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Primary production under hypertrophic conditions and its relationship with bacterial production

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Abstract

In shallow hypertrophic lakes where light availability restricts the growth of macrophytes and benthic phytoplankton, pelagic phytoplankton modulates importantly ecosystem production and the energy transfer to heterotrophic bacteria. Diel and seasonal variations in primary production (PP) were studied in the hypertrophic Albufera de Valencia (Spain). Additionally, the relationship between PP and heterotrophic bacterial production (BP) was assessed. PP was extremely high, exceeding most values reported for hypertrophic lakes to date. PP displayed marked diurnal variations defined by the solar radiation curve. Likewise, PP changed importantly across seasons. Minimum PP coincided with maximum water transparency and short water residence times in winter, whereas maximum PP was observed in late spring associated with high chlorophyll a. The spring PP maximum contrasted with the summer maximum often observed in hypertrophic lakes. When compared to spring PP values, summer PP values were lower as a result of strong nitrogen limitation. In contrast to PP, BP remained fairly constant across seasons. Nonetheless, there was a joint diminution during increased water transparency followed by an increase in early spring. Phytoplankton was always the most relevant input to particulate carbon production, but the BP/PP ratio showed clear seasonal variations. The BP/PP ratio was minimum in spring, low in summer and highest in winter. The extracellular dissolved organic carbon released by phytoplankton was sufficient to meet bacterial carbon demand in all experimental dates, suggesting that allochthonous carbon sources play a minor role in sustaining BP, though they cannot be excluded. However, we hypothesize that high availability of dissolved organic carbon might explain the lack of coupling observed between BP and PP.

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References

  • Ahn C-Y, Joung S-H, Yoon S-K, Oh H-M (2007) Alternative alert system for cyanobacterial bloom, using phycocyanin as a level determinant. J Microbiol 45:98–104

    CAS  PubMed  Google Scholar 

  • APHA (1992) Standard methods for the examination of water and wastewater, 18th edn. American Public Health Association, Washington, DC

    Google Scholar 

  • Auer B, Elzer U, Arndt H (2004) Comparison of pelagic food webs in lakes along a trophic gradient and with seasonal aspects: influence of resource and predation. J Plankton Res 26:697–709

    Article  Google Scholar 

  • Baines SB, Pace ML (1991) The production of dissolved organic-matter by phytoplankton and its importance to bacteria: patterns across marine and fresh-water systems. Limnol Oceanogr 36:1078–1090

    Article  Google Scholar 

  • Bird DF, Kalff J (1984) Empirical relationships between bacterial abundance and chlorophyll concentration in fresh and marine waters. Can J of Fish Aquat Sci 41:1015–1023. doi:10.1139/f84-118

    Article  Google Scholar 

  • Blindow I, Hargeby A, Meyercordt J, Schubert H (2006) Primary production in two shallow lakes with contrasting plant form dominance: a paradox of enrichment? Limnol Oceanogr 51:2711–2721

    Article  Google Scholar 

  • Callieri C, Stockner JG (2002) Freshwater autotrophic picoplankton: a review. J Limnol 61:1–14

    Google Scholar 

  • Chrost RJ, Siuda W (2006) Microbial production, utilization, and enzymatic degradation of organic matter in the upper trophogenic layer in the pelagial zone of lakes along an eutrophication gradient. Limnol Oceanogr 51:749–762

    Article  Google Scholar 

  • Chrost RJ, Koton M, Siuda W (2000) Bacterial secondary production and bacterial biomass in four Mazurian lakes of differing trophic status. Pol J Environ Stud 9:255–266

    CAS  Google Scholar 

  • Cole JJ, Likens GE, Strayer DL (1982) Photosynthetically produced dissolved organic carbon: an important carbon source for planktonic bacteria. Limnol Oceanogr 27:1080–1090

    Article  CAS  Google Scholar 

  • Cole JJ, Findlay S, Pace ML (1988) Bacterial production in fresh and saltwater ecosystems: a cross-system overview. Mar Ecol Prog Ser 43:1–10. doi:10.3354/meps043001

