Aquatic Ecology

, Volume 53, Issue 2, pp 303–314 | Cite as

Epipelon responses to N and P enrichment and the relationships with phytoplankton and zooplankton in a mesotrophic reservoir

  • Diego Alberto Tavares
  • Richard Wilander Lambrecht
  • Maria Carolina de Almeida Castilho
  • Raoul Henry
  • Carla FerragutEmail author


The phototrophic epipelon has been suggested to play an important role in ecosystems, especially those with shallow depths; however, only a few studies have investigated this function. Nutrient availability has been shown to be a determining factor for autotrophic interactions and can potentially interfere with the food web, as eutrophication. Thus, we evaluated the responses of epipelon, phytoplankton and zooplankton to combined and isolated N and P addition, during the enrichment period (14 days) and after 12 days with no enrichment. It was hypothesized that P addition (the limiting nutrient) should decrease the photosynthetic potential of the epipelon, due to the rapid increase in phytoplankton and zooplankton biomass, which can strongly attenuate light, and that the opposite effect would be observed after a period with no enrichment. We developed an in situ experiment with combined and isolated N and P enrichment at open-bottom mesocosms. The addition of P, individually and combined, augmented phytoplankton chlorophyll-a concentrations during the enrichment period, while zooplankton density only responded positively after day 14. After 12 days with no enrichment, the phytoplankton chlorophyll-a and zooplankton density decreased. While P enrichment had no significant effect on epipelon chlorophyll-a, there was a significant increase in the photosynthetic potential detected 12 days after the enrichment was stopped. In conclusion, the present study demonstrated that P enrichment reduces the photosynthetic potential of epipelon, and that variations in nutrient availability can modulate relationships among phytoplankton, zooplankton and epipelon. Drastic changes in the growth and development of the phototrophic epipelon, due to the input of nutrients, could directly impact the functioning of shallow tropical lakes and reservoirs.


Chlorophyll-a concentrations N and P enrichment Open-bottomed mesocosms Zooplankton density 



The authors would like to acknowledge the FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo) for financial support (Grant No. 2009/52253-4) and for a scholarship to DAT and RWL (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - CAPES). We are grateful to all the students and technicians involved in the laboratory and fieldwork.


