Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Environmental dissimilarity over time in a large subtropical shallow lake is differently represented by phytoplankton functional approaches

Juliana E. Bohnenberger A C , Lúcia R. Rodrigues A , David da Motta-Marques A and Luciane O. Crossetti B
+ Author Affiliations
- Author Affiliations

A Universidade Federal do Rio Grande do Sul, Instituto de Pesquisas Hidráulicas, Avenida Bento Gonçalves, 9500, Porto Alegre, 91501-970, RS, Brazil.

B Universidade Federal do Rio Grande do Sul, Departamento de Ecologia, Instituto de Biociências, Avenida Bento Gonçalves, 9500, Porto Alegre, 91501-970, RS, Brazil.

C Corresponding author. Email bonhju@yahoo.com.br

Marine and Freshwater Research 69(1) 95-104 https://doi.org/10.1071/MF16417
Submitted: 17 December 2016  Accepted: 18 July 2017   Published: 22 August 2017

Abstract

The aim of the present study was to understand how different phytoplankton functional approaches responded to environmental variability in a large shallow lake, namely Lake Mangueira, in southern Brazil. This coastal lake has a maximum depth of 7 m and is ~90 km long and ~3–10 km wide. Physical and chemical variables, maximum linear dimension, life forms, functional and morphofunctional groups of phytoplankton were analysed. The results showed that the phytoplankton were primarily comprised Cyanobacteria (63.9%), followed by middle-sized algae (21–50 μm; 46.7%) and colonial non-flagellated taxa (63%). The highest percentage of total biomass was accounted for by the functional group ‘K’ (as classified by Reynolds et al. 2002; 36.3%), large mucilaginous colonies (46.79%) according to morphologically based functional classification and other large colonies (mostly non-vacuolated; 36.7%) according to morphofunctional classification. Dissimilarity analysis indicated a significant correlation between abiotic data and functional approaches (P = 0.001). The dissimilarity in the functional compositions of phytoplankton was related to nutrient and light conditions, especially to silicon content and water transparency, in all functional approaches. The highest correlation with abiotic variables was seen for morphologically based functional group community structure, although the functional group composition of phytoplankton sensu Reynolds et al. seemed to be the most effective system in describing environmental variability in Lake Mangueira over the long term.

Additional keywords: functional groups, life forms, maximum linear dimension, morphology.


References

Alvares, C. A., Stape, J. L., Sentelhas, P. C., Gonçalves, J. L. M., and Sparovek, G. (2013). Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22, 711–728.
Köppen’s climate classification map for Brazil.CrossRef |

American Public Health Association (2012). ‘Standard Methods for Examination of Water and Waste Water’, 22nd edn. (Byrd Prepress: Springfield, VA, USA.)

Arfi, R., Guiral, D., and Bouvy, M. (1993). Wind induced resuspension in a shallow tropical lagoon. Estuarine, Coastal and Shelf Science 36, 587–604.
Wind induced resuspension in a shallow tropical lagoon.CrossRef | 1:CAS:528:DyaK2cXisl2gsL0%3D&md5=10044de544f3be9c6d0fcafa4e105ffdCAS |

Arfi, R., Guiral, D., and Bouvy, M. (1994). Sedimentation modified by wind induced resuspension in a shallow tropical lagoon (Cote d’Ivoire). Netherlands Journal of Aquatic Ecology 28, 427–431.
Sedimentation modified by wind induced resuspension in a shallow tropical lagoon (Cote d’Ivoire).CrossRef |

Barnett, A. J., Finlay, K., and Beisner, B. E. (2007). Functional diversity of crustacean zooplankton communities: towards a trait-based classification. Freshwater Biology 52, 796–813.
Functional diversity of crustacean zooplankton communities: towards a trait-based classification.CrossRef |

