Skip to main content

Benthic macrophyte metrics as bioindicators of water quality: towards overcoming typological boundaries and methodological tradition in Mediterranean and Black Seas

Abstract

Benthic macrophyte communities of different substratum types (soft, hard) were studied in eleven differently impacted sites belonging in two different water typologies (transitional waters: Lesina Lagoon, Varna Lake; coastal waters: Varna Bay) and two ecoregions (Mediterranean Sea, Black Sea). Species lists were compiled for each study site, 20 taxa were found at Lesina and Varna Lake and Bay, and the abundance of each taxon was determined at each site. The relationship between nine metrics related to community structure [species richness, % of total coverage, dry biomass (g/m−2), and cluster and multi-dimensional scaling plot of Bray–Curtis similarity] and function [Ecological Status Group I % coverage, ESG II % coverage, Ecological Evaluation Index (EEI-c) and Ecological Index (EIEEI)] and key abiotic factors and an anthropogenic stress index (EnII) were studied. A strong relationship (Spearman rank correlation coefficient ρ ≤ −0.89; R 2 ≥ 0.89) between anthropogenic stress and functional indices, EEI-c and EIEEI, was found. The structural index ‘species richness’ correlated negatively with EnII and positively with salinity, demonstrating a freshwater and confinement influence on species diversity. EEI-c and EIEEI indices classified the studied sites and locations in different Ecological Status Classes in accordance with the anthropogenic stress gradient.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Agostini, S., A. Capiomont, B. Marchand & G. Pergent, 2003a. Distribution and estimation of basal area coverage of subtital seagrass meadows in a Mediterranean coastal lagoon. Estuarine Coastal and Shelf Science 56: 1021–1028.

    Article  Google Scholar 

  2. Agostini, S., B. Marchand & G. Pergent, 2003b. Temporal and spatial changes of seagrass meadows in a Mediterranean coastal lagoon. Oceanologica Acta 25: 297–302.

    Article  Google Scholar 

  3. Agostini, S., G. Pergent & B. Marchand, 2003c. Growth and primary production of Cymodocea nodosa in a coastal lagoon. Aquatic Botany 76: 185–193.

    Article  Google Scholar 

  4. Andersen, J. H., L. Schlüter & G. Ærtebjerg, 2006. Coastal eutrophication: recent developments in definitions and implications for monitoring strategies. Journal of Plankton Research 28: 621–628.

    Article  CAS  Google Scholar 

  5. Aubry, A. & M. Elliott, 2006. The use of environmental integrative indicators to assess seabed disturbance in estuaries and coasts: application to the Humber Estuary, UK. Marine Pollution Bulletin 53: 175–185.

    PubMed  Article  CAS  Google Scholar 

  6. Bakker, E. S., E. Van Donka, S. A. J. Declercka, N. R. Helmsinga, B. Hiddinga & B. A. Noletd, 2010. Effect of macrophyte community composition and nutrient enrichment on plant biomass and algal blooms. Basic and Applied Ecology 11: 432–439.

    Article  Google Scholar 

  7. Ballesteros, E., X. Torras, S. Pinedo, M. García, L. Mangialajo & M. de Torres, 2007. A new methodology based on littoral community cartography dominated by macroalgae for the implementation of the European Water Framework Directive. Marine Pollution Bulletin 55: 172–180.

    PubMed  Article  CAS  Google Scholar 

  8. Basset, A., L. Sabetta, A. Fonnesu, D. Mouillot, D. Do Chi, P. Viaroli, G. Giordani, S. Reizopoulou, M. Abbiati & G. C. Carrada, 2006. Typology in Mediterranean transitional waters: new challenges and perspectives. Aquatic Conservation: Marine and Freshwater Ecosystems 16: 441–455.

    Article  Google Scholar 

  9. Birk, S., J. Strackbein & D. Hering, 2010. WISER methods database. Version: May 2010. Available at http://www.wiser.eu/programme-and-results/data-and-guidelines/method-database/.

  10. Borja, A., E. Barbone, A. Basset, G. Borgersen, M. Brkljacic, J. M. Garmendia, J. C. Marques, K. Mazik, I. Muxika, J. M. Neto, K. Norling, J. G. Rodríguez, I. Rosati, B. Rygg, H. Teixeira & A. Trayanova, 2011. Response of single benthic metrics and multi-metric methods to anthropogenic pressure gradients, in five distinct European coastal and transitional ecosystems. Marine Pollution Bulletin 62: 499–513.

