Scientia Marina, Vol 78, No 1 (2014)

Variability in the structure of epiphytic microalgae assemblages on the leaves of Posidonia oceanica in relation to human disturbance in a meadow off Tunisia

Lotfi Mabrouk
Faculté des Sciences de Sfax - Institut National des Sciences et Technologies de la Mer, Tunisia

Mounir Ben Brahim
Faculté des Sciences de Sfax - Institut National des Sciences et Technologies de la Mer, Tunisia

Asma Hamza
Institut National des Sciences et Technologies de la Mer, Tunisia

Mabrouka Mahfoudhi
Institut National des Sciences et Technologies de la Mer, Tunisia

Med Najmeddine Bradai
Institut National des Sciences et Technologies de la Mer, Tunisia


We investigated the impact of sewage discharge on Posidonia oceanica meadows in Mahdia, eastern Tunisia. We specifically addressed changes in biometric plant parameters and epiphytic microalgae composition on leaves caused by this anthropogenic interference. A hierarchical sampling design was used to compare epiphytic microalgae structure between one disturbed and two control stations. Samples were collected by SCUBA diving at 8 m depth in August 2009. A total of 58 microalgae taxa were identified on leaves. At the disturbed station, leaf length, leaf surface area and the leaf area index decreased, whereas epiphytic dinoflagellate abundances increased compared with the control stations, with more Prorocentrales, Protoperidiniales and potentially toxic species on leaves of the disturbed station. Moderate nutrient enrichment (mainly Si(OH)4 and NH4+) and low water transparency at the disturbed station were associated with the increased abundances of some dinoflagellate species.


epiphytic microalgae; sewage disturbance; spatial variability; Posidonia oceanica

Full Text:



Aligizaki K., Nikolaidis G. 2006. The presence of the potentially toxic genera Ostreopsis and Coolia (Dinophyceae) in the North Aegean Sea, Greece. Harmful Algae 5: 717-730.

Anderson D.M., Glibert P.M., Burkholder J.M. 2002. Harmful Algal Blooms and Eutrophication: Nutrient Sources, Composition, and Consequences. Estuaries 25: 704-726.

Armi Z., Turki S., Trabelsi E., BenMaiz N. 2010. First recorded proliferation of Coolia monotis (Meunier, 1919) in the North Lake of Tunis (Tunisia) correlation with environmental factors. Environ. Monit. Assess. 164: 423-433. PMid:19404758

Armitage A.R., Frankovich T.A., Fourqurean J.W. 2006. Variable responses within epiphytic and benthic microalgal communities to nutrient enrichment. Hydrobiologia 569: 423-435.

Augier H., Maudinas B. 1979. Influence of the pollution on the photosynthetic pigments of the marine phanerogam Posidonia oceanica collected from different polluted areas of the Region of Marseille (Mediterranean sea, France). Oecolog. Plantar. 14(2): 169-176.

Baker J.W., Groyer J.P., Brooks B.W., Ure-a-Boeck F., Roelke D.L., Errera R.M., Kiesling R. 2007. Growth and toxicity of Prymnesium parvum (Haptophyta) as a function of salinity, light and temperature. J. Phycol. 43: 219-222.

Balata D., Bertocci I., Piazzi L., Nesti N. 2008 Comparison between epiphyte assemblages of leaves and rhizomes of the seagrass Posidonia oceanica subjected to different levels of anthropogenic eutrophication. Estuar. Coast Shelf. Sci. 79: 533-540.

Ben Alaya H. 1972. Répartition et conditions d'installation de Posidonia oceanica Delile et Cymodocea nodosa Ascherson dans le golfe de Tunis. Bull. Inst. Nat. Sc. et Tech. d'Océanographie et de Pèche de Salammbo 2: 331-416.

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. PMid:20851462

Ben Brahim M, Hamza A., Ben Ismail S., Mabrouk L., Bouain A., 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? Mar. Pollut. Bull. 71: 286-298. PMid:23498657

Borowitzka M.A., Lavery P., Keulen M. (2006). Epiphytes of Seagrasses. In: Larkum A.W.D., Orth R.J., Duarte C.M. (eds), Seagrasses: Biology, Ecology and Conservation. Springer, The Netherlands: 441-461.

