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Spatial and seasonal changes in microphytoplankton and ciliate communities in a stressed area of the southeastern Mediterranean coast (Tunisia)

Published online by Cambridge University Press:  15 September 2023

Amira Rekik
Affiliation:
Faculty of Sciences of Sfax, Department of Sciences of Life, Laboratory LR/18ES30 Marine Biodiversity and Environment, University of Sfax, Street Soukra Km 3.5 – BP 1171 – CP 3000 Sfax, Tunisia
Marc Pagano
Affiliation:
Aix Marseille University, CNRS/INSU, University of Toulon, IRD, Mediterranean Institute of Oceanography (MIO) UM 110, 13288 Marseille, France
Habib Ayadi
Affiliation:
Faculty of Sciences of Sfax, Department of Sciences of Life, Laboratory LR/18ES30 Marine Biodiversity and Environment, University of Sfax, Street Soukra Km 3.5 – BP 1171 – CP 3000 Sfax, Tunisia
Wassim Guermazi
Affiliation:
Faculty of Sciences of Sfax, Department of Sciences of Life, Laboratory LR/18ES30 Marine Biodiversity and Environment, University of Sfax, Street Soukra Km 3.5 – BP 1171 – CP 3000 Sfax, Tunisia
Jannet Elloumi*
Affiliation:
Faculty of Sciences of Sfax, Department of Sciences of Life, Laboratory LR/18ES30 Marine Biodiversity and Environment, University of Sfax, Street Soukra Km 3.5 – BP 1171 – CP 3000 Sfax, Tunisia
*
Corresponding author: Jannet Elloumi; Email: jannetelloumi@yahoo.fr

Abstract

The spatial and seasonal variability of the microphytoplankton and ciliates communities in relation to the environmental factors were studied in the southern coastal area of Sfax. Results revealed a striking difference between seasons regarding pH, with strong acidification in autumn generated by industrial activity. Spatial distribution of pH in autumn impacted the microorganisms in different ways: acidic stations to the south showed significant correlations with Cyanobacteria, dinoflagellates and loricate ciliates whereas higher pH values in spring (pH > 8) were linked to diatoms richness. The high availability of inorganic phosphate is associated with the high release of phosphate due to residue from a phosphate treatment manufacture along the coast; consequently, N/P ratios were low (1.34–13.43) suggesting nitrogen limitation. Microphytoplankton abundance shifted from dinoflagellates dominance in autumn to dominance of diatoms during winter and of Euglenophyceae in summer. Loricate ciliates accounted for the largest proportion of the ciliates community while aloricate ciliates were relatively scarce during all seasons. Variability of ciliate community appeared not directly linked to environmental conditions, but significant positive relationships between abundance of loricate ciliates and microphytoplankton suggest that these ciliates may feed on microphytoplankton.

Type
Research Article
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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References

Abdennadher, M, Hamza, A, Fekih, W, Hannachi, I, Zouari-Belaaj, A, Bradai, N and Aleya, L (2012) Factors determining the dynamics of toxic blooms of Alexandrium minutum during a 10-year study along the shallow southwestern Mediterranean coasts. Estuarine, Coastal and Shelf Science 106, 102111.CrossRefGoogle Scholar
Agawin, NSR, Duarte, CM and Agusti, S (2000) Nutrient and temperature control of the contribution of picoplankton to phytoplankton biomass and production. Limnology and Oceanography 45, 591600.CrossRefGoogle Scholar
Alder, VA (1999) Tintinnoinea. In Boltovsky, D (ed.), South Atlantic Zooplankton. Leiden, The Netherlands: Backhuys Publishers, pp. 321384.Google Scholar
Ayata, SD, Irisson, JO, Aubert, A, Berline, L, Dutay, JC, Mayot, N, Nieblas, AE, D'Ortenzio, F, Palmiéri, J and Reygondeau, G (2017) Regionalisation of the Mediterranean basin, a MERMEX synthesis. Progress in Oceanography 163, 720.CrossRefGoogle Scholar
