Ecophysiological plasticity of shallow and deep populations of the Mediterranean seagrasses Posidonia oceanica and Cymodocea nodosa in response to hypersaline stress

Marine Environmental Research

Volumn 95, Issue , 2014, Pages 39-61

  Sandoval Gil, Jose Miguel ^a,b   Ruiz, Juan Manuel ^a   Marín Guirao, Lázaro ^a   Bernardeau Esteller, Jaime ^a,b   Sánchez Lizaso, Jose Luis ^b  

^a INSTITUTO ESPAÑOL DE OCEANOGRAFÍA   (Spain)

^b UNIVERSITY OF ALICANTE   (Spain)

Author keywords

Cymodocea nodosa; Desalination discharges; Environmental impact; Mediterranean seagrass; Mesocosm; Phenotypic plasticity; Posidonia oceanica; Salinity stress

Indexed keywords

DESALINATION; ENVIRONMENTAL IMPACT; LIGHT; PHYSIOLOGY;

CYMODOCEA NODOSA; MESOCOSMS; PHENOTYPIC PLASTICITY; POSIDONIA OCEANICA; SALINITY STRESS; SEAGRASSES;

PLANTS (BOTANY);

ABSORPTION; DESALINATION; DIVERGENCE; ECOTYPE; EXPERIMENTAL STUDY; INDUSTRIAL WASTE; OSMOREGULATION; PHENOLOGY; PHENOTYPIC PLASTICITY; PHOTOSYNTHESIS; PHYSIOLOGICAL RESPONSE; SALINITY TOLERANCE; SEAGRASS;

AEROBIC METABOLISM; ARTICLE; CARBON BALANCE; CONTROLLED STUDY; CYMODOCEA NODOSA; ECOPHYSIOLOGY; ENVIRONMENTAL EXPOSURE; LONG TERM EXPOSURE; MESOCOSM; NONHUMAN; OSMOREGULATION; PHENOTYPIC PLASTICITY; PHOTOSYNTHESIS; PIGMENTATION; PLANT LEAF; PLANT METABOLISM; POSIDONIA OCEANICA; SALT STRESS; SALT TOLERANCE; SEAGRASS; SPECIES DIFFERENCE; SPECIES DIVERSITY;

MEDITERRANEAN SEA;

CYMODOCEA NODOSA; POSIDONIA OCEANICA;

CYMODOCEA NODOSA; DESALINATION DISCHARGES; ENVIRONMENTAL IMPACT; MEDITERRANEAN SEAGRASS; MESOCOSM; PHENOTYPIC PLASTICITY; POSIDONIA OCEANICA; SALINITY STRESS;

ALISMATIDAE; CARBON; ENVIRONMENT; MEDITERRANEAN SEA; PHOTOSYNTHESIS; PIGMENTS, BIOLOGICAL; SALINITY; SALT-TOLERANCE; SPECIES SPECIFICITY; STRESS, PHYSIOLOGICAL;

EID: 84893803500     PISSN: 01411136     EISSN: 18790291     Source Type: Journal    
DOI: 10.1016/j.marenvres.2013.12.011     Document Type: Article

References (126)

