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Identification of ecological thresholds from variations in phytoplankton communities among lakes: contribution to the definition of environmental standards

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Abstract

In aquatic ecosystems, the identification of ecological thresholds may be useful for managers as it can help to diagnose ecosystem health and to identify key levers to enable the success of preservation and restoration measures. A recent statistical method, gradient forest, based on random forests, was used to detect thresholds of phytoplankton community change in lakes along different environmental gradients. It performs exploratory analyses of multivariate biological and environmental data to estimate the location and importance of community thresholds along gradients. The method was applied to a data set of 224 French lakes which were characterized by 29 environmental variables and the mean abundances of 196 phytoplankton species. Results showed the high importance of geographic variables for the prediction of species abundances at the scale of the study. A second analysis was performed on a subset of lakes defined by geographic thresholds and presenting a higher biological homogeneity. Community thresholds were identified for the most important physico-chemical variables including water transparency, total phosphorus, ammonia, nitrates, and dissolved organic carbon. Gradient forest appeared as a powerful method at a first exploratory step, to detect ecological thresholds at large spatial scale. The thresholds that were identified here must be reinforced by the separate analysis of other aquatic communities and may be used then to set protective environmental standards after consideration of natural variability among lakes.

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References

  • Andersen, T., Carstensen, J., Hernández-García, E., & Duarte, C. M. (2009). Ecological thresholds and regime shifts: approaches to identification. Trends in Ecology & Evolution, 24(1), 49–57. doi:10.1016/j.tree.2008.07.014.

    Article  Google Scholar 

  • Bade, D. L., Carpenter, S. R., Cole, J. J., Pace, M. L., Kritzberg, E., Van de Bogert, M. C., et al. (2007). Sources and fates of dissolved organic carbon in lakes as determined by whole-lake carbon isotope additions. Biogeochemistry, 84(2), 115–129. doi:10.1007/s10533-006-9013-y.

    Article  CAS  Google Scholar 

  • Baker, M. E., & King, R. S. (2010). A new method for detecting and interpreting biodiversity and ecological community thresholds. Methods in Ecology and Evolution, 1(1), 25–37. doi:10.1111/j.2041-210X.2009.00007.x.

    Article  Google Scholar 

  • Beklioglu, M., Carvalho, L., & Moss, B. (1999). Rapid recovery of a shallow hypertrophic lake following sewage effluent diversion: lack of chemical resilience. Hydrobiologia, 412, 5–15.

    Article  CAS  Google Scholar 

  • Black, R. W., Moran, P. W., & Frankforter, J. D. (2011). Response of algal metrics to nutrients and physical factors and identification of nutrient thresholds in agricultural streams. Environmental Monitoring and Assessment, 175(1–4), 397–417. doi:10.1007/s10661-010-1539-8.

    Article  CAS  Google Scholar 

  • Borics, G., Nagy, L., Miron, S., Grigorszky, I., László-Nagy, Z., Lukács, B. A., et al. (2013). Which factors affect phytoplankton biomass in shallow eutrophic lakes? Hydrobiologia, 714(1), 93–104.

    Article  CAS  Google Scholar 

  • Breiman, L. (2001). Random forests. Machine Learning, 45(1), 5–32. doi:10.1023/A:1010933404324.

    Article  Google Scholar 

  • Breiman, L., Friedman, J., Stone, C. J., & Olshen, R. A. (1984). Classification and regression trees: Chapman and Hall/CRC.

  • Brenden, T. O., Wang, L., & Su, Z. (2008). Quantitative identification of disturbance thresholds in support of aquatic resource management. Environmental Management, 42(5), 821–832. doi:10.1007/s00267-008-9150-2.

    Article  Google Scholar 

  • Camargo, J. A., & Alonso, A. (2006). Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: a global assessment. Environment International, 32(6), 831–849. doi:10.1016/j.envint.2006.05.002.

    Article  CAS  Google Scholar 

  • Cardoso, A. C., Solimini, A., Premazzi, G., Carvalho, L., Lyche, A., & Rekolainen, S. (2007). Phosphorus reference concentrations in European lakes. Hydrobiologia, 584, 3–12. doi:10.1007/s10750-007-0584-y.

    Article  CAS  Google Scholar 

  • Cardoso, A. C., Free, G., Nõges, P., Kaste, Ø., Poikane, S., & Solheim, A. L. (2009). Lake management criteria. In G. E. Likens (Ed.), Encyclopedia of Inland Waters (Vol. 1, pp. 310–331). Oxford.

