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Structure of planktonic food web in the Gulf of Gabès (Southeastern Mediterranean): potential importance of heterotrophic and mixotrophic microzooplankton

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Abstract

The planktonic food web structure was investigated in a productive Mediterranean gulf during spring and fall. Plankton communities, rates of primary production (PP), bacterial production (BP) and grazing by microzooplankton and mesozooplankton were examined in a station influenced by Saharan dust, St1; a station located in the Boughrara Lagoon, St2; and a polluted station, St3, close to a phosphate industrial site. The high nutrient (12–17 µM) and chlorophyll a (Chl a) concentrations (3.7–16.9 mg m−3) as well as the high rates of PP (1123–2638 mg C m−2 d−1) and BP (128–1337 mg C m−2 d−1), recorded throughout the sampling period, indicated the eutrophic character of the study site. Microzooplankton and mesozooplankton mostly showed seasonal changes in their composition and grazing rates. During spring, PP was dominated by nano- and micro-sized fractions, but pico-, nano- and microphytoplankton contributed equally to Chl a. Heterotrophic and mixotrophic microzooplankton consumed significant proportions of the daily production for bacterioplankton (50–72%) and size-fractioned phytoplankton (25–86%), whereas herbivorous copepods grazed daily on 13–15% of PP. These trophic links suggested that the multivorous food web prevailed in spring. During fall, picophytoplankton, mainly Synechococcus, dominated the Chl a and PP in St1, where microbivorous microzooplankton (mainly mixotrophic dinoflagellates) grazed ≥ 50% of the production of bacterioplankton and picophytoplankton, while mesozooplankton, dominated by detritivorous copepods, removed only 5% of PP, suggesting a microbial food web. In St2 and St3, Chl a and PP were dominated by large phytoplankton, which was substantially grazed by heterotrophic and mixotrophic microzooplankton (42–62% grazed d−1) and copepods (12–25% grazed d−1), indicating a carbon channeling throughout the herbivorous food web. The seasonal and spatial change in the planktonic food web implies different efficiencies in the export of carbon. Even in productive waters, picophytoplankton along with microzooplankton, including mixotrophic and heterotrophic organisms, significantly contribute to the ecological functioning of these systems and play a central role in structuring the carbon transfer pathway.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Aberle N, Lengfellner K, Sommer U (2007) Spring bloom succession, grazing impact and herbivore selectivity of ciliate communities in response to winter warming. Œcologica 150:668–681

    CAS  Google Scholar 

  • Alekseenko E, Raybaud V, Espinasse B, Carlotti F, Queguiner B, Thouvenin B, Garreau P, Baklouti M (2014) Seasonal dynamics and stoichiometry of the planktonic community in the NW Mediterranean Sea: a 3D modeling approach. Ocean Dyn 64:179–207

    Article  Google Scholar 

  • Almeda R, Calbet A, Alcaraz M, Saiz E, Trepat I, Arin L, Movilla J, Salo V (2011) Trophic role and carbon budget of metazoan microplankton in northwest Mediterranean coastal waters. Limnol Oceanogr 56:415–430

    Article  CAS  Google Scholar 

  • Alvain S, Moulin C, Dandonneau Y, Loisel H (2008) Seasonal distribution and succession of dominant phytoplankton groups in the global ocean: A satellite view. Global Biogeochemestry Cycles 22, GB3001, doi:https://doi.org/10.1029/2007GB003154

  • Aytan U, Feyzioglu AM, Valente A, Agirbas E, Fileman ES (2018) Microbial plankton communities in the coastal southeastern Black Sea: biomass, composition and trophic interactions. Oceanologia 60:139–152

    Article  Google Scholar 

  • Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263

    Article  Google Scholar 

  • Bautista B, Harris RP (1992) Copepod gut contents, ingestion rates and grazing impact on phytoplankton in relation to size structure of zooplankton and phytoplankton during a spring bloom. Mar Ecol Prog Ser 82:41–50

    Article  Google Scholar 

  • Béjaoui B, Ben Ismail S, Othmani A, Hamida OBA-BH, Chevalier C, Feki-Sahnoun W, Harzallah A, Hamida NBH, Bouaziz R, Dahech S, Diaz F, Tounsi K, Sammari C, Pagano M, Bel Hassen M (2019) Synthesis review of the Gulf of Gabes (eastern Mediterranean Sea, Tunisia): morphological, climatic, physical, oceanographic, biogeochemical and fisheries features. Estuar Coas Shelf Sci 219:395–408

    Article  Google Scholar 

  • Bec B, Husseini-Ratrema J, Collos Y, Souchu P, Vaquer A (2005) Phytoplankton seasonal dynamics in a Mediterranean coastal lagoon: emphasis on the picoeukaryote community. J Plankton Res 27:881–894

    Article  CAS  Google Scholar 

  • Bel Hassen M, Drira Z, Hamza A, Ayadi H, Akrout F, Issaoui H (2008) Summer phytoplankton pigments and community composition related to water mass properties in the Gulf of Gabes. Estuar Coast Shelf Sci 77:645–656

    Article  Google Scholar 

  • Bel Hassen M, Drira Z, Hamza A, Ayadi H, Akrout F, Messaoudi S, Issaoui H, Aleya L, Bouaïn A (2009) Phytoplankton dynamics related to water mass properties in the Gulf of Gabès: ecological implications. J Marine Syst 75:216–226

    Article  Google Scholar 

  • Ben Brahim M, Hamza A, Hannachi I, Rebai A, Jarboui O, Bouain A, Aleya L (2010) Variability in the structure of epiphytic assemblages of Posidonia oceanica in relation to human interferences in the Gulf of Gabes, Tunisia. Mar Environ Res 70:411–421

    Article  CAS  PubMed  Google Scholar 

  • Ben Lamine Y, Pringault O, Aissi M, Ensibi C, Mahmoudi E, Kefi ODY, Yahia MND (2015) Environmental controlling factors of copepod communities in the Gulf of Tunis (South western Mediterranean Sea). Cah Biol Mar 56:213–229