Cambridge M.L., Chiffings A.W., Brittan C., Moore L., McComb A.J. 1986. The loss of seagrass in Cockburn Sound, Western Australia. Possible causes of seagrass decline. Aquat. Bot. 24: 269-285.

Cancemi G., De Falco G., Pergent G. 2003. Effects of organic matter input from a fish farming facility on Posidonia oceanica meadow. Estuar. Coast. Shelf Sci. 56: 961-968.

Capiomont A., Piazzi L., Pergent G. 2000. Seasonal variations of total mercury in foliar tissues of Posidonia oceanica. J. Mar. Biol. Assoc. U. K. 80: 1119-1123.

Cattaneo A. 1983. Grazing on epiphytes. Limnol. Oceanogr. 28: 124-132.

Chikhaoui M.A., Hlaili A.S., Mabrouk H.H. 2008. Seasonal phytoplankton responses to N:Si:P enrichment ratio in the Bizerte Lagoon (southwestern Mediterranean). C. R. Biol.¡ 331(5): 389-408. PMid:18472085

Chung M.H., Lee K.S. 2008. Species composition of the epiphytic diatoms on the leaf tissues of three Zostera species distributed on the southern coast of Korea. Algae 23: 75-81.

Clarke K.R. 1993. Nonparametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18: 117-143.

Clarke K.R., Warwick R.M. 2001. Change in marine communities: an approach to statistical analysis and interpretation. PRIMER-E Ltd. Plymouth, UK, 172 pp.

Cummins S.P., Roberts D.E., Ajani P., Underwood A.J. 2004. Comparisons of assemblages of phytoplankton between open water and seagrass habitats in a shallow coastal lagoon. Mar. Freshwater. Res. 55: 447-456.

Faust M.A. 1991. Morphology of ciguatera-causing Prorocentrum lima (Pyrrhophyta) from widely differing sites. J. Phycol. 27: 642-648.

Frankovich T.A., Zieman J.C. 1994. Total epiphyte and epiphytic carbonate production on Thalassia testudinum across Florida Bay. Bull. Mar. Sci. 54: 679-695.

Frankovich T.A., Armitage A.R., Wachnicka A., Gaiser E.E., Fourqurean J.W. 2009. Nutrient effects on seagrass epiphyte community structure in Florida Bay. J. Phycol. 45: 1010-1020.

Gambi M.C., Lorenti M., Russo G.F., Scipione M.B., Zupo V. 1992. Depth and seasonal distribution of some groups of the vagile fauna of the Posidonia oceanica leaf stratum- structural and trophic analyses. Mar. Ecol. 13: 17-39.

Giraud G. 1979. Sur une méthode de mesure et de comptage des structures foliaires de Posidonia oceanica (Linnaeus) Delile. Bull. Mus. Hist. nat. Marseille 39: 33-39.

Grasshoff K., Ehrhardt M., Kremling K. 1983. Methods of Seawater Analysis. Verlag Chemie GmbH, Weinheim, Germany, 419 pp.

Green E.P., Short F.T. 2003. World Atlas of Seagrasses. University of California Press, Berkeley, USA, 286 pp.

Harrison P.J., Clifored P.J., Cochlan W.P., Yin K., St. John M.A., Thompson P.A., Sibbald M.J., Albright L.J. 1991. Nutriment and plankton dynamics in the Frazer River Plume, Strait of Georgia, British Columbia. Mar. Ecol. Prog. Ser. 70: 291-304.

Hauxwell J., Cebrian J., Valiela I. 2003. Eelgrass Zostera marina loss in temperate estuaries: Relationship to land-derived nitrogen loads and effect of light limitation imposed by algae. Mar. Ecol. Prog. Ser. 247: 59-73.

Heck Jr. K.L., Valentine J.F. 2007. The primacy of top-down effects in shallow benthic ecosystems. Estuar. Coast 30: 371-381.

Hodgkiss I.J. 2001. The N:P ratio revisited. In: Ho, K.C., Wang, Z.D. (eds), Prevention and Management of Harmful Algal Blooms in the South China Sea. School of Science and Technology, the Open University of Hong Kong: 344-355.

Ierodiaconou D.A., Laurenson L.J.B. 2002. Estimates of Heterozostera tasmanica, Zostera muelleri and Ruppia megacarpa distribution and biomass in the Hopkins Estuary, Western Victoria, by GIS. Aust. J. Bot. 50: 215-228.

