Abstract
This study investigated the major environmental factors structuring, for a year, phytoplankton assemblages in the Sfax saltern (Tunisia): salinity and nutrients. A STATICO analysis based on 11 environmental variables and the abundances of 64 phytoplanktonic species was conducted. STATICO is used to analyze the stable part of the relationships between the environment and species, and then to determine how these relationships change over time. The analysis confirmed that the salinity gradient had a considerable influence on the composition of the phytoplanktonic communities. Bacillariophyceae and Dinophyceae dominated in the least salty ponds, whereas Chlorophyceae and Cyanophyceae dominated in the saltiest ponds, in accordance with the halotolerance level estimated for each species by calculating the optimum salinity and salt tolerance. Nitrogen (N) and phosphorus (P) ions could have a secondary influence on the phytoplankton distribution and its dynamics. Dinophyceae seem to be favored by high ammonium (NH4 +) concentrations, whereas diatoms seem to be favored by high orthophosphates (PO4 3−) and nitrates (NO3 −) values. The Chlorophyceae Dunalliela salina thrived in the saltiest ponds when the NO3 − concentrations increased.
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Abid O, Sellami-Kammoun A, Ayadi H, Drira Z, Bouain A, Aleya L (2008) Biochemical adaptation of phytoplankton to salinity and nutrient gradients in a coastal solar saltern, Tunisia. Estuar Coast Shelf Sci 80:391–400
Andersson A, Haecky R, Hagström A (1994) Effect of temperature and light on the growth of micro- nano- and pico-plankton: impact on algal succession. Mar Biol 120:511–520
Anneville O, Souissi S, Gammeter S, Straile D (2004) Seasonal and inter-annual scales of variability in phytoplankton assemblages: comparison of phytoplankton dynamics in three peri- alpine lakes over a period of 28 years. Freshw Biol 49(1):98–115
Arrigo KR (2005) Marine microorganisms and global nutrient cycles. Nature 437:349–355
Asencio AD (2013) Permanent salt evaporation ponds in a semi-arid Mediterranean region as model systems to study primary production processes under hypersaline conditions. Estuar Coast Shelf Sci 124:24–33
Ayadi H, Toumi N, Abid O, Medhioub K, Hammami M, Sime-Ngando T, Amblard C, Sargos D (2002) Étude qualitative et quantitative des peuplements phyto- et zooplanctoniques dans les bassins de la saline de Sfax. Tunis Rev Sci Eau 15(1):123–135
Ayadi H, Abid O, Elloumi J, Bouaïn A, Sime-Ngando T (2004) Structure of the phytoplankton communities in two lagoons of different salinity in the Sfax saltern (Tunisia). J Plankton Res 26:669–679
Bazzuri ME, Gabellone N, Solaril L (2010) Seasonal variation in the phytoplankton of a saline lowland river (Buenos Aires, Argentina) throughout an intensive sampling period. River Res Appl 26:766–778
Britton RH, Johnson AR (1987) An ecological account of a Mediterranean salina: the Salin de Giraud, Camargue (S. France). Biol Conserv 42:185–230
Carassou L, Ponton D (2007) Spatio-temporal structure of pelagic larval and juvenile fish assemblages in coastal areas of New Caledonia, southwest Pacific. Mar Biol 150:697–711
Chatchawan T, Peerapornpisal Y, Komárek J (2011) Diversity of cyanobacteria in man-made solar saltern, Petchaburi Province, Thailand—a pilot study. Fottea 11:203–214
Chen H, Jiang JG (2009) Osmotic responses of Dunaliella to the changes of salinity. J Cell Physiol 219:251–258
Chen GQ, Jiang Y, Chen F (2008) Salt-induced alterations in lipid composition of diatom Nitzshia laevis (Bacillariophyceae) under heterotrophic culture condition. J Phycol 44:1309–1314
Chrétiennot-Dinet MJ (1990) Atlas du phytoplancton marin volume 3: Chlororachinophycées, chlorophycées, chrysophycées, cryptophycées, euglénophycées, eustigmatophycées, prasinophycées, prymnésiophycées, rhodophycées, tribophycées. Éditions du centre national de la recherche scientifique, Paris
Collos Y, Gagne C, Laabir M, Vaquer A, Cecchi P, Souchu P (2004) Nitrogenous nutrition of Alexandrium catenella (Dinophyceae) in cultures and in Thau lagoon, Southern France. J Phycol 40:96–103