    Google Scholar 

  • Ben Ltaief T, Drira Z, Devenon JL, Hamza A, Ayadia H, Pagano M (2017) How could thermal stratification affect horizontal distribution of depth-integrated metazooplankton communities in the Gulf of Gabes (Tunisia)? Mar Biol Res 13:269–287

    Article  Google Scholar 

  • Bérard-Therriault L, Poulin M, Bossé L (1999) Guide d’identification du phytoplancton marin de l’estuaire et du golfe du Saint-Laurent incluant également certains protozoaires. Publ. Spéc. Can, Sciences halieutique et aquatique, p 387p

    Google Scholar 

  • Berggreen U, Hansen B, Kigkhoe AT (1988) Food size spectra, ingestion and growth of the copepod Acartia tonsu during development: Implications for determination of copepod production. Mar Biol 99:341–352

    Article  Google Scholar 

  • Berglund J, Müren U, Båmstedt U, Andersson A (2007) Efficiency of a phytoplankton-based and a bacteria-based food web in a pelagic marine system. Limnol Oceanogr 52:121–131

    Article  CAS  Google Scholar 

  • Bi R, Sommer U (2020) Food quantity and quality interactions at phytoplankton-zooplankton interface: chemical and reproductive responses in a calanoid copepod. Front Mar Sci 7:274

    Article  Google Scholar 

  • Boudaya L, Mosbahi N, Dauvin JC, Neifar L (2019) Structure of the benthic macrofauna of an anthropogenic influenced area: Skhira Bay (Gulf of Gabès, central Mediterranean Sea). Environ Sci Pollut Res 26:13522–13538

    Article  CAS  Google Scholar 

  • Boukthir M, Ben Jaberi, Chevalier C, Abdennadher J (2019) A high-resolution three dimensional hydrodynamic model of the Gulf of Gabes (Tunisia). 42nd 545 CIESM Congress

  • Boutrup PV, Moestrup Ø, Tillmann U, Daugbjerg N (2016) Katodinium glaucum (Dinophyceae) revisited: proposal of new genus, family and order based on ultrastructure and phylogeny. Phycologia 55(2):147–164

    Article  Google Scholar 

  • Brown SL, Landry MR, Christensen S, Garrison D, Gowing MM, Bidigare RR, Campbell L (2002) Microbial community dynamics and taxon-specific phytoplankton in the Arabian Sea. Deep Sea Research II 49:2345–2376

    Article  Google Scholar 

  • Buitenhuis ET, Rivkin RB, Sailley S, Le Quéré C (2010) Biogeochemical fluxes through microzooplankton. Glob Biogeochem 24:G4015

    Google Scholar 

  • Calbet A (2008) The trophic roles of microzooplankton in marine systems. ICES J Mar Sci 65:325–331

    Article  Google Scholar 

  • Calbet A, Landry MR (2004) Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol Oceanogr 49:51–57

    Article  CAS  Google Scholar 

  • Calbet A, Saiz E (2005) The ciliate-copepod link in marine ecosystems. Aquat Microb Ecol 38:157–167

    Article  Google Scholar 

  • Calbet A, Alcaraz M, Saiz E, Estrada M, Trepat I (1996) Planktonic herbivorous food webs in the catalan Sea (NW Mediterranean): temporal variability and comparison of indices of phyto-zooplankton coupling based on state variables and rate processes. J Plankton Res 18:2329–2347

    Article  Google Scholar 

  • Calbet A, Martínez RA, Isari S, Zervoudaki S, Nejstgaard JC, Pitta P, Sazhin AF, Sousoni D, Gomes A, Berger SA, Tsagaraki TM, Ptacnik R (2012) Effects of light availability on mixotrophy and microzooplankton grazing in an oligotrophic plankton food web: evidences from a mesocosm study in Eastern Mediterranean waters. J Exp Mar Biol Ecol 424:66–77

    Article  Google Scholar 

  • Calbet A, Schmoker C, Russo F, Trottet A, Mahjoub MS, Larsen O, Tong HY, Drillet G (2016) Non-proportional bioaccumulation of trace metals and metalloids in the planktonic food web of two Singapore coastal marine inlets with contrasting water residence times. Sci Total Environ 560–561:284–294

    Article  PubMed  Google Scholar 

  • Carstensen J, Klais R, Cloern JE (2015) Phytoplankton blooms in estuarine and coastal waters: Seasonal patterns and key species. Estuar Coast Shelf Sci 162:98–109

    Article  Google Scholar 

  • Chen M, Liu H, Chen B (2017) Seasonal variability of mesozooplankton feeding rates on phytoplankton in subtropical coastal and Estuarine Waters. Front Mar Sci 4:1–17

    Article  Google Scholar 

  • Chessel D, Mercier P (1993) Couplage de triplets statistiques et liaisons espèces-environnement. In: Lebreton JD, Asselain B (Eds). Biométrie et Environnement. Masson, Paris, pp 15-44

  • Chessel D, Hanafi M (1996) Analyses de la co-inertie de K nuages depoints. Rev Stat Appl 44:35–60

    Google Scholar 

  • Christaki U, Van Wambeke F, Lefevre D, Lagaria A, Prieur L, Pujo-Pay M, Grattepanche JD (2011) Microbial food webs and metabolic state across oligotrophic waters of the Mediterranean Sea during summer. Biogeosciences 8:1839–1852

    Article  CAS  Google Scholar 

  • Courboulès J, Vidussi F, Soulié T, Mas S, Pecqueur D, Mostajir B (2021) Effects of experimental warming on small phytoplankton, bacteria and viruses in autumn in the Mediterranean coastal Thau Lagoon. Aquatic Ecol 55:647–666

    Article  Google Scholar 

  • Culhane CA, Perrière G, Considine EC, Cotter TG, Higgins DG (2002) Between group analysis of microarray data. Bioinformatics 18:1600–1608

