Skip to main content

Advertisement

Log in

Microbial food-web components in two hypertrophic human-impacted Pampean shallow lakes: interactive effects of environmental, hydrological, and temporal drivers

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Few studies have intensively assessed the dynamic of all planktonic components and their microbial communities in hypertrophic shallow lakes. The aim of this work was to study the potential drivers shaping the microbial food-web components (heterotrophic bacteria and strictly phototrophic microplankton). Thus, we studied the monthly abundances and functional groups of the different planktonic food-web components (heterotrophic bacteria, picocyanobacteria, picoeukaryotes, heterotrophic flagellates, ciliates, phytoplankton, zooplankton) in two interconnected and hypertrophic Pampean shallow lakes (Gómez and Carpincho) during dry–wet periods (27-month study). We hypothesized that temporal (intra and inter-annual) factors exert a major role in shaping the microbial food-web components in both lakes. Both shallow lakes showed similar dynamic in the environmental variables, that followed inter-annual and seasonal variations. In Gómez, the variation of microbial components was mainly explained by a combination of environmental, predation, and temporal factors (38.2%), whereas in Carpincho by pure temporal drivers (31.8%). Microbial and predator components were significantly different between dry and wet periods. The connection and closeness between both lakes seem not to play a major role in the factors driving the microbial component abundances. These lakes are strongly influenced by temporal factors, which regulate not only the microbial components, but also the physical, chemical, and biological variables.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Anderson, M. J. & D. C. I. Walsh, 2013. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersion: what null hypothesis are you testing? Ecological Monographs 83: 557–574.

    Google Scholar 

  • APHA, 2005. Standard Methods for the Examination of Water & Wastewaters. American Public Health Association, Washington.

    Google Scholar 

  • Azam, F. & F. Malfatti, 2007. Microbial structuring of marine ecosystems. Nature Reviews Microbiology 5: 782–791.

    CAS  PubMed  Google Scholar 

  • Azam, F., T. Fenchel, J. Field, J. Gray, L. Meyer-Reil & F. Thingstad, 1983. The ecological role of water-column microbes in the sea. Marine Ecology Progress Series 10: 257–263.

    Google Scholar 

  • Baho, D. L., M. N. Futter, R. K. Johnson & D. G. Angeler, 2015. Assessing temporal scales and patterns in time series: comparing methods based on redundancy analysis. Ecological Complexity 22: 162–168.

    Google Scholar 

  • Baranyi, C., T. Hein, C. Holarek, S. Keckeis & F. Schiemer, 2002. Zooplankton biomass and community structure in a Danube River floodplain system: effects of hydrology. Freshwater Biology 47: 473–482.

    Google Scholar 

  • Bautista-Reyes, F. & M. Macek, 2012. Ciliate food vacuole content and bacterial community composition in the warm-monomictic crater Lake Alchichica, México. Microbial Ecology 79: 85–97.

    CAS  Google Scholar 

  • Blanchet, F. G., P. Legendre & D. Borcard, 2008. Modelling directional spatial processes in ecological data. Ecological Modelling 215: 325–336.

    Google Scholar 

  • Blanchet, G., P. Legendre & O.Gauthier, 2015. AEM: Tools to construct Asymmetric eigenvector maps (AEM) spatial variables. R package version 0.6. http://R-Forge.R-project.org.

  • Błędzki, L. A. & A. M. Ellison, 2000. Effects of water retention time on zooplankton of shallow rheolimnic reservoirs. Verh Internat Verein Limnol 27: 2865–2869.

    Google Scholar 

  • Borcard, D., P. Lengendre & P. Drapeau, 1992. Partialling out the spatial component of ecological variation. Ecology 73: 1045–1055.

    Google Scholar 

  • Bouvy, M., S. M. Nascimento, R. J. R. Molica, A. Ferreira, V. Huszar & S. M. F. O. Azevedo, 2003. Limnological features in Tapacurá reservoir (Northeast Brazil) during a severe drought. Hydrobiologia 493: 115–130.