1. Atkin O.K., Macherel D. The crucial role of plant mitochondria in orchestrating drought tolerance. Ann. Bot. 2009, 103:581-597.
2. Baquedano F.J., Valladares F., Castillo F.J. Phenotypic plasticity blurs ecotypic divergence in the response of Quercus coccifera and Pinus halepensis to water stress. Eur. J. Forest Restor. 2008, 127:495-506.
3. Bates L. Rapid determination of free proline for water-stress studies. Plant Soil 1973, 39:205-207.
4. Beer S., Eshel A., Waisel Y. Carbon metabolism in seagrasses III. Activities of carbon-fixing enzymes in relation to internal salt concentrations. J. Exp. Bot. 1980, 31:1027-1033.
5. 2 incorporation. J. Exp. Bot. 1980, 31:1019-1026.
6. Biebl R., McRoy C.P. Plasmatic resistance and rate of respiration and photosynthesis of Zostera marina at different salinities and temperatures. Mar. Biol. 1971, 8:48-56.
7. Bisson M.A., Kirst G.O. Osmotic acclimation and turgor pressure regulation in algae. Naturwissenschaften 1995, 82:461-471.
8. Boudouresque C.F., Bernard G., Pergent G., Shili A., Verlaque M. Regression of Mediterranean seagrasses caused by natural processes and anthropogenic disturbances and stress: a critical review. Bot. Mar. 2009, 52:395-418.
9. Boyer J.S. Measuring the Water Status of Plants and Soils 1995, Academic Press, San Diego, United States.
10. Brock M.A. Accumulation of proline in a submerged aquatic halophyte Ruppia maritima L. Oecologia 1981, 51:217-219.
11. Burkholder J.M., Tomasko D.A., Touchette B.W. Seagrasses and eutrophication. J. Exp. Mar. Biol. Ecol. 2007, 350:46-72.
12. Cancemi G., Buia M.C., Mazzella L. Structure and growth dynamics of Cymodocea nodosa meadow. Sci. Mar. 2002, 66:365-373.
13. Cayabyab N.M., Enríquez S. Leaf photoacclimatory responses of the tropical seagrass Thalassia testudinum under mesocosm conditions: a mechanistic scaling-up study. New Phytol. 2007, 176:108-123.
14. Collier C.J., Lavery P.S., Ralph P.J., Masini R.J. Physiological characteristics of the seagrass Posidonia sinuosa along a depth-related gradient of light availability. Mar. Ecol. Prog. Ser. 2008, 353:65-79.
15. Dalla Via J., Sturmbauer C., Schönweger G., Sötz E., Mathekowitsch S., Stifter M., Rieger R. Light gradients and meadow structure in Posidonia oceanica: ecomorphological and functional correlates. Mar. Ecol. Prog. Ser. 1998, 163:267-278.
16. Demmig-Adams B., Adams W.W. The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci. 1996, 1:21-26.
17. Dennison W.C. Effects of light on seagrass photosynthesis, growth and depth distribution. Aquat. Bot. 1987, 27:15-26.
18. Dennison W.C. Chlorophyll content. Seagrass Research Methods 1990, 83-86. UNESCO, Paris, France. R.C. Phillips, C.P. McRoy (Eds.).
19. DeWitt T.J., Sih A., Wilson D.S. Costs and limits of phenotypic plasticity. Tree 1998, 13:77-81.
20. DeWitt T.J., Scheiner S.M. Phenotypic Plasticity: Functional and Conceptual Approaches 2004, Oxford University Press.
21. Drew E.A. Carbohydrate and inositol metabolism in seagrass Cymodocea nodosa. New Phytol. 1978, 81:249-264.
22. Drew E.A. Factors affecting photosynthesis and its seasonal variation in the seagrass Cymodocea nodosa (Ucria) Aschers, and Posidonia oceanica (L.) Delile in the Mediterranean. J. Exp. Mar. Biol. Ecol. 1978, 31:173-194.
23. Duarte C. Seagrass depth limits. Aquat. Bot. 1991, 40:363-377.
24. Dudley S.A. The functional ecology of phenotypic plasticity in plants. Phenotypic Plasticity. Functional and Conceptual Approaches 2004, 151-172. Oxford University Press, Oxford, UK. T.J. DeWitt, S.M. Scheiner (Eds.).
25. Dunton K. Photosynthetic production and biomass of the subtropical seagrass Halodule wrightii along an estuarine gradient. Estuaries 1996, 19:436-447.