    Article  CAS  PubMed  Google Scholar 

  • Cushing DH (1989) A difference in structure between ecosystems in strongly stratified waters and in those that are only weakly stratified. J Plankton Res 11:1–13

    Article  Google Scholar 

  • d’Ortenzio F, d’Alcalà MR (2009) On the trophic regimes of the Mediterranean Sea: a satellite analysis. Biogeosciences 6(2):139–148

    Article  Google Scholar 

  • d’Alcalà MR, Conversano F, Corato F et al (2004) Seasonal pattern in plankton communities in a pluriannual time series at the coastal Mediterranean site (Gulf of Naples): an attempt to discern recurrences and trends. Sci Mar 68:65–83

    Article  Google Scholar 

  • Dagg MJ, Jackson GA, Checkley DM (2014) The distribution and vertical flux of faecal pellets from large zooplankton in Monterey bay and coastal California. Deep-Sea Res Part I-Oceanographic Res Papers 94:72–86

    Article  Google Scholar 

  • Dam HG, Peterson WT (1988) The effect of temperature on the gut clearance rate constant of planktonic copepods. J Exp Mar Biol Ecol 123:1–14

    Article  Google Scholar 

  • Davidson K, Gowen RJ, Tett P, Bresnan E, Harrison PJ, McKinney A, Milligan S, Mills DK, Silke J, Crooks AM (2012) Harmful algal blooms: how strong is the evidence that nutrient ratios and forms influence their occurrence? Estuar Coast Shelf Sci 115:399–413

    Article  CAS  Google Scholar 

  • Decembrini F, Caroppo C, Azzaro M (2009) Size structure and production of phytoplankton community and carbon pathways channeling in the Southern Tyrrhenian Sea (Western Mediterranean). Deep Sea Res Part II 56:687–699

    Article  CAS  Google Scholar 

  • Decembrini F, Caroppo C, Caruso G, Bergamasco A (2021) Linking microbial functioning and trophic pathways to ecological status in a coastal mediterranean ecosystem. Water 13:1325

    Article  CAS  Google Scholar 

  • Deng XW, Chen J, Hansson LA, Zhao X, Xie P (2020) Eco-chemical mechanisms govern phytoplankton emissions of dimethylsulfide in global surface waters. Nat Sci Rev. https://doi.org/10.1093/nsr/nwaa140

    Article  Google Scholar 

  • Dokulil MT, Qian K (2021) Photosynthesis, carbon acquisition and primary productivity of phytoplankton: a review dedicated to Colin Reynolds. Hydrobiologia 848:77–94. https://doi.org/10.1007/s10750-020-04321-y

    Article  CAS  Google Scholar 

  • Dolédec S, Chessel D (1987) Rythmes saisonniers et composantes stationnelles en milieu aquatique. I- Description d’un plan d’observations complet par projection de variables. Acta Œcologica, Œcologica Generalis 8:403–426

    Google Scholar 

  • Dolédec S, Chessel D (1989) Rythmes saisonniers et composantes stationnelles en milieu aquatique II—Prise en compte et élimination d’effets dans un tableau faunistique. Acta Œcologica, Œcologica Generalis 10:207–232

    Google Scholar 

  • Dolédec S, Chessel D (1994) Co-inertia analysis: an alternative method for studying species environment relationships. Freshw Biol 31:277–294

    Article  Google Scholar 

  • Drira Z, Bel Hassen M, Hamza A, Rebai A, Bouain A, Ayadi H, Aleya L (2009) Spatial and temporal variations of microphytoplankton composition related to hydrographic conditions in the Gulf of Gabes. J Mar Biol Assoc UK 89:1559–1569

    Article  CAS  Google Scholar 

  • Drira Z, Bel Hassen M, Ayadi H, Aleya L (2014) What factors drive copepod community dynamics in the Gulf of Gabes, Eastern Mediterranean Sea? Environ Sci Pollut Res 21:2918–2934

    Article  CAS  Google Scholar 

  • Drira Z, Sahnoun H, Ayadi H (2017) Spatial distribution and source identification of heavy metals in surface waters of three coastal areas of Tunisia. Development 5:27

    Google Scholar 

  • Drira Z, Hamza A, Bel Hassen M, Ayadi H, Bouaïn A, Aleya L (2008) Dynamics of dinoflagellates and environmental factors during the summer in the Gulf of Gabes (Tunisia, Eastern Mediterranean Sea). Sci Mar 72:59–71

    Google Scholar 

  • Duarte CM, Agustí S, Vaque D, Agawin NSR, Felipe J, Casamayor EO, Gasol JM (2005) Experimental test of bacteria-phytoplankton coupling in the Southern Ocean. Limnol Oceanogr 50:1844–1854

    Article  CAS  Google Scholar 

  • El Kateb A, Stalder C, Rüggeberg A, Neururer C, Spangenberg JE, Spezzaferri S (2018) Impact of industrial phosphate waste discharge on the marine environment in the Gulf of Gabes (Tunisia). PLoS One 13(5):e0197731

    Article  PubMed  PubMed Central  Google Scholar 

  • Feng C, Han MQ, Dong CC, Jia JY, Chen JW, Wong CK (2020) Mesozooplankton selective feeding on phytoplankton in a semi-enclosed bay as revealed by HPLC pigment analysis. Water 12:2031

    Article  Google Scholar 

  • Feki-Sahnoun W, Hamza A, Mahfoudi M, Rebai A, Bel Hassen M (2014) Long-term microphytoplankton variability patterns using multivariate analyses: ecological and management implications. Environ Sci Pollut Res 21:11481–11499

    Article  CAS  Google Scholar 

  • Feki-Sahnoun W, Hamza A, Njah H, Barraj N, Mahfoudi M, Rebai A, Bel Hassen M (2017) Bayesian network approach to determine environmental factors controlling Karenia selliformis occurrences and blooms in the Gulf of Gabès, Tunisia. Harmful Algae 63:119–132