  1. Arndt H (1993) Rotifers as predators on components of the microbial web (bacteria, heterotrophic flagellates, ciliates) a review. Hydrobiologia 255(256):231–246CrossRefGoogle Scholar
  2. Bicudo CEM, Carmo CF, Bicudo DC, Henry R, Pião ACS, Santos CM, Lopes MRM (2002) Morfologia e morfometria de três reservatórios do PEFI. In: Bicudo DC, Forti MC, Bicudo CEM (eds) Parque Estadual das Fontes do Ipiranga: unidade de conservação ameaçada pela urbanização de São Paulo. Editora Secretaria do Meio Ambiente do Estado de São Paulo, São Paulo, pp 141–158Google Scholar
  3. Cano MG, Casco MA, Solari LC, Mac Donagh ME, Gabellone NA, Claps MC (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(1):33–45CrossRefGoogle Scholar
  4. Cano MG, Casco MA, Claps MC (2016) Epipelon dynamics in a shallow lake through a turbid-and a clear-water regime. J Limnol 75(2):355–368Google Scholar
  5. Dodds WK (2003) The role of periphyton in phosphorous retention in shallow freshwater aquatic systems. J Phycol 39:840–849CrossRefGoogle Scholar
  6. Fanta SE, Hill WR, Smith TB, Roberts BJ (2010) Applying the light:nutrient hypothesis to stream periphyton. Freshw Biol 55:931–940CrossRefGoogle Scholar
  7. Fernández R, Alcocer J (2017) Cyanobacteria consumption by cladocerans: a case study on facilitation. Aquat Ecol. Google Scholar
  8. Fernando CH (2002) Guide to tropical freshwater zooplankton: identification, ecology and impact on fisheries. In Guide to tropical freshwater zooplankton: identification, ecology and impact on fisheries. BackhuysGoogle Scholar
  9. Ferragut C, Bicudo DC (2010) Periphytic algal community adaptive strategies in N and P enriched experiments in a tropical oligotrophic reservoir. Hydrobiologia 646(1):295–309CrossRefGoogle Scholar
  10. Fonseca BM, Bicudo CEM (2011) Phytoplankton seasonal and vertical variations in a tropical shallow reservoir with abundant macrophytes (Ninfeias Pond, Brazil). Hydrobiologia 665:229–245CrossRefGoogle Scholar
  11. Fryer G (1986) Structure, function and behaviour, and the elucidation of evolution in copepods and other crustaceans. Syllogeus 58:150–157Google Scholar
  12. Genkai-Kato M, Vadeboncoeur Y, Liboriussen L, Jeppesen E (2012) Benthic–planktonic coupling, regime shifts, and whole-lake primary production in shallow lakes. Ecology 93(3):619–631CrossRefGoogle Scholar
  13. Golterman HL, Clymo RS, Ohmstad MAM (1978) Methods for physical and chemical analysis of freshwaters. International biological programmer (handbook 8), 2ª edn. Blackwell Scientific Publications, OxfordGoogle Scholar
  14. Hansson LA (1988) Effects of competitive interactions on the biomass development of planktonic and periphytic algae in lakes. Limnol Oceanogr 33(1):121–128CrossRefGoogle Scholar
  15. Havens KE, East TL, Rodusky AJ, Sharfstein B (1999) Littoral periphyton responses to nitrogen and phosphorus: an experimental study in a subtropical lake. Aquat Bot 63(3–4):267–290CrossRefGoogle Scholar
  16. Hill WR, Roberts BJ, Francoeur SN, Fanta SE (2011) Resource synergy in stream periphyton communities. J Ecol 99:454–463Google Scholar
  17. Hillebrand H (2002) Top-down versus bottom-up control of autotrophic biomass a meta-analysis on experiments with periphyton. J N Am Benthol Soc 21(3):349–369CrossRefGoogle Scholar
  18. Hwang SJ, Havens KE, Steinman AD (1998) Phosphorus kinetics of planktonic and benthic assemblages in a shallow subtropical lake. Freshw Biol 40(4):729–745CrossRefGoogle Scholar
  19. Johnston CA (1991) Sediment and nutrient retention by freshwater wetlands: effects on surface water quality. Crit Rev Environ Sci Technol 21(5–6):491–565Google Scholar
  20. Liboriussen L, Jeppesen E (2003) Temporal dynamics in epipelic, pelagic and epiphytic algal production in a clear and a turbid shallow lake. Freshw Biol 48:418–431CrossRefGoogle Scholar
  21. Liboriussen L, Jeppesen E (2006) Structure, biomass, production and depth distribution of periphyton on artificial substratum in shallow lakes with contrasting nutrient concentrations. Freshw Biol 51:95–109CrossRefGoogle Scholar