Azri, C, Abida, H and Medhioub, K (2010) Geochemical behaviour of the aerosol sampled in a suburban zone of Sfax City (Tunisia). International Journal of Environmental Pollution 41, 5169.CrossRefGoogle Scholar
Balech, E (1959) Tintinnoinea del Mediterraneo. Trabajos del Instituto Espanol de Oceanografia 28, 188.Google Scholar
Barrera, BC, Vasquez, I, Barcelo, QA and Bussy, AL (2008) Microalgal dynamics in batch reactors for municipal wastewater treatment containing dairy sewage water. Water, Air, & Soil Pollution 190, 259270.CrossRefGoogle Scholar
Belén Sathicq, M, Gómez, N, Bauer, DE and Donadelli, J (2016) Use of phytoplankton assemblages to assess the quality of coastal waters of a transitional ecosystem: Río de la Plata estuary. Continental Shelf Research 150, 1017.CrossRefGoogle Scholar
Ben Amor, R and Gueddari, M (2016) Major ion geochemistry of Ghannouch–Gabes coastline (at Southeast Tunisia, Mediterranean Sea): study of the impact of phosphogypsum discharges by geochemical modeling and statistical analysis. Environmental Earth Sciences 75, 851.CrossRefGoogle Scholar
Ben Brahim, M, Hamza, A, Ben Ismail, S, Mabrouk, L, Bouain, A and Aleya, L (2013) What factors drive seasonal variation of phytoplankton, protozoans and metazoans on leaves of Posidonia oceanica and in the water column along the coast of the Kerkennah Islands, Tunisia? Marine Pollution Bulletin 7, 286298.Google Scholar
Ben Brahim, M, Hamza, A, Hannachi, I, Rebai, A, Jarboui, O, Bouain, A and Aleya, L (2010) Variability in the structure of epiphytic assemblages of Posidonia oceanica in relation to human interferences in the Gulf of Gabes, Tunisia. Marine Environmental Research 70, 411421.CrossRefGoogle ScholarPubMed
Ben Salem, Z, Drira, Z and Ayadi, H (2015) What factors drive the variations of phytoplankton, ciliate and mesozooplankton communities in the polluted southern coast of Sfax, Tunisia? Environmental Science and Pollution Research 22, 1176411780.CrossRefGoogle ScholarPubMed
Ben Salem, Z, Drira, Z and Ayadi, H (2016) Biodiversity and spatial distribution of copepods community in the south coast of Sfax city (Tunisia). Regional Studies in Marine Science 8, 183191.CrossRefGoogle Scholar
Bojanić, N, Šolić, M, Krstulović, N, Šestanović, S, Marasović, I and Ninčević, Z (2005) Temporal variability in abundance and biomass of ciliates and copepods in the eutrophicated part of Kaštela Bay (Middle Adriatic Sea). Helgoland Marine Research 59, 107120.CrossRefGoogle Scholar
Daly-Yahia Kéfi, O, Souissi, S, Gomez, F and Daly Yahia, MN (2005) Spatio-temporal distribution of the dominant diatom and dinoflagellate species in the Bay of Tunis (SW Mediterranean Sea). Mediterranean Marine Science 6, 1734.CrossRefGoogle Scholar
Dolan, JR, Landry, MR and Ritchie, ME (2013) The species-rich assemblages of tintinnids (marine planktonic protists) are structured by mouth size. International Society for Microbial Ecology 7, 12371243.Google ScholarPubMed
Dolédec, S and Chessel, D (1989) Rythmes saisonniers et composantes stationnelles en milieu aquatique II. Prise en compte et élimination d'effets dans un tableau faunistique. Acta Oecologica-Oecologia Generalis 10, 207332.Google Scholar
D'Ortenzio, F and Riberad'Alcalà, M (2009) On the trophic regimes of the Mediterranean Sea: satellite analysis. Biogeosciences (Online) 6, 110.Google Scholar
Drira, Z, Hamza, A, Belhassen, M, Ayadi, H, Bouïn, 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, Kmiha-Megdiche, S, Sahnoun, H, Hammami, A, Allouche, N, Tedetti, M and Ayadi, H (2016) Assessment of anthropogenic inputs in the surface waters of the southern coastal area of Sfax during spring (Tunisia, Southern Mediterranean Sea). Marine Pollution Bulletin 104, 355363.CrossRefGoogle ScholarPubMed
