A., A. Alonso & M. de la Puente, 2005. Eutrophication downstream from small reservoirs in mountain rivers of central Spain. Water Research 39: 3376–3384.

    Article  CAS  PubMed  Google Scholar 

  • Candela, L., K. J. Wallis & R. M. Mateos, 2008. Non-point pollution of groundwater from agricultural activities in Mediterranean Spain: the Balearic Islands case study. Environmental Geology 54: 587–595.

    Article  CAS  Google Scholar 

  • Carpenter, S. R., N. F. Caraco, D. L. Corell, R. W. Howarth, A. N. Sharpley & V. H. Smith, 1998. Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecological Applications 8: 559–568.

    Article  Google Scholar 

  • Caschetto, M., M. Barbieri, D. M. P. Galassi, L. Mastrorillo, S. Rusi, F. Stoch, A. Di Cioccio & M. Petitta, 2014. Human alteration of groundwater-surface water interactions (Sagittario River, Central Italy): implication for flow regime, contaminant fate and invertebrate response. Environmental Earth Sciences 71: 1791–1807.

    Article  Google Scholar 

  • Chen, J.-C., C.-T. Chen & S.-Y. Cheng, 1994. Nitrogen excretion and changes of hemocyanin, protein and free amino acid levels in the hemolymph of Penaeus monodon exposed to different concentrations of ambient ammonia-N at different salinity levels. Marine Ecology Progress Series 110: 85–94.

    Article  CAS  Google Scholar 

  • Cheng, S.-Y., L.-W. Shieh & J.-C. Chen, 2013. Changes in hemolymph oxyhemocyanin, acid-base balance, and electrolytes in Marsupenaeus japonicus under combined ammonia and nitrite stress. Aquatic Toxicology 130–131: 132–138.

    Article  PubMed  Google Scholar 

  • Clarke, K. R., 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18: 117–143.

    Article  Google Scholar 

  • Clarke, K. R. & R. N. Gorley, 2006. PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth.

    Google Scholar 

  • Clarke, K. R., J. P. Somerfield & N. G. Raymond, 2008. Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage. Journal of Experimental Marine Biology and Ecology 366: 56–69.

  • Colt, J. E. & D. A. Armstrong, 1981. Nitrogen toxicity to crustaceans, fish and molluscs. In: Allen, L. J & E. C. Kinney (eds), Proceedings of the Bio-Engineering Symposium for Fish Culture. Fish Culture Section, American Fisheries Society, Northeast Society of Conservation Engineers. Bethesda, Maryland: 34–47.

  • Dahan, O., A. Babad, N. Lazarovitch, E. E. Russak & D. Kurtzman, 2014. Nitrate leaching from intensive organic farms to groundwater. Hydrology and Earth System Sciences 18: 333–341.

    Article  CAS  Google Scholar 

  • Di Lorenzo, T. & D. M. P. Galassi, 2013. Agricultural impact in Mediterranean alluvial aquifers: do groundwater communities respond? Fundamental and Applied Limnology 182: 271–282.

    Article  Google Scholar 

  • Di Lorenzo, T., M. Brilli, D. Del Tosto, D. M. P. Galassi & M. Petitta, 2012. Nitrate source and fate at the catchment scale of the Vibrata River and aquifer (central Italy): an analysis by integrating component approaches and nitrogen isotopes. Environmental Earth Sciences 67: 2383–2398.

    Article  CAS  Google Scholar 

  • Di Lorenzo, T., F. Stoch & D. M. P. Galassi, 2013. Incorporating the hyporheic zone within the river discontinuum: longitudinal patterns of subsurface copepod assemblages in an Alpine stream. Limnologica 43: 288–296.

    Article  Google Scholar 

  • Di Lorenzo, T., W. D. Di Marzio, M. E. Sáenz, M. Baratti, A. A. Dedonno, A. Iannucci, S. Cannicci, G. Messana & D. M. P. Galassi, 2014. Sensitivity of hypogean and epigean freshwater copepods to agricultural pollutants. Environmental Science and Pollution Research 21: 4643–4655.

