Phytoplankton response to high salinity and nutrient  limitation in the eastern Adriatic marine lakes

Marina Carić; Nenad Jasprica; Marijeta Čalić; Mirna Batistić

doi:10.3989/scimar.2011.75n3493

Authors

Marina Carić Institute for Marine and Coastal Research, University of Dubrovnik
Nenad Jasprica Institute for Marine and Coastal Research, University of Dubrovnik
Marijeta Čalić Institute for Marine and Coastal Research, University of Dubrovnik
Mirna Batistić Institute for Marine and Coastal Research, University of Dubrovnik

DOI:

https://doi.org/10.3989/scimar.2011.75n3493

Keywords:

phytoplankton, hydrography, nutrients, eutrophication, marine lakes, Adriatic Sea

Abstract

Phytoplankton and physical-chemical parameters were investigated for the first time in the only natural hyperhaline marine lakes (salinity > 40) along Croatia’s Adriatic coast, Mala Solina and Velika Solina. Two periods were recognized during the one-year investigation: one euhaline-mesotrophic from December to May and one hyperhaline- eutrophic from June to November. Nutrient limitation appears to have been important in defining the lakes’ seasonal phytoplankton composition. Phosphate was most likely limiting from October to December, silicate from January to April, and nitrogen from June to September when nitrate was depleted. Diatoms were most abundant in November to January, when temperature and salinity were low and nitrate and ammonium were high. They collapsed in March when silicate was depleted. Amphora, Navicula, and other naviculoid diatoms were the most frequent genera. Nitzschia longissima was the most abundant species. Dinoflagellate dominance began in June in Mala Solina and in March in Velika Solina. It continued while temperature, salinity, phosphate, and silicate were high. Oxyrrhis marina was the most abundant dinoflagellate (3.2 x 10⁶ cells L^-1). Nanophytoplankton was the dominant size fraction. Chroococoid cyanobacteria were most abundant from May to October, reaching 2.9 x 10⁷ cells L^-1 in July. Both nanophytoplankton and small microphytoplankton, such as Oxyrrhis, Scrippsiella, and Tetraselmis, were most abundant under hyperhaline, N-depleted conditions. Toxic and harmful taxa (e.g. Alexandrium, Dinophysis), expanding in Mediterranean waters, were not recorded in the lakes.

Downloads

Download data is not yet available.

References

Abid, O., A. Sellami-Kammoun, H. Ayadi, Z. Drira, A. Bouain and L. Aleya. – 2008. Biochemical adaptation of phytoplankton to salinity and nutrient gradients in a coastal solar saltern, Tunisia. Estuar. Coast. Shelf Sci., 80(3): 391-400. PMid:11893642

Andersson, A., P. Haecky and A. Hagstrom. – 1994. Effect of temperature and light on the growth of micro-nano- and pico-plankton: impact on algal succession. Mar. Biol., 120(4): 511-520. PMid:10638155

Anonymous. – 1959. Final resolution of the symposium on the classification of brackish waters. In: B. Battaglia (ed.), Arch. Oceanogr. Limnol., 11(Suppl.): 243-248.

Ayadi, H., O. Abid, J. Elloumi, A. Bouaïn and T. Sime-Ngando. – 2004. Structure of the phytoplankton communities in two lagoons of different salinity in the Sfax saltern (Tunisia). J. Plankton Res., 26(6): 669-679. PMid:8617138

Bérard-Therriault, L., M. Poulin and L. Bossé. – 1999. Guide d’identification du phytoplankton marin de l’estuaire et du golfe du Saint-Laurent. Les presses scientifiques du CNRC, Ottawa.

Blondel, J. and J. Aronson. – 1999. Biology and Wildlife of the Mediterranean Region. Oxford University Press, Oxford-New York.

Bode, A. and Q. Dorch. – 1996. Uptake and regeneration of inorganic nitrogen in coastal waters influenced by the Mississippi River: spatial and seasonal variations. J. Plankton Res., 18(12): 2251-2268

Bonacci, O. – 1996. Značaj meteoroloških podataka sakupljenih na Palagruži za bilancu voda Jadranskog mora. In: M. Hodžić (ed.), Zbornik radova Simpozija “Palagruža-jadranski dragulj”, pp. 287-291. DHMZ, Split.

