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Relationship between epipelon, epiphyton and phytoplankton in two limnological phases in a shallow tropical reservoir with high Nymphaea coverage


Macrophytes and phytoplankton are recognized as having roles in determining alternative stable states in shallow lakes and reservoirs, while the role of periphyton has been poorly investigated. Temporal and spatial variation of phytoplankton, epipelon and epiphyton was examined in a shallow reservoir with high abundance of aquatic macrophytes. The relationships between algae communities and abiotic factors, macrophyte coverage and zooplankton density were also analyzed. Monthly sampling was performed in three zones of the depth gradient of the reservoir. Two phases of algal dominance were found: a phytoplankton phase and epipelon phase. The phase of phytoplankton dominance was characterized by high macrophyte coverage. Rotifera was the dominant zooplankton group in all the zones. Flagellate algae were dominant in phytoplankton, epipelon and epiphyton. Macrophyte coverage was found to be a predictor for algal biomass. Changes in biomass and species composition were associated with macrophyte cover variation, mainly the Nymphaea. In addition to the abiotic factors, the macrophyte coverage was a determining factor for changes to the algal community, contributing to the alternation between dominance phases of phytoplankton and epipelon. The macrophyte–phytoplankton–periphyton relationship needs to be further known in shallow reservoirs, especially the role of epipelon as an alternate stable state.

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Fig. 1

Modified from Bicudo et al. (2007)

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  1. APHA, 2005. Standard Methods for Examination of Water and Wastewater. American Public Health Association WWA, Washington, DC.

  2. Beisner, B. E., D. T. Haydon & K. Cuddington, 2003. Alternative stable states in ecology. Frontiers in Ecology and the Environment 1: 376–382.

  3. Bicudo, D. C., B. M. Fonseca, L. M. Bini, L. O. Crossetti, C. E. M. Bicudo & T. Araújo-Jesus, 2007. Undesirable side-effects of water hyacinth control in a shallow tropical reservoir. Freshwater Biology 52: 1120–1133.

  4. Cano, M. G., M. A. Casco, L. C. Solari, M. E. MacDonagh, N. A. Gabellone & M. C. Claps, 2008. Implications of rapid changes in chlorophyll-a of plankton, epipelon, and epiphyton in a Pampean shallow lake: an interpretation in terms of a conceptual model. Hydrobiologia 614: 33–45.

  5. Casartelli, M. R. & C. Ferragut, 2015. Influence of seasonality and rooted aquatic macrophyte on periphytic algal community on artificial substratum in a shallow tropical reservoir. International Review of Hydrobiology 100: 1–11.

  6. Casco, M. A., M. E. Mac Donagh, M. G. Cano, L. Solari, M. C. Claps & N. Gabellone, 2009. Phytoplankton and epipelon responses to clear and turbid phases in a seepage lake (Buenos Aires, Argentina). International Review of Hydrobiology 94: 153–168.

  7. Castro, R. J. D., R. Henry, C. Ferragut & M. Casartelli, 2018. Comparing lacustrine environments: the importance of the kind of habitat on the structure of fishes. Acta Limnologica Brasiliensia. https://doi.org/10.1590/s2179-975x13417.

  8. Eaton, J. W. & B. Moss, 1966. The estimations of numbers and pigment content in epipelic algal populations. Limnology and Oceanography 11: 584–595.

  9. Fernando, C. H., 2002. Guide to tropical freshwater zooplankton: identification, ecology and impact on fisheries. In Guide to Tropical Freshwater Zooplankton: Identification, Ecology and Impact on Fisheries. Backhuys, Leiden.

  10. Fonseca, B. M., C. Ferragut, A. Tucci, L. O. Crossetti, F. Ferrari, D. C. Bicudo, C. L. Sant’Anna & C. E. M. Bicudo, 2014. Biovolume de cianobactérias e algas de reservatórios tropicais do Brasil com diferentes estados tróficos. Hoehnea 41(1): 9–30.

  11. Genkai-Kato, M., Y. Vadeboncoeur, L. Liboriussen & E. Jeppesen, 2012. Benthic–planktonic coupling, regime shifts, and whole-lake primary production in shallow lakes. Ecology 93: 619–631.

  12. Goldsborough, L. G. & G. G. C. Robinson, 1996. Pattern in wetlands. In Stevenson, R. J., M. L. Bothwell & R. L. Lowe (eds), Algal Ecology: Freshwater Benthic Ecosystems. Academic, San Diego: 77–117.