    CAS  Google Scholar 

  • Brown, B. L., E. R. Sokol, J. Skelton & B. Tornwall, 2017. Making sense of metacommunities: dispelling the mythology of a metacommunity typology. Oecologia 183: 643–652.

    PubMed  Google Scholar 

  • Burns, C. W. & L. M. Galbraith, 2006. Relating planktonic microbial food web structure in lentic freshwater ecosystems to water quality and land use. Journal of Plankton Research 29: 127–139.

    Google Scholar 

  • Callieri, C., 2007. Picophytoplankton in freshwater ecosystems: the importance of small-sized phototrophs. Freshwater Reviews 1: 1–28.

    Google Scholar 

  • Callieri, C. & M. L. Pinolini, 1995. Picoplankton in Lake Maggiore, Italy. Internationale Revue der Gesamten Hydrobiologie 80: 491–501.

    Google Scholar 

  • Canevari, P., D. E. Blanco, E. H. Bucher, G. Castro, & I. Davidson, 1999. Los humedales de la Argentina. Clasificación, situación actual, conservación y legislación, 2 da ed. Wetlands International Publicación N846, Buenos Aires, Argentina.

  • Chaparro, G., M. C. Marinone, R. Lombardo, M. R. Schiaffino, A. Guimarães & I. O’Farrell, 2011. Zooplankton succession during extraordinary drought–flood cycles: a case study in a South American floodplain lake. Limnologica 4: 371–381.

    Google Scholar 

  • Chaparro, G., M. S. Fontanarrosa, M. R. Schiaffino, P. de Tezanos Pinto & I. O’Farrell, 2014. Seasonal-dependence in the responses of biological communities to flood pulses in warm temperate floodplain lakes: implications for the “alternative stable states” model. Aquatic Sciences 76: 579–594.

    CAS  Google Scholar 

  • Claps, M. C., N. A. Gabellone & H. H. Benítez, 2004. Zooplankton biomass in an eutrophic shallow lake (Buenos Aires, Argentina): spatio-temporal variations. Annales de Limnologie 40: 201–210.

    Google Scholar 

  • Clarke, K. R., 1993. Nonparametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18: 117–143.

    Google Scholar 

  • Colina, M., D. Calliari, C. Carballo & C. Kruk, 2016. A trait-based approach to summarize zooplankton-phytoplankton interactions in freshwaters. Hydrobiologia 767: 221–233.

    CAS  Google Scholar 

  • Conty, A. & E. Bécares, 2013. Unimodal patterns of microbial communities with eutrophication in Mediterranean shallow lakes. Hydrobiologia 700: 257–265.

    Google Scholar 

  • Cotner, J. B. & B. A. Biddanda, 2002. Small players, large role: microbial influence on biogeochemical processes in pelagic aquatic ecosystems. Ecosystems 5: 105–121.

    CAS  Google Scholar 

  • Dickman, M., 1969. Some effects of lake renewal on phytoplankton productivity and species composition. Limnology and Oceanography 14: 660–666.

    Google Scholar 

  • Diovisalvi, N., V. Y. Bohn, M. C. Piccolo, G. M. E. Perillo, C. Baigún & H. E. Zagarese, 2015. Shallow lakes from the Central Plains of Argentina: an overview and worldwide comparative analysis of their basic limnological features. Hydrobiologia 752: 5–20.

    CAS  Google Scholar 

  • Domingues, C. D., L. H. da Silva, L. M. Rangel, L. de Magalhães, A. de Melo Rocha, L. M. Lobão, R. Paiva, F. Roland, et al., 2017. Microbial food-web drivers in tropical reservoirs. Microbial Ecology 73: 505–520.

    PubMed  Google Scholar 

  • Domis, L. N., J. J. Elser, A. S. Gsell, V. L. Huszar, B. W. Ibelings, E. Jeppesen, S. Kosten, W. M. Mooij, et al., 2013. Plankton dynamics under different climatic conditions in space and time. Freshwater Biology 58: 463–482.