Edward, ES and Burkill, PH (1995) Abundance, biomass and distribution of microzooplankton in the Irish Sea. Journal of Plankton Research 17, 771782.CrossRefGoogle Scholar
El Kateb, A, Stalder, C, Rüggeberg, A, Neururer, C, Spangenberg, JE and Spezzaferri, S (2018) Impact of industrial phosphate waste discharge on the marine environment in the Gulf of Gabes (Tunisia). PLoS One 13, e0197731. doi: 10.1371/journal.pone.0197731CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Fogg, GE (1991) The phytoplanktonic ways of life. New Phytologist 118, 191232.CrossRefGoogle ScholarPubMed
Frontier, S (1973) Etude statistique de la dispersion du zooplancton. Journal of Experimental Marine Biology and Ecology 12, 229262.CrossRefGoogle Scholar
Gong, J, Song, WB and Warren, A (2005) Periphytic ciliate colonization: annual cycle and responses to environmental conditions. Aquatic Microbial Ecology 39, 159179.CrossRefGoogle Scholar
Grasshof, KM (1983) Determination of nitrate. In Ehradt, K, Grasshof, KM and Kremling, K (eds), Methods of Seawater Analyses. Weinheim: Verlag Chemie, pp. 143150.Google Scholar
Hallegraeff, GM (1993) A review of harmful algal blooms and their apparent global increase. Phycologia 32, 7999.CrossRefGoogle Scholar
Hamza, IS, Wafa, FS, Asma, H and Malika, BH (2016) Long term characterization of Trichodesmium erythraeum blooms in Gabes Gulf (Tunisia). Continental Shelf Research 124, 95103.Google Scholar
Hannachi, I, Drira, Z, Belhassen, M, Hamza, A, Ayadi, H, Bouain, A and Aleya, L (2009) Abundance and biomass of the ciliate community during a spring cruise in the Gulf of Gabès (Eastern Mediterranean Sea, Tunisia). Acta Protozoologica 47, 293305.Google Scholar
Jeong, HJ, Yoo, YD, Kim, JS, Seong, KA, Kang, NS and Kim, TH (2010) Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Science Journal 45, 6591.CrossRefGoogle Scholar
Jiang, Y, Xu, HL, Al-Rasheid, KAS, Warren, A, Hu, XZ and Song, WB (2011) Planktonic ciliate communities in a semi-enclosed bay of Yellow Sea, northern China: annual cycle. Journal of the Marine Biological Association of the United Kingdom 91, 97105.CrossRefGoogle Scholar
Kchaou, N, Elloumi, J, Drira, Z, Hamza, A, Ayadi, H, Bouaïn, A and Aleya, L (2009) Distribution of ciliates in relation to environmental factors along the coastline of the Gulf of Gabes, Tunisia. Estuarine, Coastal and Shelf Science 83, 414424.CrossRefGoogle Scholar
Kobbi-Rebai, R, Annabi-Trabelsi, N, Khemakhem, H, Ayadi, H and 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. Environmental Monitoring and Assessment 185, 21392155.CrossRefGoogle Scholar
Küppers, GC and Claps, MC (2012) Spatio-temporal variations in abundance and biomass of planktonic ciliates related to environmental variables in a temporal pond, Argentina. Zoological Studies 51, 298313.Google Scholar
Lagaria, A, Mandalakis, M, Mara, P, Frangoulis, C, Karatsolis, B, Pitta, P, Triantaphyllou, M, Tsiola, A and Psarra, S (2016) Phytoplankton variability and community structure in relation to hydrographic features in the NE Aegean frontal area (NE Mediterranean Sea). Continental Shelf Research 149, 124137.CrossRefGoogle Scholar
Lomas, MW and Glibert, PM (2000) Comparison of nitrate uptake, storage, and reduction in marine diatoms and flagellates. Journal of Phycology 36, 903913.CrossRefGoogle Scholar
Maranon, E, Cermeno, P, Latasa, M and Tadonleke, RD (2012) Temperature, resources, and phytoplankton size structure in the ocean. Limnology and Oceanography 57, 12661278.CrossRefGoogle Scholar
Mironova, E, Telesh, I and Skarlato, S (2009) Planktonic ciliates of the Baltic Sea (a review). Inland Water Biology 2, 1324.CrossRefGoogle Scholar
