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Diazotrophic cyanobacteria signatures and their relationship to hydrographic conditions in the Gulf of Gabes, Tunisia

  • Zaher Drira (a1), Dorra Chaari (a1), Asma Hamza (a2), Malika Bel Hassen (a3), Marc Pagano (a4) and Habib Ayadi (a1)...
Abstract

Changes in the planktonic cyanobacteria structure, composition and diversity were followed over three consecutive years (2005–2006–2007) in the Gulf of Gabes (Eastern Mediterranean Sea, Tunisia). Cyanobacteria abundances, biomasses and cell lengths were measured together with selected environmental variables (pH, salinity, temperature and nutrients). The space and time variations of the cyanobacteria in relation to the environmental factors showed a close relationship between these plankton communities and the hydrographic structure of the water column. Cyanobacteria developed over semi-mixed conditions (May–June 2006) and during the thermal stratification (July 2005). The cyanobacterial abundance and biomass was evident between 20 and 35 m in inshore stations and between 20 and 25 m in deeper stations during the semi-mixing conditions and stratification. This thermocline level coincided with the euphotic layer (21.85 ± 3.76 m) allowing access of light radiation. The cyanobacteria bloom occurred during May–June 2006 when the N/P ratio (<10) was clearly below the accepted standard molar ratio of N/P = 16/1. Commonalities among cyanobacterial genera include being highly competitive for low concentrations of inorganic P (DIP) and the ability to acquire organic P compounds. Our study showed that both diazotrophic (N2-fixing) cyanobacteria such as Anabaena sp., Chroococcus sp., Trichodesmium erythraeum, Spirulina sp. and Spirulina subsalsa and non-diazotrophic cyanobacteria such as Pseudoanabaena sp. and Microcystis display a great flexibility in the N sources which allow formation of blooms.

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Corresponding author
Correspondence should be addressed to: Z. Drira, Département des Sciences de la Vie, Université de Sfax, Faculté des Sciences de Sfax, Unité de recherche UR/11ES72 Biodiversité et Ecosystèmes Aquatiques, Route Soukra Km 3,5. BP 1171 – CP 3000 Sfax, Tunisie email: zaherdrira@yahoo.fr
References
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APHA (1992) American Public Health Association standard methods for the examination of water and wastewater. Washington, DC: American Public Health Association.
Baker, P. (1991) Identification of common noxious cyanobacteria. Part I – Nostocales. Urban Water Research Association of Australia, Research Report no 29.
Baker, P. (1992) Identification of common noxious cyanobacteria. Part II – Chroococcales and Oscillatoriales. Urban Water Research Association of Australia, Research Report no. 46.
Bel Hassen, M., Drira, Z., Hamza, A., Ayadi, H., Akrout, F. and Issaoui, H. (2008) Summer phytoplankton pigments and community composition related to water mass properties in the Gulf of Gabes. Estuarine, Coastal and Shelf Science 77, 645656.
Bel Hassen, M., Drira, Z., Hamza, A., Ayadi, H., Akrout, F., Messaoudi, S., Issaoui, H., Aleya, L. and Bouain, A. (2009) Plankton-pigment signatures and their relationship to spring–summer stratification in the south-eastern Mediterranean. Estuarine, Coastal and Shelf Science 83, 296306.
Berman-Frank, I., Quigg, A., Finkel, Z.V., Irwin, A.J. and Haramaty, L. (2007) Nitrogen-fixation strategies and Fe requirements in cyanobacteria. Limnology and Oceanography 52, 22602269.
Bourrelly, P. (1985) Les Algues d'Eau Douce. Initiation à la Systématique. Tome II. Les Algues bleues et rouges. Les Euglénins, Peridiniens et Cryptomonadines. Paris: Société Nouvelle des Editions Boubée.
Bustillos-Guzman, J., Claustre, H. and Marty, J.C. (1995) Specific phytoplankton signatures and their relationship to hydrographic conditions in the coastal Northwestern Mediterranean Sea. Marine Ecology Progress Series 124, 247258.
Chessel, D., Dufour, A.B. and Thioulouse, J. (2004) The ade4 package-I-One-table methods, R News, 10 pp.
DGPA (2005–2009) Direction Générale de la pêche et de l'aquaculture. Ministère de l'agriculture, Tunisie, annuaire statistique.