    Google Scholar 

  • Dray, S., P. Legendre & G. Blanchet, 2016. packfor: forward selection with permutation (Canoco p.46). R package version 0.0-8. https://R-Forge.R-project.org.

  • Dray, S., D. Bauman, G. Blanchet, D. Borcard, S. Clappe, G. Guenard, T. Jombart, G. Larocque, et al. 2018. adespatial: Multivariate Multiscale Spatial Analysis. R package version 0.2-0. https://CRAN.R-project.org/package=adespatial.

  • Fermani, P., N. Diovisalvi, A. Torremorell, L. Lagomarsino, H. Zagarese & F. Unrein, 2013. The microbial food web structure of a hypertrophic warm-temperate shallow lake, as affected by contrasting zooplankton assemblages. Hydrobiologia 714: 115–130.

    CAS  Google Scholar 

  • Fermani, P., A. Torremorell, L. Lagomarsino, R. Escaray, F. Unrein & G. Pérez, 2015. Microbial abundance patterns along a transparency gradient suggest a weak coupling between heterotrophic bacteria and flagellates in eutrophic shallow Pampean lakes. Argentine Pampean Shallow lake. Hydrobiologia 752: 103–123.

    CAS  Google Scholar 

  • Gabellone, N., R. Sarandón & C. Claps, 2003. Caracterización y zonificación ecológica de la cuenca del río Salado. In Gabellone, N., M. Hernández & O. Maiola (eds), Inundaciones en la Región Pampeana. Editorial de la Universidad Nacional de La Plata, La Plata: 87–122.

    Google Scholar 

  • Gabellone, N., M. C. Claps, L. C. Solari & N. C. Neschuk, 2005. Nutrients, conductivity and plankton in a landscape approach to a Pampean saline lowland river (Salado River, Argentina). Biogeochemistry 75: 455–477.

    CAS  Google Scholar 

  • Gabellone, N., L. Solari & M. C. Claps, 2008. Chemical classification of the water in a lowland river basin (Salado River, Buenos Aires, Argentina) affected by hydraulic modification. Environmental Geology 53: 1353–1363.

    CAS  Google Scholar 

  • Gasol, J. M., J. Pinhassi, L. Alonso-Sáez, H. Ducklow, G. J. Herndl, M. Koblizek, M. Labrenz, Y. Luo, et al., 2008. Towards a better understanding of microbial carbon flux in the sea. Aquatic Microbial Ecology 53: 21–38.

    Google Scholar 

  • Giraut, M., R. Aguglino, C. Lupano, E. Bozzarello, J. Cornejo & C. Rey, 2007. Regiones hídricas superficiales de la provincia de Buenos Aires: actualización cartográfica digital. Congreso de la Asociación Española de Teledetección. de septiembre, Mar del Plata: 19–21.

    Google Scholar 

  • Havens, K. E., T. L. East & J. R. Beaver, 2007. Zooplankton response to extreme drought in a large subtropical lake. Hydrobiologia 589: 187–198.

    Google Scholar 

  • Huber, P., N. Diovisalvi, M. Ferraro, S. Metz, L. Lagomarsino, M. E. Llames, M. Royo-Llonch, J. Bustingorry, et al., 2017. Phenotypic plasticity in freshwater picocyanobacteria. Environmental Microbiology 19: 1120–1133.

    CAS  PubMed  Google Scholar 

  • Iriondo, M. H. & E. C. Drago, 2004. The headwater hydrographic characteristics of large plains: the Pampa case. Ecohydrology and Hydrobiology 4: 7–16.

    Google Scholar 

  • Isabwe, A., J. R. Yang, Y. Wang, L. Liu, H. Chen & J. Yang, 2018. Community assembly processes underlying phytoplankton and bacterioplankton across a hydrologic change in a human-impacted river. Science of the Total Environment 630: 658–667.