26. Durako M.J., Kunzelman J.I. Photosynthetic characteristics of Thalassia testudinum measured in situ by pulse-amplitude modulated (PAM) fluorometry: methodological and scale-based considerations. Aquat. Bot. 2002, 73:173-185.
27. Enríquez S., Agustí S., Duarte C.M. Light absorption by seagrass Posidonia oceanica leaves. Mar. Ecol. Prog. Ser. 1992, 86:201-204.
28. Enríquez S., Merino M., Iglesias-Prieto R. Variations in the photosynthetic performance along the leaves of the tropical seagrass Thalassia testudinum. Mar. Biol. 2002, 140:891-900.
29. Enríquez S., Sand-Jensen K. Variation in light absorption properties of Mentha aquatica L. as a function of leaf form: implications for plant growth. Int. J. Plant Sci. 2003, 164:125-136.
30. Enríquez S. Light absorption efficiency and the package effect in the leaves of the seagrass Thalassia testudinum. Mar. Ecol. Prog. Ser. 2005, 289:141-150.
31. Falkowski P., Raven J. Aquatic Photosynthesis 2007, Princeton University Press, Princeton. second ed.
32. Farooq M., Wahid A., Kobayashi N., Fujita D., Basra S.M.A. Plant drought stress: effects, mechanisms and management. Agron. Sust. Develop. 2009, 29:185-212.
33. Fernández-Torquemada Y., Sánchez-Lizaso J.L. Effects of salinity on leaf growth and survival of the Mediterranean seagrass Posidonia oceanica (L.) Delile. J. Exp. Mar. Biol. Ecol. 2005, 320:57-63.
34. Fernández-Torquemada Y., Sánchez-Lizaso J.L., González-Correa J.M. Preliminary results of the monitoring of the brine discharge produced by the SWRO desalination plant of Alicante (SE Spain). Desalination 2005, 182:395-402.
35. Fernández-Torquemada Y., Durako M.J., Sánchez-Lizaso J.L. Effects of salinity and possible interactions with temperature and pH on growth and photosynthesis of Halophila johnsonii Eiseman. Mar. Biol. 2005, 148:251-260.
36. Fernández-Torquemada Y., Sánchez-Lizaso J.L. Effects of salinity on growth and survival of Cymodocea nodosa (Ucria) Ascherson and Zostera noltii Hornemann. Biol. Mar. Mediter. 2006, 13:46-47.
37. Fernández-Torquemada Y., Sánchez-Lizaso J.L. Responses of two Mediterranean seagrass to experimental changes in salinity. Hydrobiologia 2011, 669:21-33.
38. García-Sánchez M., Korbee N., Pérez-Ruzafa I.M., Marcos C., Domínguez B., Figueroa F.L., Pérez-Ruzafa A. 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). Mar. Environ. Res. 2012, 79:37-47.
39. Gacia E., Invers O., Manzanera M., Ballesteros E., Romero J. Impact of the brine from a desalination plant on a shallow seagrass (Posidonia oceanica) meadow. Estuar. Coast. Shelf Sci. 2007, 72:579-590.
40. Ghalambor C.K., McKay J.K., Carroll S.P., Reznick D.N. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 2007, 21:394-407.
41. Hemminga M.A., Mateo M.A. Stable carbon isotopes in seagrasses: variability in ratios and use in ecological studies. Mar. Ecol. Prog. Ser. 1996, 140:285-298.
42. Herbert D.A., Perry W.B., Cosby B.J., Fourqurean J.W. Projected reorganization of Florida Bay seagrass communities in response to the increased freshwater inflow of Everglades restoration. Estuar. Coasts 2011, 34(5):973-992. 10.1007/s12237-011-9388-4.
43. Hofrichter R. El Mar Mediterráneo. Fauna, Flora, Ecología. I Parte General 2004, Ediciones Omega, Barcelona, España.
44. Invers O., Kraemer G.P., Pérez M., Romero J. Effects of nitrogen addition on nitrogen metabolism and carbon reserves in the temperate seagrass Posidonia oceanica. J. Exp. Mar. Biol. Ecol. 2004, 303:97-114.
45. Jenerette G.D., Lee J., Waller D.W., Carlson R.D. Multivariate analysis of the ecoregion delineation for aquatic systems. Environ. Manage. 2002, 29:67-75.
