Advertisement

Hydrobiologia

, Volume 808, Issue 1, pp 175–200 | Cite as

Submerged benthic macrophytes in Mediterranean lagoons: distribution patterns in relation to water chemistry and depth

  • Ines Le FurEmail author
  • Rutger De Wit
  • Martin Plus
  • Jocelyne Oheix
  • Monique Simier
  • Vincent Ouisse
Primary Research Paper

Abstract

A large spectrum of coastal lagoon types with a wide range of environmental conditions is observed along the French Mediterranean coast. These comprise wide trophic and salinity gradients, ranging from oligotrophic to hypertrophic status, and from nearly freshwater to slightly above marine Mediterranean Sea water salinities, respectively. The statistical analysis of a long-term dataset, including water column variables and observations of macrophyte genera, showed that salinity, depth, and then trophic status, were important factors explaining the distribution of benthic macrophytes for the soft-bottom sediments in the 34 studied French Mediterranean lagoons. Based on this, we assumed that the vegetation succession along the eutrophication gradient was different according to the lagoon salinity ranges. Euhaline and polyhaline lagoons follow the well-known Schramm schematic model, where aquatic angiosperm such as seagrasses dominate under oligotrophic conditions, and opportunistic macroalgae and phytoplankton dominate under eutrophic and hypertrophic conditions. In oligohaline and mesohaline lagoons, the succession is probably an intermediate scheme between the successions observed in small temperate lakes and in marine coastal ecosystems due to the presence of both brackish and freshwater species. We thus propose a conceptual scheme for the oligohaline and mesohaline lagoons.

Keywords

French coastal lagoons Submerged aquatic vegetation (SAV) Eutrophication Salinity Depth Canonical correspondence analysis (CCA) 

Notes

Acknowledgements

This study was supported by a Ph.D. Grant for Ines Le Fur, financed by Ifremer and the French Water Agency (Agence de l’Eau Rhône Méditerranée Corse). The authors thank the staff of the Ifremer laboratory in Languedoc-Roussillon and PACA, the Tour du Valat institute, lagoons managers of the GIPREB and of the Réserve Nationale de Camargue and all surveyors involved in the collection of the data on which this article is based.

Supplementary material

10750_2017_3421_MOESM1_ESM.docx (36 kb)
Supplementary material 1 (DOCX 36 kb)