  • Carpenter, S. R., Cole, J. J., Kitchell, J. F., & Pace, M. L. (1998). Impact of dissolved organic carbon, phosphorus, and grazing on phytoplankton biomass and production in experimental lakes. Limnology and Oceanography, 43(1), 73–80.

    Article  CAS  Google Scholar 

  • Carvalho, L., Poikane, S., Lyche Solheim, A., Phillips, G., Borics, G., Catalan, J., et al. (2013). Strength and uncertainty of phytoplankton metrics for assessing eutrophication impacts in lakes. Hydrobiologia, 704(1), 127–140. doi:10.1007/s10750-012-1344-1.

    Article  CAS  Google Scholar 

  • Catalan, J., Barbieri, M. G., Bartumeus, F., Bitusik, P., Botev, I., Brancelj, A., et al. (2009). Ecological thresholds in European alpine lakes. Freshwater Biology, 54(12), 2494–2517. doi:10.1111/j.1365-2427.2009.02286.x.

    Article  CAS  Google Scholar 

  • Chambers, P. A., Benoy, G. A., Brua, R. B., & Culp, J. M. (2011). Application of nitrogen and phosphorus criteria for streams in agricultural landscapes. Water Science and Technology, 64(11), 2185–2191. doi:10.2166/Wst.2011.760.

    Article  CAS  Google Scholar 

  • Chambers, P. A., Culp, J. M., Roberts, E. S., & Bowerman, M. (2012a). Development of environmental thresholds for streams in agricultural watersheds. Journal of Environmental Quality, 41(1), 1–6. doi:10.2134/jeq2011.0338.

    Article  CAS  Google Scholar 

  • Chambers, P. A., McGoldrick, D. J., Brua, R. B., Vis, C., Culp, J. M., & Benoy, G. A. (2012b). Development of environmental thresholds for nitrogen and phosphorus in streams. Journal of Environmental Quality, 41(1), 7–20. doi:10.2134/jeq2010.0273.

    Article  CAS  Google Scholar 

  • Claussen, U., Müller, P., & Arle, J. (2012). Comparison of environmental quality objectives, threshold values or water quality targets set for the demands of the European Water Framework Directive. WFD CIS ECOSTAT WG A Report (pp. 27). CIRCABC.

  • Cuffney, T. F., & Qian, S. S. (2013). A critique of the use of indicator-species scores for identifying thresholds in species responses. Freshwater Sci, 32(2), 471–488. doi:10.1899/12-056.1.

    Article  Google Scholar 

  • Daily, J. P., Hitt, N. P., Smith, D. R., & Snyder, C. D. (2012). Experimental and environmental factors affect spurious detection of ecological thresholds. Ecology, 93(1), 17–23.

    Article  Google Scholar 

  • De’Ath, G. (2002). Multivariate regression trees: a new technique for modeling species-environment relationships. Ecology, 83(4), 1105–1117. doi:10.2307/3071917.

    Google Scholar 

  • De’ath, G., & Fabricius, K. E. (2000). Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecology, 81(11), 3178–3192. doi:10.2307/177409.

    Article  Google Scholar 

  • Dodds, W. K., Smith, V. H., & Lohman, K. (2002). Nitrogen and phosphorus relationships to benthic algal biomass in temperate streams. Canadian Journal of Fisheries and Aquatic Sciences, 59(5), 865–874. doi:10.1139/F02-063.

    Article  Google Scholar 

  • Dodds, W. K., Clements, W. H., Gido, K., Hilderbrand, R. H., & King, R. S. (2010). Thresholds, breakpoints, and nonlinearity in freshwaters as related to management. Journal of the North American Benthological Society, 29(3), 988–997. doi:10.1899/09-148.1.

    Article  Google Scholar 

  • Donald, D. B., Bogard, M. J., Finlay, K., Bunting, L., & Leavitt, P. R. (2013). Phytoplankton-specific response to enrichment of phosphorus-rich surface waters with ammonium, nitrate, and urea. Plos One, 8(1), doi:10.1371/journal.pone.0053277.

  • Ellis, N., Smith, S. J., & Pitcher, C. R. (2012). Gradient forests: calculating importance gradients on physical predictors. Ecology, 93(1), 156–168.

    Article  Google Scholar 

  • European Commission (2000). Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for community action in the field of water policy. (pp. 72): The European Parlament and Council.