46. 2 by marine and terrestrial plants. Plant Physiol. 1962, 37:446-449.
47. Kahn A.E., Durako M.J. Thalassia testudinum seedling responses to changes in salinity and nitrogen levels. J. Exp. Mar. Biol. Ecol. 2006, 335:1-12.
48. Kamermans P., Hemminga M.A., De Jong D.J. Significance of salinity and silicon levels for growth of a formerly estuarine eelgrass (Zostera marina) population (Lake Grevelin, The Netherlands). Mar. Biol. 1999, 133:527-539.
49. Kerr E.A., Strother S. Effects of irradiance, temperature and salinity on photosynthesis of Zostera muelleri. Aquat. Bot. 1985, 23:177-183.
50. Kirk J.T.O. Light and Photosynthesis in Aquatic Ecosystems 1994, University of Cambridge Press, Cambridge, UK. second ed.
51. Kirst G.O. Salinity tolerance of eukaryotic marine algae. Annu. Rev. Plant Physiol. Mol. Biol. 1989, 40:21-53.
52. Koch E.W., Dawes C.J. Ecotypic differentiation in populations of Ruppia maritima L. germinated from seeds and cultured under algae-free laboratory conditions. J. Exp. Mar. Biol. Ecol. 1991, 152:145-159.
53. Koch M.S., Schopmeyer S.A., Kyhn-Hansen C., Madden C.J., Peters J.S. Tropical seagrass species tolerance to hypersalinity stress. Aquat. Bot. 2007, 86:14-24.
54. Kramer P.J., Boyer J.S. Water Relations of Plants and Soils 1995, Academic Press, San Diego, United States.
55. Larkum A.W.D., Drew E.A., Ralph P.J. Photosynthesis and metabolisms in seagrasses at the cellular level. Seagrasses: Biology, Ecology and Conservation 2006, 323-345. Springer, Dordrecht, The Netherlands. A.W.D. Larkum, R.J. Orth, C.M. Duarte (Eds.).
56. Levitt J. Responses of Plants to Environmental Stresses 1980, vol. 1. Academia Press, New York.
57. Lichtenthaler H.K., Wellburn A.R. Determination of total carotenoids and chlorophyll a and b of leaf extracts in different solvents. Biochem. Soc. Trans. 1983, 603:591-592.
58. Lichtenthaler H.K. Vegetation stress: and introduction to the stress concept in plants. J. Plant Physiol. 1996, 148:4-14.
59. Marbá N., Cebrián J., Enríquez S., Duarte C.M. Growth patterns of Western Mediterranean seagrasses: species-specific responses to seasonal forcing. Mar. Ecol. Prog. Ser. 1996, 133:203-215.
60. Marbà N., Duarte C.M. Rhizome elongation and seagrass clonal growth. Mar. Ecol. Prog. Ser. 1998, 174:269-280.
61. Marbá N., Duarte C.M. Growth and sediment space occupation by seagrass Cymodocea nodosa roots. Mar. Ecol. Prog. Ser. 2001, 224:291-298.
62. Marbá N., Hemminga M.A., Mateo M.A., Duarte C.M., Mass Y., Terrados J., Gacia E. Carbon and nutrient translocation between seagrass ramets. Mar. Ecol. Prog. Ser. 2002, 226:287-300.
63. Margalef R. Western Meditarranean 1985, Pergamon Press, London, UK.
64. Marín-Guirao L., Marín-Atucha A., Lloret-Barba J., Martínez-López Emma, García-Fernández A.J. Effects of mining wastes on a seagrass ecosystem: metal accumulation and bioavailability, seagrass dynamics and associated community structure. Mar. Environ. Res. 2005, 60:317-337.
65. Marín-Guirao L., Sandoval-Gil J.M., Ruiz J.M., Sánchez-Lizaso J.L. Photosynthesis, growth and survival of the Mediterranean seagrass Posidonia oceanica in response to simulated salinity increases in a laboratory mesocosm system. Estuar. Coast. Shelf Sci. 2011, 92:286-296.
66. Marín-Guirao L., Sandoval-Gil J.M., Bernardeau-Esteller J., Ruiz J.M., Sánchez-Lizaso J.L. Responses of the Mediterranean seagrass Posidonia oceanica to hypersaline stress duration and recovery. Mar. Environ. Res. 2013, 84:60-75.
67. Marín-Guirao L., Ruiz J.M., Sandoval-Gil J.M., Bernardeau-Esteller J., Stinco C.M., Meléndez-Martínez A.J. Xanthophyll cycle-related photoprotective mechanism in the Mediterranean seagrasses Posidonia oceanica and Cymodocea nodosa under normal and stressful hypersaline conditions. Aquat. Bot. 2013, 109:14-24.