    Article  PubMed  Google Scholar 

  • Feki-Sahnoun W, Njah H, Hamza A, Barraj N, Mahfoudi M, Rebai A, Bel Hassen M (2018) Using general linear model, Bayesian networks and naive Bayes classifier for prediction of Karenia selliformis occurrences and blooms. Eco Inform 43:12–23

    Article  Google Scholar 

  • Feki-Sahnoun W, Njah H, Hamza A, Barraj N, Mahfoudi M, Rebai A, Bel Hassen M (2020) Using a naive Bayes classifier to explore the factors driving the harmful dinoflagellate Karenia selliformis blooms in a Southeastern Mediterranean lagoon. Ocean Dyn 70:897–911

    Article  Google Scholar 

  • Fonda Umani S, Beran A (2003) Seasonal variations in the dynamics of microbial plankton communities: first estimates from experiments in the Gulf of Trieste, Northern Adriatic Sea. Mar Ecol Prog Ser 247:1–16

    Article  Google Scholar 

  • Fonda Umani S, Tirelli V, Beran A, Guardiana B (2005) Relationships between microzooplankton and mesozooplankton: competition versus predation on natural assemblages of the Gulf of Trieste (northern Adriatic Sea). J Plankton Res 27:973–986

    Article  Google Scholar 

  • Gallegos CL (1989) Microzooplankton grazing on phytoplankton in the Rhode River, Maryland: non-linear feeding kinetics. Mar Ecol Prog Ser 57:22–33

    Article  Google Scholar 

  • Gentleman W, Leising A, Frost B, Strom S, Murray J (2003) Functional responses for zooplankton feeding on multiple resources: a review of assumptions and biological dynamics. Deep Sea Res Part II 50:2847–2875

    Article  CAS  Google Scholar 

  • Giannakourou A, Tsiola A, Kanellopoulou M, Magiopoulos I, Siokou F, Pitta P (2014) Temporal variability of the microbial food web (viruses to ciliates) under the influence of the Black Sea Water inflow (N. Aegean, E. Mediterranean). Mediterr Mar Sci 15:769–780

    Article  Google Scholar 

  • Girault M, Arakawa H, Hashihama F (2013) Phosphorus stress of microphytoplankton community in the western subtropical North Pacific. J Plankton Res 35:146–157

    Article  CAS  Google Scholar 

  • Gómez F, Claustre H, Raimbault P, Souissi S (2007) Two high-nutrient low-chlorophyll phytoplankton assemblages: the tropical central Pacific and the offshore Perú-Chile Current. Biogeosciences 41:101–1113

    Google Scholar 

  • Grami B, Niquil N, Sakka Hlaili A, Gosselin M, Hamel D, Hadj Mabrouk H (2008) The plankton food web of the Bizerte Lagoon (South-Western Mediterranean): II. Carbon steady state modelling using inverse analysis. Estuar Coast Shelf Sci 79:101–113

    Article  Google Scholar 

  • Grattepanche JD, Vincent D, Breton E, Christaki U (2011) Microzooplankton herbivory during the diatom Phaeocystis spring succession in the eastern English Channel. J Exp Mar Biol Ecol 404:87–97

    Article  Google Scholar 

  • Greve W, Reiners F, Nast J, Hoffmann S (2004) Helgoland roads meso- and macrozooplankton time-series 1974 to 2004: lessons from 30 years of single spot, high frequency sampling at the only off-shore island of the North Sea. Helgol Mar Res 58:274–288

    Article  Google Scholar 

  • Grinienė E, Šulčius S, Kuosa H (2016) Size-selective microzooplankton grazing on the phytoplankton in the Curonian Lagoon (SE Baltic Sea). Oceanologia 58:292–301

    Article  Google Scholar 

  • Hamdi I, Denis M, Bellaaj-Zouari A, Khemakhem H, Bel Hassen M, Barani A, Bezac C, Maalej S (2015) The characterization and summer distribution of ultraphytoplankton in the Gulf of Gabès (Eastern Mediterranean Sea, Tunisia) by using flow cytometry. Cont Shelf Res 93:27–38

    Article  Google Scholar 

  • Hamza IS, Feki-Sahnoun W, Hamza A, Bel Hassen M (2016) Long term characterization of Trichodesmium erythraeum blooms in Gabès Gulf (Tunisia). Cont Shelf Res 124:95–103

    Article  Google Scholar 

  • Hannachi I, Drira Z, Bel Hassen M, Hamza A, Ayadi H, Bouain A, Aleya L (2008) Abundance and biomass of the ciliate community during a spring cruise in the gulf of Gabes (East Mediterranean Sea, Tunisia). Acta Protozoologica 47:293–305

    CAS  Google Scholar 

  • Hannides CCS, Siokou I, Zervoudaki S, Frangoulis C, Lange MA (2015) Mesozooplankton biomass and abundance in Cyprus coastal waters and comparison with the Aegean Sea (Eastern Mediterranean). Mediterr Mar Sci 16:373–384

    Article  Google Scholar 

  • Hargraves PE (2002) The ebridian flagellates Ebria and Hermesinum. Plankton Biol Ecol 49:9–16

    Google Scholar 

  • Irigoien X (1998) Gut clearance rate constant, temperature and initial gut contents: a review. J Plankton Res 20(5):997–1003

    Article  Google Scholar 

  • Jacobson DM, Anderson DM (1996) Widespread phagocytosis of ciliates and other protists by marine mixotrophic and heterotrophic thecate dinoflagellates. J Phycol 32:279–285

    Article  Google Scholar 

  • Jafari F, Ramezanpour Z, Sattari M (2015) First record of Ebria tripartita (Schumann) Lemmermann, 1899 from south of the Caspian Sea. Caspian J Environ Sci 13(3):283–288