  • Evans-White, M. A., Dodds, W. K., Huggins, D. G., & Baker, D. S. (2009). Thresholds in macroinvertebrate biodiversity and stoichiometry across water-quality gradients in Central Plains (USA) streams. Journal of the North American Benthological Society, 28(4), 855–868. doi:10.1899/08-113.1.

    Article  Google Scholar 

  • Feret, T., & Laplace-Treyture, C. (2013). IPLAC: l’indice Phytoplancton Lacustre: Méthode de développement, description et application nationale 2012. Rapport convention Onema/Irstea 2012 (pp. 69). Bordeaux: Irstea, UR REBX.

  • Free, G., Little, R., Tierney, D., Donnelly, K., & Caroni, R. (2006). A reference based typology and ecological assessment system for Irish lakes. Prelimnary investigations. (pp. 266). Wexford, Ireland: Environmental Protection Agency.

  • García-Ferrer, I., Camacho, A., Armengol, X., Miracle, M. R., & Vicente, E. (2003). Seasonal and spatial heterogeneity in the water chemistry of two sewage-affected saline shallow lakes from central Spain. Hydrobiologia, 506–509, 101–110.

    Article  Google Scholar 

  • Graham, J. L., Jones, J. R., Jones, S. B., Downing, J. A., & Clevenger, T. E. (2004). Environmental factors influencing microcystin distribution and concentration in the Midwestern United States. Water Research, 38(20), 4395–4404. doi:10.1016/j.watres.2004.08.004.

    Article  CAS  Google Scholar 

  • Groffman, P., Baron, J., Blett, T., Gold, A., Goodman, I., Gunderson, L., et al. (2006). Ecological thresholds: the key to successful environmental management or an important concept with no practical application? Ecosystems, 9(1), 1–13, doi:10.1007/s10021-003-0142-z.

  • Holt, C. A., Yan, N. D., & Somers, K. M. (2003). pH 6 as the threshold to use in critical load modeling for zooplankton community change with acidification in lakes of south-central Ontario: accounting for morphometry and geography. Canadian Journal of Fisheries and Aquatic Sciences, 60(2), 151–158. doi:10.1139/f03-008.

    Article  Google Scholar 

  • Jansson, M., Bergström, A.-K., Blomqvist, P., & Drakare, S. (2000). Allochthonous organic carbon and phytoplankton/bacterioplankton production relationships in lakes. Ecology, 81(11), 3250–3255. doi:10.1890/0012-9658(2000)081[3250:AOCAPB]2.0.CO;2.

    Article  Google Scholar 

  • Katsiapi, M., Moustaka-Gouni, M., Vardaka, E., & Kormas, K. A. (2013). Different phytoplankton descriptors show asynchronous changes in a shallow urban lake (L. Kastoria, Greece) after sewage diversion. Fundamental and Applied Limnology, 182(3), 219–230.

    Article  Google Scholar 

  • King, R. S., & Baker, M. E. (2010). Considerations for analyzing ecological community thresholds in response to anthropogenic environmental gradients. Journal of the North American Benthological Society, 29(3), 998–1008. doi:10.1899/09-144.1.

    Article  Google Scholar 

  • King, R. S., Baker, M. E., Kazyak, P. F., & Weller, D. E. (2011). How novel is too novel? Stream community thresholds at exceptionally low levels of catchment urbanization. Ecological Applications, 21(5), 1659–1678. doi:10.1890/10-1357.1.

    Article  Google Scholar 

  • Konig, A., Pearson, H. W., & Silva, S. A. (1987). Ammonia toxicity to algal growth in waste stabilization ponds. Water Science and Technology, 19(12), 115–122.

    CAS  Google Scholar 

  • Laplace-Treyture, C., Barbe, J., Dutartre, A., Druart, J.-C., Rimet, F., & Anneville, O. (2009). Standard protocol for sampling, conservation, observation and counting of lake phytoplankton for application of the WFD. Version 3.3.1. (pp. 42). Cestas, France: Cemagref UR REBX.

  • Luck, G. W. (2005). An introduction to ecological thresholds. Biological Conservation, 124(3), 299–300. doi:10.1016/j.biocon.2005.01.042.

    Article  Google Scholar 

  • Maileht, K., Nõges, T., Nõges, P., Ott, I., Mischke, U., Carvalho, L., et al. (2013). Water colour, phosphorus and alkalinity are the major determinants of the dominant phytoplankton species in European lakes. Hydrobiologia, 704(1), 115–126. doi:10.1007/s10750-012-1348-x.

