Abstract
Aquatic plants and benthic algae have long been used as indicators for nutrient enrichment in lakes and streams. Evaluations of the performance of indices calculated from species assemblages of aquatic plants and algae are generally based on correlations with water nutrient concentrations. We argue that this is a misinterpretation, because water chemistry is both cause and effect: higher nutrient concentrations may cause enhanced plant and algal growth and change their assemblages, but plants and benthic algae also remove nutrients from the water. Additionally, biotic interactions blur water chemistry – aquatic plant relationships. We suggest that indices can be improved by relating biotic responses to quantifiable causal stressors, such as nutrient loading, instead of using water chemistry for performance evaluation of the indices. In addition, a tiered approach, i.e., the use of simpler indices for getting an overview and of sophisticated methods in doubtful cases, could avoid unnecessary costs and efforts while giving important monitoring and management information.
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References
Arts GHP, Roelofs JGM, De Lyon MJH (1990) Differential tolerances among soft-water macrophyte species to acidification. Can J Bot 68:2127–2134
Bakker ES, Sarneel JM, Gulati RD, Liu ZW, van Donk E (2013) Restoring macrophyte diversity in shallow temperate lakes: biotic versus abiotic constraints. Hydrobiologia 710:23–37
Barko JW, Smart RM (1981) Sediment-based nutrition of submersed macrophytes. Aquat Bot 10:339–352
Barton DR, Howell ET, Fietsch CL (2013) Ecosystem changes and nuisance benthic algae on the southeast shores of Lake Huron. J Great Lakes Res 39:602–611
Bennett C, Owen R, Birk S, Buffagni A, Erba S, Mengin N et al (2011) Bringing European river quality into line: an exercise to intercalibrate macro-invertebrate classification methods. Hydrobiologia 667:31–48
Billen G, Garnier J, Deligne C, Billen C (1999) Estimates of early-industrial inputs of nutrients to river systems: implication for coastal eutrophication. Sci Total Environ 243(244):43–52
Birk S, Bonne W, Borja A, Brucet S, Courrat A, Poikane S, Solimini A, van de Bund WV, Zampoukas N, Hering D (2012) Three hundred ways to assess Europe’s surface waters: an almost complete overview of biological methods to implement the Water Framework Directive. Ecol Indic 18:31–41
Blindow I, Hargeby A, Hilt S (2014) Facilitation of clear-water conditions in shallow lakes by macrophytes: differences between charophyte and angiosperm dominance. Hydrobiologia 737:99–110
Bouleau G, Pont D (2015) Did you say reference conditions? Ecological and socio-economic perspectives on the European Water Framework Directive. Environ Sci Policy 47:32–41
Brothers S, Köhler J, Meyer N, Attermeyer K, Grossart HP, Mehner T, Scharnweber K, Hilt S (2014) A feedback loop links brownification and anoxia in a temperate, shallow lake. Limnol Oceanogr 59:1388–1398
Butcher RW (1933) Studies on the ecology of rivers: I. On the distribution of macrophytic vegetation in the rivers of Britain. J Ecol 21:58–91
Cairns J, Pratt JR (1993) A history of biological monitoring using benthic macroinvertebrates. In: Rosenberg DM, Resh VH (eds) Freshwater biomonitoring and benthic macroinvertebrates. Chapman and Hall, New York
Carignan R, Kalff J (1980) Phosphorus sources for aquatic weeds: water or sediments? Science 207:987–988
CEMAGREF (1982) Etude de méthodes biologiques quantitatives d’appreciation de la qualité des eaux. Rapport Q.E. Lyon-A.F.B. Rhône-Mediterranée-Corse
Chambers PA, Prepas EE, Bothwell ML, Hamilton HR (1989) Roots versus shoots in nutrient uptake by aquatic macrophytes in flowing waters. Can J Fish Aquat Sci 46:435–439
del Pozo R, Fernandez-Alaez C, Fernandez-Alaez M (2010) An assessment of macrophyte community metrics in the determination of the ecological condition and total phosphorus concentration of Mediterranean ponds. Aquat Bot 92:55–62
DeNicola DM, Kelly MG (2014) Role of periphyton in ecological assessment of lakes. Freshw Sci 33:619–638
Descy JP (1979) A new approach to water quality estimation using diatoms. Nova Hedwigia 64:305–323