    PubMed  Article  CAS  Google Scholar 

  11. Breber P., R. Povilanskas & A. Armaitiene, 2008. Recent evolution of fishery and land reclamation in Curonian and Lesina lagoons. Hydrobiologia 611: 105–114.

    Article  Google Scholar 

  12. Calado, G. & P. Duarte, 2000. Modelling growth of Ruppia cirrhosa. Aquatic Botany 68: 29–44.

    Article  Google Scholar 

  13. Carletti, A. & A.S. Heiskanen, 2009. Water Framework Directive intercalibration technical report – Part 3: coastal and transitional waters. EUR 23838 EN/3.

  14. Carr, M. R., 1997. Primer user manual. Plymouth Marine Laboratory, Plymouth: 44 pp.

    Google Scholar 

  15. Casagranda, C. & C. F. Boudouresque, 2007. Biomass of Ruppia cirrhosa and Potamogeton pectinatus in a Mediterranean brackish lagoon, Lake Ichkeul, Tunisia. Archiv für Hydrobiologie 168: 243–255.

    Article  Google Scholar 

  16. Cecere, E., A. Petrocelli, G. Izzo & A. Sfriso, 2009. Flora and vegetation of the Italian transitional water systems. Corila, Lagunet, Venezia.

    Google Scholar 

  17. Cloern, J. E., 2001. Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology Progress Series 210: 223–253.

    Article  CAS  Google Scholar 

  18. Coutino, R. & U. Seeliger, 1984. The horizontal distribution of the benthic algal flora in the Patos Lagoon estuary, Brazil, in relation to salinity, substratum and wave exposure. Journal of Experimental Marine Biology and Ecology 80: 247–257.

    Article  Google Scholar 

  19. Curiel, D., A. Rismondo, G. Bellemo & M. Marzocchi, 2004. Macroalgal biomass and species variations in the lagoon of Venice (Northern Adriatic Sea, Italy): 1981–1998. Scientia Marina 68: 57–67.

    Article  Google Scholar 

  20. Curiel, D., A. Falace, V. Bandelj & A. Rismondo, 2012. Applicability and intercalibration of macrophyte quality indices to characterise the ecological status of Mediterranean transitional waters: the case of the Venice lagoon. Marine Ecology 33: 437–459.

    Article  Google Scholar 

  21. De Jonge, V. N., M. Elliott & E. Orive, 2002. Causes, historical development, effects and future challenges of a common environmental problem: eutrophication. Hydrobiologia 475(476): 1–19.

    Article  Google Scholar 

  22. De Vries, I., C. J. M. Philippart, E. G. De Groot & M. W. M. Van der Tol, 1996. Coastal eutrophication and marine benthic vegetation: a model analysis. In Schramm, W. & P. H. Nienhuis (eds), Marine benthic vegetation: recent changes and the effects of eutrophication. Springer, Berlin: 79–113.

    Chapter  Google Scholar 

  23. Dencheva, K., 2010. State of macrophytobenthic communities and ecological status of the Varna Bay, Varna lakes and Burgas Bay. Phytologia Balcanica 16: 43–50.

    Google Scholar 

  24. Dennison, W. C., R. J. Orth, K. A. Moore, J. C. Stevenson, V. Carter, S. Kollar, P. W. Berstrom & R. A. Batiuk, 1993. Assessing water quality with submerged aquatic vegetation. BioScience 43: 86–94.

    Article  Google Scholar 

  25. Domin, A., H. Schubert, J. C. Krause & U. Schiewer, 2004. Modelling of pristine depth limits for macrophyte growth in the southern Baltic Sea. Hydrobiologia 514: 29–39.

    Article  Google Scholar 

  26. Duarte, C. M., 1995. Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia 41: 87–112.

    Article  Google Scholar 

  27. Duke, C. S., A. Cezeaux & M. M. Allen, 1989. Changes in polypeptide composition of Synechocystis sp. strain 6308 phycobilisomes induced by nitrogen starvation. Journal of Bacteriology 4: 1960–1966.

    Google Scholar 

  28. Duraco, M. J., 1995. Indicators of seagrass ecological conditions: an assessment based on spatial and temporal changes associated with the mass mortality of the tropical seagrass Thalassia testudinum. In Dyer, K. R. & R. J. Orth (eds), Changes in fluxes in estuaries: implications for science to management. Olsen and Olsen, Fredensborg: 261–266.