    Article  Google Scholar 

  • del Giorgio PA, Cole JJ (1998) Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Syst 29:503–541. doi:10.1146/annurev.ecolsys.29.1.503

    Article  Google Scholar 

  • Dickman M (1969) Some effects of lake renewal on phytoplankton productivity and species composition. Limnol Oceanogr 14:660–666

    Article  Google Scholar 

  • Falkowski PG, Laroche J (1991) Acclimation to spectral irradiance in algae. J Phycol 27:8–14. doi:10.1111/j.0022-3646.1991.00008.x

    Article  Google Scholar 

  • Fouilland E, Mostajir B (2010) Revisited phytoplanktonic carbon dependency of heterotrophic bacteria in freshwaters, transitional, coastal and oceanic waters. FEMS Microbiol Ecol 73:419–429. doi:10.1111/j.1574-6941.2010.00896.x

    Article  CAS  PubMed  Google Scholar 

  • Fraga F (2001) Phytoplanktonic biomass synthesis: application to deviations from Redfield stoichiometry. Sci Mar 65:153–169

    Article  CAS  Google Scholar 

  • Gao G, Qin B, Sommaruga R, Psenner R (2007) The bacterioplankton of Lake Taihu, China: abundance, biomass, and production. Hydrobiologia 581:177–188. doi:10.1007/s10750-006-0511-7

    Article  Google Scholar 

  • Gasol JM, Doval MD, Pinhassi J, Calderon-Paz JI, Guixa-Boixareu N, Vaque D, Pedros-Alio C (1998) Diel variations in bacterial heterotrophic activity and growth in the northwestern Mediterranean Sea. Mar Ecol Prog Ser 164:107–124. doi:10.3354/meps164107

    Article  Google Scholar 

  • Gocke K, Hernandez C, Giesenhagen H, Hoppe HG (2004) Seasonal variations of bacterial abundance and biomass and their relation to phytoplankton in the hypertrophic tropical lagoon Cienaga Grande de Santa Marta, Colombia. J Plankton Res 26:1429–1439. doi:10.1093/plankt/fbh131

    Article  Google Scholar 

  • Harding WR (1997) Phytoplankton primary production in a shallow, well-mixed, hypertrophic South African lake. Hydrobiologia 344:87–102. doi:10.1023/a:1002954311328

    Article  CAS  Google Scholar 

  • Hart EA, Lovvorn JR (2000) Vegetation dynamics and primary production in saline, lacustrine wetlands of a Rocky Mountain basin. Aquat Bot 66:21–39

    Article  Google Scholar 

  • Hillebrand H, Durselen CD, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424

    Article  Google Scholar 

  • ISO (International Organization for Standardization) (1997) Water analysis - Guidelines for the determination of total organic carbon (TOC) and dissolved organic carbon (DOC). ISO EN 1484.ISO, Geneva

  • ISO (International Organization for Standardization) (1999) Water quality - Determination of turbidity. ISO EN 7027, ISO, Geneva

  • Jacoby J, Welch E (2004) Pollutant effects in freshwater: applied limnology, 3rd edn. Spon Press, London

    Google Scholar 

  • Jones I, Elliott J (2007) Modelling the effects of changing retention time on abundance and composition of phytoplankton species in a small lake. Freshw Biol 52:988–997

    Article  Google Scholar 

  • Joniak T, Goldyn R, Kozak A (2003) The primary production of phytoplankton in the restored Maltanski Reservoir in Poland. Hydrobiologia 506:311–316. doi:10.1023/b:hydr.0000008584.22153.86

    Article  Google Scholar 

  • Kamjunke N, Boing W, Voigt H (1997) Bacterial and primary production under hypertrophic conditions. Aquat Microb Ecol 13:29–35. doi:10.3354/ame013029