DIN 4049-2 (1990) Hydrologie; Begriffe der Gewässerbeschaffenheit. Deutsches Institut fuer Normung, Berlin, p 25
Dodds WK (2003) The role of periphyton in phosphorus retention in shallow freshwater aquatic systems. J Phycol 39:840–849
Dollan A, Hupfer M (2003) Immobilisation of phosphorus by iron-coated roots of submerged macrophytes. Hydrobiologia 506–509:635–640
Eigemann F, Mischke U, Hupfer M, Schaumburg J, Hilt S (2016) Biological indicators track differential responses of pelagic and littoral areas to nutrient load reductions in German lakes. Ecol Indic 61:905–910
European Commission (2000) Directive 2000/60/EC. Establishing a framework for community action in the field of water policy. European Commission PE-CONS 3639/1/100 Rev 1, Luxembourg
European Commission (2009) Guidance document on eutrophication assessment in the context of European water policies. Technical Report - 2009 – 030, Luxembourg
European Court of Justice (2009) Judgment of the Court (Third Chamber) of 10 December 2009 (Case C-390/07). European Commission v United Kingdom of Great Britain and Northern Ireland. Failure of a Member State to fulfill obligations – Environment – Directive 91/271/EEC – Urban waste water treatment – Article 3(1) and (2), Article 5(1) to (3) and (5) and Annexes I and II – Initial failure to identify sensitive areas – Concept of ‘eutrophication’ – Criteria – Burden of proof – Relevant date when considering the evidence – Implementation of collection obligations – Implementation of more stringent treatment of discharges into sensitive areas. Official Journal of the European Union, C 24/4
Fisher J, Deflandre-Vlandas A, Coste M, Delmas F, Jarvie HP (2010) Assemblage grouping of European benthic diatoms as indicators of trophic status of rivers. Fundam Appl Limnol 176:89–100
Friberg N (2014) Impacts and indicators of change in lotic ecosystems. WIREs Water 1:513–531
Friedrich G (1990) Eine Revision des Saprobiensystems. Zeitschrift fur Wasser- und Abwasserforschung 23:141–152
Gabriels W, Lock K, De Pauw N, Goethals PLM (2010) Multimetric Macroinvertebrate Index Flanders (MMIF) for biological assessment of rivers and lakes in Flanders (Belgium). Limnologica 40:199–207
Hassall AH (1850) Memoir on the organic analysis or microscopic examination of water supplied to the inhabitants of London and the suburban districts. Lancet 1:230–235
Haury J, Peltre MC, Tremolieres M, Barbe J, Thiebaut G, Bernez I et al (2006) A new method to assess water trophy and organic pollution – the Macrophyte biological index for rivers (IBMR): its application to different types of river and pollution. Hydrobiologia 570:153–158
Hawes I, Smith R (1993) Effect of localised nutrient enrichment on the shallow epilithic periphyton of oligotrophic Lake Taupo, New Zealand. N Z J Mar Freshw Res 27:365–372
Hering D, Meier C, Rawer-Jost C, Feld CK, Biss R, Zenker A, Sundermann A, Lohse S, Bohmer J (2004) Assessing streams in Germany with benthic invertebrates: selection of candidate metrics. Limnologica 34:398–415
Hering D, Johnson RK, Kramm S, Schmutz S, Szoszkiewicz K, Verdonschot PFM (2006a) Assessment of European streams with diatoms, macrophytes, macroinvertebrates and fish: a comparative metric-based analysis of organism response due to stress. Freshw Biol 51:1757–1785
Hering D, Feld CK, Moog O, Ofenbock T (2006b) Cook book for the development of a multimetric index for biological condition of aquatic ecosystems: experiences from the European AQEM and STAR projects and related initiatives. Hydrobiologia 566:311–324
Hering D, Borja A, Carstensen J, Carvalho L, Elliott M, Feld CK, Heiskanen AS, Johnson RK, Moe J, Pont D, Lyche Solheim A, van de Bund W (2010) The European Water Framework Directive at the age of 10: a critical review of the achievements with recommendations for the future. Sci Total Environ 408:4007–4019
Hidding B, Bakker ES, Hootsmans MJM, Hilt S (2016) Synergy between shading and herbivory triggers plant loss and regime shifts in aquatic systems. Oikos (in press). doi:10.1111/oik.03104
Hill BH, Herlihy AT, Kaufmann PR, Stevenson RJ, McCormick FH, Johnson CB (2000) Use of periphyton assemblage data as an index of biotic integrity. J N Am Benthol Soc 19:50–67