Collos Y, Jauzein C, Ratmaya W, Souchu P, Abadie E, Vaquer A (2014) Comparing diatom and Alexandrium catenella/tamarense blooms in Thau lagoon: importance of dissolved organic nitrogen in seasonally N-limited systems. Harmful Algae 37:84–91
DasSarma S, Arora P (2001) Halophiles, encyclopedia of life sciences. Nature Publishing Group. www.els.net. Accessed March 2012
Davis J (2000) Structure, function and management of the biological system for seasonal solar saltworks. Glob Nest 2:217–226
Davis J, Giordano M (1996) Biological and physical events involved in the origin, effects, and control of organic matter in solar saltworks. Int J Salt Lake Res 4:335–347
Debelius B, Gomez-Parra A, Forja JM (2009) Oxygen solubility in evaporated seawater as a function of temperature and salinity. Hydrobiologia 632:157–165
Dolapsakis NP, Tafas T, Abatzopoulos TJ, Ziller S, Economou-Amilli A (2005) Abundance and growth response of microalgae at Megalon Embolon solar saltworks in northern Greece: an aquaculture prospect. J Appl Phycol 17:39–49
Dolédec S, Chessel D (1994) Co-inertia analysis: an alternative method for studying species—environment relationships. Freshw Biol 31:277–294
Dufour P, Durand JR (1982) La production végétale des lagunes de Côte d’Ivoire. Rev Biol Trop 15:209–230
Egge JK (1998) Are diatoms poor competitors at low phosphate concentrations? J Mar Syst 16:191–198
Elloumi J, Guermazi W, Ayadi H, Bouaïn A, Abderrahmen, Aleya L (2007) Detection of water and sediments pollution of an arid saltern (Sfax, Tunisia) by coupling the distribution of microorganisms with hydrocarbons. Water Air Soil Pollut 187:157–171
Elloumi J, Carrias JF, Ayadi H, Sime-Ngando T, Bouaïn A (2009) Communities structure of the planktonic halophiles in the solar saltern of Sfax, Tunisia. Estuar Coast Shelf Sci 81:19–26
Fehling J, Davidson K, Bolch CJS, Brand TD, Narayanaswamy BE (2012) The relationship between phytoplankton distribution and water column characteristics in north west european shelf sea waters. PLoS One 7:e34098. doi:10.1371/journal.pone.0034098
Gilabert J (2001) Seasonal plankton dynamics in a Mediterranean hypersaline coastal lagoon: the Mar Menor. J Plankton Res 23:207–217
Girault M, Arakawa H, Hashihama F (2013) Phosphorus stress of microphytoplankton community in the western subtropical North Pacific. J Plankton Res 35:146–157
Grover JP, Chrzanowski TH (2006) Seasonal dynamics of phytoplankton in two warm temperate reservoirs: association of taxonomic composition with temperature. J Plankton Res 28:1–17
IPCC (Intergovernmental Panel on Climatic Change) (2007) Fourth assessment report. In: Climatic change impacts, adaptation and vulnerability. http://www.ipcc.ch/
Ismael AA (2003) Succession of heterotrophic and mixotrophic dinoflagellates as well as autotrophic microplankton in the harbour of Alexandria. Egypt J Plankton Res 25:193–202
Joint I, Henriksen P, Garde K, Riemann B (2002) Primary production, nutrient assimilation and microzooplankton grazing along a hypersaline gradient. FEMS Microbiol Ecol 39:245–257
Karandashova IV, Elanskaya IV (2005) Genetic control and mechanisms of salt and hyperosmotic stress resistance in cyanobacteria. Russ J Genet 41:1311–1321
Khemakhem H, Elloumi J, Moussa M, Aleya L, Ayadi H (2010) The concept of ecological succession applied to phytoplankton over four consecutive years in five ponds featuring a salinity gradient. Estuar Coast Shelf Sci 88:33–44
Kobbi-Rebai R, Annabi-Trabelsi N, Khemakhem H, Ayadi H, Aleya L (2013) Impacts of restoration of an uncontrolled phosphogypsum dumpsite on the seasonal distribution of abiotic variables, phytoplankton, copepods, and ciliates in a man-made solar saltern. Environ Monit Assess 185:2139–2155
Koffi K, Philippe DK, Marcel KA, Maryse AN, Kagoyire KA, Adingra AA (2009) Seasonal distribution of phytoplankton in Grand-Lahou Lagoon (Côte d’Ivoire). Eur J Sci Res 26:329–341
Larsen H (1986) Halophilic and halotolerant microorganisms—an overview and historical perspective. FEMS Microbiol Lett 39:3–7
Legendre L, Legendre P (1979) Ecologie numérique 1. Masson, Paris