Beamud, S. G., León, J. G., Kruk, C., Pedrozo, F., and Diaz, M. (2015). Using trait-based approaches to study phytoplankton seasonal succession in a subtropical reservoir in arid central western Argentina. Environmental Monitoring and Assessment 187, 271–287.
Using trait-based approaches to study phytoplankton seasonal succession in a subtropical reservoir in arid central western Argentina.CrossRef | 1:STN:280:DC%2BC2MjmsVOlsQ%3D%3D&md5=6e3b8c8479427588fd354f36b698e912CAS |

Becker, V., Huszar, V. L. M., Naselli-Flores, L., and Padisák, J. (2008). Phytoplankton equilibrium phases during thermal stratification in a deep subtropical reservoir. Freshwater Biology 53, 952–963.
Phytoplankton equilibrium phases during thermal stratification in a deep subtropical reservoir.CrossRef |

Becker, V., Cardoso, L. S., and Huszar, V. L. M. (2009). Diel variation of phytoplankton functional groups in a subtropical reservoir in southern Brazil, during an autumnal stratification period. Aquatic Ecology 43, 285–293.
Diel variation of phytoplankton functional groups in a subtropical reservoir in southern Brazil, during an autumnal stratification period.CrossRef |

Borics, G., Tóthmérész, B., Várbíro, G., Grigorszky, I., Czébely, A., and Görgényi, J. (2016). Functional phytoplankton distribution in hypertrophic systems across water body size. Hydrobiologia 764, 81–90.
Functional phytoplankton distribution in hypertrophic systems across water body size.CrossRef | 1:CAS:528:DC%2BC2MXmt1Oju7w%3D&md5=c24aa8c0d84524d9c7366482ee5de1f6CAS |

Bortolini, J. C., Moresco, G. A., Paula, A. C. M., Jati, S., and Rodrigues, L. C. (2016). Functional approach based on morphology as a model of phytoplankton variability in a subtropical floodplain lake: a long-term study. Hydrobiologia 767, 151–163.
Functional approach based on morphology as a model of phytoplankton variability in a subtropical floodplain lake: a long-term study.CrossRef | 1:CAS:528:DC%2BC2MXhsFeju7%2FO&md5=f30e2602552ddde14b3c61eec81bbd3fCAS |

Brasil, J., and Huszar, V. L. M. (2011). O papel dos traços funcionais na ecologia do fitoplâncton continental. Oecologia Australis 15, 799–834.
O papel dos traços funcionais na ecologia do fitoplâncton continental.CrossRef |

Cardoso, L. S., Fragoso, C. R. J., Souza, R. S., and Motta-Marques, D. M. L. (2012). Hydrodynamic control of plankton spatial and temporal heterogeneity in subtropical shallow lakes. In ‘Hydrodynamics – Natural Water Bodies’. (Ed. H. Schulz.) pp. 27–48. (InTech: Rijeka, Croatia.) Available at http://www.intechopen.com/books/hydrodynamics-natural-water-bodies/hydrodynamic-control-of-plankton-spatial-and-temporal-heterogeneity-in-subtropical-shallow-lakes [Verified 23 November 2016].

Clarke, K. R., and Ainsworth, M. (1993). A method of linking multivariate community structure to environmental variables. Marine Ecology Progress Series 92, 205–219.
A method of linking multivariate community structure to environmental variables.CrossRef |

Costa, L. S., Huszar, V. L. M., and Ovalle, A. R. (2009). Phytoplankton functional groups in a tropical estuary: hydrological control and nutrient limitation. Estuaries and Coasts 32, 508–521.
Phytoplankton functional groups in a tropical estuary: hydrological control and nutrient limitation.CrossRef | 1:CAS:528:DC%2BD1MXktF2ktbg%3D&md5=b746e38077c970865fb1434c91c17d59CAS |

Crossetti, L. O., and Bicudo, C. E. M. (2008b). Phytoplankton as a monitoring tool in a tropical urban shallow reservoir (Garças Pond): the assemblage index application. Hydrobiologia 610, 161–173.
Phytoplankton as a monitoring tool in a tropical urban shallow reservoir (Garças Pond): the assemblage index application.CrossRef | 1:CAS:528:DC%2BD1cXotFalu70%3D&md5=f9dadf5bc3a3b330130811be2cc93ca3CAS |