    Google Scholar 

  29. Elliot, M. & V. Quintino, 2007. The estuarine quality paradox, environmental homeostatis and the difficulty of detecting anthropogenic stress in naturally stressed areas. Marine Pollution Bulletin 54: 640–645.

    Article  Google Scholar 

  30. European Commission (EC), 2000. Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for Community actions in the field of water policy. Official Journal of the European Communities L327, 1–73. 22.12.2000.

  31. European Parliament Council (EPC), 2008. Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008 Establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive).http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2008:164:0019:0040:EN:PDF.

  32. Falace, A., D. Curiel & A. Sfriso, 2009. Study of the macrophyte assemblages and application of phytobenthic indices to assess the Ecological Status of the Marano–Grado Lagoon (Italy). Marine Ecology 30: 480–494.

    Article  Google Scholar 

  33. Gambi C., C. Totti & E. Manini, 2008. Impact of organic loads and environmental gradients on microphytobenthos and meiofaunal distribution in a coastal lagoon. Chemistry and Ecology 19: 207–223.

    Article  Google Scholar 

  34. García-Sánchez, M., N. Korbee, I. M. Pérez-Ruzafa, C. Marcos, B. Domínguez, F. L. Figueroa & Á. Pérez-Ruzafa, 2012. Physiological response and photoacclimation capacity of Caulerpa prolifera (Forsskål) J.V. Lamouroux and Cymodocea nodosa (Ucria) Ascherson meadows in the Mar Menor lagoon (SE Spain). Marine Environmental Research 79: 37–47.

    PubMed  Article  Google Scholar 

  35. Gibson, G.R., M .L. Bowman, J. Gerritsen & B. D. Snyder, 2000. Estuarine and coastal marine waters: bioassessment and biocriteria technical guidance. EPA 822-B-00-024. US Environmental Protection Agency, Office of Water, Washington, DC. Available online at http://www.epa.gov/ost/biocriteria/States/estuaries/Estuaries-final.pdf.

  36. Grece, T. M. & T. Binzer, 2004. Which factors regulate seagrass growth and distribution? In Borum, J., C.M. Duarte, D. Krause-Jensen & T. M. Greve (ed.), European seagrasses: an introduction to monitoring and management. Monitoring and Managing of European Seagrasses Project (M&MS): 19–23.

  37. Guiry, M.D. & G.M. Guiry, 2013. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org.

  38. Hein, M., M. F. Pedersen & K. Sand-Jensen, 1995. Size-dependent nitrogen uptake in micro- and macroalgae. Marine Ecology Progress Series 118: 247–253.

    Article  Google Scholar 

  39. Hemminga, M. A. & C. M. Duarte, 2000. Seagrass Ecology. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  40. Holling, C.S., 1973. Resilience and stability of ecological systems. Annual Review of Ecology & Systematics 4: 1–23. http://publications.jrc.ec.europa.eu/repository/bitstream/111111111/10473/1/3010_08-volumecoast.pdf.

  41. Irving, A. D. & S. D. Connell, 2006. Predicting understorey structure from the presence and composition of canopies: an assembly rule for marine algae. Oecologia 148: 491–502.

    PubMed  Article  Google Scholar 

  42. Iveša, L., D. M. Lyons & M. Devescovi, 2009. Assessment of the ecological status of north-eastern Adriatic coastal waters (Istria, Croatia) using macroalgal assemblages for the European Union Water Framework Directive. Aquatic Conservation: Marine & Freshwater Ecosystems 19: 14–23.

    Article  Google Scholar 

  43. Kautsky, H., 1995. Quantitative distribution of sublittoral plant and animal communities along the Baltic Sea gradient. In Eleftheriou, A., A. D. Ansell & C. J. Smint (eds), Biology and Ecology of Shallow Coastal Waters. Proceedings of the 28th European Marine Biology Symposium, Olsen and Olsen, Fredensborg: 23–30.

  44. Körner, S. & A. Nicklisch, 2002. Allelopathic growth inhibition of selected phytoplankton species by submerged macrophytes. Journal of Phycology 38: 862–871.

    Article  Google Scholar 

  45. Krause-Jensen, D., T. M. Greve & K. Nielsen, 2004. Eelgrass as bioindicator under the European Water Framework Directive. Water Resources Management 19: 63–75.