    Google Scholar 

  • Jeong HJ, Yoo YD, Kim ST, Kang NS (2004) Feeding by the heterotrophic dinoflagellate Protoperidinium bipes on the diatom Skeletonema costatum. Aquatic Microbiol Ecol 36:171–179

    Article  Google Scholar 

  • Jeong HJ, Yoo YD, Park JY, Song JY, Kim ST, Lee SH, Kim KY, Yih WH (2005) Feeding by the phototrophic red-tide dinoflagellates: five species newly revealed and six species previously known to be mixotrophic. Aquat Microb Ecol 40:133–155

    Article  Google Scholar 

  • Jeong HJ, Yoo YD, Kim JS, Seong KA, Kang NS, Kim TH (2010) Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci J 45:65–91

    Article  CAS  Google Scholar 

  • Kase L, Metfes K, Kraberg AC, Neuhaus S, Meunier CL, Wiltshire KH, Boersma M (2021) Metabarcoding analysis suggests that fexible food web interactions in the eukaryotic plankton community are more common than specific predator–prey relationships at Helgoland Roads, North Sea. ICES J Mar Sci 78:3372–3386

    Article  Google Scholar 

  • Khammeri Y, Hamza IS, Bellaaj Zouari A, Hamza A, Sahlia E, Akrout F, Ben Kacem MY, Messaoudi S, Bel Hassen M (2018) Atmospheric bulk deposition of dissolved nitrogen, phosphorus and silicate in the Gulf of Gabès (South Ionian Basin); implications for marine heterotrophic prokaryotes and ultraphytoplankton. Cont Shelf Res 159:1–11

    Article  Google Scholar 

  • Khammeri Y, Bellaaj-Zouari A, Hamza A, Medhioub W, Sahli E, Akrout F, Barraj N, Ben Kacem MY, Bel Hassen M (2020) Ultraphytoplankton community composition in Southwestern and Eastern Mediterranean Basin: relationships to water mass properties and nutrients. J Sea Res 158:101875. https://doi.org/10.1016/j.seares.2020.101875

    Article  Google Scholar 

  • Khedhri I, Djabou H, Afli A (2014) Trophic and functional organization of the benthic macrofauna in the lagoon of Boughrara–Tunisia (SW Mediterranean Sea). J Mar Biological Assoc UK 95:647–659

    Article  Google Scholar 

  • Kleppel G, Pieper R (1984) Phytoplankton pigments in the gut contents of planktonic copepods from coastal waters off Southern California. Mar Biol 78:193–198. https://doi.org/10.1007/BF00394700

    Article  CAS  Google Scholar 

  • Kmiha Megdiche S, Drira Z, Pagano M, Ayadi H (2019) Changes in copepod community between two contrasting samplings in a highly polluted Mediterranean coastal zone (Sfax Bay, Tunisia). Oceanogr Fish Open Access J. https://doi.org/10.19080/OFOAJ.2019.10.555785

    Article  Google Scholar 

  • Landry MR, Calbet A (2004) Microzooplankton production in the oceans. ICES J Mar Sci 61:501–507

    Article  Google Scholar 

  • Landry MR, Décima MR (2017) Protistan microzooplankton and the trophic position of tuna: quantifying the trophic link between micro- and mesozooplankton in marine foodwebs. ICES J Mar Sci 74:1885–1892

    Article  Google Scholar 

  • Landry MR, Hassett RP (1982) Estimating the grazing impact of marine Micro-zooplankton. Mar Biol 67:283–288

    Article  Google Scholar 

  • Landry MR, Brown SL, Neveux J, Dupouy C, Blanchot J, Christensen S, Bidigare RR (2003) Phytoplankton growth and microzooplankton grazing in high-nutrient, low chlorophyll waters of the equatorial Pacific: community and taxon-specific rate assessments from pigment and flow cytometric analyses. J Geophys Res 108:8142

    Article  Google Scholar 

  • Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–18

    Article  Google Scholar 

  • Leblanc K, Queguiner B, Diaz F, Cornet V, Michel-Rodriguez M, De Madron XD, Bowler C, Malviya S, Thyssen M, Grégori G, Rembauville M, Grosso O, Poulain J, De Vargas C, Pujo-Pay M, Conan P (2018) Nanoplanktonic diatoms are globally overlooked but play a role in spring blooms and carbon export. Nat Commun 9(1):953

    Article  PubMed  PubMed Central  Google Scholar 

  • Legendre L, Gosselin M (1989) New production and export of organic matter to the deep ocean: consequences of sorne recent discoveries. Limnol Oceanogr 34:1374–1380

    Article  CAS  Google Scholar 

  • Legendre L, Le Fèvre J (1989) Hydrodynamical singularities as controls of recycled versus export production in oceans. In: Berger WH, Smetacek VS, Wefer G (eds) Productivity of the ocean: present and past. John Wiley and sons Limited, Dahlem, pp 49–63

    Google Scholar 

  • Legendre L, Rassoulzadegan F (1995) Plankton and nutrient dynamics in marine waters. Ophelia 41:153–172

    Article  Google Scholar 

  • Liu X, Li Y, Wu Y, Huang B, Dai M, Fu F, Hutchins DA, Gao K (2017) Effects of elevated CO2 on phytoplankton during a mesocosm experiment in the southern eutrophicated coastal water of China. Sci Rep 7:6868

    Article  PubMed  PubMed Central  Google Scholar 

  • Livanou E, Lagaria A, Santi I, Mandalakis M, Pavlidou A, Lika K, Psarra S (2019) Pigmented and heterotrophic nanoflagellates: abundance and grazing on prokaryotic picoplankton in the ultra-oligotrophic Eastern Mediterranean Sea. Deep Sea Res Part II 164:100–111

    Article  CAS  Google Scholar 

  • López-Abbate MC (2021) Microzooplankton communities in a changing ocean: a risk assessment. Diversity 13:82