Lim DSS, Douglas MSV, Smol JP (2001) Diatoms and their relationship to environmental variables from lakes and ponds on Bathurst Island, Nunavut, Canadian High Arctic. Hydrobiologia 450:215–230
Lopez-Flores R, Boix D, Badosa A, Brucet S, Quintana XD (2006) Pigment composition and size distribution of phytoplankton in a confined Mediterranean salt marsh ecosystem. Mar Biol 149:1313–1324
Maar M, Nielsen TG, Richardson K, Christaki U, Hansen OS, Zervoudaki S, Christou ED (2002) Spatial and temporal variability of food web structure during the spring bloom in the Skagerrak. Mar Ecol Prog Ser 239:11–29
Madkour FF, Gaballah MM (2012) Phytoplankton assemblage of a solar saltern in Port Fouad. Egypt Oceanol 54:687–700
Mallin MA, Paerl HW (1994) planktonic trophic transfer in an estuary: seasonal, diel, and community structure effects. Ecology 75:2168–2184
Marques SC, Pardal MÂ, Mendes S, Azeiteiro UM (2011) Using multitable techniques for assessing the temporal variability of species environment relationship in a copepod community from a temperate estuarine ecosystem. J Exp Mar Biol Ecol 405:59–67
Mendes S, Fernandez-Gomez MJ, Resende P, Pereira MJ, Galindo-Villardon MP, Azeiteiro UM (2009) Spatio- temporal structure of diatom assemblages in a temperate estuary. A STATICO analysis. Estuar Coast Shelf Sci 84:637–644
Mishra A, Mandoli A, Jha B (2008) Physiological characterization and stress-induced metabolic responses of Dunaliella salina isolated from salt pan. J Ind Microbiol Biotechnol 35:1093–1101
Moll RA (1977) Phytoplankton in a temperate-zone salt marsh: net production and exchanges with coastal waters. Mar Biol 42:109–118
Montoya H (2009) Algal and cyanobacterial saline biofilms of the Grande Coastal Lagoon, Lima, Peru. Nat Resour Environ Issue 15:127–134
Nagasathya A, Thajuddin N (2008) Cyanobacterial diversity in the hypersaline environment of the saltpans of southeastern coast of India. Asian J Plants Sci 7:473–478
Olaveson MM, Stokes PM (1989) Responses of the acidophilic alga Euglena mutabilis (Euglenophyceae) to carbon enrichment at pH 3. J Phycol 25:529–539
Oren A (2009) Saltern evaporation ponds as model systems for the study of primary production processes under hypersaline conditions. Aquat Microbiol Ecol 56:193–204
Ortega-Mayagoitia E, Rojo C, Rodrigo MA (2003) Controlling factors of phytoplankton assemblages in wetlands: an experimental approach. Hydrobiologia 502:177–186
Pedros-Alio C, Calderon-Paz JI, MacLean MH, Medina G, Marrase C, Gasol JM, Guixa-Boixereu N (2000) The microbial food web along salinity gradients. FEMS Microbiol Ecol 32:143–155
Pinckney JL, Paerl HW, Harrington MB, Howe KE (1998) Annual cycles of phytoplankton community- structure and bloom dynamics in the Neuse River Estuary, North Carolina. Mar Biol 131:371–381
Quintana XD, Amich RM, Comin FA (1998) Nutrient and plankton dynamics in a Mediterranean salt marsh dominated by incidents of flooding. Part 1: differential confinement of nutrients. J Plankton Res 20:2089–2107
Rai LC, Gaur JP (2001) Algal adaptation to environmental stresses: physiological, biochemical and molecular mechanisms. Springer, Berlin
Ramírez F, Abdennadher A, Sanpera C, Jover L, Wassenaar LI, Hobson KA (2011) Assessing waterbird habitat use in coastal evaporative systems using stable isotopes (δ13C, δ15N and δD) as environmental tracers. Estuar Coast Shelf Sci 92:217–222
Resende P, Azeiteiro U, Pereira MJ (2005) Diatom ecological preferences in a shallow temperate estuary (Ria de Aveiro, Western Portugal). Hydrobiologia 544:77–88
Ricard M (1987) Atlas du phytoplancton marin volume 2: Diatomophycées Éditions du centre national de la recherche scientifique, Paris
Richardson K, Pedersen FB (1998) Estimation of new production in the North Sea: consequences for temporal and spatial variability of phytoplankton. J Mar Sci 55:574–580
Richardson K, Nielsen TG, Bo Pedersen F, Heilmann JP, Lokkegaard B, Kaas H (1998) Spatial heterogeneity in the structure of the planktonic food web in the North Sea. Mar Ecol Prog Ser 168:197–211
Salm CR, Saros JE, Martin CS, Erickson JM (2009) Patterns of seasonal phytoplankton distribution in prairie saline lakes of the Northern Great Plains (USA). Saline Syst 5:1448–1746