    Article  Google Scholar 

  46. Kunii, H. & K. Minamoto, 2000. Temporal and spatial variation in the macrophyte distribution in coastal lagoon Lake Nakaumi and its neighbouring waters. Journal of Marine Systems 26: 223–231.

    Article  Google Scholar 

  47. Lüning, K., 1990. Seaweeds: Their Environment, Biogeography and Ecophysiology. Wiley, New York.

    Google Scholar 

  48. Lobban, C. S. & P. J. Harrison, 1994. Seaweed Ecology and Physiology. Cambridge University Press, Cambridge: 163–209.

    Book  Google Scholar 

  49. Lugoli, F., M. Garmendia, S. Lehtinen, P. Kauppila, S. Moncheva, M. Revilla, L. Roselli, N. Slabakova, V. Valencia, K. M. Dromph & A. Basset, 2012. Application of a new multi-metric phytoplankton index to the assessment of ecological status in marine and transitional waters. Ecological Indicators 23: 338–355.

    Article  Google Scholar 

  50. Malea, P., T. Kevrekidis & A. Mogias, 2004. Annual versus perennial growth cycle in Ruppia maritima L.: temporal variation in population characteristics in Mediterranean lagoons (Monolimni and Drana Lagoons, Northern Aegean Sea). Botanica Marina 47: 357–366.

    Article  Google Scholar 

  51. Mannino, A. M. & G. Sarà, 2006. The effect of Ruppia cirrhosa features on macroalgae and suspended matter in a Mediterranean shallow system. Marine Ecology 27: 350–360.

    Article  CAS  Google Scholar 

  52. Marbà, N., D. Krause-Jensen, T. Alcoverro, S. Birk, A. Pedersen, J. A. Neto, S. Orfanidis, J. M. Garmendia, I. Muxika, A. Borja, K. Dencheva & C. M. Duarte, 2013. Diversity of European seagrass indicators: patterns within and across regions. Hydrobiologia 704: 265–278.

    Article  Google Scholar 

  53. May, R. M., 1977. Thresholds and breakpoints in ecosystems with a multiplicity of stable states. Nature 267: 471–477.

    Article  Google Scholar 

  54. McGlathery, K. J., K. Sundbäck & I. C. Anderson, 2007. Eutrophication in shallow coastal bays and lagoons: the role of plants in the coastal filter. Marine Ecology Progress Series 348: 1–18.

    Article  CAS  Google Scholar 

  55. Menéndez, M., 2002. Net production of Ruppia cirrhosa in Ebro Delta. Aquatic Botany 73: 107–113.

    Article  Google Scholar 

  56. Middelboe, A. L., K. Sand-Jensen & D. Krause-Jensen, 1998. Patterns of macroalgal species diversity in Danish estuaries. Journal of Phycology 34: 457–466.

    Article  Google Scholar 

  57. Mouillot, D., S. Spatharis, S. Reizopoulou, T. Laugier, L. Sabetta, A. Basset & T. Do Chi, 2006. Alternatives to taxonomic-based approaches to assess changes in transitional water communities. Aquatic Conservation: Marine and Freshwater Ecosystems 16: 469–482.

    Article  Google Scholar 

  58. Nedwell, D. B., A. S. Sage & G. J. C. Underwood, 2002. Rapid assessment of macro algal cover on intertidal sediments in a nutrified estuary. The Science of Total Environment 285: 97–105.

    Article  CAS  Google Scholar 

  59. Nielsen, S. L. & K. Sand-Jensen, 1990. Allometric scaling of maximal photosynthetic growth rate to surface/volume ratio. Limnology & Oceanography 35: 177–181.

    Article  CAS  Google Scholar 

  60. Odum, E. P., 1985. Trends expected in stressed ecosystems. Bioscience 35: 419–422.

    Article  Google Scholar 

  61. Orfanidis, S., M. Pinna, L. Sabetta, N. Stamatis & K. Nakou, 2008. Variation of structural and functional metrics in macrophyte communities within two habitats of eastern Mediterranean coastal lagoons: natural versus human effects. Aquatic Conservation: Marine and Freshwater Ecosystems 18: S45–S61.

    Article  Google Scholar 

  62. Orfanidis, S., P. Panayotidis & K. Ugland, 2011. Ecological Evaluation Index continuous formula (EEI-c) application: a step forward for functional groups, the formula and reference condition values. Mediterranean Marine Science 12: 199–231.