Drira, Z., Bel Hassen, M., Ayadi, H. and Aleya, L. (2014a) What factors drive copepod community dynamics in the Gulf of Gabes, Eastern Mediterranean Sea? Environmental Science and Pollution Research 21, 29182934.
Drira, Z., Bel Hassen, M., Hamza, A., Rebai, A., Bouain, A., Ayadi, H. and Aleya, L. (2009) Spatial and temporal variations of microphytoplankton composition related to hydrographic conditions in the Gulf of Gabes. Journal of the Marine Biological Association of the United Kingdom 89, 15591569.
Drira, Z., Elloumi, J., Guermazi, W., Bel Hassen, M., Hamza, A. and Ayadi, H. (2014b) Seasonal changes on planktonic diatom communities along an inshore-offshore gradient in the Gulf of Gabes (Tunisia). Acta Ecologica Sinica 34, 3443.
Drira, Z., Hamza, A., Bel Hassen, M., Ayadi, H., Bouaïn, A. and Aleya, L. (2008) Dynamics of dinoflagellates and environmental factors during the summer in the Gulf of Gabes (Tunisia, Eastern Mediterranean Sea). Scientia Marina 72, 5971.
Drira, Z., Hamza, A., Bel Hassen, M., Ayadi, H., Bouaïn, A. and Aleya, L. (2010) Coupling of phytoplankton community structure to nutrients, ciliates and copepods in the Gulf of Gabes (south Ionian Sea, Tunisia). Journal of the Marine Biological Association of the United Kingdom 90, 12031215.
Elloumi, J., Drira, Z., Guermazi, W., Hamza, A. and Ayadi, H. (2015) Space-time variation of ciliates related to environmental factors in 15 nearshore stations of the Gulf of Gabes (Tunisia, Eastern Mediterranean Sea). Mediterranean Marine Science 16, 162179.
Feki, W., Hamza, A., Frossard, V., Abdennadher, M., Hannachi, I., Jacquot, M., Bel Hassen, M. and Aleya, L. (2013) What are the potential drivers of blooms of the toxic dinoflagellate Karenia selliformis? A 10-year study in the Gulf of Gabes, Tunisia, southwestern Mediterranean Sea. Harmful Algae 23, 818.
Fremy, A.P. and Feldmann, J. (1935) Matériaux pour la flore algologique marine de la Tunisie: contribution à l’étude biologique et systématique de la muffa. Notes Station océanographique 29, 524.
Gallon, J.R. (1992) Tansley review No. 44/reconciling the incompatible: N2 fixation and O2 . New Phytologist 122, 571609.
Giacobbe, M.G., Oliva, F., La Ferla, R., Puglisi, A., Crisafi, E. and Maimone, G. (1995) Potentially toxic dinoflagellates in Mediterranean waters (Sicily) and related hydrobiological conditions. Aquatic Microbial Ecology 9, 6368.
Granéli, E., Wallstrom, K., Larsson, U., Graneli, W. and Elmgren, R. (1990) Nutrient limitation of primary production in the Baltic Sea area. Ambio 19, 142151.
Guerzoni, S., Chester, R., Dulac, F., Herut, B., Loye-Pilot, M.D., Measures, C., Migon, C., Molinaroli, E., Moulin, C., Rossini, P., Saydam, C., Soudine, A. and Ziveri, P. (1999) The role of atmospheric deposition in the biogeochemistry of the Mediterranean Sea. Progress in Oceanography 44, 147190.
Guieu, C., Loye-Pilot, M.D., Benyaya, L. and Dufour, A. (2010) Spatial variability of atmospheric fluxes of metals (Al, Fe, Cd, Zn and Pb) and phosphorus over the whole Mediterranean from a one year monitoring experiment: biogeochemical implications. Marine Chemistry 120, 164178.
Häder, D.P., Kumar, H.D., Smith, R.C. and Worrest, R.C. (2007) Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochemical and Photobiological Sciences 6, 267285.
Hamza, A. and Ben Maiz, N. (1990) Sur l'apparition du phénomène “d'eau rouge” dans le golfe de Gabès en Eté 1988. Bulletin de l'Institut National Scientifique et Technique d'Océanographie et de Pêche de Salammbô 17, 515.
Hannachi, I., Drira, Z., Bel Hassen, M., Hamza, A., Ayadi, H. and Aleya, L. (2011) Species composition and spatial distribution of abundances and biomass of phytoplankton and ciliates during summer stratification in the Gulf of Hammamet (Tunisia). Journal of the Marine Biological Association of the United Kingdom 91, 14291442.