68. Mercado J.M., Niell F.X., Silva J., Santos R. Use of light and inorganic carbon acquisition by two morphotypes of Zostera noltii Hornem. J. Exp. Mar. Biol. Ecol. 2003, 297:71-84.
69. Migliaccio M., De Martino F., Silverstre F., Procaccini G. Meadow scale genetic structure in Posidonia oceanica. Mar. Ecol. Prog. Ser. 2005, 304:55-65.
70. Munns R. Comparative physiology of salt and water stress. Plant Cell Environ. 2002, 25:239-250.
71. Murphy L.R., Kinsey S.T., Durako M.J. Physiological effects of short-term salinity changes on Ruppia maritima. Aquat. Bot. 2003, 75:293-309.
72. Nicotra A.B., Atkin O.K., Bonser S.P., Davidson A.M., Finnegan E.J., Mathesius U., Poot P., Purugganan M.D., Richards C.L., Valladares F., van Kleunen M. Plant phenotypic plasticity in a changing climate. Trends Plant Sci. 2010, 15:684-692.
73. Niyogi K.K. Safety valves for photosynthesis. Curr. Opin. Plant Biol. 2000, 3:455-460.
74. Nobel P.S. Physicochemical and Environmental Plant Physiology 2009, Academic Press, San Diego, USA. fourth ed.
75. Ogata E., Matsui T. Photosynthesis in several marine plants of Japan as affected by salinity, drying and pH, with attention to their growth habitat. Bot. Mar. 1964, 8:199-217.
76. Ogata E., Takada H. Studies on the relationship between the respiration and the changes in salinity in some marine plants in Japan. J. Shimonseki Univ. Fish. 1968, 16:67-88.
77. Olesen B., Enríquez S., Duarte C., Sand-Jensen K. Depth-acclimation of photosynthesis, morphology and demography of Posidonia oceanica and Cymodocea nodosa in the Spanish Mediterranean Sea. Mar. Ecol. Prog. Ser. 2002, 236:89-97.
78. Olivé I., García-Sánchez M.P., Brun F.G., Vergara J.J., Pérez-Llorens J.L. Interactions of light and organic matter under contrasting resource simulated environments: the importance of clonal traits in the seagrass Zostera noltii. Hydrobiologia 2009, 629:199-208.
79. Orth R.J., Carruthers T.J.B., Dennison W.C., Duarte C.M., Fourqurean J.W., Heck K.L., Hughes A.R., Kendrick G.A., Kenworthy W.J., Olyarnik S., Short F.T., Waycott M., Williams S. A global crisis for seagrass ecosystem. Bioscience 2006, 56:987-996.
80. Pagés J.F., Pérez M., Romero J. Sensitivity of the seagrass Cymodocea nodosa to hypersaline conditions: a microcosm approach. J. Exp. Mar. Biol. Ecol. 2012, 386:34-38.
81. Parida A.K., Das A.B. Salt tolerance and salinity effects on plants: a review. Ecotoxicol. Environ. Safety 2005, 60:324-349.
82. Peralta G., Pérez-Lloréns J.L., Hernández I., Brun F., Vergara J.J., Bartual A., Gálvez J.A., García C.M. Morphological and physiological differences between two morphotypes of Zostera noltii Hornem. from the south-western Iberian Peninsula. Helgoland Mar. Res. 2000, 54:80-86.
83. Pérez M., Romero J. Growth dynamics, production, and nutrient status of the seagrass Cymodocea nodosa in a Mediterranean semi-estuarine environment. PSZN I: Mar. Ecol. 1994, 15:51-64.
84. Pergent G., Djellouli A., Hamza A.A., Ettayeb K.S., El Mansouri A.A., Talha F.M., Hamza M.A., Pergent-Martini C., Platini F. Characterization of the benthic vegetation in the Farwà Lagoon (Libya). J. Coast. Conserv. 2002, 8:119-126.
85. Pirc H. Growth dynamics in Posidonia oceanica (L.) Delile. PSZNI: Mar. Ecol. 1985, 6:141-165.
86. Pirc H., Wollenweber B. Seasonal-changes in nitrogen, free amino-acids, and C/N Ratio in Mediterranean seagrasses. PSZNI: Mar. Ecol. 1988, 9:167-179.
87. Puignaire F.I., Valladares F. Functional Plant Ecology. Taylor & Francis Group 2007, CRC Press, Boca Raton, USA, 724 pp.