    Article  Google Scholar 

  • Makhlouf Belkahia N, Pagano M, Chevalier C, Devenon JL, Daly Yahia MN (2021) Zooplankton abundance and community structure driven by tidal currents in a Mediterranean coastal lagoon (Boughrara, Tunisia, SW Mediterranean Sea). Estuar Coast Shelf Sci 250:107101

    Article  Google Scholar 

  • Marrec P, Heather MN, Gayantonia F, Françoise M, Jacob PS, Menden-Deuer S (2021) Seasonal variability in planktonic food web structure and function of the Northeast U.S. Shelf. Limnol Oceanogr 66:1440–1458. https://doi.org/10.1002/lno.11696

    Article  Google Scholar 

  • Meddeb M, Grami B, Chaalali A, Haraldsson H, Niquil N, Pringault O, Sakka Hlaili A (2018) Plankton food-web functioning in anthropogenically impacted coastal waters (SW Mediterranean Sea): an ecological network analysis. Prog Oceanogr 162:66–82

    Article  Google Scholar 

  • Meddeb M, Niquil N, Grami B, Mejri K, Haraldsson M, Chaalali A, Pringault O, Sakka Hlaili A (2019) A new type of plankton food web functioning in coastal waters revealed by coupling Monte Carlo Markov chain linear inverse method and ecological network analysis. Ecol Ind 104:67–85

    Article  Google Scholar 

  • Mercado JM, Cortés D, Gómez-Jakobsen F, García-Gómez C, Ouaissa S, Yebra L, Ruíz JM (2021) Role of small-sized phytoplankton in triggering an ecosystem disruptive algal bloom in a Mediterranean hypersaline coastal lagoon. Mar Pollut Bull 164:111989

    Article  CAS  PubMed  Google Scholar 

  • Moigis AG, Gocke K (2003) Primary production of phytoplankton estimated by means of the method in coastal waters. J Plankton Res 25:1291–1300

    Article  CAS  Google Scholar 

  • Morales CE, Harris RP, Head RN, Tranter PRG (1993) Copepod grazing in the oceanic northeast Atlantic during a 6 week drifting station: the contribution of size classes and vertical migrants. J Plankton Res 15:185–211

    Article  Google Scholar 

  • Morán XAG, Ducklow HW, Erickson M (2011) Single-cell physiological structure and growth rates of heterotrophic bacteria in a temperate estuary (Waquoit Bay, Massachusetts). Limnol Oceanogr 56:37–48

    Article  Google Scholar 

  • Ning X, Li W, Cai YM, Shi J (2005) Comparative analysis of bacterioplankton and phytoplankton in three ecological provinces of the northern South China Sea. Mar Ecol Prog Ser 293:17–28

    Article  Google Scholar 

  • Numerical and Taxonomic Index of ICES Plankton Identification Leaflets, 1939–2001

  • Othmani A, Béjaoui B, Chevalier C, Elhmaidi D, Devenon JL, Aleya L (2017) High-resolution numerical modelling of the barotropic tides in the Gulf of Gabes, eastern Mediterranean Sea (Tunisia). J Afr Earth Sc 129:224–232

    Article  Google Scholar 

  • Paklar GB, Vilibić I, Grbec B, Matić F, Mihanović H, Džoić T, Šantić D, Šestanović S, Šolić M, Ivatek-Šahdan S, Kušpilić G (2020) Record-breaking salinities in the middle Adriatic during summer 2017 and concurrent changes in the microbial food web. Prog Oceanogr 185:102345

    Article  Google Scholar 

  • Parsons TP, Maita Y, Lalli CM (1984) A manuel of chemical and biological methods for seawater analysis. Pergamon Press, Oxford, England 1:173

    Google Scholar 

  • Pecqueur D, Vidussi F, Fouilland E, Le Floc’h E, Mas S, Roques C, Salles C, Tournoud MG, Mostajir B (2011) Dynamics of microbial planktonic food web components during a river flash flood in a Mediterranean coastal lagoon. Hydrobiologia 673:13–27

    Article  CAS  Google Scholar 

  • Pecqueur D, Courboulès J, Roques C, Mas S, Pete R, Vidussi F, Mostajir B (2022) Simultaneous study of the growth and grazing mortality rates of microbial food web components in a Mediterranean Coastal Lagoon. Diversity 14(3):186

    Article  Google Scholar 

  • Pulido-Villena E, Baudoux AC, Obernosterer I, Landa M, Caparros J, Catala P, Georges C, Harmand J, Guieu C (2014) Microbial food web dynamics in response to a Saharan dust event: results from a mesocosm study in the oligotrophic Mediterranean Sea. Biogeosci Discuss 11:337–371

    Google Scholar 

  • Quemeneur M, Bel Hassen M, Armougom F, Khammeri Y, Lajnef R (2020) Prokaryotic diversity and distribution along physical and nutrient gradients in the tunisian Coastal Waters (South Mediterranean Sea). Front Microbiol 11:593540

    Article  PubMed  PubMed Central  Google Scholar 

  • Raimbault P, Garcia N, Cerutti F (2008) Distribution of inorganic and organic nutrients in the South Pacific Ocean−evidence for long-term accumulation of organic matter in nitrogen-depleted waters. Biogeosciences 5(2):281–298

    Article  CAS  Google Scholar 

  • Rhyter JH (1969) Photosynthesis and fish production in the sea. Science 166:72–76

    Article  Google Scholar 

  • Romano F, Symiakaki K, Pitta P (2021) Temporal variability of planktonic ciliates in a coastal oligotrophic environment: mixotrophy, size classes and vertical distribution. Front Mar Sci 8:113p

    Article  Google Scholar 

  • Ross ON, Fraysse M, Pinazo C, Pairaud I (2016) Impact of an intrusion by the Northern Current on the biogeochemistry in the eastern Gulf of Lion, NW Mediterranean. Estuar Coast Shelf Sci 170:1–9

