Aquatic Sciences

, Volume 76, Issue 4, pp 579–594 | Cite as

Seasonal-dependence in the responses of biological communities to flood pulses in warm temperate floodplain lakes: implications for the “alternative stable states” model

  • Griselda Chaparro
  • María Soledad Fontanarrosa
  • María Romina Schiaffino
  • Paula de Tezanos Pinto
  • Inés O’Farrell
Research Article

Abstract

In floodplains located in temperate regions, seasonal variations in temperature affect biological communities and these effects may overlap with those of the flood regime. In this study we explored if and how timing (with regard to temperature seasonality) influences the responses of planktonic and free-floating plants communities to floods in a warm temperate floodplain lake and assessed its relevance for determining state shifts. We took samples of zooplankton, phytoplankton, picoplankton, heterotrophic nanoflagellates and free-floating macrophytes at four sites of the lake characterized by the presence-absence of emergent or free-floating macrophytes along a 2-year period with marked hydrological fluctuations associated to river flood dynamics. We performed ANOVA tests to compare the responses of these communities to floods in cold and warm seasons and among sites. Planktonic communities developed high abundances in response to floods that occurred in the cold season, while the growth of free-floating macrophytes was impaired by low winter temperatures. Spring and summer floods favored profuse colonization by free-floating plants and limited the development of planktonic communities. The prolonged absence of floods during warm periods caused environmental conditions that favored Cyanobacteria growth, leading to a “low turbid waters” regime. The occurrence of floods early in the warm season caused phytoplankton dilution and promoted free-floating plant colonization and a shift towards a “high clear waters” state. Zooplankton:phytoplankton biomass ratio was very low during floods in warm seasons, thus zooplankton grazing on phytoplankton seemed to play a minor role in the maintenance of the clear regime.

Keywords

Flood pulses Temperature seasonality Zooplankton Macrophytes Alternative stable states 