    CAS  PubMed  Google Scholar 

  • Izaguirre, I. & A. Vinocur, 1994. Typology of shallow lakes of the Salado River basin (Argentina), based on phytoplankton communities. Hydrobiologia 277: 49–62.

    Google Scholar 

  • Izaguirre, I., M. L. Sánchez, M. R. Schiaffino, I. O’Farrell, P. Huber, N. Ferrer, J. Zunino, L. Lagomarsino, et al., 2015. Which environmental factors trigger the dominance of phytoplankton species across a moisture gradient of shallow lakes? Hydrobiologia 752: 47–64.

    Google Scholar 

  • Jeppesen, E., S. Brucet, L. Naselli-Flores, E. Papastergiadou, K. Stefanidis, T. Nõges, P. Nõges, J. L. Attayde, et al., 2015. Ecological impacts of global warming and water abstraction on lakes and reservoirs due to changes in water level and related changes in salinity. Hydrobiologia 750: 201–227.

    Google Scholar 

  • José de Paggi, S. B., M. Devercelli & F. Rojas Molina, 2014. Zooplankton and their driving factors in a large subtropical river during low water periods. Fundamental and Applied Limnology 184: 125–139.

    Google Scholar 

  • Junk, W. J., P. B. Bayley & R. E. Sparks, 1989. The flood pulse concept in river-floodplain systems. Canadian Special Publication of Fisheries and Aquatic Sciences 106: 110–127.

    Google Scholar 

  • Jürgens, K. & E. Jeppesen, 2000. The impact of metazooplankton on the structure of the microbial food web in a shallow, hypertrophic lake. Journal of Plankton Research 22: 1047–1070.

    Google Scholar 

  • Jürgens, K., O. Skibbe & E. Jeppesen, 1999. Impact of meta-zooplankton on the composition and population dynamics of planktonic ciliates in a shallow, hypertrophic lake. Aquatic Microbial Ecology 17: 61–75.

    Google Scholar 

  • Kalff, J., 2003. Limnology. Prentince Hall, Upper Saddle River.

    Google Scholar 

  • Kobayashi, T., D. S. Ryder, G. Gordon, I. Shannon, T. Ingleton, M. Carpenter & S. J. Jacobs, 2009. Short-term response of nutrients, carbon and planktonic microbial communities to floodplain wetland inundation. Aquatic Ecology 43: 843–858.

    CAS  Google Scholar 

  • Küppers, G. C. & M. C. Claps, 2012. Spatiotemporal variations in abundance and biomass of planktonic ciliates related to environmental variables in a temporal pond, Argentina. Zoological Studies 51(3): 298–313.

    Google Scholar 

  • Kruk, C., V. L. M. Huszar, E. Peeters, S. Bonilla, L. Costa, M. Lurling, C. S. Reynolds & M. Scheffer, 2010. A morphological classification capturing functional variation in phytoplankton. Freshwater Biology 55: 614–627.

    Google Scholar 

  • Legendre, P. & H. J. B. Birks, 2012. From classical to canonical ordination. In Birks, H. J. B., A. F. Lotter, S. Juggins & J. P. Smol (eds), Tracking Environmental Change Using Lake Sediments, Data Handling and Numerical Techniques. Springer, Dordrecht: 201–248.

    Google Scholar 

  • Legendre, P. & O. Gauthier, 2014. Statistical methods for temporal and space-time analysis of community composition data. Proceedings of the Royal Society 281: 20132728.

    Google Scholar 

  • Llames, M., L. Lagomarsino, N. Diovisalvi, P. Fermani, A. Torremorell, G. Pérez, F. Unrein, J. Bustingorry, et al., 2009. The effects of different degrees of light availability in shallow, turbid waters: a mesocosm study. Journal of Plankton Research 31: 1517–1529.

    Google Scholar 

  • Macek, M., K. Šimek & T. Bittl, 2001. Conspicuous peak of oligotrichous ciliates following winter stratification in a bog lake. Journal of Plankton Research 23: 353–363.