    Article  CAS  Google Scholar 

  • Saito H, Ota T, Suzuki K, Nishioka J, Tsuda A (2006) Role of heterotrophic dinoflagellate Gyrodinium sp. in the fate of an iron induced diatom bloom. Geophys Res Lett 33:L09602

    Article  Google Scholar 

  • Saiz E, Rodriguez V, Alcaraz M (1992) Spatial distribution and feeding rates of Centropages typicus in relation to frontal hydrographic structures in the Catalan Sea (Western Mediterranean). Mar Biol 112:49–56

    Article  Google Scholar 

  • Sakka Hlaili A, Grami B, Hadj Mabrouk H, Gosselin M, Hamel D (2007) Phytoplankton growth and microzooplankton grazing rates in a restricted Mediterranean lagoon (Bizerte Lagoon, Tunisia). Mar Biol 151:767–783

    Article  Google Scholar 

  • Sakka Hlaili A, Grami B, Niquil N, Gosselin M, Hamel D, Troussillier M (2008) The planktonic food web of the Bizerte lagoon (South-Western Mediterranean) during summer: I. Spatial distribution under different anthropogenic pressures. Estuar Coast Shelf Sci 78:61–77

    Article  Google Scholar 

  • Sakka Hlaili A, Niquil N, Legendre L (2014) Planktonic food webs revisited Reanalysis of results from the linear inverse approach. Prog Oceanogr 120:216–229

    Article  Google Scholar 

  • Salgado-Hernanz PM, Racault MF, Font-Muñoz JS, Basterretxea G (2019) Trends in phytoplankton phenology in the Mediterranean Sea based on ocean-colour remote sensing. Remote Sens Environ 221:50–64

    Article  Google Scholar 

  • Sammari C, Koutitonsky VG, Moussa M (2006) Sea level variability and tidal resonance in the Gulf of Gabes. Tunisia. Cont Shelf Res 26(3):338–350

    Article  Google Scholar 

  • Sandhu SK, Morozov AY, Mitra A, Flynn K (2019) Exploring nonlinear functional responses of zooplankton grazers in dilution experiments via optimization techniques. Limnol Oceanogr 64:774–784

    Article  Google Scholar 

  • Šantić D, Krstulović N, Šolić M, Kušpilić G (2011) Distribution of Synechococcus and Prochlorococcus in the central Adriatic Sea. Acta Adriat 52:101–114

    Google Scholar 

  • Sato M, Yoshikawa T, Takeda S, Furuya S (2007) Application of the size-fractionation method to simultaneous estimation of clearance rates by heterotrophic flagellates and ciliates of pico- and nanophytoplankton. J Exp Mar Biol Ecol 349:334–343

    Article  Google Scholar 

  • Sautour B, Artigas LF, Delmas D, Herbland A, Laborde P (2000) Grazing impact of micro-and mesozooplankton during a spring situation in coastal waters off the Gironde estuary. J Plankton Res 22(3):531–552

    Article  Google Scholar 

  • Seong KA, Jeong HJ, Kim S, Kim GH, Kang JH (2006) Bacterivory by co-occurring red-tide algae, heterotrophic nanoflagellates, and ciliates on marine bacteria. Mar Ecol Prog Ser 322:85–97

    Article  Google Scholar 

  • Sherr EB, Sherr BF (1993) Preservation and storage of samples for enumeration of heterotrophic protests. In: Kemp PF, Sherr BF, Sherr EB, Cole JJ (eds) Handbook of methods in aquatic microbial ecology. Lewis Publishers, London, pp 207–212

    Google Scholar 

  • Sherr EB, Sherr BF, Hartz AJ (2009) Microzooplankton grazing impact in the western Arctic Ocean. Deep-Sea Res II. https://doi.org/10.1016/jdsr2.2008.10.036

    Article  Google Scholar 

  • Shinada A, Ban S, Yamada Y, Ikeda T (2005) Seasonal variations of plankton food web structure in the coastal water off Usujiri southwestern Hokkaido, Japan. J Oceanogr 61:645–654

    Article  Google Scholar 

  • Šimek K, Bobkova J, Macek M, Nedoma J, Psenner R (1995) Ciliate grazing on picoplankton in a eutrophic reservoir during the summer phytoplankton maximum: A study at the species and community level. Limnol Oceanogr 40:1077–1090

    Article  Google Scholar 

  • Siokou-Frangou I, Christaki U, Mazzocchi MG, Montresor M, d’Alcala MR, Vaque D, Zingone A (2010) Plankton in the open Mediterranean Sea: a review. Biogeosciences 7(5):1543–1586

    Article  Google Scholar 

  • Slaughter AM, Bollens SM, Bollens GR (2006) Grazing impact of mesozooplankton in an upwelling region off northern California, 2000–2003. Deep Sea Res II 53:3099–3115

    Article  Google Scholar 

  • Šolić M, Krstulović N, Kušpilić G, Ninčević Gladan Ž, Bojanić N, Šestanović S, Šantić D, Ordulj M (2010) Changes in microbial food web structure in response to changed environmental trophic status: a case study of the Vranjic Basin (Adriatic Sea). Mar Environ Res 70:239–249

    Article  PubMed  Google Scholar 

  • Stoecker DK (1999) Mixotrophy among dinoflagellates. J Eukaryot Microbiol 46:397–401

    Article  Google Scholar 

  • Sun J, Feng Y, Zhang Y, Hutchins DA (2007) Fast microzooplankton grazing on fast growing, low-biomass phytoplankton: a case study in spring in Chesapeake Bay, Delaware Inland Bays and Delaware Bay. Hydrobiologia 589(1):127–139

    Article  Google Scholar 

  • Tanaka T, Rassoulzadegan F, Thingstad TF (2003) Measurements of phosphate affinity constants and phosphorus release rates from the microbial food web in Villefranche Bay, northwestern Mediterranean. Limnol Oceanogr 48:1150–1160