References

  1. Alves GM, Velho LFM, Lansac-Tôha FA, Robertson B, Bonecker CC (2005) Effect of the connectivity on the diversity and abundance of cladoceran assemblages in lagoons of the upper Paraná river floodplain. Acta Limnol Bras 17:317–327Google Scholar
  2. APHA (American Public Health Association) (2005) Standard Methods for the examination of waters and wastewater, 21st edn. APHA, WashingtonGoogle Scholar
  3. Auge M (2004) Vulnerabilidad de acuíferos. Rev Latinoam Hidrogeol 4:85–103Google Scholar
  4. Baigún CRM, Puig A, Minotti PG, Kandus P, Quintana R, Vicari R, Bo R, Oldani NO, Nestler JA (2008) Resource use in the Parana River Delta (Argentina): moving away from an ecohydrological approach? Ecohydrol Hydrobiol 8:245–262CrossRefGoogle Scholar
  5. Baranyi C, Hein T, Holarek C, Keckeis S, Schiemer F (2002) Zooplankton biomass and community structure in a Danube River floodplain system: effects of hydrology. Freshwater Biol 47:473–482CrossRefGoogle Scholar
  6. Bicudo DDC, Fonseca BM, Bini LM, Crossetti LO, Bicudo CEDM, Araújo-Jesus T (2007) Undesirable side-effects of water hyacinth control in a shallow tropical reservoir. Freshwater Biol 52:1120–1133CrossRefGoogle Scholar
  7. Boschilia SM, Oliveira EF, Thomaz SM (2008) Do aquatic macrophytes co-occur randomly? An analysis of null models in a tropical floodplain. Oecologia 156:203–214PubMedCrossRefGoogle Scholar
  8. Bottrell HH, Duncan A, Gliwicz ZM, Grygierek E, Herzig A, Hillbricht-Ilkowska A, Kurasawa H, Larsson P, Weglenska T (1976) A review of some problems in zooplankton production studies. Norw J Zool 24:419–456Google Scholar
  9. Bouvy M, Nascimento SM, Molica RJR, Ferreira A, Huszar V, Azevedo SMFO (2003) Limnological features in Tapacurá Reservoir (Northeast Brazil) during a severe drought. Hydrobiologia 493:115–130CrossRefGoogle Scholar
  10. Burks RL, Mulderij G, Gross E, Jones I (2006) Center stage: the crucial role of macrophytes in regulating trophic interactions in shallow lake wetlands. In: Bobbink R, Beltman B, Verhoeven JTA, Whigham DF (eds) Wetlands: functioning, biodiversity conservation and restoration. Springer, Berlin, Heidelberg, pp 37–59Google Scholar
  11. Callieri C, Pinolini M (1995) Photosynthetic efficiency and seasonality of autotrophic picoplankton in Lago Maggiore after its recovery. Freshwater Biol 47:941–956CrossRefGoogle Scholar
  12. Camilloni IA, Barros VR (2003) Extreme discharge events in the Paraná River and their climate forcing. J Hydrol 278:94–106CrossRefGoogle Scholar
  13. Cancian LF, Monteiro Camargo AF, Gonzaga Silva GH (2009) Crescimento de Pistia stratiotes em diferentes condições de temperatura e fotoperíodo. Acta Bot Bras 23:552–557CrossRefGoogle Scholar
  14. Casatti L, Mendes HF, Ferreira KM (2003) Aquatic macrophytes as feeding site for small fishes in the Rosana Reservoir, Paranapanema River, Southeastern Brazil. Braz J Biol 63:213–222PubMedCrossRefGoogle Scholar
  15. Castillo MM (2000) Influence of hydrological seasonality on bacterioplankton in two neotropical floodplain lakes. Hydrobiologia 437:57–69CrossRefGoogle Scholar
  16. Chaparro G, Marinone MC, Lombardo R, Schiaffino MR, Guimarães A, O’Farrell I (2011) Zooplankton succession during extraordinary drought–flood cycles: a case study in a South American floodplain lake. Limnologica 4:371–381CrossRefGoogle Scholar
  17. Chaparro G, Kandus P, O’Farrell I (2013) Effect of spatial heterogeneity on zooplankton diversity: a multiscale habitat approximation in a floodplain lake. Riv Res Appl. doi:10.1002/rra.2711 Google Scholar
  18. Chichizola SE (1993) Las comunidades vegetales de la Reserva Natural Estricta Otamendi y sus relaciones con el ambiente. Parodiana 8:227–263Google Scholar
