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Assessing the relevance of top-down and bottom-up effects as phytoplankton structure drivers in a subtropical hypereutrophic shallow lake

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Abstract

Although several studies explain the trophic cascade in water systems, we lack knowledge about top-down–bottom-up effects on phytoplankton from eutrophic lakes. In this study, we tested the importance of trophic cascades on phytoplankton structure, predicting that environmental variations are the main drivers. We performed a monthly sampling during a year to measure environmental variables, phytoplankton and zooplankton, plus two samplings (winter and summer) to assess fish structure. Furthermore, we analyzed zooplanktivorous fish stomach-gut contents and completed a hatching zooplankton resting egg experiment to assess the effect of fish on dormant populations. We ran a partial redundancy analysis (pRDA) for phytoplankton using zooplankton, nutrient availability and environmental variables as predictor variables. We finally calculated several ratios of the zooplankton:phytoplankton biovolume to assess potential predation effects. Phytoplankton was correlated with variations in temperature and conductivity plus nutrients (pRDA: 63.4%, F = 4.6, P = 0.001) and was dominated alternatively by diatoms and cyanobacteria. Zooplankton was dominated by microphagous rotifers (> 45% of the total biovolume), and only the ratio of microphagous rotifer:small chlorophytes was significant during summer and autumn (F = 10.6, P = 0.005). The fish community was dominated by insectivorous-planktivorous fish (> 65% of total density), yet a negative selection of zooplankton items (Ivlev’s index < 0) was found. Nevertheless, the zooplankton resting stage analysis showed that microphagous Rotifera were dominant (29 species emerged), suggesting a structuring effect of fish on the zooplankton size. We conclude that phytoplankton was mainly controlled by environmental variations plus nutrient availability, while top-down had a less evident effect.

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References

  • Acuña P, Vila I, Marín VH (2008) Short-term responses of phytoplankton to nutrient enrichment and planktivorous fish in a temperate South American mesotrophic reservoir. Hydrobiologia 600:131–138

    Article  CAS  Google Scholar 

  • Alekseev VR (2002) Copepoda. In: Fernando CH (ed) A guide to tropical freshwater zooplankton. Backhuys Publications, Leiden

    Google Scholar 

  • Almirón A, Casciotta J, Cioteck L, Georgis P (2015) Guía de los peces del Parque Nacional Pre-Delta. Administración Parques Nacionales, Buenos Aires

    Google Scholar 

  • APHA (2005) Standard methods for the examination of water and wastewater, 21st edn. American Public Health Association, United States

    Google Scholar 

  • Azzali I, Morozov A, Veturino E (2017) Exploring the role of vertical heterogeneity in the stabilization of planktonic ecosystems under eutrophication. J Biol Syst 25:715–741

    Article  Google Scholar 

  • Baer A, Langdon C, Mills S, Schulz C, Hamre K (2008) Particle size preference, gut filling and evacuation rates of the rotifer Brachionus “Cayman” using polystyrene latex beads. Aquaculture 282:75–82

    Article  Google Scholar 

  • Battauz Y, José de Paggi S, Paggi JC (2014) Passive zooplankton community in dry littoral sediment: reservoir of diversity and potential source of dispersal in a subtropical floodplain lake of the Middle Paraná River (Santa Fe, Argentina). Int Rev Hydrobiol 99:277–286

    Article  Google Scholar 

  • Benndorf J, Böing W, Koop J, Neubauer I (2002) Top-down control of phytoplankton: the role of time scale, lake depth and trophic state. Freshw Biol 47:2282–2295

    Article  Google Scholar 

  • Burson A, Stomp M, Greenwell E, Grosse J, Huisman J (2018) Competition for nutrients and light: testing advances in resource competition with a natural phytoplankton community. Ecology 99:1108–1118

    Article  PubMed  Google Scholar 

  • Carmichael WW, Boyer G (2016) Health impacts from cyanobacteria harmful algae blooms: implications for the North American Great Lakes. Harmful Algae 54:194–212

    Article  PubMed  Google Scholar 

  • Casciotta JA, Becchara J (2005) Peces del Iberá. Hábitat y Diversidad, Grafikar, Argentina