Hilt S, Van de Weyer K, Köhler A, Chorus I (2010) Submerged macrophyte responses to reduced phosphorus concentrations in two peri-urban lakes. Restor Ecol 18(S2):452–461
Hilt S, Köhler J, Kozerski HP, Scheffer M, Van Nes E (2011) Abrupt regime shifts in space and time along rivers and connected lakes systems. Oikos 120:766–775
Hilt S, Adrian R, Köhler J, Monaghan MT, Sayer C (2013) Clear, crashing, turbid and back – long-term changes of macrophyte assemblages in a shallow lake. Freshw Biol 58:2027–2036
Holmes NTH, Newman JR, Chadd S, Rouen KJ, Saint L, Dawson FH (1999) Mean trophic rank: a user’s manual. R&D Technical Report E38. Environment Agency, Bristol
Hutchinson GE (1973) Eutrophication – the scientific background of a contemporary practical problem. Am Sci 61:269–279
James WF, Barko JW, Butler MG (2004) Shear stress and sediment resuspension in relation to submersed macrophyte biomass. Hydrobiologia 515:181–191
Janse JH, De Senerpont Domis LN, Scheffer M, Lijklema L, Van Liere L, Klinge M, Mooij W (2008) Critical phosphorus loading of different types of shallow lakes and the consequences for management estimated with the ecosystem model PCLAKE. Limnologica 38:203–219
Jones JI, Sayer CE (2003) Does a fish-invertebrate-periphyton cascade precipitate plant loss in shallow lakes? Ecology 84:2155–2167
Juggins S, Kelly M, Allott T, Kelly-Quinn M, Monteith D (2016) A Water Framework Directive-compatible metric for assessing acidification in UK and Irish rivers using diatoms. Science of the total environment (in press)
Karr JR (1991) Biological integrity: a long-neglected aspect of water resource management. Ecol Appl 1:66–84
Karr JR (1999) Defining and measuring river health. Freshw Biol 41:221–234
Kelly MG (2006) A comparison of diatoms with other phytobenthos as indicators of ecological status in streams in northern England. In: Witkowski A (ed) Proceedings of the 18th international diatom symposium 2004. Biopress, Bristol, pp 139–151
Kelly MG (2013) Data rich, information poor? Phytobenthos assessment and the Water Framework Directive. Eur J Phycol 48:437–450
Kelly MG, Whitton BA (1995) The Trophic Diatom Index: a new index for monitoring eutrophication in rivers. J Appl Phycol 7:433–444
Kelly MG, King L, Jones RI, Barker PA, Jamieson BJ (2008) Validation of diatoms as proxies for phytobenthos when assessing ecological status in lakes. Hydrobiologia 610:125–129
Kelly MG, Bennett C, Coste M, Delgado C, Delmas F, Denys L et al (2009) A comparison of national approaches to setting ecological status boundaries in phytobenthos assessment for the European Water Framework Directive: results of an intercalibration exercise. Hydrobiologia 621:169–182
Kelly MG, Schneider SC, King L (2015) Customs, habits and traditions: the role of non-scientific factors in the development of ecological assessment methods. WIREs Water 2:159–165
Kohler A, Brinkmeier R, Vollrath H (1974) Verbreitung und Indikatorwert der submsersen Makrophyten in den Fliessgewässern der Friedberger Au. Ber Bay Bot Ges 45:5–36
Köhler J, Hachoł J, Hilt S (2010) Regulation of submersed macrophyte biomass in a temperate lowland river: interactions between shading by bank vegetation, epiphyton and water turbidity. Aquat Bot 92:129–136
Kolada A, Willby N, Dudley B, Noges P, Sondergaard M, Hellsten S, Mjelde M, Penning E, van Geest G, Bertrin V, Ecke F, Maemets H, Karus K (2014) The applicability of macrophyte compositional metrics for assessing eutrophication in European lakes. Ecol Indic 45:407–415
Kolkwitz R, Marsson M (1902) Grundsätze für die biologische Beurteilung des Wassers nach seiner Flora und Fauna. Mitteilungen der königlichen Prüfanstalt für Wasserversorgung und Abwasserbeseitigung 1:33–72
Kolkwitz R, Marsson M (1908) Ökologie der pflanzlichen Saprobien. Mitteilung aus der Königlichen Prüfungsanstalt für Wasserversorgung und Abwässerbeseitigung Heft 1:508–519
Krupska J, Pełechaty M, Pukacz A, Ossowski P (2012) Effects of grass carp introduction on macrophyte communities in a shallow lake. Oceanol Hydrobiol Stud 41:35–40
Lange-Bertalot H (1979) Pollution tolerance as a criterion for water quality estimation. Nova Hedwigia 64:285–304