References

  1. Adams, P., J. C. Thomas, D. M. Vernon, H. J. Bohnert & R. G. Jensen, 1992. Distinct cellular and organismic responses to salt stress. Plant and Cell Physiology 33: 1215–1223.Google Scholar
  2. Agostini, S., G. Pergent & B. Marchand, 2003. Growth and primary production of Cymodocea nodosa in a coastal lagoon. Aquatic Botany 76: 185–193.CrossRefGoogle Scholar
  3. Anonymous, 1958. The Venice System for the classification of marine waters according to salinity. Limnology and Oceanography 3: 346–347.CrossRefGoogle Scholar
  4. Anthony, A., J. Atwood, P. August, C. Byron, S. Cobb, C. Foster, C. Fry, A. Gold, K. Hagos, L. Heffner, D. Kellogg, K. Lellis-Dibble, J. Opaluch, C. Oviatt, A. Pfeiffer-Herbert, N. Rohr, L. Smith, T. Smythe, J. Swift & N. Vinhateiro, 2009. Coastal lagoons and climate change: ecological and social ramifications in U.S. Atlantic and Gulf Coast ecosystems. Ecology and Society 14: 8.CrossRefGoogle Scholar
  5. Antunes, C., O. Correia, J. M. da Silva, A. Cruces, M. Conceição Freitas & C. Branquinho, 2012. Factors involved in spatiotemporal dynamics of submerged macrophytes in a Portuguese coastal lagoon under Mediterranean climate. Estuarine, Coastal and Shelf Science 110: 93–100.CrossRefGoogle Scholar
  6. Bakker, E. S., E. Van Donk, S. A. J. Declerck, N. R. Helmsing, B. Hidding & B. A. Nolet, 2010. Effect of macrophyte community composition and nutrient enrichment on plant biomass and algal blooms. Basic and Applied Ecology 11: 432–439.CrossRefGoogle Scholar
  7. Barnes, R. S. K., 1980. Coastal Lagoons; the Natural History of a Neglected Habitat. Cambridge University Press, Cambridge.Google Scholar
  8. Bec, B., Y. Collos, P. Souchu, A. Vaquer, J. Lautier, A. Fiandrino, L. Benau, V. Orsoni & T. Laugier, 2011. Distribution of picophytoplankton and nanophytoplankton along an anthropogenic eutrophication gradient in French Mediterranean coastal lagoons. Aquatic Microbial Ecology 63: 29–45.CrossRefGoogle Scholar
  9. den Berg, M. S. V., M. Scheffer, E. V. Nes & H. Coops, 1999. Dynamics and stability of Chara sp. and Potamogeton pectinatus in a shallow lake changing in eutrophication level. Hydrobiologia 408–409: 335–342.CrossRefGoogle Scholar
  10. Blindow, I., 1992. Decline of charophytes during eutrophication: comparison with angiosperms. Freshwater Biology 28: 9–14.CrossRefGoogle Scholar
  11. Borcard, D., P. Legendre & P. Drapeau, 1992. Partialling out the spatial component of ecological variation. Ecology 73: 1045–1055.CrossRefGoogle Scholar
  12. Borgnis, E. & K. E. Boyer, 2016. Salinity tolerance and competition drive distributions of native and invasive submerged aquatic vegetation in the upper San Francisco estuary. Estuaries and Coasts 39: 707–717.CrossRefGoogle Scholar
  13. Brock, M. A., 1986. Adaptation to fluctuations rather than to extremes of environmental parameters. In Deckker, P. D. & W. D. Williams (eds), Limnology in Australia. Springer, Netherlands: 131–140.CrossRefGoogle Scholar
  14. Caliński, T. & J. Harabasz, 1974. A dendrite method for cluster analysis. Communications in Statistics 3: 1–27.Google Scholar
  15. Burkholder, J. M., D. A. Tomasko & B. W. Touchette, 2007. Seagrasses and eutrophication. Journal of Experimental Marine Biology and Ecology 350: 46–72.CrossRefGoogle Scholar
  16. Casagranda, C. & C. F. Boudouresque, 2007. Biomass of Ruppia cirrhosa and Potamogeton pectinatus in a Mediterranean brackish lagoon, Lake Ichkeul, Tunisia. Fundamental and Applied Limnology 168: 243–255.CrossRefGoogle Scholar
  17. Castel, J., P. Caumette & R. Herbert, 1996. Eutrophication gradients in coastal lagoons as exemplified by the Bassin d’Arcachon and the Étang du Prévost. Hydrobiologia 329: ix–xxviii.CrossRefGoogle Scholar