Hansen, G., Erard-Le Denn, E., Daugbjerg, N. and Rodriguez, F. (2004) Karenia selliformis responsible for the fish-kills in the Gulf of Gabes, Tunisia 1994. Harmful Algal Blooms, Programme and Abstracts of the 11 th International Conference, Cape Town, pp. 135.
Hattour, M.J., Sammari, C. and Ben Nassrallah, S. (2010) Hydrodynamics of the Gulf of Gabes deduced from the observations of currents and water levels. Revue Paralia 3, 112.
Hillebrand, H., Durselen, C.D., Kirschtel, D., Pollingher, U. and Zohary, T. (1999) Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35, 403424.
Howarth, R.W., Cole, J.J., Marino, R. and Lane, J. (1988) Nitrogen fixation in freshwater, estuarine and marine ecosystems: rates and importance. Limnology and Oceanography 33, 669687.
Jacques, G., Cahet, G., Fiala, M. and Panouse, M. (1973) Enrichissement de communautés phytoplanctoniques néritiques de Méditerranée nord occidentale. Journal of Experimental Marine Biology and Ecology 11, 287295.
Kivi, K., Kaitala, S., Kuosa, H., Kuparinen, J., Leskinen, E., Lignell, R., Marcussen, B. and Tamminen, T. (1993) Nutrient limitation and grazing control of Baltic plankton community during annual succession. Limnology and Oceanography 38, 893905.
Legendre, P. and Legendre, L. (1998) Numerical ecology. 2nd English edition. Amsterdam: Elsevier Science BV.
Leppänen, J.M., Niemi, A. and Rinne, I. (1988) Nitrogen fixation of cyanobacteria (blue-green algae) and the nitrogen cycle of the Baltic sea. Symbiosis 6, 181194.
Lohman, H. (1908) Untersuchungen zur Feststellung des Vollstandigen Gehaltes des Meeres an Plankton. Wissenschaftliche Meeresuntersuchungen 10, 131170.
Lotze, H.K. and Worm, B. (2009) Historical baselines for large marine animals. Trends in Ecology and Evolution 24, 254262.
Mabrouk, L., Hamza, A. and Bradai, M.N. (2014) Variability in the structure of planktonic microalgae assemblages in water column associated with Posidonia oceanica (L.) bed in Tunisia. Journal of Marine Biology 2014, 17.
Maffucci, F., Kooistra, W.H.C.F. and Bentivegna, F. (2006) Natal origin of loggerhead turtles, Caretta caretta, in the neritic habitat off the Italian coasts, Central Mediterranean. Biological Conservation 127, 183189.
Marty, J.C., Chiaverini, J., Pizay, M.D. and Avril, B. (2002) Seasonal and inter-annual dynamics of nutrients and phytoplankton pigments in the western Mediterranean Sea at the DYFAMED time-series station (1991–1999). Deep-Sea Research 49, 19651985.
Menden-Deuer, S. and Lessard, E.J. (2000) Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnology and Oceanography 45, 569579.
Minas, H.J., Minas, M., Coste, M., Gostan, P., Nival, P. and Bonin, M.C. (1988) Production de base et recyclage; une revue de la problématique en Méditerranée nordoccidentale. Oceanologia Acta 9, 155162.
Oksanen, J., Kindt, R., Legendre, P. and O'Hara, R.B. (2006) Vegan: Community Ecology Package. R package version 1, 8–3.
O'Neil, J.M., Davis, T.W., Burford, M.A. and Gobler, C.J. (2012) The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14, 313334.
Paerl, H.W. and Otten, T.G. (2013) Harmful cyanobacterial blooms: causes, consequences and controls. Microbial Ecology 65, 9951010.
Peres-Neto, P., Legendre, P., Dray, S. and Borcard, D. (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87, 26142625.
Pinckney, J.L., Richardson, T.L., Millie, D.F. and Paerl, H.W. (2001) Application of photopigment biomarkers for quantifying microalgal community composition and in situ growth rates. Organic Geochemistry 32, 585595.
R-Development Core Team (2006) R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. ISBN 3-900051-070.