  22. Mackereth FJH, Heron J, Talling JF (1978) Water analysis: some revised methods for limnologists. Freshwater Biological Association, LondonGoogle Scholar
  23. Pasternak A, Hillebrand H, Flöder S (2009) Competition between benthic and pelagic microalgae for phosphorus and light–long-term experiments using artificial substrates. Aquat Sci 71(2):238–249CrossRefGoogle Scholar
  24. Poulíčková A, Hašler P, Lysáková M, Spears B (2008) The ecology of freshwater epipelic algae: an update. Phycologia 47(5):437–450CrossRefGoogle Scholar
  25. Poulíčková A, Dvořák P, Mazalová P, Hašler P (2014) Epipelic microphototrophs: an overlooked assemblage in lake ecosystems. Freshw Sci 33(2):513–523CrossRefGoogle Scholar
  26. Rautio M, Vincent WF (2006) Benthic and pelagic food resources for zooplankton in shallow high-latitude lakes and ponds. Freshw Biol 51(6):1038–1052CrossRefGoogle Scholar
  27. Ruttner-Kollisko A (1974) Rotatoria. Supplement. Die Binnengewässer 27(1):146Google Scholar
  28. Sanches LF, Guariento RD, Caliman A, Bozelli RL, Esteves FA (2011) Effects of nutrients and light on periphytic biomass and nutrient stoichiometry in a tropical black-water aquatic ecosystem. Hydrobiologia 669(1):35–44CrossRefGoogle Scholar
  29. Santos SAM, Santos TR, Furtado MS, Henry R, Ferragut C (2017) 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 19:209–218CrossRefGoogle Scholar
  30. Sartory DP, Grobbelaar JU (1984) Extraction of chlorophyll a from freshwater phytoplankton for spectrophotometric analysis. Hydrobiologia 114:177–187CrossRefGoogle Scholar
  31. Solorzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceanogr 14:799–801CrossRefGoogle Scholar
  32. Strickland JDH, Parsons TR (1960) A manual of seawater analysis. J Fish Res Board Can 125:1–185Google Scholar
  33. Vadeboncoeur Y, Lodge DM (2000) Periphyton production on wood and sediment: substratum-specific response to laboratory and whole-lake nutrient manipulations. J N Am Benthol Soc 19:68–81CrossRefGoogle Scholar
  34. Vadeboncoeur Y, Lodge DM, Carpenter SR (2001) Whole-lake fertilization effects on distribution of primary production between benthic and pelagic habitats. Ecology 82(4):1065–1077CrossRefGoogle Scholar
  35. Vadeboncoeur Y, Vander Zanden MJ, Lodge DM (2002) Putting the lake back together: reintegrating benthic pathways into lake food web models. Bioscience 52:44–54CrossRefGoogle Scholar
  36. Vadeboncoeur Y, Jeppesen E, Zanden MJV, Schierup HH, Christoffersen K, Lodge DM (2003) From Greenland to green lakes: cultural eutrophication and the loss of benthic pathways in lakes. Limnol Oceanogr 48:1408–1418CrossRefGoogle Scholar
  37. Vadeboncoeur Y, Devlin SP, McIntyre PB, Vander Zanden MJ (2014) Is there light after depth? Distribution of periphyton chlorophyll and productivity in lake littoral zones. Freshw Sci 33(2):524–536CrossRefGoogle Scholar
  38. Valderrama GC (1981) The simultaneous analysis of total nitrogen and total phosphorus in natural waters. Mar Chem 10:109–112CrossRefGoogle Scholar
  39. Vogt RA, Ignoffo TR, Sullivan LJ, Herndon J, Stillman JH, Kimmerer WJ (2013) Feeding capabilities and limitations in the nauplii of two pelagic estuarine copepods, Pseudodiaptomus marinus and Oithona davisae. Limnol Oceanogr 58(6):2145–2157CrossRefGoogle Scholar
  40. Wetzel RG, Likens GE (1991) Limnological analyses. Springer, New YorkCrossRefGoogle Scholar
  41. Yoshida T, Urabe J, Elser JJ (2003) Assessment of ‘top-down’ and ‘bottom-up’ forces as determinants of rotifer distribution among lakes in Ontario, Canada. Ecol Res 18(6):639–650CrossRefGoogle Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Programa de Pós-Graduação em Biodiversidade e Meio AmbienteInstituto de BotânicaSão PauloBrazil
  2. 2.Instituto de Botânica, Núcleo de Pesquisas em EcologiaSão PauloBrazil
  3. 3.Departamento de Zoologia, Instituto de Biociências, Campus de BotucatuUniversidade Estadual Paulista - UNESPRubião Júnior, BotucatuBrazil

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