Shannon CE, Weaver G (1949) The mathematical theory of communication. University of Illinois Press, Urbana
Sherwood JE, Stagnitti F, Kokkinn MJ, Williams WD (1992) A standard table for predicting equilibrium dissolved oxygen concentrations in salt lakes dominated by sodium chloride. J Int J Salt Lake Res 1:1–6
Silkin VA, Pautova LA, Pakhomova SV, Lifanchuk AV, Yakushev EV, Chasovnikov VK (2014) Environmental control of phytoplankton community structure in the NE Black Sea. J Exp Mar Biol Ecol 461:267–274
Sournia A (1986) Atlas du phytoplancton marin volume 1: Cyanophycées, dictyochophycées, dinophycées et raphidophycées. Éditions du centre national de la recherche scientifique, Paris
Stephens DW, Gillespie DM (1976) Phytoplankton production in the Great Salt Lake, Utah, and a laboratory study of algal response to enrichment. Limnol Oceanogr 21:74–87
Sterner RW, Andersen T, Elser JJ, Hessen DO, Hood JM, McCauley E, Urabe J (2008) Scale-dependent carbon: nitrogen: phosphorus seston stoichiometry in marine and freshwaters. Limnol Oceanogr 53:1169–1180
Sylvestre F, Beck-Eichler B, Duleba W, Debenay JP (2001) Modern benthic diatom distribution in a hypersaline coastal lagoon: the Lagoa de Araruama (RJ), Brazil. Hydrobiologia 443:213–231
R Core Team (2014) R: A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. URL http://www.R-project.org/
Thioulouse J (2011) Simultaneous analysis of a sequence of paired ecological tables: a comparison of several methods. Ann Appl Stat 5:2300–2325
Thioulouse J, Chessel D (1987) Les analyses multitableaux en écologie factorielle. Acta Oecol-Oec Gener 8:463–480
Thioulouse J, Simier M, Chessel D (2004) Simultaneous analysis of a sequence of paired ecological tables. Ecology 85:272–283
Trigui H, Masmoudi S, Brochier-Armanet C, Maalej S, Dukan S (2011) Characterization of Halorubrum sfaxense sp. nov., a new halophilic archaeon isolated from the solar saltern of Sfax in Tunisia. Int J Microbiol. doi:10.1155/2011/240191
Utermöhl H (1958) Zur Vervollkommung der quantitativen Phytoplankton Methodik. Mitteilungen Internationale Vereinigung für Theoretische und Angewandte. Limnologie 9:1–38
Ventosa A, Arahal DR (2009) Physico-chemical characteristics of hypersaline environments and their biodiversity. Extremophiles 2:1–6
Vieler A, Wilhelm C, Goss R, Süß R, Schiller J (2007) The lipid composition of the unicellular green alga Chlamydomonas reinhardtii and the diatom Cyclotella meneghiniana investigated by MALDI- TOF MS and TLC. Chem Phys Lipids 150:143–155
Vos J, De la Rosa NL (1980) Manual on Artemia production in salt ponds in the Philippines. Quezon City. In: BFAR/UNDP/FAO, Brackishwater aquaculture and demonstration training project, PHI/75/005, FAO, Rome p 49
Wen Z, Zhi-Hui H (1999) Biological and ecological features of inland saline waters in North Hebei. China Int J Salt Lake Res 8:267–285
Wieland A, Kühl M (2006) Regulation of photosynthesis and oxygen consumption in a hypersaline cyanobacterial mat (Camargue, France) by irradiance, temperature, and salinity. FEMS Microbiol Ecol 55:195–210
Yin K, Qian PY, Chen JC, Hsieh DPH, Harrison PJ (2000) Dynamics of nutrients and phytoplankton biomass in the Pearl River estuary and adjacent waters of Hong Kong during summer: preliminary evidence for phosphorus and silicon limitation. Mar Ecol Prog Ser 194:295–305
Acknowledgments
The authors would like to express their special thanks to COTUSAL staff for giving us access to the saltern and permission to take samples. This work was conducted as part of a collaborative project between the University of Sfax (Tunisia) and the University of Maine (France). This study was supported by the Tunisian Ministry of Scientific Research and Technology. We thank Monika Ghosh for correcting the English language.
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Masmoudi, S., Tastard, E., Guermazi, W. et al. Salinity gradient and nutrients as major structuring factors of the phytoplankton communities in salt marshes. Aquat Ecol 49, 1–19 (2015). https://doi.org/10.1007/s10452-014-9500-5
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DOI: https://doi.org/10.1007/s10452-014-9500-5