Crossetti, L. O., Schneck, F., Freitas-Teixeira, L. M., and Motta-Marques, D. (2014). The influence of environmental variables on spatial and temporal phytoplankton dissimilarity in a large shallow subtropical lake (Lake Mangueira, southern Brazil. Acta Limnologica Brasiliensia 26, 111–118.
The influence of environmental variables on spatial and temporal phytoplankton dissimilarity in a large shallow subtropical lake (Lake Mangueira, southern Brazil.CrossRef |

Fragoso, C., Motta-Marques, D., Collischonn, W., Tucci, C., and van Nes, E. (2008). Modelling spatial heterogeneity of phytoplankton in Lake Mangueira, a large shallow subtropical lake in South Brazil. Ecological Modelling 219, 125–137.
Modelling spatial heterogeneity of phytoplankton in Lake Mangueira, a large shallow subtropical lake in South Brazil.CrossRef | 1:CAS:528:DC%2BD1cXht12kurnP&md5=86341c27b19eed0ea91c9aa90c60d5e2CAS |

Freitas-Teixeira, L. M., Bohnenberger, J. E., Rodrigues, L. R., Schulz, U. H., Motta-Marques, D., and Crossetti, L. O. (2016). Temporal variability determines phytoplankton structure over spatial organization in a large shallow heterogeneous subtropical lake. Inland Waters 6, 325–335.

Gallego, I., Davidson, T. A., Jeppesen, E., Pérez-Martínez, C., Sánchez-Castillo, P., Juan, M., Fuentes-Rodríguez, F., León, D., Peñalver, P., Toja, J., and Casas, J. J. (2012). Taxonomic or ecological approaches? Searching for phytoplankton surrogates in the determination of richness and assemblage composition in ponds. Ecological Indicators 18, 575–585.
Taxonomic or ecological approaches? Searching for phytoplankton surrogates in the determination of richness and assemblage composition in ponds.CrossRef |

Gemelgo, M. C. P., Mucci, J. L. N., and Navas-Pereira, D. (2009). Population dynamics: seasonal variation of phytoplankton functional groups in Brazilian reservoirs (Billings and Guarapiranga, São Paulo). Brazilian Journal of Biology 69, 1001–1013.
Population dynamics: seasonal variation of phytoplankton functional groups in Brazilian reservoirs (Billings and Guarapiranga, São Paulo).CrossRef | 1:STN:280:DC%2BD1MfgvVKntA%3D%3D&md5=1fd84802953b00c6ebb6f5c4be999aa1CAS |

Gligora, M., Plenković-Moraj, A., Kralj, K., Grigorszky, I., and Peroš-Pucar, D. (2007). The relationship between phytoplankton species dominance and environmental variables in a shallow lake (Lake Vrana, Croatia). Hydrobiologia 584, 337–346.
The relationship between phytoplankton species dominance and environmental variables in a shallow lake (Lake Vrana, Croatia).CrossRef | 1:CAS:528:DC%2BD2sXlsVeqtbc%3D&md5=8bbacbf701220f2f1341de88fa42f28bCAS |

Gran, G. (1952). Determination of the equivalence point in potentiometric titration, part II. Analyst 77, 661–671.
Determination of the equivalence point in potentiometric titration, part II.CrossRef | 1:CAS:528:DyaG3sXlvFSm&md5=80240217517260c0ff3ad0ce08a976baCAS |

Grime, J. P., and Pierce, S. (2012). ‘The Evolutionary Strategies that Shape Ecosystems.’ (Wiley-Blackwell: Chichester, UK.)

Hillebrand, H., Dürseken, D., Kirschiel, D., Pollingher, U., and Zohary, T. (1999). Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35, 403–424.
Biovolume calculation for pelagic and benthic microalgae.CrossRef |

Huszar, V. L. M., and Caraco, N. (1998). The relationship between phytoplankton composition and physical–chemical variables: a comparison of taxonomic and morphological approaches in six temperate lakes. Freshwater Biology 40, 1–18.