    Article  CAS  Google Scholar 

  • May, R. M. (1977). Thresholds and breakpoints in ecosystems with a multiplicity of stable states. Nature, 269(5628), 471–477. doi:10.1038/269471a0.

    Article  Google Scholar 

  • OECD. (1982). Eutrophication of waters—monitoring, assessment and control. Paris: Organisation for Economic Co-operation and Development.

    Google Scholar 

  • Penning, W. E., Dudley, B., Mjelde, M., Hellsten, S., Hanganu, J., Kolada, A., et al. (2008). Using aquatic macrophyte community indices to define the ecological status of European lakes. Aquatic Ecology, 42(2), 253–264. doi:10.1007/s10452-008-9183-x.

    Article  CAS  Google Scholar 

  • Phillips, G., Lyche-Solheim, A., Skjelbred, B., Mischke, U., Drakare, S., Free, G., et al. (2013). A phytoplankton trophic index to assess the status of lakes for the Water Framework Directive. Hydrobiologia, 704(1), 75–95. doi:10.1007/s10750-012-1390-8.

    Article  Google Scholar 

  • Pitcher, C. R., Lawton, P., Ellis, N., Smith, S. J., Incze, L. S., Wei, C. L., et al. (2012). Exploring the role of environmental variables in shaping patterns of seabed biodiversity composition in regional-scale ecosystems. Journal of Applied Ecology, 49(3), 670–679. doi:10.1111/j.1365-2664.2012.02148.x.

    Article  Google Scholar 

  • Poikane, S., Portielje, R., van den Berg, M., Phillips, G., Brucet, S., Carvalho, L., et al. (2014). Defining ecologically relevant water quality targets for lakes in Europe. Journal of Applied Ecology, 51(3), 592–602. doi:10.1111/1365-2664.12228.

    Article  CAS  Google Scholar 

  • Prasad, A. M., Iverson, L. R., & Liaw, A. (2006). Newer classification and regression tree techniques: bagging and random forests for ecological prediction. Ecosystems, 9(2), 181–199. doi:10.1007/s10021-005-0054-1.

    Article  Google Scholar 

  • Qian, S. S. (2014). Ecological threshold and environmental management: a note on statistical methods for detecting thresholds. Ecological Indicators, 38, 192–197. doi:10.1016/j.ecolind.2013.11.008.

    Article  Google Scholar 

  • Qian, S. S., King, R. S., & Richardson, C. J. (2003). Two statistical methods for the detection of environmental thresholds. Ecological Modelling, 166(1–2), 87–97. doi:10.1016/S0304-3800(03)00097-8.

    Article  CAS  Google Scholar 

  • R_Core_Team (2013), R: a language and environment for statistical computing.

  • Richardson, C. J., King, R. S., Qian, S. S., Vaithiyanathan, P., Qualls, R. G., & Stow, C. A. (2007). Estimating ecological thresholds for phosphorus in the Everglades. Environmental Science & Technology, 41(23), 8084–8091. doi:10.1021/es062624w.

    Article  CAS  Google Scholar 

  • Scheffer, M., & Carpenter, S. R. (2003). Catastrophic regime shifts in ecosystems: linking theory to observation. Trends in Ecology & Evolution, 18(12), 648–656. doi:10.1016/j.tree.2003.09.002.

    Article  Google Scholar 

  • Scheffer, M., Rinaldi, S., Gragnani, A., Mur, L. R., & vanNes, E. H. (1997). On the dominance of filamentous cyanobacteria in shallow, turbid lakes. Ecology, 78(1), 272–282.

    Article  Google Scholar 

  • Scheffer, M., Szabo, S., Gragnani, A., van Nes, E. H., Rinaldi, S., Kautsky, N., et al. (2003). Floating plant dominance as a stable state. Proceedings of the National Academy of Sciences of the United States of America, 100(7), 4040–4045. doi:10.1073/pnas.0737918100.

    Article  CAS  Google Scholar 

  • Schindler, D. W. (1977). Evolution of phosphorus limitation in lakes. Science, 195(4275), 260–262. doi:10.1126/science.195.4275.260.

    Article  CAS  Google Scholar 

  • Smith, A. J., & Tran, C. P. (2010). A weight-of-evidence approach to define nutrient criteria protective of aquatic life in large rivers. Journal of the North American Benthological Society, 29(3), 875–891. doi:10.1899/09-076.1.