    Google Scholar 

  • Chellappa NT, Medeiros Costa MA (2003) Dominant and co-existing species of Cyanobacteria from a Eutrophicated reservoir of Rio Grande do Norte State, Brazil. Acta Oecol 24:S3–S10

    Article  Google Scholar 

  • Cho SH, Ji SC, Hur SB, Bae J, Park IS, Song YC (2007) Optimum temperature and salinity conditions for growth of green algae Chlorella ellipsoidea and Nannochloris oculata. Fish Sci 73:1050–1056

    Article  CAS  Google Scholar 

  • Cyr H (1998) Cladoceran and copepod-dominated zooplankton communities graze at similar rate in low productivity lakes. Can J Fish Aquat Sci 55:414–422

    Article  Google Scholar 

  • Daliry S, Hallajisani A, Mohammadi Roshandeh J, Nouri H, Golzary A (2017) Investigation of optimal condition for Chlorella vulgaris microalgae growth. Glob J Environ Sci Manag 113:217–230

    Google Scholar 

  • de Ruiter PV, Wolters V, Moore J (2005) Dynamic food webs: multispecies assemblages, ecosystem development, and environmental change. Academic Press, London

    Book  Google Scholar 

  • Devetter M (2009) Clearance rates of the bdelloid rotifer, Habrotrocha thienemanni, a tree-hole inhabitant. Aquat Ecol 43:85–89

    Article  CAS  Google Scholar 

  • 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 19:79–97

    Article  Google Scholar 

  • Frau D, Devercelli M, José de Paggi S, Scarabotti P, Mayora G, Battauz Y, Senn M (2015) Can top-down and bottom-up forces explain phytoplankton structure in a subtropical and shallow groundwater connected lake? Mar Freshw Res 66:1106–1115

    Article  Google Scholar 

  • Frau D, Battauz Y, Sinistro R (2017) Why predation is not a controlling factor of phytoplankton in a Neotropical shallow lake: a morpho-functional perspective. Hydrobiologia 788:115–130

    Article  CAS  Google Scholar 

  • Frau D, de Tezanos Pinto P, Mayora G (2018) Are Cyanobacteria total, specific and trait abundance regulated by the same environmental variables? Ann Limnol Int J Lim. https://doi.org/10.1051/limn/2017030

    Article  Google Scholar 

  • García-Roger EM, Carmona M, Serra MJ (2005) Deterioration patterns in diapausing egg banks of Brachionus (Muller, 1786) rotifer species. J Exp Mar Biol Ecol 314:149–161

    Article  Google Scholar 

  • García-Roger EM, Armengol X, Carmona MJ, Serra M (2008) Assessing rotifer diapausing egg bank diversity and abundance in brackish temporary environments: an ex situ sediment incubation approach. Fundam Appl Limnol 173:79–88

    Article  Google Scholar 

  • Hammer Ø, Harper DA, Ryan PD (2018) PAST-palaeontological statistics, version 3.18. University of Oslo, Norway

    Google Scholar 

  • Havens KE, Beaver JR, East TL (2007) Plankton biomass partitioning in a eutrophic subtropical lake: comparison with results from temperate lake ecosystems. J Plankton Res 29:1087–1097

    Article  CAS  Google Scholar 

  • Heath MR, Speirs DC, Steele JH (2014) Understanding patterns and processes in models of trophic cascades. Ecol Lett 17:101–114

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Huisman JM, Matthijs HCP, Visser PM (2005) Harmful cyanobacteria. Aquatic ecology series 3. Springer, Dordrech

    Book  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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. Freshw Biol 53:1797–1807

    Article  Google Scholar 

  • Iglesias C, Mazzeo N, Meerhoff M, Lacerot G, Clemente JM, Scasso F, Kruk C, Goyenola G et al (2011) High predation is of key importance for dominance of small-bodied zooplankton in warm shallow lakes: evidence from lakes, fish enclosures and surface sediments. Hydrobiologia 667:133–147

    Article  Google Scholar 

  • Ivlev VS (1961) Experimental ecology of the feeding of fishes. Yale University Press, New Haven

    Google Scholar 

  • Jeppesen E, Søndergaard M, Mazzeo N, Meerhoff M, Branco C, Huszar V, Scasso F (2005) Lake restoration and biomanipulation in temperate lakes: relevance for subtropical and tropical lakes. Chapter 11. In: Reddy MV (ed) Tropical eutrophic lakes: their restoration and management. Science Publishers, Enfield, pp 331–359