Bonilla, S., D. Conde, L. Aubriot, and M. del C. Pérez. – 2005. Influence of Hydrology on Phytoplankton Species Composition and Life Strategies in a Subtropical Coastal Lagoon Periodically Connected with the Atlantic Ocean. Estuaries, 28(6): 884-895. PMid:16759404 PMCid:1459267

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

Bravo, I., M. Vila, M. Masó, R.I. Figueroa and I. Ramilo. – 2008. Alexandrium catenella and Alexandrium minutum blooms in the Mediterranean Sea: Toward the identification of ecological niches. Harmful Algae, 7(4): 515-522. PMid:16300270

Brzezinski, M.A. – 1985. The Si:C:N ratio of marine diatoms: interspecific variability and the effect of some environmental variables. J. Phycol., 21(3): 347-357. PMid:12938612

Carić, M. and N. Jasprica. – 1998. Seasonal variability of nutrient and chlorophyll a concentrations in the karstic coastal lake Veliko jezero (Mljet island, Adriatic Sea). In: B. Frederic (ed.). Rapport du 37 e Congrès de la CIESM, pp. 238-239. CIESM, Mónaco.

Carić, M. and N. Jasprica. – 2005. Resource ratios and phytoplankton in the marine Lake Vlaška (NE Mediterranean). In: E. Ozhan (ed.), Proceeding of the Seventh International Conference on the Mediterranean Coastal Environment, MEDCOAST 05, pp. 541-546. Middle East Technical University, Ankara.

Carlsson, P. and E. Granéli. – 1999. Effects of N:P:Si ratios and zooplankton grazing on phytoplankton communities in the northern Adriatic Sea. II. Phytoplankton species composition. Aquat. Microb. Ecol., 18: 55-65.

Ciglenečki, I., M. Carić, F. Kršinić, D. Viličić and B. Ćosović. – 2005. The extinction by sulfide turnover and recovery of a naturally eutrophic, meromitic seawater lake. J. Mar. Syst., 56: 29-44. PMid:8286833

Clarke, K.R. and R.N. Gorley. – 2001. Primer v5: user manual/tutorial. PRIMER-E Ltd, Plymouth.

Clarke, K.R. and R.M. Warwick. – 2001. Change in marine communities: an approach to statistical analysis and interpretation, 2nd edition. PRIMER-E Ltd, Plymouth.

Council Directive 92/43/EEC of 21 May. – 1992. Conservation of natural habitats and of wild fauna and flora. Official Journal L, 206: 07-50.

Cupp, E.E. – 1943. Marine plankton diatoms of the west coast of North America. Bull. Scripps Inst. Oceonog., 5(1):1-238. University of California Press. PMid:15974242

Cushman-Roisin, B., K.A. Korotenko, C.E. Galos and D.E. Dietrich. – 2007. Simulation and characterization of the Adriatic Sea mesoscale variability. J. Geophys. Res., 112, C03S14.

Čalić, M., M. Carić and N. Jasprica. – 2007. Hydrography and planktonic diatoms in the marine lake Mir (eastern Adriatic sea, Croatia). Rapports du 38e Congrès de la CIESM, p. 354. CIESM, Mónaco.

Domijan, N. (ed.). – 2006. Izvješće o mareografskim mjerenjima na istočnoj obali Jadrana. Hrvatski hidrografski institut, Split.

Dorth, Q. and T.E. Whitledge. – 1992. Does nitrogen or silicon limit phytoplankton production in the Mississippi River plume and nearby regions? Cont. Shelf Res., 12(11): 1293-1309.

Elloumi, J., J.-F. Carrias, H. Ayadi, T. Sime-Ngando and A. Bouain. – 2009. Communities structure of the planktonic halophiles in the solar saltern of Sfax, Tunisia. Estuar. Coast. Shelf Sci., 81(1): 19-26.

Eppley, R.W., J.N. Rogers and J.J. McCarthy. – 1969. Half-saturation constants for uptake of nitrate and ammonium by marine phytoplankton. Limnol. Oceanogr., 14: 912-920.