    Article  CAS  Google Scholar 

  • Tanaka T, Thingstad TF, Christaki U, Colombet J, CornetBarthaux V, Courties C, Grattepanche JD, Lagaria A, Nedoma J, Oriol L, Psarra S, Pujo-Pay M, Van Wambeke F (2011) Lack of P-limitation of phytoplankton and heterotrophic prokaryotes in surface waters of three anticyclonic eddies in the stratified Mediterranean Sea. Biogeosciences 8:525–538

    Article  CAS  Google Scholar 

  • Thompson RM, Brose U, Sunne JA, Hall RO, Hladyz S, Kitching RL, Martinez ND, Rantala H, Romanuk TN, Stouffer DB, Tylianakis JM (2012) Food webs: reconciling the structure and function of biodiversity. Trends Ecol Evol 27:689–697

    Article  PubMed  Google Scholar 

  • Trégouboff G, Rose M (1957) Manuel de Planctonologie Méditerranéenne. Centre National de la Recherche Scientifique, Paris 1:587

    Google Scholar 

  • Tseng LC, Kumar R, Dahms HU, Chen QC, Hwang JS (2008) Copepod gut contents, ingestion rates and feeding impact in relation to their size structure in the southeastern Taiwan Strait. Zoological Studies 47(4):402–416

    Google Scholar 

  • Utermöhl H (1931) Neue Wege in der quantitativen Erfassung des Plankton. (Mit besonderer Berücksichtigung des Ultraplanktons). Vereinigung Für Theoretische und Angewandte Limnologie 5:567–596

    Google Scholar 

  • Vargas CA, Martínez RA, Cuevas LA, Pavez MA, Cartes C, Humberto E, González HE, Escribano R, Daneri G (2007) The relative importance of microbial and classical food webs in a highly productive coastal upwelling area. Limnol Oceanogr 52(4):1495–1510

    Article  Google Scholar 

  • Vézina AF, Pahlow M (2003) Reconstruction of ecosystem flows using inverse methods: how well do they work? J Mar Syst 40:55–77

    Article  Google Scholar 

  • Viñas MD, Negri RM, Cepeda GD, Hernández D, Silva R, Daponte MC, Capitanio FL (2013) Seasonal succession of zooplankton in coastal waters of the Argentine Sea (Southwest Atlantic Ocean): prevalence of classical or microbial food webs. Mar Biol Res 9:371–382

    Article  Google Scholar 

  • Zakaria HY, Hassan AKM, El-Naggar HA, Abo-Senna FM (2018) Biomass determination based on the individual volume of the dominant copepod species in the Western Egyptian Mediterranean Coast. Egypt J Aquatic Res 44:89–99

    Article  Google Scholar 

  • Zmemla R, Chaurand P, Benjdidia M, Elleuch B, Bottero JY (2016) Characterization and pH dependent leaching behavior of tunisian phosphogypsum. Am Sci Res J Eng, Technol Sci (ASRJETS) 24:230–244

    Google Scholar 

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Acknowledgements

The study was carried out in the frame of the national projet GAMA (Gabès Modelling Assesment) funded by the National Institute for Marine Science and Technology (INSTM, Tunisia) and the project COZOMED-MERMEX (Effets of physical forcing on Coastal ZOoplankton community structure: study of the unusual case of a MEDiterranean ecosystem under strong tidal influence) funded by the French MAEE (ENVI-MED/MISTRALS AP 2014). English grammar and syntax of the manuscript were revised by Proof-Reading-Service.com. We thank two anonymous reviewers for their useful suggestions and comments.

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  1. Kaouther Mejri Kousri

    Present address: Institut National des Sciences et Technologies de la Mer (INSTM), 28, rue 2 mars 1934, 2025, Salammbô, Tunisia

Authors and Affiliations

  1. Faculté des Sciences de Bizerte, Laboratoire de Biologie Végétale et Phytoplanctonologie, Université de Carthage, Bizerte, Tunisia

    Kaouther Mejri Kousri, Marouan Meddeb, Oumayma Chkili & Asma Sakka Hlaili

  2. Institut National des Sciences et Technologies de la Mer (INSTM), 28, rue 2 mars 1934, 2025, Salammbô, Tunisia

    Amel Belaaj Zouari, Cherif Sammari, Yosra Khammeri & Malika Bel Hassen

  3. Faculté des Sciences de Tunis, Laboratoire des Sciences de l’environnement, Biologie et Physiologie des Organismes Aquatiques LR18ES41, Université de Tunis El Manar, Tunis, Tunisia

    Marouan Meddeb, Oumayma Chkili & Asma Sakka Hlaili

  4. CNRS, Normandie Université, UNICAEN, UMR BOREA (MNHN, CNRS-8067, Sorbonne Université, Université Caen Normandie, IRD-207, Université des Antilles), 14032, Caen, France

    Oumayma Chkili & Nathalie Niquil

  5. Aix-Marseille University, Université de Toulon, CNRS, IRD, MIO UM 110, Marseille, France

    Marc Tedetti & Marc Pagano

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Contributions

KMK: Conceptualization, Methodology, Investigation, Writing-original draft, Supervision. ABZ: Resources, Methodology, Investigations, Writing—review and editing. MM: Resources, Investigations. OC: Resources, Investigations. NN: Methodology, Investigation, Writing—review and editing. MT: Resources, Writing—review and editing. MP: Resources, Writing—review and editing. CS: Resources, Investigations. YK: Investigations, Software. MBH: Resources, Writing—review and editing. ASH: Project administration, Conceptualization, Methodology, Investigation, Writing—original draft, Supervision.

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Correspondence to Asma Sakka Hlaili.

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Mejri Kousri, K., Belaaj Zouari, A., Meddeb, M. et al. Structure of planktonic food web in the Gulf of Gabès (Southeastern Mediterranean): potential importance of heterotrophic and mixotrophic microzooplankton. Aquat Sci 85, 61 (2023). https://doi.org/10.1007/s00027-023-00954-y

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