Huszar, V. L. M., Kruk, C., and Caraco, N. (2003). Steady state of phytoplankton assemblage of phytoplankton in four temperate lakes (NE USA). Hydrobiologia 502, 97–109.
Steady state of phytoplankton assemblage of phytoplankton in four temperate lakes (NE USA).CrossRef |

Izaguirre, I., Allende, L., Escaray, R., Bustingorry, J., Pérez, G., and Tell, G. (2012). Comparison of morphofunctional phytoplankton classifications in human-impacted shallow lakes with different stable states. Hydrobiologia 698, 203–216.
Comparison of morphofunctional phytoplankton classifications in human-impacted shallow lakes with different stable states.CrossRef | 1:CAS:528:DC%2BC38XhsVagtb3F&md5=755675af7a38c0ff801fe3cfad56679dCAS |

Jespersen, A. M., and Christoffersen, K. (1987). Measurements of chlorophyll-a from phytoplankton using ethanol as extraction solvent. Archiv für Hydrobiologie 109, 445–454.
| 1:CAS:528:DyaL2sXkvFaqu78%3D&md5=72187b389e62e2617e625a48d7c05d5dCAS |

Körner, C. (1993) Scaling from species to vegetation: the usefulness of functional groups. In ‘Biodiversity and Ecosystem Function’. (Eds E. D. Schulze and H. A. Mooney.) pp. 117–140. (Springer-Verlag: Berlin, Germany.)

Kruk, C., Huszar, V. L. M., Peeters, E. T. H. M., Bonilla, S., Costa, L., Lürling, M., Reynolds, C. S., and Scheffer, M. (2010). A morphological classification capturing functional variation in phytoplankton. Freshwater Biology 55, 614–627.
A morphological classification capturing functional variation in phytoplankton.CrossRef |

Kruk, C., Peeters, E. T. H. M., Van Nes, E. H., Huszar, V. L. M., Costa, L. S., and Scheffer, M. (2011). Phytoplankton community composition can be predicted best in terms of morphological groups. Limnology and Oceanography 56, 110–118.
Phytoplankton community composition can be predicted best in terms of morphological groups.CrossRef |

Lavorel, S., Díaz, S., Cornelissen, J. H. C., Garnier, E., Harrison, S. P., and McIntyre, S. (2007). Plant functional types: are we getting any closer to the Holy Grail? In ‘Terrestrial Ecosystems in a Changing World’. (Eds J. G. Canadell, D. Pataki, and L. Pitelka.) pp. 149–160. (Springer-Verlag: Heidelberg, Germany.)

Legendre, P., and Legendre, L. (1998). ‘Numerical Ecology.’ (Elsevier: Amsterdam, Netherlands.)

Lehman, J. T. (1988). Selective herbivory and its role in the evolution of phytoplankton growth strategies. In ‘Growth and Reproductive Strategies of Freshwater Phytoplankton’. (Ed. C. D. Sandgren.) pp. 369–387. (Cambridge University Press: Cambridge, UK.)

Litchman, E., and Klausmeier, C. A. (2008). Trait-based community ecology of phytoplankton. Annual Review of Ecology and Systematics 39, 615–639.
Trait-based community ecology of phytoplankton.CrossRef |

Lund, J. W. G., Kipling, C., and LeCren, E. D. (1958). The invert microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11, 143–170.
The invert microscope method of estimating algal numbers and the statistical basis of estimations by counting.CrossRef |

Mackereth, F. J. H., Heron, J., and Talling, J. F. (1978). ‘Water Analysis: Some Revised Methods for Limnologists.’ (Freshwater Biological Association: Far Sawrey, Ambleside, UK.)

Margalef, R. (1978). Life-forms of phytoplankton as survival alternatives in an unstable environment. Acta Oceanologica 1, 493–509.