Escaravage, V., T.C. Prins, A.C. Smaal and J.C.H. Peeters. – 1996. The response of phytoplankton communities to phosphorus input reduction in mesocosm experiments. J. Exp. Mar. Biol. Ecol., 198(1): 55-79.

Evagelopoulos, A., E. Spyrakos and D. Koutsoubas. – 2007. The biological system of the lower salinity ponds in Kalloni Saltworks (NE. Aegean Sea, Greece): phytoplankton and macrobenthic invertebrates. Transit. Waters Bull., 3: 23-25.

Evagelopoulos, A., E. Spyrakos and D. Koutsoubas. – 2009. Phytoplankton and macrofauna in the low salinity ponds of a productive solar saltworks: spatial variability of community structure and its major abiotic determinants. Global NEST J., 11 (2): 64-72.

Facca, C. and A. Sfriso. – 2007. Epipelic diatom spatial and temporal distribution and relationship with the main environmental parameters in coastal waters. Estuar. Coast. Shelf. Sci., 75: 35-49.

Fisher, T.R., L.W. Harding, D.W. Stanley and L.G. Ward. – 1988. Phytoplankton, nutrients and turbidity in the Chesapeake, Delaware and Hudson estuaries. Estuar. Coast. Shelf Sci., 27(1): 61-93.

Goldman, J.C., M.R. Dennett and H. Gordin. – 1989. Dynamics of herbivorous grazing by the heterotrophic dinoflagellate Oxyrrhis marina. J. Plankton Res., 11: 391-407.

Granéli, E., P. Carlsson, J.T. Turner, P.A. Tester, C. Béchemin, R. Dawson and E. Funari. – 1999. Effects of N:P:Si ratios and zooplankton grazing on phytoplankton communities in the northern Adriatic Sea. I. Nutrients, phytoplankton biomass, and polysaccharide production. Aquat. Microb. Ecol., 18: 37-54.

Hansen, P.J. – 1991. Quantitative importance and trophic role of heterotrophic dinoflagellates in a coastal pelagial food web. Mar. Ecol. Prog. Ser., 73: 253-261.

Hansen, F.C., H.J. Witte and J. Passarge. – 1996. Grazing in the heterotrophic dinoflagellate Oxyrrhis marina: size selectivity and preference for calcified Emiliania huxleyi cells. Aquat. Microb. Ecol., 10: 307-313.

Heil, C.A., P.M. Glibert and C. Fan. – 2005. Prorocentrum minimum (Pavillard) Schiller - a review of a harmful algal bloom species of growing worldwide importance. Harmful Algae, 4 (3): 449-470.

Holm-Hansen, O., C.J. Lorenzen, R.W. Holmes and J.D.H. Strickland. – 1965. Fluorometric determination of chlorophyll. J. Conseil., 301: 3-15.

Horner, R.A. – 2002. A Taxonomic Guide to some Common Marine Phytoplankton. Biopress Ltd., Bristol.

Hustedt, F. – 1930. Die Kieselalgen Deutschlands, Österreichs und der Schweiz mit Berücksichtigung der übrigen Länder Europas sowie der angrenzenden Meeresgebeite. Rabenhorst‘s Kryptogramen- Flora von Deutschland, Österreich und der Schweiz, Band VII. Akademische Verlagsgesellschaft m. b. H., Leipzig.

Ignatiades, L. and O. Gotsis-Skretas. – 2010. A Review on Toxic and Harmful Algae in Greek Coastal Waters (E. Mediterranean Sea). Toxins, 2: 1019-1037.

Irwin, A.J., Z.V. Finkel, O.M.E. Schofield and P.G. Falkowski. – 2006. Scaling-up from nutrient physiology to the size-structure of phytoplankton communities. J. Plankton Res., 28: 459-471.

Jaccard, P. – 1908. Nouvelle recherches sur ladistribution florale. Bull. Soc. Vaud. Sci. Nat., 44: 223-270.