  19. Costa Bonecker C, Da Costa CL, Machado Velho LF, Lansac-Tôha FA (2005) Diversity and abundance of the planktonic rotifers in different environments of the Upper Paraná River floodplain (Paraná State-Mato Grosso do Sul State, Brazil). Hydrobiologia 2005:405–414CrossRefGoogle Scholar
  20. de Huszar VLM, Reynolds CS (1997) Phytoplankton periodicity and sequence of dominance in an Amazonian flood-plain lake (Lago Batata, Pará, Brazil): Response to gradual environmental change. Hydrobiologia 346:169–181CrossRefGoogle Scholar
  21. de Tezanos Pinto P, Allende L, O’Farrell I (2007) Influence of free-floating plants on the structure of a natural phytoplankton assemblage: an experimental approach. J Plankton Res 29:47–56CrossRefGoogle Scholar
  22. den Hollander NG, Schenk WI, Diouf S, Kropff MJ, Pieterse AH (1999) Survival strategy of Pistia Stratiotes in the Djoudj National Park in Senegal. Hydrobiologia 415:21–27CrossRefGoogle Scholar
  23. Deng D, Zhang S, Li Y, Meng X, Wei Y, Yan L, Xiuxiu L (2010) Effects of Microcystis aeruginosa on population dynamics and sexual reproduction in two Daphnia species. J Plankton Res 32:1385–1392CrossRefGoogle Scholar
  24. Dewald LB, Lounibos LP (1990) Seasonal growth of Pistia stratiotes L. in South Florida. Aquat Bot 36:263–275CrossRefGoogle Scholar
  25. Dumont HJ, van de Velde I, Dumont S (1975) The dry weight estimate of biomass in a selection of Cladocera, Copepoda and Rotifera from the plankton, periphyton and benthos of continental waters. Oecologia 19:79–97CrossRefGoogle Scholar
  26. Fantin-Cruz I, Loverde-Oliveira SM, Costa Bonecker C, Girad P, da Motta-Marque D (2011) Relationship between the structure of zooplankton community and the water level in a floodplain lake from the Pantanal, Mato Grosso State, Brazil. Acta Sci Biol Sci 33:271–279CrossRefGoogle Scholar
  27. Fontanarrosa MS, Chaparro G, de Tezanos Pinto P, Rodriguez P, O’Farrell I (2010) Zooplankton response to shading effects of free-floating plants in shallow warm temperate lakes: a field mesocosm experiment. Hydrobiologia 646:231–242CrossRefGoogle Scholar
  28. Frutos SM, Poi de Neiff ASG, Neiff JJ (2006) Zooplankton of the Paraguay River: a comparison between sections and hydrological phases. Ann Limnol Int J Limnol 42:277–288CrossRefGoogle Scholar
  29. García de Emiliani MO (1997) Effects of water level fluctuations on phytoplankton in a riverfloodplain lake system (Paraná River, Argentina). Hydrobiologia 357:1–15CrossRefGoogle Scholar
  30. Giblin SM, Houser JN, Sullivan JF, Langrehr HA, Rogala JT, Campbell BD (2014) Thresholds in the response of free-floating plant abundance to variation in hydraulic connectivity, nutrients, and macrophyte abundance in a large floodplain river. Wetlands. doi:10.1007/s13157-013-0508-8 Google Scholar
  31. Górski K, Collier KJ, Duggan IC, Taylor CM, Hamilton DP (2013) Connectivity and complexity of floodplain habitats govern zooplankton dynamics in a large temperate river system. Freshwater Biol 58:1458–1470CrossRefGoogle Scholar
  32. Haller WT, Sutton DL, Barlowe WC (1974) Effects of salinity on growth of several aquatic macrophytes. Ecology 55:891–894CrossRefGoogle Scholar
  33. Havens KE, Beaver JR (2012) Zooplankton to phytoplankton biomass ratios in shallow Florida Lakes: an evaluation of seasonality and hypotheses about factors controlling variability. Hydrobiologia. doi:10.1007/s10750-012-1357-9 Google Scholar
  34. Havens KE, Elia AC, Taticchi MI, Fulton RS (2009) Zooplankton–phytoplankton relationships in shallow subtropical versus temperate lakes Apopka (Florida, USA) and Trasimeno (Umbria, Italy). Hydrobiologia 628:165–175CrossRefGoogle Scholar