    CAS  Google Scholar 

  • Mantel, N. & R. S. Valand, 1970. A technique of nonparametric multivariate analysis. Biometrics 26: 547–558.

    CAS  PubMed  Google Scholar 

  • Marker, A. F. H., E. A. Nusch, H. Rai & B. Riemann, 1980. The measurement of photosynthetic pigments in freshwater and standardization of methods: conclusions and recommendations. Archiv für Hydrobiologie Behandlung Ergebnisse der Limnologie 14: 91–106.

    CAS  Google Scholar 

  • Meira, B. R., F. M. Lansac-Toha, B. T. Segovia, P. R. B. Buosi, F. A. Lansac-Tôha & L. F. M. Velho, 2018. The importance of herbivory by protists in lakes of a tropical floodplain system. Aquatic Ecology 52: 193–210.

    CAS  Google Scholar 

  • Miller, J. K. & S. D. Farr, 1971. Bimultivariate redundancy: a comprehensive measure of interbattery relationship. Multivariate Behavioral Research 6: 313–324.

    Google Scholar 

  • Niño-García, J. P., C. Ruiz-González & P. A. del Giorgio, 2016. Interactions between hydrology and water chemistry shape bacterioplankton biogeography across boreal freshwater networks. ISME Journal 10: 1755–1766.

    PubMed  Google Scholar 

  • Obertegger, U., G. Flaim, M. G. Braioni, R. Sommaruga, F. Corradini & A. Borsato, 2007. Water residence time as a driving force of zooplankton structure and succession. Aquatic Science 69: 575–583.

    Google Scholar 

  • Oksanen, J., G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, R. B. O’Hara, G. L. Simpson & P. Solymos, 2017. Vegan: community ecology package. R package version 2.5-2. https://CRAN.R-project.org/package=vegan.

  • Özen, A., Ü. N. Tavşanoğlu, Aİ. Çakıroğlu, E. T. Levi, E. Jeppesen & M. Beklioğlu, 2018. Patterns of microbial food webs in Mediterranean shallow lakes with contrasting nutrient levels and predation pressures. Hydrobiologia 806: 13–27.

    Google Scholar 

  • Pace, M. L. & J. J. Cole, 1994. Comparative and experimental approaches to top-down and bottom-up regulation of bacteria. Microbial Ecology 28: 181–193.

    CAS  PubMed  Google Scholar 

  • Pace, M. L., S. E. G. Findlay & D. Lints, 1992. Zooplankton in advective environments, The Hudson River community and a comparative analysis. Canadian Journal of Fisheries and Aquatic Sciences 49: 1060–1069.

    Google Scholar 

  • Padial, A. A., F. Ceschin, S. A. J. Declerck, L. De Meester, C. C. Bonecker, F. A. Lansac-Tôha, L. Rodrigues, L. C. Rodrigues, et al., 2014. Dispersal ability determines the role of environmental, spatial and temporal drivers of metacommunity structure. PLoS ONE 9: e111227.

    PubMed  PubMed Central  Google Scholar 

  • Pagano, M., 2008. Feeding of tropical cladocerans (Moina micrura, Diaphanosoma excisum) on natural phytoplankton: effect of phytoplankton size-structure. Journal of Plankton Research 30: 401–414.

    Google Scholar 

  • Pérez, S., E. Sierra, F. Momo & M. Massobrio, 2015. Changes in average annual precipitation in Argentina’s Pampa region and their possible causes. Climate 3: 150–167.

    Google Scholar 

  • Pernthaler, J., 2005. Predation on prokaryotes in the water column and its ecological implications. Natural Reviews Microbiology 3: 537–546.

    CAS  Google Scholar 

  • Pernthaler, J., B. Sattler, K. Simek, A. Schwarzenbacher & R. Psenner, 1996. Top-down effects on the size-biomass distribution of a freshwater bacterioplankton community. Aquatic Microbial Ecology 10: 255–263.