Montagnes, DJS, Allen, J, Brown, L, Bulit, C, Davidson, R, Fielding, S, Heath, M, Holliday, NP, Rasmussen, J, Sanders, R, Waniek, JJ and Wilson, D (2010) Role of ciliates and other microzooplankton in the Irminger Sea (NW Atlantic Ocean). Marine Ecology Progress Series 411, 101115.CrossRefGoogle Scholar
Naifar, I, Pereira, F, Zmemla, R, Bouaziz, M, Elleuch, B and Garcia, D (2018) Spatial distribution and contamination assessment of heavy metals in marine sediments of the southern coast of Sfax, Gabes Gulf, Tunisia. Marine Pollution Bulletin 131, 5362.CrossRefGoogle ScholarPubMed
Nausch, M, Nausch, G, Wasmund, N and Nagel, K (2008) Phosphorus pool variations and their relation to cyanobacteria development in the Baltic Sea: a three-year study. Journal of Marine Systems 71, 99111.CrossRefGoogle Scholar
Parsons, TP, Maita, Y and Lalli, CM (1984) A Manuel of Chemical and Biological Methods for Seawater Analysis. Oxford, UK: Pergamon Press, vol. 1, p. 173.Google Scholar
Petz, W (1999) Ciliophora. In Boltovsky, D (ed.), South Atlantic Zooplankton. Leiden, The Netherlands: Backhuys Publishers, pp. 265319.Google Scholar
Plumley, FG (1997) Marine algal toxins: biochemistry, genetics, and molecular biology. Limnology and Oceanography 42, 12521264.CrossRefGoogle Scholar
Rakshit, D, Ganesh, S and Sarkar, SK (2015) Choreotrich ciliate tintinnid (Protozoa: Ciliophora) in a tropical meso–macrotidal estuary, eastern part of India. Regional Studies in Marine Science 3, 89100.CrossRefGoogle Scholar
Rekik, A, Ayadi, H and Elloumi, J (2017 a) Seasonal and spatial distributions of dinoflagellates in relation to environmental factors along the north and south coasts of Sfax (Tunisia, Eastern Mediterranean Sea). Journal of Coastal Life Medicine 7, 299308.CrossRefGoogle Scholar
Rekik, A, Ayadi, H and Elloumi, J (2017 b) The characterisation and seasonal distribution of diatoms along Sfax northern and southern coasts (Gulf of Gabes, Eastern Mediterranean Sea) in relation to environmental conditions. The Journal Earth Sciences & Environmental Studies 2, 227237.Google Scholar
Rekik, A, Ayadi, H and Elloumi, J (2018) Distribution of the plankton assemblages during the winter and summer along the southern coast of the Kerkennah Islands (Tunisia, Eastern Mediterranean Sea). Marine Ecology 39, e12494. doi: 10.1111/maec.12494CrossRefGoogle Scholar
Rekik, A, Ben Salem, Z, Ayadi, H and Elloumi, J (2016 a) Spring phytoplankton variability along a south coast of Sfax at the water-sediment interface (Tunisia, Eastern Mediterranean Sea). Journal of Coastal Life Medicine 4, 121127.CrossRefGoogle Scholar
Rekik, A, Ben Salem, Z, Ayadi, H and Elloumi, J (2016 b) Species composition and spring ciliates variability on the south coast of Sfax (Eastern Mediterranean Sea). Journal of Applied Environmental and Biological Sciences 6, 5771.Google Scholar
Rekik, A, Denis, M, Aleya, L, Maalej, S and Ayadi, H (2013 a) Spring plankton community structure and distribution in the north and south coasts of Sfax (Tunisia) after north coast restoration. Marine Pollution Bulletin 67, 8293.CrossRefGoogle ScholarPubMed
Rekik, A, Denis, M, Maalej, S and Ayadi, H (2015 b) Spatial and seasonal variability of pico-, nano- and microphytoplankton at the water-sediment interface in the north coast of Sfax, Eastern Mediterranean Sea. Environmental Science and Pollution Research 84, 280305.Google Scholar
Rekik, A, Denis, M, Maalej, S and Ayadi, H (2015 c) Planktonic ciliates in relation to abiotic variables on the north coast of Sfax after environmental restoration: species composition, and abundance-biomass seasonal variation. Journal of Oceanography, Research and Data 8, 116.Google Scholar
Rekik, A, Drira, Z, Guermazi, W, Elloumi, J, Maalej, S, Aleya, L and Ayadi, H (2012) Impacts of an uncontrolled phosphogypsum dumpsite on summer distribution of phytoplankton, copepods and ciliates in relation to abiotic variables along the near-shore of the southwestern Mediterranean coast. Marine Pollution Bulletin 64, 336346.CrossRefGoogle ScholarPubMed