Jasprica, N., D. Viličić, M. Carić and J. Njire. – 1995. Fitoplankton u Malom i Velikom jezeru (otok Mljet, južni Jadran). In: P. Durbešić and A. Benović (eds.), Zbornik radova sa simpozija Prirodne značajke i društven valorizacija otoka Mljeta, pp. 454-463. Hrvatsko ekološko društvo, Državna uprava za zaštitu kulturne i prirodne baštine, Nacionalni park Mljet.

Jasprica, N. and M. Carić. – 1997. A comparison of phytoplankton biomass estimators and their environmental correlates in the Mali Ston Bay (Southern Adriatic). Mar. Ecol., 18(1): 35-50.

Jasprica, N. and M. Carić. – 2001. Planktonic diatoms and their relation to environmental factors at three stations in the Southern Adriatic, Mediterranean Sea. In: R. Jahn, J.P. Kociolek, A. Witkowski and P. Compère (eds.), Lange-Bertalot-Festschrift: Studies on Diatoms, pp. 517-536. Gantner, Ruggell.

Jasprica N. and M. Carić. – 2003. Mikrofitoplankton u jezeru Vlaška. In: P. Marijanović (ed.), Zbornik radova znanstveno-stručnog simpozija Voda u kršu slivova Cetine, Neretve i Trebišnjice, pp. 575-579. Sveučilište u Mostaru, Bosna i Hercegovina.

Jasprica, N., M. Carić and F. Kršinić. – 2005. Plankton and nutrients in Lake Vlaška (Neretva River estuary, SE Adriatic Sea). In: P. Wassmann and B. Ćosović (eds.), Book of Extended Abstracts of the Symposium “Eutrophication in the coastal zone of the eastern Adriatic Sea”, pp. 33-35. Norwegian Research Council, South-eastern Europe Programme Symposium.

Johnson, R.K and T. Wiederholm. – 1992. Pelagic - benthic coupling - the importance of diatom interannual variability for population oscillations of Monoporeia affinis. Limnol. Oceanogr., 37(8): 1596-1607.

Karydis, M. – 2009. Eutrophication assessment of coastal waters based on indicators: a literature review, Global NEST J., 11(4): 373-390.

Kemp, W.M. and W.R. Boynton. – 1984. Spatial and temporal coupling of nutrient inputs to estuarine primary production: the role of particulate transport and decomposition. Bull. Mar. Sci., 35(3): 522-535.

Kofoid, C.A. and O. Swezy. – 1921. The free-living unarmored dinoflagellata. University of California Press, Barkley.

Kršinić, F., M. Carić, D. Viličić and I. Ciglenički. – 2000. The calanoid copepod Acartia italica Steuer, phenomenon in the small saline lake Rogoznica (Eastern Adriatic coast). J. Plankton Res., 22(8): 1441-1464.

Lee, R.E. – 1999. Phycology. Cambridge University Press, Cambridge.

Longhurst, A.R. – 1998. Ecological Geography of the Sea. Academic Press, San Diego.

Margalef, R. – 1965. Composición y distribución del fitoplancton. Mem. Fund. La Salle Cienc. Nat., 25: 141-205.

Margalef, R. – 1978. Life-forms as survival alternatives in an unstable environment. Oceanol. Acta, 1: 493-509.

Margalef, R. – 1983. Limnologia. Editorial Omega, Barcelona.

McQuoid, M.R. and A. Godhe. – 2004. Recruitment of coastal planktonic diatoms from benthic versus pelagic cells: Varia tions in bloom development and species composition. Limnol. Oceanogr., 49(4): 1123-1133.

Miller-Way, T. and R.R. Twilley. – 1996. Theory and operation of continuous flow systems for the study of benthic-pelagic coupling. Mar. Ecol. Prog. Ser., 140: 257-269.

Morais, P., M.A. Chícharo and A. Barbosa. – 2003. Phytoplankton dynamics in a coastal saline lake (SE Portugal). Acta Oecol., 24 (Suppl.1): 87-96.

Morel, F.M.M., R.J.M. Hudson and N.M. Price. – 1991. Limitation of productivity by trace metals in the sea. Limnol. Oceanogr., 36(8): 1742-1755.