  18. Charpentier, A., P. Grillas, F. Lescuyer, E. Coulet & I. Auby, 2005. Spatio-temporal dynamics of a Zostera noltii dominated community over a period of fluctuating salinity in a shallow lagoon, Southern France. Estuarine, Coastal and Shelf Science 64: 307–315.CrossRefGoogle Scholar
  19. Chesworth, J. C., M. E. Donkin & M. T. Brown, 2004. The interactive effects of the antifouling herbicides Irgarol 1051 and Diuron on the seagrass Zostera marina (L.). Aquatic Toxicology (Amsterdam, Netherlands) 66: 293–305.CrossRefGoogle Scholar
  20. Christia, C. & E. S. Papastergiadou, 2007. Spatial and temporal variations of aquatic macrophytes and water quality in six coastal lagoons of western Greece. Belgian Journal of Botany 140: 39–50.Google Scholar
  21. Cloern, J. E., 2001. Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology Progress Series 210: 223–253.CrossRefGoogle Scholar
  22. Coops, H., 2002. Ecology of charophytes: an introduction. Aquatic Botany 72: 205–208.CrossRefGoogle Scholar
  23. Cromwell, J. E., 1971. Barrier coast distribution: a world-wide survey. Second National Coastal Shallow Water research Conference. Baton Rouge, LA: 50.Google Scholar
  24. 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.CrossRefGoogle Scholar
  25. De Wit, R., 2011. Chapter 2. Biodiversity of coastal lagoon ecosystems and their vulnerability to global change. Ecosystems Biodiversity: 29–40.Google Scholar
  26. Dennison, W. C., 1987. Effects of light on seagrass photosynthesis, growth and depth distribution. Aquatic Botany 27: 15–26.CrossRefGoogle Scholar
  27. Dray, S. & A.-B. Dufour, 2007. The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software 22: 1–20.CrossRefGoogle Scholar
  28. Duarte, C. M., 1991. Seagrass depth limits. Aquatic Botany 40: 363–377.CrossRefGoogle Scholar
  29. Duarte, C. M., 1995. Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia 41: 87–112.CrossRefGoogle Scholar
  30. Duarte, C. M. & J. Cebrián, 1996. The fate of marine autotrophic production. Limnology and Oceanography 41: 1758–1766.CrossRefGoogle Scholar
  31. Dubois, A. & M. Lauret, 1991. Macroflore benthique. In ECOTHAU, synthèse des résultats, D.Jouffre et M.Amanieu éditeurs. Laboratoire d’Hydrologie marine et continentale, Université Montpellier II: 115–118Google Scholar
  32. Eisma, D., 1998. Intertidal Deposits: River Mouths, Tidal Flats, and Coastal Lagoons. CRC Press, Boca Raton.Google Scholar
  33. European Commission (EC), 2000. Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework community actions in the field of water policy. Official Journal of the European Communities L327,1-73.22.12.2000.Google Scholar
  34. Fiandrino, A., V. Ouisse, F. Lagarde, R. Pete, S. Le Noc & R. de Wit, 2017. Spatial patterns in coastal lagoons related to the hydrodynamics of seawater intrusion. Marine Pollution Bulletin 119: 132–144.CrossRefPubMedGoogle Scholar
  35. Flindt, M. R., M. A. Pardal, A. I. Lillebø, I. Martins & J. C. Marques, 1999. Nutrient cycling and plant dynamics in estuaries: a brief review. Acta Oecologica 20: 237–248.CrossRefGoogle Scholar
  36. Fonseca, M. S. & W. J. Kenworthy, 1987. Effects of current on photosynthesis and distribution of seagrasses. Aquatic Botany 27: 59–78.CrossRefGoogle Scholar
  37. Gerbal, M. & M. Verlaque, 1995. Macrophytobenthos de substrat meuble de l’étang de Thau (France, Méditerranée) et facteurs environnementaux associés. Oceanologica Acta 18: 557–571.Google Scholar
  38. Glibert, P. M., D. C. Hinkle, B. Sturgis & R. V. Jesien, 2014. Eutrophication of a Maryland/Virginia coastal lagoon: a tipping point, ecosystem changes, and potential causes. Estuaries and Coasts 37: 128–146.CrossRefGoogle Scholar
  39. Graffelman, J. & R. Tuft, 2004. Site scores and conditional biplots in canonical correspondence analysis. Environmetrics 15: 67–80.CrossRefGoogle Scholar
  40. Greve, T. M. & T. Binzer, 2004. Which factors regulate seagrass growth and distribution? In Borum, J et al. (ed.), European Seagrasses: An Introduction to Monitoring and Management.Google Scholar