  35. Hillebrand H, Durselen CD, Kirshtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424CrossRefGoogle Scholar
  36. Ibelings BW, Havens KH (2008) Cyanobacterial toxins: a qualitative meta-analysis of concentrations, dosage and effects in freshwater, estuarine and marine biota. In: Hudnell KH (ed) Proceedings of the interagency, international symposium on cyanobacteria harmful algal blooms. Advances in Experimental Medicine and Biology. Springer, New York, pp 675–732Google Scholar
  37. Iglesias C, Goyenola G, Jeppesen E (2007) Horizontal dynamics of zooplankton in subtropical Lake Blanca (Uruguay) hosting multiple zooplankton predators and aquatic plant refuges. Hydrobiologia 584:179–189CrossRefGoogle Scholar
  38. Iglesias C, Mazzeo N, Goyenola G, Fosalba C, Teixeira de Mello F, García S, Jeppesen E (2008) Field and experimental evidence of the effect of Jenynsia multidentata, a small omnivorous-planktivorous fish, on the size distribution of zooplankton in subtropical lakes. Freshwater Biol 53:1797–1807CrossRefGoogle Scholar
  39. Iglesias C, Mazzeo N, Meerhoff M, Lacerot G, Clemente JM, Flavio S, Kruk C, Goyenola G, García-Alonso J, Amsinck SL, Paggi JC, José de Paggi S, Jeppesen E (2011) High predation is of key importance for dominance of small bodied zooplankton in warm shallow lakes: evidence from lakes, fish exclosures and surface sediments. Hydrobiologia 667:133–147CrossRefGoogle Scholar
  40. Izaguirre I, Pizarro H, de Tezanos Pinto P, Rodríguez P, O’Farrell I, Unrein F, Gasol JM (2010) Macrophyte influence on the structure and productivity of photosynthetic picoplankton in wetlands. J Plankton Res 32:221–238CrossRefGoogle Scholar
  41. Izaguirre I, Sinistro R, Schiaffino MR, Sánchez ML, Unrein F, Massana R (2012) Grazing rates of protists in wetlands under contrasting light conditions due to floating plants. Aquat Microb Biol 65:221–232CrossRefGoogle Scholar
  42. Jentsch AJ, Kreyling J, Beierkuhnlein C (2007) A new generation of climate-change experiments: events, not trends. Front Ecol Environ 5:365–374CrossRefGoogle Scholar
  43. Jeppesen E, Sondergaard M, Sondergaard M, Christoffersen K (1997) The structuring role of submerged macrophytes in lakes, ecological studies. Springer, New YorkGoogle Scholar
  44. José de Paggi SB (1981) Variaciones temporales y distribución horizontal del zooplancton en algunos cauces secundarios del Río Paraná medio. Stud Neotrop Fauna E 16:185–199CrossRefGoogle Scholar
  45. José de Paggi SB (1993) Composition and seasonality of planktonic rotifers in limnetic and littoral regions of a floodplain lake (Paraná River system). Rev Hydrobiol Trop 26:53–63Google Scholar
  46. José de Paggi SB, Paggi JC (2008) Hydrological connectivity as a shaping force in the zooplankton community of two lakes in the Paraná River floodplain. Intern Rev Hydrobiol 93:659–678CrossRefGoogle Scholar
  47. Jun S, Dongyan L (2003) Geometric models for calculating cell biovolume and surface area for phytoplankton. J Plankton Res 25:1331–1346CrossRefGoogle Scholar
  48. Junk WJ (1997) The Central Amazon floodplain, ecology of a pulsing system. Springer, BerlinCrossRefGoogle Scholar
  49. Junk WJ, Piedade MTF (1997) Plant life in the floodplain with special reference to herbaceous plants. In: Junk WJ (ed) The Central Amazon floodplain: ecology of a pulsing system. Springer, Berlin, pp 147–185CrossRefGoogle Scholar