McIntyre, S., Díaz, S., Lavorel, S., and Cramer, W. (1999). Plant functional types and disturbance dynamics response in herbaceous vegetation. Journal of Vegetation Science 10, 603–608.
Plant functional types and disturbance dynamics response in herbaceous vegetation.CrossRef |

Melo, A. S., Schneck, F., Hepp, L. U., Simões, N. R., Siqueira, T., and Bini, L. M. (2011). Focusing on variation: methods and applications of the concept of beta diversity in aquatic ecosystems. Acta Limnologica Brasiliensia 23, 318–331.
Focusing on variation: methods and applications of the concept of beta diversity in aquatic ecosystems.CrossRef |

Naselli-Flores, L. (2014). Morphological analysis of phytoplankton as a tool to assess ecological state of aquatic ecosystems: the case of Lake Arancio, Sicily, Italy. Inland Waters 4, 15–26.
Morphological analysis of phytoplankton as a tool to assess ecological state of aquatic ecosystems: the case of Lake Arancio, Sicily, Italy.CrossRef |

Naselli-Flores, L., Padisák, J., and Albay, M. (2007). Shape and size in phytoplankton ecology: do they matter? Hydrobiologia 578, 157–161.
Shape and size in phytoplankton ecology: do they matter?CrossRef |

Pacheco, J. P., Iglesias, C., Meerhoff, M., Fosalba, C., Goyenola, G., Mello, F. T., García, S., Gelós, M., and García-Rodríguez, F. (2010). Phytoplankton community structure in five subtropical shallow lakes with different trophic status (Uruguay): a morphology-based approach. Hydrobiologia 646, 187–197.
Phytoplankton community structure in five subtropical shallow lakes with different trophic status (Uruguay): a morphology-based approach.CrossRef | 1:CAS:528:DC%2BC3cXksF2rsr4%3D&md5=bd5a2d735719c1b6bfb2042caf0c78dcCAS |

Padisák, J., and Dokulil, M. (1994). Contribution of green algae to the phytoplankton assemblage in a large, turbid shallow lake (Neusiedlersee, Austria/Hungary). Biológia Bratislava 49, 571–579.

Padisák, J., Soróczki-Pintér, É., and Rezner, Z. (2003). Sinking properties of some phytoplankton shapes and relation of form resistance to morphological diversity of plankton – an experimental study. Hydrobiologia 500, 243–257.
Sinking properties of some phytoplankton shapes and relation of form resistance to morphological diversity of plankton – an experimental study.CrossRef |

Padisák, J., Crossetti, L. O., and Naselli-Flores, L. (2009). Use and misuse in the application of the phytoplankton functional classification: a critical review with updates. Hydrobiologia 621, 1–19.
Use and misuse in the application of the phytoplankton functional classification: a critical review with updates.CrossRef |

Peretyatko, A., Teissier, S., Symoens, J. J., and Triest, L. (2007). Phytoplankton biomass and environmental factors over a gradient of clear to turbid peri-urban ponds. Aquatic Conservation 17, 584–601.
Phytoplankton biomass and environmental factors over a gradient of clear to turbid peri-urban ponds.CrossRef |

Rangel, L. M., Soares, M. C. S., Paiva, R., and Silva, L. H. S. (2016). Morphology-based functional groups as effective indicators of phytoplankton dynamics in a tropical cyanobacteria-dominated transitional river–reservoir system. Ecological Indicators 64, 217–227.
Morphology-based functional groups as effective indicators of phytoplankton dynamics in a tropical cyanobacteria-dominated transitional river–reservoir system.CrossRef |

Reynolds, C. S. (1980). Phytoplankton assemblages and their periodicity in stratifying lake systems. Holarctic Ecology 3, 141–159.

Reynolds, C. S. (1988). Functional morphology and the adaptive strategies of freshwater phytoplankton. In ‘Growth and Reproductive Strategies of Freshwater Phytoplankton’. (Ed. C. D. Sandgren.) pp. 388–433. (Cambridge University Press: New York, NY, USA.)

Reynolds, C. S. (1997). ‘Vegetation Processes in the Pelagic: a Model for Ecosystem Theory.’ (Ecology Institute: Oldendorf, Germany.)