  41. Guerlorget, O. & J. P. Perthuisot, 1992. Paralic ecosystems. Biological organization and functioning. Vie Milieu 42: 215–251.Google Scholar
  42. Guiry, M. D. & G. M. Guiry, 2016. AlgaeBase. World-wide electronic publication. National University of Ireland, Galway [available on internet at http://www.algaebase.org].
  43. Häder, D. & F. L. Figueroa, 1997. Photoecophysiology of marine macroalgae. Photochemistry and Photobiology 66: 1–14.CrossRefGoogle Scholar
  44. Hansen, J. W., J. W. Udy, C. J. Perry, W. C. Dennison & B. A. Lomstein, 2000. Effect of the seagrass Zostera capricorni on sediment microbial processes. Marine Ecology Progress Series 199: 83–96.CrossRefGoogle Scholar
  45. Hartvig, C., N. Kjell Magnus & F. Stein, 2009. Macrophytes as habitat for fauna. Marine Ecology Progress Series 396: 221–233.CrossRefGoogle Scholar
  46. Haynes, D., P. Ralph, J. Prange & B. Dennison, 2000. The impact of the herbicide diuron on photosynthesis in three species of tropical seagrass. Marine Pollution Bulletin 41: 288–293.CrossRefGoogle Scholar
  47. Hurd, C. L., P. J. Harrison, K. Bischof & C. S. Lobban, 2014. Seaweed Ecology and Physiology. Cambridge University Press, Cambridge, NY.CrossRefGoogle Scholar
  48. Ifremer, 2007. Réseau de Suivi Lagunaire du Languedoc-Roussillon: Bilan des résultats 2006.Google Scholar
  49. Ifremer, Cepralmar, Agence de l’Eau RMC, & Région Languedoc-Roussillon, 2011. Guide de reconnaissance et de suivi des macrophytes des lagunes du Languedoc-Roussillon.Google Scholar
  50. Kennish, M. J. & H. W. Paerl, 2010. Coastal Lagoons: Critical Habitats of Environmental Change. CRC Press, Boca Raton.CrossRefGoogle Scholar
  51. Kinne, O., 1971. Salinity: animals-invertebrates. Marine Ecology 1: 821–995.Google Scholar
  52. Kjerfve, B., 1994. Chapter 1. Coastal lagoons. In Kjerfve, B. (ed.), Elsevier Oceanography Series. Elsevier, Amsterdam: 1–8.Google Scholar
  53. Larkum, A., R. J. Orth & C. M. Duarte, 2006. Seagrasses: Biology, Ecology and Conservation. Springer, The Netherland.Google Scholar
  54. Lawson, S. E., P. L. Wiberg, K. J. McGlathery & D. C. Fugate, 2007. Wind-driven sediment suspension controls light availability in a shallow coastal lagoon. Estuaries and Coasts 30: 102–112.CrossRefGoogle Scholar
  55. Leruste, A., N. Malet, D. Munaron, V. Derolez, E. Hatey, Y. Collos, R. De Wit & B. Bec, 2016. First steps of ecological restoration in Mediterranean lagoons: shifts in phytoplankton communities. Estuarine, Coastal and Shelf Science 180: 190–203.CrossRefGoogle Scholar
  56. Levin, L. A., D. F. Boesch, A. Covich, C. Dahm, C. Erséus, K. C. Ewel, R. T. Kneib, A. Moldenke, M. A. Palmer, P. Snelgrove, D. Strayer & J. M. Weslawski, 2001. The function of marine critical transition zones and the importance of sediment biodiversity. Ecosystems 4: 430–451.CrossRefGoogle Scholar
  57. Lirman, D., G. Deangelo, J. Serafy, A. Hazra, D. S. Hazra, J. Herlan, J. Luo, S. Bellmund, J. Wang & R. Clausing, 2008. Seasonal changes in the abundance and distribution of submerged aquatic vegetation in a highly managed coastal lagoon. Hydrobiologia 596: 105.CrossRefGoogle Scholar
  58. Littler, M. M. & D. S. Littler, 1984. Relationships between macroalgal functional form groups and substrata stability in a subtropical rocky-intertidal system. Journal of Experimental Marine Biology and Ecology 74: 13–34.CrossRefGoogle Scholar
  59. McCune, B., 1997. Influence of noisy environmental data on canonical correspondence analysis. Ecology 78: 2617–2623.CrossRefGoogle Scholar
  60. McGlathery, K. J., K. Sundbck & 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.CrossRefGoogle Scholar
  61. Menéndez, M. & F. A. Comín, 1989. Seasonal patterns of biomass variation of Ruppia cirrhosa (Petagna) Grande and Potamogeton pectinatus L. in a coastal lagoon. Scientia Marina 53: 633–638.Google Scholar
