Variability patterns of epibenthic microalgae in eastern Tunisian coasts

Authors

DOI:

https://doi.org/10.3989/scimar.04651.17A

Keywords:

Prorocentrum lima, Ostreopsis cf. ovata, Coolia monotis, Prorocentrum micans, magnoliophytes, macroalgae

Abstract


Epiphytic microalgae were monitored on various substrates of seagrass and macroalgae and in the water column for one year (from March 2013 to March 2014) in Oued Lafrann along the eastern coast of Chebba (Tunisia) with a focus on the distribution patterns of the epibenthic toxic dinoflagellates Ostreopsis cf. ovata, Prorocentrum lima and Coolia monotis. Microalgae assemblages were dominated by diatoms and dinoflagellates both in the water column and on vegetation. High concentrations of epiphytic toxic and potentially toxic dinoflagellates were preferentially hosted by Posidonia leaves, mainly in the apical and middle regions of the leaves, and P. lima was the dominant species. A significant positive correlation was found between P. lima concentrations on Posidonia and in the water column, suggesting that macrophytes should be sampled in the framework of harmful algal species monitoring. Ostreopsis cf. ovata, exhibited low concentrations and was mainly present on the inner surface of the Posidonia leaf, whereas P. lima was mainly present on the outer surface of the leaf, suggesting a likely space competition.

Downloads

Download data is not yet available.

References

Abdennadher M. 2014. Étude taxonomique et écophysiologique des dinoflagellés toxiques du Golfe de Gabès: Alexandrium minutum, Prorocentrum lima, Coolia spp. and Ostreopsis ovata. Ph.D. thesis. Univ. Science. Sfax, Tunisia.

Accoroni S., Romagnoli T., Pichierri S., et al. 2014. New insights on the life cycle stages of the toxic benthic dinoflagellate Ostreopsis cf. ovata. Harmful Algae 34: 7-16. https://doi.org/10.1016/j.hal.2014.02.003

Accoroni S., Romagnoli T., Pichierri S., et al. 2016a. Effects of the bloom of harmful benthic dinoflagellate Ostreopsis cf. ovata on the microphytobenthos community in the northern Adriatic Sea. Harmful Algae 55: 179-190. https://doi.org/10.1016/j.hal.2016.03.003 PMid:28073531

Accoroni S., Romagnoli T., Penna A., et al. 2016b. Ostreopsis fattorussoi sp. nov. (Dinophyceae), a new benthic toxic Ostreopsis species from the eastern Mediterranean Sea. J. Phycol. 52: 1064-1084. https://doi.org/10.1111/jpy.12464 PMid:27633521

Aissaoui A., Amri Z., Akrout F., et al. 2014. Environmental factors and seasonal dynamics of Prorocentrum lima population in coastal waters of the Gulf of Tunis, South Mediterranean. Water. Environ. Res. 86: 2256-2270. https://doi.org/10.2175/106143014X13975035526266 PMid:25654928

Alcoverro T., Perez M., Romero J. 2004. Importance of within-shoot epiphyte distribution for the carbon budget of seagrasses: the example of Posidonia oceanica. Bot. Mar. 47: 307-312. https://doi.org/10.1515/BOT.2004.036

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. https://doi.org/10.1016/j.hal.2006.02.005

Aligizaki K., Nikolaidis G., Katikou P., et al. 2009. Potentially toxic epiphytic Prorocentrum (Dinophyceae) species in Greek coastal waters. Harmful Algae 8: 299-311. https://doi.org/10.1016/j.hal.2008.07.002

APHA. 1992. Standard methods for examination of water and waste water. APHA, AWWA. Washington, DC., USA.

Armi Z., Turki S., Trabelsi E., et al. 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. https://doi.org/10.1007/s10661-009-0903-z PMid:19404758

Ben Brahim M., Hamza A., Hannachi I., et al. 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. https://doi.org/10.1016/j.marenvres.2010.08.005

Ben Brahim M., Hamza A., Ben Ismail S., et al. 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. https://doi.org/10.1016/j.marpolbul.2013.01.024 PMid:23498657

Bomber J.W., Rubio M.G., Norris D.R. 1989. Epiphytism of dinoflagellates associated with the disease ciguatera: substrate specificity and nutrition. Phycologia 28: 360-368. https://doi.org/10.2216/i0031-8884-28-3-360.1

Borowitzka M.A., Lethbridge R.C. 1989. Seagrass epiphytes. In: Larkum A.W.D., McComb A.J., Shepherd S.A. (eds), Biology of Seagrasses. Elsevier, Amsterdam, pp. 304-345.