  13. Hammer, O., D. A. T. Harper & P. D. Ryan, 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4: 1–9.

  14. Hillebrand, H., C. D. Dürselen, D. Kirschtel, U. Pollingher & T. Zohary, 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35: 403–424.

  15. Hilt, S., 2015. Regime shifts between macrophytes and phytoplankton – concepts beyond shallow lakes, unravelling stabilizing mechanisms and practical consequences. Limnética 34: 467–480.

  16. Hobbs, W. O., J. M. Ramstack Hobbs, T. Lafrançois, K. D. Zimmer, K. M. Theissen, M. B. Edlund, N. Michelutti, M. G. Butler, M. A. Hanson & T. J. Carlson, 2012. A 200-year perspective on alternative stable state theory and lake management from a biomanipulated shallow lake. Ecology Applications 22: 1483–1496.

  17. Iglesias, C., G. Goyenola, N. Mazzeo, M. Meerhoff, E. Rodo & E. Jeppesen, 2007. Horizontal dynamics of zooplankton in subtropical Lake Bianca (Uruguay) hosting multiple zooplankton predators and aquatic plant refuges. Hydrobiologia 584: 179–189.

  18. Jansson, M., P. Blomqvist, A. Jonsson & A. K. Bergström, 1996. Nutrient limitation of bacterioplankton, autotrophic and mixotrophic phytoplankton, and heterotrophic nanoflagellates in Lake Örträsket. Limnology and Oceanography 41: 1552–1559.

  19. Kosten, S. G., E. Jeppesen, D. Motta Marques, E. H. van Nes, N. Mazzeo & M. Scheffer, 2009. Effects of submerged vegetation on water clarity across climates. Ecosystems 12: 1117–1129.

  20. Legendre, P. & L. Legendre, 2012. Numerical Ecology. Elsevier Science Publication, London.

  21. Liboriussen, L. & E. Jeppesen, 2003. Temporal dynamics in epipelic, pelagic and epiphytic algal production in a clear and a turbid shallow lake. Freshwater Biology 48: 418–431.

  22. Margalef, R., 1983. La imprecisa frontera entre el plâncton y otros tipos de comunidades. In Azevedo, M. T. P., Santos, D. P., Sormus, L., Menezes, M., Fujii, M. T., Yokoya, N. S., Senna P. A. C. & Guimarães, S. M. P. B. (eds), Anais do 4º Congresso Latino-Americano, 2ª Reunião Ibero-Americana, 7ª Reunião Brasileira de Ficologia, Caxambu: 319–326.

  23. McCune, B. & M. J. Mefford, 2011. PC-ORD. Multivariate analysis of ecological data.

  24. O’Farrell, I., I. Izaguirre, G. Chaparro, F. Unrein, R. Sinistro, H. Pizarro, P. Rodriguez, P. T. Pinto, R. Lombardo & G. Tell, 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. Aquatic Sciences 73: 275–287.

  25. Olrik, K., 1998. Ecology of mixotrophic flagellates with special reference to Chrysophyceae in Danish lakes. In Phytoplankton and Trophic Gradients. Springer, Dordrecht: 329–338.

  26. Olsen, S., F. Chan, W. Li, S. Zhao, M. Søndergaard & E. Jeppesen, 2015. Strong impact of nitrogen loading on submerged macrophytes and algae: a long-term mesocosm experiment in a shallow Chinese lake. Freshwater Biology 60: 1525–1536.

  27. Padial, A. A. & S. M. Thomaz, 2008. Prediction of the light attenuation coefficient through the Secchi disk depth: empirical modeling in two large Neotropical ecosystems. Limnology 9: 143–151.

  28. Passarge, J., S. Hol, M. Escher & J. Huisman, 2006. Competition for nutrients and light: stable coexistence, alternative stable states, or competitive exclusion? Ecological Monographs 76: 57–72.

  29. Pellegrini, B. G. & C. Ferragut, 2018. Association between epiphyton species composition and macrophyte diversity in a shallow tropical reservoir. Fundamental and Applied Limnology 191: 111–122.

  30. Poulíčková, A., P. Dvořák, P. Mazalová & P. Hašler, 2014. Epipelic microphototrophs: an overlooked assemblage in lake ecosystems. Freshwater Science 33: 513–523.

  31. Robinson, G. G., S. E. Gurney & L. G. Goldsborough, 1997. Response of benthic and planktonic algal biomass to experimental water-level manipulation in a prairie lakeshore wetland. Wetlands 17: 167–181.

  32. Sand-Jensen, K. & J. Borum, 1991. Interactions among phytoplankton periphyton and macrophytes in temperate freshwaters and estuaries. Aquatic Botany 41: 137–175.

  33. Santos, S. A. M., T. R. Santos, M. S. Furtado, R. Henry & C. Ferragut, 2018. Periphyton nutrient content, biomass and algal community on artificial substrate: response to experimental nutrient enrichment and the effect of its interruption in a tropical reservoir. Limnology 19: 209–218.

  34. Sartory, D. P. & J. U. Grobbelaar, 1984. Extraction of chlorophyll a from freshwater phytoplankton for spectrophotometric analysis. Hydrobiologia 114: 177–187.

  35. Sayer, C. D., T. A. Davidson & J. I. Jones, 2010. Seasonal dynamics of macrophytes and phytoplankton in shallow lakes: a eutrophication-driven pathway from plants to plankton? Freshwater Biology 55: 500–513.

  36. Scheffer, M. & E. H. van Nes, 2007. Shallow lakes theory revisited: various alternative regimes driven by climate, nutrients, depth and lake size. Hydrobiologia 584: 455–466.

  37. Scheffer, M., S. H. Hosper, M. L. Meijer, B. Moss & E. Jeppesen, 1993. Alternative equilibria in shallow lakes. Trends in Ecology and Evolution 8: 275–279.

  38. Schindler, D. E. & M. D. Scheuerell, 2002. Habitat coupling in lake ecosystems. Oikos 98: 177–189.

  39. Sommer, U., 1988. Some size relationships in phytoflagellate motility. Hydrobiologia 161: 125–131.

  40. Souza, M. L., B. G. Pellegrini & C. Ferragut, 2015. Periphytic algal community structure in relation to seasonal variation and macrophyte richness in a shallow tropical reservoir. Hydrobiologia 755: 183–196.

  41. Tezanos-Pinto, P. & I. O’Farrell, 2014. Regime shifts between free-floating plants and phytoplankton: a review. Hydrobiologia 740: 13–24.

  42. Thomas, S., P. Cecchi, D. Corbin & J. Lemoalle, 2000. The different primary producers in a small African tropical reservoir during a drought: temporal changes and interactions. Freshwater Biology 45: 43–56.

  43. Thomaz, S. M., L. M. Bini & T. A. Pagioro, 2004. Métodos em Limnologia: macrófitas aquáticas. In Bicudo, C. E. & D. C. Bicudo (eds), Amostragem em Limnologia. Editora Rima, São Carlos: 193–212.

  44. Vadeboncoeur, Y. & M. E. Power, 2017. Attached algae: the cryptic base of inverted trophic pyramids in freshwaters. Annual Review of Ecology, Evolution, and Systematics 48: 255–279.

  45. Vadeboncoeur, Y. & A. D. Steinman, 2002. Periphyton function in lake ecosystems. The World Journal 2: 1–20.

  46. Vadeboncoeur, Y., D. M. Lodge & S. R. Carpenter, 2001. Whole-lake fertilization effects on distribution of primary production between benthic and pelagic habitats. Ecology 82: 1065–1077.

  47. Yang, H., R. J. Flower & R. W. Battarbee, 2009. Influence of environmental and spatial variables on the distribution of surface sediment diatoms in an upland loch, Scotland. Acta Botanica Croatica 68: 367–380.

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The authors thank Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for doctoral grants for TRS (Grant No. 2013/03130-2) and financial support (Grant No. 2009/52253-4). The authors are very grateful to the students and technicians involved in the laboratory work and in the field.

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Correspondence to Carla Ferragut.

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dos Santos, T.R., Castilho, M.C., Henry, R. et al. Relationship between epipelon, epiphyton and phytoplankton in two limnological phases in a shallow tropical reservoir with high Nymphaea coverage. Hydrobiologia 847, 1121–1137 (2020). https://doi.org/10.1007/s10750-019-04172-2

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  • Autotroph interactions
  • Algal communities
  • Macrophyte coverage
  • Pelagic and littoral zones
  • Zooplankton