88. Pulich W.M. Variations in leaf soluble amino acids and ammonium content in subtropical seagrasses related to salinity stress. Plant Physiol. 1986, 80:283-286.
89. Ralph P.J. Photosynthetic responses of Halophila ovalis (R. Br.) Hook. f. to osmotic stress. J. Exp. Mar. Biol. Ecol. 1998, 227:203-220.
90. Ralph P.J. Photosynthetic response of Halophila ovalis (R. Br.) Hook. f. to combined environmental stress. Aquat. Bot. 1999, 65:83-96.
91. Ralph P.J., Polk S.M., Moore K.A., Orth R.J., Smith W.O.J. Operation of the xanthophyll cycle in the seagrass Zostera marina in response to variable irradiance. J. Exp. Mar. Biol. Ecol. 2002, 271:189-207.
92. Ralph P.J., Durako M.J., Enríquez S., Collier C.J., Doblin M.A. Impact of light limitation on seagrasses. J. Exp. Mar. Biol. Ecol. 2007, 350:176-193.
93. Raniello R., Lorenti M., Brunet C., Buia M.C. Photosynthetic plasticity of and invasive variety of Caulerpa racemosa in a coastal Mediterranean area: light harvesting capacity and seasonal acclimation. Mar. Ecol. Prog. Ser. 2004, 271:113-120.
94. Rudnick D.T., Ortner P.B., Browder J.A., Davis S.M. A conceptual ecological model of Florida Bay. Wetlands 2005, 25:870-883.
95. Ruiz J.M., Pérez M., Romero J. Effects of fish farm loadings on seagrass (Posidonia oceanica) distribution, growth and photosynthesis. Mar. Pollut. Bull. 2001, 42:749-760.
96. Ruiz J.M., Romero J. Effects of disturbances caused by coastal constructions on spatial structure, growth dynamics and photosynthesis of the seagrass Posidonia oceanica. Mar. Pollut. Bull. 2003, 46:1523-1533.
97. Ruiz J.M., Marín-Guirao L., Sandoval-Gil J.M. Responses of the Mediterranean seagrass Posidonia oceanica to in situ simulated salinity increase. Bot. Mar. 2009, 52:459-470.
98. Sánchez-Lizaso J.L., Romero J., Ruiz J.M., Gacia E., Buceta J.L., Invers O., Fernández-Torquemada Y., Mas J., Ruiz-Mateo A., Manzanera M. Salinity tolerance of Mediterranean seagrass Posidonia oceanica: recommendations to minimize the impact of brine discharges from desalination plants. Desalination 2008, 221:602-607.
99. Sandoval-Gil J.M. Ecophysiological Responses of Mediterranean Seagrasses (Posidonia oceanica and Cymodocea nodosa) under Hypersaline Stress Conditions 2012, PhD thesis, University of Alicante, Spain.
100. Sandoval-Gil J.M., Marín-Guirao L., Ruiz J.M. Tolerance of Mediterranean seagrasses (Posidonia oceanica and Cymodocea nodosa) to hypersaline stress: water relations and osmolyte concentrations. Mar. Biol. 2012, 159:1129-1141.
101. Sandoval-Gil J.M., Marín-Guirao L., Ruiz J.M. Effect of salinity increase on photosynthesis, growth and survival of the seagrass Cymodocea nodosa. Estuar. Coast. Shelf Sci. 2012, 115:260-271.
102. Santamaría L., Figuerola J., Pilón J.J., Mjelde M., Green A.J., De Boer T., King R.A., Gornall R.J. Plant performance across latitude: the role of plasticity and local adaptation in an aquatic plant. Ecology 2003, 84:2454-2461.
103. Schreiber U. Pulse-Amplitude-Modulation (PAM) fluorometry and saturation pulse method: an overview. Chlorophyll a Fluorescence: A Signature of Photosynthesis 2004, 279-319. Springer, Dordrecht, The Netherlands. G.C. Papageorgiou, Govindjee (Eds.).
104. Shibata K. Spectrophotometry of translucence biological materials-opal glass transmission method. Methods Biochem. Anal. 1959, 7:77-109.
105. ter Braak C.J.F. Ordination. Data Analysis in Community and Landscape Ecology 1995, 91-173. Cambridge University Press, Cambridge, UK. R.H.G. Jongman, C.J.F. ter Braak, O.F.R. van Tongeren (Eds.).
106. ter Braak C.J.F., Šmilauer P. CANOCO Reference Manual and CanoDraw for Windows User's Guide: Software for Canonical Community Ordination, Version 4.5 2002, Microcomputer Power, Ithaca, New York, USA.