  50. Junk WJ, Wantzen KM (2004) The Flood Pulse Concept: new aspects, approaches and applications- an update. Proceedings of the Second International Symposium on the Management of Large Rivers for Fisheries. FAO and Mekong River Commission, FAO Regional Office for Asia and the Pacific, Bangkok, ThailandGoogle Scholar
  51. Junk WJ, Bayley PB, Sparks RE (1989) The Flood Pulse Concept in river floodplains systems. Proceedings of the international large river Symposium. Can Spec Publ Fish Aquat Sci 106:110–127Google Scholar
  52. Kosten S, Huszar VML, Becarés E, Costa LS, van Donk E, Hansson L-A, Jeppesen E, Kruk C, Lacerot G, Mazzeo N, de Meester L, Moss B, Lürling M, Nõges T, Romo S, Scheffer M (2011) Warmer climates boost cyanobacterial dominance in shallow lakes. Glob Change Biol 18:118–126CrossRefGoogle Scholar
  53. Lampert W, Sommer U (1997) Limnoecology: the ecology of lakes and streams. Oxford University Press, OxfordGoogle Scholar
  54. Lansac-Tôha FA, Bonecker CC, Velho LFM, Simões NR, Dias JD, Alves GM, Takahashi EM (2009) Biodiversity of zooplankton communities in the Upper Paraná River floodplain: Interannual variation from long-term studies. Braz J Biol 69:539–549PubMedCrossRefGoogle Scholar
  55. Laurén-Määttä C, Hietala J, Andwalls M (1997) Responses of Daphnia pulex populations to toxic cyanobacteria. Freshwater Biol 37:635–647CrossRefGoogle Scholar
  56. Loverde-Oliveira SM, Huszar VLM, Mazzeo N, Scheffer M (2009) Hydrology-driven regime shifts in a shallow tropical lake. Ecosystems 12:807–819CrossRefGoogle Scholar
  57. Marker AFH, Nusch A, Rai H, Riemann B (1980) The measurement of photosynthetic pigments in freshwater and standardization of methods: conclusions and recommendations. Archiv Hydrobiol Beihandlung Ergebnisse Limnol 14:91–106Google Scholar
  58. Meerhoff M, Mazzeo N, Moss B, Rodríguez-Gallego L (2003) The structuring role of free-floating versus submerged plants in a subtropical shallow lake. Aquat Ecol 37:377–391CrossRefGoogle Scholar
  59. Meerhoff M, Fosalba C, Bruzzone C, Mazzeo N, Noordoven W, Jeppesen E (2006) An experimental study of habitat choice by Daphnia: plants signal danger more than refuge in subtropical lakes. Freshwater Biol 51:1320–1330CrossRefGoogle Scholar
  60. Meerhoff M, Iglesias C, Teixeira de Mello F, Clemente JM, Jensen E, Lauridsen TL, Jeppesen E (2007a) Effects of habitat complexity on community structure and predator avoidance behaviour of littoral zooplankton in temperate versus subtropical shallow lakes. Freshwater Biol 52:1009–1021CrossRefGoogle Scholar
  61. Meerhoff M, Clemente JM, Teixeira de Mello F, Iglesias C, Pedersen AR, Jeppesen E (2007b) Can warm climate-related structure of littoral predator assemblies weaken the clear water state in shallow lakes? Glob Change Biol 13:1888–1897CrossRefGoogle Scholar
  62. Mihaljević M, Stević F (2011) Cyanobacterial blooms in a temperate river-floodplain ecosystem: the importance of hydrological extremes. Aquat Ecol 45:335–349CrossRefGoogle Scholar
  63. Mihaljević M, Spoljarić D, Stević F, Cvijanović V, Kutuzoví BH (2010) The influence of extreme floods from the River Danube in 2006 on phytoplankton communities in a floodplain lake: shift to a clear state. Limnologica 40:260–268CrossRefGoogle Scholar
  64. Mormul RP, Thomaz SM, Agostinho AA, Bonecker CC, Mazzeo N (2012) Migratory benthic fishes may induce regime shifts in a tropical floodplain pond. Freshwater Biol 57:1592–1602CrossRefGoogle Scholar
  65. Nestler JM, Baigún CRM, Larry NO, Weber J (2007) Contrasting the Middle Paraná and Mississippi Rivers to develop a template for restoring large floodplain river ecosystem. Intl J River Basin Manag 5:305–319CrossRefGoogle Scholar
