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

Published online by Cambridge University Press:  13 January 2016

Zaher Drira*
Affiliation:
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
Dorra Chaari
Affiliation:
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
Asma Hamza
Affiliation:
Institut National des Sciences et Technologie de la Mer, Centre de Sfax BP1035- CP 3018 Sfax, Tunisie
Malika Bel Hassen
Affiliation:
Institut National des Sciences et Technologie de la Mer, 2025 Salammbô Tunis, Tunisie
Marc Pagano
Affiliation:
Mediterranean Institute of Oceanography, Université d'Aix Marseille, CNRS, Université de Toulon, IRD, MIO UM 110, 13288, Marseille, France
Habib Ayadi
Affiliation:
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
*
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

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.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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References

REFERENCES

APHA (1992) American Public Health Association standard methods for the examination of water and wastewater. Washington, DC: American Public Health Association.Google Scholar
Baker, P. (1991) Identification of common noxious cyanobacteria. Part I – Nostocales. Urban Water Research Association of Australia, Research Report no 29.Google Scholar
Baker, P. (1992) Identification of common noxious cyanobacteria. Part II – Chroococcales and Oscillatoriales. Urban Water Research Association of Australia, Research Report no. 46.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Chessel, D., Dufour, A.B. and Thioulouse, J. (2004) The ade4 package-I-One-table methods, R News, 10 pp.Google Scholar
DGPA (2005–2009) Direction Générale de la pêche et de l'aquaculture. Ministère de l'agriculture, Tunisie, annuaire statistique.Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Gallon, J.R. (1992) Tansley review No. 44/reconciling the incompatible: N2 fixation and O2 . New Phytologist 122, 571609.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Legendre, P. and Legendre, L. (1998) Numerical ecology. 2nd English edition. Amsterdam: Elsevier Science BV.Google Scholar
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.Google Scholar
Lohman, H. (1908) Untersuchungen zur Feststellung des Vollstandigen Gehaltes des Meeres an Plankton. Wissenschaftliche Meeresuntersuchungen 10, 131170.Google Scholar
Lotze, H.K. and Worm, B. (2009) Historical baselines for large marine animals. Trends in Ecology and Evolution 24, 254262.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Menden-Deuer, S. and Lessard, E.J. (2000) Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnology and Oceanography 45, 569579.CrossRefGoogle Scholar
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.Google Scholar
Oksanen, J., Kindt, R., Legendre, P. and O'Hara, R.B. (2006) Vegan: Community Ecology Package. R package version 1, 8–3.Google Scholar
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.Google Scholar
Paerl, H.W. and Otten, T.G. (2013) Harmful cyanobacterial blooms: causes, consequences and controls. Microbial Ecology 65, 9951010.Google Scholar
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.Google Scholar
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.Google Scholar
R-Development Core Team (2006) R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. ISBN 3-900051-070.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Utermöhl, H. (1958) Zur Vervollkommung der quantitativen Phytoplankton Methodik. Mitteilungen Internationale Vereinigung fur Theoretische und Angewandte. Limnologie 9, 138.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar