Academic Scientific JournalsSize-fractionated chlorophyll a and phycocyanin temporal variations in a highly eutrophic lake and its isolated karstic springs
Keywords:
photosynthetic pigments, size fraction, primary producers, eutrophy, hypereutrophy, Lake Pamvotis, man-made lakeAbstract
Monthly variations of size-fractionated chlorophyll a and phycocyanin were studied in Lake Pamvotis between August 2016 and January 2017. Sampling was conducted at two sampling sites: in the main lake (Site 1: Lake) and in an adjacent man-made water ski lake with karstic springs (Site 2: Springs). Samples were fractionated into three size classes: 0.2–2 um (pico), 2–20 um (nano) and 20–180 um (micro). According to chlorophyll a values, eutrophic to hypereutrophic conditions prevail at Site 1 and oligotrophic to mesotrophic conditions – at Site 2. Similarly, Site 1 was distinguished by higher concentration of phycocyanin compared to Site 2. Fractionated chlorophyll a showed monthly variations at Site 1 with alternations in the dominance between the two larger fractions. The maximum of the 0.2–2 um fraction was observed in October but it contributed less to the total chlorophyll a content than nano- or microphytoplankton. Its contribution was higher at Site 2, reaching occasionally ~ 40% of the bulk chlorophyll a. However, nanophytoplankton was the fraction found to respond faster when disturbances occurred. At Site 1, phycocyanin correlated well with total chlorophyll a as well as with the micro- and nanophytoplankton fractions, indicating that cyanobacteria represent an important component of the large-sized phytoplankton in Lake Pamvotis.
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Agawin, N.S.R., Duarte, C.M. & Agustí, S. (2000). Nutrient and temperature control of the contribution of picoplankton to phytoplankton biomass and production. Limnol. Oceanogr. 45: 591–600. DOI: 10.4319/lo.2000.45.8.1891a.
Agustí, S. & Duarte, C.M. (2013). Phytoplankton lysis predicts dissolved organic carbon release in marine plankton communities. Biogeosciences 10: 1259–1264. DOI: 10.5194/bg-10-1259-2013.
Albanis, T., Pomonis, P. & Sdoukos, A. (1986). Seasonal fluctuation of organochlorine and triazines pesticides in the aquatic system of Ioannina basin (Greece). Sc. of Total Environment 58: 243–253. DOI: 10.1016/0048-9697(86)90204-4.
Andersson, A., Haecky, P. & Hagström, Å. (1994). Effect of temperature and light on the growth of micro- nano- and pico-plankton: impact on algal succession. Marine Biology 120: 511. DOI: 10.1007/BF00350071.
Azam, F., Fenchel, T., Field, J.G., Gray, J.S., Meyer-Reil, L.A. et al. (1983). The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10: 257–263. DOI: 10.3354/meps010257.
Bell, T. & Kalff, J. (2001).The contribution of picophytoplankton in marine and freshwater systems of different trophic status and depth. Limnol. Oceanogr. 46(5): 1243–1248. DOI: 10.4319/lo.2001.46.5.1243.
Beversdorf, L.J., Miller, T.R. & McMahon, K.D. (2013).The Role of Nitrogen Fixation in Cyanobacterial Bloom Toxicity in a Temperate, Eutrophic Lake. PLoS ONE 8(2): e56103. DOI: 10.1371/journal.pone.0056103.
Buchan, A., Le Cleir, G.R., Gulvik, C.A. & González, J.M. (2014). Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat. Rev. Micro. 12: 686–698. DOI:10.1038/nrmicro3326.
Carpenter, J.H. (1965). The accuracy of the Winkler method for dissolved oxygen. Limnol. Oceanogr. 10: 135–140. DOI: 10.4319/lo.1965.10.1.0135.
Chisholm, S.W. (1992). Phytoplankton size. In: P.G. Falkowski, A.D. Woodhead & K. Vivirito (Eds.), Primary productivity and biogeochemical cycles in the sea (pp. 213–236). Boston, MA: Springer. DOI: 10.1007/978-1-4899-0762-2_12.
Cook., C., Vardaka, E. & Lanaras, T. (2004). Toxic cyanobacteria in Greek freshwaters, 1997–2000: Occurrence, toxicity and impacts in the Mediterranean region. Acta Hydrochim. Hydrobiol. 32: 107–124. DOI: 10.1002/aheh.200300523.
Fenchel, T. (1988). Marine plankton food chains. Annu. Rev. Ecol. Syst. 19: 19–38. DOI: 10.1146/annurev.es.19.110188.000315.
Gaedke, U. (1995). A comparison of whole-community and ecosystem approaches (biomass size distributions, food web analysis, network analysis, simulation models) to study the structure, function and regulation of pelagic food webs. J. Plankton Res. 17: 1273–1305.
Hadjisolomou, E., Stefanidis, K., Papatheodorou, G. & Papastergiadou, E. (2016). Assessing the Contribution of the Environmental Parameters to Eutrophication with the Use of the “PaD” and “PaD2” Methods in a Hypereutrophic Lake. Int. J. Environ. Res. Public Health 13(8): 764. DOI: 10.3390/ijerph13080764.
Horváth, H., Kovács, A.W., Riddick, C. & Présing, M. (2013). Extraction methods for phycocyanin determination in freshwater filamentous cyanobacteria and their application in a shallow lake. Eur. J. Phycol. 48(3): 278–286. DOI: 10.1080/09670262.2013.821525.
Kagalou, I., Papastergiadou, E. & Leonardos, I. (2008a). Long term changes in the eutrophication process in a shallow Mediterranean lake ecosystem of W. Greece: Response after the reduction of external load. J. Env. Managem. 87: 497–506. DOI: 10.1016/j.jenvman.2007.01.039.
Kagalou, I., Papadimitriou, T., Bacopoulos, V. & Leonardos, I. (2008b). Assessment of microcystins in lake water and the omnivorous fish (Carassiusgibelio, Bloch) in Lake Pamvotis (Greece) containing dense cyanobacterial bloom. Environ. Monit. Assess. 137: 185–195. DOI: 10.1007/s10661-007-9739-6.
Kagalou, I., Papastergiadou, E., Tsimarakis, G. & Petridis, D. (2003). Evaluation of the trophic state of Lake Pamvotis Greece, a shallow urban lake. Hydrobiologia 506: 745. DOI: 10.1023/B:HYDR.0000008603.69847.9e.
Kagalou, I., Tsimarakis, G. & Paschos, I. (2001). Water chemistry and biology in a shallow lake (Lake Pamvotis – Greece): Present state and perspectives. Global Nest: the Int. J. 3(2): 85–94.
Katsiapi, M., Stefanidou, N., Karayanni, H., Kormas, K.A. & Moustaka, M. (2011).Water blooms and their implications in the ecological water quality of Lake Pamvotis. In: 4th Congress of Mikrobiokosmos, 21–23 October 2011. Ioannina, Greece: Scientific Society of Mikrobiokosmos.
Kirchman, D.L. (1993). Statistical analysis of direct counts of microbial abundance. Handbook of Methods in Aquatic Microbial Ecology 117–119, Lewis Publishers, Boca Raton, FL, USA.
Kormas, K.A., Garametsi, V. & Nicolaidou, A. (2002). Sizefractionated phytoplankton chlorophyll in an Eastern Mediterranean coastal system (Maliakos Gulf, Greece). Helgol. Mar. Res. 56: 125. DOI: 10.1007/s10152-002-0106-2.
Kotti, M., Vlessidis, A. & Evmiridis, N. (2000). Determination of phosphorous and nitrogen in thesediment of Lake Pamvotis (Greece). Int. J. Environ. An. Ch. 78(3–4): 455–467. DOI: 10.1080/03067310008041360.
Koussouris, T.S., Diapoulis, A.C. & Photis, G.D. (1991). Evaluating the trophic status of a shallow polluted lake, Lake Ioannina, Greece. Toxicol. Environ. Chem. 31(1):303–313 DOI: 10.1080/02772249109357702.
Labasque, T., Chaumery, C., Aminot, A. & Kergoat, G. (2004). Spectrophotometric Winkler determination of dissolved oxygen: reexamination of critical factors and reliability. Mar. Chem. 88(1–2): 53–60. DOI: 10.1016/j.marchem.2004.03.004.
Lawrenz, E., Fedewa, J.E. & Richardson, T.L. (2011). Extraction protocols for the quantification of phycobilins in aqueous phytoplankton extracts. J. Applied Phycol. 23: 865–871. DOI: 10.1007/s10811-010-9600-0.
Lee R.E. (2008). 2. Cyanobacteria. Phycology (pp. 31–79), Cambridge University Press, New York, NY, USA.
Li, Y., Liu, B., Liu, S. & Li, D. (2017). The trophic state of lake water regulates spatial-temporal variations of bloomforming Microcystis. Chin. J. Ocean. Limnol. 35: 415–422. DOI: 10.1007/s00343-016-5266-z.
Lima-Mendez, G., Faust, K., Henry, N., Decelle, J., Colin, S. et al. (2015). Ocean plankton. Determinants of community structure in the global plankton interactome. Science. 348(6237): 1262073. DOI: 10.1126/science.1262073.
Loisa, O., Kaaria, J., Laaksonlaita, J., Niemi, J., Sarvala, J. et al. (2015). From phycocyanin fluorescence to absolute cyanobacteria biomass: An application using in-situ fluorometer probes in the monitoring of potentially harmful cyanobacteria blooms. Water Pract. Technol.10: 695–698. DOI:. 10.2166/wpt.2015.083.
Lyu, H., Wang, Q., Wu, C., Zhu, L., Yin, B. et al. (2013). Retrieval of phycocyanin concentration from remotesensing reflectance using a semi-analytic model in eutrophic lakes. Ecol. Inform. 18: 178–187. DOI: 10.1016/j.ecoinf.2013.09.002.
Masson S., Pinel-Alloul, B. & Smith, V.H. (2000). Total phosphorus–chlorophyll a size fraction relationships in southern Québec lakes. Limnol. Oceanogr. 3: 732–740. DOI: 10.4319/lo.2000.45.3.0732.
Mouillot, D., Spatharis, S., Reizopoulou, S., Laugier, T., Sabetta, L. et al. (2006). Alternatives to taxonomic-based approaches to assess changes in transitional water communities. Aquatic Conserv.: Mar. Freshw. Ecosyst. 16: 469–482. DOI: 10.1002/aqc.769.
Moustaka-Gouni, M. (1993). Phytoplankton succession and diversity in a warm monomictic relatively shallow lake: Lake Volvi, Macedonia, Greece. Hydrobiologia 249: 33–42. DOI: 10.1007/BF00008841.
Moustaka-Gouni, M., Vardaka, E., Michaloudi, E., Kormas, K.Ar.,Tryfon, E. et al. (2006). Plankton food web structure in a eutrophic polymictic lake with a history in toxic cyanobacterial blooms. Limnol. Oceanogr. 51(1, part 2): 715-727. DOI: 10.4319/lo.2006.51.1_part_2.0715.
OECD. (1982). Eutrophication of Waters.Monitoring, Assessment and Control. Paris: OECD.
Papadimitriou, T. (2010). Effects of Microcystins on aquatic organisms. Unpublished doctoral dissertation (In Greek), University of Ioannina, Greece.
Papadimitriou, T., Armeni, E., Stalikas, C.D., Kagalou, I. & Leonardos, I.D. (2012). Detection of microcystins in Pamvotis lake water and assessment of cyanobacterial bloom toxicity. Environ. Monit. Assess. 184(5): 3043–52. DOI: 10.1007/s10661-011-2169-5.
Papastergiadou, E., Kagalou, I., Stefanidis, Retalis, K.A. & Leonardos, I. (2010). Effects of Anthropogenic Influences on the Trophic State, Land Uses and Aquatic Vegetation in a Shallow Mediterranean Lake: Implications for Restoration. Water Resour. Manag. 24: 415. DOI: 10.1007/s11269-009-9453-y.
Parsons, T.R., Maita, Y. & Malli, C.M. (1984) Determination of chlorophylls and total carotenoids: Spectrophotometric method. In: A manual of chemical and biological methods for seawater analysis (pp. 101–104). Oxford, UK: Pergamon Press. DOI: 10.1016/B978-0-08-030287-4.50032-3.
Porter, K.G., Feig, Y.S. (1980). The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr. 25(5): 943–948. DOI: 10.4319/lo.1980.25.5.0943.
Pyo, J.C., Pachepsky, Y., Baek, S.S., Kwon, Y.S., Kim, M.J. et al. (2017). Optimizing Semi-Analytical Algorithms for Estimating Chlorophyll-a and Phycocyanin Concentrations in Inland Waters in Korea. Remote Sens. 9(6): 542. DOI: 10.3390/rs9060542.
Randolph, K., Wilson, J., Tedesco, L., Li, L., Pascual, D.L. et al. (2008). Hyperspectral remote sensing of cyanobacteria in turbid productive water using optically active pigments, chlorophyll a and phycocyanin. Remote Sens. Environ. 112: 4009–4019. DOI: 10.1016/j.rse.2008.06.002.
Romero, J.R., Kagalou, I., Imberger, J. Hela, D., Kotti, M. et al. (2002). Seasonal water quality of shallow and eutrophic Lake Pamvotis, Greece: implications for restoration. Hydrobiologia. 474: 91. DOI: 10.1023/A:1016569124312.
Smith, V.H.,Tilman, G.D. & Nekola, J.C. (1999). Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environ. Pollut. 100: 179–196. DOI: 10.1016/S0269-7491(99)00091-3.