Nikolić, D. – 2000. Bilten iz područja meteorologije, hidrologije, primjenjene meteorologije i zaštite čovjekova okoliša 1-12/2000. Državni hidrometeorološki zavod, Zagreb.

Nicolaidou, A., S. Reizopoulou, D. Koutsoubas, S. Orfanidis and T. Kevrekidis. – 2005. Biological components of greek lagoonal ecosystems: an overview. Medit. Mar. Sci. 6(2): 31-50. Olujić, G. – 2007. Comparison of hydrographic properties of the Zrmanja and the Krka estuaries. MSc thesis, University of Zagreb.

Patil, J.S. and A.C. Anil. – 2005. Influence of diatom exopolymers and biofilms on metamorphosis in the barnacle Balanus amphitrite. Mar. Ecol. Prog. Ser., 301: 231-245.

Pavlova, P., K. Markova, S. Tanev and J.S. Davis. – 1998. Observation on a solar saltworks near Burgas, Bulgaria. Int. J. Salt Lake Res., 7(4): 357-368.

Polat, S., E. Sarihan and T. Koray. – 2000. Seasonal changes in the phytoplankton of the northeastern Mediterranean (Bay of Iskenderun). Turk. J. Bot., 24: 1-12.

Quintana, X.D. and R. Moreno-Amich. – 2002. Phytoplankton composition of Empordà salt marshes, Spain and its response to freshwater flux regulation. J. Coast. Res. (spec. issue), 36: 581-590.

Raghukumar, S. and A.C. Anil. – 2003. Marine biodiversity and ecosystem functioning: A perspective. Curr. Sci., 84(7): 884-982.

Redfield, A.C., B.H. Ketchum and A. Richards. – 1963. The influence of organisms on the composition of sea water. In: M. M. Hill (ed.), The sea, vol. 2, pp. 26-77. Interscience, New York.

Reynolds, C.S. – 1997. Vegetation Processes in the Pelagic: A Model for Ecosystem theory. Ecology Institute, Oldendorf/Luhe, Germany.

Reynolds, C.S. – 2006. The Ecology of Phytoplankton. Cambridge University Press, Cambridge.

Rocha, C., H. Galvão and A. Barbosa. – 2002. Role of transient silicon limitation in the development of cyanobacteria blooms in the Guadiana estuary, south-western Iberia. Mar. Ecol. Prog. Ser., 228: 35-45. http://dx.doi.org/10.3354/meps228035

Sakka Hlaili, A. and B. El Grami. – 2004. Rôle trophique des protozoaires dans la lagune de Bizerte (Côte Nord de la Tunisie). Rapports du 37e Congrès de la CIESM, p. 546. CIESM, Mónaco.

Sakka Hlaili, A., M.-A. Chikhaoui, B. El Grami and H. Hadj Mabrouk.– 2006. Effects of N and P supply on phytoplankton in Bizerte Lagoon (western Mediterranean). J. Exp. Mar. Biol. Ecol., 333(1): 79-96. http://dx.doi.org/10.3354/meps228035

Sakka Hlaili, A., B. Grami, H. Hadj Mabrouk, M. Gosselin and D. Hamel. – 2007. Phytoplankton growth and microzooplankton grazing rates in a restricted Mediterranean lagoon (Bizerte Lagoon, Tunisia). Mar. Biol., 151(2): 767-783. http://dx.doi.org/10.1007/s00227-006-0522-y

Saracino, O.D. and F. Rubino. – 2006. Phytoplankton composition and distribution along the Albanian coast, South Adriatic Sea. Nova Hedwigia, 83(1-2): 253-266. http://dx.doi.org/10.1127/0029-5035/2006/0083-0253

Schiller, J. – 1933. Dinoflagellatae (Peridineae) in monographischer Behandlung. 1. Teil. Rabenhorst‘s Krypotgamen-Flora von Deutschland, Österreich un der Schweiz. Akademische Verlagsgesellshaft M.B.H., Leipzig.

Schiller, J. – 1937. Dinoflagellatae (Peridineae) in monographischer Behandlung. 2. Teil. Rabenhorst‘s Kryptogamen-Flora von Deutschland, Österreich un der Schweiz. Akademische Verlagsgesellschaft M. B. H., Leipzig.