Rekik, A, Elloumi, J, Chaari, D and Ayadi, H (2015 a) Microphytoplankton and ciliate communities’ structure and distribution in a stressed area of the south coast of Sfax, Tunisia (eastern Mediterranean Sea). Marine and Freshwater Research 67, 14451462.CrossRefGoogle Scholar
Rekik, A, Maalej, S, Ayadi, H and Aleya, L (2013 b) Restoration impact of an uncontrolled phosphogypsum dump site on the seasonal distribution of abiotic variables, phytoplankton and zooplankton along the near shore of the south-western Mediterranean coast. Environmental Science and Pollution Research 20, 37183734.CrossRefGoogle ScholarPubMed
Ryther, JH and Dunstan, WM (1971) Nitrogen, phosphorus, and eutrophication in the coastal marine environment. Science (New York, N.Y.) 171, 10081013.CrossRefGoogle ScholarPubMed
SCOR-UNESCO (1966) Determination of Photosynthetic Pigments in Sea Water. Paris: UNESCO.Google Scholar
Serbaji, MM, Azri, C and Medhioub, K (2012) Anthropogenic contributions to heavy metal distributions in the surface and sub-surface sediments of the northern coast of Sfax, Tunisia. International Journal of Environmental Research 6, 613626.Google Scholar
Sherr, EB and Sherr, BF (1993) Preservation and storage of samples for enumeration of heterotrophic protests. In Kemp, PF, Sherr, BF, Sherr, EB and Cole, JJ (eds), Handbook of Methods in Aquatic Microbial Ecology. London: Lewis Publishers, pp. 207212.Google Scholar
Sherr, EB and Sherr, BF (2007) Heterotrophic dinoflagellates: a significant component of microzooplankton biomass and major grazers of diatoms in the sea. Marine Ecology Progress Series 352, 187197.CrossRefGoogle Scholar
Sin, Y and Wetzel, RL (2000) Seasonal variations of size-fractionated phytoplankton along the salinity gradient in the York River estuary, Virginia (USA). Journal of Plankton Research 22, 19451960.CrossRefGoogle Scholar
Smayda, TJ (1997) Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnology and Oceanography 42, 11371153.CrossRefGoogle Scholar
Stelfox-Widdicombe, CE, Archer, SD, Burkill, PH and Stefels, J (2004) Microzooplankton grazing in Phaeocystis and diatom-dominated waters in the southern North Sea in spring. Journal of Sea Research 51, 3751.CrossRefGoogle Scholar
Stoecker, DK (1999) Mixotrophy among dinoflagellates. Journal of Eukaryotic Microbiology 46, 397401.CrossRefGoogle Scholar
Strüder-Kypke, MC and Montagnes, DJS (2002) Development of web-based guides to planktonic protists. Aquatic Microbial Ecology 27, 203207.CrossRefGoogle Scholar
Tomas, CR, Hasle, GR, Steidinger, AK, Syvertsen, EE and Tangen, C (1996) Identifying Marine Diatoms and Dinoflagellates. Academic Press, Inc, p. 598.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, 253259.Google Scholar
Utermöhl, H (1958) Zurvervolkommungder quantitativen phytoplankton Methodik. Mitteilungen Internationale Vereinigung fur Theoretische und Angewandte. Journal of Limnology 9, 138.Google Scholar
Yang, J, Löder, MGJ, Gerdts, G and Wiltshire, KH (2015) Structural composition and temporal variation of the ciliate community in relation to environmental factors at Helgoland Roads, North Sea. Journal of Sea Research 101, 1930.CrossRefGoogle Scholar
Ying, Y, Wuchang, Z, Shiwei, W and Tian, X (2013) Abundance and biomass of planktonic ciliates in the sea area around Zhangzi Island, Northern Yellow Sea. Acta Oceanologica Sinica 33, 4551.Google Scholar
Zaghden, H, Kallel, M and Elleuch, B (2014) Evaluation of hydrocarbon pollution in marine sediments of Sfax coastal areas from the Gabes Gulf of Tunisia, Mediterranean Sea. Environmental Earth Sciences 72, 10731082.CrossRefGoogle Scholar
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