    Article  Google Scholar 

  63. Orth, R. J., T. J. B. Carruthers, W. C. Dennison, C. M. Duarte, J. W. Fourqurean, K. Heck, A. R. Hughes, G. A. Kendrick, W. J. Kenworthy, S. Olyarnik, F. T. Short, M. Waycott & S. L. Williams, 2006. A global crisis for seagrass ecosystems. BioScience 56: 987–996.

    Article  Google Scholar 

  64. Panayotidis, P., B. Montesanto & S. Orfanidis, 2004. Use of low-budget monitoring of macroalgae to implement the European Water Framework Directive. Journal of Applied Phycology 16: 49–59.

    Article  Google Scholar 

  65. Patrício, J., J. M. Neto, H. Teixeira & J. C. Marques, 2007. Opportunistic macroalgae metrics for transitional waters. Testing tools to assess ecological quality status in Portugal. Marine Pollution Bulletin 54: 1887–1896.

    PubMed  Article  Google Scholar 

  66. Pauly, D., 1995. Anecdotes and the shifting baseline syndrome of fisheries. Tree 10: 430.

    PubMed  CAS  Google Scholar 

  67. Pedersen, M. F. & J. Borum, 1997. Nutrient control of estuarine algae: growth strategy and the balance between nitrogen requirements and uptake. Marine Ecology Progress Series 161: 155–163.

    Article  Google Scholar 

  68. Peychev, V. & M. Stancheva, 2009. Changes of sediment balance at the Bulgarian Black Sea coastal zone influenced by anthropogenic impacts. Comptes rendus de l’Académie bulgare des Sciences 62(2): 277–285.

    CAS  Google Scholar 

  69. Phillips, G. L., D. Eminson & B. Moss, 1978. A mechanism to account for macrophyte decline in progressively eutrophicated freshwaters. Aquatic Botany 4: 103–126.

    Article  Google Scholar 

  70. Pinedo, S., M. García, M. P. Satta, M. de Torres & E. Ballesteros, 2007. Rocky-shore communities as indicators of water quality: a case study in the Northwestern Mediterranean. Marine Pollution Bulletin 55: 126–135.

    PubMed  Article  CAS  Google Scholar 

  71. Renzi, M., A. Specchiulli, D. Baroni, T. Scirocco, L. Cilenti, S. Focardi, P. Breber & S. Focardi, 2012. Trace elements in sediments and bioaccumulation in European eels (Anguilla anguilla) from a Mediterranean lagoon (SE Italy). International Journal of Environmental Analytical Chemistry 92: 676–697.

  72. Rismondo, A., D. Curiel, M. Marzocchi & M. Scattolin, 1997. Seasonal patterns of Cymodocea nodosa biomass and production in the lagoon of Venice. Aquatic Botany 58: 55–64.

    Article  Google Scholar 

  73. Roselli, L., A. Fabbrocini, C. Manzo & R. D’Adamo, 2009. Hydrological heterogeneity, nutrient dynamics and water quality of a non-tidal lentic ecosystem (Lesina Lagoon, Italy). Estuarine Coastal and Shelf Science 84: 539–552.

    Article  CAS  Google Scholar 

  74. Roselli L., M. Cañedo-Argüelles, P. Costa Goela, S. Cristina, M. Rieradevall, R. D’Adamo & A. Newton, 2013. Do physiography and hydrology determine the physico-chemical properties and trophic status of coastal lagoons? A comparative approach. Estuarine, Coastal & Shelf Science 117: 29–36.

    Article  CAS  Google Scholar 

  75. Rosenberg, G. & J. Ramus, 1984. Uptake of inorganic nitrogen and seaweed surface area: volume ratios. Aquatic Botany 19: 65–72.

    Article  CAS  Google Scholar 

  76. Rozhdestvensky, A., 1986. Hydrochemistry of the Bulgarian sector of the Black Sea. Publishing House Bulgarian Academy of Science, Sofia. (in Bulgarian).

    Google Scholar 

  77. Rozhdestvensky, A., 1992. The impact of anthropogenic factors on the hydrology and on the hydrochemistry of the Varna Lake. Proceedings of Institute of Oceanology, Bulgarian Academy of Science 1: 48–57.

    Google Scholar 

  78. Sand-Jensen, K., T. Binzer & A. L. Middelboe, 2007. Scaling of photosynthetic production of aquatic macrophytes – a review. Oikos 116: 280–294.

    CAS  Google Scholar 

  79. Scanlan, C. M., J. Foden, E. Wells & M. A. Best, 2007. The monitoring of opportunistic macroalgal blooms for the water framework directive. Marine Pollution Bulletin 55: 162–171.

    PubMed  Article  CAS  Google Scholar 

  80. Scheffer, M., S. Carpenter, J. A. Foley, C. Folke & B. Walker, 2001. Catastrophic shifts in ecosystems. Nature 413: 591–596.

    PubMed  Article  CAS  Google Scholar 

  81. Schernewski, G. & M. Wielgat, 2004. A Baltic Sea typology according to the EC-Water Framework Directive: integration of national typologies and the water body concept. In Schernewski, G. & M. Weilgat (eds), Baltic Sea Typology. Coastline Reports, Vol. 4. EUCC – The Coastal Union, Leiden: 1–26.

  82. Schramm, W., 1999. Factors influencing seaweed responses to eutrophication: some results from EU-project EUMAC. Journal of Applied Phycology 11: 69–78.

    Article  Google Scholar 

  83. Schramm, W. & P. H. Nienhuis, 1996. Marine Benthic Vegetation. Recent Changes and the Effects of Eutrophication. Springer, New York.

    Book  Google Scholar 

  84. Schubert, H., P. Feuerpfeil, R. Marquardt, I. Telesh & S. Skarlato, 2011. Macroalgal diversity along the Baltic Sea salinity gradient challenges Remane’s species-minimum concept. Marine Pollution Bulletin 62: 1948–1956.

    PubMed  Article  CAS  Google Scholar 

  85. Sfriso, A. & P. F. Ghetti, 1998. Seasonal variation in biomass, morphometric parameters and production of seagrasses in the lagoon of Venice. Aquatic Botany 61: 1–17.

    Article  Google Scholar 

  86. Sfriso, A., A. Marcomini & B. Pavoni, 1987. Relationships between macroalgal biomass and nutrient concentration in a hypertrophic area of the Venice Lagoon Italy. Marine Environmental Research 22: 297–312.

    Article  CAS  Google Scholar 

  87. Sfriso, A., B. La Rocca & E. Godini, 2002. Inventario dei taxa macroalali in tre aree della laguna di Venezia a differente livello di trofia. Società Veneziana Scienze Naturali 27: 85–99.

    Google Scholar 

  88. Shtereva, G., O. Hristova, B. Dzurova & A. Krastev, 2012. Hydrochemistry of Varna Bay (2000–2008). Journal of Environmental Protection and Ecology (JEPE) 13: 1695–1702.

    CAS  Google Scholar 

  89. Spatharis, S., S. Orfanidis, P. Panayotidis & G. Tsirtsis, 2011. Assembly processes in upper sublittoral macroalage: the effect of wave exposure. Estuarine, Coastal & Shelf Science 91: 298–305.

    Article  Google Scholar 

  90. Specchiulli, A., R. D’Adamo, M. Renzi, F. Vignes, A. Fabbrocini, T. Scirocco, L. Cilenti, M. Florio, P. Breber & A. Basset, 2009. Fluctuations of physicochemical characteristics in sediments and overlying water during an anoxic event: a case study from Lesina lagoon (SE Italy). Transitional Waters Bulletin 3: 15–32.

    Google Scholar 

  91. Specchiulli, A., M. Renzi, T. Scirocco, L. Cilenti, M. Florio, P. Breber, S. Focardi & S. Bastianoni, 2010. Comparative study based on sediment characteristics and macrobenthic communities in two Italian lagoons. Environmental Monitoring and Assessment 160: 237–256.

    PubMed  Article  CAS  Google Scholar 

  92. Specchiulli A., M. Renzi, G. Perra, L. Cilenti, T. Scirocco, M. Florio, S. Focardi, P. Breber & S. Focardi, 2011. Distribution and sources of polycyclic hydrocarbons (PAHs) in surface sediments of some Italian lagoons exploited for aquaculture and fishing activities. International Journal of Environmental Analytical Chemistry 91: 367–386.

    Article  CAS  Google Scholar 

  93. Stojanov, A., 1991. Negative changes in hydrochemical regime in Beloslav Lake – Varna Bay area. In Union of Scientists, Rational Use and Protection of Natural Resources of Varna Region, Varna: 38–46 (in Bulgarian).

  94. Telesh, I. V. & V. V. Khlebovich, 2010. Principal processes within the estuarine salinity gradient: a review. Marine Pollution Bulletin 61: 149–155.