Schreurs, H. – 1992. Cyanobacterial dominance. Relations to eutrophication and lake morphology. PhD thesis. University of Amsterdam.

Schumann, R., B. Munzert, J.-U. Wuensch and H.-P. Spittler. – 1994. The feeding biology of Oxyrrhis marina Dujardin (Flagellata). Limnologica, 24(1): 29-34.

Schumann, R. and U. Karsten. – 2006. Phytoplankton im Zingster Strom der Darβ-Zingster Boddenkette – 13 Yahre Remesotrophierung. Rostock. Meeresbiol. Beitr., 16: 47-59.

Smayda, T.J. – 1980. Phytoplankton species successions. In: I. Morris (ed.), The Physiological Ecology of Phytoplankton, pp. 493-570. University of California Press, Berkeley.

Smayda, T.J. and C.S. Reynolds. – 2001. Community assembly in marine phytoplankton: application of recent models to harmful dinoflagellate blooms. J. Plankton Res., 23(5): 447–461.

Sommer, U. – 1994. Planktologie. Springer-Verlag, Berlin.

Sournia, A. – 1986. Atlas du phytoplankton marin. Vol. I: Introduction, Cyanophycées, Dictyochophycées, Dinophycées et Raphidophycées. Éditions du CNRS, Paris.

Steiner, R.Y., R. Kunisawa, M. Mandel and G. Cohen-Bazire. – 1971. Purification and properties of unicellular blue-green algae (Order Chroococcales). Bacteriol. Rev., 35(2): 171-205. PMid:4998365 PMCid:378380

Strickland, J.D.H. and T.R. Parsons. – 1972. A practical handbook of seawater analysis. J. Fish. Res. Board. Can., 167: 1-310.

Tomas, C.R. (ed.). – 1993. Marine Phytoplankton: A Guide to Naked Flagellates and Coccolithophorids. Academic Press, London.

Tomas, C.R. (ed.). – 1996. Identifying marine diatoms and dinoflagellates. Academic Press, Inc., San Diego.

Totti, C., G. Civitarese, F. Acri, D. Barletta, G. Candelari, E. Paschini and A. Solazzi. – 2000. Seasonal variability of phytoplankton populations in the middle Adriatic sub-basin. J. Plankton Res., 22(9): 1735-1756. http://dx.doi.org/10.1093/plankt/22.9.1735

UNESCO. – 1973. International oceanographic tables, Volume 2. National Institute of Oceanography of Great Britain and UNESCO, Paris.

Utermöhl, H. – 1958. Zur Vervollkommnung der quantitativen Phytoplankton-Metodik. Mitt. Int. Ver. Theor. Angew. Limnol., 9: 1-38.

Viličić, D. – 1989. Phytoplankton population density and volume as indicators of eutrophication in the eastern part of the Adriatic Sea. Hydrobiologia, 174:117-132. http://dx.doi.org/10.1007/BF00014060

Vollenweider, R.A., F. Giovanardi, G. Montanari and A. Rinaldi. – 1998. Characterization of the trophic conditions of marine coastal waters with special reference to the NW Adriatic Sea: proposal for a trophic scale, turbidity and generalized water quality index. Environmetrics, 9: 329-357. http://dx.doi.org/10.1002/(SICI)1099-095X(199805/06)9:3<329::AID-ENV308>3.0.CO;2-9

Weiss, R.F. – 1970. The solubility of nitrogen, oxygen and argon in water and seawater. Deep Sea Res., 17: 721-735.

Yamada, S.S. and C.F. D’Elia. – 1984. Silicic-Acid Regeneration from Estuarine Sediment Cores. Mar. Ecol. Prog. Ser., 18: 113-118. http://dx.doi.org/10.3354/meps018113

Yin, K., P.Y. Quian, M.C.S. Wu, J.C. Chen, L.M. Huang, X. Song and W.J. Jian. – 2001. Shift from P to N limitation of phytoplankton biomass across the Pearl River estuarine plume during summer. Mar. Ecol. Prog. Ser., 221: 17-28. http://dx.doi.org/10.3354/meps221017