  62. Menéndez, M. & F. A. Comín, 2000. Spring and summer proliferation of floating macroalgae in a Mediterranean coastal lagoon (Tancada Lagoon, Ebro Delta, NE Spain). Estuarine, Coastal and Shelf Science 51: 215–226.CrossRefGoogle Scholar
  63. Menéndez, M., O. Hernandez & F. A. Comin, 2002. Spatial distribution and ecophysiological characteristics of macrophytes in a Mediterranean coastal lagoon. Estuarine, Coastal and Shelf Science 55: 403–413.CrossRefGoogle Scholar
  64. Millet, B., C. Robert, P. Grillas, C. Coughlan & D. Banas, 2010. Numerical modelling of vertical suspended solids concentrations and irradiance in a turbid shallow system (Vaccares, Se France). Hydrobiologia 638: 161–179.CrossRefGoogle Scholar
  65. Mouronval, J.-B. & S. Baudouin, 2010. Plantes aquatiques de Camargue et de Crau. Paris.Google Scholar
  66. Munaron, D., N. Tapie, H. Budzinski, B. Andral & J.-L. Gonzalez, 2012. Pharmaceuticals, alkylphenols and pesticides in Mediterranean coastal waters: results from a pilot survey using passive samplers. Estuarine, Coastal and Shelf Science 114: 82–92.CrossRefGoogle Scholar
  67. Neveux, J. & F. Lantoine, 1993. Spectrofluorometric assay of chlorophylls and phaeopigments using the least squares approximation technique. Deep Sea Research Part I: Oceanographic Research Papers 40: 1747–1765.CrossRefGoogle Scholar
  68. Obrador, B. & J. L. Pretus, 2008. Light regime and components of turbidity in a Mediterranean coastal lagoon. Estuarine, Coastal and Shelf Science 77: 123–133.CrossRefGoogle Scholar
  69. Obrador, B. & J. L. Pretus, 2010. Spatiotemporal dynamics of submerged macrophytes in a Mediterranean coastal lagoon. Estuarine, Coastal and Shelf Science 87: 145–155.CrossRefGoogle Scholar
  70. Oksanen, J., 2016. Design decisions and implementation details in vegan. Vignette of the package vegan. R package version 2.4-1.Google Scholar
  71. Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, R. B. O’Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens, & H. Wagner, 2016. Vegan: Community Ecology Package. R package version 2.4-1.Google Scholar
  72. 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.CrossRefGoogle Scholar
  73. Orfanidis, S., K. Dencheva, K. Nakou, S. Tsioli, V. Papathanasiou & I. Rosati, 2014. Benthic macrophyte metrics as bioindicators of water quality: towards overcoming typological boundaries and methodological tradition in Mediterranean and Black Seas. Hydrobiologia 740: 61–78.CrossRefGoogle Scholar
  74. Orth, R. J., T. J. B. Carruthers, W. C. Dennison, C. M. Duarte, J. W. Fourqurean, K. L. 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.CrossRefGoogle Scholar
  75. Palmer, M. W., 1993. Putting things in even better order: the advantages of canonical correspondence analysis. Ecology 74: 2215–2230.CrossRefGoogle Scholar
  76. Pérez-Ruzafa, A., C. Marcos & I. M. Pérez-Ruzafa, 2011. Mediterranean coastal lagoons in an ecosystem and aquatic resources management context. Physics and Chemistry of the Earth, Parts A/B/C 36: 160–166.CrossRefGoogle Scholar
  77. Plus, M., A. Chapelle, P. Lazure, I. Auby, G. Levavasseur, M. Verlaque, T. Belsher, J.-M. Deslous-Paoli, J.-M.Zaldívar & C. N. Murray, 2003. Modelling of oxygen and nitrogen cycling as a function of macrophyte community in the Thau lagoon. Continental Shelf Research 23: 1877–1898.CrossRefGoogle Scholar
  78. Prado, P., N. Caiola & C. Ibáñez, 2013. Spatio-temporal patterns of submerged macrophytes in three hydrologically altered Mediterranean coastal lagoons. Estuaries and coasts 36: 414–429.CrossRefGoogle Scholar
  79. R development team, 2016. R: a language and environment for statistica computing. R foundation for Statistical Computing. Vienna, Austria, http://www.R-project.org.
  80. Remane, A., 1934. Die Brackwasserfauna. Verhandlungen Der Deutschen Zoologischen Gesellschaft 36: 34–74.Google Scholar