Loeb SL (1986) Algal biofouling of oligotrophic Lake Tahoe: causal factors affecting production. In: Evans LV, Hoagland KD (eds) Algal biofouling. Elsevier Science Publishers, Amsterdam, pp 159–173
Lyche-Solheim A, Feld CK, Birk S, Phillips G, Carvalho L, Morabito G, Mischke U, Willby N, Søndergaard M, Hellsten S, Kolada A, Mjelde M, Böhmer J, Miler O, Pusch MT, Argillier C, Jeppesen E, Lauridsen TL, Poikane S (2013) Ecological status assessment of European lakes: a comparison of metrics for phytoplankton, macrophytes, benthic invertebrates and fish. Hydrobiologia 704:57–74
Mjelde M, Hellsten S, Ecke F (2013) A water level drawdown index for aquatic macrophytes in Nordic lakes. Hydrobiologia 704:141–151
Naumann E (1929) Einige neue Gesichtspunkte zur Systematik der Gewässertypen. Arch Hydrobiol 20:191–198
Newbold C, Palmer M (1979) Trophic adaptations of aquatic plants. NCC CST Notes number 18. Nature Conservancy Council, Peterborough
Ohle W (1955) Beiträge zur Produktionsbiologie der Gewässer. Arch Hydrobiol XXII(Suppl):456–479
Pantle K, Buck H (1955) Die biologische Überwachung der Gewässer und die Darstellung der Ergebnisse. Gas- und Wasserfach Wasser/Abwasser 96:609–620
Pardo I, Gomez-Rodriguez C, Wasson JG, Owen R, van de Bund W, Kelly M, Bennett C, Birk S, Buffagni A, Erba S, Mengin N, Murray-Bligh J, Ofenboeck G (2012) The European reference condition concept: a scientific and technical approach to identify minimally-impacted river ecosystems. Sci Total Environ 420:33–42
Penning WE, Dudley B, Mjelde M, Hellsten S, Hanganu J, Kolada A, van den Berg M, Poikane S, Phillips G, Willby N, Ecke F (2008) Using aquatic macrophyte community indices to define the ecological status of European lakes. Aquat Ecol 42:253–264
Perillon C, Hilt S (2016) Groundwater influence differentially affects periphyton and macrophyte production in lakes. Hydrobiologia (in press). doi:10.1007/s10750-015-2485-9
Phillips GL, Eminson DF, Moss B (1978) A mechanism to account for macrophyte decline in progressively eutrophicated waters. Aquat Bot 4:103–125
Piggott JJ, Salis RK, Lear G, Townsend CR, Matthaei CD (2015) Climate warming and agricultural stressors interact to determine stream periphyton community composition. Glob Chang Biol 21:206–222
Prygiel J, Coste M (1993) The assessment of water quality in the Artois-Picardie water basin (France) by the use of diatom indices. Hydrobiologia 269(270):343–349
Ricart M, Guasch H, Alberch M, Barcelo D, Bonnineau C, Geiszinger A, Farre M, Ferrer J, Ricciardi F, Romani AM, Morin S, Proia L, Sala L, Sureda D, Sabater S (2010) Triclosan persistence through wastewater treatment plants and its potential toxic effects on river biofilms. Aquat Toxicol 100:346–353
Rodhe W (1969) Crystallization of eutrophication concepts in Northern Europe. In: Proceedings of a symposium on eutrophication: causes, consequences, correctives. National Academy of Sciences, Washington, pp 50–64
Rott E, Pipp E, Pfister P, van Dam H, Ortler K, Binder N, Pall K (1999) Indikationslisten für Aufwuchsalgen in Österreichischen Fliessgewassern. Teil 2: Trophieindikation. Bundesministerium für Land- und Forstwirtschaft, Vienna, Austria
Schaumburg J, Schranz C, Foerster J, Gutowski A, Hofmann G, Meilinger P, Schneider S, Schmedtje U (2004) Ecological classification of macrophytes and phytobenthos for rivers in Germany according to the Water Framework Directive. Limnologica 34:283–301
Scheffer M, Hosper SH, Meijer ML, Moss B, Jeppesen E (1993) Alternative equilibria in shallow lakes. Trends Ecol Evol 8:275–279
Schmetje U, Kohmann F (1987) Bioindikation durch Makrophyten – indizieren Makrophyten Saprobie? Arch Hydrobiol 199:455–469
Schneider S, Lindstrøm EA (2009) Bioindication in Norwegian rivers using non-diatomaceous benthic algae: the acidification index periphyton (AIP). Ecol Indic 9:1206–1211
Schneider S, Lindstrøm EA (2011) The periphyton index of trophic status PIT: a new eutrophication metric based on non-diatomaceous benthic algae in Nordic rivers. Hydrobiologia 665:143–155
Schneider S, Melzer A (2003) The Trophic Index of Macrophytes (TIM) – a new tool for indicating the trophic state of running waters. Int Rev Hydrobiol 88:49–67