Jernakoff P., Nielsen J. 1997. The relative importance of amphipod and gastropod grazers in Posidonia sinuosa meadows. Aquat. Bot. 56: 183-202.

Jernakoff P., Brearley B., Nielsen J. 1996. Factors affecting grazer-epiphyte interactions in temperate seagrass meadows. Oceanogr. Mar. Biol. Ann. Rev. 34: 109-162.

Johnson M.P., Edwards M., Bunker F., Magg C.A. 2005. Algal epiphytes of Zostera marina: Variation in assemblage structure from individual leaves to regional scale. Aquat. Bot. 82: 12-26.

Kendrick G.A., Lavery P.S. 2001. Assessing biomass, assemblage structure and productivity of algal epiphytes on seagrasses. In: Short F.T., Coles R.G. (eds), Glogal Seagrass Research Methods. Elsevier, Amesterdam. pp. 199-222.

Lepoint G., Jacquemart J., Bouquegneau J.M., Demoulin V., Gobert S. 2007. Field measurements of inorganic nitrogen uptake by epiflora components of the seagrass Posidonia oceanica (Monocotyledons, Posidoniaceae). J. Phycol. 43: 208-218.

Leriche A., Boudouresque C.F., Bernard G., Bonhomme P., Denis J., 2004. A one-century suite of seagrass bed maps: can we trust ancient maps? Estuar. Coast. Shelf Sci. 59: 353-362.

Lin H.J., Nixon S.W., Taylor D.I., Granger S.L., Buckley B.A. 1996. Responses of epiphytes on eelgrass, Zostera marina L., to separate and combined nitrogen and phosphorus enrichment. Aquat. Bot. 52: 243-258.

Mabrouk L., Hamza A., Sahraoui H., Bradai M.N. 2009. Caractéristique et phénologie de l'herbier de Posidonia oceanica (L.) Delile sur les côtes de Mahdia (région est de la Tunisie). Bull. Inst. Nat. Sc. et Tech. d'Océanographie et de Pèche de Salammbo 36: 139-148.

Mabrouk L., Hamza A., Ben Brahim M., Bradai M.N. 2011. Seasonal and bathymetric variations of epiphytic microorganisms on Posidonia oceanica (L.) Delile leaves in Mahdia (Tunisia). Mar. Ecol. 32: 148-161.

Mabrouk L., Hamza A., Mahfoudi M., Bradai M.N. 2012. Spatial and temporal variations of epiphytic Ostreopsis siamensis on Posidonia oceanica (L.) Delile leaves in Mahdia (Tunisia). Cah. Biol. Mar. 53: 419-427.

Mabrouk L., Hamza A., Ben Brahim M., Bradai M.N. 2013. Variability in the structure of epiphyte assemblages on leaves and rhizomes of Posidonia oceanica in relation to human disturbances in a seagrass meadow off Tunisia. Aquat. Bot. 108: 33-40.

Mangialajo L., Bertolotto R., Cattaneo Vietti R., Chiantore M., Grillo C., Lemee R., Melchiorre C., Moretto P., Povero P., Ruggieri N. 2008. The toxic benthic dinoflagellate Ostreopsis ovata: Quantification of proliferation along the coastline of Genoa, Italy. Mar. Pollut. Bull. 56: 1209-1214. PMid:18381216

Marbà N., Santiago R., Dıaz-Almela E., Alvarez E., Duarte C.M. 2006. Seagrass (Posidonia oceanica) vertical growth as an early indicator of fish farm-derived stress. Estuar. Coast Shelf. Sci. 67: 475-483.

Marr J.C., Jackson A.E., McLachlan J.L. 1992. Occurrence of Prorocentrum lima, a DSP toxin-producing species from the Atlantic coast of Canada. J. Appl. Phycol., 4: 17-24.

Mazzella L., Russo G.F., 1989. Grazing effect of two Gibbula species (Mollusca, Archaeogastropoda) on the epiphytic community of Posidonia oceanica leaves. Aquat. Bot. 35: 357-373.

Mazzella L., Scipione M.B., Buia M.C. 1989. Spatio-temporal distribution of algal and animal communities in a Posidonia oceanica (L.) Delile meadow. Mar. Ecol. 10: 107-131.