    Article  Google Scholar 

  • Kisand V, Noges T (1998) Seasonal dynamics of bacterio—and phytoplankton in large and shallow eutrophic Lake Vortsjarv, Estonia. Int Rev Hydrobiol 83:205–216. doi:10.1002/iroh.19980830304

    Article  Google Scholar 

  • Liboriussen L, Jeppesen E (2003) Temporal dynamics in epipelic, pelagic and epiphytic algal production in a clear and a turbid shallow lake. Freshw Biol 48:418–431. doi:10.1046/j.1365-2427.2003.01018.x

    Article  Google Scholar 

  • Mague TH, Friberg E, Hughes DJ, Morris I (1980) Extracellular release of carbon by marine phytoplankton; a physiolocial approach. Limnol Oceanogr 25:262–279

    Article  CAS  Google Scholar 

  • Margalef R (1997) Our biosphere. Excellence in ecology, vol 10. Oldenforf-Luhe, Germany

    Google Scholar 

  • Miracle MR, Vicente E, Sarma S, Nandini S (2014) Planktonic rotifer feeding in hypertrophic conditions. Int Rev Hydrobiol 99:141–150

    Article  Google Scholar 

  • Morán X, Estrada M, Gasol J, Pedrós-Alió C (2002) Dissolved primary production and the strength of phytoplankton–bacterioplankton coupling in contrasting marine regions. Microb Ecol 44:217–223

  • Moustaka-Gouni M et al (2006) Plankton food web structure in a eutrophic polymictic lake with a history of toxic cyanobacterial blooms. Limnol Oceanogr 51:715–727

    Article  Google Scholar 

  • Myklestad SM (1995) Release of extracellular products by phytoplankton with special emphasis on polysaccharides. Sci Total Environ 165:155–164

    Article  CAS  Google Scholar 

  • Oliver RL, Whittington J, Lorenz Z, Webster IT (2003) The influence of vertical mixing on the photoinhibition of variable chlorophyll a fluorescence and its inclusion in a model of phytoplankton photosynthesis. J Plankton Res 25:1107–1129

    Article  CAS  Google Scholar 

  • Onandia G, Miracle MR, Blasco C, Vicente E (2014) Diel and seasonal variations in bacterial producation in a hypertrophic shallow lagoon. Aquat Microb Ecol 72:255–267

    Article  Google Scholar 

  • Padisák J, Köhler J, Hoeg S (1999) Effect of changing flushing rates on development of late summer Aphanizomenon and Microcystis populations in a shallow lake. Müggelsee, Berlin

    Google Scholar 

  • Pugnetti A, Del Negro P, Giani M, Acri F, Aubry FB, Bianchi F, Berto D, Valeri A (2010) Phytoplankton–bacterioplankton interactions and carbon fluxes through microbial communities in a microtidal lagoon. FEMS Microbiol Ecol 72:153–164

    Article  CAS  PubMed  Google Scholar 

  • Reynolds CS (2006) The ecology of phytoplankton, 1st edn. Cambridge University Press, New York

    Book  Google Scholar 

  • Robarts RD (1988) Heterotrophic bacterial activity and primary production in a hypertrophic African lake. Hydrobiologia 162:97–107. doi:10.1007/bf00014532

    Article  Google Scholar 

  • Robarts RD, Sephton LM (1989) Phytoplankton extracellular dissolved organic-carbon production in a hypertrophic African lake. Hydrobiologia 182:137–148. doi:10.1007/bf00006039

    Article  CAS  Google Scholar 

  • Robarts RD, Arts MT, Evans MS, Waiser MJ (1994) The coupling of heterotrophic bacterial and phytoplankton production in a hypertrophic, shallow prairie lake. Can J Fish Aquat Sci 51:2219–2226. doi:10.1139/f94-224

    Article  Google Scholar 

  • Romo S et al (2005) Response of a shallow Mediterranean lake to nutrient diversion: does it follow similar patterns as in northern shallow lakes? Freshw Biol 50:1706–1717. doi:10.1111/j.1365-2427.2005.01432.x