    Google Scholar 

  • Pirlot, S., J. Vanderheyden, J. P. Descy & P. Servais, 2005. Abundance and biomass of heterotrophic microorganisms in Lake Tanganyika. Freshwater Biology 50: 1219–1232.

    Google Scholar 

  • Pomeroy, L. R., 1974. The ocean’s food web, a changing paradigm. BioScience 24: 499–504.

    Google Scholar 

  • Porter, K. G., J. D. Orcutt & J. Gerritsen, 1983. Functional response and fitness in a generalist filter feeder, Daphnia magna (Cladocera, Crustacea). Ecology 64: 735–742.

    Google Scholar 

  • Porter, K. G., H. Pearl, R. Hodson, M. Pace, J. Priscu, B. Riemann, D. Scavia & J. Stockner, 1988. Microbial interactions in lake food webs. In Carpenter, S. R. (ed.), Complex Interactions in Lakes Communities. Springer, New York: 209–227.

    Google Scholar 

  • Quirós, R., 2003. The relationship between nitrate and ammonia concentrations in the pelagic zone of lakes. Limnetica 22: 37–50.

    Google Scholar 

  • Quirós, R., A. M. Rennella, M. A. Boveri, J. J. Rosso & A. Sosnovsky, 2002a. Factores que afectan la estructura y el funcionamiento de las lagunas pampeanas. Ecología Austral 12: 175–185.

    Google Scholar 

  • Quirós, R., J. J. Rosso, A. Rennella, A. Sosnovsky & M. Boveri, 2002b. Análisis del estado trófico de las lagunas pampeanas (Argentina). Interciencia 27: 584–591.

    Google Scholar 

  • Quirós, R., M. B. Boveri, C. A. Petracchi, A. M. Rennella, J. J. Rosso, A. Sosnovsky & H. T. Von Bernard, 2006. Los efectos de la agriculturización del humedal Pampeano sobre la eutrofización de sus lagunas. In Tundisi, J. G., T. Matsmura-Tundisi, C. Sidagis Galli, J. G. Tundisi, T. Matsumura-Tundisi & C. S. Galli (eds), Eutrofizaçaõ na América do Sul: Causas, Conseqüências e Tecnologias Degerenciamento e Controle. The International Institute of Ecology, Sao Carlos: 1–16.

    Google Scholar 

  • R Development Core Team, 2017. R 3.4.1: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.

  • Rennella, A. M. & R. Quirós, 2002. Relations between planktivorous fish and zooplankton in two very shallow lakes of the pampa plain. Verhandlungen des Internationalen Verein Limnologie 28: 887–891.

    Google Scholar 

  • Rennella, A. M. & R. Quirós, 2006. The effects of hydrology on plankton biomass in shallow lakes of the Pampa Plain. Hydrobiologia 556: 181–191.

    Google Scholar 

  • Rosso, J. J., 2008. Relación entre la abundancia y estructura de la comunidad de peces y el régimen hidrológico, en lagunas de la alta cuenca del río Salado. PhD Thesis, Universidad de Buenos Aires, Argentina.

  • Sarmento, H., 2012. New paradigms in tropical limnology: the importance of the microbial food web in tropical lakes. Hydrobiologia 686: 1–14.

    Google Scholar 

  • Segovia, B. T., D. G. Pereira, L. M. Bini, B. R. de Meira, V. S. Nishida, F. A. Lansac-Tôha & L. F. Velho, 2015. The role of microorganisms in a planktonic food web of a floodplain lake. Microbial Ecology 69: 225–233.

    PubMed  Google Scholar 

  • Segovia, B. T., B. R. Meira, F. M. Lansac-Toha, F. E. Amadeo, F. Unrein, L. F. M. Velho & H. Sarmento, 2018. Growth and cytometric diversity of bacterial assemblages under different top-down control regimes by using a size-fractionation approach. Journal of Plankton Research 40: 129–141.