  66. Netten JJC, Van Zuidam J, Kosten S, Peeters ETHM (2011) Differential response to climatic variation of free-floating and submerged macrophytes in ditches. Freshwater Biol 56:1761–1768CrossRefGoogle Scholar
  67. Nielsen DL, Hillman TJ, Smith FJ, Shiel RJ (2002) The influence of seasonality and duration of flooding on zooplankton in experimental billabongs. River Res Appl 18:227–237CrossRefGoogle Scholar
  68. O’Farrell I, de Tezanos Pinto P, Rodriguez P, Chaparro G, Pizarro H (2009) Experimental evidence of the dynamic effect of free-floating plants on phytoplankton ecology. Freshwater Biol 54:363–375CrossRefGoogle Scholar
  69. O’Farrell I, Izaguirre I, Chaparro G, Unrein F, Sinistro R, Pizarro H, Rodríguez P, de Tezanos Pinto P, Lombardo R, Tell G (2011) Water level as the main driver of the alternation between a free-floating plant and a phytoplankton dominated state: a long-term study in a floodplain lake. Aquat Sci 73:275–287CrossRefGoogle Scholar
  70. Paerl HW, Huisman J (2009) Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ Microbiol Rep 1:27–37PubMedCrossRefGoogle Scholar
  71. Paerl HW, Fulton RS, Moisander PH, Dyble J (2001) Harmful freshwater algal blooms, with an emphasis on Cyanobacteria. Sci World 1:76–113CrossRefGoogle Scholar
  72. Paggi JC, Mendoza RO, Debonis CJ, José de Paggi SB (2001) A simple and inexpensive trap-tube sampler for zooplankton collection in shallow waters. Hydrobiologia 464:45–49CrossRefGoogle Scholar
  73. Paidere J (2009) Influence of flooding frequency on zooplankton in the floodplains of the Daugava River (Latvia). Acta Zool Lit 19:306–313CrossRefGoogle Scholar
  74. Peduzzi P, Aspetsberger F, Hein T, Huber F, Kargl-Wagner S, Luef B, Tachkova Y (2008) Dissolved organic matter (DOM) and bacterial growth in floodplains of the Danube River under varying hydrological connectivity. Fundam Appl Limnol Archiv Hydrobiol 171:49–61CrossRefGoogle Scholar
  75. Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Sys Sci 11:1633–1644CrossRefGoogle Scholar
  76. Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948CrossRefGoogle Scholar
  77. Quirós R (2003) The La Plata river basin. International basin development and riverine fisheries. Second International Symposium on the management of large rivers for fisheries (LARS2). Phnom Penh, Kingdom of Cambodia, 11–14 February 2003Google Scholar
  78. Rennella AM, Quirós R (2006) The effects of hydrology on plankton biomass in shallow lakes of the Pampa Plain. Hydrobiologia 556:181–191CrossRefGoogle Scholar
  79. Robertson AI, Bacon P, Heagney G (2001) The responses of floodplain primary production to flood frequency and timing. J Appl Ecol 38:126–136CrossRefGoogle Scholar
  80. Rodríguez-Gallego LR, Mazzeo N, Gorga J, Meerhoff M, Clemente J, Kruk C, Scasso F, Lacerot G, García J, Quintans F (2004) The effects of an artificial wetland dominated by free-floating plants on the restoration of a subtropical, hypertrophic lake. Lakes Reserv Res Manag 9:203–215CrossRefGoogle Scholar
  81. Ruttner-Kolisko A (1977) Suggestions for biomass calculations of plankton rotifers. Arch Hydrobiol Beih Ergebn Limnol 8:71–76Google Scholar
  82. Scheffer M (1998) Ecology of shallow lakes. Chapman and Hall, LondonGoogle Scholar
  83. Scheffer M (2009) Critical Transitions in nature and Society. Princeton University Press, Princeton and OxfordGoogle Scholar
  84. Scheffer M, van Ness EH (2007) Shallow lakes theory revisited: various alternative regimes driven by climate, nutrients, depth and lake size. Hydrobiologia 584:455–466CrossRefGoogle Scholar
  85. Scheffer M, Hosper SH, Meijer ML, Moss B, Jeppesen E (1993) Alternative equilibria in shallow lakes. Trends Ecol Evol 8:275–279PubMedCrossRefGoogle Scholar