    Google Scholar 

  • Johansson LS, de Meesteret L (2005) Uncovering hidden species: hatching diapausing eggs for the analysis of cladoceran species richness. Limnol Oceanogr Methods 3:399–407

    Article  Google Scholar 

  • José de Paggi SB, Paggi JC (1995) Determinación de la abundancia y biomasa zooplanctónica. In: Lopretto E, Tell G (eds) Ecosistemas de Aguas Continentales. Metodologías para su estudio. Ediciones Sur, La Plata, pp 315–321

    Google Scholar 

  • Ke Z, Xie P, Guo L, Liu Y, Yang H (2007) In situ study on the control of toxic Microcystis blooms using phytoplanktivorous fish in the subtropical Lake Taihu of China: a large fish pen experiment. Aquaculture 265:127–138

    Article  Google Scholar 

  • Koenings JP, Edmundson JA (1991) Secchi disk and photometer estimates of light regimes in Alaskan lakes: effects of yellow color and turbidity. Limnol Oceanogr 36:91–105

    Article  Google Scholar 

  • Komárek J (2013) Cyanoprokaryota.Teil/3rd part: heterocytous genera. In: Gärtner L, Krienitz M, Chagerl M (eds) Süswasserflora von Mitteleuropa (Freshwater flora of Central Europe). Springer, Berlin

    Google Scholar 

  • Komárek J, Anagnostidis K (1998) Cyanoprokaryota. Teil 1: Chroococcales. In: Ettl H, Gärtner G, Heynig H, Mollenhauer D (eds) Süsswasserflora von Mitteleuropa 19/1. Gustav Fisher Verlag, Stuttgart, p 548 (in German)

    Google Scholar 

  • Komárek J, Anagnostidis K (2005) Cyanoprokaryota. Teil 2: Oscillatoriales. In: Büdel B, Gärtner G, Krienitz L, Schagerl M (eds) Süsswasserflora von Mitteleuropa 19/2. Elsevier, München (in German)

    Google Scholar 

  • Komárek J, Fott B (1983) Chlorophyceae, chlorococcales. In: Huber-Pestalozzi G (ed) Das Phytoplankton des Sdwasswes. Die Binnenggewasser, vol 16(5). Schweizerbart’sche Verlagsbuchhandlung, Stuttgart

    Google Scholar 

  • Korínek V (2002) Cladocera. In: Fernando CH (ed) A guide to tropical freshwater 558 zooplankton. Backhuys Publications, Leiden

    Google Scholar 

  • Kosten S, Huszar LM, Mazzeo N, Scheffer M, Da L, Sternberg SL, Jeppensen E (2009) Lake and watershed characteristics rather than climate influence nutrient limitation in shallow lakes. Ecol Appl 19:1791–1804

    Article  PubMed  Google Scholar 

  • Kozlowsky-Suzuki B, Karjalainen M, Lehtiniemi M, Engström-Öst J, Koski M, Carlsson P (2003) Feeding, reproduction and toxin accumulation by the copepods Acartia bifilosa and Eurytemora affinis in the presence of the toxic cyanobacterium Nodularia spumigena. Mar Ecol Prog Ser 249:237–249

    Article  CAS  Google Scholar 

  • Krammer K, Lange-Bertalot H (1991) Bacillariophyceae. 3. Teil Centrales, Fragilariaceae, Eunotiaceae. In: Ettl H, Gerloff J, Heynig H, Mollenhauer D (eds) Süsswasserflora von Mitteleuropa. Gustav Fischer Verlag, Stuttgart

    Google Scholar 

  • Lacerot G, Kruk C, Luerling M, Scheffer M (2013) The role of subtropical zooplankton as grazers of phytoplankton under different predation levels. Freshw Biol 58:494–503

    Article  Google Scholar 

  • Lazzaro X, Bouvy M, Ribeiro-Filho RA, Oliviera VS, Sales LT, Vasconcelos ARM, Mata MR (2003) Do fish regulate phytoplankton in shallow eutrophic northeast Brazilian reservoirs? Freshw Biol 48:649–668