Reynolds, C. S. (2006). ‘The Ecology of Phytoplankton: Ecology, Biodiversity and Conservation.’ (Cambridge University Press: Cambridge, UK).

Reynolds, C. S., and Irish, A. E. (1997). Modelling phytoplankton dynamics in lakes and reservoirs: the problem of in-situ growth rates. Hydrobiologia 349, 5–17.
Modelling phytoplankton dynamics in lakes and reservoirs: the problem of in-situ growth rates.CrossRef | 1:CAS:528:DyaK2sXnslOit7g%3D&md5=246057410be8a30dba43c49bed22a19aCAS |

Reynolds, C. S., Huszar, V. L. M., Kruk, C., Naselli-Flores, L., and Melo, S. (2002). Towards a functional classification of the freshwater phytoplankton. Journal of Plankton Research 24, 417–428.
Towards a functional classification of the freshwater phytoplankton.CrossRef |

Rodrigues, L. R., Motta-Marques, D., and Fontoura, N. F. (2015). Fish community in a large coastal subtropical lake: how an environmental gradient may affect the structure of trophic guilds. Limnetica 34, 495–506.

Rosa, L. M., Cardoso, L. S., Crossetti, L. O., and Motta-Marques, D. (2017). Spatial and temporal variability of zooplankton–phytoplankton interactions in a large subtropical shallow lake dominated by non-toxic cyanobacteria. Marine and Freshwater Research 68, 226–243.
Spatial and temporal variability of zooplankton–phytoplankton interactions in a large subtropical shallow lake dominated by non-toxic cyanobacteria.CrossRef |

Sawyer, C. N., McCarty, P. L., and Parkin, G. F. (2003). ‘Chemistry for Environmental Engineering and Science’, 5th edn. (MacGraw-Hill Education: Columbus, OH, USA.)

Salmaso, N., and Padisák, J. (2007). Morpho-functional groups and phytoplankton development in two deep lakes (Lake Garda, Italy and Lake Stechlin, Germany). Hydrobiologia 578, 97–112.
Morpho-functional groups and phytoplankton development in two deep lakes (Lake Garda, Italy and Lake Stechlin, Germany).CrossRef |

Salmaso, N., Naselli-Flores, L., and Padisák, J. (2015). Functional classifications and their application in phytoplankton ecology. Freshwater Biology 60, 603–619.
Functional classifications and their application in phytoplankton ecology.CrossRef |

Schneck, F., Schwarzbold, A., Rodrigues, S. C., and Melo, A. S. (2011). Environmental variability drives phytoplankton assemblage persistence in a subtropical reservoir. Austral Ecology 36, 839–848.
Environmental variability drives phytoplankton assemblage persistence in a subtropical reservoir.CrossRef |

Sneath, P. H. A., and Sokal, R. R. (1973). ‘Numerical Taxonomy – the Principles and Practice of Numerical Classification.’ (W. H. Freeman: San Francisco, CA, USA.)

Sommer, U. (1984). The paradox of the plankton: fluctuations of phosphorus availability maintain diversity of phytoplankton in flow-through cultures. Limnology and Oceanography 29, 633–636.
The paradox of the plankton: fluctuations of phosphorus availability maintain diversity of phytoplankton in flow-through cultures.CrossRef |

Tang, E. P. (1995). The allometry of algal growth rates. Journal of Plankton Research 17, 1325–1335.
The allometry of algal growth rates.CrossRef |

Utermöhl, H. (1958). Zur Vervollkommnung der quantitativen Phytoplankton: Methodik. Mitteilungen der Internationalen Vereinigung für theoretische und angewandte Limnologie 9, 1–38.

Žutinić, P., Gligora Udovič, M., Kralj Borojević, K., Plenković-Moraj, A., and Padisák, J. (2014). Morpho-functional classifications of phytoplankton assemblages of two deep karstic lakes. Hydrobiologia 740, 147–166.
Morpho-functional classifications of phytoplankton assemblages of two deep karstic lakes.CrossRef |



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