Siegelman, H. & Kycia, J.H. (1978). Alga biliproteins. In: J.A. Hellebust & J.S. Craigie (Eds.), Handbook of phycological methods: physiological and biochemical methods (pp. 72–78). Cambridge, UK: Cambridge University Press. DOI: 10.1017/S0025315400045811.
Simis, S.G., Peters, S.W.M. & Gons, H.J. (2005). Remote sensing of the cyanobacterial pigment phycocyanin in turbid inland water. Limnol. Oceanogr. 50(1): 237–245.
Søndergaard, M. (1997). Bacteria and dissolved organic carbon in lakes. In Freshwater Biology. Priorities and Development in Danish research (pp. 138–161). København: Gad.
Song, K., Li, L., Li, S., Tedesco, L., Hall, B. et al. (2012). Hyperspectral retrieval of phycocyanin in potable water sources using genetic algorithm – partial least squares (GA–PLS) modeling. Inter. J. Appl. Earth Obs. Geoinf. 18: 368–385. DOI: 10.1016/j.jag.2012.03.013.
Sprules, W.G. & Munawar, M. (1986). Plankton size spectra in relation to ecosystem productivity, size, and perturbation. Can. J. Fish. Aquat. Sci. 43: 1789–1794. DOI: 10.1139/f86-222.
Stockner, J.G. & Shortreed, K.S. (1991). Autotrophic picoplankton: Community composition, abundance and distribution across a gradient of oligotrophic British Columbia and Yukon Territory lakes. Int. Rev. Gesamten Hydrobiol. 76: 581–601. DOI: 10.1002/iroh.19910760410.
Szelag-Wasielewska, E. (1997). Picoplankton and other size groups of phytoplankton in various shallow lakes. Hydrobiologia 342/343: 79–85. DOI: 10.1007/978-94-011-5648-6_9.
Takamura, N. & Nojiri, Y. (1994). Picophytoplankton biomass in relation to lake trophic status and the TN:TP ratio of lake water in Japan. J. Phycol. 30: 439–444. DOI: 10.1111/j.0022-3646.1994.00439.x.
Tilzer, M.M. (1988). Secchi disk-chlorophyll relationships in a lake with highly variable phytoplankton biomass. Hydrobiologia. 162: 163–171. DOI: 10.1007/BF00014539.
Vardaka, E.,Moustaka-Gouni, M., Cook, C.M. & Lanaras T. (2005). Cyanobacterial blooms and water quality in Greek waterbodies. J. Appl. Phycol. 17: 391. DOI: 10.1007/s10811-005-8700-8.
Wang, G., Cao, W., Wang, G. & Zhou, W. (2013). Phytoplankton size class derived from phytoplankton absorption and chlorophyll-a concentrations in the northern South China Sea. Chin. J. Ocean. Limnol. 31: 750. DOI: 10.1007/s00343-013-2291-z.
Wang, J., Shi, R. & Gao, W. (2014). Retrieval of phycocyanin concentration in the eutrophic Taihu Lake. In Proc. Of SPIE Remote Sensing and Modeling of Ecosystems for Sustainability XI, 92210Z, 8 October 2014. San Diego, California, United States. DOI: 10.1117/12.2061208.
Watson, S. & McCauley, E. (1988).Contrasting patterns of netand nanoplankton production and biomass among lakes. Can. J. Fish. Aquat. Sci. 45: 915–920. DOI: 10.1139/f88-112.
Watson, S.B., McCauley, E. & Downing, J.A. (1997). Patterns in phytoplankton taxonomic composition across temperate lakes of different nutrient status. Limnol. Oceanogr. 42: 487–495. DOI: 10.4319/lo.1997.42.3.0487.
Wetzel, R.G. & Likens, G. (2000). Composition and biomass of phytoplankton. In Limnological Analysis (pp. 147–174). Springer, New York, NY. DOI: 10.1007/978-1-4757-3250-4_10.
Ye, L.L., Wu, X.D., Liu, B., Yan, D.Z. & Kong, F.X. (2014). Dynamics of dissolved organic carbon in eutrophic Lake Taihu and its tributaries and their implications for bacterial abundance during autumn and winter. J. Freshw. Ecol. 30(1): 129–142. DOI: 10.1080/02705060.2014.939108.
Zhu, Y., Chen, X.B., Wang, K.B., Li. Y.X., Bai, K.Z. et al. (2007). A simple method for extracting C-phycocyanin from Spirulina platensis using Klebsiella pneumonia. App. Microb. Biotech. 74: 244–248. DOI: 10.1007/s00253-006-0636-7.
Zimba, P.V. (2012). An improved phycobilins extraction method. Harmful Algae 17: 35–39. DOI: 10.1016/j.hal.2012.02.009.