    Article  CAS  Google Scholar 

  • Romo S, Garcıa-Murcia A, Villena MJ, Balleste VSA (2008) Tendencias del fitoplancton en el lago de la Albufera de Valencia e implicaciones para su ecología, gestión y recuperación. Limnetica 27:11–28

    Google Scholar 

  • Schelske CL, Aldridge FJ, Carrick HJ, Coveney MF (2003) Phytoplankton community photosynthesis and primary production in a hypereutrophic lake, Lake Apopka, Florida. Arch Hydrobiol 157:145–172. doi:10.1127/0003-9136/2003/0157-0145

    Article  Google Scholar 

  • Seitzinger SP (1988) Denitrification in fresh-water and coastal marine ecosystems: ecological and geochemical significance. Limnol Oceanogr 33:702–724

    Article  CAS  Google Scholar 

  • Shoaf TW, Lium BW (1976) Improved extraction of chlorophyll a and b from algae using dimethylsulphoxide. Limnol Oceanogr 21:926–928

    Article  CAS  Google Scholar 

  • Simon M, Cho BC, Azam F (1992) Significance of bacterial biomass in lakes and the ocean: comparison to phytoplankton biomass and biogeochemical implications. Mar Ecol-Prog Ser 86:103–110

  • Søballe D, Kimmel B (1987) A large-scale comparison of factors influencing phytoplankton abundance in rivers, lakes, and impoundments. Ecology 68:1943–1954

  • Sommaruga R, Robarts RD (1997) The significance of autotrophic and heterotrophic picoplankton in hypertrophic ecosystems. FEMS Microbiol Ecol 24:187–200. doi:10.1111/j.1574-6941.1997.tb00436.x

    Article  CAS  Google Scholar 

  • Søndergaard M (1993) Organic carbon pools in two Danish lakes. Flow of carbon to bacterioplankton. Verh Int Ver Angew Theor Limnol 25:593–598

    Google Scholar 

  • Steeman-Nielsen EJ (1952) The use of radioactive carbon (14C) for measuring organic production in the sea. J Cons Perm Int Pour l’Explor Mer 18:117–140

    Article  Google Scholar 

  • Vicente E, Miracle M (1992) The coastal lagoon Albufera de Valencia: an ecosystem under stress. Limnetica 8:87–100

    Google Scholar 

  • Villena M-J, Romo S (2003) Temporal changes of cyanobacteria in the largest coastal Spanish lake. Algol Stud 109:593–608

    Article  Google Scholar 

  • Wetzel RG, Likens GE (2000) Limnological analyses, 3rd edn. Springer, New York

    Book  Google Scholar 

  • Wetzel RG, Likens GE (2001) Limnology: lake and river ecosystems, 3rd edn. Springer, San Diego

    Google Scholar 

  • Winter C, Herndl GJ, Weinbauer MG (2004) Diel cycles in viral infection of bacterioplankton in the North Sea. Aquat Microb Ecol 35:207–216

    Article  Google Scholar 

  • Wu X, Kong F, Zhang M (2011) Photoinhibition of colonial and unicellular Microcystis cells in a summer bloom in Lake Taihu. Limnology 12:55–61

    Article  Google Scholar 

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Acknowledgments

We thank the rangers of the Oficina Técnica Devesa-Albufera, C. Blasco and X. Soria for their assistance in the field. We are grateful to J.M. Soria and O. Kramer for their help in the laboratory activities and to M.D. Sendra for phytoplankton data on January and April 2011. We also thank the Agencia Estatal de Metereología (AEMET) for providing data on wind and solar radiation. This work was supported by the Spanish Ministry of Economy and Competitiveness through the project CGL2009-12229 and grant BES-2010-032212.

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Correspondence to Gabriela Onandia.

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Onandia, G., Miracle, M.R. & Vicente, E. Primary production under hypertrophic conditions and its relationship with bacterial production. Aquat Ecol 48, 447–463 (2014). https://doi.org/10.1007/s10452-014-9497-9

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