  • Di Marzio, W. D., D. Castaldo, T. Di Lorenzo, A. Di Cioccio, M. E. Sáenz & D. M. P. Galassi, 2013. Developmental endpoints of chronic exposure to suspected endocrine-disrupting chemicals on benthic and hyporheic freshwater copepods. Ecotoxicology and Environmental Safety 96: 86–92.

    Article  PubMed  Google Scholar 

  • Distretto Idrografico delle Alpi Orientali, 2010. Piano di Gestione delle Acque. http://www.alpiorientali.it/new/index.php/direttiva-2000-60/piano-di-gestione-acque-2009-2015/documenti-preliminari-h2o. Accessed 22 July 2014.

  • Dole-Olivier, M.-J., D. M. P. Galassi, P. Marmonier & M. Creuzé des Chatelliers, 2000. The biology and ecology of lotic microcrustaceans. Freshwater Biology 44: 63–91.

    Article  Google Scholar 

  • Dumas, P., 2004. Irrigation as a disturbance for interstitial crustacean communities in a French Pyrenean alluvial aquifer. International Journal of Limnology 40: 139–147.

    Article  Google Scholar 

  • Erisman, J. W., A. Bleeker, J. Galloway & M. S. Sutton, 2007. Reduced nitrogen in ecology and the environment. Environmental Pollution 150: 140–149.

    Article  CAS  PubMed  Google Scholar 

  • European Commission, 2006. Directive 2006/118/EC of the European Parliament and of the Council of 12 December 2006 on the protection of groundwater against pollution and deterioration. Official Journal of the European Union L 372/19.

  • European Commission, 2010. Commission Staff Working Document accompanying the Report from the Commission in accordance with Article 3.7 of the Groundwater Directive 2006/118/EC on the establishment of groundwater threshold values Brussels, SEC(2010) 166 final.

  • European Union, 2012. Statistical and Economic Information. Report 2012. Directorate-General for Agriculture and Rural Development. http://ec.europa.eu/agriculture/statistics/agricultural/2012/pdf/full-report_en.pdf.

  • Fiasca, B., F. Stoch, M.-J. Olivier, C. Maazouzi, M. Petitta, A. Di Cioccio & D. M. P. Galassi, 2014. The dark side of springs: What drives small-scale spatial patterns of subsurface meiofaunal assemblages? Journal of Limnology 73: 55–64.

    Article  Google Scholar 

  • Galassi, D. M. P., 2001. Groundwater copepods (Crustacea: Copepoda): diversity patterns over ecological and evolutionary scales. Hydrobiologia 453(454): 227–253.

    Article  Google Scholar 

  • Galassi, D. M. P., R. Huys & J. W. Reid, 2009. Diversity, ecology and evolution of groundwater copepods. Freshwater Biology 54: 691–708.

    Article  Google Scholar 

  • Gibert, J., D. L. Danielopol & J. A. Stanford (eds), 1994. Groundwater Ecology. Academic Press, San Diego.

    Google Scholar 

  • Griebler, C., F. Malard & T. Lefébure, 2014. Current developments in groundwater ecology—from biodiversity to ecosystem function and services. Current Opinion in Biotechnology 27: 159–167.

    Article  CAS  PubMed  Google Scholar 

  • Hahn, H. J. & D. Matzke, 2005. A comparison of stygofauna communities inside and outside groundwater bores. Limnologica 35: 31–44.

    Article  Google Scholar 

  • Hahn, H. J. & A. Fuchs, 2008. Distribution patterns of groundwater communities across aquifer types in southwestern Germany. Freshwater Biology 54: 848–860.

    Article  Google Scholar 

  • Hartland, A., G. D. Fenwick & S. J. Bury, 2011. Tracing sewage-derived organic matter into a shallow groundwater food web using stable isotope and fluorescence signatures. Marine and Freshwater Research 62: 119–129.