    Google Scholar 

  • Sharp, J. H., 1993. Procedures subgroup report. Marine Chemistry 41: 37–49.

    CAS  Google Scholar 

  • Sherr, E. B. & B. F. Sherr, 1993. Protistan grazing rates via uptake of fluorescently labeled prey. In Kemp, P., B. Sherr, E. Sherr & J. Cole (eds), Handbook of Methods in Aquatic Microbial Ecology. Lewis Publ, Boca Raton: 695–701.

    Google Scholar 

  • Sherr, E. B. & B. F. Sherr, 2002. Significance of predation by protists in aquatic microbial food webs. Antonie van Leeuwenhoek 81: 293–308.

    CAS  PubMed  Google Scholar 

  • Sieburth, J. M. N., V. Smetacek & J. Lenz, 1978. Pelagic ecosystem structure: heterotrophic compartments of the plankton and their relationship to plankton size fractions. Limnology Oceanography 23: 1256–1263.

    Google Scholar 

  • Sinistro, R., 2010. Top-down and bottom-up regulation of planktonic communities in a warm temperate wetland. Journal of Plankton Research 32: 209–220.

    CAS  Google Scholar 

  • Sinistro, R., M. L. Sanchez, M. Marinone & I. Izaguirre, 2007. Experimental study of the zooplankton impact on the trophic structure of phytoplankton and the microbial assemblages in a temperate wetland (Argentina). Limnologica 37: 88–99.

    Google Scholar 

  • Silva, L. H. S., V. L. M. Huszar, M. M. Marinho, L. M. Rangel, J. Brasil, C. D. Domingues, C. C. Branco & F. Roland, 2014. Drivers of phytoplankton, bacterioplankton, and zooplankton carbon biomass in tropical hydroelectric reservoirs. Limnologica 48: 1–10.

    CAS  Google Scholar 

  • Silvoso, J., I. Izaguirre & L. Allende, 2011. Picoplankton structure in clear and turbid eutrophic shallow lakes: a seasonal study. Limnologica 41: 181–190.

    CAS  Google Scholar 

  • Šimek, K., P. Hartman, J. Nedoma, J. Pernthaler, D. Springmann, J. Vrba & R. Psenner, 1997. Community structure, picoplankton grazing and zooplankton control of heterotrophic nanoflagellates in a eutrophic reservoir during the summer phytoplankton maximum. Aquatic Microbial Ecology 12: 49–63.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Sommer, U. & F. Sommer, 2006. Cladocerans versus copepods: the cause of contrasting top-down controls on freshwater and marine phytoplankton. Oecologia 147: 183–194.

    PubMed  Google Scholar 

  • Sommaruga, R., 1995. Microbial and classical food webs: a visit to a hypertrophic lake. Microbial Ecology 17: 257–270.

    CAS  Google Scholar 

  • ter Braak, C. J. F., 1987. Ordination. In Jongman, R. H. G., C. J. F. ter Braak & O. F. R. van Tongeren (eds), Data analysis in community and landscape ecology. Cambridge University Press, Wageningen: 91–173.

    Google Scholar 

  • ter Braak, C. J. F. & P. Smilauer, 2002. CANOCO Reference Manual and CanoDraw for Windows Urser’s Guide: Software for Canonical Community Ordination (version 4.5). Microcomputer Power, Ithaca, NY.

  • Torremorell, A., J. Bustigorry, R. Escaray & H. E. Zagarese, 2007. Seasonal dynamics of a large, shallow lake, laguna Chascomús: the role of light limitation and other physical variables. Limnologica 37: 100–108.

    CAS  Google Scholar 

  • Torremorell, A. M., M. E. Llames, G. L. Pérez, R. Escaray, J. Bustingorry & H. Zagarese, 2009. Annual patterns of phytoplankton density and primary production in a large, shallow lake: the central role of light. Freshwater Biology 54: 437–449.