Montefalcone M. 2009. Ecosystem health assessment using the Mediterranean seagrass Posidonia oceanica: a review. Ecol. Indic. 9: 595-604.

Montefalcone M., Chiantore M., Lanzone A., Morri C., Bianchi C.N., Albertelli G. 2008. BACI design reveals the decline of the seagrass Posidonia oceanica induced by anchoring. Mar. Pollut. Bull. 56: 1637-1645. PMid:18603267

Moore K.A., Wetzel R.L. 2000. Seasonal variations in eelgrass (Zostera marina L.) responses to nutrient enrichment and reduced light availability in experimental ecosystems. J. Exp. Mar. Biol. Ecol. 244: 1-28.

Morton S.L., Norris D.R., Bomber J.W. 1992. Effect of temperature, salinity and light intensity on the growth and seasonality of toxic dinoflagellates associated with ciguatera. J. Exp. Mar. Biol. Ecol. 157: 79-90.

Nakajima I., Oshima Y., Yasumoto T. 1981. Toxicity of benthic dinoflagellates in Okinawa. B. JPN. Soc. Sci. Fish. 47: 1029-1033.

Nascimento S.M., Purdie D.A., Morris S. 2005. Morphology, toxin composition and pigment content of Prorocentrum lima strains isolated from a coastal lagoon in southern UK. Toxicon 45: 633-649. PMid:15777960

Neckles H. A. 1993. The role of epiphytes in seagrass production and survival: Microcosm studies and simulation modelling. In: Morris L.J., Tomasko D.A. (eds), Proceedings and Conclusions of Workshops on: Submerged Aquatic Vegetation and Photosynthetically Active Radiation. Special Publication St Johns River Water Management District, Palatka, Florida, pp. 91-105.

Neckles H.A., Koepfler E.T., Haas L.W., Wetzel R.L., Orth R.J., 1994. Dynamics of epiphytic photoautotrophs and heterotrophs in Zostera marina (eelgrass) microcosms: responses to nutrient enrichment and grazing. Estuaries 17: 597-605.

Nesti U., Piazzi L., Balata D. 2009. Variability in the structure of epiphytic assemblages of the Mediterranean seagrass Posidonia oceanica in relation to depth. Mar. Ecol. 30 : 276-287.

ONAS. 2008. Etude de pré-investissement sur la dépollution du golfe de Tunis–Titre II: Caractérisation du golfe de Tunis Synthèse. Synthèse générale sur l'état du golfe de Tunis. 12 pp.

Orth R.J., Carruthers T.J.B., Dennison W.C., Duarte C.M., Fourqurean J.W., Heck Jr K.L., Hughes A.R., Kendrick G.A., Kenworthy W.J., Olyarnik S., Short F.T., Waycott M., Williams S.L. 2006. A global crisis for seagrass ecosystems. Bioscience 56: 987-996.[987:AGCFSE]2.0.CO;2

Pergent G., Pergent-Martini C., Boudouresque C.F. 1995. Utilisation de l'herbier à Posidonia oceanica comme indicateur biologique de la qualité du milieu littoral en Méditerranée: état des connaissances. Mésogée 54: 3-29.

Pergent-Martini C., 1994. Impact d'un rejet d'eaux usées urbaines sur l'herbier à Posidonia oceanica, avant et après la mise en service d'une station d'épuration. PhD thesis, University of Corsica, Corte, France, 191 pp.

Pergent-Martini C., Pergent G., 2000. Marine phanerogams as a tool in the evaluation of marine trace-metal contamination: an example from the Mediterranean. Int. J. Environ. Pollut. 13: 1-6.

Philippart C.J.M., Cadee G.C., Raaphorst W.V., Riegman R. 2000. Long-term phytoplankton-nutrient interactions in a shallow coastal sea: algal community structure, nutrient budgets, and denitrification potential. Limnol. Oceanogr. 45: 131-144.

Piazzi L., Balata D., Cinelli F., Benedetti-Cecchi L. 2004. Patterns of spatial variability in epiphytes of Posidonia oceanica. Differences between a disturbed and two reference locations. Aquat. Bot. 79: 345-356.