    Article  Google Scholar 

  • Lee RD (2008) Phycology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Lemmens P, Declerck SAJ, Tuytens K, Vanderstukken M, de Meester L (2018) Bottom-up effects on biomass versus top-down effects on identity: a multiple-lake fish community manipulation experiment. Ecosystems 21:166–177

    Article  Google Scholar 

  • Lepš J, Šmilauer P (1999) Multivariate Analysis of Ecological Data. Faculty of Biological Sciences. University of South Bohemia, Ceské Budejovice

  • Levine SN, Borchardt MA, Braner M, Shambaugh AD (1999) The impact of zooplankton grazing on phytoplankton species composition and biomass in Lake Champlain (USA-Canada). J Great Lakes Res 25:61–77

    Article  Google Scholar 

  • Litchman E, de Tezanos Pinto P, Klausmeier CA, Thomas MK, Yoshiyama K (2010) Linking traits to species diversity and community structure in phytoplankton. Hydrobiologia 653:15–28

    Article  CAS  Google Scholar 

  • Loures de Oliveira Marcionilio SM, Borges Machado K, Melo Carneiro F, Ferreira ME, Carvalho P, Galli Vieira LC, Huszar V, Nabout JC (2016) Environmental factors affecting chlorophyll-a concentration in tropical floodplain lakes, Central Brazil. Environ Monit Assess 188:611

    Article  CAS  Google Scholar 

  • Malone CFS, Santos KRS, Sant’Anna CL (2012) Algas e cianobactérias de ambientes extremos do Pantanal Brasileiro. Oecol Austr 16:745–755

    Article  Google Scholar 

  • McCann K (2011) Foodwebs. Monographs in population biology 50. Princeton University Press, Princeton

    Google Scholar 

  • Merel S, Walker D, Chicana R, Snyder S, Baurès E, Thomas O (2013) State of knowledge and concerns on Cyanobacterial blooms and cyanotoxins. Environ Int 59:303–327

    Article  CAS  PubMed  Google Scholar 

  • Modenutti B (2014) Mixotrophy in Argentina freshwaters. In: Tell G, Izaguirre I, O’Farrell I (eds) Freshwater phytoplankton of Argentina. E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart, pp 359–374

    Google Scholar 

  • Nielsen DL, Smith FJ, Hillman TJ, Shiel RJ (2000) Impact of water regime and fish predation on zooplankton resting egg production and emergence. J Plankton Res 22:433–446

    Article  Google Scholar 

  • Ning NSP, Nielsen D, Hillman TJ, Suter PJ (2010) The influence of planktivorous fish on zooplankton resting-stage communities in riverine slackwater regions. J Plankton Res 32:411–421

    Article  CAS  Google Scholar 

  • Okun N, Brasil JJ, Attayde L, Costa IAS (2008) Omnivory does not prevent trophic cascades in pelagic food webs. Freshw Biol 53:129–138

    Google Scholar 

  • Oliveros OB (1980) Campaña Limnológica “Keratella I” en el río Paraná medio: aspectos tróficos de los peces de ambientes leníticos. Ecologia 4:115–126

    Google Scholar 

  • Paerl HW (2017) Controlling harmful cyanobacterial blooms in a climatically more extreme world: management options and research needs. J Plankton Res 39:763–771

    Article  Google Scholar 

  • Panosso R, Carlsson P, Kozlowsky-Suzuki B, Azevedo SM, Granéli E (2003) Effect of grazing by a neotropical copepod, Notodiaptomus, on a natural cyanobacterial assemblage and on toxic and non-toxic cyanobacterial strains. J Plankton Res 25:1169–1175

    Article  Google Scholar 

  • Rejas D, Declerck S, Auwerkerken J, Tak P, de Meester L (2005) Plankton dynamics in a tropical floodplain lake: fish, nutrients, and the relative importance of bottom-up and top-down control. Freshw Biol 50:52–69

    Article  CAS  Google Scholar 

  • Reynolds CS (1994) The long, the short and the stalled: on the attributes of phytoplankton selected by physical mixing in lakes and rivers. Hydrobiologia 289:9–21

    Article  Google Scholar 

  • Reynolds CS (2006) The ecology of freshwater phytoplankton. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Reynolds CS, Huszar V, Kruk C, Naselli-Flores L, Melo S (2002) Towards a functional classification of the freshwater phytoplankton. J Plankton Res 24:417–428