    Article  Google Scholar 

  • Solheim, A. L., Rekolainen, S., Moe, S. J., Carvalho, L., Phillips, G., Ptacnik, R., et al. (2008). Ecological threshold responses in European lakes and their applicability for the Water Framework Directive (WFD) implementation: synthesis of lakes results from the REBECCA project. Aquatic Ecology, 42(2), 317–334. doi:10.1007/s10452-008-9188-5.

    Article  Google Scholar 

  • Soranno, P. A., Cheruvelil, K. S., Stevenson, R. J., Rollins, S. L., Holden, S. W., Heaton, S., et al. (2008). A framework for developing ecosystem-specific nutrient criteria: integrating biological thresholds with predictive modeling. Limnology and Oceanography, 53(2), 773–787. doi:10.4319/lo.2008.53.2.0773.

    Article  Google Scholar 

  • Stomp, M., Huisman, J., Mittelbach, G. G., Litchman, E., & Klausmeier, C. A. (2011). Large-scale biodiversity patterns in freshwater phytoplankton. Ecology, 92(11), 2096–2107.

    Article  Google Scholar 

  • Strobl, C., Boulesteix, A. L., Kneib, T., Augustin, T., & Zeileis, A. (2008). Conditional variable importance for random forests. Bmc Bioinformatics, 9, doi:10.1186/1471-2105-9-307.

  • Utz, R. M., Hilderbrand, R. H., & Boward, D. M. (2009). Identifying regional differences in threshold responses of aquatic invertebrates to land cover gradients. Ecological Indicators, 9(3), 556–567. doi:10.1016/j.ecolind.2008.08.008.

    Article  Google Scholar 

  • Villena, M. J., & Romo, S. (2003). Phytoplankton changes in a shallow Mediterranean lake (Albufera of Valencia, Spain) after sewage diversion. Hydrobiologia, 506–509, 281–287.

    Article  Google Scholar 

  • Vollenweider, R. A. (1975). Input–output models—with special reference to the phoshorus loading concept in limnology. Source of the Document Schweizerische Zeitschrift für Hydrologie, 37(1), 53–84.

    CAS  Google Scholar 

  • Wall, D., & Briand, F. (1979). Response of lake phytoplankton communities to in situ manipulations of light intensity and colour. Journal of Plankton Research, 1(1), 103–112. doi:10.1093/plankt/1.1.103.

    Article  Google Scholar 

  • Watson, S. B., McCauley, E., & Downing, J. A. (1997). Patterns in phytoplankton taxonomic composition across temperate lakes of differing nutrient status. Limnology and Oceanography, 42(3), 487–495.

    Article  Google Scholar 

  • Williamson, C. E., Morris, D. P., Pace, M. L., & Olson, A. G. (1999). Dissolved organic carbon and nutrients as regulators of lake ecosystems: resurrection of a more integrated paradigm. Limnology and Oceanography, 44(3), 795–803.

    Article  CAS  Google Scholar 

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Acknowledgments

This research was funded by the French National Agency for Water and Aquatic Environments (ONEMA). The authors are grateful to the French Water Basin Agencies and their partners who contributed to the lake data acquisition and to the Onema-Irstea Consortium for Lake Hydroecology (Pôle Onema-Irstea d’études et de recherche “hydroécologie des plans d’eau”, Aix-en-Provence, France), who currently maintains the national biological and physico-chemical database for French lakes; special thanks to Nathalie Reynaud and Thierry Point (database) and Milena Borissova (text edition). We also thank two anonymous referees for their positive comments, which have improved the paper.

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  1. Irstea, UR RECOVER, Pôle Onema-Irstea hydroécologie plans d’eau, Centre d’Aix-en-Provence, 3275 route Cézanne, F-13182, Aix-en-Provence, France

    Vincent Roubeix

  2. Onema, Pôle Onema-Irstea hydroécologie plans d’eau, F-13182, Aix-en-Provence, France

    Pierre-Alain Danis & Jean-Marc Baudoin

  3. Irstea, UR EABX, Centre de Bordeaux, F-33612, Gazinet Cestas, France

    Thibaut Feret

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Roubeix, V., Danis, PA., Feret, T. et al. Identification of ecological thresholds from variations in phytoplankton communities among lakes: contribution to the definition of environmental standards. Environ Monit Assess 188, 246 (2016). https://doi.org/10.1007/s10661-016-5238-y

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