    Google Scholar 

  • Utermöhl, H., 1958. Zur vervollkommnung der quantitativen phytoplankton-methodik. Mitteilungen Internationale Vereinigung Limnologie 9: 1–38.

    Google Scholar 

  • Venrick, E. L., 1978. How many cells to count? In Sournia, A. (ed.), Phytoplankton Manual. UNESCO, Paris: 167–180.

    Google Scholar 

  • Weisse, T., H. Müller, R. M. Pinto-Coelho, A. Schweizer, D. Springmann & G. Baldringer, 1990. Response of the microbial loop to the phytoplankton spring bloom in a large prealpine lake. Limnology Oceanography 35: 781–794.

    Google Scholar 

  • Weisse, T., R. Anderson, H. Arndt, A. Calbelt, P. J. Hansen & D. Montagnes, 2016. Functional ecology of aquatic phagotrophic protists: concepts, limitations, and perspectives. Protistologica 55: 50–74.

    Google Scholar 

  • Yang, J., H. Lv, J. Yang, L. Liu, X. Yu & H. Chen, 2016. Decline in water level boosts cyanobacteria dominance in subtropical reservoirs. Science of the Total Environment 557(558): 445–452.

    PubMed  Google Scholar 

  • Yang, J. R., H. Lv, A. Isabwe, L. Liu, X. Yu, H. Chen & J. Yang, 2017. Disturbance-induced phytoplankton regime shifts and recovery of cyanobacteria dominance in two subtropical reservoirs. Water Research 120: 52–63.

    CAS  PubMed  Google Scholar 

  • Zingel, P. & T. Nõges, 2010. Seasonal and annual population dynamics of ciliates in a shallow eutrophic lake. Fundamental and Applied Limnology 176: 133–143.

    Google Scholar 

  • Zingel, P., H. Agasild, T. Nõges & V. Kisand, 2007. Ciliates are the dominant grazers on pico- and nanoplankton in a shallow, naturally highly eutrophic lake. Microbial Ecology 53: 134–142.

    PubMed  Google Scholar 

  • Zingel, P., H. Agasild, K. Karus, K. Kangro, H. Tammert, I. Tõnno, T. Feldemann & T. Nõges, 2016. The influence of zooplankton enrichment on the microbial loop in a shallow, eutrophic lake. European Journal of Protistology 52: 22–35.

    PubMed  Google Scholar 

Download references

Acknowledgements

We thank Viviana Lobato for her aid during sampling campaigns and Irina Izaguirre for her general support. This study was supported by the National Council of Scientific and Technical Research (Network project for the assessment and monitoring of Pampean shallow lakes, PAMPA2) and the National Agency of Scientific and Technical Promotion (PICT 2014-0918).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. R. Schiaffino.

Additional information

Handling editor: Stefano Amalfitano

Electronic supplementary material

Below is the link to the electronic supplementary material.

10750_2018_3874_MOESM1_ESM.eps

Supplementary Fig. 1. Correlations between the microbial component similarity matrices (Bray–Curtis) and the water level difference matrices (Euclidean distances) in Gómez (a) and Carpincho (b) using Mantel tests. Supplementary material 1 (EPS 4613 kb)

10750_2018_3874_MOESM2_ESM.eps

Supplementary Fig. 2. Temporal variation of values along the significant (P < 0.05) axes of canonical asymmetric eigenvector maps (AEM) models of the Napierian-transformed microbial community matrix, constructed using forward selection of positive (black curves) and negatives (red curves) AEM. AEM were selected at the 0.05 level. Supplementary material 2 (EPS 6645 kb)

Supplementary material 3 (DOCX 46 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schiaffino, M.R., Diovisalvi, N., Marfetán Molina, D. et al. Microbial food-web components in two hypertrophic human-impacted Pampean shallow lakes: interactive effects of environmental, hydrological, and temporal drivers. Hydrobiologia 830, 255–276 (2019). https://doi.org/10.1007/s10750-018-3874-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-018-3874-7

Keywords

Navigation