  86. Scheffer M, Szabó S, Gragnani A, van Nes E, Rinaldi S, Kautsky N, Norberg J, Roijackers R, Franken R (2003) Floating plant dominance as a stable state. PNAS 100:4040–4045PubMedCrossRefPubMedCentralGoogle Scholar
  87. Schooler SS, Salau B, Julien MH, Ives AR (2011) Alternative stable states explain unpredictable biological control of Salvinia molesta in Kakadu. Nature 470:86–89PubMedCrossRefGoogle Scholar
  88. Silva Busso A, Santa Cruz J (2005) Distribución de elementos traza en las aguas subterráneas del partido de Escobar, Buenos Aires, Argentina. Ecol Austral 15:31–47Google Scholar
  89. Sinistro R, Sanchez ML, Marinone MC, Izaguirre I (2007) Experimental study of the zooplankton impact on the trophic structure of phytoplankton and the microbial assemblages in a temperate wetland (Argentina). Limnologica 37:88–99CrossRefGoogle Scholar
  90. Sommer U, Gliwicz M, Lampert W, Duncan A (1986) The PEG-model of seasonal succesion of planktonic events in fresh waters. Archiv Hydrobiol 106:433–471Google Scholar
  91. Stević F, Mihaljević M, Spoljarić D (2013) Changes of phytoplankton functional groups in a floodplain lake associated with hydrological perturbations. Hydrobiologia. doi:10.1007/s10750-013-1444-6 Google Scholar
  92. Tockner K, Standford JA (2002) Riverine flood plains: present state and future trends. Environ Conser 3:308–330Google Scholar
  93. Tockner K, Malard F, Ward JV (2000) An extension of the Flood Pulse Concept. Hydrol Process 14:2861–2883CrossRefGoogle Scholar
  94. Unrein F, O’Farrell I, Izaguirre I, Sinistro R, dos Santos Afonso M, Tell G (2010) Phytoplankton response to pH rise in a N-limited floodplain lake: relevance of N2-fixing heterocystous Cyanobacteria. Aquat Sci 72:179–190CrossRefGoogle Scholar
  95. Utermöhl H (1958) Zur vervollkommnung der quantitativen phytoplankton-methodik. Mitteil. Verh Int Ver Theor Angew Limnol 9:1–38Google Scholar
  96. Van Geest GJ, Roozen FCJM, Coops H, Roijackers RMM, Buijse AD, Peeters ETHM, Scheffer M (2003) Vegetation abundance in lowland flood plain lakes determined by surface area, age and connectivity. Freshwater Biol 48:440–454CrossRefGoogle Scholar
  97. Van Geest GJ, Coops H, Scheffer M, van Nes EH (2007) Long transients near the ghost of a stable state in eutrophic shallow lakes with fluctuating water levels. Ecosystems 10:36–46Google Scholar
  98. Wantzen KM, Junk WJ, Rothhaupt K-O (2008) An extension of the Flood Pulse Concept (FPC) for lakes. Hydrobiologia 613:151–170CrossRefGoogle Scholar
  99. White PA, Kalff J, Rasmussen JB, Gasol JM (1991) The effects of temperature and algal biomass on bacterial production and specific growth rate in freshwater and marine habitats. Microb Ecol 21:99–118PubMedCrossRefGoogle Scholar
  100. Williamson CE, Saros JE, Vincent WF, Smol JP (2009) Lakes and reservoirs as sentinels, integrators and regulators of climate change. Limnol Ocenogr 54:2273–2282CrossRefGoogle Scholar
  101. Zalocar de Domitrovic Y (2003) Effect of fluctuations in water level on phytoplankton development in three lakes of the Paraná River floodplain (Argentina). Hydrobiologia 510:175–193CrossRefGoogle Scholar
  102. Zar J (1999) Biostatistical analysis, 4th edn. Prentice Hall, New JerseyGoogle Scholar

Copyright information

© Springer Basel 2014

Authors and Affiliations

  • Griselda Chaparro
    • 1
  • María Soledad Fontanarrosa
    • 1
  • María Romina Schiaffino
    • 1
  • Paula de Tezanos Pinto
    • 1
  • Inés O’Farrell
    • 1
  1. 1.Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y NaturalesUniversidad de Buenos Aires-IEGEBA (CONICET-UBA)Buenos AiresArgentina

Personalised recommendations