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, Dordrecht, pp. 441-461.

Calabretti C., Citterio S., Delaria M.A., et al. 2017. First record of two potentially toxic dinoflagellates in tide pools along the Sardinian coast. Biodiversity 18: 2-7. https://doi.org/10.1080/14888386.2017.1310058

Caye G., Meinesz A. 1985. Observations on the vegetative development, flowering and seeding of Cymodocea nodosa (Ucria) Ascherson on the Mediterranean coasts of France. Aquat. Bot. 22: 277-289. https://doi.org/10.1016/0304-3770(85)90005-1

Chessel D., Dufour A.B., Dray S., et al. 2012. Analysis of ecological data: Exploratory and euclidean methods in environmental sciences. R package version 1.5-1. http://CRAN.Rproject. org/package=ade4.

Clarke K.R., Warwick R.M. 2001. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. 2nd Edition, PRIMER-E, Plymouth, 172 pp.

Cohu S., Thibaut T., Mangialajo L., et al. 2011. Occurrences of the toxic dinoflagellate Ostreopsis cf. ovata in relation with environmental factors in Monaco (NW Mediterranean). Mar. Pollut. Bull. 62: 2681-2691. https://doi.org/10.1016/j.marpolbul.2011.09.022 PMid:22030108

Cohu S., Mangialajo L., Thibaut T., et al. 2013. Proliferations of the toxic dinoflagellate Ostreopsis cf. ovata in relation to depth, biotic substrate and environmental factors in North Western Mediterranean Sea. Harmful Algae 24: 32-44. https://doi.org/10.1016/j.hal.2013.01.002

Dauby P. 1989. The stable carbon isotope ratios in benthic food webs of the gulf of Calvi, Corsica. Contin. Shelf. Res. 9: 181-195. https://doi.org/10.1016/0278-4343(89)90091-5

David H., Kromkamp J.C., Orive E. 2017. Relationship between strains of Coolia monotis (Dinophyceae) from the Atlantic Iberian Peninsula and their sampling sites. J. Exp. Mar. Biol. Ecol. 487: 59-67. https://doi.org/10.1016/j.jembe.2016.11.014

Dolédec S., Chessel D. 1994. Co-inertia analysis: an alternative method for studying species: environment relationships. Freshw. Biol. 31: 277-293. https://doi.org/10.1111/j.1365-2427.1994.tb01741.x

Dumay O., Costa J., Desjobert J.M., et al. 2004. Variations in the concentration of phenolic compounds in the seagrass Posidonia oceanica under conditions of competition. Phytochemistry 65: 3211-3220. https://doi.org/10.1016/j.phytochem.2004.09.003 PMid:15643707

Fistarol G.O., Legrand C., Selander E., et al. 2004a. Allelopathy in Alexandrium spp.: effect on a natural plankton community and on algal monocultures. Aquat. Microb. Ecol. 35: 45-56. https://doi.org/10.3354/ame035045

Foden J., Purdie D.A., Morris S., et al. 2005. Epiphytic abundance and toxicity of Prorocentrum lima populations in the Fleet Lagoon, UK. Harmful Algae 4: 1063-1074. https://doi.org/10.1016/j.hal.2005.03.004

Frontier S. 1973. Etude statistique de la dispersion du zooplancton. J. Exp. Mar. Biol. Ecol. 12: 229-262. https://doi.org/10.1016/0022-0981(73)90056-7

Gambi M.C., Lorenti M., Russo G.F., et al. 1992. Depth and seasonal distribution of some groups of the vagile fauna of the Posidonia oceanica leaf stratum: structural and trophic analyses. PSZN I. Mar. Ecol. 13: 17-39. https://doi.org/10.1111/j.1439-0485.1992.tb00337.x

Gestoso I., Olabarria C., Troncoso J.S. 2010. Variability of epifaunal assemblages associated with native and invasive macroalgae. Mar. Freshw. Res. 61: 724-731. https://doi.org/10.1071/MF09251

Gray C.A., Otway N.M., Laurenson F.A., et al. 1992. Distribution and abundance of marine fish larvae in relation to effluent plumes from sewage outfalls and depth of water. Mar. Biol. 113: 549-559. https://doi.org/10.1007/BF00349698

Hallegraeff G.M. 2010a. Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge. J. Phycol. 46: 220-235. https://doi.org/10.1111/j.1529-8817.2010.00815.x

Hallegraeff G.M., Bolch C.J.S., Huisman J.M., et al. 2010b. Planktonic dinoflagellates. Algae of Australia phytoplankton of temperate coastal waters. CSIRO Publishing/ABRS. Melbourne, 145-212.