107. Terrados J., Ros J. Production dynamics in a macrophyte dominated ecosystem: the Mar Menor coastal lagoon (SE Spain). Oecol. Aquat. 1991, 10:255-270.
108. Tomasello A., Di Maida G., Calvo S., Pirrota M., Borra M., Procaccini G. Seagrass meadow at the extreme of environmental tolerance: the case of Posidonia oceanica in a semi-enclosed coastal lagoon. Mar. Ecol. 2009, 30:288-300.
109. Touchette B.W. Seagrass-salinity interactions: physiological mechanisms used by submersed marine angiosperms for a life at sea. J. Exp. Mar. Biol. Ecol. 2007, 350:194-215.
110. Touchette B.W., Burkholder J.M. Carbon and nitrogen metabolism in the seagrass, Zostera marina L.: environmental control of enzymes involved in carbon allocation and nitrogen assimilation. J. Exp. Mar. Biol. Ecol. 2007, 350:216-233.
111. Trevathan S.M., Kahn A., Ross C. Effects of short-term hypersalinity exposure on the susceptibility to wasting disease in the subtropical seagrass Thalassia testudinum. Plant Physiol. Biochem. 2011, 49:1051-1058.
112. Tyerman S.D. Stationary volumetric elastic modulus and osmotic pressure of the leaf cells of Halophila ovalis, Zostera capricorni, and Posidonia australis. Plant Physiol. 1982, 69:957-965.
113. Tyerman S.D., Hatcher A.I., West R.J., Larkum A.W.D. Posidonia australis growing in altered salinities: leaf growth, regulation of turgor and the development of osmotic gradients. Aust. J. Plant Physiol. 1984, 11:35-47.
114. Tyerman S.D. Solute and water relations of seagrasses. Biology of Seagrasses: A Treatise on the Biology of Seagrasses with Special Reference to the Australian Region 1989, 723-759. Elsevier, Amsterdam, The Netherlands. A.W.D. Larkum, A.J. Mc Comb, S.A. Sheperd (Eds.).
115. Valladares F., Sánchez D., Zavala M.A. Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J. Ecol. 2006, 94:1103-1116.
116. Valladares F., Gianoli E., Gómez J.M. Ecological limits to plant phenotypic plasticity. New Phytol. 2007, 176:749-763.
117. Van Katwijk M.M., Schimtz G.H.W., Gasseling A.P., Avesaath P.H. Effects of salinity and nutrient load and their interaction on Zostera marina. Mar. Ecol. Prog. Ser. 1999, 190:155-165.
118. Van Tyenderen P.H. Evolution of generalists and specialists in spatially heterogeneous environments. Evolution 1991, 45:1317-1331.
119. Vasapollo C., Gambi M.C. Spatio-temporal variability in Posidonia oceanica seagrass meadows of the Western Mediterranean: shoot density and plant features. Aquat. Biol. 2012, 16:163-175.
120. Vogelmann T.C. Plant tissue optics. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1993, 44:231-251.
121. Walker D.A. The Use of the Oxygen Electrode and Fluorescence Probes in Simple Measurements of Photosynthesis 1987, Oxygraphics, Sheffield, UK.
122. Winters G., Nelle P., Fricke B., Rauch G., Reusch T.B.H. Effects of a simulated heat wave on photophysiology and gene expression of high- and low-latitude populations of Zostera marina. Mar. Ecol. Prog. Ser. 2011, 435:83-95.
123. Yemm E.W., Willis A.J. The estimation of carbohydrates in plant extracts by anthrone. Biochem. J. 1954, 57:508-514.
124. Zar J.H. Statistical significance of mutation frequencies, and the power of statistical testing using the Poisson-distribution. Biometric. J. 1984, 26:83-88.
125. Zimmermann U. Physics of turgor and osmoregulation. Annu. Rev. Plant Physiol. 1978, 29:121-148.
126. Zoppa M., Gallo L., Zacchello F., Giordano G. Method for the quantification of underivatized amino acids on dry blood spots from newborn screening by HPLC-ESI-MS/MS. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 2006, 831:267-273.