Ribera d'Alcalà, M., Conversano, F., Corato, F., Licandro, P., Mangoni, O., Marino, D., Mazzocchi, M.G., Modigh, M., Montresor, M., Nardella, M., Saggiomo, V., Sarno, D. and Zingone, A. (2004) Seasonal patterns in plankton communities in a pluriannual time series at a coastal Mediterranean site (Gulf of Naples): an attempt to discern recurrences and trends. In Ros, J.D. Packard, T.T., Gili, J.M., Pretus, J.L. and Blasco, D. (eds) Biological oceanography at the turn of the millennium. Scientia Marina (Barcelona) 67, 6583.
Ridame, C., Guieu, C. and L'Helguen, S. (2013) Strong stimulation of N2 fixation in oligotrophic Mediterranean Sea: results from dust addition in large in situ mesocosms. Biogeosciences 10, 73337346.
Ridame, C., Le Moal, M., Guieu, C., Ternon, E., Biegala, I.C., L'Helguen, S. and Pujo-Pay, M. (2011) Nutrient control of N2 fixation in the oligotrophic Mediterranean Sea and the impact of Saharan dust events. Biogeosciences 8, 27732783.
Sorokovikova, E.G., Belykh, O.I., Gladkikh, A.S., Kotsar, O.V., Tikhonova, I.V., Timoshkin, O.A. and Parfenova, V.V. (2013) Diversity of cyanobacterial species and phylotypes in biofilms from the littoral zone of Lake Baikal. Journal of Microbiology 51, 757765.
Stief, P., Fuchs-Ocklenburg, S., Kamp, A., Manohar, C.S., Houbraken, J., Boekhout, T., Beer, D. and Stoeck, T. (2014) Dissimilatory nitrate reduction by Aspergillus terreus isolated from the seasonal oxygen minimum zone in the Arabian Sea Stief. BMC Microbiology 14, 4712180.
Thingstad, T.F. and Rassoulzadegan, F. (1995) Nutrient limitations, microbial food webs, and ‘‘biological C-pumps’’: suggested interactions in a P-limited Mediterranean. Marine Ecology Progress Series 117, 299306.
Thingstad, F., Zweifel, U.L. and Rassoulzadegan, F. (1998) P-limitation of heterotrophic bacteria and phytoplankton in the northwest Mediterranean. Limnology and Oceanography 43, 8894.
Tilman, D., Kilham, S.S. and Kilham, P. (1982) Phytoplankton community ecology: the role of limiting nutrients. Annual Review of Ecology and Systematics 13, 349372.
Tuomainen, J.M., Hietanen, S., Kuparinen, J., Martikainen, P.J. and Servomaa, K. (2003) Baltic Sea cyanobacterial bloom contains denitrification and nitrification genes, but has negligible denitrification activity. Microbiology Ecology 45, 8396.
Turki, S. and El Abed, A. (2001) On the presence of potentially toxic algae in the lagoons of Tunisia. Harmful Algae News 22, 12 pp.
Turki, S., Harzallah, A. and Sammari, C. (2006) Occurrence of harmful dinoflagellates in two different Tunisian ecosystems: the Lake of Bizerte and the Gulf of Gabes. Cahiers de Biologie Marine 47, 17.
Utermöhl, H. (1958) Zur Vervollkommung der quantitativen Phytoplankton Methodik. Mitteilungen Internationale Vereinigung fur Theoretische und Angewandte. Limnologie 9, 138.
Vahtera, E., Conley, D.J., Gustafsson, B.G., Kuosa, H., Pitkanen, H., Savchuk, O.P., Tamminen, T., Viitasalo, M., Voss, M., Wasmund, N. and Wulff, F. (2007) Internal ecosystem feedbacks enhance nitrogen-fixing cyanobacteria blooms and complicate management in the Baltic Sea. Marine Ecology Progress Series 36, 186194.
Walve, J., Gelting, J. and Ingri, J. (2014) Trace metals and nutrients in Baltic Sea cyanobacteria: internal and external fractions and potential use in nitrogen fixation. Marine Chemistry 158, 2738.
Westman, P., Borgendahl, J., Bianchi, T.S. and Chen, N. (2003) Probable causes for cyanobacterial blooms in the Baltic sea: role of anoxia and phosphorus retention. Estuaries 26, 680689.
Zehr, J.P., Waterbury, J.B., Turner, P.J., Montoya, J.P., Omoregie, E., Steward, G.F., Hansen, A. and Karl, D.M. (2001) Unicellular cyanobacteria fix N2 in the subtropical North Pacific Ocean. Nature 412, 635638.
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