Schneider S, Melzer A (2004) Sediment and water nutrient characteristics in patches of submerged macrophytes in running waters. Hydrobiologia 527:195–207
Schneider SC, Moe TF, Hessen DO, Kaste O (2013a) Juncus bulbosus nuisance growth in oligotrophic freshwater ecosystems: different triggers for the same phenomenon in rivers and lakes? Aquat Bot 104:15–24
Schneider SC, Kahlert M, Kelly MG (2013b) Interactions between pH and nutrients on benthic algae in streams and consequences for ecological status assessment and species richness patterns. Sci Total Environ 444:73–84
Schneider SC, Cara M, Eriksen TE, Budzakoska Goreska B, Imeri A, Kupe L, Lokoska T, Patceva S, Trajanovska S, Trajanovski S, Talevska M, Veljanoska Sarafilovska E (2014) Eutrophication impacts littoral biota in Lake Ohrid while water phosphorus concentrations are low. Limnologica 44:90–97
Schulz M, Kozerski HP, Pluntke T, Rinke K (2003) The influence of macrophytes on sedimentation and nutrient retention in the lower River Spree (Germany). Water Res 37:569–578
Siong K, Asaeda T (2006) Does calcite encrustation in Chara provide a phosphorus nutrient sink? J Environ Qual 35:490–494
Smith MJ, Ough KM, Scroggie MP, Schreiber ESG, Kohout M (2009) Assessing changes in macrophyte assemblages with salinity in non-riverine wetlands: a Bayesian approach. Aquat Bot 90:137–142
Steyaert P, Ollivier G (2007) The European Water Framework Directive: how ecological assumptions frame technical and social change. Ecol Soc 12(1):25
Timm H, Moels T (2012) Littoral macroinvertebrates in Estonian lowland lakes: the effects of habitat, season, eutrophication and land use on some metrics of biological quality. Fundam Appl Limnol 180:145–156
Tremp H, Kohler A (1995) The usefulness of macrophyte monitoring-systems, exemplified on eutrophication and acidification of running waters. Acta Botanica Gallica 142:541–550
Twilley RR, Ejdung G, Romare P, Kemp WM (1986) A comparative study of decomposition, oxygen consumption and nutrient release for selected aquatic plants occurring in an estuarine environment. Oikos 47:190–198
Vermaat JE, Santamaria L, Roos PJ (2000) Water flow across and sediment trapping in submerged macrophyte beds of contrasting growth form. Arch Hydrobiol 148:549–562
Vollenweider RA, Kerekes J (1982) Eutrophication of waters. Monitoring, assessment and control. OECD cooperative programme on monitoring of inland waters (Eutrophication control), Environment Directorate, OECD, Paris, p 154
von der Ohe PC, Apitz S, Arbaciauskas K, Beketov MA, Borchardt D, de Zwart D, Goedkoop W, Hein M, Hellsten S, Hering D, Kefford BJ, Panov VE, Schafer RB, Segner H, van Gils J, Vegter JJ, Wetzel MA, Brack W (2014) Status and causal pathway assessments supporting River Basin management. In: Brils J, Brack W, Müller-Grabherr D, Négrel P, Vermaat JE (eds) Risk-informed management of European River Basins. Springer, Heidelberg, p 395
Wagenhoff A, Lange K, Townsend CR, Matthaei CD (2013) Patterns of benthic algae and cyanobacteria along twin-stressor gradients of nutrients and fine sediment: a stream mesocosm experiment. Freshw Biol 58:1849–1863
Wetzel RG (2001) Limnology – lake and river ecosystems, 3rd edn. Academic, San Diego
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This manuscript resulted from >15 years of work on ecological assessment and the Water Framework Directive. Numerous colleagues have participated in discussions, and many organizations provided funding for a multitude of different projects. We thank the authors of the Water Framework Directive for putting ecology into focus, the editor and a reviewer for constructive feedback, and a countless number of colleagues for inspiring discussions.
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Schneider, S.C., Hilt, S., Vermaat, J.E., Kelly, M. (2016). The “Forgotten” Ecology Behind Ecological Status Evaluation: Re-Assessing the Roles of Aquatic Plants and Benthic Algae in Ecosystem Functioning. In: Cánovas, F., Lüttge, U., Matyssek, R. (eds) Progress in Botany Vol. 78. Progress in Botany, vol 78. Springer, Cham. https://doi.org/10.1007/124_2016_7
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