Prézelin B.B., Haxo F.T. 1976. Purification and characterization of peridinin- chlorophyll a-proteins from the marine dinoflagel lates Gleodinium sp. and Gonyaulax polyedra. Planta (Berl). 128: 133-141. PMid:24430688

Romdhane M.S., Eilertsen H.C., Yahia O.K.D., Yahia M.N.D., 1998. Toxic dinoflagellate blooms in Tunisian lagoons: causes and consequences for aquaculture. In: Reguera B., Blanco J., Fernandez M.L., Wyatt T. (eds), Harmful Algae. Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO, Vigo, pp. 80-83.

Ruiz J.M., Pérez M., Romero J., Tomas F. 2009. The importance of herbivory in the decline of a seagrass (Posidonia oceanica) meadow near a fish farm: an experimental approach. Bot. Mar. 52: 449-458.

Sarnelle O., Kratz K.W., Cooper S.D. 1993. Effects of an invertebrate grazer on the spatial arrangement of a benthic microhabitat. Oecologia 96: 208-218.

Shen Z.L. 2001. Historical changes in nutrient structure and its influences on phytoplantkon composition in Jiaozhou Bay. Estuar. Coast. Shelf Sci. 52: 211-224.

Sirota L., Hovel K.A. 2006. Eelgrass (Zostera marina) structural complexity: relative effects of shoot length, shoot density, and surface area on epifaunal community composition in San Diego Bay, California, USA. Mar. Ecol. Prog. Ser. 326: 115-131.

Smayda T.J., Borkman D.G., Beaugrand G., Belgrano A.G. 2004. Ecological effects of climate variation in the North Atlantic: phytoplankton. In: Stenseth N.C., Ottersen G., Hurrell J., Belgrano A. (eds), Ecological Effects of Climate Variations in the North Atlantic. Oxford Univ. Press, pp. 49-54.

Somerfield P.J., Clarke K.R., Olsgard F. 2002. A comparison of the power of categorical and correlational tests applied to community ecology data from gradient studies. J. Anim. Ecol. 71: 581-593.

Sournia, A. (ed.). 1978. Phytoplankton manual. Monogr. oceanogr. Methodol. Unesco 6: xvi-337 pp.

Tall L., Cattaneo A., Cloutier L., Dray S., Legendre P. 2006. Resource partitioning in a grazer guild feeding on a multilayer diatom mat. J. N. Am. Benthol. Soc. 25: 800-810.[0800:RPIAGG]2.0.CO;2

ter Braak C.J.F., Verdonschot P.F.M. 1995. Canonical correspondence analysis and related multivariate methods in aquatic ecology. Aquat. Sci. 57: 255-289.

Totti C., Accoroni S., Cerino F., Cucchiari E., Romagnoli T. 2010. Ostreopsis ovata bloom along the Conero Riviera (northern Adriatic Sea): Relationships with environmental conditions and substrata. Harmful Algae 9: 233-239.

Turki S. 2005. Distribution of toxic dinoflagellates along the leaves of seagrass Posidonia oceanica and Cymodocea nodosa from the Gulf of Tunis. Cah. Biol. Mar. 46: 29-34.

Underwood A.J. 1992. Beyond BACI: the detection of environmental impacts on populations in the real, but variable, world. J. Exp. Mar. Biol. Ecol. 161: 145-178.

UNEP/WHO 1996. Guidelines for submarine outfall structures for Mediterranean small and medium-sized coastal communities. MAP Technical Reports Series, 112. UNEP, Athens.

Utermöhl H. 1958. Zur vervollkommung der quantitativen Phytomicroorganisms-Methodik. Mitteilungen. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 9: 1-38.

Wear D.J., Sullivan M.J., Moore A.D., Millie D.F. 1999. Effects of water-column enrichment on the production dynamics of three seagrass species and their epiphytic algae. Mar. Ecol. Prog. Ser. 179: 201-213.

Zar J.H. 1999. Biostatistical analysis (Fourth ed.). Upper Saddle River, N.J. Prentice Hall, New Jersey, 663 pp.

Zieman J.C. 1989. Distribution, abundance and productivity of seagrasses and macroalgae in Florida Bay. Bull. Mar. Sci. 44: 292-311.

Copyright (c) 2014 Consejo Superior de Investigaciones Científicas (CSIC)

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

Contact us

Technical support