Hauxwell J., Cebrian J., Furlong C., et al. 2001. Macroalgal canopies contribute to eelgrass (Zostera marina) decline in temperate estuarine ecosystems. Ecology 82: 1007-1022. https://doi.org/10.1890/0012-9658(2001)082[1007:MCCTEZ]2.0.CO;2

Ingarao C., Lanciani G., Verri C., et al. 2009. First record of Prorocentrum lima (Dinophyceae) inside harbor areas and along the Abruzzo region coast, W Adriatic. Mar. Poll. Bull. 58: 596-600. https://doi.org/10.1016/j.marpolbul.2009.02.012

Johnson M.P., Edwards M., Bunker F., et al. 2005. Algal epiphytes of Zostera marina: Variation in assemblage structure from individual leaves to regional scale. Aquat. Bot. 82: 12-26. https://doi.org/10.1016/j.aquabot.2005.02.003

Kikuchi T., Peres J.M. 1977. Consumer ecology of seagrass beds. In: McRoy C.P., Helfferich C. (ed.) Seagrass ecosystems: a scientific perspective. Marcel Dekker, New York. pp. 147-194.

Koch E.W., Ackerman J.D., Verduin J., et al. 2006. Fluid dynamics in seagrass ecology, In: Larkum A.W.D., Orth R.J., Duarte C.M. (eds), Seagrasses: Biology, Ecology and Conservation, Springer, Amsterdam, The Netherlands, pp. 193-225.

Legendre P., Legendre L. 1998. Numerical ecology (2nd English Edn). Elsevier Science B.V., Amsterdam. 853 pp. PMCid:PMC107859

Levasseur M., Couture J.Y., Weise A.M., et al. 2003. Pelagic and epiphytic summer distributions of Prorocentrum lima and P. mexicanum at two mussel farms in the Gulf of St. Lawrence, Canada. Aquat. Microb. Ecol. 30: 283-293. https://doi.org/10.3354/ame030283

Lewis F.G. 1984. Distribution of macrobenthic crustaceans associated with Thalassia, Halodule, and bare sand substrata. Mar. Ecol. Prog. Ser. 19: 101-113. https://doi.org/10.3354/meps019101

Mabrouk L., Hamza A., Sahraoui H., et al. 2009. Caractéristique et phénologie de l'herbier de Posidonia oceanica (L.) Delile sur les cotes de Mahdia (région est de la Tunisie). Bull. Inst. Nat. Sci. Tech. Océan. Pêche Salammbô. 36: 139-148.

Mabrouk L., Hamza A., Ben Brahim M., et al. 2011. Temporal and depth distribution of microepiphytes on Posidonia oceanica (L.) Delile leaves in a meadow off Tunisia. Mar. Ecol. 32: 148-161. https://doi.org/10.1111/j.1439-0485.2011.00432.x

Mabrouk L., Ben Brahim M., Hamza A., et al. 2014. Temporal and spatial zonation of macroepiphytes on Posidonia oceanica (L.) Delile leaves in a meadow off Tunisia. Mar. Ecol. 36: 77-92. https://doi.org/10.1111/maec.12118

Mangialajo L., Bertolotto R., Cattaneo-Vietti R., et al. 2008. The toxic benthic dinoflagellate Ostreopsis ovata: quantification of proliferation along the coastline of Genoa, Italy. Mar. Poll. Bull. 56: 1209-1214. https://doi.org/10.1016/j.marpolbul.2008.02.028

Mangialajo L., Ganzin N., Accoroni S., et al. 2011. Trends in Ostreopsis proliferation along the Northern Mediterranean coasts. Toxicon 57: 408-420. https://doi.org/10.1016/j.toxicon.2010.11.019 PMid:21145339

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. https://doi.org/10.1007/BF00003956

Maso M., Garcés E. 2006. Harmful microalgae blooms (HAB); problematic and conditions that induce them. Mar. Pollut. Bull. 53: 620-630. https://doi.org/10.1016/j.marpolbul.2006.08.006 PMid:17010385

Mazzella L., Buia M.C., Spinoccia L. 1994. Biodiversity of epiphytic diatom community on leaves of Posidonia oceanica. In: Marino D. and Montresor M. (eds), Proceedings of the 13th Diatom Symposium, Biopress, Bristol, UK.