  81. Sanchez, A. & P. Grillas, 2012. Indicateur macrophytes dans les lagunes oligo-halines et mésohalines. Université Aix-Marseille, Tour du valat: 71.Google Scholar
  82. Sanchez, A. & P. Grillas, 2013. Mise au point d’un indicateur DCE compatible pour les lagunes oligo et mésohalines. Tour du Valat: 66.Google Scholar
  83. Sand-Jensen K., 1980. Balancen mellem autotrofe komponenter i tempererede soer med forskellig neringsbelastnig. Vatten 2: 80–89Google Scholar
  84. Sand-Jensen, K. & J. Borum, 1991. Interactions among phytoplankton, periphyton, and macrophytes in temperate freshwaters and estuaries. Aquatic Botany 41: 137–175.CrossRefGoogle Scholar
  85. Sargian, P., B. Andral, & V. Derolez, 2013. Réseaux de surveillance DCE-Campagne 2012-District “Rhône et côtiers méditerranéens”. Ifremer.Google Scholar
  86. Scheffer, M., M. R. de Redelijkheid & F. Noppert, 1992. Distribution and dynamics of submerged vegetation in a chain of shallow eutrophic lakes. Aquatic Botany 42: 199–216.CrossRefGoogle Scholar
  87. Scheffer, M., S. H. Hosper, M.-L. Meijer, B. Moss & E. Jeppesen, 1993. Alternative equilibria in shallow lakes. Trends in Ecology & Evolution 8: 275–279.CrossRefGoogle Scholar
  88. Schramm, W., 1999. Factors influencing seaweed responses to eutrophication: some results from EU-project EUMAC. Journal of applied Phycology 11: 69–78.CrossRefGoogle Scholar
  89. Schramm, W. & P. Nienhuis, 1996. Marine Benthic Vegetation: Recent Changes and the Effects of Eutrophication. Springer, NewYork.CrossRefGoogle Scholar
  90. 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.CrossRefPubMedGoogle Scholar
  91. Sfriso, A. & C. Facca, 2007. Distribution and production of macrophytes and phytoplankton in the lagoon of Venice: comparison of actual and past situation. Hydrobiologia 577: 71–85.CrossRefGoogle Scholar
  92. Sfriso, A., C. Facca & P. F. Ghetti, 2009. Validation of the macrophyte quality index (MaQI) set up to assess the ecological status of Italian marine transitional environments. Hydrobiologia 617: 117–141.CrossRefGoogle Scholar
  93. Sfriso, A., B. Pavoni, A. Marcomini & A. A. Orio, 1992. Macroalgae, nutrient cycles, and pollutants in the Lagoon of Venice. Estuaries 15: 517.CrossRefGoogle Scholar
  94. Souchu, P., B. Bec, V. H. Smith, T. Laugier, A. Fiandrino, L. Benau, V. Orsoni, Y. Collos & A. Vaquer, 2010. Patterns in nutrient limitation and chlorophyll a along an anthropogenic eutrophication gradient in French Mediterranean coastal lagoons. Canadian Journal of Fisheries and Aquatic Sciences 67: 743–753.CrossRefGoogle Scholar
  95. Steinhardt, T. & U. Selig, 2011. Influence of salinity and sediment resuspension on macrophyte germination in coastal lakes. Journal of Limnology 70: 11–20.CrossRefGoogle Scholar
  96. Tagliapietra, D. & A. V. Ghirardini, 2006. Notes on coastal lagoon typology in the light of the EU Water Framework Directive: Italy as a case study. Aquatic Conservation: Marine and Freshwater Ecosystems 16: 457–467.CrossRefGoogle Scholar
  97. Teeter, J. W., 1965. Effects of sodium chloride on the sago pondweed. The Journal of Wildlife Management 29: 838–845.CrossRefGoogle Scholar
  98. Teichberg, M., S. E. Fox, Y. S. Olsen, I. Valiela, P. Martinetto, O. Iribarne, E. Y. Muto, M. A. V. Petti, T. N. Corbisier, M. Soto-Jiménez, F. Páez-Osuna, P. Castro, H. Freitas, A. Zitelli, M. Cardinaletti & D. Tagliapietra, 2010. Eutrophication and macroalgal blooms in temperate and tropical coastal waters: nutrient enrichment experiments with Ulva spp. Global Change Biology 16: 2624–2637.PubMedCentralGoogle Scholar
  99. Telesh, I., H. Schubert & S. Skarlato, 2013. Life in the salinity gradient: discovering mechanisms behind a new biodiversity pattern. Estuarine, Coastal and Shelf Science 135: 317–327.CrossRefGoogle Scholar
  100. Ter Braak, C. J. F., 1986. Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67: 1167–1179.CrossRefGoogle Scholar