    PubMed  Article  CAS  Google Scholar 

  95. Terrados, J. & J. D. Ros, 1992. Growth and primary production of Cymodocea nodosa (Ucria) Ascherson in a Mediterranean coastal lagoon: the Mar Menor (SE Spain). Aquatic Botany 43: 63–78.

    Article  Google Scholar 

  96. Thiebaut, G., F. Guérold & S. Muller, 2002. Are trophic and diversity indices on macrophyte communities pertinent tools to monitor water quality? Water Research 36: 3602–3610.

    PubMed  Article  CAS  Google Scholar 

  97. United States Environmental Protection Agency (USEPA), 2003. Guidance for 2004 Assessment, Listing and Reporting Requirements Pursuant to Sections 303(d) and 305(b) of the Clean Water Act. United States Environmental Protection Agency, Office of Water, Office of Wetlands, Oceans, and Watersheds.

  98. Vadrucci, M. R., A. Fiocca, F. Vignes, A. Fabbrocini, L. Rosselli, R. D’Adamo, N. Ungaro & A. Basset, 2009. Dynamics of phytoplankton under dystrophic pressures in Lesina lagoon. Transitional Waters Bulletin 3: 89–103.

    Google Scholar 

  99. Verhoeven, J. T. A., 1979. The ecology of Ruppia-dominated communities in western Europe. I. Distribution of Ruppia representatives in relation to their autecology. Aquatic Botany 6: 197–268.

    Article  CAS  Google Scholar 

  100. Verhoeven, J. T. A., 1980. The ecology of Ruppia-dominated communities in western Europe. III. Aspects of production, consumption and decomposition. Aquatic Botany 8: 209–253.

    Article  CAS  Google Scholar 

  101. Viaroli, P., M. Bartoli, G. Giordani, M. Naldi, S. Orfanidis & J. M. Zaldivar, 2008. Community shifts, alternative stable states, biogeochemical controls and feedbacks and in eutrophic coastal lagoons: a brief review. Aquatic Conservation: Marine and Freshwater Ecosystems 18: S105–S117.

    Article  Google Scholar 

  102. Vignes, F., E. Barbone, P. Breber, R. D’Adamo, L. Roselli, N. Ungaro, S. Focardi, M. Renzi & A. Basset, 2009. Spatial and temporal description of the dystrophic crisis in Lesina lagoon during summer 2008. Transitional Waters Bulletin 3: 114–119.

    Google Scholar 

  103. Wallentinus, I., 1991. The Baltic Sea gradient. In Mathieson, A. C. & P. H. Nienhuis (eds), Ecosystems of the World. Elsevier, Amsterdam: 83–108.

    Google Scholar 

  104. Waycott, M., C. M. Duarte, T. J. B. Cattuthers, R. J. Orth, W. C. Dennison, S. Olayarnik, A. Calladine, J. W. Fourqurean, K. Heck, A. R. Hughes, G. A. Kenrick, W. J. Kenworthy, F. T. Short & S. Williams, 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences of the United States of America 106: 12377–12381.

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  105. Wilkinson, M., P. Wood, E. Wells & C. Scanlan, 2007. Using attached macroalgae to assess ecological status of British estuaries for the European water framework directive. Marine Pollution Bulletin 55: 136–150.

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

This paper is a result of the project WISER (Water bodies in Europe: Integrative Systems to assess Ecological status and Recovery) funded by the European Union under the 7th Framework Programme, Theme 6 (Environment including Climate Change) (Contract No. 226273), http://www.wiser.eu. The Greek team is also very grateful to the TOTAL Foundation (Paris; Project ‘Brown algal biodiversity and ecology in the Eastern Mediterranean Sea’) for additional support. We are very grateful to Dr. Claire Gachon for her contribution in the tentative identification of Oedogonium sp.

Author information

Affiliations

Authors

Corresponding author

Correspondence to S. Orfanidis.

Additional information

Handling editor: Pierluigi Viaroli

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 42 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Orfanidis, S., Dencheva, K., Nakou, K. et al. Benthic macrophyte metrics as bioindicators of water quality: towards overcoming typological boundaries and methodological tradition in Mediterranean and Black Seas. Hydrobiologia 740, 61–78 (2014). https://doi.org/10.1007/s10750-014-1938-x

Download citation

Keywords

  • Macroalgae
  • Angiosperms
  • Functional groups
  • Water quality
  • Eutrophication
  • Biotic indices
  • Alternative stable stages