Mirella P.C.V., Brendan P.K., Melanie J.B., et al. 2012. Epiphyte grazing enhances productivity of remnant seagrass patches. Aust. Ecol. 37: 885-892. https://doi.org/10.1111/j.1442-9993.2011.02332.x

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. https://doi.org/10.1111/j.1439-0485.2008.00275.x

Pagliara P., Caroppo C. 2012. Toxicity assessment of Amphidinium carterae, Coolia cfr. monotis and Ostreopsis cfr. ovata (Dinophyta) isolated from the northern Ionian Sea (Mediterranean Sea). Toxicon 60: 1203-1214. https://doi.org/10.1016/j.toxicon.2012.08.005 PMid:22925842

Parsons M.L., Preskitt L.B. 2007. A survey of epiphytic dinoflagellates from the coastal waters of the island of Hawaii. Harmful Algae 6: 658-669. https://doi.org/10.1016/j.hal.2007.01.001

Peirano A., Cocito S., Banfi V., et al. 2011. Phenology of the Mediterranean seagrass Posidonia oceanica (L.) Delile: medium and long-term cycles and climate inferences. Aquat. Bot. 94: 77-92. https://doi.org/10.1016/j.aquabot.2010.11.007

Perez M., Garcia T., Invers O., et al. 2008. Physiological responses of the seagrass Posidonia oceanica as indicators of fish farm impact. Mar. Pollut. Bull. 56: 869-879. https://doi.org/10.1016/j.marpolbul.2008.02.001 PMid:18334257

Richlen M.L., Lobel P.S. 2011. Effects of depth, habitat, and water motion on the abundance and distribution of ciguatera dinoflagellates at Johnston Atoll, Pacific Ocean. Mar. Ecol. Prog. Ser. 421: 51-66. https://doi.org/10.3354/meps08854

Rizvi S.J.H., Rizvi V. 1992. Allelopathy: basic and applied aspect. Chapman & Hall, London, 480 pp. https://doi.org/10.1007/978-94-011-2376-1

Romagnoli T., Bavestrello G., Cucchiari E., et al. 2007. Microalgal communities epibiontic on the marine hydroid Eudendrium racemosum in the Ligurian Sea, during an annual cycle. Mar. Biol. 151: 537-552. https://doi.org/10.1007/s00227-006-0487-x

R-Development Core Team. 2006. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

Sugg L.M., VanDolah F.M. 1999. No evidence for an allelopathic role of okadaic acid among ciguatera-associated dinoflagellates. J. Phycol. 35: 93-103. https://doi.org/10.1046/j.1529-8817.1999.3510093.x

Tindall D.R., Morton S.L. 1998. Community dynamics and physiology of epiphytic/benthic dinoflagellates associated with ciguatera. In: Anderson D.M., Cembella A.D., Hallegraeff G.M. (eds), Physiological Ecology of Harmful Algal Blooms, NATO ASI Series G41. Springer-Verlag, Berlin. pp. 293-313.

Totti C., Poulin M., Romagnoli T., et al. 2009. Epiphytic diatom communities on intertidal seaweeds from Iceland. Polar Biol. 32: 1681-1691. https://doi.org/10.1007/s00300-009-0668-4

Totti C., Accoroni S., Cerino F., et al. 2010. Ostreopsis ovata bloom along the Conero Riviera (northern Adriatic Sea): relationships with environmental conditions and substrata. Harmful Algae 9: 233-239. https://doi.org/10.1016/j.hal.2009.10.006

Trautman D.A., Borowitzka M.A. 1999. Distribution of the epiphytic organisms on Posidonia australis and P. sinuosa, two seagrasses with differing leaf morphology. Mar. Ecol. Prog. Ser. 179: 215-229. https://doi.org/10.3354/meps179215

Underwood A.J. 1997. Experiments in ecology. Their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge. 504 pp.

Utermohl H. 1958. Zur Vervollkommung der quantitativen Phytomicroorganisms-Methodik. Mitt. Int. Ver. Theor. Angew. Limnol. 9: 1-38.

Van Dolah F. 2000. Marine algal toxins. Env. Health Persp. 108: 133-141. https://doi.org/10.1289/ehp.00108s1133 PMid:10698729 PMCid:PMC1637787

Published

2017-12-30

How to Cite

1.
Moncer M, Hamza A, Feki-Sahnoun W, Mabrouk L, Bel Hassen M. Variability patterns of epibenthic microalgae in eastern Tunisian coasts. Sci. mar. [Internet]. 2017Dec.30 [cited 2024Mar.29];81(4):487-98. Available from: https://scientiamarina.revistas.csic.es/index.php/scientiamarina/article/view/1732

Issue

Section

Articles