  101. Ter Braak, C. J. F., 1987. The analysis of vegetation-environment relationships by canonical correspondence analysis. Vegetatio 69: 69–77.CrossRefGoogle Scholar
  102. Ter Braak, C. J. F., 1994. Canonical community ordination. Part I: basic theory and linear methods. Écoscience 1: 127–140.CrossRefGoogle Scholar
  103. Thomaz, S. M. & E. R. da Cunha, 2010. The role of macrophytes in habitat structuring in aquatic ecosystems: methods of measurement, causes and consequences on animal assemblages’ composition and biodiversity. Acta Limnologica Brasiliensia 22: 218–236.CrossRefGoogle Scholar
  104. Van Wijk, R. J., 1988. Ecological studies on Potamogeton pectinatus L. I. General characteristics, biomass production and life cycles under field conditions. Aquatic Botany 31: 211–258.CrossRefGoogle Scholar
  105. Vaquer, A. & P. Heurteaux, 1989. Modifications récentes de la végétation aquatique de l’étang du Vaccarès (Camargue, France) liées aux perturbations anthropiques. Annales de Limnologie 25: 25–38.CrossRefGoogle Scholar
  106. Verhoeven, J. T. A., 1980. The ecology of Ruppia-dominated communities in Western Europe. II. Synecological classification. Structure and dynamics of the macroflora and macrofauna communities. Aquatic Botany 8: 1–85.CrossRefGoogle Scholar
  107. Verlaque, M., 2000. Actualisation de la flore des macrophytes des étangs de Thau (Hérault) et de Salses-Leucate (Aude-Pyrénées-Orientales). In: PNEC “Lagunes Méditerranéennes”, Thème 1, le compartiment “Macrophytes”. GIS Posidonie - IFREMER Report, Marseille.Google Scholar
  108. Verlaque, M., 2001. Checklist of the macroalgae of Thau Lagoon (Hérault, France), a hot spot of marine species introduction in Europe. Oceanologica Acta 24: 29–49.CrossRefGoogle Scholar
  109. Viaroli, P., M. Bartoli, C. Bondavalli, R. R. Christian, G. Giordani & M. Naldi, 1996. Macrophyte communities and their impact on benthic fluxes of oxygen, sulphide and nutrients in shallow eutrophic environments. Hydrobiologia 329: 105–119.CrossRefGoogle Scholar
  110. Viaroli, P., M. Bartoli, G. Giordani, M. Naldi, S. Orfanidis & J. M. Zaldivar, 2008. Community shifts, alternative stable states, biogeochemical controls and feedbacks in eutrophic coastal lagoons: a brief overview. Aquatic Conservation: Marine and Freshwater Ecosystems 18: S105–S117.CrossRefGoogle Scholar
  111. Vincent, C., D. Mouillot, M. Lauret, T. D. Chi, M. Troussellier & C. Aliaume, 2006. Contribution of exotic species, environmental factors and spatial components to the macrophyte assemblages in a Mediterranean lagoon (Thau lagoon, Southern France). Ecological Modelling 193: 119–131.CrossRefGoogle Scholar
  112. Vizzini, S. & A. Mazzola, 2008. The fate of organic matter sources in coastal environments: a comparison of three Mediterranean lagoons. Hydrobiologia 611: 67–79.CrossRefGoogle Scholar
  113. WoRMS Editorial Board, 2016. World Register of Marine Species [available on internet at http://www.marinespecies.org at VLIZ. Accessed 16 Nov 2016. doi:  http://doi.org/10.14284/170.
  114. Zaldívar, J.-M., P. Viaroli, A. Newton, R. De Wit, C. Ibañez, S. Reizopoulou, F. Somma, A. Razinkovas, A. Basset, M. Holmer & N. Murray, 2008. Eutrophication in transitional waters: an overview. Transitional Waters Monographs 2: 1–78.Google Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Ifremer, UMR MARBEC (IRD, Ifremer, Université de Montpellier, CNRS)Sète CedexFrance
  2. 2.Ifremer, Laboratoire Environnement Ressources Languedoc Roussillon (LER LR)Sète CedexFrance
  3. 3.CNRS, UMR MARBEC (IRD, Ifremer, Université de Montpellier, CNRS), Université de MontpellierMontpellier Cedex 5France
  4. 4.IRD, UMR MARBEC, (IRD, Ifremer, Université de Montpellier, CNRS)SèteFrance
  5. 5.Ifremer, Laboratoire d’écologie pélagique (DYNECO-PELAGOS)PlouzanéFrance

Personalised recommendations