    Article  Google Scholar 

  • Ruttner-Kolisko A (1977) Suggestions for biomass calculation of plankton rotifers. Arch Hydrobiol 8:71–76

    Google Scholar 

  • Salmaso N, Padisák J (2007) Morpho-Functional Groups and phytoplankton development in two deep lakes (Lake Garda, Italy and Lake Stechlin, Germany). Hydrobiologia 578:97–112

    Article  Google Scholar 

  • Saros JE, Fritz SC (2000) Nutrients as a link between ionic concentration/composition and diatom distributions in saline lakes. J Paleolimnol 23:449–453

    Article  Google Scholar 

  • Scarabotti PA, López JA, Pouilly M (2011) Flood pulse and the dynamics of fish assemblage structure from neotropical floodplain lakes. Ecol Freshw Fish 20:605–618

    Article  Google Scholar 

  • Scarabotti PA, Demonte LD, Pouilly M (2017) Climatic seasonality, hydrological variability, and geomorphology shape fish assemblage structure in a subtropical floodplain. Freshw Sci 36:653–668

    Article  Google Scholar 

  • Scasso F, Mazzeo N, Gorga J, Kruk C, Lacerot G, Clemente J, Fabián D, Bonilla S (2001) Limnological changes of a subtropical shallow hypertrophic lake during its restoration. Two years of whole-lake experiments aquatic conservation. Mar Freshw Ecosyst 11:31–44

    Article  Google Scholar 

  • Tell G, Conforti V (1986) Euglenophyta pigmentadas de Argentina. Bibliotheca Phycologica 75:1–301

    Google Scholar 

  • ter Braak CJ, Šmilauer P (2012) Canoco reference manual and user’s guide: software for ordination, version 5.0. Microcomputer Power, United States

  • Tonk L, Bosch K, Visser PM, Huisman VJ (2007) Salt tolerance of the harmful cyanobacterium Microcystis aeruginosa. Aquat Microb Ecol 46:117–123

    Article  Google Scholar 

  • UNESCO (2006) Evaluación de los Recursos Hídricos. Elaboración del balance hídrico integral por cuencas hidrográficas. Documentos Técnicos del PHI-LAC, N°4. UNESCO, Uruguay

  • Utermöhl H (1958) ZurVervollkommnung der quantitative Phytoplankton: methodik. Mitt Int Verein Theor Angew 9:1–38

    Google Scholar 

  • Vandekerkhove J, Declerck S, Brendonck L, Conde-Porcuna JM, Jeppesen E, Von Rückert G, Giani G (2008) Biological interactions in the plankton community of a tropical eutrophic reservoir: is the phytoplankton controlled by zooplankton? J Plankton Res 30:1157–1168

    Article  CAS  Google Scholar 

  • Venrick EL (1978) How many cells to count? In: Von Sournia A (ed) Phytoplankton manual. UNSECO, Paris, pp 167–180

    Google Scholar 

  • Von Rückert G, Giani G (2008) Biological interactions in the plankton community of a tropical eutrophic reservoir: is phytoplankton controlled by zooplankton? J Plankton Res 30:1157–1168

    Article  CAS  Google Scholar 

  • Zalocar de Domitrovic Y, Maidana NI (1997) Taxonomic and ecological studies of the Parana River diatom flora (Argentina). In: Lange-Bertalot F, Kociolek P (eds) Bibliotheca Diatomologica. Cramer, Berlin

    Google Scholar 

Download references

Acknowledgements

We thank C. de Bonis for his assistance in the field and Dr. P. de Tezanos Pinto for language assistance. This manuscript was also improved by the suggestions of anonymous reviewers and was supported by the SECTEI 2010-044-13 project awarded by Secretaría de Ciencia y Técnica de la Provincia de Santa Fe (Argentina) and by the PICT-2013 no. 214-14 project awarded by Agencia Nacional de Promoción Científica y Tecnológica.

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Frau, D., Battauz, Y., Alvarenga, P.F. et al. Assessing the relevance of top-down and bottom-up effects as phytoplankton structure drivers in a subtropical hypereutrophic shallow lake. Aquat Ecol 53, 265–280 (2019). https://doi.org/10.1007/s10452-019-09687-3

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