    CAS  Google Scholar 

  • Hurlbert, S. H., 1984. Pseudoreplication and the design of ecological field experiments. Ecological Monographs 54: 187–192.

    Article  Google Scholar 

  • ISTAT, 2006. Agricoltura. Fertilizzanti distribuiti, per tipo di produzione, stato, utilizzo consentito in agricoltura in quintali, allo stadio solido. Dettaglio per Provincia. Anno 2006. http://www3.istat.it/dati/catalogo/20061109_00/PDF/cap13.pdf. Accessed 22 July 2014.

  • Jensen, F. B., 1995. Uptake and effects of nitrite and nitrate in animals. In Walsh, P. J. & P. Wright (eds), Nitrogen Metabolism and Excretion. CRC Press, Boca Raton: 289–303.

    Google Scholar 

  • Jensen, F. B., 2003. Nitrite disrupts multiple physiological functions in aquatic animals. Comparative Biochemistry and Physiology, Part A 135: 9–24.

    Article  Google Scholar 

  • Jiao, J. J., Y. Wang, J. A. Cherry, X. Wang, B. Zhi, H. Du & D. Wen, 2010. Abnormally high ammonium of natural origin in a coastal aquifer-aquitard system in the Pearl River Delta, China. Environmental Science and Technology 44: 7470–7475.

    Article  CAS  PubMed  Google Scholar 

  • Korbel, K. L., P. J. Hancock, P. Serov, R. P. Lim & G. C. Hose, 2013. Groundwater ecosystems vary with land use across a mixed agricultural landscape. Journal of Environmental Quality 42: 380–390.

    Article  CAS  PubMed  Google Scholar 

  • Kota, S., R. C. Borden & M. A. Barlaz, 1999. Influence of protozoan grazing on contaminant biodegradation. Federation of European Microbiological Societies Microbiology Ecology 29: 179–189.

    Article  CAS  Google Scholar 

  • Marshall, M. C. & R. O. Hall, 2004. Hyporheic invertebrates affect nitrogen cycling and respiration in stream sediment microcosms. Journal of the North American Benthological Society 23: 416–428.

    Article  Google Scholar 

  • McGarvey, J. A., W. G. Miller, R. Zhang, Y. Ma & F. Mitloehner, 2007. Bacterial population dynamics in diary waste during aerobic and anaerobic treatment and subsequent storage. Applied and Environmental Microbiology 73: 193–202.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Melo, A., E. Pinto, A. Aguiar, C. Mansilha, O. Pinho & I. Ferreira, 2012. Impact of intensive horticulture practices on groundwater content of nitrates, sodium, potassium, and pesticides. Environmental Monitoring and Assessment 184: 4539–4551.

    Article  CAS  PubMed  Google Scholar 

  • Morari, F., E. Lugato, R. Polese, A. Berti & L. Giardini, 2012. Nitrate concentrations in groundwater under contrasting agricultural management practices in the low plains of Italy. Agriculture, Ecosystems & Environment 147: 47–56.

    Article  CAS  Google Scholar 

  • Mosier, A. R., J. K. Syers & J. R. Freney, 2004. Agriculture and the nitrogen cycle: assessing the impacts of fertilizer use on food production and the environment. Island Press, Washington, DC.

    Google Scholar 

  • Poch-Massegu, R., J. Jimenez-Martinez, K. J. Wallis, F. Ramirez de Cartagena & L. Candela, 2014. Irrigation return flow and nitrate leaching under different crops and irrigation methods in Western Mediterranean weather conditions. Agricultural Water Management 134: 1–13.

    Article  Google Scholar 

  • R Development Core Team, 2008. A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org. Accessed 22 July 2014.

  • Raave, H., I. Keres, K. Kauer, M. Nõges, J. Rebane, M. Tampere & E. Loit, 2014. The impact of activated carbon on NO3 -N, NH4 +-N, P, K leaching in relation to fertilizer use. European Journal of Soil Science 65: 120–127.

    Article  CAS  Google Scholar 

  • Repubblica Italiana, 2009. Decreto Legislativo 16 Marzo 2009, n. 30: Attuazione della direttiva 2006/118/CE, relativa alla protezione delle acque sotterranee dall’inquinamento e dal deterioramento. Gazzetta Ufficiale 79.

  • Romano, N. & C. Zeng, 2013. Toxic effects of ammonia, nitrite, and nitrate to decapod crustaceans: a review on factors influencing their toxicity, physiological consequences, and coping mechanisms. Reviews in Fisheries Science 21: 1–21.

    Article  CAS  Google Scholar 

  • Rouch, R., A. Pitzalis & A. Descouens, 1993. Effets d’un pompage à gros débit sur le peuplement des crustacés d’un aquifère karstique. Annales de Limnologie 29: 15–29.

    Article  Google Scholar 

  • Schmidt, S. I., H. J. Hahn, T. J. Hatton & W. F. Humphreys, 2007. Do faunal assemblages reflect the exchange intensity in groundwater zones? Hydrobiologia 583: 1–19.

    Article  CAS  Google Scholar 

  • Sharma, B. & R. C. Ahlert, 1977. Nitrification and nitrogen removal. Water Research 11: 897–925.

    Article  CAS  Google Scholar 

  • Sket, B., 1999. The nature of biodiversity in hypogean waters and how it is endangered. Biodiversity and Conservation 8: 1319–1338.

    Article  Google Scholar 

  • Stein, H., C. Kellermann, S. I. Schmidt, H. Brielmann, C. Steube, S. E. Berkhoff, A. Fuchs, H. J. Hahn, B. Thulin & C. Griebler, 2010. The potential use of fauna and bacteria as ecological indicators for the assessment of groundwater quality. Journal of Environmental Monitoring 12: 242–254.

    Article  CAS  PubMed  Google Scholar 

  • Stoch, F. & D. M. P. Galassi, 2010. Stygobiotic crustacean species richness: a question of numbers, a matter of scale. Hydrobiologia 653: 217–234.

    Article  CAS  Google Scholar 

  • Tilman, D., 1999. Global environmental impacts of agricultural expansion: the need for sustainable and efficient practices. PNAS 96: 5995–6000.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • van Grinsven, H. J. M., H. F. M. ten Berge, T. Dalgaard, B. Fraters, P. Durand, A. Hart, G. Hofman, B. H. Jacobsen, S. T. J. Lalor, J. P. Lesschen, B. Osterburg, K. G. Richards, A.-K. Techen, F. Vertès, J. Webb & W. J. Willems, 2012. Management, regulation and environmental impacts of nitrogen fertilization in northwestern Europe under the Nitrates Directive; a benchmark study. Biogeoscience 9: 5143–5160.

    Article  Google Scholar 

  • Weihrauch, D., J. C. McNamara, D. W. Towle & H. Onken, 2004. Ion-motive ATPases and active transbranchial NaCl uptake in the red freshwater crab Dilocarcinus pagei (Decapoda Trichodactylidae). Journal of Experimental Zoology 207: 4623–4631.

    CAS  Google Scholar 

  • Wood, P. J., J. Gunn & S. D. Rundle, 2008. Response of benthic cave invertebrates to organic pollution events. Aquatic Conservation 18: 909–922.

    Article  Google Scholar 

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Acknowledgements

The project was funded by a grant from the Basin Authority of the River Adige (Trento, Italy). We thank Fabio Lazzeri for the design and concept of Fig. 1, and Andrea Marchetti and Enrico Gattone for help in field sampling. Constructive criticism by Dr. Grant C. Hose (Macquarie University, NSW, Australia) and an anonymous reviewer also improved the paper.

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Di Lorenzo, T., Cifoni, M., Lombardo, P. et al. Ammonium threshold values for groundwater quality in the EU may not protect groundwater fauna: evidence from an alluvial aquifer in Italy. Hydrobiologia 743, 139–150 (2015). https://doi.org/10.1007/s10750-014-2018-y

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